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Bryophyte Biology
Second Edition
Bryophyte Biology provides a comprehensive yet succinct overview of the
hornworts, liverworts, and mosses: diverse groups of land plants that occupy a
great variety of habitats throughout the world. This new edition covers essential
aspects of bryophyte biology, from morphology, physiological ecology and
conservation, to speciation and genomics. Revised classifications incorporate
contributions from recent phylogenetic studies. Six new chapters complement
fully updated chapters from the original book to provide a completely up-to-date
resource. New chapters focus on the contributions of Physcomitrella to plant
genomic research, population ecology of bryophytes, mechanisms of drought
tolerance, a phylogenomic perspective on land plant evolution, and problems
and progress of bryophyte speciation and conservation. Written by leaders in
the field, this book offers an authoritative treatment of bryophyte biology, with
rich citation of the current literature, suitable for advanced students and
researchers.
BERNARD GOFFINET is an Associate Professor in Ecology and Evolutionary
Biology at the University of Connecticut and has contributed to nearly 80
publications. His current research spans from chloroplast genome evolution in
liverworts and the phylogeny of mosses, to the systematics of lichen-forming
fungi.
A. JONATHAN SHAW is a Professor at the Biology Department at Duke
University, an Associate Editor for several scientific journals, and Chairman
for the Board of Directors, Highlands Biological Station. He has published over
130 scientific papers and book chapters. His research interests include the
systematics and phylogenetics of mosses and liverworts and population
genetics of peat mosses.
Bryophyte Biology
Second Edition
BERNARD GOFFINET
University of Connecticut, USA
AND
A. J O N A T H A N S H A W
Duke University, USA
CAMBRIDGE UNIVERSITY PRESS
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo
Cambridge University Press
The Edinburgh Building, Cambridge CB2 8RU, UK
Published in the United States of America by Cambridge University Press, New York
www.cambridge.org
Information on this title: www.cambridge.org/9780521872256
© Cambridge University Press 2000, 2009
This publication is in copyright. Subject to statutory exception and to the
provision of relevant collective licensing agreements, no reproduction of any part
may take place without the written permission of Cambridge University Press.
First published in print format 2008
ISBN-13
978-0-511-45577-3
eBook (EBL)
ISBN-13
978-0-521-87225-6
hardback
ISBN-13
978-0-521-69322-6
paperback
Cambridge University Press has no responsibility for the persistence or accuracy
of urls for external or third-party internet websites referred to in this publication,
and does not guarantee that any content on such websites is, or will remain,
accurate or appropriate.
To Lewis Anderson
Contents
List of contributors
Preface xi
1
page ix
Morphology and classification of the Marchantiophyta
BARBARA CRANDALL-STOTLER, RAYMOND E. STOTLER
DAVID G. LONG 1
2
Morphology, anatomy, and classification of the Bryophyta
BERNARD GOFFINET, WILLIAM R. BUCK
3
AND
AND
R. JOEL DUFF 139
Phylogenomics and early land plant evolution
BRENT D. MISHLER
5
A. JONATHAN SHAW 55
New insights into morphology, anatomy, and systematics of
hornworts
KAREN S. RENZAGLIA, JUAN C. VILLARREAL
4
AND
AND
DEAN G. KELCH 173
Mosses as model organisms for developmental, cellular,
and molecular biology
ANDREW C. CUMING 199
6
Physiological ecology
MICHAEL C. F. PROCTOR 237
7
Biochemical and molecular mechanisms of desiccation
tolerance in bryophytes
MELVIN J. OLIVER 269
8
Mineral nutrition and substratum ecology
JEFF W. BATES 299
vii
viii
Contents
9
The structure and function of bryophyte-dominated peatlands
DALE H. VITT
10
AND
R. KELMAN WIEDER 357
Population and community ecology of bryophytes
HAKAN RYDIN 393
11
Bryophyte species and speciation
A. JONATHAN SHAW 445
12
Conservation biology of bryophytes
ALAIN VANDERPOORTEN
Index
535
AND
T O M A S H A L L I N G B Ä C K 4 8 7
Contributors
J. W. Bates
Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire
SL5 7PY, UK.
W. R. Buck
New York Botanical Garden, Bronx, NY 10458-5126, USA.
B. Crandall-Stotler
Department of Plant Biology, Southern Illinois University, Carbondale,
IL 62901-6509, USA.
A. C. Cuming
Centre for Plant Sciences, Faculty of Biological Sciences, Leeds University,
Leeds LS2 9JT, UK.
R. J. Duff
Department of Biology, ASEC 185, University of Akron, Akron, OH 443253908, USA.
B. Goffinet
Department of Ecology and Evolutionary Biology, 75 North Eagleville Road,
University of Connecticut, Storrs, CT 06269-3043, USA.
T. Hallingbäck
Swedish Species Information Centre, Swedish University of Agricultural
Sciences, PO Box 7007, SE-750 07 Uppsala, Sweden.
D. G. Kelch
California Department of Food and Agriculture, Plant Pest Diagnostics
Laboratory, CDA Herbarium, 3294 Meadowview Road, Sacramento, CA
95832-1448, USA.
ix
x
List of contributors
D. G. Long
Bryology Section, Royal Botanic Garden, Edinburgh EH3 5LR, UK.
B. D. Mishler
University Herbarium, Jepson Herbarium, and Department of Integrative
Biology, University of California, Berkeley, 1001 Valley Life Sciences
Building #2465, Berkeley, CA 94720-2465, USA.
M. J. Oliver
USDA-ARS-MWA-PGRU, 205 Curtis Hall, University of Missouri, Columbia,
MO 65211, USA.
M. C. F. Proctor
School of Biosciences, University of Exeter, The Geoffrey Pope Building,
Stocker Road, Exeter EX4 4QD, UK.
K. S. Renzaglia
Department of Plant Biology, Southern Illinois University, Carbondale,
IL 62901-6509, USA.
H. Rydin
Department of Plant Ecology, Evolutionary Biology Centre, Uppsala
University, Villavagen 14, SE-752 36 Uppsala, Sweden.
A. J. Shaw
Department of Biology, Duke University, Durham, NC 27708, USA.
R. E. Stotler
Department of Plant Biology, Southern Illinois University, Carbondale,
IL 62901-6509, USA.
A. Vanderpoorten
Département des Sciences de la Vie Université de Liége, Sart Tilman B22,
B-4000 Liége, Belgium.
J. C. Villarreal
Department of Ecology and Evolutionary Biology, 75 North Eagleville Road,
University of Connecticut, Storrs, CT 06269-3043, USA.
D. H. Vitt
Department of Plant Biology, Southern Illinois University, Carbondale, IL
62901-6509, USA.
R. K. Wieder
Room 105, St. Augustine Center, Villanova University, 800 Lancaster
Avenue, Villanova, PA 19085, USA.
Preface
Bryophytes have gained a lot of publicity in the past 10–15 years, at least
among scientists. While there have always been those who for inexplicable
reasons have had a particular fondness for bryophytes, in academic circles
these organisms were generally viewed as just ‘‘poor relatives’’ of the more
flashy and exciting angiosperms. The bryophytes include fewer species, of
smaller stature, with more subdued colors, of less obvious ecological significance, and with apparently simpler and less exciting evolutionary stories to tell.
That view has changed.
The three major groups of bryophytes – mosses, liverworts, and hornworts –
comprise the earliest lineages of land plants derived from green algal ancestors.
Although we still do not know with certainty which of the three lineages is the
sister group to all other land plants, we do know that the earliest history of
plants in terrestrial environments is inextricably bound to the history of bryophytes. If we wish to understand fundamental aspects of land plant structure
and function, we should turn to the bryophytes for insights. These aspects
include the origin and nature of three-dimensional plant growth from apical
cells and meristems, the evolution of cellular mitotic mechanisms and machinery, the development of thick, water- and decomposition-resistant spore (and
later pollen) walls, the molecular and biochemical mechanisms underlying
desiccation tolerance, and plant genome structure, function, and evolution.
Even if our ultimate goal is to understand the structure and function of angiosperms because it is indeed those plants that feed the human world as agricultural crops, we are nevertheless wise to look more deeply into plant history for a
thorough understanding of plant unity and diversity. We cannot fully understand how evolution has tinkered with structure and function in angiosperms
without a sense of history. Although the angiosperms are impressively diverse
in numbers and structure, they are, we now know from phylogenetic insights
into plant evolution, just glorified bryophytes!
xi
xii
Preface
Although it is well established that the bryophytes do not constitute a single
monophyletic lineage, these organisms share a fundamentally similar life cycle
with a perennial and free-living, photosynthetic gametophyte alternating with a
short-lived sporophyte that completes its entire development attached to the
maternal gametophyte. There are a number of bryophytes that have variously
reduced gametophytes and/or sporophytes, and at least one liverwort that is
parasitic and non-photosynthetic, but however much the morphological details
vary from species to species, the basic bryophyte life cycle is shared among
mosses, liverworts, and hornworts. The gametophytes of many species have the
ability to replicate clonally either through specialized asexual propagules or by
fragmentation, and at sexual maturity they form multicellular female and male
gametangia, archegonia and antheridia, respectively. Water is required for
fertilization, as bryophyte sperm are flagellated and must swim to reach an
egg. Because of their life cycles, bryophytes are ideally and uniquely suited to
address some questions of fundamental significance in biology.
Sporophytes and gametophytes differ greatly in morphology, yet under some
circumstances (e.g. bryophytes with bisexual gametophytes that self-fertilize)
they differ only in ploidy: the sporophyte has the exact but duplicated genome
of the gametophyte. This alternation of haploid gametophytes and diploid
sporophytes that differ in morphology and function is one of the most basic
aspects of plant (and indeed organismal) life cycles, and control of morphological and functional differences between gametophyte and sporophyte generations has intrigued scientists since these alternating life cycles were discovered
in the nineteenth century. Given the identity in genome sequence between
isogenic sporophytes and gametophytes, differences between the generations
obviously derive from differences in gene expression rather than genetic composition. Technological advances during the past 20 years have for the first time
allowed us to begin to understand molecular processes that underlie the alternation of generations in plants, and bryophytes have proven to be invaluable
organisms for this sort of research. Yet we are only now scratching the surface in
this area of inquiry: bryophytes will continue to play a central role in new
developments.
For many years, bryophytes had a reputation of being ‘‘unmoving, unchanging sphinxes of the past’’ with little going on in terms of current evolutionary
activity. In other words, evolutionarily boring! This view has proven inaccurate.
Bryophyte species show local adaptation to heterogeneous environments,
demonstrating their responsiveness to natural selection, and have engaged in
complex speciation processes that include hybridization, polyploidization,
and morphologically cryptic genetic differentiation. Indeed, the homosporous
life cycle of bryophytes provides an opportunity for these organisms to exhibit
Preface
more – not fewer – variations in reproductive biology than is possible in heterosporous seed plants, including angiosperms. Bryophyte species with bisexual
gametophytes, those that produce both archegonia and antheridia, can undergo
true or intragametophytic self-fertilization, which results in a completely homozygous sporophyte in a single generation. This is not possible in heterosporous
plants because, unlike bryophytes, they form male and female gametes meiotically rather than mitotically. ‘‘Self-fertilization’’ in a seed plant describes the
situation in which two genetically different (albeit related) gametophytes produced from the same sporophyte mate to form the next sporophyte generation.
Bryophytes can engage in such sexual behavior as well, in addition to true selffertilization. This reproductive mode, mating between different but related
gametophytes, is commonly referred to as ‘‘selfing’’ in the seed plant literature
because of a bias in the way we view plant life cycles. Coming from an angiosperm point of view, gametophytes (e.g. pollen, embryo sacs) are seen as part of
the reproductive apparatus of the ‘‘individual’’ or ‘‘self ’’, which is the sporophyte. There is nothing objectively accurate about viewing sexual crosses
between genetically different gametophytes as ‘‘selfing’’, even if those gametophytes came from the same sporophyte. The common perception of sporophytes as individuals or ‘‘selfs’’ and gametophytes as simply parts of those
‘‘selfs’’ is an example of ploidy-ism, which can cloud our ability for insight akin
to the way racism clouds our perceptions in humanistic issues. It is just as
correct to think of a chicken as an egg’s way of reproducing itself, as the reverse!
Bryophytes offer a fresh perspective in plant reproductive biology that can
loosen the intellectual shackles of an angiosperm-centered worldview.
The second edition of Bryophyte Biology is thoroughly revised and should be
viewed as complementary to, rather than as a substitute for, the first edition.
Our goal when the first edition of Bryophyte Biology was being developed was to
produce a volume that could serve simultaneously as an intermediate to
advanced text for a bryology course, and as a reference for scientists dealing
with bryophytes in physiological, biochemical, molecular, or ecological
research. In retrospect we felt that we only partly fulfilled our goal in making
a hybrid book that serves both of these sometimes conflicting purposes. The
second edition of Bryophyte Biology is also designed to serve both functions, and
we feel that we have come closer to our goal by including new and revised
chapters that cover the breadth of subjects that should be included in a bryology
course, and that are also relevant to researchers working in other fields. As
in the first edition, every chapter provides extensive bibliographic citations
to primary literature. We consider this resource important, both for the developing student of bryology and for established scientists in some more specialized field who want to learn more about bryophytes. The first three chapters
xiii
xiv
Preface
dealing with the morphology and classification of liverworts (Chapter 1), mosses
(Chapter 2), and hornworts (Chapter 3) have expanded coverage of morphology
as appropriate for a textbook, and also have revised classifications that reflect
developments since the first edition was published. We include a new chapter
(Chapter 4) on phylogenomics, reviewing relatively recent developments from
using whole-genome characters to resolve phylogenetic relationships among
early land plants. With the growing importance of Physcomitrella patens for
molecular genetic research, Chapter 5 provides a timely overview of mosses as
model organisms. Chapters 6–12 deal with the physiology, biochemistry, ecology, evolution, and conservation of bryophytes. A new chapter (Chapter 7)
focused on desiccation tolerance in bryophytes reflects the importance of
these organisms for modern molecular and biochemical research in this area.
Desiccation tolerance is arguably the most thoroughly studied physiological
adaptation in plants, and mosses have proven to be an invaluable group of
organisms for such research. This value derives both from the relative structural
simplicity of mosses and their phylogenetic position in the land plant tree of
life. All chapters in the second edition of Bryophyte Biology are either completely
new or completely revised relative to those included in the first edition.
We hope that Bryophyte Biology, edition 2, will provide an entry for established
scientists into the literature dealing with bryophytes, and will stimulate enthusiasm among young bryology students for careers focusing on these humble but
fantastic organisms.
1
Morphology and classification
of the Marchantiophyta
b a r b a r a c r a n d a l l - s t o t l e r , r a y m o n d e . s t ot l e r a n d
d a v i d g . lo n g
1.1
Introduction
Liverworts are a diverse phylum of small, herbaceous, terrestrial plants,
estimated to comprise about 5000 species in 391 genera. They occupy an assortment of habitats, including disturbed soil along stream banks, road cuts and
trails, as well as rocks, logs and trees in natural landscapes. They occur on all
continents, including Antarctica, but are most diversified in the montane rain
forests of the southern hemisphere. Many species are quite tolerant of repeated
cycles of drying and wetting (Clausen 1964, Wood 2007), a feature that has
allowed them also to exploit epiphytic substrates, including leaves and branches
of the forest canopy. Like mosses and hornworts, they have a heteromorphic life
cycle with a sporophyte that is comparatively short-lived and nutritionally dependent on the free-living, usually perennial gametophyte. However, they differ from
both of these groups in numerous cytological, biochemical, and anatomical
features as detailed by Crandall-Stotler (1984). Significant diagnostic characters
of the phylum include the following: they tend to have a flattened appearance,
even when leafy, because their leaves are always arranged in rows, never in spiral
phyllotaxis; rhizoids are unicellular, thin-walled, and usually hyaline; both leafy
and thalloid forms frequently develop endosymbiotic associations with fungi;
sporophytes mature completely enclosed by gametophytic tissue and are incapable of self-sustaining photosynthesis; sporophyte setae are parenchymatous and
elongate by cell expansion, rather than cell division; and capsules lack the
stomates, cuticle, and columella that are common in mosses and hornworts.
Liverworts occupy a critical position in land plant evolution, forming the
sister group to all other extant land plants (e.g. Groth-Malonek et al. 2005, Qiu
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
2
B. Crandall-Stotler and others
et al. 2006). Fossil spores that are comparable to liverwort spores date back to 475
million years before present (Wellman et al. 2003), and estimates of divergence
times based on molecular evidence suggest a Late Ordovician origin for the
phylum (Heinrichs et al. 2007). Despite rather sparse representation in the fossil
record of the Paleozoic, all major (backbone) lineages of hepatics appear to have
been established by the Permian (Oostendorp 1987, Heinrichs et al. 2007).
Traditionally, liverworts have been subdivided into the marchantioid group, or
complex thalloids, and the jungermannioid group, which comprises two morphological subgroups, the anacrogynous, simple thalloids and the acrogynous, leafy
hepatics. These groups have been defined in the hierarchy of most classification
schemes and have long been viewed as natural phylogenetic units. For example, in
Crandall-Stotler & Stotler (2000) they are recognized as classes, Marchantiopsida
and Jungermanniopsida, with the latter comprising two subclasses, Metzgeriidae
(simple thalloids) and Jungermanniidae (leafy hepatics). A large suite of anatomical
and ontogenetic characters differentiates the two classes, including different
patterns of gametangial development, spermatid architecture, capsule wall anatomy (Crandall-Stotler & Stotler 2000), and mechanisms involved in defining cytokinetic planes during meiosis (Shimamura et al. 2004, Brown & Lemmon 2006).
Recent molecular phylogenetic studies (e.g. Heinrichs et al. 2005, 2007, Forrest et al.
2006, He-Nygrén et al. 2006, Qiu et al. 2006) have greatly modified this morphologybased concept, especially as regards the simple thalloid group. Whereas the
monophyly of the complex thalloids and the leafy hepatics is broadly supported
in all of these analyses, the simple thalloids are paraphyletic with representatives
in four of the six backbone clades. One of these, comprising the Haplomitriaceae
and Treubiaceae, has been identified as the earliest diverging lineage of the hepatics
and relegated to a third class, Haplomitriopsida (Forrest et al. 2006). Liverworts
are unambiguously resolved in these more recent, comprehensive multilocus
analyses as monophyletic, in contrast to earlier postulates that they are polyphyletic (Capesius & Bopp 1997, Bopp & Capesius 1998).
This chapter provides a conspectus of liverwort morphology, with emphasis
on the defining characters of the major lineages (clades) currently recognized.
Although our knowledge of morphological character diversity has changed little
since the first edition of this book, many interpretations of character evolution
within the group have been modified (e.g. He-Nygrén et al. 2004, 2006, CrandallStotler et al. 2005). A classification scheme that links morphological data with
the well-supported relationships generated in recent molecular phylogenetic
analyses is provided, with brief morphological diagnoses for the taxon ranks
above the level of family. Unless otherwise indicated, class, subclass, ordinal and
family names used in the text refer to these ranks as they are defined and
circumscribed in this classification.
1 Morphology and classification of the Marchantiophyta
1.2
Conspectus of liverwort morphology
The foundations for morphological studies in hepatics were laid in the
nineteenth century with the seminal publications of Hofmeister (1851) and
Leitgeb (1874–1881), whose comparative studies clarified the homologies
among embryophytes, and documented the structural diversity and complexity
of hepatics, respectively. Later workers, including Goebel (1893, 1895, 1912),
Douin (1912), Evans (1912), Knapp (1930), Crandall (1969) and Renzaglia (1982)
among others, have contributed additional anatomical descriptions of selected
structures across broad groups of hepatics. Nevertheless, many gaps persist in
our knowledge, with the vast majority of liverwort taxa known only at the level
of a taxonomic description. This conspectus serves to provide a general overview of what is currently known about the structural organization and diversity
of liverworts. To date, few reconstructions of morphological character state
evolution have been published, so definitive statements about evolutionary
trends in many characters cannot yet be made. Comprehensive reviews of the
comparative anatomy and morphology of hepatics can be found in Schuster
(1966, 1984a) and Crandall-Stotler (1981).
1.2.1
Apical cells and gametophyte growth
Whether leafy or thalloid, liverwort gametophytes display modular
organization, with each module composed of a series of merophytes that trace
their origin back to a single apical cell, the dynamic generative center of the
gametophyte (Hallet 1978, Crandall-Stotler 1981). All metamers derived from a
single apical cell compose a module that is a single branch or shoot (Mishler &
DeLuna 1991). Since branching is common, most plants are composed of more
than one module.
Four geometrically different types of apical cell occur within hepatics,
namely, tetrahedral (or pyramidal), cuneate (or wedge-shaped), lenticular (or
lens-shaped) and hemidiscoid types (Crandall-Stotler 1981: Fig. 1.1). As the name
suggests, a tetrahedral apical cell has four somewhat curved, triangular surfaces, one of which forms the external or free surface of the cell. The other three
surfaces, referred to as the cutting faces, are surrounded by the ranks of daughter cells generated from division of the apical cell. This type of apical cell has a
triangular outline in all planes of section (Fig. 1.1A, B), and produces merophytes
in three ranks. A lenticular apical cell has a lens-shaped free surface and two
triangular cutting faces. It produces merophytes in two lateral ranks, has a
triangular outline in both vertical and horizontal longitudinal sections, and is
shaped like a convex lens in transverse section (Fig. 1.1C, D). A cuneate apical
cell is wedge-shaped with five surfaces, a narrow, rectangular free surface, two
3
4
B. Crandall-Stotler and others
Fig. 1.1. Apical cell diversity in liverworts; apical cells are marked with asterisks. (A, B) Apices
with tetrahedral apical cells; (A) Porella platyphylla, horizontal longitudinal section, bar ¼ 25 mm;
(B) Haplomitrium hookeri, transverse section, bar ¼ 5.4 mm. (C, D) Apices with lenticular apical
cells; (C) Pallavicinia ambigua, transverse section, bar ¼ 10 mm; (D) Aneura pinguis, vertical
longitudinal section, bar ¼ 25 mm. (E, F) Apices with cuneate apical cells, Phyllothallia nivicola;
(E) horizontal longitudinal section, bar ¼ 50 mm; (F) vertical longitudinal section, bar ¼ 18 mm.
(G) Apex with a hemidiscoid apical cell, Pellia epiphylla, vertical longitudinal section,
bar ¼ 18 mm. Note the slime cells overarching the apical cell in (D–G); in Aneura (D) they form
only on the ventral surface, but in Phyllothallia and Pellia they arise from both dorsal and
ventral surfaces.
1 Morphology and classification of the Marchantiophyta
vertically aligned, triangular surfaces and two horizontally aligned, broad
rectangular surfaces. Apical cells of this type have rectangular outlines in
transverse and horizontal longitudinal sectioning planes, but triangular outlines in vertical longitudinal section (Fig. 1.1E, F). They produce merophytes in
four ranks: dorsal, ventral, and two lateral. Finally, the rather specialized hemidiscoid apical cell appears rectangular in both transverse and horizontal longitudinal sections, but has a prismatic to semicircular outline in vertical
longitudinal section (Fig. 1.1G). This type of apical cell has two lateral cutting
faces and a single basal cutting face, rather than a dorsal and a ventral face as in
the cuneate form. According to Hutchinson (1915) and Campbell (1913), respectively, in Pellia epiphylla and Sandeothallus radiculosus (= Calycularia radiculosa), the
hemidiscoid geometry is developmentally derived from a cuneate form by a
rounding out of the dorsal and ventral faces into a single, curved basal face.
Although there is substantial variation in apical cell dimensions as well as
pattern and rate of merophyte formation, typically apical cell geometry is
conserved within taxa. A tetrahedral apical cell, which has been reconstructed
as the plesiomorphic state in hepatics (Crandall-Stotler et al. 2005), is characteristic of the Haplomitriopsida and all of the Jungermanniidae, as well as select
genera of the Pelliidae. The assumption by He-Nygrén et al. (2004, 2006) that a
cuneate geometry is the plesiomorphic state and that tetrahedral geometries
have been derived independently in several lineages is not supported by analyses of character evolution. All Marchantiopsida possess cuneate apical cells,
often with lenticular types in early stages of ontogeny (Leitgeb 1881). Lenticular
apical cells are characteristic of all genera of the Metzgeriidae, with the lenticular apical cell of Pleurozia, in fact, providing the sole morphological signal of
its relationship with the Metzgeriales. Only the Pelliidae exhibit multiple apical
cell types: tetrahedral in Noteroclada, Petalophyllum, and Sewardiella; cuneate in
Makinoa, Allisonia, the Pellia endiviifolia species complex, Phyllothallia, Moerckia, and
Symphyogyna; and hemidiscoid in Calycularia, Sandeothallus, and the Pellia epiphylla
species complex.
There is no absolute correlation between plant form and apical cell type but
taxa with tetrahedral apical cells do tend to have ‘‘leafy’’ morphologies, and taxa
with hemidiscoid apical cells are always thalloid. Lenticular and cuneate apical
cells typically occur in thalloid taxa, but some leafy plants, e.g. Fossombronia and
Pleurozia, possess lenticular apical cells and others, like Phyllothallia, have cuneate apical cells (Renzaglia 1982).
Distinctive patterns of early merophyte division lead to the formation of
leaves in the Jungermanniidae and the foliar appendages and thallus wings in
the rest of the hepatics (Crandall-Stotler 1981). As verified by many workers (e.g.
Leitgeb 1875, Evans 1912, Crandall 1969), in the Jungermanniidae the first
5
6
B. Crandall-Stotler and others
division of a lateral merophyte is perpendicular to its free surface (i.e. anticlinal), partitioning the merophyte into two halves. Subsequent divisions that are
parallel to the free surface (i.e. periclinal) generate a five-celled merophyte
comprising two primary leaf and three primary stem initials; in many groups
one or both leaf initials divide again to form three or four secondary leaf initials.
Leaf growth occurs first from apical cells delimited from each of the leaf initials,
which establish the segments or lobes of the leaf, and then from a basal meristematic zone that forms the undivided lamina (Bopp & Feger 1960). The number
and size of lobes that occur in a leaf are dependent on the number of apical cells
differentiated and the relative proportion of apical to basal growth that occurs.
Leaf apical growth is terminated with the conversion of the apical cells to clubshaped papillae. If apical growth is pronounced, these papillae occur at the tips of
the leaf lobes, as in Lepidozia or Lophocolea; however, if growth is mostly from the
basal meristem, they are found near the base of the leaf, as in Jungermannia or the
dorsal lobe of Porella (Bopp & Feger 1960, Fig. 23).
In groups other than the Jungermanniidae, two successive anticlinal divisions partition the lateral merophyte into three cells, the middle one of which
forms the single wedge-shaped initial from which the thallus wing or foliar
appendages are derived (Renzaglia 1982, Bartholomew-Began 1991). The cells to
either side generate the tissues of the stem, midrib, or central portion of the
thallus. Since there is only a single foliar (or wing) apical cell per merophyte,
leaves in taxa such as Haplomitrium, Noteroclada, and Fossombronia are never
deeply lobed although they can be marginally incised owing to the activity of
secondarily produced centers of marginal growth (Bartholomew-Began 1991).
The basal meristem is established early in leaf or wing ontogeny. Leaves of this
type are polystratose at the base, often have scattered marginal papillae, and are
homologous to the wings of both simple and complex thalloid taxa. A modification of this pattern occurs in Treubia and perhaps Pleurozia. In the former, the
large lobes or ‘‘leaves’’ of the plant develop from the wedge-shaped central cell
of the three-celled merophyte and a small lobule develops from the cell dorsal to
it (Renzaglia 1982). In Pleurozia early divisions appear to produce a wedge-shaped
central cell, but subsequent leaf development is like that of a true leafy liverwort, involving multiple initials and apical cells (Crandall-Stotler 1976).
1.2.2
Oil bodies
Liverworts are distinguished from all other embryophytes by their
almost universal production of oil bodies, unique membrane-bound organelles
that synthesize and sequester a vast array of terpenoids and other aromatic
compounds (Flegel & Becker 2000, Suire et al. 2000). Oil bodies are formed during
early stages of cell maturation (Crandall-Stotler 1981) as dilatations of the
1 Morphology and classification of the Marchantiophyta
endoplasmic reticulum (Duckett & Ligrone 1995, Suire 2000) or from dictyosome vesicle fusion (Galatis et al. 1978, Apostolakos & Galatis 1998). The enclosing membrane of the oil body resembles the tonoplast in having an asymmetric,
tripartite appearance but differs from it in enzyme composition and transport
capabilities (Suire 2000). The oil body interior consists of small osmiophilic
droplets suspended in a granular stroma that is rich in proteins and carbohydrates (Pihakaski 1972, Suire 2000). Frequently, in addition to oil bodies, cells
contain dispersed lipid droplets (oleosomes) in their cytoplasm. These are droplets of triacylglycerides and neither these, nor the plastoglobules common in
plastids, are involved in or part of oil body development (Suire 2000).
In Jungermanniopsida and Haplomitrium, oil bodies are usually produced in
all cells of both the sporophyte and gametophyte generations. In these taxa
variations in oil body size, shape, color, number and distribution are taxonomically informative (Pfeffer 1874, Müller 1939, Schuster 1966, 1992a, Gradstein
et al. 1977), with five broadly defined categories recognized (Fig. 1.2). Massulaand Bazzania-type oil bodies are shiny, homogeneous, and either very small and
abundant (Massula-type) (Fig. 1.2B) or larger and fewer per cell (Bazzania-type)
(Fig. 1.2C). Oil bodies of the Calypogeia type are botryoidal, consisting of grapelike clusters of discrete, shiny globules; they can be translucent or pigmented, of
small to medium size and usually many per cell (Fig. 1.2D). Oil bodies that are
opaque, gray to gray-brown and granulose to papillose in texture (Jungermanniatype) are the most common type in the Jungermanniopsida; these can be small
and numerous per cell, or very large and solitary as in Radula (Fig. 1.2E). In
Treubia and most genera of the Marchantiopsida, oil bodies occur only in scattered idioblastic cells of the gametophyte; they are large, solitary, granular and
opaque, gray to gray-brown (Fig. 1.2F). These idioblastic ‘‘oil cells’’ differ from
the surrounding vegetative cells only by the presence of the large oil bodies in
them (Suire 2000), in contrast to earlier views that they lack chloroplasts
(Schuster 1984b).
Unfortunately, because of the volatility of the oils contained in them, oil
bodies rapidly ‘‘disappear’’ in dried specimens. In fact, their morphology is often
modified even during short-term storage in the dark, so observations of oil
body morphology must be conducted only on freshly collected samples.
Ultrastructural evidence confirms that the oil body membrane and internal
matrix remain intact for up to six weeks in dark-stored specimens, but the oil
droplets within the matrix disappear within a few days (B. Crandall-Stotler,
unpublished data).
In phylogenetic reconstructions, the presence of oil bodies is a synapomorphy of the Marchantiophyta, and oil bodies of the Massula-type are reconstructed
as the plesiomorphic state (Crandall-Stotler et al. 2005). Oil bodies have been
7
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Fig. 1.2. Cells and oil bodies of liverworts. (A) Thallus wing cells of Blasia pusilla, thin-walled
and lacking oil bodies, bar ¼ 15 mm. (B) Leaf cells of Austrofossombronia peruviana, with
inconspicuous trigones and numerous small, homogeneous oil bodies of the Massula-type,
bar ¼ 25 mm. (C) Leaf cells of Marsupella emarginata, with large, triangular trigones and large
homogeneous oil bodies of the Bazzania-type, bar ¼ 20 mm. (D) Leaf cells of Calypogeia
muelleriana, with medium triangular trigones, and botryoidal oil bodies of the Calypogeiatype, bar ¼ 20 mm. (E) Leaf cells of Radula obconica, with inconspicuous trigones and large,
solitary, papillose oil bodies of the Jungermannia-type, bar ¼ 15 mm. (F) Longitudinal section
of the thallus of Marchantia polymorpha, showing an idioblastic oil cell at the arrow,
bar ¼ 15 mm.
independently lost in several families, including the Antheliaceae,
Cephaloziaceae, Lepidoziaceae, and Metzgeriaceae of the Jungermanniopsida,
and the Blasiaceae (Fig. 1.2A), Sphaerocarpaceae, and Ricciaceae of the
Marchantiopsida (Schuster 1966, Crandall-Stotler et al. 2005).
Various hypotheses have been formulated regarding the adaptive value of oil
bodies, including suggestions that oil bodies deter herbivores and provide cold
and/or UV protection (Schuster 1966). Immunolabeling techniques have shown
that oil bodies contain enzymes involved in isoprenoid biosynthesis (Suire et al.
2000), confirming that they are active metabolic compartments of the liverwort
cell. In addition, they sequester terpenoids and other secondary aromatics,
much like the secretory glands of vascular plants (Flegel & Becker 2000).
1 Morphology and classification of the Marchantiophyta
1.2.3
Gametophyte organizations
Three very different types of gametophyte organization occur within the
phylum. The most widespread morphology is the leafy shoot, or nodal type
organization, in which the gametophyte is composed of a stem and two or
three rows of leaves. This type of organization is distributed across the phylogeny,
occurring in all of the subclasses delineated in this work (Figs. 1.3–1.7), and
characterizes almost all of the genera of the Jungermanniidae (Fig. 1.7). Simple
thalloid morphology is common in the Pelliidae (Fig. 1.5) and Metzgeriidae
(Fig. 1.6), but is also found in a few Marchantiopsida (e.g. Blasiales and Monoclea
and Monosolenium in the Marchantiales), and Jungermanniidae (e.g. Pteropsiella and
Schiffneria). In this morphology, plants consist of an unspecialized, planate thallus
that is usually composed of a somewhat thickened central midrib and two lateral
wings. In contrast, a dorsiventrally differentiated thallus, bearing a system of
dorsal air pores and air chambers and a ventral storage zone, characterizes
complex thalloid organization. This is the most restricted type of morphology,
occurring only in the Marchantiidae (Fig. 1.4). Since the variation that occurs in
each of these morphological categories employs a different suite of descriptors,
they will be discussed separately. It should be noted, however, that leafy, simple
thalloid and complex thalloid categories do not necessarily imply natural groupings, but simply refer to a type of morphological organization.
Variation in leafy morphologies
Multiplicity in the distribution, form, size and insertion of leaves provides many of the characters that define genera and species of foliose liverworts.
In Haplomitrium (Fig. 1.3) and a few genera of the Jungermanniidae, e.g., Herbertus
and Lepicolea, plants are erect and radially symmetric with three ranks of identical leaves (isophylly). The vast majority of leafy forms, however, display bilateral symmetry in which plants bear two rows of lateral leaves with or without a
single row of smaller ventral leaves or underleaves (= amphigastria). In anisophyllous taxa the underleaves can be morphologically like the leaves, but
smaller, or differ both in size and morphology. In traditional classification
schemes, isophyllous taxa were considered primitive and evolution was presumed to progress toward planation and anisophylly (e.g. Evans 1939, Stotler &
Crandall-Stotler 1977, Schuster 1984b). Recent phylogenetic hypotheses derived
from sequence data suggest, however, that isophylly is a derived state (Davis
2004, Crandall-Stotler et al. 2005, He-Nygrén et al. 2006).
With a few exceptions, such as Pachyglossa and Herzogiaria, leaves in the
Jungermanniidae are completely unistratose, whereas those of Treubia, Haplomitrium, and leafy taxa of the Pelliidae and Marchantiopsida are polystratose for
9
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Fig. 1.3. Characters of the Haplomitriopsida. (A) Treubia lacunosoides, dorsal view,
showing the lobate thallus and small dorsal lobules (at arrow) associated with each
thallus lobe, bar ¼ 4 mm. (B–D) Representatives of three lineages of Haplomitrium. (B) Male
shoots of Haplomitrium gibbsiae (subg. Haplomitrium sect. Archibryum), arising from a slimecovered stolon system; antheridia are clustered at the apices of the leafy shoots. This
species is sister to all other species in the genus, bar ¼ 1.5 mm. (C) Male shoot of
Haplomitrium hookeri (subg. Haplomitrium sect. Haplomitrium), showing antheridia
(arrow) in the axils of unmodified leaves just below the shoot apex, bar ¼ 300 mm. (D)
Haplomitrium mnioides (subg. Calobryum), dorsal view; note the branched, leafless stolon
system and anisophyllous shoots, with the smaller third row of leaves on the dorsal side,
bar ¼ 2 mm.
1 Morphology and classification of the Marchantiophyta
Fig. 1.4. Characters of the Marchantiopsida. (A) Asterella tenella, lateral view of a
carpocephalum, showing the pseudoperianth (at arrow) emerging from a tubular
involucre, bar ¼ 2.6 mm. (B) Conocephalum conicum, dorsal view, showing hexagonal
outlines of the air chambers and a conical carpocephalum; a tubular involucre (at arrow)
encloses the nearly mature sporophyte, bar ¼ 2 mm. (C) Monoclea gottschei, dorsal view; oil
cells appear as scattered white dots throughout the thallus, bar ¼ 5 mm. (D, E) Marchantia
polymorpha, longitudinal sections of gametangiophores, bars ¼ 1 mm: (D) antheridiophore
with antheridium indicated by arrow; (E) archegoniophore with archegonium indicated by
arrow.
several cell rows at the base, gradually becoming unistratose distally. They are
generally composed of a uniform network of isodiametric to slightly elongate
chlorophyllous cells with thin or unevenly thickened walls (Fig. 1.2). Trigones, the
corner wall thickenings between leaf cells (Fig. 1.2C), consist mostly of hemicelluloses (Zwickel 1932) and are important in the apoplastic conduction of water
(Proctor 1979). In some taxa the surface walls are roughened with papillae,
granulae, or striae. Although these are treated as cuticle markings in taxonomic
descriptions, they are actually projections of the wall proper, not waxy deposits
(Duckett & Soni 1972). To date, there is no unequivocal evidence that a true cuticle
exists in jungermannioid liverworts (Cook & Graham 1998). Occasionally, idioblastic oil cells, or ocelli, are interspersed among the normal leaf cells, e.g., some
species of Frullania, or a line of highly elongate, thick-walled cells forms a vitta or
nerve in the leaf as in Herbertus.
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Fig. 1.5. Characters of the Jungermanniopsida, subclass Pelliidae. (A) Noteroclada confluens, dorsal
view, plants with undivided succubous leaves and two rows of naked archegonia on the midrib,
bar ¼ 2.3 mm. (B) Pellia epiphylla, dorsal view, showing acrogynous perichaetium (at arrow)
positioned between furcate thallus branches, bar ¼ 3 mm. (C) Allisonia cockaynei, dorsal view, male
plant with a cluster of antheridia and perigonial scales near thallus apex, bar ¼ 2 mm. (D)
Phyllothallia nivicola, dorsal view, with developing perichaetia and archegonia (at arrow) at node,
between a pair of opposite leaves, bar ¼ 1.5 mm. (E) Jensenia connivens, illustrating a dendroid
thallus habit; note the sporophyte emerging from a perichaetial pseudoperianth to the
right, bar ¼ 1.1 mm.
Leaves are commonly lobed or divided in the Jungermanniidae, but undivided leaves characterize some families, such as the Jungermanniaceae and
Plagiochilaceae, as well as Haplomitrium (Fig. 1.3) and the foliose taxa of the
Pelliidae (Fig. 1.5) and Marchantiopsida. Divided leaves can be bifid, trifid,
quadrifid, multifid, or bisbifid, i.e., having the two lobes of a bifid leaf themselves less deeply divided into two lobes (see e.g. Schuster 1984a, Fig. 15). In
addition, lobe margins may be ciliated or toothed, as in Trichocolea, which
1 Morphology and classification of the Marchantiophyta
Fig. 1.6. Characters of the Jungermanniopsida, subclass Metzgeriidae. (A) Pleurozia acinosa,
showing leafy shoots with abundant tubes, often referred to as sterile gynoecia, on abbreviated
lateral branches, bar ¼ 1.8 mm. (B) Metzgeria leptoneura, ventral view, illustrating hyaline hairs
on the involute wing margins and midrib, bar ¼ 2.1 mm. (C) Aneura pinguis, male plants bearing
numerous androecia, each on an abbreviated lateral branch, bar ¼ 6 mm. (D) Verdoornia
succulenta, female plants with a gynoecium on the dorsal surface of the thallus (at arrow),
bar ¼ 4 mm.
enhances the uptake and ectohydric transport of water by creating capillary
spaces between leaves. Lobes can be equal in size and symmetric, as in many
genera of the Lepidoziaceae, or different in size, shape and even form, as in most
genera of the Porellales. Lobe number and size are established early in leaf
ontogeny and may prove to be phylogenetically informative (Bopp & Feger
1960, Schuster 1984a). In the Porellales and some Jungermanniales, e.g.,
Schistochilaceae and Scapaniaceae, leaves are complicate-bilobed, meaning
that the asymmetrically bifid leaves are longitudinally folded so that the smaller
lobe, or lobule, is appressed to either the dorsal or ventral surface of the larger
lobe. Although usually described as complicate-bilobed, leaves in many, but not
all, of the Porellales are actually trifid, consisting of a dorsal lobe, ventral lobule
and small ventral stylus. According to Heinrichs et al. (2005) and He-Nygrén et al.
(2006), this trifid type of organization is fundamental to the Porellales. However,
leaves in both Porella and Radula are truly bifid, as demonstrated by Bopp & Feger
(1960) and Leitgeb (1871a), respectively.
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Fig. 1.7. Characters of the Jungermanniopsida, subclass Jungermanniidae. (A) Bazzania novaezelandiae, illustrating an incubous leaf insertion, bar ¼ 2.5 mm. (B) Proskauera pleurata,
illustrating a succubous leaf insertion and terminal, pluriplicate perianths (at arrow),
bar ¼ 1.4 mm. (C) Balantiopsis rosea, lateral view, immature, hollow marsupium of the
Calypogeia-type, bar ¼ 800 mm. (D) Megalembidium insulanum, dendroid plant with extensively
branched rhizome system, bar ¼ 3 mm. (E) Male plants of Tylimanthus saccatus, illustrating a
terminal androecium and succubous leaf arrangement, bar = 1.25 mm. (F) Isotachis lyellii,
with an erect stem perigynium bearing a highly reduced perianth at its apex (at arrow),
bar ¼ 750 mm.
Frequently, in complicate leaves the lobules form inflated water sacs, which
are of two developmentally different types. In the Lejeunea-type water sac, cell
divisions restricted to just below the free margin of the lobule enroll it against
the lobe. The mouth or opening of the water sac is directed towards the leaf
apex. The water sac is confluent with the lobe for most of its length and has a
long, vertical line of insertion on the stem (Crandall 1969, Fig. 91). This type of
water sac is characteristic of the Lejeuneaceae, the largest family of liverworts,
but is also found in Trichocoleopsis (Neotrichocoleaceae), Nowellia (Cephaloziaceae),
Tetracymbaliella (Lophocoleaceae) and Delavayella (Delavayellaceae). The galeate or
Frullania-type water sac, in contrast, is inflated medially, like a balloon, from cell
1 Morphology and classification of the Marchantiophyta
divisions restricted to the middle of the lobule. The free margins are not enrolled,
but instead are constricted around the mouth, which is usually directed downwards. The water sac is scarcely confluent with the lobe but is joined to the stylus
that in turn is attached to the stem (Crandall 1969, p. 97). This second type of
water sac occurs in several families of the Porellales, including the Lepidolaenaceae and Frullaniaceae, and in Neotrichocolea (Neotrichocoleaceae, Ptilidiales).
The water sac of Pleurozia is unique in developing through a combination of
marginal enrolling and ballooning processes and differentiating a flap-like valve
that opens or closes the mouth in response to hydration levels (Crandall-Stotler
1976). Water sacs enhance the uptake of water during periods of hydration, but
appear to quickly lose water with drying (Blomquist 1929, Proctor 1979), so they
probably do not function in water storage, except perhaps in the valvate types
found in Pleurozia and Colura (Schuster 1966). It has also been suggested that small
invertebrates that inhabit the water sacs may provide nitrogenous compounds to
the mostly epiphytic taxa that bear them (Verdoorn 1930, Hess et al. 2005).
Underleaves are always transversely inserted and have their laminae
appressed to the ventral surface of the stem. Lateral leaf insertions are variable,
with the fundamental line of insertion dependent upon the orientation of the
shoot apical cell (Buch 1930, Crandall 1969). If the medial axis of the apical cell is
vertically aligned with the center of the shoot, leaves will be transversely
inserted as occurs in erect-growing, isophyllous taxa, e.g. Haplomitrium
(Fig. 1.3B, C) and Herbertus, as well as a few prostrate taxa, e.g. Cephaloziella. In
most prostrate taxa the medial axis of the apical cell is tilted and leaves are
obliquely inserted; a dorsal tilt results in a succubous insertion and a ventral tilt
in an incubous insertion. In both of these insertions, the leaf lamina extends
horizontally out from the stem. In plants with a succubous insertion, the shoot
apex bends up, away from the substrate, the lower or basiscopic margin of the
leaf is inserted on the dorsal side of the stem, and the adaxial surface of the leaf
is dorsal (Fig. 1.7B, E). In contrast, in plants with an incubous insertion, the shoot
apex bends down toward the substrate, the upper or acroscopic margin of the
leaf is inserted on the dorsal side of the stem, and the abaxial surface of the leaf
is dorsal (Fig. 1.7A). In complicate leaves, lobe and lobule insert differently,
resulting in an oblique J- or U-shaped line of insertion. Succubous insertions
tend to occur in taxa that grow on moist, soil substrates, whereas incubous
insertions seem to be more common in epiphytes. Clee (1937) postulated that
succubous insertions favor water movement from below, whereas plants with
incubous insertions are better adapted to capturing water flowing from above.
Schuster (1966) suggests that incubous and especially incubous-complicate
leaves can be more tightly overlapped or shingled than succubous leaves and
are hence better adapted to retaining water in their ventral lobules. This
15
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B. Crandall-Stotler and others
inherent ability of incubous taxa to limit water loss may contribute to the
widespread success of the Porellales as epiphytes.
The stems of leafy liverworts are relatively unspecialized, consisting mostly
of parenchymatous cells. However, in some genera, like Plagiochila and Herbertus,
the outer three or four layers of cells, including the epidermis, are thick-walled
and prosenchymatous as compared to the cells of the interior, and in others, like
Lejeunea and Cephalozia, the epidermis is replaced by a hyalodermis of highly
inflated, thin-walled cells. In the Treubiaceae and Scapaniaceae, cells in the
ventral part of the stem form a distinct mycorrhizal zone, and in Goebeliella all
cells of the stem are prosenchymatous. Among leafy forms, only Haplomitrium
possesses a central strand of elongate, hydrolyzed ‘‘conducting’’ cells; these are
smaller in diameter than the surrounding cells of the cortex, thin-walled, and
minutely perforate. Note that in the absence of substantial anatomical differentiation the outer zone of shorter stem cells is often referred to as a cortex and
the inner zone of more elongated cells as a medulla. For consistency with other
plant groups, however, we suggest that the terms epidermis, cortex, and central
strand be applied to hepatics, as defined in Magill (1990).
Rhizoids are typically found on the ventral surface of the plant, developing
from either specialized cells of the underleaves or the stem epidermis. They are
generally hyaline, although deeply pigmented rhizoids are diagnostic of some
genera, e.g. Fossombronia, Herzogianthus, and Schistochila. In Radula rhizoids are
formed from the center of the ventral lobules of the leaf, but in most taxa that
lack underleaves, rhizoids are widely scattered on the ventral surface of the
stem, as in Jungermannia. In some taxa, like Megalembidium and Pleurozia, they are
restricted to stoloniferous or rhizomatous branches (Fig. 1.7D). In many epiphyllous Lejeuneaceae, the rhizoid initials form a sucker-like disc on the underleaf
that firmly attaches the liverwort to its substrate. In fact, the primary function of
rhizoids seems to be substrate attachment, but an important secondary function
may be to host symbiotic fungi, as demonstrated by Duckett et al. (1991). Such
mycorrhizal rhizoids have swollen, branched tips. Among liverworts, only
Haplomitrium completely lacks rhizoids.
Branching systems can be furcate or superficially dichotomous (e.g. Bazzania
and Fossombronia) or sympodial with formation of subfloral innovations (e.g.
Scapaniaceae) or more commonly monopodial (Buchloh 1951). Often branch
modules are heteroblastic so that the first-formed leaves or appendages at the
base of the branch are morphologically distinct from those differentiated from
subsequent merophytes. The form of these modified first-branch leaves and
underleaves can be systematically informative, as demonstrated repeatedly
in studies of the Frullaniaceae (Verdoorn 1930, Stotler 1969, von Konrat &
Braggins 2001). Branches may resemble the main stem, or be differentiated as
1 Morphology and classification of the Marchantiophyta
microphyllous shoots, flagellae, or stolons. In a few taxa, e.g. Bryopteris and
Megalembidium (Fig. 1.7D), a dendroid, monopodial leafy shoot system arises
sympodially from a creeping rhizome or caudex that is attached to the substrate.
Twelve patterns of branch ontogeny, based on differences in the delineation
of the branch initial and/or early stages of bud differentiation, have been
described (Crandall-Stotler 1972, Thiers 1982). As first recognized by Leitgeb
(1871b, 1872), these patterns can be classified into three groups based on the
spatial relationship between the branch and the shoot apex, namely (1) terminal
with stem leaf modified, (2) terminal with stem leaf unmodified, and (3) intercalary. In the first group, which includes branches of the Frullania-, Kurzia(= Microlepidozia) and Acromastigum-types, the branch apical cell is formed very
near the shoot apex from an outer cell, or ‘‘segment half ’’, of the three-celled
merophyte, thereby restricting leaf development to half of its usual initials.
Consequently, a half-leaf (or -underleaf) develops on the stem at the position of
branch emergence. In Frullania-type branches, which are the most common type
in this group, the branch replaces the ventral part of the leaf. The degree of halfleaf modification varies greatly among taxa; e.g. in Frullania the half-leaf lacks a
lobule and stylus, whereas in Chiloscyphus, it is only slightly reduced in size but
lacks insertion on the ventral side of the stem (Crandall 1969, Fig. 248).
In the second group of terminal branches, the branch begins development
very close to the apex but from an epidermal cell that is basiscopic to a leaf
primordium. Leitgeb (1871b) described this as the Radula pattern, but branches
of the Bryopteris-, Lejeunea-, Aphanolejeunea- and Fontinalis-types [Fontinalistype ¼ Haplomitrium-type of Schuster (1966)] also belong to this group. Since
the branch initial is differentiated later in merophyte development, leaf morphology is unaffected by branch formation. In Fontinalis-type branching, one or
more stem cells occur between the branch primordium and the basiscopic
insertion of the stem leaf, but in the other types in this group, the stem leaf
partially inserts on the upper side of the branch. In Radula-type branching,
branch growth by apical cell segmentation begins near the shoot apex so
there is synchronous maturation of stem and branch tissues along a 45–608
angle of branch divergence (Crandall-Stotler 1972, Fig. 23). In the other types,
the branch usually remains as a bud or primordium to some distance below the
shoot apex. Since branch maturation occurs after the stem cells have elongated,
the tissues of the branch appear to abut those of the stem at a 908 angle
(Crandall-Stotler 1972, Fig. 52). In branches of the Lejeunea- and Bryopteris-types
a layer of tissue derived from the basiscopic part of the leaf in the former, or by
longitudinal division of the branch initial in the latter, internalizes the branch
primordium prior to branch apical cell formation. When growth resumes, the
branch pushes through this tissue, leaving it as a collar at its base. These
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B. Crandall-Stotler and others
branches mimic intercalary branches in their production of basal collars even
though they originate from epidermal cells.
In contrast to Lejeunea- and Bryopteris-type branches, intercalary branches
develop from undifferentiated cells of the stem cortex usually near the axils of
leaves (lateral intercalary or Plagiochila- and Anomoclada-types) or underleaves
(ventral intercalary or Bazzania-type). Grolle (1964) first applied type names to
these patterns; they are equivalent to the Lophozia-, Andrewsianthus- and postical
intercalary types of Schuster (1966, p. 445). Although the enlarged, usually
rounded initials of intercalary branches are actually formed near the shoot
apex, they remain dormant until some distance below the meristematic zone.
In some cases, in fact, they do not break dormancy unless the stem apex is
physically destroyed or replaced by a gynoecium (Crandall 1969). When dormancy is broken and the branch bud begins to grow, the contiguous epidermal
cells divide to form a bulging cover layer. This epidermal tissue is subsequently
torn when the branch elongates, forming a collar at the branch base. The tissues
of the branch abut the main axis at a 908 angle, but are more deeply inserted into
the cortex than occurs in the exogenous types described above.
Dormant branch initials and/or primordia provide a mechanism for replacing
a damaged shoot apex, but in Cephalozia, Blepharostoma, and Radula this potential
is supplemented by formation of adventive branches (Evans 1912, Hollensen
1973, Crandall-Stotler 1981). Adventive branches originate from mature epidermal cells that dedifferentiate. They resemble stem regenerants in being easily
detached from the stem, but otherwise look like normal branches. To date, they
are known from only a few taxa.
The majority of leafy liverworts are dioicous, but there are also monoicous
taxa, especially those with Laurasian distributions (Longton & Schuster 1983).
Both archegonia and antheridia develop from superficial cells near the apex of a
stem or branch. In general, antheridia consist of a spheroidal to ovoidal or
occasionally ellipsoidal body and subtending stalk. The body is usually white,
but bright orange to yellow antheridia are characteristic of some genera, e.g.
Fossombronia and Haplomitrium (Fig. 1.3C). Typically the jacket cells are randomly
arranged and the stalk is short, straight and biseriate. Systematically important
variation does, however, occur as detailed in Müller (1948). For example, the
stalk is four- to seven-seriate in several genera, including Schistochila,
Haplomitrium, and Fossombronia, and is characteristically uniseriate in most
Porellales. Tiered jacket cells are diagnostic of the Cephaloziaceae and some
Calypogeiaceae and Lepidoziaceae as well as select species of Haplomitrium
(Schuster 1966, Bartholomew-Began 1991).
In the Jungermanniidae, Haplomitriopsida, and Pleurozia, antheridia develop
in the axils of modified perigonial leaves and rarely underleaves, referred to as
1 Morphology and classification of the Marchantiophyta
male bracts and bracteoles, respectively. The number of antheridia per bract
varies from one or two in many groups, e.g. Lejeuneaceae, to over 100 in
Schistochilaceae; sometimes the antheridia are intermixed with paraphyllia,
e.g. Scapaniaceae. In Treubia and some species of Haplomitrium, androecia are
rather loosely organized, with bracts dispersed along the stem and scarcely
modified from the vegetative leaves (Fig. 1.3C). In most leafy taxa, however,
male bracts are smaller than vegetative leaves and ventricose at the antical base
(Fig. 1.7E). Androecia may terminate the main stem or leading branch, or be
intercalated between vegetative segments, as in the Plagiochilaceae, or be
restricted to spicate to capitate branches, e.g. Pleurozia and most Porellales.
A disciform, splash-cup type of androecium, consisting of three enlarged bracts
surrounding up to 100 antheridia and intermixed slime hairs on a terminal
receptacle, occurs only in Haplomitrium subg. Calobryum. In the leafy members of
the Pelliidae (Fossombronia, Noteroclada, and Phyllothallia) and Marchantiopsida
(Sphaerocarpales), the androecium is usually diffuse on the dorsal surface of
the stem and there is no association between the antheridia and leaves. For
example, in Fossombronia the antheridia are spread out along the stem and are
naked or subtended individually by a single perigonial scale. Noteroclada and
Sphaerocarpos produce rows of antheridia, each enclosed in a flask-shaped involucre, and Phyllothallia forms clusters of antheridia intermixed with perigonial
scales and slime hairs.
There are two schemes of gynoecial formation in hepatics. In acrogynous
liverworts the apical cell of the reproductive module is eliminated during
archegonial formation and consequently, the gynoecium terminates further
growth of the module. In anacrogynous liverworts, the apical cell of the reproductive module is unaffected by archegonial production, and the module continues to grow past the gynoecium. Acrogynous taxa produce a single
gynoecium per module, while anacrogynous taxa can produce a succession of
gynoecia along the dorsal surface of the module. Within acrogynous taxa,
gynoecia can terminate a sparingly branched main stem, or normal leafy
branches, or be restricted to short branches that lack vegetative leaves, simulating acrocarpy, cladocarpy, and pleurocarpy, respectively.
All Jungermanniidae are acrogynous and most Haplomitriopsida are anacrogynous, the only exception being Haplomitrium subg. Calobryum. Of the leafy taxa
in other clades, only Pleurozia is acrogynous. In Fossombronia and Noteroclada,
archegonia are naked and dispersed dorsally on the stem (Fig. 1.5A), but in
most liverworts they are clustered and protected by foliar structures
(Fig. 1.5D). In Treubiaceae and Haplomitrium subg. Haplomitrium, small groups
of archegonia are scattered in the axils of unmodified leaves near the shoot
apex, but in other species of Haplomitrium 20–100 archegonia are intermixed
19
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B. Crandall-Stotler and others
with slime hairs and scales on a terminal disc-like receptacle, surrounded in
turn by one or two cycles of small inner bracts, and enlarged outer bracts. In the
Jungermanniidae several cycles of modified leaves and underleaves, the perichaetial or female bracts and bracteoles, are produced prior to archegonial
development. The perichaetia bear numerous marginal slime papillae and are
more highly divided than the vegetative leaves. In most Jungermanniidae, the
last cycle of perichaetial leaves/underleaves fuse, forming a very short tubular
perianth just to the outside of the archegonial cluster (Schuster 1966, Fig. 9–9).
Prior to fertilization, the perichaetia shield the archegonia and provide capillary
channels for water movement into the gynoecium. Although bracts and bracteoles usually enlarge without fertilization, perianths typically remain vestigial
in the absence of embryo formation.
Most leafy liverworts are capable of regenerating from fragments of leaves or
stems but many liverworts also produce special asexual diaspores for vegetative
reproduction and dispersal. These include caducous leaves, small branchlets, or
cladia, multicellular discoid gemmae, and one- to few-celled, catenate gemmae
that arise in fascicles from embryonic leaves. The first three types of broodbodies occur primarily in epiphytic taxa and are consequently most prevalent in
the Porellales; the last type is restricted to the Jungermanniales (Schuster 1966).
Variation in simple thalloid morphologies
Simple thalloid morphologies vary from broad thalli with a distinct,
multistratose midrib and unistratose wings, as in most of the Pallaviciniaceae,
to strap-shaped thalli that are multistratose throughout, e.g. Riccardia, or rarely,
thalli that are completely unistratose, e.g. Mizutania (Figs. 1.5, 1.6). Thalli are
bilaterally symmetric and usually prostrate, but can also be ascending to erect,
as in Jensenia (Fig. 1.5E) and Hymenophyton. In the Pallaviciniales, the thallus often
arises from a wingless, cylindrical stipe that is embedded in the substrate.
Rhizoids that are structurally like those of leafy liverworts are usually dispersed
along the ventral surface of the midrib, but may also be produced from cells of
the wing margin, especially in the Metzgeriidae.
The ventral surface of the midrib at the thallus apex frequently elaborates
two or more rows of foliose scales (e.g. Petalophyllaceae, Calyculariaceae,
and Blasiaceae), uniseriate hairs (e.g. Allisoniaceae, Moerckiaceae, and
Makinoaceae), or stalked slime papillae (e.g. Hymenophytaceae and
Metzgeriaceae). Scales and hairs typically persist for a considerable distance
below the apex, but slime papillae are usually seen only near the apex (e.g.
Monoclea and Pellia, Fig. 1.1G); they may be distributed in two rows on the midrib,
as in the Hymenophytaceae and Metzgeriaceae, or be widely dispersed on both
dorsal and ventral surfaces of the thallus as in some Pallaviciniaceae. In a few
1 Morphology and classification of the Marchantiophyta
taxa of the latter, slime papillae may also occur along the wing margins. The
Blasiidae are unique in having two rows of Nostoc-containing auricles derived
from slime hairs that lie to the inside of the two rows of persistent ventral scales.
In most simple thalloid taxa, cells of both the central polystratose midrib
(= costa), and the thallus wings are uniformly chlorophyllose and thin-walled,
without conspicuous trigones. However, in Cavicularia (Marchantiopsida) and
most taxa of the Pallaviciniales strands of differentiated, elongate cells are
formed in the thallus midrib. These strand cells are smaller in diameter than
the surrounding thallus cells, devoid of protoplasm at maturity, and hypothesized to function as water reservoirs or conduits. In Hymenophytaceae and
Pallaviciniaceae the strand cells possess thick, pitted, and finely perforate
walls (Ligrone & Duckett 1996), whereas in Moerckia and Cavicularia they are
thin-walled and unperforated (Hébant 1977, Kobiyama 2003). Strand cells in
Hattorianthus have uniquely thickened walls, but lack both pits and perforations
like Moerckia (Kobiyama 2003, Murray & Crandall-Stotler 2005).
Branching is predominantly terminal, with thallus apices appearing to bifurcate or dichotomize (Crandall-Stotler 1981, Renzaglia 1982). In only a few simple
thalloid taxa (e.g. Pellia) are these bifurcations true dichotomies as in the
Marchantiopsida. In most taxa the branch apical cell arises exogenously from
the central cell of the three-celled merophyte, yielding a false dichotomy. In
many Pallavicinaceae, in addition to terminal furcations, dormant branch primordia are produced just ventral to the wing from epidermal cells of the midrib.
Such branch primordia can generate a sympodial branching habit, with ventral
exogenous intercalary branches arising near the base of the main thallus, as in
Pallavicinia and Jensenia, or they may form short ventral androecial or gynoecial
branches, as in Podomitrium and Hymenophyton. Among simple thalloid taxa, only
Metzgeriaceae form ventral endogenous branches as well as ventral exogenous
branches and terminal furcations. Monopodial branching habits of vegetative
thalli are common only in the Aneuraceae (Fig. 1.6C).
Simple thalloid taxa are often sexually dimorphic, with male thalli smaller
than the female (Renzaglia 1982, Table 2). As in leafy taxa, antheridia vary in
color, stalk size and jacket cell orientation. They are arranged in two or more
rows (e.g. Pallavicinia), or aggregated in clusters (e.g. Allisonia, Fig. 1.5C), on the
dorsal surface of the midrib, and are either associated with perigonial scales or
contained in flask-shaped, ostiolate perigonial chambers. Androecia of
Podomitrium, Hymenophyton, Metzgeriaceae, and Aneuraceae (except Verdoornia)
are restricted to short exogenous branches that are lateral in Aneuraceae, but
otherwise ventral. Monoclea (Fig. 1.4C) and Monosolenium, which are best interpreted as complex thalloid plants that have lost their air chambers, have
androecial organizations comparable to those of other complex thalloid taxa.
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B. Crandall-Stotler and others
Most simple thalloid liverworts are anacrogynous, having their archegonia
and perichaetial scales aggregated on small receptacles posterior to the thallus
apex along the dorsal surface of the midrib. In Pellia most species are anacrogynous, but in Pellia epiphylla the gynoecium and subsequently formed sporophyte
terminate the growth of the original thallus module (Fig. 1.5B) and a new apical
cell is formed to either side of the young gynoecium (Renzaglia 1982). Thus, this
species is actually acrogynous. Other acrogynous simple thalloid taxa include
those that produce their gynoecia on short, determinate branches. This feature
is characteristic of Metzgeriidae (except Verdoornia), as well as Podomitrium and
Hymenophyton of the Pelliidae and the simple thalloid taxa of the
Jungermanniidae. Archegonial characters are mostly taxonomically uninformative, but distinctive archegonia having extremely short, thick necks are diagnostic of the Metzgeriales as here defined (Crandall-Stotler et al. 1994). In most
simple thalloid taxa the archegonia and intermixed slime hairs or papillae are
subtended by one or more series of laciniate to dentate, leaf-like scales or
perichaetia. In some, e.g. Pallavicinia and Moerckia, an additional short, tubular
perichaetium encircles the archegonial cluster, just to the inside of the much
larger perichaetial scales. This tubular structure, deemed analogous to the
perianth of the Jungermanniidae, has been termed an inner involucre, inner
perichaetium, or more commonly a pseudoperianth (Schuster 1992b). The term
pseudoperianth has, however, also been applied to two non-homologous structures, including perianth-like enclosures that originate only after fertilization as
in Calycularia, and the envelope that develops from the archegonial stalk in
Marchantiidae, e.g. Asterella (Fig. 1.4A). The term involucre has also been loosely
applied, and in complex thalloid liverworts refers to tissue of thalline origin that
encloses the cluster of archegonia (Bischler 1998) (Fig. 1.4B). Crandall-Stotler
et al. (2002) resurrected the term caulocalyx from Chalaud (1928) to replace the
term pseudoperianth for post-fertilization structures of thalline origin and
reserved the term pseudoperianth for structures derived from the inner perichaetium. Until an ontology is completed for the Marchantiophyta, we suggest
that in simple thalloids the term pseudoperianth be accompanied by the modifier ‘‘perichaetial’’ to differentiate it from the pseudoperianth of the
Marchantiidae and that the term involucre should be restricted to gynoecial
structures of thalline origin in the Marchantiopsida.
Special asexual diaspores are formed by only a few simple thalloid taxa. In
Riccardia 1- or 2-celled gemmae are formed endogenously, i.e. within the walls of
existing cells, at the thallus apex. This rare type of asexual diaspore has also
been described in Jungermannia caespiticia (Buch 1911). Exogenously produced,
shortly stalked, multicellular, bulbous gemmae occur in Blasiales, Treubiaceae,
Aneura, and Xenothallus; fragile brood branches, or cladia (sometimes referred to
1 Morphology and classification of the Marchantiophyta
as gemmae) are common in Metzgeria and Greeneothallus. Subterranean tubers
provide a means of both perennation and vegetative propagation in
Petalophyllaceae, as well as in the related leafy taxa, Fossombronia and
Noteroclada.
Variation in complex thalloid morphologies
Liverworts with complex thalloid morphologies are normally terrestrial, with a few aquatic species (Riccia and Ricciocarpos). Many are xeromorphic,
drought-resistant and able to withstand strong insolation. Many gametophyte
characters seem to be environmentally modulated. The thallus is a dorsiventrally flattened, prostrate to suberect, usually bilaterally symmetric shoot
(Fig. 1.4); it is mostly multistratose apart from the wings, which may be marginally unistratose. The lower surface often has a prominent midrib on which are
borne rhizoids and ventral scales. The thallus shows three types of branching:
terminal innovations that appear as constrictions in the thallus due to seasonal
cessation of growth and subsequent new growth from the same or a new apical
cell; terminal dichotomies or furcations, which may be symmetric or asymmetric; and ventral intercalary branches, which arise exogenously from the
lower epidermis of the midrib as in simple thalloids and have a characteristic
stipitate base.
Complex thalloids by definition show internal differentiation into a dorsal
epidermis with air pores, an assimilatory (photosynthetic) layer with air chambers and a ventral non-photosynthetic layer without air chambers. The epidermis is unistratose, with or without chloroplasts, and the air pores can be simple,
with surrounding cells undifferentiated, e.g. Riccia, highly differentiated with
several rings of narrow cells, e.g. Conocephalum (Fig. 1.4B), or compound (barrelshaped) as in Neohodgsonia and Marchantiaceae. In Dumortiera air pores are
vestigial. The assimilatory layer contains air chambers, which may be tall and
columnar, broad and spreading, or irregular and spongy, with more than one
type in a single thallus in some genera. They are bounded by unistratose walls of
chlorophyllose cells and sometimes contain free-standing chlorophyllose filaments (Fig. 1.2F). Evans (1918) classified them into three types, Riccia-type
(columnar), Reboulia-type (spreading, more than one layer) and Marchantia-type
(spreading with free-standing filaments). Bischler (1998) showed that different
types of air chambers can occur in a single genus; for example, in Riccia the
assimilatory layer can be absent and air chambers, when present, can be either
Riccia-type or Reboulia-type. In Monocarpus the air chambers are completely open
dorsally and in Dumortiera they are vestigial.
The ventral tissue is usually multistratose in the thallus midrib, but can
be reduced to only ventral epidermis in the thallus wings, or in a few taxa,
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B. Crandall-Stotler and others
e.g. Cyathodium, reduced throughout. This layer is composed of achlorophyllose
cells with thin, sometimes pitted walls, and may contain mucilage cavities and
mycorrhizal fungal hyphae. The ventral epidermis is scarcely differentiated and
in the median part of the midrib bears both unicellular rhizoids and ventral
scales. In most genera ventral rhizoids are dimorphic, with typical smooth
rhizoids and pegged rhizoids with intracellular wall projections.
Ventral scales are unistratose, foliose structures borne mostly in two rows (up
to eight rows in Bucegia and Marchantia or in ill-defined rows in Cleveaceae,
Ricciocarpos, and Corsinia), with or without an apical appendage and often with
oil cells and marginal slime papillae (Bischler 1998). Their function may be
water conduction by capillary action as well as affording protection to the apical
cell and, in some xeromorphic taxa (e.g. Riccia, Targionia, Plagiochasma), to the
rolled-up thallus.
Complex thalloid species are dioicous and monoicous in approximately equal
proportions (Bischler 1998). Many genera such as Asterella, Athalamia, Cyathodium,
and Riccia contain both monoicous and dioicous species. Monoicous species
usually bear antheridia and archegonia on different branches, and display distinctive sexual conditions that are species-specific, as in Asterella (Long 2006a).
Gametangia are exogenous and develop acropetally on the dorsal surface of
the thallus. They are scattered or arranged in groups or cushions on the main
thallus or its branches, or on specialized receptacles on highly modified branches
(antheridiophores and archegoniophores) (Fig. 1.4). The stalks of these modified
branches show vestigial features of vegetative branches, such as one or more
‘‘rhizoid furrows’’ containing pegged rhizoids in most genera and vestigial air
chambers in others (Asterella, Neohodgsonia, Marchantia, and Reboulia). However,
they lack air pores and ventral scales. Similarly, the sporophyte-containing
disks, or carpocephala, retain some vegetative traits, particularly air chambers
and air pores; some taxa (Aytoniaceae, Conocephalum, and Wiesnerella) with ‘‘simple’’
air pores in the thallus display ‘‘compound’’ air pores in the carpocephalum.
In complex thalloids the antheridial chambers are formed initially by divisions in more than one plane, then later in a single plane to form a protruding
ostiole; these can be in scattered cavities on the thallus (Riccia) or along the midline of the thallus (e.g. Corsinia, Cronisia, Oxymitra, and Ricciocarpos), loosely
aggregated in groups (e.g. Cyathodium, Mannia, and Targionia), or in sessile cushions that may be bounded by scales and contain simple air-pores (e.g. Asterella,
Conocephalum, Lunularia, Monosolenium, Plagiochasma, Reboulia, and Wiesnerella), or
aggregated into stalked antheridiophores (Dumortiera, Neohodgsonia, and
Marchantiaceae) that have one or two rhizoid furrows (or up to four in some
Marchantia species) (Fig. 1.4D). In Monocarpus antheridia are borne on the floor of
open air chambers.
1 Morphology and classification of the Marchantiophyta
Archegonia also may be borne in several ways: embedded in the thallus along
its mid-line (Riccia and Ricciocarpos), in a dorsal group becoming ventrally displaced (Cyathodium and Targionia), loosely aggregated on the thallus (Oxymitra), in
cavities on the thallus (Corsinia and Cronisia), in cushions on the thallus which
later become elevated on a stalk (Aitchisoniella, Exormotheca, Cleveaceae, Aytoniaceae,
Wiesnerella, and Conocephalum), or under the lobes of a stalked receptacle
(Dumortiera, Lunularia, Neohodgsonia, and Marchantiaceae). In carpocephalate
taxa the stalk may elongate before or after fertilization. The archegonia are
protected by an involucre (= perichaetium of some authors, e.g. Goebel 1930)
that is scale-like, cup-shaped, bivalved, tubular or pyriform (Fig. 1.4B). A pseudoperianth (Fig. 1.4A) is developed around the sporophyte only in Asterella,
Marchantia, and Neohodgsonia.
As in leafy and simple thalloid forms, many complex thalloid forms can
regenerate from fragments of thallus, but a few genera distributed in several
families produce specialized vegetative reproductive structures such as cupshaped or crescent-shaped gemmae receptacles on the thallus (Lunularia,
Marchantia, and Neohodgsonia), or specialized fragmenting thallus apices
(Conocephalum and Cyathodium). The gemmae are always pluricellular and discoid
to lenticular in form. In others, perennating tubers may be produced ventrally
(Conocephalum) or as xeromorphic thallus tips (Asterella).
1.2.4
Sporophytes and associated structures
In all liverworts the sporophyte is enclosed by and physiologically
dependent on the gametophyte until just prior to spore release (Thomas et al.
1979). Early embryology is known for relatively few taxa, but among these, a
three- or four-celled filamentous embryo is most common (Schuster 1984a).
Several complex thalloid liverworts, including members of the Cleveaceae,
Marchantiaceae, Corsiniaceae and Ricciaceae (Müller 1954, p. 324, Schuster
1992c, p. 15), are reported to have octant-type embryos and Monoclea has been
shown to have a free nuclear pattern of embryogeny (Campbell 1954, Ligrone
et al. 1993). As the embryo develops, it becomes embedded in tissues derived
solely from the archegonium (= true calyptra or epigonium), or solely from the
female gametophore (= coelocaule or solid perigynium), or from a combination
of the two (= shoot calyptra) (Knapp 1930). In a true calyptra, only tissue just
below or of the archegonial venter divides, so there is little penetration of the
sporophyte foot into the gametophore and the associated perichaetial structures insert below the calyptra; in the Jubulineae the calyptrae are stalked and
the sporophyte foot is in contact only with tissue of venter origin. In shoot
calyptrae and coelocaules, gametophore cells below the archegonial cluster are
stimulated to divide after fertilization. If this meristematic zone is active for
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B. Crandall-Stotler and others
only a short period, the foot and basal part of the seta will be embedded in
gametophore tissue, while the upper part of the seta and capsule will be surrounded by cells derived from the archegonial venter. A shoot-calyptra can
usually be differentiated from a true calyptra by the presence of unfertilized
archegonia part way up the outer surface of the calyptra. When a coelocaule is
formed, in contrast, the sporophyte is completely embedded in tissue derived
from the meristematic zone below the gynoecium; unfertilized archegonia,
foliar elements of the perichaetium, and even vegetative leaves are distributed
over the outer surface of the thick, fleshy coelocaule up to the apex of the
embedded sporophyte (see Bartholomew-Began 1991, Fig. 311). In leafy forms
with coelocaules, e.g. Trichocolea and Lepicolea, the sporophyte appears to be
buried in a swollen stem apex (= the coelocaule), whereas in simple thalloid
forms, e.g. Symphyogyna, Xenothallus (Fig. 1.8A), and Aneura, the coelocaule is a
fleshy, club-shaped structure, ornamented with scales, papillae and archegonia.
Since the entire gynoecial receptacle is involved in forming a coelocaule, it
alone protects the sporophyte. However, additional structures of perichaetial
and/or axis origin frequently develop to the outside of calyptrae and shoot
calyptrae. These include perianths (Fig. 1.7B), perichaetial pseudoperianths
and caulocalyces, all of which are uni- or bistratose sheath-like structures that
enclose the developing sporophyte. Variations in the shape and size, the number and position of keels, and the form and ornamentation of the mouth of these
structures provide a suite of important taxonomic characters (e.g. see Schuster
1966, Figs. 51, 52). In the Jungermanniidae, the perianth in turn is basally
ensheathed by enlarged bracts and bracteoles. In some taxa, e.g., Isotachis,
Marsupella, and Nardia, an additional structure, referred to as a stem-perigynium,
essentially replaces the perianth (Fig. 1.7F). A stem-perigynium is derived from a
peripheral ring of meristematic cells to the outside of the archegonial cluster
and just below the perichaetium. It can superficially resemble a perianth, but
actually is a multistratose, fleshy sheath of axis origin that bears the bracts on its
surface and the reduced perianth at its apex. Coelocaules, shoot-calyptrae and
stem-perigynia in prostrate taxa of Jungermanniidae can be further modified by
more growth of the ventral tissues beneath the gynoecial receptacle than the
dorsal (Knapp 1930, Fig. 212). This asymmetric pattern of shoot growth, or
geocauly, results in the formation of a pendant marsupium and the reorientation of the sporophyte to a vertical axis (Fig. 1.7C). There are two ontogenetically
distinct types of marsupia, the Tylimanthus-type derived from a coelocaule and
the Calypogeia-type formed from a stem-perigynium with a shoot-calyptra.
In most Marchantiopsida, protection of the sporophyte is afforded by a true
calyptra and the involucre (Fig. 1.4B). In Blasia, Cavicularia, and Monoclea a thick
tubular involucre is confluent with and indistinguishable from the thallus and
1 Morphology and classification of the Marchantiophyta
Fig. 1.8. Sporophyte generation, general structure. (A) Xenothallus vulcanicola,
sporophyte emerging from a fleshy coelocaule, bar ¼ 1 mm. (B) Paracromastigum
bifidum, intact sporophyte foot, showing the elongate placental cells of the haustorial
collar and the basal 2-celled haustorium (at arrow), bar ¼ 40 mm. (C) Porella platyphylla,
transverse section of multistratose capsule wall, showing I-band thickenings in the
epidermal cells; note the elaters dispersed among the spores, bar ¼ 75 mm. (D, E) Aneura
maxima, capsule wall in surface view, showing wall thickening bands; (D) outer wall
surface; (E) inner wall surface, bars ¼ 50 mm. (F) Radula obconica, deeply furrowed
sporocyte, bar ¼ 10 mm.
consequently the sporophyte appears to be embedded in thallus tissue. In
the Sphaerocarpales the sporophyte and calyptra develop within bottle-shaped
pseudoperianths, and in the Ricciaceae and Monocarpus only calyptrae are formed
(Bischler 1998). Usually the calyptrae are hyaline and 2- or 3-layered, but in
Corsinia they can be fleshy, green and tuberculate. In a few taxa, e.g. Asterella,
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B. Crandall-Stotler and others
Neohodgsonia and Marchantiaceae, each sporophyte is surrounded by a calyptra
and pseudoperianth, inside the involucre, which in some Marchantiaceae may
include several sporophytes.
Sporophytes are differentiated into a basal foot that functions in nutrient
transfer from the gametophyte, a seta consisting of thin walled, parenchymatous cells, and a sporangium or capsule (Fig. 1.8). The sporophyte of Ricciaceae is
exceptional in lacking a foot and seta; a unistratose capsule wall is the only nonsporogenous tissue it possesses. In all other liverworts, a one- to few-celled
suspensor-like structure, called the haustorium, subtends the foot (Fig. 1.8B).
This structure mediates nutrient transfer from the gametophyte to the embryonic sporophyte and orients the embryo in the venter; in mature sporophytes it
may be obscured by the enlarged cells of the foot. Foot shape is variable, but is
often conoidal, sometimes with a unistratose haustorial collar, or involucellum,
originating at its juncture with the seta. In some taxa with coelocaules or
marsupia, e.g. Schistochila and Jackiella, the involucellum consists of elongate
filaments that more or less ensheath the seta (Schuster 1966, p. 584). At the
placenta, or zone of contact between the foot and the gametophyte, differentiated transfer cells are formed in both sporophyte and gametophyte in the
Marchantiopsida, but usually only in the sporophyte in the Jungermanniopsida
(Ligrone et al. 1993, Table 3). In Jubula and Radula of the Porellales, there are no
transfer cells in either generation, but instead small filamentous ingrowths of
the gametophyte intercalate with radially elongate, epidermal cells of the foot
(Crandall-Stotler & Guerke 1980, Ligrone et al. 1993). Further studies of foot
structure and placental organization are needed to decipher the phylogenetic
signal that may be implicit in their diversity.
Setae can be either chlorophyllose or hyaline when young, but are always
white when mature. They are basically cylindrical, but are often tapered or
constricted just above the foot. Seta anatomy varies from a massive, generalized
type consisting of ten or more cells in width, as in many Pelliidae, to highly
reduced types with obvious quadrant organization, e.g. Cephaloziaceae,
Cephaloziellaceae, and Lejeuneaceae (Schuster 1966, p. 584). In some taxa the
epidermal cells are larger than those of the interior; in most Lejeuneaceae the
setae are articulate, meaning that the rectangular epidermal cells are arranged
in regular tiers. In almost all liverworts, after sporogenesis is completed, the
fragile parenchymatous cells of the seta elongate up to 20 times their original
length, thus elevating the capsule up and out of the enclosing gametophytic
tissues. This elongation process involves substantial uptake of water, is auxinmediated, and can involve the synthesis of additional wall materials (Thomas &
Doyle 1976). In most Marchantiidae, seta elongation is abbreviated or absent,
but the structure of the unelongated seta is comparable to that of other
1 Morphology and classification of the Marchantiophyta
liverworts. Capsule dehiscence and spore release occur shortly after seta elongation ceases, often within a few hours of capsule emergence. The seta collapses
soon thereafter due to loss of cell turgor.
Variations in capsule shape, capsule wall structure, and dehiscence properties are of considerable taxonomic importance. Shapes vary from the generalized ovoidal type to spheroidal, ellipsoidal or long cylindric forms. In all
Jungermanniopsida, as well as Treubia and Blasiales, the capsule wall consists
of two or more layers of cells, each of which typically displays a specific pattern
of darkly pigmented wall thickenings (Fig. 1.8C–E). The thickenings are secondary wall deposits, laid down after expansion of the capsule wall cells is complete, during the late stages of sporogenesis and elater differentiation.
Commonly, in the outer layer of wall cells, the thickenings are deposited as
scattered I- or J-shaped bands on the longitudinal, radial walls to produce a
nodular pattern in surface view (Fig. 1.8D). Cells in the inner wall layers, in
contrast, deposit annular or semiannular, U-shaped thickenings that extend
from the radial walls across the inner tangential wall; these impart a banded
appearance in surface view (Fig. 1.8E). In the vast majority of liverworts, capsule
dehiscence occurs along differentiated sutures. Usually two such sutures extend
longitudinally from near the capsule base, over the capsule apex and down to
the base on the other side, thereby dividing the capsule wall into four sectors, or
valves. With drying, the cell walls between the two rows of suture cells tear
along the middle lamella. The transverse thickening bands of the inner wall
layers make them more rigid than the outer, and consequently when the sutures
tear, the separated valves bend outwards (Ingold 1939), releasing the mass of
spores and elaters. In several taxa, the valves are very long and spirally twisted
(e.g. Balantiopsidaceae). Neither the chemical nature of the thickening bands
nor the mechanisms regulating their deposition are known. The fact that they
are autofluorescent and have a homogeneous, osmiophilic appearance in TEM
micrographs, however, suggests that they are composed of polyphenolics.
In Haplomitrium and the Marchantiidae, capsule walls are unistratose and
dehiscence rarely occurs along four valves. In Haplomitrium each capsule wall
cell bears a single longitudinal, annular thickening band and the capsule opens
along one to four slits (Bartholomew-Began 1991). In many Marchantiidae the
capsule breaks apart into irregular plates of cells, a phenomenon also seen in
some of the Pelliidae, e.g. Fossombronia, whereas in others, e.g. the Aytoniaceae,
dehiscence involves an apical operculum. In the Ricciaceae, the capsule wall
actually deteriorates before the spores are mature, leaving them in a cavity
lined by the calyptra; spore dispersal in this group requires thallus degeneration.
An almost universal feature of liverwort sporophytes is the presence of
elaters in the capsule (Fig. 1.8C). The elaters are always unicellular and dead at
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B. Crandall-Stotler and others
maturity, and are usually thin and elongate with spiral thickening bands in their
walls. In some Marchantiopsida, e.g. the Aytoniaceae, the division that produces
the elater initials is followed directly by sporocyte meiosis and elater differentiation, resulting in a 4:1 spore:elater ratio in the mature capsule. In most
hepatics, however, the sporocyte initial divides several times prior to meiosis,
while the elater initial remains undivided. As a consequence, in most hepatics,
including many genera of the Marchantiopsida, spore:elater ratios are 8:1 or
greater. Among liverworts, Pellia epiphylla and Conocephalum conicum, both of
which display endosporic, precocious spore germination, are reported to have
spore:elater ratios less than 4:1 (Bischler 1998). In Pelliaceae many of the elaters
arise from a basal pad of sterile tissue, or elaterophore; these are not homologous to the elaters that are sister cells to the sporocytes. In other groups, e.g.
Aneuraceae, an elaterophore is formed at the capsule apex; in the Jubulaceae,
Frullaniaceae, and Lejeuneaceae, the elaters are dispersed, but remain attached
to the apices of the capsule valves after dehiscence.
Hygroscopically induced movements of the elaters help to break up the spore
mass after the capsule opens (Ingold 1939). In developing capsules, however,
these sterile cells may serve as a dispersed tapetum (Crandall-Stotler 1984).
Bartholomew-Began (1991) has shown that the immature elaters of
Haplomitrium contain lipids and starch bodies, both of which disappear as elater
thickenings are deposited. At the same time, the capsule lumen itself also
contains numerous lipid droplets (Crandall-Stotler 1984). A similar nutritive
function has often been postulated for the nurse cells of the Sphaerocarpales
(Parihar 1961). Schuster (1992b, p. 799) suggested that the nurse cells are not
homologous to elaters because they are not formed as a consequence of a fixed
spore/elater division, but instead seem to be sporocytes that fail to undergo
meiosis. The studies of Doyle (1962) and Kelley & Doyle (1975), while demonstrating that the nurse cells are tapetal, do not resolve the question of origin.
Although variation in form occurs, the production of dispersed sterile unicells
in the archesporium appears to be a significant defining character of the
Marchantiophyta as suggested by Mishler & Churchill (1984).
Prophase sporocytes in the Haplomitriopsida and Jungermanniopsida are
deeply quadrilobed (Fig. 1.8F), whereas in the Marchantiidae they are spheroidal
and unlobed. This difference in sporocyte morphology has historically been
cited to support the basic dichotomy between marchantioids and other liverworts (Schuster 1984b). Recently, Brown & Lemmon (2006) have shown that
quadrilobed-shaping involves two intersecting girdling bands of microtubules
that develop in very early prophase to establish the planes of meiotic cytokinesis. Polar organizers differentiated in each of the lobes then generate the
quadripolar microtubular system (QMS) that is involved in karyokinesis.
1 Morphology and classification of the Marchantiophyta
Comparable premeiotic girdling bands have not been observed in the
Marchantiidae, but only Conocephalum and Dumortiera have been studied
(Brown & Lemmon 1988, Shimamura et al. 2004). In most liverworts, sporocytes
bear multiple plastids and meiosis is polyplastidic, but in Haplomitrium blumii,
Blasiales, and several genera of the Marchantiidae (Monoclea, Dumortiera,
Wiesnerella, Lunularia, and Marchantia), plastid number is reduced to one in the
sporocyte and meiosis is monoplastidic (Renzaglia et al. 1994, Shimamura et al.
2003). Conocephalum has polyplastidic sporocytes, but produces spores in rhomboidal or linear rather than tetrahedral arrays through a unique process of
cytoplasmic partitioning (Brown & Lemmon 1988, 1990).
Spores vary greatly in size, shape and ornamentation, tending to be smaller
and less highly ornamented in the Jungermanniidae and Metzgeriidae than in
the Pelliidae and Marchantiopsida (Schuster 1984a). Spore wall ornamentation
is due to sculpturing of the exine, which in several taxa is patterned by callosic
deposits in the preprophase sporocyte (Brown et al. 1986, Brown & Lemmon
1987). Variations in spore wall architecture are informative in the systematics of
some taxa, e.g. Fossombronia, Riccia, and the Aytoniaceae. All liverworts are isosporous and most disperse their spores as monads. Spores that remain in tetrads
after dispersal are, however, diagnostic of some species of Sphaerocarpos and
Riccia, and may occasionally also be found in other taxa, e.g. Haplomitrium,
Fossombronia, and Aneura.
1.2.5
Spore germination and sporeling patterns
Spore germination is initiated with swelling and division of the spore
protoplast to form a multicellular protonema. In exosporic germination, the
swollen protoplast ruptures the spore wall before it divides, usually after release
from the capsule. In many epiphytic taxa, including all members of the
Porellales, in contrast, the protonema is formed inside the stretched spore
wall, i.e. germination is endosporic. Endosporic germination is usually precocious, i.e. germination occurs prior to capsule dehiscence, but in a few taxa, e.g.
Radula and Trichocoleopsis, endosporic germination occurs after spore release. In
the Jungermanniopsida, the most common protonema is a multicellular, globose to cylindrical structure, from which a single gametophore develops. Other
expressions include a filamentous protonema, as in Cephaloziaceae, a plate-like
protonema, as in Radulaceae and Metzgeriaceae, and a biphasic protonema, as
in some Lejeuneaceae. The exosporic protonema of Haplomitrium initially comprises two tiers of quadrants from which a cell mass and then a system of highly
branched cylindrical, leafless axes, or stolons, arise (Bartholomew-Began 1991).
Among the Marchantiopsida only the Blasiales and Conocephalum exhibit
endosporic germination. In most taxa, an elongate hyaline germ tube emerges
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B. Crandall-Stotler and others
from the ruptured spore, often bearing a germ rhizoid at its base. Initially,
transverse divisions at the apex of the germ tube form a short filamentous
protonema, the terminal cell of which is soon partitioned into quadrants. The
quadrants may continue to produce tiers of cells basally, forming a quadriseriate
cylindrical phase, e.g. Sphaerocarpos (Nehira 1983, p. 369), or the quadrant
stage may be very abbreviated, e.g., Marchantia. With additional vertical divisions, the terminal quadrant may be converted to a discoid plate. Ultimately, the
apical cell of the young thallus is formed in one of the cells of either the
quadrant stage or the plate. This very distinctive pattern of sporeling development, known as the ‘‘golf-tee’’ type, is restricted to the Marchantiidae. Although
it has been suggested that the fine details of sporeling ontogeny are phylogenetically informative (Fulford 1956, Nehira 1983), this view has yet to be
critically tested.
1.3
Morphology, molecules, and classification
The application of molecular methods to unraveling the evolutionary
history of liverworts has resulted in revolutionary changes in our concepts of
liverwort phylogeny (see, for example, Heinrichs et al. 2005, Forrest et al. 2006,
He-Nygrén et al. 2006). Analyses of character evolution have demonstrated that
there is substantial homoplasy in many of the characters previously used to
define genera, families and even suborders (Crandall-Stotler et al. 2005). That
does not mean, however, that morphology cannot provide phylogenetically
informative characters. In fact, many of the novel relationships resolved in
molecular analyses are supported by morphological signals, e.g. the relationships between Haplomitrium and Treubia, Blasia and the Marchantiopsida, and
Pleurozia and the Metzgeriales (for discussion see Crandall-Stotler et al. 2005,
Forrest et al. 2006, Renzaglia et al. 2007). Resolving incongruency between
molecule-based phylogenies and traditional schemes derived intuitively from
morphology requires critical re-evaluation of morphological characters to correct faulty interpretations of homology, as well as re-assessment of specimen
identity to eliminate erroneous DNA sequences (see discussion in Forrest et al.
2006). Total evidence analyses that incorporate ontogenetic and ultrastructural
data are essential to future efforts to clarify the evolution of structural characters (Renzaglia et al. 2007).
To accommodate the many changes arising from molecular phylogenetic
studies, several authors have proposed modifications to the taxonomic hierarchy of liverworts above the family level (Frey & Stech 2005, Heinrichs et al. 2005,
Forrest et al. 2006, He-Nygrén et al. 2006). The classification scheme presented
below, which circumscribes families as well as higher ranks, integrates
1 Morphology and classification of the Marchantiophyta
morphology with these hypotheses and others generated from molecular analyses, including but not limited to the following: Schill et al. (2004), Yatsentyuk
et al. (2004), Heinrichs et al. (2006, 2007), Hentschel et al. (2006), de Roo et al.
(2007), Hendry et al. (2007), Heselwood & Brown (2007), Liu et al. (2008), and
Wilson et al. (2007). The resolution of liverwort phylogeny is very much a
work in progress, with fewer than 30% of liverwort genera (< 5% of species)
sampled for molecular analyses. Consequently, the relationships of many
lineages are unresolved. For example, in the Marchantiidae the branching
order of Sphaerocarpales and the recently established Neohodgsoniales and
Lunulariales (Long 2006b) are equivocal, and the hierarchial relationships of
the paraphyletic assemblage of families in the crown group of the Marchantiales
are unresolved. For this reason, we have not recognized any subordinal rankings
in the Marchantiales. There are substantial changes at all hierarchial levels from
our previously published classification (Crandall-Stotler & Stotler 2000). A discussion of these changes and a complete classification that provides author
citations, place of publication and diagnoses for ranks of family and above are
presented in Crandall-Stotler et al. (2008). The classification scheme that follows
has been extracted from this publication and reflects our current state of understanding of liverwort phylogeny. Certainly, as new ontogenetic, ultrastructural
and molecular data are generated, the scheme presented herein will be scrutinized and refined.
PHYLUM MARCHANTIOPHYTA Stotler & Crand.-Stotl.
CLASS HAPLOMITRIOPSIDA Stotler & Crand.-Stotl.
Plants bearing foliar appendages at discrete nodes; axes (stems) secreting copious mucilage from epidermal cells, forming unique associations with
glomeromycotean fungi; apical cells tetrahedral; androecia and gynoecia
loosely organized (apical disks in some species of Haplomitrium); early antheridial ontogeny forming one primary androgonial initial; spermatids with a
massive spline; anacrogynous (acrogynous in Haplomitrium subg. Calobryum);
sporophytes large, enclosed by a fleshy shoot calyptra or coelocaule.
SUBCLASS TREUBIIDAE Stotler & Crand.-Stotl.
Plants prostrate, dorsiventrally flattened; leaves in two rows, unequally
divided into a small dorsal lobule and large ventral lobe, with the lobe fleshy,
confluent with the stem, longitudinal or slightly succubous, polystratose except
near the margins; rhizoids ventral, scattered; oil bodies large, in specialized
cells; gemmae multicellular, not in receptacles; gametangia protected by dorsal
lobules; capsules ovoidal, wall 3- to 5-stratose; dehiscence 4-valved.
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B. Crandall-Stotler and others
ORDER TREUBIALES Schljakov
Treubiaceae Verd: Apotreubia S. Hatt. & Mizut., Treubia K. I. Goebel
SUBCLASS HAPLOMITRIIDAE Stotler & Crand.-Stotl.
Plants differentiated into highly branched leafless stolons and erect
leafy shoots, isophyllous or anisophyllous; leaves in three rows, with the third
row of leaves dorsal, transverse or weakly succubous, undivided, polystratose
only near the base; stems with a central strand of thin-walled, hydrolyzed cells;
rhizoids absent; oil bodies small, homogeneous, in all cells; gemmae absent;
antheridia and archegonia scattered on the stem, in leaf axils, or on apical discs;
capsules cylindrical, wall unistratose, dehiscence along 1, 2 or 4 sutures, nonvalvate.
ORDER CALOBRYALES Hamlin
Haplomitriaceae Dědeček: Haplomitrium Nees
CLASS MARCHANTIOPSIDA Gonquist, Takht & W. Zimm.
Plants thalloid, or rarely leafy; apical cell cuneate with four cutting
faces; thallus often differentiated into assimilatory and storage tissues, usually
with persistent ventral scales with appendages and dimorphic rhizoids;
oil-bodies single in specialized cells or lacking; gametangia on specialized
branches or embedded dorsally in the thallus; early antheridial ontogeny forming four primary androgonial initials; archegonial neck of six cell rows; embryos
often octamerous; sporophytes with seta usually short or absent; capsule wall
usually unistratose; sporocytes unlobed, spores usually polar and highly
ornamented.
SUBCLASS BLASIIDAE He-Nygrén, Juslén, Ahonen, Glenny & Piippo
Thallus simple, lacking dorsiventral differentiation; wing margins
scarcely (Cavicularia) to deeply lobed and ‘‘leaf-like’’ (Blasia), with the lobes longitudinal in insertion; midrib bearing a strand of calcium oxalate deposits (Blasia)
or with three strands of elongate, hydrolyzed cells (Cavicularia); air chambers
and air pores absent; ventral scales without appendages, in two rows on midrib,
with a row of Nostoc-containing auricles (domatia) to the outside of each row
of scales; rhizoids all smooth; oil bodies absent or few in unspecialized cells;
multicellular gemmae present (in flasks or crescent-shaped cups); dioicous;
antheridia partially embedded dorsally on thallus, arranged in two rows; sporophytes dorsal at thallus apex; pseudoperianth absent; involucre tubular; seta
elongate, massive; elaters present; capsule wall 2- to 4-stratose, dehiscence by
four valves.
1 Morphology and classification of the Marchantiophyta
ORDER BLASIALES Stotler & Crand.-Stotl.
Blasiaceae H. Klinggr.: Blasia L., Cavicularia Steph.
SUBCLASS MARCHANTIIDAE Engl.
Thallus differentiated into layers or not; air chambers and air pores
present or absent; ventral scales present or absent, appendaged or not; rhizoids
smooth or smooth and pegged; specialized oil cells usually present; multicellular gemmae present in specialized structures or absent; antheridia embedded in
dorsal part of thallus, or in cushions on thallus, or in stalked receptacles;
sporophytes on stalked receptacles or borne dorsally on thallus or embedded
in thallus; involucre present, rarely absent; seta usually very short or absent,
rarely elongate; elaters usually present; capsule dehiscence by longitudinal
valves or slits, or by a lid, sometimes cleistocarpous.
ORDER SPHAEROCARPALES Cavers
Plants delicate, with stems bearing longitudinally inserted leaves
(Sphaerocarpaceae) or small ventral scales and a large dorsal wing (Riellaceae),
sometimes sexually dimorphic (Sphaerocarpos); leaves and dorsal wing unistratose; air chambers and air pores absent; ventral scales absent (Sphaerocarpaceae) or present (Riella); rhizoids all smooth; specialized oil cells absent or
present (Riella); specialized asexual structures absent (gemmae in Riella); dioicous, rarely monoicous; antheridia in flask-shaped dorsal perigonial involucres
(Sphaerocarpaceae) or embedded in pockets on margin of wing (Riella); each
archegonium and sporophyte enclosed in dorsal or ventral flask-shaped pseudoperianth; seta very short; elaters absent; capsule cleistocarpous; spores shed
singly or in tetrads.
Sphaerocarpaceae Heeg: Sphaerocarpos Boehm., Geothallus Campb.
Riellaceae Engl.: Riella Mont.
ORDER NEOHODGSONIALES D. G. Long
Thallus differentiated into layers, with compound air pores; ventral scales in
two rows, without appendages; rhizoids all smooth; specialized oil cells present;
specialized asexual structures present (gemma cups); monoicous; antheridia on
unbranched stalked receptacle; archegonia and young sporophytes enclosed in
campanulate pseudoperianths; sporophytes on branched stalked receptacle;
involucre bivalved; seta not elongated; elaters present; capsule dehiscence by
irregular valves.
Neohodgsoniaceae D. G. Long: Neohodgsonia Perss.
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B. Crandall-Stotler and others
ORDER LUNULARIALES D. G. Long
Thallus differentiated into layers, upper layer with air chambers, dorsal surface
with simple air pores; ventral scales in two rows, with single appendage; rhizoids smooth and pegged; specialized oil cells present; specialized asexual
structures present (crescent-shaped gemma cups); dioicous; antheridia in terminal cushions on thallus; sporophytes on stalked deeply 4-lobed receptacle;
pseudoperianth absent; involucre tubular; seta elongate, massive; elaters present; capsule dehiscence by lid and four valves.
Lunulariaceae H. Klinggr.: Lunularia Adans.
ORDER MARCHANTIALES Limpr.
Thallus usually differentiated into layers, upper layer with air chambers,
dorsal surface with simple or compound air pores (rarely absent);
ventral scales in 2–10 rows, sometimes absent, usually with 1–3(6) appendages; rhizoids usually smooth and pegged, sometimes only smooth; specialized oil cells usually present; specialized asexual structures absent or present;
monoicous or dioicous; antheridia embedded dorsally in thallus or on stalked
receptacles; sporophytes on stalked receptacle, or terminal or dorsal on
thallus or embedded in thallus; pseudoperianth absent or present; involucre
bivalved, cup-shaped, scale- or flap-like or tubular, sometimes absent; seta
usually very short or absent, rarely elongate; elaters present or absent; capsule
dehiscence by longitudinal valves, longitudinal slit or lid, sometimes
cleistocarpous.
Marchantiaceae Lindl.: Bucegia Radian, Marchantia L., Preissia Corda
Aytoniaceae Cavers: Asterella P. Beauv., Cryptomitrium Austin ex Underw.,
Mannia Opiz, Plagiochasma Lehm. & Lindenb., Reboulia Raddi
Cleveaceae Cavers: Athalamia Falconer, Sauteria Nees, Peltolepis Lindb.
Monosoleniaceae Inoue: Monosolenium Griff.
Conocephalaceae Müll. Frib. ex Grolle: Conocephalum Hill
Cyathodiaceae Stotler & Crand.-Stotl.: Cyathodium Kunze
Exormothecaceae Müll. Frib. ex Grolle: Aitchisoniella Kashyap, Exormotheca
Mitt., Stephensoniella Kashyap
Corsiniaceae Engl.: Corsinia Raddi; Cronisia Berk.
Monocarpaceae D. J. Carr ex Schelpe: Monocarpus D. J. Carr
Oxymitraceae Müll. Frib. ex Grolle: Oxymitra Bisch. ex Lindenb.
Ricciaceae Rchb.: Riccia L., Ricciocarpos Corda
Wiesnerellaceae Inoue: Wiesnerella Schiffn.
Targioniaceae Dumort.: Targionia L.
1 Morphology and classification of the Marchantiophyta
Monocleaceae A. B. Frank: Monoclea Hook.
Dumortieraceae D. G. Long: Dumortiera Nees
CLASS JUNGERMANNIOPSIDA Stotler & Crand.-Stotl.
Plants thalloid or leafy; oil bodies usually present in all cells (absent in a
few taxa); rhizoids monomorphic, smooth-walled; early antheridial ontogeny
forming two primary androgonial cells; archegonial neck usually of five cell
rows; embryos filamentous; sporophytes with seta elongation pronounced;
capsule wall 2- or more stratose; sporocytes lobed, spores cryptopolar to apolar,
rarely polar.
SUBCLASS PELLIIDAE He-Nygrén, Juslén, Ahonen, Glenny & Piippo
Plants mostly thalloid without air chambers, if leafy, leaves developing
from one primary initial, never lobed, arranged in two ranks; branches exogenous in origin, terminal or intercalary, lateral or ventral; antheridia on dorsal
surface of midrib or stem, with or without perigonia (on abbreviated ventral
branches in Hymenophyton); gynoecia usually anacrogynous, on dorsal surface of
midrib or stem (acrogynous on thallus in Pellia, on abbreviated branches in
Hymenophyton and Podomitrium).
ORDER PELLIALES He-Nygrén, Juslén, Ahonen, Glenny & Piippo
Plants thalloid or leafy with the leaves succubous; apical cell tetrahedral, cuneate, or hemidiscoid; stalked papillae or uniseriate hairs dispersed or in two rows
on ventral surface; rhizoids hyaline or brownish to pale reddish brown; ventral
branches rare; antheridia arranged in two rows, or scattered to weakly clustered
on the thallus, each in a conical or flask-shaped chamber with an apical ostiole;
archegonia naked and arranged in two rows along the midrib (Noteroclada), or in
an acrogynous cluster, protected by a perichaetial flap or sheath (Pellia); sporophytes enclosed by a shoot calyptra and caulocalyx (Noteroclada) or perichaetial
pseudoperianth (Pellia); capsules spheroidal, with conspicuous basal elaterophore, dehiscing into four valves; spore germination precocious and
endosporic.
Pelliaceae H. Klinggr.: Noteroclada Taylor ex Hook. & Wilson, Pellia Raddi
ORDER FOSSOMBRONIALES Schljakov
Plants thalloid or leafy; foliose scales, uniseriate hairs, or stalked papillae,
arranged in two rows on the ventral surface of the midrib or stem; oil bodies
of the Massula type; ventral branches rare; gynoecia anacrogynous; capsules
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B. Crandall-Stotler and others
usually spheroidal (cylindrical in Makinoa); dehiscence not valvate, irregular (by
a single slit in Makinoa); spore germination exosporic.
SUBORDER Calyculariineae He-Nygrén, Juslén, Ahonen, Glenny & Piippo
Plants thalloid with well defined midrib; apical cell hemidiscoid; foliose ventral
scales; rhizoids hyaline; antheridia in several rows on the midrib, with laciniate
perigonial scales; gynoecia anacrogynous, with archegonia and perichaetial
scales clustered; sporophytes enclosed by a shoot-calyptra and caulocalyx; capsules spheroidal, with a basal elaterophore, dehiscing irregularly into 5 to 7
unequal segments.
Calyculariaceae He-Nygrén, Juslén, Ahonen, Glenny & Piippo: Calycularia Mitt.
SUBORDER Makinoineae He-Nygrén, Juslén, Ahonen, Glenny & Piippo
Plants thalloid with an inconspicuous midrib; apical cell cuneate; 3- to 6-celled
ventral hairs; rhizoids reddish brown; androecia large, up to 80 antheridia
sunken in thallus depressions, protected by a posterior lunulate ridge of thallus
tissue; archegonia in small dorsal clusters protected by a posterior flap of thallus
tissue; sporophytes enclosed by a coelocaule; capsules cylindrical, with rudimentary basal elaterophore, dehiscing along one slit.
Makinoaceae Nakai: Makinoa Miyake
SUBORDER Fossombroniineae R. M. Schust. ex Stotler & Crand.-Stotl.
Plants thalloid or leafy; apical cell tetrahedral (Petalophyllaceae), lenticular
(Fossombroniaceae) or cuneate (Allisoniaceae); ventral appendages foliose
scales or filamentous hairs or stalked slime papillae; rhizoids purplish or brownish (hyaline in Petalophyllaceae); antheridia scattered (Fossombroniaceae) or in
clusters on the midrib, with or without perigonial scales; archegonia scattered
or clustered, with or without perichaetial scales; sporophytes protected by a
shoot calyptra and either a caulocalyx or perichaetial pseudoperianth (only a
true calyptra in Allisonia); capsules spheroidal, lacking an elaterophore, dehiscence irregular or in 5–7 unequal segments.
Petalophyllaceae Stotler & Crand.-Stotl.: Petalophyllum Nees & Gottsche ex
Lehm., Sewardiella Kashyap
Allisoniaceae Schljakov: Allisonia Herzog
Fossombroniaceae Hazsl.: Austrofossombronia R. M. Schust., Fossombronia Raddi
ORDER PALLAVICINIALES W. Frey & M. Stech
Plants thalloid (leafy in Phyllothallia), midrib usually well defined; apical
cells cuneate, lenticular or hemidiscoid; ventral appendages stalked papillae
or hairs, dispersed or in two rows; ventral branches common; antheridia
1 Morphology and classification of the Marchantiophyta
associated with perigonial scales, in clusters or rows on midrib; archegonia
associated with perichaetial scales, clustered; sporophytes enclosed by a coelocaule or by a shoot calyptra and perichaetial pseudoperianth or caulocalyx;
capsules ellipsoidal to cylindrical, with a multistratose apical cap (except
Phyllothallia), dehiscence usually 2- or 4-valved, valves apically coherent (irregular in Phyllothallia).
SUBORDER Phyllothalliineae R. M. Schust.
Plants leafy, with the leaves opposite, distant to contiguous, with well defined
internodes; apical cell cuneate; ventral stalked papillae dispersed; antheridia and
perigonial scales in clusters at nodes; archegonia and perichaetial scales in clusters at nodes; sporophytes enclosed by a coelocaule; capsules spheroidal, wall
multistratose, dehiscing into 12–14 irregular segments.
Phyllothalliaceae E. A. Hodgs.: Phyllothallia E. A. Hodgs.
SUBORDER Pallaviciniineae R. M. Schust.
Plants thalloid, with wings sometimes deeply lobed, midrib with 1 or 2(4) strands
of elongate, hydrolyzed conducting cells (strands lacking in Sandeothallus and
some species of Moerckia).
Sandeothallaceae R. M. Schust.: Sandeothallus R. M. Schust.
Moerckiaceae Stotler & Crand.-Stotl.: Hattorianthus R. M. Schust. & Inoue,
Moerckia Gottsche
Hymenophytaceae R. M. Schust.: Hymenophyton Dumort.
Pallaviciniaceae Mig.: Greeneothallus Hässel, Jensenia Lindb., Pallavicinia Gray,
Podomitrium Mitt., Seppeltia Grolle, Symphyogyna Nees & Mont.,
Symphyogynopsis Grolle, Xenothallus R. M. Schust.
SUBCLASS METZGERIIDAE Barthol.-Began
Plants mostly thalloid, without air chambers, if leafy, leaves developing
from three primary initials, arranged in two ranks; apical cells lenticular;
branches exogenous or endogenous in origin, terminal or intercalary, lateral
or ventral; androecia on abbreviated lateral or ventral branches (except
Verdoornia); gynoecia acrogynous, on abbreviated lateral or ventral branches
(except Verdoornia); capsule dehiscence 4-valved.
ORDER PLEUROZIALES Schljakov
Plants leafy; leaves succubous, unequally complicate-bilobed, with the
larger lobe shallowly bifid and the small lobule usually forming a complex,
valvate water sac (leaves simple in P. paradoxa); underleaves and ventral
slime papillae lacking; branches endogenous, lateral (Plagiochila-type); androecia on abbreviated branches, with antheridia solitary in the axils of
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B. Crandall-Stotler and others
reduced perigonial leaves; gynoecia on abbreviated branches, with archegonia
enclosed by a perianth and 2 to 5 series of modified perichaetial leaves; sporophytes enclosed by a shoot calyptra and perianth; capsules ovoid to subspheroidal, wall 8- to 10-stratose, epidermal cells with 2-phase ontogeny, walls of
inner cells with complex reticulate thickenings; spore germination endosporic.
Pleuroziaceae Müll. Frib.: Pleurozia Dumort. [including Eopleurozia R. M. Schust.]
ORDER METZGERIALES Chalaud
Plants thalloid; 1- or 2-celled ventral slime papillae dispersed or in two rows;
archegonial neck reduced, only weakly differentiated from the venter; sporophytes enclosed by a fleshy shoot calyptra or coelocaule; capsules ovoid, ellipsoid or cylindric, with an apical elaterophore, capsule wall 2-stratose, cells in
both layers with wall thickenings; spore germination exosporic; asexual reproduction by gemmae common.
Metzgeriaceae H. Klinggr.: Apometzgeria Kuwah., Austrometzgeria Kuwah,
Metzgeria Raddi, Steereella Kuwah.
Aneuraceae H. Klinggr.: Aneura Dumort. [including Cryptothallus Malmb.],
Riccardia Gray, Lobatiriccardia (Mizut. & S. Hatt.) Furuki, Verdoornia
R. M. Schust.
Mizutaniaceae Furuki & Z. Iwats.: Mizutania Furuki & Z. Iwats.
Vandiemeniaceae Hewson: Vandiemenia Hewson
SUBCLASS JUNGERMANNIIDAE Engl.
Plants leafy, very rarely thalloid (e.g., Pteropsiella); leaves developing
from two primary leaf initials, frequently divided into two or more lobes,
arranged in two or three rows, with the third row ventral; isophyllous, or
anisophyllous with the ventral leaves (underleaves or amphigastria) smaller
and/or morphologically different from the lateral leaves; apical cell tetrahedral;
antheridia in axils of modified leaves, rarely underleaves (male bracts and
bracteoles); archegonia acrogynous, usually surrounded by a perianth and modified leaves and underleaves (female bracts and bracteoles); capsules variable in
shape, wall 2- to 10-stratose, dehiscence 4-valved.
ORDER PORELLALES Schljakov
Leaves incubous, complicate, unequally 2- or 3-lobed, with the smaller lobe(s)
or lobules, ventral; lobules commonly forming inflated water sacs; underleaves present or absent, sometimes with water sacs, morphologically different from the leaves; rhizoids fascicled, from the underleaf base; branches
exogenous, lateral; spore germination precocious and endosporic (unknown
in Goebeliella).
1 Morphology and classification of the Marchantiophyta
SUBORDER Porellineae R. M. Schust.
Plants robust, highly branched, pinnate or bipinnate; leaves 3-lobed (2-lobed in
Porellaceae); water sacs when present of the Frullania-type; branches normally of
the Frullania-type; underleaves present; gynoecia with multiple archegonia and
several series of bracts and bracteoles; sporophytes enclosed by a calyptra and
perianth (coelocaule in Lepidolaenaceae); perianths 3-keeled; elaters free and
randomly dispersed in the capsule.
Porellaceae Cavers: Ascidiota C. Massal., Macvicaria W. E. Nicholson, Porella L.
Goebeliellaceae Verd.: Goebeliella Steph.
Lepidolaenaceae Nakai: Gackstroemia Trevis., Lepidogyna R. M. Schust.,
Lepidolaena Dumort., Jubulopsis R. M. Schust.
SUBORDER Radulineae R. M. Schust.
Plants irregularly pinnate to bipinnate, with branches of the Radula-type; leaves
2-lobed, with the ventral lobule slightly inflated near the keel; underleaves
absent; rhizoids in fascicles from leaf lobules; androecia on abbreviated branches;
gynoecia usually on a leading axis, with 2 to 4 archegonia; bracts in a single series;
bracteoles absent; sporophytes enclosed by a shoot calyptra or stem perigynium
and perianth; perianths 2-keeled, dorsiventrally compressed, with the mouth
truncate; capsules cylindric, wall 2-stratose, both epidermal and inner cells
with wall thickenings; multicellular discoid gemmae in some species.
Radulaceae Müll. Frib.: Radula Dumort.
SUBORDER: Jubulineae Müll. Frib.
Plants usually with underleaves (absent in a few Lejeuneaceae); leaves 2- or
3-lobed; water sacs of the Frullania- or Lejeunea-types; rhizoids fascicled from the
underleaf base; sporophytes enclosed by a stalked, true calyptra and perianth;
perianths beaked; capsules spheroidal, wall 2-stratose; elaters vertically aligned,
attached to the valve apices; spores with rosette markings (absent in Jubula).
Frullaniaceae Lorch: Frullania Raddi [including Amphijubula R. M. Schust.,
Neohattoria Kamim., Schusterella S. Hatt., Sharp & Mizut., and Steerea S.
Hatt. & Kamim.]
Jubulaceae H. Klinggr.: Jubula Dumort., Nipponolejeunea S. Hatt.
Lejeuneaceae Cavers: Acanthocoleus R. M. Schust., Acantholejeunea (R. M. Schust.)
R. M. Schust., Acrolejeunea (Spruce) Schiffn., Amblyolejeunea Ast,
Anoplolejeunea (Spruce) Schiffn., Aphanolejeunea A. Evans, Aphanotropis
Herzog, Archilejeunea (Spruce) Schiffn., Aureolejeunea R. M. Schust.,
Austrolejeunea (R. M. Schust.) R. M. Schust., Blepharolejeunea S. W. Arnell,
Brachiolejeunea (Spruce) Schiffn., Bromeliophila R. M. Schust., Bryopteris
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B. Crandall-Stotler and others
(Nees) Lindenb. Calatholejeunea K. I. Goebel, Caudalejeunea (Steph.)
Schiffn., Cephalantholejeunea (R. M. Schust. & Kachroo) R. M. Schust.,
Cephalolejeunea Mizut., Ceratolejeunea (Spruce) J. B. Jack & Steph.,
Cheilolejeunea (Spruce) Schiffn. [including Cyrtolejeunea A. Evans],
Chondriolejeunea (Benedix) Kis & Pócs, Cladolejeunea Zwick., Cololejeunea
(Spruce) Schiffn. [including Metzgeriopsis K. I. Goebel], Colura (Dumort.)
Dumort., Cyclolejeunea A. Evans, Cystolejeunea A. Evans, Dactylolejeunea
R. M. Schust., Dactylophorella R. M. Schust., Dendrolejeunea (Spruce)
Lacout., Dicranolejeunea (Spruce) Schiffn., Diplasiolejeunea (Spruce)
Schiffn., Drepanolejeunea (Spruce) Schiffn. [including Capillolejeunea
S. W. Arnell and Rhaphidolejeunea Herzog], Echinocolea R. M. Schust.,
Echinolejeunea R. M. Schust., Evansiolejeunea Vanden Berghen, Frullanoides
Raddi, Fulfordianthus Gradst., Haplolejeunea Grolle, Harpalejeunea (Spruce)
Schiffn., Hattoriolejeunea Mizut., Kymatolejeunea Grolle, Leiolejeunea
A. Evans, Lejeunea Lib. [including Amphilejeunea R. M. Schust.,
Crossotolejeunea (Spruce) Schiffn., Cryptogynolejeunea R. M. Schust. and
Dicladolejeunea R. M. Schust.], Lepidolejeunea R. M. Schust., Leptolejeunea
(Spruce) Schiffn., Leucolejeunea A. Evans, Lindigianthus Kruijt & Gradst.,
Lopholejeunea (Spruce) Schiffn., Luteolejeunea Piippo, Macrocolura
R. M. Schust., Macrolejeunea (Spruce) Schiffn., Marchesinia Gray,
Mastigolejeunea (Spruce) Schiffn., Metalejeunea Grolle, Microlejeunea Steph.,
Myriocolea Spruce, Myriocoleopsis Schiffn., Neopotamolejeunea E. Reiner,
Nephelolejeunea Grolle, Neurolejeunea (Spruce) Schiffn., Odontolejeunea
(Spruce) Schiffn., Omphalanthus Lindenb. & Nees, Oryzolejeunea
(R. M. Schust.) R. M. Schust., Otolejeunea Grolle & Tixier, Phaeolejeunea
Mizut., Physantholejeunea R. M. Schust., Pictolejeunea Grolle, Pluvianthus
R. M. Schust. & Schäf.-Verw., Prionolejeunea (Spruce) Schiffn., Ptychanthus
Nees, Pycnolejeunea (Spruce) Schiffn., Rectolejeunea A. Evans,
Schiffneriolejeunea Verd., Schusterolejeunea Grolle, Siphonolejeunea Herzog,
Sphaerolejeunea Herzog, Spruceanthus Verd., Stenolejeunea R. M. Schust.,
Stictolejeunea (Spruce) Schiffn., Symbiezidium Trevis., Taxilejeunea (Spruce)
Schiffn., Thysananthus Lindenb., Trachylejeunea (Spruce) Schiffn.
[including Potamolejeunea (Spruce) Lacout.], Trocholejeunea Schiffn.,
Tuyamaella S. Hatt., Tuzibeanthus S. Hatt., Verdoornianthus Gradst.,
Vitalianthus R. M. Schust. & Giancotti, Xylolejeunea X-L. He & Grolle
ORDER PTILIDIALES Schljakov
Plants regularly pinnate to bipinnnate; leaves asymmetrically 3-lobed, with
the dorsal lobe largest; lobes with marginal cilia, plane, or with the ventralmost
1 Morphology and classification of the Marchantiophyta
lobe forming a water sac of either the Frullania-type (Neotrichocolea, branch leaves
only) or the Lejeunea-type (Trichocoleopsis); leaf insertion transverse to weakly
incubous or succubous (Herzogianthus); underleaves bifid or quadrifid; rhizoids
in fascicles from the underleaf base; branches of the Frullania-type; androecia on
leading axes; gynoecia on leading axes; capsules ovoid to ellipsoidal, walls 4- to
7-stratose; spore germination exosporic or endosporic (Trichocoleopsis); gemmae
absent.
SUBORDER Ptilidiineae R. M. Schust.
Ptilidiaceae H. Klinggr.: Ptilidium Nees
Neotrichocoleaceae Inoue: Neotrichocolea S. Hatt., Trichocoleopsis S. Okamura
Herzogianthaceae Stotler & Crand.-Stotl.: Herzogianthus R. M. Schust. See p. 54.
ORDER JUNGERMANNIALES H. Klinggr.
Leaves succubous, incubous, or transverse, undivided or variously lobed, sometimes complicate, but then usually with the smaller lobe(s), or lobules, dorsal,
rarely with inflated water sacs of the Lejeunea-type; underleaves present or
absent; rhizoids fascicled from the underleaf base or scattered along the ventral
side of the stem; branches exogenous or endogenous, lateral or ventral; spore
germination usually exosporic.
SUBORDER Perssoniellineae R. M. Schust.
Plants large, anisophyllous or distichous (isophyllous in Pleurocladopsis); leaves
complicate-bilobed, with the lobes symmetric or if unequal, usually with the
smaller lobe dorsal, with the keel often winged; leaf insertion transverse, but
with dorsal lobes incubously shingled; rhizoids scattered (fascicled in
Pachyschistochila), magenta to purple (hyaline in Pachyschistochila), with the apices
highly branched and sometimes septate; branches lateral, of the Plagiochila-,
Frullania-, and Radula-type; androecia dispersed on leading axes, with the bracts
scarcely differentiated, with the antheridia long-stalked; perianths absent; sporophytes enclosed in a coelocaule; gemmae absent.
Perssoniellaceae R. M. Schust. ex Grolle: Perssoniella Herzog
Schistochilaceae H. Buch: Gottschea Nees ex Mont. [including Paraschistochila
R. M. Schust.], Pachyschistochila R. M. Schust. & J. J. Engel, Pleurocladopsis
R. M. Schust., Schistochila Dumort.
SUBORDER Lophocoleineae Schljakov
Leaves transverse, succubous, or incubous, divided into 2 to 4 lobes or undivided;
underleaves usually conspicuous (reduced or lacking in Phycolepidozia, Brevianthus,
Chonocolea, and Plagiochilaceae); perianths, when present, often with three broad
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B. Crandall-Stotler and others
keels; capsule wall usually polystratose, only rarely 2-stratose; spore germination
exosporic, mostly of the Nardia-type; gemmae rare.
Pseudolepicoleaceae Fulford & J. Taylor: Archeophylla R. M. Schust.,
Blepharostoma (Dumort.) Dumort., Chaetocolea Spruce, Herzogiaria
Fulford ex Hässel, Isophyllaria E. A. Hodgs. & Allison, Pseudolepicolea
Fulford & J. Taylor [including Archeochaete R. M. Schust. and Lophochaete
R. M. Schust.], Temnoma Mitt.
Trichocoleaceae Nakai: Eotrichocolea R. M. Schust., Leiomitra Lindb., Trichocolea
Dumort.
Grolleaceae Solari ex R. M. Schust.: Grollea R. M. Schust.
Mastigophoraceae R. M. Schust.: Dendromastigophora R. M. Schust.,
Mastigophora Nees
Herbertaceae Müll. Frib. ex Fulford & Hatcher: Herbertus Gray, Olgantha
R. M. Schust., Triandrophyllum Fulford & Hatcher
Vetaformataceae Fulford & J. Taylor: Vetaforma Fulford & J. Taylor
Lepicoleaceae R. M. Schust.: Lepicolea Dumort.
Phycolepidoziaceae R. M. Schust.: Phycolepidozia R. M. Schust.
Lepidoziaceae Limpr.: Acromastigum A. Evans, Amazoopsis J. J. Engel & G. L. S.
Merr., Arachniopsis Spruce, Bazzania Gray, Chloranthelia R. M. Schust.,
Dendrobazzania R. M. Schust. & W. B. Schofield, Drucella E. A. Hodgs.,
Hyalolepidozia S. W. Arnell ex Grolle, Hygrolembidium R. M. Schust.,
Isolembidium R. M. Schust., Kurzia G. Martens, Lembidium Mitt., Lepidozia
(Dumort.) Dumort., Mastigopelma Mitt., Megalembidium R. M. Schust.,
Micropterygium Lindenb., Nees & Gottsche, Monodactylopsis (R. M. Schust.)
R. M. Schust., Mytilopsis Spruce, Neogrollea E. A. Hodgs., Odontoseries
Fulford, Paracromastigum Fulford & J. Taylor, Protocephalozia (Spruce)
K. I. Goebel, Pseudocephalozia R. M. Schust., Psiloclada Mitt., Pteropsiella
Spruce, Sprucella Steph., Telaranea Spruce ex Schiffn., Zoopsidella
R. M. Schust., Zoopsis Hook. f. ex Gottsche, Lindenb. & Nees
Lophocoleaceae Vanden Berghen: Amphilophocolea R. M. Schust., Chiloscyphus
Corda [including Campanocolea R. M. Schust.], Clasmatocolea Spruce,
Conoscyphus Mitt., Cyanolophocolea R. M. Schust., Evansianthus R. M. Schust. &
J. J. Engel [including Austrolembidium Hässel], Hepatostolonophora J. J. Engel &
R. M. Schust., Heteroscyphus Schiffn., Lamellocolea J. J. Engel, Leptophyllopsis
R. M. Schust., Leptoscyphopsis R. M. Schust., Leptoscyphus Mitt., Lophocolea
(Dumort.) Dumort.], Pachyglossa Herzog & Grolle, Perdusenia Hässel,
Physotheca J. J. Engel & Gradst., Pigafettoa C. Massal., Platycaulis R. M. Schust.,
Pseudolophocolea R. M. Schust. & J. J. Engel, Stolonivector J. J. Engel,
Tetracymbaliella Grolle, Xenocephalozia R. M. Schust.
1 Morphology and classification of the Marchantiophyta
Brevianthaceae J. J. Engel & R. M. Schust.: Brevianthus J. J. Engel & R. M. Schust.
Chonecoleaceae R. M. Schust. ex Grolle: Chonecolea Grolle
Plagiochilaceae Müll. Frib. & Herzog: Acrochila R. M. Schust., Chiastocaulon Carl,
Pedinophyllopsis R. M. Schust. & Inoue, Pedinophyllum (Lindb.) Lindb.,
Plagiochila (Dumort.) Dumort. [including Rhodoplagiochila R. M. Schust.,
Steereochila Inoue, Szweykowskia Gradst. & E. Reiner], Plagiochilidium Herzog,
Plagiochilion S. Hatt., Proskauera Heinrichs & J. J. Engel, Xenochila R. M. Schust.
SUBORDER Cephaloziineae Schljakov
Leaves usually succubous (transverse in Cephaloziellaceae), undivided or
2-lobed, with the margins entire or with small teeth; underleaves absent or
very small; rhizoids scattered; branches of the ventral Bazzania-type common;
sporophytes usually enclosed by a calyptra and perianth; gemmae common.
Adelanthaceae Grolle: Adelanthus Mitt. [including Pseudomarsupidium Herzog],
Calyptrocolea R. M. Schust., Wettsteinia Schiffn.
Jamesoniellaceae He-Nygrén, Juslén, Ahonen, Glenny & Piippo: Anomacaulis
(R. M. Schust.) Grolle, Cryptochila R. M. Schust., Cuspidatula Steph.,
Denotarisia Grolle, Jamesoniella (Spruce) Carrington, Nothostrepta
R. M. Schust., Pisanoa Hässel, Protosyzygiella (Inoue) R. M. Schust.,
Syzygiella Spruce, Vanaea (Inoue & Gradst.) Inoue & Gradst.
Cephaloziaceae Mig.: Alobiella (Spruce) Schiffn., Alobiellopsis R. M. Schust.,
Anomoclada Spruce, Apotomanthus (Spruce) Schiffn., Cephalozia (Dumort.)
Dumort., Cladopodiella H. Buch, Fuscocephaloziopsis Fulford, Haesselia
Grolle & Gradst., Hygrobiella Spruce, Iwatsukia N. Kitag., Metahygrobiella
R. M. Schust., Nowellia Mitt., Odontoschisma (Dumort.) Dumort.,
Pleurocladula Grolle, Schiffneria Steph., Schofieldia J. D. Godfrey, Trabacellula
Fulford
Cephaloziellaceae Douin: Allisoniella E. A. Hodgs. [including Protomarsupella
R. M. Schust.], Amphicephalozia R. M. Schust., Cephalojonesia Grolle,
Cephalomitrion R. M. Schust., Cephaloziella (Spruce) Schiffn., Cephaloziopsis
(Spruce) Schiffn., Cylindrocolea R. M. Schust., Gymnocoleopsis (R. M. Schust.)
R. M. Schust., Kymatocalyx Herzog, Stenorrhipis Herzog
Scapaniaceae Mig. [including Chaetophyllopsidaceae R. M. Schust. and
Lophoziacae Cavers]: Anastrepta (Lindb.) Schiffn., Anastrophyllum (Spruce)
Steph., Andrewsianthus R. M. Schust. [including Cephalolobus R. M. Schust.],
Barbilophozia Loeske, Chaetophyllopsis R. M. Schust., Chandonanthus Mitt.,
Diplophyllum (Dumort.) Dumort., Douinia (C. N. Jensen) H. Buch,
Gerhildiella Grolle, Gymnocolea (Dumort.) Dumort., Hattoria R. M. Schust.,
Isopaches H. Buch, Krunodiplophyllum Grolle, Lophozia (Dumort.) Dumort.,
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B. Crandall-Stotler and others
Macrodiplophyllum (H. Buch) Perss., Plicanthus R. M. Schust.,
Pseudocephaloziella R. M. Schust., Roivainenia Perss., Scapania (Dumort.)
Dumort., Scapaniella H. Buch, Schistochilopsis (N. Kitag.) Konst.,
Sphenolobopsis R. M. Schust. & N. Kitag., Sphenolobus (Lindb.) Berggr.,
Tetralophozia (R. M. Schust.) Schljakov, Tritomaria Schiffn. ex Loeske
SUBORDER Jungermanniineae R. M. Schust. ex Stotler & Crand.-Stotl.
Leaves succubous, rarely transverse (incubous in Isotachis and Calypogeiaceae),
undivided or 2(4)-lobed; anisophyllous or distichous (isophyllous in Antheliaceae); stem perigynia, hollow marsupia of the Calypogeia-type or solid marsupia
of the Tylimanthus-type common; perianths often absent; capsules ellipsoidal to
cylindric, with the wall often 2-stratose; gemmae present in some taxa.
Myliaceae Schljakov: Leiomylia J. J. Engel & Braggins, Mylia Gray
Trichotemnomataceae R. M. Schust.: Trichotemnoma R. M. Schust.
Balantiopsidaceae H. Buch: Anisotachis R. M. Schust., Acroscyphella N. Kitag. &
Grolle [= Austroscyphus R. M. Schust., nom. illeg.], Balantiopsis Mitt.,
Eoisotachis R. M. Schust., Hypoisotachis (R. M. Schust.) J. J. Engel & G. L. S.
Merr., Isotachis Mitt., Neesioscyphus Grolle, Ruizanthus R. M. Schust.
Blepharidophyllaceae R. M. Schust.: Blepharidophyllum Aº ngstr., Clandarium
(Grolle) R. M. Schust.
Acrobolbaceae E. A. Hodgs.: Acrobolbus Nees, Austrolophozia R. M. Schust.,
Enigmella G. A. M. Scott & K. G. Beckm., Goebelobryum Grolle, Lethocolea
Mitt., Marsupidium Mitt., Tylimanthus Mitt.
Arnelliaceae Nakai: Arnellia Lindb., Gongylanthus Nees, Southbya Spruce,
Stephaniella J. B. Jack, Stephaniellidium S. Winkl. ex Grolle
Jackiellaceae R. M. Schust.: Jackiella Schiffn.
Calypogeiaceae Arnell: Calypogeia Raddi, Eocalypogeia (R. M. Schust.)
R. M. Schust., Metacalypogeia (S. Hatt.) Inoue, Mnioloma Herzog.
Delavayellaceae R. M. Schust.: Delavayella Steph.
Mesoptychiaceae Inoue & Steere: Hattoriella (Inoue) Inoue, Leiocolea (Müll. Frib.)
H. Buch, Liochlaena Nees, Mesoptychia (Lindb.) A. Evans
Jungermanniaceae Rchb.: Arctoscyphus Hässel, Bragginsella R. M. Schust.,
Cryptocolea R. M. Schust., Cryptocoleopsis Amak., Cryptostipula R. M.
Schust., Diplocolea Amak., Gottschelia Grolle, Horikawaella S. Hatt. &
Amakawa [Invisocaulis R. M. Schust. nom. nud.], Jungermannia L., Nardia
Gray, Notoscyphus Mitt., Scaphophyllum Inoue, Solenostoma Mitt. [including
Plectocolea (Mitt.) Mitt.]
Geocalycaceae H. Klinggr.: Geocalyx Nees, Harpanthus Nees, Saccogyna Dumort.,
Saccogynidium Grolle
1 Morphology and classification of the Marchantiophyta
Gyrothyraceae R. M. Schust.: Gyrothyra M. Howe
Antheliaceae R. M. Schust.: Anthelia (Dumort.) Dumort.
Gymnomitriaceae H. Klinggr.: Acrolophozia R. M. Schust., Apomarsupella
R. M. Schust., Eremonotus Lindb. & Kaal. ex Pearson [including
Anomomarsupella R. M. Schust.], Gymnomitrion Corda, Herzogobryum
Grolle, Lophonardia R. M. Schust., Marsupella Dumort., Nanomarsupella
(R. M. Schust.) R. M. Schust., Nothogymnomitrion R. M. Schust.,
Paramomitrion R. M. Schust., Poeltia Grolle, Prasanthus Lindb.
Acknowledgments
The financial support of NSF grant EF-0531750 is gratefully acknowledged. We also thank John Engel and Matt von Konrat for providing us with
critical field specimens from New Zealand, and Christine Davis for sharing
unpublished sequence data with us.
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Note added in proof.
Herzogianthaceae Stotler & Crand.-Stotl., fam. nov. Type genus: Herzogianthus R. M. Schust.
(Familia haec a Ptilidiaceis similis sed differt foliis dimorphis, succubis vel subtransversalibus, cum foliis
ramorum vaginatis et connatis dorsaliter, cum ciliis foliorum setosis, unicellulis; amphigastriis quadrifidis in
caulibus robustioribus; sporis > 60 mm.)
2
Morphology, anatomy, and
classification of the Bryophyta
b e r n a r d g o f f i n e t , w i l l i a m r . b u ck a n d
a. jonathan shaw
2.1
Introduction
With approximately 13 000 species, the Bryophyta compose the
second most diverse phylum of land plants. Mosses share with the
Marchantiophyta and Anthocerotophyta a haplodiplobiontic life cycle that
marks the shift from the haploid-dominated life cycle of the algal ancestors
of embryophytes to the sporophyte-dominated life cycle of vascular plants. The
gametophyte is free-living, autotrophic, and almost always composed of a leafy
stem. Following fertilization a sporophyte develops into an unbranched axis
bearing a terminal spore-bearing capsule. The sporophyte remains physically
attached to the gametophyte and is at least partially physiologically dependent
on the maternal plant. Recent phylogenetic reconstructions suggest that three
lineages of early land plants compose an evolutionary grade that spans the
transition to land and the origin of plants with branched sporophytes (see
Chapter 4). The Bryophyta seem to occupy an intermediate position: their
origin predates the divergence of the ancestor to the hornworts and vascular
plants but evolved from a common ancestor with liverworts (Qiu et al. 2006).
The origin of the earliest land plants can be traced back to the Ordovician and
maybe the Cambrian (Strother et al. 2004). Although unambiguous fossils of
mosses have only been recovered from sediments dating from younger geological periods (Upper Carboniferous), divergence time estimates based on molecular phylogenies suggest that the origin of mosses dates back to the
Ordovician (Newton et al. 2007) and thus that their unique evolutionary history
spans at least 400 million years. During this time, the lineage has undergone
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
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B. Goffinet and others
multiple radiations that have resulted in a broad spectrum of morphological,
ontogenetic, anatomical, and cytological diversity.
In this chapter, we describe the features that unite the Bryophyta and
characterize their main lineages. Detailed descriptions of moss morphology
are provided by Ruhland (1924), Goebel (1898a), and Campbell (1895). The
morphological diversity of the Bryophyta is exceptionally well illustrated
in the second edition of the illustrated glossary of bryophytes by Malcolm &
Malcolm (2006).
2.2
Modular architecture of the vegetative plant body
The vegetative plants correspond to the gametophyte: a haploid multicellular body whose function is to develop sex organs or gametangia. The architecture of the gametophyte follows a modular pattern: the meristematic activity
of the apical cell yields cells undergoing divisions to form building blocks or
metamers, which are assembled into modules (Mishler & DeLuna 1991). A hierarchical arrangement of modules forms a branch system, which may be reiterated. The shape of the apical cell typically approximates an inverted tetrahedron,
as seen in some liverworts, with three oblique triangular cutting faces and a
convex outer surface (Crandall-Stotler 1980). Only members of Fissidens possess a
lenticular apical cell with two sides, but even here the apical cell starts out as a
tetrahedral cell early in stem ontogeny (Chamberlin 1980). The apical cell gives
rise to derivatives in three (two) directions in a clockwise sequence. Each derivative follows a precise pattern of divisions that leads to a building block or
metamer. The first division in the derivative cell isolates an inner cell from
which cortical and conducting tissues will be formed. The outer cell develops
into the epidermis, including the leaf and branch initials. The branch initial
occurs always below the leaf initial. All metamers formed by an apical cell
compose a module. Longitudinal growth of the module is accomplished through
division, enlargement and elongation of cells composing each metamer. In
Takakia lepidozioides the meristematic activity is accounted for by a ring of cells
surrounding a rather quiescent central cell (Crandall-Stotler 1986). In Sphagnum,
the activity of the tetrahedral apical cell is complemented by that of a secondary
subapical meristem composed of cells of the primary metamer that undergo
several anticlinal divisions resulting in lines of about nine cells, which each
dramatically elongate by a factor of nearly ten (Ligrone & Duckett 1998).
Vegetative growth of mosses results from the accumulation of cell lines, and
all cells of one module have an origin that can be traced to a single apical cell.
The apical cell of each branch started out as an initial on the epidermis of the
axis (stem or branch) onto which it is attached.
2 Morphology and classification of Bryophyta
2.3
Organography of the gametophyte
Macroscopically the vegetative body of mosses can be divided into
rhizoids, stems and branches, and leaves.
2.3.1
Rhizoids
The filaments that function in anchoring the plant to the substrate,
and may be involved in water conduction, are analogous to roots but differ in
their very simple architecture. Each rhizoid is in fact a uniseriate (rarely multiseriate) filament of elongate and smooth or roughened cells separated by oblique crosswalls. The multicellular rhizoids of mosses, except for those of
Sphagnum, Andreaea, and Andreaeobryum, are thigmotropic, winding tightly
around solid objects (Newton et al. 2000). This ability is best expressed in some
Polytrichaceae, where rhizoids may form rope-like bundles composed of narrow
rhizoids coiling around a central larger rhizoid (Whigglesworth 1947). Rhizoids
grow from epidermal cells either at the base of the stem, along the ventral side
of the stem and branches, or the costa. Rhizoids rarely emerge from specialized
cells, nematogens, at the apical portion of the lamina. The stems of various
terricolous mosses are sheathed in a more or less extensive coat of white or
reddish brown rhizoids, which may serve in the external conduction of water
(Schofield 1981; see Chapter 6), although a clear pattern between rhizoid abundance and water availability is not evident (Crundwell 1979). In some mosses,
large, highly branched rhizoids originate from large cells lining the branch
initials, and may have a protective function like pseudoparaphyllia (Schofield
1985). In Sphagnum rhizoids occur only at the base of the thalloid protonemata
and are lacking on mature leafy plants, except for a single species from New
Caledonia (Iwatsuki 1986). Takakia is characterized by the complete absence of
rhizoids (Schuster 1997), as are some pleurocarpous mosses, such as species of
Scorpidium (Koponen 1982). In most cases, the lack of rhizoids in nature contrasts
with their presence in vitro, suggesting that their development may be environmentally controlled in the wild (Duckett 1994a) as it is in culture (Duckett
et al. 1998). Furthermore, the density, length, and branching of rhizoids produced by pleurocarpous mosses is very much influenced by the nature of the
substrate colonized (Odu 1978). The environmental factors that stimulate rhizoid production continue to elude bryologists.
Some mosses develop perennating structures called gemmae or tubers on
their rhizoids (Imura & Iwatsuki 1990). Tubers, which lack an abscission cell
diagnostic of gemmae (Duckett et al. 1998) may be uni- or multicellular, uniseriate or spherical. Their development may be triggered by drought (Arts 1990),
which may support the view that tubers offer a means to resist prolonged dry
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B. Goffinet and others
periods (Arts 1986) but their adaptive value to dry environments remains to be
critically tested (Newton & Mishler 1994). Rhizoidal tubers occur in various
lineages of acrocarpous mosses, including the Polytrichaceae, Funariaceae,
Bryaceae, Pottiaceae, and Dicranaceae. They seem, by contrast, to be absent in
pleurocarpous mosses. Some rhizoidal appendages similar to tubers result from
modification of rhizoidal cells following fungal infections (Martı́nez-Abaigar
et al. 2005). Indeed the development of zoosporangia within the moss cells
leads to swelling of the rhizoid tip cells or the side branch initials. Both cells
are characterized by thin walls, and hence are vulnerable to infection by oomycetes. Points of entry of the fungus in the rhizoid are often revealed by pegs or
ingrowths of cell wall material deposited by the cell as a likely response to the
fungal aggression (Martı́nez-Abaigar et al. 2005).
2.3.2
Stems
Vegetative axes display an architecture that follows a very simple
Bauplan: epidermal cells surround a cortex of large parenchyma cells, which
may surround a central strand of narrow, putative structural and waterconducting cells. Some authors (e.g. Zander 1993) refer to the outer two layers
as cortex and central cylinder, respectively, and others such as Malcolm &
Malcolm (2006) equate ‘‘central cylinder’’ with ‘‘central strand’’. The transition
between epidermis and cortex can be either abrupt (Fig. 2.1K) or gradual. The
pigmentation of the outer cells is sometimes shared with cortical cells, and both
tissues can have incrassate cell walls. The epidermis is uni- to multistratose and
its cells retain their cytoplasm and organelles. Stomata are always lacking, but a
cuticle, even if thin, covers the surface. In various mosses, the epidermal
cells are thin-walled and inflated, and the epidermis is then referred to as a
hyalodermis. This tissue is conspicuously developed in Sphagnum, where the
hyalocysts, which may have one or more conspicuous pores on their surface,
function in external water movement. In many pleurocarpous mosses the
stems and branches are clothed with paraphyllia, slightly branched epidermal
outgrowths that differ from rhizoids in their green color and shorter cells.
Paraphyllia likely serve in external water conduction, but are also photosynthetically active given the abundance of chloroplasts.
Juvenile leaves hide delicate filaments that line the insertion of the leaf.
These hairs originate from the leaf initial and secrete a mucilage of polysaccharides (Ligrone 1986) that may be essential in preventing the delicate growing
apices from dehydrating (Schofield & Hébant, 1984). In various pleurocarpous
mosses, axillary hairs may develop elsewhere on the stem (Ignatov & Hedenäs
2007); in these cases their function remains ambiguous. Axillary hairs typically
consist of a single unbranched row of several short to elongate hyaline cells
2 Morphology and classification of Bryophyta
Fig. 2.1. Brymela websteri (Pilotrichaceae), as an example of a moss. (A) Aspect
showing plagiotropic habit with somewhat erect branches. (B) Detail of branch system showing
sporophyte borne on a lateral branch; the sporophyte is composed of a seta, capsule and
operculum with the urn covered by a calyptra. (C) Young capsule with calyptra. (D) Calyptra. (E)
Operculum. (F) Exostome tooth, composed of two columns of cells. (G) Leaves with strong
double costa. (H) Leaf apex. (I) Laminal cells at mid-leaf. (J) Cells at base of leaf. (K) Portion of stem
cross-section. (L) Axillary hair.
(rarely only one such cell) that often are subtended by one or more brown cells
(Fig. 2.1L). The apical cell is typically longer and club-shaped. They vary greatly in
size, number and shape, and although generally overlooked, seem to be taxonomically and hence phylogenetically informative (Hedenäs 1989a, Kruijer 2002),
although infraspecific variation is possible (Zander 1993). Similar hairs are occasionally found associated with branches, as in Dicranum or Encalypta. These trichomes, like ordinary axillary hairs, exude mucilage, but because they originate
from a metamer distinct from that of the leaf that subtends them they are in fact
best seen as mucilaginous leaves (Berthier et al. 1971). Andreaeobryum and Takakia
carry beaked mucilage or slime papillae (Murray 1988, Schuster 1984).
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Each metamer develops a superficial branch and leaf initial. Berthier (1973)
offered a comprehensive account of the ontogenetic series leading to their
formation (see his Fig. 8Z1C). The two initials are isolated early in metameric
development. The derivative of the apical cell undergoes a first periclinal division that separates an initial for the external tissues (IE) from the initial for the
internal tissues. The first anticlinal division in the IE isolates the primary foliar
initial to the outside. The inner cell undergoes another anticlinal division that
will yield the primary branch initial downward. At this point the branch initial
is separated from the leaf initial by a single cell. This cell undergoes numerous
divisions that at the proximal end will yield the cells contributing to the base of
the leaf, including the cells from which axillary hairs are developed, and below
the leaf insertion the cells composing the stem epidermis (Crandall-Stotler
1980). The elongation of the latter results in the branch and leaf initial to be
separated, to the extent that the branch initial of a metamer will seem located in
the axil of the leaf of the metamer below. Except in taxa that lack branches, the
branch initial undergoes divisions to form a bud or a primordium. The primordium develops either readily into a new module such as in feathermosses with
pinnately branched stems (e.g. Ptilium crista-castrensis and Thuidium delicatulum)
or it becomes dormant. A bud is a juvenile module that enters dormancy after
developing tiny leaves. A primordium that halts its development after a short
series of divisions before any leaves are produced is said to be naked. In various
pleurocarpous mosses, primordia are protected by small appendages called
pseudoparaphyllia. The term has traditionally been reserved for specialized
structures restricted to the immediate vicinity of a branch primordium or
branch bud. The shape of pseudoparaphyllia varies from filamentous to foliose;
most species seem to produce only one type, but exceptions exist (Akiyama
1986). Akiyama & Nishimura (1993) distinguish ‘‘true’’ pseudoparaphyllia from
scaly leaves based on ontogenetic grounds: the former arises from the stem, the
latter from the branch bud. Ignatov & Hedenäs (2007) reject such distinction and
broaden the concept of pseudoparaphyllia to include all appendages produced
near leaf decurrencies and corners, and around primordia, and even those
scattered along the stem, that have traditionally been called paraphyllia. They
restrict the latter term to those structures developed in longitudinal rows on the
stem. The phylogenetic significance of these appendages remains ambiguous, in
part due to the controversy about their homology across lineages.
The anatomical complexity of the stem varies among mosses (Hébant 1977),
with the Polytrichopsida exhibiting the greatest internal differentiation,
whereas the Andreaeopsida show the least cytological variation (Kawai 1989).
The parenchyma cells composing the cortex are typically somewhat larger
than the epidermal cells, and in many peristomate mosses, outer and inner
2 Morphology and classification of Bryophyta
parenchyma cells may be morphologically distinct (Kawai 1989 and references
therein). The cortex may serve as a structural or a storage tissue, and the
thickness of the cell wall varies accordingly. A photosynthetic function may
be restricted to the outer layers or to the young portions of the stem. Stereids are
rather narrow prosenchymatous cells (i.e. long-tapered) with incrassate walls
impregnated with a polyphenolic compound (other than lignin; Schofield &
Hébant 1984). Stereids typically retain their protoplast at maturity. They occur
in the central axis along with hydroids (see below) or below the epidermis
in the cortex. The remainder of the cortex typically consists of more or less
large parenchymatous cells, with flat or somewhat rounded ends. These cells
may accumulate lipids or starch, which can be hydrolyzed and redistributed
throughout the plant.
Transport within the plant is accomplished in part by undifferentiated
parenchyma cells of the cortex, or by specialized conducting cells, the hydroids (Hébant 1977). These hydroids, with the associated parenchyma cells and
stereids compose the water conducting tissue or hydrome. It is best developed
in members of the Polytrichopsida, and is reduced to completely lacking
in various lineages of the Bryopsida (Hébant 1977), most notably in aquatic
mosses (Haberlandt 1886, Vitt & Glime 1984). Hydroids resemble stereids in
their prosenchymatous shape, but lack protoplastic content at maturity. They
occur in Takakia and peristomate mosses but are lacking in the Sphagnopsida,
Andreaeopsida, and Andreaeobryopsida (Ligrone et al. 2000). Their walls are
impregnated with polyphenols other than lignin, which is diagnostic of tracheids of vascular plants (Miksche & Yasuda 1978). Hydroids also lack spiral or
annular secondary wall depositions. Furthermore, xylans that link strands of
cellulose in secondary cell walls in vascular plants, and are considered essential
for the evolution of vascular and supportive tissues, are lacking in mosses
(Carafa et al. 2005). Immunocytological techniques Ligrone et al. (2002) revealed
that water-conducting cells in particular exhibit great diversity in cell wall
chemistry. Takakia differed from other bryophytes in the composition of its
cell walls, suggesting that their water-conducting cells are not homologous to
those of peristomate mosses. Furthermore, in Takakia the cells are short with
the end walls nearly perpendicular to the axis. The contact surface between
two consecutive cells is thus reduced but flow is facilitated by the presence of
small perforations derived from plasmodesmata. By contrast, the hydroids of
the Polytrichopsida and Bryopsida are slightly to highly elongate and lack
small pores, at least at maturity. The thickness of the hydroid walls varies:
thin all around to thickened and heterogeneous lateral walls and thin endwalls across which much of the transport takes place (Scheirer 1980, Ligrone
et al. 2000).
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Actively dividing cells are by definition undifferentiated and hence unlikely
to engage in photosynthetic activities to sustain their energetic needs. Similarly,
cell elongation and differentiation requires large amounts of energy to fuel
anabolic reactions. Developing moss metamers depend on supplies of photosynthates and likely other organic compounds from other metamers and even
modules. Long-distance symplastic transport from old to young tissues has been
demonstrated in Sphagnum and the Polytrichaceae (Raven 2003). Although the
speed of such transport seems hardly indicative of optimal specialization, cells
involved in it share a series of attributes that are reminiscent of those exhibited
by the sieve cells of tracheophytes, such as the lack of a vacuole and nuclear
degeneration (Ligrone et al. 2000). Food-conducting cells are elongate and their
end-walls contain many pores derived from plasmodesmata. Differentiation
of these cells is most pronounced in the Polytrichales, and the term leptoid
is restricted to these. For the food-conducting cells of other mosses the
term ‘‘conducting parenchyma cells’’ is preferred (Ligrone et al. 2000). Foodconducting cells are characterized primarily by cytological aspects of their
organization. Such features are found in other cells throughout the moss
plant, suggesting that food transport occurs not just in the stem (e.g. rhizoids;
see tables in Ligrone et al. 2000). Hence conducting parenchyma cells, even more
than leptoids, are not distinguished with ease in light microscopy. In the stem,
leptoids and their analogous parenchyma cells can be found throughout the
cortex, with maybe a preferential location around hydroid strands.
The transverse section of the stem of various mosses reveals satellite bundles
of water and food-conducting cells around the main axial strand. In longitudinal
section these strands would connect at their distal ends with the conducting
tissues in the leaf nerve, and hence are called leaf traces. In most mosses, these
traces do not join with the main axial conducting tissues, and instead disappear
within the cortex. True leaf traces reach the central strand. The thickness of the
leaf trace (i.e. the number of hydroids composing it) and whether or not leaf
traces join the axial hydrome varies among and even within species, although
true leaf traces are commonly developed in the Polytrichaceae, whereas false
traces seem to characterize the Bryopsida. It is worth noting that both the
strength of the leaf trace and its contact with the main strand, as well as the
width of the axial hydrome itself, may weaken along a moisture gradient
(Hébant 1977), for example when a species is transferred to and grown in
aquatic conditions (Zastrow 1934).
The moss stem is typically a solid organ, except for a central cavity resulting
from the collapse of the axial hydrome. Only in Canalohypopterygium and
Catharomnion (Hypopterygiaceae) are axillary cavities present in the cortex,
extending from the stolon through the stipe and rachis to the branches
2 Morphology and classification of Bryophyta
(Kruijer 2002). Whether these cavities form via schizogeny or lysogeny is not
clear. These cavities are filled with lipids, which may serve to store energy, or
they may be useful in deterring herbivores or infectious bacteria and fungi, but
such function remains to be tested (Pelser et al. 2002).
2.3.3
Modifications of the stem
In mosses the female gametangia are developed at the apex of a module.
The transition from vegetative to sexual module results in the cessation of
growth of that module, except in the Sphagnopsida and the Andreaeopsida. In
these lineages, the gametophytic tissue resumes growth after fertilization to
elevate the sporangium above the gametangial leaves, a role restricted to the
sporophytic seta in other mosses. The gametophytic stalk elevating the sporophyte is called a pseudopodium. In Andreaea the pseudopodium develops
through a meristematic activity of cells from the archegonial stalk (Roth
1969). In some taxa, it retains a stem-like appearance with scattered reduced
leaves, axillary hairs and even archegonia (Murray 1988), which suggests that in
these species the cauline tissue (i.e. the receptacle) participates in pseudopodium formation. The pseudopodium of peatmosses develops solely from the
receptacle beneath the vaginula (Roth 1969), as evidenced by the presence of
scattered aborted archegonia. Murray (1988) speculated that the Andreaeopsida
and Sphagnopsida acquired a pseudopodium independently. All other mosses
except for some species of Neckeropsis (Neckeraceae; Touw 1962) lack a pseudopodium, at least one elevating the capsule. In Aulacomnium, the term pseudopodium is used differently and represents a defoliated extension of the stem
that carries brood bodies typically arranged in a terminal crown. Whether the
apical or a new subapical meristematic region provides the metamers to the
pseudopodium formation is not known.
One last series of modifications in the stem anatomy occurs at the
gametophyte–sporophyte junction. The sporophyte in mosses as in all bryophytes is permanently attached to and nutritionally dependent on the female
gametophyte. Such maternal care or matrotrophy is considered a critical innovation preceding the origin of embryophytes and thus essential to the evolution
of land plants (Graham & Wilcox 2000). Matrotrophy is facilitated by cytological
and ultrastructural modifications on one or both sides of the generational
junction, a region called the placenta (Ligrone et al. 1993). Here we address
only changes pertaining to the gametophytic tissues (see below for characteristics of the sporophytic foot). A space resulting from the lysis of gametophytic
placental cells exists in all mosses (Frey et al. 2001). The degree of ingrowths
varies from short to labyrinth-like and long and from fine to coarse. Such
cell-wall modifications are lacking in Takakia, Sphagnum, Andreaea, and the
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B. Goffinet and others
Polytrichaceae, as well as in Dicranum among the Bryopsida. Although labyrinth
walls are lacking, specialization may occur in the thickness and texture of the wall.
All other mosses examined, from Tetraphis to Brachythecium, develop gametophytic
transfer cells early and in one to three layers depending on the lineage. Ligrone
et al. (1993) reported that in Diphyscium and Bryum the gametophytic tissues are
penetrated by tubular outgrowths of elongate epidermal cells of the foot. Frey et al.
(2001) could not confirm such haustoria, which Roth (1969) described as developing late in the ontogeny of the sporophyte. Specialization of the placental cells
pertains further to their cytological and ultrastructural characteristics: the cytoplasm is often dense and rich in lipids, the vacuole is typically reduced but large in
Sphagnum, the endoplasmic reticulum extensive, mitochondria numerous and
large, chloroplasts numerous, often less differentiated, rich in lipid-filled globuli
and sometimes filled with starch (Ligrone et al. 1993).
Stems have a broad range of morphological and anatomical diversity, with
the most complex anatomy displayed by the Polytrichaceae (Hébant 1977). One
member of this family holds the record for tallest terricolous moss: Dawsonia
superba can reach 70 cm in height. Pendent epiphytes in moist tropical forests or
aquatic species that benefit from buoyancy may have their gametophyte grow to
one meter or more in length. Alternatively, reductionary trends lead to virtually
invisible shoots: in Buxbaumia the female stem is reduced to a tiny axis with a
few leaves, and the sole antheridium is protected by one leaf, sessile on the
protonema (Goebel, fide Ruhland 1924).
2.3.4
Leaves
The sole unifying character of moss leaves is that they are always sessile
on the stem, inserted along their entire base, and hence are never petiolate. In
some species of Calymperaceae, the leaf lamina is contracted to the costa
between the distal end of the sheathing base and the lower end of the green
lamina; here the ‘‘petiole’’ is intralaminar rather than supporting the whole leaf
(Reese & Tan 1983). Leaves develop from the single leaf initial present in each
metamer. Their arrangement on the stem or phyllotaxy is shaped first by the
spatial arrangement of metamers, and thus the shape of the apical cell, and
further dictated by ecophysiological constraints. In most mosses, a spiral
arrangement of leaves, especially on orthotropic shoots minimizes shade and
maximizes light interception. The apical cell produces two successive derivatives at an angle closer to 1378 (Crandall-Stotler 1984). If the angle were 1208 (as
would be predicted if the apical cell were perfectly triangular in section), every
fourth leaf would be aligned vertically with the first one. Any deviation from
1208 results in more spiral turns needed for any two leaves to be aligned. In some
cases, the leaves form five conspicuous ranks (e.g. Conostomum); in others the
2 Morphology and classification of Bryophyta
phyllotaxy is such that the alignment of leaves is obscure at best. In Fissidens
leaves are developed in two opposing rows. Such distichous arrangement is
due to the lenticular shape of the apical cell, which thus has two rather than
three cutting faces. Distichous leaves also characterize other genera, such as
Bryoxiphium or Distichum, but their apical cells are tetrahedral. In Schistostega, the
distichous arrangement results from torsion of the stem, and consequently
characterizes only leaves below the apex. Apical leaves and all those on fertile
stems are radially inserted.
Mosses creeping over the substrate in low light environments seem to adopt a
complanate posture of their leaves, which, although inserted in more than two
ranks, lie at maturity in a single plane (e.g. Plagiothecium). The shift to complanate leaves is likely dependent on an oblique versus transverse insertion of the
leaves. In many taxa, the base of the leaf is differentiated to fulfill a function
other than or in addition to photosynthesis. In various Polytrichaceae or
Bartramiaceae, the base of the leaf clasps the stem, providing additional robustness to the insertion and thus support to the leaf. Clasping leaf-bases may also
create capillary spaces essential for the external conduction of water.
The leaves developing on young stems or branches often lack the characters
of mature leaves. A sharp morphological contrast between juvenile leaves at the
base of the module and mature leaves apically (sensu Mishler 1988), often
coupled with a gradual transition between them, is referred to as a heteroblastic
leaf series. This series refers to transformations in morphology of leaves along
the length of the shoot, and is thus different from the transformational series of
a given leaf during its maturation: an immature or ‘‘young’’ mature leaf may not
resemble a juvenile leaf at any of its developmental stages. Heteroblastic series
are common in mosses, although rarely very conspicuous. Juvenile leaves may
offer important phylogenetic clues (Mishler 1988). For one, it seems that even
distantly related mosses exhibiting strikingly different mature leaf morphologies exhibit highly similar juvenile leaf morphologies (e.g. Tortula and
Funaria, Mishler 1986).
In many branched plagiotropic mosses, stem and branch leaves are morphologically distinct. In Macromitrium the leaves on the creeping stems are much
reduced compared to those of the erect branches, which are similar to the stem
leaves of the close relative Orthotrichum, whose stems grow upright. In mosses
with erect stems composed of a vertical stipe with a horizontal branched rachis,
the stipe bears reduced, often scale-like and ecostate leaves whereas the rachis
produces well-developed leaves with a strong midrib. Such variations in leaf
morphology between modules is referred to as anisophylly (Newton 2007).
Leaf dimorphism also occurs around the circumference of a module (heterophylly), with dorsal and ventral leaves much reduced compared to the lateral
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B. Goffinet and others
ones. Reduced ventral leaves are often called amphigastria. Although common
in liverworts, they occur only in few lineages of mosses, and most notably the
Hypopterygiaceae. Such reduction may serve to maximize light exposure of
lateral leaves in plagiotropic mosses (e.g. Racopilum), but remains to be explained
in orthotropic taxa such as Epipterygium. Amphigastria may perform other functions such as create capillary spaces for external water or actually hold water as
in Cyathophorum tahitense, where the amphigastrium base is inflated into a little
pouch.
A functional basis for foliar dimorphism is evident when certain leaves
are specialized for asexual reproduction, such as the stenophylls of some
Calymperaceae with their reduced lamina and rod-like costa crowned by
gemmae (Reese 2000). Splash-cups may be formed by dense rosettes of differentiated leaves surrounding discoid gemmae (Tetraphis) or clusters of antheridia (e.g. Polytrichaceae and various Mniaceae). In most mosses, foliar
dimorphism occurs simply as a differentiation of vegetative and gametangial
leaves, and between perigonial and perichaetial leaves. In autoicous species,
the leaves surrounding antheridia often resemble juvenile leaves: they are
much smaller than the vegetative or perichaetial leaves on the same plant.
Perichaetial leaves are by contrast often larger and longer, sometimes following post-fertilization growth. The innermost perichaetial leaves can either be
the smallest (e.g. Mniaceae) or more often the largest of the perichaetial leaves
(e.g. Hypnales).
The interval between two successive leaves is determined by the elongation
of the epidermal cells of each metamer. Most mosses seem to have a regular
foliation of the axes. Stems that do not participate much in photosynthetic
activity have widely spaced leaves. For example, in Dendrohypopterygium arbuscula
the internodes on the erect stipe are long and the leaves distant from one
another. Similarly, in Rhodobryum roseum long internodes separate the lower
leaves, whereas the upper metamers hardly elongate, and as a result the upper
leaves form a dense rosette.
Each metamer derived from the cauline apical cells yields an initial from
which a leaf will develop. In most mosses, the apical cell of the leaf is two-sided,
producing derivatives in two directions, alternating between the left and the
right, but always in one plane. Only six derivatives may be produced in each
direction, before the apical cells cease to divide (Frey 1970). Thus the lamina
forms from building blocks resulting from the divisions of the derivative cells.
The ontogenetic patterns differ between leaves composed of a parenchymatous
network of five- to six-sided cells common to the Polytrichopsida and most
acrocarps, and those leaves composed of elongate prosenchymatous cells,
found in most pleurocarps (Frey 1970). The differences lay in the timing (delayed
2 Morphology and classification of Bryophyta
versus immediate) and the pattern of division of derivatives. Leaves with wide
rhombic cells, such as those of the Bryaceae and Hookeriaceae, seem to be
intermediate in their morphology, and hence may mark the transition from a
parenchymatous to prosenchymatous cell network (Frey 1970). Detailed ontogenetic studies of these taxa are lacking. In Andreaea, the apical cell exhibits two
or one cutting face(s). In Buxbaumia, the highly reduced leaves resemble those of
jungermannioid liverworts, in that they lack a single apical cell (Goebel 1898a).
Whether their development involves a basal meristem is not clear.
The lamina is unistratose in most mosses, except for the costa and in some
cases the marginal region. Stomata are always absent. A cuticle may be present
but if present then thin and largely ineffective in preventing water loss (Proctor
1979, 1984). The costa is derived from a variable number of so-called
‘‘Grundzellen’’ or fundamental cells. A series of periclinal and anticlinal divisions early in leaf ontogeny, results in multiple median layers of cells, present
even in young leaves at the apex of the stem. In Leucobryum, whose leaves are 3–6stratose for much of their width (except for a narrow winglike margin), periclinal divisions occur in juvenile leaves, suggesting that this region corresponds
to the costa. Other multistratose streaks in the leaf, including the margin, are
formed later in development.
Except for the deeply segmented leaves of Takakia, and the perigonial leaves
of Buxbaumia, moss leaves are never lobed: the lamina is a single blade. In fertile
stems of Schistostega, consecutive leaves may be connected by their lamina at
their base, giving the impression of a deeply incised or pinnately lobed ribbon,
but the leaves themselves are entire. In all other respects the leaves of mosses
exhibit a tremendous diversity, clearly too vast to fully describe here. The leaf is
typically composed of a single chlorophyllose blade. The most notable exception is the leaf of Fissidens, which, at least in the lower half, appears Y-shaped in
transverse section. The two arms of the Y correspond to the vaginant laminae
that embrace the stem and the leaf above it. The vaginant lamina makes up half
to 3/4 of the leaf length. The lower portion of the Y represents the dorsal lamina.
At the intersection of the three blades lies the costa. The dorsal lamina extends
down the costa but most often does not contribute to the insertion of the leaf,
although in some rare cases it is decurrent (Robinson 1970). Where the vaginant
lamina ends in the upper half of the leaf, a single ventral laminal blade faces the
dorsal wing. The dorsal and ventral blades are complanate with the stem, and
are best seen as outgrowth of the costa. The vaginant laminae that are transversely inserted onto the stem constitute the true leaf (Salmon 1899).
The general outline of the lamina varies between orbicular, to lingulate
truncate to linear. The margin of the lamina is sometimes entire but various
degrees of dentation and serration are common. Long multicellular marginal
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B. Goffinet and others
cilia are rare (e.g. Thelia), and sometimes restricted to perichaetial leaves
(e.g. Hedwigia ciliata). Teeth and cilia may be evenly distributed but they often
characterize only a particular segment of the margin. The teeth may occur in
pairs or singly. Depending on the length of the protrusion, we distinguish
laciniae composed of multiple cells, serrations composed of one whole cell,
serrulations due to protruding cell apices only and dentations due to lateral
conical projection of the cell wall. All these, except for laciniae, are common in
mosses and scattered across the phylogenetic tree. In Sphagnum walls of the
marginal and some laminal cells may be partially resorbed and the affected area
appears fringed.
The thickness of the lamina (excluding the costa, see below) varies from unito multistratose. In some mosses, only the margin is composed of multiple
layers (Mniaceae), whereas in others, the leaf is several cell-layers thick across
its width or only in discrete longitudinal strands (Vittia, Orthotrichum spp., or
Grimmia spp.). Among pleurocarpous mosses, pachydermous leaves have been
acquired independently in several lineages (Hedenäs 1993, Vanderpoorten et al.
2003), seemingly as a response to a transition to an aquatic habitat.
Whereas all mosses predating the origin of Oedipodium lack a midrib in their
leaves, such costae characterize many taxa of the Bryopsida. The costa is typically single, and unbranched, vanishing in the upper lamina, or extending well
beyond the leaf border (excurrent), forming a smooth or densely toothed awn. In
many pleurocarpous taxa and very few acrocarps, the costa is double and
V-shaped (see Fig. 2.1G), with the arms of the V varying from barely visible and
short to conspicuous and long. Only in a few taxa, does the costa appear truly
branched (e.g. Antitrichia). In some mosses (e.g. Eurhynchium and Pohlia spp.), the
costa ends below the leaf apex and forms a spine projecting from the dorsal
surface of the leaf. In Pilotrichum the costa emerges as a crest for part of its length,
and may even produce propagula (Buck 1998). Although the appearance of the
costa is generally fixed for a given species, its development can be environmentally altered: growing costate species in an aquatic medium results in the loss of
expression of the costa in newly formed leaves (Zastrow 1934). This may be
indicative of the costa fulfilling a role in water and nutrient transport. The costa
may contain water- (hydroids) and food-conducting cells. The latter are less
specialized than leptoids per se, and the term deuter or guide cell may be
preferred (Hébant 1977). Bands of stereids may cover the guide cells on one or
both sides and the surfaces of the costa may be covered by laminal cells. Thus in
transverse section the costa may appear homo- or heterogeneous. In fact the
costal anatomy varies significantly among mosses (Kawai 1968) and offers diagnostic features and hence phylogenetic information. The true pleurocarpous
mosses share a homogeneous costa, i.e., a costa lacking cell differentiation
2 Morphology and classification of Bryophyta
(Hedenäs 1994). In the Leucobryaceae, the costa is extremely broad, occupying
more than half the leaf width. The costa of the Polytrichaceae is typically
mounted by lamellae of green cells that run from the apex of the green lamina
to the transition of the sheathing base. The margin of the lamellae is covered in
wax (Proctor 1992) preventing water from filling the intralamellar space,
thereby allowing for CO2 absorption over a much larger surface (Proctor 2005).
In the Dicranaceae, ridges characterize the dorsal surface of the costa of various
taxa, and in Bryoxiphium and Sorapilla a single chlorophyllose dorsal extension
may run partially down the costa.
Laminal cells are far from monomorphic along the dimensions of the leaf. In
many acrocarpous mosses, the basal cells are rectangular, compared with short
isodiametric upper cells. In the angles of the leaf insertion, primarily in pleurocarps, the alar cells may form groups of small, dense, quadrate or of inflated
and thin-walled cells, as is diagnostic of the Sematophyllaceae. Large hyaline
cells seem designed for rapid absorption of excessive water that may be essential
for delaying dehydration of the leaf, as their differentiation is weakened when
the shoots develop under submerged conditions (Zastrow 1934). However, the
absorption of excess water would also result in increased turgor and the resulting forces may lead to changes in leaf posture, for example by pushing the leaf
away from the stem. In Ulota the basal marginal cells differ from inner laminal
cells in their quadrate shape and incrassate transverse walls. The differentiation
of marginal cells extends in many mosses further up the blade. In Mnium linear
cells line the whole lamina, forming a differentiated margin two or more cells
wide and thick. Such a margin of elongate cells may be essential for conducting
water within the leaf. Alternatively, a strong border may provide a structural
reinforcement to the strength of the leaf against abrasion in rheophilous taxa
(Vitt & Glime 1984). An intramarginal band of elongate cells, or teniolae, diagnoses various species of Calymperaceae, but not necessarily those with the
longest leaves. A structural role is thus not obvious.
Cells may vary in morphological attributes across the leaf blade, but walls of a
given cell may also vary in thickness and ornamentation. Racomitrium is diagnosed by wavy longitudinal anticlinal walls, and in Dicranum the thick axial
walls are often porose. In Steyermarkiella the transverse walls of the hyalocysts
(see below) are perforate. External ornamentations of the periclinal walls determines, along with the thickness of the cuticle, the shine of the leaf surface.
Mammillae are protrusions of the cell lumina above the surface of the cell,
whereas papillae are solid cell-wall protuberances. Papillae vary from small
and knobby to tall and antler-like, from cylindrical to crescent-shaped, from
single to numerous per cell. The presence of papillae (or that of a cuticle) is
revealed by the matte appearance of the leaf, versus a shininess when cells are
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smooth. Whether the role of papillae is to merely increase light absorption is
doubtful. Their presence dramatically increases the surface of the cell through
which water or gases needed for photosynthesis are exchanged. Papillae also
create capillary spaces essential for holding excessive water needed to delay loss
of turgor in photosynthetic cells (Proctor 2000a). Papillae may thus be a necessary evil for some plants: they need to hold on to water when available, but by
doing so they cover the cells with a CO2-impermeable layer. A solution may be to
impregnate the apex of the papilla with a water-repellent cuticle, and hence to
use papillae as snorkels emerging from the water surface (Proctor 2000b).
The pattern of cell wall thickening within cells and across the lamina determines the three-dimensional shape of the leaf and the changes in habit of the
leaf when dry. Differences in width and thickness of dorsal and ventral cell walls
in unistratose leaves shape the general curvature of the leaf: concave or convex.
When such differentiation is more localized, discrete shifts in curvature occur
along the laminar surface, such as longitudinal plications (plicate leaves), or
transverse or random undulations (undulate or rugose leaves). The adaptive
value of such modifications of the leaf are obscure, but it is worth noting that
in Tomentypnum nitens plications are lacking in leaves grown in submerged
conditions (Zastrow 1934). Many mosses exhibit hygroscopic movements of
the leaf. For example, the leaves of Helicophyllum always roll inward from the
apex down. In Ulota the leaves are curled or crisped when dry, but spreading
when moist. The basis for these movements must be accounted for by differences in length or thickness of adjacent walls of individual cells. Van Zanten
(1974) studied the role that is played by the marginal swelling tissue at the
transition between the clasping base and the green lamina in Dawsonia
(Polytrichaceae). He showed that the movement of the lamina is controlled by
the vertical lamellae in the joint area, which are composed of cells with differentially thickened walls: thicker walls swell upon hydration and pressure is
exerted, resulting in the leaf bending. The swelling tissue composed of transversely elongate incrassate cells serves not in directing the movement but rather
in preventing tearing under the torsion of the blade upon wetting.
The most conspicuous dimorphism in laminal cells involves the juxtaposition of chlorophyllose or assimilative cells and hyaline leucocysts either in a
single stratum or across the thickness of the leaf. Metabolic activities in mosses
may be constantly limited by the scarcity of water, and in the absence of
stringent mechanisms to control water balance mosses have acquired means
to hold excess water to delay dehydration and thus prolong periods suitable for
photosynthetic activities (Proctor 2000a,b; Chapter 6). Leuco- or hyalocysts are
cells devoid of their cytoplasm that function as reservoirs to temporarily store
water. In Sphagnum, chlorophyllose assimilative cells alternate with leucocysts
2 Morphology and classification of Bryophyta
within the unistratose lamina. The walls of the hyalocysts often bear internal
thickenings in the form of fibrils spun anticlinally. Dying the walls reveals
pores on exposed surfaces of the leucocysts. This diagnostic cell dimorphism
is lacking in juvenile leaves of Sphagnum (Mishler 1988), in late leaves of species
such as S. ehyalinum (Shaw & Goffinet 2000), and can be lost in newly developed
shoots when a typical species is grown in a water-saturated low-light environment (BG, pers. obs.).
Leucocysts are also conspicuously developed in some Bryopsida. In Encalypta
and some Pottiaceae, for example, the typically hyaline basal cells are elongate
and perforate on their outer (periclinal) and inner (anticlinal) walls, and likely
involved in water storage or conduction. In the Leucobryaceae, leucocysts form
multiple layers with one or more rows of chlorophyllose cells embedded in
between. The walls of the leucocysts are pored, but unlike in Sphagnum the pores
connect adjacent hyaline cells, rather than opening the cell to the atmosphere;
the outer wall may be broken but actual pores are lacking (Robinson 1985). A
water-holding function for the leucocysts seems intuitive, but would lead to the
chlorophyllose cells being sealed from the gaseous atmosphere and hence
deprived of essential carbon dioxide. Robinson (1985) argued that the hyaline
cells of older mature leaves down the stem serve primarily in excess water
storage, and that in young, photosynthetically active leaves the leucocysts are
filled with air needed for gas exchange. A leucobryaceous leaf architecture is
otherwise known only from some Calymperaceae and Dicranaceae.
Leaves offer many of the features essential for the identification of bryophytes. None of the mosses has entirely lost leaves, although some species rely
on a persistent protonema to form their vegetative body, but even here a few
leaves are produced to protect sex organs. By contrast, the leaves of Syrrhopodon
prolifer var. tenuifolius reach nearly 6 cm in length!
2.4
Branching in mosses
The vegetative body of mosses is typically composed of modules of
either identical or distinct hierarchical ranks as a result of branching. Every
metamer derived from the apical cell comprises a single branch initial below the
leaf initial, with the two separated by several epidermal cells. Although every
metamer thus has the potential to develop into a branch, not all initials develop
into primordia and branches, and if they do, their relative location on the
module may vary among species or higher rank lineages. Depending on the
distribution of branches, the polarity of their maturation along the stem, their
density and their function in the hierarchical system, mosses exhibit fairly
distinct life forms (LaFarge-England 1996).
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Fig. 2.2. Close-up of branching in Thuidium delicatulum. Note the monopodial type
of branching with modules of secondary and tertiary rank, giving the branch system
a feathery outline.
The development of branch initials is triggered in some mosses by the cessation of meristematic activity at the apex of the module, due, for example, to the
consumption of the apical cell in the formation of a sex organ. Such putative
apical dominance, likely mediated by auxin (Cooke et al. 2002) is much weaker
and maybe non-existent in mosses that branch freely. Determinate growth
characterizes the primary module of many acrocarps and subsequent hierarchical modules of many pleurocarps (Newton 2007). Branch development is
initiated either at the base of a module (basitonous branching) or at the apex
(acrotonous branching), and older branches are thus located above or below
younger branches, respectively. Based on the function of the new module, two
main branching patterns are recognized. Sympodial branching refers to the
development of innovations of the same hierarchical rank. Thus, a stem that
ceases to grow because of determinate growth produces a new axis, which acts
as a stem. Sympodial branching basically refers to a preservation of function
between two successive modules, in other words the reiteration of a module or
branch system. Most mosses with plagiotropic shoots develop branches continuously. Production of gametangia is transferred to the branches and the main
module remains vegetative, capable of virtually indeterminate growth. Such
monopodial branching pattern results in a somewhat feathery outline of the
moss (Fig. 2.2), depending on the frequency of branch production. The branches
themselves may repeat the pattern. As a result, beside the primary module (i.e.
the stem), and secondary modules (the first set of branches), the plant body may
2 Morphology and classification of Bryophyta
further be composed of tertiary and more rarely quaternary modules. A function
or even morphological differentiation of successive modules is not always
evident, and in such cases, all modules are best regarded as primary modules
(Newton 2007). The spatial distribution of the branches is dependent on (a)
the elongation of each metamer, in particular of the cells that separate
two consecutive branch initials, and (b) the dormancy of branch initials or
bud primordia, since not all primordia necessarily develop into branches. In
Dendrohypopterygium arbusculum the umbrella-like disposition of branches likely
results from a lack of elongation of internodes, and in Hypnum imponens the
pinnate branches that line the stem at regular intervals alternate with dormant
buds. In Sphagnum, only every fourth (Ruhland 1924; but third according to
Crum 2001) branch initial develops into a branch. Furthermore, each branch
undergoes a series of immediate branching events, giving rise to fascicles of two
to seven branches. At first the fascicles are tightly arranged at the apex of the
stem into a compact capitulum. Further down the stem, branches differentiate
and become either spreading or pendent. Such fascicular arrangement of
branches is lacking in Ambuchanania, the sister taxon of Sphagnum, and some
Sphagna.
Although the distribution of the sex organs (i.e., carpy, see below) influences
the mode of branching, it only shapes the potential of individual modules. The
function of the module ultimately determines which ability is expressed. For
example, in Macromitrium the stem gives rise to erect monopodial branches,
whose function it is to develop terminal sex organs. These branches may indeed
produce a sympodial innovation to carry on the function of the sexual module.
However, under some circumstances, the branch continues to grow and
becomes plagiotropic, ultimately contributing to the clonal growth of the
plant through indeterminate growth and monopodial branches. Thus, in this
case the branch has reverted to a stem function and thereby adopted the alternative branching mode. In essence, the type of branching pattern may vary
among modules of distinct hierarchical rank, and within a module over time.
Rarely does sexual dimorphism pertain to branching, but in phyllodioicous
species with genetically determined dwarf males, the latter lack the ability to
branch whereas the female plant may produce abundant innovations.
Branching is not merely a process whereby new foliate shoots are added to
the vegetative body. Some innovations are functionally more specialized. In
most acrocarpous mosses, sympodial innovations are the only means for the
plant to persist and engage in more than one sexual reproductive cycle.
Branching contributes significantly to clonal growth either above or below
ground. Indeed, many Polytrichaceae develop subterranean stolons or rhizomes
from which aerial branches develop. In the Gigaspermaceae, the rhizomes are
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perennial and offer a means of survival from destruction of the delicate aboveground shoots. In Canalohypopterygium rudimentary bristle-like branches may
serve as storage organs for oils. A few mosses rely on highly specialized
branches for asexual reproduction. In Orthodicranum flagellare, stiff branches
with minute leaves occur in clusters at the apex of the stem. Similar brood
branches are crowded at the apices of primary branches of Platygyrium repens.
Acrocarpous mosses producing both male and female sex organs on the same
plant but in distinct clusters (i.e. autoicous) produce the female sex organs at
the apex of stems, and rely on branches to host the perigonia (male inflorescences), or vice versa.
Branching patterns in mosses are diverse and complex (Meusel 1935, LaFargeEngland 1996). Branching results in branch systems that are reiterated as the
moss grows. In its simplest form, the branch system is composed of a primary
module that is repeated by sympodial branching; most primordia remain dormant. Complex vegetative bodies arise from the reiteration of a branch system
composed of multiple modules of distinct hierarchical rank. Variations in termination, origin, and orientation of modules, combined with differences in
modularity and reiteration, allow for virtually endless combinations of architectural patterns in mosses, and most notably among the pleurocarpous mosses
(Newton 2007). Assessing the phylogenetic significance of characters associated
with branching has been plagued by ambiguities regarding the homology of
modules within and between plant bodies, in part due to the functional plasticity of stems and branches in some species.
2.5
Sex organs: distribution, development and dehiscence
The sex of a plant is likely genetically determined. Heteromorphic
bivalents, reminiscent of the XY sex chromosomes, occur in various mosses
(Anderson 1980), and their distribution among plants seem to correlate with the
sex in at least some of them, although the mechanisms by which they function
is not understood (Newton 1984). However, not every plant produces gametangia, and sex expression may vary over short distances with patterns of expressions varying between the sexes (Stark et al. 2005). Sex organs are thus
genetically determined but their development is triggered by environmental
parameters (Bopp & Bhatla 1990).
As in all embryophytes, the sex organs are multicellular, offering some type
of protection to the developing gametes, the sperms and egg. Gametangia
are often accompanied by sterile unbranched filaments (i.e. paraphyses), and
are surrounded by specialized leaves to form the perichaetium and perigonium.
Sex organs are always developed superficially and at the apex of a module. In
2 Morphology and classification of Bryophyta
some cases the gametangium is the module. Female and male sex organs may be
borne on one bisexual individual (monoicy) or two unisexual plants (dioicy).
Plants capable of producing both sex organs may do so within a single cluster
with either antheridia surrounding (paroicy) or mixed with archegonia
(synoicy), or in distinct clusters on distinct modules (autoicy). Rarely is the
production of different sex organs spread in time, resulting in only one sex
present at any given time (pseudodioicy; Ramsay 1979). Sexual dimorphism in
dioicous species is rare in mosses (Vitt 1968), at least in terms of morphological
differentiation (Stark 2005). The most striking dimorphism between male and
female plants characterizes phyllodioicous or pseudoautoicous species,
wherein the male plants are reduced to a single bud emerging from the protonema growing epiphytically on the female plant (Ramsay 1979).
All mosses develop their archegonia at the apex of a module, and hence all
bryophytes are acrogynous (Goebel 1898a). Acrocarpy is defined by the terminal
cauline position of the perichaetium. Cladocarpy and pleurocarpy refer to the
apical location of the female sex organ on branches that are well developed and
bearing a heteroblastic series of leaves or that are highly reduced, respectively
(LaFarge-England 1996), although exceptions exist (Newton 2007). The distinction between these two modes of perichaetial position may be somewhat
ambiguous given the continuum in branch development, and this ambiguity
leads to conflicting interpretations of the phylogenetic significance of pleurocarpy (e.g., Buck & Vitt 1986, Hedenäs 1994, LaFarge-England 1996, Bell &
Newton 2007, O’Brian 2007).
Archegonia are rarely developed as single organs, such as in Takakia (Schuster
1997), some Sphagna (Crum 2001), or Splachnobryum obtusum (Arts 1996). The sole
or first archegonium is always derived from the apical cell. When multiple
archegonia occur in a perichaetium, the additional sex organs seem to originate
from the branch initial of segments below, suggesting that perichaetia are
condensed branching systems with highly reduced branches.
At maturity, the archegonium consists of three main parts: a solid, more or
less elongate stalk, a venter with a multistratose jacket and a single egg, and a
neck. The first division of the archegonial initial yields a lower and an upper cell.
The latter undergoes a couple of vertically oblique divisions that demarcate a
two-side apical cell, whose divisions may lead to a biseriate column that will
mostly compose the stalk of the archegonium. Unlike in liverworts and hornworts, the upper cell will then be reshaped into a tetrahedral apical cell with
three cutting faces. Among the Bryophyta, only Sphagnum lacks this newly
derived apical cell (Ruhland 1924). The derivatives of the new apical cell form
the venter. The apical cell then divides transversely to yield a cover cell and a
central cell, the latter undergoing a series of transverse divisions giving rise to
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the canal cells and the egg. Further longitudinal growth involves divisions of
existing cells and derivatives from the apical cell with now four cutting faces
(three obliquely lateral ones and one facing downward), although in some
species this cell ceases to divide soon after the development of the central
initials.
Six cells compose the circumference of the neck. The number of cells composing the vertical axis of the canal varies among, but seemingly not within
species. Fertilization is made possible following the disintegration of the neck
canal cells and opening of the distal end of the neck. According to Zielinski
(1909), the ‘‘dehiscence’’ of the archegonium is due to the swelling of the
mucilage in the apical cells and not in the canal. The mucilage accumulating
in the distal cells swells upon hydration, resulting in an increase of the internal
pressure. This pressure acts on the superficial cuticle, which breaks and rolls
back, taking with it the adhering cell walls.
Male gametangia are typically formed at the apex of a module and in that
sense all mosses are also acrandrous. The first and in some cases the sole
antheridium is always derived from the actual apical cell. Consequently, a
module developing antheridia will cease to grow. Additional antheridia are
formed from segments below. The next antheridium occupies the position of a
leaf (Ruhland 1924). Additional antheridia can be developed from either basal
cells of the primary antheridium, or epidermal cells of the segments; whether
this ambiguity has been resolved since Ruhland (1924) is not clear. In Polytrichum
piliferum, antheridia are developed from cells below the leaf initial (Frey 1970).
Similarly, in Sphagnum, antheridia occur singly below a leaf, and hence seem to
be derived from the branch-initial (Leitgeb 1882). Polytrichum modules retain
their vegetative apical cell, which enables them to resume growth following
sexual maturation. Here the antheridia occur in terminal splash-cups.
At maturity the antheridium is typically elongate-cylindrical, but rarely subspherical as in Sphagnum and Buxbaumia. Their development in bryophytes is
described and contrasted to that of other land plants by Renzaglia & Garbary
(2001). The antheridium consists of a stalked spermatogenous cylinder. Their
development involves at first a two-sided apical cell that forms a short biseriate
nascent antheridium. A set of two oblique divisions cuts each upper cell into
three derivatives, and each of the central cells undergoes one additional division. At this stage, the apex of the developing antheridium is composed of four
inner cells, and four outer cells. The former will compose the spermatogenous
tissue and the latter, the protective jacket. The inner cell of each segment
undergoes a series of divisions to yield a vast number of sperm mother cells.
With the final division a pair of spermatids are formed. A spectacular transformation (Renzaglia & Garbary 2001) results in two sperm cells each surrounded
2 Morphology and classification of Bryophyta
by a thick wall and bathed in a medium rich in lipid droplets. The lipid, which is
lacking in Sphagnum, may be essential to the dispersal of the sperm, favoring their
spreading on the surface of the water by lowering the surface tension (Muggoch &
Walton 1942). Sperm carry the bare necessities in terms of organelles (e.g., one
large mitochondrion and one plastid) and cytoplasm (Miller & Duckett 1985). At
syngamy only the nucleus is transferred to the egg, and organelles are only
maternally inherited by the zygote (Natcheva & Cronberg 2007).
The antheridial jacket remains unistratose, and grows primarily through cell
elongation. Bryophyte antheridia differ from those of liverworts and hornworts
in the mode of dehiscence that involves specialized opercular cells (Renzaglia &
Garbary 2001). At maturity the antheridium is more than half filled by a pressurized fluid, and hence the sperm mass only occupies a fraction of the inner volume
(Paolillo 1975, Hausmann & Paolillo 1977). At the tip thick-walled cells compose
an operculum (Goebel 1898b) which ruptures from the jacket below as the
internal pressure increases. According to Ruhland (1924), the cuticle covering
the antheridium prevents the tear from spreading, and thus insures that the
dehiscence is narrow. Sphagnum lacks differentiated opercular cells, and its
antheridia dehisce ‘‘by irregular valvelike tears rolling down from the apex’’
(Crum 2001).
Paraphyses are likely homologues of axillary hairs. They are typically uniseriate, chlorophyllose at first, typically becoming hyaline or brownish at maturity.
Paraphyses are lacking in all peatmosses, and in some species they are absent
from either the perichaetium or the perigonium. The role of the perigonial
paraphysis is not fully elucidated. Beside their potential role in protecting the
developing gametangia from dehydration either by their globose terminal cell
sheltering the antheridia, or through mucilage production (which seems to have
been shown only in Diphyscium), Goebel (1898b) suggested that paraphyses filled
with water may, when in dense formation in the perigonium, favor the expulsion
of the sperm mass by exerting pressure on the mature antheridium. Finally, these
filaments may be involved in attracting vectors recruited to disperse sperm
(Harvey-Gibson & Miller-Brown 1927), but such a hypothesis remains to be tested,
although it has recently been demonstrated that microarthropods can mediate
sperm dispersal (Cronberg et al. 2006). In the absence of a biotic vector, sperm of
most mosses are dispersed by water and in a most spectacular fashion in antheridia arranged in splash-cups (Andersson 2002).
2.6
Asexual reproduction
Sexual reproduction in mosses as in other bryophytes is strictly dependent on the availability of water, for the motile sperm to reach the apex of the
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archegonial neck and then move down the neck to fertilize the egg. Even
following syngamy, successful reproduction may be compromised by sporophyte abortion due to desiccation stress (Stark 2001). Given this constraint, it
is not surprising that mosses developed means of reproduction independent of
water availability. Reproduction without sex is known from most if not all
families of mosses (Correns 1899), and various mosses engage in both forms
of reproduction. Individual plant fragments offer a common means of reproduction, but leaf fragments alone rarely regenerate a plant (Correns 1899).
Despite their delicate nature, leafy shoots remain viable even after passing
through the digestive tracts of bats (Parson et al. 2007). With a few exceptions,
the specialized diaspores are formed exogenously, on stems, leaves, rhizoids
and protonemata (Imura & Iwatsuki 1990). They vary greatly in shape and size,
germination type and even mode of abscission, and two or three diaspore types
may be produced by a single species and even a single specimen, at least in
culture (Correns 1899, Duckett & Ligrone 1992). Newton & Mishler (1994)
recognized 15 groups of diaspores, from protonematal gemmae, modified
shoots and leaves, to cauline and foliar gemmae. Laaka-Lindberg et al. (2003)
followed a similar classification, but recognized only 13 classes. The main
inconsistency among classifications relates to the usage of the terms asexual
versus vegetative, and propagule versus gemmae. Newton & Mishler (1994)
reserved the term ‘‘asexual’’ in a strict sense to spores produced via selfing or
sex reproduction involving two clones or siblings. All other diaspores are
referred to as vegetative. They further follow Imura & Iwatsuki (1990) in defining propagules by the presence of an apical cell from which the new gametophore will arise, but restrict the term gemmae to small structures derived from
a secondary protonema. Laaka-Lindberg et al. (2003), however, considered only
those diaspores such as gemmae, whose germination will recapitulate the
ontogeny of the whole plant as truly asexual. Consequently, propagules,
which are defined by the presence of an apical cell, are treated as vegetative
diaspores. Leaves and rhizoids may occur on propagules but are lacking in
asexual diaspores. Whereas Imura & Iwatsuki (1990) emphasized that germination of gemmae always leads to a protonemal phase before a gametophore is
formed, Laaka-Lindberg et al. (2003) saw this more as a trend rather than as a
diagnostic feature. In fact, Duckett & Ligrone (1992) argued that the vast majority of diaspores produce filaments first. These strands emanate from specific
cells that can be recognized prior to germination (Correns 1899). The liberation
mechanisms for moss diaspores are similar to those described for other bryophytes or even sporic vascular plants, except in some taxa, where breakage
occurs through a differentiated abscission or tmema cell, unlike in any other
group of land plants (Duckett & Ligrone 1992, Ligrone et al. 1996).
2 Morphology and classification of Bryophyta
2.7
Components of the sporophyte
With more than one archegonium maturing within a single perichaetium,
multiple fertilization events are likely and may even be common, unless unfertilized eggs and their archegonium abort rapidly. Should syngamy have occurred in
two or more archegonia, typically only one embryo will pursue its development.
Polysety is indeed rare but has evolved independently in various lineages.
2.7.1
Early embryogenesis
Upon sexual reproduction a zygote, the first diploid cell, is formed,
marking the beginning of the sporophytic phase. The zygote always undergoes
a transverse division. The lower or hypobasal cell never develops into a conspicuous part of the mature sporophyte and carries no significance for the development of the mature sporophyte (Roth 1969). The epibasal cell divides
transversely again, forming a small uniseriate filament. Soon an apical cell
with two cutting faces is differentiated. The derivative cells form two lines,
and each cell will develop into a segment. About 20 segments are formed by
the time the apical region ceases to grow. Each segment undergoes further
divisions, in all three planes, and the embryo soon has a three-dimensional
architecture (Wenderoth 1931). The frequency of divisions in each segment
decreases gradually downward and rather abruptly upward. The transition
between the more or less median segments and the upper ones marks the
location of the new meristem. The segments above this region form the capsule.
Those below will develop into the seta and the foot. The seta meristem contributes cells only acropetally, and hence only to the seta. Apical growth thus
ceases early and when the embryo is less than a millimeter long the presumptive tissues yielding the capsule and the seta are in place. All subsequent growth
of the sporophyte is thus of an intercalary nature, by means of a seta meristem
(Roth 1969, French & Paolillo 1975a). The Sphagnopsida and the Andreaeopsida
lack a seta meristem and hence lack a seta altogether. Ligrone & Duckett (1998)
viewed the intercalary meristems as a residual primary meristem. The ontogenetic origin of the seta from an intercalary meristem rather than an apical cell
led Kato & Akiyama (2005) to question the homology of the seta and the
branched sporophytic axes of polysporangiophytes. They preferred to view the
moss sporophyte as a sporogonium, homologous to a vascular plant sporangium. Under this hypothesis the seta would be homologous to a sporangial stalk.
Polysporangiophytes would have acquired the ability to branch by delaying the
‘‘inception of the sporangial phase’’ through interpolation of a more complex
vegetative phase. As a consequence the intercalary meristem would likely be an
autapomorphy for the Bryophyta or a fraction thereof.
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2.7.2
The sporophytic placenta
The base of the sporophyte lacks an apical meristem, and hence the foot
is formed by segments derived from the intercalary meristem. The foot is
broadly defined as the portion of the sporophyte that is enveloped by the
gametophyte, and thus includes the portion of the seta sheathed by the vaginula
and the base of the sporophyte that is anchored in the actual cauline tissue (Roth
1969). The basalmost portion of the foot is typically elongate and tapered, except
in Sphagnum and Andreaea that have a bulbous or short conical foot, respectively.
In many lineages conspicuous cytological modifications insure the stability of
the gametophyte/sporophyte junction and favor transfer of nutrients and water
from the haploid to the diploid generation (Roth 1969, Ligrone et al. 1993).
Matrotrophy characterizes all embryophytes, and takes place at the junction
of the maternal tissues and the developing embryo (see also features of the
vaginula below). The placenta is composed of tissues of both generations.
Ultrastructural and cytological modifications on the gametophyte-side (see
above) are always matched by similar changes in adjacent sporophytic cells,
but in many cases the differentiation is unbalanced and conspicuous only on
the sporophytic side of the junction (Ligrone et al. 1993). Only in Sphagnum is
specialization absent on both sides of the junction. In Takakia, Andreaea,
Andreaeobryum, and all other mosses studied, transfer cells occur in the sporophyte. The morphology of the ingrowth varies among lineages (Ligrone et al.
1993). In Diphyscium and Bryum, cells of the sporophytes penetrate the gametophytic tissue in a manner that resembles a haustorium. Roth (1969) argued
against the ingrowth of the placental cells being essential to the transfer of
organic nutrients to the developing embryo since, in all cases, their development
continues at a time when the capsule begins enlarging, and when the sporophyte
builds its own assimilative capabilities. Although sugars are transferred from the
gametophyte to the sporophyte (Renault et al. 1992), sporophytes past a certain
age are able to complete their development autonomously (Haberlandt 1886,
Bopp 1954). Roth (1969) considered that the differentiation of the foot cells (and
those of the vaginula) fulfill primarily mechanical functions, strengthening the
connection between the sporophyte and gametophyte, even with regard to
environmental stresses such as periodic drought. Certainly in the case of
Diphyscium, with its massive sporophyte inserted by a short stalk on a short
female plant, such a function would seem essential.
2.7.3
Protection of the developing embryo
Following sexual reproduction the apex of the gametophyte undergoes
a series of transformations designed to nurture and protect the embryo. The urn
2 Morphology and classification of Bryophyta
enclosing the developing embryo develops from tissues of the archegonium, the
receptacle and even the perichaetial leaves, with contributions varying among
lineages (Roth 1969). The development of the epigonium (i.e., post-fertilization
archegonium) parallels that of the embryo, and in most mosses ruptures well
before sporogenesis into a calyptra (Fig. 2.1C, D) and a vaginula. The calyptra is
derived basipetally (i.e. with the youngest tissues at the base) nearly exclusively
from the archegonial stalk. The calyptra of Andreaea is composed of a membranous body topped by an archegonial neck. By contrast, in Andreaeobryum the
calyptra is multistratose and massive, and persistent to maturity (Murray 1988).
The multistratose epigonium of Sphagnum degenerates rapidly to a delicate
unistratose membrane.
The role of the calyptra continues to elude bryologists. Although widely
considered as essential for the normal development of the capsule, the mechanisms of control are ambiguous. Developmental phenotypes of the sporophyte
obtained after removing the calyptrae include: swelling of the seta (Bopp 1956);
erect and actinomorphic capsule, and stronger and faster negative geotropic
response in Funaria hygrometrica (Herzfelder 1923); decreased spore development
and viability based on isolated capsules of the same species (Bopp 1954); and
acceleration of capsule swelling in the Polytrichaceae (Bopp 1956). French &
Paolillo (1975b) showed that the effect of calyptra removal decreased with the
age of the sporophyte: the development was more dramatically altered when
the calyptra was removed from young vs. old sporophytes. Similar phenotypes
were described from mutants of Funaria hygrometrica and Physcomitrium pyriforme
(Oehlkers & Bopp 1957). Apogamous sporophytes (see below) grow without a
calyptra and always exhibit a deviant morphology, which may further indicate
the critical role of the calyptra in the development of the sporangium. Bopp
(1961) summarized the role of the calyptra as follows: the calyptra inhibits the
development of the capsule (i.e. its swelling) until the internal differentiation
within the sporophyte apex is complete. The premature loss of the calyptra
inevitably results in abnormal, incomplete and non-functional capsules. The
nature of the underlying mechanisms is still poorly if at all understood.
Calyptrae boiled in solvents and refitted onto the developing sporophytes retain
their ability to dictate capsule ontogeny, suggesting that the control is not
hormonal but rather mechanical in nature (Bopp 1961).
At maturity the calyptrae, and to a lesser extent vaginulae, display a broad
spectrum of morphologies (Janzen 1917). In some mosses, the calyptra clasps
around the mature sporangium and remains attached to the sporophyte (e.g.
Pyramidula), although even in this case tearing occurs to allow for spores to be
dispersed. Unless the calyptra covers only the operculum (e.g. Physcomitrella) it
must be shed along with or before sporangial dehiscence. Mosses lack active
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mechanisms to free themselves of calyptrae, and can only facilitate the removal
by wind by loosening the fit of the calyptra on the urn. Mitrate calyptrae sit like a
cap on the capsule. In Orthotrichum, the rostrum of the operculum elevates the
calyptra, which is then easily blown off. A cucullate calyptra is characterized by
a single long slit extending nearly to the apex. Its loss is facilitated either by the
asymmetric growth of the capsule (e.g. Funaria) or by an oblique rostrum (e.g.
Zygodon). The base of the calyptra is entire, broadly (e.g. Schlotheimia) or deeply
lobed (e.g. Macromitrium sp.), or fringed (e.g. Daltonia). The surface is commonly
smooth, but ridges or pleats (e.g. Orthotrichum), papillae (e.g. Leratia) or hairs (e.g.
Racopilum sp.) occur in various lineages.
The hairiness of the vaginula often matches that of the calyptra (e.g. Zygodon,
Malta 1926). In other aspects, the vaginula is morphologically fairly uniform,
except for its size, across mosses, although a systematic survey is lacking. The
inner layer of the vaginula may also exhibit wall ingrowths similar to those
seen in the placenta, except that they are developed even later with respect to
the ontogeny of the sporophyte (Roth 1969). The vaginula forms a tight but
still independent cylinder around the sporophyte (the upper portion of the
foot). Its function is likely structural, by solidifying the anchor of the
sporophyte.
2.7.4
Architecture of the mature sporophyte
The function of the sporophyte is to produce and disperse spores. The
sporangial tissue is enclosed in an urn that can be elevated onto a stalk, or seta
(Fig. 2.3). Although some species mature their sporangia among the perichaetial
leaves, favoring establishment of offspring in situ, most mosses raise the sporebearing capsules above the vegetative leaves. Like the vegetative axes, the seta is
composed of an epidermis, a cortex and a central strand of conducting cells,
except if the seta is highly reduced in size. The epidermal and sometimes the
cortical cells are pigmented and the color of the seta varies from yellow, bright
red, brown to rarely black. Stomata are always lacking in the seta. The surface is
rarely roughened by projecting cell ends (e.g. Brachythecium spp.), cilia (e.g.
Calyptrochaeta) or warts (e.g. Buxbaumiaceae). The seta is often strongly twisted
upward either clock- or counterclockwise (dextrorse or sinistrorse, respectively). In some species of Campylopus, the seta is cygneous or flexuose when
dry and unwinds upon moistening (Frahm & Frey 1987). In Rhachitheciopsis
tisserantii the seta is curved downward when moist, hiding the capsule among
the vegetative leaves and elevates the capsules when dry (Goffinet 1997a). Rapid
hygroscopic movements of the seta most likely promote the dispersal of spores.
They are accounted for in both cases by asymmetrically thickened cortical cells
of the seta.
2 Morphology and classification of Bryophyta
Fig. 2.3. Funaria hygrometrica. This typical acrocarpous moss is characterized by a ruderal
habitat, an annual life cycle, small gametophytes and an asymmetric capsule borne on a long
seta. Note the line on the capsule, marking the line of dehiscence. The sporogenous mass
occupies the upper half of the capsule.
An axial strand of hydroids is typically present in the seta of mosses,
including in species lacking such conducting cells in the gametophyte
(e.g. Orthotrichum spp.). The surface of the seta is covered in a waxy cuticle and
lacks appendages essential for external water conduction (Ligrone et al. 2000).
The anatomical complexity of the seta parallels that of the stem in the
Polytrichaceae, which exhibit the most highly developed strands of hydroids
surrounded by leptoids (Hébant 1977). In other mosses, organic compounds are
transferred between specialized parenchyma cells (Ligrone et al. 2000), even if
such cells are lacking in the gametophyte (e.g. Funaria; Hébant 1977). A hydroid
strand may be lacking in taxa with immersed capsules (e.g. Stoneobryum; Goffinet
1997b), in which capillary forces may suffice to supply the capsule with water.
When present, the hydrome rarely extends far into the central axis (i.e. the
columella) of the capsule (Hébant 1977).
Bryophytes are characterized by a single sporangium born at the apex of an
unbranched axis. Abnormal sporophytes bearing two sporangia have been
reported for various mosses (e.g., Győrffy 1929, 1934), including Sphagnum
(Győrffy 1931), and Leitgeb (1876) even considered such ‘‘doublefruits’’ not to
be that uncommon. In most cases the branching occurs distally so that the two
capsules are close to one another, even sheltered under a single calyptra. The
sister capsules differ in shape and size at maturity, but both produce viable
spores. Considering that the seta is developed by the intercalary meristem and
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that the tissues of the capsule are derived from the last set of divisions of the
apical cell, the ultimate development of two capsules must be initiated at the
earliest stages of embryogenesis (Leitgeb 1876). Alternatively, a dual fertilization, involving two eggs is also possible, although less likely considering that
the anatomy of the seta suggests that a single axis with one axial hydrome of
normal size is formed. Lal (1984) reported one or more capsules budding off
laterally from parthenogenic sporophytes (i.e., developed from unfertilized
eggs) in species of Physcomitrium. Similarly Tanahashi et al. (2005) observed
occasionally branched sporophytes in cultures of mutant Physcomitrella; whether
these are phenotypic expressions of the mutations or result from parthenogenesis is not clear, although the authors favored the latter explanation. If parthenogenesis is indeed demonstrated, and not merely hypothesized because
cultures were not flooded to allow for fertilization, it may be an explanation
for other occurrences of polysporangy in mosses. For example, in Sphagnum
karyogamy between egg and ventral canal cells may result in a diploid cell
that could develop into a sporophyte (Crum 2001). It is possible that in other
mosses, too, the ventral canal cell fails to disintegrate (Ruhland 1924) and is
involved in sporophyte formation.
Maturation of the sporophyte from fertilization to sporogenesis is likely a
continuous process even if it is slowed down by environmental factors such as
low temperatures (Greene 1960, Stark 2002). The phase of elongation of the
sporophyte (the spear stage) culminates in the swelling of the capsule, which
is composed of a sterile neck, the urn, and the operculum (see Fig. 2.3). The
basal sterile tissues may be well developed and result in a distinct region
below the urn tapered to the seta, or abruptly constricted to it (Győrffy
1917). In various Dicranales it forms a goiter-like protuberance, a struma.
Several entomophilous Splachnaceae develop an inflated and brightly colored
hypo- or apophysis designed to aid in attracting insects recruited for spore
dispersal.
The spectrum of variation in capsule shape is seemingly endless. Sphagnum,
Physcomitrella, and Pleurophascum, for example, have spherical capsules, whereas
most other mosses have rather elongate and sometimes cylindrical ones, as in
Encalypta. The capsule of Buxbaumia is conspicuously bilaterally symmetric, a
feature shared with various taxa of the Funariaceae and Dicranaceae with
curved capsules. Erect and radially symmetric capsules are common among
epiphytic or saxicolous mosses, but rare among terricolous mosses, and the
transformation between curved to erect capsules seems correlated with a shift
to epiphytism in various lineages of the Hypnales (Buck et al. 2000). In the
Mniaceae and many Bryaceae the radially symmetric capsule hangs from a
strongly curved seta.
2 Morphology and classification of Bryophyta
The capsule wall is the only tissue in mosses that may contain stomata,
typically less than fifteen, rarely more than 100 (Paton & Pearce 1957). Heavily
cuticularized guard cells typically occur in pairs (rarely four) but in the
Funariaceae the cytokinesis is incomplete and the new wall only partially
divides the two cells; the single guard cell is shaped like a tire inner tube with
a central stoma (Sack & Paolillo 1983). The shape of the stoma is either round or
elongate, with the former being more common. The shape may be correlated to
the thickness of guard cell wall (Paton & Pearce 1957). The phylogenetic significance of the characteristics of the stomata is ambiguous (Hedenäs 1989b).
The distribution of the stomata over the capsule surface is not random: often
restricted to the sterile base, they are formed only rarely in the distal portion of
the urn, and never in the operculum. The guard cells are generally exposed on
the surface of the capsule (phaneroporous stomata) but in various lineages the
guard cells are sunken below the surface and may even be overarched by
subsidiary cells, creating a suprastomatal chamber. Cryptoporous stomata are
homoplasious. Although these could likely reduce rates of transpiration,
immersed stomata are not restricted to or common among xerophytic mosses.
In Sphagnum the stoma-like structures are not involved in gas exchange, but
may be essential to the dehiscence of the capsule and dispersal of the spores (see
Section 2.9 on spore dispersal), and hence are referred to as pseudostomata
(Boudier 1988). Even in other mosses, the function of stomata is not clearly
understood (Paton & Pearce 1957) although they behave like those of vascular
plants, at least in young capsules (Garner & Paolillo 1973). In capsules nearing
maturity, the stomata tend to remain open, possibly to favor dehydration of the
tissues surrounding the spores, to prevent premature germination but also to
allow for hygroscopic movements of the capsule (e.g., shrinkage of the wall) to
favor spore dispersal. Although stomata and pseudostomata accomplish distinct
functions it is not clear whether the latter are derived or not from the former.
Given the absence of stomata in Takakia, Andreaea, and Andreaeobryum it is
possible that stomata are not a defining feature of the Bryophyta (Cox et al.
2004), and hence they may not be considered homologous to those of hornworts
and polysporangiophytes (as considered by Mishler & Churchill 1984).
A prerequisite to stomatal function is the presence of a cuticle and intercellular gas spaces (Raven 2002). The latter results in a dramatic increase in the
surface area through which gases can be exchanged by the photosynthetic
cells in multistratose tissues. A spongy tissue occurs in the capsule of all
mosses bearing stomata (Crosby 1980), except maybe Tetrodontium, and is
particularly conspicuous in Buxbaumia, where it lines much of the sporogenous
tissue below the capsule wall (Fig. 769 in Brotherus 1924). The assimilative
tissue either surrounds the sporogenous tissue in species lacking a distinct
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neck (e.g. Buxbaumia), extends into the sterile base (e.g. Funaria), or is restricted
to the apophysis (e.g. Splachnum). A lacunose tissue is lacking in all lineages
preceding Oedipodium, a pattern congruent with the view that air spaces are
essential for stomata, which are lacking in all early lineages of the Bryophyta.
Dimorphism among exothecial cells is not restricted to the guard cells. In
many species, the wall of the urn shrinks or contracts upon drying. As in all
other hygroscopic movements in mosses, changes in capsule shape with atmospheric moisture are determined by patterns of cell wall thickness. In the
Orthotrichaceae, the capsule is often ribbed when dry. The cells between the
ribs are thin-walled and collapse when losing turgor. Those marking the ridges
have thick walls and remain firm, even in the lack of cellular water. The
constriction may affect only the upper portion of the capsule, thereby narrowing the opening, potentially regulating spore dispersal. In entomophilous
Splachnaceae, the exothecial cells may have thinner longitudinal walls, and
hence shrink vertically when losing water. Here the effect may be to push the
spore mass closer to the capsule mouth to favor contact between insects and the
sticky spores.
The axis of the capsule of mosses, unlike that of liverworts, is occupied at
least partially by a columella; the only exception is Archidium (Snider 1975). In
Takakia, Sphagnum, Andreaea and Andreaeobryum, the columella is dome-shaped
and hence overarched by the sporogenous tissue. In all other mosses, the
columella extends beyond the spore sac, in some cases remaining attached to
the operculum upon dehiscence (systylious). The form of the columella varies
among taxa and may be of taxonomic value. In all Bryopsida, the columella is of
endothecial origin (Crum 2001). The spore sac is either of endothecial or
amphithecial (Sphagnopsida only) origin.
Dehiscence of the capsule (see below) involves in most species of the
Superclass V of the Bryophyta the loss of a lid or operculum at the apex of the
capsule. Only in Takakia, Andreaea, Acroschisma, and Andreaeobryum are the lines of
dehiscence vertical. In Takakia dehiscence begins in the center of the capsule and
extends towards the poles in a spiral line (Smith & Davison 1993). Andreaeobryum
and Andreaea (incl. Acroschisma) share valvate capsules, but in the former the
valves vary in number and are formed irregularly along lines of least resistance,
whereas in the latter the four valves are defined by distinct suture lines, composed of thin-walled cells, visible prior to the dehiscence (Murray 1988). The
valves of Andreaea typically extend for much of the length of the capsule and
remain connected at the apex. Only in Acroschisma wilsonii is the dehiscence
restricted to the apical region, forming 4–8 valves.
The line of dehiscence in operculate mosses is sometimes defined by the
presence of an annulus, a ring of cells at the capsule mouth composed of cells
2 Morphology and classification of Bryophyta
from the capsule wall or the underlying tissue. The annulus is often simple and
not well differentiated. By contrast, in the Rhachitheciaceae or Funariaceae, the
annulus is composed of 2–3 layers of cells and revoluble: it arches outward,
unzipping the lid from the urn. Such movement is again indicated by patterns in
cell-wall thickenings.
2.7.5
Sporogenesis and spores
Sporogenesis occurs relatively late in the development of the sporophyte, after seta elongation, which itself is often delayed by several months
following fertilization. Brown & Lemmon (1990) broke down sporogenesis
into five major stages: (1) differentiation of the spore mother cells (sporocytes), (2) nuclear divisions of meiosis, (3) cytoplasmic cleavage, (4) formation
of the spore wall, and (5) dehydration and accumulation of storage compounds. The development of the sporogenous tissue coincides with the
expansion of the capsule. Meiotic divisions within the sporangium are fairly
synchronized. Each sporocyte contains, unlike other cells of the sporophyte
or gametophyte, a single chloroplast that undergoes two consecutive divisions to yield four plastids equally distributed among the newly formed four
lobes of the cytoplasm with each destined to belong to one of the future
spores in the tetrad. The plastids are thus located at the poles of a tetrahedron, and are connected to one another by microtubules forming the
quadripolar microtubule system that will later form the spindles essential
to nuclear division.
The spores of extant bryophytes are always produced in tetrads, whereby
every spore is in contact with the other three products of meiosis. However, a
distinct trilete mark on the proximal pole is typically lacking. Patterns in spore
wall development fall within three broad categories, according to the architecture of the wall: penta lamellate in Sphagnum, spongy exine and no tripartite
lamellae in Andreaea and Andreaeobryum, and tripartite lamellate in the remainder of mosses, with a perine, a median exine, and an inner intine (Brown &
Lemmon 1990). The exine is composed of sporopollenin or a sporopollenin-like
compound that confers to it its highly mechanical and likely also physiological
resistance to degradation and desiccation, as in other land plants. By contrast,
polysaccharides compose the intine, which is laid down last by the spore. The
intine of most mosses is thickened in one particular area where it faces a thinner
exine. This area, called the aperture or leptoma, likely offers less resistance for
the germ tube to emerge. The outermost layer, or perine, is contributed by the
sporophytic tissues or their breakdown, rather than by the spores themselves.
This layer, composed of pectin and callose-like compounds like the intine,
contributes also to the resistance of the spore.
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Since bryophytes are characterized by a single terminal sporangium, all
spores are thus produced by the same sporogenous tissue, and hence cases of
heterospory are by definition impossible. The sporangium yields a mass of
spores whose size varies around single mean in most species (isospory). In
some cases, a bimodal distribution of spore size reveals the presence of aborted
spores (Mogensen 1978, 1983). Sexual dimorphism is rarely apparent at the
spore stage. In many phyllodioicous species, each tetrad holds two large and
two small spores. Upon germination the small spores yield small male gametophytes. The larger spores are assumed to develop into female gametophytes,
although empirical observations are still lacking. Such production of two size
classes of spores within a single sporangium is termed anisospory (Vitt 1968).
Anisospory always leads to profound sexual dimorphism with males being
dwarf; however, the reverse is not true. Hence many more mosses exhibit
dwarf males than anisospory. Furthermore, not all mosses that develop dwarf
males lack the ability to form regular-sized male plants. Une (1985) thus distinguished physiologically from genetically determined male dwarfism.
The number of sporocytes and hence ultimately the number of spores varies
among species. Some species of Archidium may produce only four spores per
indehiscent sporangium, several million spores are formed in each capsule of
Dawsonia lativaginata (Crum 2001).
2.8
Fundamental peristome types
Early in their evolutionary history, mosses acquired a peristome, a set of
teeth forming one or two rings lining the mouth of the sporangium. The peristome
arises in virtually all cases from cells of the amphithecium. The peristome of the
Polytrichopsida and the Tetraphidopsida is composed of teeth that are bundles of
whole, thick-walled cells, hence the name nematodontous for the thread-like
appearance of the teeth. As is revealed by its name, the urn of Tetraphis bears
four teeth, which are massive and erect (Shaw & Anderson 1988). Most
Polytrichaceae have 32 or 64 short teeth, protruding only slightly above the rim
of the capsule. All other peristomate mosses (i.e. Bryopsida) have teeth composed
solely of cell plates or cell wall remnants. Because the vertical plates within a
column are jointed, permitting the tooth to bend in or outward, the peristome is
called arthrodontous. Several architectural types of arthrodontous peristome can
be recognized based on ontogenetic and morphological features: the Timmia-, the
Funaria-, the Dicranum- and the Bryum-type peristome (Budke et al. 2007).
Three layers of the amphithecium contribute cells to the peristome: the
inner, primary and outer peristomial layers, respectively referred to as the IPL,
PPL and OPL (Fig. 2.4B). All peristomes share a developmental sequence that
2 Morphology and classification of Bryophyta
A
C
E
1/8th
B
4 : 2 : 8
4 : 2 : 3
Timmia
Dicranum
D
F
e
OPL :
PL :
IPL
4 : 2 : 4
Funaria
4 : 2 : 4–12
Bryum
H
G
I
J
K
Fig. 2.4. Peristome architecture in mosses. (A) Diagram of a transverse section through
the putative peristome forming region at the apex of an immature moss sporophyte.
(B) Detail of 18 of the section in (A), showing the endothecium (e) and the three innermost
amphithecial layers that contribute to peristome formation: outer (OPL), primary (PPL)
and inner (IPL) peristomial layer. (C–F) Diagram of 18 of a Timmia-, Funaria-, Dicranum- and
Bryum-type peristome. Black areas identify thickened cell walls composing the peristomes;
dotted lines mark the walls of the IPL, PPL, and OPL cells that are resorbed and hence that
are not contributing to the peristome. (A–F) Redrawn from Budke et al. (2007). (G)
Diplolepideous peristome of Timmia megapolitana, showing the 64 filamentous appendages of
the endostome. (H) Inner view of the peristome of Funaria hygrometrica, showing the four IPL
cells composing the two segments, which lie opposite the two exostome teeth. (I) Outer view
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leads to an IPL of eight cells surrounded by a PPL of 16 cells and an OPL of 32 cells
(Goffinet et al. 1999). Subsequent stages differ among the major peristome types.
The Timmia-, Funaria- and Bryum-type peristomes are double, comprising an
outer exostome composed of teeth and an endostome composed of segments
and cilia. The exostome is always built from the inner periclinal walls of the OPL
and the outer periclinal walls of the PPL (heavy lines in Fig. 2.4C, D, F). The three
other vertical walls of each OPL cell are degraded (dotted lines in Fig. 2.4C–F).
The inner periclinal wall of the PPL contributes, with the outer periclinal wall of
the IPL, to the endostome. Thus, the endostome and the exostome share one cell
layer, namely the PPL, in their architecture. Typically, the exostome comprises
16 teeth. In some cases, these are split into 32 or fused into eight teeth. The OPL
is always composed of 32 cells, and hence, two columns of cells contribute to
the outer surface of each of the 16 exostome teeth. The inner surface of the tooth
is built from one of the 16 columns of cells composing the PPL. The PPL also
contributes to the endostome. In the Funaria- and Dicranum-type peristome, each
endostome tooth is composed of one column of PPL cells (Fig. 2.4D, E). In the
Bryum-type, each endostome segment shows a median vertical wall, revealing
that each segment is composed of one half from two PPL cells (Fig. 2.4F, J).
Because two columns of cells compose the outer surface each exostome
tooth, Philibert (1884) introduced the term diplolepideous for this architecture.
A diplolepideous peristome thus typically comprises an exostome. In the
Dicranidae the peristome is reduced to an endostome whose teeth bear only
one column of cells on their outer surface: the peristome is said to be haplolepideous. By coincidence, the haplolepideous peristome is single and the diplolepideous one is double. Both peristome architectures can be further reduced
and one or both rings of teeth lost completely (Vitt 1981).
The Timmia-, Funaria- and Bryum-types represent three diplolepidous peristomes that differ in the architecture of the endostome. The Dicranum-type is
the sole model of a haplolepideous peristome. In the Funaria-type the endostome is composed of 16 segments that each lay opposite an exostome tooth
(Fig. 2.4H). The Bryum-endostome is characterized by a basal membrane
mounted with 16 segments alternate to exostome teeth and separated by
Caption for Fig. 2.4. (cont.)
of the peristome of Tortula plinthobia, each tooth is fenestrate along the vertical walls of the IPL,
and hence one and half cells of the IPL face each PPL cell (outer cells in view here). (J)
Diplolepideous peristome of Pseudoscleropodium purum, showing the keeled endostome
segments alternating with the exostome teeth, and the cilia between two consecutive
segments. (K) Inner view of the diplolepideous peristome of Mnium thomsonii, showing the
numerous cells composing the IPL.
2 Morphology and classification of Bryophyta
small, slender appendages called cilia (Fig. 2.4J). The cilia are thus opposite the
teeth. This peristome is also referred to as diplolepideous alternate, in contrast
to the diplolepideous opposite of Funaria. In Timmia the membrane bears only 64
filiform appendages similar to cilia (Fig. 2.4C, G). Their homology to the endostome segments of other diplolepideous mosses is ambiguous (Cox et al. 2004).
The conspicuous morphological differences between the main peristome types
are paralleled by developmental divergences. In Funaria each of the eight IPL cells
undergoes a set of three symmetric divisions that yield four identical cells for
every two PPL cells (Fig. 2.4H; Schwartz 1994). In Timmia, the IPL cells undergo
one additional round of symmetric divisions, leading to eight cells per eighth of
the peristome (Budke et al. 2007). The first division in each of the eight IPL cells
of the remaining diplolepideous mosses is strongly asymmetric (Shaw et al. 1989a).
The number of subsequent divisions varies and yields between four and 12 cells
per pair of PPL cells (Fig. 2.4K). Haplolepideous mosses, too, are characterized by
an asymmetric division. Here it is followed by a single division, hence only three
cells compose the IPL adjacent to two PPL cells (Shaw et al. 1989a,b). Thus, each
segment of Dicranum bears one column of cells on the outer surface and one and
one half columns on the inner surface (Fig. 2.4I). Patterns in cell division may be
inferred from the arrangement of anticlinal walls in mature peristome. However,
lateral displacements of IPL walls during the development may mislead assessments of symmetry of the division at maturity. Similarly, amphithecial cells
immediately below the narrow presumptive peristome-forming zone lack the
constraints that dictate the patterns of cell division in the IPL, and great care must
be taken in ontogenetic studies to identify homologous layers (Budke et al. 2007).
These architectures and ontogenies characterize typical peristomes in the
Timmiidae, Funariidae, Dicranidae, and Bryidae, but are by no means shared
by all their species. For example, the peristome of the Orthotrichaceae is diplolepideous, with alternate segments but lacking cilia (Goffinet et al. 1999). The
Encalyptaceae share with the Funariaceae a symmetric division, but at maturity
their highly divided peristome is morphologically unique (Horton 1982, Vitt 1984).
In the Rhachitheciaceae (Dicranidae), the endostome is composed of eight segments each built from a single column of PPL cells (Goffinet 1997a). In Mittenia,
another haplolepideous moss, the peristome is derived from one endostomial layer
(Shaw 1985). Bruchia flexuosa belongs to the Dicranales but its development prematurely stops, and the last divisions expected in the IPL are lacking (Shaw et al. 2000).
2.9
Spore dispersal
The dehiscence of the sporangium (stegocarpy) exposes the spore mass
and allows for the dispersal of the spores. In the Sphagnopsida the line of
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dehiscence is horizontal, and the release of spores is explosive. The mechanism
relies on the presence of pseudostomata along the equatorial line. Pseudostomata
are essentially cavities resulting from the collapse of the outer periclinal wall
(Boudier 1988). The base of the depression is formed by thick cell walls. Upon
dehydration the neighboring exothecial walls collapse toward the floor of the
cavity pushing it inward. As the mature capsule emerges from the calyptra and is
exposed to drying winds, the cells lose water; the capsule constricts along the
equator. At the same time the columella degenerates and is replaced by gases,
which are compressed by the shrinking capsule. The internal pressure and thus the
tension on the exothecial cell walls increases. The thin walls of the subapical cells
tear and the operculum is projected at once, and a cloud of spores is released
(Ingold 1965). In Andreaea, the capsule dehisces along vertical lines but the valves
remain connected at their apex. As the atmospheric moisture decreases, the
exothecial cells lose their water content and the valves arch outward, thereby
exposing the spores. As the humidity increases, the cells swell and a reverse movement occurs. This closes the sporangium and protects the spore mass from water,
which would trigger the premature germination of spores, but also agglutinate the
spores and inhibit their effective dispersal by wind. In Takakia, a similar movement
of the capsule wall is likely to control the release of spores. In all other mosses,
except of course for the indehiscent or cleistocarpous ones, the line of dehiscence is
equatorial or (typically) subapical, and the mouth of the capsule is typically lined
with peristome teeth.
In nematodontous and arthrodontous mosses, the peristome may control the
release of spores (Ingold 1959). In the Polytrichopsida, the peristome teeth are
short. The mouth of the capsule is closed by a thin membrane, the epiphragm,
that expands from the apex of the columella to the inner surface of the teeth.
Between the teeth, the epiphragm is free and hence small holes persist. The
capsule resembles a salt-shaker, as the small spores are released through the
marginal pores between the teeth. Dawsonia lacks an epiphragm, but the teeth
are long and twisted, forming a mesh-like tissue over the capsule mouth. The
massive teeth of Tetraphis move only slightly as the ambient humidity changes,
but sufficiently so to open tiny gaps between them for the spores to escape when
the air dries out.
The movement of teeth is most spectacular in arthrodontous mosses. Here
the teeth may bend from an overarching position all the way back whereby the
teeth are recurved over the capsule wall. Such dramatic movements are made
possible by (a) the fundamental architecture of the teeth and (b) much thicker
outer versus inner surfaces of the teeth. Species contrasting in their habitat
preferences may favor spore release under different conditions. Many terricolous species have peristomes that close the capsule mouth under moist
2 Morphology and classification of Bryophyta
conditions and expose the spore mass when the air is dry (xerocastique peristome). Other mosses, especially epiphytes, favor dispersal under moist conditions (hygrocastique peristome). In some aquatic mosses, such as Cinclidotus and
Fontinalis, the inner peristome forms a trellis or a solid dome that prevents water
from entering the capsule and all spores from leaving the urn at once.
Wind is the primary and in the vast majority of mosses the sole dispersal
vector. Insects are only recruited as dispersal agents by the Splachnaceae, and
only those that grow on substrates of animal origin. Olfactory and visual cues
attract flies foraging or looking for these substrates to lay their eggs (Koponen
1990). The chemical adaptation is complemented by morphological innovations
such as sticky spores, a pseudocolumella which acts as a piston to elevate the
spore mass to the mouth of the capsule or, more strikingly, the expansion of the
sterile base of the urn either to amplify the visual cue or to provide a suitable
landing platform for insects (Koponen 1990). Recent phylogenetic investigation
suggests that entomophily, insect-mediated spore dispersal, arose early in the
evolutionary history of the Splachnaceae, and was subsequently lost, maybe due
to the severe biotic constraints shaping this system (Goffinet & Buck 2004).
A few mosses lack specific dehiscence mechanisms, and the sporangium
remains closed. Such cleistocarpy characterizes various taxa such as Kleioweisiopsis
and other Ditrichaceae, Pleurophascum, Gigaspermum, and Bryobartramia, among
others, but is not known among the Hypnanae (Shaw et al. 2000). Spores are
dispersed following the disintegration of the capsule wall, either in situ if the
plant is an annual, or away from the maternal plant if the whole capsule is
dispersed. Only for Voitia have birds been invoked as a dispersal agent, after
ingesting the capsule. Dispersal following trampling of the colonies by herds of
caribou is also a possibility. In all cases, cleistocarpy seems to be a result of
reduction from peristomate ancestors and in a few cases peristomial fragments
remain inside the indehiscent capsule (e.g. Tetraplodon paradoxus).
2.10
Early gametophyte development
The vegetative phase of the life cycle begins with the germination of the
spore, typically a single cell protected by a wall with a complex ultrastructure
and impregnated with sporopollenin, conferring physical and physiological
protection as well as resistance against decay on the meiotic product. The
aperture is a specialized area in the spore wall through which a germ tube
typically emerges (Brown & Lemmon 1981). It is not prominent because it is
beneath the exine ornamentation. Germination is fuelled by the combustion of
protein, lipid, and starch reserves accumulated in the spore during its maturation in the capsule (Stetler & DeMaggio 1976).
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Upon germination, a sporeling is formed. Based on the timing of the first
divisions, and the architecture of the sporeling, Nehira (1983) distinguished 14
sporeling types in mosses. The series of studies focusing on protonematal
morphogenesis in mosses by Duckett and his coworkers (see references in
Duckett et al. 2004) sheds further light on the diversity of structures and patterns
involved in the earliest stages of vegetative growth. Cell divisions may precede
actual germination of the spore. Such endosporic development occurs in several
unrelated mosses. A more extreme head-start is provided to the sporeling of
Brachymenium leptophyllum wherein spores often germinate within the protective
confines of the capsule and with protonemata emerging from capsules bent
down to the ground (Kürschner 2004). In this case, like in the majority of
mosses, the development of the spore is exosporic: the spore germinates and
all divisions add cells to the emerging germ tube.
The architecture of the protonema (i.e. the first multicellular stage in the life
cycle of most mosses) in exosporic mosses is typically filamentous, with three
components (chloronema, caulonema, and rhizoids) that are rather distinct but
morphogenetically connected, in the sense that transformations between any
two of them are not unidirectional or irreversible (Duckett et al. 1998). In
exemplars of most major lineages preceding the Bryopsida, a thalloid protonema emerges from the filaments. In Sphagnum the rosette-shaped thallus
dominates the protonematal stage. Similarly in Tetraphis and Oedipodium, leaflike assimilative appendages are developed from the green filaments. At the
base of each such thalloid structure in Tetraphis, a leafy gametophore arises. In
Andreaea small appendages unlike any other protonemata (Duckett et al. 2004)
may form, but are not essential to the development of gametophores (Murray
1988). In Diphyscium the protonema comprises filaments, but clavate branches
and funnel-shaped structures are also formed, which Duckett (1994b) regarded
as caulonematal derivatives. Germination of spores of Takakia has not yet succeeded, but vegetative regeneration lacks a filamentous stage, suggesting that
spores also do not form a uniseriate protonema. Among the Bryopsida, and also
Buxbaumia, thalloid appendages are lacking, and the protonemata are typically
entirely filamentous in nature. Buxbaumia develops a highly reduced protonema
composed of rather short rhizoids and an erect chloronema.
The chloronema is always filamentous, composed of green cells, and characterized by intercalary growth. It lacks buds and its function is essentially
assimilative in nature. The caulonema, dark-pigmented filaments of cells separated by oblique crosswalls with numerous plasmadesmata, emanates from the
chloronema and in most bryopsid mosses develops the actual buds from which
shoots will arise. Like rhizoids, caulonematal cells exhibit a cytoplasmic organization reminiscent of leptoids, suggesting that they are the site of cytoplasmic
2 Morphology and classification of Bryophyta
transport, essential to the growing gametophores. The caulonematal stage is
lacking in some lineages (e.g. Orthotrichales) where buds are thus formed by the
chloronema (Duckett et al. 1998). Protonematal cells are generally elongate,
rarely short-cylindrical. In Encalypta, Ptychomitrium, and Hedwigia the primary
protonemata are composed of globose cells.
The protonema of most mosses is ephemeral, but in Pogonatum pensylvanicum
and some species (e.g. Ephemeraceae) it is perennial, producing short female
shoots every year. In other mosses, the protonema contributes to the longevity
of the population by producing asexual propagules. Indeed, much like rhizoids,
protonematal filaments can bear gemmae that are filamentous (Duckett &
Ligrone 1994), or spherical (Arts 1994), and in some cases even bulbils (i.e. highly
undifferentiated shoot with a leaf primordium) may be formed (Mallón et al.
2006). Protonematal gemmae occur in an estimated 25% of all mosses (Duckett
et al. 1998). Regardless of the germination or sporeling type, or the presence of
differentiated asexual propagules, protonemata account for significant clonal
reproduction since virtually all mosses, including Sphagnum, share the ability to
form multiple gametophores from a single spore (Crum 2001). Indeed, monogametophytic protonemata characterize only a few species (Duckett et al. 1998).
2.11
Apogamy and apospory: a life cycle without sex and meiosis
The gametophyte is by definition the plant that bears the sex organs
needed to develop sperms and eggs essential to sexual reproduction and thus
sporophyte formation. The function of the sporophyte is to yield spores from
which gametophytes can be regenerated. The apparent robust fundamental
functional differentiation between the two alternating phases of the life cycle
of sexually reproducing bryophytes is compromised by the observations of
sporophytes emerging from gametophytic tissues and that of sporophytes ‘‘germinating’’, and protonemata developing leafy stems! Pringsheim (1876) and
Stahl (1876) were the first to report cases of apospory or of ‘‘regeneration’’,
that is the formation of protonemata from young sporophytic tissue and in
particular the seta (Bryan 2001). Such observations have been extended to
other taxa (e.g. Wettstein 1925), across much of the phylogenetic spectrum of
mosses (from Tetraphis to Hypnum), but these refer exclusively to experimentally
induced diploid gametophytes; in vivo observations seem to be lacking.
Aposporous gametophytes differ from their haploid progenitors in the larger
cells (Moutschen 1951), and larger gametangia but not in larger vegetative
organs (Marchal & Marchal 1911). Furthermore, given their diploid nature,
regenerants of dioicous species carry, as does the sporophyte, the loci defining
both sexes. Aposporous leafy stems of the dioicous Bryum caespiticium produce
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primarily male inflorescences, which over time tend to acquire a single archegonium (rarely more), and hence become synoicous; few purely perichaetial
plants are developed (Marchal & Marchal 1907). Great variation in the sex ratio
among clonal bisexual plants suggests that sex expression is determined by
external factors. Furthermore, sexual reproduction leading to a tetraploid sporophyte and the induction of a tetraploid aposporic gametophyte has been
achieved primarily if not only with monoicous taxa (Marchal & Marchal 1911).
Apogamy, that is the formation of a sporophyte directly from gametophytic
tissues rather than following sexual reproduction, was first described by
Springer (1935) on aposporic gametophytes of Phascum cuspidatum. Marchal &
Marchal (1911) observed club-shaped outgrowths on leaves and stems of diploid
plants but interpreted these as asexual reproductive structures. Springer
revealed that these so-called broodbodies actually contain spores. Although
the sporophytes typically deviate in their morphology from normal sporophytes, in terms of shape and lack of stomata, they do produce viable spores
that germinate into a protonema that in turn forms leafy stems, bearing gametangia and capable of sexual reproduction. The gametophytes derived from
these spores exhibit much morphological variation, which Springer attributed
to mutations due to faulty chromosomal reduction during sporogenesis, even
though she was unable to demonstrate that meiosis actually occurred in the
apogamous sporangium. Apogamy has been triggered in several species by
Lazarenko (Crum 2001).
Only mosses whose genome is truly monoploid seem to lack the ability to
develop apogamous sporogonia on vegetative plants (Chopra 1988). Bauer (1959)
described apogamic behavior in wild diploid races of Funaria hygrometrica, a
species that occurs in the wild with distinct ploidy levels (Fritsch 1991). In vitro,
apogamous development of sporophytes is induced by various factors, such as
low light intensity, increased sugar concentration in the medium, or growth
hormones such as indol acetic acid (Chopra 1988), which are not exclusively
artificial. It should be noted that apogamous sporophytes develop unprotected
by a calyptra, which may explain their abnormal morphologies (see Springer
1935), and perhaps their incomplete ontogenies accounting for the generalized
observation of ‘‘sterile sporophytes’’ (Chopra 1988). The significance of apospory
as a mechanism of speciation and for the occurrence of ploidy races within some
species (Fritsch 1991), remains unexplored (see Shaw, Chapter 11).
2.12
Origin and evolution of the Bryophyta
The fossil record of mosses is a poor indicator of absolute age of the
phylum and its main lineages. Unequivocal records date from the Carboniferous
2 Morphology and classification of Bryophyta
(Kenrick & Crane 1997) and Sporogonites, from the Lower Devonian, exhibits
sporophytic characters reminiscent of mosses, but in the absence of a gametophyte its affinities remain ambiguous. Inferences from variation in chloroplast
sequence data suggest that the transition to land occurred 425–490 mya,
roughly during the Silurian or Ordovician period (Sanderson 2003), an estimate
congruent with microfossil evidence (Edwards 2000, Wellman & Gray 2000,
Wellman et al. 2003). Another estimate based on sequence data suggests, by
contrast, an origin of the terrestrial flora at about 1000 mya, with a divergence
between the mosses and polysporangiophytes as early as 700 mya (Heckman
et al. 2001). This hypothesis is congruent with the report of a single bryophytelike fossil from the Middle Cambrian (Yang et al. 2004). Recent reports of cryptospores from the Cambrian further point to an earlier origin of a land plant
flora (Strother et al. 2004). Thus, although the relative relationships among land
plants (Kenrick & Crane 1997) and particularly extant land plants (Qiu et al. 2006)
are becoming increasingly resolved, the origin of the land plant flora as well as
the timing of the major early radiation continue to elude plant biologists. It is,
however, clear that bryophytes arose and diversified early with most orders and
even various families established by the Cretaceous, as inferred from a twoplastid gene phylogeny (Newton et al. 2007) as well as actual fossil evidence (e.g.
Konopka et al. 1997, 1998, Bell & York 2007).
In the early 1980s Crosby (1980) and Vitt (1984) proposed two distinct views of
bryophyte phylogeny, and in particular the relationships among the Bryopsida
sensu Vitt. Mishler and Churchill (1985) provided the first formal cladistic analysis of the mosses. Only over a decade later have these hypotheses been critically tested further, based on inferences from either DNA sequence data alone
(e.g. Goffinet et al. 2001, Cox et al. 2004, Tsubota et al. 2004) or in combination
with morphological characters (Newton et al. 2000; see Goffinet & Buck 2004 for
review). Emerging from these analyses are the following hypotheses (Renzaglia
et al. 2007): Takakia and Sphagnum compose the earliest divergence, but their
relative branching order remains ambiguous. Similarly, the Andreaeopsida
and Andreaeobryopsida may compose a grade or a clade. One major contribution of these recent studies is the resolution of Oedipodium as a sister-taxon to all
peristomate mosses (Newton et al. 2000). Nematodontous mosses (Polytrichales
and Tetraphidales) form a sister-group or more likely a basal grade to the true
mosses, the Bryopsida. The Buxbaumiales and Diphysciales represent early
evolutionary lines within the Bryopsida, with the latter sister to all true arthrodontous mosses. Within the Bryopsida the main relationships are: Timmia likely
composes the earliest divergence within the Bryopsida; the Encalyptales share a
common ancestor with the Funariales and Gigaspermales; the Dicranidae may
compose a monophyletic lineage with either the Funariidae or Bryidae; the
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latter composes a grade leading to the pleurocarpous mosses or Hypnanae, with
the Ptychomniales and Hookeriales composing a grade to the largest and ultimate clade of mosses, the Hypnales.
The ambiguity of the branching order in critical areas of the tree, whether
near the root of all mosses or that of the pleurocarps, may indicate a rapid
diversification, that is divergences over periods of time too short to allow for
much fixation of characters in the ancestor of successive radiations. One such
rapid and putative adaptive radiation may characterize the Hypnales (Shaw et al.
2003). If increase in lineages of the Hypnales over time was gradual, as suggested
by inferences by Newton et al. (2007), the lack of resolution, and thus the lack of
shared substitutions at critical nodes, may be explained by a dramatic reduction
in the rate of molecular evolution.
Phylogenetic hypotheses provide the evolutionary history upon which character transformations can be reconstructed. Although much emphasis has been
placed on reconstructing the relationships among lineages of mosses (e.g. Cox
et al. 2004), including use of morphological characters (Newton et al. 2000),
no critical or explicit attempt has been made to establish a phylogenetic pattern
in character transformations. This shortcoming is explained by (a) the relative
lack of robustness of critical nodes (see above), (b) difficulties in assessing
homology (e.g. for early divisions in inner peristome formed by the amphithecial layer), (c) lack of pertinent studies elucidating the character-state for certain
lineages (e.g. amphithecial development in basal lineages) and (d) the diversity
of character-states encountered near a particular node (e.g. mode of dehiscence
near root of the tree).
The morphological evolution of the Bryophyta is not a unidirectional trend,
and hence the polarities in early character transformations are reversible: an
acquired state can be lost, resulting in a putative plesiomorphy in an otherwise
highly derived taxon. Reverse evolution (e.g. the loss of a costa, papillae, hydroids, stomata, peristome, or operculum, among others) is widespread in mosses,
and may be associated with a shift in habitat (e.g. in epiphytic Hypnales;
Huttunen et al. 2004) or in other life history traits (e.g. anemophilous
Splachnaceae; Goffinet & Buck 2004). Such reduction significantly hampers
testing phylogenetic affinities based on morphology. The problem is compounded by the possibility that even complex characters, such as peristomes,
may be regained (Zander 2006).
2.13
Classification of the Bryophyta
Mosses offer a large array of structural diversity from which relationships can be inferred and hence lineages defined. Throughout the 200 year
2 Morphology and classification of Bryophyta
history of bryophyte systematics, which is well summarized by Vitt (1984) and
Buck (2007), much weight has been placed on the complexity of the peristome
and the distribution of sex organs for defining taxonomic units above the
species rank. Modern classifications (e.g. Crosby 1980, Walther 1983, Vitt
1984) reflect major systematic concepts proposed by Fleischer (1920) and
Brotherus (1924, 1925), wherein the peristomate mosses are divided into nematodontous and arthrodontous mosses (following Mitten 1859), with the latter
subdivided into acrocarpous and pleurocarpous mosses based on the position of
the perichaetia (following Bridel 1826–1827), and into haplolepideous and
diplolepideous mosses based on the architecture of the outer ring of peristome
teeth. Sphagnum, Andreaea, Andreaeobryum, and Takakia represent additional
groupings distinguished by the presence of a pseudopodium and the mode of
sporangial dehiscence.
The classification of the Bryophyta is undergoing constant revisions, particularly
in the light of phylogenetic inferences. Most recent revisions (Buck & Goffinet 2000,
Goffinet & Buck 2004) rest on results from phylogenetic reconstructions. Although
some transfers have subsequently been reversed, and correctly so, as the original
data were incomplete (e.g. Pleurophascum in Goffinet et al. 1999), based on misidentified vouchers (e.g. Goniomitrium; Goffinet & Cox 2000) or based on contaminant
DNA, others have withstood critical testing (e.g. Ephemerum; Goffinet & Cox 2000).
Other changes may be challenged for subjective reasons. Zander (2008) for example
retains members of the Rhabdoweisiaceae in the Dicranaceae, on the grounds that
the monophyly of the former family is not well supported, and that the Dicranaceae
are not resolved as polyphyletic. However, nothing prevents two sister taxa from
being treated as distinct taxa of the same rank. The lack of support for the recognition of a distinct Rhabdoweisiaceae cannot be translated as support for a broadly
defined Dicranaceae. Nodal support is preferable but not necessary. For example,
the sister-group relationship of the Gigaspermaceae to the remainder of the
Funariales and the Encalyptales combined is weakly supported by nucleotide substitutions but consistent with the architecture of the chloroplast genome, which led
Goffinet et al. (2007) to accommodate the Gigaspermaceae in their own order.
The classification proposed here builds on those presented by Buck & Goffinet
(2000) and Goffinet & Buck (2004). The rank of superclass is adopted to unite all
arthrodontous mosses in one taxon (i.e. Superclass V). Although we aim at accepting
only monophyletic taxa, given the limited number of ranks available, paraphyletic
taxa are inevitable (e.g. Bryanae). Much effort is currently dedicated to resolving the
relationships among genera of the Hypnanae (Newton & Tangney 2007). Although
current results reveal that many familial delimitations fail to reflect shared ancestry, it is premature to propose significant changes within the pleurocarpous mosses
because of a lack of resolution between the major clades, and the lack of sequence
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data for many of the genera. Also, some new classifications are based solely on
regional taxa (e.g. Ignatov & Ignatova 2004) and we have been unable to expand
them to a global scale. Therefore, until such time as we can understand generic
inclusions on a world basis, we are not following such examples.
Classification of mosses
BRYOPHYTA Schimp.
SUPERCLASS I
C L A S S T A K A K I O P S I D A Stech & W. Frey: Leaves divided into terete
filaments; capsules dehiscent by a single longitudinal spiral
slit; stomata lacking.
O R D E R T A K A K I A L E S Stech & W. Frey
Takakiaceae Stech & W. Frey Type: Takakia S. Hatt. & Inoue
S U P E R C L A S S II
C L A S S S P H A G N O P S I D A Ochyra: Branches usually in fascicles; leaves
composed of a network of chlorophyllose and hyaline cells;
setae lacking; capsules elevated on a pseudopodium; stomata
lacking.
O R D E R S P H A G N A L E S Limpr.: Plants mostly branched, with branches in
fascicles; stems with wood cylinder; leaves unistratose; antheridia
subglobose; archegonia terminal on branches; capsules ovoid.
Sphagnaceae Dumort. Type: Sphagnum L.
O R D E R A M B U C H A N A N I A L E S Seppelt & H. A. Crum: Plants sparsely
branched, with branches not in fascicles; stems without wood
cylinder; leaves partially bistratose; antheridia oblong-cylindric;
archegonia terminal on stems; capsules cylindrical.
Ambuchananiaceae Seppelt & H. A. Crum. Type: Ambuchanania
Seppelt & H. A. Crum
S U P E R C L A S S III
C L A S S A N D R E A E O P S I D A Rothm.: Plants on acidic rocks, generally
autoicous; cauline central strand absent; calyptrae small;
capsules valvate, with four valves attached at apex; seta
absent, pseudopodium present; stomata lacking.
O R D E R A N D R E A E A L E S Limpr.
Andreaeaceae Dumort. Type: Andreaea Hedw.
Acroschisma (Hook.f. & Wilson) Lindl., Andreaea Hedw.
2 Morphology and classification of Bryophyta
S U P E R C L A S S IV
C L A S S A N D R E A E O B R Y O P S I D A Goffinet & W. R. Buck: Plants on calcareous
rocks, dioicous; cauline central strand lacking; calyptrae large and
covering whole capsule; capsules valvate, apex eroding and valves
free when old; stomata lacking; seta present.
O R D E R A N D R E A E O B R Y A L E S B. M. Murray
Andreaeobryaceae Steere & B. M. Murray. Type: Andreaeobryum
Steere & B. M. Murray
SUPERCLASS V
C L A S S O E D I P O D I O P S I D A Goffinet & W. R. Buck: Leaves unicostate;
calyptrae cucullate; capsule symmetric and erect, neck very
long; stomata lacking; capsules gymnostomous.
O R D E R O E D I P O D I A L E S Goffinet & W. R. Buck
Oedipodiaceae Schimp. Type: Oedipodium Schwägr.
C L A S S P O L Y T R I C H O P S I D A Doweld: Plants typically robust, dioicous;
cauline central strand present; stems typically rhizomatous;
costa broad, with adaxial chlorophyllose lamellae; peristome
nematodontous, mostly of (16)32–64 teeth.
O R D E R P O L Y T R I C H A L E S M. Fleisch.
Polytrichaceae Schwägr. Type: Polytrichum Hedw.
Alophozia Card., Atrichopsis Card., Atrichum P. Beauv., Bartramiopsis
Kindb., Dawsonia R. Br., Dendroligotrichum (Müll. Hal.) Broth.,
Hebantia G. L. Sm. Merr., Itatiella G. L. Sm., Lyellia R. Br.,
Meiotrichum (G. L. Sm.) G. L. Sm. Merr., Notoligotrichum G. L. Sm.,
Oligotrichum Lam. & DC., Plagioracelopus G. L. Sm. Merr., Pogonatum
P. Beauv., Polytrichadelphus (Müll. Hal.) Mitt., Polytrichastrum G. L.
Sm., Polytrichum Hedw., Pseudatrichum Reimers, Pseudoracelopus
Broth., Psilopilum Brid., Racelopodopsis Thér., Racelopus Dozy &
Molk., Stereobryon G. L. Sm.
C L A S S T E T R A P H I D O P S I D A Goffinet & W. R. Buck: Leaves unicostate;
calyptrae small conic; capsule symmetric and erect, neck short;
peristome nematodontous, of four erect teeth.
O R D E R T E T R A P H I D A L E S M. Fleisch.
Tetraphidaceae Schimp. Type: Tetraphis Hedw.
Tetraphis Hedw., Tetrodontium Schwägr.
C L A S S B R Y O P S I D A Rothm.: Plants small to robust; leaves costate or not,
typically lacking lamellae; capsules operculate; peristome at least
partially arthrodontous.
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B. Goffinet and others
S U B C L A S S B U X B A U M I I D A E Ochyra: Leaves ecostate; calyptrae cucullate
or mitrate; capsule strongly asymmetric and horizontal, neck
short; peristome double.
O R D E R B U X B A U M I A L E S M. Fleisch.
Buxbaumiaceae Schimp. Type: Buxbaumia Hedw.
S U B C L A S S D I P H Y S C I I D A E Ochyra: Gametophore small, perennial;
leaves costate, often bistratose; capsules asymmetric, immersed
among long perichaetial leaves; peristome double.
O R D E R D I P H Y S C I A L E S M. Fleisch.
Diphysciaceae M. Fleisch. Type: Diphyscium D. Mohr
S U B C L A S S T I M M I I D A E Ochyra: Plants acrocarpous; leaves with
sheathing bases; costa single, mostly with 2 stereid bands;
laminal cells short, mammillose on upper surface; peristome
double; endostome of 64 cilia from a high basal membrane;
calyptrae cucullate, often adhering to the tip of the seta at
maturity.
O R D E R T I M M I A L E S Ochyra
Timmiaceae Schimp. Type: Timmia Hedw.
S U B C L A S S F U N A R I I D A E Ochyra: Plants terricolous, acrocarpous; stem
typically with central strand; annulus often well developed.
O R D E R G I G A S P E R M A L E S Goffinet, Wickett, O. Werner, Ros, A. J. Shaw &
C. J. Cox: Plants stoloniferous; capsules immersed, gymnostomous.
Gigaspermaceae Lindb. Type: Gigaspermum Lindb.
Chamaebryum Thér. & Dixon, Costesia Thér., Gigaspermum Lindb.,
Lorentziella Müll Hal., Oedipodiella Dixon
O R D E R E N C A L Y P T A L E S Dixon: Plants mostly of bare soil; upper
laminal cells mostly pluripapillose, often with C-shaped papillae,
basal laminal cells usually differentiated, smooth; calyptra
completely covering the capsule.
Bryobartramiaceae Sainsb. Type: Bryobartramia Sainsb. Plants
very small, acrocarpous; calyptrae remaining attached to
vaginula, persisting as an epigonium; capsules cleistocarpous;
stomata with two guard cells.
Bryobartramia Sainsb.
Encalyptaceae Schimp. Type: Encalypta Hedw. Plants very
small to medium-size; laminal cells thick-walled, isodiametric
above, rectangular and hyaline or reddish below; annulus not
differentiated; calyptrae very large, enclosing the entire erect
capsule.
2 Morphology and classification of Bryophyta
Bryobrittonia R. S. Williams, Encalypta Hedw.
O R D E R F U N A R I A L E S M. Fleisch.: Peristome diplolepideous, opposite,
endostome lacking cilia.
Funariaceae Schwägr. Type: Funaria Hedw. Protonema short-lived;
costa well developed; laminal cells smooth and thin-walled;
perigonial paraphyses with swollen apical cell; calyptrae
smooth and naked; stomata with single guard cell; peristome
opposite, following a 4:2:4 pattern, or lacking.
Aphanorhegma Sull., Brachymeniopsis Broth., Bryobeckettia Fife,
Clavitheca O. Werner, Ros & Goffinet, Cygnicollum Fife & Magill,
Entosthodon Schwägr., Funaria Hedw., Funariella Sérgio,
Goniomitrium Hook.f. & Wilson, Loiseaubryum Bizot, Nanomitriella
E. B. Bartram, Physcomitrella Bruch & Schimp., Physcomitrellopsis
Broth. & Wager, Physcomitrium (Brid.) Brid., Pyramidula Brid.
Disceliaceae Schimp. Type: Discelium Brid. Protonemata persistent;
costa weak to absent; calyptrae persistent below the urn; stomata
lacking; stomata none, peristomes reduced.
Discelium Brid.
S U B C L A S S D I C R A N I D A E Doweld: Plants typically acrocarpous; peristome
haplolepideous, with a formula of (4):2:3; exostome typically absent;
late state division in the IPL asymmetric.
O R D E R S C O U L E R I A L E S Goffinet & W. R. Buck: Plants blackish, acroor cladocarpous, saxicolous in riparian habitats; calyptrae
mitrate, smooth; annulus not differentiated; capsules urceolate to
globose.
Scouleriaceae S. P. Churchill in Funk & D. R. Brooks. Type: Scouleria
Hook.
Scouleria Hook., Tridontium Hook.f.
Drummondiaceae Goffinet. Type: Drummondia Hook. Stem with
central strand, cladocarpous; costa with differen-tiated adaxial
stereids; laminal cells thick-walled; peristome reduced.
Drummondia Hook.
O R D E R B R Y O X I P H I A L E S H. A. Crum & L. E. Anderson: Leaves
distichous with small dorsal extension along costa; capsules
gymnostomous.
Bryoxiphiaceae Besch. Type: Bryoxiphium Mitt.
O R D E R G R I M M I A L E S M. Fleisch.: Plants slender to robust, usually
saxicolous; laminal cells with thick and often wavy walls;
peristome of 16 entire or divided teeth.
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104
B. Goffinet and others
Grimmiaceae Arn. Type: Grimmia Hedw. Plants typically of acidic
rocks; leaves little different wet or dry, often terminated by hairpoint; laminal cells mostly with sinuose walls.
Bucklandiella Roiv., Codriophorus P. Beauv., Dryptodon Brid., Grimmia
Hedw., Leucoperichaetium Magill, Niphotrichum (BednarekOchyra) Bednarek-Ochyra & Ochyra, Racomitrium Brid.,
Schistidium Bruch & Schimp.
Ptychomitriaceae Schimp. Type: Ptychomitrium Fürnr. Leaves
often crispate when dry; laminal cells with straight walls, often
bistratose; calyptrae cucullate.
Aligrimmia R. S. Williams, Campylostelium Bruch & Schimp.,
Indusiella Broth. & Müll. Hal., Jaffueliobryum Thér.,
Ptychomitriopsis Dixon, Ptychomitrium Fürnr.
Seligeriaceae Schimp. Type: Seligeria Bruch & Schimp..
Plants small, typically of calcareous rocks; alar cells
differentiated; peristome mostly deeply inserted, relatively well
developed.
Blindia Bruch & Schimp., Brachydontium Fürnr., Hymenolomopsis
Thér., Seligeria Bruch & Schimp., Trochobryum Breidl. & Beck
O R D E R A R C H I D I A L E S Limpr. Plants small, often with persistent
protonemata; seta lacking; capsules cleistocarpous, with fewer
than 200 large spores (often 4–60); columella lacking.
Archidiaceae Schimp. Type: Archidium Brid.
O R D E R D I C R A N A L E S H. Philib. ex M. Fleisch.: Plants small to large;
laminal cells generally smooth; alar cells often differentiated;
peristome single, lacking basal membrane, segments trabeculate
and striate.
Fissidentaceae Schimp. Type: Fissidens Hedw. Leaves distichous
and complanate, with vaginant lamellae; apical cell two-sided.
Fissidens Hedw.
Hypodontiaceae Stech & W. Frey Type: Hypodontium Müll.
Hal. (Plantae grandes, caulis filio centrali, folia limbata in sicco
incurvatae, basi amplectenti, cellulis foliorum papillatis, costa turmis
stereidarum duabus basi hyalina.) Plants large, terricolous or
saxicolous; central strand present; leaves incurled when dry,
with clasping base; costa with 2 stereid bands; inner
perichaetial leaves sheathing below but narrowly subulate or
awned apically; calyptra cucullate; spores large.
Hypodontium Müll. Hal.
2 Morphology and classification of Bryophyta
Eustichiaceae Broth. Type: Eustichia (Brid.) Brid. Leaves distichous;
laminal cells quadrate and thick-walled; capsules ribbed;
peristome of 16 teeth.
Eustichia (Brid.) Brid.
Ditrichaceae Limpr. Type: Ditrichum Hampe. Plants slender; alar
cells not differentiated; peristome of 16 completely divided,
terete teeth.
Astomiopsis Müll. Hal., Austrophilibertiella Ochyra, Bryomanginia
Thér., Ceratodon Brid., Cheilothela Broth., Chrysoblastella
R. S. Williams, Cladastomum Müll. Hal., Cleistocarpidium Ochyra &
Bednarek-Ochyra, Crumuscus W. R. Buck & Snider, Cygniella
H. A. Crum, Distichium Bruch & Schimp., Ditrichopsis Broth.,
Ditrichum Hampe, Eccremidium Hook.f. & Wilson, Garckea Müll.
Hal., Kleioweisopsis Dixon, Pleuriditrichum A. L. Andrews & F. J.
Herm., Pleuridium Rabenh., Rhamphidium Mitt., Saelania Lindb.,
Skottsbergia Cardot, Strombulidens W. R. Buck, Trichodon Schimp.,
Tristichium Müll. Hal., Wilsoniella Müll. Hal.
Bruchiaceae Schimp. Type: Bruchia Schwägr. Alar cells not
differentiated; capsules with elongate necks; spores mostly with
trilete markings, usually strongly ornamented.
Bruchia Schwägr., Cladophascum Sim, Eobruchia W. R. Buck,
Pringleella Cardot, Trematodon Michx.
Rhachitheciaceae H. Rob. Type: Rhachithecium Le Jolis. Laminal
cells rectangular in lower half, short to isodiametric above; alar
cells not differentiated; perichaetial leaves differentiated;
capsules ribbed, rarely smooth; endostome teeth fused or not;
IPL of 8 or 16 cells only (peristome formula: (4):2:2 or (4):2:1).
Hypnodontopsis Z. Iwats. & Nog., Jonesiobryum B. H. Allen & Pursell,
Rhachitheciopsis P. de la Varde, Rhachithecium Le Jolis, Tisserantiella
P. de la Varde, Uleastrum W. R. Buck, Zanderia Goffinet
Erpodiaceae Broth. Type: Erpodium (Brid.) Brid. Plants
cladocarpous; costa lacking; laminal cells often papillose;
calyptrae mitrate.
Aulacopilum Wilson, Erpodium (Brid.) Brid., Solmsiella Müll. Hal.,
Venturiella Müll. Hal., Wildia Müll. Hal. & Broth.
Schistostegaceae Schimp. Type: Schistostega D. Mohr. Gametophores
dimorphic, small, annual, arising from persistent luminescent
protonemata; leaves ecostate, distichous or in five rows; capsules
globose, gymnostomous, lacking stomata and annulus.
Schistostega D. Mohr
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B. Goffinet and others
Viridivelleraceae I. G. Stone Type: Viridivellus I. G. Stone.
Protonemata persistent; stems producing gametangia and
associated leaves only; capsules gymnostomous.
Viridivellus I. G. Stone
Rhabdoweisiaceae Limpr. Type: Rhabdoweisia Bruch & Schimp.
Plants small to medium size; stem lacking central strand;
capsules ribbed, widest at mouth.
Amphidium Schimp., Arctoa Bruch & Schimp., Cynodontium
Schimp., Dichodontium Schimp., Dicranoweisia Milde, Glyphomitrium
Brid., Holodontium (Mitt.) Broth., Hymenoloma Dusén, Kiaeria
I. Hagen, Oncophorus (Brid.) Brid., Oreas Brid., Oreoweisia (Bruch &
Schimp.) De Not., Pseudohyophila Hilp., Rhabdoweisia Bruch &
Schimp., Symblepharis Mont., Verrucidens Cardot
Dicranaceae Schimp. Type: Dicranum Hedw. Plants generally
robust, acrocarpous or cladocarpous; cauline central strand
present or not; leaves often with well differentiated alar cells;
laminal cells elongate, thick-walled and porose; calyptra mitrate
or cucullate; peristome of 16 flat teeth divided in upper twothirds, typically with vertically pitted outer surface.
Anisothecium Mitt., Aongstroemia Bruch & Schimp., Aongstroemiopsis M. Fleisch., Braunfelsia Paris, Brotherobryum M. Fleisch.,
Bryotestua Thér. & P. de la Varde, Camptodontium Dusén,
Campylopodium (Müll. Hal.) Besch., Chorisodontium (Mitt.) Broth.,
Cnestrum I. Hagen, Cryptodicranum E. B. Bartram, Dicnemon
Schwägr., Dicranella (Müll. Hal.) Schimp., Dicranoloma (Renauld)
Renauld, Dicranum Hedw., Diobelonella Ochyra, Eucamptodon
Mont., Eucamptodontopsis Broth., Holomitriopsis H. Rob.,
Holomitrium Brid., Hygrodicranum Cardot, Leptotrichella (Müll.
Hal.) Lindb., Leucoloma Brid., Macrodictyum (Broth.) E. H.
Hegew., Mesotus Mitt., Mitrobryum H. Rob., Muscoherzogia
Ochyra,
Orthodicranum
(Bruch
&
Schimp.)
Loeske,
Paraleucobryum (Limpr.) Loeske, Parisia Broth., Platyneuron
(Cardot) Broth., Pocsiella Bizot, Polymerodon Herzog,
Pseudephemerum (Lindb.) I. Hagen, Pseudochorisodontium
(Broth.) C. H. Gao, Vitt, D. H. Fu & T. Cao, Schliephackea Müll.
Hal.,
Sclerodontium
Schwägr.,
Sphaerothecium
Hampe,
Steyermarkiella H. Rob., Wardia Harv. & Hook., Werneriobryum
Herzog
Leucobryaceae Schimp. Type: Leucobryum Hampe. Plants robust,
glaucous; cauline central strand lacking; costa broad, occupying
2 Morphology and classification of Bryophyta
most of the leaf, with median chlorophyllose cells and adaxial
and abaxial layers of hyaline cells.
Atractylocarpus Mitt., Brothera Müll. Hal., Bryohumbertia P. de la
Varde & Thér., Campylopodiella Cardot, Campylopus Brid.,
Cladopodanthus Dozy & Molk., Dicranodontium Bruch & Schimp.,
Leucobryum Hampe, Microcampylopus (Müll. Hal.) Fleisch.,
Ochrobryum Mitt., Pilopogon Brid., Schistomitrium Dozy & Molk.
Calymperaceae Kindb. Type: Calymperes Sw. Plants epiphytic; stem
lacking central strand; leaves narrowly to broadly lanceolate;
laminal cells papillose or smooth; often with hyaline
cancellinae on either side of costa at leaf base; calyptrae
persistent or not; peristome of 16 (rarely fused into 8) segments,
smooth, papillose or vertically striate.
Arthrocormus Dozy & Molk., Calymperes Sw., Exodictyon Cardot,
Exostratum L. T. Ellis, Leucophanes Brid., Mitthyridium H. Rob.,
Octoblepharum Hedw., Syrrhopodon Schwägr.
O R D E R P O T T I A L E S M. Fleisch.: Plants minute to robust, generally
orthotropic; upper laminal cells usually isodiametric and
papillose; alar cells not differentiated; perichaetial leaves
typically not differentiated; capsules erect; peristome typically
papillose, not trabeculate.
Pottiaceae Schimp. Type: Pottia (Rchb.) Fürnr. Plants small to
robust, primarily terrestrial; cauline central strand often
present; leaves narrowly lanceolate to ligulate; laminal cells
typically papillose; calyptrae cucullate, naked, smooth;
peristome of 16 or 32 segments.
Acaulon Müll. Hal., Aloinia Kindb., Aloinella Cardot, Anoectangium
Schwägr., Aschisma Lindb., Barbula Hedw., Bellibarbula P. C.
Chen, Bryoceuthospora H. A. Crum & L. E. Anderson,
Bryoerythrophyllum P. C. Chen, Calymperastrum I. G. Stone,
Calyptopogon (Mitt.) Broth., Chenia R. H. Zander, Chionoloma
Dixon, Cinclidotus P. Beauv., Crossidium Jur., Crumia W. B.
Schofield, Dialytrichia (Schimp.) Limpr., Didymodon Hedw.,
Dolotortula R. H. Zander, Ephemerum Schimp., Erythrophyllopsis
Broth., Eucladium Bruch & Schimp., Ganguleea R. H. Zander,
Gertrudiella Broth., Globulinella Steere, Gymnostomiella M.
Fleisch., Gymnostomum Nees & Hornsch., Gyroweisia Schimp.,
Hennediella Paris, Hilpertia R. H. Zander, Hymenostyliella E. B.
Bartram, Hymenostylium Brid., Hyophila Brid., Hyophiladelphus
(Müll. Hal.) R. H. Zander, Leptobarbula Schimp., Leptodontiella
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B. Goffinet and others
R. H. Zander & E. H. Hegew., Leptodontium (Müll. Hal.) Lindb.,
Luisierella Thér. & P. de la Varde, Microbryum Schimp.,
Micromitrium Austin, Mironia R. H. Zander, Molendoa Lindb.,
Nanomitriopsis Cardot, Neophoenix R. H. Zander & During,
Pachyneuropsis H. Mill., Phascopsis I. G. Stone, Plaubelia Brid.,
Pleurochaete Lindb., Pottiopsis Blockeel & A. J. E. Sm.,
Pseudocrossidium R. S. Williams, Pseudosymblepharis Broth.,
Pterygoneurum Jur., Quaesticula R. H. Zander, Reimersia P. C.
Chen, Rhexophyllum Herzog, Sagenotortula R. H. Zander,
Saitobryum R. H. Zander, Sarconeurum Bryhn, Scopelophila (Mitt.)
Lindb., Splachnobryum Müll. Hal., Stegonia Venturi, Stonea R. H.
Zander, Streptocalypta Müll. Hal., Streptopogon Mitt.,
Streptotrichum Herzog, Syntrichia Brid., Teniolophora W. D. Reese,
Tetracoscinodon R. Br. ter, Tetrapterum A. Jaeger, Timmiella (De
Not.) Schimp., Tortella (Lindb.) Limpr., Tortula Hedw.,
Trachycarpidium Broth., Trachyodontium Steere, Trichostomum
Bruch, Triquetrella Müll. Hal., Tuerckheimia Broth., Uleobryum
Broth., Weisiopsis Broth., Weissia Hedw., Weissiodicranum W. D.
Reese, Willia Müll. Hal.
Pleurophascaceae Broth. Type: Pleurophascum Lindb. Plants
robust; stems creeping with erect secondary stems; leaves
concave, ecostate; cells short above, elongate below, smooth,
strongly porose; setae elongate; capsules large, globose,
cleistocarpous; calyptra cucullate.
Pleurophascum Lindb.
Serpotortellaceae W. D. Reese & R. H. Zander. Type: Serpotortella
Dixon. Plants robust, cladocarpous, epiphytic; cauline central
strand present; leaf margins entire and unistratose; perichaetial
leaves differentiated; peristome well developed, reflexed when
dry.
Serpotortella Dixon
Mitteniaceae Broth. Type: Mittenia Lindb. Plants small, with
luminescent protonemata; cauline central strand lacking;
leaves complanate, decurrent; perichaetia polysetous;
peristome double, outer row homologous to bryoid endostome.
Mittenia Lindb.
S U B C L A S S B R Y I D A E Engl.: Peristome double, of alternating teeth and
segments; endostome ciliate; late stage division in the IPL asymmetric
Superorder Bryanae (Engl.) Goffinet & W. R. Buck: Plants acrocarpous, cladocarpous or pseudopleurocarpous; pseudoparaphyllia
2 Morphology and classification of Bryophyta
generally lacking; leaves erect to spreading, lanceolate to ovate,
mostly costate, costal anatomy mostly heterogeneous; laminal cells
generally short.
O R D E R S P L A C H N A L E S Ochyra: Laminal cells rhombic to elongate,
typically smooth; capsules erect with differentiated neck;
peristome single or double; cilia rudimentary or lacking.
Splachnaceae Grev. & Arn. Type: Splachnum Hedw. Plants mostly
coprophilous; laminal cells thin-walled, rhomboidal; annulus
not differentiated; capsules erect, neck often differentiated
into broad hypophysis; endostome fused to exostome or
lacking.
Aplodon R. Br., Moseniella Broth., Splachnum Hedw., Tayloria
Hook., Tetraplodon Bruch & Schimp., Voitia Hornsch.
Meesiaceae Schimp. Type: Meesia Hedw. Plants acrocarpous,
often of moist habitats; leaves often in rows; lower laminal
cells often delicate and hyaline; setae elongate; capsules
inclined to suberect but strongly curved and asymmetric,
oblong-pyriform with a well-differentiated neck; peristome
double with exostome teeth usually shorter than endostome
segments; calyptra cucullate.
Amblyodon P. Beauv., Leptobryum (Bruch & Schimp.) Wilson,
Meesia Hedw., Neomeesia Deguchi, Paludella Brid.
O R D E R B R Y A L E S Limpr.: Plants primarily terricolous; cauline central
strand present; laminal cells rhombic to elongate, smooth;
annulus differentiated; capsules pendent, neck differentiated;
peristome double, typically well developed and ciliate;
exostome incurved.
Catoscopiaceae Broth. Type: Catoscopium Brid. Plants small,
slender; leaves in three ranks; laminal cells quadrate and
smooth; capsules black, asymmetric, horizontal; peristome
double and reduced.
Catoscopium Brid.
Pulchrinodaceae D. Quandt, N. E. Bell & Stech. Type:
Pulchrinodus B. H. Allen. Plants with foliose pseudoparaphyllia;
stems with central strand; leaves ecostate; laminal cells
smooth, strongly porose, bistratose at base; alar cells strongly
differentiated; perigonia terminal, discoid; perigonia stalked.
Pulchrinodus B. H. Allen
Bryaceae Schwägr. Type: Bryum Hedw. Plants erect, mostly
unbranched, acrocarpous; laminal cells mostly rhomboidal,
109
110
B. Goffinet and others
smooth, thin-walled; costa single, strong; capsules inclined to
pendulous, smooth, with differentiated neck.
Acidodontium Schwägr., Anomobryum Schimp., Brachymenium
Schwägr., Bryum Hedw., Leptostomopsis (Müll. Hal.) J. R. Spence
& H. P. Ramsay, Mniobryoides Hörmann, Osculatia De Not.,
Perssonia Bizot, Ptychostomum Hornsch., Rhodobryum (Schimp.)
Limpr., Roellia Kindb., Rosulabryum J. R. Spence
Phyllodrepaniaceae Crosby. Type: Phyllodrepanium Crosby. Plants
small; leaves complanate, in four rows; peristome single, of 16
segments.
Mniomalia Müll. Hal., Phyllodrepanium Crosby
Pseudoditrichaceae Steere & Z. Iwats. Type: Pseudoditrichum
Steere & Z. Iwats. Plants very small; leaves ovate lanceolate;
laminal cells thick-walled; capsules erect; peristome double;
cilia lacking.
Pseudoditrichum Steere & Z. Iwats.
Mniaceae Schwägr. Type: Mnium Hedw. Plants acro- or
cladocarpous; leaves often bordered and often toothed; laminal
cells thin-walled, rhomboidal to elongate.
Cinclidium Sw., Cyrtomnium Holmen, Epipterygium Lindb., Leucolepis
Lindb., Mielichhoferia Nees & Hornsch., Mnium Hedw., Ochiobryum
J. R. Spence & H. P. Ramsay, Orthomnion Wilson, Plagiomnium T. J.
Kop., Pohlia Hedw., Pseudobryum (Kindb.) T. J. Kop., Pseudopohlia
R. S. Williams, Rhizomnium (Broth.) T. J. Kop., Schizymenium Harv.,
Synthetodontium Cardot, Trachycystis T. J. Kop.
Leptostomataceae Schwägr. Type: Leptostomum R. Br. Plants
forming dense mats; stems heavily tomentose; leaf margins
entire, unbordered; annulus poorly differentiated to lacking;
stomata cryptoporous; peristome strongly reduced.
Leptostomum R. Br.
O R D E R B A R T R A M I A L E S D. Quandt, N. E. Bell & Stech: Plants often
robust; laminal cells isodiametric, quadrate or rectangular,
smooth or prorulose; annulus typically undifferentiated; capsules
subglobose, erect or slightly curved, typically ribbed; neck
undifferentiated.
Bartramiaceae Schwägr. Type: Bartramia Hedw.
Anacolia Schimp., Bartramia Hedw., Breutelia (Bruch & Schimp.)
Schimp., Conostomum Sw., Fleischerobryum Loeske, Flowersia
D. G. Griffin & W. R. Buck, Leiomela (Mitt.) Broth., Neosharpiella
H. Rob. & Delgad., Philonotis Brid., Plagiopus Brid.
2 Morphology and classification of Bryophyta
O R D E R O R T H O T R I C H A L E S Dixon: Plants medium-size, epiphytic or
saxicolous; cauline central strand lacking; laminal cells typically
papillose; capsules erect; peristome double or reduced; exostome
recurved.
Orthotrichaceae Arn. Type: Orthotrichum Hedw. Plants acrocarpous
or cladocarpous; laminal cells mostly isodiametric, thick-walled;
calyptrae typically plicate and hairy; capsules erect, rarely
immersed, often ribbed; OPL thick and teeth recurved when dry;
cilia lacking.
Cardotiella Vitt, Ceuthotheca Lewinsky, Codonoblepharon Schwägr.,
Desmotheca Lindb., Florschuetziella Vitt, Groutiella Steere, Leiomitrium
Mitt., Leratia Broth. & Paris, Macrocoma (Müll. Hal.) Grout,
Macromitrium Brid., Matteria Goffinet, Orthotrichum Hedw.,
Pentastichella Müll. Hal., Pleurorthotrichum Broth., Schlotheimia Brid.,
Sehnemobryum Lewinsky-Haapasaari & Hedenäs, Stoneobryum D. H.
Norris & H. Rob., Ulota D. Mohr, Zygodon Hook. & Taylor
O R D E R H E D W I G I A L E S Ochyra: Plants medium to robust, plagiotropic,
acrocarpous or cladocarpous; laminal cells thick-walled, papillose
or smooth; capsules gymnostomous and immersed.
Hedwigiaceae Schimp. Type: Hedwigia P. Beauv. Protonemata
globular; leaves ecostate; laminal cells pluripapillose; calyptrae
smooth, naked.
Braunia Bruch & Schimp., Bryowijkia Nog., Hedwigia P. Beauv.,
Hedwigidium Bruch & Schimp., Pseudobraunia (Lesq. & James)
Broth.
Helicophyllaceae Broth. Type: Helicophyllum Brid. Leaves
unicostate, dimorphic, with lateral leaves strongly inrolled
when dry, dorsal and ventral leaves reduced and appressed;
laminal cells smooth.
Helicophyllum Brid.
Rhacocarpaceae Kindb. Type: Rhacocarpus Lindb. Leaves ecostate,
bordered by narrow cells; laminal cells roughened; alar cells
inflated.
Pararhacocarpus Frahm, Rhacocarpus Lindb.
O R D E R R H I Z O G O N I A L E S Goffinet & W. R. Buck: Plants pseudopleurocarpous, often with basal sporophytes; leaves often
complanate and asymmetric; laminal cells mostly short, smooth
or unipapillose, basal cells not or weakly differentiated; setae
elongate; capsules cylindric, often asymmetric; peristome often
reduced.
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B. Goffinet and others
Rhizogoniaceae Broth. Type: Rhizogonium Brid. Plants small to
large; cauline central strand present; marginal laminal cells
often differentiated, bi- or multistratose, often toothed; costa
typically toothed above; annulus differentiated; capsules
generally smooth; peristome typically well developed, ciliate, or
reduced to endostome or exostome, or peristome absent.
Calomnion Hook.f. & Wilson, Cryptopodium Brid., Goniobryum
Lindb., Pyrrhobryum Mitt., Rhizogonium Brid.
Aulacomniaceae Schimp. Type: Aulacomnium Schwägr. Plants
acrocarpous but sporophytes sometimes lateral, often with leaflike gemmae; leaves unicostate; capsules usually asymmetric,
often furrowed.
Aulacomnium Schwägr., Hymenodontopsis Herzog, Mesochaete
Lindb.
Orthodontiaceae Goffinet. Type: Orthodontium Wilson. Plants
small to robust, acrocarpous but often with basal sporophytes;
laminal cells short to elongate, lax; capsules often ribbed;
annulus lacking; peristome often reduced, sometimes with
exostome lacking, endostomial membrane reduced or lacking.
Hymenodon Hook.f. & Wilson, Leptotheca Schwägr., Orthodontium
Wilson, Orthodontopsis Ignatov & B. C. Tan
Superorder Hypnanae W. R. Buck, Goffinet & A. J. Shaw: Plants
pleurocarpous, typically freely branching; pseudoparaphyllia
usually present; leaves mostly ovate, costate or not, costal anatomy
usually homogeneous; laminal cells generally elongate.
O R D E R H Y P N O D E N D R A L E S N. E. Bell, Ang. Newton & D. Quandt: Plants
often stipitate; costae single, with anatomy heterogeneous; laminal
cells mostly short; setae elongate; peristome double.
Braithwaiteaceae N. E. Bell, Ang. Newton & D. Quandt. Type:
Braithwaitea Lindb. Leaves cymbiform, obtuse; costa strong,
excurrent; peristome reduced, exostome teeth with vestigial
trabeculae, endostome segments linear from a low basal
membrane.
Braithwaitea Lindb.
Racopilaceae Kindb. Type: Racopilum P. Beauv. Stems plagiotropic;
leaves dimorphic with dorsal ones reduced; costa excurrent;
capsules long-exserted; peristome double, well developed.
Powellia Mitt., Racopilum P. Beauv.
Pterobryellaceae W. R. Buck & Vitt. Type: Pterobryella (Müll.
Hal.) A. Jaeger. Plants robust and large, stipitate from
2 Morphology and classification of Bryophyta
rhizomatous stem, frondose to dendroid; cauline central strand
lacking; capsules short oval; annulus differentiated; peristome
double, with long teeth and segments but reduced cilia.
Cyrtopodendron M. Fleisch., Pterobryella (Müll. Hal.) A. Jaeger,
Sciadocladus Lindb. ex Kindb.
Hypnodendraceae Broth. Type: Hypnodendron (Müll. Hal.) Mitt.
Plants robust, rhizomatous and stipitate; secondary stems erect,
frondose to dendroid; laminal marginal cells differentiated or
not, unistratose, often toothed; capsules often ribbed when dry;
annulus differentiated; peristome well developed, ciliate.
Bescherellia Duby, Cyrtopus (Brid.) Hook.f., Dendro-hypnum Hampe,
Franciella Thér., Hypnodendron (Müll. Hal.) Mitt., Mniodendron
Lindb. ex Dozy & Molk., Spiridens Nees, Touwiodendron N. E.
Bell, Ang. Newton & D. Quandt
O R D E R P T Y C H O M N I A L E S W. R. Buck, C. J. Cox, A. J. Shaw & Goffinet.
Plants usually robust and turgid, often phyllodioicous; stems
sympodially branched, usually lacking a central strand; leaves
usually plicate, often strongly toothed; costae short and double;
laminal cells elongate, often thick-walled and porose; alar cells
often colored; capsules mostly ribbed; endostomial segments
lacking baffle-like cross walls; calyptrae often cucullate.
Ptychomniaceae M. Fleisch. Type: Ptychomnion (Hook.f. & Wilson)
Mitt. Alar cells little or well differentiated, except for color;
capsules long-exserted or immersed, smooth to strongly
8-ribbed, anisosporous or isosporous, calyptrae mitrate or
cucullate.
Cladomnion Hook.f. & Wilson, Cladomniopsis M. Fleisch., Dichelodontium
Broth., Endotrichellopsis During, Euptychium Schimp., Garovaglia
Endl., Glyphotheciopsis Pedersen & Ang. Newton, Glyphothecium
Hampe, Hampeella Müll. Hal., Ombronesus N. E. Bell, Pederson &
Ang. Newton, Ptychomniella (Broth.) W. R. Buck, C. J. Cox, A. J.
Shaw & Goffinet, Ptychomnion (Hook.f. & Wilson) Mitt.,
Tetraphidopsis Broth. & Dixon
O R D E R H O O K E R I A L E S M. Fleisch.: Laminal cells mostly thin-walled,
often short; alar cells mostly not differentiated; exothecial cells
mostly collenchymatous; opercula mostly rostrate; exostome
teeth often furrowed, endostomial segments with baffle-like cross
walls; calyptrae often mitrate.
Hypopterygiaceae Mitt. Type: Hypopterygium Brid. Plants
dendroid; amphigastria differentiated; leaves often limbate;
113
114
B. Goffinet and others
costa single; laminal cells short, mostly smooth; alar cells not
differentiated; exostome teeth not furrowed; endostomial
segments lacking baffle-like cross walls.
Arbusculohypopterygium Stech, T. Pfeiffer & W. Frey, Canalohypopterygium W. Frey & Schaepe, Catharomnion Hook.f. & Wilson,
Cyathophorum P. Beauv., Dendrocyathophorum Dixon, Dendrohypopterygium Kruijer, Hypopterygium Brid., Lopidium Hook.f. &
Wilson
Saulomataceae W. R. Buck, C. J. Cox, A. J. Shaw & Goffinet Type:
Sauloma (Hook.f. & Wils.) Mitt. Plants slender, usually erect; leaves
ecostate; laminal cells short, firm-walled; capsules erect,
symmetric; exostome teeth usually furrowed.
Ancistrodes Hampe, Sauloma (Hook.f. & Wilson) Mitt., Vesiculariopsis
Broth.
Daltoniaceae Schimp. Type: Daltonia Hook. & Taylor. Stems
lacking central strand; pseudoparaphyllia absent or rarely
filamentous; laminal cells oval to long-hexagonal, differentiated
at leaf margins or rarely not; costa single; calyptrae unistratose at
middle, fringed at base or not, usually naked but rarely densely
hairy.
Achrophyllum Vitt & Crosby, Adelothecium Mitt., Benitotania H.
Akiyama, Yamaguchi & Suleiman, Bryobrothera Thér.,
Calyptrochaeta Desv., Crosbya Vitt, Beeveria Fife, Daltonia Hook. &
Taylor, Distichophyllidium M. Fleisch., Distichophyllum Dozy &
Molk.,
Ephemeropsis
K. I.
Goebel,
Leskeodon
Broth.,
Leskeodontopsis Zanten, Metadistichophyllum Nog. & Z. Iwats.
Schimperobryaceae W. R. Buck, C. J. Cox, A. J. Shaw & Goffinet.
Type: Schimperobryum Margad. Plants robust, epiphytic; leaves
complanate with short, double costa; laminal cells hexagonal,
porose; setae short; capsules erect; exostome teeth crossstriolate, not furrowed; cilia absent; calyptra mitrate, not fringed.
Schimperobryum Margad.
Hookeriaceae Schimp. Type: Hookeria Sm. Stems with central
strand; pseudoparaphyllia filamentous or absent; gemmae often
on rhizoids; laminal cells large and lax; costa usually short and
double; calyptrae multistratose at middle, naked.
Crossomitrium Müll. Hal., Hookeria Sm.
Leucomiaceae Broth. Type: Leucomium Mitt. Stems lacking central
strand; pseudoparaphyllia absent; laminal cells linear, lax; costa
lacking; calyptrae cucullate.
2 Morphology and classification of Bryophyta
Leucomium Mitt., Rhynchostegiopsis Müll. Hal., Tetrastichium (Mitt.)
Cardot
Pilotrichaceae Kindb. Type: Pilotrichum P. Beauv. Stems lacking
central strand; pseudoparaphyllia none or foliose; laminal cells
various; costa strong and double, or short and double; calyptrae
unistratose at middle, usually hairy.
Actinodontium Schwägr., Amblytropis (Mitt.) Broth., Brymela Crosby &
B. H. Allen, Callicostella (Müll. Hal.) Mitt., Callicostellopsis Broth.,
Cyclodictyon Mitt., Diploneuron E. B. Bartram, Helicoblepharum
(Mitt.) Broth., Hemiragis (Brid.) Besch., Hookeriopsis (Besch.)
A. Jaeger, Hypnella (Müll. Hal.) A. Jaeger, Lepidopilidium (Müll.
Hal.) Broth., Lepidopilum (Brid.) Brid., Neohypnella E. B. Bartram,
Philophyllum Müll. Hal., Pilotrichidium Besch., Pilotrichum P. Beauv.,
Stenodesmus (Mitt.) A. Jaeger, Stenodictyon (Mitt.) A. Jaeger,
Thamniopsis (Mitt.) M. Fleisch., Trachyxiphium W. R. Buck
O R D E R H Y P N A L E S (M. Fleisch.) W. R. Buck & Vitt: Stems monopodially
or sympodially branched; alar cells often differentiated; opercula
various, mostly not rostrate; exostome seldom furrowed; calyptrae
mostly cucullate, naked.
Rutenbergiaceae M. Fleisch. Type: Rutenbergia Besch. Stems
sympodially branched, lacking a central strand; secondary
stems little branched; costa single; laminal cells prorulose; alar
cells well differentiated; capsules immersed; calyptrae mitrate,
hairy.
Neorutenbergia Bizot & Pócs, Pseudocryphaea Broth., Rutenbergia
Besch.
Trachylomataceae W. R. Buck & Vitt. Type: Trachyloma Brid. Stems
sympodially branched; secondary stems stipitate frondose,
complanate-foliate; alar cells weakly differentiated; asexual
propagula of stem-borne, filamentous gemmae; exostome teeth
pale, densely papillose.
Trachyloma Brid.
Fontinalaceae Schimp. Type: Fontinalis Hedw. Plants aquatic;
stems sympodially branched; costa single or short and double
(and then the leaves concave to carinate); capsules immersed or
short-exserted; endostome forming a trellis; calyptrae mitrate or
cucullate.
Brachelyma Cardot, Dichelyma Myrin, Fontinalis Hedw.
Climaciaceae Kindb. Type: Climacium F. Weber & D. Mohr. Plants
dendroid; stems sympodially branched, with paraphyllia or
115
116
B. Goffinet and others
longitudinal lamellae on stipe; leaves decurrent or not; costa
single; laminal cells relatively short, smooth.
Climacium F. Weber & D. Mohr, Pleuroziopsis E. Britton
Amblystegiaceae G. Roth. Type: Amblystegium Schimp. Plants
typically growing in moist areas; stems monopodially branched;
paraphyllia sometimes present; costa mostly single but often
variable; laminal cells mostly short, sometimes elongate,
smooth or rarely prorulose; alar cells not to strongly
differentiated; setae often relatively long in comparison to size
of plants; capsules strongly curved and asymmetric; exostome
teeth yellow-brown, cross-striolate.
Amblystegium Schimp., Anacamptodon Brid., Bryostreimannia Ochyra,
Campyliadelphus (Kindb.) R. S. Chopra, Campylium (Sull.) Mitt.,
Conardia H. Rob., Cratoneuron (Sull.) Spruce, Cratoneuropsis (Broth.)
M. Fleisch., Drepanocladus (Müll. Hal.) G. Roth, Gradsteinia Ochyra,
Hygroamblystegium Loeske, Hygrohypnella Ignatov & Ignatova,
Hygrohypnum Lindb., Hypnobartlettia Ochyra, Koponenia Ochyra,
Leptodictyum (Schimp.) Warnst., Limbella (Müll. Hal.) Müll. Hal.,
Limprichtia Loeske, Ochyraea Váňa, Palustriella Ochyra, Pictus C. C.
Towns., Pseudocalliergon (Limpr.) Loeske, Pseudohygrohypnum Kanda,
Sanionia Loeske, Sasaokaea Broth., Sciaromiella Ochyra, Sciaromiopsis
Broth., Scorpidium (Schimp.) Limpr., Sinocalliergon Sakurai,
Serpoleskea (Limpr.) Loeske, Vittia Ochyra
Calliergonaceae Vanderpoorten, Hedenäs, C. J. Cox & A. J. Shaw.
Type: Calliergon (Sull.) Kindb. Plants typically growing in
moist areas; stems monopodially branched; costa single;
laminal cells mostly elongate, smooth; alar cells often enlarged
and inflated; setae elongate; capsules mostly asymmetric;
peristome hypnoid.
Calliergon (Sull.) Kindb., Hamatocaulis Hedenäs, Loeskypnum H. K. G.
Paul, Straminergon Hedenäs, Warnstorfia Loeske
Helodiaceae Ochyra. Type: Helodium Warnst. Stems monopodially
branched; paraphyllia present, filamentous to narrowly foliose,
the cells elongate, not papillose; costa single; laminal cells mostly
prorulose; alar cells often well differentiated; exostome teeth
cross-striolate.
Actinothuidium (Besch.) Broth., Bryochenea C. H. Gao & K. C. Chang,
Helodium Warnst.
Rigodiaceae H. A. Crum. Type: Rigodium Schwägr. Plants terrestrial
or weakly epiphytic, more or less stipitate; stems monopodially
2 Morphology and classification of Bryophyta
branched; paraphyllia absent; stipe, stem and branch leaves
differentiated; costa single; laminal cells short, smooth; alar
cells not or weakly differentiated; setae smooth; capsules
curved and asymmetric; exostome teeth densely cross-striolate.
Rigodium Schwägr.
Leskeaceae Schimp. Type: Leskea Hedw. Plants terrestrial or
epiphytic; stems monopodially branched, often terete-foliate;
paraphyllia non-papillose; leaves mostly short-acuminate; costa
mostly single; laminal cells short, usually unipapillose; alar cells
weakly differentiated; capsules curved and asymmetric when
plants terrestrial but in epiphytes often erect; exostome striate
in terrestrial taxa but in epiphytes often pale, weakly
ornamented; endostome often reduced.
Claopodium (Lesq. & James) Renauld & Cardot, Fabronidium Müll.
Hal., Haplocladium (Müll. Hal.) Müll. Hal., Hylocomiopsis Cardot,
Leptocladium Broth., Leptopterigynandrum Müll. Hal., Lescuraea
Bruch & Schimp., Leskea Hedw., Leskeadelphus Herzog, Leskeella
(Limpr.) Loeske, Lindbergia Kindb., Mamillariella Laz., Miyabea
Broth., Orthoamblystegium Dixon & Sakurai, Platylomella
A. L. Andrews, Pseudoleskea Bruch & Schimp., Pseudoleskeella
Kindb.,
Pseudoleskeopsis
Broth.,
Ptychodium
Schimp.,
Rigodiadelphus Dixon, Rozea Besch., Schwetschkea Müll. Hal.
Thuidiaceae Schimp. Type: Thuidium Bruch & Schimp. Plants
terrestrial; stems monopodially branched; paraphyllia present,
the cells papillose; stem and branch leaves differentiated; costa
single; laminal cells short, papillose; alar cells not or weakly
differentiated; setae often roughened; capsules typically curved
and asymmetric; exostome teeth densely cross-striolate;
calyptrae naked or sparsely hairy.
Abietinella Müll. Hal., Boulaya Cardot, Cyrto-hypnum (Hampe) Hampe &
Lorentz, Fauriella Besch., Pelekium Mitt., Rauiella Reimers, Thuidiopsis
(Broth.) M. Fleisch., Thuidium Bruch & Schimp.
Regmatodontaceae Broth. Type: Regmatodon Brid. Plants
epiphytic; stems monopodially branched; paraphyllia absent;
costa single; laminal cells short, smooth; alar cells not or
weakly, differentiated; capsules erect; exostome teeth much
shorter than endostome segments.
Regmatodon Brid.
Stereophyllaceae W. R. Buck & Ireland. Type: Stereophyllum
Mitt. Plants terrestrial or epiphytic; stems monopodially
117
118
B. Goffinet and others
branched; costa typically single; laminal cells elongate,
mostly smooth, rarely unipapillose; alar cells differentiated,
collenchymatous, extending across base of costa; setae smooth;
capsules inclined to erect; exostome teeth cross-striolate to
papillose.
Catagoniopsis Broth., Entodontopsis Broth., Eulacophyllum W. R. Buck &
Ireland, Juratzkaea Lorentz, Pilosium (Müll. Hal.) M. Fleisch.,
Sciuroleskea Broth., Stenocarpidium Müll. Hal., Stereophyllum Mitt.
Brachytheciaceae G. Roth. Type: Brachythecium Schimp. Plants
mostly growing in mesic woodlands, terrestrial; stems
monopodially branched; leaves often plicate; costa single, often
projecting as a small spine; laminal cells elongate; alar cells
mostly weakly differentiated; setae sometimes roughened;
capsules often relatively short, curved, asymmetric; opercula
conic to rostrate; exostome teeth mostly red-brown; calyptrae
mostly naked.
Aerobryum Dozy & Molk., Aerolindigia M. Menzel, Brachytheciastrum
Ignatov & Huttunen, Brachythecium Schimp., Bryhnia Kaurin,
Bryoandersonia H. Rob., Cirriphyllum Grout, Clasmatodon Hook.f. &
Wilson, Donrichardsia H. A. Crum & L. E. Anderson, Eriodon Mont.,
Eurhynchiadelphus Ignatov & Huttunen, Eurhynchiastrum Ignatov &
Huttunen, Eurhynchiella M. Fleisch., Eurhynchium Bruch & Schimp.,
Flabellidium Herzog, Helicodontium Schwägr., Homalotheciella
(Cardot) Broth., Homalothecium Schimp., Juratzkaeella W. R. Buck,
Kindbergia Ochyra, Lindigia Hampe, Mandoniella Herzog,
Meteoridium (Müll. Hal.) Manuel, Myuroclada Besch., Nobregaea
Hedenäs, Okamuraea Broth., Oxyrrhynchium (Schimp.) Warnst.,
Palamocladium Müll. Hal., Plasteurhynchium Broth., Platyhypnidium
M. Fleisch., Pseudopleuropus Takaki, Pseudoscleropodium (Limpr.)
M. Fleisch., Remyella Müll. Hal., Rhynchostegiella (Schimp.) Limpr.,
Rhynchostegium Bruch & Schimp., Schimperella Thér., Sciuro-hypnum
(Hampe) Hampe, Scleropodium Bruch & Schimp., Scorpiurium
Schimp., Squamidium (Müll. Hal.) Broth., Stenocarpidiopsis M.
Fleisch., Tomentypnum Loeske, Zelometeorium Manuel
Meteoriaceae Kindb. Type: Meteorium (Brid.) Dozy & Molk. Plants
epiphytic, often pendent; stems monopodially branched, often
very elongate; costa short and double or single; laminal cells
mostly elongate, sometimes short, often variously papillose;
alar cells not or weakly differentiated; setae often short,
roughened; capsules often immersed, erect, symmetric; exostome
2 Morphology and classification of Bryophyta
teeth cross-striolate to papillose; endostome often reduced; calyptrae
mitrate or cucullate, often hairy.
Aerobryidium M. Fleisch., Aerobryopsis M. Fleisch., Barbella M. Fleisch.,
Barbellopsis Broth., Chrysocladium M. Fleisch., Cryptopapillaria
M. Menzel, Diaphanodon Renauld & Cardot, Duthiella Renauld,
Floribundaria M. Fleisch., Lepyrodontopsis Broth., Meteoriopsis
Broth., Meteorium (Brid.) Dozy & Molk., Neodicladiella W. R. Buck,
Neonoguchia S. H. Lin, Pseudospiridentopsis (Broth.) M. Fleisch.,
Pseudotrachypus P. de la Varde & Thér., Sinskea W. R. Buck, Toloxis
W. R. Buck, Trachycladiella (M. Fleisch.) M. Menzel & W. SchultzeMotel, Trachypodopsis M. Fleisch., Trachypus Reinw. & Hornsch.
Myriniaceae Schimp. Type: Myrinia Schimp. Plants often epiphytic,
small; stems monopodially branched; costa single, often slender;
laminal cells elongate, smooth; alar cells weakly differentiated;
capsules often erect; peristomes mostly variously reduced;
calyptrae rarely hairy.
Austinia Müll. Hal., Macgregorella E. B. Bartram, Merrilliobryum Broth.,
Myrinia Schimp., Nematocladia W. R. Buck
Fabroniaceae Schimp. Type: Fabronia Raddi. Plants epiphytic, often
small; stems monopodially branched, sometimes fragile; leaves
mostly acuminate; costa single, slender; laminal cells short,
smooth; alar cells mostly weakly differentiated; capsules typically
erect; peristome often reduced; exostome teeth often paired.
Dimerodontium Mitt., Fabronia Raddi, Ischyrodon Müll. Hal., Levierella
Müll. Hal., Rhizofabronia (Broth.) M. Fleisch.
Hypnaceae Schimp. Type: Hypnum Hedw. Stems monopodially
branched; pseudoparaphyllia foliose or rarely filamentous;
paraphyllia none; leaves often falcate or homomallous; costa
short and double (or absent); laminal cells mostly linear; capsules
mostly inclined and asymmetric; exothecial cells usually not
collenchymatous; opercula apiculate to short-rostrate; exostome
teeth mostly cross-striolate; calyptrae mostly naked.
Acritodon H. Rob., Andoa Ochyra, Bardunovia Ignatov & Ochyra,
Breidleria Loeske, Bryocrumia L. E. Anderson, Buckiella Ireland,
Callicladium H. A. Crum, Calliergonella Loeske, Campylophyllopsis
W. R. Buck nom. nov. (Campylidium (Kindb.) Ochyra, nom. inval.
[Art. 20.2], Biodiversity Poland 3: 182. 2003; Campylium [unranked]
Campylidium Kindb., Eur. N. Amer. Bryin. 2: 119. 1896),
Campylophyllum (Schimp.) M. Fleisch., Caribaeohypnum Ando &
Higuchi, Chryso-hypnum (Hampe) Hampe, Crepidophyllum Herzog,
119
120
B. Goffinet and others
Ctenidiadelphus M. Fleisch., Cyathothecium Dixon, Ectropotheciella M.
Fleisch., Ectropotheciopsis (Broth.) M. Fleisch., Ectropothecium Mitt.,
Elharveya H. A. Crum, Elmeriobryum Broth., Entodontella M. Fleisch.,
Eurohypnum Ando, Foreauella Dixon & P. de la Varde, Gammiella
Broth., Giraldiella Müll. Hal., Gollania Broth., Hageniella Broth.,
Herzogiella Broth., Homomallium (Schimp.) Loeske, Hondaella
Dixon & Sakurai, Horridohypnum W. R. Buck, Hyocomium Bruch &
Schimp., Hypnum Hedw., Irelandia W. R. Buck, Isopterygiopsis Z.
Iwats., Leiodontium Broth., Leptoischyrodon Dixon, Macrothamniella
M. Fleisch., Mahua W. R. Buck, Microctenidium M. Fleisch.,
Mittenothamnium Henn., Nanothecium Dixon & P. de la Varde,
Orthothecium Bruch & Schimp., Phyllodon Bruch & Schimp.,
Plagiotheciopsis Broth., Platydictya Berk., Platygyriella Cardot,
Podperaea Z. Iwats. & Glime, Pseudohypnella (M. Fleisch.) Broth.,
Pseudotaxiphyllum Z. Iwats., Ptilium De Not., Pylaisia Schimp.,
Rhacopilopsis Renauld & Cardot, Rhizohypnella M. Fleisch.,
Sclerohypnum Dixon, Stenotheciopsis Broth., Stereodon (Brid.) Mitt.,
Stereodontopsis R. S. Williams, Syringothecium Mitt., Taxiphyllopsis
Higuchi & Deguchi, Taxiphyllum M. Fleisch., Tripterocladium (Müll.
Hal.) A. Jaeger, Vesicularia (Müll. Hal.) Müll. Hal., Wijkiella Bizot &
Lewinsky
Catagoniaceae W. R. Buck & Ireland. Type: Catagonium Broth. Stems
monopodially branched; pseudoparaphyllia filamentous; leaves
conduplicate; costa short and double or absent; laminal cells
linear, smooth; alar cells not differentiated; exostome teeth crossstriolate.
Catagonium Broth.
Pterigynandraceae Schimp. Type: Pterigynandrum Hedw. Plants
terrestrial or epiphytic, mostly relatively small; stems
monopodially branched, mostly terete-foliate; paraphyllia absent;
costa short and double; laminal cells short, prorulose; alar cells
weakly differentiated; gemmae stem-borne; setae smooth;
capsules often erect; peristome often reduced.
Habrodon Schimp., Heterocladium Bruch & Schimp., Iwatsukiella W. R.
Buck & H. A. Crum, Myurella Bruch & Schimp., Pterigynandrum
Hedw., Trachyphyllum A. Gepp
Hylocomiaceae M. Fleisch. Type: Hylocomium Bruch & Schimp. Plants
mostly robust; stems monopodially or sympodially branched;
paraphyllia often present; leaves often strongly toothed; costae
often strong and double; laminal cells elongate, smooth or
2 Morphology and classification of Bryophyta
prorulose; alar cells weakly differentiated; setae very elongate;
capsules typically curved and asymmetric; exostome teeth yellowto red-brown, often with reticulate pattern.
Ctenidium (Schimp.) Mitt., Hylocomiastrum Broth., Hylocomium Bruch &
Schimp., Leptocladiella M. Fleisch., Leptohymenium Schwägr.,
Loeskeobryum Broth., Macrothamnium M. Fleisch., Meteoriella S.
Okamura, Neodolichomitra Nog., Orontobryum M. Fleisch., Pleurozium
Mitt., Puiggariopsis M. Menzel, Rhytidiadelphus (Limpr.) Warnst.,
Rhytidiopsis Broth., Schofieldiella W. R. Buck
Rhytidiaceae Broth. Type: Rhytidium (Sull.) Kindb. Plants robust;
stems monopodially branched; paraphyllia none; leaves plicate,
rugose; costa single; laminal cells linear, strongly porose,
prorulose; alar cells well differentiated; exostome teeth yellowbrown, cross-striolate.
Rhytidium (Sull.) Kindb.
Symphyodontaceae M. Fleisch. Type: Symphyodon Mont. Stems
monopodially branched; laminal cells mostly prorulose; alar cells
not or weakly differentiated; setae mostly roughened; capsules
symmetric, typically spinose; exostome teeth papillose to crossstriolate; calyptrae cucullate or mitrate.
Chaetomitriopsis M. Fleisch., Chaetomitrium Dozy & Molk.,
Dimorphocladon Dixon, Symphyodon Mont., Trachythecium M.
Fleisch., Unclejackia Ignatov, T. Kop. & D. Norris
Plagiotheciaceae (Broth.) M. Fleisch. Type: Plagiothecium Bruch &
Schimp. Plants terrestrial; stems monopodially branched, mostly
complanate-foliate; leaves decurrent; costa short and double or
absent; laminal cells elongate, often strongly chlorophyllose; alar
cells differentiated into the decurrencies; setae smooth; capsules
often curved and asymmetric; peristome teeth mostly pale yellow;
exostome typically cross-striolate below; endostome well
developed.
Plagiothecium Bruch & Schimp., Struckia Müll. Hal.
Entodontaceae Kindb. Type: Entodon Müll. Hal. Plants often
epiphytic; stems monopodially branched; costa short and double
or absent; laminal cells linear, smooth; alar cells subquadrate,
numerous; capsules erect and symmetric, long-exserted;
columella often exserted; peristome inserted below mouth of
capsule; endostome mostly strongly reduced.
Entodon Müll. Hal., Erythrodontium Hampe, Mesonodon Hampe,
Pylaisiobryum Broth.
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B. Goffinet and others
Pylaisiadelphaceae Goffinet & W. R. Buck. Type: Pylaisiadelpha
Cardot. Stems monopodially branched; leaves usually not falcate;
costa short and double or none; laminal cells mostly linear, mostly
smooth, sometimes papillose; alar cells quadrate, few; exothecial
cells not collenchymatous; opercula often straight-rostrate;
exostome teeth not furrowed.
Aptychella (Broth.) Herzog, Brotherella M. Fleisch., Clastobryopsis M.
Fleisch., Clastobryum Dozy & Molk., Heterophyllium (Schimp.)
Kindb., Isocladiella Dixon, Isopterygium Mitt., Mastopoma
Cardot, Platygyrium Bruch & Schimp., Pterogonidium Broth.,
Pseudotrismegistia H. Akiyama & Tsubota, Pylaisiadelpha Cardot,
Taxitheliella Dixon, Taxithelium Mitt., Trismegistia (Müll. Hal.) Müll.
Hal., Wijkia H. A. Crum
Sematophyllaceae Broth. Type: Sematophyllum Mitt. Stems
monopodially branched; leaves often golden green, often falcate;
costa short and double or none; laminal cells mostly linear, smooth
or papillose; alar cells well differentiated; exothecial cells
collenchymatous; opercula mostly obliquely rostrate; exostome
teeth often furrowed, cross-striolate.
Acanthorrhynchium M. Fleisch., Acroporium Mitt., Allionellopsis Ochyra,
Aptychopsis (Broth.) M. Fleisch., Chinostomum Müll. Hal., Clastobryella
M. Fleisch., Clastobryophilum M. Fleisch., Colobodontium Herzog,
Donnellia Austin, Hydropogon Brid., Hydropogonella Cardot,
Macrohymenium Müll. Hal., Meiotheciella B. C. Tan, W. B. Schofield &
H. P. Ramsay, Meiothecium Mitt., Papillidiopsis (Broth.) W. R. Buck &
B. C. Tan, Paranapiacabaea W. R. Buck & Vital, Potamium Mitt.,
Pterogoniopsis Müll. Hal., Piloecium (Müll. Hal.) Broth., Radulina W. R.
Buck & B. C. Tan, Rhaphidostichum M. Fleisch., Schraderella Müll. Hal.,
Schroeterella Herzog, Sematophyllum Mitt., Timotimius W. R. Buck,
Trichosteleum Mitt., Trolliella Herzog, Warburgiella Müll. Hal.
Cryphaeaceae Schimp. Type: Cryphaea D. Mohr. Stems sympodially
branched; secondary stems little or not branched; costa single;
laminal cells short, smooth or sometimes prorulose; alar cells
numerous; capsules immersed or seldom emergent; exostome teeth
pale, papillose; endostome rudimentary to absent; calyptrae mitrate.
Cryphaea D. Mohr, Cryphaeophilium M. Fleisch., Cryphidium (Mitt.) A.
Jaeger, Cyptodon (Broth.) M. Fleisch., Cyptodontopsis Dixon,
Dendroalsia E. Britton, Dendrocryphaea Broth., Dendropogonella E.
Britton, Pilotrichopsis Besch., Schoenobryum Dozy & Molk.,
Sphaerotheciella M. Fleisch.
2 Morphology and classification of Bryophyta
Prionodontaceae Broth. Type: Prionodon Müll. Hal. Plants epiphytic;
stems sympodially branched; axillary hairs as in Breutelia
(Bartramiaceae); leaves usually plicate and with strongly toothed
margins; costa single; laminal cells short, papillose; alar cells
differentiated in large areas; capsules immersed to emergent;
annulus revoluble; exostome teeth papillose; endostome
segments united into a reticulum.
Prionodon Müll. Hal.
Leucodontaceae Schimp. Type: Leucodon Schwägr. Plants mostly
epiphytic; stems sympodially branched; secondary stems often
not or little branched, mostly curled when dry; leaves rapidly
spreading when moist, mostly plicate; costa short and double or
none; laminal cells oval to linear, mostly smooth, rarely prorulose;
alar cells numerous; capsules usually exserted, often anisosporous;
annulus not differentiated; exostome teeth pale, papillose;
endostome mostly rudimentary; spores often large.
Antitrichia Brid., Dozya Sande Lac., Eoleucodon H. A. Mill. & H.
Whittier, Felipponea Broth., Leucodon Schwägr., Pterogonium Sw.,
Scabridens E. B. Bartram
Pterobryaceae Kindb. Type: Pterobryon Hornsch. Plants mostly
epiphytic; stems sympodially branched; secondary stems often
well branched, and thus stipitate; pseudoparaphyllia filamentous;
stem and branch leaves often differentiated, branch leaves
sometimes 5-seriate; costa mostly single, sometimes short and
double or absent; laminal cells mostly linear, mostly smooth,
sometimes prorulose; alar cells usually differentiated, often thickwalled and colored; capsules mostly immersed; exostome teeth
pale, often smooth; endostome most rudimentary; calyptrae
cucullate or mitrate, often hairy.
Calyptothecium Mitt., Cryptogonium (Müll. Hal.) Hampe, Henicodium (Müll.
Hal.) Kindb., Hildebrandtiella Müll. Hal., Horikawaea Nog., Jaegerina
Müll. Hal., Micralsopsis W. R. Buck, Muellerobryum M. Fleisch.,
Neolindbergia M. Fleisch., Orthorrhynchidium Renauld & Cardot,
Orthostichidium Dusén, Orthostichopsis Broth., Osterwaldiella Broth.,
Penzigiella M. Fleisch., Pireella Cardot, Pseudopterobryum Broth.,
Pterobryidium Broth. & Watts, Pterobryon Hornsch., Pterobryopsis
M. Fleisch., Renauldia Müll. Hal., Rhabdodontium Broth., Spriridentopsis
Broth., Symphysodon Dozy & Molk., Symphysodontella M. Fleisch.
Phyllogoniaceae Kindb. Type: Phyllogonium Brid. Plants epiphytic;
stems sympodially branched; secondary stems irregularly
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B. Goffinet and others
branched, strongly complanate-foliate; leaves conduplicate,
cucullate, auriculate; costa short and double or absent; laminal
cells linear, smooth; alar cells differentiated in small groups;
capsules immersed or shortly exserted; exostome teeth pale, not
or scarcely ornamented; endostome rudimentary or absent;
calyptrae cucullate or mitrate, naked or hairy.
Phyllogonium Brid.
Orthorrhynchiaceae S. H. Lin. Type: Orthorrhynchium Reichardt.
Plants terrestrial; stems monopodially branched; leaves
conduplicate, cucullate; costa short and double or absent; laminal
cells linear, smooth; alar cells undifferentiated; capsules shortexserted, erect; exostome teeth pale, unornamented; endostome
none; calyptrae mitrate, hairy.
Orthorrhynchium Reichardt
Lepyrodontaceae Broth. Type: Lepyrodon Hampe. Plants terrestrial
or epiphytic; stems sympodially branched; secondary stems not or
little branched; leaves sometimes plicate; costa single and weak or
short and double to absent; laminal cells linear, smooth, thickwalled and porose; alar cells few or scarcely differentiated;
capsules long-exserted; peristome usually only endostomial.
Lepyrodon Hampe
Neckeraceae Schimp. Type: Neckera Hedw. Plants terrestrial or
epiphytic; stems mostly sympodially branched, sometimes
monopodial; stipes sometimes differentiated and plants then
frondose; leaves mostly complanately arranged; costa typically
single, sometimes short and double; laminal cells fusiform to
linear, rarely shorter, mostly smooth, rarely prorulose or
papillose; alar cells mostly few or weakly differentiated; capsules
immersed (mostly in epiphytes) to long-exserted (mostly in
terrestrial taxa); exostome teeth often pale, usually cross-striolate
at least at extreme base, papillose above; endostome often reduced;
calyptrae mostly cucullate.
Baldwiniella M. Fleisch., Bissetia Broth., Bryolawtonia D. H. Norris &
Enroth, Caduciella Enroth, Crassiphyllum Ochyra, Cryptoleptodon
Renauld & Cardot, Curvicladium Enroth, Dixonia Horik. & Ando,
Dolichomitra Broth., Handeliobryum Broth., Himantocladium (Mitt.)
M. Fleisch., Homalia (Brid.) Bruch & Schimp., Homaliadelphus
Dixon & P. de la Varde, Homaliodendron M. Fleisch., Hydrocryphaea
Dixon, Isodrepanium (Mitt.) E. Britton, Metaneckera Steere, Neckera
Hedw., Neckeropsis Reichardt, Neomacounia Ireland, Noguchiodendron
2 Morphology and classification of Bryophyta
Ninh & Pócs, Pendulothecium Enroth & S. He, Pinnatella M. Fleisch.,
Porotrichodendron M. Fleisch., Porotrichopsis Broth. & Herzog,
Porotrichum (Brid.) Hampe, Thamnobryum Nieuwl., Touwia Ochyra
Echinodiaceae Broth. Type: Echinodium Jur. Plants epipetric or less
often on soil or bases of trees; stems sympodially branched, wiry;
secondary stems irregularly branched; leaves mostly subulate;
costa single, mostly excurrent; laminal cells short, smooth; alar
cells weakly differentiated; capsules long-exserted, inclined to
horizontal; exostome teeth reddish, cross-striolate; endostome
well developed.
Echinodium Jur.
Leptodontaceae Schimp. Type: Leptodon D. Mohr. Plants mostly
epiphytic; stems sympodially branched, often curled when dry;
secondary stems irregularly branched to bipinnate; costa typically
single; laminal cells isodiametric to long-hexagonal, smooth,
unipapillose or prorulose; alar cells numerous; capsules
immersed to short-exserted; exostome teeth pale, unornamented
to spiculose; endostome rudimentary; calyptrae hairy.
Alsia Sull., Forsstroemia Lindb., Leptodon D. Mohr, Taiwanobryum Nog.
Lembophyllaceae Broth. Type: Lembophyllum Lindb. Plants often
turgid; stems monopodially branched; leaves mostly strongly
concave; costa mostly short and double (rarely single); laminal
cells elongate, smooth; alar cells often somewhat differentiated;
capsules mostly erect and immersed to short-exserted; endostome
mostly reduced; calyptrae rarely mitrate, naked or hairy.
Acrocladium Mitt., Bestia Broth., Camptochaete Reichardt,
Dolichomitriopsis S. Okamura, Fallaciella H. A. Crum, Fifea H. A.
Crum, Isothecium Brid., Lembophyllum Lindb., Neobarbella Nog.,
Orthostichella Müll. Hal., Pilotrichella (Müll. Hal.) Besch.,
Weymouthia Broth.
Myuriaceae M. Fleisch. Type: Myurium Schimp. Stems sympodially
branched; secondary stems little or not branched; leaves mostly
long-acuminate; costa short and double or none; laminal cells
linear, smooth; alar cells well differentiated, mostly colored;
capsules long-exserted, erect; exostome teeth reduced, smooth,
often perforate; endostome rudimentary.
Eumyurium Nog., Myurium Schimp., Oedicladium Mitt., Palisadula
Toyama
Anomodontaceae Kindb. Type: Anomodon Hook. & Taylor. Plants
mostly epiphytic; stems sympodially or monopodially branched,
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B. Goffinet and others
secondary stems and/or branches often curled when dry, not
complanate-foliate; paraphyllia none; leaves often acute to
obtuse; costa single or short and double; laminal cells mostly
short, papillose or prorulose; alar cells mostly poorly
differentiated; capsules exserted, erect; exostome teeth pale to
white, cross-striolate sometimes with overlying papillae to
papillose; endostome often reduced.
Anomodon Hook. & Taylor, Bryonorrisia L. R. Stark & W. R. Buck,
Chileobryon Enroth, Curviramea H. A. Crum, Haplohymenium Dozy
& Molk., Herpetineuron (Müll. Hal.) Cardot, Schwetschkeopsis Broth.
Theliaceae M. Fleisch. Type: Thelia Sull. Plants terrestrial or on bases
of trees; stems monopodially branched; paraphyllia present; leaves
imbricate, little altered when moist, deltoid-ovate; costa single;
laminal cells short, stoutly unipapillose; alar cells differentiated;
capsules exserted, erect; exostome teeth white, smooth to
papillose; endostome strongly reduced.
Thelia Sull.
Microtheciellaceae H. A. Mill. & A. J. Harr. Type: Microtheciella Dixon.
Plants epiphytic; stems monopodially branched; costa single;
laminal cells short, smooth; alar cells weakly differentiated;,
capsules short-exserted, erect; exostome teeth truncate, reduced,
weakly ornamented; endostome rudimentary.
Microtheciella Dixon
Sorapillaceae M. Fleisch. Type: Sorapilla Spruce & Mitt. Leaves
distichous and complanate; capsules cladocarpous, immersed;
peristome double, of 16 slender segments and 32 stout exostome
knobs, cilia absent.
Sorapilla Spruce & Mitt.
Acknowledgments
The National Science Foundation is acknowledged for its financial
support to A. J. Shaw through grant DEB-0529593.
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Zielinski, F. (1909). Beiträge zur Biologie des Archegoniums und der Haube der
Laubmoose. Flora, 100, 1–36.
3
New insights into morphology,
anatomy, and systematics
of hornworts
k a r e n s . re n z a g l i a , j u a n c . v i l la rr e a l a n d
r. joel duff
3.1
Introduction
Hornworts are a key lineage in unraveling the early diversification of land
plants. An emerging, albeit surprising, consensus based on recent molecular
phylogenies is that hornworts are the closest extant relatives of tracheophytes
(Qiu et al. 2006). Prior to comprehensive molecular analyses, discrepant hypotheses positioned hornworts as either sister to all embryophytes except liverworts or
the closest living relatives of green algae (Mishler et al. 1994, Qiu et al. 1998,
Goffinet 2000, Renzaglia & Vaughn 2000). Morphological features are of little
value in resolving the placement of hornworts within the green tree of life because
this homogeneous group of approximately 150 species exhibits numerous developmental and structural peculiarities not found in any extant or fossil archegoniate. Until recently, hornworts were neglected at every level of study and thus even
the diversity and the relationships within this group have remained obscure.
Virtually every aspect of hornwort evolution has been challenged and/or revised
since the publication of the first edition of this book (Duff et al. 2004, 2007, Shaw &
Renzaglia 2004, Cargill et al. 2005, Renzaglia et al. 2007). Phylogenetic hypotheses
based on multigene sequences have revolutionized our concepts of interrelationships. New classification schemes have arisen from these analyses and continue to
be fine-tuned as more taxa are sampled. Three new genera have been named,
increasing the number of hornwort genera to 14, namely Leiosporoceros, Anthoceros,
Sphaerosporoceros, Folioceros, Hattorioceros, Mesoceros, Paraphymatoceros, Notothylas,
Phaeoceros, Phymatoceros, Phaeomegaceros, Megaceros, Dendroceros, and Nothoceros (Duff
et al. 2007, Stotler et al. 2005). Developmental and ultrastructural studies have
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
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K. S. Renzaglia and others
extended the morphological boundaries in the group and have revealed parallelisms and reversals in characters previously viewed as taxonomically informative.
Coupled with robust molecular phylogenies, the newly acquired morphological
data have provided a clearer picture of character transformations within the group.
The focus of this chapter is to synthesize and interweave newly gained insights
on hornwort structure, phylogeny, and classification. We present a molecular
phylogeny that provides the basis for the revised classification included herein.
Classical morphological information is updated with more comprehensive studies of ultrastructure and development across a wide sampling of hornworts. We
conclude with a brief discussion of inferences on the evolution of diagnostic
hornwort characters, namely chloroplasts, stomata, antheridia, and spores.
3.2
Phylogeny
The past five years have witnessed both the advent and wide application of
molecular systematic tools toward the development of a phylogeny and classification of hornworts. The first studies by Stech et al. (2003) and Duff et al. (2004)
reported sequence-based phylogenies based on trnL–trnF and rbcL regions of the
chloroplast genome, respectively. Though limited in taxon sampling, these studies
revealed new and startling relationships among hornwort taxa. Duff et al. (2007)
reported a more comprehensive molecular phylogeny utilizing three genes, one
each from the nuclear, mitochondrial, and plastid genomes, and up to 62 hornwort
samples, representing 12 of the 14 genera and one third of the recognized species.
The results of this study are summarized in the phylogeny presented in Fig. 3.1.
Several major features of hornwort relationships are well supported both by
these molecular phylogenies and through subsequent detailed morphological and
ultrastructural analyses. The salient features are: (1) there is significant genetic
distance between three lineages of hornworts: Leiosporoceros, Anthoceros s. lat., and
the remaining hornworts; (2) taxa formerly recognized as belonging to Phaeoceros
are polyphyletic and consequently, three new genera were segregated from this
genus: Phymatoceros (Stotler et al. 2005), Paraphymatoceros (Hässel de Menéndez
2006), and Phaeomegaceros (Duff et al. 2007); (3) American species of Megaceros plus
Nothoceros form a monophyletic clade sister to the Paleotropical Megaceros and
Dendroceros, suggesting a new generic status to this Nothoceros/American Megaceros
alliance; and (4) a sister relationship exists between Phaeoceros s. str. and Notothylas.
3.3
Classification
The classification scheme presented in Table 3.1 is based on the most
current molecular data. There are few congruencies with any of the four
3 Morphology and systematics of hornworts
Fig. 3.1. Phylogenetic reconstruction of hornworts based on Bayesian analyses of three
genomic regions; nuclear 18S, chloroplast rbcL, and mitochondrial nad5 (modified from Duff et al.
2007). Values on top of branches are Bayesian posterior probabilities and below branches are
parsimony non-parametric bootstrap values. Hornwort clades discussed in the text are labeled
A–E and represent the orders: A, Leiosporocerotales; B, Anthocerotales; C, Notothyladales; D,
Phymatocerotales; E, Dendrocerotales.
classification schemes based on morphology that were highlighted in the first
edition of this chapter (Schuster 1987, Hässel de Menéndez 1988, Hyvönen &
Piippo 1993, Hasegawa 1994, Duff et al. 2007). One has only to look at the
number and placement of genera in the revised classification scheme presented
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K. S. Renzaglia and others
Table 3.1 General classification of hornworts
PHYLUM ANTHOCEROTOPHYTA rothm. ex Stotler & Crand.-Stotler
CLASS LEIOSPOROCEROTOPSIDA Stotler & Crand.-Stotler emend. Duff et al.
Order Leiosporocerotales Hässel
Family Leiosporocerotaceae Hässel
Leiosporoceros Hässel: Thalli typically solid, but with schizogenous cavities in older thalli;
mucilage clefts absent in Nostoc-infected tissues, present in young uninfected plants. Nostoc
colonies in longitudinally oriented strands in mucilage-filled schizogenous canals.
Chloroplasts 1 per cell without pyrenoid. Antheridia numerous (to 80 per chamber) with
tiered jacket cell arrangement. Capsules with stomata. Massive sporogenous tissue (6–9
layers). Spore tetrads bilateral alterno-opposite. Spores yellow, minute, ovoid, nearly smooth;
Y-shaped to monolete mark present. Pseudoelaters usually unicellular, thick-walled.
CLASS ANTHOCEROTOPSIDA de bary ex Jancz. corr. Prosk.
S U B C L A S S A N T H O C E R O T I D A E Rosenv. corr. Prosk.
Order Anthocerotales Limpr. in Cohn
Family Anthocerotaceae (Gray) Dumort. corr. Trevis. emend. Hässel
Anthoceros L.: Thalli and involucres with mucilage-containing schizogenous cavities.
Chloroplasts 1 (–4) per cell with pyrenoid (A. punctatus) or starch-free area (A. fusiformis).
Antheridia numerous (to 45) per chamber with tiered jacket cell arrangement. Capsules with
stomata. Spores smoky gray, dark brown to blackish with a defined trilete mark;
ornamentation spinose, punctate, baculate, or lamellate. Pseudoelaters thin-walled.
Folioceros D. C. Bharadwaj: Thalli and involucres with mucilage-containing schizogenous
cavities. Chloroplasts 1 (–2) per cell with a pyrenoid (F. fuciformis) or absent (F. assamicus).
Antheridia numerous (to 60) per chamber with tiered jacket cell arrangement. Capsules with
stomata, except F. incurvus. Spores smoky gray, brown to blackish without a defined trilete
mark; ornamentation spinose, reticulate, mamillose, or lamellate. Pseudoelaters elongated
strongly, thick-walled.
Sphaerosporoceros Hässel: Thalli and involucres with mucilage-containing schizogenous
cavities. Chloroplasts 1 per cell with a pyrenoid. Capsules with stomata. Spores dark brown to
blackish with a reduced defined trilete mark; ornamentation connate-cristate with ridges to
short blunt-spines. Pseudoelaters quadrate–subglobose to cylindrical cells, thin-walled with
faint thickenings.
S U B C L A S S N O T O T H Y L A T I D A E Duff et al.
Order Notothyladales Hyvönen & Piippo
Family Notothyladaceae (Milde) Müll. Frib. ex Prosk.
Subfamily Notothyladoideae Grolle
Notothylas Sull. ex A. Gray: Thalli solid. Chloroplasts 1 (–3) per cell with a pyrenoid (N. orbicularis)
or absent (N. nepalensis). Antheridia 2–4 (–6) per chamber usually with non-tiered jacket cell
arrangement. Sporophytes short, lying horizontally in the thallus, mostly or totally enclosed
within the involucre. Stomata absent. Suture elaborate, rudimentary, or absent. Columella
present (N. dissecta) or absent (N. javanica). Spores yellow to blackish with an equatorial girdle;
ornamentation finely vermiculate, granulose to tuberculate. Pseudoelaters absent to subquadrate–elongated with or without annular thickenings.
Subfamily Phaeocerotoideae Hässel
3 Morphology and systematics of hornworts
Table 3.1 (cont.)
Phaeoceros Prosk.: Thalli solid. Marginal or short ventral tubers present or absent. Chloroplasts
1 (–2) per cell with pyrenoid present (P. laevis) or absent (P. pearsonii). Antheridia (1–) 2–6 (–8)
per chamber with non-tiered jacket cell arrangement. Stomata present. Spores yellow to
brownish when completely mature, with equatorial girdle; ornamentation spinose
(P. laevis–carolinianus group) to distally covered by rounded protuberances (P. himalayensis).
Pseudoelaters thin-walled.
Paraphymatoceros Hässel: Thalli solid. Apical flattened and disk-shaped tubers. Chloroplasts
1 (–2) per cell, without pyrenoid. Antheridia 2–5 per chamber with non-tiered jacket cell
arrangement. Stomata present. Spores yellow to blackish-brownish when completely
mature, with equatorial girdle; ornamentation of rounded protuberances in distal face.
Pseudoelaters mostly unicellular (P. hallii), 4-celled in the other taxa (disintegrating in
P. diadematus).
Hattorioceros (J. Haseg.) J. Haseg.: Thalli solid. Chloroplast and antheridium morphology
unknown. Stomata present. Spores yellow to brownish. Spores small (usually less than 20 mm)
without a triradiate mark, variable in shape, mostly ovoidal; ornamentation surface deeply
canaliculate–striate. Pseudoelaters unevenly thick-walled.
Mesoceros Piippo: Thalli solid. Chloroplast morphology unknown. Antheridia 2–3 per chamber
with a non-tiered jacket cell arrangement. Spores dark brown; ornamentation papillate to
connate with reticulate ridges. Pseudoelaters thin-walled with faint thickenings.
S U B C L A S S D E N D R O C E R O T I D A E Duff et al.
Order Phymatocerales Duff et al.
Family Phymatocerotaceae Duff et al.
Phymatoceros Stotler et al. emend. Duff et al.: Thalli solid. Long-stalked ventral tubers.
Chloroplasts 1 (–2) per cell with a pyrenoid (P. bulbiculosus) or absent (P. phymatodes). Antheridia
1–3 (–4) per chamber with non-tiered jacket cell arrangement (Schiffner 1937). Stomata
present. Spores yellow to brownish when completely mature, with equatorial girdle;
ornamentation finely vermiculate with a distal protuberance, distal spore ornamentation
obscured by late spore wall deposition. Pseudoelaters thin-walled.
Order Dendrocerotales Hässel emend. Duff et al.
Family Dendrocerotaceae (Milde) Hässel
Subfamily Dendrocerotoideae R. M. Schust.
Dendroceros Nees: Epiphytic and epiphyllic. Thalli solid (subg. Dendroceros) or with mucilagecontaining schizogenous cavities (subg. Apoceros), involucres solid in both subgenera. Thalli
with a conspicuous midrib and perforated wings. Nostoc present as bulging globose colonies
in the ventral and dorsal side of the thallus. Band or pit-field-like thickenings present in the
thallus cell walls. Chloroplasts 1 per cell with a conspicuous pyrenoid with spherical
inclusions. Antheridia 1 per chamber with a non-tiered jacket cell arrangement. Stomata
absent. Spores multicellular owing to endosporic germination, colorless to pale yellow,
appearing green in live spores owing to large chloroplasts and thin exine; ornamentation
papillose to shortly tuberculate. Pseudoelaters with helical thickenings.
Megaceros Campb.: Thalli solid. Band or pit-field-like thickenings present in the thallus cell
walls. Chloroplasts 1–8 (–12) per cell without pyrenoid. Antheridia 1 (–2) per chamber with
non-tiered jacket cell arrangement. Stomata absent. Spores colorless to pale yellow,
appearing green in live spores due to large chloroplasts and thin exine; ornamentation
mamillose and/or tuberculate. Pseudoelaters with helical thickenings.
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Table 3.1 (cont.)
Nothoceros (R. M. Schust.) J. Haseg.: Thalli solid, in rosette or pinnately branched with thin (less
than 1 mm) branches resembling Riccardia or with a conspicuous midrib and imperforated
wings. Band or pit-field-like thickenings present in the thallus cell walls. Chloroplasts 1–2 (–8)
per cell. Pyrenoid absent (N. endiviaefolius) or present (M. vincentianus). Antheridia 1 (–2) per
chamber with a non-tiered jacket cell arrangement. Stomata absent. Spores colorless to pale
yellow, appearing green in live spores owing to large chloroplasts and thin exine;
ornamentation mammillose and/or tuberculate, similar to that of Megaceros. Pseudoelaters
with helical thickenings.
Subfamily Phaeomegacerotoideae Duff et al.
Phaeomegaceros Duff et al.: Thalli solid. Band or pit-field-like thickenings present in the thallus
cell walls. Chloroplasts 1–2 per cell without a pyrenoid. Antheridia 1 (–rarely 8) per chamber
with a non-tiered antheridial jacket cell arrangement. Stomata present. Spores yellow to
brownish when completely mature, with equatorial girdle; ornamentation finely
vermiculate with distal dimples. Pseudoelaters thin-walled to unevenly thick-walled.
Source: Based on Duff et al. (2007).
herein to understand the magnitude of change that has occurred in the past six
years in regards to hornwort systematics. Hornworts are now accommodated in
14 genera compared with the previously widely recognized six, which were
Anthoceros, Phaeoceros, Folioceros, Notothylas, Megaceros, and Dendroceros.
The sister relationship between Leiosporoceros and the remaining hornworts is
reflected in the erection of a separate class, Leiosporocerotopsida, for this
monospecific genus (Frey & Stech 2005, Stotler & Crandall-Stotler 2005). The
Anthocerotopsida contains the remaining taxa and is divided into three subclasses: Anthocerotidae, Notothylatidae, and Dendrocerotidae. Within the
Anthocerotidae, three morphologically similar genera, Anthoceros, Sphaerosporoceros, and Folioceros, are placed together in a single family and order. The
Notothyladales comprises a single family and composes the only order of
the Notothylatidae. The subfamily Notothyladoideae contains a single genus,
while the remaining four genera, two of which have not yet been sampled
for molecular analyses (Mesoceros and Hattorioceros), are accommodated in
the Phaeocerotoideae. Sampling of Paraphymatoceros in our molecular analyses is restricted to one species, P. hallii. Analyses of rbcL sequences place
Phaeoceros pearsonii sister to P. hallii and thus support transfer of P. pearsonii to
this newly transcribed genus. The subclass Dendrocerotidae includes two
genetically and morphologically distant orders: the monospecific Phymatocerales and the Dendrocerotales with four genera in a single family and two
subfamilies.
3 Morphology and systematics of hornworts
3.4
Anatomy and development
The uniformity and uniqueness of morphological features within hornworts has been recognized for over a century (Campbell 1895, Goebel 1905, Bower
1935). Peculiarities in the structure and development of the sporophyte, chloroplasts, gametangia, and Nostoc colonies, among other traits, distinguish this small
assemblage of bryophytes from all other land plants (Campbell 1895, Bartlett
1928, Renzaglia 1978, Renzaglia & Vaughn 2000). Based on the leafless habit of
the gametophyte, hornworts were traditionally included within liverworts and
were viewed as having an affinity with simple thalloids. With phylogenetic reconstructions pointing to a sister relationship between hornworts and tracheophytes,
a thorough reappraisal of morphological transformations across cryptogams in
both generations is warranted. This is beyond the scope of this chapter, and hence
we consider here only the diversity and evolution of morphological features from
the cell to the organ level within hornworts. This new synthesis is particularly
timely owing to the recent contribution of significant new morphological knowledge across hornworts, especially within obscure tropical taxa (Villarreal &
Renzaglia 2006a, b, Duff et al. 2007, Renzaglia et al. 2007). The recent morphological studies, in turn, were prompted by the surprising phylogenetic conclusions
that emerged from molecular analyses focused solely on hornworts.
The vegetative gametophyte of hornworts is a flattened thallus, with or
without a thickened midrib (Fig. 3.2A, B). Growing regions that contain solitary
apical cells and immediate derivatives are located in thallus notches and are
covered by mucilage that is secreted by epidermal cells (Fig. 3.2C, D). The apical
cell and immediate derivatives contain well-developed chloroplasts that are
intimately associated with the nucleus (Fig. 3.2C). Growth forms are correlated
with apical cell geometry. The wedge-shaped apical cell of most taxa segments
along four cutting faces: two lateral, one dorsal, and one ventral (Fig. 3.2E). The
resulting growth forms tend to be orbicular and the thallus in cross-section
gradually narrows from the center to lateral margins. In comparison, the hemidiscoid apical cell (Fig. 3.2D, F) of Dendroceros cuts along two lateral and one basal
face and is responsible for producing a ribbon-shaped thallus with an enlarged
midrib and monostromatic wings (Fig. 3.2B). A parallelism in this general habit
is found in some Nothoceros, where the large thallus develops from a wedgeshaped apical cell but has a prominent midrib that tapers laterally to fragile
wings (Duff et al. 2007, Villarreal et al. 2007). Aside from anthocerotes, wedgeshaped apical cells occur only in thalloid liverworts and some pteridophyte
gametophytes (Crandall-Stotler 1980, Shaw & Renzaglia 2004). Hemidiscoid
apical cells are rare and known only from Dendroceros and a few simple thalloid
liverworts (Renzaglia 1982).
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A
D
E
F
C
Fig. 3.2. (A) Leiosporoceros dussii. Light micrograph (LM) of female gametophyte with two
mature sporophytes (S) and overlying male plant with abundant antheridial chambers (An)
and longitudinal Nostoc canals (Ns). Bar ¼ 1.0 mm. (B) Dendroceros tubercularis. Scanning
electron micrograph (SEM) of ventral thallus showing swollen central midrib and
monostromatic wings. Pore-like mucilage clefts (C) occur in two irregular rows on either side
of the midrib and a tuft of rhizoids (R) is positioned below the terminal bifurcation.
Bar ¼ 0.25 mm. (C) Phaeoceros carolinianus. Transmission electron microscope (TEM) horizontal
longitudinal section of growing notch overarched by mucilage (M). The rectangular apical cell
(AC) and surrounding derivatives are highly vacuolated and contain a nucleus (N) associated
with a well-developed chloroplast (P) containing a pyrenoid. Bar ¼ 4.0 mm. (D) Dendroceros
3 Morphology and systematics of hornworts
At the cellular level, hornworts are known to contain solitary chloroplasts
with central pyrenoids (or starch-free areas) and channel thylakoids, features
shared with algae but found in no other land plants (Duckett & Renzaglia 1988,
Vaughn et al. 1992) (Fig. 3.3A–D). Recent comparative studies, however, have
revealed remarkable variability in chloroplast shape, number, and especially
ultrastructure in hornworts (Duff et al. 2007, Renzaglia et al. 2007) (Fig. 3.3). For
example, Leiosporoceros has plastids that lack a pyrenoid but often contain a
central aggregation of large grana surrounded by starch (Fig. 3.3F). Channel
thylakoids are abundant in these chloroplasts.
The classical hornwort pyrenoid is traversed by thylakoids, which separate
lens-shaped to elongated subunits giving the appearance of ‘‘multiple pyrenoids’’ (Fig. 3.3A, B). The shape of pyrenoid subunits and the existence or
location of pyrenoid inclusions have been considered to be of taxonomic
value. For example, chloroplast structure in Dendroceros deviates from that of
the typical hornworts in that the pyrenoid is spherical and contains irregularly
shaped subunits with regularly spaced electron-opaque inclusions (Fig. 3.3G).
Chloroplasts of Megaceros lack pyrenoids and may number as many as 14 per
internal thallus cell (Fig. 3.3E) (Burr 1969). RUBISCO localizations in the pyrenoids and lack of grana end membranes (Fig. 3.3G) that characterize land plants
may be viewed as plesiomorphies and suggest ties with charophytes (Vaughn
et al. 1990, 1992). As in other land plants, RUBISCO is scattered among starch
grains in the chloroplast stroma of Megaceros.
Cell division in all hornworts is monoplastidic and involves plastic division and
morphogenetic migration that is tightly linked with nuclear division (Brown &
Lemmon 1990, 1993). Spindle microtubules originate from an aggregation of
electron-dense material at the poles, suggesting the vestige of algal-like centriolar
centrosomes (Vaughn & Harper 1998). Further investigations into cell cycle and
cytoskeletal proteins are required to clarify any homologies of this structure to the
polar bodies of liverworts and to centrosomes of other eukaryotes.
Caption for Fig. 3.2. (cont.)
cavernosus. LM vertical longitudinal section of apical region. A hemidiscoid apical cell (AC) is
overarched by mucilage. Bar ¼ 0.5 mm. (E) Wedge-shaped apical cell characteristic of most
hornworts. Two triangular lateral cutting-faces, one rectangular dorsal cutting face, and one
rectangular ventral cutting face produce a total of four derivatives in spiraled rotation.
Modified from Renzaglia (1978). (F) Hemisdiscoid apical cell of Dendroceros with two
semicircular lateral cutting faces and a single rectangular basal cutting face. Modified from
Renzaglia (1978).
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B
A
C
D
E
F
G
Fig. 3.3. (A) Anthoceros agrestis. LM of upper epidermis of gametophyte, each cell contains
single plastid with central pyrenoid (Py). Bar ¼ 10 mm. (B) Folioceros fuciformis. TEM of
pyrenoid (Py) consisting of lens-shaped subunits delimited by thylakoids (Th) and scattered
pyrenoglobuli (Pg). Starch (St) surrounds the pyrenoid and narrow grana traverse the plastid.
Bar ¼ 0.5 mm. (C) Megaceros cf. vincentianus. LM of upper epidermal cells of gametophyte, each
with single spherical to lens-shaped plastid containing a modified central pyrenoid (Py) with
abundant starch granules. Bar ¼10 mm. (D) Anthoceros angustus. TEM of chloroplast from thallus
3 Morphology and systematics of hornworts
The thickened thallus of the hornwort gametophyte lacks internal differentiation (Fig. 3.4A), except for the occurrence of rather extensive schizogenous
mucilage canals in species of Anthocerotaceae (Fig. 3.4B) and Dendroceros (subgenus Apoceros). In some taxa, especially Megaceros, epidermal cells are smaller
than in internal parenchyma cells (Fig. 3.4A). Unlike the sporophyte epidermis,
all epidermal cells of the gametophyte contain chloroplasts (Fig. 3.4A, B, D).
Mucilage-filled cells are abundant and scattered among photosynthetic parenchyma in most taxa (Fig. 3.4A). Band-like wall thickenings (Fig. 3.4C) and
primary pit fields may occur in cells of the thallus that subtend archegonia
and later the sporophyte foot (Leitgeb 1879, Proskauer 1960, Renzaglia 1978).
Ultrastructural observations of the cells will enable an evaluation of the potential role in food transport. Vesicular–arbuscular endomycorrhizas are common
in internal thallus cells of most taxa, and swollen, terminal tubers characterize
some genera and species (Fig. 3.4E) (see below) (Renzaglia 1978, Ligrone 1988).
Rhizoids are unicellular, smooth and may have branched tips (Hasegawa 1983).
They are typically ventral in position and may develop from the outer cell
derived from a periclinal division of an epidermal cell.
A distinctive feature of anthocerotes is the occurrence of apically derived
mucilage clefts, primarily on the ventral thallus (Figs. 3.2B, 3.4D). Two cells that
resemble stomatal guard cells surround a pore, which lacks the ability to close
and open. Although considered by some to be homologous to the stomata in the
sporophyte (Schuster 1992), this interpretation is dubious due to the function of
these mucilage clefts as the site of entry for Nostoc, the colonial endosymbiont
that is found in all hornworts. In most species, clefts are regularly produced
from apical derivatives and each may attract the phycobiont. Once in the
mucilage-filled internal chamber, the Nostoc increases in size and forms a
Caption for Fig. 3.3. (cont.)
epidermis. The modified pyrenoid (‘‘starch-free area’’) is less dense than in other taxa
and contains large subunits delimited by thylakoids. Abundant small pyrenoglobuli (Pg) line
thylakoids and are scattered within the pyrenoid. Starch grains (St). Bar ¼ 1.0 mm. (E) Megaceros
aenigmaticus. LM of internal cells of thallus with seven starch-filled plastids that lack
pyrenoids; the plastids on the right may be preparing for division. Bar ¼ 10 mm. (F)
Leiosporoceros dussii. TEM of chloroplast without a pyrenoid from thallus epidermis.
Numerous channel thylakoids (Ch) run perpendicular to the main axis and interconnect
short grana (G). Nucleus (N). Bar ¼ 1.0 mm. (G) Dendroceros tubercularis. TEM of spherical
pyrenoid (Py) with irregularly shaped subunits containing uniform electron-dense inclusions.
Thylakoids, including grana, interrupt the pyrenoid. Grana (G) lack end membranes.
Bar ¼ 5.0 mm.
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A
B
C
D
E
Fig. 3.4. (A) Megaceros aenigmaticus. LM transverse section of undifferentiated, simple
thallus. Epidermal cells are smaller than internal cells, of which one is mucilage-filled (M).
Bar ¼ 25 mm. (B) Anthoceros punctatus. LM transverse section of gametophyte with
numerous mucilage-containing schizogenous cavities near upper epidermis. Bar ¼ 25 mm.
(C) Nothoceros giganteus. SEM of internal gametophyte cell with band-like thickenings in
cell wall as also occurs in Megaceros, Phaeomegaceros and Dendroceros. Bar ¼15 mm.
(D) Megaceros aenigmaticus. LM surface view of mucilage cleft in ventral epidermis of
gametophyte. Both cleft cells contain recently divided plastids. Bar ¼10 mm.
(E) Phymatoceros phymatodes. LM longitudinal section of ventral spherical tuber,
consisting of small oil-rich cells surrounded by 3–4 layers of cells. The tuber stalk
(Sk) is 13–18 cells wide. Bar ¼100 mm.
discrete spherical colony (Fig. 3.5A). Thallus outgrowths penetrate the algal
colony (Fig. 3.5B). In Leiosporoceros, clefts are produced only in the sporeling;
Nostoc enters and forms an intimate association directly behind the apical cell
(Fig. 3.5C–E) (Villarreal & Renzaglia 2006a). As the thallus elongates through
apical segmentation, so too does the Nostoc colony within an advancing narrow
schizogenous canal (Fig. 3.5D, E). Unknown elsewhere in plants, these branching Nostoc canals run through the central thallus (Fig. 3.5C) and are visible to the
naked eye as dark green strands.
3 Morphology and systematics of hornworts
B
A
C
D
E
Fig. 3.5. (A) Phymatoceros bulbiculosus. LM transverse section of a mature thallus with
embedded ventral cyanobacterium colony (Cy). Thallus cells (clear areas) interdigitate with
and traverse Nostoc filaments. Bar ¼ 100 mm. (B) Phaeoceros carolinianus. LM section through
Nostoc colony. Thallus cells (T) penetrate the colony and are interspersed amongst small,
spherical cells of cyanobacterium (Cy). Bar ¼ 20 mm. (C) Leiosporoceros dussii. LM transverse
section of a mature thallus with two central Nostoc canals (Ns) and scattered mucilage cells
(M). Bar ¼ 100 mm. (D) Leiosporoceros dussii. LM vertical longitudinal section of apical region
showing schizogenous origin of Nostoc canal (Ns) between ventral and dorsal derivatives
from the wedge-shaped apical cell (A). Bar ¼ 15.0 mm. (E) Leiosporoceros dussii. Vertical
longitudinal section of female plant showing central Nostoc canal (Ns) that originates
behind the wedge-shaped apical cell (A) between ventral and dorsal derivatives.
Bar ¼ 100 mm.
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As in most bryophytes, asexual reproduction is widespread in anthocerotes.
Indeed, taxa such as Megaceros aenigmaticus, in which the male and female plants
are geographically separated into different watersheds, rely entirely on vegetative reproduction for dissemination and propagation (Renzaglia & McFarland
1999). Fragmentation, regenerant formation, and gemmae production have
been reported in various taxa. Under adverse environmental conditions or
simply as a means of asexual reproduction, some genera or species of hornwort
produce nutrient-filled tubers as perennating bodies (Goebel 1905, Renzaglia
1978, Hässel de Menéndez 2006, Stotler & Doyle 2006) (Fig. 3.4E).
Gametangia are produced along the dorsal thallus midline. Archegonia are
exogenous, i.e. they develop from surface cells, and ultimately are sunken in
thallus tissue (Fig. 3.6A–C). In addition to the central cells of the archegonium,
the archegonial initial gives rise to a one- to two-layered venter (Fig. 3.6B), and
six rows of neck cells that slightly protrude from the thallus surface and are
overarched by a layer of mucilage (Fig. 3.6C, D). Two to four cover cells cap the
canal until the egg reaches maturity, at which time they are dislodged from the
neck (Fig. 3.6A). Venter cells are smaller than the surrounding parenchyma; they
are less vacuolated and contain a prominent nucleus with nucleolus and an
associated flattened plastid (Fig. 3.6B). The central archegonial cells typically
consist of four to six neck canal cells, a ventral canal cell and egg (Fig. 3.6A, D).
The ventral canal cell and egg originate from the venter canal cell and contain
dense cytoplasm including abundant lipid reserve and a single elongated undifferentiated plastid that encircles the nucleus (Fig. 3.6D). The ventral canal cell
persists beyond degradation of the neck canal cells and disintegrates when the
egg reaches maturity. Both cells are surrounded by callose.
Antheridia are referred to as endogenous because they develop from subepidermal cells and ultimately are positioned within internal thallus chambers
(Fig. 3.7A). One to 80 antheridia (all derived from the same subepidermal cell)
are enclosed in each sunken chamber (Fig. 3.7A, B). In other embryophytes,
antheridia develop from epidermal cells. In hornworts, the epidermal cell develops into the two-layered chamber roof. A schizogenous chamber forms below the
roof and antheridial initials arise internally at the base of the chamber from
epithelial (layer surrounding an internal space) cells. The designation of hornwort
antheridia as endogenous refers only to the location of development and not to a
developmental pathway inherently different from that in other bryophytes
(Renzaglia et al. 2000). In fact, development of the antheridium proper in hornworts resembles that of other bryophytes, especially complex thalloid liverworts,
in that the antheridial initial elongates without apical cell involvement and four
primary spermatogones with eight peripheral jacket initials are produced in the
formative stages of organogenesis. Thousands of minute spermatozoids are
3 Morphology and systematics of hornworts
B
A
C
D
Fig. 3.6. (A) Phaeoceros carolinianus. LM longitudinal section of sunken archegonium with two
cover cells (CC), six neck canal cells (NC), ventral canal cell (V), and egg (E)-containing
nucleus. Bar ¼ 20.0 mm. (B) Phaeoceros carolinianus. TEM oblique cross-section of venter of
nearly mature archegonium containing ventral canal cell (V) and egg (E); both are embedded
in a callosic matrix and contain an elongated plastid near a large central nucleus (visible in
ventral canal cell) and dense lipid-filled cytoplasm. The surrounding venter is one- or
two-layered. Venter cells are smaller than other thallus cells and contain less-dense
cytoplasm with small vacuoles and an elongated plastid (P) adjacent to the nucleus.
Bar ¼ 4.0 mm. (C) Dendroceros japonicus. LM longitudinal section of mature archegonium that
projects from the dorsal thallus, is overarched by mucilage (M), and has discharged the cover
cells (CC). The venter contains an egg cell (E). Bar ¼ 20.0 mm. (D) Phaeoceros carolinianus. LM
surface view of mature archegonium containing six rows of neck cells, each with a single
prominent chloroplast. Bar ¼ 20.0 mm.
produced in each antheridium (Fig. 3.7A, C). When antheridia are mature, the
plastids of the jacket layer typically have converted to orange-colored chromoplasts (Duckett 1975). The roof of each antheridial chamber ruptures and the
jacket cells dissociate, thus liberating the spermatozoids (Fig. 3.7B).
Spermatogenesis provides clues to the phylogenetic history of hornworts
(Renzaglia & Carothers 1986, Renzaglia & Duckett 1989, Garbary et al. 1993,
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A
C
B
D
Fig. 3.7. (A) Leiosporoceros dussii. LM section of antheridial chamber showing eleven antheridia in
different stages of development. Bar ¼ 50 mm. (B) Dendroceros tubercularis. SEM of dorsal thallus
with ruptured, projecting chamber containing a single antheridium. Bar ¼ 0.1 mm. (C) Notothylas
orbicularis. TEM of antheridium showing diagonal final mitotic division (D) that produces pairs of
polygonal spermatids. Bar ¼ 3.0 mm. (D) Phaeomegaceros hirticalyx. Three-dimensional
reconstruction of biflagellated sperm cell. The locomotory apparatus consists of two flagella (Fl)
that are inserted symmetrically into the cell anterior over a spline (SI) of 12 microtubules and an
underlying anterior mitochondrion (Ma). The cylindrical nucleus (N) with central constriction
occupies most of the cell length, and a round posterior mitochondrion (Mp) is positioned in front
of a plastid (P) with a single starch grain. Bar ¼ 0.5 mm.
Graham 1993, Vaughn & Renzaglia 1998, Renzaglia & Garbary 2001). During
spermatogenesis, pairs of bicentrioles arise de novo at the poles in the cell
generation prior to the spermatid mother cell (Vaughn & Renzaglia 1998).
Bicentrioles are diagnostic of archegoniates that produce biflagellated sperm
3 Morphology and systematics of hornworts
cells but the timing of their origin in hornworts is earlier than in other taxa,
where these organelles originate in the spermatid mother cell. Because green
algal cells typically contain centrioles in all cell generations, this feature in
hornworts was interpreted as a plesiomorphy (Vaughn & Harper 1998, Vaughn &
Renzaglia 1998). As in Coleochaete, liverworts, and some pteridophytes, the
final mitotic division in the spermatid mother cell is diagonal and spermatids
develop in pairs (Fig. 3.7C). Sperm cell architecture varies little in the six
genera (Leiosporoceros, Anthoceros, Phaeoceros, Notothylas, Phaeomegaceros, and
Megaceros) that have been examined to date (Fig. 3.7D) (Renzaglia et al. 2007,
K. S. Renzaglia, unpublished data). The mature spermatozoid is extremely small
(approximately 3.0 mm in diameter), coiled, biflagellated, and symmetrical. Both
flagella insert at the anterior extreme of the cell over a spline of 12 microtubules
and are directed posteriorly. Spermatozoids contain an anterior mitochondrion,
a cylindrical nucleus with mid-constriction, and a posterior mitochondrion
associated with a plastid containing one starch grain. Unlike sperm cells in all
other archegoniates which are sinistrally coiled, the hornwort cell is dextrally
coiled (Fig. 3.7D).
Following fertilization, the first division of the zygote is longitudinal and the
endothecium of the embryo gives rise to a central columella, if one exists
(Renzaglia 1978). The amphithecium forms the sporogenous tissue, assimilative
layer, and epidermis (Fig. 3.8A). This is in contrast to liverworts and most mosses
in which the zygote undergoes a transverse first division and the endothecium
gives rise to sporogenous tissue (the notable exception is Sphagnum) in addition
to the columella. The foot matures before the remaining histogenic regions
(Fig. 3.8A, B). The basal meristem is established early in development and is
unifacial, producing cells above the foot that differentiate upwardly. Division
patterns from this meristem upward mimic that of the embryo in the origin and
differentiation of an amphithecium and endothecium (Fig. 3.8C). Growth of
overarching gametophytic tissue occurs as the embryo develops, thus forming
a protective involucre that in most taxa is ruptured with continued maturation
of the sporophyte (see Fig. 3.2A). The involucre remains as a cylinder that
surrounds the base of the sporophyte (Fig. 3.8A). Numerous archegonia are
produced in an acropetal fashion and thus young plants will bear young sporophytes at different stages of development.
Although globose in general structure, the anatomical organization of the
foot is highly variable among species (Renzaglia 1978, Renzaglia & Vaughn
2000). For example, palisade-like epidermal cells surround the relatively small
foot of Anthoceros whereas the massive foot of Megaceros contains thousands of
small undifferentiated cells (Renzaglia 1978). Typically, a parenchymatous
inner foot is bordered by numerous smaller cells, including haustorial cells
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A
B
C
D
E
F
Fig. 3.8. (A) Leiosporoceros dussii. LM median longitudinal section of young sporophyte less than
1.0 mm long enclosed in the involucre (I). The prominent foot (F) consists of large central cells and
smaller peripheral cells that interdigitate with gametophyte cells to form the placenta (Pl). A basal
meristem (B) has begun to produce columella (C) and assimilative tissue (AS). Mature cells from
embryonic divisions cap the sporophyte. Bar ¼ 100.0 mm. (B) Leiosporoceros dussii. LM median
longitudinal section of sporophyte more than 30 mm long showing placental region (Pl) at the
interface between gametophyte (Ga) and foot. The slightly bulbous foot lacks a palisade layer as
occurs in Anthoceros. Bar ¼ 100 mm. (C) Phaeomegaceros fimbriatus. LM nearly median longitudinal
section illustrating three histogenic regions: five or six layers of cells in assimilative region (As),
archesporium with a single row of fertile tissue (B) and central columella (C). Bar ¼ 50 mm. (D)
Phaeomegaceros fimbriatus. LM of haustorial cells (S) intermingled with gametophytic cells (Ga) with
wall ingrowths. Bar ¼ 15 mm. (E) Folioceros appendiculatus. TEM of gametophyte cells (Ga) of the
placenta with elaborate wall ingrowths adjacent to sporophyte cells (S) that lack ingrowths.
Bar ¼ 2.0 mm. (F) Folioceros fuciformis. TEM of protein crystals between sporophyte (S) and
gametophyte (not visible) generations. Bar ¼ 0.5 mm. Inset: Higher magnification showing
substructure of protein crystal. Bar ¼ 0.2 mm.
that penetrate and interdigitate with surrounding gametophytic cells (Villarreal &
Renzaglia 2006b; Fig. 3.8A, B). Collectively, the cells at the interface between
generations compose the placenta through which the sporophyte obtains nourishment. Transfer cells with elaborate wall labyrinths that facilitate
3 Morphology and systematics of hornworts
intercellular transport are restricted to gametophyte cells (Fig. 3.8D, E), a feature
that is shared with Coleochaete and rare in other bryophytes (Graham 1993,
Ligrone et al. 1993). A distinctive feature of the hornwort placenta is the occurrence of abundant protein crystals between gametophyte and sporophyte cells
in Folioceros, and some species of Phaeoceros, Notothylas, Dendroceros, and Megaceros
(Ligrone et al. 1993, Vaughn & Hasegawa 1993) (Fig. 3.8F). These crystals likely
derive from gametophytic cells and may be a source of amino acids for the
developing sporophyte (Ligrone & Renzaglia 1990).
At maturity, the aerial sporophyte is an elongated cylindrical spore-bearing
region which includes an epidermis, assimilative layer, sporogenous tissue, columella, and basal meristem (Fig. 3.9). Because of the programmed divisions from the
basal meristem, spore production is continuous throughout the growing season,
with spore maturation progressing from the base to the apex of the sporophyte. In
Notothylas, the basal meristem functions for a limited period; the sporophyte
remains small and is frequently retained within the protective tissue of the gametophyte. No parallels of the sporophyte developmental strategy of hornworts,
which is essentially a process of elongating a sporangium from its base, are evident
in any other embryophytes. Other monosporangiate archegoniates have determinate growth that produces a defined capsule and seta, whereas polysporangiate
land plants exhibit apical growth of the sporophyte that produces repeating modules, some of which may bear discrete sporangia (Kenrick & Crane 1997). In all land
plants except hornworts, spore maturation in a single sporangium is synchronized.
Stomata that resemble those of mosses and tracheophytes occur in the sporophyte of many hornworts. Guard cells are characterized by inner (ventral) wall
thickenings and apparently they are the only epidermal cells that contain prominent plastids, especially amyloplasts (Fig. 3.9D, E). These features suggest homology with stomata of other embryophytes. Epidermal cells typically are elongated
and less commonly isodiametric in some species that lack stomata (Fig. 3.9G). At
the tip of the sporophyte, where spores are mature, walls of epidermal cells are
thickened along the outer tangential and radial walls (Fig. 3.9A, C).
An assimilative (photosynthetic) layer of variable thickness (4–13 layers)
underlies the epidermis (Fig. 3.9A–C). Substomatal cavities and prominent intercellular spaces characterize the outer assimilative layer in taxa with stomata
(Fig. 3.9A). The inner region in species with thick assimilative layers is compacted, with smaller cells and chloroplasts than those in the spongy outer layer.
In taxa without stomata such as Megaceros and Dendroceros, there is no spongy
layer, i.e. the assimilate layer lacks intercellular spaces (Fig. 3.9C).
The sporogenous tissue is situated between the assimilative region and
the columella. The columella usually comprises 16 cells in four rows of four
in cross-section but may contain as many as 40 irregularly arranged cells
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B
A
C
E
D
F
G
Fig. 3.9. (A) Leiosporoceros dussii. LM of sporophyte in transverse section. A single-layered
epidermis with highly indented suture surrounds assimilative tissue (As) that consists of a
spongy outer region with air spaces (*) open to stomata and compacted inner zone.
Sporogenous tissue, with several layers of tetrads (Sp) intermixed with pseudoelaters (El), is
bathed in mucilage. Bar ¼ 100.0 mm. (B) Phaeoceros carolinianus. SEM of sporophyte in transverse
section. A mostly compact assimilative tissue (As) surrounds a single layer of spore tetrads (Sp)
and central columella (C). Bar 100.0 mm. (C) Megaceros pellucidus. LM of sporophyte in
transverse section. Five or six layers of compact assimilative tissue (As) have slightly smaller
and aligned cells along the suture (Su). Three or four layers of spore tetrads (Sp) are
interspersed with longitudinally aligned pseudoelaters and bathed in mucilage around a
central columella (C). Bar ¼ 100 mm. (D) Leiosporoceros dussii. SEM of closed stoma in sporophyte
epidermis. Bar ¼ 20 mm. (E) Phaeoceros carolinianus. LM of open stoma in sporophyte epidermis
showing massive starch-filled plastids in guard cells. Bar ¼ 30.0 mm. (F) Phaeoceros carolinianus.
SEM of sporophyte in transverse section showing 16-celled columella with small intercellular
spaces. Bar ¼ 15 mm. (G) Dendroceros crispatus. SEM of sporophyte epidermis with no stomata.
Unlike those of most hornworts, epidermal cells in this species are not elongated.
Bar ¼ 40 mm.
3 Morphology and systematics of hornworts
(Fig. 3.9B, C, F). Sporogenous tissue is bathed in mucilage and consists of sporogenous cells or spores with pseudoelaters interspersed (Fig. 3.9A, C). Spore
shape, wall ornamentation and pseudoelater architecture are variable across
taxa and are widely used in taxonomy (Fig. 3.10A–F). Pseudoelaters are multicellular and range from thin-walled and isodiametric to elongated with tapering
ends and evenly-thick or spirally thickened walls (Fig. 3.10B, C, E, F). These
sterile cells do not undergo meiosis and are interspersed among sporogenous
cells, thus separating sporocytes during differentiation. Sporophyte expansion
further facilitates tetrad development that involves enlargement of nascent
spores and the development of a sculptoderm.
Spore ornamentation and color offer the main characters to delimitate hornwort taxa. Leiosporoceros is the only known hornwort with nearly smooth, beanshaped spores that are arranged in bilateral alterno-opposite tetrads (Fig. 3.10A)
(Hässel de Menéndez 1986). Because of the arrangement, the proximal surface of
these spores exhibits a modified Y-shaped mark. The remaining hornworts have
tetrahedral, sometimes cruciate, tetrads (except Hattorioceros). Variability in
distal wall ornamentation is seen in Anthoceros where it ranges from spinose
and punctate (A. punctatus group) to lamellose (A. angustus). The sculptoderm on
proximal faces is generally less ornate, but shows considerable variability, even
within species of Anthoceros (e.g. hollows in A. punctatus, lamellae in A. cavernosus,
and warts in A. tuberculatus). Sphaerosporoceros and Folioceros have rounded spores
with inconspicuous trilete ridges (Asthana & Srivastava 1991) (Fig. 3.10B). In
Phaeoceros, species of the laevis–carolinianus group have spinose spores with a
conspicuous cingulum (Fig. 3.10C). Spores of Hattorioceros are strikingly different
from other hornworts: they are small (< 20 mm) with a canaliculate–striate surface and irregular shape (Fig. 3.10D). Phymatoceros spores are yellow–vermiculate
spores with a distal bump (Fig. 3.10E). In Phaeomegaceros the yellow–vermiculate
spores are differentiated by dimples on the distal surface (Fig. 3.10F). In the
subfamily Dendrocerotoideae, Dendroceros has multicellular spores with finely
spinulose (D. crispus) surfaces. Spores of Megaceros and Nothoceros are virtually
identical with distal mammillae (Duff et al. 2007, Villarreal et al. 2007).
Although wall architecture has significant taxonomic value, we have discovered cases of convergent evolution, or perhaps hybridization, in our studies. For
example, an unnamed species from Venezuela that nests within the Phaeoceros
clade has spores similar to those of Phymatoceros, but the thallus and sporophyte
anatomy are Phaeoceros-like.
Spore color is related to spore longevity. Yellow and brown spores are long-lived
(up to 21 years in herbarium packets) because they have thicker walls and are filled
with oils. The oil reserve performs a dual function of nutrient storage and protection against desiccation (Fig. 3.10G). Yellow spore color is plesiomorphic in
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A
C
B
E
D
G
H
F
I
Fig. 3.10. (A) Leiosporoceros dussii. SEM of tetrads showing smooth spores in bilateral
alterno-opposite arrangement. Bar ¼ 10.0 mm. (B) Folioceros appendiculatus. LM of distal face
of spore with thick-walled pseudoelater. Bar ¼ 10.0 mm. (C) Phaeoceros carolinianus. SEM of
spore tetrad with spinose spores surrounded by short smooth pseudoelater (El) and still
enclosed in the sporophyte. Note remnant spore mother cell wall (SW) over spore
surfaces. Bar ¼ 10.0 mm. (D) Hattorioceros striatisporus. SEM of isolated minute spores of
different sizes and shapes with striate-canaliculate ornamentation and no trilete mark.
Bar ¼ 5.0 mm. (E) Phymatoceros phymatodes. SEM of distal face of spore in a tetrad showing
prominent mammilla and associated pseudoelater (El). Remnants of spore mother cell wall
cover tetrad. Bar ¼ 10.0 mm. (F) Phaeomegaceros fimbriatus. SEM of distal face of spore
showing vermiculate surface with six depressions around a larger central one.
El ¼ pseudoelater. Bar ¼ 8.0 mm. (G) Folioceros fuciformis. TEM of a mature spore full of
lipids (Li) with a slightly thick spore wall (W). The aperture is arrowed. Bar ¼ 10 mm.
(H) Megaceros gracilis. TEM of a mature green spore with thin spore wall (W) and large
chloroplast (P). External ornamentation is arrowed. Bar ¼ 10 mm. (I) Dendroceros granulatus.
TEM of precocious spore with multiple cells, each with a plastid (P) and conspicuous
pyrenoid (Py).
3 Morphology and systematics of hornworts
hornworts and occurs in Leiosporoceros, Phaeoceros, Paraphymatoceros, some Notothylas
taxa, Hattorioceros, Phymatoceros, and Phaeomegaceros. Dark spores are present in
Anthoceros, (Mesoceros), Folioceros, Sphaerosporoceros and some species of Notothylas.
‘‘Green’’ spores, due to the presence of a chloroplast and a thin, colorless spore
wall, are short-lived and restricted to tropical genera: Megaceros, Nothoceros, and the
epiphytic Dendroceros (Fig. 3.10H, I).
Sporogenesis in hornworts resembles that in many other basal embryophytes
in that meiosis is monoplastidic. The single plastid undergoes two series of
division and the four resulting plastids define the meiotic poles (Fig. 3.11A).
Associated with monoplastidy in achegoniates, but not in green algae, is a
unique quadripolar microtubule system that is organized at the plastids and
predicts polarity of the two meiotic divisions (Brown & Lemmon 1997).
A
C
B
D
E
F
Fig. 3.11. (A) Leiosporoceros dussii. TEM of spore wall in nascent spore. A multilayered lamellae
composed of tripartite lamellae (TPL) is seen just after meiosis; sporopollenin deposition
obscures TPL in more mature spores (see B). Bar ¼ 0.10 mm. (B) Leiosporoceros dussii. TEM of distal
face of nearly mature spore. The three-layered wall is composed of a compacted and uniform
exine 1 (E1), electron-translucent and granular exine 2 (E2), and electron-translucent intine (In).
Bar ¼ 1.0 mm. (C) Anthoceros punctatus. TEM of distal face of nearly mature spore. The threelayered wall is composed of a thin, compacted, homogeneous E1, a densely globular E2, and an
electron-dense intine (In). Bar ¼ 1.0 mm. (D) Dendroceros granulatus. TEM of distal face of
multicellular spore. The three-layered wall is composed of an undulating homogeneous E1, a
fibrillar electron-dense E2, and a thin translucent intine (In). Bar ¼ 1.0 mm. (E) Notothylas
temperata. TEM of nearly mature spore wall with complex wall. Dark-perine-like layer (Pe)
deposited from spore mother cell wall covers outer exine (E1). One or two lamellae (L) lie
between exine 2 (E2) and intine (In) of three layers: electron-lucent outer and inner layers, with
an electron-dense layer between. Bar ¼ 0.5 mm. (F) Notothylas orbicularis. TEM of proximal face at
trilete mark where developing aperture (Ap) has greatly expanded exine 2 (E2) with globular
sporopollenin deposition. Sporopollenin will eventually fill all but the mid-line of the aperture.
Intine (In) and exine 1 (E1) layers are similar to remainder of spore. Bar ¼ 1.0 mm.
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Spore wall development in hornworts involves the presence of tripartite
lamellae (TPL), not reported for hornworts prior to our studies. TPL are laid
down immediately after meiosis and they coalesce to form a multilamellate
layer (MLL) that delimits the outer exine (exine 1; Fig. 3.11A). Through precisely
produced folds in the MLL, the spore wall sculpturing is determined in the initial
stages of wall development. The TPL are reinforced with sporopollenin soon
after ornamentation is established, and thus the fine lines are entirely obscured
(Fig. 3.11B). To date, TPL have been found in early post-meiotic spore walls of
Leiosporoceros (Fig. 3.11A), Notothylas (D. Long & K. S. Renzaglia, unpublished data)
and Megaceros, but not in Dendroceros (S. Schuette & K. S. Renzaglia, unpublished
data). The spore wall is deposited centripetally and consists of a thin outer layer
(exine 1), a thick inner exine (exine 2) that forms by deposition of flocculent
electron-dense material, and an inconspicuous fibrillar intine (Fig. 3.11B–E).
Variations across genera are evident from Leiosporoceros with a simple spore
wall layering (Fig. 3.11B) to Anthoceros with a thick, globular exine 2 (Fig. 3.11C)
and Dendroceros, which has a highly undulated outer exine that stretches by
unfolding as the cells divide during endosporic germination (Figs. 3.10I, 3.11D).
In Notothylas temperata, the spore wall displays bands of varying opacity in the
intine: an electron-lucent layer, an electron-dense layer, and an inner electronlucent zone (Fig. 3.11E). During the final stages of spore wall development in
most taxa, a thin dark band of fibrous material is laid down on the outer spore
surface. This layer is derived from deposition of remnant sporocyte wall and
intrasporal septum (Fig. 3.11E). Thus, although it is of extrasporic origin, this
covering is not a true perine, which by definition derives from the inner sporangial wall. In a few species of yellow-spored genera, the remnant spore mother
cell wall is responsible for secondary ‘‘browning’’ of the spores.
The trilete ridge serves as the site for spore germination and is differentiated
into a simple aperture (Fig. 3.11F). In this aperture, exine 2 is greatly expanded
whereas intine and exine 1 remain unchanged. Sporopollenin deposition is
increased along the flanks of the aperture and thus fortifies the ridge, while
the center of the aperture at maturity is nearly devoid of sporopollenin
(Fig. 3.11F). An aperture-like region with similarly thickened exine 2 and a
break in sporopollenin deposition occurs along the spore equator and forms
the cingulum of many taxa (Villarreal & Renzaglia 2006b).
Dehiscence typically occurs along two longitudinal lines that originate near
the sporophyte tip. Pseudoelaters and the columella facilitate spore separation
and assist in dispersal. Spores remain in tetrads until nearly mature and are
dispersed individually.
Spore germination results in the production of a single gametophyte. Dendroceros
spores are precocious and initially endosporic. Multicellular ‘‘spores’’ are released
3 Morphology and systematics of hornworts
from the capsule and develop upon contact with the substrate. In most taxa, germination is exosporic, resulting in a globose sporeling that produces an apical cell and
flattens with continued development (Renzaglia 1978). Spores may overwinter or
remain quiescent until favorable conditions for germination are encountered.
3.5
Evolution
Because the paleontological record for hornworts is depauperate it is
difficult to assign dates to hornwort divergences. It is well accepted that the
evolution of monosporangiate body plans preceded polysporangiate architectures and thus the hornwort clade was established prior to the appearance of
tracheophytes in the Silurian. Yet no hornwort fossils have been found in any
Paleozoic strata. It is particularly intriguing, therefore, that spores of
Leiosporoceros (Fig. 3.10A) are remarkably similar in size, shape, and ornamentation to those of the earliest occurring land plants from the Ordovician (Kenrick
2003, Wellman et al. 2003). The primary difference is that these simple fossil
spores are arranged in tetrahedral tetrads and not in the peculiar bilateral
alterno-opposite arrangement that typifies Leiosporoceros.
The oldest confirmed hornwort fossils are sparse reports of spores and sporangia resembling the extant Phaeoceros and Notothylas from the Cretaceous (Jarzen
1979, Chitaley & Yawale 1980, Dettmann 1994). Cenozoic fossils of spores resembling Phaeoceros and Phaeomegaceros have been reported from Europe, Central
America, and South America (Hooghiemstra 1984, Graham 1987, Ivanov 1997).
Spore ornamentation of these fossils strongly resembles that of extant taxa,
suggesting morphological stasis over the past hundred million years.
The fragile nature of the hornwort thallus explains the absence of fossil
gametophytes. Without such tissue, morphological evolution within the
group can only be inferred from phylogenetic analyses. It is plausible that
hornworts were a highly diverse group in Pre-Cretaceous times and that they
experienced episodes of extinctions. The nested phylogenetic position of epiphytic taxa (Megaceros and Dendroceros) supports the interpretation that diversification of these clades was correlated with angiosperm and fern radiation in the
Cretaceous. A recent report of a preserved hornwort fossil from the Dominican
Amber (Eocene–Oligocene) attributed to Dendroceros is consistent with this conjecture (Frahm 2005). With spore wall diversity and ultrastructure recently
documented in hornworts (Duff et al. 2007), a critical assessment of spore fossils
prior to the Cretaceous may reveal additional clues about hornwort diversification and provide valuable calibration points for molecular phylogenies.
The generic divergence of Leiosporoceros from the remaining hornworts
prompted further morphological and molecular studies that reaffirm the
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K. S. Renzaglia and others
distance between this and the other taxa (Duff & Moore 2005, Villarreal &
Renzaglia 2006a). This robust taxon possesses features not seen in other hornworts, such as lack of RNA editing, small, smooth ‘‘monolete’’ spores, lack of
ventral clefts in mature gametophytes, and central canals with Nostoc that run
the length of the thallus. Unfortunately, it is impossible to determine whether
these peculiarities are plesiomorphic in hornworts or simply features that
evolved after Leiosporoceros diverged from the remaining taxa.
With only a few exceptions, morphological boundaries between hornwort
genera remain ambiguous even though interrelationships have solidified as a
result of phylogenetic inferences from DNA sequence data (Fig. 3.1). For example, based on appearance, several species within the genus Nothoceros could
readily be placed within Megaceros. Moreover, genera such as Sphaerosporoceros
and Phymatoceros are defined by single features pertaining to tubers, and spore
shape and ornamentation; thus mature fertile plants are required for identification (Cargill & Scott 1997). Notothylas and Dendroceros are two of the 14 genera
that are clearly demarcated by a suite of diagnostic characters. The placement of
Notothylas within a paraphyletic Phaeoceros confirms the traditional view that the
sporophyte of Notothylas is derived through extensive evolutionary reduction
(Campbell 1895, Proskauer 1960, Renzaglia 1978, Schofield 1985, Schuster
1987). Nested within the Megaceros–Nothoceros assemblage, Dendroceros is defined
by the midrib and monostromatic perforated wings, a hemidiscoid apical cell, a
unique pyrenoid microanatomy, and precocious, endosporic germination that
is associated with a peculiar spore wall structure. These features are viewed as
adaptations to the epiphytic habit of this taxon.
With a solid backbone of relationships it is now possible to examine character evolution within hornworts (Fig. 3.12). Here we present brief descriptions
of character transformations that demonstrate reductions, parallelisms, reversals, and niche-specific adaptations.
3.5.1
Stomata
Stomata are plesiomorphic in hornworts and were lost independently
in two clades: Notothylas and the Megaceros–Nothoceros–Dendroceros assemblage.
Genera that lack stomata have involucres that cover the epidermis in the region
where guard cells differentiate, suggesting that developmental constraints may
regulate stomata differentiation. In Notothylas and Dendroceros, most of the young
sporophyte is covered by involucre, whereas in Megaceros and Nothoceros the
involucre is markedly longer than those of other genera. It remains to be tested
whether the capacity to produce stomata exists in these taxa but is inhibited by
immersion within a mucilage-filled involucre. There are no examples of stomata, once lost, being regained in hornworts.
3 Morphology and systematics of hornworts
Dendroceros
Megaceros
1 antheridium
Phaeomegaceros
1–4 antheridia
(1–)2–6 antheridia
Phymatoceros
Notothylas
Non-tiered anther idia
Nothoceros
Phaeoceros
Paraphymatoceros
(4–)15–60 antheridia
Folioceros
Anthoceros
30–80 antheridia
Tiered antheridia
Sphaerosporoceros
Leiosporoceros
Outg roup
Fig. 3.12. Skeleton phylogeny of hornworts based on three genes (see Duff et al. 2007) with
simplified inferences on the evolution of four characters. Chloroplast structure is shown with hollow
rectangular bars: three bars
¼ pyrenoid gain, two bars
¼ partial loss of pyrenoid in
some species of lineage, and one bar ¼ no pyrenoid in entire lineage. Stomatal evolution is
represented by solid black bars: ¼ stomata present,
¼ loss of stomata. Stomata are present in
most lineages with two independent losses in Notothylas and Dendrocerotoideae. Antheridial number
is shown above branches and presents a trend from abundant antheridia (30–80 in Leiosporoceros), to
15–60 in Anthocerotidae, to (1–) 2–6 in Notothyladaceae, 1–4 in Phymatoceros, to typically only one in
the Dendrocerotaceae. Antheridial jacket cell arrangement is indicated with side arrows and
transforms from tiered in the taxa with more than six antheridia per chamber to non-tiered in all
other taxa.
3.5.2
Chloroplast evolution
The evolution of pyrenoids in hornworts involves parallelisms and
reversals with multiple losses and gains. If a single chloroplast with a central
pyrenoid is viewed as plesiomorphic, pyrenoid loss occurred independently at
least six times. The pyrenoid is the site of occurrence of RUBISCO and is associated with a carbon concentration mechanism (CCM) and low D13C values
similar to those found in plants using C4 photosynthesis and crassulacean acid
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K. S. Renzaglia and others
metabolism (Smith & Griffiths 1996, Hanson et al. 2002). Megaceros lacks pyrenoids and has a lower CCM activity than taxa with pyrenoids such as Notothylas
and Phaeoceros (Hanson et al. 2002).
Lack of a pyrenoid accompanied a reduction in plastid size and increase in
number per cell. The pyrenoid was lost in the crown group that includes
Phaeomegaceros, Megaceros, and Nothoceros, and was gained in Dendroceros and
two species of Nothoceros (Fig. 3.3C). Thus, multiple pyrenoidless plastids in
each cell are diagnostic of only two genera, Phaeomegaceros and Megaceros. The
ultrastructurally unique pyrenoid of Dendroceros is an autapomorphy that may
be associated with protecting the photosynthetic machinery during desiccation
in this epiphyte (Fig. 3.3G). Hornworts, like other bryophytes, are poikilohydric
and inhabit moist habitats. The presence of pyrenoids may have allowed the
ancestor of hornworts to survive in a recently colonized semi-aquatic habitat.
Perhaps hornworts have flexibility in their carbon requirements in nature,
using the CCM under situations of low carbon availability. However, experimental work is needed to test these speculations.
3.5.3
Antheridia
A striking trend during hornwort evolution is a systematic reduction in
antheridial number per chamber. Leiosporoceros antheridia are extremely numerous,
with 30–80 proliferated within a single sunken chamber. This number progressively decreases from 15–60 in Anthoceros–Folioceros–Sphaerosporoceros to 2–6 in most
genera to only one (rarely two) in the Megaceros–Nothoceros–Dendroceros crown group.
A tiered arrangement of jacket cells around the antheridium is associated with large
numbers of antheridia per chamber (Fig. 3.12). In chambers with six or fewer
antheridia, the antheridial body expands to fill the chamber space. This process
involves multiple divisions in the jacket, resulting in random cell arrangements.
3.5.4
Spermatogenesis
Ultrastructural examinations of sperm cell differentiation and mature
architecture have revealed little variability among the five hornwort genera
studied. A three-dimensional model that is characteristic of all species examined
has been developed for the mature sperm cell of Phaeomegaceros hirticalyx
(Fig. 3.7D). Hornwort spermatozoids are markedly different from those of other
bryophytes and from those of all other land plants in a number of features. The
two flagella are inserted side-by-side at the cell anterior and wrap twice around
the cell. The nucleus is constricted in the middle and the plastid contains a single
large starch grain. When viewed from the anterior end, the cell coils to the left,
the opposite direction from other land plant sperm. Because these cells are
bilaterally symmetrical, as opposed to asymmetrical as in other embryophytes,
3 Morphology and systematics of hornworts
the direction of coiling may be inconsequential to swimming and thus was free to
change during the evolutionary history of anthocerotes (Renzaglia et al. 2000).
3.6
Innovative morphology
Hornworts are unique among embryophytes in key morphogenetic
characters. Diagnostic morphological features of the group includes chloroplast
structure, endogenous antheridia, details of the microtubule-organizing center
during mitosis, sperm cell architecture, sporophyte growth from a basal meristem, placental transfer cells restricted to the gametophyte generation, and
non-synchronized sporogenesis. A striking contrast of hornworts when compared with mosses and liverworts is the lack of organized external appendages.
No leaves, scales, slime papillae, or superficial gametangia occur in the
group. Sex organs and Nostoc colonies are embedded within the thallus, and
mucilage canals and cells are integrated into the undifferentiated thallus chlorenchyma. Vulnerable tissues such as the apical meristem and archegonia are
protected externally by mucilage secreted by epidermal cells, and not by appendages. Small size, rapid life cycle, internal sequestration of structures, and
mucilage proliferation may be the key to the persistence of this relatively
isolated taxon through the millennia. Further insights into early land colonization strategies will be attain by continued investigation of the ultrastructure,
morphogenesis, physiology, biochemistry, and phylogeny of this engaging
plant group.
Acknowledgments
This study was supported by NSF grants DEB-9207626 and DEB-9527735.
We thank Jeff Duckett, Scott Schuette, and one anonymous reviewer for comments on the manuscript, and Drs John Bozzola, Steven Schmitt, and H. Dee
Gates at the Center for Electron Microscopy, Southern Illinois University, for
assistance and use of the facility. Thanks to William Buck and the New York
Botanical Garden (NYBG) for access to the holotype of Hattorioceros striatisporus.
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4
Phylogenomics and early land plant
evolution
brent d. mishler and dean g. kelch
4.1
Introduction
This is the era of whole-genome sequencing; molecular data are becoming available at a rate unanticipated even a few years ago. Sequencing projects in
a number of countries have produced a growing number of fully sequenced
organellar and nuclear genomes, providing computational biologists with tremendous opportunities, but also major challenges. The sheer amount of data is
nearly overwhelming; comparative frameworks are needed. Comparative genomics was initially restricted to pairwise comparisons of genomes based on
sequence similarity matching. The importance of taking a multispecies phylogenetic approach to systematically relating larger sets of genomes has only
recently been realized.
Something can be learned about the function of genes by examining them in
one organism, or by comparisons between two organisms. However, a much
richer approach is to compare many organisms at once by using a phylogenetic
approach, which lets us take advantage of the burgeoning number of phylogenetic comparative methods. A synthesis of phylogenetic systematics and
molecular biology/genomics – two fields once estranged – is beginning to form
a new field that could be called ‘‘phylogenomics’’ (Eisen 1998). We need to take
advantage of the rich, multispecies approach provided by taking into account
the history of life. Repeated, close sister-group comparisons between lineages
differing in a critical phenotype (e.g. desiccation- or freezing-tolerance) can
allow a quick narrowing of the search for genetic causes in a sort of natural
experiment. Dissecting a complicated, evolutionarily advanced genotype–
phenotype complex (e.g. development of the angiosperm flower), by tracing
the components back through simpler ancestral reconstructions, can lead to
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
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B. D. Mishler and D. G. Kelch
quicker understanding via standard functional genomics approaches. Hence,
phylogenomics allows one to go beyond the use of pairwise sequence similarities, and use phylogenic comparative methods to confirm and/or to establish
gene function and interactions across many genomes at once.
Cross-genome phylogenetic approaches have the potential to provide
insights into many open functional questions. A short list includes understanding the processes underlying genomic evolution, identifying key regulatory
regions, understanding the complex relationship between phenotype and genomic changes, and understanding the evolution of complex physiological pathways in related organisms. Using such a comparative approach will aid in
elucidating how these genes interact to perform specific biological processes.
For example, Stuart et al. (2003) used microarray data from four completely
sequenced genomes (yeast, nematode, insect, and human) to show co-expression
relationships that have been conserved across a wide spectrum of animal
evolution.
There are reciprocal benefits for the phylogeneticist as well, of course: the
new comparative genomic data should also greatly increase the accuracy of
reconstructions of the Tree of Life. Even though nucleotide sequence comparisons have become the workhorse of phylogenetic analysis at all levels, there are
clearly phylogenetic problems for which nucleotide sequence data are poorly
suited, because of their simple nature (having only four possible character
states) and tendency to evolve in a regular, more or less clockwork fashion. In
particular, ‘‘deep’’ branching questions (with relatively short internodes of
interest mixed with long terminal branches) are notoriously difficult to resolve
with DNA sequence data. Examples of such difficult cases in bryology range
from the fundamental relationships of the major groups of bryophytes to
embedded relationships within these groups such as the apparently rapid radiations of pleurocarpous mosses and leafy liverworts.
It is fortunate therefore, that fundamentally new kinds of structural genomic
characters such as inversions, translocations, losses, duplications, and insertion/deletion of introns will be increasingly available in the future. These characters need to be evaluated by using much the same principles of character
analysis that were originally developed for morphological characters. They
must be looked at carefully to establish likely homology (e.g. examining the
ends of breakpoints across genomes to see whether a single rearrangement
event is likely to have occurred), independence, and discreteness of character
states. It is also necessary to consider carefully the appropriate terminal units
for comparative genomic analysis, especially since different parts of an organism’s genome may or may not have exactly the same history. Thus close collaboration between systematists and molecular biologists will be required to code
4 Phylogenomics and early land plant evolution
these genomic characters properly, and to assemble them into matrices with
other data types.
The purpose of this chapter is to explore the relationships between genomics
and phylogenetics in the land plants, in both directions, i.e. the uses of genomic
characters in phylogenetic analysis and the uses of phylogenies in functional
analysis of genes. We use examples involving bryophytes when possible; their
position as the basal extant lineages in the land plants makes them especially
important for comparative genomics.
4.2
The uses of comparative genomics in functional studies
Evolution by descent with modification is the most important organizing principle in biology. All living things are related to each other to a greater or
lesser extent; thus similarities in the attributes they bear are dependent largely
on their degree of relatedness. This was brought home to all biologists when the
human genome was sequenced, and it became clear that very little of its
structure has to do with being a human per se, but rather with being a great
ape, a mammal, a metazoan, etc. For example, only 94 of 1278 protein families
in the human genome appear to have arisen in vertebrates (Baltimore 2001)! The
ubiquitous influence of the Tree of Life provides the key for exploring the full
richness of biological data.
Realization of this interplay between phylogenetic history and functional/
structural processes has ushered in a new era of scientific rigor in comparative
biology, especially given the rapid development of explicit and testable hypotheses of phylogenetic relationships. Many advances have been made in improving evolutionary model building; ‘‘tree-thinking’’ is now central to all areas of
systematics, ecology, and evolution (Donoghue 1989, Funk & Brooks 1990,
Wanntorp et al. 1990, Brooks & McLennan 1991, Harvey & Pagel 1991, Martins
1996, Ackerly 1997, Weller & Sakai 1999).
Two main forms of phylogenetic reasoning are used in comparative genomics: sister-group comparisons and ancestor–descendant reconstructions
(Fig. 4.1). The first approach, known as a sister-group contrast (also known as a
phylogenetic contrast), involves the comparison of two closely related species
that differ in some critical phenotype. It is much better to compare close
relatives (as in Fig. 4.1A, right), than very distant relatives (as in Fig. 4.1A, left),
because the background differences (i.e. biological differences not related to this
particular phenotype) will be much less. Such contrasts are essentially natural
experiments that can point to candidate genes likely to be causal for a particular
trait. This is particularly true if one has several phylogenetically independent
contrasts (i.e. pairs of species that are distantly related to other pairs) as this
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(A)
(B)
Deep change
in function
Recent change
in function
Increasing
complexity
Fig. 4.1. A diagrammatic representation of two forms of phylogenetic reasoning discussed in
the text. (A) Sister-group comparison. A phylogenetically distant comparison is shown on the
left; there is a large background difference between these extant taxa in addition to the target
functional difference, thus this is not a good natural experiment. A phylogenetically close
comparison is shown on the right; we expect a low background difference except for the target
functional difference, thus this a good natural experiment. (B) Ancestor–descendant
comparison. Ancestral state reconstruction is used to model earlier historical stages of a process
or structure. Thus one can make inferences about a complex modern process from examining
simpler beginnings.
allows for an estimate of statistical significance to be developed, since each
contrast is an independent replicate.
To gain a deeper understanding of the adaptive significance of a gene one can
also assess its evolutionary history by using a second form of phylogenetic
reasoning, ancestor–descendant comparison (Fig. 4.1B). In this approach, one uses
modern-day species and their inferred relationships based on other data, to
reconstruct ancestral states for some functional characteristics – following the
algorithmic approach of Maddison (1990), and implemented in such software as
MacClade (http://www.sinauer.com) and Mesquite (http://mesquiteproject.org/
mesquite/mesquite.html). This allows one to infer the most likely historical
sequence of events involved is assembling a modern phenotype. This can be
extremely useful in dissecting a complicated endpoint into its earlier, simpler
components – or conversely, in inferring how a character system has become
less complex over evolutionary time, something that seems to happen often in
bryophytes.
We will illustrate these approaches with two main examples of processes in
which bryophytes are of special importance: desiccation-tolerance and reproduction. The bryophytes include three quite distinct lineages (which are likely
not monophyletic when taken together – see below): mosses, hornworts, and
liverworts. These plants, while small in stature, are very diverse and occupy
most terrestrial and freshwater habitats ranging from lakes and streams to
mesic forests, rain forests, arctic tundra, and desert boulders. The bryophytes
4 Phylogenomics and early land plant evolution
have a basal phylogenetic position among the extant embryophytes, remnant
lineages surviving today from the spectacular radiation of the land plants in
the Devonian period, some 450 million years ago. The three main bryophyte
lineages, plus a fourth extant lineage, the tracheophytes (i.e. the so-called
vascular plants), make up the entirety of the monophyletic, extant, embryophytes, arguably one of the most important lineages to have arisen in Earth’s
history: they made possible the colonization of the land by animals, and evolved
an unparalleled diversity of size, structure, chemistry, and function.
It is difficult or impossible to study many of the important physiological or
genomic causes for adaptation to life on land when looking at fossils, so it is
fortunate that we have the bryophyte lineages living today to study. The bryophytes are clearly a ‘‘key’’ to understanding how the embryophytes are related
to each other and deciphering how they came to conquer the hostile land
environment from their primitive home in fresh water – habitats still occupied
by relatives of the land plants, the green algae (Graham 1993). Limited water
availability is probably the most important environmental factor that early
lands plants had to contend with. When living on at least periodically dry
land, plants needed to deal with limitations inherent in their biology, due to
their aquatic ancestry: the need for free water for physiological activity, and
their swimming sperm.
An understanding of the complex water relationships of the tracheophytes
can be gained by using ancestor–descendant comparisons as described above, by
mapping traits onto the most current phylogeny of the land plants and their
closest relatives in the charophycean green algae (Oliver et al. 2000, 2005). These
authors argued that when land plants were still small and delicate, it was not
possible to retain sufficient water within the plant body. These early plants had
a strategy for dealing with water called poikilohydry (defined as the rapid equilibration of the organism’s water content with its immediate external environment). They wet up quickly when free water was available in their surroundings,
and dried up just as fast when it was not. Oliver et al. (2000, 2005) also showed
that vegetative desiccation-tolerance (defined as the ability of cells to dry down
completely to low ambient water content) was primitively present in the land
plants (as seen today in nearly all bryophytes), but was then lost early in the
evolution of tracheophytes. The initial evolution of vegetative desiccationtolerance was a crucial step required for the colonization of the land, but that
tolerance came at a cost: metabolic rates are lower in tolerant plants than in
plants that do not maintain costly mechanisms for tolerance. Thus, a trade-off
between productivity and tolerance exists. The loss of tolerance appears to have
been favored as soon as an internalization of water relationships happened as
the vascular plants became more complex and gained a cuticle, vascular tissue,
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stomata, etc. However, at least two independent evolutions (or re-evolutions)
of vegetative desiccation-tolerance occurred in Selaginella, and a few more in the
ferns. Within the angiosperms, at least eight independent cases of evolution
(or re-evolution) of vegetative desiccation-tolerance occurred, often in association with spread into largely barren, very dry habitats on outcrops of rock in the
tropics (Porembski & Barthlott 2000). Furthermore, a special form of irreversible
desiccation-tolerance, related to reproduction, was evolved when seeds arose
(Black & Pritchard 2002). The specific mechanisms were different in detail each
time the general phenotype of desiccation-tolerance was re-evolved.
New phylogenomic studies suggest that most, if not all, land plants have
retained the genetic potential for desiccation-tolerance, whether they can
express the phenotype of desiccation-tolerance or not. Genes identified with
vegetative desiccation-tolerance in mosses appear to be resident in tracheophyte species that are not vegetatively desiccation-tolerant. Oliver et al. (2004)
produced cDNA libraries from both rehydrated and rapidly dried Syntrichia
ruralis, and conducted extensive EST sequencing (more than 10 000 ESTs). Over
40% of the genes represented by these ESTs were classified as unknowns, but a
number of the genes encode Late Embryogenesis Abundant (LEA) proteins that
are normally known from drying angiosperm tissues, particularly seeds. Thus,
evolutionary transitions between different levels of desiccation-tolerance may
be largely controlled by changes in regulatory genes (Bartels & Salamini 2001,
Bernacchia & Furini 2004).
Understanding these sorts of small-scale evolutionary changes in function
may best be addressed by sister-group contrasts (as described above) between
close relatives that differ in their level of desiccation-tolerance, such as within
the genus Syntrichia where relatively close relatives to S. ruralis appear to be more
tolerant (e.g. S. caninervis, a desert moss) or less tolerant (e.g. S. norvegica, an
Arctic–Alpine moss; Oliver et al. 1993). Deciphering the physiological mechanisms and genes behind different desiccation-tolerant phenotypes, both vegetative and reproductive, will be an exciting endeavor in the next few years,
and will clearly be aided by a comparative, phylogenetic approach (see also
Chapters 5 and 7, this volume).
A similar use of comparative genomics has begun to address the other major
hurdle that early land plants faced in life on land: effecting sexual reproduction.
How do the free-living gametophytes bearing male and female gametangia, with
free-swimming sperm, in bryophytes become the complex endosporic gametophytes encased within parent sporophytes in the more complex tracheophytes,
culminating in the angiosperm flower? This is another area where ancestor–
descendant comparisons can help us understand where the complicated flower
comes from, with its many parts and sophisticated pollination systems moving
4 Phylogenomics and early land plant evolution
male gametophytes close enough to the female that sperm no longer need to
swim in the environment.
The Floral Genome Project (http://www.floralgenome.org/) has been working
towards understanding these issues through broad phylogenetic sampling of
the major lineages of angiosperms and gymnosperms. Results are promising so
far within the seed plants; extensive sampling of ESTs has revealed evidence for
repeated gene duplication followed by subsequent specialization (Albert et al.
2005). At least some members of the MADS-box gene family have been discovered in bryophytes (Henschel et al. 2002, Singer et al. 2007), indicating that there
is a relationship between the simple fertilization systems of bryophytes and the
much more complex ones in angiosperms. Mosses also share the KNOX gene
family, which is involved in meristem patterning, with angiosperms
(Champagne & Ashton 2001). Comparative genomic studies have the potential
for understanding these and other morphogenetic processes (Cronk 2001); it
will be exciting to extend the sampling of genes extensively through ferns,
clubmosses, and bryophytes in the coming years.
4.3
The uses of comparative genomics in phylogenetic
reconstruction
Some of the most intriguing questions in systematics concern the origin
and relationships of diverse, ecologically dominant lineages. Such groups
include metazoans, vertebrates, land plants, and flowering plants. These groups
are all thought to have undergone an early rapid radiation, perhaps mediated by
an ecological release or the development of a key innovation. This period of
rapid diversification was followed by long periods of additional diversification,
specialization, and extinction (Kenrick & Crane 1997, Qiu & Palmer 1999,
Bromham 2003). The rapidity of the early diversification, compared with the
length of subsequent time spent following distinct histories, makes phylogenetic reconstruction of the relative branching order of basal nodes in these
groups difficult (see Chapman & Waters 2002). This pattern leaves little evidence
of the order of branching due to the inferred short time periods spanned by
the deepest branches, leaving few synapomorphies to define subsets of taxa.
Therefore, the search has been intense for evidence to give support to phylogenies of these groups.
Several analyses spanning land plants have utilized data from different
genetic markers (Hori et al. 1985, Mishler et al. 1992, 1994, Albert et al. 1994,
Barnabas et al. 1995, Malek et al. 1996, Kallersjo et al. 1998, Qiu et al. 1998, Soltis
et al. 1999, Duff & Nickrent 1999, Nickrent et al. 2000, Nishiyama et al. 2004).
Most of these analyses show the ‘‘bryophytes’’ (mosses, liverworts, and
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hornworts; quotation marks indicate inferred paraphyly) forming a paraphyletic group at the base of the living land plants (see Goffinet 2000 for summary).
However, there is disagreement about the order of branching among the major
clades. Qiu et al. (2006) is perhaps the most inclusive phylogenetic study of this
question to date; they used sequences from various chloroplast, nuclear, and
mitochondrial genes and mitochondrial gene intron presence/absence characters to infer a branching order of liverworts(((mosses((hornworts(vascular
plants))). The inclusion of genomic characters in the form of intron presence/
absence characters is especially important, as given the apparently rapid radiation of major land plant lineages, DNA sequence data alone may not be reliable
in definitively inferring phylogeny (Mishler 2000). This is particularly true of
studies that use data from only one gene. In such cases, even extensive sampling
cannot counteract the effects of extinction and character saturation (see discussion in Soltis et al. 1999). Instead, the use of genomic structural characters may
contribute to minimizing the issues of extinction and character saturation in
regard to phylogenetic reconstruction.
Studies using RFLPs to map the makeup of the chloroplast plastome found a
large structural rearrangement that is a synapomorphy for tracheophytes (vascular plants) minus lycophytes (Raubeson & Jansen 1992). In addition, a 22 kilobase (kb) inversion in the choloroplast genome was detected in most genera of
the sunflower family, Compositae, but is lacking in Barnadesioideae (Jansen &
Palmer 1987), and a 50 kb inversion defines a group of Phaseoleae in the
legumes, Leguminosae (Doyle 1994, 1995). Recent studies using a PCR-based
strategy have shown the phylogenetic utility of chloroplast rearrangements in
mosses (Sugiura et al. 2003, Goffinet et al. 2005, 2007). Likewise, structural
characteristics of mitochondrial genomes such as intron presence/absence
have been shown to be of phylogenetic significance (Pruchner et al. 2002,
Knoop 2004).
Because gene rearrangements are unusual events (Raubeson & Jansen 1992)
and presumably can occur anywhere in the plastome, they are viewed as being
much less subject to homoplasy than sequence data (Boore et al. 1995, Boore &
Brown 1998, Rokas & Holland 2000). Therefore, even a few potentially informative characters from the structure of the genome (herein we will call these
genomic characters) can be extremely useful in reconstructing phylogenies
(Dowton et al. 2002, Gallut & Barriel 2002). In this regard, rare genomic characters are analogous to significant morphological characters that often define
major plant clades (Mishler et al. 1994). For example, Qiu et al. (1998) found that
the acquisition of three mitochondrial gene introns supports liverworts as the
sister group to the remainder of land plants (embryophytes). Although these
represent few characters, they are quite significant given the rarity of such
4 Phylogenomics and early land plant evolution
modifications in the organisms studied. This rarity is inferred a priori from the
low numbers of such characters detected in the current sampling of major plant
lineages, although even then homoplasy may be present (Kelch et al. 2004).
Recent developments in genomics mean that ever-increasing amounts of DNA
sequence data and genomic structural data will become available in the near
future. Several plant nuclear genomes have been sequenced or are in the process
of being sequenced. In addition, several laboratories across the U.S.A. are actively
sequencing the chloroplasts and mitochondria of a large number of green plants
(see table at: http://ucjeps.berkeley.edu/TreeofLife/data_table.php). Although the
resultant comparative DNA sequence data no doubt will contribute much to
phylogenetic reconstruction, short, deep branches could prove recalcitrant to
such investigation. Thus, the use of genomic structural data may be instrumental
in reconstructing such difficult phylogenies.
The land plants provide an excellent study system for this approach. There is a
broad consensus, based on both morphological and molecular data, that land
plants are a monophyletic group. After appearing in the Ordovician period (Gray
1993), they underwent a rapid radiation in the Silurian, with most major lineages
appearing by the Early Devonian (see Kenrick & Crane 1997). Many of the groups
are well defined morphologically and there is a developing consensus, based on
fossil evidence and DNA sequence data, on the arrangement of many of the
interior branches of the phylogeny. Most of the main clades (e.g. angiosperms,
conifers, moniliforms) have a representative taxon with a complete sequence of
the chloroplast genome available. The land plants as a whole are rooted somewhere among the three bryophyte lineages. Nevertheless, there is a great deal of
uncertainty concerning the initial branching order at the base of the land plant
phylogeny; nearly every possible branching order among the bryophyte lineages
and tracheophytes has had some support (Mishler & Churchill 1984, Garbary et al.
1993, Garbary & Renzaglia 1998, Hedderson et al. 1996, Nishiyama & Kato 1999,
Karol et al. 2001, Qiu et al. 2006; see an excellent summary at http://www.science.
siu.edu/landplants/PhylogRelsGen.html). Therefore, land plant phylogeny, with
both well-supported (e.g. vascular plants, seed plants) and ambiguous (e.g. the
deepest branches in land plants) subclades, provides a suitable subject for evaluating the utility of chloroplast genomic data.
4.4
A new example of the use of characters from comparative
chloroplast genomics
In order to illustrate this approach, we provide an updated analysis to
Kelch et al. (2004). We have identified potentially informative genomic characters that may help to elucidate the branching order at the base of the land plant
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phylogeny. In our utilization of gene arrangement, intron, and gene presence or
absence characters, we address theoretical and practical issues involved in the
phylogenetic analysis of whole genome sequences.
4.4.1
Materials and methods
The plants examined for this study may be found in Table 4.1 and
include one or more examples of charophytes, liverworts, mosses, hornworts,
moniliforms, conifers, and angiosperms. Gene maps were downloaded from
Genbank (Table 4.1) and manually added into a spreadsheet by using Microsoft
Excel X for Mac (Microsoft Corp. 2001). We aligned the genes linearly, beginning
with a section of the plastome in the large single copy region at rpoA that has one
of the longest regions that is invariant across sampled taxa. Sequence alignment
was done by hand, with particular attention to regions of putative inversions.
Because inversions are uncommon across land plants, overlapping inversions
are extremely rare; therefore, no special efforts were needed to minimize
inversion characters. Nevertheless, large inverted sections of gene sequences
were analyzed in reverse order to facilitate identification of additional gene
rearrangements within the inverted region.
Visual inspection revealed that the presence, location, and order of tRNA
genes were the most variable elements in the plastome. In order to prevent
misalignment, tRNA genes were removed for the initial alignment and subsequently added in their appropriate positions. Characters were searched for by
using basic principles of character analysis originally developed for morphological characters (Mishler & De Luna 1991, Mishler 2005). Characters comprised
three types: gene rearrangement characters representing inversions of two or
more genes in the plastome, gene presence/absence characters representing a
gene missing from a particular position in the plastome (whether the latter
missing genes are lost or transferred to other places in the genomes will be
detectable only when more information is available on the genomic make-up of
the studied organisms), and intron presence/absence representing the presence
of a particular intron within genes in the plastome. Duplications of genes via
inclusion in the IR region were included with gene rearrangement characters.
Coding of inversion characters was binary and chosen to minimize the number
of inversion characters. Introns were located in gene sequences and coded
separately. In addition, copies of genes or pseudogenes were coded as present
or absent based on synteny (their location in relation to other genes in other
taxa in the analysis). In the coding of characters 0 represents absence or a
putative plesiomorphy and 1 represents presence or putative apomorphy. The
final comparative alignment is available as an Excel file on the Green Tree of Life
website (http://ucjeps.berkeley.edu/TreeofLife).
4 Phylogenomics and early land plant evolution
Table 4.1 Genbank accession numbers and sources of chloroplast gene maps for
sampled taxa
Genbank
Taxon
accession no.
Reference
Charophytes
Chara vulgaris L.
NC_008097
Turmel et al. 2006
Chaetosphaeridium globosum (Nordstedt)
NC_004115
Turmel et al. 2002
NC_001319
Umesono et al. 1988
NC_005087
Sugiura et al. 2003
Unpubl.
Murdock, Oliver & Mishler
Klebahn
Liverworts
Marchantia polymorpha L.
Mosses
Physcomitrella patens (Hedwig)
Bruch & W. P. Schimper
Tortula ruralis
in prep.
Hornworts
Anthoceros formosae Stephani
NC_004543
Kugita et al. 2003
AY660566
Wolf et al. 2005
Unpubl.
Karol et al. in prep.
Lycophytes
Huperzia lucidula (Michx.)
Trevisan
Isoetes flaccida Shuttlew.
Moniliphytes
Adiantum capillis-veneris L.
NC_004766
Wolf et al. 2003
Angiopteris evecta
Unpubl.
Roper et al. 2007
Equisetum arvense L.
Unpubl.
Karol et al. in prep.
Psilotum nudum (L.) P.Beauv.
NC_003386
Wakasugi et al. unpubl.
Conifers
Pinus koraiensis Siebold & Zucc.
NC_004677
Noh et al. unpubl.
Pinus thunbergiana Franco
NC_001631
Wakasugi et al. 1994
Angiosperms
Acorus calamus L.
NC_007407
Goremykin et al. 2005
Amborella trichopoda
EMBL AJ506156
Goremykin et al. 2003
Arabidopsis thaliana (L.) Heynh.
NC_000932
Sato et al. 1999
Atropa belladonna L.
NC_004561
Schmitz-Linneweber et al. 2002
Epifagus virginiana L. (Bart.)
NC_001568
Wolfe et al. 1992
Calycanthus floridus L. var. glaucus
NC_004993
Goremykin et al. 2004
Lotus japonicus ( Regel ) K.Larsen
NC_002694
Kato et al. 2000
Nicotiana tobacum L.
NC_001879
Kunnimalaiyaan & Nielsen 1997
Oenothera elata H. B.& K. ssp.
NC_002693
Hupfer et al. 2000
(Willd.) Torrey & A. Gray (as C. fertilis)
hookeri ( Torr. & A.Gray )
W.Dietr. & W. L.Wagner
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B. D. Mishler and D. G. Kelch
Table 4.1 (cont.)
Genbank
Taxon
accession no.
Reference
Oryza sativa L.
NC_001320
Morton & Clegg 1993
Phalaenopsis aphrodite Rchb. f.
NC_007499
Chang et al. 2006
Spinacia oleracea L.
NC_002202
Schmitz-Linneweber et al. 2001
Triticum aestivum L.
NC_002762
Ogihara et al. 2002
Zea mays L.
NC_001666
Maier et al. 1995
All characters that varied among sampled taxa were included in the data matrix,
including autapomorphies, as future sampling will no doubt change some autapomorphic characters into synapomorphies (for example, character 7 in ferns; see
Stein et al. 1992). Forty-seven characters (39 potentially informative) were discovered in all (listed in Appendix 4.1), and placed in a nexus file (Table 4.2). All analyses
were done with PAUP*4.0b10 (Swofford 2003). The matrix was analyzed using the
branch-and-bound algorithm with the furthest addition sequence setting. The
resulting trees were rooted by using the charophyte Chara as the outgroup taxon.
A bootstrap analysis was performed using 1000 replicates of heuristic searches
employing stepwise addition and TBR branch swapping. Analyses were performed
(1) with all characters included and (2) with three gene copy characters excluded
from analyses. The three characters excluded in some analyses comprise gene
inclusion/exclusion within the inverted repeat located at the boundary of the
large single copy and inverted repeat. A previous study (Kelch et al. 2004) indicated
that these particular characters likely have been subject to homoplasy within green
plants.
4.4.2
Results
The analysis including all characters produced 84 equally parsimonious
trees (MPT; CI ¼ 0.73, RI = 0.90). Of the 47 characters, 19 rearrangement characters, 11 of the gene presence or absence characters, and 2 of the intron
characters proved parsimony-informative. Seven characters currently are autapomorphic based on current sampling and five others are synapomorphies for
the two species of Pinus (some of these may prove to be Pinaceae or conifer
synapomorphies in the future). One of these synapomorphies (Character 40:
loss of ndhJ) represents the loss of all ndh genes from the plastome of Pinus.
Although this may be the result of independent gene losses, a conservative
approach was adopted here and lack of ndh genes was treated as a single
character change.
4 Phylogenomics and early land plant evolution
Table 4.2 Data matrix for 47 genomic characters (see Appendix 4.1) for 28 exemplars
of land plants
10
20
30
40
.
.
.
.
Chara
000001001000?01000101101011000000000?0?11111101
Chaetosphaeridium
000001001000?0100100110101100000000001111111010
Marchantia
000001001000?0100000000101100000000001111111110
Physcomitrella
000001001000?011000000010110000000000?111111111
Tortula
000001001000?010000000010110000000000?111??????
Anthoceros
011011001000?0100000000101100000010001111111111
Huperzia
000011001000?0100000000101100000000001011111111
Isoetes
010011001000?0100000000101100000010001?11??????
Psilotum
11101101?00010000000000101100000110001111111111
Equisetum
11000100100010000000000101100000100001111??????
Angiopteris
11101100100010000000000101100000110001111111111
Adiantum
?1111100110010000001000101100000010001111111111
Pinus koraiensis
????1010101010000000001011100000?1001110001111?
Pinus thunbergii
?1101010101110000000001011100000?10011100111111
Oenothera
1110?100000011001000000000100110110010110111111
Oryza
1110?100000011000000000001111??1111010010011101
Triticum
1110?100000011000000000001111??1111010010011101
Zea
1110?100000011000000000001111??1111010010011101
Acorus
111011000000010000000000011101?1110110110111111
Phalaenopsis
111011000000010000000000011101?1110010110111111
Spinacia
111011000000110000000000011001?0110010110101111
Amborella
11101100000011000000000001100110110010110111111
Calycanthus
11101100000011000000000001100110110010110111111
Arabidopsis
11101100000011000000000000100110110110110110110
Atropa
11101100000011000000000000100110110110110111111
Nicotiana
11101100000011000000000000100110110110110111111
Lotus
11101100000011000000000000000110110110110111110
Epifagus
111011000000110000000000010001?1110?10110111111
Notable bootstrap values included strong support for a monophyletic Pinus
(100), monophyly of the grasses (99) and angiosperms (92), and some support for
monophyly of land plants (72) and seed plants (76). Resolution and support were
lacking for relationships among major lineages of vascular plants, other than
the groups mentioned above (see Fig. 4.2). Five putative synapomorphies unite
angiosperms; these are rearrangement and gene characters (Appendix 4.1, characters 9, 14, 30, 31, and 38). Three characters (5, 21, and 22) support the monophyly of land plants, three others (24, 37, and 41) that of seed plants, and two
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B. D. Mishler and D. G. Kelch
100
93
72
99
95
Chara
Chaetosphaeridium
Marchantia
Physcomitrella
Tortula
Anthoceros
Psilotum
Angiopteris
Adiantum
Pinus koraiensis
Pinus thunbergii
Oenothera
Oryza
Triticum
Zea
Acorus
Phalaenopsis
Spinacia
Amborella
Calycanthus
Arabidopsis
Atropa
Nicotiana
Lotus
Epifagus
Isoetes
Huperzia
Equisetum
Fig. 4.2. A strict consensus tree of 84 MPT utilizing all characters. Bootstrap values above 50%
appear above branches.
characters (28 and 32) support monocotyledons as monophyletic. Character 15
supports a common ancestry for euphyllophytes, 17 that of the two mosses
included, and 33 the monophyly of the monilophytes. Land plants minus
Marchantia is supported by a single intron character (46) with some homoplasy.
An analysis was carried out of the data set excluding three gene copy characters corresponding to expansion of the inverted repeat in relation to other
taxa (1, 2, and 3). This resulted in six MPT. The strict consensus tree of the results
of this analysis is shown in Fig. 4.3 along with the strict consensus of the 84 trees
resulting from the analysis of all characters.
Discussion
The retention index for the analysis of land plant genomic data is higher
than the average for published data sets (see Mishler et al. 1994, Sanderson &
Donoghue 1989); this indicates a relatively low level of inferred homoplasy for
the genomic character set. This is consistent with the expectation that genomic
characters are less prone to homoplasious change than DNA sequence characters. About 11 characters (out of 47) show inferred homoplasy, higher than
might be expected a priori for genomic characters. However, putative homoplasious characters comprise those characters involving changes in single genes.
Multigene inversions are without inferred homoplasy. In some cases of inferred
4 Phylogenomics and early land plant evolution
58
55
96
97
68
86
Chara
Chaetosphaeridium
Marchantia
Physcomitrella
Tortula
Anthoceros
Huperzia
Isoetes
Psilotum
Equisetum
Angiopteris
Adiantum
Pinus koraiensis
Pinus thunbergii
Oenothera
Oryza
Triticum
Zea
Acorus
Phalaenopsis
Spinacia
Amborella
Calycanthus
Arabidopsis
Atropa
Nicotiana
Lotus
Epifagus
Fig. 4.3. A strict consensus tree of 6 MPT when three inverted repeat gene inclusion/exclusion
characters are omitted (for explanation, see discussion in text). Bootstrap values above 50%
appear above branches.
homoplasy, the loss of a particular gene in a certain location may not be true
homoplasy, in that they represent independent events that result in loss of the
gene or its movement to different parts of the genome. Most clades with strong
bootstrap support originate within groups that have long been recognized based
on morphology. These include exemplars from angiosperms, grasses, monocots, and pines. In our data set, the clade ‘‘land plants minus Marchantia’’ is
supported by one synapomorphy, an intron loss (46, intron 2 missing from ycf3).
This supports a topology in agreement with the other studies identifying liverworts as the earliest branch in land plants: studies based on morphology
(Mishler & Churchill 1984, 1985) and sequence data from the chloroplast gene
rbcL (Lewis et al. 1997). In addition, multiple intron presence/absence characters
in the mitochondrial genome, as well as many gene sequences from chloroplasts, nuclei, and mitochondria support Marchantia as sister group to the rest of
the land plants (Qiu et al. 1998, 2006).
The sister group relationship of the hornwort exemplar, Anthoceros, to the
vascular plants, supported in a previous study by two genomic characters (Kelch
et al. 2004), is equivocal in this study. The expansion of sampling in the freesporing vascular plants in this study reveals that the expansion of the inverted
repeat by incremental inclusion of genes from the large single copy region was
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by no means unidirectional. Either a shrinking of the inverted repeat within
lycophytes or a separate expansion in hornworts is inferred from the present
data. Small changes in size of the inverted repeat are known to have happened
within angiosperms (Goulding et al. 1996, Plunckett & Downie 2000) and the
reversal of larger changes involving the inclusion of whole genes is quite
plausible. Within this study, the exclusion from the analysis of three characters
related to the expansion of the inverted repeat resulted in fewer most parsimonious trees (6 vs. 84) and more structure revealed in the strict consensus tree
(Fig. 4.3). In addition, this improved structure was consistent with accepted
ideas of land plant phylogeny based on evidence from both nucleotide
sequences and morphology.
Genomic characters used as phylogenetic markers have been compared to
morphological characters in that they are complex and their evolution cannot
easily be modeled (Mishler 2005). The current study shows that they also mirror
morphological data in the varying degree of homoplasy to be expected by different
classes of genomic characters. In this study, multigene inversions proved to be
rare, unique synapomorphies (a general principle reinforced by the increased
sampling in this study in regard to Kelch et al. 2004). Other characters, particularly
those associated with the copying of genes via inclusion in the inverted repeat,
show evidence of homoplasy. The presence of homoplasy in gene inclusion characters at the boundary of the IR and LSC region has been further supported by the
larger sampling in this study in regard to Kelch et al. (2004). In particular, Huperzia
has been shown to be more similar in IR gene inclusion to mosses than to other
vascular plants included in this study. Given the comparative rarity of these
genomic characters, even a small number of homoplasious characters might
have significant effects on the topology of the trees resulting from phylogenetic
analysis. Nevertheless, even characters subject to homoplasy can reveal phylogenetic structure within subsets of the included taxa.
4.5
Summary
The relationships of the three major lineages of bryophytes and the
tracheophytes have been controversial. It is a very difficult phylogenetic problem; whatever periods of shared history there are among these lineages, they are
relatively short branches a long time before the present. We need to be cautious
about over-reliance on any one kind of data, including DNA sequences and
genomic structural data. Clearly an extensive analysis of all appropriate nuclear
and organellar DNA sequence data, plus morphology and genomic structural
data, will be needed before we can confidently resolve relationships in this
important region of the Tree of Life.
4 Phylogenomics and early land plant evolution
As we clarify the phylogeny at this deep level, the ability to use it for
comparative genomics will be enhanced. In addition to all the chloroplast
and mitochondrial genomes that are being sequenced, it will be essential to
have some key nuclear genomes completely sequenced, ideally at least one
from each of the three bryophyte lineages. Fortunately, the first of these is just
completed, for the moss Physcomitrella patens. Its complete sequence is available
on the DOE Joint Genome Institute Genome Browser at http://genome.jgi-psf.
org/Physcomitrella. This species is becoming widely recognized as an experimental organism of choice not only for basic molecular, cytological, and
developmental questions in plant biology, but also as a key link in understanding plant evolutionary questions, especially those related to genome
evolution. It is well placed phylogenetically to provide important comparisons
with the flowering plants; in terms of evolutionary distance, Physcomitrella is to
the flowering plants what the Drosophila is to humans! The liverwort Marchantia
polymorpha was proposed to the Joint Genome Institute as the next bryophyte
to be completely sequenced; an announcement has recently been made that
this proposal has been accepted (http://www.jgi.doe.gov/News/news_6_8_07.
html). When complete, it will add a deeper anchor point for comparative
genomics in land plants (as would having a genome available for hornworts).
The bryophyte genomes will greatly inform bioinformatic comparisons and
functional genomics in plants, just as the mouse, Fugu, Drosophila, and
Caenorhabditis genomes have informed animal biology. As more nuclear genomes are completed, we will eventually reach the point where we can look for
genomic structural characters as described above for chloroplasts. Large
regions of nuclear genomes appear to be conserved in gene order and arrangement (called synteny). This is apparent when comparing the human genome
with the mouse genome, or the maize genome with the rice genome, where a
high degree of synteny is present. With better sampling, unusual and complex
rearrangements should provide an exciting source of new phylogenetic characters for use in resolving deep branching events. However, the more complex
nature of the nuclear genome means that automated algorithms for detecting
the minimal number of rearrangements to change from one genome region to
another (for example, GRAPPA, http://www.cs.unm.edu/moret/GRAPPA/) will
need to be used.
Researchers currently talk about ‘‘whole-genome phylogenetic analyses’’
when what they mean is an alignment of nucleotides for all the genes in a
genome. A ‘‘whole-genome phylogenetic analysis’’ actually should look at all the
genomic structural information available, in addition to nucleotide variation.
These advances in truly genomic-level analyses will lead to a new era in plant
phylogenetics.
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Acknowledgments
The work presented here was supported in part by NSF grants DEB9712347 (Deep Gene Research Coordination Network), DEB-0228729 (the Green
Tree of Life AToL grant), and EF-0331494 (CIPRES) to BDM. We thank Bernard
Goffinet and an anonymous reviewer for helpful suggestions on the manuscript.
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Appendix 4.1 Description of genomic characters
1: Inclusion of trnL from the large single copy (LSC) edge of IRa into the IR region.
2: Inclusion of rps7 from the LSC edge of IRa into the IR region.
3: Inclusion of ndhB from the LSC edge of IRa into the IR region.
4: Inversion of the gene order within the IRs.
5: Inclusion of rps12 from the LSC edge of IRa into the IR region.
6: Loss of IRb.
7: Inferred loss of six genes: ndhD, ndhE, ndhG, ndhI, ndhA, and ndhH.
8: Inclusion of rpl21, rpl32, trnP, and trnL.
9: Inferred loss of chlL and chlN.
10: Inversion of most genes in IR region.
11: Inferred loss of trnV, rps12, and ndhB genes in IR region.
12. Inferred loss of rps7 in IR region.
13: Inferred loss of ycf15.
14: Inclusion of rpl23 and rpl2 from IRb end of LSC into the IR region.
15: Multigene (c. 27 gene) inversion between trnL and atpF.
16: Inversion of c. 30 genes between trnC and rps11.
17: Inversion of c. 20 genes between rps16 and petN.
18: Inversion of c. 14 genes between trnG and ycf3.
19: Presence/absence of petA.
20: Insertion/deletion of trnD, trnY, and trnE.
21: Presence/absence of odpB.
22: Insertion/deletion of c. 18 genes from matK to trnfM.
23: Insertion/deletion of 5 genes; trnS, psbC, psbD, trnT, and trnfM.
24: Presence/absence of trnS.
25: Inversion of trnfM, rps14, psaB, and psaA.
26: Inversion of 32 gene section from trnG to rpoA.
27: Presence/absence of infA between rpl36 and rps8.
28: Presence/absence of rpl22 between rps3 and rps19.
29: Presence/absence of trnH between rps19 and rpl12.
30: Presence/absence of ycf2 between trnL and ycf15 or trnL.
31: Presence/absence of ycf2 in inverted repeat.
32: Presence/absence of ycf15 in inverted repeat.
33: Presence/absence of ycf15 between ycf2 and trnL.
34: Presence/absence of trnL between trnI or ycf2 and ndhB.
35: Presence/absence of rps7 between ndhB and rps12.
4 Phylogenomics and early land plant evolution
36: Presence/absence of rps15 between ycf1 and ndhH.
37: Presence/absence of ycf1 between trnN and ndhF.
38: Presence/absence of rpl21 between ndhF and rpl32.
39: Presence/absence of trnP between rpl32 and trnL.
40: Presence/absence of ycf1 adjacent to rps15.
41: Presence/absence of ndhJ between trnF and ndhK.
42: Intron missing from gene (pseudogene) of rpl2.
43: Intron missing from gene rps12.
44: Intron missing from gene atbF.
45: Intron missing from gene rpoC1.
46: Second intron missing from gene ycf3.
47: Second intron missing from gene clpP2.
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5
Mosses as model organisms
for developmental, cellular,
and molecular biology
andrew c. cuming
5.1
Introduction
There is a popular genre of politically incorrect jokes on the theme of
‘‘The World’s Shortest Books’’ (of which the least offensive example is the title
‘‘Different Ways to Spell Bob’’). Until recently, it would have been fair to surmise
that the title of this chapter might have qualified with ease. Certainly, that
would have been the view of many soi-disant ‘‘mainstream’’ plant developmental
biologists, whose Arabidocentric view of the plant kingdom had tended to
ignore any organism outside the angiosperms (and most within). Thankfully,
this is no longer the case. It is now appreciated that an understanding of the
evolution of gene function and of the roles of genes in the programming of
developmental transitions (generically known as ‘‘Evo-Devo’’) requires a comparative analysis of species representative of a wide range of diverse taxa. This
has coincided with an explosion of molecular knowledge of at least one species
of moss, Physcomitrella patens, the study of which is being facilitated by the
complete sequencing of its genome. Consequently, we can expect to see a
much greater interest in this species, and in mosses as a group of plants with
their own unique features and fascination, developing within the wider plant
science community. In this chapter I shall therefore concentrate on the recent
discoveries made in Physcomitrella, and – more importantly – attempt to sketch
out some of the challenges that lie ahead for researchers intending to make use
of the burgeoning Physcomitrella resources.
The peripheralization of interest in the mosses is a comparatively recent
phenomenon, for this group has long been a source of interest for botanical
scholars. As is made abundantly clear in other chapters in this book, the mosses
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
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represent a highly species-rich group within the bryophytes – the extant representatives of the earliest group of land plants – and consequently have much to
teach us about the adaptations that were necessary for the conquest of the
land. Anyone who has observed mosses colonizing apparently inhospitable
habitats (bare rocks, walls, roofs) will be aware of their resilience to environmental stresses, a subject discussed in Chapters 6 and 7, this volume. Through
their colonization of apparently featureless substrates, and their subsequent
posthumous decomposition, mosses can be fairly considered to be habitatforming organisms that enabled the subsequent evolution of more complex
land plants.
The history of research on mosses has been one of ‘‘boom and bust’’. Indeed,
during the early years of the twentieth century, mosses represented a fertile
field of discovery in genetics, cytogenetics, and developmental biology. Much of
this history has been forgotten, or has been neglected owing to the relative
difficulty for today’s predominantly anglophone scientific community in reading and appreciating the pioneering studies, published in Latin or highly formal
and archaic German, by Hedwig, Staehelin, Hofmeister, von Wettstein and
others. Since the author (somewhat embarrassingly) has to number himself
among the linguistically challenged majority, it is therefore a great relief to be
able to recommend the illuminating account by Reski (1998) of the early history
of moss research, detailing the contributions made by these pioneers.
5.2
Physcomitrella patens: a twenty-first century model
Early research on mosses investigated a number of species. More
recently a greater focus has been concentrated on Funaria hygrometrica,
Physcomitrium pyriforme, Ceratodon purpureus, Physcomitrella patens, Tortula ruralis,
and Sphagnum spp. (Wood et al. 2004). However, it is likely that, for the foreseeable future, Physcomitrella patens will be at the center of attention for studies that
seek to achieve a synthesis of cellular, biochemical, and molecular genetic
approaches. If Arabidopsis can claim to be the ‘‘Drosophila of plant biology’’,
then Physcomitrella can make a claim to be the counterpart of the nematode
Caenorhabditis.
Physcomitrella is principally studied because of its suitability for genetic analysis. As in all mosses, the dominant phase of the life cycle – the gametophyte – is
haploid. Thus mutagenesis results in the immediate revelation of mutant phenotypes. The first mutagenic studies of this species identified a number of
auxotrophic and developmental mutants (Engel 1968), and subsequently Cove
and his colleagues developed the use of Physcomitrella for the genetic analysis of
such mutants, with an increasing focus on the genetic control of cell shape,
5 Mosses as model organisms
morphogenesis, and polar cell growth (Ashton & Cove 1977, Ashton et al. 1979a,b,
Grimsley et al. 1977, Courtice & Cove 1983, Knight et al. 1991, Jenkins et al. 1986).
These latter studies coincided with the wider development of molecular tools
for the study of gene regulation, in particular the ability to undertake genetic
transformation of plant cells. Schaefer et al. (1991) achieved the first stable
transformation of Physcomitrella. Subsequent studies revealed that if the transforming DNA contained a sequence homologous with sequences resident
within the moss genome, then the transforming DNA was preferentially integrated into the genome at the homologous site (Kammerer & Cove 1996,
Schaefer & Zrÿd 1997).
The ability to undertake ‘‘gene targeting’’ by homologous recombination
between transforming DNA and a specific locus in the host genome provides a
powerful and sophisticated tool for genetic manipulation. It occurs with high
frequency in bacteria and in simple eukaryotes (in yeast, gene targeting is a
routine procedure for genetic analysis (Orr-Weaver et al. 1981)) and is used to
make specific genetic alterations in a small number of vertebrate experimental
systems (chicken DT40 cell lines undertake gene targeting by homologous
recombination with high frequency (Sonoda et al. 2001), whilst mouse embryonic stem cells can not only be transformed by gene targeting, they can also be
regenerated to develop into transgenic mice containing the specifically altered
gene (Soriano 1995)). Gene targeting does not normally occur in flowering
plants, following genetic transformation. Although transgenic plants in which
gene targeting events have occurred have been isolated, the frequency with
which these events occur is low (Kempin et al. 1997, Terada et al. 2002, Hanin &
Paszkowski 2003). By contrast, the efficiency with which gene targeting
occurs in Physcomitrella is high – up to 100% of transformants may exhibit gene
targeting – a rate equivalent to that observed in yeast (Schaefer & Zrÿd 1997,
Schaefer 2002, Kamisugi et al. 2005).
The ability to undertake such genetic manipulation in a plant has important
consequences. First, it provides a tool for ‘‘reverse genetics’’: the creation of a
specific mutation in any given gene permits the functional analysis of that gene
through study of its mutant phenotype. Second, such reverse genetic analysis
can be directly applied for the comparative analysis of gene function. What are
the consequences in the moss of a mutation in a gene whose ortholog in flowering plants regulates a process specific to angiosperms (for example floral development, seed formation, etc.)? What does this tell us about the way in which any
particular gene has been recruited to participate in a specific morphogenetic or
developmental process in different classes of plant?
The discovery of gene targeting in Physcomitrella provided a spur to the more
widespread adoption of Physcomitrella as a model species for the study of plant
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processes. The realization that specific genes could be manipulated with exquisite precision indicated the need for gene discovery programs that resulted in
the generation of first a substantial resource of expressed sequence tags (ESTs),
derived by the high-throughput sequencing of cDNA clones (Nishiyama et al.
2003, Rensing et al. 2002), followed by the establishment of a genome sequencing programme that has culminated in the release of the first draft of the
complete Physcomitrella genome in 2007.
Thus, the early years of the twenty-first century usher in a new era of
‘‘molecular bryology’’, where the resources available through the genome
program, allied with technical developments in transformation and highresolution cellular analysis promise to return the study of mosses to a position
of prominence as plant biologists strive to understand the processes that have
shaped land plant evolution, and to manipulate these processes for applied
ends.
5.3
Physcomitrella: life cycle and development
The life cycle of Physcomitrella patens is typical of mosses (Fig. 5.1). The
cycle commences with the germination of a haploid spore. The spores are
environmentally resilient, single-celled propagules, contained within a thick
wall comprising an inner, fibrillar intine, and an outer exine composed of
sporopollenin. The exine is typically covered with an outer ‘‘perine’’ layer
produced by the developing spore capsule (by contrast with the intine and
exine, which are produced by the spore during its development). Mature spores
are rich in oil, the principal storage reserve, and contain several immature
chloroplasts derived by the division, late during spore maturation, of the large
single plastid present during the earlier stages of sporogenesis (Knoop 1984,
Schulte & Renzaglia, pers. comm.)
The germ tube penetrates the spore wall, reportedly through an aperture
characterized by the presence of a pectin-rich intine, to form the first protonemal filament. However, it is not unusual to observe germinating spores in
which two or three filaments emerge from different parts of the surrounding
wall. The protonemata consist of uniseriate filaments, which extend through
elongation and successive divisions of the meristematically active apical cell.
The apical cell of the filament continually divides to generate a new, mitotically
active apical cell and a subapical daughter cell, thus extending the filament.
Subapical cells may undergo a subsequent mitotic division to generate a sidebranch initial, from which a branching filament is formed. The first filamentous
cell is typically a chloronemal cell. Chloronemata are filaments that contain
relatively large numbers of chloroplasts. The apical cell typically possesses a
5 Mosses as model organisms
Fig. 5.1. Stages in the life cycle of Physcomitrella patens. Clockwise, from top left: (1) Gametangia
(an archegonium, and two antheridia). (2) An archegonium with fertilized egg (arrowed) and
two unfertilized archegonia. (3) Early sporophyte development: the archegonial neck is still
attached to the developing sporophyte. (4) A mature sporophyte attached to the gametophore.
(5) An ungerminated spore and germinated sporeling. (6, 7) Filament types: chloronemal and
caulonemal filaments (arrowed). (8) A bud initial. (9) A gametophore: the dark coloration is the
result of staining for GUS activity in a transgenic strain.
rounded apical dome, and the walls that separate the successive cells of the
filament lie perpendicular to the long axis of the filament. The chloronemata
are relatively slow-growing, and represent the first autotrophic cells of the
developing plant. The apical cells elongate at a rate of 2–5 mm/h, and divide
approximately every 24 h (Cove 2005).
A second filament type, caulonemata, develops by progressive differentiation of
chloronemal apical cells. The induction of caulonemal differentiation is believed
to be auxin-regulated (Johri & Desai 1973, Ashton et al. 1979a). Caulonemata
grow much more rapidly than chloronemata, the caulonemal apical cell extending
at a rate of 25–40 mm/h, and dividing with a reduced cell cycle time of approximately 7 h (Cove 2005). The caulonemal filaments are characterized by being
relatively reduced in the numbers of chloroplasts they contain. Their apical cells
have a more sharply pointed apical dome than the chloronemal apical cells, and
the cross walls between the cells of the filament are oblique, rather than perpendicular to the length of the filament. The rapid growth of the caulonemata
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allows the developing plant to colonize the available substrate more rapidly.
Caulonemal subapical cells also undergo mitosis to generate side-branches
that are mostly initially chloronemal in nature. However, some side-branches
differentiate to produce buds, establishing a nearly tetrahedral meristematic
cell that establishes a more obviously three-dimensional leafy shoot: the gametophore. Bud formation is strongly stimulated by cytokinins and light (Cove
1984, Reski & Abel 1985). The gametophores are supported by the development
of rhizoids at their base. It is on the gametophores that the sexual organs – the
gametangia – develop.
The gametangia are of two different types. Antheridia, produced generally in
the axils of the terminally located leaves of the gametophore, produce motile
spermatozoids: the male gametes. Archegonia are the female gametangia, and
develop on the end of the gametophore stalk. Each contains a single egg cell.
Because the vegetative moss plant is haploid, the male and female gametes are
produced by mitosis, not meiosis. Fertilization is achieved by a spermatozoid
swimming through a surface film of water to enter an archegonium and so fuse
with the egg cell to produce a diploid zygote. Because both antheridia and
archegonia are produced in close proximity on the same gametophore, selffertilization is a common occurrence. In nature, Physcomitrella is an ephemeral
annual plant, appearing on the banks of ponds whose water level recedes in
summer (it is sometimes known as the ‘‘reservoir moss’’), and self-fertilization
presumably offers an assured means of sexual reproduction. In culture, gametangial development, fertilization, and the production of sporophytes are
promoted by reduced temperatures and short daylength, corresponding to the
conditions prevalent during autumn, the time at which sexual reproduction in
Physcomitrella typically occurs (Hohe et al. 2002). The zygote develops into the
diploid sporophyte: in mosses the diploid generation is anatomically reduced
and is dependent upon the dominant, vegetative, gametophyte generation.
Unlike in typical mosses, such as Funaria hygrometrica, the sporophyte is borne
on a very short seta, so that it remains closely surrounded by the terminal, or
perichaetial, leaves of the gametophore during its development. It is spherical
and initially green in colour, becoming orange to brown in colour as it matures
following sporogenesis. Within the sporophyte, the spore mother cells enlarge
and are released into the mucilaginous interior of the sporophyte, where they
undergo meiosis. Each spore mother cell initially contains a single chloroplast
in addition to its nucleus, and the chloroplast undergoes two cycles of division,
in concert with the meiotic division of the nucleus, to deposit a single chloroplast in each cell of the meiotically derived tetrad (Schulte & Renzaglia, pers.
comm.). Each of these cells matures to become a single spore, and a single spore
capsule may contain approximately 4000 spores at maturity. The spore capsules
5 Mosses as model organisms
may be stored dry for extended periods of time, without significant loss of spore
viability, and there may be some ‘‘after-ripening’’ processes during dry storage,
since spores germinated from stored spore capsules germinate more synchronously than do those released from freshly harvested capsules. However, to date
no systematic investigation of spore dormancy has been undertaken.
5.4
The molecular biology of Physcomitrella: sequencing
the genome
It is a truism to state that the size of an organism’s genome is correlated
with the degree of biological complexity it displays. However, it is also a gross
oversimplification. Although this relationship holds true in general terms
(e.g. E. coli, 4.6 Mbp; yeast, 12 Mbp; Arabidopsis, 150 Mbp; Drosophila, 165 Mbp), it
is clear that among the complex multicellular eukaryotes the DNA content of
the genome can vary widely (http://www.cbs.dtu.dk/databases/DOGS/index.
php). Thus the largest plant genome size is an estimated 90 000 Mbp for the
Easter lily, Lilium longiflorum, despite this plant not being markedly more complex than Arabidopsis. Incidentally, it should be noted that the current ‘‘world
record holder’’ in the genome size stakes is the protist Amoeba dubia, with an
estimated genome size of 670 000 Mbp (Winstead 2001)! Genome size, therefore,
does not necessarily reflect complexity. Instead, it depends on the quantity of
repetitive non-coding DNA – usually retrotransposon-derived – that the host can
maintain before suffering a selective disadvantage.
Although it exhibits a structural complexity that is apparently less than that of
a flowering plant, Physcomitrella does not have a particularly small genome.
Fortunately, neither is it exceptionally large. Estimates of genome size, based on
flow cytometry of propidium-iodide-stained nuclei, indicated a DNA content
equivalent to 511 Mbp DNA (Schween et al. 2003): approximately three times
greater than that of Arabidopsis thaliana. Cytogenetic analysis is difficult, owing to
the small size of the chromosomes when mitotic figures are analyzed, but it is
believed that the genome is distributed among 27 chromosomes (Reski et al. 1994).
The first steps towards defining the coding capacity of the Physcomitrella genome comprised the establishment of EST sequencing programs (Rensing
et al. 2002, Nishiyama et al. 2003). Expressed sequence tags are obtained by the
systematic sequencing of cDNA clones, and are collated following the singlepass sequencing of individual clones. This experimental approach enables a
‘‘snapshot’’ of the genes expressed in any selected cell type to be obtained.
Because of the inherently error-prone nature of both cDNA synthesis by reverse
transcriptase and DNA sequencing reactions using thermostable DNA polymerases, ESTs do not necessarily generate high-quality sequence information
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for any individual gene, unless a number of redundant sequences can be compared,
but they do provide a valuable tool for gene discovery and comparative sequence
analysis. Currently, nearly 200 000 ESTs have been deposited in the GenBank
database, all derived from the ‘‘Gransden’’ laboratory strain. (This strain, the most
widely used by Physcomitrella researchers, derives from a single spore collected near
Gransden Wood, Huntingdonshire, U.K., by H. L. K. Whitehouse in 1962.) A further
c. 100 000 ESTs have been sequenced from a second genotype (named ‘‘Villersexel’’,
after the town in the Haute Sâone region of France near which it was collected in
2003 by Michael Lüth), which has been crossed with the Gransden genotype in
order to construct a genetic linkage map: the intention is that this collection will
facilitate the identification of single-nucleotide polymorphisms between the
Gransden and Villersexel genotypes. In addition to these resources, a further
110 000 EST sequences have been generated as a proprietary resource in a BASFsponsored research program (Rensing et al. 2002). It is expected that these will
eventually be released into the public domain. The cDNA libraries from which
these sequences were obtained derived from mRNA isolated from a range of
different stages of moss development, including protonemata growing on defined
growth medium and supplemented with different growth regulators (auxin, cytokinin, ABA), tissue subjected to drought stress, gametophores and during different
stages of sporophyte development, in order to identify transcripts from the widest
possible array of Physcomitrella genes. Bioinformatic analyses of the sequences,
which entailed clustering the sequences by multiple sequence alignment to enable
the assembly of individual consensus sequences, have estimated the numbers of
expressed genes as approximately 25 000: a figure not very different from that
estimated for the genome of Arabidopsis.
The formidable task of determining the whole genome sequence of
Physcomitrella commenced in 2005, in a program undertaken for the
Community Sequencing Program of the U.S. Department of Energy’s Joint
Genome Institute (http://www.jgi.doe.gov/sequencing/why/CSP2005/physcomitrella.html). The approach taken was a ‘‘whole-genome shotgun’’ approach.
Essentially, nuclear DNA isolated from the Gransden strain of Physcomitrella
was subjected to physical shearing, and a series of size-fractions were selected
for cloning by blunt-end ligation into a ‘‘fosmid’’ vector. This generated a
number of libraries of genomic DNA, with average insert sizes of 3 kb, 8 kb
and 40 kb, respectively. Clones from each of these libraries were end-sequenced,
and the sequences aligned in order to identify overlaps to create an assembly. By
undertaking sequencing to a high level of redundancy (over 6.7 million individual sequence traces were obtained), and applying appropriate quality filters to
the sequence output, it has been possible to obtain an approximately 8-fold
depth of coverage of the genome sequence (i.e. all regions of the genome were
5 Mosses as model organisms
sequenced, on average, 8 times: in total, nearly 5 billion bp of sequence data
were obtained for an estimated genome size of c. 500 Mbp).
The first draft of this sequence (http://shake.jgi-psf.org/Phypa1/), released in
2007, corresponds to a length estimate for the Physcomitrella genome of approximately 490 Mbp, a figure quite close to the 511 Mbp estimated by flow cytometry
(Schween et al. 2003). However, despite the average 8-fold depth of the sequencing, the sequence is incomplete. This is a common occurrence in first-draft
sequences obtained by using the random shotgun approach, and the draft will
undergo further revisions as more data are obtained. The first-draft version
comprised over 2500 ‘‘scaffolds’’ – individual assemblies made up by combining
overlapping sequences (‘‘contigs’’) derived from clusters of clones of different
lengths. Clearly, in a complete sequence, the number of scaffolds should be
equal to the number of chromosomes (n = 27). However, at this stage in the
sequence assembly, there are a number of gaps in the sequence that result
from (i) lack of overlap between the individual scaffolds, (ii) uncertainty about
overlapping sequences, and (iii) mis-assembly that occurs owing to the presence
of highly repetitive sequences within the genome. Additionally, within the
individual scaffolds, there are regions where the sequence is unknown (these
are represented in the sequence as runs of ‘‘NNNNNNNN’’). These unknown
regions correspond to as-yet unsequenced tracts in the interior of longer clones,
whose terminal sequences could otherwise be clearly aligned with those of
other clones that contributed to the scaffold assembly.
Refinement of the sequence will require the incorporation of additional information. One source of this will be the inclusion of terminal sequences derived
from BAC clones. These are large-insert ‘‘Bacterial Artificial Chromosome’’ clones
(over 100 kb of DNA can be accommodated). Because of its length, a single BAC
clone will contain very many smaller-insert clones within its length, and by
determining the end-sequences of the BAC inserts, the long-range linkage of
currently unresolved scaffolds can be achieved. Another means of linking scaffolds will be the incorporation of genetic linkage data. A genetic linkage map is
currently being constructed by using molecular markers: amplified fragment
length polymorphisms (AFLPs) and simple sequence repeats (SSRs) (von
Stackelberg et al. 2006). Because these correspond, in many cases, to identifiable
DNA sequences, they will provide additional long-range sequence data to assign
scaffolds to individual Physcomitrella chromosomes.
5.5
The discovery of homologous recombination
The discovery that propelled the study of Physcomitrella patens from a
fascinating sideshow to center stage was the discovery that transforming DNA
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could integrate into the Physcomitrella genome by homologous recombination.
This discovery has led directly to the development of high-efficiency gene
targeting in this organism, and indirectly provided the impetus, within the
plant science community, for the establishment of the Physcomitrella Genome
Program.
For many years prior to this discovery, Physcomitrella had been pioneered as a
tool for the study of plant development and cellular differentiation in the
laboratory of Professor David Cove, at Leeds University. These studies had
been primarily genetic, involving the identification of mutant strains exhibiting
altered patterns of development, and altered responses to polar growth stimuli –
in particular the phototropic and gravitropic stimuli. At this time, genetic
analysis in Physcomitrella was hampered by the low fertility exhibited by many
of the existing, mutagenized laboratory strains, but complementation analysis could still be undertaken by generating somatic hybrids between mutant
strains through polyethylene glycol-mediated fusion of protoplasts, to generate
diploids (Grimsley et al. 1977).
Complementation testing is an essential and necessary first step in the
analysis of the genetic basis of any given phenotype. When two genomes,
containing independently isolated mutations that result in the same recognizable phenotype, are combined in the same cell, then two outcomes are possible.
Either the mutant phenotype is restored (‘‘complementation’’) or the mutant
phenotype persists. Complementation indicates that the original mutations
that gave rise to the mutant phenotype were in different genes. If the mutant
phenotype persists, it indicates that the mutations are in the same gene. Such
non-complementing mutations are known as a ‘‘complementation group’’. By
assigning independently isolated mutants to complementation groups, the
investigator can determine the number of different genes that might control
that phenotype. However, unless genetic analysis is allied to powerful molecular tools, it is very difficult to identify the underlying genes.
In the 1990s, it was becoming clear that the genetic analysis of Arabidopsis
mutants, coupled with the development of a high-resolution genetic linkage
map provided one way in which mutant genes could be identified by ‘‘mapbased cloning’’: through their close linkage to a genetic marker defined by a
known DNA sequence that could be used as a hybridization probe to initiate
a ‘‘chromosome walk’’ (the successive isolation of overlapping, large-insert
genomic clones). However, even this technique was labor-intensive, since at
this time for Arabidopsis the genetic linkage map was relatively sparsely marked,
and its genome sequencing had only recently been initiated (Lukowitz et al.
2000). Consequently, alternative means were sought to identify genes regulating key developmental processes. The most successful of these are based on
5 Mosses as model organisms
insertional mutagenesis either following transformation by T-DNA delivered by
Agrobacterium – which was found to be incorporated essentially at random sites
within the genome, at low copy number – or by the activation of exogenous
transposons introduced into transgenic lines. Such insertional mutagenesis
protocols enabled the direct cloning of the genes disrupted by these agents.
Initially, the inserted DNA acted as a sequence-defined ‘‘tag’’, so that the insertionally mutated gene could be identified in a cloned library of genomic DNA
derived from the mutated strain, by using the inserted sequence as a hybridization probe. For Arabidopsis, it subsequently became possible to identify the
genomic sequences flanking the inserted DNA by using ‘‘inverse PCR’’ – a
procedure illustrated in Fig. 5.2. The generation of a number of collections of
publicly accessible` insertionally mutated, transgenic lines, in which the
mutated sequences were deposited in searchable databases (http://signal.salk.
edu/cgi-bin/tdnaexpress; http://atidb.org/; Pan et al. 2003) enabled the consequences of disruption of Arabidopsis genes to be functionally analyzed.
Because insertional mutagenesis combines the power of randomly generating mutants with the ability rapidly to isolate the disrupted sequence, it is a very
attractive genetic tool, and efforts were made to develop a similar tool for the
genetic analysis of Physcomitrella mutants. The ease with which protoplasts of
Physcomitrella could be isolated from protonemal tissue, and their rapid and
efficient regeneration to form new plants, suggested that they might also be
susceptible to genetic transformation by plasmid DNA, and a program was
initiated to develop a stable transformation system for this organism.
This was largely successful, and a collaboration between the Leeds group
and that of Professor Jean-Pierre Zrÿd, in Lausanne, demonstrated how plasmid DNA carrying selectable marker genes could be delivered to Physcomitrella
protoplasts in the presence of calcium ions and polyethylene glycol, and
incorporated into the cells (Schaefer et al. 1991). Interestingly, three classes
of transformed cell could be identified. Most cells were of class one: they took
up the DNA and expressed the selectable marker genes, but only transiently.
These protoplasts did not maintain the DNA, and soon died following the
application of the selective agent (typically an aminoglycoside antibiotic,
such as hygromycin or G418). The second class of transformant prospered
on selective medium, but if the selective pressure was withdrawn the transgenic colonies failed to survive a subsequent exposure to selection. These
so-called ‘‘unstable’’ transformants are thought to maintain the transforming
DNA in an extrachromosomal form, such that following the relaxation of
selection this DNA was lost from the cells. It was subsequently demonstrated
that this transforming DNA could be maintained for very long periods (years),
as extrachromosomal arrays of concatenated plasmid DNA, so long as selection
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Fig. 5.2. ‘‘Inverse PCR’’: a method for the identification of insertionally mutagenized
genes. DNA is isolated from an insertionally mutated plant (I) and is digested with
a number of restriction enzymes that have defined recognition sites not found
within the inserted DNA (II). The digested DNA is diluted and incubated with DNA
ligase (III); ligation takes place between the ends of DNA molecules in closest proximity,
and at low DNA concentration these are the two ends of the same molecule. This
results in the formation of a population of circular molecules. PCR amplification with
‘‘outward-pointing’’ primers corresponding to the inserted DNA (IV) will amplify the
flanking genomic sequences. These can then be readily identified by DNA sequence
analysis.
5 Mosses as model organisms
was continuously maintained (Ashton et al. 2000). The third class of transformant (and the least numerous) continued to exhibit the transgenic selection
marker following several cycles of alternating subculture on selective and
non-selective medium, and were demonstrated by Southern blot analysis to
have incorporated the transforming DNA covalently into the moss genome.
Typically, the incorporated DNA corresponded to concatenated repeats of the
plasmid DNA inserted at one or a few loci. Stable integration of transforming
DNA is favored by transformation with linear fragments of DNA, whereas
transformation with circular plasmids results in a preponderance of transformants of the ‘‘unstable’’ class.
The development of a reliable transformation procedure stimulated research
into the development of an insertional mutagenesis technique that could be
used to create tagged mutants, thereby enabling the cloning of the genes underlying developmental transitions. At this time, the characterization of a number
of transposons active in maize suggested that the Ac/Ds transposition system
might be particularly effective, since this system could be transgenically
imported into Arabidopsis for gene tagging (Long et al. 1993). In maize, these
transposable elements are actually two different forms of the same transposon
(McClintock 1948, Coupland et al. 1988). The Ac (‘‘Activator’’) element is an
autonomous transposon that encodes a transposase responsible for recognition of the terminal repeats that delimit the transposon, excising the element
from its genomic locus, and subsequently causing its reinsertion at another
(usually linked) genomic locus. The Ds (‘‘Dissociator’’) element is an internally
deleted variant of Ac. It retains the terminal repeats that are the target for
the transposase activity, but does not encode an active transposase element.
The Ds element is not autonomously active, and is unable to cut itself out and
reinsert elsewhere. Thus plants that carry a Ds element inserted within their
genome are genetically stable (Coupland et al. 1988). This genetic system has
been exploited within the Arabidopsis community by the construction of
a number of independent transgenic lines carrying single copies of the Ds
element at different transgenic loci scattered around the genome. These genetically stable lines can be mutagenized by introducing a second transgenic construct, carrying an active transposase gene derived from the Ac element.
Expression of the transposase results in mobilization of the resident Ds elements and the consequent generation of a new series of insertion mutants
(Muskett et al. 2003).
It seemed not unreasonable that this system might also function in
Physcomitrella, as a means of creating tagged insertional mutants, with the
added advantage that if the Ac transposase were to be introduced on an unstably
maintained plasmid to a stably transformed line carrying the Ds element, then
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the Ds element could be mobilized to a new genetic locus, and then stabilized
there as a consequence of the subsequent loss of the Ac transposase gene
upon the relaxation of selection.
The generation of stably transformed lines containing the Ds element did
not prove problematic, it being delivered on a transgenic plasmid that also
conferred resistance to the antibiotic kanamycin (or G418), and integrating
stably into the genome. Introduction of the Ac transposase on a second plasmid,
conferring resistance to hygromycin, did indeed mobilize the Ds element, but
although it appeared to be excised from the genome it was not re-inserted
elsewhere (D. J. Cove, pers. comm.). Thus the maize transposition system did
not function in Physcomitrella in the same way as it did in higher plants. However,
it appeared that the frequency with which stable hygromycin-resistant transformants were generated following retransformation of the G418-resistant Ds
lines was significantly higher than expected. Certainly it was higher than the
rate at which the hygromycin-resistance-carrying plasmid generated stable
transformants in previously untransformed lines.
This led to the hypothesis that the second plasmid, which shared substantial lengths of sequence homology with the first transforming plasmid (both
constructs used the same basic cloning vector), might be becoming preferentially integrated in the genome by homologous recombination with the first
transgenic locus, a hypothesis that was subsequently strengthened by genetic
analysis of double transformants. Both the hygromycin-resistance and G418
resistance markers were found to co-segregate in independent sexual crosses,
indicating their close linkage in the genome (Kammerer & Cove 1996).
Molecular confirmation of the occurrence of homologous recombination
was provided by Schaefer & Zrÿd (1997) who analyzed the insertion of a number
of recombinant plasmids carrying fragments of cloned Physcomitrella DNA.
Southern blot analysis of a number of transgenic lines conclusively demonstrated that these constructs were preferentially targeted to the homologous
loci with very high efficiency: in some transgenic lines, 100% of the stable
transformants resulted from integration of the transforming DNA into the
targeted locus. Additionally, there was an apparent association of targeting
efficiency with the length of homology between the targeting construct and
the targeted locus. Moreover, targeting was precise, and both genomic DNA
sequences and cDNA sequences could be used to build targeting constructs.
Thus, when a member of a highly homologous multigene family (a gene encoding a light-harvesting chlorophyll a/b protein) was used in a targeting experiment, it was found to target exclusively the cognate member of the gene family,
and not the other family members, despite their very high nucleotide sequence
similarity (Hoffman et al. 1999).
5 Mosses as model organisms
Gene targeting does not occur efficiently in higher plants. The rates that have
been detected in Arabidopsis are of the order of 10–3 or lower (Kempin et al. 1997,
Hanin et al. 2001, Hanin & Paszkowski 2003). The rates of gene targeting seen in
Physcomitrella are more reminiscent of those that occur in the yeast Saccharomyces
cerevisiae, in which gene targeting is routinely used as a way of generating novel
mutant alleles, either by the disruption of specific genes or by the replacement
of wild-type alleles with variants containing defined point mutations (OrrWeaver et al. 1981). This provides a very powerful and sophisticated means
of genetic manipulation, and the significance of this was not lost on the
Physcomitrella community. The first mutant phenotype generated by gene targeting in moss was the disruption of the ftsZ gene: a nuclear-encoded chloroplast
tubulin, the homologous recombination-mediated knockout of which resulted
in the failure of chloroplast division, and the presence in each cell of a single
large chloroplast (Strepp et al. 1998). Since that first demonstration of the utility
of gene targeting in Physcomitrella, there has been a burgeoning of interest and
activity, with the construction of large ‘‘knock-out’’ mutant collections generated by high-throughput transformation using randomly disrupted cDNA and
genomic fragments (Egener et al. 2002, Schween et al. 2005) and the development
of specific ‘‘knock-in’’ lines in which reporter genes are fused to specific gene
sequences for targeting to the corresponding loci (Nishiyama et al. 2000).
The availability of the complete genome sequence will further enable the
functional analysis of specific genes through the ‘‘reverse genetic’’ route: the
creation of defined mutants in specific genes to determine the details of their
regulation and function. A series of overriding questions remain. What is it
about Physcomitrella that causes it to preferentially incorporate DNA by homologous recombination at specific sites, rather than randomly as occurs in flowering plants? What is the mechanism by which homologous recombination
occurs? Can we identify the components that undertake homologous recombination in Physcomitrella, and use this knowledge to inform attempts to develop a
high-frequency gene targeting technology for crop species?
5.6
Homologous recombination and DNA repair
The incorporation of exogenously supplied DNA into the genome is not
a normal plant function. It is generally agreed that when transforming DNA is
incorporated into a genome, the mechanisms responsible for its integration are
those that are more commonly used for the repair of DNA damage (Schaefer
2001). The maintenance of the integrity of the genome is essential for the
survival of all organisms, and a plethora of DNA damage repair systems are
known to exist. The most catastrophic form of DNA damage that a cell can suffer
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is a double-strand break of the DNA. If both strands of the DNA are broken at the
same site in a chromosome, and these are not repaired, then the loss of the
telomeric fragment will occur. To prevent this, eukaryotic cells have developed
two pathways for the repair of double-strand breaks that occur both as a consequence of environmental agencies (radiation or genotoxic chemicals) and
routinely during DNA replication. These pathways are highly conserved
among eukaryotes (Schuerman et al. 2005) but have been most exhaustively
characterized in yeast (Fig. 5.3). They involve either non-homologous end joining between fragments (NHEJ: the ligation of two broken ends (Weterings & Van
Gent 2004) or homologous recombination-mediated repair, in which the broken
ends are repaired using a homologous chromosome as a template for repair
(Aylon & Kupiec 2004). The frequency with which ds-DNA breaks occur during
DNA replication, and the requirement to use the homologous chromosome as a
template for HR-mediated repair, means that DNA damage repair by homologous recombination is usually tightly correlated with the cell cycle: DNA
damage typically imposes a cell-cycle arrest at the G2/M boundary, during
which ds-DNA breaks can be repaired before the cell is allowed to divide (Lisby
et al. 2004, Lisby & Rothstein 2004). Consequently, it is significant that in
Physcomitrella protonemal cultures the majority of the cells have been shown
to be arrested in G2, and to contain the 2C complement of DNA (Schween et al.
2003). Most of these cells will be postmitotic subapical cells, and it has been
proposed that if these contribute a major proportion of the protoplasts used for
a transformation experiment, then the machinery may be already in place for
the integration of transforming DNA by homologous recombination in the
majority of protoplasts. Arrest at this stage of the cell cycle can also be seen to
be a good strategy for survival for cells of a haploid organism, since the two
copies of the genome will provide templates for each other’s mutual repair of
ds-breaks should they occur as a consequence of the organism’s experiencing
genotoxic stress.
The most efficient way to generate a gene targeting event is to transform
protoplasts with linear fragments of DNA, rather than with circular plasmids.
Although many of the first Physcomitrella transformation studies utilized supercoiled plasmids, it became clear that such molecules typically generated a very
high ratio of unstable to stable transformants, whereas stable transformation
was favored by the use of linear fragments. It is probable that when linear DNA
fragments enter a cell their termini are recognized by the cellular DNA repair
machinery as double-strand breaks. The very large number of such fragments
that a cell will take up in the course of a transformation experiment would be
recognized as a catastrophic number of ds-breaks, and is likely to elicit a massive
DNA damage-repair response by the cell.
5 Mosses as model organisms
Fig. 5.3. Pathways of DNA repair by NHEJ and HR. The following model is based on our
knowledge of DNA damage repair in yeast and mammalian cells, and for NHEJ, in Arabidopsis.
A double-strand break in DNA can be repaired either by NHEJ or by HR. The first step in both
pathways is the binding of the broken termini by the Mre11–Rad50–XRS1 (‘‘MRX’’) complex.
For the NHEJ pathway, this complex tethers the broken ends. NHEJ proceeds through the
interaction of the broken ends of the DNA with the Ku70 and Ku80 proteins, then the
broken ends are ‘‘polished’’ and rejoined by DNA ligase IV. This can result in either small
sequence rearrangements at the point of ligation, or the random joining of DNA sequences of
different genomic origin. HR occurs by resection of the DNA to generate a 30 -ss overhang,
followed by recruitment of the Replication Protein A complex to the 30 -ss DNA, before the
Rad52 protein acts to catalyze its replacement by the Rad51 protein. This forms a
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Both the NHEJ and HR pathways of DNA repair have a shared initial component. Double-strand breaks are recognized by a protein complex known as
the ‘‘MRN’’ complex in mammalian cells (MRX in yeast) (Krogh & Symington
2004). This complex binds to the ends of the DNA and cross-links adjacent DNA
strands. A first consequence of this is most likely to prevent the two fragments
generated by the ds-break from drifting apart (Stracker et al. 2004). Fragments
whose ends are held together in close proximity to one another by the MRN
complex can thus be rejoined by NHEJ, following the recruitment of a complex
of specific proteins and ligases (Ku70, Ku80, and DNA ligase IV/XRCC4; Daley
et al. 2005).
Because NHEJ is a very rapid process, NHEJ is likely to be the predominant
event in the first stages of transformation, and results in the concatenation of
the transforming DNA. Certainly, concatenated DNA is frequently found integrated in the moss genome following transformation, both at loci where adventitious insertion of the transgenic DNA has occurred, and following integration
at targeted loci (Kamisugi et al. 2006). When DNA repair in yeast is effected by the
homologous recombination pathway, cell cycle checkpoint activation occurs,
and the ends that are bound by the MRN complex become resected, to generate
long 30 -single-stranded overhangs. This commits the cell to HR-mediated repair.
The single-stranded ends become coated with another protein complex: the
trimeric Replication Protein A (RPA complex). In yeast and mammalian cells,
the subsequent stages of HR-mediated DNA repair utilize a series of gene products encoded by a group of genes defined as the ‘‘Rad52 epistasis group’’ (Krogh &
Symington 2004). Originally identified in yeast as a group of interacting genes
defined by radiation-sensitive (DNA repair-deficient) mutant phenotypes, these
genes encode a number of proteins required for homologous recombinationmediated DNA repair. The Rad52 gene product is a crucial component in this
process, since it is responsible for interacting with the RPA-coated singlestranded DNA end and recruiting the Rad51 gene product to replace the RPA
complex, to form a nucleoprotein strand that is capable of invading an intact
DNA double helix and annealing with its complementary sequence (Benson et al.
Caption for Fig. 5.3. (cont.)
nucleoprotein filament, stabilized by other products of the Rad52 epistasis group genes (Rad55
and Rad57), that is able to invade a homologous duplex DNA. Unwinding of the duplex DNA is
facilitated by the Rad54 DNA unwinding activity. The invading strand can then be extended by
copying the invaded template sequence. The details of the HR pathway in plants are not known,
but must differ in detail, since plants lack a recognizable RAD52 gene.
5 Mosses as model organisms
1998, New et al. 1998, Shinohara & Ogawa 1998). Rad 51 is highly conserved in
evolution, being the eukaryotic equivalent of the bacterial RecA protein.
Typically there are several paralogous Rad51 genes in eukaryotes, all of which
have counterparts in Physcomitrella. Interestingly, in Physcomitrella, there are two
copies of the RAD51 gene encoding the principal ss-DNA-interacting protein
(Markmann-Mulisch et al. 2002) which show relatively higher levels of expression in the apical cells of protonemal filaments. (This is not surprising, since the
highest incidences of DNA double-strand breakage are expected to occur in
mitotically active cells.) The genes are redundant in function, knockout mutants
of each having no phenotypic effect, whereas the double-mutant shows a highly
radiation-sensitive phenotype, and is additionally meiotically defective (B. Reiss,
pers. comm.). Most interesting is that an examination of higher plant genome
sequences reveals no homolog of the RAD52 gene. Since in both yeast and
mammalian cells this gene is essential for the formation of an invasive DNA
strand, it suggests that plants use an alternative mechanism for homologous
recombination-based DNA repair. The Physcomitrella genome also lacks a RAD52
homolog, so it remains an open question as to how homologous recombination
occurs in plants. The readiness with which Physcomitrella incorporates transforming DNA by HR implies that homologous recombination is the default
pathway for DNA repair, recommending it as a model for studies of this essential
process.
Our understanding of eukaryotic HR processes stems largely from mutational analyses in yeast. In particular, the characterization of the DNA damagedeficient Rad mutants revealed the identity of all the components of the
HR-mediated DNA repair pathway. The homologs of these genes can be identified
in many organisms, and in recent years the availability of T-DNA insertion
mutants of most Arabidopsis genes has spawned a number of ‘‘reverse genetic’’
analyses of DNA repair processes in mutants of the known DNA repair-related
genes. However, these have failed to shed any significant light on the process of
HR, probably for two reasons. First, because Arabidopsis, like all higher plants, is
largely incompetent to undertake HR, and second because there are some
key differences in the regulation of the process between yeast and plants, such
as the absence of an obvious homolog of Rad52. If we are to identify novel,
plant-specific components, the best way forward is to apply the power of
mutational analysis in a ‘‘forward genetic’’ screen. This must necessarily be
undertaken in an organism in which the HR-mediated DNA repair pathway
predominates over the NHEJ-mediated pathway. Only Physcomitrella offers this
opportunity. Thus, this is one fundamental plant process in which mosses
may be more useful than the otherwise ubiquitous Arabidopsis as an experimental
platform.
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5.7
Homologous recombination for reverse genetics
‘‘Reverse genetics’’ is the term given to the deduction of gene function,
starting with knowledge of the sequence of a gene. Certainly, gaining an understanding of the mechanism of homologous recombination has intrinsic fascination, as well as ultimate strategic relevance. However, the process can also
directly be used for the manipulation of the moss genome without recourse to
a detailed knowledge of the precise mechanism. Gene knockouts and ‘‘knockins’’ provide tools by which gene function can be studied.
By using homologous recombination, one can construct reporter gene fusions
that enable the activity of promoters to be tested within their original genomic
context (unlike promoter analyses in which fusion constructs are tested in
transient expression experiments, or following the stable, but ectopic insertion
of transgenes). This enables observation of the cellular dynamics of individual
gene products by in vivo imaging of proteins fused to fluorescent proteins
(such as the jellyfish Green Fluorescent Protein (GFP) and its numerous spectral
variants CFP (cyan) ,YFP (yellow), RFP (red), etc.) in conjunction with high resolution laser-scanning confocal microscopy. One may also examine interactions
between gene products in vivo by using proteins fused to (i) different fluorescent
reporters in techniques such as FRET (fluorescence resonance energy transfer) or
(ii) to individually non-functional but combinatorially active fluorescent reporters (bimolecular fluorescence complementation: BiFC), and to isolate native
multiprotein complexes from cells by ‘‘pull-down’’ experiments following the
construction of fusion proteins by ‘‘knock-in’’ of affinity tags or specific epitopes.
5.8
Requirements for efficient gene targeting
All of these procedures require a minimal knowledge of the requirements
for efficient gene targeting that boil down to a small number of requirements:
*
*
*
*
*
*
What is the optimal length and design for a gene targeting construct?
What is the best method of DNA delivery and selection of transformants?
How can mutant lines containing targeted genes most conveniently be
identified?
What analyses are necessary to confirm that a mutation is responsible
for an observed phenotype?
What is the best way of obtaining multiply mutated lines? (For example,
in cases where the existence of a family of similar genes suggests that
there may be extensive redundancy.)
Can gene targeting methodologies be applied to other moss species, or
is it only possible in Physcomitrella?
5 Mosses as model organisms
5.8.1
Length and design
For a knockout construct, with the intention to inactivate a Physcomitrella
gene, the DNA used for transformation should be a linear fragment, corresponding to the 50 - and 30 -terminal sequences of the gene, interrupted by a selection
cassette: typically an antibiotic resistance gene driven by a constitutively active
promoter. The most frequently used cassettes comprise a bacterial nptII gene
conferring resistance to kanamycin or G418, under the control of the CaMV
35S promoter, and either a nopaline synthetase or CaMV-derived transcription
terminator. Such cassettes are approximately 2 kb in length. Since linear fragments for transformation are most easily generated in highly pure form by PCR
amplification, the overall length of the fragment should not exceed 4 kb, since
fragments larger than this are less easily amplified. In a study of the minimum
length requirements for high-frequency targeting, flanking targeting sequences
of c. 500 bp each were sufficient to achieve a frequency of allele replacement
of 50% of total transformants (Kamisugi et al. 2005). Flanking sequences 1 kb in
length can generate gene targeting events in up to 100% of the stable transformants recovered. To ensure that a knockout of gene activity is achieved, it is
recommended that a significant length of the coding sequence should be
replaced by the selection cassette. Either genomic DNA or cDNA sequences can
be used in the construction of targeting constructs, but no rigorous comparison
between the efficiencies achieved with such constructs has been made. It has
been suggested that for targeting sequences of less than 300 bp a cDNA-based
vector may target its cognate locus with higher efficiency than the corresponding
genomic sequence of the same length, if the cDNA sequence comprises a number
of exons. However, this remains to be tested.
5.8.2
DNA delivery
DNA can be delivered either by polyethylene glycol-mediated protoplast transformation (Schaefer et al. 1991) or directly to intact tissue by particle
bombardment (Sawahel et al. 1992). Both procedures are suitable for obtaining
targeted gene knockouts, although our experience indicates that gene targeting
is approximately two to four times as efficient (in terms of the percentage of
transformants that exhibit allele replacement) using protoplast transformation.
However, protoplast transformation and regeneration is a more technically
demanding procedure, requiring high skill levels in tissue culture to achieve
high transformation efficiencies. Protoplasts are produced by digesting protonemal tissue with the enzyme ‘‘Driselase’’, a commercially available cocktail of
fungal cellulases. The cell walls of protonemal filaments are readily digested
by the enzyme preparation, releasing protoplasts which are prevented from
undergoing osmotic lysis by maintaining them in an isotonic concentration of
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mannitol. Individual protoplasts retain their totipotency, being able to regenerate, initially as chloronemal filaments, and then subsequently to reiterate all the
stages of normal Physcomitrella development to generate whole plants. Although
protoplast regeneration is very efficient in the hands of a skilled tissue culture
worker, it may take some time to master the technique. Consequently biolistic
transformation may be preferable for investigators with less experience of plant
tissue culture.
‘‘Biolistic’’ transformation is the delivery of transforming DNA into intact
tissues by bombardment of the tissue with microprojectiles. These are small
(1 mm diameter) particles of an inert metal (gold or tungsten) that can be coated
with DNA and delivered by using a commercially available instrument (for
example, the BioRad PDS1000 microprojectile bombardment device). Tissue
bombarded in this way can be directly submitted to selection for transformed
cells by incubation on the appropriate selective medium without any need for
extensive manipulation, in culture.
5.8.3
Identification of gene-targeted mutants
PCR amplification of the targeted locus provides the most rapid assessment of the outcome of a gene targeting experiment (Fig. 5.4). Typically, following DNA delivery to protoplasts, the cells are allowed to regenerate in the
absence of selection for a period of 4–5 days, before transfer to selective medium
for two weeks. This is sufficient to kill off the untransformed cells, and the small
colonies that survive are then subcultured onto non-selective medium for a
further two weeks, in order to allow the loss of unintegrated DNA from
‘‘unstable’’ transformants. Stably transformed plants are identified as those
that continue to grow, two weeks following their return to selective conditions.
They can then be permanently grown on non-selective medium (Knight et al.
2002). At this stage the colonies are still small, and a further two to four weeks’
growth may be necessary until a colony has grown to a size sufficient for the
isolation of DNA for PCR analysis. DNA from transformants is analyzed by PCR
with a pair of gene-specific, inward-pointing primers that anneal to sequences
that lie outside the sequence used in the targeting construct. When these are
used with outward-pointing primers that anneal to the selection cassette, it is
possible to identify amplification products that result from homologous recombination events that occur (i) only between the 50 -arm of the targeting construct
and its target in the genome, (ii) only between the 30 -arm of the construct and its
target in the genome, and (iii) between both the 50 - and 30 -arms of the targeting
construct and their targets in the genome. If no amplification is seen, it is
indicative that the targeting construct has integrated adventitiously, elsewhere
in the genome. Only where amplification occurs for both ends of the targeting
5 Mosses as model organisms
Fig. 5.4. Assaying gene targeting in Physcomitrella. A linear targeting construct containing two
sequences (‘‘a’’ and ‘‘c’’) corresponding to the 50 - and 30 -terminal sequences of the target gene
‘‘a-b-c’’. Sequence ‘‘b’’ is replaced in the construct by a selectable marker cassette.
Homologous recombination at the 50 -end of the targeted gene is assayed by PCR by using
the external gene-specific primer ‘‘pX’’ in combination with the selectable marker primer
‘‘pM1’’. Homologous recombination at the 30 -end of the targeted gene is assayed by PCR by
using the external gene-specific primer ‘‘pY’’ in combination with the selectable marker
primer ‘‘pM2’’. The results of such a targeting assay are shown in the agarose gel photograph.
Tracks marked with open circles correspond to transgenic lines targeted at the 50 -end only.
The track marked by a filled grey circle corresponds to a transgenic line targeted at the 30 -end
only. Tracks marked by filled black circles indicate transgenic lines where targeted gene
replacement has occurred. The track marked by a crossed circle derives from a transgenic line
where integration of the transgene occurred elsewhere, in an untargeted region of the
genome.
construct has an allele replacement event occurred. Such events are termed
‘‘targeted gene replacements’’ (TGRs) (Kamisugi et al. 2005, 2006). Where targeting has occurred in only one arm of the construct, this may cause a gene
disruption (depending on the design of the construct), but not necessarily so.
In these cases, ‘‘targeted insertion’’ (TI) has occurred (Fig. 5.5). This results from
concatenation of the transforming DNA in the cell, prior to its integration into
the targeted locus, and occurs as a consequence of homologous recombination
between the targeted sequence in the genome and two repeated identical
sequences in the concatemer (Kamisugi et al. 2006). As noted earlier, concatenation of transforming DNA is a common occurrence when large numbers of
linear molecules are delivered to a protoplast, and TGR events include both
single-copy replacement of the targeted locus and replacement by multiple,
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Fig. 5.5. Targeted insertion in Physcomitrella. Targeted insertion occurs by concatenation of
(1) the transforming DNA. Here, (2) head-to-tail concatemers are integrated by (3) homologous
recombination between the 50 -end of the targeted gene (sequence ‘‘a’’) by homologous
recombination between this sequence and two repeated sequences ‘‘a’’ in the concatemer. This
was demonstrated by sequencing the DNA integration junctions in transgenic lines resulting
from transformation by using a targeting construct carrying non-homologous termini:
sequences ‘‘1’’ and ‘‘2’’ in the targeting construct (Kamisugi et al. 2006).
concatenated copies of the targeting construct. Both will result in gene knockouts, but analysis of single-copy gene replacements is preferred. These can be
identified by PCR amplification of the targeting cassette from the targeted locus
by using the pair of external, gene-specific primers, and typically account for
25–50% of TGR transformants (Kamisugi et al. 2005).
5.8.4
Confirmation that a targeted mutation causes a mutant phenotype
It is clearly important to ensure that any mutant phenotype identified
in the course of a gene targeting experiment results directly from the disruption
of the targeted gene, and is not a consequence of some other event. The first
priority is to ensure that a targeted gene replacement has not been accompanied
by an additional, adventitious insertion of the targeting construct at another
locus. This is most conveniently achieved by Southern blot analysis. Previous
investigations of the incidence of adventitious incorporation of targeting fragments indicate that this occurs, but at a relatively low frequency: only c. 20% of
transgenic plants exhibiting single-copy TGRs contain additional copies of the
transgene inserted elsewhere in the genome (Kamisugi et al. 2005). Non-targeted
5 Mosses as model organisms
insertion of DNA is a more serious problem where targeting fragments have
been isolated from a plasmid vector by restriction enzyme digestion, and not
subsequently separated from the vector backbone prior to moss transformation.
Although not carrying selectable marker genes, adventitiously inserted plasmid
DNA can often be detected in transgenic moss (Kamisugi et al. 2006) and consequently the use of PCR-amplified DNA is preferable for the generation of the
transformation construct.
Even where a highly pure fragment has been delivered, and is shown to have
inserted very precisely by single-copy TGR at the targeted locus alone, there is a
possibility that a mutant phenotype might derive from a tissue-culture-induced
artefact. Somaclonal variation is a well-attested phenomenon among plants
derived from tissue culture, and likely arises through the stress-activation of
retrotransposons (Soleimani et al. 2006). Since the Physcomitrella genome contains retrotransposon sequences, it would be surprising if some were not to be
mobilized during protoplast regeneration, with unforeseeable consequences.
Consequently, analysis of a mutant phenotype is better not to be restricted to a
single individual mutant line. If many appropriately targeted independent
transformants are identified in the course of a transformation experiment,
then as large a number of them as is convenient should be phenotypically
analyzed to ensure the association of the phenotype with the targeted gene. If
this is not possible, then an alternative means of verification should be undertaken. This could include crossing the transgenic line with a wild-type strain, in
order to determine whether the mutant phenotype and the transgene (the
selectable marker) co-segregate. Alternatively, retransformation of the mutant
with a wild-type gene should be undertaken to demonstrate that the wild-type
phenotype can be restored by complementation.
5.8.5
Analysis of a multigene family
Many genes are members of paralogous multigene families, in which
the individual gene family members may have redundant, overlapping, or
partially redundant functions. In such cases, the targeted knockout of a single
family member may not generate a mutant phenotype, or may have an effect
whose impact is too subtle to be easily recognizable. In such cases, combinatorial mutagenesis may be required to reveal the relationships between the genes.
Transformation with a construct corresponding to one member of the family
appears not to target other members of the same family, even if they are only
slightly divergent: such ‘‘homeologous targeting’’ is suppressed by the endogenous mismatch repair mechanism (Trouiller et al. 2006). In such cases, a series of
targeting constructs, specific to each member of the gene family, will have to be
prepared. These can be used either individually, to create a series of transgenic
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lines in which each gene family member is mutated following a single-copy
TGR event, or combinatorially, in which a number of different gene-specific
targeting constructs are simultaneously delivered in the same transformation
(co-transformation: Hohe et al. 2004). In co-transformation, the incidence with
which multiple transformed lines are obtained is probabilistically determined
from the frequencies with which the individual genes are targeted. Both
approaches have their merits and difficulties.
The first approach requires that combinations of mutants be assembled,
either by crossing independent lines, or by retransformation with a second
gene-specific targeting construct. In the former case, the process of establishing
sexual crosses may be time-consuming (approximately 3 months are required to
identify hybrid sporophytes): however, this method was used successfully to
generate plants doubly mutant for the PpRAD51 genes (B. Reiss, pers. comm.).
For retransformation, it is necessary either to use a second selectable marker, or
to first remove the selectable marker used in the construction of the recipient
strain. Marker removal can readily be achieved by using the ‘‘Cre-lox’’ system
(Kuhn & Torres 2002). This is a technique of site-specific recombination derived
from the bacteriophage P1 that enables the insertion and excision of the bacteriophage genome into and out of the genome of a bacterial host. The Cre gene is a
site-specific recombinase (its name derives from ‘‘cyclization recombination’’) that
recognizes a specific 34 bp sequence called loxP (for ‘‘locus of X-over in P1’’).
Essentially, if a DNA sequence within a genome is flanked by two direct copies of
the loxP sequence, then the action of the Cre recombinase can recombine these two
sites, resulting in the deletion of any intervening sequence. This can be exploited to
remove a selectable marker from within the moss genome, if the selectable marker
in a targeting construct is flanked by loxP sites. By introducing a second plasmid
carrying the Cre gene, under the control of a constitutively active promoter, the
transient expression of the Cre recombinase (for example in an unstable transformant), will cause the deletion of the selection cassette (Trouiller et al. 2006).
In cotransformation experiments, a large number of transgenic lines may
have to be screened in order to identify suitably targeted plants containing no
adventitious transforming DNA.
A third approach to generating mutants defined by the inactivation of multiple related genes is to use an RNAi-interference (RNAi) approach. Sequence
similarity between closely related genes is most strongly conserved within the
mRNA coding sequences, whereas intron sequences are usually highly divergent. Multiple related mRNAs can be subjected to RNAi-mediated ‘‘knockdown’’, and the construction and use of such RNAi expression vectors has
recently been demonstrated for Physcomitrella (Bezanilla et al. 2003, 2005). This
approach has the additional advantage that it can be used to deplete cells of
5 Mosses as model organisms
specific mRNAs through the expression of the RNAi construct under the control
of an inducible promoter, thereby providing a means of interfering with the
expression of genes whose permanent knockout might prove lethal.
5.8.6
Is gene targeting generally applicable?
Although proponents of Physcomitrella frequently refer to this organism’s unique ability, among plants, to undertake homologous recombinationmediated gene targeting at high frequency, this is actually not a true statement.
There is no reason not to expect that this property is shared, if not by all, then by
a significant number of other moss species, and that the technique of gene
targeting should therefore be applicable to a number of species that offer
particular experimental advantages that Physcomitrella does not. Thus Ceratodon
purpureus has been more widely used for the study of gravitropic responses,
because it exhibits more vigorous growth in darkness than does Physcomitrella,
whereas the desiccation-tolerant properties of Tortula ruralis commend it as a
model for the study of anhydrobiosis.
Indeed, it has already been demonstrated that gene targeting can be undertaken in C. purpureus by the elegant targeted ‘‘knock-in’’ repair of a point mutation
in the haem oxygenase gene, required for phytochrome synthesis and the phototropic response (Brücker et al. 2005). The particular disadvantage of other species,
relative to Physcomitrella, is their comparative lack of genomic resources. With
the availability of the Physcomitrella genome sequence, any gene can be readily
amplified and mutagenic targeting constructs generated. However, it is possible
to use the Physcomitrella genome sequence as a springboard for the isolation of the
corresponding genes in other moss species. Homology-based searches of the
existing sequence databases frequently demonstrate that Physcomitrella genes
have significantly greater sequence homology with that small number of gene
sequences that have been derived from other bryophytes, than with the very
much greater number of angiosperm sequences. For example, BLAST searches
with Physcomitrella sequences encoding LEA (late embryogenesis abundant) proteins implicated in desiccation tolerance frequently identify more similar
sequences from the liverwort Riccia fluitans than from angiosperms, and comparisons between cDNAs from Physcomitrella, Ceratodon and Tortula exhibit nucleotide
sequence identities of 80%–95% within the protein coding regions. This level of
sequence identity is sufficiently high to suggest that Physcomitrella sequences can
be used either as hybridization probes to select genes from DNA libraries of other
moss species without difficulty (my laboratory has cloned a number of Ceratodon
genes in this way), or for the design of degenerate PCR primers for the direct
amplification of desired genes. For Ceratodon purpureus, both cDNA and genomic
DNA libraries are available through the Leeds Physcomitrella EST Programme.
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5.9
Mosses and the study of development
The beginning of the twentieth century marked the invention, in
Britain, of a model construction kit called ‘‘Meccano’’. It gained massive popularity as a present for (almost exclusively) boys in order to inculcate them with
a love for what was then the mainstay of the British economy: heavy engineering. The kit comprised a selection of strips, sheets, and brackets of perforated
metal that could be fixed together with small nuts, bolts and washers. A handy
12-year-old could use a small selection of the same basic parts to construct all
manner of structures: railway engines, cranes, model cars, bridges. Generations
of middle-aged men (although not the author, who was distinctly unhandy) have
fond recollections of childhood hours spent piecing together some miniature
marvel of civil engineering.
‘‘Meccano’’ provides an apt metaphor for the way in which evolution has used
a limited number of molecular components in order to construct a diverse array
of living structures. The diversity of life, and the different developmental strategies that are displayed by organisms from widely different taxa, are all based
on their particular specialized use of a largely identical set of gene products. This
is particularly true of those gene products that act as the central regulators
of developmental processes: receptors, signal transduction components, and
transcription factors. Understanding how such essentially similar components
can be differently assembled to carry out very different functions is at the heart
of comparative approaches to the study of developmental programming. ‘‘EvoDevo’’ is the Meccano of biology.
This is exemplified by the evolution of transcriptional control networks
crucial to plant development. Development in plants, as in all complex multicellular organisms, is under close genetic control. Thus a fertilized egg cell
divides, proliferates, and undergoes cellular differentiation to generate a
three-dimensional structure with an architecture that is characteristic of its
particular species and that can be modified or disrupted by mutations in genes
that regulate the process. However, at the same time, plant morphogenesis
exhibits a high degree of plasticity, whereby the genetic programming of the
formation of specific structures is responsive to external cues. Thus the timing
of particular processes, for example flowering, may be determined by external
stimuli such as light or temperature. Directional growth responds to light and
gravity vectors, and to nutrient availability, and the ultimate size of the ‘‘adult’’
organs of a plant – for example the leaves – may depend on responses to external
forces such as grazing. Such plasticity is a necessary adaptation for organisms
with a sessile growth habit that are inescapably subject to the vagaries of the
environment.
5 Mosses as model organisms
Moreover, unlike development in animals, where morphogenesis frequently
entails gross changes in cellular organization brought about by the movement
of cells relative to each other (gastrulation being a striking example), the architecture of plants is constrained by the specific properties of the plant cell: in
particular its enclosure within a relatively rigid cell wall. Thus generation of a
specific three-dimensional structure is entirely dependent on processes that
control the orientation of the planes of cell division, the direction of cell
expansion, and the extent of cell expansion. We can add to this complexity,
different responses by plant cells to internal morphogenetic cues. Plant cells
exhibit a high degree of totipotency, especially when compared with animal
cells. Upon tissue culture, cells of many apparently terminally differentiated
organs can become dedifferentiated and recapitulate an organogenic pathway
via somatic embryogenesis in response to simple manipulation of the concentrations of morphogenetically active substances (plant hormones).
The experimental dissection of these processes can be challenging, particularly
where they involve the concerted action of groups of cells that must become
organized into a particular structure through intercellular communication. Thus,
our current models for the formation and maintenance of complex structures
such as the root and shoot meristems of flowering plants rely on the identification
through mutagenesis of ‘‘master genes’’ that regulate developmental processes,
and the identification and analysis of their ‘‘subject genes’’ by using promoter
fusions with reporter genes such as the E. coli b-glucuronidase (GUS) gene, or vital
reporters that permit gene expression analysis in vivo, in real time, such as the
green fluorescent protein (GFP) and its variants. These powerful experimental
tools for the study of plant developmental processes have all developed as a
consequence of the intense focus on the model plant Arabidopsis thaliana. The
availability of molecular genetic resources – in particular the ability to undertake
mutagenic interrogation of the plant to identify genes responsible for specific
mutant phenotypes by genetic linkage, coupled with the availability of a fully
sequenced genome – has been the principal force in driving this understanding.
The deployment of such experimental approaches is now possible in mosses,
using the resources that are accumulating for Physcomitrella. Moreover, there are
certain advantages that Physcomitrella offers that have few parallels in Arabidopsis.
Although the ability to conduct precise genetic manipulation by gene targeting
offers one such advantage, it is arguably an even greater advantage that the
architecture of Physcomitrella lends itself to the analysis of processes that take
place at the level of the single cell in a way that is not possible in multicellular
plant organs.
For much of its life, Physcomitrella can be regarded as an organism that is one
cell thick. The protonemata comprise filaments made up of single cells joined
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end-to-end. These are readily observed by using high-resolution in vivo imaging,
by laser-scanning confocal microscopy. The gametophores, although threedimensional structures, derive from a primordium (the ‘‘bud’’) in which the
meristematic architecture can be readily examined microscopically, and the
leaves themselves are only one cell in thickness, with the possible exception
of the differentiated midrib cells. This reinforces the facile comparison between
Physcomitrella and Caenorhabditis, the latter having achieved prominence as a
model organism in part through its particular amenability to microscopic visualization of every cell in its body.
5.10
The evolution of transcriptional networks
The ‘‘Meccano’’ analogy is most strikingly demonstrated in the way in
which transcriptional networks have evolved in plants. Comparative analysis of
different taxa – including mosses – demonstrates how different groups of transcription factors have selectively been used. One such example is discussed in
Chapter 7 of this volume: the evolution of desiccation tolerance. If we examine
the phenomenon of anhydrobiosis, we find that it is widely dispersed in nature,
occurring in microorganisms (bacteria and yeasts) and animals (typically invertebrates: nematodes, rotifers, and tardigrades) as well as in plants. Within the
plant kingdom we can recognize anhydrobiosis to be an ancient trait, widespread among the bryophytes, and doubtless an essential adaptive feature
required for the conquest of the land by previously aquatic organisms (Oliver
et al. 2000). In the tracheophytes, the property of desiccation tolerance has been
lost in vegetative tissues, but retained – or rather, partitioned by an evolutionary
process – in reproductive propagules (seeds and spores).
We are now able to identify the collection of genes whose expression is
required for desiccation tolerance. This is a complex collection that includes a
substantial number that encode the so-called ‘‘Late Embryogenesis Abundant’’
(LEA) proteins (Cuming 1999, Wise & Tunnacliffe 2004). These genes are present
in both mosses and seed plants (and algae and animals), demonstrating their
early evolutionary origin (Browne et al. 2002, Goyal et al. 2005). In plants, these
genes are expressed by transcriptional activation, often mediated by abscisic
acid, using a small number of transcription factors: the basic-domain leucinezipper (‘‘bZip’’) and Apetala 2 (Ap2) drought-responsive element binding (DREB)
families that interact with specific cis-acting motifs within the promoters of the
LEA genes, and under the control of a transcriptional activator encoded (in
Arabidopsis) by the ABI3 (ABA-insensitive 3) gene (Himmelbach et al. 2003). LEA
genes in moss and flowering plants alike utilize the same transcriptional activation mechanisms (Knight et al. 1995, Kamisugi & Cuming 2005), and the
5 Mosses as model organisms
transcription factors responsible for these processes in moss and flowering
plants are largely interchangeable (Marella et al. 2006). However, in the angiosperms the transcriptional network dependent upon the ABI3 transcriptional
activator has become developmentally sequestered to later stages of seed development through the restriction of ABI3 gene expression to this phase of development in the course of tracheophyte divergence.
This represents one method of evolutionary ‘‘capture’’ of a gene expression
network. Other forces also act to recruit different sets of genes to the control of
specific developmental activators. Thus, a transcription factor can acquire or
lose ‘‘subject’’ genes in two ways: it can undergo modification of its DNA-binding
domain, so that it recognizes a novel cis-acting promoter sequence, thereby
potentially recruiting an entirely new collection of genes, or it can gradually
acquire or lose individual subject genes through the occurrence of mutations in
the respective cis-acting sequences of the subjects that cause them to change
their ‘‘transcriptional allegiance’’.
Since modifications in the DNA-binding specificity of a transcription factor
are likely to prove deleterious, more often than not, such modifications are
most commonly found associated with gene duplication and the subsequent
subfunctionalization of the duplicated genes. ‘‘Subfunctionalization’’ describes
the evolution of gene families through gene duplication, followed by the accumulation of mutations resulting in the two copies sharing aspects of the original
gene’s function. Striking examples of this occur in the very well characterized
MADS-box transcription factor family (Causier et al. 2005). The origins of this
family are ancient, pre-dating the Cambrian explosion (Nam et al. 2003; De Bodt
et al. 2003). In Arabidopsis there are over 100 MADS-box transcription factor genes
(Parenicova et al. 2003) of which the best characterized are the so-called ‘‘MIKC’’
class that have been identified as regulating most aspects of floral morphogenesis, and whose complex interactions contribute to the great diversity of floral
structures found in the angiosperms, and whose evolution must necessarily
have underpinned the explosive speciation within this group. This subfamily
of transcriptional regulators is exclusive to plants, but is still ancient in origin,
representatives being found in mosses (Krogan & Ashton 2000, Henschel et al.
2002), ferns (Hasebe et al. 1998), and gymnosperms (Munster et al. 1997,
Mouradov et al. 1998a, 1999, Winter et al. 1999, Becker et al. 2000). However,
the amplification of this gene family, and its recruitment to the regulation of
reproductive development, occurred relatively late in land plant evolution. The
identification of MADS-box gene transcripts in the developing reproductive
organs of Pinus radiata (Mouradov et al. 1998b) suggests that this capture
occurred prior to the divergence of the gymnosperms, but after that of the
ferns in the land plant lineage, since in this latter group MADS-box genes have
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been found to be expressed ubiquitously in both the gametophytic and sporophytic tisses (Münster et al. 1997). Expression of the floral homoeotic genes in
angiosperms occurs only following the respecification of the vegetative meristem to an inflorescence meristem. This is mediated through the transcription
factor encoded by the FLO/LFY gene – a homoeotic gene whose expression is
essential for the transition from a vegetative shoot apical meristem to an
inflorescence meristem. Whilst the Pinus homologue of this gene exhibits
meristem-specific gene expression, and is capable of complementing Arabidopsis
lfy mutants (Mouradov et al. 1998b), the FLO/LFY homologues of ferns are less
closely associated with reproductive development. Expression does occur predominantly in the reproductive meristem, indicating that the developmental
transition mediated by FLO/LFY had evolved at this relatively early stage in land
plant evolution (Himi et al. 2001) but the expression of the fern MADS box genes is
not closely correlated with that of FLO/LFY (Hasebe et al. 1998, Himi et al. 2001),
implying that these genes had not yet been subordinated to FLO/LFY regulation. In
Physcomitrella, there are two FLO/LFY paralogues, exhibiting a high degree of
sequence identity. Analysis of the expression of each gene by reporter ‘‘knockin’’, and by the generation of knock-out mutants, showed that the two genes have
highly overlapping, largely redundant functions. This implies that the two copies
result from a relatively recent gene duplication event. The PpLFY-1 and PpLFY-2
genes are expressed during sporophyte development, being required for the first
division of the zygote (Tanahashi et al. 2005). This presumably represents an
ancestral function from which a gene duplication in the ancestors of a subsequent
lineage enabled the acquisition of a new role in the specification of reproductive
development in the seed plants.
The use of powerful bioinformatic tools to undertake comparative genomic
analyses of genes implicated in the regulation of development of Arabidopsis,
coupled with the ease with which the functional analysis of their counterparts
in Physcomitrella can be conducted, highlights the value of ‘‘molecular bryology’’ in gaining a fuller understanding of the evolution of plant developmental
strategies.
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6
Physiological ecology
m i c h a e l c. f . p r oc t o r
6.1
Introduction
Bryophytes are on average some two orders of magnitude smaller than
vascular plants, and this difference of scale brings in its train major differences
in physiology, just as many of the differences in the structural organization and
physiology of insects and vertebrates are similarly scale-driven. Surface area
varies as the square, and volume and mass as the cube, of linear dimensions.
Hence gravity is a major limiting factor for vertebrates or trees, but trivial for
insects or bryophytes. Bryophytes in general have much larger areas for evaporation in proportion to plant mass than do vascular plants. Surface tension,
which operates at linear interfaces, is of little significance at the scale of the
vascular plant shoot but is a powerful force at the scale of many bryophyte
structures. There are also major scale-related differences in the relation of
bryophytes and vascular plants to their atmospheric environment. Vascularplant leaves are typically deployed in the turbulent air well above the ground.
The diffusion resistance of the thin laminar boundary layer is small, so the
epidermis with its cuticle and stomata in effect marks the boundary between
(relatively slow) diffusive mass transfer within the leaf and (much faster) turbulent mixing in the surrounding air. By contrast the small leaves of many bryophytes lie largely or wholly within the laminar boundary layer of the bryophyte
carpet or cushion, or of the substratum on which it grows. For these reasons it is
important to approach bryophyte physiology from cell-biological and physical
first principles; preconceptions and concepts carried over from vascular-plant
physiology can be grossly misleading.
Raven (1977, 1984, 1995) has emphasized the importance of supracellular
transport systems in the evolution of land plants, and the physiological
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
238
M. C. F. Proctor
correlates that we must read alongside the anatomical structures of fossil
plants. But the highly differentiated supracellular conducting systems exemplified by xylem and phloem are really only a prerequisite for large land
plants. In adapting to the erratic subaerial supply of water, vascular land
plants evolved tracheids and vessels, bringing water from the soil to meet
the needs of the above-ground shoots and leaves. Bryophytes in general
adopted the alternative strategy of allowing free water loss (poikilohydry)
and evolving desiccation tolerance, photosynthesizing and growing during
moist periods and suspending metabolism during times of drought. These
two patterns of adaptation are in many ways complementary. Bryophytes
may appear to be limited by their lack of roots, but their poikilohydric habit
means that they can colonize hard and impermeable surfaces such as tree
trunks and rock outcrops, impenetrable to roots, from which vascular plants
are excluded. Bryophytes typically take up water and nutrients over the
whole surface of the shoots. They efficiently intercept and absorb solutes
in rainwater, cloud and mist droplets, and airborne dust. This ability underlies both their conspicuous success in many nutrient-limited habitats and the
vulnerability of many species to atmospheric pollution. The vascular-plant
pattern of adaptation is undoubtedly optimal for a large land plant; there is
much reason to believe that the poikilohydric pattern of adaptation is optimal for a small one. The divergence of bryophytes and the various vascularplant groups goes back to the early history of plant life on land – certainly
400 million years, and probably longer (Edwards et al. 1998, Goffinet 2000).
Mosses, Hepaticae, and Anthocerotae may well have been evolutionarily
independent for equally long. Physiologically, bryophytes are neither simple
nor primitive. They should be seen not as primitive precursors of vascular
plants, but as the diverse and highly evolved representatives of an alternative
strategy of adaptation, prominent in the vegetation of such habitats as
subpolar and alpine fell-fields and tundra, bogs and fens, and the understorey of many forests from the boreal zone to the ‘‘mossy forests’’ of tropical
mountains. They are challenged at their own scale only by the comparably
adapted lichens.
The physiological ecology of bryophytes has been the subject of a number of
reviews (Longton 1981, 1988, Proctor 1981a, 1982, 1990). Poikilohydry as an
adaptive strategy has been discussed by Kappen & Valladares (1999) and Proctor
& Tuba (2002). Mineral nutrition and pollution responses are reviewed by Brown
(1982, 1984), Brown & Bates (1990), Bates & Farmer (1992) and Bates in Chapter 8
of this volume. Bryophyte production, and its responses to major environmental factors, has been reviewed by Russell (1990), Frahm (1990), Vitt (1990) and
Sveinbjörnsson & Oechel (1992). The present chapter does not cover aspects
6 Physiological ecology
(such as temperature relations of photosynthesis) that are essentially similar in
all green plants, but concentrates on some ecophysiological features more
particularly characteristic of bryophytes.
6.2
Water relations
Vascular plants have internal water conduction – they are endohydric –
and the surface of the leaves and young stems is typically covered by an epidermis with a more or less waterproof and water-repellent cuticle, gas exchange
taking place through stomata. Most bryophytes are ectohydric, free liquid water
moving predominantly in capillary spaces outside the plant. In some large
mosses, exemplified by the tall, robust Dawsonia and Polytrichum species and
the large Mniaceae, the stems possess a well-developed central strand of
water-conducting hydroids, and a substantial proportion of water conduction
is internal. However, in these more or less endohydric mosses significant conduction generally takes place externally in the capillary spaces of sheathing leaf
bases or rhizoid tomentum, and they have little or no control over water loss, so
like other bryophytes they are poikilohydric. In all bryophytes, as in vascular
plant tissues at a comparable scale, much internal water movement must be
relatively diffuse, within the cell walls, through the cells themselves, or some
combination of the two. Most water movement must be of this kind in the large
marchantialean liverworts, and many small acrocarpous mosses must rely on a
(probably always variable) balance between external and internal conduction.
Bryophytes are likely to be scarcely less complex in respect of tissue water
movement than vascular plants (Proctor 1979a, Steudle & Petersen 1998).
Thus, typically in bryophytes conduction of water is predominantly external,
in an interconnecting network of capillary spaces on the outside surface of the
plant. These include the spaces within sheathing leaf bases, in the concavities of
overlapping imbricate leaves as in Scleropodium or Pilotrichella, within the felts of
rhizoids or paraphyllia that cover the stem in such genera as Philonotis and
Thuidium, in the interstices between the papillae that cover the leaf surfaces
in, for example, Encalypta, Syntrichia and Anomodon, and between tightly packed
shoots or between shoots and the substratum. The external water of ectohydric
bryophytes is as much a part of the plant’s physiological functioning as the
water in the xylem of vascular plants.
The cell water relations of bryophytes are essentially the same as those of
other plant cells and are illustrated by the ‘‘Höfler diagram’’ of Fig. 6.1(a). In a
fully turgid cell the osmotic potential Cp is exactly balanced by the turgor
pressure CP of the cell wall; the cell is externally in equilibrium with pure liquid
water, and its water potential C (or CW) is zero (by definition). If the external
239
240
M. C. F. Proctor
Fig. 6.1. (a) Höfler diagram for a bryophyte illustrating the relationship of cell water
potential (C) and its components osmotic potential (Cp) and turgor pressure (CP) to relative cell
volume and external capillary water. Based on the data of Fig. 6.1b. (b) The relation of
relative water content to water potential for the leafy liverwort Porella platyphylla, from
thermocouple–psychrometer measurements. Water content was originally plotted as per cent
dry mass, and the full-turgor point estimated from the graph, as described by Proctor et al.
(1998). The horizontal dotted line indicates the turgor-loss point. A rectangular hyperbola has
been fitted to the data points below this, and a polynomial regression to the points between full
turgor and turgor loss. This graph is in effect a Höfler diagram with water potential taken as the
x-axis, and matches the presentation used by Proctor et al. (1998) and Proctor (1999). Compare
Fig. 6.1a and the ‘‘pressure–volume’’ curve of Fig. 6.2a.
water potential becomes negative, the cell must lose water. The reduction in cell
volume causes turgor pressure to fall and osmotic potential to become more
negative (numerically greater). When the turgor pressure falls to zero, the water
potential of the cell is equal to the osmotic potential of its contents. At any lower
water content, osmotic potential and cell water potential are equal, and inversely proportional to the volume of water in the cell. The relation between
osmotic potential and cell volume plots onto the Höfler diagram as a rectangular
hyperbola. The relation of cell water potential to cell water content follows this
hyperbola up to the turgor-loss point. It then breaks away to follow a line,
generally slightly concave to the water-potential axis, to the full-turgor point,
where the relative water content (RWC) ¼ 1.0 (by definition), and C = 0. Practical
measurements are generally of tissues rather than individual cells, but if the
cells all have similar properties the same principles apply. Bryophyte shoots
generally carry some external water, held at small negative water potentials
determined by the dimensions of the capillary spaces in which it lies. The effect
of this water in a Höfler diagram is illustrated by the dotted line in Fig. 6.1a.
6 Physiological ecology
Fig. 6.2. (a) Pressure–volume graph from the same data as Fig. 6.1b. Water content is plotted as
1 – RWC and decreases from left to right; the y-axis is the reciprocal of water potential. Turgor
loss is indicated by the vertical dotted line. A linear regression has been fitted to the points to
the right of this. It intersects the y-axis at the reciprocal of the full-turgor osmotic potential, the
turgor-loss line at the reciprocal of the osmotic potential at turgor loss, and the x-axis at a point
which gives a measure of the effective osmotic volume of the cells. (b) The relation of turgor
pressure to relative water content for Porella platyphylla, from thermocouple–psychrometer
measurements. The curve leaves the x-axis at the turgor-loss point and cuts the y-axis at the fullturgor osmotic potential. The slope of the curve gives a measure of the bulk modulus of
elasticity ("B) of the tissues.
If one of the axes of the graph relating water potential to water content is
plotted on a reciprocal scale, the hyperbola of Fig. 6.1 becomes a straight line.
The graph of 1/C against (1 – RWC) (Fig. 6.2a) is referred to as a pressure–volume
(P–V) curve (Jones 1992). Turgor loss is marked by the point at which the relation
of 1/C to (1 – RWC) breaks away from linearity, and the reciprocal of the osmotic
potential at this point can be read from the graph. The intercept of the straight
line on the 1/C axis gives the reciprocal of the osmotic potential at full turgor.
The intercept on the RWC axis is commonly taken as a measure of non-osmotic
(or ‘‘apoplast’’) water but its exact significance is debatable (Proctor et al. 1998).
From the data in the P–V curve, turgor pressure can be calculated for water
contents between full turgor and the turgor-loss point (Fig. 6.2b). The steepness
of slope of this curve (and the difference in water content between full turgor
and turgor loss) depends on cell-wall extensibility, measured by the bulk elastic
modulus, "B, which varies continuously between turgor loss and full turgor in a
manner depending on the exact physical properties of the cell walls.
Some representative water-relations data for bryophytes are summarized in
Table 6.1. Osmotic potentials at full turgor mostly lie between –1.0 and –2.0 MPa,
241
Table 6.1 Water-relations parameters of bryophytes
Figures are in general mean s.d. from three or four replicates. The sign * indicates a single value from the combined data of all replicates; z, that the
values from individual replicates were not distinguishable.
Species
Osmotic potential
x-intercept of P–V
RWC at
Bulk elastic modulus
Water content at
Water content
at full turgor ( MPa)
curve (RWC)
turgor loss
"B at RWC 1.0 (MPa)
full turgor (% d.m.)
blotted (% d.m.)
n.d.
Targionia hypophylla
0.74 0.03
0.069 0.003
0.70
Conocephalum conicum
0.54 0.08
0.002 0.032
0.45
Marchantia polymorpha
0.38 0.02
0.052 0.027
Dumortiera hirsuta
0.49 0.05
0.014 0.023
Metzgeria furcata
1.11 0.03
0.043 0.017
0.75
11.3 0.7
Pellia epiphylla
0.72 0.08
0.031 0.032
0.80
1003 45
940 37
2.2 0.8
1400 132
1277 108
0.60
1.5*
1025 35
956 65
0.90
7.6 1.2
1636 118
1628 109
4.8*
300z
363 22
1020z
1046 157
Bazzania trilobata
1.41 0.07
0.081 0.025
0.80
17.3 3.5
253 6
300 11
Porella platyphylla
1.37 0.03
0.053 0.013
0.80
13.3 1.2
273 5
312 8
Frullania tamarisci
1.78 0.20
0.189 0.017
0.60
7.6 0.5
134 3
216 7
Jubula hutchinsiae
1.02 0.04
0.097 0.010
0.70
6.3 2.8
353 21
353 17
Andreaea alpina
1.59 0.03
0.265 0.006
0.70
6.8 0.4
110 4
141 9
Polytrichum commune
2.09 0.09
0.116 0.023
0.75
19.2 0.4
179 6
186 11
Dicranum majus
1.27 0.04
0.126 0.025
0.80
12.2 1.2
185 15
193 7
Tortula ruralis
1.36 0.18
0.266 0.093
0.75
5.8 1.5
108 11
n.d.
Racomitrium lanuginosum
1.29 0.08
0.224 0.030
0.65
5.3 1.9
121 4
135 5
Mnium hornum
1.21 0.07
0.099 0.049
0.70
6.1 1.7
215 7
175 6
Antitrichia curtipendula
1.47 0.28
0.175 0.033
0.65
5.9 0.6
152 11
174 16
Neckera crispa
1.27 0.09
0.271 0.092
0.65
7.7 1.6
140 5
150 13
Hookeria lucens
0.95 0.03
0.021 0.004
0.70
6.2 1.5
571 42
n.d.
Anomodon viticulosus
1.65 0.07
0.230 0.009
0.65
8.5 2.3
133 3
176 10
Homalothecium lutescens
2.08 0.08
0.086 0.054
0.70
18.8 2.9
193 15
218 27
Rhytidiadelphus triquetrus
1.440.16
0.1360.028
0.75
9.6 1.3
182z
n.d.
Rhytidiadelphus loreus
1.34 0.02
0.237 0.049
0.70
5.9 1.2
142 10
180 13
Sources: Data from Proctor et al. (1998) and Proctor (1999).
6 Physiological ecology
but are generally less negative (numerically around half these values) in thalloid
liverworts. Metzgeria furcata, matching leafy liverworts and mosses in its unistratose thallus and tolerance of drying, is an interesting exception. The moss
Hookeria lucens and the leafy liverwort Jubula hutchinsiae, both species of wet shady
habitats, have notably low osmotic potentials, around –1.0. However, there is no
clear indication that species of dry habitats have osmotic potentials markedly
more negative than the norm; many of the more extreme older published
figures based on plasmolysis are certainly wrong. The intercept of the P–V
curve on the water-content axis correlates with cell-wall thickness relative to
the cell lumen; it is high in such species as Andreaea alpina, Racomitrium lanuginosum, and Neckera crispa, and low in, for example, Hookeria lucens and the big
thalloid liverworts. Water content at full turgor as a percentage of dry mass is
also related to the proportion of cell-wall material, and varies widely from about
100% dry mass in small desiccation-tolerant species of sun-baked rocks to 2000%
or more in thalloid liverworts of wet habitats. Both these measures change as
the shoots develop and mature, and are sensitive to the inclusion of moribund
older material, so they vary with the seasons and can never be very precise.
Relative water content at turgor loss and "B are also correlated, but somewhat
loosely. By vascular-plant standards, bryophyte cell walls are typically rather
readily extensible (low "B), but some mosses (e.g. Polytrichum commune, Dicranum
majus, Homalothecium lutescens) and leafy liverworts (e.g. Bazzania trilobata, Porella
platyphylla) show "B values that would pass unnoticed among those of herbaceous vascular plants (Zimmerman & Steudle 1978). Cell-wall extensibility also
varies with time, "B increasing as the shoots mature.
The division between apoplast water in the cell walls, symplast water within the
cells, and external capillary water (and especially the latter two) is important for
several reasons (Dilks & Proctor 1979, Beckett 1996, Proctor et al. 1998). First (for the
physiological investigator) it is essential to know the full-turgor water content in
order to calculate RWC values physiologically comparable with those for vascular
plants. ‘‘RWC’’ values based on ‘‘saturated’’ water contents are wholly misleading,
and it is much less easy to obtain an accurate estimate of the full-turgor water
content of a bryophyte than of a vascular plant leaf. As Table 6.1 shows, acceptable
approximate estimates of full-turgor water content can often be obtained by carefully blotting samples of saturated shoots; underestimates can arise through thumb
pressure expressing symplast water from large-celled species, and overestimates
through incomplete removal of external water from species with intricate external
capillary spaces, or the presence of large amounts of apoplast water. When compared in terms of true RWC (i.e. cell water content relative to cell water content at
full turgor), photosynthesis in bryophytes of widely differing adaptive types, and
vascular-plant cells, responds similarly to water deficit (Fig. 6.3).
243
244
M. C. F. Proctor
Fig. 6.3. Response of net photosynthesis to water deficit in two contrasting bryophytes,
from gas-exchange measurements. The data for the desiccation-tolerant moss Tortula
(Syntrichia) ruralis are recalculated from Tuba et al. (1996), taking as full turgor a value of 165% dry
mass estimated from measurements at their field site in July 1998, and assuming 10% of the
full-turgor water content to be apoplast water. The data for the thalloid liverwort
Conocephalum conicum are recalculated from Slavik (1965), assuming that full-turgor water
content coincides with the maximum value for net photosynthesis (900% dry mass).
Measurements for spinach (Spinacia oleracea), a mesophytic vascular plant, are included for
comparison (Kaiser 1987).
Second (for the bryophyte), the external capillary water is exceedingly important physiologically. Its significance in relation to external water movement has
already been alluded to. External water is also of prime importance in relation to
water storage, which in turn is a major determinant of the length of time the
shoots remain turgid and able to photosynthesize and grow. It is often the
largest component of water associated with the plant, and it can vary widely
without affecting the water status of the cells. It is common to find that external
capillary water exceeds symplast water by a factor of five or more; a not
especially wet-looking sample of the pendulous African forest moss Pilotrichella
ampullacea that I took to make measurements for a P–V curve turned out to have
a total water content corresponding to a RWC of more than 12! Most of this
water would have been held in the concavities of the overlapping ‘‘ampulla-like’’
leaves. The effect of external storage of large amounts of water is that for most of
the time the shoots are either functioning at full turgor, or they are too dry to
support metabolism, with only brief interludes at water potentials between
these states. From the bryophyte’s point of view, any habitat is ‘‘wet’’ during
and following rain, and ‘‘dry’’ at other times. The primary difference is in the
6 Physiological ecology
relative times spent wet and dry; drought stress and drought tolerance as they
affect vascular plants hardly enter the picture, and the drought metabolites of
vascular plants such as proline and glycine–betaine are conspicuously absent
from bryophytes. We should remember that desert ephemeral vascular plants
are mesophytes, which flourish following occasional periods of rain and escape
drought by means of their desiccation-tolerant seeds. Bryophytes escape
drought by means of their desiccation-tolerant vegetative shoots. Desiccationtolerant bryophytes and vascular desert ephemerals may equally be seen as
‘‘drought-escaping’’ plants. It is a paradox that ‘‘poikilohydric’’ bryophytes
may spend less time metabolizing at sub-optimal water content than many
‘‘homoiohydric’’ vascular plants! (Proctor 2000).
6.3
Bryophyte shoots as photosynthetic systems
It is easy to show by experiment in the laboratory that the rate of water
loss from a vascular-plant shoot is largely determined by stomatal aperture.
However, this leaves out of consideration two important factors in the field
situation, one general and one particularly applicable to bryophytes. First, the
latent heat of evaporation must come from the surroundings: by convective
heat exchange with the air, by conduction from the substrate, or by radiative
exchange with the wider environment. In a laboratory experiment with an
isolated plant the amount of heat involved is small and easily left out of
consideration. In the vegetation cover of a landscape it becomes a major factor
in determining water loss (Jarvis & McNaughton 1986). Second, boundary-layer
conditions for bryophytes are often largely determined by the extensive substrata on which they grow. Further, many bryophytes grow in the shelter of
trees or smaller vascular plants which reduce the ambient windspeed to varying
degrees. Thus, various environmentally determined parameters are major controls on water loss from bryophytes, and laboratory experiments on isolated
bryophyte shoots or cushions that do not take this into account may have little
relevance to what goes on in the field.
The small leaves of many bryophytes lie largely or wholly within the laminar
atmospheric boundary layer of the bryophyte carpet or cushion, or of the
substratum on which it grows. This is the layer in which the streamlines of
the airflow are essentially parallel to the surface, so that transfer of heat and
gases through it must take place by (slow) molecular diffusion by contrast with
the much more rapid turbulent mixing in the surrounding air. The thickness of
the laminar boundary layer is in the region of a few hundred micrometers at a
windspeed of 1 m s 1; it varies inversely as the square root of the windspeed up
to the point at which the leaf or moss colony begins to generate turbulence
245
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M. C. F. Proctor
itself. Wind-tunnel measurements (Proctor 1981b) show that at very low windspeeds a moss cushion behaves as a smooth simple object; water loss increases
approximately as the square root of the windspeed, reflecting the corresponding decrease in boundary-layer thickness. Hair-points on the leaves (e.g. in
Grimmia pulvinata) can have the effect of separating the sites of momentum
and water-vapor transfer, in effect trapping an additional thickness of stagnant
air between the moist leaf surfaces and the airstream, reducing the rate of water
loss. (Hair-points can have other effects, increasing albedo for one.) Beyond a
certain point, evaporation rises more rapidly with windspeed; the ‘‘rougher’’ the
cushion surface (in terms of its interaction with the airstream), the lower the
windspeed at which this occurs. At low windspeeds, the bryophyte colony
functions, in effect, as a single ‘‘leaf’’, and gas exchange in the spaces between
the individual leaves proceeds mainly by the comparatively slow process of
molecular diffusion. Increasing evaporation at higher windspeeds reflects
both the increasing tendency of the moss surface to generate turbulence in
the airstream, and the fractally increasing area of the evaporating area of the
cushion as measured by a boundary layer of progressively decreasing thickness.
Moss or leafy-liverwort canopies operate at a scale intermediate between vascular-plant leafy canopies on the one hand, and the cells of a vascular-plant
mesophyll on the other, and analogies may be sought in both directions.
Bryophytes show high leaf-area index values (LAI: area of leaves divided by
area occupied by the plant). A few estimates of my own gave figures of c. 6 in
Syntrichia intermedia, 18 in Mnium hornum, and 20–25 in Scleropodium purum
(Proctor 1979a), in the same range as the few other (unpublished) figures I
have encountered. They are nearer the range of vascular-plant ratios of mesophyll area to leaf area (c. 14–40; Nobel 1977) than to LAIs for vascular plant
canopies, which are usually less than 10 and commonly around 5. The growth
forms and ‘‘life forms’’ of bryophytes vary greatly and in a manner certainly
related to ecophysiological adaptation and microclimatic conditions in their
habitats (Gimingham & Birse 1957, Mägdefrau 1982, Proctor & Smith 1995,
Bates 1998, Rice et al. 2001).
The diffusive path for water loss is from the leaf surface to the atmosphere;
that for CO2 uptake is from the atmosphere to the chloroplasts. Therefore, CO2
uptake encounters additional liquid-phase diffusive resistance in the cell walls
and cytoplasm. As molecular diffusion is slower in water than in air by a factor
of about 104, this additional resistance is large, even if the liquid diffusion path
is only a few micrometers, and underlies the selection pressure for evolution of
high LAI values in bryophytes and high mesophyll/leaf-area (Ames/A) ratios in
vascular-plant leaves. In addition to these diffusive resistances, the photosynthetic system of the chloroplasts may be regarded as imposing a ‘‘carboxylation
6 Physiological ecology
resistance’’ to CO2 uptake. An indication of the relative importance of these two
limitations is given by the overall discrimination of photosynthesis against the
heavy isotope of carbon, 13C, conventionally expressed in (‰) relative to an
arbitrary standard as d13C (Raven et al. 1987, Farquhar et al. 1989). The generally
similar values for bryophytes (averaging around –27‰) and C3 vascular plants
(Rundel et al. 1979, Teeri 1981) suggests that the relative magnitude of diffusion
and biochemical limitations on CO2 uptake is similar in the two groups, probably reflecting convergence on an adaptive optimum in the deployment of
Rubisco relative to supporting tissues (Raven 1984, appendix 3). Substantially
more negative d13C values are seen in aquatic bryophytes utilizing a proportion
of respired CO2 (e.g. Fontinalis antipyretica [Rundel et al. 1979, Raven et al. 1987],
Sphagnum cuspidatum [Proctor et al. 1992, Price et al. 1997]). Less negative d13C
values can be the consequence of high diffusive limitation by superincumbent
water (Rice & Giles 1996, Williams & Flanagan 1996, Price et al. 1997, Rice 2000).
Anthocerotae such as Anthoceros and Phaeoceros show consistently low discrimination against 13CO2, giving d13C values of –15 to –20‰, because uniquely
among bryophytes they have a carbon-concentrating mechanism associated
with the pyrenoid (Smith & Griffiths 1996a,b, Hanson et al. 2002). C4 vascular
plants typically have d13C values around –10 to –12‰.
Morphological adaptation in bryophytes must reconcile the potentially conflicting requirements of water conduction and storage, and free gas exchange
for photosynthesis. This is achieved in various ways. Many, and probably most,
bryophyte leaf surfaces carry at least a thin layer of water-repellent cuticular
material, and some bear conspicuous granular or crystalline epicuticular
wax (Proctor 1979b). This is most striking in some glaucous-looking species,
often of moist places or shady crevices, in which water conduction must be
largely internal, such as Pohlia cruda, P. wahlenbergii, Saelania glaucescens, many
Bartramiaceae, and leafy liverworts such as Douinia ovata and Gymnomitrion
obtusum. Many mosses (and some leafy liverworts) have shoot systems with
closely overlapping concave leaves, the inner faces functioning for water storage, and the outer surfaces, kept free of superincumbent water by surface
tension, serving for gas exchange. Striking instances of shoots of this kind are
seen in, for example, Anomobryum filiforme, Scleropodium spp., Myurium hochstetteri,
Pleurozium schreberi, Pilotrichella spp., Weymouthia spp., and Nowellia curvifolia, but
there are many less extreme variations on the same theme. Densely papillacovered or mammillate leaf surfaces are also common, and in many cases these
too appear to provide a division between water conduction and gas exchange,
the papilla (or mammilla) apices remaining dry while the interstices between
them provide a continuous network of water-conducting channels (Buch 1945,
1947, Proctor 1979a).
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M. C. F. Proctor
A simple calculation shows that, assuming reasonable values for the liquidphase diffusion resistance to CO2 uptake, the rate of carbon fixation of a simple
unistratose bryophyte leaf (two surfaces) would become limited by CO2 diffusion at an irradiance of about 500 mmol m 2 s 1, or about a quarter of full
sunlight (Proctor 2005). This assumes that both leaf surfaces are completely
clear for gas exchange. In reality, most bryophyte shoots or canopies consist of
overlapping leaves or thallus lobes, increasing the area available for carbon
fixation without greatly increasing the gas-phase diffusion path (most resistance
is in the liquid phase within the leaves). On the other hand, CO2 uptake will
seldom take place over the whole leaf surface. Concave leaves holding water on
the inner surface are one-sided for gas exchange, and superincumbent water
will reduce gas exchange of many bryophyte shoots. In a sample of 39 mosses
and 16 liverworts, chlorophyll-fluorescence estimates of 95%-saturating irradiance ranged widely, but most were <1000 mmol m 2 s 1; the median for mosses
was a little under 600 and for liverworts just over 200 mmol m 2 s 1 (Marschall &
Proctor 2004). The mosses showed a bimodality between forest species peaking
at 200–300 mmol m 2 s 1 and species of more open situations peaking between
500 and 700 mmol m 2 s 1. Values higher than this came from either species of
dry, very sun-exposed habitats (Andreaea rothii, Grimmia pulvinata, Racomitrium
lanuginosum, Syntrichia intermedia, S. ruralis), or from open and sunny but constantly moist bogs and fens (Aulacomnium palustre, Philonotis calcarea, Splachnum
ampullaceum, Scorpidium scorpioides). Photosynthesis–irradiance curves from
infrared gas analysis of CO2 uptake give 95% saturation irradiances broadly in
the same range as the chlorophyll-fluorescence data (given in parentheses). For
four species, Marschall & Proctor (2004) found 551 (711) mmol m 2 s 1 for
Andreaea rothii, 583 (617) mmol m 2 s 1 for Racomitrium aquaticum, 832 (935)
mmol m 2 s 1 for Syntrichia ruralis, and 228 (327) mmol m 2 s 1 for Marchantia
polymorpha. In general, chlorophyll fluorescence would be expected to give
rather higher figures than CO2 uptake because it measures electron flow to
photorespiration as well as to carbon fixation.
The leaves of Polytrichales and thalli of Marchantiales have complex ventilated photosynthetic tissues paralleling leaves of vascular plants. In the past
these have tended to be seen in terms of restriction of water loss, but we
should see them rather as an adaptation increasing the area for CO2 uptake
when the plant is adequately supplied with water. In Polytrichales, with their
regular longitudinal lamellae, it is relatively easy to estimate the ratio
between area for CO2 uptake and projected leaf area, analogous to Ames/A
for a vascular-plant leaf. There is a very clear correlation between this value
and the 95%-saturation irradiance (Fig. 6.4) (Proctor 2005). It is less easy to
construct a similar graph for the Marchantiales because their photosynthetic
6 Physiological ecology
Fig. 6.4. Relation of irradiance at 95% saturation (PPFD95%) to the ratio of area available for
CO2 uptake to projected leaf area (Ames/A) for some Polytrichaceae. The lower left-hand
corner of the diagram is occupied by species of shady forest, including the common
European Atrichum undulatum with a broad unistratose lamina and only few lamellae,
Pogonatum semipellucidum from shady Andean cloud forest with a broader band of low
lamellae in the middle of the lamina, and the New Zealand temperate-rainforest species
Dendroligotrichum dendroides with a Polytrichum-like leaf but only low lamellae. The upper
right-hand part of the diagram includes species of sun-exposed habitats, here four
Polytrichum species from open moorlands in Britain, and Pogonatum perichaetiale,
Polytrichadelphus aristatus, and Polytrichum juniperinum from the high páramo of the Venezuelan
Andes. All these species have well-developed lamella systems. The bold pecked line is a linear
regression on the data; the lighter dotted line is the theoretical limit assuming that the
maximum CO2 uptake through a single plane surface is 250 mmol m
2
s
1
. Higher values may
arise from measurements on overlapping leaves, lower values from limiting factors other
than CO2 diffusion.
tissues are more irregular, but a similar relation clearly holds. Both groups
include species of open, sun-exposed habitats (e.g. the moss Polytrichum piliferum and the liverwort Exormotheca pustulosa) with saturating irradiances far
outside the range of most other bryophytes. Conspicuous surface wax is
notably a feature of the margins of the lamellae of the leaves of
Polytrichaceae (Clayton-Greene et al. 1985, Proctor 1992) where it serves the
function of preventing the entry of water into the interlamellar spaces. The
water-repellent pore margins of Marchantiales similarly prevent flooding of
the ventilated photosynthetic tissues of the thallus, in the same way that the
sharp water-repellent edges of the stomata prevent waterlogging of the mesophyll in vascular plants (Schönherr & Ziegler 1975).
249
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M. C. F. Proctor
Bryophytes have often been said to show ‘‘shade plant-like’’ features in their
photosynthetic physiology (Valanne 1984). Some of these characteristics may
have more to do with the long evolutionary independence of bryophytes and
vascular plants than with real adaptive differences. Some may stem from the
poikilohydry of bryophytes; as noted already they will most often be photosynthesizing in rainy or overcast conditions, and metabolically inactive in dry
sunny weather. Bryophytes typically have rather low chlorophyll a/b quotients,
in the range of shade-adapted vascular plants (Egle 1960). Martin & Churchill
(1982) found an overall mean value of 2.69 0.27 (mean SD) from 14 species of
exposed habitats in Kansas, and 2.38 0.20 for 20 forest species after canopy
closure. Kershaw & Webber (1986) found a progressive change in the chlorophyll a/b quotient in an old-orchard population of Brachythecium rutabulum
from 2.9 in young shoots before tree-canopy expansion to c. 2.0 in deep shade
in autumn. In 39 mosses from diverse habitats mostly in southwest England the
overall mean chlorophyll a/b was 2.39 0.51; for 16 liverworts the corresponding figures were 1.98 0.30 (Marschall & Proctor 2004). In general, sun plants
tend to have lower chlorophyll/dry mass quotients, higher chlorophyll a/b
quotients and higher carotenoid/chlorophyll quotients than shade plants.
Correspondingly, in Marschall and Proctor’s bryophyte data there were significant correlations between 95%-saturation irradiance of photosynthesis (from
chlorophyll fluorescence measurements) and the quotients of chlorophyll/dry
mass (negative), chlorophyll a/b (positive), and total carotenoids/total chlorophylls (positive).
Chlorophyll fluorescence (Krause & Weis 1991, Schreiber et al. 1995, Maxwell &
Johnson 2000) is such a valuable tool in bryophyte ecophysiology that it is
important to appreciate both its potentialities and its limitations. It can provide,
non-invasively, much useful information about the state of the photosynthetic
system in a green plant. Moreover, fluorescence measurements can be made on
small amounts of material, and this makes it particularly valuable for working
on small bryophytes. The energy absorbed by chlorophyll may suffer one of
three fates: it may drive photochemistry, it may be re-emitted as red fluorescence, or it may be dissipated as heat. A green plant tissue will always emit a
basal level of fluorescence (F0). After a period of adaptation in the dark, the
energy in a short saturating flash, too short for significant photochemistry to
occur, is emitted entirely as fluorescence (Fm). At a constant level of actinic light,
the steady-state fluorescence (Fs or Ft) will typically be greater than F0 but less
than Fm, and both the basal fluorescence (F00 ) and the fluorescence given by a
0
saturating flash (Fm
) will be different from those measured in dark-adapted
material. Measurement of these quantities is automated in modulated fluorometers, which calculate various parameters from them (Fig. 6.5). Dark-adapted
6 Physiological ecology
Fluorescence yield (relativ e units)
Dark-adapted
6
Illuminated
Fm
Some useful parameters:
5
Fv / Fm = (Fm – F0)/ Fm
Fv
4
F ′m
ΦPSII = (F ′m – F )/ F m
′
3
∆F
2
1
NPQ = (
F m – Fm
′ )/ F m
′
F
F0
F 0′
qp = (F m
′ – F )/( F ′m – F0′)
0
Modulated
beam on
Actinic
light on
Actinic
light off
Fig. 6.5. Schematic diagram of chlorophyll-fluorescence output. Starting with a dark-adapted
plant, the low-intensity modulated beam stimulates a basal level of fluorescence, F0. A brief flash
(c. 1 s) of saturating intensity produces a maximal peak of fluorescence (Fm), which then takes a few
minutes to return to F0. Turning on a light sufficient to drive photosynthesis (actinic light) gives an
initial peak from which fluorescence settles gradually to a more or less steady level (F or Ft); a
0
saturating flash at this point gives a peak (Fm
) lower than Fm. If the actinic light is now turned off
(best in presence of far-red light) fluorescence drops to a level (F00 ) typically below the initial F0. This
gives five measurements, two initial (F0 and Fm) and three measured in the course of the
0
and F00 ). The four most generally useful parameters calculated
treatments of the experiment (F, Fm
from them are given on the right of the diagram.
Fv/Fm is a measure of maximum quantum yield of the material (c. 0.75–0.85). The
0
0
ratio (Fm
– Fs)/Fm
, often called PSII, is a measure of the effective quantum yield
0
0
– Fs)/(Fm
– F00 ), often called qP, is a measure of
under actinic light. The quotient (Fm
the oxidation state of QA, the first electron acceptor of Photosystem II; it is often
0
used in the inverse form 1 – qP. Non-photochemical quenching (NPQ), (Fm – Fm
)/
0
, is largely a measure of the harmless dissipation of excess excitation energy
Fm
as heat. Because these quantities are quotients, they are independent of the
absolute value of fluorescence omitted, and hence of the quantity of material
used. This is an advantage in that it allows measurements on small amounts of
material, but it can also be an insidious source of error in experiments extending over a period of time, especially when they include a stress event that may
lead to death of a proportion of cells in the material. It then becomes important
to be sure that the absolute value of the fluorescence has remained sufficiently
constant throughout the experiment. As this is sensitive to the optical
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M. C. F. Proctor
configuration of the fluorometer probe and the material, as well as to the
amount of chlorophyll present, careful matching and adequate replication are
important in making the measurements.
The effective quantum yield PSII multiplied by irradiance (in quantum units)
provides a relative measure of electron flow through PSII, offering a useful
alternative to gas-exchange measurements of photosynthesis. However, it measures also photorespiration, and electron flow to any other electron sink: a
source of error for photosynthesis measurements, but a potential source of
insights into other aspects of photosynthetic physiology, particularly taken
alongside CO2-exchange measurements. Many bryophytes give electron-flow/
irradiance data which are a good fit to negative-exponential saturation curves of
the form y ¼ A (1 – e–kx) (Fig. 6.6a): A is the asymptote, k is a rate constant defining
the steepness of the curve, and Ak is the initial slope. Desiccation-tolerant species
of dry sun-exposed habitats often give a good fit to these negative-exponential
saturation curves at irradiances less than about 400 mmol m 2 s 1, but at high
irradiances fail to saturate, electron flow continuing to increase more or less
linearly with irradiance (Fig. 6.6b) (Marschall & Proctor 2004). This reflects
electron flow to O2, not attributable to photorespiration but possibly due to the
Mehler reaction (Asada 1999). The non-saturating electron flow at high irradiance
is generally suppressed at high CO2 concentrations, and it is not seen in
Polytrichales (Proctor 2005), and rarely in Marchantiales.
Bryophytes generally give (by vascular-plant standards) high values of NPQ;
the levels in desiccation-tolerant mosses of dry sun-exposed sites may reach
10–15 or more at high irradiances. These high NPQ levels relax almost completely within a few minutes in the dark (Marschall & Proctor 1999, M. C. F. Proctor,
unpublished data), and are largely suppressed by the violaxanthin de-epoxidase
inhibitor dithiothreitol (DTT). This suggests that they are linked to xanthophyll
cycle-mediated photoprotection, dissipating harmlessly as heat excess excitation energy, which could otherwise lead to production of damaging reactive
oxygen species (Björkman & Demmig-Adams 1995, Horton et al. 1996, Gilmore
1997, Deltoro et al. 1998, Smirnoff 2005, Logan 2005, Heber et al. 2006).
6.4
Desiccation tolerance
Desiccation tolerance is a common and characteristic but not universal
feature of bryophytes (Proctor 1981a, Bewley & Krochko 1982, Oliver & Bewley
1997, Alpert & Oliver 2002, Proctor & Pence 2002, Wood 2007, Proctor et al.
2007b). Some species of constantly moist or shady habitats are very sensitive to
drying out, and there is every gradation between these and species of sunbaked
bare soil or rock surfaces, which not only survive but flourish in habitats where
6 Physiological ecology
Fig. 6.6. Chlorophyll-fluorescence data from Fabronia ciliata (epiphyte on Juniperus ashei, Longhorn
Cavern State Park, Texas, U.S.A.) and Tortula (Syntrichia) intermedia (exposed limestone rocks,
Chudleigh, southwest England, U.K.). Relative electron transport rate (RETR) is often a useful
surrogate for gas-exchange measurements of photosynthesis, although it includes flow to other
electon sinks, e.g. photorespiration. Fabronia pusilla gives a good saturation curve for RETR, reaching
95% of saturation at c. 475 mmol m
2
s
1
(about a quarter of full sunlight). The curve of 1 – qP does
not suggest any downstream limitation on electron flow. NPQ, rising to c. 5.5, is high by vascularplant standards. The curves for Tortula intermedia are more complex. RETR gives a good fit to a
saturation curve below c. 400, with calculated PPFD95% 940 mmol m
2
s 1. However, above this
point RETR continues to rise more or less linearly, implying electron flow to some as yet unknown
sink. The curve for 1 – qP suggests that T. intermedia can handle the electron flow generated even in
full sunlight. Non-photochemical quenching (NPQ) rises to very high levels, implying a
correspondingly high level of photoprotection. Most of the NPQ is suppressed by the violaxanthin
de-epoxidase inhibitor dithiothreitol (DTT). Its effect is seen also in a marked raising of 1 – qP,
reduction of RETR, and complete suppression of the non-saturating electron flow at high
irradiance. For further explanation see text.
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M. C. F. Proctor
they spend a large part of their time in a state of intense desiccation. Two points
about desiccation tolerance may be made at the outset. The first is that it is a
very widespread phenomenon among living organisms, occurring among
microorganisms, algae, fungi including lichens, bryophytes, and vascular plants
(where it is uncommon in vascular tissues but the norm in spores, pollen and
seeds), as well as in such animal groups as ciliates, rotifers, tardigrades, nematodes, and the eggs of Crustacea of impermanent water bodies (Alpert 2000,
2005). The second point is that vegetative desiccation tolerance has certainly
evolved (or re-evolved) independently a number of times in the plant kingdom.
While we might expect some features (and desiccation-related genes) in common throughout, there is no reason to suppose that the details will be the same
in every case (Oliver et al. 2000, 2005).
The ecological context of desiccation tolerance is intermittent availability of
water to the plant. The limiting minimum is set by the duration of precipitation
sufficient to bring the bryophyte to full turgor. In practice all bryophytes store
sufficient water to extend the moist periods substantially beyond this – how
much beyond, depends on environmentally determined rates of evaporation
(Proctor 1990, Proctor & Smith 1995). Generally, in the open under the highradiation conditions of late spring and summer, moist periods for bryophytes
tend to be closely tied to precipitation events. With declining radiation income
and the prevailing leafy canopies of late summer and autumn, water storage in
bryophyte mats and cushions can bridge progressively longer gaps between
spells of rain (Zotz et al. 2000, Proctor 2004a). As a consequence, the main period
of growth in many bryophytes in temperate climates with moderately even
rainfall distribution round the year tends to be in autumn, lack of water limiting
growth in summer, and low temperature in winter (Pitkin 1975, Proctor 1990,
Zotz & Rottenberger 2001). Clearly this will work out differently for different
species, and in different habitats and climates. Heavy dewfall may provide
sufficient water for significant early-morning photosynthesis by such species
as the steppe-grassland and sand-dune moss Tortula (Syntrichia) ruralis (Csintalan
et al. 1999), and the pendulous species (and other canopy epiphytes) of tropical
cloud forests and temperate rainforests (e.g. species of Meteorium, Pilotrichella,
Phyllogonium, Weymouthia) depend on storage of water from frequent rainfall or
interception of cloudwater droplets (Proctor 2002, 2004b, León-Vargas et al.
2006). Even in these moist forests dry periods of a few days or longer are not
uncommon, so a degree of desiccation tolerance is important for the majority of
the epiphytic bryophytes. Over much of temperate northern and western
Europe, or the northeastern United States, dry periods typically range from an
hour or two to a few weeks. At a site in southwest England in 1989, the longest
dry period recorded was 15 days (in spring); dry periods of 11 and 10 days were
6 Physiological ecology
Fig. 6.7. Desiccation tolerance: the relation of net photosynthesis (measured as oxygen
evolution) to desiccation time (at 50% relative humidity, c. 20 8C), and time after subsequent
remoistening, in the moss Anomodon viticulosus. Shading shows the area over which net
assimilation is negative. Redrawn, somewhat simplified, from the manometric data of Hinshiri
& Proctor (1971). See text for further explanation.
recorded later in the same year (Proctor 2004a). Much longer dry periods occur
in highly seasonal climates. In the Mojave Desert, where there is significant
winter bryophyte growth, more than 100 days of continuous desiccation
occurred on five occasions during 2001–2004, reaching 191 days in the drought
year of 2002 (Stark 2005). In general, growth of bryophytes requires at least
reasonably regular seasonal rainfall. Deserts with only irregular rainfall do not
support bryophytes, even though lichen growth may survive on dewfall (Negev
Desert, Israel) or fog deposition (coastal Namibia and northern Chile).
Ecophysiological responses of bryophytes to desiccation are complex. Some
basic general features are illustrated in Fig. 6.7, showing the results of a series of
experiments with Anomodon viticulosus. After short periods of desiccation (up to
about 2 weeks in this case), the moss recovers rapidly and completely on
remoistening and normal rates of photosynthesis are re-established within a
few hours. With longer desiccation, the recovery process becomes progressively
more prolonged, and final recovery less complete. In the example here, recovery
is markedly slowed, but still substantially complete within 10 h after 22 days’
desiccation. After 35 days’ desiccation recovery on remoistening is very slow,
and net photosynthesis has reached less than half its predesiccation value after
20 h remoistening. Prolonged desiccation (beyond c. 40 days in this instance)
leads to prolonged net carbon loss, with only limited ultimate recovery.
255
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M. C. F. Proctor
Results with other species differ from the pattern seen here in the time scales
on the two axes. Responses also depend on the intensity of desiccation to which
the plant has been exposed. Generally, mosses of dry sun-exposed places such as
Racomitrium lanuginosum and Tortula (Syntrichia) ruralis survive best kept at 20–50%
relative humidity, losing viability more rapidly (like most seeds) at higher
humidities (Dilks & Proctor 1974, Proctor 2003). Many woodland mosses (e.g.
Anomodon viticulosus, Plagiothecium undulatum, Weymouthia mollis) show the opposite response, surviving best at relatively high humidities (c. 75%) and worse
damaged the more intense the desiccation, recalling ‘‘recalcitrant’’ seeds.
Perhaps surprisingly, the desiccation-tolerant leafy liverworts Porella platyphylla
and P. obtusata fall into this group (Proctor 2001, 2003), although will both will
withstand drying for weeks at water contents that would immediately kill most
vascular plants.
Bryophytes are much more tolerant of high (or very low) temperatures dry
than wet. Lethal temperatures for moist, metabolically active bryophytes are in
the same range as for C3 vascular plants, about 40–50 8C (Larcher 1995, Liu et al.
2004). Survival of desiccation is related to temperature. The desiccation-tolerant
species Anomodon viticulosus, Tortula (Syntrichia) intermedia, and Frullania tamarisci,
gave a good straight-line ‘‘Arrhenius plot’’, with the logarithm of survival time
linearly proportional to the reciprocal of the absolute temperature (Hearnshaw
& Proctor 1982), an expected result if loss of viability follows essentially chemical degradation. In Racomitrium lanuginosum and R. aquaticum, the relation was
curvilinear; it is possible that different systems are critical at different temperatures. In either case, survival times are measured in minutes at 100 8C and in
months or years at 0 8C.
There clearly must be a lower limit to the time for which a bryophyte can
usefully be moist. ‘‘Moist-break’’ experiments showed that Hylocomium splendens
desiccated for 11 days at 32% relative humidity recovered to substantially its predesiccation photosynthetic activity after 24 h, but not after 6 h moist (Dilks &
Proctor 1976). Tuba et al. (1996) found that Tortula (Syntrichia) ruralis, rehydrated
after 24 h dry, attained positive net photosynthesis within 30 minutes, and
recovered its predesiccation carbon balance within an hour or less. Gasexchange measurements on Grimmia pulvinata, Andreaea rothii, and Polytrichum
formosum have yielded similar figures (Proctor & Pence 2002, Proctor et al. 2007a).
However, full recovery to predesiccation rates of photosynthesis may take
24 hours or more, while chloroplasts and other organelles and subcellular
structures regain their normal conformation and spatial relationships (Proctor
et al. 2007a). Studies of desiccation tolerance have most often used some aspect
of photosynthesis as an index of recovery, but other systems are important too.
Respiration begins immediately on rehydration. Protein synthesis is quickly
6 Physiological ecology
re-established (Gwózdz et al. 1974, Oliver 1991), and is clearly a necessary part of
full recovery. The photosystems become active within seconds or a minute or
two of remoistening, but the enzyme systems of the ‘‘dark reactions’’ of photosynthesis recover more slowly. Recovery of the cell cycle seems to be much
slower. Mansour & Hallet (1981) studied the effect of 24 h dehydration on the
cell cycle in Polytrichum formosum. The first 2 h of water stress provoked completion of mitosis. On rehydration, 24 h passed before the first cell began to divide.
DNA synthesis resumed in the nuclei of a few cells after 4 h, but cell-cycle
activity rose steeply only after 24 h rehydration. Pressel et al. (2006) found a
similar time scale for full re-establishment of the microtubular cytoskeleton on
rehydration in food-conduction cells of Polytrichum formosum. There are indications that the reversible depolymerization and reassembly of the microtubular
cytoskeleton may be critical in limiting the rate of drying that can be tolerated,
and in full recovery of viability and cell function (Pressel 2006). Thus it is
possible to envisage different levels of ‘‘recovery’’. Short periods at full turgor
may suffice for maintenance of a positive carbon balance, yet be inadequate for
cell division, or significant translocation or growth. Very little attention has been
given to the desiccation tolerance of gametangia or the sporophyte generation,
although sporophytes of many species must be exposed to desiccation in the early
stages of their development following spring or early summer fertilization, as
commonly occurs. Those that take more than a year to come to maturity (e.g. Ulota
spp., Pylaisia polyantha (Lackner 1939)) face desiccation in a second summer later in
their development. In Tortula inermis the evidence indicates either that sporophytes are more sensitive to rapid drying than the gametophytes, or that abortion
of sporophytes arises from a gametophyte response to desiccation stress (Stark
et al. 2007).
Recovery seems to be largely a matter of physical re-assembly of components
conserved intact through the drying/rewetting cycle. In a number of mosses that
have been studied, the recovery process itself (as measured by either chlorophyll
fluorescence or gas exchange) is virtually unaffected by protein-synthesis inhibitors (Proctor & Smirnoff 2000, Proctor 2001, Proctor et al. 2007a). Chlorophyllfluorescence data from Racomitrium lanuginosum are shown in Fig. 6.8, using Fv/Fm
as an index of recovery. In the dark, there is no significant difference in the Fv/Fm
values given by material recovering in water, in 3 mmol l 1 chloramphenicol
(inhibiting chloroplast-encoded protein synthesis), in 0.3 mmol l 1 cycloheximide (inhibiting nuclear-encoded protein synthesis) or in 3 mmol l 1 dithiothreitol (which inhibits de-epoxidation of the xanthophyll violaxanthin to
zeaxanthin, suppressing photoprotection). In the light, all treatments give
quite good initial recovery, but after 18 h the curves have diverged widely.
Cycloheximide has only a modest effect, but chloramphenicol leads to a strong
257
258
M. C. F. Proctor
Fig. 6.8. An experiment showing the effect of metabolic inhibitors on recovery of Fv/Fm in the
moss Racomitrium lanuginosum after c. 10 days’ desiccation. Open circles control (water); open
squares, 3 mmol l
1
dithiothreitol; solid triangles, 3 mmol l
diamonds, 0.3 mmol l
1
1
chloramphenicol; solid
cycloheximide; superimposed squares and triangles, dithiothreitol þ
chloramphenicol. (a) In dark; the cycloheximide treatment is scarcely distinguishable from the
control, and dithiothreitol and chloramphenicol have only modest effects alone or in
combination. (b) In light (c. 125 mmol m
2
s 1), cycloheximide (inhibiting nuclear-encoded
protein synthesis) produces a slow but progressive fall in Fv/Fm. With dithiothreitol, Fv/Fm drops
rather quickly to values around 0.4, probably reflecting suppression of the photoprotection
associated with NPQ. Chloramphenicol produces a rapid and progressive drop in Fv/Fm,
especially in the presence of dithiothreitol. This is likely to reflect the rapid turnover of the
D1 protein of Photosystem II in the light (Anderson et al. 1997), with the effect of
chloramphenicol inhibiting its replacement accentuated when photoprotection is suppressed
by dithiothreitol.
progressive decline in dark-adapted Fv/Fm over the 54 h duration of the experiment, indicating photo-damage to a chloroplast-encoded protein, probably the D1
protein of Photosystem II, which is known to turn over rapidly in the light.
Dithiothreitol has a marked effect on its own by removing xanthophyll cyclemediated photoprotection, and it increases the effect of chloramphenicol. Other
species differ in details, but the broad picture is similar in all. Recovery in the dark
is complete, and very little affected by protein-synthesis inhibitors. In the light
there is ongoing photo-damage, and protein synthesis is essential to repair it.
What are the essential requirements for desiccation tolerance? In very general terms, tolerance clearly requires a cell structure that can lose most of its
water without disruption, and membranes that retain the essentials of their
structure in the dry state or are readily and quickly reconstituted on remoistening. All the essential metabolic systems of the plant must remain intact or be
6 Physiological ecology
Fig. 6.9. (a) Recovery of the chlorophyll-fluorescence parameters Fv/Fm and FPSII
(at 50 mmol m
2
s
1
PPFD) following remoistening of the moss Anomodon viticulosus after 21
days’ desiccation, with NPQ estimated from the mean values of Fm and F 0 m of two sets of
matched samples (n ¼ 3). Note the rapid recovery of Fv/Fm, the slower recovery of FPSII, and the
sharp peak of NPQ in the early minutes of recovery (redrawn from data of Csintalan et al. 1999).
(b) Response of NPQ (at c. 200 mmol m
2
s
1
PPFD) to water loss in Polytrichum formosum; portions
are shown of curves fitted to three overlapping segments of the data (redrawn from
measurements of Proctor et al. 2007a).
readily reconstituted, and it is a reasonable prima facie supposition that there is
unlikely to be any one critically sensitive system because selection pressure will
bear heavily on any weak link. One might expect to find ‘‘molecular packaging’’
materials, most likely sugars (Seel et al. 1992, Smirnoff 1992) and/or proteins
(Oliver 1996, Oliver et al. 2005), protecting macromolecules in the absence of
water. Drying of the cell contents to a vitrified or ‘‘glassy’’ state is probably also
important (Crowe et al. 1998, Buitink et al. 2002), both in slowing metabolic
reactions and in maintaining the spatial relationships of cell components and
membrane and enzyme systems – in effect, providing a reversible biological
equivalent of good electron-microscopy fixation. Again both sugars and proteins
are probably implicated (Buitink et al. 2002). Another reasonable expectation is
good antioxidant and photo-protection, minimizing the production of damaging reactive oxygen species, and detoxifying those that form (Foyer et al. 1994,
Alscher et al. 1997, Smirnoff 1993, 2005, Logan 2005, Heber et al. 2006). The high
levels of NPQ seen in many desiccation-tolerant bryophytes must be important
in photoprotection; NPQ also rises with desiccation stress, and peaks in the
minutes following rehydration (Fig. 6.9, Csintalan et al. 1999, Marschall &
Proctor 1999, Proctor et al. 2007a).
259
260
M. C. F. Proctor
Many highly desiccation-tolerant bryophytes tolerate drying within half an
hour or less without damage. Their tolerance is clearly constitutive. Others are
intolerant of rapid drying but become tolerant in the course slow drying, or if
they are first exposed to a period of relatively mild water stress (Abel 1956).
However, there is undoubtedly a spectrum of possibilities between extreme
constitutive desiccation-tolerant bryophytes, and species in which tolerance is
induced in the course of slow drying or periods of subcritical water stress. In
such species tolerance depends heavily on ‘‘hardening’’ processes and may be
under abscisic acid (ABA) control, as in Funaria hygrometrica protonema (Werner
et al. 1991, Bopp & Werner 1993) and the marchantialean liverwort Exormotheca
holstii (Hellewege et al. 1994), or seasonally switched as in Lunularia cruciata
(Schwabe & Nachmony-Bascomb 1963). That some degree of hardening/dehardening can occur in even the most tolerant species is shown by the results of
Dilks & Proctor (1976) and Schonbeck & Bewley (1981). Much more investigation
of desiccation tolerance, drought-hardening and possible effects of ABA in
common forest and grassland bryophytes is greatly needed.
6.5
Overview
How can the special ecophysiological characteristics of bryophytes be
summarized in a few words? First, most bryophytes carry substantial amounts
of external water, which is physiologically important and can vary widely without affecting the water status of the cells, so bryophytes spend most of their time
either fully turgid, or dry and metabolically inactive. It is essential to know (at least
approximately) the true full-turgor water content for research on effects of
water stress on bryophyte cells and tissues. Second, bryophytes grow and function largely within the laminar boundary layer of the atmosphere next to the
ground or other substratum, and their immediate surroundings are in effect an
integral part of their physiology. Third, intermittent availability of water is the
norm for many bryophytes; their desiccation tolerance may be more usefully
thought of as a means of evading drought, than as an extreme form of drought
tolerance. Initial recovery from normal desiccation is rapid and seems to depend
little on protein synthesis, but we still have much to learn about the fundamental basis and consequences of desiccation tolerance. Fourth, a tendency to
shade-plant features in bryophytes springs mainly from their common situation
in the understorey of vegetation, and their poikilohydry, photosynthesizing
mainly in rainy and overcast weather. Unistratose leaves can be CO2 diffusionlimited at high irradiance. Most bryophytes of dry sunny habitats show only
moderately high light-saturation levels, but very high levels of NPQ (and photoprotection) at high irradiances. The highest saturation irradiances are found
6 Physiological ecology
among the Polytrichales and Marchantiales with complex ventilated photosynthetic tissues. All bryophytes are C3 plants; anthocerotes are unique in having a
carbon-concentrating mechanism. Finally, this last point is a reminder that
bryophytes are phylogenetically diverse: the major groups – mosses, hepatics,
anthocerotes – have been evolutionarily independent from one another and
from vascular plants through most of the history of plant life on land.
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Rice, S. K. & Giles, L. (1996). The influence of water content and leaf anatomy on
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7
Biochemical and molecular
mechanisms of desiccation
tolerance in bryophytes
melvin j. oliver
7.1
Introduction
Bryophytes, because they descend from the earliest branching events in
the phylogeny of land plants, hold an important position in our investigations into
the mechanisms by which plants respond to dehydration and by what paths such
mechanisms have evolved. This is true regardless of what aspect of plant
responses to dehydration one is interested in; whether it be mild water deficit
stress as seen in most plants including those of agronomic importance, or desiccation as seen in orthodox seeds or in the leaves of desiccation-tolerant (or resurrection) plants. It is quite possible that the mechanisms by which bryophytes tolerate
dehydration closely reflect the way that the first land plants coped with the rigors
of a drying atmosphere as they began their colonization of the land. In a recent
phylogenetic synthesis of the evolution of desiccation tolerance within the land
plants (Oliver et al. 2000), it was postulated that vegetative desiccation tolerance
was required for plants to transition from an aqueous environment to the dry
land. In the initial ventures into dehydrating atmospheres, plants were of a very
simple architecture and had yet to evolve the complex strategies to prevent water
loss that we see in modern day plants. Once the cells of these plants were no longer
surrounded by liquid water they would rapidly lose water and dry. Thus it is highly
likely that primitive plants spent much of their time in the air-dried state, which
generally means they would experience water deficits of 100 MPa or more
(Alpert & Oliver 2002). To survive such water deficits (most modern day plants
do not survive 3 to 5 MPa) these plants had to evolve vegetative desiccation
tolerance. Given that, as we believe, desiccation tolerance first evolved in spores as
a means of surviving the rigors of dispersal, it is quite likely that the type of
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
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desiccation tolerance that these early land plants exhibited was co-opted for use in
vegetative cells (Oliver et al. 2005). Spores appear to utilize, if one can extrapolate
from studies of desiccation tolerance in pollen (Hoekstra 2002), a relatively simple
mechanism of cellular protection to survive drying to very low water potentials. As
plants evolved to fill the multitude of different types of habitats and environmental niches that dry land offered, the ways in which plants were able to tolerate
dehydration also evolved from a simple protective mechanism to ones of greater
complexity and efficiency. It is clear, however, that as plants became more complex and gained the capability to transport water and nutrients through specialized conduits or vascular tissues, they lost the ability to tolerate desiccation of
their vegetative tissues (Oliver et al. 2000). Bryophytes, whose ancestors marked
the transition to land and hence preceded the development of tracheophytes in
the land plant phylogeny, present a unique opportunity to look at mechanisms of
dehydration tolerance, in particular vegetative desiccation tolerance, that have
directly evolved from the earliest stages of land plant evolution.
7.2
Phenotypic considerations
Dehydration tolerance describes the ability of plants to survive and
recover from the loss of cellular water. Desiccation tolerance, however, is the
ability of plants (or plant tissues) to withstand the severest dehydration stress,
namely to dry to equilibrium with moderately dry air and to fully recover when
rehydrated. Vegetative desiccation tolerance is reported to be relatively common,
but not universal, in the bryophytes (Proctor 1990, Proctor & Pence 2002); it is rare
in vascular plants with only 330 species listed so far (Porembski & Barthlott (2000).
The commonality of vegetative desiccation tolerance in bryophytes is a widely
held belief but is derived from anecdotal reports and personal observations in the
field. Wood (2007) attempts to bring a more scientific accounting to the question
of the occurrence of desiccation tolerance in the bryophytes by only reporting
those species for which there has been an experimental demonstration of tolerance. By this strict cataloging Wood identifies 158 species of mosses, 51 liverworts, and 1 species of hornwort as being vegetatively desiccation-tolerant, about
1% of all bryophytes. Wood (2007) also provides a protocol for the experimental
determination of desiccation tolerance for bryophytes and as this is more widely
applied the number of species that can be documented as desiccation tolerant will
undoubtedly rise. Although many bryophytes seem to be able to survive desiccation, very few have been the subjects of in-depth studies into how such a phenotype is mechanistically delivered. Indeed, much of what we know about the
mechanistic aspects of desiccation tolerance in bryophytes comes from the
study of single species, the moss Tortula ruralis (Syntrichia ruralis).
7 Desiccation tolerance mechanisms in bryophytes
Modern day bryophytes face much the same environment, with regards to
water relations, as primitive plants did when first they occupied dry land habitats.
The leaves of bryophytes are generally one cell layer thick and rely on an external
supply of liquid water to remain turgid. Bryophyte cells freely lose water to the
atmosphere when liquid water is no longer present on their surface and as a
consequence they rapidly and directly equilibrate with the water potential of the
air, which is generally dry, and thus they desiccate. The speed at which desiccation
is achieved is dependent upon the relative humidity of the surrounding air: the
dryer the air the more rapid the rate of dehydration. The speed of desiccation has
important consequences for the cells of bryophytes and has a direct impact on the
type of mechanism these plants have evolved to survive the air-dried state (as will
be discussed below). The extent of water loss, which is dependent upon both the
relative water content of the air and the temperature of the habitat, is also an
important factor in how bryophytes tolerate desiccation. For example, equilibration at 50% relative humidity (RH) at 28 8C would generate a 100 MPa water
deficit in the cells of a bryophyte. Most bryophytes can survive dehydration to 20
to 40 MPa for a short time but these are not considered desiccation-tolerant,
even though such water deficits are an order of magnitude greater than what most
plants can survive (Proctor & Pence 2002). Desiccation-tolerant bryophytes can
survive rapid drying rates, more extensive water loss, and remain dry for longer
periods than those that are simply dehydration tolerant. Tortula caninervis (Syntrichia
caninervis), a desert relative of Tortula ruralis, can survive rapid desiccation (within
30 min) to approximately 540 MPa (equilibrated to the atmosphere above activated silica gel; 2%–4% RH) for up to six years, returning to normal metabolic
activity upon rehydration (Oliver et al. 1993, unpublished data (pers. obs.)).
Some desiccation-tolerant bryophytes also increase their level of desiccation
tolerance if they experience mild dehydration events prior to desiccation, a process known as hardening (Proctor & Pence 2002). This is true for most of the Tortula
(Syntrichia) species, including Tortula ruralis (Schonbeck & Bewley 1981, unpublished data). Rehydration, as one would expect, is almost instantaneous and
creates in its own right a stressful cellular event. Thus the phenotype of desiccation tolerance is not a simple one, as speed of drying, time in the dried state, how
dry the tissue becomes, previous drying history, and the rigors of rehydration all
play a role in determining how desiccation tolerance is achieved.
7.3
General aspects of desiccation tolerance
as they relate to bryophytes
Early observations of bryophyte tissues undergoing desiccation and
rehydration led workers to postulate that it was the mechanical properties of
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cells that formed the underlying basis of vegetative desiccation tolerance in
plants. Structural features such as small cells, flexible cell walls, small vacuoles,
and a lack of plasmodesmata were all suggested as important aspects of desiccation tolerance in plants (Iljin 1957). Although this viewpoint has been largely
discarded as a means of explaining desiccation tolerance in bryophytes (Oliver &
Bewley 1984), the ability to tolerate the mechanical stresses of desiccation and
rehydration is an important factor for all plants but is more evident in the
desiccation-tolerant angiosperms (Vicré et al. 2004). Bewley (1979) proposed
the current theory that desiccation tolerance is primarily an inherent property
of the cellular contents (protoplasm), an hypothesis that has so far stood the test
of experimental inquiry. Bewley (1979), based on available microscopic and
biochemical evidence, further defined what the properties of a desiccationtolerant protoplasm must encompass: it must (a) limit damage to a repairable
level; (b) maintain integrity when in the dried state; and (c) upon rehydration,
rapidly mobilize mechanisms that repair any damage that has been sustained as
a result of both desiccation and from the rapid influx of water. Basically this
means that desiccation tolerance can be achieved by protection of cellular
structures and components, damage control during the dried state, and an
active cellular repair activity that functions during and following rehydration
(Bewley & Oliver 1992). Thompson and co-workers (Platt et al. 1994, Thompson &
Platt 1997), based on freeze fracture and freeze substitution electron microscopy of dried and drying Tortula ruralis (freeze fracture only) and Selaginella
lepidophylla (a fern relative) vegetative tissues, extended the Bewley (1979) view
of desiccation tolerance to include the requirement that a critical level of
physical cell order be maintained in the dry state. This conservation of cell
order requires a high degree of effective packing and shape fitting of cellular
constituents driven by the compaction forces of dehydration. Alpert and Oliver
(2002) elaborated further by contending that desiccation tolerance must also
require an orderly shutdown of metabolism during drying so as to avoid the
possibility of a build up in toxic intermediates and the generation of reactive
oxygen species (ROS), a major stress associated with desiccation (Smirnoff 1993).
The effectiveness of the cellular protection aspects of a particular mechanism
for desiccation tolerance, and to some extent the repair processes, determines
the intensity of the desiccation (the minimum water potential) that a particular
species can survive. In general, desiccation-tolerant bryophytes are capable of
surviving water potentials below 300 MPa, and most can survive long periods
in air that is dried to <2% RH (over silica gel) that generates water potentials
closer to 500 MPa. In contrast, desiccation-tolerant pteridophytes cannot survive such treatment (Gaff 1977). The effectiveness of cellular protection and the
efficiency of repair processes probably combine to determine the length of time
7 Desiccation tolerance mechanisms in bryophytes
desiccation-tolerant plants can remain in the dried state. Bryophytes are particularly hardy in this regard. Tortula caninervis and Tortula ruralis have been
documented to resume normal metabolic activity after being stored dry for
three years (Oliver et al. 1993), and Grimmia laevigata grew when hydrated after
ten years of storage in a herbarium (Keever 1957). However, Tortula norvegica,
although capable of tolerating desiccation to a water potential of 540 MPa, was
severely damaged following storage for 12 months or more (Oliver et al. 1993),
suggesting that the level of cellular protection and efficiency of cellular repair
are not as well developed in this species compared to its close relatives. Most
desiccation tolerant bryophytes survive best and thus longer if kept equilibrated
to atmospheres between 20% and 50% RH at 20 8C ( 100 to 400 MPa), storage at
lower RH leads to a quicker loss in viability (Proctor & Tuba 2002).
Levels of cellular protection vary not only between desiccation-tolerant species of bryophytes but also seasonally and between generations. The South
African moss Atrichum androgynum is more tolerant, as measured by ion leakage
assays, during the dry months of the year and less tolerant when moisture is
readily available (Beckett & Hoddinott 1997). This may partially reflect a seasonal hardening/dehardening process but this in turn is directly related to the
availability of cellular protectants stored within the cells; in times when water is
plentiful more energy is directed towards growth than to the sequestration and
biosynthesis of protectants. Stark et al. (2007) demonstrate that the sporophytes
of Tortula inermis, a highly tolerant desert species, are clearly less desiccationtolerant than the gametophytic generation that supports them. This may be
generally true for most desiccation-tolerant bryophytes although evidence is
generally anecdotal; gametangia of desiccation-tolerant mosses are apparently
desiccation-tolerant as they persist over several months during which the
mosses spend a considerable time dry (Mishler & Oliver 1991, Stark 1997).
7.4
Biochemical and molecular aspects of desiccation
tolerance in bryophytes
7.4.1
Constitutive cellular protection
The ability of desiccation-tolerant bryophytes to withstand and recover
from very rapid water loss, to water potentials below 500 MPa within 30 min,
indicates that they have a constitutive cellular protection mechanism that is
ready and waiting to be challenged (or activated) by desiccation. The effectiveness
of this constitutive cellular protection is evidenced by the fact that the plasmamembrane and organellar membranes of Tortula ruralis cells remain intact and
maintain their normal bilayer organization in the dried state (Platt et al. 1994).
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The loss of water in very dry atmospheres is far too rapid to allow for the
induction and de novo establishment of cellular protection processes as this
would require not only a switch in metabolic activity to generate protective
components, but also the induction of transcription and synthesis of novel
proteins that are required for tolerance: both of which require a significant
amount of time. This notion is substantiated by the overwhelming evidence that
in Tortula ruralis (and other moss species) protein synthesis, in particular the
translation initiation process, is extremely sensitive to the loss of water from the
cytoplasm and quickly ceases, rendering the synthesis of proteins for cellular
stability impossible (reviewed by Bewley 1979, Bewley & Krochko 1982).
Furthermore, even if drying is slow (within 6 h) novel transcripts are not
recruited into the protein synthetic machinery during dehydration and so
desiccation tolerance in bryophytes, at least in the moss Tortula ruralis, does
not require the synthesis of novel proteins during the drying phase of a desiccation event (Oliver 1991). The inference from these observations is that proteins,
whether protective or involved in establishing protective components, are
already present in the cells in sufficient quantities to establish desiccation
tolerance. This is not the case for any other mechanism or cellular strategy for
vegetative desiccation tolerance where such proteins are synthesized de novo
during drying (Bartels & Sunkar 2005); it is, however, similar to the strategy for
developmentally programmed desiccation tolerance where cells are primed for
a desiccation event prior to dispersal from the mature plant. This may further
emphasize the evolutionary link between desiccation tolerance in spores and
mechanisms for vegetative desiccation tolerance in bryophytes.
At this point it is worth, for the sake of contrast, briefly discussing mechanisms
of vegetative desiccation tolerance that are seen in the angiosperms. As mentioned above, vegetative desiccation-tolerant angiosperms can only survive desiccation if the rate of dehydration allows for the establishment of cellular
protective measures (Oliver & Bewley 1997, Phillips et al. 2002, Proctor & Pence
2002). The early phase of drying in the desiccation-tolerant angiosperms is
marked by a major switch in transcriptional activity, resulting in the generation
of a large number of novel transcripts, which in turn generate proteins specific
for the drying phase (Ingram & Bartels 1996, Oliver et al. 2000, Alpert & Oliver
2002, Phillips et al. 2002, Collett et al. 2004). The induced change in transcriptional
control reveals a broad range of dehydration-regulated genes that have an equally
broad range of putative functions, testament to the severity of the stress and the
complexity of the interactions between cellular processes designed to deliver
tolerance (Phillips & Bartels 2000). The induction of gene expression in response
to dehydration in desiccation-tolerant angiosperms involves two classes of signal
induction pathway, one that is controlled by the plant hormone abscisic acid
7 Desiccation tolerance mechanisms in bryophytes
(ABA) and the other ABA-independent (Phillips et al. 2002, Ramanjulu & Bartels
2002). Endogenous ABA concentrations increase in vegetative tissues in response
to dehydration in all angiosperms studied to date, even those that are sensitive to
this stress (Bray 1997). Although some signaling pathways involved in the
response of plants to dehydration are ABA-independent, application of exogenous
ABA is sufficient to induce desiccation tolerance in desiccation-sensitive callous
tissue derived from the leaves of the desiccation-tolerant angiosperm
Craterostigma plantagineum (Bartels et al. 1990). Pretreatment of fronds of the
resurrection fern Polypodium virginianum with exogenous ABA allows the plant to
survive otherwise lethal rates of dehydration (Reynolds & Bewley 1993).
In orthodox seeds and vegetative tissues of desiccation-tolerant angiosperms
two cellular components, the Late Embryogenesis Abundant (LEA) proteins and
soluble sugars, accumulate in response to desiccation (for review see Phillips et al.
2002, Buitink et al. 2002, Kermode & Finch-Savage 2002). These two components
are generally considered critical to the acquisition of cellular desiccation tolerance, although the actual function of the LEA proteins remains unclear (Cuming
1999). The types of gene that are induced by desiccation (and in many cases ABA
treatment) code for proteins that fall into several categories: proteins involved in
signal transduction pathways that regulate genes during stress responses, proteins participating in carbohydrate metabolism (generally involved in sucrose
accumulation), protective proteins such as chloroplast stabilizing proteins, LEAs
and heat shock proteins, aquaporins, and proteins involved in anti-oxidant biosynthesis and ROS scavenging (Phillips & Bartels 2000, Ramanjulu & Bartels 2002,
Phillips et al. 2002, Collett et al. 2004, Illing et al. 2005). The physiological significance of these gene products will be discussed in more detail where relevant to
the discussion of desiccation tolerance in bryophytes.
How is constitutive desiccation tolerance achieved in the bryophytes? This is
a question for which we have lots of theories but few answers. Much of the
uncertainty is a result of the fact that we do not fully understand desiccation
tolerance per se and much of what we do know comes mainly from inference and
observation of what components are present in desiccated cells. Given this, it is
generally accepted that there are at least three components necessary for desiccation tolerance in bryophytes: (1) sugars, in general sucrose, (2) protective
proteins, in particular proteins with homology to the LEA proteins of angiosperms, and (3) antioxidants and enzymes involved in protection from ROS.
Sugars: The accumulation of soluble sugars has long been correlated with the
acquisition of desiccation tolerance in plants and other organisms (Gaff 1977,
Scott 2000, Phillips et al. 2002, Walters et al. 2002). Orthodox seeds, pollen, and
most plants that accumulate soluble sugars in response to desiccation utilize the
disaccharide sucrose. Sucrose makes up approximately 10% of the dry mass of
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Tortula ruralis gametophytes and does not change in amount during desiccation
or rehydration in the dark or light (Bewley et al. 1978). This is apparently
common for desiccation-tolerant bryophytes (Smirnoff 1992). The current
hypotheses are that sugars either protect the cell via a process known as
vitrification, i.e. the formation of a biological glass (a supersaturated liquid
with the mechanical properties of a solid that prevents the crystallization of
cellular solutes and slows chemical activity), and/or by maintaining hydrogen
bonds within and between macromolecules, thus stabilizing their structure, e.g.
membranes (Hoekstra et al. 2001). Sucrose has long been associated with glass
formation and it is currently thought that LEA proteins are also required for the
vitrification process (Buitink et al. 2002). However, biological glass formation
during desiccation has not been verified for bryophytes as yet.
Proteins: The major group of proteins associated with cellular protection
during drying is the LEA proteins. LEA proteins, of which there are at least five
major groups, have functions that remain largely unknown, but are assumed to
be important in the establishment of desiccation tolerance in seeds and, by
inference, vegetative tissues (Cuming 1999, Buitink et al. 2002, Kermode &
Finch-Savage 2002). The most compelling evidence for their role in desiccation
tolerance comes from work with Arabidopsis mutants, a double mutant of ABAdeficient (aba – lesion in ABA biosynthesis) and ABA-insensitive (abi3 – lesion in
responsiveness to ABA), that lack many of the LEA proteins and which do not
tolerate desiccation (Koorneef et al. 1989, Meurs et al. 1992). Also, overexpression
of a single LEA protein, HVA1 from barley, in transgenic rice plants increased
their tolerance to water deficit stress (Xu et al. 1996). LEA proteins have been
identified in the vegetative tissues of all desiccation-tolerant plants studied so
far (Ingrams & Bartels 1996, Oliver & Bewley 1997, Blomstedt et al. 1998) and one
class in particular, the Group 2 LEAs (dehydrins) have been associated with the
vegetative response of non-tolerant plants to water stress (Skriver & Munday
1990, Bray 1997, Bartels & Sunkar 2005). Using antibodies specific for a conserved motif within dehydrin protein sequences, Bewley et al. (1993) demonstrated that dehydrins are sequestered in leaf cells of Tortula ruralis under
hydrated conditions and are unaffected by desiccation and rehydration, except
for a slight loss of the main dehydrin during slow drying. This is consistent with
a constitutive cellular protection strategy and in stark contrast to the induction
of synthesis and sequestration of dehydrins during dehydration in both sensitive and desiccation-tolerant angiosperms (Bartels et al. 1990, Cuming 1999,
Bartels 2005, Illing et al. 2005).
Many hypotheses as to how LEA proteins protect cells from the rigors of
dehydration have been proposed (Cuming 1999) but as of yet there is no definitive mechanism that can be attributed to any of the LEA proteins or groups.
7 Desiccation tolerance mechanisms in bryophytes
Studies have provided evidence for LEA proteins acting as hydration buffers, in
ion sequestration, renaturation of unfolded proteins, direct protection of membranes, and binding to DNA to stabilize chromatin (Crowe et al. 1992, Cuming
1999). In vitro studies point to a role for LEA proteins in the stabilization of
enzymes under denaturating conditions, either by preventing aggregation
(Goyal et al. 2005) or by direct protection (Grelet et al. 2005). Of note is the
suggestion, driven from data derived from molecular modeling of Group 3 LEA
proteins, that LEA proteins could form cytoskeletal filaments that could perhaps
aid in the ordered drying of the cytoplasm to prevent damage or to simply
stabilize membranes (Wise & Tunnacliffe 2004).
Other protective proteins that have been associated with vegetative desiccation tolerance in angiosperms, such as the low-molecular-mass heat shock
proteins (Alamillo et al. 1995), have not been investigated in bryophytes as yet.
These proteins have been shown to have chaperone-like properties that help
proteins fold and maintain their active structures, and are thought to play this
role in vivo during dehydration (Bartels & Sunkar 2005).
7.4.2
Reactive oxygen scavenging pathways
The generation of ROS (e.g. singlet oxygen, hydroxyl radicals, hydrogen
peroxide, and superoxide anions) during dehydration occurs mainly from the
inhibition of photosynthesis, by oxidation of the D1 protein and inhibition of
the repair of Photosystem II reaction centers, and is potentially the major source
of cellular damage for desiccation-tolerant bryophytes (and all plants) as they
dry (Smirnoff 1993, Apel & Hurt 2004). ROS accumulation has many damaging
effects on cellular components besides the effect on Photosystem II components, including protein denaturation via the oxidation of sulfhydryl groups,
pigment loss, and lipid peroxidation and free fatty acid accumulation in membranes (McKersie 1991, Smirnoff 1993, Apel & Hurt 2004).
Tortula ruralis appears to have the capability of preventing the peroxidation of
membrane fatty acids during dehydration by suppressing lipoxygenase activity,
an enzyme that if released from sequestering peroxisomes or the vacuole catalyzes the peroxidation of fatty acids within the cells. Part of the protection may
be afforded by the observed maintenance of oil droplets within the cytoplasm of
Tortula ruralis gametophyte cells, which may act as a sort of peroxidation buffer
(Stewart & Bewley 1982). This is not true of all mosses, as dehydration of the
moderately desiccation-tolerant moss Atrichum androgynum results in significant
peroxidation of membrane phospholipids (Guschina et al. 2002). Oxidative
denaturation of sulfhydryl-containing enzymes during dehydration has been
reported for several desiccation-tolerant mosses (Stewart & Lee 1972). These
workers also reported that they could alleviate this damage by incubating the
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mosses in reduced glutathione (GSH) solutions; reduced glutathione is a natural
antioxidant present in all plant cells. The pool of GSH in Tortula ruralis is reduced
to 30% of its hydrated cell level during slow drying, indicating a reduced ability
of the moss to buffer ROS and therefore withstand oxidative injury when in the
dried state (Dhindsa 1987). Tortula ruraliformis, on the other hand, does not
exhibit a reduction of its GSH pool during desiccation (Seel et al. 1992b) but it
does suffer a decline in another cellular antioxidant, ascorbate. Thus in Tortula
ruralis maintaining a significant pool of GSH in the dried state may not be an
important strategy for protection whereas it is for Tortula ruraliformis. These
studies are somewhat difficult to reconcile because the ascorbate and glutathione systems are closely linked in plants (Foyer et al. 1994, Alscher et al.
1997, Smirnoff 2005). Obviously the antioxidant pathways and their synthetic
and catabolic activities during desiccation in desiccation-tolerant (and sensitive)
bryophytes are a ripe target for further research.
When plant tissues are desiccated in the light, ROS levels increase dramatically and oxidative damage increases (Smirnoff 1993). The increased generation
of ROS by light in drying or dried plant tissues results from the inability of the
light harvesting complexes of the photosynthetic machinery to pass on the
energy absorbed from light into the normal photochemical pathways which
are inactive under dehydrated conditions. The unchanneled energy, if not dissipated in some manner, can directly result in the formation of reactive oxygen
species from water. Seel et al. (1992a) demonstrated that Tortula ruraliformis was
capable of preventing lipid peroxidation and pigment loss under high light
conditions whereas a more desiccation-sensitive moss, Dicranella palustris, suffered both increased oxidative damage and an inability to recover from dehydration under the same conditions. It thus appears that for desiccation-tolerant
mosses, photoprotective mechanisms that limit ROS production or detoxify
them are important if survival, especially long-term survival in high-light environments such as deserts, is to be achieved. One obvious means of limiting lightinduced ROS production is to dissipate the excess excitation energy generated
by the photosynthetic machinery as heat, and in plants this is achieved via the
xanthophyll cycle (Demmig-Adams & Adams 1992). Several studies point to this
as a mechanism for photoprotection in both liverworts (Deltoro et al. 1998,
Marschall & Proctor 1999) and mosses (Heber et al. 2001, 2006).
It is obvious from this discourse that we have a limited knowledge of how
bryophytes develop and maintain cellular protection to limit desiccationinduced damage and thus achieve desiccation tolerance. The process of vitrification in desiccating vegetative tissues is largely underexplored and bryophytes
offer an ideal model for such studies. How biological glasses form and what is
required (e.g. sugar content, types of sugars, protein–sugar interactions, level of
7 Desiccation tolerance mechanisms in bryophytes
dehydration, etc.) for their formation would greatly increase our understanding
of the constitutive protection system in desiccation-tolerant bryophytes. In
addition, much more work is needed before we fully understand how bryophytes protect themselves from the oxidative damage associated with desiccation and rehydration.
7.5
Induced desiccation tolerance in bryophytes
As mentioned earlier, bryophytes can exhibit an increase in desiccation
tolerance if they experience mild dehydration events prior to desiccation (hardening). This result implies, at least in part, that desiccation tolerance, and by
inference cellular protection strategies, are inducible under some circumstances. Beckett (1999) demonstrated that desiccation tolerance of the mesic
moss Atrichum androgynum could be increased by a previous drying treatment
and that addition of abscisic acid (ABA) to the hydrated moss could produce the
same increase in tolerance. ABA treatment of Funaria hygrometrica not only
increases tolerance to desiccation, allowing for survival of rapid desiccation
that is normally lethal, but also results in the induction of the synthesis of a
number of proteins that accumulate during drying (Werner et al. 1991, Bopp &
Werner 1993). Werner et al. (1991) also determined that endogenous levels of
ABA increased 5–6-fold during slow drying, indicating that an induced protection system operates in this moss to develop desiccation tolerance. However, in
these experiments the protonemal cultures were dried for only short periods of
time in air of unknown water content and it is unclear whether equilibrium
with the water potential of the air was achieved. ABA has similar effects on the
tolerance of some liverworts to desiccation (Hellewege et al. 1994) and its precursor, lunularic acid, controls the switch from a sensitive to a tolerant stage of
Lunularia cruciata (Schwabe & Nachmony-Bascomb 1963). These reports are of
interest here because they indicate the possibility that in some bryophytes,
those that normally do not face extreme dehydrating conditions for any length
of time, vegetative desiccation tolerance can be induced via a mechanism that
involves ABA and is, at least on the surface, similar to that seen in the vegetative
desiccation-tolerant angiosperms. It is clear that bryophytes have the ability and
the molecular machinery to respond to ABA, a point that was elegantly demonstrated by Knight et al. (1995) who introduced a b-glucuronidase reporter gene
driven by the Em ABA-responsive promoter from wheat into Physcomitrella
patens, a desiccation-sensitive moss. Not only was the reporter gene responsive
to ABA, but the researchers were also able to demonstrate the presence of DNA
binding proteins that were specific to the ABA Responsive Elements (ABREs)
present in the Em promoter. The reporter gene was also able to respond to
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osmotic stress caused by exposing the transgenic moss to mannitol solutions,
albeit to a lesser degree than when exposed to exogenous ABA.
Parenthetically, ABA was undetectable in Tortula ruralis gametophytes in
either the hydrated or the drying stages of the wet–dry–wet cycle and was not
detected in dried tissues (Bewley et al. 1993). Furthermore, ABA does not induce
dehydrin accumulation in hydrated gametophytes (Bewley et al. 1993,
M. J. Oliver, unpublished observations). However, in contrast, treatment of
Tortula ruralis gametophytes with ABA does result in the induction of two early
light-inducible protein (ELIP) genes such that the transcripts for these proteins
accumulate (Zeng et al. 2002). This clearly indicates that Tortula ruralis can also
respond to exogenous ABA. Oliver et al. (2005) interpret these observations as
illustrating the complexity of desiccation tolerance and posed two interesting
evolutionary questions: (1) Did mesic bryophytes forego the constitutive cellular
protection aspect of desiccation tolerance in favor of an inducible system that
allows them to better compete in a mesic habitat? Or (2) did the constitutive
cellular protection system evolve from a primitive developmental system in
spores that allowed some mosses to move into progressively more extreme xeric
habitats? Only a phylogenetic approach to desiccation tolerance can address the
hypotheses these questions generate.
7.6
Cellular recovery
An equally important aspect to desiccation tolerance in bryophytes, in
conjunction with constitutive cellular protection, is the ability to quickly
recover cellular and metabolic activity when rehydration occurs. It would be
easy to assume that the cellular protection capabilities of bryophytes are sufficiently effective that cells could simply pick up where they left off when water
returns. Indeed, some aspects of cellular activity appear to do just that, in
particular the Photosystem II activity of photosynthesis (an important site to
protect, as discussed above), which recovers normal function within minutes
following rehydration, as measured by chlorophyll fluorescence measurement
(Fv/Fm) (Proctor & Smirnoff 2000; see Chapter 6, this volume). Nevertheless,
considerable evidence indicates that desiccation-tolerant bryophytes do suffer
cellular damage that becomes evident when they are rehydrated. Whether the
damage occurs directly as a result of the process of desiccation or is caused by
the rapid influx of water into bryophyte cells when free water becomes available
is still a question for debate.
We do know that changes in desiccated cells occur. We have already discussed physical and structural changes in membranes associated with the generation of ROS production associated with desiccation. We also know that the
7 Desiccation tolerance mechanisms in bryophytes
composition of membranes is altered in desiccation-tolerant tissues during
desiccation; for example, Buitink et al. (2000) demonstrated that tolerant tissues
differ from sensitive tissues in the partitioning of amphiphilic substances into
membranes. As cells dry, amphiphilic substances partition from the soluble
cytoplasmic compartment in to the membranes, resulting in a deleterious
change in the integrity of the membrane. Buitink et al. (2000) found that transfer
of amphiphilic molecules occurred at higher water contents in desiccationsensitive tissues than in those that are desiccation-tolerant. They suggest that
the amphiphilic molecules that enter membranes at the higher water content
lead to a disruption of membrane integrity, whereas those compounds that enter
at low water content increase membrane stability, perhaps acting as antioxidants. Regardless, at least for Tortula ruralis, visible and extensive membrane
damage is not evident (Platt et al. 1994).
The rehydration of dried cells is also known to result in significant injury;
all desiccation tolerance mechanisms have to include a process that attempts
to prevent or limit such damage (Osborne et al. 2002). Orthodox seeds manage to
lessen the effect of rehydration by slowing it down and allowing water to
re-enter cells in a controlled and somewhat ordered fashion. The structure of
bryophytes precludes this possibility and they rehydrate almost instantaneously
when water is added. In light of this one would hypothesize that bryophytes, in
order to combat rehydration (or desiccation) induced damage, would have to
rely on a process that was induced as water enters the cells to protect them from
damage or rapidly repair any damage that was inflicted by the inrush of water.
The phenological evidence would suggest that this hypothesis is a valid one. The
first sign that damage has occurred is the leakage of solutes from the protoplasm, possibly as a result of an alteration in membrane structure even though
it is not visible. In desiccation-tolerant tissues this leakage is transient, however,
indicating that damage has been limited to a level at which mechanisms activated by rehydration can effectively repair it. The extent of leakage is dependent
upon the rate at which the prior desiccation event occurred. The faster the
drying rate, the more solutes are leaked during rehydration (Bewley &
Krochko 1982, Oliver & Bewley 1984, Oliver et al. 1993). The cessation of solute
leakage occurs relatively quickly, within minutes, suggesting that the repair
components are present at all times and are activated by rehydration. It is
generally accepted that membrane phase transitions are the cause of rehydration leakage in vegetative tolerant tissues (for review see Crowe et al. 1992).
When water enters the dried cells of Tortula ruralis the condensed cytoplasm
rapidly expands to fill the cavity that formed as a result of plasmolysis (Tucker
et al. 1975). Over the next five minutes, as seen by using Nomarsky optics (without fixation), the chloroplasts swell and take on a globular appearance and
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thylakoids appear disrupted, as confirmed by electron microscopy after fixation
of cells five minutes after rehydration (Tucker et al. 1975). The extent of thylakoid disruption is directly related to the speed at which desiccation occurred
prior to the rehydration event: the faster the desiccation, the greater the disruption (Oliver & Bewley 1984). Mitochondria also swell and exhibit disruption
of their inner membranes but the level of damage to these organelles appears
to be unrelated to the rate of prior drying. Such events seem common for
desiccation-tolerant mosses in the few minutes following rehydration (Oliver &
Bewley 1984) and in all cases normal cellular structure is achieved within 24 h. It
has been suggested that such cellular observations are artefacts caused by the
fixation process in preparation for microscopy (Wesley-Smith 2001). Such explanation seems, however, in this case very unlikely as fixation occurred five minutes
after rehydration when cells were fully hydrated and hydrated controls show no
such abnormalities. In addition, chloroplast swelling was clearly evident by
Nomarsky optics and dried cells of desiccation-sensitive species exhibit structural
abnormalities upon rehydration identical to those seen in desiccation-tolerant
mosses, but in the sensitive species the cells do not recover, but die (Bewley &
Pacey 1978, Krochko et al. 1978).
Recently, Proctor et al. (2007) elegantly demonstrated the effectiveness of the
constitutive protection mechanism for desiccation tolerance in the moss
Polytrichum formosum. Using moss that had been slowly dried to equilibrium
with ambient air at 40%–50% RH, they were able to demonstrate that the fine
structure of the moss was unaffected by the desiccation event and that physiologically both photosynthesis and respiration recover rapidly and reach predesiccation levels 24 h post-rehydration. Furthermore, this study provides
evidence that under these conditions the initial recovery is independent of
protein synthesis. Earlier work by Pressel et al. (2006) also indicated little or no
damage in the leptoids and specialized parenchymal cells, which are involved in
nutrient transport, of Polytrichum formosum under the same drying conditions.
These authors also demonstrate a recovery to the predesiccation state within
12–24 h following rehydration and, interestingly, provide strong evidence for a
key role of the microtubular cytsokeleton in the rapid cellular recovery process.
These studies confirm those of Platt et al. (1994) for Tortula ruralis and Selaginella
lepidophylla in that desiccation per se does not appear to result in cellular injury,
perhaps as a result of an ordered collapse of the cells during drying, for which
the activities of the cytoskeletal components are key as suggested by Pressel et al.
(2006) and supported by Proctor et al. (2007). It is clear from these studies that the
constitutive protection mechanism present in this species is sufficiently efficient to prevent any major or observable cellular damage under relatively mild
drying conditions.
7 Desiccation tolerance mechanisms in bryophytes
These studies taken in isolation tend to make it difficult to invoke the need
for a cellular repair aspect to the desiccation tolerance mechanism in bryophytes as proposed by Bewley (1979) and expanded upon by Bewley & Oliver
(1992), a point that is argued by Proctor et al. (2007). However, the conditions
under which these plants were dried are ideal and invoke a drying rate that has
proven to be the least stressful for bryophytes (Bewley 1979, Bewley & Oliver
1992, Oliver & Wood 1997) and does not reflect reliable conditions in the field,
especially with regards to the more tolerant desert species. As discussed previously, there is a great deal of evidence for cellular damage during desiccation,
and the level of that damage depends upon the rate of dehydration, the extent of
dehydration, and the length of time that the plant remains dry (as evidenced by
a loss of viability over time). Hence it is clear that cellular repair is a necessary
part of the mechanism of tolerance in these plants. The need to invoke this
particular aspect of the desiccation tolerance mechanism and the extent to
which it is operative may vary with the particular circumstance, however. As
we move forward to better understand the roles and activities of the gene
products that are induced during rehydration in bryophytes, as I discuss in the
following sections, the relative importance and depth of the repair process in
desiccation tolerance mechanisms in bryophytes will become evident.
7.7
Biochemical and molecular aspects of recovery
The complexity of the recovery of bryophytes from desiccation is only
just becoming clear and it is equally clear that understanding this complexity
will be a lengthy and intricate endeavor. Over the years, Tortula ruralis has been
the model for studies directed at understanding the recovery from desiccation
in bryophytes and much has been achieved.
All desiccation-tolerant bryophytes rapidly recover synthetic metabolism
following rehydration although, as was the case for structural components,
the speed of the recovery of synthetic metabolism is affected by the rate at
which desiccation occurred (Oliver & Bewley 1997). Protein synthesis, one of the
more sensitive processes to desiccation, recovers to normal levels within the
first two hours following the addition of water to dried gametophytes of Tortula
ruralis (Gwózdz et al. 1974), closer to three to four hours if the moss is rapidly
dried (M. J. Oliver, unpublished data). The recovery of protein synthesis is fast
because many of the components necessary for active protein synthesis are
conserved in the dried moss, the only exception being an unidentified translation initiation factor(s) (Gwózdz & Bewley 1975, Dhindsa & Bewley 1976) which
presumably has to be synthesized during the initial recovery phase (probably
from sequestered transcripts; see below).
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Although protein synthesis recovers relatively rapidly, the moss does not
simply start where it left off when desiccation occurred. Within the first two
hours following rehydration the pattern of protein synthesis is dramatically
altered from that seen in hydrated moss prior to drying (Oliver 1991). This marks
a major switch in the control of gene expression such that the synthesis of a
number of proteins is reduced or terminated (termed hydrins) and the synthesis
of other proteins is initiated or substantially increased (termed rehydrins).
Hydrin and rehydrin are functional terms and do not refer to any common
sequence motif or structural property nor imply a common enzymatic function,
and so a protein is designated as one or the other by virtue of its biosynthetic
response to desiccation and rehydration. Oliver (1991) was able to detect 25
hydrins and 74 rehydrins by using radioactive labeling of proteins and 2-D gel
analysis, and was also able to demonstrate that the controls of the changes in the
synthesis of the two groups of protein are not mechanistically linked. It takes a
certain amount of prior water loss to fully activate the synthesis of rehydrins
upon rehydration, whereas the synthesis of hydrins responds almost immediately upon the initiation of drying. The observation that there is a critical point
in the loss of water from the gametophytic cells that will trigger the synthesis of
rehydrins when water becomes available again suggests that the moss has
evolved a strategy that allows it to respond only when it is likely that the
plant will desiccate rather than simply experience a short period of dehydration.
This would make sense as a means of conserving energy in an uncertain
environment.
The change in gene expression, as observed by the change in the pattern of
protein synthesis upon rehydration in Tortula ruralis, occurs within a background of a qualitatively unaltered mRNA population (Oliver 1991), suggesting
that mosses respond to desiccation and rehydration primarily by an alteration
in the control of translation rather than transcription as is the case with the
stress and desiccation responses of angiosperms (Ingram & Bartels 1996, Phillips
et al. 2002). In other words, the genes that code for proteins involved in the
response to rehydration are already transcribed into mRNA. But what prevents
their immediate translation? The main role of translational controls in regulating the gene expression response to rehydration was confirmed when rehydrin
cDNAs were constructed and used to follow transcript accumulations by using
northern blot analysis (Scott & Oliver 1994) and has since been further validated
in genomic level studies (see below, Wood et al. 1999, Oliver et al. 2004, 2005)
including expression profile analysis (M. J. Oliver, unpublished data). The manner in which the translational response to dehydration is controlled, as with
most other processes, appears to be dependent upon the rate at which the
previous desiccation event was achieved. If desiccation is rapid, rehydrin
7 Desiccation tolerance mechanisms in bryophytes
transcripts accumulate during the first hour following rehydration, apparently
to replenish the pool of transcripts that has been reduced by rapid drying (Scott &
Oliver 1994, Oliver & Wood 1997, Velten & Oliver 2001). One could argue that for
rehydration following rapid desiccation the change in gene expression is transcription driven, however no novel transcripts are made, i.e. there appear to be
no genes whose transcription is initiated during rehydration as seen in the
angiosperm response, nor is transcription rapid enough to drive the change in
protein synthesis one observes in these samples. Clearly translational controls
still override the response. If desiccation occurs slowly, in contrast, rehydrin
transcripts have accumulated to peak levels in the dried moss prior to the
rehydration event such that they are readily available for translation as water
returns to the cells (Scott & Oliver 1994, Oliver & Wood 1997, Wood & Oliver
1999). The accumulation of transcripts occurs during the slow drying phase, not
by a process of increased transcription of selected genes, but by the sequestration of rehydrin mRNAs in a stable form, packaged with proteins that must be
pre-existent in the moss (Wood & Oliver 1999). The sequestered rehydrin
transcripts are maintained in an untranslatable form, presumably as a result
of protein–RNA interactions during packaging, as messenger ribonucleoprotein
particles (mRNPs) in the slow-dried gametophytic cells. Upon rehydration, it is
postulated that the inrush of water results in the rapid release of the rehydrin
transcripts from their associated proteins and their rapid recruitment into the
protein synthetic complex for the biosynthesis of the various rehydrins. This is
supported by their rapid inclusion in the polysomal fraction of rehydrated
gametophytes (Scott & Oliver 1994, Wood & Oliver 1999). The sequestration of
rehydrin transcripts during drying in preparation for the rigors of rehydration
support the notion that the repair mechanism in rehydrated slow-dried Tortula
ruralis, perhaps reflecting the natural response, is activated rather than induced
(which implies a de novo assembly of components). The prevention of the storage
of rehydrin transcripts by rapid desiccation may, at least in part, explain the
slower recovery rate of rapid dried moss, as these gametophytes will have to rely
upon what little was stored prior to dehydration until new components can be
synthesized and assembled.
Some physiological studies into the recovery of photosynthesis following
rehydration of desiccation-tolerant mosses have questioned the need for protein
synthesis and repair with respect to the recovery of chloroplasts and chloroplast
functions (reviewed by Proctor & Pence 2002, Proctor & Tuba 2002). Essentially,
recovery of chloroplastic function, specifically Photosystem II, is extremely
rapid (10–20 min) and is unaffected by protein synthesis inhibitors in the dark
for rehydrated dried gametophytes (dried to 70 MPa) of several desiccationtolerant mosses (Proctor & Smirnoff 2000, Proctor 2001). Protein synthesis is,
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however, required if rehydration takes place in the light, presumably to repair
photo-oxidative damage. CO2 uptake and assimilation do not recover instantaneously and require protein synthesis. Measurements of the rapid recovery of
photosynthesis upon rehydration for dried T. ruralis also suggest that protein
synthesis may not be required for the recovery of chloroplast structure and
function (Tuba et al. 1996, Csintalan et al. 1999). These studies suffer, however,
from some caveats. The effectiveness of protein synthesis inhibitors is difficult
to assess as they can also affect the rate of uptake of the radiolabeled amino
acids used to assess protein synthetic rates (Jacobyj & Sutcliffe 1962, Parthier
et al. 1964). Protein synthesis inhibitors also rarely prevent protein synthesis
completely, even when used in combination. Proctor & Smirnoff (2000)
report an effective inhibition of 90% after 20 min in the presence of two inhibitors (to inhibit both cytoplasmic and organellar synthesis); however, no
uptake measurements or amino acid pool size measurements were reported.
The level of desiccation obtained in the mosses used in these investigations is
relatively moderate, approximately 70 MPa, and as discussed above the
rate and depth of desiccation has a major effect on the amount of cellular
damage seen in bryophytes. If damage is limited, 10% of normal protein synthetic rates may be sufficient to effect repair of the chloroplasts in these studies.
This remains to be tested, however. Even with these considerations it does
appear that parts of the photosynthetic machinery are well protected and may
require little repair. It is interesting to speculate that, because of the need to
rapidly utilize the time that water is available and the need for energy to repair
other cellular damage, part of the bryophyte mechanism of tolerance lies in a
focused and effective protection of the chloroplast, especially those processes
involved in the generation of ATP. This may explain why transcripts for ELIPs,
proteins that are involved in photo-protection of the chloroplast (Lindahl
et al. 1997, Montane & Kloppstech 2000), are stable to rapid desiccation (Zeng
et al. 2002).
7.8
Genomic approach to desiccation tolerance
In more recent times a genomic approach has been taken in order to
fully understand the complexity of the desiccation-rehydration response of
desiccation-tolerant mosses, again using Tortula ruralis as the bryophyte model
(Wood & Oliver 2004). The genomic level approach best suited to this endeavor,
at least at this stage, is to build an expressed sequence tag (EST) collection and
use this as a resource for an expression profiling strategy using cDNA-based
microarrays. Scott and Oliver (1994) isolated the first 18 rehydrin cDNAs; Wood
et al. (1999) subsequently recovered 152 ESTs from a cDNA expression library
7 Desiccation tolerance mechanisms in bryophytes
constructed from mRNAs extracted from the mRNP fraction of slow-dried gametophytes. Of these cDNAs only 29% exhibited any sequence similarity to previously identified nucleotide and/or peptide sequences deposited in public
databases. Of those ESTs that could be annotated with a putative identity or
function, several were identified as encoding ribosomal proteins, indicating the
importance of protein synthesis in the response, and others encoded protective
proteins such as ELIPs and LEA proteins. The inability to annotate a significant
portion of the isolated ESTs may be due perhaps to the dearth of bryophyte
sequences in the public databases (a situation that is rapidly improving with the
sequencing of the Physcomitrella patens genome: www.jgi.doe.gov/sequencing/
why/CSP2005/physcomitrella.html), but may also indicate, as is seen with
many of the desiccation-tolerant tracheophyte genomic resources (Illing et al.
2005, Iturriaga et al. 2006), that some genes associated with desiccation tolerance are truly novel and represent processes for which little is known. The large
percentage of unknowns in the small Tortula ruralis EST collection was underscored by the more recent addition of 10 368 ESTs from a non-normalized
rehydration specific library to the collection (Oliver et al. 2004). The 10 368
ESTs represent 5563 clusters (contig groups representing individual genes),
40.3% of which could not be assigned an identity by comparison to annotated
sequences in the public databases (Oliver et al. 2004). The larger EST collection
was derived from a non-normalized rehydration-specific library to allow for a
qualitative look at transcript abundance during the recovery phase. Genome
ontology (GO) mapping of the Tortula clusters gave a broad look at what cellular
activities appear to be emphasized in the rehydrated gametophytes and confirmed that the protein synthetic machinery, membrane structure and metabolism, and plastid integrity are central to the response. The GO analysis also
revealed previously unresearched areas of cellular recovery such as membrane
transport processes, phosphorylation, and signal transduction. Signal transduction is especially intriguing given that translational controls appear more
important in the alteration of gene expression than are transcriptional activities
that respond at the culmination of a signal transduction. However, the rehydration cDNA library was derived from rehydrated rapid-dried gametophytes and
these rely, at least in part, on the replenishment of rehydrin transcripts via
transcription.
The qualitative aspects of the large Tortula ruralis EST collection allowed for a
general look at the most abundant transcripts present in the early phases of
recovery following rehydration. Surprisingly, seven of the 30 most abundant
transcripts present in the rehydrated moss encode LEA or LEA-like proteins
(Oliver et al. 2004, 2005), including one that we consider to be a ‘‘primitive’’
dehydrin like LEA, Tr288 (Velten & Oliver 2001). This observation led to the
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suggestion that in desiccation-tolerant mosses some LEA proteins may play a
dual role by protecting cells during both dehydration and rehydration.
Alternatively, a more provocative hypothesis would be that LEA proteins in
desiccation-tolerant plants and seeds are not sequestered during dehydration
to protect cells from the effects of water loss but are accumulated to deal with
the rigors of rehydration/imbibition. The significance of the relatively crude
bioinformatics measure of transcript abundance was given a strong boost by an
expression profile study using a cDNA microarray constructed from the 5563
individual clusters derived from the large EST collection (Oliver et al. 2005).
Twenty-four of the clusters (representing individual genetic elements) that
exhibited at least a two-fold increase in transcripts accumulation levels within
gametophytes that had been rehydrated for between 1 and 2 h have sequence
similarity to known LEA protein sequences. These transcripts are also elevated
greater than two-fold in the polysomal RNA fraction indicating their recruitment into the translational mRNA pool. One of these transcripts represents
Tr288, a previously identified rehydrin that has been extensively characterized
as belonging to the LEA protein group (Velten & Oliver 2001). Since each cluster
represents a unique nucleotide sequence it would suggest that following rehydration Tortula ruralis has a wide range of LEA-like proteins available for use in
the recovery process, again suggesting that these proteins play an important
role in cellular protection from rehydration-induced damage or directly in its
repair. Koag et al. (2003) demonstrated that a maize dehydrin (DHN1) was capable of binding to lipid vesicles with some degree of specificity, preferring lipid
bilayers that contained a significant proportion of acidic phospholipids. Oliver
et al. (2005) report some preliminary work with the protein encoded by Tr288
that suggests that it too is capable of selective binding to lipid vesicles, also
preferring acidic phospholipid mixtures. This leads us to the hypothesis that in
rehydrating Tortula ruralis gametophytes LEA proteins may serve to stabilize
membranes, or perhaps serve a role in lipid transport for reconstitution of
damaged membranes, during the cellular upheaval that results from the inrush
of water to dried tissues.
7.9
Final comments
The genomic approach to understanding the very complex trait of vegetative desiccation tolerance offers much in the way of cataloging those genes
whose products play some role in the response of bryophytes to desiccation and
rehydration. Coupled with bioinformatics and expression profiling, the genomic
approach can also, by inference, provide clues as to which cellular processes and
activities should be targeted for further studies. It may even point towards
7 Desiccation tolerance mechanisms in bryophytes
important regulatory proteins or processes that offer the promise of controlling
the response and ultimately, perhaps, by a biotechnological approach, be useful
in establishing or improving dehydration tolerance (not desiccation tolerance) in
an important agronomic species. However, there is reason for caution when
considering these hopes and assertions. The genomic approach is only going to
bear fruit if the hard cellular, metabolic, and biochemical studies accompany the
identification of possible key targets. We must also understand which genes and
processes are truly adaptive and are central to the phenomenon of cellular
desiccation tolerance. Bray (1997) suggests that the change in expression of
specific genes resulting from a dehydration stress can be misleading. It is possible
that changes in gene expression result from cellular injury, a scenario not unlikely during desiccation and rehydration. Injury may trigger the upregulation of
specific genes or gene products that are not directly involved in promoting
adaptation to dehydration but rather simply responding to the injury and therefore of secondary importance. One way to approach this problem is to look at
desiccation tolerance in a phylogenetic context as discussed by Oliver et al. (2000,
2005). Ongoing studies using a comparative genomic approach to alterations in
gene expression as a result of desiccation and rehydration may form the foundation for such studies. Using a combination of bioinformatics and expression
profiling to compare the response to desiccation and rehydration in a number
of species that occupy significant and key positions in the phylogeny of land
plants, we can start to sort out the details of the evolution of desiccation tolerance
and gain an insight into what genes are truly adaptive and central to this phenotype. A recent report by Illing et al. 2005 is a small but important first step in this
endeavor, revealing the evolutionary link between vegetative desiccation tolerances in angiosperms with the mechanism of desiccation tolerance exhibited in
orthodox seeds. Comparisons using bryophyte models will be invaluable in this
process and will underpin the evolutionary conclusions that can be drawn from
such studies, which are now underway.
The overall picture of desiccation tolerance in bryophytes is rapidly growing
and details are being flushed out in all areas of plant biology, from ecology to
physiology, from physiology to cellular biology, from cellular biology to biochemistry, and from biochemistry to genetics (in all its forms). At the moment
it is still in its infancy, as can be seen in Fig. 7.1. What we know is not overwhelming but we have many hypotheses to test and we have established a solid
structure on which to build: exciting times lie ahead. The most exciting bryological breakthrough that offers much in these efforts is the sequencing of the full
genome of the moss Physcomitrella patens (see above). Although this is not a
desiccation-tolerant bryophyte the full genomic sequence of a moss, and the
expanding genomic and genetic tools that accompany it, will revolutionize how
289
290
M. J. Oliver
Fig. 7.1. Summary depiction of the current view of desiccation tolerance in bryophytes from
a biochemical and molecular perspective.
we study important traits, not only in bryophytes but also in all plants. The
ability to introduce, knock out, and replace genes via homologous recombination truly make this bryophyte model not only unique in plant biology at
present but also very powerful for the analysis of gene function and importance
in many plant specific processes (Frank et al. 2005). The full genome sequence
increases the power of this plant model exponentially.
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8
Mineral nutrition and substratum
ecology
jeff w. bates
8.1
Introduction
Bryophytes do not appear to differ fundamentally from higher plants
and green algae in their basic requirements for mineral macronutrients and
trace elements. However, bryophytes differ significantly from vascular plants in
pathways for nutrient acquisition and these may sometimes have far-reaching
consequences for the ecosystems in which they grow. Owing to their specific
modes of nutrient capture, bryophytes frequently accumulate chemicals to
concentrations far exceeding those in the ambient environment. This property
has led to the development of moss biomonitoring methods, which have taken
hold firmly in the wider scientific community since the first edition of this book
appeared.
As in the earlier edition, this chapter describes the special problems that
bryophytes encounter in obtaining essential mineral nutrients, and in dealing
with non-essential elements and compounds. Far more is known now than in
the earlier edition about nitrogen deposition and utilization by bryophytes, and
hence the chapter will focus on these aspects of mineral nutrition and substrate
ecology.
The substratum on which a bryophyte grows can be a source of nutrients and
other chemicals that may cause stresses. I have retained the useful distinction
between ‘‘substrate’’, used for the substance on which an enzyme or biochemical process works (as in Section 8.3.1), and ‘‘substratum’’, used for the surface
supporting a plant or lichen, although the etymological grounds for this are
slight. Substratum specificity and chemical specialisms are considered in some
detail but aspects involving competition and population dynamics are now
largely covered in Chapter 10 by Rydin.
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
300
J. W. Bates
8.2
Mineral nutrition
Knowledge about the elemental requirements of bryophytes has
accrued slowly from cultivation experiments employing defined nutrient solutions, from chemical analyses of tissues and by studies of ion uptake and cell
electrophysiology. Over the past ten years or so, modern developments for
manipulating genes and identifying and visualizing their protein products
have further revolutionized our understanding of the apparatus by which ions
and molecules pass through plant cell membranes (e.g. Roberts 2006). Much of
this work has involved Arabidopsis thaliana, now routinely employed as the
‘‘model’’ vascular plant. Fortunately, some comparable work has been undertaken in cultures (usually protonematal) of the ‘‘model’’ bryophyte Physcomitrella
(Aphanorrhegma) patens; however, we are still largely ignorant about the diversity
of molecular transport mechanisms present among bryophytes.
8.2.1
Cell transport processes
Transporter proteins
The thoughtful reviews of J. A. Raven (e.g. Raven 1977, 2003, Raven et al.
1998) about solute transport and molecular transport systems in bryophytes in
comparison with other plant groups form useful starting points for anyone
interested in this topic. In all living cells the lipid bilayer comprising the
plasmalemma, the tonoplast, and other membranous organelles is penetrated
by an array of proteins with specific functions. Among those with a solute
transporter function are ion channels, envisaged as charge-lined tubes admitting hydrated ions or solutes of a specific size and charge, and carrier proteins
that may change shape to pass the substrate ion or molecule through the
membrane providing that it correctly fits the active site(s). In either case the
direction of this ‘‘facilitated diffusion’’ depends on the existing gradients of
concentration and electrical charge across the membrane. Control is provided
by ‘‘gating’’ and ‘‘ungating’’ of channels in response to signals provided by
chemical messengers, light, charge, etc. Passage of the substrate is only possible
when the channels are ungated. Only a few simple molecules, including ammonia, carbon dioxide, and oxygen, are believed to be capable of diffusing through
lipid membranes without such aids.
Aquaporins
Water is now known to diffuse through cell membranes predominantly
via special channel proteins termed aquaporins (Chaumont et al. 2005). At least
12 different aquaporin proteins are believed to occur in Physcomitrella patens
(Borstlap 2002). These include representatives of all four main subfamilies of
8 Mineral nutrition and substratum ecology
aquaporins found in vascular plants, indicating that they had evolved prior to
the diversification of tracheophytes and bryophytes. As Borstlap (2002) notes,
the surprising diversity of aquaporin proteins in land plants is probably related
to the central importance of hydraulics in their everyday functioning.
Active transport of ions and solutes
Active transport is required when the direction of movement is against
a transmembrane gradient in concentration and/or electrical charge. Bryophyte
cells closely resemble vascular plant and green algal cells of Characeae in
maintaining an electronegative cell interior, in part due to active efflux of Hþ,
probably catalyzed by a ‘‘P’’ type ATPase, which expends one mole of ATP per
mole of Hþ pumped out. This proton pump also regulates cytoplasmic pH in
bryophytes at around 7.3–7.6 and provides the driving force for a number of
specific symporter proteins, allowing passage through the plasmalemma and
against a concentration/charge gradient for NHþ
4 , sugars and amino acids.
Related mechanisms probably operate for active entry of Kþ, NO3 , SO24 and
H2PO4 and for efflux of Ca2þ and Naþ (via antiporter proteins) but not all have
yet been unequivocally demonstrated in bryophytes. Much less is known about
the specific details of tonoplast transport in bryophytes.
Transfer cells
Of relevance to the uptake and cell to cell fluxes of nutrients is the
occurrence in bryophytes of specialized cells known as transfer cells. These are
characterized by extensive and often complex ingrowths of the secondary cell
wall into the cell lumen. This is necessarily accompanied by an increased area of
the lining plasma membrane, which also becomes richly furnished with transporter proteins, and thus enhances rates of nutrient transfer with neighboring
cells. Offler et al. (2003) note that these cells are known in all major plant
taxonomic groups including bryophytes, algae, and fungi, and occur at sites
where there are uptake bottlenecks, often involving apoplastic–symplastic
transfers. In bryophytes, transfer cells have so far been detected only at the
relatively protected gametophyte–sporophyte junction (Ligrone & Gambardella
1988). In vascular plant roots they also occur under certain types of nutrient
deficiency and might be expected to occur in bryophytes under similar conditions. However, it can be imagined that cell plasmolysis during desiccation of
poikilohydric plants would damage the convoluted membrane, which may
explain their scarcity in bryophytes.
Significant intracellular (symplastic) conduction of photosynthate and other
nutrients has only recently been claimed to be widespread in bryophytes
(Ligrone & Duckett 1994, 1996, Ligrone et al. 2000), although largely on the basis
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of ultrastructural evidence (Raven 2003). Apart from the long-known and relatively
well differentiated leptoids of some ectohydric mosses implicated in transport of
photosynthate, many less obviously differentiated conducting parenchyma cells
are believed to fulfil a similar function in bryophytes (Ligrone et al. 2000).
Action potentials
Action potentials are losses (depolarization) of the normal transmembrane potential difference that last in plant cells typically for a few seconds. They
have been observed in the liverwort Conocephalum conicum and the hornwort
Anthoceros. The depolarization in C. conicum is caused by Ca2þ influx and Cl efflux.
The following repolarization is connected with entry of Kþ and efflux of Hþ
(Trebacz et al. 1994). In aquatic green algae of the Characeae the ion fluxes
(measured in large nodal cells) are believed to permit osmotic regulation of cell
turgor (e.g. Shepherd et al. 2002). Virtually nothing is known about the occurrence
of action potentials in the major groups of bryophytes or whether they have any
involvement in membrane repair as implicated in higher plants. Action potentials could conceivably have an important role in osmotic adjustment as poikilohydric bryophyte cells undergo cycles of dehydration and rehydration.
8.2.2
Mineral nutrient requirements
Growth on defined media
An example is provided by Hoffman’s (1966) study of the nutrient relations of the cosmopolitan moss Funaria hygrometrica. The effects of nutrient
deficiencies were investigated in protonemata grown on agar containing
Hoagland’s solution with individual elements lacking. The results showed that
F. hygrometrica has macronutrient and micronutrient requirements closely similar
to those of vascular plants. Hoffman also performed ‘‘nutrient triangle’’ experiments to define the optimal ratios of the major anions (N:P:S) and cations (K:Ca:
Mg) for growth. These overly complex factorial experiments are difficult to
analyze effectively. Nevertheless, an important conclusion was that the growth
of protonemata and the development of numerous gametophores were favored
by quite different cation combinations. By contrast, in the anion experiments, the
absence of any one of the elements resulted in poor protonemal growth and no
gametophores. Hoffman and many subsequent investigators have used mature
shoots (and protonemata) or thalli as the experimental material. Compared with
experiments starting with spores, these have the potential problem that elements
initially present in the plants may be in sufficient quantity to mask or confound
the effects of the applied nutrient treatments.
Bryophytes need relatively dilute nutrient media, in contrast to those
required for optimal growth of crop plants. Working with the thalloid liverwort
8 Mineral nutrition and substratum ecology
Marchantia polymorpha, Voth (1943) varied the dilution of a basic nutrient solution to alter osmotic pressure but not the ratios of the elements. When a
concentrated solution was used (solution 1), many of the thallus tips and
wings were killed, the thallus dry mass and area were small, and production
of gemmae cups was low. Over the intermediate concentration range (solutions
3–5), the plants increased in size, were darker, had more ascending tips, and
developed more rhizoids in response to greater dilution of the nutrients. At the
lowest concentrations (solutions 6–10) a greater intensity of red–purple coloration developed in the rhizoids, scales, and lower epidermis, and rhizoids were
especially numerous whereas gemmae cups became fewer. Cell walls were
extremely thin in the strongest solutions, with many collapsed cells seen, but
a maximum thickness of cell walls was seen in the most dilute solutions, with
most cells appearing healthy. Although survival of M. polymorpha is possible over
a wide range of extreme concentrations, the species clearly grows best in dilute
media. Only a handful of bryophytes has been subjected to scrutiny in solution
culture experiments (Brown 1982) and further careful work is desirable.
Chemical analysis of tissues
Chemical analyses of bryophytes can provide useful clues about
mineral requirements and about tolerance of non-essential elements, and
offer a means of biomonitoring the deposition of elements such as heavy metals.
Numerous studies have investigated total element concentrations of bryophyte
tissues, usually employing dry-ashing or wet-ashing techniques to solubilize the
minerals for analysis by spectrophotometric methods. Many authors have discussed the protocols for preparing materials for analysis and particularly the
need to remove surface contamination by soil particles and rock fragments (e.g.
Shacklette 1965, Woollon 1975, Brown 1982). However, washing of previously
dried material is not recommended because of the risk of leakage of cell solutes
during rehydration (Brown & Buck 1979). Washing with tapwater, a potentially
mineral rich solution, is also likely to alter element levels through cation
exchange (below). Therefore, before embarking upon a program of chemical
analyses, it is important to consider the possible cellular locations of the elements in question and to design the sampling and extraction method to provide
the maximum information for the effort involved.
8.2.3
Mineral uptake by whole bryophytes
Kinetics of ion uptake
The few studies of the kinetics of absorption of ions by bryophytes have
concentrated upon heavy metal pollutants and radionuclides (Brown 1984).
For metals, zinc absorption by the aquatic moss Fontinalis antipyretica
303
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J. W. Bates
(Pickering & Puia 1969) is typical in showing a phase of rapid (30 minutes)
uptake of 50% of the absorbed Zn. The remainder is absorbed slowly over several
days; the absorption is sensitive to light, temperature and metabolic inhibitors.
The rapid uptake represents passive sorption of zinc ions onto the extracellular
cation exchange sites of the moss tissue (see below), whereas the slower phase is
believed to represent true uptake into the cells. Wells & Richardson (1985)
reported that a range of physiological anions and non-essential analogs displayed similar saturation kinetics in Hylocomium splendens. Cadmium uptake by
Rhytidiadelphus squarrosus exhibited Michaelis–Menten kinetic constants (Km,
Vmax) that differed quite markedly between field populations exhibiting slightly
different morphologies (Brown & Beckett 1985). This is particularly relevant to
the use of bryophytes in monitoring heavy metal deposition.
Cation exchange
Clymo (1963) emphasized the importance of cation exchange in accumulation of cations by Sphagnum in mires. In fact, the cell walls of most plants
possess a net negative charge owing to the ionization of weak acid moieties built
into their fibrillar structure. The cation exchange capacity (CEC) can be determined
by saturating these sites with a suitable cation (Anþ) and then displacing this
with another cation (Bnþ) and measuring the quantity of Anþ released into
solution. The plasmalemma is probably not exposed directly to the ionic composition of the exterior solution as the negative charges tend to repel anions and
alter the ratio of cations entering the wall environment. Detailed study (Richter
& Dainty 1989a) of the cation-exchanger in Sphagnum russowii suggests that
polymeric uronic acids account for over half the CEC, phenolic compounds
are responsible for about 25%, and amino acids, silicates, and sulfate esters
deposited in the wall all make lesser contributions. Dependent on the pH of the
external solution, all or a fraction of the acid moieties may ionize, and thereby
release a proton; e.g., for carboxyls in uronic acids and amino acids,
R.COOH ¼ R.COO þ Hþ.
Under strongly acid conditions the reaction is driven to the left and CEC falls as
ionization is suppressed, but progressively through less acidic, neutral, and alkaline conditions the net negative charge increases. The extent of ionization of a
given weak acid group is indicated by its pK, i.e. the pH at which 50% has ionized
and 50% remains un-ionized. By varying pH stepwise in the presence of metals
with contrasted valencies (Naþ, Ca2þ, La3þ), Richter & Dainty (1989a) showed that
S. russowii possesses two classes of cation binding site. One, with a low pK (2–4),
appears to be principally due to uronic acids and amino acids; the other, with a
high pK (>5), is almost certainly due mainly to weak phenolic acids.
8 Mineral nutrition and substratum ecology
% adsorption
100
b
P
50
Cu
Mn
Ni
Co
Cd
n
Z
0
0
500
1000
Initial concentration (µmol)
1500
Fig. 8.1. Percentage absorption of metal ions onto the cation-exchanger of Hylocomium
splendens from solutions containing equimolar concentrations of seven metal ions. The
solutions were supplied (5 g of air-dried moss to 500 ml) at a range of initial concentrations
and their final metal contents were determined after incubation for 2 h. Redrawn from
Rühling & Tyler (1970).
Metals and other cations permeating the cell wall easily displace the protons
from the ionized weak acids and may become relatively firmly held by the
negative charges. At the same time the external medium receives the displaced
protons and, in some circumstances, this may lead to its acidification.
Exchangeably bound cations are readily displaced by other cations in the external medium, particularly if the latter: (a) are present at higher concentration, (b)
have larger hydrated atomic radii, or (c) possess a higher valency. The data
presented in Fig. 8.1 were obtained by incubating the moss Hylocomium splendens
in a mixture of cations (Rühling & Tyler 1970). They reveal an order of binding
affinity for several heavy metal cations (Cu, Pb > Ni > Co > Zn, Mn) that appears
to be widespread. The heavy ions Cu and Pb were adsorbed preferentially onto
the exchange sites even when supplied in the presence of much higher concentrations of the lighter cations Ca, K, Mg and Na. The behavior of the exchange
sites varies with the species of cation employed to determine CEC. This is
305
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J. W. Bates
probably because the larger polyvalent cations combine strongly with and
‘‘condense’’ the fixed anions to varying extents (Sentenac & Grignon 1981,
Richter & Dainty 1989b). Wide variations occur in CEC between bryophyte
taxa and some of this variation appears to have ecological significance.
In Sphagnum-dominated mires the cation-exchanger of the Sphagnum plants is
believed to be a mechanism, albeit probably not the only one, by which acidic
conditions are attained (Clymo 1963, 1967, Brehm 1971, Clymo & Hayward
1982). According to this hypothesis, incoming cations are adsorbed and the
released protons are added to those already present in the mire water, the
production of fresh exchange sites by new growth keeping pace with cation
inputs. More recent studies, summarized in Chapter 9 of this volume by Vitt &
Wieder, strongly suggest that the availability of cations in mire waters is insufficient to drive this process and that the major cause of acidity is decomposition of
humic compounds dissolved in the interstitial water.
Clymo (1963) also observed strong correlations between the CEC of Sphagnum
spp., their optimal heights above the water table, and the hydrogen ion concentration of the interstitial water. Thus hummock species had the highest CEC
and hummock water had the lowest pH. It is quite probable that the cationexchanger has a role in nutrient absorption, the higher values of hummock
species perhaps compensating for shorter periods of hydration in this position.
Among plants Sphagnum has unusually high CEC under acid conditions, a factor
that coincidentally favors heavy metal accumulation; however, an elevated CEC
is also a characteristic of calcicole bryophytes (see Section 8.3.3).
Element location within the tissues
Much of the natural variability in total cation contents of bryophytes
appears to reflect extracellular accumulations by the cation-exchanger rather
than wide variations in the living cells. In many situations a clearer picture can
be obtained if the intracellular and cation-exchanger compartments are analyzed separately. This can be achieved by employing a sequential elution technique as described by Brown & Wells (1988) and Bates (1992a).
Clear patterns emerge for the major cations when bryophyte taxa from
different habitats are compared. Those with a clear metabolic function are
accumulated within the cells at consistently high concentrations: a relatively
high K concentration is believed to be essential for the normal folding of
cytoplasmic enzymes; Mg is present in chlorophyll and is an activator of several
enzymes; Ca is believed to act primarily as a ‘‘messenger’’ in plant cells and is
largely absent from the cytoplasm but it is often the predominant cation
externally on the cation-exchanger, reflecting its abundance in many natural
situations as well as its importance as a stabilizer of cell membranes and cell
Concentration (% dry mass)
8 Mineral nutrition and substratum ecology
1.5
1.0
N
K
Ca
0.5
P
0.0
1
2
3
Seg ment
4
5
Fig. 8.2. Concentrations of some major nutrient elements in the annual stem segments of
Hylocomium splendens on 7 August 1948 in boreal forest at Grenholmen, Uppland, Sweden.
Segment 1 was initiated in 1948, segment 2 in 1947, and so on. After Tamm (1953).
walls (e.g. Hirschi 2004). In response to environmental stresses (low temperature, osmotic stress, abscisic acid), a signal is issued in the form of a transient
release of Ca2þ that binds to the protein calmodulin. In Physcomitrella patens the
calmodulin then binds to transporter-like proteins that catalyze ion fluxes that
in turn may help alleviate the imposed stresses (Takezawa & Minami 2004).
Roughly half of the total Mg in bryophyte tissues may also be exchangeable.
Many other metals and some other cations, including the ammonium ion and
cationic pesticides may also enter the cation-exchanger.
Element concentrations alter as tissues age. Tamm (1953) neatly demonstrated this in Hylocomium splendens. The shoots or ‘‘fronds’’ of H. splendens consist
of chains of annual ‘‘segments’’. Each segment is normally clearly demarcated
from its forbears and offspring owing to a predominantly sympodial pattern of
growth that makes dating of the tissues comparatively simple. N, P, and K
reached their highest concentrations in the young shoot apices and declined
in older segments (Fig. 8.2). Ca, however, increased in the older segments on a
dry mass basis. According to Bates (1979) this is partly an artefact arising
through an increase in the cell wall : protoplasm ratio owing to slow degradation of the cell walls. Eckstein & Karlsson (1999) have provided a more detailed
analysis of nitrogen dynamics in the segment chains of H. splendens.
Element concentrations in bryophytes also exhibit seasonal fluctuations that
may be related to changes in the supply rates from the various sources and also
biological factors such as growth dilutions in the plants themselves (e.g. Lewis
Smith 1978, Bates 1987, Markert & Weckert 1989, Martı́nez-Abaigar et al. 2002a).
There are a few recent reports of the occurrence of biomineralization in
bryophytes. This is the process whereby soluble elements combine to form
307
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J. W. Bates
crystals of insoluble compounds within living cells, a phenomenon that is well
known in vascular plants. Ron et al. (1999) described a range of minerals including bohemite, ferrihydrite, gibbsite, jarosite, lepidocrocite, and pirolusite in
cells of the moss Hookeria lucens in Spain. The same group (Estébanez et al.
2002) reported amorphous crusts of opal, carbonates, and Al and Fe hydroxides
in healthy material of Homalothecium sericeum. They conclude that biomineralization occurs mainly in non-growing regions of the plant where the supply of
elements from the substratum exceeds the requirement. Satake (2000) reported
iron containing crystals on the cell walls of the moss Drepanocladus fluitans
growing in an acid and iron-rich lake. A similar phenomenon, involving deposits containing Fe and Mn on the leaves of Fontinalis antipyretica, was reported
from a stream polluted with mine effluent (Sérgio et al. 2000).
Mineral supply to the sporophyte
Mineral nutrients appear to reach the developing sporophyte from the
gametophyte via conducting cells in the central strand of the seta. When
Chevalier et al. (1997) supplied radioactively labeled orthophosphate to gametophores of Funaria hygrometrica, a proportion of the 32P was eventually detected in
the capsule and its spores. The proportion translocated was highest (18% of total
absorbed) when the capsule was green without recognizable spores, but fell to
zero in plants with mature brown capsules. Uptake of 32P also occurred when
the solution was applied directly to the capsule, indicating that absorption of
nutrients from wet deposition by young sporophytes may occur in nature.
Brown & Buck (1978) used an analytical approach to infer a similar pattern of
nutrient cation movements from the leafy gametophores of F. hygrometrica to the
developing sporophyte. By contrast, Basile et al. (2001), employing X-ray microanalysis, demonstrated that conduction of the heavy metals Pb and Zn is largely
blocked in its passage from gametophyte to sporophyte by the transfer cells of
the placenta. Zinc, an essential micronutrient, was able to pass this barrier more
effectively than the inessential Pb. Rydin (1997) suggested that the production of
sporophytes may be an important sink for nutrient resources in bryophyte
populations but this needs verification for mineral nutrients.
8.2.4
Nutrient inputs in nature
Figure 8.3 shows the three most likely sources of nutrients for terrestrial bryophyte gametophores in nature: (1) the substratum; (2) wet deposition, i.e. precipitation including leachates from any plant or other surfaces over
which it flows; (3) dry deposition, i.e. dust and gases (e.g. NH3, SO2, NO2).
Bryophytes may utilize several sources for the different essential elements.
Techniques that have been used to study nutrient supply include: (i) analysis
8 Mineral nutrition and substratum ecology
Fig. 8.3. A dynamic model of the potential inputs and losses of nutrients and non-essential
elements to a bryophyte. Reproduced from Bates (1992a) with permission of the British
Bryological Society.
of tissues and of precipitation (including canopy throughfall and tree stemflow)
before and after passing through a bryophyte layer; (ii) nutrient application
experiments.
Analytical studies
Tamm’s (1953) study of growth and nutrition of the boreal forest moss
Hylocomium splendens is widely regarded as a ‘‘classic’’ in bryology, having provided the foundation for many later investigations. Uptake of water from the
soil by the ectohydric ‘‘fronds’’ of H. splendens is poor and he considered it
unlikely that mineral nutrients were input by this pathway. Growth rates of
H. splendens were higher under the forest canopy than in clearings, and particularly rapid in the zone under the boundaries of tree canopies. This was also
the region where Tamm demonstrated the greatest nutrient enrichment of
throughfall by leachates from the tree canopy. Thus, a major conclusion was
that H. splendens received mineral nutrients predominantly as wet deposition.
Canopy leachates appeared to be important as a source of P, which is present at
very low concentrations in precipitation. Tamm also deduced that, despite a
strong dependency of growth on moisture supply, nutrient limitation was the
most important obstacle to the productivity of H. splendens in Norwegian forests.
309
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J. W. Bates
Fig. 8.4. Nitrate reductase (NR) activity in Sphagnum fuscum in relation to natural
precipitation (upper graph) on an ombrotrophic, subarctic mire at Abisko, Sweden. Day 1
corresponds to 18 July 1983. NR activities are means of four replicates. Redrawn from Woodin
et al. (1985).
The importance of wet deposition in supplying mineral elements to
Sphagnum species in Scandinavian ombrotrophic (‘‘rain-fed’’) mires was also
inferred by Malmer (1988). Total concentrations of several elements and especially N and S showed, in some cases, correlations with known wet depositions
of the elements at the mires. With regard to N utilization by ombrotrophic peatmosses, Woodin et al. (1985) demonstrated a remarkably close coupling between
the atmospheric supply of nitrate ions in wet deposition and the assimilation of
this N source by the nitrate reductase enzyme. During dry periods the nitrate
reductase activity in S. fuscum at an unpolluted site in Northern Sweden
remained low, but activity rapidly increased during natural precipitation containing dilute NO3 (Fig. 8.4), or during experimental treatments of the moss
carpet with 1 mM NO3 . Woodin et al. (1985) noted that by efficient capture of the
NO3 in rainwater the Sphagnum plants deprive higher plants rooted in the peat
of this nutrient supply.
An experimental approach to the problem of determining the sources of
mineral nutrients to Calliergonella cuspidata in Dutch chalk grassland was
adopted by van Tooren et al. (1990). They determined nutrient concentrations
in rainfall, in the water dripping from C. cuspidata, and in the shoots of the moss.
8 Mineral nutrition and substratum ecology
In this instance, NHþ
4 was the only ion that appeared to be absorbed by the moss
in significant amounts from the natural wet and dry deposition received.
Interestingly, N and P concentrations were significantly higher at the end of
the experiment in plants on soil compared to those on acid-washed sand, and
uptake of N, P and K were all significantly higher in shoots on soil, and these also
had a higher growth rate than the sand plants, when they were maintained in a
humid garden frame. These results, although achieved under artificial conditions, show that nutrient uptake from soil cannot be ignored in ectohydric
bryophytes.
Nutrient application experiments
The application of nutrients to natural swards of bryophytes has been
increasingly used to examine the effectiveness of different supply pathways and
to assess the likely impacts of anthropogenic increases in nutrient (mainly N)
supply (see Section 8.2.9).
Elements present at elevated concentrations in the substratum are often
found in high concentrations in bryophytes, indicating direct uptake. Hébrard
et al. (1974) provided a unique demonstration of this by fashioning artificial
boulders from a concrete mixture into which a solution of the radionuclide 90Sr
had been mixed. The isotope readily entered shoots of Grimmia orbicularis and
Leucodon sciuroides later implanted into cracks in the boulders. Maximal concentrations in the shoots were attained during prolonged wet periods, these providing the most suitable conditions for solubilization and uptake of the 90Sr.
Although pleurocarpous mosses in forests generally have a poorer contact
with their underlying soil, Bates & Farmer (1990) eventually found elevated Ca
concentrations in the young apices of Pleurozium schreberi plants growing over a
layer of calcium carbonate powder. It was concluded that Ca2þ ions had moved
to the apices through the cell wall (apoplast) system under the influence of an
evaporative moisture flow. Similar conclusions were reached by Brūmelis et al.
(2000) following a transplant study with turves of Hylocomium splendens. Nutrient
flow from underlying litter is also implied in a study of grassland bryophytes by
Rincón (1988).
The importance of wet deposition in supplying macronutrients to ectohydric
mosses was investigated by Bates (1987, 1989a,b) in Pseudoscleropodium
(Scleropodium) purum in nutrient application experiments performed under field
conditions. This pleurocarpous species, like Hylocomium splendens and Pleurozium
schreberi, forms monospecific carpets that are separated from the underlying soil
by a layer of accumulated litter in grassland, scrub and open forest habitats.
Addition of K and Ca caused immediate increases of these metals in the cationexchanger, moreover the addition of Ca displaced natural exchangeable Mg, but
311
J. W. Bates
K ( µmol g
–1
d.m.)
(a)
180
160
140
120
100
80
60
40
20
0
Ca (µmol g
–1
d.m.)
(b)
200
180
160
140
120
100
80
60
40
20
0
µmol g
–1
d.m.)
(c)
Mg (
312
70
60
50
40
30
20
10
0
0
J ul
20 40 60 80 100 120 140 160 180 200
Days after treatment
A ug
Sep
Oct
No v
Dec
J an
F eb
Fig. 8.5. Metal concentrations on the cation exchanger of Pseudoscleropodium purum
immediately before nutrient application, and at intervals afterwards, in Windsor Forest,
Berkshire, England. Filled circles, untreated; squares, KH2PO4-treated; open circles, CaCl2treated. (a) Potassium, (b) calcium, (c) magnesium. Significance of treatment effect at each
harvest: ***, p<0.001; ** p<0.01; * p<0.05. Vertical bars represent LSD0.05. Reproduced from Bates
(1989a) with permission of the British Bryological Society.
levels of all three cations gradually equilibrated with their ambient availabilities
as revealed by the control (Fig. 8.5). Interestingly, the Ca-treated shoots, in which
exchangeable Mg had been displaced, experienced a period of significantly lowered Mg concentration in the intracellular fraction (Fig. 8.6). This result indicates
Mg (
µmol g
–1
d.m.)
8 Mineral nutrition and substratum ecology
45
40
35
30
25
20
15
10
5
0
0
J ul
20 40 60 80 100 120 140 160 180 200
Days after treatment
A ug
Sep
Oct
No v
Dec
J an
F eb
Fig. 8.6. Intracellular Mg concentration of Pseudoscleropodium purum before nutrient
application, and at intervals afterwards. See Fig. 8.5 for details. Reproduced from Bates (1989a)
with permission of the British Bryological Society.
that sequestration onto the cation exchanger is probably an important first stage
in the absorption of Mg into the living protoplasts. In these experiments, a
marked and protracted rise in the level of intracellular P was observed, but
cellular absorption of K occurred only under conditions of prolonged moisture
availability.
The ecological importance of the nutrient-retaining capacity of
Pseudoscleropodium purum has been emphasized in a comparative study with
Brachythecium (Bates 1994). In field conditions B. rutabulum normally maintains
a higher productivity than P. purum (Rincón 1988, Rincón & Grime 1989) by
exploiting nutrients in plant litter (see ‘‘litter species’’, below). However, when
nutrients were supplied in an initial short ‘‘pulse’’ and the plants cultivated in a
nutrient-free environment, the relative growth rate of P. purum was higher than
that of B. rutabulum. It was concluded that P. purum utilizes the unpredictable
nutrient supply in wet deposition in an efficient and opportunistic manner,
whereas B. rutabulum relies upon a more or less continuous input of nutrients
from its litter substratum.
Hoffman (1972) made a detailed study of 137Cs transfers in a Liriodendron
forest stand at Oak Ridge, Tennessee, that is extremely revealing about sources
of elements to bryophytes. He introduced the radionuclide, which behaves as an
analog of K in plant cells, into the tree stems through vertical slits. Eventually
radioactivity was recovered in epiphytes and woodland floor bryophytes, the
main pathway being via leachates from the tree canopy in the throughfall. On a
dry mass basis the levels were ultimately higher in the bryophytes than in the
tree foliage. A study of element concentrations in Rhytidiadelphus triquetrus
transplants also suggested that the chemistry of this terricolous moss was
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J. W. Bates
strongly influenced by the tree canopy. Cation concentrations in the moss
appeared to be more closely correlated with the soil type (calcareous or noncalcareous) in which the canopy trees were rooted than with the soil type
immediately beneath the moss carpet (Bates 1993).
An eight-year study of nutrient absorption by Hylocomium splendens in a
Swedish forest has provided additional valuable insights into the sources and
utilization of N by this moss (Forsum et al. 2006). Importantly it was discovered
that amino acids, derived from the coniferous canopy of the forest, particularly
under conditions of high N deposition, constituted a significant proportion of
the total N received in throughfall and absorbed by the moss.
8.2.5
Desiccation effects on nutrient retention
Bryophytes leak cell solutes during rehydration following a period of
desiccation (e.g. Gupta 1977, Brown & Buck 1979). Until recently this process
had been investigated only under laboratory conditions, but Coxson (1991)
reported major losses of electrolytes from tropical forest epiphytes during
rehydration. Wilson & Coxson (1999) described pulse releases of solutes from
Hylocomium splendens in coniferous forest. The extent to which these losses may
be disadvantageous or benefit other organisms merits further investigation.
The effects of desiccation–rehydration cycles on ion uptake and nutrient utilization have been little studied, but results from several field studies (Bates 1987,
1989a,b, van Tooren et al. 1990, Bakken 1994) suggest that desiccation may often
impair the capacities of bryophytes to benefit from favorable nutrient regimes.
Bates (1997) compared the growth and nutrient accumulation from regular applications of NPK in the mosses Brachythecium rutabulum and Pseudoscleropodium purum
growing continuously hydrated or subject to intermittent drying. Pseudoscleropodium
purum proved to be significantly more tolerant of desiccation than B. rutabulum and
was able to absorb nutrients (e.g. P) almost as well under intermittent desiccation as
under continuous hydration. Growth and nutrient uptake were both strongly
suppressed by intermittent desiccation in B. rutabulum, whose high productivity
depends on long periods of continuous hydration. These observations have been
extended by Bates & Bakken (1998) and Badacsonyi et al. (2000).
Brown & Buck (1979) were among the first investigators to demonstrate
convincingly that the cell wall cation exchanger of mosses probably functions
to sequester and aid, via an apoplast–symplast route, the reabsorption of
cations, such as Kþ and Mg2þ, leaked from the protoplasts during rehydration
episodes. Supportive data are also presented by Bates (1997), Bates & Bakken
(1998) and Badacsonyi et al. (2000).
In the case of nitrogen uptake as NO3 , assimilation by the enzyme nitrate
reductase (NR) is a key process and one that is often sensitive to drought in
8 Mineral nutrition and substratum ecology
vascular plants. In a comparison of NR activity following desiccation and rehydration in the highly desiccation-tolerant Tortula ruralis and Porella platyphylla,
Marschall (1998) found some major differences. In the liverwort, NR activity
remained unchanged in the light, but rose progressively within the first hour
after rehydration in the dark. By contrast, NR activity declined sharply over the
same period in the moss T. ruralis. These differences may result from fundamental differences in the pools of available sugars and reductants in mosses and
liverworts upon rehydration, however, further work on NR in bryophytes is
needed to clarify the situation.
8.2.6
Evidence for internal recycling of nutrients
Several writers (e.g. Malmer 1988, Brown & Bates 1990, Bates 1992a)
have speculated that internal recycling of essential elements (i.e. from old to
young tissues) may occur in bryophytes, thus removing the need for continued
ion absorption. What evidence is there for such recycling?
Older work (e.g. Collins & Oechel 1974, Callaghan et al. 1978) had suggested
that translocation of resources such as photosynthates did not occur in bryophytes, except in taxa like Polytrichum with obvious conducting tissues.
However, Alpert (1989) demonstrated movement of photoassimilate (but not
mineral nutrients) from leaves to stem bases and underground stems of the
ectohydric moss Grimmia laevigata. Rydin & Clymo (1989) also obtained evidence
of movement, from old to young tissues of Sphagnum recurvum, of both carbon
and phosphorus compounds, and demonstrated the presence of numerous
plasmodesmata linking stem cells and thus affording a possible symplast pathway. Neither of these species possesses recognizable conducting tissues in the
sense of Hébant (1977). Ligrone & Duckett (1994, 1996) have described ‘‘food
conducting’’ cells in many mosses that lack conventional conducting tissues but
it is currently unknown whether these are involved in translocation of inorganic nutrients.
Wells & Brown (1996) devised an ingenious method for testing the recycling
hypothesis employing shoots of Rhytidiadelphus squarrosus cut to different initial
sizes (4 and 8 cm) and cultivated in nutrient-free conditions. Nutrient contents
were determined in the new growth (N) and in the existing 2 cm segment. New
growth was being supported entirely by the nutrient content of the existing
growth, with elements moving from the latter for this purpose. When the
shorter (4 cm) segments were used, the withdrawal of nutrients from the parent
segments was proportionately greater in response to the smaller overall pool
size. Brümelis & Brown (1997) working with segment chains of Hylocomium
splendens also adjusted the internal nutrient pool available to the developing
juvenile segment by removing branches from the parent segment. Branch
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J. W. Bates
removal led to a lowered K, Mg, Ca and Zn content of the juveniles. A similar
approach was employed by Bates & Bakken (1998) except that nutrient pools
were altered by killing (steaming) sections of stem and the two ecologically
contrasted mosses Brachythecium rutabulum and Pseudoscleropodium purum were
compared. Internal relocation of nutrients was important in the ‘‘low productivity’’ P. purum but not in the ‘‘high productivity’’ B. rutabulum.
An important contribution has been made by Eckstein & Karlsson (1999) who
compared recycling of 15N among segments of H. splendens with that occurring in
ramets of Polytrichum commune in arctic Sweden. Young growth of both species
was an important ‘‘sink’’ for N. In late summer all older segments in P. commune
showed a net loss as the element was moved to subterranean stems. In H.
splendens the dynamics can be summarized as follows: current-year’s segments
are totally dependent upon older segments for nitrogen and received a disproportionate supply of 15N (i.e. the most recently absorbed N); one-year-old segments still import 15N from older segments but also absorb external N and so act
largely as conduits for N-supply to the juveniles; two-year-old segments act as
storage sites for resources; three-year-old segments are degenerating and act
only as sources of N. In a related study on H. splendens growing in subarctic birch
woodland, Eckstein (2000) demonstrated that mean retention times for nitrogen
in this moss varied from 3 to 10 years owing to effective acropetal transport and
relocation of the element in younger tissues. Aldous (2002) has also demonstrated substantial translocation of nitrogen from older to younger tissues in
Sphagnum capillifolium by using the tracer 15NH415NO3 added to field plots in four
North American bogs. She applied an analysis of 15N dynamics in the capitulum
(1 cm) and top 2 cm of the stem and concluded that translocation mainly offered
a second opportunity for the young tissues to benefit from recently deposited N
and possibly also from N mineralized within the peat. This investigation did not
provide conclusive information about whether the N translocation in S. capillifolium occurs in the symplast or by another pathway.
Collectively, these studies indicate that the relocation of elements within
growing bryophytes is probably a widespread and important facet of their
mineral nutrition.
8.2.7
Role of bryophytes in ecosystem nutrient dynamics
Bryophytes assume long-term dominance only in peatlands and some
tundra environments where competition from higher plants is absent (Bates
1998). Nevertheless, they can also form conspicuous components of ecosystems
dominated by higher plants, notably in moist forests, or become dominant for
short periods in successional or ephemeral communities. In these situations
they may have an importance in the overall nutrient economy of the ecosystem
8 Mineral nutrition and substratum ecology
Table 8.1 Mineral inputs and accumulation in two forests with luxuriant bryophyte
ground covers
(a) Coed Cymerau oakwood, Wales (after Rieley et al. 1979)
kg ha
1
yr
1
Ca
Mg
K
Na
Throughfall
10.0
13.9
19.0
103.8
Litterfall
21.0
4.2
10.2
3.1
Total input (T þ L)
31.0
18.1
29.2
106.9
4.1
3.9
14.3
1.6
Bryophyte accumulation
(b) Washington Creek black spruce forest, Alaska (after Oechel & Van Cleve 1986)
meq m
2
per season
N
P
Ca
Mg
K
Combined throughfall and litterfall
24.0
0.6
29.0
5.0
4.0
Bryophyte accumulation
92.0
5.0
14.0
12.0
16.0
that is disproportionate in relation to their often modest biomass (see reviews
by Longton 1988, 1992, Slack 1988, Brown & Bates 1990, Bates 1992a).
In a successional community on glacial sands dominated by the mosses
Polytrichum juniperinum and Polytrichum piliferum in New Hampshire, U.S.A., Bowden
(1991) concluded that measurements of N in bulk precipitation accounted for
58%, and nitrogen fixation and coarse organic N for 7% of the total N input. The
remaining 35% of N was input as wet deposited organic N, dry deposition, and
dew. Nitrogen was retained, with only small losses, by both the mosses and the
accumulating organic matter in the soil. This moss-ecosystem was extremely
efficient at removing N from precipitation; when the moss was removed
experimentally, N losses from the ecosystem temporarily exceeded inputs.
Bryophytes may be important in more complex ecosystems by absorbing
nutrients in precipitation, dust, and litter before they can be taken up by the
roots of higher plants (Oechel & Van Cleve 1986). This has already been mentioned with respect to utilization of wet-deposited NO3 by Sphagnum in ombrotrophic mires (Section 8.2.4). Detailed estimates of nutrient inputs by throughfall
and litterfall to the bryophyte layer in two forests are summarized in Table 8.1.
Nutrient accumulation by bryophytes, which formed about 90% of the ground
flora in the Welsh oakwood, was comfortably exceeded by the inputs, but there is
little excess K for tree and other higher plant growth. In the nutrient-poor
Alaskan black spruce forest (Table 8.1b) the bryophyte layer appears to have
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J. W. Bates
accumulated more of every element except Ca than was input as throughfall
and litter. Moreover, the moss layer retained considerable further potential for
nutrient sequestering on its cation exchange complex. Additional nutrients
may have been obtained by the bryophytes from the underlying soil (Oechel &
Van Cleve 1986). Despite this efficiency in nutrient capture, two species
(Hylocomium splendens, Sphagnum nemoreum) responded with higher photosynthesis when fertilized with a complete nutrient (Hoagland’s) solution, suggesting
that they had been nutrient limited. Bryophytes may also have significance in
the nutrient economies of other communities where they are less conspicuous
than in forest. In Dutch chalk grassland they grow and absorb nutrients during
autumn and winter when higher plants are inactive, and they release nutrients
by decomposition in spring and summer, which are utilized by the higher
plants (van Tooren et al. 1988).
Bryophytes may also influence ecosystems by retaining nutrients for long
periods in their undecomposed dead matter (Longton 1988, van Tooren 1988,
Brown & Bates 1990). Bryophyte tissues decompose at much slower rates than
those of higher plants, major factors being low temperatures, waterlogging,
acidity, high cation exchange capacity, presence of high contents of ligninlike compounds, accumulation of lipids, and high carbon:nitrogen ratios.
Insufficient data on bryophyte decomposition rates exist for many key habitats
(Brown & Bates 1990).
Whether fungi are involved in mineral nutrient cycling between bryophytes
and other ecosystem components remains uncertain. Chapin et al. (1987) presented data suggesting that mycorrhizal fungi of the dominant tree Picea mariana
(black spruce) in Alaskan forest stimulated the release of phosphorus from the
overlying bryophyte carpet to the tree roots. Quite a different picture was obtained
by Wells & Boddy (1995) who observed translocation of 32P from pieces of inoculated wood (buried in the leaf litter) to the living apices of the moss Hypnum
cupressiforme. This occurred via the saprotrophic basidiomycete Phanerochaete velutina, which was observed to connect to the older parts of H. cupressiforme. Although
true mycorrhizas involving mosses are unknown, this type of association might
account for the uptake of scarce elements such as P from the underlying soil.
Liverwort–fungus symbioses, in contrast, are relatively common (e.g. Duckett et al.
1991, Duckett & Read 1995) but little is known about their importance in mineral
nutrition. Further important discoveries can be anticipated in this field.
8.2.8
Effects of nutrient scarcity and nutrient excess
Among vascular plants the often low availabilities of the two macronutrients, nitrogen and phosphorus, in natural habitats have provided a major
stimulus to the evolution of a range of nutritional specialisms which often
8 Mineral nutrition and substratum ecology
involve symbioses with micro-organisms. These include N2-fixing root nodules,
the carnivorous habit, mycorrhizas, and the ‘‘cluster roots’’ of Proteaceae and
some other plant families. It is pertinent to ask whether any similarities exist
among bryophytes. Ironically, the release of large quantities of anthropogenic
nitrogen and phosphorus compounds into the atmosphere and waterways has
come to characterize the modern age. There has been a recent surge of interest
among plant scientists about the effects of excess N inputs on bryophytes and
bryophyte-containing plant communities that had originally established by coping with shortages of these elements. Although pollution is outside the scope of
this chapter, some mention of this work is required as it is informative about
nutrient assimilation pathways and physiological effects of macronutrients.
Nitrogen
No carnivorous bryophytes are known, neither do bryophytes appear to
enter into symbioses with soil bacteria such as Rhizobium, presumably because
they lack roots and a sophisticated vascular system. Nevertheless, nitrogen
fixation, by micro-organisms (sometimes unidentified) containing the nitrogenase enzyme, in ‘‘biological soil crusts’’ represents the main input of this element
into a number of bryophyte-rich ecosystems, and particularly in polar tundra in
both the Arctic and Antarctic (Belnap 2001). Studies in the High Arctic have
revealed a high species diversity of nitrogen-fixing cyanobacteria growing epiphytically on the leaves and stems of mosses and probably benefiting from the
moisture held amongst these structures (Zielke et al. 2002, 2005). N2-fixation in
other ecosystems may be responsible for smaller but still significant inputs (e.g.
Brasell et al. 1986, Matzek & Vitousek 2003). Whether any of these associations
represents specific mutualisms is currently unknown.
Associations of nitrogen-fixing cyanobacteria with hornworts and liverworts
have long been known, but it is only recently that a glimpse of the biochemical
sophistication of the symbiotic relationship has been obtained (Meeks 1998,
Adams 2000). Based on studies of the Anthoceros–Nostoc and Blasia–Nostoc associations it is clear that the bryophyte, when starved of nitrogen compounds,
releases one or more chemical signals that induce the formation of short,
infective filaments called hormogonia by the Nostoc and may also have an
attractant function towards these motile filaments (Meeks et al. 1999, Adams
2002). The hormogonia have smaller cells than parent Nostoc filaments, lack the
characteristic N2-fixing heterocysts, and exhibit gliding motion, which is vital
for infection. They eventually inhabit mucilage-filled cavities on the ventral
surfaces of the hornworts and the ventral auricles of Blasia. Upon infection,
developmental changes lead to the generation of Nostoc filaments with greater
densities of heterocysts than in the free-living parent filaments and the
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J. W. Bates
cyanobacteria begin to leak about 80% of their fixed nitrogen to the host plant in
the form of NH3. As in cyanobacterial lichens, where a similar leakage of
reduced N occurs to the fungal symbiont, this release is connected with a
reduced activity of glutamine synthetase in the symbiotic Nostoc, which partly
blocks its entry into normal nitrogen metabolism within the cyanobacterium.
Considerable progress has been made in identifying the genes in Nostoc (the
hrmUA operon) switching the changeover from hormogonia to heterocystcontaining filaments in response to a hormogonium-repressing factor (HRF)
discovered in aqueous extracts of Anthoceros (Meeks et al. 1999, Adams 2002).
Studies on the effects of increased wet deposited nitrogen to bryophytes have
concentrated upon ombrotrophic mires, but have also involved minerotrophic
(including calcareous) fens (Bergamini & Pauli 2001, Paulissen et al. 2005), acid
grasslands (Morecroft et al. 1994, Carroll et al. 2000), boreal forest (Bakken 1994,
Skrindo & Økland 2002, Forsum et al. 2006), arctic heath (Gordon et al. 2001),
montane species (Woolgrove & Woodin 1996a,b, Pearce et al. 2003) and epiphytes (Mitchell et al. 2004, 2005). Mires are among the most nutrient deficient
habitats and also locations where the peaty substratum contains a large body of
fixed carbon that might be released into the atmosphere as greenhouse gases
should conditions alter to favor its decomposition. Major shifts in vegetation
composition, especially the ousting of bryophytes by higher plants, invariably
accompany the application of macronutrients to natural bryophyte-rich ground
communities (Mickiewicz 1976, Jäppinen & Hotanen 1990, Kellner &
Maº rshagen 1991, Virtanen et al. 2000, Aude & Ejrnæs 2005). However, much
depends on the nature of the initial community, its degree of isolation from
sources of potential invaders, and the type and intensity of fertilization.
One of the first effects of the quickly dissolving solid fertilizers used to
improve timber yield in northern European forests is to cause ‘‘burning’’ of
the bryophyte tissues contacted (Jäppinen & Hotanen 1990). Most of the common species (Pleurozium schreberi, Hylocomium splendens, Dicranum spp., Sphagnum
spp.) decreased markedly in these studies, but Polytrichum commune appeared
more resistant. The decline of Rhytidiadelphus squarrosus in acidic and calcareous
grassland plots observed by Morecroft et al. (1994) and Carroll et al. (2000) in
response to ammonium nitrate or ammonium sulfate additions was not accompanied by a detectable increase in higher plant cover and appears to have
resulted from direct disturbance of the moss’s nitrogen metabolism. This may
also have been the cause of a loss of bryophyte biomass and diversity in response
to N and NPK additions (as solids) in the calcareous fens studied in Switzerland by
Bergamini & Pauli (2001).
In originally pristine mires, applications of combined-N may cause a stimulation of the elongation growth of Sphagnum species in the first year (e.g. Aerts et al.
8 Mineral nutrition and substratum ecology
1992, Gunnarsson & Rydin 2000) but have generally reduced growth of bogmosses in the longer term (however, see Vitt et al. 2003). At sites already
experiencing high N deposition, additions of the nutrient generally do not
cause further growth increases of Sphagnum, instead other factors such as P
availability or low temperature appear to limit growth (Aerts et al. 1992,
Limpens et al. 2003a, Gunnarsson et al. 2004). No evidence was found that the
fen moss Calliergonella cuspidata was directly damaged by high N deposition
(Bergamini & Peintinger 2002). Much of the experimental work has used ammonium nitrate as the N source. Where ammonium and nitrate ions have been
supplied separately there is evidence that the former is more detrimental to
bryophytes (Pearce et al. 2003, Paulissen et al. 2005). Although there is strong
evidence that Sphagnum and other bryophytes are competitively displaced by
faster-growing vascular plants under high N deposition (e.g. Limpens et al.
2003b), there may also be detrimental effects owing to stimulation of the fungal
parasite Lyophyllum palustre and of epiphyllic algae (Limpens et al. 2003c).
Baxter et al. (1992) showed that when Sphagnum species accumulate excess N,
they do so in the form of increased free cytosolic amino acids. Production of
these ‘‘useless’’ amino acids requires carbon ‘‘skeletons’’ and may eventually
become harmful by depriving metabolism of fixed carbon. Nordin &
Gunnarsson (2000) showed that where amino acid-N accumulation exceeded
2 mg g 1 dry mass in the capitulum, growth began to be retarded. Paulissen et al.
(2005) demonstrated large differences in the abilities of some fen bryophytes to
form amino acids as a detoxification mechanism when challenged with excess
NHþ
4 : Calliergonella cuspidata, the most sensitive species in terms of growth
reduction, did not accumulate N and produced only moderate amounts of
arginine; Sphagnum squarrosum and Polytrichum commune, the most tolerant taxa,
showed strong accumulation of total N and several amino acids. For further
information about this complex and rapidly expanding subject also see the
review by Turetsky (2003).
Phosphorus
P is often scarce in natural ecosystems or else present in unavailable
forms within organic matter. Press & Lee (1983) demonstrated significant acid
phosphatase activity in 11 species of Sphagnum surveyed in Britain and Sweden.
Acid phosphatase activity was negatively correlated with the total P concentration of the plants and, in experiments, increased under conditions of phosphate
starvation. The study was presented against the background of increased P
supply due to atmospheric pollution, but the results imply that Sphagnum may
often utilize simple organic forms of P in the peatland environment, the supply
of inorganic P in precipitation being poor.
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J. W. Bates
Christmas & Whitton (1998) have described appreciable surface phosphatase
activity in the aquatic mosses Fontinalis antipyretica and Rhynchostegium riparioides,
implying that these mosses can also utilize simple organic forms of P. Activities
of phosphomonoesterase (PMEase) were highest in the nutrient-poor headwaters of a stream where tissue P concentrations were low. Downstream the
activity of PMEase declined progressively as concentrations of P in water (and
moss) increased. The authors suggest that assays of PMEase in aquatic mosses
could provide a simple and reliable indication of nutrient status in streams
where nutrient concentrations may fluctuate widely in the short-term.
Extending this study to a range of upland and mainly terrestrial mosses in
northern England, Turner et al. (2003) demonstrated wide seasonal variations in
phosphatase activities (usually highest in winter and lowest in summer)
whereas tissue P concentrations remained relatively constant through the
year. Noting a negative correlation between enzyme activity and nutrient availability, these authors suggest that information about past nutrient (P) conditions could be obtained by determining phosphatase activities of herbarium
specimens.
Although P is one of the key nutrients responsible for anthropogenic eutrophication of waterways, its effects on aquatic bryophytes have received comparatively little attention (e.g. Bowden et al. 1994, Steinman 1994). In a
laboratory study, Martı́nez-Abaigar et al. (2002b) demonstrated ‘‘luxury’’ accumulation of P by the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia
from culture solutions enriched with KH2PO4 and significant negative effects of
the absorbed nutrient on net photosynthesis and pigment concentrations.
8.2.9
Biomonitoring of mineral deposition
As a result of their efficient mineral-absorbing capabilities, bryophytes
have become popular organisms for biomonitoring levels and identifying
sources of elements, especially pollutants, by analyzing their tissues. Indeed,
based on the sheer numbers of surveys and published studies appearing in all
parts of the world, a strong case can be made that biomonitoring is currently the
primary justification for scientists spending valuable public resources studying
bryophytes!
Bryophytes commonly sequester mineral elements, including those of major
physiological importance, those that are required only in trace quantities (e.g.
Cu, Fe, Mn, Zn) and those that are non-essential (e.g. Cd, Cr, Hg, Ni, Pb, Se, Sr, Ti,
V). Some of these elements may be picked up from the substratum and others
from wind-blown particles or in wet deposition. The absorption appears to
involve three separate processes. First, there is passive adsorption onto the
bryophyte’s cation-exchanger. Generally, heavy metals are more effectively
8 Mineral nutrition and substratum ecology
adsorbed than physiological cations like Kþ and Ca2þ and they may ‘‘condense’’
the exchange sites so that they are effectively immobilized. Second, some
mineral elements are capable of entering the cells via transporter proteins
(e.g. Brown & Beckett 1985, Brown & Sidhu 1992, Basile et al. 1994). Third, the
numerous small leaves and intricate surfaces of bryophytes offer many possibilities for entrapment of metal-containing soil and ash particles. Collectively,
these processes allow bryophytes to bioaccumulate heavy elements to concentrations far in excess of ambient concentrations or of concentrations found in most
vascular plants.
Two main approaches have been used: (1) surveys involving analysis of
indigenous bryophytes; (2) surveys with transplanted mosses and ‘‘moss
bags’’. Both have the advantage that the basic materials are cheap and widely
available, but there are also problems of sample reproducibility that must be
carefully addressed if the results are to be meaningful. Besides revealing
patterns in metal deposition, any survey of concentrations in living plant
material is likely to be distorted to some extent by variations in moss growth,
element uptake, and losses imposed by microhabitat variations (Damman
1978, Gerdol et al. 2002, Zechmeister et al. 2003, Leblond et al. 2004). In surveys
with indigenous bryophytes, widespread pleurocarpous mosses have become
the preferred subjects from a practical (and conservation) viewpoint. Careful
protocols are required to standardize the samples used for analysis (see
reviews of Brown 1984, Burton 1986, 1990, Tyler 1990, Berg & Steinnes 1997,
Onianwa 2001).
Monitoring heavy metal deposition
Countrywide surveys of metals in mosses (usually Hylocomium splendens
or Pleurozium schreberi) have been repeated over a long period in Norway and
Sweden (Rühling & Tyler 2004). Figure 8.7 shows some results from repeated
surveys in Norway. The tightly clustered Ni-isopleths in the north and south are
explained by emissions from copper–nickel smelters on the Kola Peninsula and
by long-range transport from industrial Europe, respectively. Lead reaches
Norway principally through long-range atmospheric transport; the data
suggest that deposition has decreased by 30%–40% since the first survey in
1977. Further reductions have been reported in the latest survey (Rühling &
Tyler 2004). Similar surveys have now been carried out at five-yearly intervals in
a coordinated way in the majority of European countries under the ‘‘Heavy
Metals in European Mosses’’ monitoring program of the United Nations
Economic Commission for Europe since 1990 (e.g. Markert et al. 1996, Herpin
et al. 1996, Gombert et al. 2004). Multivariate analyses of these multielement
surveys enable the ‘‘signatures’’ from different sources to be distinguished.
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J. W. Bates
Fig. 8.7. Contour maps showing average nickel and lead concentrations (mg g 1) of
Hylocomium splendens in Norway based on samples collected at 495 sites (redrawn from Berg
et al. 1995).
Berg et al. (1995) subjected the 1990 Norwegian data to principal components
analysis and obtained the following major ‘‘axes’’: (1) with highest values in the
south, representing long-range transport from other European countries of
many elements (Bi, Pb, Sb, Mo, Cd, V, As, Zn, Tl, Hg, Ga); (2) elements associated
with mineral particles in soil dust (e.g. Y, La, Al, Fe, V, Cr); (3) related to coppernickel smelters producing Ni, Cu, Co and As; (4) marine influence (Mg, B, Na, Sr,
Ca); (5) explained by a zinc smelter in the southwest (Zn, Cd, Hg); (6) related to
iron mining in the far north (Fe, Cr, Al); (7) believed to reflect leachates from
8 Mineral nutrition and substratum ecology
vascular plants, Cs and Rb are absorbed by roots and later transfer to mosses.
Similar conclusions were reached by Kuik & Wolterbeek (1995) from a comparable analysis of heavy metal data from Pleurozium schreberi samples in the
Netherlands.
Measurements of metal concentrations and their isotopes in herbarium
specimens provide an alternative perspective on temporal changes in deposition in regions where there has been a long history of bryological exploration
(Johnsen & Rasmussen 1977, Farmer et al. 2002).
In areas where the natural bryophyte vegetation is poor owing to atmospheric pollution or other stresses, metal deposition can be surveyed by transplanting bryophytes or employing moss bags. The latter consist of small samples
of moss enclosed in an inert mesh bag that can be tied to tree branches or
otherwise exposed for standard periods. The moss in these bags will usually die
quickly from drought stress, if it has not already been killed by acid washing to
remove contamination. Therefore very long exposure times will lead to disintegration and need to be avoided. Metal accumulation depends mainly on
particulate trapping and cation exchange capacity, and although several species
have been used, Sphagnum spp. have proved most popular (Brown 1984, Burton
1986). Other types of exposure may be necessary where longer exposure periods
are required. Tuba & Csintalan (1993) described the exposure of living cushions
of Tortula ruralis within wooden boxes for three months to determine metal
deposition in and around an industrial town in Hungary.
Monitoring with aquatics
Submerged aquatics accumulate metals and other substances from
water to a much greater extent than vascular plants, partly because their
nutrient uptake is less seasonal, and partly because they can absorb over their
entire surface. Drainage from disused metal mines is a common cause of water
contamination but metals may also be in solution and accumulated owing to
natural geological features (Samecka-Cymerman et al. 2000). In mid-Wales (U.K.)
the liverwort Scapania undulata has proved to be one of the most metal-tolerant
taxa among the common species of acid upland streams. Metal concentrations
in its shoots reflect those in the water (McLean & Jones 1975). In many situations
levels of metals in bryophytes appear to be at equilibrium with those in the
water. Kelly & Whitton (1989) established the nature of these relationships for
three mosses and a liverwort based on measurements of Zn, Cd, and Pb accumulation in many European streams. Each species and element exhibited a
different pattern; moreover, the bryophytes absorbed greater quantities of
metals than three algae with which they were compared. Garcı́a-Álvaro et al.
(2000) established relationships between water concentrations and those in
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J. W. Bates
Rhynchostegium riparioides for five major nutrient elements, Fe, and Na. Uptake of
metals is rapid, probably largely representing adsorption onto the cationexchanger, and levels in bryophytes may also decrease (depuration) following
a concentration spike (Mouvet et al. 1993, Claveri et al. 1994, Martins &
Boaventura 2002). However, uptake of mercury by Jungermannia vulcanicola and
Scapania undulata from an acid stream in Japan involved formation of crystals of
HgS in the cell walls (Satake et al. 1990). Both indigenous aquatics and transplanted samples have been widely used to monitor heavy metal pollution in
rivers. Mouvet (1985) and Mouvet et al. (1986) give examples where pollutant
releases from industrial premises have been precisely identified by monitoring
metal levels in mosses at intervals along watercourses. Chlorinated hydrocarbons and pharmacological compounds derived from faeces and urine may also
enter water courses and be accumulated by aquatic bryophytes (Mouvet et al.
1993, Delépée et al. 2003).
Monitoring nitrogen deposition
Several recent studies indicate that bryophytes may also make effective
biomonitors for assessing deposition of atmospheric N. Herbarium specimens
were analyzed by Baddeley et al. (1994) to demonstrate increases in N content of
the upland moss Racomitrium lanuginosum in Britain. Solga et al. (2005) and Solga
& Frahm (2006) found significant correlations of N content and negative correlations of biomass with N deposition in some common pleurocarpous mosses in
Germany. d15N ratios in the moss tissue were correlated with the ratios of
ammonium-N to nitrate-N deposition among the sites. Pearson et al. (2000) also
reported that d15N values calculated from isotopic assays of mosses growing on
roofs and walls discriminated between the reduced and oxidized forms of atmospheric nitrogen in urban and rural environments.
8.3
Substratum ecology
8.3.1
Range of substrata occupied
Bryophytes grow on a wide range of natural substrata: soil, rock, bark,
rotting wood, dung, animal carcases and leaf cuticles (Smith 1982a). From an
ecological viewpoint (During 1979, 1992, Bates 1998) the main properties that
determine whether a substratum can be colonized by a particular bryophyte
species are: (1) the lifespan of the surface; (2) its chemical properties; (3) its
water-holding capacity. It will be appreciated that if each of these properties
offered just a few distinct habitat classes, collectively they would yield a range of
contrasted ecological niches. In fact many bryophytes are faithful indicators for
particular sets of substratum-related conditions.
8 Mineral nutrition and substratum ecology
8.3.2
Longevity of substrata
During (1979) emphasized the importance of the lifespan of the substratum (or its surface) in determining the kinds of bryophytes that might
colonize it and successfully reproduce. It had already been established in higher
plants that certain integrated sets of morphological and physiological characteristics favored particular life-strategies (e.g. Grime 1974). During (1979, 1992)
argued that the most important habitat properties shaping the evolution of
bryophytes are (1) longevity of the substratum, determining the effort to be
put into rapid reproduction, and (2) the need for long-range dispersal to colonize
new substratum patches, influencing the number and size of spores produced
(many, small spores give the greatest chance of successful long-range dispersal).
Where there is little need for long-range dispersal, a third factor, the evolutionary option to avoid any unfavorable season as a dormant spore rather than a
more tender gametophyte, presents itself and favors large spore size.
The main life-strategies recognized by During (1992) are shown in Table 8.2.
The first column shows types that, before the end of their lives, must colonize
new substratum patches at some distance from the existing patch. Thus they
produce many light spores to increase the chance of success. Funaria hygrometrica
is the best known example of a fugitive, a mobile species that colonizes briefly
available habitat patches (e.g. gaps in turf), then spreads to other, often distant
sites. Colonists occupy similar unpredictably appearing habitats that persist for
longer. Local population multiplication may be brought about by gemmae and
rhizoid tubers (e.g. Bryum bicolor). Bryophytes that form long-lasting carpets on
relatively stable forest floors (e.g. Hylocomium splendens) are perennial stayers. Their
annual spore output is small but occurs over many successive years. The righthand column includes species with larger spores where there is less need
for long-range dispersal. Annual shuttle species are ephemeral plants that
Table 8.2 Bryophyte life-strategies based on the revised system of During (1992)
Spores
Potential life span
Numerous, small (<20 mm)
Few, large (>20 mm)
Reproductive effort
High
<1 year
Fugitives
Annual shuttle
A few years
Colonistsa
Medium shuttlec
Many years
Perennial stayersb
Dominants
a
Consisting of Ephemeral colonists, Colonists s.s. and Pioneers.
b
Consisting of Competitive perennials and Stress-tolerant perennials.
c
Consisting of Short-lived shuttle and Long-lived shuttle.
Low
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J. W. Bates
recolonize almost the same place (suitable ‘‘microsites’’) year after year from
large immobile spores left by the previous generation(s). Their wider dispersal is
often positively hindered by production of cleistocarpic capsules (e.g.
Ephemerum, Riccia). Some of these species possess long-lived spores that remain
dormant and enter a diaspore bank in the soil from which they may germinate in
any of several successive years (During 1997). Short-lived shuttle and long-lived
shuttle species occupy longer-lived microsites. Examples are provided by
Splachnum spp. on dung patches and many epiphytes on twigs and branches.
The longer-lived types also commonly have asexual propagules. Lastly, dominants refers to large-spored bryophytes that dominate certain ecosystems.
Sphagnum species in peatlands are the only clear example (During 1992).
During’s classification rests upon a subjective assessment of the correlations
between bryophyte habitats and their morphological and physiological attributes. Hedderson & Longton (1995) employed multivariate analysis to study
these plant and habitat concordances more objectively in three large orders of
mosses (see also Longton 1997). They concluded that many of the life strategies
did exist in fact, but that these should be regarded as ‘‘noda’’ in a continuous
network of life history variation.
8.3.3
Substratum and chemical specialists
It is a well-established paradigm that many bryophytes are faithful indicators of particular microhabitats (Birks et al. 1998). One suspects that these
associations often have a chemical basis as far as the substratum is concerned,
although in other cases there appears to be some other ecophysiological explanation. Unraveling the causes of these relations is at the very heart of bryophyte
ecology, yet in surprisingly few instances do we have a clear understanding of the
reasons for substratum specificity (Cleavitt 2001, Pharo & Beattie 2002). Wiklund &
Rydin (2004) remind us that the critical constraints on niche occupation may
operate during establishment from spores rather than in mature gametophores.
Using the examples of Buxbaumia viridis and Neckera pennata, rare mosses in
Sweden, they show how environmental factors (in this case pH and moisture
availability) interact to provide favorable but time-limited windows for successful colonization of the substratum. The following sections describe some
of the more important specializations found among bryophytes.
Epiphytes
Plants that grow upon the stems of other plants without deriving
sustenance from their living tissues are called epiphytes. The ‘‘host’’ is termed
a phorophyte. The bark of trees in many parts of the world supports a diverse flora
of epiphytic bryophytes, although they become scarce in very deep forest shade,
8 Mineral nutrition and substratum ecology
on very acid surfaces (e.g. some conifers), under atmospheric pollution, and
where the bark is abraded by winter ice or rubbed by livestock. The epiphytic
flora reaches greatest luxuriance under continuously moist conditions, notably
in high-altitude cloud forest (Pócs 1982). Numerous earlier studies of epiphytic
communities have been reviewed by Smith (1982b). He separated epiphytes into
‘‘obligate’’ and ‘‘facultative’’ kinds, the latter also occurring in other habitats.
Trees at maturity frequently support distinct vertical zones of communities
(e.g. Trynoski & Glime 1982, Cornelissen & ter Steege 1989). Young twigs often
support open communities with desiccation-tolerant taxa of Orthotrichaceae,
Frullania, and small Lejeuneaceae, whereas the lower trunk may become completely swathed in a carpet of more desiccation-sensitive Brachytheciaceae and
Hypnaceae. Phorophyte axes probably support a successional progression of
communities as they age, but most studies have inferred this from measurements made at only one time (Tewari et al. 1985, Stone 1989, Lara & Mazimpaka
1998). Direct studies of epiphyte successional dynamics are badly needed.
Obligate epiphytes mostly appear to be early successional species, whereas the
luxuriant climax communities of the trunk base are usually dominated by
facultative epiphytes (Smith 1982b, Bates et al. 1997).
Although a degree of ‘‘host specificity’’ is encountered among epiphyte communities, it is now clear that individual epiphytes respond to the nature of the
environment rather than ‘‘recognize’’ a particular phorophyte species (Palmer
1986, Schmitt & Slack 1990). Much ecological work has been directed at discovering the main environmental factors affecting epiphytic communities. Numerous
earlier data are brought together in the monumental Phytosociology and Ecology of
Cryptogamic Epiphytes (Barkman 1958), which may still be consulted with profit.
Sampling problems are also considered by Bates (1982a) and John & Dale (1995).
Major substratum factors influencing community composition include longevity
of the tree, rate of renewal of the bark surface, water-holding capacity of the bark,
and its acidity and nutrient content. Lifespan of the tree becomes important if one
likens it to an island that is progressively acquiring a flora. This concept has
mostly been discussed in the context of conservation of ‘‘old forest’’ taxa by
sympathetic forest management (Rose 1992). Trees with rapidly flaking or peeling
bark like many conifers, Eucalyptus and Betula will clearly only be able to support
rapidly establishing bryophytes with colonist and short-lived shuttle life-strategies. In dry climates a high water-holding capacity of the bark (e.g. as in Sambucus
nigra) may be critical in allowing some species to survive as epiphytes, but this
aspect has been little studied. Among trees with similar physical properties, bark
acidity assumes major importance in determining community composition
(Studlar 1982, Bates 1992b). Bark pH ranges from neutrality (e.g. Ulmus) to markedly acid (pH 3.5 or less in many conifers), but there is much intraspecific
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Fig. 8.8. Leaves bearing epiphyllous liverworts and lichens from tropical-montane forest, near
Ruhija, Bwindi Impenetrable Forest National Park, Uganda.
variation. Acidity and nutrient content of bark appear to be at least partially
influenced by soil conditions (Bates 1992b, Gustafsson & Eriksson 1995) as well
as by acid atmospheric pollutants, which can easily overwhelm the limited
buffering capacity (Farmer et al. 1991). Nutrients in precipitation, canopy leachate, and dust are likely to be the main sources for epiphytes, together with any
from decomposing bark (Bengstrom & Tweedie 1998, Hietz et al. 2002). Trees and
their epiphytic coverings may also be highly effective in scavenging aerosol
droplets from mists, especially in cloudy upland situations (Romero et al. 2006).
Luxuriant epiphytes must frequently have a significant effect on forest nutrient
dynamics (Rieley et al. 1979, Nadkarni 1984, Clark et al. 1998).
Epiphylls
In certain constantly humid forests bryophytes can colonize almost any
relatively stable surface. In these conditions some species (called epiphylls) are
capable of growing on the leaves of higher plants (Fig. 8.8). The phenomenon is
most noticeable in the tropics and subtropics where large-leaved evergreens are
prominent (e.g. Sjögren 1975, Pócs 1982). The most frequent epiphylls are tiny
leafy liverworts of the Lejeuneaceae, but larger taxa of Frullania, Plagiochila,
Radula and mosses frequently occur facultatively. Most of the specialist epiphylls are short-lived shuttle species (Table 8.2). Surprisingly, the most longlived leaves support the lightest epiphyllous coverings and possibly these have
adaptations that inhibit epiphyll growth (Coley et al. 1993). Following a long
8 Mineral nutrition and substratum ecology
debate, it is generally agreed that epiphylls do not significantly reduce the
photosynthetic output of host leaves. Coverings of epiphylls may actually
deter herbivores but colonization by fungal pathogens is probably increased.
Little is known about their nutrient relationships; however, Berrie & Eze (1975)
showed movement of water and phosphate from host leaves to the epiphyllous
liverwort Radula flaccida. Some of the rhizoids of R. flaccida were observed to
penetrate the host’s cuticle and contact the walls of epidermal and mesophyll
cells. This does not appear to be an instance of outright parasitism, however, as
no transfer of photosynthate was detected (Eze & Berrie 1977). The epiphyll–
host relationship evidently merits fuller investigation.
Epiliths
Bryophytes inhabiting rocks have received less attention than epiphytes
(Smith 1982b). Once again it is convenient to recognize ‘‘obligate’’ and ‘‘facultative’’ types, the genera Gymnomitrion, Marsupella, Andreaea, Grimmia, and Racomitrium
containing many obligate epiliths. Such species possibly require a considerably
more permanent and less water-retentive substratum than is provided by bark,
but the reasons for their substratum selection are not well understood. Their
competitive exclusion from more benign habitats on other substrata by fastergrowing species is probably a factor. Bates et al. (1997) speculated that reduced
competition, following atmospheric pollution, accounted for occurrences as epiphytes of normally epilithic bryophytes in parts of southern Britain. However, the
balance between precipitation amounts and water-holding capacity of bark may
also be important, with bark in drier areas being best able to support epiliths (Bates
et al. 2004). Aho & Weaver (2006) present some useful ideas on methods for
studying water relations and acidity on rock surfaces.
Most work on epiliths has aimed at delimiting the niches of species. Alpert
(1985, 1988) studied the ability of Grimmia laevigata to colonize xeric microsites
on rock surfaces. These were not colonized naturally, but adult plants transplanted to xeric sites survived without impairment, suggesting that a greater
desiccation-sensitivity of the establishment phase limits a wider distribution.
Jonsgard & Birks (1993) and Heegaard (1997) investigated the physical and
chemical niches of Racomitrium and Andreaea species, respectively, in western
Norway, using multivariate analyses and generalized linear modeling methods.
Litter species
Litter, meaning undecomposed dead plants, constitutes substrata
ranging from the ephemeral (leaves) to the reasonably long-lasting (fallen tree
trunks). All are potentially rich in plant nutrients although this may often be
unavailable to bryophytes.
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It is now evident that several bryophytes originally thought of as normal
inhabitants of the soil surface are, at least seasonally, exploiters of litter deposited by dominant vascular plants. Rincón (1988) investigated the effects of a
range of plant litter types on growth of some common grassland bryophytes.
Nutrient-rich litter of the stinging nettle (Urtica dioica) stimulated the growth of
all species and notably that of Brachythecium rutabulum, a moss that is frequently
associated with the dense stands of U. dioica and other tall herbs. Rhizoidal
attachments to the litter are important in nutrient exploitation (Rincón 1990).
A number of bryophytes, sometimes called epixylic species, occur more often on
rotting logs than on other types of substratum. Most studies have been concerned
with description of the succession of their bryophyte communities as fallen logs
and cut stumps decay (Muhle & LeBlanc 1975). These go through a number of
physical changes, such as loss of bark, softening of the wood, and break-up, and
they may present a moister environment in later stages than initially. In a
Swedish spruce forest Söderström (1988) recognized four stages in the succession:
(1) facultative epiphytes that had fallen with the log (mostly lichens and Ptilidium
pulcherrimum); (2) early epixylics (Anastrophyllum hellerianum, Lophozia spp.,
Drepanocladus unciniatus, Cladonia lichens) colonize soon after the log falls; (3) late
epixylics (e.g. Lepidozia reptans, Brachythecium starkei, Dicranum scoparium,
Plagiothecium denticulatum) do not colonize until decay is advanced; (4) ground
flora species (e.g. Hylocomium splendens, Pleurozium schreberi, Ptilidium crista-castrensis)
colonize as the log becomes indistinguishable. No evidence appears to have been
obtained of mineral nutrient transfers from rotting logs to bryophytes. As some of
the commonest species (e.g. Brachythecium rutabulum, Eurhynchium praelongum) also
exploit leaf litter, however, this seems highly likely. Saprotrophic fungi could be
involved in cryptic nutrient transfers (cf. Wells & Boddy 1995).
Decaying logs provide a classic example of a patchily distributed habitat of
limited duration and their specialist bryophytes present opportunities to test
several hypotheses in population biology (e.g. Herben & Söderström 1992).
Kimmerer (1994) compared the dissemination of Dicranum flagellare, an asexually
reproducing species, with Tetraphis pellucida, which produces both spores and
gemmae. Tetraphis pellucida was highly successful at rapidly colonizing new logs
and stumps, whereas D. flagellare persisted mainly by rapidly colonizing local
gaps appearing through disturbance rather than by finding wholly new surfaces. Slugs appeared to be a major dispersal vector for the detachable branches
of D. flagellare (Kimmerer & Young 1995).
Fire mosses
Fire is a natural event in many forest and grassland ecosystems but
today humans are also responsible for a very large number of accidental and
8 Mineral nutrition and substratum ecology
deliberately started fires. These range from small bonfires, through rejuvenating ‘‘burns’’ (e.g. of moor and scrub) to conflagrations that engulf wildlife over
vast areas of countryside. Bryophytes are usually readily destroyed in fires, but
they are often a conspicuous element in the early succession on burned land.
Southorn (1976) pointed out that Funaria hygrometrica is associated with old fire
sites throughout the world. At seven experimental bonfire sites in Surrey
(England) she first observed bryophyte protonemata nine weeks after burning
in spring-burnt sites but only after 25 weeks when burning was carried out in
winter. Eventually a community composed of F. hygrometrica, Ceratodon purpureus, Bryum argenteum, and tuberous Bryum spp. became established in the first
year after burning. This pioneer community was progressively deposed by
recolonizing angiosperms in the second year, and bryophytes had vanished by
the third year. In burnt Picea mariana forests in Labrador, Foster (1985) also
recorded F. hygrometrica and Ceratodon purpureus as colonists of charred unstable
surfaces, together with Polytrichum juniperinum. These were gradually replaced by
normal forest mosses like Pleurozium schreberi, Ptilium crista-castrensis, and
Hylocomium splendens when the tree cover had re-established, enabling light
intensities to decrease and atmospheric humidity to increase. Bell &
Newmaster (2002) and Newmaster et al. (2003), working in western Canadian
forests, observed wide variations in the temperatures of wildfires and the degree
to which the original bryophyte vegetation survived. Southorn (1976) demonstrated that under hot bonfires and slow forest fires the soil is greatly changed.
Organic matter in the soils is burnt off and much soluble inorganic matter is
deposited as ash, including the plant nutrients K, Mg, Ca, and P. The bases cause
a dramatic rise in pH (up to 10.1 units in the Surrey bonfires). From culture
experiments Southorn (1977) concluded that a requirement of F. hygrometrica for
relatively high concentrations of nitrate-N and P was a major reason for its
success on bonfire sites. Brown (1982), however, deduced that the raised pH
may also be critical. The lag in colonization mentioned above was probably due
to the presence in the ash of large quantities of ammonium-N, which was found
in culture work (Southorn 1977, Dietert 1979) to be detrimental to growth.
Detoxification of this by leaching and the action of nitrifying micro-organisms
appears to be a prerequisite for colonization by F. hygrometrica. Southorn (1977)
speculated that soluble organic toxins in ash might be responsible for delaying
the colonization by vascular plants that enables F. hygrometrica to flourish in the
first year. Brasell et al. (1986) reported high rates of nitrogen fixation from
bryophyte/soil cores taken from Eucalyptus forest fire sites in Tasmania that are
presumably a result of microbial activity.
Fast litter fires of grassland and heathland cause much less damage to the
original vegetation and alter soil conditions comparatively little, and regrowth
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may occur from surviving underground parts. Following heathland fires in
Scotland, Hobbs & Gimingham (1984) found that much variation in the pattern
of recovery reflected the varying diversities of the preburn communities. The
latter was determined partly by compositional differences during the heather
(Calluna vulgaris) growth cycle. A bryophyte-dominated early recovery phase
(Campylopus paradoxus, Ceratodon purpureus, Polytrichum juniperinum, P. piliferum)
was obtained when heather stands in the ‘‘pioneer’’ and ‘‘building’’ stages were
burnt. However, the pleurocarpous mosses Hylocomium splendens, Hypnum jutlandicum and Pleurozium schreberi also regrew quickly from partly combusted mats in
older stands in some cases.
Under conditions of acute drought heath fires may ignite the underlying peat
with much more serious consequences for the preburn vegetation (Clément &
Touffet 1990, Maltby et al. 1990, Gloaguen 1990). Here a bonfire type of succession
is initiated; however, the poor conditions and lack of propagules can retard higher
plant recolonization for ten years or more. On the North York Moors (England) this
was mainly due to droughting of the Calluna seedlings (Legg et al. 1992), but after
some fires colonization by the invasive southern hemisphere moss Campylopus
introflexus prevented Calluna regeneration (Equihua & Usher 1993).
Dung and cadaver mosses
Dung and the decomposing corpses of animals are sometimes colonized
by a distinctive group of coprophilous bryophytes. Obligate coprophiles are
restricted to the moss family Splachnaceae. Coprophiles are most frequent in
otherwise nutrient-poor environments such as ombrotrophic mires, moors, and
alpine and polar tundras. Among the commoner genera Splachnum is favoured by
wetter ground conditions than Tetraplodon. In north Wales Tetraplodon mnioides is
most abundant beneath dangerous mountain crags where there is a steady
supply of the carcases of unfortunate sheep (Hill 1988). Under ideal conditions
these mosses are highly successful so that in central Alberta uncolonized droppings are rare (Marino 1997). Useful comments on substratum preferences of
individual Splachnaceae are given in Smith (1982a).
It is likely that these mosses are exploiting a rich nutrient source but surprisingly little appears to have been published on the specific nutrient requirements of the Splachnaceae. Some Tayloria species like T. lingulata are not
coprophilous but grow in basic flushes. This may indicate a general high base
requirement in members of the family. Those that grow on the pellets of birds of
prey and carcases may endure when only the bones remain, probably indicating a high phosphorus requirement. However, in a laboratory experiment no
difference was found in the abilities of dung- and bone-inhabiting species to
grow on moose (herbivore) and wolf (carnivore) dung (Marino 1991a). Marino
8 Mineral nutrition and substratum ecology
Fig. 8.9. The curious capsules of Splachnum luteum Hedw., one of the so-called ‘‘dung mosses’’
that are habitat specialists on decaying animal remains.
(1997) suggested that moose droppings may lose nutrients quicker than wolf
dung under field conditions by leaching. The latter author also marshaled
evidence suggesting that high pH is not always characteristic of dung and
carcases, thus weakening an earlier hypothesis of Cameron & Wyatt (1989).
One of the essential traits of coprophilous mosses is their entomophilous
behavior: a dependence on insects for spore dispersal (Koponen & Koponen
1978). The sporophyte of coprophiles is highly adapted with some flower-like
properties that appear to lure dung-flies (Koponen 1978, Cameron & Troili 1982).
The seta is long and often unusually thick, and the capsule is usually brightly
colored: red in Splachnum rubrum; yellow in S. luteum; purplish in S. ampullaceum
and Tetraplodon mnioides. Its apophysis region is swollen and in some cases (e.g., S.
luteum) it is drawn out radially into a disk-like structure (Fig. 8.9). Dung-flies are
also believed to be attracted by the emission of volatile attractants by the
capsule. A range of volatile octane derivatives, organic acids, aldehydes,
ketones, and alcohols has been identified but it is not known which are active
(Pyysalo et al. 1983). The spores are sticky and readily dispersed by the flies to
fresh dung or corpses.
The substrata colonized by Splachnaceae represent spectacularly small and
short-lived targets for spore dispersal, but they possess a highly focused
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dispersal mechanism. Commonly, several Splachnaceae will colonize a single
dung patch and a competitive struggle may ensue (Marino 1991a). Differences in
spore maturation dates of species and the types of fly vector, however, probably
enable several coprophiles to coexist in an area (Marino 1991b). A successional
sequence may be observed with members of the Splachnaceae colonizing first,
followed by less specialized colonists like Ceratodon purpureus, Bryum spp., and
Pohlia spp., and finishing with common pleurocarpous mosses of the surrounding community (e.g. Webster & Sharp 1973, Lloret 1991). Marino (1997) has
summarized what is currently known about the competitive hierarchies and
population dynamics of these highly specialized and fascinating mosses.
In some countries Splachnaceae are noticeably much rarer today than in the
first half of the twentieth century. Discussing reasons why Splachnum ampullaceum had become rare in lowland Britain, Crundwell (1994) concluded that
widespread land drainage was to blame, and this may indeed be a contributory
factor. Ironically, however, the main reason is likely to be an insidious, and
equally well-targeted, destruction of the dung-flies that disperse Splachnaceae
spores by modern pesticides, especially ivermectins (D. A. Holyoak, pers.
comm.), although this requires confirmation in specific instances. These chemicals are widely used to treat horses, cattle, and sheep against a range of internal
and external parasites. They are excreted in the dung and destroy flies and other
invertebrates that feed upon it (Wall & Strong 1987, Strong & Wall 1988, 1994,
Strong et al. 1996). Here is a classic instance of a conflict between the interests of
bryophytes (and bryologists) on the one hand, and progress in animal welfare
and agriculture on the other, for conservationists to resolve!
Calcicoles and calcifuges
The distinction between calcicole (‘‘calcium-loving’’) and calcifuge
(‘‘calcium-hating’’) species can be the principal dichotomy in a regional bryophyte flora (e.g. Bates 1995). Calcicoles are restricted to rocks and soils containing calcium carbonate, or inhabit waters that have flowed over or percolated
through these substrata. Some calcicoles also occur on the least acid types of
tree bark. Calcifuges live on substrata with an acid reaction, or in soft waters.
Many bryophytes are apparently indifferent to the acidity of their substratum
(e.g. the common grassland mosses Pseudoscleropodium purum and Rhytidiadelphus
squarrosus) whereas others may need near neutral conditions (‘‘neutrocline’’
taxa). Much less is known about the specific adaptations of calcicole and calcifuge bryophytes than their vascular plant equivalents. We may suspect that
aluminum and iron, if present in the substratum, will be relatively mobile
under acid conditions, but become extremely immobile under mildly alkaline
conditions. This is partly supported by analyses of bryophytes growing on
8 Mineral nutrition and substratum ecology
Table 8.3. The cation exchange capacity in a range of epilithic calcicole and calcifuge
mosses from western England and south Wales
Values were determined by using unbuffered CaCl2 solution (25 mM) to saturate the exchange
sites and SrCl2 solution (25 mM) to elute the adsorbed Ca2þ ions. Values are means of three
replicates and the estimated 95% confidence interval.
Rock
Ca adsorbed (mg g
Ctenidium molluscum
Carboniferous limestone
15510 3497
Homalothecium sericeum
Carboniferous limestone
12460 319
Orthotrichum cupulatum
Carboniferous limestone
12250 1382
Schistidium apocarpum
Carboniferous limestone
12940 955
Tortella tortuosa
Carboniferous limestone
15160 679
Tortula ruralis
Carboniferous limestone
1
dry wt)
Calcicoles
10160 684
Mean 13080
Calcifuges
Andreaea rothii
Granite
2660 124
Dicranoweisia cirrata
Old Red Sandstone
3200 287
Grimmia donniana
Vitrified lead slag
2610 114
Ptychomitrium polyphyllum
Old Red Sandstone
6690 160
Racomitrium fasciculare
Old Red Sandstone
3330 287
Racomitrium lanuginosum
Old Red Sandstone
2330 287
Mean
3470
From Bates 1982b.
contrasted rock types in Scotland. A selection of calcifuges, and notably Andreaea
rothii, contained large concentrations of Fe, whereas the calcicoles contained up
to 17 times more Ca (Bates 1978, 1982b). The highest Al concentrations were also
found in A. rothii, but concentrations of this element were not consistently
higher in calcifuges than in calcicoles.
The differences in total metal concentrations correlate with marked differences in CEC of calcicole and calcifuge bryophytes (Bates 1982b). Among epiliths, CEC is 3–4 times higher in calcicoles than calcifuges (Table 8.3). Following
experiments using EDTA to remove Ca2þ from the tissues, Bates (1982b)
hypothesized that calcicoles had inherently leakier cell membranes than calcifuges. The elevated CEC of calcicoles was hypothesized to be necessary to ensure
adequate Ca2þ adsorption for permeability control. Working with bryophytes of
woodland soils, Büscher et al. (1990) found similar differentiation of CEC
between calcifuge and calcicole species but reached a different conclusion. In
laboratory experiments they investigated the selectivity of ion adsorption onto
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J. W. Bates
the cation-exchanger from mixtures of cations resembling soil solutions. They
concluded that lower CEC in calcifuge mosses was an adaptation allowing
avoidance of high Al3þ uptake, as plants with low CEC absorbed relatively less
Al3þ from a mixed Al–Fe–Mn–Ca solution than those with high CEC. Although
excessive Fe has been shown to be toxic to the calcicole bryophyte Fissidens
cristatus (Woollon 1975), we still know very little about the susceptibilities of
bryophytes to elevated Al3þ. Indeed, the ombrotrophic peatland environments
favored by many Sphagnum spp. may often be acid but contain relatively little
available Al3þ, which possibly explains the high CECs found in this genus.
By analogy with vascular plants, we may expect bryophytes to encounter Fedeficiency in calcareous habitats. Structures analogous to the rhizodermal
transfer cells of dicotyledonous calcicoles (e.g. Marschner 1986) have not yet
been demonstrated in calcicole bryophytes but physiological adaptations to
improve Fe-mobility from the substratum are likely to be present.
Importantly, calcium status, when isolated from variables like pH, appears to
be relatively unimportant to bryophytes. Calliergonella cuspidata, a common moss
of chalk downland and calcareous fen, shows a strong preference for pH values
around neutrality and will not grow below pH 6 even if the calcium concentration is increased (Streeter 1970). Clymo (1973) demonstrated that high calcium
concentrations were relatively harmless to most Sphagnum spp., as were high pH
values, but the combination of high pH and high Ca proved to be lethal to all
taxa except those characteristic of base-rich flushes (e.g. S. squarrosum).
Hummock species like S. capillifolium are the most susceptible to these conditions. Similar conclusions were drawn by Vanderpoorten & Klein (1999) based
on field measurements of water chemistry and distribution patterns of some
common aquatic bryophytes in waterfalls of the River Rhine. The putative
calcifuges Marsupella emarginata and Scapania undulata only grew in waters with
low solute content, but were relatively indifferent to pH. Conversely, the ‘‘calcicoles’’ Chiloscyphus polyanthos, Cratoneuron filicinum, Rhynchostegium riparioides, and
Thamnobryum alopecurum usually occurred in base-rich water but they were also
found when Ca2þ concentration was low. Although relatively indifferent to
calcium status, these species are all strongly intolerant of low pH.
Building on recent studies of organic acid metabolism, Lee (1999) has proposed
a general model for vascular plants in which ungating of channel proteins,
permitting release of malate and citrate anions, is provided by Al3þ in calcifuges
and by Ca2þ in calcicoles. In the soil solution these anions either precipitate Al3þ
and thus ameliorate its toxicity (acid conditions), or they chelate Fe3þ and promote its uptake (alkaline conditions). The main tenets of Lee’s model (see also
Roberts 2006) are consistent with many of the foregoing observations; however,
much further work is needed to validate it generally for bryophytes.
8 Mineral nutrition and substratum ecology
Halophytes
No bryophytes live permanently submerged in the oceans although the
aquatic moss Fontinalis dalecarlica is able to grow in the northern Baltic Sea owing
to its low salinity (Söderlund et al. 1988). On land very few species are true
halophytes. Even in coastal dunes where deposition of saltwater spray is likely,
Boerner & Forman (1975) found that none of the beach mosses survived a spray
treatment with natural seawater. They concluded that survival in nature
depended on dilution of the incoming salt before it contacted the mosses. In
British saltmarshes, Adam (1976) recorded 66 bryophyte taxa living in situations
where at least occasional tidal immersion would be experienced. Most of these
species are widely distributed in non-saline habitats and it was suggested that
some may represent halophytic ecotypes, but many probably experience relatively low salinities, which are less harmful than full oceanic strength seawater.
A few bryophytes occur in association with inland salt deposits (Zechmeister
2005). One of the best-known coastal halophytes is Schistidium maritimum (syn.
Grimmia maritima) which grows in the splash zone on non-calcareous seashore
rocks (and occasionally on stones in saltmarshes) on shores around the
Northern Atlantic (Fig. 8.10). On very sheltered shores it may be immersed by
the highest spring tides. It is commonly accompanied by an epilithic form
of Ulota phyllantha and Tortella flavovirens, which also appear to be highly salttolerant (Bates 1975).
Fig. 8.10. Dark cushions of the halophytic moss Schistidium maritimum growing with
lichens of the ‘‘splash zone’’ of a rocky seashore at Montrose, northeast Scotland
(photo M. C. F. Proctor).
339
J. W. Bates
0.70
0.60
0.50
Fv / Fm
340
0.40
0.30
0.20
0.10
0.00
0
50
100
150
200
Time since w etting (min)
250
300
Fig. 8.11. Recovery of quantum efficiency (Fv/Fm) in Schistidium maritimum following
rehydration in different dilutions of artificial seawater. Sizes of squares represent dilution (0,
25, 50, 75 or 100% seawater): smallest ¼ 0% (distilled water), largest ¼ 100% artificial seawater.
Data are means and standard errors of three replicate determinations. Material: exposed
granite seashore rocks, Cap de Flamanville, Manche, France. Treatment: material was air dried
at room temperature for two weeks and then stored over saturated NaOH (6% R.H.) for five days
prior to rehydration in the stated seawater dilution. Measurements of quantum efficiency were
made with a Hansatech FMS1 fluorometer. See Bates & Brown (1974) for artificial seawater
recipe. (X.-Y. Phoon & J. W. Bates, unpublished data.)
Salt tolerance in S. maritimum appears to depend principally on the exclusion of
salt by means of a markedly impermeable cell membrane. There is also some
evidence for the existence of a metabolically active Naþ efflux pump (Bates 1976).
In contrast, glycophytic mosses like Grimmia pulvinata suffer a major loss of cell Kþ
and influx of Naþ if confronted with seawater (Bates & Brown 1974). This increased
permeability in G. pulvinata is probably caused by Naþ ions in the seawater competing
with and displacing Ca2þ ions that normally stabilize the polar heads of the membrane lipids. Schistidium maritimum withstands the normal ratio of Ca : Na in seawater
but if this is experimentally lowered it also suffers some K-loss and Na-entry.
The simple ‘‘salt exclusion’’ mechanism of salt tolerance operating in
S. maritimum should make it highly susceptible to osmotic water loss (‘‘physiological drought’’) to the salty external solution. Indeed, most cushions of this
moss can be demonstrated to contain appreciable quantities of sea salt. Except
during periods of heavy rainfall, one imagines that full turgor of the cells is
constantly challenged by outward osmosis. Laboratory measurements of chlorophyll fluorescence of this species in a range of seawater dilutions (Fig. 8.11)
show that the higher external salinities are indeed inhibitory to quantum
8 Mineral nutrition and substratum ecology
efficiency (Fv/Fm), whereas lower salinities (25%, 50% seawater) are stimulatory.
Schistidium maritimum is also highly desiccation-tolerant and it probably frequently
avoids the consequences of low external solute potentials by entering a metabolically inactive dehydrated state, something that vascular halophytes cannot do.
These observations may explain why S. maritimum does not extend very far southwards on the Atlantic coast of Europe and also why it appears to luxuriate in
rainier climates and on shores where there is some freshwater seepage.
Metallophytes
Some bryophytes are demonstrably ‘‘metal-tolerant’’, being able to
withstand levels of heavy metals that are toxic to other species. One famous
group of species is known as the copper mosses. These (e.g. Grimmia atrata,
Mielichhoferia spp., Scopelophila cataractae) generally occur on rocks rich in copper
sulfide and may be of some use in prospecting for copper ore. It is doubtful that
copper mosses have a definite nutritional requirement for Cu, but quite likely
that they are extremely poor competitors with an unusually high tolerance of
Cu and/or its associated sulfide-generated acidity (Brown 1982). Metal-tolerant
populations have also been recognized in some wide-ranging bryophytes (e.g.
Marchantia polymorpha, Solenostoma crenulata, Ceratodon purpureus, Funaria hygrometrica; see Jules & Shaw 1994) but the underlying physiological mechanisms
remain obscure and require further investigation (Shaw 1994).
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9
The structure and function
of bryophyte-dominated peatlands
d a l e h . v i t t a n d r . k e lm a n w i e d e r
9.1
Introduction
Peatlands are unbalanced ecosystems where plant production exceeds
decomposition of organic material. As a result, considerable quantities of organic
material, or peat, accumulate over long periods of time: millennia. This organic
material is composed primarily of plant fragments remaining after partial
decomposition of the plants that at one time lived on the surface of the peatland. Decomposition occurs through the action of micro-organisms that have
the ability to utilize dead plant components as sources of carbon for respiration
(Thormann & Bayley 1997) in both the upper, aerobic peat column (the acrotelm) and the lower, anaerobic peat (the catotelm) (Ingram 1978, Clymo 1984,
Wieder et al. 1990, Kuhry & Vitt 1996). Labile cell contents, cellulose, and
hemicellulose are more readily available sources of carbon than recalcitrant
fractions that contain lignin-like compounds, with these latter compounds
being concentrated in peat by decomposition (Williams et al. 1998, Turetsky
et al. 2000). The vascular plant-dominated, tree, shrub, and herb layers produce
less biomass (Campbell et al. 2000) and decompose more readily than the bryophyte-dominated ground layer (Moore 1989). Surfaces of northern peatlands are
almost always completely covered by a continuous mat of moss (National
Wetlands Working Group 1988, Vitt 1990), and the large amount of biomass
contained in this layer is composed of cell wall material that decomposes slowly.
This slow decomposition, coupled with water-saturated, anaerobic conditions
in the peat, cool climate, and a cool moist growing season conducive to bryophyte growth, allows organic matter to accumulate over large areas. In northern
peatlands, the peat that accumulates is generally composed of a high percentage
of material derived from bryophytes.
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
358
D. H. Vitt and R. K. Wieder
9.2
Structure and peatland types
Wetlands are, in general, ecosystems that have accumulated some
organic matter and have an abundance of hydrophytic vegetation. They can
be divided into five basic types, three of which are non-peat forming systems
that are often defined as areas with less than 40 cm of peat (Zoltai & Vitt 1995).
These three non-peat-forming wetland types may have a well-developed tree
or shrub layer (swamps), be dominated by sedges, grasses, and rushes without
trees and shrubs (marshes), or contain emergent vegetation in less than a
meter of water (shallow open water) (National Wetlands Working Group
1988, Zoltai & Vitt 1995). All of these wetland types have seasonally fluctuating
water tables that are strongly influenced by surrounding surface and ground
waters (Zoltai & Vitt 1995, Vitt 2006). Nitrogen mineralization rates are high
(Bridgham et al. 1998) and surface inflows may be nutrient-enriched, so that
these wetlands are often eutrophic (Mitch & Gosselink 1993) (Fig. 9.1). The lack
of a well-developed bryophyte-dominated ground layer, coupled with abundant vascular plant litter, allows relatively rapid decomposition and results in
little peat accumulation (Thormann et al. 1999). Peat-forming wetlands (often
termed ‘‘mires’’ in Europe and ‘‘peatlands’’ in North America) are ecosystems
that accumulate organic matter. Although only two basic types of peatlands
have generally been recognized (bogs and fens), peatlands can be more precisely defined by using a combination of hydrologic, chemical, and floristic
criteria (Zoltai & Vitt 1995).
9.2.1
Hydrology
Peatlands that derive their water and nutrient supplies from precipitation and from water that has been in contact with upland soils are termed fens.
Water flows through fens via one to several inflows and outflows (Fig. 9.2). The
chemistry of surrounding upland soil water, and/or groundwater, influences
the water chemistry of fens (Siegel & Glaser 1987) and often causes them to be
relatively rich in base cations. However, if the surrounding uplands are relatively acidic, the fens may be poor in base cations (Halsey et al. 1997a,b).
Peatlands that derive their water and nutrient supplies solely from precipitation are termed bogs. These peatlands are somewhat elevated above the surrounding area, such that water flows from the raised bog surface on to the
surrounding wetland or upland (Fig. 9.2). Therefore, bogs have relatively stagnant waters that do not reflect the surrounding soil conditions. For this reason,
the chemistry of the precipitation has the most important influence on
the chemistry of the bog waters (Malmer 1962, Vitt et al. 1990, Malmer et al.
1992). If hydrology is considered the most significant criterion for peatland
9 Bryophyte-dominated peatlands
Fig. 9.1. Ternary diagram showing five wetland classes in relation to hydrology, chemistry, and
vegetation. Modified from Vitt (1994) and Zoltai & Vitt (1995).
classification, then the primary division of these ecosystems is ombrogenous
bogs and geogenous fens. Bogs can be viewed as ecosystems that are oligotrophic
with ombrotrophic vegetation and fens are ecosystems that may be either
oligotrophic or mesotrophic and are dominated by minerotrophic vegetation.
9.2.2
Chemistry
In the 1940s, Einar DuReitz recognized that Scandinavian peatlands
could be divided into several types based on vegetation structure and floristic
species composition (DuReitz 1949). He recognized that some peatlands have a
large number of plant species with high fidelity to particular site conditions. The
fens that were ‘‘rich’’ in floristic site indicators he called rich fens. Other fens
had fewer species with high fidelity and he called these poor fens. He recognized
that ombrotrophic bogs had no, or very few, plant species that were exclusive to
bog conditions.
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D. H. Vitt and R. K. Wieder
Fig. 9.2. Aerial view of two Sphagnum-dominated peatlands from northeastern Alberta,
Canada. The large peatland on the left is a continental bog wooded with scattered Picea
mariana, surrounded by a narrow fen border (lagg) where inflow water to the basin is channeled.
The peatland on the right represents a patterned fen, with strings and flarks oriented
perpendicular to waterflow. Outflows for both peatlands are present at the top of
the photo.
In the 1950s, Hugo Sjörs published two classic papers that related pH and
electrical conductivity of the surface waters to the floristic types described by
DuReitz. Sjörs (1950, 1952) described pH and ‘‘corrected’’ conductivity gradients
(the latter calculated by subtracting conductivity due to hydrogen ions and
serving as a surrogate for base cation abundance) that ranged from acidic, low
conductivity in bogs through somewhat less acidic poor fens to basic, high
conductivity in waters of rich fens. He proposed that rich fens could be subdivided into two types: moderate- (transitional) rich fens and extreme-rich fens.
Further work by a number of researchers has carefully characterized these four
peatland types (bogs, poor fens, moderate-rich fens, extreme-rich fens) in terms
of both chemistry and vegetation (e.g. Gorham 1956, Slack et al. 1980, Malmer
1986, Vitt & Chee 1990, Gorham & Janssens 1992, Vitt et al. 1995a).
In general, peatland surface water pH is in the range 3.0–4.2 in bogs, 4.2–5.5
in poor fens, 5.5–7.0 in moderate-rich fens, and 7.0–8.0 or higher in extreme-rich
fens (reviewed in Vitt 1990). Associated with this acidity gradient is one
of alkalinity, with bogs and poor fens having no alkalinity, moderate-rich
fens having some alkalinity (500–1000 meq l 1 of CaCO3) and extreme-rich
fens having highly alkaline waters to the extent that CaCO3 may be deposited
as marl (Vitt et al. 1995b). Along these acidity/alkalinity gradients, base cation
9 Bryophyte-dominated peatlands
(Ca2þ; Mg2þ; Naþ; Kþ) concentrations in peatland surface waters increase.
Typically, surface water concentrations of Ca2þ are less than 3 mg l 1 in bogs,
around 5 mg l 1 in poor fens, and from 5 to 35 mg l 1 or more in rich fens (Fig. 9.3).
However, concentrations of potentially limiting nutrients (dissolved inorganic
forms of N and P) (Walbridge & Navaratnam 2006) are highly variable and show
little correlation with the defining chemical gradients of acidity, alkalinity, and
base cations (Fig. 9.3). Chemically, poor fens are more similar to bogs than they
are to rich fens. Thus, when surface water chemical characteristics are considered, the critical division is between systems that are acidic and possess no
alkalinity (poor fens and bogs) and systems that are neutral to basic and alkaline
(rich fens).
At the regional scale, surface water sampling of over 100 peatlands reveals a
clearly bimodal pH distribution: bogs and poor fens with pH less than about 5.0
form one group and rich fens with pH greater than about 6.0 form a second
group (Fig. 9.4). Peatlands with intermediate surface water pH values between
5.2 and 5.7 can be rare on the northern landscape (e.g. Glaser et al. 2004);
however, there are other regions where this gap is not so apparent (Glaser
1992b). As surface water pH increases within this narrow pH range, alkalinity
becomes established as a key chemical characteristic (Vitt et al. 1995a).
9.2.3
Vegetation and flora
In terms of physiognomy, peatlands vary considerably. Bogs are relatively dry and have a relatively thick acrotelm (aerobic layer), and a large
percentage of their area is covered by hummocks; they may be wooded, shrubdominated, or completely without trees (open) (Glaser & Janssens 1986, Belland &
Vitt 1995). Generally, maritime bogs are open, often contain a sedge component
on lawns (see Table 9.1 for definitions), and contain pools of water (which may
be arranged in reticulate or parallel patterns), whereas continental bogs are
wooded, have almost no sedges, and have no open water (Damman 1979, Glaser &
Janssens 1986, Davis & Anderson 1991, Vitt et al. 1994). Bogs are always dominated by Sphagnum mosses (or feather mosses and lichens), almost exclusively
lack a sedge component, and often have abundant shrubs (Glaser 1992a,
Belland & Vitt 1995). Poor and rich fens are relatively wet, have a thin acrotelm,
and have a higher percentage of their area covered by lawns and carpets (Vitt
1990). Pools are sometimes present (Vitt et al. 1975). These fens may exhibit
surface patterning of reticulate or parallel arrangements of raised, dry, elongate
strings separated by pools (flarks) of water often filled with carpets of moss
(Fig. 9.2) (Foster et al. 1983, Halsey et al. 1997b). Fens are usually sedge-dominated.
They may be wooded, shrubby, or open (Vitt & Chee 1990, Halsey et al. 1997b).
Poor fens are dominated by Sphagnum moss and ericaceous shrubs may be
361
D. H. Vitt and R. K. Wieder
Reduced conductivity
2.5
Slope = 0.01
r 2 = 0.97
A
40
Ammonium
(µg l–1)
Alkalinity
(meq l–1)
2.0
pH
50
1.5
1.0
0.5
Slope = 3.13
r 2 = 0.12
D
Slope = 0.86
r 2 = 0.16
E
30
20
10
0
14
0.0
Slope = 0.01
r 2 = 0.97
30
B
12
Nitrate
(µg l–1)
Calcium
(mg l–1)
10
20
10
8
6
4
2
0
8.0
0
7.0
C
Soluble reactive
phosphorus (µg l–1)
Slope = 3.18*log
r 2 = 0.68
6.0
pH
362
5.0
BOG
POOR FEN
4.0
3.0
FMR
OMRF
ERF
0
50
100
150
200
250
200
Slope = 12.42 F
r 2 = 0.04
150
100
50
0
3.0
4.0
5.0
6.0
7.0
8.0
Fig. 9.3. Relationship between reduced conductivity (mS cm 1) and (A) calcium, (B) alkalinity,
and (C) pH, and between pH and the nutrients (D) ammonium, (E) nitrate, and (F) soluble
reactive phosphorus for surface waters along the bog–rich fen gradient. Open symbols include
bogs and poor fens; closed symbols include several rich fens. Modified from Vitt et al. (1995a).
Reduced conductivity (often termed corrected conductivity) is the total electrical conductivity
minus that supplied by Hþ (Sjörs 1952). (Reprinted with permission from the National Research
Council Press/Canadian Journal of Fisheries and Aquatic Sciences, Vol. 52, 1995, Seasonal variation in
water chemistry over a bog-rich fen gradient in continental western Canada, by Dale H. Vitt,
Suzanne E. Bayley, and Tai-Long Jin, Figs. 16 and 17, p. 602.)
present; furthermore, they differ from bogs by the appearance of a few rare fen
indicators with high fidelity to poor fens (i.e. species of Juncus and Carex). ‘‘Brown
mosses’’ dominate moderate- and extreme-rich fens, and ericaceous shrubs are
sparse or absent (Vitt 1990); rich fens have relatively high numbers of indicator
species. Vascular plant indicator species of these peatland types are regionally
9 Bryophyte-dominated peatlands
50
Bogs
Rich f ens
P oor fens
Number of sites
40
30
20
10
0
3
3.5
4
4.5
5
5.5
pH
6
6.5
7
7.5
8
Fig. 9.4. Histogram of pH and peatland type. There are relatively few sites that have surface
water pH between 5.2 and 5.7, when alkalinity values approach zero. Data for sites (n ¼ 100)
from continental western Canada.
based; however, the broad ranges of bryophytes coupled with their sensitivity to
nutrient, acidity/alkalinity gradients, and water levels make bryophytes nearly
perfect sensitive indicators of peatland conditions (Table 9.1).
In summary, when bogs, poor fens, and rich fens are compared floristically
through multivariate techniques (e.g. Nicholson et al. 1996, Gignac et al. 1998),
bogs and poor fens are generally more similar to each other than are poor fens
and rich fens. Any of these three peatland types may be wooded, shrubby, or
totally without trees (Glaser 1992a, Belland & Vitt 1995, Halsey et al. 1997b).
Bogs, especially continental ones, differ from fens in their general lack of sedges
(Glaser 1992a, Belland & Vitt 1995). Bogs and poor fens are Sphagnum-dominated;
rich fens are brown moss-dominated. In oceanic areas, bogs may be patterned,
whereas fens tend to be patterned more frequently in more continental areas.
Bogs have water flowing away from their centers, but fens have water flowing
through the system. Bogs have a well-developed acrotelm and are drier, whereas
fens of all types have a poorly developed acrotelm and are wetter (Vitt et al.
1994). The dominance of Sphagnum in poor fens and bogs and lack of it in rich
fens correlates well with acidity/alkalinity criteria (compare open symbols:
Sphagnum-dominated peatlands, with closed symbols: brown moss-dominated
peatlands of Fig. 9.3). Thus, if chemical, vegetational, and floristic criteria are
used to categorize peatlands, then poor fens and bogs should be grouped
together as ‘‘Sphagnum-dominated peatlands’’ (or ‘‘acidic peatlands’’) versus rich
363
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D. H. Vitt and R. K. Wieder
Table 9.1 Sequence of bryophyte species along the pool–hummock microtopographic
gradient for the bog–rich fen vegetation – chemical gradients
Species are the dominant ones found in central* and western Canada. Species found in oceanic
peatlands of the east and west coast are not included. Hummocks are raised areas 20 to more than
50 cm above the lowest surface level and have drier occurring bryophyte species, sedges, and
shrubs; lawns have bryophyte/sedge surfaces from 5 to 20 cm above the water table and wellconsolidated peat; carpets have bryophyte surfaces from 5 cm below to 5 cm above the water
table (emergent bryophyte species) and poorly consolidated peat; and pools are areas with open,
standing water. Abbreviations C., Calliergonella; D., Drepanocladus; H., Hamatocaulis; S., Sphagnum; T.,
Tomenthypnum; W., Warnstorfia.
Permafrost
Continental
bog
bog
Poor fen
Moderate-rich Extreme-rich
fen
fen
Hummock:
S. fuscum
S. capillifolium
S. fuscum
S. fuscum
S. fuscum
Top
S. lenense
S. fuscum
T. falcifolium
S. warnstorfii
S. warnstorfii
T. nitens
Hummock:
S. magellanicum S. magellanicum S. magellanicum S. warnstorfii
T. nitens
Side
Lawn
S. angustifolium S. angustifolium S. angustifolium H. vernicosus
T. nitens
S. warnstorfii
T. nitens
Campylium
stellatum
Carpet
S. balticum
S. rubellum*
S. papillosum*
S. teres
S. jensenii
S. lindbergii
S. jensenii
C. cuspidata
S. riparium
S. subsecundum
W. exannulata
D. aduncus
Scorpidium
revolvens
S. majus
S. riparium
Pool
W. fluitans
S. cuspidatum*
Scorpidium
scorpioides
H. lapponicus
Data derived from numerous sources, including Slack et al. (1980), Crum (1988), Gignac and
Vitt (1990), Gignac et al. (1991), Vitt et al. (1995b). Modified from Vitt (1994).
fens that should be called ‘‘brown moss-dominated peatlands’’ (or ‘‘alkaline
peatlands’’). However if hydrological criteria are used, ombrogenous bogs
stand alone and can be contrasted with geogenous rich and poor fens.
9.3
Function and ecological importance of the moss layer
A 90%–100% cover of mosses dominates the ground layer in peatlands;
although several species of hepatics occur in peatlands, only Leiomylia (Mylia)
anomala is ever abundant. Functioning of the peatland ecosystem is highly
9 Bryophyte-dominated peatlands
dependent on this moss layer, and both production and decomposition, as well
as community development, are all influenced by this layer of mosses. In
particular, the moss layer influences peatland function in several ways.
Especially noteworthy are: (1) nutrient uptake, (2) water-holding abilities, (3)
decomposition, and (4) acidification.
9.3.1
Nutrient uptake and the consequences of atmospheric deposition
Some of the earliest studies in Great Britain suggested that elevated
atmospheric nitrogen deposition could inhibit the growth of Sphagnum and also
alter the habitats of some species. These responses of Sphagnum species were
implicated as causally related to the loss of some Sphagnum species from British
peatlands (Press & Lee 1982, Woodin et al. 1985, Press et al. 1986). In North
America, however, subsequent experiments revealed that increasing nitrogen
input to bogs (Rochefort et al. 1990) and rich fens (Rochefort & Vitt 1988) resulted
in increases in moss growth, suggesting that nitrogen was limiting to Sphagnum
growth. Other factors, such as precipitation (Bayley 1993) and phosphorus
availability (Aerts et al. 1992), have been shown to influence plant growth. At
high nitrogen deposition sites, Sphagnum growth has been shown to be phosphorus limited (Bragazza et al. 2004, Limpens et al. 2004).
When isotopically labeled nitrogen was experimentally added to peatlands (a
bog and a rich fen) in simulated precipitation at sites with low nitrogen deposition, 98% of the nitrogen was recovered in the top 12 cm of peat after one year.
After two years, less than 2% of the added nitrogen was found in the vascular
plants. In both cases, the mosses increased in growth but the vascular plants did
not (Li & Vitt 1997). This particular study did not distinguish whether the added
nitrogen that was recovered in the ground layer and in the peat was sequestered
in micro-organisms, within moss cell walls, or contained in the moss living
cell cytoplasm. Under low nitrogen deposition, it appears that nitrogen is
quickly sequestered by the moss layer and subsequent movement to vascular
plants is dependent on release of the nitrogen from the moss and mineralization
rates within the moss layer. Sphagnum tightly holds much of this added nitrogen
and in the second year 19% of the first year’s nitrogen was found in the new
second year’s growth, indicating that Sphagnum can translocate nitrogen
upward (Li & Vitt 1997). However, under moderate and high deposition, nitrogen may pass through the Sphagnum layer directly to vascular plants and microorganisms.
In summary, it appears that in Sphagnum (and probably all mosses), both the
growth response and the sequestration of nitrogen is triphasic. First, under
pristine boreal conditions, nitrogen limits the growth of Sphagnum (and true
mosses in rich fens as well) and the Sphagnum layer is able to sequester nearly all
365
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D. H. Vitt and R. K. Wieder
of the deposited atmospheric nitrogen for its own use; moss growth occurs
without a measurable change in moss tissue nitrogen concentration. Second,
with increasing deposition nitrogen no longer limits Sphagnum growth, but is
taken up by the growing mosses and is sequestered in the living plant tissues
(thus concentrations of nitrogen in the Sphagnum plants increase). Third, at even
higher nitrogen deposition, the living Sphagnum layer becomes nitrogen-saturated
and some of the newly deposited nitrogen bypasses the living Sphagnum and is
leached downward in the upper peat column, becoming available for either
vascular plant or micro-organism growth (Lamers et al. 2000, Berendse et al.
2001, Limpens & Berendse 2003, Limpens et al. 2003). Sphagnum responses in
the early studies in Great Britain appear to reflect this third phase, whereas
Sphagnum responses in the later North American studies appear to reflect phase 1.
Thus, under phase 1 and 2 conditions, Sphagnum is able to scavenge nearly all of
the atmospheric nitrogen and act as a ‘‘gatekeeper’’ for accessibility of nitrogen
into peatlands. However, under high nitrogen deposition regimes (phase 3), this
gatekeeper role is overrun (Wieder 2006). Vitt et al. (2003) suggested that the
boundary between phases one and two may be reached at atmospheric nitrogen
deposition rates of around 16 kg ha 1 yr 1.
A recent synthesis of ground layer net primary production suggests that
at the regional scale in continental western Canada the four peatland types
do not differ (Campbell et al. 2000). Overall, variability in ground layer production is high both spatially and temporally, but in general, the ground layer
produces about 41% of the total annual plant production (Table 9.2). In a global
review of Sphagnum production, Gunnarsson (2005) reported an overall mean
of 259 g m 2 yr 1 with large variation (standard deviation þ 206). Thus, mosses
sequester nutrients efficiently, and through release and mineralization the
moss layer can effectively control subsequent nutrient (at least nitrogen) availability, and hence plant production. However, changes in atmospheric nitrogen
deposition can have serious consequences in ground layer functioning. A more
thorough review of peatland production is provided in Wieder (2006).
9.3.2
Water-holding capacity
In comparison to almost all vascular plants, which are drought-avoiding
and unable to survive water deficit, most mosses are drought-tolerant and can
survive water deficit (Wood 2005). A few mosses are desiccation-tolerant and can
survive even severe water deficit (Wood 2007; see also Chapters 6 and 7, this
volume). Mosses are photosynthetically active when they are wet, have the ability
to become inactive when dry, and can revitalize when rewetted (Bewley 1979,
Proctor 1979, 1984, Proctor et al. 2007). Whereas mosses occurring in dry habitats
(e.g. Grimmia, Orthotrichum, Syntrichia) have evolved to be able to survive in the face
9 Bryophyte-dominated peatlands
Table 9.2 Summary of net primary production pooled state/province means by layer
for wetland types
Ground layer in peatlands is moss-dominated. Peatland and northern wetland means are
pooled by wetland type and location. Standard deviations are shown in brackets for those layers
where original published data did not include pooled means. For layers containing pooled
means no standard deviations could be calculated. Symbol x, layers that are not present for
the particular peatland type. Amounts given are in g m
2
yr 1. For details see Campbell et al.
(2000).
Tree
Bog
Wooded fen
106 (192)
44
Shrubby fen
x
Open fen
x
Shrub
Herb
Ground
156 (157)
Total
247 (104)
13
108
34
74
358
449 (215)
63
125
118
263
x
365 (458)
163
268 (34)
88 (68)
210 (136)
166 (298)
139 (106)
337 (142)
Wooded swamp
542 (279)
31 (29)
Shrubby swamp
x
480 (260)
Marsh
x
Northern wetlands
542 (279)
Peatlands
62
x
654 (197)
727 (667)
x
1232 (405)
x
999 (529)
x
934 (518)
255 (296)
820 (592)
x
970 (467)
of daily cycles of drying and rewetting, peatland mosses tolerate frequent drought
to a much lesser extent (Glime & Vitt 1984). Instead, peatland mosses have
developed morphological adaptations to retain moisture, allowing longer photosynthetically active periods and thus greater growth (St aº lfelt 1937). Pool and
carpet species such as Scorpidium scorpioides, Hamatocaulis lapponicus, Warnstorfia
(Drepanocladus) exannulata, and Sphagnum cuspidatum live submerged or form poorly
consolidated, emergent carpets (Vitt & Chee 1990). These species appear to have
limited physiological abilities to live for extended time after drying out (but little
information is available on this topic). Among the rich fen species, hummock
species such as Tomenthypnum nitens have abundant stem tomentum and numerous side branches apparently facilitating water uptake through capillarity. In
addition, the dense canopy structure of Tomenthypnum plant communities may
diminish evaporative water losses. These adaptations can also be seen in other
peatland species such as Aulacomnium palustre, Catoscopium nigritum, Dicranum
undulatum, Polytrichum strictum, and Tomenthypnum falcifolium. Interestingly,
among these mosses and their dense canopies, it is common to find less doughttolerant species of hepatics, with species of Cephalozia, Calypogeia, and Lophozia
occurring as mini-lianas among the larger mosses.
Although dead hyaline leaf cells that contain pores and hold large amounts
of water occur sporadically throughout mosses (Proctor 1984), they are
367
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D. H. Vitt and R. K. Wieder
Fig. 9.5. Sphagnum papillosum, with its complex canopy of dense capitula and turgid
spreading branches.
particularly well developed in the genus Sphagnum. In species of this genus, the
leaves consist of alternating, large, hyaline cells enclosing smaller, living, green
cells, in a 1:2 ratio, an arrangement that is unique among plants. Additionally,
the stems and branches are often encased in one or more layers of dead enlarged
hyaline cells, forming a hyalodermis. As hyaline cells develop, they lose their
living cell contents, resulting in a relatively high C/N ratio of the dead cells that
compose peat, with implications for peat decomposition rates. However, the
large hyaline cells, reinforced with internal cell wall thickenings (termed
fibrils), partly to entirely enclose photosynthetically active green cells. Thus,
through internal hyaline cell water-holding capacity and through a complex
canopy of dense capitula (Rydin & McDonald 1985), spreading and hanging
branches, and concave leaves (Fig. 9.5), Sphagnum produces a plant morphology
suggestive of drought avoidance, not drought tolerance.
Communities of hummock species such as S. fuscum and S. capillifolium have
the most highly developed canopies that protect the living green cells from
drying out; communities of lawn species such as S. angustifolium have a looser
canopy structure and less well developed water-retention abilities. Sphagnum
species occurring on the highest hummocks occur there not because they are
physiologically drought-tolerant, but because they are morphologically
drought-avoidant (Titus & Wagner 1984). Lawn species, however, occurring in
wetter but more variable conditions, are in fact physiologically more droughtinsensitive and lack the highly developed canopy modifications of the true
hummock-formers (Titus & Wagner 1984). These interpretations have been
9 Bryophyte-dominated peatlands
corroborated experimentally through establishment experiments showing that
the lawn species S. angustifolium established efficiently on bare peat without the
protection of a developed canopy, whereas S. fuscum and S. magellanicum, both
hummock-formers, did not establish efficiently on bare peat (Li & Vitt 1994).
The high water-holding capacities of Sphagnum plant communities can result
in local water table raising that facilitates the lateral expansion of peatlands into
adjacent upland areas. This swamping, or paludification, of neighboring habitats is a major factor in increasing the amount of organic terrain in northern
landscapes (Vitt & Kuhry 1992).
In summary, the dead hyaline cells allow Sphagnum species to maintain
hydrated conditions of the living cells for extended periods of time, lengthening
photosynthetically active periods and promoting net primary production and
vertical plant growth. Hyaline cells of individual Sphagnum plants, along with the
dense packing of Sphagnum species into communities, result in the upward
movement of water from the water table, elevating the peatland water table
and apparently facilitating lateral peatland expansion. At the same time, the high
water-holding capacity promotes the development of anaerobic conditions in
microsites above the peatland water table, where dissolved oxygen consumption
rates exceed oxygen diffusion rates into wet peat. In addition, the water-holding
capabilities of moss plants and moss communities buffer peatland ground-layer
temperatures against changes in air temperature at the moss–atmosphere interface, conferring some degree of protection of individual moss plants against
evaporative stress and diminishing evaporative losses from peatlands as a
whole. Together these conditions promote the accumulation of peat by limiting
decomposition.
9.3.3
Decomposition
Bryophytes are small organisms that appear to have difficulties tolerating large water level fluctuations (Zoltai & Vitt 1990). In wetlands such as swamps
and marshes where water level fluctuations are seasonally quite variable, bryophytes are not dominant (Vitt 1994). These non-peat-forming wetlands, dominated by vascular plants that produce copious litter, have relatively high rates
of decomposition (Mitch & Gosselink 1993). Although it has been commonly
argued that one of the factors attributing to slow decomposition rates in peatlands is acidity, in fact both acidic and basic peatlands accumulate large amounts
of peat. Both true-moss and Sphagnum-dominated peatlands accumulate large
amounts of peat. In continental boreal Canada, an analysis of 341 peatland
cores clearly indicates that rich fens accumulate peat to depths similar to those
found in poor fens and bogs (Fig. 9.6). Although the basal portions of some cores
may largely be detrital without recognizable plant parts, in many of these cores
369
D. H. Vitt and R. K. Wieder
30
Bog
Poor fen
Rich fen
25
Per cent of sites by peatland type
20
15
10
>500
501–550
451–500
401–450
351–400
301–350
251–300
201–250
151–200
101–150
0
51–100
5
0–50
370
Depth (cm)
Fig. 9.6. Peatland depths partitioned by per cent of bogs, poor fens, and rich fens (as
determined by present-day surface vegetation). Number of sites: bog, 129; poor fen, 66; rich fen,
146. All sites are from continental western Canada (Alberta, Saskatchewan, and Manitoba). Data
are from Zoltai et al. 1999.
the major component of the accumulated peat is bryophytic; Sphagnum in poor
fens and bogs, and brown mosses in rich fens (including species of the genera
Aulacomnium, Catoscopium, Campylium, Drepanocladus [sensu lato], Meesia, Scorpidium,
and Tomenthypnum). Mass losses in the upper 30 cm of true moss-dominated rich
fens and Sphagnum-dominated poor fens are slightly (but significantly) greater
than in bogs, with fens averaging 6.4% of total peat mass lost compared with 5.3%
in bogs over a 26 month period of time (Fig. 9.7, unpublished data). However,
higher initial inputs (NPP) to the peat column of fens cause substantial quantities
of peat to be deposited in both peatland types.
Comparison of hummock decomposition by using litter bags (placed just
beneath the peatland surface) in rich fens (Tomenthypnum nitens) compared
9 Bryophyte-dominated peatlands
3.0
Bog
Bog regression
Poor fen
Rich fen
Fen regression
Total mass loss (kg m–2)
2.5
2.0
1.5
1.0
0.5
0.0
5
10
15
20
25
Total mass (kg m–2)
30
35
Fig. 9.7. Relation between the total mass and total mass loss of peat in the upper 30 cm
of the peat column in fens and bogs in continental western Canada. Details of methods in
Benscoter 2007. Slopes for bog (r2 ¼ 0.40, p ¼ 0.0001) and fen (r2 = 0.486, p ¼ 0.0009) are
significantly different (ANCOVA p ¼ 0.561; however, elevations of the slopes are
significantly different at p ¼ 0.0025). Y (% lost over a 24 month period) ¼ 5.3% for bog and
6.4% for fen.
with bogs (Sphagnum fuscum) indicates that over the short term (16 months)
significantly more decomposition occurred in hummocks composed of
Tomenthypnum nitens (Vitt 1990, Li & Vitt 1997). Within bogs along the hummock–
hollow gradient, hummock species retain about 86% of their initial dry mass
after three years, but hollow species retain only 74% after a similar time period
(Rochefort et al. 1990). In addition, bryophyte material decomposes at slower
rates than vascular plant material, and moss net primary production (NPP) in
hummocks is about half that of bog hollows (carpets and lawns) (Vitt 1990,
Gunnarsson 2005) whereas moss NPP of fen hummocks is greater than or
equal to that of hollows (reviewed in Vitt 1990). Although few data exist on
true moss production it appears that hummocks can develop higher than
hollows above the water table in both bogs and rich fens, owing to higher
rates of moss NPP (fens) and/or less decomposition in hummocks compared
with hollows (bogs).
When Sphagnum-dominated hummocks were compared with brown mossdominated hummocks, both with well-developed acrotelms, the Sphagnum system decomposed 11% less than the brown moss hummocks after two years (Li &
Vitt 1997). These data suggest that there should be a fundamental difference in
371
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D. H. Vitt and R. K. Wieder
plant chemistry upon entry to the catotelm; however, there have been no
comparative studies of peat quality in rich fens and bogs to our knowledge. In
summary, decomposition studies using litter bag results indicate that individual
species (both bryophytic and vascular plant) have distinctive and often different
rates of decay (Turetsky 2004, reviewed in Moore & Basiliko 2006) and when
decomposition losses for the intact upper peat column are compared between
bogs and fens, each with entirely different species, significant differences
appear to be present.
Changes in the organic chemical composition of peat as it undergoes decomposition have received little attention. Although mosses do not contain true
lignin, a lignin-like polyphenolic network consisting of p-hydroxyphenyl groups
has been characterized in the cell walls of Sphagnum plants (Wilson et al. 1989,
Rasmussen et al. 1995, Williams et al. 1998). The ratio of cellulose to these ligninlike compounds decreases with depth in the peat column (Williams et al. 1998,
Turetsky et al. 2000), suggesting compound-specific differences in susceptibility
to decay.
An empirical modeling approach based on 210Pb dating of peat cores was used
to estimate annual net primary production and depth-dependent decomposition rates within the upper 30–40 cm of bog peat (Wieder 2001). We have
expanded on this modeling approach to estimate that ‘‘lignin’’ and holocellulose
constitute 27%–32% and 57%–60%, respectively, of annual net primary production in three Alberta bogs (as compared with measured values of 18%–21% and
59%–62%, respectively, in these same bogs; Turetsky et al. 2000). The holocellulose fraction is composed mainly of a-cellulose (70%–85%), with a smaller contribution from hemicellulose (15%–22%), as determined from both the empirical
modeling approach and measurements of peat at the surface of the peat deposit
(Turetsky et al. 2000).
The empirical modeling approach to simulating bulk peat decomposition
(Wieder 2001) can also be applied to the decomposition of cellulose and lignin
fractions of newly formed peat over a 100 year period (Fig. 9.8). Using this
approach, we predicted that after 100 years of decomposition, only 14%–27%
of the initial mass (i.e. material produced at the surface in one year’s net primary
production), 14%–22% of the initial holocellulose, 12%–16% of the initial
a-cellulose, 4%–16% of the initial hemicellulose, and 13%–32% of the initial
lignin would remain. Correspondingly, the lignin : holocellulose ratio would
change from about 0.4:1 in the peat produced from net primary production at
the surface of the peat column to about 0.8:1 after 100 years of decomposition.
Although cellulosic components of peat decompose more rapidly than ligninlike components, it is not the case that cellulosic components disappear, with
lignin-like components showing great recalcitrance to decomposition; rather,
350
300
250
200
150
100
50
0
Bleak Lak e Bog - Core 2
yr–1)
300
Sylvie’ s Bog - Core 1
–2
9 Bryophyte-dominated peatlands
250
1.0
0.6
0.4
Propor tion of initial mass remaining
0.2
Mass remaining (gm
200
150
100
50
0
300
Sylvie’ s Bog - Core 2
250
0
1.0
Sylvie’ s Bog - Core 1
0.8
0.6
0.4
0.2
0
1.0
Sylvie’ s Bog - Core 2
0.8
200
0.6
150
0.4
100
0.2
50
0
Bleak Lak e Bog - Core 2
0.8
0
40
80
120
160
200
0
Organic Matter
Lignin
Holocellulose
α-cellulose
0
40
80
120
160
200
Hemicellulose
Fig. 9.8. Fate of a single year’s cohort of organic matter and its components estimated by
using the 210Pb-based empirical modeling approach described by Wieder (2001) and the
quantitative characterization of organic matter components as a function of depth
in 210Pb-dated peat cores, following the procedure of Wieder & Starr (1998).
both cellulose and lignin decay in concert with a slow, but progressive, enrichment in lignin-like compounds in the remaining peat. It may be that the ligninlike compounds are intimately associated with the cellulosic compounds in
Sphagnum cell walls (Rasmussen et al. 1995, Wilson et al. 1989, Williams et al.
1998) in a way that confers some degree of overall resistance to decay.
Peat decomposition continues, albeit at a considerably slower pace, throughout the deeper, permanently water-saturated peat column, the catotelm. For
example, in some Sphagnum-dominated bogs, the anaerobic catotelm receives
from the acrotelm a relatively large amount (although probably less than 20%
of the original mass) of undecomposed material with low bulk density. Once in
the catotelm, deposition is considerably less, and has been modeled following
simple exponential decay functions (Clymo 1984) that when plotted as a graph
373
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D. H. Vitt and R. K. Wieder
(and when they have a constant rate of catotelmic input) produce a characteristic concave curve of accumulated peat over time. In contrast, many fens
and some continental boreal bogs have linear or even convex accumulation
curves that apparently do not fit the exponential decay function (Yu et al.
2003a). When long-term accumulation curves are compared to the exponential
model prediction, accumulation is consistently greater than expected (Yu et al.
2003a).
In summary, it is apparent that some aspects of bryophyte function are
becoming better known (such as Sphagnum primary production), yet others
lack comprehensive data sets gathered from a wide range of peatland types
and geographic localities (e.g. true moss production). Decomposition within the
acrotelm needs to be explored further by using a variety of approaches over a
range of peatland types, and long-term accumulation patterns need to be
explored over a range of peatland types, especially in the peatlands dominated
by true mosses that are so dominant across the boreal region.
9.3.4
Acidification
In 1963, R. S. Clymo (Clymo 1963) argued that peatland acidity is produced by Sphagnum cell walls. The hydrogens of the carboxylic acid moieties of
uronic acid cell wall components are exchanged for base cations contained in
pore waters, releasing hydrogen ions into peatland pore waters. This cation
exchange ability of Sphagnum can easily be demonstrated by immersing some
living or dead Sphagnum into doubly distilled water and measuring the pH
change and then by adding common table salt to the same solution and again
measuring the pH change. In the former case, no pH change is evident; in the
latter, the pH will immediately decrease by 2–3 pH units. In 1980, Harry
Hemond argued that although this process of cation exchange by Sphagnum
undoubtedly occurs, it is not sufficient to produce the acidity that is present
in bogs (i.e. pH 3.0–3.7). He concluded that bog acidity is largely due to decomposition and the production of humic acids present in pore water as DOC, and
that acidity in bogs is a result of hydrogen release through decomposition of
organic molecules that in turn are dissolved in the pore water as organic carbon.
Under the former scenario, the anions are attached to the Sphagnum cell walls
(Richter & Dainty 1989), whereas in the latter case the anions are dissolved in the
pore water as DOC (Hemond 1980) and thus create the predominant ‘‘brown
water’’ characteristic of bogs.
Regional landscape analyses of natural lake acidity support this pattern.
Halsey et al. (1997a) showed that across 29 watersheds, watershed bog cover
and lake DOC concentrations are positively correlated. Watersheds with a high
percentage of poor fen cover also tend to have acidic lakes (Fig. 9.9). Importantly,
9 Bryophyte-dominated peatlands
Fig. 9.9. Biplot of the chemical parameters measured in water from 29 boreal lakes in
northeastern Alberta, Canada. Watershed variables that explain a significant amount of the
variation on the first two axes are shown by directed arrows. Abbreviations: %WATER, per cent
of open water in the watershed; ALK, alkalinity; BICARB, bicarbonates; CA, calcium; CL,
chlorine; COND, reduced conductivity; DOC, dissolved organic carbon; MG, magnesium; NA,
sodium; PH, pH; TDP, total dissovled phosphorus; TDS, total dissolved solids; TKN, total
Kjehldahl nitrogen; TP, total potassium. DEPTH and AREA refer to lake and area depth; SLOPE is
the regional watershed slope. (Reprinted with permission from Kluwer Academic Publishers/
Water, Air, and Soil Pollution, Vol. 96, 1997, Influence of peatlands on the acidity of lakes in
northeastern Alberta, Canada, by Linda A. Halsey and Dale H. Vitt, Fig. 5, p. 33.)
this study indicates that lakes occurring in watersheds with greater than 30%
cover of poor fens and bogs are nearly always acidic, while those without
extensive acidic peatland cover have higher pH (all lakes of this study were
situated on glacial deposits over acidic shales). In addition, outputs from poor
fens appear to have more influence on downstream acidity than do stagnant
bogs.
Sphagnum cation exchange activity is dependent on the presence of free cations
in the surface waters of a peatland. Rich fens have high concentrations of free
cations (Vitt et al. 1995a); however, the charge of these free base cations – largely
Ca2þ – is balanced, mainly by HCO3 (Vitt & Chee 1990). Gignac (1994) has shown
that Sphagnum quickly dies when grown in water having any amount of alkalinity.
Bogs, on the other hand, have low concentrations of free base cations (Vitt et al.
375
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D. H. Vitt and R. K. Wieder
1995a), such that a large percentage of cation exchange sites on Sphagnum cell
walls are occupied by hydrogen ions. Thus, under bog conditions one would
expect that cation exchange capacity would not be base-saturated, and that
Hemond is correct: Sphagnum-produced acidity in bogs is not sufficient to explain
the low pH of bog waters. However, the question then becomes whether there are
conditions where the alkalinity is low enough to allow Sphagnum to live and yet
have sufficient base cations to allow acidification to occur.
The answer may actually lie in the fact that Sphagnum acidity is critical for
successional transitions between moderate-rich fens and poor fens and may
continue to dominate in flow-through poor fens where base cations are more
abundant than in bogs. The switch from a brown moss-dominated system to one
dominated by Sphagnum is critical in the evolution of acidic peatlands and many
bogs. The macrofossil record clearly shows that the change from rich fen to
poor fen occurs very rapidly (Kuhry et al. 1993). This species change is associated
with changes in acidity, generally from around pH 7 in moderate-rich fens to 5
in poor fens. Acidity produced via exchange of base cations (readily available in
the minerotrophic fens) for hydrogen ions via the Sphagnum ion exchange
system will be relatively more important in accounting for the acidity at higher
pH (4–7). At low pH (3–4), where much higher concentrations of hydrogen ions
are required and where base cations are low due to ombrotrophic conditions,
acidity is due more to humic acid decomposition. This acidity would in many
cases produce waters with high concentrations of DOC and these would be
more heavily colored. Thus, a corollary is that Sphagnum-produced acidity may
more strongly influence external downstream chemistry, while decomposition
acidity may be more internally influential, especially in stagnant bogs. The
relative importance of these two types of acidity needs further study, especially
in poor fens.
The available evidence suggests that rich fens may persist without change for
thousands of years, with fens being just as deep as bogs (Fig. 9.6). However, if
alkalinity concentrations allow establishment of Sphagnum, then rapid acidification via Sphagnum cation exchange may result in the development of poor fen
vegetation within 100–200 years (Vitt & Kuhry 1992). This rapid change at pH
around 5.5 appears to be responsible for the rarity of peatlands of this transitional nature in many areas of the boreal landscape (cf. Fig. 9.4).
9.4
Responses to environmental change and disturbance
Bryophytes are small plants closely tied to their substrate. This is especially true in peatlands, where changes in height above water table and in water
chemistry affect both the structure of bryophyte communities and the
9 Bryophyte-dominated peatlands
functioning of these moss-dominated peatland ecosystems. Although most of
the bryophyte species that dominate the ground layers of peatlands have broad
geographical ranges, they have extremely narrow habitats. For example,
Sphagnum fuscum and Scorpidium scorpioides are two species that have circumboreal ranges across northern Eurasia and North America, and both are clear and
abundant indicators of specific water level and water chemistry conditions in
northern peatlands (S. fuscum on hummocks in bogs and S. scorpioides in carpets
and pools of extreme-rich fens). Thus responses of bryophytes to environmental
changes are useful across the hemisphere, as opposed to most peatland vascular
plant species that are confined to narrower geographic ranges (Vitt 2006). The
abundance of bryophytes in northern peatlands, and their narrow habitat tolerances yet broad geographic ranges, make bryophytes useful as key indicators
of both community changes and ecosystem responses to disturbance and environmental change.
Disturbances across the boreal forest are tightly coupled to both the activities
of humans and changes in climate: both natural climatic cycles and global
climate change. Turetsky et al. (2002a) examined cumulative effects of disturbance on peatlands of western Canada and estimated that current disturbances
reduce carbon uptake in continental peatlands by about 85% when compared
with a non-disturbance scenario. These authors concluded that wildfire was by
far the major disturbance, followed by peat extraction, permafrost melt (having
a positive influence on carbon uptake), then reservoirs, and mining of oil sands.
The two most important disturbances, fire and permafrost melt, affect peatland
community structure as well as ecosystem function in contrasting ways
(Robinson & Moore 2000).
9.4.1
Permafrost melt
Near the southern boundary of discontinuous permafrost, permafrost is confined to wooded peatlands. In these wooded peatlands, permafrost
occurs as sporadic lenses of ice, creating distinctive landscape features
termed frost mounds (Beilman et al. 2001), generally believed to have
aggraded during the past climatic cold spell (the Little Ice Age). Frost mounds
are most often found in bogs and differ from unfrozen bog areas by having
more dense populations of trees that are taller and of larger diameter and a
ground layer with more abundant feather mosses (Hylocomium splendens and
Pleurozium schreberi) and reindeer lichens (Cladina mitis and Cladonia uncialis).
Comparatively, unfrozen bogs have a less well-developed tree layer and
greater abundance of Sphagnum fuscum, S. magellanicum, and S. angustifolium.
Warming climate over the past 100–150 years has resulted in permafrost
gradually melting, and the southern boundary of permafrost has migrated
377
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D. H. Vitt and R. K. Wieder
A
B
Fig. 9.10. Melting of permafrost at the southern edge of discontinuous permafrost, (see Vitt
et al. 1994 for details). (A) Area of peat collapse due to localized permafrost melt at the edge
of a frost mound in a continental bog. Emergent mounds of moss are Pleurozium schreberi that in
the previous year formed hummocks 0.5–1.0 m high on the frost mound. Photo taken in
northern Alberta. (B) Internal lawn formed by collapse of frost mound. Leaning snags of
dead Picea mariana trees are visible. Vegetation is sedge- and Sphagnum-dominated,
especially S. riparium.
northward some 200 km in western Canada (Vitt et al. 1994, Halsey et al. 1995,
Camill 1999, Halsey et al. 2000).
At the local scale, the results of this melting are spectacular. Frost mounds,
elevated one meter or more above the water table, collapse, thereby submerging
the previously dry surface of feather mosses (Fig. 9.10a). Submergence continues
and the newly created internal lawn is quickly vegetated by sedges (Carex spp.)
and a variety of carpet-dwelling sphagna (Fig. 9.10b), including Sphagnum riparium, S. jensenii, S. majus, and more rarely, S. obtusum and S. lindbergii. Since the
original feather moss surface layer is identifiable in the peat column as a dense
sylvic [=woody]-feather moss horizon, modern 210Pb dating methods can determine the age of the melt and the rates of peat accumulation since the melt,
compared with both neighboring frost mound and unfrozen bog.
Bogs, frost mounds, and internal lawns differ not only in terms of moss and
vascular plant communities, but also in rates of recent net peat accumulation. In
particular, peat accumulation in internal lawns is substantially greater than in
the frost mound features, whose degradation through permafrost melt lead to
internal lawn creation (Robinson & Moore 2000, Turetsky et al. 2002b). However,
internal lawns undergo autogenic succession over time, with progressive development toward bogs (Beilman et al. 2001, Camill et al. 2001) and concurrent
decreases in peat accumulation rates. Through 210Pb dating of internal lawn
peat, Turetsky et al. (2007) estimated that within about 70 years following initial
permafrost melt, peat accumulation rates in internal lawns become stable and
similar to peat accumulation rates in bogs.
9 Bryophyte-dominated peatlands
9.4.2
Wildfire
When peatlands are affected by fire, peat (and stored carbon) is lost both
directly (from the aboveground vegetation and surface peat) as well as indirectly
(organic matter losses through ongoing peat decomposition with little or no
plant production, at least early on after fire). Turetsky et al. (2002a) estimated
that across continental western Canada, 75% of the organic matter lost as a
result of wildfire was from the direct action of the fire itself, and 25% was from
indirect effects of post-fire mineralization of organic matter.
Re-establishment of the ground layer in peatlands is critical for the return of
long-term ecosystem processes, especially those that lead to the formation of
peat and accumulation of carbon in the long-term peatland sink. Until recently,
the time frame and trajectories of vegetation succession were unknown.
Detailed examination of vegetation recovery along a 102-year bog chronosequence in Alberta, Canada, indicates that post-fire ground layer recovery
takes place in three phases. True mosses are dominant in early succession
during the first 20 years post-fire, and of these mosses Polytrichum strictum and
Aulacomnium palustre are especially important (Benscoter 2007). Initial populations of these mosses begin in the wet depressions and expand outward
(Benscoter 2006). Sphagnum recruits, especially S. angustifolium, establish within
the true moss populations and aggressively expand, and at about 20 years postfire a continuous ground layer of Sphagnum has become established. From 20 to
80 years post-fire, Sphagnum hummock and hollow topography becomes established and persists. Gradually in late succession, as tree canopy density increases
feather mosses become more abundant (Benscoter 2007, Fig. 9.11). Whereas
continuous ground layer cover is established at about 20 years post-fire, tree
layer density, canopy cover, and biomass continue to increase, thus lagging
behind development of the ground layer.
These structural changes in the bog ground layer are reflected in temporal
changes in net ecosystem exchange (net CO2 flux) after fire. Immediately after
fire, bogs function as a net C source to the atmosphere, with a rate of 8.9
8.4 mol C m 2 yr 1. Bogs switch from C sources to C sinks at about 13 years after
fire, as the moss and shrub layers become re-established. The strength of the bog
C sink peaks at about 18.4 mol C m 2 yr 1 at about 74 years after fire, concomitant with the peak in aboveground net primary production of black spruce trees.
At 100 years after fire, the bog C sink reaches a fairly stable value of about
10 mol C m 2 yr 1 (Fig. 9.12; Wieder et al. 2009). Projecting the carbon balance
recovery trajectory across the 2280 km2 of bogs in the well studied Wabasca region
of north-central Alberta, with a bog fire return interval of 120 yr, the regional
bog C sink is about 171 61 Gg C yr 1. However, two likely consequences of
379
D. H. Vitt and R. K. Wieder
150
y = –39.3 + 53.1ln x – 6.4 (In x )2
r2 = 0.95
100
g m2 yr–1
380
50
0
–50
Bare/burned and true moss
Sphagnum and shrubs
Feather moss
No vegetation data
0
20
40
60
80
100
Time since fire (yrs)
Fig. 9.11. The response for net primary production (NPP) of the ground layer (dominated by
species of Sphagnum, Cladina, and feather mosses) along a chronosequence of bog sites after fire.
Data for 2003–2006 from Benscoter (2007). Species groups based on cluster and indictor species
analyses. Mean SD, n = 5.
ongoing climate change are a shortening of the fire return interval and a
temperature-driven enhancement of peatland respiratory carbon losses, either
or both of which will diminish the regional peatland carbon sink across
continental western Canada (Wieder et al. 2009).
9.4.3
Climatic cycles
In the examples of environmental disturbance discussed above, the
influences of change were sufficiently severe to modify the vegetation, with
ecosystem responses tied closely to wholesale plant community changes that
were driven by successional patterns of the ground layer, and structure was tied
closely to function. However, ecosystem processes can change without evidence
of community change, and even though key species may remain unchanged,
changes in the rates of important processes may take place and modify the
overall functioning of the ecosystem. Such a situation appears to be evident in
some fens in western Canada over a large part of the past 10 000 years.
One of the unique properties of peatlands is that the peat is deposited
in situ, and plant parts are incorporated into the peat column exactly where
they grew. Analysis of these plant macrofossils provides insight into patterns of
local plant succession. One of the important conclusions that can be reached
from the study of numerous paleo-records of a core is that in fens and bogs the
9 Bryophyte-dominated peatlands
Fig. 9.12. Changes in net ecosystem production (NEP) of C accumulation along a time-since-fire
chronosequence of 10 bog peatlands in central Alberta, Canada (Wieder et al. 2007). Annual
NEP from static chambers is based on measurements of CO2 at different intensities of
photosynthetically active radiation (PAR; from full sun to full dark), fitting a rectangular
equation to the resulting NEP versus PAR measurements collected over a 3-year period,
applying hourly measurements for PAR and air temperature (from a weather station installed
at one of the bog sites) to the fitted equation, and summing the hourly estimates of NEP over
a full year. Accumulation of C in black spruce aboveground tissues and roots was calculated
from the derivative of the best fit equations describing changes over time in aboveground
and root biomass at the 10 chronosequence sites.
key and most abundant species may exist for hundreds and even thousands
of years unchanged in composition (Kuhry et al. 1993). However, fine-scale paleoanalysis of long (2–5 m) peat cores from sites that have a continuous, single
species occurrence suggest that functional long-term changes clearly have
occurred. A case in point is Upper Pinto Fen in western Alberta (Yu et al. 2003b)
(see below).
Interpretation of these data requires some additional background. Aboveground organic matter is deposited at the peatland surface from vascular plant
litter and combines with moss plants and belowground vascular plant roots to
form the peat column. Decomposition is relatively rapid in the aerobic acrotelm; after spending some time in the acrotelm, peat arrives at the anaerobic
catotelm, where decomposition rates are relatively uniform and very low
(Clymo 1984). So, in a given peatland and for a given species, the amount of
381
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D. H. Vitt and R. K. Wieder
decomposition that takes place is largely a function of the time spent in the
acrotelm. Drier environmental conditions produce lower water tables, which in
turn increase the depth of the acrotelm; thus drier conditions result in material
reaching the catotelm in a more decomposed state. These varying amounts of
decomposition throughout peat profiles are manifested both as the amount
of debris vs. clearly identifiable plant macrofossil material, and also as changes
in peat bulk density. High amounts of debris and high bulk densities are
indicative of advanced decomposition and provide surrogates of past surface
processes – that is, they are surrogates of the amount of decomposition of
specific and dominant species of bryophytes. These attributes essentially assess
the quality of the peat that has been processed through the aerobic decomposition process. Additionally, the actual amount of organic matter that is produced
must be accounted for, so the amount of peat that reaches the catotelm is the
result of the processes of decomposition discussed above as well as the amount
of plant production; together, these determine the gross input to the peat
column. Bryophytes are desiccation-tolerant, and as such photosynthesize as
long as they are wet and turgid. Rates of photosynthesis decrease as the mosses
become drier; thus high water tables throughout the growing season increase
the bryophyte production and increase the gross organic matter inputs to
peatlands.
In conclusion, dry climatic conditions and the resultant lowered peatland
water table affect the accumulating peat surface in two ways: bryophytic production decreases because the growing apices are subjected to an increased
frequency of desiccation, and total acrotelmic decomposition increases not
because of enhanced rates but because lower water table effectively extends
the aerobic acrotelm deeper into the peat column. These functional changes are
manifested in the peat column as changes in vertical peat accumulation
(g cm 1), the ratio of debris to recognizable bryophyte macofossils, and peat
bulk density (g cm 3).
Upper Pinto Fen (UPF), Western Alberta, Canada
At this site, Yu et al. (2003b) found that both ash-free bulk density and
debris did not increase with depth (indicating that substantial decomposition
was not occurring in the catotelm); however, both ash-free bulk density and per
cent debris as well as per cent Scorpidium scorpioides (in the macrofossil analysis)
exhibited extremely variable profiles (Fig. 9.13). All three of these parameters
showed periodicities at both millennial (1500–2190 yr with a mean of 1795 yr)
and century scales (386 and 667 yr). Especially significant are three periods of
200–600 yr duration at 4000, 5500, and 6900 cal years BP of high rates of peat
accumulation. In this peatland that was dominated by one bryophyte species
9 Bryophyte-dominated peatlands
Fig. 9.13. Climate, peatland and carbon-cycle correlation. (A) Percentage of hematitestained grains from the North Atlantic. Numbers show the cold events for the North
Atlantic region, together with the ‘‘Little Ice Age’’ (LIA). Rectangles on the right are
locations and 2 standard deviation ranges (180–480 years, with a mean of 300 years) of
12 calibrated
14
C dates. There might be an additional age error of 200 years owing to
variable reservoir correction. The correlation with the Upper Pinto Fen (UPF) record
(shaded in B) is suggestive within the dating uncertainty. (B) Ash-free bulk density from
the UPF core in central Alberta. The UPF wet events (shaded bands) were defined as the
lowest ash-free density values (shaded in B). Rectangles on the right are locations and
2 s.d. ranges (45–335 years, with a mean of 190 years) of calibrated
14
C dates. (C) Peat-
accumulation rates from the UPF core. (D) Weight of calibrated basal peat dates from
79 paludified peatlands in Continental western Canada as a measure of probability of
peatland initiation. Cumulative curve can be used as a proxy for the increase of new
peatland areas. See Halsey et al. (1997b) for detailed information on location, peat depth
and reference of each basal date. (E) Atmospheric CO2 concentrations from Taylor Dome
in Antarctica. Rectangles indicate periods of decreases in the CO2 rising rate, especially
during the CO2 plateaus E, D, and C shortly after the peat accumulation and peatland
initiation peaks, and during the phase of rapid increase in new peatland area (C, D).
The suggestive correlation with the UPF and western interior Canadian peatlands is
shown as shaded bands. (F) Atmospheric CH4 concentrations from GRIP core in
Greenland and from Taylor Dome core in Antarctica. Legend shortened from Yu
et al. 2003b.
continually for 5200 years (between 6500 and 1300 cal yr BP), few species
changes are evident in the paleoecological record and past environmental
change produced no detectable species changes. However, peat accumulation
rates varied considerably (Fig. 9.13) from a norm of less than 100 g m 2 yr 1
to peaks of more than 400 g m 2 yr 1. These peaks in peat accumulation
383
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D. H. Vitt and R. K. Wieder
(associated with low bulk densities and high per cent S. scorpioides fragments)
indicate high water tables and wet climatic events. The wet UPF events correlate
with peaks in peatland initiation across western Canada and declines in the rate
of atmospheric CO2 concentrations (as evidenced in Antarctic ice cores).
Furthermore, these UPF wet climatic events are coeval to warm climatic periods
documented from the North Atlantic (Bond et al. 1997, 1999). These paleoecological reconstructions from Upper Pinto Fen in western Alberta suggest that a
pervasive and cyclic climatic signal influenced rates of peat accumulation in a
rich fen dominated by a single species, Scorpidium scorpioides. The functioning of
this single keystone species, through either changes in rates of production and/
or rates of decomposition, largely controlled the carbon sequestered from the
atmosphere and demonstrated functional responses of climatic fluctuations to
both bryophytes and the peatland ecosystems in which they live. Future climatic
changes may also influence function dynamics of individual keystone bryophytes and may affect carbon sequestration of boreal peatlands.
9.5
Conclusions
In many northern areas of the world with cool climates and short growing seasons, bryophyte-dominated peatlands form a substantial part of the landscape. These ecosystems have expanded over the past 6000 to 10 000 years, and
have sequestered large amounts of carbon. The functioning of these northern
peatlands is strongly influenced by bryophytes, and our understanding of the
nutrient flow, diversity, and carbon sequestering of these ecosystems can only be
advanced by thorough knowledge of the bryophytes that dominate in these
ecosystems.
Acknowledgments
This chapter is based on research made possible through research
funded by the National Science Foundation (U.S.) and also by the Natural
Science and Engineering Research Council (Canada). Support for individual
projects includes funding from the Province of Alberta, Sun Gro Horticulture
(through Tony Cable); Networks of Centers of Excellence in Sustainable Forest
Management; Canadian Forest Service; and the University of Alberta. We are
especially grateful to the efforts of Sandi Vitt for technical expertise. These ideas
and the data on which they are founded have accumulated through the years
by interactions with students and colleagues; in particular D. Beilman,
B. Benscoter, D. Gignac, L. Halsey, P. Kuhry, Y. Li, B. Nicholson, L. Rochefort,
K. Scott, M. Turetsky, M. Vile, A. Wood, B. Xu, Z. Yu, and S. Zoltai.
9 Bryophyte-dominated peatlands
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Bryophytes and Lichens in a Changing Environment, ed. J. W. Bates & A. M. Farmer,
pp. 178–210. Oxford: Clarendon Press.
Vitt, D. H., Achuff, P. & Andrus, R. E. (1975). The vegetation and chemical properties
of patterned fens in the Swan Hills, north central Alberta. Canadian Journal of
Botany, 53, 2776–95.
Vitt, D. H., Bayley, S. E. & Jin, T.-L. (1995a). Seasonal variation in water chemistry
over a bog-rich fen gradient in continental western Canada. Canadian Journal of
Fisheries and Aquatic Sciences, 52, 587–606.
Vitt, D. H., Halsey, L. A. & Zoltai, S. C. (1994). The bog landforms of continental western
Canada, relative to climate and permafrost patterns. Arctic and Alpine Research,
26, 1–13.
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Vitt, D. H., Halsey, L. A., Thormann, M. N. & Martin, T. (1995b). Peatland Inventory of
Alberta. Edmonton, Alberta: Alberta Peat Task Force, University of Alberta.
Vitt, D. H., Horton, D. G., Slack, N. G. & Malmer, N. (1990). Sphagnum-dominated
peatlands of the hyperoceanic British Columbia coast: patterns in surface water
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Vitt, D. H., Halsey, L. A., Wieder, K. & Turetsky, M. (2003). Response of Sphagnum fuscum
to nitrogen deposition: A case study of ombrogenous peatlands in Alberta,
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Wagner, D. J. & Titus, J. E. (1984). Comparative desiccation tolerance of two Sphagnum
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Walbridge, M. R. & Navaratnam, J. A. (2006). Phosphorus in boreal peatlands. In
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9 Bryophyte-dominated peatlands
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10
Population and community ecology
of bryophytes
hakan rydin
10.1
Introduction
Modern textbooks in general ecology contain very few, if any, bryophyte
examples of patterns and processes such as population and metapopulation
dynamics, dispersal, competition, herbivory, and species richness variation. A question then arises: can we freely adapt theories developed from studies of vascular
plants or even animals and apply them to bryophytes? In this chapter I give
examples of population and community-level processes based on bryophyte studies,
and discuss how life history, morphology and physiology of bryophytes can help us
to understand population dynamics, community diversity, and species composition.
Bryophytes are important in terms of species richness and cover in many
habitats, and also for ecosystem functions. Most obvious is the role of Sphagnum
as peat former. A calculation based on an average peat depth of 2 m indicates
that the amount of carbon in northern hemisphere peatlands is 320 Gt, about
44% of the amount held in the atmosphere as carbon dioxide (Rydin & Jeglum
2006; see Chapter 9, this volume). Another example is the finding that nitrogenfixation by the cyanobacterium Nostoc associated with Pleurozium schreberi
contributes substantially to the nutrient budget of boreal forests (DeLuca et al.
2002). An illustration of the community importance of bryophytes is their
contribution to biodiversity in many ecosystems at northern latitudes. As an
example, Sweden hosts c. 0.8% of the world’s vascular plant species, and 7.5% of
the bryophytes (Table 10.1). Using bryophytes as model organisms in population
and community studies has the advantage that many species, especially the
dominant ones, have very wide distributions. Detailed studies of, for example,
niche relations among peat mosses or forest feather mosses in boreal Europe
and North America are highly comparable down to species level.
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
394
H. Rydin
Table 10.1 Bryophytes (mosses, liverworts, and hornworts) constitute a
large share of the plant diversity at northern latitudes
Data from Sweden (Gustafsson & Ahlén 1996) are used as an example.
Proportion
of world’s species
World
Sweden
found in Sweden
Bryophyte species
14 000
1050
7.5%
Vascular plant species
261 000
1972
0.8%
Ratio bryophyte : vascular
1 : 19
1 : 1.9
—
Even though most ecological theories apply to bryophytes as well as to
vascular plants (Steel et al. 2004), a sound interpretation of population and
community processes must take into account that several morphological, physiological and life-history attributes are basically different in bryophytes. Most
obvious are the simpler morphology with absence of roots, stomata, and in
many species, of conducting tissues, and the peculiar life cycle (Table 10.2).
Most bryophytes are modular and clonal, a fact with a number of ecological
consequences (Svensson et al. 2005), and particularly important is the ability to
regenerate vegetatively from almost any part of the gametophyte after fragmentation (During 1990) and from the specialized asexual propagules produced
by many species of liverworts and acrocarpous mosses. Bryophytes are able
to tolerate a range of habitat conditions owing to a considerable phenotypic
plasticity in morphological or physiological attributes. Finally, dioicy is much
more common in bryophytes than in vascular plants.
Grazing animals, parasitic fungi, and mycorrhiza exert strong influences on
populations and communities of vascular plants, but in most circumstances these
can be ignored in studies of bryophytes. With their low nutrient content, and in
many cases peculiar biochemistry, bryophytes are generally avoided by grazers.
However, in some northern habitats mosses may be heavily grazed. Examples are
several goose species in the Arctic, and mice, voles and lemmings in alpine heath
ecosystems and boreal forests (listed in Prins 1981) where much grazing can occur
under snow cover during the winter. In years, when their populations are large,
lemmings may severely reduce moss biomass in alpine snow beds (Virtanen et al.
1997, and references therein) and boreal forests (Ericson 1977), and strongly influence the species richness and composition. In other ecosystems the most obvious
effect of grazing is to reduce the light competition from vascular plants, and as
secondary effects to decrease the amount of litter covering the bryophytes and to
produce small-scale gaps for colonization. Additional effects could be trampling
and fertilizing by grazers. Parasitic fungi may cause necrosis, but lacking roots,
10 Population and community ecology
Table 10.2 Some features that are unique to bryophytes, or more typical for bryophytes than
for vascular plants, and that affect patterns and processes in populations and communities
Attribute
Ecological consequence
Morphology
No roots
*
Photosynthesis, water and nutrient uptake in same
tissue (leaves).
*
Dependent on environment in immediate contact
No stomata in leaves
*
No control of water losses (poikilohydric) or of gas
Most species lack conducting tissue
*
with the green shoot.
(CO2, O2) exchange.
Transport of water in external capillary network
(ectohydric). Some internal nutrient translocation via
cell-to-cell connections (plasmodesmata). Specialized
conducting tissue in few (e.g. Polytrichum), but even these
(endohydric) have mostly external water transport.
Many species grow at apex and
decay at base
*
No accumulation of respiring tissue.
*
Photosynthesizing green part always young; no
senescence.
Physiology
Tolerate desiccation and freezing
*
Less control of growth phenology
*
Quick recovery after dry and cold periods during
vegetation season.
Can grow any part of the year as soon as weather
permits.
than in vascular plants
Life history
Haploid dominant (vegetative)
*
No ‘‘sheltering’’ of recessive alleles in dominant life
*
Dispersal by large numbers covering long distances
stage; all alleles exposed to environment.
phase
Sexual dispersal by spores
but with low probability of establishment.
Male gametes transported in water
to female archegonium
*
Wide distribution of many species.
*
Fertilization usually only between shoots within a
cm–dm distance.
bryophytes are less susceptible to soil pathogens than vascular plants. The full
range of interactions with micro-organisms that occur among bryophytes was
reviewed by During & van Tooren (1990).
10.2
Population patterns and processes
The basis for understanding population processes in a species is its life
history. Life-history traits are characteristics that affect the transition between
395
396
H. Rydin
different stages of the life cycle, such as birth, reproduction, dispersal, and death.
Life-history traits evolve as the organism faces a trade-off in the use of limited
resources, so that, for instance, in disturbed habitats a genotype with a large
number of spores has the highest fitness, whereas in other habitats fewer but
larger vegetative propagules is a more viable strategy. Life-history strategies are
co-evolved integrated combinations of traits, and the most common scheme used
to group bryophyte species based on life-history strategies is that by During (1979,
1992; Fig. 10.1). His classification is drawn on variation in lifespan (annual, few
years, long-lived) and spore trade-off (many small or few large) in response to
habitat duration and distances among suitable habitats (see Chapter 8, this
volume). A more elaborate classification can include breeding system (monoicous, dioicous, and various intermediates), gametophyte size and longevity, presence of asexual propagules, features of the capsule that affect dispersal, and
spore size and number (Longton 1997). In the following sections we will see how
life histories affect population processes. Further details on life histories and their
evolution in bryophytes are found in Longton (1997). For a thorough review of the
reproductive biology of bryophytes, see Longton & Schuster (1984).
10.2.1
Spore production
Sexual reproduction is a process that spans many months and is vulnerable
to environmental stress at all stages. A tremendous variation in spore production
between years can be caused by weather variation. For example, in some boreal
Sphagnum species gametangia are formed in the late summer, and if this period is
dry the next year’s sporophyte production will be reduced. In the next stage, spring
precipitation has an effect on fertilization rates, and finally large numbers of
developing sporophytes abort in dry summers (Sundberg 2002). The total result is
that, even in the generally wet peatland habitat, spore output in some species varies
between years by four orders of magnitude because of desiccation (and may even
totally fail in some years). Similar large effects of variation in wetness has been
demonstrated in such contrasting species as the epixylic Buxbaumia viridis (Wiklund
2002) and the forest floor feather moss Hylocomium splendens (Rydgren et al. 2006).
Monoicous species (potentially selfing) produce spores more frequently than
dioicous ones (Cronberg 1993), which may explain why fewer monoicous
mosses (compared with dioicous ones) are rare (Longton 1992, Laaka-Lindberg
et al. 2000, Söderström & During 2005). In dioicous species the distance between
male and female shoots may limit fertilization, and variation in spore capsule
density will depend on the distribution and ratio of male and female shoots
(Pujos 1994). Sexual reproduction may be completely lacking owing to the
absence of male shoots in the population (Longton & Greene 1979). Rydgren
et al. (2006) found that the probability that a female shoot in the dioicous
398
H. Rydin
Hylocomium splendens produced a sporophyte decreased with distance to the nearest male plant: 85% of the sporophytes had a male plant within 5 cm, and
fertilization beyond 10–12 cm is unlikely in this species. These ranges seem to
hold for a variety of species: McQueen (1985) reported a mean gamete dispersal
distance of 2.2 cm in Sphagnum and Wyatt (1977) reported a mean of 2.1 cm and
maximum of 11 cm in Atrichum angustatum. By experimentally placing a male
shoot in a female carpet of two other dioicous mosses, Rhytidiadelphus triquetrus
and Abietinella abietina, Bisang et al. (2004) similarly found that almost all fertilizations occurred within 12 cm. However, they also noted that water flow governed
by microtopograpy extended the distance, so that downslope (>58) fertilization
easily reached 20 cm, with a maximum recorded at 34 cm. In species with splashcup dispersal of male gametes, such as Polytrichum, it appears that fertilization
distances can easily be over a meter (van der Velde et al. 2001). Cronberg et al.
(2006a) recently showed that arthropods such as springtails and mites could
transfer gametes between patches of Bryum argenteum separated by some centimeters, and that the animals also preferentially visited sexual shoots of the moss.
There is an evolution of fecundity in response to habitat duration and this is
reflected in the proportion of moss species regularly forming spores or gemmae.
In habitats with very short duration (animal excrement) or annual disturbance
(arable fields) 95%–100% of the species form propagules regularly. In habitats
with somewhat longer duration (decaying wood and tree trunks) 60%–70% do so,
whereas in habitats with long duration (grassland, heath, bog) the proportion is
only 25%–30% (Herben 1994; based on data for the British moss flora).
10.2.2
Cost of reproduction
An important issue in life-history theory is the cost of reproduction.
Such a cost appears when reproduction leads to increased mortality or
Caption for Fig. 10.1.
Life strategies of bryophytes according to During (1979; reproduced with permission). The
vertical bars indicate the end of the period during which the habitat is suitable for the species.
Fugitives (a) are species that conclude their life cycle within one year and disperse to ephemeral
habitats with numerous small spores. Colonists (b) have a life span of a few years and are found in
habitats that last somewhat longer. Perennial stayers (c) are longlived and often rely on vegetative
reproduction in stable habitats. Shuttle species have larger spores than the fugitives and
colonists and are adapted to habitats that disappear predictably after some time, so that the
species have to disperse to another habitat patch within the community. There are three
categories that are adapted to different types of habitats depending on how quickly they
produce spores after establishment: annual shuttles (d), short-lived shuttles (e) and long-lived
shuttles (f).
10 Population and community ecology
reduced growth rate such that ultimately reproduction in the future will
decrease. A cost of reproduction has only recently been demonstrated in bryophytes. In Dicranum polysetum growth was lower in shoots that developed
sporophytes than in those where sporophyte formation was aborted or experimentally terminated (Ehrlen et al. 2000), and in Anastrophyllum hellerianum there
appeared to be a higher mortality in fertile female shoots than in males
(Pohjamo & Laaka-Lindberg 2003). In many bryophytes the sporophytes are
minute compared with the gametophyte, and intuitively a reproductive cost
seems unlikely. However, in D. polysetum as much as 75% of the year’s growth
could be allocated to reproduction (Ehrlen et al. 2000). Furthermore, nitrogen,
phosphorus, or potassium, which are limiting nutrients, occur in high concentrations in the sporophyte. It is possible that the reproductive effort in terms of
these nutrients is large and even leads to a significant cost of reproduction for
the gametophyte. Several types of cost appear in fertile female shoots of the
dioicous Hylocomium splendens: reduced number of growing points, higher risk of
shoot termination, and reduced daughter segment size (Rydgren & Økland
2003). As a result, a non-sporulating shoot population has a higher population
growth rate. Since successful spore establishment has not been observed in the
natural habitat of this species it seems unlikely that the sporulating shoots can
reach equal fitness under ‘‘equilibrium’’ conditions (Rydgren & Økland 2002b),
but instead they may be superior in colonizing new substrates.
It is not always that the sporophyte is the most costly part of reproduction. In
the desert dioicous moss Syntrichia caninervis, the reproductive effort in male
organs was larger than in female ones, and this has been proposed as one factor
behind the strongly female-biased sex ratio in this species (Stark et al. 2000).
10.2.3
Dispersal
Several experiments have been made in which a source colony with a
known number of capsules and spores has been set up, and spores collected on
sticky surfaces at different distances. Because the density of spore deposition
decreases rapidly with distance, such experiments can only reveal the shape of
the dispersal curve up to a few meters. In Sphagnum, spore density fitted well to
an inverse power function, i.e., a linear relationship after log-transforming
spore density and distance (Sundberg 2005). Despite the fact that the spore
density was quickly reduced to undetectable levels, a majority of the spores
(60%–90%) traveled beyond the sampled distance of 3.2 m. The proportion of
spores that disappear beyond a few meters is somewhat dependent on spore size
(Miles & Longton 1992), but even in species with quite large spores most of the
spores traveled beyond 2 m (Söderström & Jonsson 1989). The wood-inhabiting
liverwort Anastrophyllum hellerianum has small spores (about 10 mm) and in an
399
400
H. Rydin
experiment more than 50% dispersed further than 10 m (Pohjamo et al. 2006).
Whereas the gradient of the power function for Sphagnum was around 2
(Sundberg 2005; implying that a tenfold increase in distance from source
reduced the spore density by a factor of 100), the gradient for Anastrophyllum
was close to 1 (a tenfold increase in distance leads to a tenfold decrease in
density). Anastrophyllum also produces gemmae of the same size as its spores, and
they can be dispersed equally well (Pohjamo et al. 2006).
These experiments give some understanding of within-community dispersal
and how species can fill small vegetation gaps created after disturbances.
However, since they predict near-zero spore density at distances beyond a few
meters, extrapolations to between-community dispersal or species migrations
should be made with caution. For epiphytes (which start their dispersal at some
height above ground) a somewhat more realistic appreciation of spore densities
at longer distances can be achieved with functions other than the commonly
used inverse power or negative exponential. In particular, the log-normal function is considered useful and realistic, and gives a ‘‘fatter’’ tail (i.e. higher densities
at larger distances). Dispersal experiments indicate that a single patch has a great
impact on spore deposition at close range, but for dispersal at a larger scale
(colonization of more isolated sites), spores produced by numerous sources
further away play an increasingly important role.
At a larger geographic scale, colonizations depend on events that may occur
with very low probability but over a much longer time. To study this, spore
trapping is not a feasible method. Instead dispersal can be inferred from distribution patterns, and especially useful are habitats that are of known age and/
or of known distance from dispersal sources. In the northern part of the Baltic
Sea, the land is rising at a rate of 5–9 mm yr 1, and the height of an island is a
measure of its age. Colonization patterns on islands can thus be related to age,
size, and distance from the mainland. In a study of Hylocomium splendens molecular markers were used to identify clones (Cronberg 2002). There was a linear
relation between number of clones and island age, increasing from on average
12.5 clones on an island 100 yr old to 27.5 at 300 yr, but no indications of
isolation by distance. With increasing island age the moss patches tended to
be multiclonal, indicating repeated recruitment to the island. This species is
dioicous, and the probability that male and female shoots colonize the same
patch is low. Therefore only the oldest island had spore capsules and it may take
as much as three centuries before any dispersal can take place within or
between islands.
Species of Sphagnum also colonize the uplift islands in the Baltic Sea to form
patches in rock crevices. Island species richness correlated positively with
island area, but not with distance from the mainland (up to 40 km) or island
10 Population and community ecology
age (Sundberg et al. 2006). The species were differently successful in reaching the
islands. The highest colonization rate was found in species with a high regional
spore output, which was estimated by the product of regional abundance,
sporophyte frequency, and number of spores per capsule. Similar to
Hylocomium, the rarity of spore capsules in most species on the islands indicates
the mainland as a source for colonization rather than dispersal among islands.
Another system indicating the effectiveness of long-distance dispersal in
Sphagnum is peat pits, in which block-cut peat extraction has ceased and left a
bare peat surface. After 50 years, abandoned pits in eastern Sweden contained
species that are not observed in natural peatlands in the region, such as
S. lindbergii, S. aongstroemii, and S. molle, as evidence for spore dispersal over
tens of kilometres (Soro et al. 1999). The ecological importance of Sphagnum
spores have been questioned, since their germination seems to be strongly
phosphorus-limited in most peatland habitats. However, recent experiments
show that they germinate readily in the presence of decaying vascular plant
litter or animal faeces (Sundberg & Rydin 2002), and the studies on islands and
in peat pits show that spores are indeed important for establishment in disturbed and newly formed wetlands. Similarly, Miller & McDaniel (2004) could
demonstrate dispersal over at least 5 km of calcicole species reaching mortared
(i.e. calcium-rich) roads built 65 years ago in an area with acidic rocks in New
York State, U.S.A.
One way to test the importance of dispersal vs. habitat limitation is to
experimentally introduce diaspores. Lloret (1994) compared the success of
three dominant forest floor mosses to colonize experimental gaps 1 m2. All
three species colonized after experimental planting; this result shows that the
environmental conditions were not limiting. The experiment indicated that
Dicranum scoparium and Hylocomium splendens were dispersal-limited, whereas
Pleurozium schreberi was not, and this species probably colonized effectively
from the adjacent carpet. Such short-distance dispersal may often be by vegetative fragments or specialized asexual diaspores produced in many species. For
such diaspores it is generally concluded that effective dispersal is in the centimeter range (Laaka-Lindberg et al. 2003), with the above-mentioned small gemmae in Anastrophyllum hellerianum as exceptions.
We normally assume that bryophytes are wind-dispersed, but other vectors
may be involved. In wetlands and along rivers, fragments and spores could
easily be water-dispersed (Dalen & Söderström 1999). The adaptation to dispersal by flies in Splachnaceae is discussed below. Breil & Moyle (1976) found
65 species of bryophyte in birds’ nests in Virginia, U.S.A.; this finding indicates
that birds may assist in the dispersal of fragments as they forage (for instance in
bark crevices) and collect nesting material.
401
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H. Rydin
A quickly developing research field is to use genetic markers and infer
dispersal from the distribution of haplotypes or from the relationship between
genetic similarity and distance (e.g. Skotnicki et al. 2000, Cronberg 2002, Snäll
et al. 2004a). In the metapopulation section below, an approach in which dispersal distances are modeled from distribution patterns is discussed.
10.2.4
Germination and establishment
The germinability of spores is often high. Hassel & Söderström (1999)
reported that 97% of the spores in Pogonatum dentatum germinated in the laboratory, and they found similar values for other species in the literature.
Establishment in the field occurs with much lower probability; even when spores
are spread out experimentally in what appears to be a suitable habitat, establishment probabilities seem to be of the order of 10 4 to 10 3 (Hassel & Söderström
1999) or even lower. Sphagnum spores hardly germinate at all on the peat where the
adult plants grow; some nutrient additions from decaying litter seems to be
required (Sundberg & Rydin 2002). Spore germination is of course dependent on
moisture, and an example of the highly specific requirements during spore germination comes from studies of Neckera pennata (epiphyte on tree trunks) and
Buxbaumia viridis (on decaying wood). The germination depends on an interaction
between moisture and pH so that high water availability facilitates germination at
suboptimal pH, and vice versa (Wiklund & Rydin 2004b). For Neckera, which
normally occupies rather desiccation-prone tree trunks, this may explain its preference for host trees with high pH where it can germinate quickly and therefore
exploit the short windows of opportunity with wet bark after rain events. Not only
is spore germination difficult, but there is probably also high mortality in the
protonema stage (Lloret 1991) as an effect of desiccation (Thomas et al. 1994).
Establishment from vegetative fragments has a much higher probability of
success, but is a habitat-sensitive process, too (Cleavitt 2001). A very practical
example are the methods developed for re-establishing Sphagnum on peatlands
after peat harvest (summarized by Rochefort et al. 2003). Here fragments are
used, and for success the hydrology must be controlled to produce a wet peat
surface and the fragments need initial protection by a layer of straw mulch.
Hence, the technique highlights the fact that surface desiccation is the critical
factor for the establishment of bryophyte fragments.
10.2.5
Diaspore banks
The presence of spores as a diaspore bank in the soil has been demonstrated for many species (During 2001), and it also appears that gemmae can
enter a state of dormancy (Laaka-Lindberg & Heino 2001). The ecological importance of the diaspore bank is difficult to assess, but it suggests at least a potential
10 Population and community ecology
Table 10.3 The relative contribution (%) of bryophytes with different life-histories
in the diaspore bank and in the vegetation in Dutch chalk grassland sites
Data are for an average of three sites (During & ter Horst 1983) and Swedish boreal forest
(Jonsson 1993). The numbers relate to abundance of the different strategies, not to number
of species.
Chalk grassland
Life history
Diaspore bank
Vegetation
Colonists
76
1
Short-lived shuttle species 12
Long-lived shuttle species
—
Perennials
10
Annual shuttle species
Boreal forest
Diaspore bank
Vegetation
27
32
<1
4
—
—
14
23
<1
—
15
15
56
18
84
for secure and rapid colonization after disturbance. In Swiss arable fields
15 species germinated from soil samples. Five of these were not present in the
surface vegetation, and only four species in the vegetation were absent from the
diaspore bank (Bisang 1996). From a mixed forest in New Brunswick, Canada,
Ross-Davis & Frego (2004) list 29 species from the diaspore bank, of which 13 did
not appear in the extant community. From peat samples down to 30 cm, regeneration of three Sphagnum and eleven liverwort species was observed (Clymo &
Duckett 1986, Duckett & Clymo 1988). Many of the shoots came from buried
stems, indicating that these may retain a regenerating capacity up to perhaps
60 years. Some plants probably also developed from spores, and experiments
with buried Sphagnum capsules show that spores may survive for several decades, perhaps even a century (Sundberg & Rydin 2000), an observation that will
increase the significance of the spore bank.
As in flowering plants, the representation of species in the diaspore bank is
strongly related to life-history attributes. Relative to their abundance in the
vegetation cover, colonists are considerably more common than perennials in
the diaspore bank (Table 10.3). As expected, monoicous species with frequent
production of spores or gemmae are often found in the diaspore bank, but
contrary to observations in seed banks (where small seeds are often numerous),
Jonsson (1993) noted that the species found in the diaspore bank had on average
larger spores than those found in the vegetation cover.
10.2.6
Clonal expansion and population persistence
As noted above, many bryophytes have the capacity to expand and
disperse by vegetative fragments or specialized propagules. Of particular
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H. Rydin
ecological importance is clonal expansion by branching, since the new shoots
benefit from being physiologically integrated with the mother plant and hence
have a higher chance of survival than detached propagules. Clonal species may
be very persistent (During 1990), and Sphagnum individuals can probably survive
for centuries (Rydin & Barber 2001) as they slowly expand clonally and at the
same time avoid a respiratory burden by losing old tissue to peat formation.
A distinction is sometimes made between ‘‘guerrilla’’ and ‘‘phalanx’’ strategies of clonal growth. Among bryophytes the typical phalanx species are the
acrocarps forming dense cushions, whereas guerrilla species are weft- or matforming pleurocarps (Cronberg et al. 2006b). Even in the phalanx type clones
tend to mix with time since the mixing is not merely dependent on the type of
clonal growth but also on longevity, spore dispersal, etc. For example, a square
decimeter of Hylocomium splendens often has 2–3 genotypes, and sometimes even
5 (Cronberg 2004). The presence of guerrilla and phalanx species has several
community consequences (review in Svensson et al. 2005). Phalanx growth leads
to aggregation of individuals of the same species which diminishes the interspecific competition, whereas guerrilla species evade intraspecific competition
and encounter more interspecific contacts. Expanding as a physiologically integrated front, phalanx species are generally considered strong resource competitors in an undisturbed community. Instead guerrilla ramets carry fewer
resources from the mother plant, but they could capture new space effectively,
and be good at pre-emptive competition.
Clonal growth potentially gives the plant an opportunity to explore the
habitat, thereby reaching positions with favorable conditions. There are not
many tests of such ‘‘foraging’’ in bryophytes, but experiments by Rincon &
Grime (1989) indicate that species with high growth potential (Brachythecium
praelongum and Thuidium tamariscinum) may have some ability to expand laterally
from dark to light patches.
10.2.7
Density-dependence in bryophyte populations
Intraspecific competition in vascular plants is often described by the
negative effects (such as decreased growth or increased mortality) that follow
from increasing shoot density. For example, if the reduced growth per individual exactly compensates for increase in density, the total biomass produced
per unit area will be independent of sowing density as described by the law of
constant final yield. When mean shoot mass is plotted against density in a log–log
diagram a slope of approximately –1 is observed (i.e. a tenfold increase in density
results in a tenfold decrease in shoot size, Fig. 10.2). In many cases, an increase
in density is also followed by an increase in mortality. This is referred to as selfthinning, and it has often been found that the average size of the surviving
10 Population and community ecology
Fig. 10.2. Conceptual models of density-dependence in plant populations showing the log–log
relation between density and individual plant size. Plants are sown at different densities, and
the growth of the individuals per unit time (e.g. per month) is lower at higher density (as
indicated by the shorter arrows). If the population follows the law of constant final yield the total
biomass produced per unit area will be independent of sowing density. Dense populations often
suffer from earlier and higher mortality (as indicated by the arrows showing a reduced density
as the plants grow), and many natural populations fit a line with a slope of approximately –1.5;
hence the
3/2 self-thinning rule.
individuals increases more rapidly than density decreases. The result is that
many natural populations fit a line with a slope of approximately –1.5, a pattern
that is referred to as the 3/2 self-thinning rule (Fig. 10.2; Begon et al. 2006).
Collins (1976) found that log mass–log density slopes for Polytrichum alpestre in
the maritime Antarctic were in the range –0.66 to –0.82. This indicates a weaker
intraspecific competition than predicted by the law of constant final yield, so that
increased density led to increased total yield. Although there was a considerable
flux in the populations (up to 37% of the population lost, and equally many gained
over a year), this turnover was not related to density, which remained constant.
Scandrett & Gimingham (1989) assessed intraspecific competition by growing
monocultures of Pleurozium schreberi, Hylocomium splendens, and Hypnum jutlandicum
from fragments that were spread out at densities of 0.8 and 8 mg cm 2 (dry mass).
Yield was in most cases reduced by more than 50% at the higher density, indicating a stronger density-effect on individual size than predicted from the law of
constant final yield. An example in which density-dependence was manifested as
self-thinning was given by Lloret (1991), who observed high mortality rates
among sporophytes in dense populations of the coprophytic Tayloria tenuis.
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While the above studies exemplify expected negative effects of density, the
largest difference between bryophytes and vascular plants is that in bryophytes
we often note positive effects of increased density on shoot growth, reproduction and survival. The reason is that bryophytes are poikilohydric (Table 10.2),
and water losses are higher from a separate shoot than from a shoot in a dense
carpet. We may expect that the effect should be larger in ectohydric species than
in endohydric ones, but so far decreased water loss with increasing density has
been demonstrated in both types and in a variety of growth forms, exemplified
by Polytrichum formosum, Leucobryum glaucum, Rhytidiadelphus triquetrus (Filzer
1933), and Sphagnum (Li et al. 1992). Tallis (1959) stated that the evaporation
rate in Racomitrium lanuginosum was four to six times lower from a compact
carpet than from an isolated shoot. As in vascular plants, the effect of shading
at high density can lead to etiolation (long slender shoots), but although this
plastic response leads to smaller shoots it need not result in self-thinning. Bates
(1988) grew Rhytidiadelphus triquetrus at a range of shoot spacing and noted that
individual growth increased with increasing density. There was no mortality,
and the production of offshoots was not restricted by initial high density. Hence,
total growth was highest in dense populations. Watson (1979) studied several
coexisting species of the Polytrichaceae that could be aged through their distinct annual growth increments. She noted a positive relation between shoot
density and mean age in the populations, indicating that increased density led
to increased shoot longevity. Water and light availability will determine how
biomass growth is affected by density (Pedersen et al. 2001), but overall it
appears that in most cases the positive effects on moisture outweigh the negative effects of shading (van der Hoeven 1999).
In experiments with Sphagnum some negative effects of density on net recruitment (number of new shoots minus mortality), were observed (Rydin 1995). In
most cases this negative density-dependence was weak, so that shoot density
increased during the experiment even in samples that started with a density
similar to natural ones. This reflects the phenotypic plasticity in Sphagnum;
although there is an upper size limit for a shoot, there is virtually no limit to
how slender a Sphagnum shoot can be. In S. tenellum, for example, the natural
density is about 10 capitula cm 2, but occasionally populations can be three
times as dense (Rydin 1995). As demonstrated by Hayward & Clymo (1983)
Sphagnum carpets are controlled by an intriguing balance between shading and
desiccation. Shoots growing more rapidly in length than their neighbors will be
more prone to desiccation, which leads to diminished growth. In contrast,
shoots that accumulate less biomass will escape burial as long as they can
form slender but tall shoots through etiolation. In the extreme case they will
of course be overtopped, but since shoot size is very plastic they can keep their
10 Population and community ecology
apex at the surface even if the shoot becomes very slender. This explains how
Sphagnum mats maintain a very smooth surface by forces acting on individuals.
Shoot size variation can be even larger in other bryophytes. In Hylocomium
splendens, shoot size can vary by a factor of 1000 (Økland 1995, 2000) indicating
a considerable potential to avoid burial. Thinning and disturbance can also lead
to increased size variation when light suddenly reaches farther down and
activates sprouting from basal parts (van der Hoeven & During 1997).
10.2.8
Population dynamics in Hylocomium splendens: a case study using
matrix modeling
The use of matrix models has been a standard method in the study of
population dynamics in animals and vascular plants for some time (Caswell
2001), especially for structured populations. Such a population can be divided in
discrete classes (according to size, age or stage, or a combination) and the fate of
each individual is followed from one census to the next, most often from one
year to the next. Using these data a matrix is produced with transition probabilities between stages. The number of individuals in each stage in the next
year is calculated by multiplying the transition matrix by the vector of number
of individuals in each stage class, and by doing this repeatedly, the long-term
population growth rate, l, can be calculated (l > 1 in a population that increases
in numbers, l ¼ 1 in a stable population and l < 1 in a decreasing population).
Matrix models may thus be used to project future population sizes. As for all
models certain assumptions are made; for the basic matrix models (the deterministic ones) the most important one is that biotic and abiotic conditions
recorded at the time data were collected will not change. Other outputs we get
from this type of analysis are stable age–size–stage structures, reproductive
values (the expected number of offspring produced by individuals in different
life-stage class per time interval), and different measures of sensitivity of population change to variation in transition probabilities. The most commonly used
matrix models also assume that the transitions are independent of history, that
is, the fate of an individual depends only on its present stage, not on its previous
history. For bryophytes this is probably a reasonable assumption.
The practical difficulties in marking and relocating very small plants have
restrained most bryologists from using matrix models. An extremely thorough
study of population dynamics in bryophytes is that by Rune Økland and associates on Hylocomium splendens (Økland 1995, Økland & Økland 1996, Økland 1997,
Rydgren et al. 1998, Økland 2000, Rydgren et al. 2001, Rydgren & Økland 2001).
They use colored plastic rings to tag individual shoots and are thus able to follow
the fate of these over many years. Some results from their papers are compiled
in the following section, to illustrate population processes in bryophytes and
407
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H. Rydin
Fig. 10.3. Life-cycle graph and transition probabilities in Hylocomium splendens from a study in
SE Norway, simplified from Rydgren & Økland (2002a) by merging some stage classes. Circles
represent the different stages in the life cycle, and arrows are the transitions from one stage to
another. Most often the current year’s vegetative segment (S) produces a growing point (G)
forming next year’s segment (this is the S ! S loop with probability 0.78). Sometimes an extra
growing point develops on the current (G0) or last year’s (G1) segment. Growing points (G2) can
also develop from older segments or on detached segments of unknown age (in the model such
segments are treated as a diaspore bank, D). Peculiar to this life-cycle is that spores and spore
bank are not included: earlier studies had implied that they were unimportant in mature stands
of Hylocomium.
also to indicate the usefulness of the method. A methodological summary was
given by Rydgren & Økland (2002a) in which they suggest that this method can
be applied to a range of bryophytes.
The first and critical point is to identify the life-cycle stages in a way that is
biologically meaningful and reproducible. With its peculiar annually reiterating
growth form, Hylocomium splendens is a classic example (Fig. 10.3). From each
segment (‘‘frond’’) a new growing point normally develops to form next year’s
segment. In some shoots an extra growing point develops, and sometimes
growing points emerge also from older segments. The population size does
not refer to number of physiologically independent units, but instead reflects
the total number of active growing points. Which study units will be appropriate depend on the structure of the plant; in non-clonal plants the individual
shoots can be used, but in clonal plants number of ramets, modules, or meristems must normally be used as a measure of population size.
The life cycle in Hylocomium splendens is (as in clonal plants in general)
characterized by shoot persistence: a large majority of the current year’s segments form a growing point (G) to build a new segment next year (S ! S loop
with probability 0.78 in Fig. 10.3). Extra growing points (G0), and new growing
10 Population and community ecology
points in one-year-old segments (G1) are much rarer, but once formed they have
a very high probability of developing into a new segment, which leads to
branching of the moss: an increase in population size. Even regenerations by
growing points developing on older segments or on detached segments of
unknown age (G2; acting as a ‘‘diaspore bank’’) have a high probability of
growing into a mature new segment. Matrix models not only predict the growth
or decline of the population and changes in numbers in the different life-stages,
they also suggest which stages and transitions have the highest influence on
changes in population size. This is referred to as elasticity, which measures the
proportional change in l as a function of a proportional change in the transition
probability (elasticities for all transitions sum to 100%). In Hylocomium it seems
that elasticity for the S ! S loop (persistence via a normal growing point) is
normally in the range 60%–70%, whereas all other transitions in general have
values <10%. This is probably quite typical for long-lived perennials.
Detailed monitoring of natural populations and thinning experiments have
revealed both negative and positive density-effects. One negative effect was the
reduced regenerations from old segments (G2) with increasing density. Another
was the increased risk that shoots were overtopped and buried by neighbors. By
contrast, density and segment size are positively correlated, which can be
attributed to the more favorable moisture regime in denser carpets. Larger
segments have a higher probability of forming new growing points, larger
daughter segments, and lower risk of termination. Density effects on reproduction are central in population studies of vascular plants, but studies on bryophytes are rare. As indicated in the section on spore production above, density
may also have both negative and positive effects on reproduction. Reduced
density stimulated sporophyte production, probably through reduced shading,
but the increased distances between male and female shoots may be problematic at too low a density: all in all, it appears that the direct effects of density on
population regulation are relatively weak, and the indirect effect of segment
size is stronger.
While the basic use of matrix models – to project future changes in population size – assumes that the transition probabilities are the same from year to
year and that they are not affected by population density, the effects of external
factors can be studied by comparing the transition probabilities among years
and sites. Variation in population dynamics among sites is expected and related
to microclimate and other local factors. More interesting is that some of the
between-year variation is synchronous in different localities: favorable (wetter)
years result in larger segments with higher probability of successful production
of next year’s segment (survival of growing point G; Fig. 10.3). The variation in l
between years (0.87–1.22) in Hylocomium is similar to values reported for vascular
409
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H. Rydin
clonal plants in these forest communities. Even short wet periods in a critical
period of the year can lead to bursts of regeneration from lower and detached
segments (growing point G2), and in years with large lemming and vole populations, grazing under snow can have large impacts on the demographic structure.
10.3
Metapopulation patterns and processes
Many bryophyte species grow on substrates that are patchily distributed, such as boulders, dead wood, and tree trunks. Lacking a root system that
could ‘‘explore’’ the surface and deeper soils, bryophytes are more strongly
linked to substrate patches than are vascular plants. For these reasons, metapopulation theory is particularly applicable to bryophytes. A metapopulation is a set
of populations linked by dispersal. A patch is the place with conditions that are
suitable for the species, for instance the tree trunk for an epiphytic species.
Where the species is present in a patch it is referred to as a local population. Local
dynamics are caused by population processes and interactions with other species.
The local population may eventually become extinct – local extinction – in which
case it can only re-occur if it is successfully dispersed from another local population in the metapopulation. The occupancy – the proportion of patches that is
occupied by the studied species – is determined by the balance between local
extinctions and colonizations.
Several types of metapopulation model have been developed over the past
decades, and they somewhat differently describe the factors affecting local
extinctions and colonizations. A common assumption is that local population
size fluctuates with time because of demographic and environmental stochasticity, and the larger the population, the smaller the extinction risk. Since
population size is often correlated with patch area, many models use patch
area as a predictor for extinction probability (the larger the area, the lower the
extinction risk). In early metapopulation models the immigration (recolonization) probability was the same for all patches, but in most modern models
immigration probabilities depend on patch connectivity, which is a central concept in metapopulation theory. It is inversely related to isolation and should
reflect the expected number of immigrants arriving at the patch per unit time
(Hanski 1999). A patch has high connectivity if it is surrounded by many other
patches, if the distances to these patches are small and if they host large
populations of the studied species (see Fig. 10.4 for details). If a statistical effect
of connectivity on the occupancy pattern can be established, it is taken as an
indication of dispersal limitation. The fitted slope parameter of the connectivity
function ( ) indicates how quickly the influence of a source patch declines with
distance, and hence gives an indication of effective dispersal distances. More
10 Population and community ecology
Species present
i
dij
Species absent
Connectivity for patch i, Si = ∑ exp(–α dij) Nj .
j ≠i
Fig. 10.4. The connectivity of the focal patch i, Si, describes the expected number of
immigrants per unit time from the surrounding patches j (Hanski 1999). In this graphic
model diaspore density is shown by the width of the grey wedges. The surrounding patches
are at different distances (dij) from the focal patch, have different areas (circle size), and are
occupied (filled) or unoccupied (open). In the equation, Nj represents the potential diaspore
output from patch j, most realistically measured by the population size. Since population
sizes are often unknown, area is commonly used as an indicator of population size (Nj ¼ 0 if
the species is absent and Nj ¼ Aj if it is present). More simply, but less realistically, Nj could
represent presence (Nj ¼ 1) or absence (Nj ¼ 0) of the study species. In the simplest form all
patches are equal (Nj ¼ 1). The parameter
determines how quickly the diaspore
rain decreases with increasing distance from the source patch according to the negative
exponential function. In some cases, e.g. for epiphytes, a log-normal function is often
considered more realistic than the negative exponential (see, for example, Snäll et al. 2005
for details).
rarely, experimentally measured dispersal curves (e.g. Söderström & Jonsson
1989) could be inserted in the connectivity function.
The connectivity measure illustrates an important aspect of metapopulations, namely source–sink dynamics. A local population in a patch with negative
population growth rate is doomed to extinction (sink population), but it may
reappear because other patches with positive growth rates (source populations)
deliver a surplus of migrants. The patches thus have unequal influence on the
metapopulation, and the exporting patches would be the ones that are large or
411
H. Rydin
Extinct
100
Occupancy (%)
412
Dispersallimited
Substrate-limited
75
50
25
0
10–10
10–9
10–8
10–7
10–6
10–5
Establishment probability, Pest
10–4
10–3
Fig. 10.5. The effect of spore establishment probability (Pest) on the metapopulation occupancy
(proportion of patches occupied). Over a narrow range of Pest the metapopulation is
dispersal-limited. If the Pest increases, all patches will become occupied and the species
becomes substrate-limited. If Pest decreases the metapopulation is unable to persist, and
becomes extinct. Redrawn from Herben & Söderström (1992).
have high habitat quality. By incorporating the area or population size of
surrounding patches in the connectivity measure (Fig. 10.4), the metapopulation model will capture the essence of source–sink dynamics.
In metapopulation models ‘‘colonization’’ summarizes two processes that are
in practice quite difficult to separate: dispersal and establishment. A crucial
parameter is the probability that a diaspore establishes once it has reached the
patch. With a simulation model based on field data for the fugitive species
Orthodontium lineare growing on decaying wood patches, Herben et al. (1991)
suggested that the range of values under which the establishment probability
affects the metapopulation size is rather narrow. Within this range the metapopulation is dispersal-limited (Fig. 10.5). With increasing establishment success all patches will become occupied, and the metapopulation size becomes
substrate limited (Herben & Söderström 1992). For lower probabilities the metapopulation will become extinct because the colonization rate cannot match the
extinction rate.
Metapopulation theory pictures the landscape as consisting of hospitable
patches and an inhospitable matrix. This applies well to species that are confined to such patches, but makes the theory unsuitable for, for example, facultative epiphytes. Even for species that are truly confined to the particular
substrate type, a notorious difficulty is to determine whether an unoccupied
patch is in fact hospitable. It is often necessary to use rather rough criteria to
10 Population and community ecology
define the ‘‘suitable’’ patches in a study; for epiphytes one may, for example, assume
that all trunks of a host tree species are suitable patches even though many suitable
patches of the same tree species are never colonized for unknown reasons.
Traditionally, studies of bryophytes focused on substrate factors (Chapter 8,
this volume) to explain the presence and composition of species, whereas
metapopulation studies focus on colonization–extinction dynamics, dispersal
limitation, and the spatial configuration of the patches in the landscape. Recent
studies combine the approaches by trying to disentangle the relative importance of substrate quality and colonization–extinction dynamics for the occupancy pattern. Another recent development is models that account for the fact
that the patches are also dynamic. They may change in quality over time, and
more importantly they may have a limited duration. Boulders are permanently
available patches, tree trunks last for decades to centuries, and dung patches for
a couple of years (and are open for new colonizations only when the dung is
fresh). It is therefore necessary to include in metapopulation models the fact
that extinctions can happen as a deterministic effect of patch destruction. New
patches arise at different spots, so the connectivity pattern also changes over
time. How important the dynamics of patches is depends on the patch turnover
rate. At one extreme, classical metapopulation models assume that patches are
invariable in quality and position, and all extinctions are caused by internal
population dynamics. At the other end of the spectrum is a system in which the
local populations are extremely persistent and the only factor that causes local
extinction is the destruction of the patch. In the latter case the species must
have the capacity to disperse to new patches as these appear, and this can be
referred to as a patch-tracking metapopulation (Snäll et al. 2003). In the following, bryophyte metapopulation processes are exemplified for species growing
on dung patches and for epiphytes on tree stems, but the ideas apply also to
other systems, such as epiphyllous bryophytes (Zartman 2003, Zartman & Shaw
2006, Zartman & Nascimento 2006) and decaying logs (see Söderström & Herben
1997 for a general review).
10.3.1
Bryophytes on dung: patch quality, local interactions,
and metapopulation processes
Several species of Splachnaceae growing on droppings of large mammals exemplify the dynamics of mosses confined to ephemeral, patchy habitats.
The moss spores are dispersed from one dropping to another by flies, which also
are dependent on the dung for their breeding. Both the moss and the insect have
to conclude their life cycle before the dung patch becomes inhospitable. The
moss species attract somewhat different sets of flies (Marino 1991a), and each
moss species is dispersed by 10–17 fly species. The adaptation is remarkable:
413
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H. Rydin
several species have a long seta with the hypophysis under the capsule bright
red or yellow and even umbrella-shaped. Most important is probably that entomophilous species have sticky spores and produce volatile attractants (Pyysalo
et al. 1983). The following discussion of the processes affecting coexistence
and persistence of Splachnum ampullaceum, S. luteum, Tetraplodon angustatus, and
T. mnioides growing on droppings of large mammals is based on the thorough
investigation by Marino (1991a,b,c, 1997).
Marino noted that unoccupied droppings were rare, and that the mosses
often occupied the whole dung patch. This contrasts with many epiphytic
systems and indicates that local interspecific competition is superimposed on
the metapopulation processes and may strongly affect local extinctions and
spore output from the patches. Each species produced more spores when growing alone than when co-occurring in a mixture with another species, an observation that indicates resource competition. However, the competitive ability
was dependent on habitat. In wet habitats Splachnum species had a competitive
advantage, produced more spores, and even eliminated Tetraplodon, and in dry
sites the relations were reversed. The fundamental niches seem largely to be
overlapping, and in absence of competitors the species could occupy both
habitat types (Marino 1991b). The altered competitive relations may be
mediated by habitat effects on patch chemistry, and this causes the infrequency
of co-occurrence between species of Splachnum and Tetraplodon so that Splachnum
was found in peatlands with Sphagnum and brown mosses and Tetraplodon in dry
upland sites with Cladonia lichens and feather mosses. Competition between
congeners was rather symmetric, but from laboratory experiments it appears
that Splachnum ampullaceum was slightly competitively inferior to S. luteum in wet
habitats (Marino 1991b). Balancing this, flies captured on S. ampullaceum carried
more than twice as many spores as those on S. luteum, and several of the flies
specializing in S. ampullaceum were also strongly related to wetland habitats,
indicating some degree of colonization–competition trade-off.
Theoretical models, for instance lottery models, suggest that competitive
species may coexist if they have equal chance to be the first settler as sites
become available for colonization. Of particular interest is that coexistence of
competitive equivalents should be facilitated by phenological separation
(Fagerström & Aº gren 1979) if patches are renewed randomly in time. The first
diaspore to arrive has an advantage so that the phenological separation may
lead to pre-emptive space competition among the dung mosses. Spores of
Tetraplodon angustatus were dispersed in May (Marino 1991a) and T. mnioides
and the Splachnum species in the summer from mid-June. The power of preemption should be especially strong in this case since the dung patch is suitable
for the insects for a very short time, with almost all visits taking place during the
10 Population and community ecology
first day. For this reason, the metapopulation of T. angustatus is probably rather
independent of the other species since it is based on a different set of patches:
those deposited in spring.
Dung patches have a more rapid turnover than most other patch types
inhabited by bryophytes. To understand the metapopulation one must account
for the short time window for colonization, and that local extinctions may be
caused by interspecific competition. We do not have a spatially explicit model
for Splachnaceae, but Marino (1991c) has attempted to model the relative
importance of different factors for the Splachnum species. The model implies
that the number of patches, interspecific competition and aggregation within
species were all important in explaining the persistence time of the metapopulations. Aggregation may follow, for instance, from short dispersal distances,
and its effect would be to decrease the degree of interspecific contacts and hence
promote coexistence by reducing the risk of competitive exclusion (Bengtsson
et al. 1994).
10.3.2
Epiphytes: local environment, connectivity and tree dynamics
Bryophytes confined to deciduous trees that occur as scattered individuals in an otherwise inhospitable conifer forest matrix are useful study
systems. Here it is possible to test the relative importance of local factors,
patch connectivity and tree dynamics for the occupancy pattern. A starting
point is to verify that the study species is really confined to one or several tree
species, so that all suitable trees (hosts) can be mapped and checked for occurrence of the epiphyte. Such epiphytes generally do not appear on saplings of the
host, and therefore a lower diameter limit can be set for the host definition. The
next step is to measure relevant local environmental variables. The selection is
difficult and must be based on previous knowledge on the biology of epiphytic
bryophytes in general and the focal species in particular. Tree species (if several
hosts are used) together with age and/or diameter are obvious variables, and
substrate factors of interest are depth of bark crevices (indicating microenvironmental variation) and bark pH. The local environment also includes microclimatic measures of light, temperature, and humidity. These can be measured
directly, but more commonly indicated by crown cover, stem density, shading,
local soil moisture, etc.
Heegaard (2000) partitioned the variance in the distribution of Ulota crispa in
mixed forests in Norway. A regression model could explain 55% of the variation
of number of moss cushions per forest plot (2.5 m 2.5 m). Of this 20% could
be accounted for by metapopulation processes (i.e. related to number of host
trees per plot and spatial co-ordinates) and 20% by substrate factors. Since tree
density influences both the environment (shading) and dispersal distance, the
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H. Rydin
remaining explained variance could not be split into substrate and patch
dynamics. A tentative conclusion was then that dispersal and habitat factors
were approximately equally important.
Intuitively, spatial aggregation of the epiphyte would indicate dispersal limitation, but such aggregation could also follow from an aggregation of host trees
or from spatial variation in environmental factors (Hedenaº s et al. 2003). A useful
strategy is instead to test how well the occupancy pattern can be predicted from
patch connectivity, given that the environmental factors have been accounted
for. An example of this approach is the study of Neckera pennata growing on
broadleaved trees in a conifer-dominated landscape in eastern Sweden. The
species occupied 30% of 1050 studied trees in three forest stands. The probability
of finding N. pennata on a particular host tree increased with tree diameter and
depth of bark crevices, and it differed among tree species, with Acer platanoides
having the highest, and Populus tremula the lowest occupancy (Snäll et al. 2004b).
Tree diameter, crevices and tree species were approximately equally important,
but, in comparison, connectivity had a much stronger effect (Fig. 10.6) which
resulted in a spatial aggregation of the Neckera in these forests.
200
150
χ2
416
100
50
0
d
an
St
ies
ID
e
e
Tr
s
c
pe
.
e
e
Tr
r
Ba
e
ic
ev
r
kc
h
n
pt
m
dia
de
ee
Tr
tio
na
cli
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Tr
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a
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So
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t
ois
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Co
Fig. 10.6. The effects of environmental variables and connectivity on the probability of
occurrence of Neckera pennata on deciduous host trees in coniferous forests in eastern Sweden.
Connectivity was here calculated according to a log-normal function based on population size
of N. pennata on potential source trees. The w2 for each predictor variable indicates its
importance for explaining the occurrence of N. pennata. Occupancy differed among sites and
tree species. Tree stem diameter and depth of bark crevices had positive effects on occupancy,
but connectivity appeared to be more important than all the environmental variables together.
Based on data in Snäll et al. (2004b).
10 Population and community ecology
Patch area is obviously an important variable for metapopulation processes,
and tree diameter is often a good predictor for occupancy and cover of many
epiphytes (McGee & Kimmerer 2002). However, the causal relationship is
obscure since tree diameter affects the occupancy in several ways, as follows.
(1) The area per se effect, by which larger areas have larger populations and
therefore lower extinction risks. (2) Larger trees are older and have had longer
time to catch diaspores, which for Neckera seemed to be the most important
mechanism (Snäll et al. 2005). (3) Larger trees have had longer times to develop
spore-producing colonies, and dispersal within the tree can increase population
size and decrease the extinction risk. In Neckera pennata, for example, it was
estimated that first spore production occurs when the moss patch is 20–30 years
old (Wiklund & Rydin 2004a). (4) The bark structure, and probably also its
chemistry, changes with tree age. A complete separation of habitat factors and
dispersal limitation is obviously difficult.
Trees die and new trees are established, and an understanding of the effect of
the dynamics of the patches requires repeated surveys. In the Neckera project,
the sites were re-analyzed after 2 and 4 years, and even such a large effort yielded
only a few colonizations and extinctions; hence the conclusions are somewhat
tentative. Starting with 280 of 831 trees being occupied in year 0, there were
38 colonizations, 3 extinctions on standing trees, and 5 extinctions caused by
tree death in the first year (Snäll et al. 2005). Thus, indications are that ‘‘deterministic extinctions’’ caused by the death of host trees are at least as important
as ‘‘metapopulation extinctions’’, but even though a considerable number of
trees fell, the metapopulation is growing. Once established, epiphytic bryophyte
populations seem quite resistant to the extinction causes depicted in classical
metapopulation theory. The fact that many extinctions are caused by patch
destruction means that extinctions may often occur when the local population
is large, rather than striking small populations (as in the classical metapopulation model).
There is also a less dramatic form of dynamics in the patch structure with a
successional sequence of bryophytes occupying the tree as it grows and attains a
different bark structure. Some early successional species experience a decreasing patch quality as the tree grows, and the trunk becomes inhospitable long
before the tree falls (Studlar 1982), unless the bryophyte can move to younger
branches of the tree.
The metapopulation concept can be scaled up to model presence/absence of
the species in separate forest stands in a larger landscape. In the Neckera study, it
was possible to define 128 ‘‘suitable stands’’, i.e. forest patches that contained at
least some of the deciduous host trees in a 2565 ha conifer-dominated landscape
(Snäll et al. 2004b). The probability of occurrence of N. pennata in a stand was
417
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H. Rydin
most strongly affected by the densities and stem diameters of the main hosts
(Acer platanoides and Fraxinus excelsior). Also at this scale dispersal limitations were
indicated: occupancy increased with increasing connectivity to other stands
with N. pennata, and it was later found that the occupancy of a number of
other epiphytic bryophytes was also affected by host tree densities and diameters as well as by landscape connectivity (Löbel et al. 2006a). Logging operations have changed the landscape structure, and to some extent a connectivity
measure based on the analysis of 25-year-old air photos could be used as predictor for today’s occupancy of N. pennata and other epiphytes (Snäll et al. 2004b,
Löbel et al. 2006b). This again indicates that the metapopulations are quite
resistant, but also that there is a time lag to extinction, so that these species
may be approaching a new equilibrium with lower metapopulation sizes as a
result of the decreasing landscape connectivity. Forest landscapes are dynamic
also in absence of forestry: in the boreal forests many epiphytes depend on
deciduous trees that appear as successional stages after storms and fire.
The understanding of population processes in epiphytes has increased with
the use of metapopulation models and spatial statistics. Experimental studies
are fewer, but a promising tool is to install tree branches differing in size,
species, bark structure, and isolation to test how environment and connectivity
affect colonizations. Using an experimental approach in Douglas fir stands in
Oregon, Sillett et al. (2000) could show that rates of colonization for bryophytes
were higher in old growth forests than in young ones (particularly for Antitrichia
curtipendula).
10.3.3
Bryophyte metapopulations: a synthesis
In general terms we have seen that patch duration, patch size, patch
configuration, patch quality, and internal dynamics (population dynamics,
competition, and small-scale disturbances) can all affect colonizations and
extinctions in bryophyte metapopulations. An attempt can be made to compare
the importance of different factors that affect colonizations and extinctions and
thereby determine the occupancy patterns in different types of patchy substrates (see also discussion in Herben 1994). If the patches are permanent, for
instance boulders, extinctions are caused by demographic and environmental
stochasticity (as depicted in classical metapopulation models), small-scale
within-patch dynamics, or local competition. Deterministic extinctions caused
by patch destruction becomes relatively more important with decreasing patch
duration from tree stems via fallen logs and smaller parts of dead wood to dung
patches and leaves inhabited by epiphyllous bryophytes, and the inhabitants
will have to disperse for successful patch-tracking. In most metapopulation
models colonizations are limited by dispersal, and this should be relatively
10 Population and community ecology
more important in patches that do not differ much in habitat quality or local
environmental condition. Finally, life-history characteristics have evolved in
response to patch dynamics (Southwood 1977); early reproduction is required
to cope with rapid patch turnover, and species with efficient dispersal can
persist in systems with low connectivity.
10.4
Community patterns and processes
Studies in community ecology focus on processes affecting species
composition and richness at local scale. Classical competition theory, founded
on Lotka–Volterra dynamics and Gause’s principle, states that species coexistence must be based on niche separation, otherwise competitive exclusion will
take place and after some time an equilibrium will be reached when the competitively weak species are ousted. While niche separation undoubtedly promotes coexistence, the modern view is that niche-overlapping species often
coexist because the competitive equilibrium is not reached. Habitat conditions
always change (as in a sequence of wet and dry years, for instance) and this may
alter the competitive relations among species. Physical disturbances could open
up gaps in the carpet of competitive dominants and promote species with a
trade-off to colonization rather than competition. In this section we will look at
niche differentiation, disturbance, and competition in bryophyte communities.
10.4.1
Niche differentiation and coexistence patterns
Niche separation among bryophyte species has been demonstrated in
many cases (Slack 1997), by using techniques such as regression models to
demonstrate species response curves (e.g. Gignac et al. 1991), calculation of
niche breadth and niche separation along one or several habitat gradients (for
methods see Soro et al. 1999), separation of species in multivariate analysis of
environmental factors (Hedderson & Brassard 1990, Nordbakken 1996) and
analysis of positive and negative associations of species in small sample plots
(Økland 1994). Niche relations are often discussed in terms of the physiological
and morphological attributes of the species, but as shown in the metapopulation section, a complete understanding of distribution patterns requires that
life-history attributes are also taken into account. Such an approach was taken
by Vanderpoorten and Engels (2002). They found that the presence of many
bryophytes could be predicted by soil variables (by using logistic regression),
and that the predictability of the species was correlated with life-history attributes, such as spore size.
If competition is a strong structuring force, one would expect that bryophyte
species should not be able to coexist in close contact. However, Økland (1994)
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H. Rydin
Table 10.4 Positive and negative associations between pairs of
bryophyte species in a Norwegian boreal spruce forest
The values for positive associations refer to the proportion (of all potential
associations) of species pairs that co-occur in sample plots more often than
expected if they were independently distributed, and negative associations
indicate the proportion of species pair that co-occur more seldom than
expected.
Plot size (m2)
Positive associations (%)
1
13.1
0.3
9.6
0.9
1/16
9.8
2.7
1/64
15.8
2.1
1/256
7.8
2.1
1/4
Negative associations (%)
Data from Økland (1994).
observed that it is much more common that species are positively than negatively associated, i.e. they co-occur in sample square plots ranging in size from
6.25 cm 6.25 cm to 1 m 1 m more often than would be expected if they were
distributed independently (Table 10.4). The rarity of negative associations indicates that interspecific competition was not an important structuring force
at the scales studied. For several reasons more positive associations are to
be expected as the plot size increases. (1) Larger plots will have more environmental variation, enabling species with different niches to inhabit the plot.
(2) Facilitation by assisted water balance is discussed above, and enables interstitial species that require a moss matrix as substrate to inhabit the plot. Such
positive interaction may counteract the effect of competition (During & Lloret
2001). (3) Resource competition in bryophytes can only occur through direct
contacts between gametophytes, and larger plots include shoots that do not
interact. The zone of interaction is within one or a few centimeters, in contrast
with vascular plants where shading and root interactions can span over several
decimeters. Studying plots as small as 13 mm 13 mm (a relevant size for
individual interactions in bryophytes), Wilson et al. (1995) found a large number
of negative associations indicating that species interactions may affect individual shoots even if it does not structure the community at larger scale.
10.4.2
Regeneration processes and the role of disturbance
Since all plants basically need the same resources, it has been difficult
to explain all coexistences by niche differentiation. Grubb (1977) introduced the
10 Population and community ecology
concept of regeneration niche, including all stages of reproduction, dispersal,
and establishment. This opens up a whole range of coexistence-promoting
mechanisms. Of particular interest is the trade-off between attributes that
make a species persistent and competitive in the habitat and attributes that
confer dispersal ability. An example that outlines the mechanisms of these
relationships is the co-habitation of Dicranum flagellare and Tetraphis pellucida on
decaying logs. In D. flagellare, high reproductive allocation to asexual brood
branches with high establishment potential gives a successful short-range dispersal, whereas T. pellucida puts most of its reproductive effort into spores that
enable the species to colonize a larger proportion of more isolated logs
(Kimmerer 1994). Kimmerer (1993) used a matrix model to describe the
dynamics of Tetraphis pellucida (Fig. 10.7). When it occupies an open patch, it
Fig. 10.7. The dynamics in patches of decaying wood in the Adirondack Mountains, New York
State, showing the stages of change in the dominant species Tetraphis pellucida. Disturbed
(vegetation-free) patches are colonized by T. pellucida. The colonization starts with an asexual
stage that later can develop into sexual and also decline into senescence. All three stages, but
particularly the senescent one, can be invaded by competing species, and disturbance can open
up for recolonization. The probabilities of annual transition between the stages are shown (also
indicated by line thickness), and the proportion of patches of each type (stable stage
distribution) is shown by the diameter of the circles. The proportions are strongly dependent on
disturbance regime. If disturbances are reduced by 50%, the proportion of patches with
competitors will increase from 26% to 47%. Based on data in Kimmerer (1993).
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H. Rydin
often starts as an asexual colony, which gradually becomes sexual. Such colonies may be quite persistent, but may also be overcome by competitors or wiped
out by disturbance. Recurrent disturbances enables the species to maintain
dominance in the system, even though it cannot resist local competitive exclusion. It also turns out that the brood branches produced by D. flagellare are much
more desiccation-tolerant than the gemmae produced by T. pellucida. This leads
to a niche differentiation that may facilitate species coexistence: D. flagellare can
colonize the drier parts of log tops, whereas T. pellucida is primarily found on
moister sides of the logs (Kimmerer & Young 1996).
There are probably many cases in which coexistence of species can be
explained by disturbances breaking the competitive dominance. One example
is Conocephalum conicum and Fissidens obtusifolius in riparian habitats. On frequently flooded cliffs C. conicum was overgrowing F. obtusifolius, but the latter
species is more flood-tolerant and more efficient at colonizing disturbed patches
(Kimmerer & Allen 1982). Another example of such a ‘‘competition–colonization’’
trade-off is Aulacomnium palustre, which can effectively colonize peat by vegetative
reproduction, but is later competitively inferior to species of Polytrichum and
Sphagnum (Li & Vitt 1995).
According to classical theories the most intense competition is expected among
closely related species with similar morphological and physiological characteristics, and hence similar resource use. Watson (1980, 1981) investigated six coexisting species of the Polytrichaceae. She found that the species differed in their
realized niches along light and pH gradients. However, the niches were not broader
when the species grew in pure stands than when it grew with potential competitors. Whereas classical competition theory suggests that niche overlap should
decrease as a result of interspecific competition, the overlap actually increased
with increasing contacts among Polytrichum species. Again, this is a case where
stochastic processes, dispersal, and order of establishment seem more important
than the competitive abilities for community structure, and a strict competitive
hierarchy is difficult to envisage. In another case with strong dominance and
almost complete cover of bryophytes, the boreal forest floor, niches are also highly
overlapping, and it is difficult to explain the spatial occupancy of different species
by habitat partitioning (Frego & Carleton 1995a). Similarities in response to habitat
conditions leads to symmetric competition among established plants and if all
species suffer equally they are unable to outcompete each other. The results are
more compatible with the interpretation that local non-equilibrium and stochastic
processes rather than competition are structuring the community.
The ‘‘intermediate disturbance hypothesis’’ predicts that species richness in a
community should peak at intermediate frequency or severity of disturbance.
Without disturbances, a few species tend to dominate, and with too much
10 Population and community ecology
disturbance only the most effective colonizers will persist. In the boreal forests,
dominance of a few species (notably feather mosses) leads to low bryophyte
diversity. In small gaps the colonization will reflect the abundance of the
adjacent vegetation, and in experiments with gaps of 10 cm diameter in black
spruce forest in Ontario, the forest floor dominant Pleurozium schreberi was the
most successful colonizer by virtue of its high abundance of propagules (Frego
1996). It appears that the gaps must be of certain size to promote diversity.
Tree fall, for instance, causes larger gaps with exposed soil where some earlysuccessional species can colonize (Jonsson & Esseen 1990). Such gaps will contribute to overall diversity in the forest, even if dispersal limitation means that
each gap or tree fall mound only support few colonizing species (Heinken &
Zippel 2004, Kimmerer 2005). During & van Tooren (1988) followed colonization
and succession in experimentally cleared plots in Dutch forests. Early colonists
were mosses growing in adjacent vegetation which had short-range dispersal by
gemmae and spores, and liverworts and perennial mosses followed after the
second year. There were no indications that the early-arriving species inhibited
the possibilities for the forest floor dominants to regain control of the area.
10.4.3
Competition studies
Evidence for interspecific competition in bryophytes comes from (1) studies of niche separation and spatial segregation of species; (2) peat stratigraphy;
(3) monitoring of permanent plots during succession or assumed equilibrium
conditions; (4) observations of dead remnants of species under the living
ones; (5) reciprocal transplant experiments; and (6) experimental assemblages,
such as replacement series starting from plant fragments. The evidence from
descriptive methods is somewhat circumstantial; experiments are required to
convincingly demonstrate the role of competition.
The two main mechanisms for competition among vascular plants are resource
depletion in the root zone and shading by foliage. In contrast, bryophytes typically
form a monolayer, and the effect of competition is that shoots can be buried. If
shoot number is used to monitor interspecific competition it should be combined
with a measure of shoot size, since we have seen above that a declining population
can survive as a constant number of very small etiolated shoots. In experiments
with vascular plants biomass is often used as a response, but in bryophytes the
border between living and dead parts is often obscure, sometimes to the point of
making ‘‘biomass’’ a useless concept. Growth rate (length or biomass) can be used,
but one should be cautious with the use of relative growth rate. It uses initial mass
or length as denominator, and this makes it a somewhat dubious concept in
bryophytes: a shoot that grows 1 cm (or x mg) in a year will probably do so
regardless of whether it was cut to 2 or 4 cm at the start, but the relative growth
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H. Rydin
rate will be very different in the two cases. A practical way to monitor the effects of
competition on the community is often to measure the change in area covered by
the competing species. Competition is then manifested as a struggle for space (see
Crowley et al. 2005 for a modeling approach of overgrowth competition), even if the
underlying mechanism is a resource competition (light, water, or nutrients).
Detailed niche studies backed up by experiments have been made on Sphagnum
and other peatland species along gradients of water level and pH (Rydin & Jeglum
2006, Chapter 9, this volume, and references therein). Sphagnum offers a system in
which interspecific contacts are tight and therefore competition may at least
potentially acts as a structuring force. Ten species of Sphagnum may coexist in a
floating soft carpet community even with little variation in topography (Vitt &
Slack 1975), and up to five species in a plot 4 cm in diameter (Rydin 1986). To some
degree, differences in fundamental niches and competitive relations along the
gradients can explain the distribution patterns (for instance, hollow species
cannot grow high up on a hummock because they will dry out and die), but the
hummock-former S. fuscum seems able to grow also in sites closer to the water
table (Rydin 1993a, see also Mulligan & Gignac 2001). However, it appears that
several species are competitive equivalents. As discussed above, competition
might still be very intense, but it may not lead to competitive exclusion, or at
least the competitive replacement may take a very long time (Rydin & Barber
2001). It is likely that colonization order and pre-emptive competition is important for the distribution patterns (Rydin 1993b).
Results from a number of other experimental investigations on interspecific
competition are summarized in Table 10.5. Overall, it appears that many communities dominated by bryophytes are characterized by high niche overlap with
no clear competitive hierarchy among the community dominants. The bryophyte cover often shows a close mixing of several species. Competitive replacements occur very slowly, if at all, in the closed bryophyte cover. Instead, the
species composition is often affected by small-scale disturbances. These are
invaded and held by pre-emptive competition by the same species that dominate the closed community (founder control), but when the disturbance is large
or drastically alters the substrate (for instance after fire) a different set of
species will colonize and gradually be outcompeted by the dominants (dominance control). Anthropogenic changes, notably nitrogen deposition, can shift
the competitive relations and lead to dominance of one or a few species, but
sometimes the change in environment is more important than competition.
10.4.4
Interactions with vascular plants
Being small and lacking roots, bryophytes have a disadvantage in
exploitation competition with vascular plants, even though this is partly
Table 10.5 Examples of experimental studies of interspecific competition in bryophytes
Habitat (reference)
Approach; species
Result
Grassland (van der Hoeven
Transplants; Calliergonella cuspidata, Ctenidium molluscum
Differences in growth rate among species, but no clear effects of competition.
Replacement series from fragments; two acrocarps
Differences in biomass growth indicate a competitive hierarchy. Species composition,
1999)
Calcareous grassland
(Zamfir & Goldberg 2000)
Boreal forest (Frego &
and seven pleurocarps
Highly overlapping tolerance ranges; differences in growth rate among species,
Fragments and patches of Mnium arizonicum transplanted
Dominance control: Mnium established well in gaps but was overgrown by
Carleton 1995b)
Subalpine forests (Cleavitt
2004)
but no clear community effects of competition.
into mats of Hylocomium splendens
Bog (Rydin 1993a,b, 1997)
Tr ans pl ant s, p er man ent pl ot s, gr o wth of as sem b lages
Poor fen (Mulligan &
Transplants, effect on the growth of a phytometer
in different microhabitats; Sphagnum spp.
Gignac 2001, 2002)
Bog (Lütke Twenhöven,
1992)
Fen (Kooijman 1993,
but not evenness, affected by interactions. No competitive exclusions.
Transplants; feather mosses
(Aulacomnium palustre); Sphagnum spp. and feather mosses
Growth rate and cover with different nitrogen doses;
Sphagnum fallax, S. magellanicum
Transplants and replacement series; Scorpidium
Hylocomium.
No competitive exclusion and no clear competitive hierarchy. Some species
limited by microhabitat conditions.
Feather mosses may be limited by habitat; indications of a competitive hierarchy
among Sphagnum species.
In general shoot growth rate increased in S. fallax when N was added, but no
increase in cover could be detected.
Scorpidium transplanted into Sphagnum squarrosum was overgrown after 8 months.
Kooijman & Kanne 1993,
scorpioides, Calliergonella cuspidata, Sphagnum subnitens,
However, competitive relations (length growth in monoculture vs. mixed stands)
Kooijman & Bakker 1995)
S. squarrosum
cannot fully explain recent decrease in Scorpidium scorpioides and Sphagnum subnitens
in the Netherlands: the species are largely restricted by the chemical environment,
rather than competition.
Decaying wood (McAlister
1995)
Peatlands (Li et al. 1993)
Replacement series from fragments; Anomodon rostratus,
Biomass growth not affected by interspecific competition.
Leucobryum albidum, Platygyrium repens
Pure and mixed cultures; Sphagnum
No difference in length or biomass growth between pure and mixed cultures
under different phosphate concentrations.
Shore cliffs (Kimmerer &
Allen 1982)
Replacement series in greenhouse, permanent plots in
field; Conocephalum conicum, Fissidens obtusifolius
C. conicum showed increased cover in experimental mixture and F. obtusifolius
decreased relative to pure stands, but this did not lead to competitive
replacement in the field.
Oceanic heath (Scandrett &
Gimingham 1989)
Replacement series; Pleurozium schreberi, Hylocomium
splendens and Hypnum jutlandicum
In mixtures H. jutlandicum was the most successful and Pleurozium schreberi the least
successful (biomass growth). Mixture yield probably also depends on the
relative ability to establish from fragments, and thus reflect pre-emption as well
as resource competition.
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H. Rydin
balanced by their generally lower demands for light and nutrients. The light
competition is generally completely asymmetric (not affecting the vascular
plant), and often amplified by the accumulation of litter (Chapman & Rose
1991).
In most plant communities it is doubtful whether there is any direct nutrient
competition since the uptake zones of roots and gametophytes hardly overlap.
In ecosystems with nutrient-poor soils (such as leached podsols) or peat, the
situation is different. Here a considerable share of the nutrients enters through
precipitation (in bogs, all nutrients) or become available in throughfall from
trees or from decomposing litter (Oechel & van Cleve 1986, Bayley et al. 1987).
The nutrients are trapped in the thick mat of feather mosses or Sphagnum, and
the vascular plants have to rely on nutrients released from decaying basal parts
of the mosses (Malmer et al. 1994, Svensson 1995). An intriguing balance
between light and nutrient interactions was demonstrated in Tamm’s classical
study of Hylocomium splendens: the maximum growth of the moss was at the edge
of the spruce crown where shading was not too strong and water and nutrients
from crown drip were most readily available (Tamm 1953).
Other cases where nutrient limitations lead to bryophyte dominance can
be mentioned. In heathland fire successions Gloaguen (1993) observed
Polytrichum commune invading and covering the grass Agrostis curtisii, and the
constant struggle by gardeners trying to keep their lawns free from mosses
such as Rhytidiadelphus squarrosus and Pseudoscleropodium purum is a classic
demonstration that bryophytes are not always competitively weaker than
vascular plants. These relations become completely changed with increased
anthropogenic nitrogen deposition or fertilization. At low doses the bryophytes will increase their growth, and some cover of vascular plants may
also reduce desiccation and facilitate the growth of bryophytes (Ingerpuu et al.
2005). With higher nutrient doses more nitrogen will reach the root zone, and
a circle of positive feedbacks is initiated. The growth of the vascular plants is
promoted, and by the increasing shading the bryophytes’ growth and capacity
to retain nutrients will decline and even more nutrients pass down to the
roots. The decrease in bryophyte abundance or richness at high cover of
vascular plants has been documented in many cases: bog vegetation with
Sphagnum (see Rydin & Jeglum 2006 for discussion and further references),
fens (Bergamini et al. 2001), grasslands (Aude & Ejrnaes 2005), and Tasmanian
eucalypt woodlands (Pharo et al. 2005). When boreal forests are fertilized to
increase timber production, an expansion of grasses is coupled with a drastic
decrease in dominant feather mosses, but other bryophytes such as
Brachythecium starkei, B. reflexum, and Plagiothecium denticulatum may increase
(Strengbom et al. 2001).
10 Population and community ecology
Direct competition for nutrients may occur between Sphagnum and vascular
plants with very shallow root systems, such as Drosera spp. They could easily be
overgrown, and with higher Sphagnum growth the vascular plant will have to
invest more assimilate into stem biomass (Thum 1988) to keep pace with the
moss carpet. Redbo-Torstensson (1994) found that mortality in Drosera rotundifolia increased as nitrogen was added, suggesting that the decrease in light
availability following the increase in Sphagnum growth was more important
than nitrogen competition.
Bryophytes often have a negative effect on seed germination and establishment. Examples are Campylopus introflexus hampering germination of Calluna
vulgaris (Equihua & Usher 1993) in British heaths, and bryophyte mats inhibiting
germination of non-native species in Australian grasslands (Morgan 2006).
Sometimes seedling mortality after germination is the main problem. Scots
pine (Pinus sylvestris) germinate well in Sphagnum, but many seedlings are overgrown by the moss. The seedlings may initially be distributed at random, but
surviving pines are only found in bog hummocks where Sphagnum height
growth is low and aeration is sufficient for the pine roots (Gunnarsson &
Rydin 1998). In calcareous grasslands, Zamfir (2000) showed that seedling mortality by burial was high in a moss carpet, except in the grass Festuca ovina, which
develops a cotyledon that quickly penetrates the moss layer. In the thick feather
moss mat in boreal forests, conifer seedlings face the opposite problem. In a
study in Sweden, 99% of the spruce seedlings died within a year (Leemans 1991).
The most common cause of death was desiccation because the seedlings were
unable to grow a primary root sufficiently long to reach the mineral soil beneath
the moss carpet, and seedling establishment can increase after heavy grazing in
years with peak populations of voles and lemmings (Ericson 1977).
In summary, the interactions between bryophytes and vascular plants are
complex, but the bryophyte features listed in Table 10.2 can help to explain
under what circumstances bryophytes are likely to be competitive. Especially
important for success are the low resource requirements, the long growing
season, the capture of nutrients directly into photosynthesizing tissue, and
the ability to form thick carpets that monopolize the ground. Further examples
of negative and positive interactions are described in Longton (1988).
10.5
Species richness on patchy substrates and islands
Bryophytes on patchy substrates have been used to investigate factors
affecting species richness. Boulders, host trees, decaying logs, and forest stands
can be viewed as ‘‘habitat islands’’ with conditions contrasting to the surrounding matrix, and the theory of island biogeography is often applied to predict a
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H. Rydin
positive species–area relationship in habitat islands. In several ways this analogy can be questioned. (1) Island biogeography assumes that there is a ‘‘mainland’’: an area in which all species in the system occur and from which they
disperse to the islands. In reality it is more common that dispersal occurs
between the patches and the patch inhabitants are better described as a set of
metapopulations, i.e., a metacommunity (Holyoak et al. 2005). (2) Both the island
biogeography and the metapopulation theories are applicable for the obligate
patch species for which the matrix is inhospitable, but many species have the
matrix as their main habitat and appear in the patch only because they expand
clonally or from spores from the immediately adjacent matrix. Without a continuous inflow of propagules they would not appear in the patches. This can be
referred to as a mass effect (Shmida & Ellner 1984), and is clearly related to the
source–sink dynamics discussed above. Since so many bryophytes depend on
patchy substrates, the diversity at a larger scale, such as a whole forest stand,
also depends on the amount and configuration of suitable substrates within the
stand (Berglund & Jonsson 2001, Pharo et al. 2004, Mills & Macdonald 2004).
10.5.1
Species richness on true islands
Studies of true islands invariably demonstrate a strong species–area
relationship, and bryophytes are no exception. According to island biogeography the reason is that larger islands have larger populations of each species, and
therefore the extinction risks are lower. However, it is also a universal phenomenon that larger islands have more habitat types and therefore should hold
more species, and to separate the effect of area from that of habitat diversity
is notoriously difficult. For example, Nakanishi (2001) studied bryophyte species
richness in islands off Japan ranging in area from 11 m2 to 12 000 km2. The
species–area relationship was very strong (R2 ¼ 0.98 for the log–log function).
The islands ranged in elevation between 10 and 217 m and there was a strong
correlation between elevation and log area (r ¼ 0.87), and hence also a strong
relation between species richness and elevation (R2 ¼ 0.84). Therefore the effects
of habitat diversity (as reflected by elevation) cannot be separated from that of
area. The islands ranged in distance from mainland between 50 m and 10 km,
but there were no indications of any effects of isolation on species richness.
Among vascular plants, it is common that isolation distances of the order of
kilometers do not affect species richness (Rydin & Borgegaº rd 1988), and
Sphagnum diversity on islands in the Baltic Sea seemed unaffected by distances
to mainland up to 40 km (Sundberg et al. 2006). In an attempt to isolate the effect
of island area, Tangney et al. (1990) studied bryophyte species richness in sample
plots on lake islands in New Zealand. They found a strong effect of island area
that demonstrated an effect that was independent of habitat diversity.
10 Population and community ecology
Therefore the results are in agreement with island biogeography theory, but
again there was almost no effect of isolation. A tentative conclusion from island
studies is that species richness of bryophytes as well as vascular plants will
almost always depend both on area and habitat diversity, and (at least within
kilometer-scale ranges) be independent of distance to mainland.
10.5.2
Species richness in epiphytes
A question remains, namely whether it is possible to understand species
richness in patchy substrates as simply the sum of the occurrences determined
by the metapopulation processes of the different species. The answer would
probably be ‘‘no’’ in saturated communities where colonizations and extinctions may depend on the number and identity of other species in the patch,
since interspecific competition would modify the metapopulation processes.
There may also be facilitation, for instance if bryophyte mats provide water
storage and sheltered conditions for desiccation-sensitive species (Ellyson &
Sillett 2003). In the sites where Neckera pennata was studied, however, large
proportions of each tree stem were not covered by epiphytes, and it seems
reasonable to try to separate the importance of habitat factors and dispersal
for patch species richness in much the same way as described above for the
occupancy of N. pennata. In this case a main predictor of species richness was tree
diameter, but spatial aggregation (indicating dispersal limitation and metapopulation processes) was equally important (Löbel et al. 2006b). Total species
richness is composed of both obligate and facultative epiphytes, and to gain
further understanding of the processes it is necessary to divide the total diversity into functional groups (Fig. 10.8). For facultative epiphytes (generalists in
Fig. 10.8), tree diameter and other habitat factors were important, whereas the
diversity of obligate epiphytes differed considerably among forest sites and was
also influenced by tree species. Most interestingly, among the obligate epiphytes the spatial processes were more important for asexually dispersed species than for those mostly dispersed by spores. It appears that species dispersed
by small spores are less limited by dispersal distances, but instead more
demanding in the establishment phase: host tree species was the most important diversity predictor for this group. Conversely, vegetative diaspores are
larger, and epiphytes dispersed by gemmae or gemma-like branchlets showed
stronger spatial aggregation (dispersal limitation), but were less dependent on
specific host trees for their establishment.
Following island biogeography theory a strong effect of area on species
richness is expected, and also because patch area is an important predictor for
occupancy in metapopulations of individual species. However, in this study
system tree diameter explained only 12% of the variation in bryophyte species
429
430
H. Rydin
All species
Diversity predictors
Tree species
DBH
Other habitat
Site
Spatial
Unexplained
Generalists
Specialists
Sexual
Asexual
Fig. 10.8. The relative importance of tree species, local habitat factors and spatial factors
(related to dispersal) for species richness of bryophytes growing as epiphytes on deciduous tree
in a coniferous landscape in eastern Sweden. For generalists (facultative epiphytes), tree
diameter at breast height (DBH) and a range of habitat factors were important. In sexual (mostly
spore-dispersed) specialists (obligate epiphytes), local species richness differed among tree
species, whereas for asexual species (mostly dispersed by gemmae) the importance of spatial
factors indicates dispersal limitations. Based on data in Löbel et al. (2006b).
richness (Löbel et al. 2006b). At a larger scale, this changes drastically: species
richness of obligate epiphytes in separate forest stands was strongly related
to forest stand area (R2 ¼ 0.41) and even stronger when the number of host
trees per stand was used a measure of area (R2 ¼ 0.57) (Löbel et al. 2006a). A
similar study of epiphytes on Populus tremula in the boreal coniferous landscape was made in Finland and adjacent parts of Russia. At local scale, the
presence of several species was here favored by larger tree diameter and
denser tree cover (probably through the effect on microclimate), and at
10 Population and community ecology
regional scale the stand diversity increased with increasing abundance of
Populus (Ojala et al. 2000).
10.5.3
Species richness on boulders
In a study of bryophyte species richness on boulders in eastern Sweden,
Weibull & Rydin (2005) noted a strong species–area relationship. This is consistent with island biogeography theory. However, in addition to (or alternative to)
a direct effect of area, the relationship can also be caused by a positive correlation between island area and habitat diversity. In this case species richness was
higher on boulders with more variation in microhabitats, e.g. variation in leaf
litter cover, smoothness, shape, and amount of fissures. An important factor
was also the species identity of the tree above the boulder, with lowest richness
under Picea abies, intermediate under Betula pendula and Quercus robur, and highest under Acer platanoides, Ulmus glabra, and Fraxinus excelsior (twice as many
species on boulders under the latter three trees compared with Picea). The
ranking indicates that chemical base saturation of throughfall is important.
Hence there were three main determinants of species richness: area per se,
habitat diversity, and local environment. In a similar study in the northeastern
U.S.A. (Kimmerer & Driscoll 2000), there was some effect of microhabitat diversity on species richness, but more important were small-scale disturbances.
Small moss patches often fall off, or are washed away. This prevents the dominance of competitive species and creates open spaces for colonization. Thereby,
the equilibrium between area-dependent extinctions and isolation-dependent
immigrations assumed in island biogeography becomes less important than the
disturbance regime. Species richness seems to peak at some intermediate level
of disturbance (Weibull & Rydin 2005), and therefore illustrate the intermediate
disturbance hypothesis: too frequent or intense levels of disturbance would
allow only the most efficient colonists to grow on the boulder, but intermediate
levels allow the coexistence of competitive dominants and fugitive species.
Boulders often contain many of the ground-dwelling forest floor species, and
therefore connectivity effects on species richness are not to be expected.
Virtanen & Oksanen (2007) studied cryptogams (bryophytes, lichens and ferns)
on erratic calcareous boulders in an area with acidic soils. This is a particularly
useful study system for metacommunity patterns, and for the calcicolous species (not growing in the matrix) the species richness was positively affected both
by boulder area and connectivity.
10.5.4
Species richness on decaying wood
Decaying wood is an important substrate for many bryophytes. Even
though many of the species also grow on other substrates (McAlister 1997) there
431
432
H. Rydin
are a number of wood specialists for which the habitat island or metacommunity concepts are applicable. As an example, Andersson & Hytteborn (1991)
found 16 epixylic specialists in an old-growth coniferous forest in eastern
Sweden but only five in an adjacent managed site. The old-growth site had
more dead wood, larger pieces of wood, and more substrate in suitable stages
of decay than the managed stand. These variables describe the patch network,
but the more humid local climate in old-growth forests may be equally important for many bryophytes (Söderström 1988a). Fallen logs become hospitable
when the bark has disappeared and the wood has softened to achieve some
water-holding capacity, and there is a clear successional sequence with facultative epiphytes as first colonizers, followed by species that could be classified as
early and late epixylics. At a very late stage of decay the wood specialists become
overgrown by forest floor mosses (Söderström 1988b), and fallen logs are suitable patches for only a few decades (Hytteborn & Packham 1987, Söderström
1988b). Considering that it takes considerable time for some of the inhabitants
to start to reproduce, for instance about nine years in Ptilidium pulcherrimum
(Jonsson & Söderström 1988), the time to build up high diversity is short.
10.6
Species composition and richness at different temporal
and spatial scales
The discussion so far indicates that species composition and richness in
the community not only depend on local processes but are also affected by
processes operating between communities (e.g. Zobel 1997) as described by
the theories of metapopulation biology and island biogeography. We can use
the conceptual model in Fig. 10.9 for a discussion on the role of scale-dependent
processes for the composition in bryophyte assemblages, and how they appear
to differ from those of vascular plants.
With their numerous small spores, bryophytes appear less dispersal-limited
than vascular plants at the continental scale. This is witnessed by the large
similarity in species composition over continental distances mentioned initially. This also indicates that bryophyte distributions may be less governed by
climatic factors, which makes sense considering their tolerance to hazards such
as desiccation and frost. The filter between continental and regional scales
appears quite coarse.
At the interface between regional and local scales we have seen that the
theories of metapopulation biology and island biogeography apply to bryophytes in much the same way as to vascular plants, and dispersal limitations
at this scale have been repeatedly demonstrated. Species richness in the community is constrained by the fact that the species do not have the dispersal
10 Population and community ecology
Fig. 10.9. Species composition and diversity depends on processes acting at different temporal
and spatial scale. Long-range dispersal over the continental scale can operate over centuries and
millennia and explain, for example, species migration after the last glaciation. The local
community is affected by other communities in the region as described by metapopulation
dynamics and island biogeography. Species are filtered out from the continental to the regional
and down to the local scale. Classical equilibrium theories assume that the local species
richness is further reduced by competition, unless there is some heterogeneity in habitat
conditions that matches a niche differentiation among species. According to nonequilibrium theories, species can be rescued by several mechanisms that prevent or slow
down competitive exclusion. Herbivory or fine-scale disturbance may break the dominance
of strong competitors and favor competitively weak species with good local dispersal and
establishment.
capacity required to counteract local extinctions. The tight connection between
the bryophytes and their substrate (in the absence of a spatially integrating root
system) makes the environmental filter quite fine-meshed for many species.
Entering into the community level, we have seen cases of coexistence by
niche differentiation and a separation among species along microscale environmental gradients. More striking are the many ecosystems dominated by
bryophytes in which several species with similar morphology and life history
closely coexist. They may well compete intensively but the symmetric nature of
the interactions makes competitive exclusion a very slow process. In fact,
433
434
H. Rydin
facilitation may sometimes have a stronger effect on community composition:
the moist environment created by the dominants is necessary for the presence
and persistence of some subordinate species. Whereas herbivory in most bryophyte assemblages is of little importance, small-scale disturbances and the
continuous generation of patchily distributed substrates are strong determinants of community species richness and composition.
Acknowledgments
I thank Urban Gunnarsson, Haº kan Hytteborn, Bengt-Gunnar Jonsson,
Swantje Löbel, Rune Økland, Tord Snäll, Brita Svensson, Joachim Strengbom,
and Sebastian Sundberg for comments on the manuscript. Financial support
was obtained from VR and Formas.
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11
Bryophyte species and speciation
a. jonathan shaw
11.1
Introduction
The three lineages of bryophytes, mosses, liverworts, and hornworts,
compose successful groups of early embryophytes. The mosses are estimated to
include some 12 700 species (Crosby et al. 2000), the liverworts approximately
6000–8000 extant species (Crandall-Stotler & Stotler 2000, Chapter 1, this
volume), and the hornworts about 100–150 species (Chapter 3, this volume).
Mosses are comparable in species richness to the monilophytes, which are
estimated to include about 11 500 species (Pryer et al. 2004). Among the extant
land plants, therefore, only the angiosperms are currently more species-rich
than are the bryophytes.
It is often stated that bryophytes are most diverse in the tropics and fit the
general pattern found in many groups of organisms, with increasing species
richness toward the equator (Rosenzweig 1995). However, a quantitative analysis
of latitudinal diversity patterns in the mosses failed to detect any such latitudinal
gradient, except perhaps a weak one in the Americas (Shaw et al. 2005a). It appears
that liverwort diversity is highest at moderate to high latitudes of the Southern
Hemisphere, although one family, the Lejeuneaceae, is hyperdiverse in wet
tropical forests of both the New and Old Worlds (Gradstein 1979).
The fossil record for mosses, liverworts, and hornworts is too incomplete to
assess whether these groups were more or less diverse in the geological past
(Miller 1984, Oostendorp 1987). Many early Tertiary or even older fossils look
quite similar to extant taxa (e.g. Janssens et al. 1979), and this interpretation has
contributed to the view held by some (e.g. Anderson 1963, Crum 1972) that
many or most bryophytes have changed little over vast amounts of time (measured in tens of millions of years, at least), and as such, should be viewed as
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
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‘‘living fossils’’. One case of morphological stasis over tens of millions of years
is provided by Frahm’s (2005) report of plants seemingly identical to
Hypnodontopsis mexicana from Baltic amber of Eocene age (45–58 million years
old). Crum’s (1972) claim that mosses represent ‘‘unchanging, unmoving
sphinxes of the past’’ that are ‘‘evolutionary failures nonetheless well adapted
to a modest role in nature’’ is one of the most oft-quoted speculations in the
literature of bryophyte evolutionary biology. Most quotations of Crum’s statements are given as introduction to evidence that many bryophytes are in fact
highly diverse at the genetic level, in contradiction to the situation expected if
they are indeed unmoving, unchanging, living fossils characterized by very low
rates of evolution. Moreover, recent studies have documented ecotypic differentiation among populations of some bryophyte species (Shaw 2001), as well as
complex interspecific evolutionary patterns that include cryptic speciation,
hybridization, and allopolyploidy (see below, and previous reviews by Wyatt
et al. 1989, Stoneburner et al. 1991, Bischler & Boisselier-DuBayle 1997, Shaw
2000a). Interestingly, Stenøien (unpublished) compared nucleotide substitution
rates in mosses and seed plants using relative rates tests applied to phylogenies
for the groups and found that substitution rates were indeed lower in mosses
than in seed plants. The difference held true for analyses of nuclear (26S),
chloroplast (rps4), and mitochondrial (nad5) substitution rates.
Nevertheless, there is systematic and phylogenetic evidence that some
groups of bryophytes have undergone periods of rapid diversification.
Gradstein (1979, 1994, 1997) speculated that the liverwort family Lejeuneaceae,
which includes at least 1000 species, has undergone relatively recent spurts of
diversification and is actively diversifying in tropical regions. In the first attempt
to put a time frame on evolutionary rates in bryophytes, Wall (2005) estimated a
rate of 0.56 (0.004) new lineages per million years in the moss genus
Mitthyridium, which is fast even in comparison to estimates for rapidly radiating
angiosperm groups (e.g. Baldwin & Sanderson 1998). Shaw et al. (2003b) used
phylogenetic tree shape to infer relative rates of net diversification (speciation
minus extinction) in pleurocarpous mosses and found evidence for an increase in
diversification rate associated with the origin of hypnalian pleurocarpous mosses.
Newton et al. (2007), however, did not detect evidence for an early period of rapid
diversification in their study of pleurocarp phylogeny.
Based on a phylogeny including bryophytes and seed plants and calibrated by
a date for the origin of embryophytes estimated from fossils, Newton et al. (2007)
came up with a date for the origin of pleurocarpous mosses of 194–161 million
years ago (mya). They estimated the diversification of major pleurocarpous
lineages (mainly families) at 165–131 mya. Their calibrated phylogeny suggested
that many moss families may have originated in the Cretaceous, but that some
11 Bryophyte species and speciation
families, at least, appear to have diversified more recently. The Hypnodendraceae
and Racopilaceae, for example, appear to have originated in the Cretaceous
(>100 mya) but Racopilum itself may have diversified within the past 20–40 my.
Similarly, an origin for Ptychomniaceae was dated at 172–140 mya, but the
divergence between Garovaglia and Euptychium might have been as recent as
28–16 mya. Accuracy of dating estimates for bryophytes is very much limited by
the paucity of good calibration by fossils. Wall (2005) used oceanic islands whose
geologic history is understood to provide maximum age estimates for endemics.
A similar analysis of liverwort diversification was recently published by
Heinrichs et al. (2007). They estimated that the Jungermanniopsida (leafy plus
simple thalloid liverworts) diverged from the Marchantiopsida (complex thalloid liverworts) approximately 370 mya in the late Devonian period, and that
the leafy and simple thalloid lineages diverged about 310 mya, in the late
Carboniferous. They further suggested that many of the genera of leafy liverworts diverged as early as the late Cretaceous or early Tertiary. Based on fossils
preserved in amber, Hartmann et al. (2006) dated the origin of the genus
Bryopteris (Lejeuneaceae) as minimally 50 mya, during the Cretaceous Period.
Using that date and an estimate of the mutation rate for the nuclear ribosomal
ITS region, these authors suggested that clades of Bryopteris (B. diffusa versus B.
filicina plus B. gaudichaudii) diverged in the Miocene, about 15 mya.
These estimates would suggest that many families of bryophytes are quite old,
although we still know little about the ages of extant species. Morphologically
cryptic species and allopolyploids are now known to be common in mosses and
liverworts and we might think of these cases as evidence of recent divergence and
speciation, but there is no a priori reason to assume that their origins were recent;
genetic patterns in some allopolyploids suggest ancient origins (see below).
11.2
Species concepts
If we wish to study the origin of species, we must first ask the question:
what are species? The conceptual basis for defining and delimiting species has
been the subject of voluminous discussion since (and even before) Darwin (1859)
argued that species differ in no fundamental way from infraspecific taxa such as
varieties and subspecies. Hey (2001) gleaned from the literature 24 different
attempts to define species. One thing that most systematists agree on is that
species should on some level be ‘‘units of evolution’’.
11.2.1
Morphological definitions
In a survey of taxonomic literature, McDade (1995) noted that most
monographers do not discuss species concepts at all. As in most groups of
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organisms, the most commonly applied approach to delimiting species of bryophytes is morphological: species are groups of individuals or populations that
are morphologically distinguishable from other groups. Bryologists rarely have
any information beyond ‘‘these recurring morphotypes are distinguishable’’,
and therefore represent separate species. Geographic and ecological information can provide useful supplementary data to the extent that distinct distributions and/or ecological characteristics suggest that morphologically defined
species have biological meaning as evolutionary entities. Indeed, the observation that two morphotypes differ in their geographic distributions strongly
suggests that they have unique evolutionary histories as separate lineages.
Morphological variation within and among species results from environmental
and genetic differences, and too few studies have employed experimental
approaches to determine the extent to which morphological variation is genetically based (but see, for example, Mishler 1985, Saº stad 1999, Buryova & Shaw
2005).
11.2.2
Biological and phylogenetic species concepts
A flurry of papers discussing alternative species concepts were published during the 1980s and 1990s (e.g. Mishler & Donoghue 1982, Nixon &
Wheeler 1990, Baum & Donoghue 1995, McDade 1995, Olmstead 1995, Davis
1997). A main issue surrounds the conceptual (dis)advantages of the so-called
biological species concept (BSC, Mayr 1965), versus various phylogenetic concepts. According to the BSC, primacy is given to reproductive isolation as the
most important criterion for delimiting species. That is, species comprise
gene pools that are reproductively isolated from other gene pools (species).
There are a number of methodological and conceptual problems with the
BSC. These include the fact that reproductive information is lacking for the
vast majority of species on the planet, and it is difficult or impossible to
apply the BSC to asexual or nearly asexual taxa (Wheeler & Meier 2000). In
addition, reproductive isolation is in many groups a matter of degree rather
than all or nothing, and species defined by reproductive isolation sometimes
result in taxa that are not congruent with delimitations based on morphology
or phylogenetic history.
The development of cladistic methodologies, the ability to easily gather
molecular data, and the conceptual framework of phylogenetic systematics,
has yielded a number of (phylogenetic) tree-based species concepts.
Proponents of phylogenetic species agree about the use of phylogenetic methods and reconstructing ancestor–descendant relationships for ‘‘discovering’’ the
units we call species, but differ in exactly what criterion is most appropriate for
delineating species in practice. An important point of disagreement among
11 Bryophyte species and speciation
those supporting some form of phylogenetic species concept is whether species
have to be monophyletic.
Aside from the conceptual controversies surrounding which variant of the
phylogenetic species concept is most appropriate, there is every reason to
expect that many ‘‘good’’ species in nature may not be monophyletic. The
basic coalescence model is a relatively new paradigm in population genetics
focused on reconstructing the ancestry of allele copies sampled from a population. Coalescence theory tells us that in the absence of mitigating processes such
as changes in population size, natural selection, mutation, or population structure, coalescence of allele copies backward in time to the most recent common
ancestor (MRCA) of all extant copies through the process of genetic drift (the
so-called coalescence time) takes 2N generations in a diploid, where N is the
population size (Hudson 1990). Thus, coalescence times are proportional to
the population size and the absolute time to coalescence depends on generation
time. It is significant that the time to coalescence is faster in a small population
than in a large population. A population that has gone through a bottleneck may
be a ‘‘small’’ population in terms of genetic characteristics, even if the census
population size subsequently rebounded.
Molecular data gathered for the purpose of delineating species consist of
allele copies sampled from individuals representing putative species.
Resolution of monophyletic groups of allele copies (which are sequenced to
represent the species) depends on the amount of time since the species have
exchanged genes and the effective population sizes of the two divergent taxa.
For any particular gene, allele copies from a population (or species) should
coalesce to the MRCA after 2N generations in the case of a diploid, or 1N
generation for a locus with uniparental inheritance (i.e. chloroplast or mitochondrial genes).
Rosenberg (2003) found that we should expect allele trees sampled from
recently diverged taxa to show polyphyly until about 1.3N generations after
isolation, paraphyly from 1.3N to 1.6N generations, and only after 1.6N generations should we expect an allele tree to indicate reciprocal monophyly. Those
numbers are for a randomly selected gene, but studies nowadays generally
utilize sequence data from multiple genes to infer species status. Reciprocal
monophyly for 99% of sampled genes is expected after approximately 5.3N
generations (Rosenberg 2003). As time since divergence increases, the required
sample size (number of individuals or populations) required to demonstrate
monophyly decreases. Two species that have been reproductively isolated for
many generations and represent independently evolving lineages may not display reciprocal monophyly for genes sampled in a systematic study. In such
cases, allele trees may not reflect the underlying species trees. Rosenberg &
449
450
A. J. Shaw
Nordberg (2002) provided a readable overview of coalescence theory as it relates
to the sorts of questions frequently addressed by systematists.
The likelihood of resolving reciprocally monophyletic species in a phylogenetic analysis depends in part on the mode and timing of speciation. In the
case of a long-distance founder, monophyly of the derived taxon might occur
relatively quickly because of the population size bottleneck through which it
passes, but phylogenetically it would be seen as nested within the ancestral,
larger population. The ancestral (source) population would appear paraphyletic
until it accumulates enough mutations to be resolved as monophyletic relative
to the derived founder population. If speciation through peripheral isolation or
long-distance dispersal is common, we might expect to find many paraphyletic
species in molecular systematic analyses. When speciation occurs because an
ancestral taxon is divided into relatively large population fragments, coalescence times would be long and neither derived taxon might appear monophyletic from analyses of gene trees. As per inferences made by Rosenberg (2003, see
above), such species would initially be seen as polyphyletic in terms of individual gene trees, then, over time, paraphyletic, and only later, reciprocally
monophyletic. Factors such as population structure in the widespread ancestral
species, selective sweeps, or changes in population size since isolation can also
affect the coalescence process.
These considerations suggest that many species would appear to be nonmonophyletic when studied with a limited sample of genes and during one
slice of time. Based on a survey of published species-level phylogenetic analyses
for plants, Crisp & Chandler (1996) found that more than 30% of commonly
recognized species appear to be paraphyletic (see also Funk & Omland 2003).
Paraphyletic bryophyte species were resolved by Shaw (2000a), and Shaw &
Allen (2000).
It is important to keep in mind that molecular evidence that two taxa are
not genetically differentiated (or monophyletic) is negative evidence, and it
can always be argued that additional data would demonstrate them to be
differentiated. Taxonomic decisions based on short sequences from just one
genomic region should be viewed cautiously. So-called DNA bar-coding has
become popular in recent years and shows much promise for rapid species
identification in some groups. Bar-coding is based on comparing short
sequences from an unknown to a database of homologous sequences from
known taxa. As an identification tool, bar-code sequences have value, but
they are of limited utility and can be positively misleading for discovering
new species and for making evolutionary inferences because of the stochastic
nature of the coalescent process and the limited information content of short
sequences.
11 Bryophyte species and speciation
11.3
Bryophyte species delimitation based on molecular markers
A variety of molecular tools have been applied to evolutionary and
systematic problems in bryology. Most such studies have focused on deeper
relationships among genera and families, but genetic data have also been
applied to species-level problems. Isozyme markers and DNA-based methods
provide valuable information that is complementary to – but not a good
substitute for – careful morphological studies. Isozyme-based research is
briefly summarized below and papers aimed at resolving species-level systematic problems are listed in Table 11.1. Since DNA-based work on resolving species has not been previously summarized, these studies are discussed
in somewhat more detail, but are also listed in Table 11.1. Papers documenting allopolyploid speciation in bryophytes are discussed separately and listed
in Table 11.2.
11.3.1
Isozyme-based studies
Isozymes, defined broadly as allelic variants of enzyme-encoding
genes, have been and continue to be important sources of information
about infraspecific population structure and genetic relationships among
species. Isozymes have the important characteristic of being co-dominant
markers (both alleles are expressed in heterozygotes), making them valuable
for studies of hybridization and allopolyploidy. They are also relatively inexpensive and once the protocols are worked out for a given taxon, they are
highly reproducible. Disadvantages of isozymes relative to DNA-based methods is that isozyme analyses require living material, and levels of variation
may be lower than with some DNA-based fingerprinting methods.
Table 11.1 provides a list of studies that have addressed species-level
taxonomic problems using isozyme markers. The table does not include
papers focused on population structure and geographic patterns within
individual species rather than the genetic delimitation of species. Nor does
Table 11.1 list papers that resolve relationships among species with no or
only limited sampling within species. Earlier isozyme studies were reviewed
by Wyatt et al. (1989), Stoneburner et al. (1991), and Bischler & BoisselierDuBayle (1997).
Isozyme data are not amenable to phylogenetic analyses of ancestor–
descendant relationships, but phenograms provide insight into genetic differences among species and conspecific populations. Several generalities have
emerged from isozyme analyses of bryophytes. One is that morphological
variation does not always reveal the underlying genetic structure of species.
Morphologically cryptic or nearly cryptic species have been documented in
451
452
A. J. Shaw
Table 11.1 Published studies that have utilized isozymes and DNA-based information
to address problems of species delimitation in mosses and liverworts
Taxonomic group
Marker
Reference(s)
Amblystegium
DNA sequences
Vanderpoorten et al. 2001, 2004
Anacolia menziesii – A. webbii
ISSRs, DNA
Werner et al. 2003
sequences
Aneura pinguis
isozymes
Szweykowski & Odrzykoski 1990
Calypogeia
isozymes
Buczkowska 2004, Buczkowska
Campylopus pilifer, C. introflexus
DNA sequences
Stech & Dohrmann 2004
et al. 2004
Cinclidotus
isozymes
Ahmed & Frahm 2003
Climacium americanum – C. dendroides
isozymes
Shaw et al. 1994
Climacium americanum – C. kindbergii
isozymes
Shaw et al. 1987
Conocephalum conicum
isozymes
Akiyama & Hiraoka 1994, Itouga
et al. 1999, Odrzykoski 1987,
Odrzykoski et al. 1981,
Odrzykoski & Szweykowski
1991, Szweykowski et al. 1981b,
Szweykowski & Krzakowa 1979
Dicranoloma
DNA sequences
Stech et al. 2006a
Eurhynchium crassinervium
DNA sequences
Frahm et al. 2000
Eurhynchium, Rhynchostegiella,
DNA sequences
Stech & Frahm 1999b
Fontinalis antipyretica group
DNA sequences
Shaw & Allen 2000
Herbertus
DNA sequences
Feldberg & Heinrichs 2006
Rhynchostegium
Herbertus borealis
DNA sequences
Feldberg & Heinrichs 2005
Herbertus sendtneri
DNA sequences
Feldberg et al. 2004
Hymenophyton
DNA sequences
Pfeiffer 2000b
Hypnobartlettia fontana
DNA sequences
Stech et al. 1999
Hypopterygium ‘‘rosulatum’’
DNA sequences
Pfeiffer 2000a
Hypopterygium tamarisci complex
DNA sequences
Pfeiffer et al. 2000
Isothecium
DNA sequences
Ryall et al. 2005
Jensenia
DNA sequences
Schaumann et al. 2004
Leucobryum
DNA sequences
Vanderpoorten et al. 2003a
Leucobryum albidium – L. glaucum
PCR–RFLP
Patterson et al. 1998
Leucodon
isozymes
Akiyama 2004
Lunularia
isozymes
Boisselier-Dubayle et al. 1995a
Marchantia polymorpha
isozymes,
Boisselier-Dubayle et al. 1995b
PCR–RFLP, RAPDs
Mielichhoferia elongata –
isozymes, DNA
M. mielichhoferiana
sequences
Shaw 1994, 1998, 2000b
Mnium orientale– M. hornum
isozymes
Wyatt et al. 1997
Mitthyridium
DNA sequences
Wall 2005
11 Bryophyte species and speciation
Table 11.1 (cont.)
Taxonomic group
Marker
Reference(s)
Neckera
isozymes
Appelgren & Cronberg 1999
Orthotrichum freyanum
DNA sequences
Goffinet et al. 2007
Pellia
DNA sequences
Fiedorow et al. 2001
Pellia endiviifolia
isozymes
Szweykowski 1984,
Szweykowski et al. 1981b,
1995, Zielinski 1987
Pellia epiphylla complex
isozymes
Pacek et al. 1998, Pacek &
Szweykowska-Kulinska 2003,
Zielinski 1987, Zielinski et al.
1985
Philonotis
isozymes
Buryova 2004
Plagiochila
DNA sequences
Groth et al. 2003, 2004, Heinrichs
Plagiochila carringtonii
DNA sequences
Renker et al. 2002
Plagiochila cucullifolia var. anomala
DNA sequences
Heinrichs et al. 2003
Plagiochila detecta
RAPDs
So & Grolle 2000
Plagiochila virginica
DNA sequences
Heinrichs et al. 2002a
Platyhypnidium riparioides –
DNA sequences
Stech & Frahm 1999a
Polytrichum
microsatellites
van der Velde & Bijlsma 2000
Polytrichum
RAPDs
Zouhair et al. 2000
Polytrichum commune
isozymes
Bijlsma et al. 2000
et al. 2002a,b, 2003, 2005
P. mutatum
Polytrichum commune – P. uliginosum
microsatellites
van der Velde & Bijlsma 2004
Porella
isozymes, RAPDs
Boisselier-Dubayle & Bischler
Porella
isozymes
Boisselier-Dubayle et al. 1998a,
Porella platyphylla – P. platyphylloidea
isozymes
Therrien et al. 1998
Preissia quadrata
isozymes
Boisselier-Dubayle & Bischler
Ptilidium
isozymes
Adamczak et al. 2005
Pyrrhobryum mnioides
DNA sequences
McDaniel & Shaw 2003
Racopilum
isozymes
Vries et al. 1983
Reboulia
isozymes
Boisselier-Dubayle et al. 1998b
Rhynchostegium, Rynchostegiella
DNA sequences
Stech & Frahm 1999b
Rhytidiadelphus
ISSRs, DNA sequences Vanderpoorten et al. 2003b
Riccia
isozymes
Schizymenium shevockii
PCR–RFLP
Shaw 2000c
Sphagnum cuspidatum, S. viride
isozymes
Hanssen et al. 2000
Sphagnum rubellum –
isozymes
Cronberg 1987, 1989, 1998
isozymes
Melosik et al. 2005
1994
Bischler et al. 2006
1997
Dewey 1989
S. capillifolium
Sphagnum subsecundum complex
453
454
A. J. Shaw
Table 11.1 (cont.)
Taxonomic group
Marker
Reference(s)
Sphagnum (3 species)
isozymes, RAPDs
Stenøien & S aº stad 1999
Sphagnum capillifolium –
isozymes
Cronberg & Natcheva 2002
DNA sequences
Shaw & Goffinet 2000
S. quinquefarium
Sphagnum ehyalinum
Sphagnum macrophyllum – S. cribrosum DNA sequences
Zhou & Shaw 2008
Sphagnum mirum – S. tundrae
isozymes
Flatberg & Thingsgaard 2003
Sphagnum pylaesii
DNA sequences
Shaw et al. 2004
Sphagnum recurvum complex
isozymes
S aº stad et al. 1999b
Sphagnum sect. Acutifolia
DNA sequences
Shaw et al. 2005b
Sphagnum sect. Subsecunda
DNA sequences
Shaw et al. 2005c
Symphogyna
DNA sequences
Schaumann et al. 2003
Syntrichia laevipila complex
ISSRs
Gallego et al. 2005
Targionia
isozymes
Boisselier-Dubayle & Bischler
Timmia
DNA sequences
Budke & Goffinet 2006
Tortula subulata complex
DNA sequences
Cano et al. 2005
Weissia wimmeriana
ISSRs
Werner et al. 2004
Weymouthia
DNA sequences
Quandt et al. 2001
1999
both moss and liverwort genera (Shaw 2001). Early studies by Polish workers
(e.g. Szweykowski & Krzakowa 1979, Szweykowski et al. 1981b) demonstrated
that widespread species of the liverwort genera Conocephalum and Pellia in fact
consist of morphologically cryptic or nearly cryptic taxa that appear to
represent non-recombining gene pools, and subsequent examples of cryptic
species have been documented in Calypogeia, Marchantia, Riccia, and Reboulia,
among others. Morphologically cryptic or nearly cryptic species resolved by
isozymes have also been discovered in mosses (e.g. Climacium [Shaw et al.
1987, Shaw et al. 1994], Neckera [Appelgren & Cronberg 1999], Polytrichum
[Bijlsma et al. 2000]).
A second general observation from accumulating isozyme studies is that congeneric species tend to be more genetically divergent from one another than
is typical of seed plants (Gottlieb 1981, Wyatt et al. 1989). Whereas the mean
genetic identity (Nei 1972) between congeneric seed plants is 0.67, many congeneric bryophyte species are more genetically differentiated. Indeed, even some
pairs of morphologically cryptic species exhibit genetic identities of less than 0.50
(Wyatt et al. 1989, and papers listed in Table 11.1). Reasons for this may be several,
including possibly older ages for many bryophyte species compared with species
of seed plant genera. It should also be kept in mind that the taxonomic level
Table 11.2 Putative allopolyploid species of bryophytes
Species names in bold indicate the plastid DNA parent, presumed to be maternal.
Genus
Polyploid name
Technique
Parent(s)
Calypogeia
C. azurea, C. muelleriana,
isozymes
unknown
Origins Reference(s)
Buczkowska et al. 2004
C. sphagnicola
Corsinia
C. coriandrina
isozymes
C. coriandrina unknown
Pellia
P. borealis
isozymes,
P. epiphylla ‘‘N’’ P. epiphylla ‘‘S’’ >2
>1
P. rupestre
Odrzykoski et al. 1996, Fiedorow et al. 2001,
Pacek & Szweykowska-Kulinska 2003
DNA sequences
Plagiochasma
Boisselier-Dubayle & Bischler 1998
isozymes
?
Boisselier-Dubayle et al. 1996
Plagiomnium
P. medium
isozymes
P. insigne P. ellipticum
>3
Wyatt et al. 1988, 1992
Plagiomnium
P. cuspidatum
isozymes
P. acutum unknown
?
Wyatt & Odrzykoski 1998
Plagiomnium
P. curvatulum
Polytrichastrum P. pallidisetum,
isozymes
P. ellipticum P. elatum?
?
Wyatt et al. 1993a
isozymes
unknown
?
Derda & Wyatt 2000
P. formosum? unknown
?
van der Velde & Bijlsma 2001
P. cordaeana P. platyphylla
>1
Boisselier-Dubayle et al. 1998a,
P. sexulare, P. ohioense
Polytrichum
P. longisetum
isozymes,
Porella
P. baueri
isozymes
microsatellites
Jankowiak & SzweykowskaKulinska 2004
Reboulia
R. queenslandica
isozymes
R. hemisphaerica v. hemisphaerica 1?
Boisselier-Dubayle et al. 1998b
Rhizomnium
R. pseudopunctatum
isozymes
R. magnifolium R. gracile
?
Wyatt et al. 1993b
Sphagnum
S. russowii
isozymes,
S. girgensohnii S. rubellum or
>1
Cronberg 1996, Shaw et al. 2005b
R. h. v. orientalis
DNA sequences
S. quinquefarium (S. warnstorfii)
Sphagnum
S. majus
isozymes
S. cuspidatum S. ? annulatum
?
Saº stad et al. 2000
Sphagnum
S. troendelagicum
isozymes
S. tenellum S. balticum
?
Saº stad et al. 2001
Sphagnum
S. auriculatum,
DNA sequences,
S. subsecundum unknown
>1
A. J. Shaw, unpublished
S. carolinianum,
microsatellites
S. inundatum, S. lescurii
Sphagnum
S. jensenii
isozymes
S. balticum S. annulatum
?
Saº stad et al. 1999a
Targionia
T. lorbeeriana
isozymes
T. hypophylla unknown /
>2
Boisselier-Dubayle & Bischler 1999
unknown unknown
456
A. J. Shaw
we call genus is a human construct and ‘‘genera’’ really are not comparable in
bryophytes and seed plants.
11.3.2
DNA-based studies
DNA-based methods include nucleotide sequencing as well as various
‘‘DNA fingerprinting’’ approaches. Fingerprinting methods that have been used
to address systematic problems in the bryophytes include random amplified
polymorphic DNA (RAPDs, Welsh & McClelland 1990), amplified fragment
length polymorphism (AFLPs, Vos et al. 1995), inter-simple sequence repeats
(ISSRs, Zietkiewicz et al. 1994), and microsatellites (also known as simple
sequence repeats). One advantage of DNA-based methods over isozymes is that
dried herbarium collections can be used to more easily sample from across the
ranges of taxa without conducting additional and often expensive fieldwork.
RAPD markers were developed in the 1990s and have been used extensively in
plant and animal breeding, as well as in studies of population genetics. Much
concern has been expressed, however, about the reproducibility of RAPD data.
The journal Molecular Ecology, for example, cautions that RAPD-based studies are
discouraged for submission because of such concerns (www.blackwellpublishing.
com). AFLP markers are generally reproducible, but artefacts can arise, as with
RAPDs (Stevens et al. 2007), because of contamination of samples by microorganisms such as fungi. Recent work (e.g. Davis et al. 2003) has shown that
liverworts contain multiple species of fungi living endosymbiotically within the
gametophytes, and the same is true for mosses (A. J. Shaw, unpublished). It has
been suggested that high levels of apparent genetic variation detected in some
mosses could result at least in part from external and/or endophytic fungi
(Stevens et al. 2007).
Microsatellite primers, in contrast, are specifically designed for the organisms
under study and are highly unlikely to amplify endophytes or other contaminating
organisms. Also, unlike RAPDs, AFLPs, and ISSRs, microsatellites are codominant
markers so heterozygotes can be distinguished from homozygotes. This feature is
especially valuable to studies of mating patterns, hybridization, and polyploidy.
Korpelainen et al. (2007) described a relatively simple (and therefore economical)
method for developing microsatellite markers. RAPDs, AFLPs, and ISSRs provide
highly polymorphic data because the number of loci that can be investigated is
virtually unlimited. Much fewer microsatellite loci are typically investigated, but
high resolving power is gained because each locus is multi-allelic. In a group of
closely related Sphagnum species, we (B. Shaw & A. J. Shaw, unpublished) resolve up
to ten alleles at some loci. One potential problem with microsatellite loci is the
possibility of size homoplasy: the independent evolution of indistinguishable
alleles because of high microsatellite mutation rates (Estoup et al. 2002).
11 Bryophyte species and speciation
DNA sequence data are more expensive than fingerprint data to gather, but
have been used for species-level research in both bryophytes and vascular
plants. Researchers have three genomes from which to choose markers: mitochondrial (mtDNA), chloroplast (cpDNA), and nuclear (nDNA). Nacheva &
Cronberg (2007b) recently confirmed that both mitochondrial and chloroplast
DNA are inherited through the maternal parent in Sphagnum. Mitochondrial
genes tend to be relatively conserved and are rarely useful at the population
and species levels in plants (in contrast to animals, where mtDNA is the preferred marker for such studies). No species-level studies based on mtDNA
sequences has been published, although mtDNA genes have been utilized for
phylogenetic problems involving genera, families, and orders (e.g. Cox et al.
2004). cpDNA exhibits moderate levels of variation, and can be useful for
separating species and even for resolving phylogenetic patterns within species.
The two most common regions are trnL–trnF, which includes both intron and
non-coding spacer sequences as well as a small portion of coding region (Quandt &
Stech 2004) and trnG, which includes non-coding intron sequences (Pacak &
Szweykowska 2003). Coding genes such as rbcL are generally too conserved to be
useful at the intraspecific level. The most common nuclear region for speciesand population-level research is the internal transcribed spacer (ITS) of the
ribosomal RNA repeat (nrDNA) (Vanderpoorten et al. 2006). Other nuclear
genes (or, more commonly, introns within them) that have been used for
species-level bryophyte studies include glyceraldehyde 3-phosphate dehydrogenase (gpd: Wall 2005), adenosine kinase (adk: Vanderpoorten et al. 2004,
McDaniel & Shaw 2005), phytochrome (phy: McDaniel & Shaw 2005), glyceraldehyde 3-phosphate dehydrogenase (GapC: Szövényi et al. 2006), and LEAFY/FLO
(Shaw et al. 2004, 2005a). Shaw et al. (2003a) developed anonymous nuclear
regions from which sequence data have proven informative for resolving relationships between and within Sphagnum species. These regions were developed
specifically for Sphagnum; however, the protocol outlined in Shaw et al. (2003a)
could be applied to any other genus.
Following up on research based on isozymes, Pacek et al. (1998) found that
RAPD markers clearly resolve Polish populations of two morphologically cryptic
forms of Pellia epiphylla. The two forms are less differentiated from one another
than between P. epiphylla and P. neesiana, which are morphologically distinguishable, but appear to represent different gene pools.
Stenøien & Saº stad (1999) used RAPD markers, along with isozymes, in a study
of Sphagnum angustifolium, S. lindbergii, S. fallax, and S. isoviitae. Of the four species,
only S. angustifolium varied at isozyme loci, and this species was the most variable
for RAPD markers. Sphagnum fallax and S. isoviitae could not be distinguished by
either marker type, although populations within S. fallax were polymorphic and
457
458
A. J. Shaw
differentiated for RAPDs. The authors considered S. isoviitae and S. fallax to be
conspecific based on their results.
Saº stad et al. (1999b) used isozyme markers and RAPDs to examine genetic
relationships among species in the so-called Sphagnum recurvum complex. Both
types of data resolved two groups, one characterized by brown and the other
by yellow spores. The two populations each of S. angustifolium, S. flexuosum, and
S. recurvum (brown spores) grouped together, but no such grouping could be
discerned in a complex that includes S. fallax, S. brevifolium, and S. isoviitae (yellow
spores). The authors consequently questioned whether the latter represent
different species.
Werner et al. (2004) used ISSR markers to compare the common, widespread
species Weissia controversa and the rare congener W. wimmeriana. The two species
are clearly differentiated, and the rare W. wimmeriana was relatively depauperate in genetic variability.
Patterson et al. (1998) used a PCR–RFLP technique, in which the ITS region
is amplified and then cut with restriction enzymes, for a genetic study of
Leucobryum albidum and L. glaucum in a mixed population where colonies of
these two clump-forming taxa seemed to grade from one species to another.
The main difference between the two species is size, and in particular, the
length of the leaves. Although the distribution of leaf length measurements
taken from plants was continuous with no hint of bimodality, two ITS genotypes
were found at the site. A comparison of morphological and molecular results
showed that plants with one ITS genotype always had leaves greater than 5 mm
long, whereas the other had leaves less than 5 mm. Despite morphological
continuity, at least two distinguishable genetic types are present, and they
differed, on average, morphologically. Data from additional markers are needed
to determine whether the two species are reproductively isolated, since one
locus is insufficient to address that question.
Vanderpoorten et al. (2003b) used the same PCR–RFLP technique to compare
species of Rhytidiadelphus. ISSRs distinguished the four putative species
they sampled but ITS haplotypes only distinguished R. japonicus, R. loreus, and
R. triquetrus from R. squarrosus plus R. subpinnatus. Morphological differences were
correlated with ISSR–ITS haplotypes. This is an example of a circumboreal group
where intercontinental sampling is necessary to thoroughly assess the taxonomic status of the putative species because the study was based on a total of
16 samples from a limited geographic area.
Stech et al. (2006b) used trnL intron and trnL–trnF spacer sequences in a
study of the liverwort genus Tylimanthus. They resolved that two endemic
Macaronesian taxa are sister species and appear to be closely related to a species
that occurs in Reunion and is also disjunct in the Neotropics.
11 Bryophyte species and speciation
Shaw et al. (2005b) gathered sequence data from seven cpDNA and nuclear
genes representing about 20 species of Sphagnum section Acutifolia. Most morphologically defined species were distinguishable, but there was also some
evidence of interspecific gene flow. Sphagnum subtile could not be distinguished
from S. capillifolium, and S. andersonianum could not be separated from S. rubellum.
Surprisingly, S. tenerum, which Crum (1984) considered a variety of S. capillifolium,
turned out to be unambiguously monophyletic, and one of the most genetically
divergent species in the section.
Zhou & Shaw (2008) found that the nearly cryptic species Sphagnum macrophyllum and S. cribrosum (section Subsecunda) are reciprocally monophyletic based
on multilocus sequence data. Fixed nucleotide differences suggest that interspecific gene flow is limited or non-existent. A morphologically aberrant morphotype of S. cribrosum, known informally as the ‘‘wave-form’’ (L. E. Anderson,
pers. comm.), is known only from two Carolina Bays (shallow lakes) in the North
Carolina Coastal Plain. The wave-form is remarkably distinctive, characterized
by sparsely forking stems with no branch fascicles or capitula, but it is anatomically similar to normal S. cribrosum. It looks much more like a Fontinalis than a
Sphagnum. As the name suggests, it had been assumed that the wave-form is a
non-genetic habitat expression, but molecular data revealed that it differs
from normal S. cribrosum, including plants growing in the same lake, in a
number of nucleotide substitutions. Normal S. cribrosum growing at the site
with the wave-form also has a 25 base-pair insertion that is not shared with
sympatric wave-form plants.
European and American populations of Sphagnum pylaesii are reciprocally
monophyletic based on sequence data, but plants from Newfoundland and
South America were barely different (Shaw et al. 2004). Shaw et al. (2005c)
found that haploid and polyploid species in the S. subsecundum complex do not
sort out on the basis of sequences from eight nuclear and cpDNA loci. This turns
out in part to be a result of reticulate evolution involving polyploidy, and
geographically correlated cryptic speciation that was undetected at the time
(A. J. Shaw, unpublished).
Using isozymes, Shaw & Schneider (1995) found two groups of populations
in the rare ‘‘copper moss’’ Mielichhoferia elongata, and resolved the same two
groups in a sequence-based (ITS) study of nearly the same set of populations
(Shaw 2000b). Based on rooting provided by a congeneric outgroup species,
M. mielichhoferiana was resolved as paraphyletic, within which was nested both
(morphologically cryptic) groups of M. elongata. The two groups of populations
within M. elongata have partially allopatric geographic ranges but occur in the
same general area of Colorado, in the Rocky Mountains. Inter-group mixtures
were not observed within individual colonies.
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Discriminant analysis of morphological characters scored from 76 herbarium
specimens representing four putative species in the Tortula subulata complex
resolved four morphotypes (with some overlap) (Cano et al. 2005). Sequence data
from the ITS region indicated that morphological types attributable to T. mucronifolia and T. schimperi are monophyletic. Two clades that differ in 17 indel
mutations were resolved within T. mucronifolia. The two clades are partly allopatric along a north–south gradient in Europe; one found in Spain and Italy east to
Ukraine, and the other found in Sweden, Greenland, Russia, and also Canada
and Alaska. Cano et al. (2005) interpreted these two clades as cryptic species. In
contrast to T. mucronifolia and T. schimperi, T. inermis was more weakly supported
as monophyletic and may be nested within a paraphyletic T. subulata. Taxonomic
varieties of T. subulata were not resolved as reciprocally monophyletic, but
support in that part of the tree was weak so monophyly probably could not be
rejected (and the authors did not explicitly test this). ITS sequences from North
America and Europe, respectively, were very similar in both T. mucronifolia and
T. schimperi.
Stech & Dohrmann (2004) sequenced the nuclear ITS region and the
cpDNA atpB–rbcL spacer in 22 species of Campylopus, with a focus on C. pilifer
and C. introflexus. Campylopus introflexus was resolved as monophyletic, with little
infraspecific variation, whereas C. pilifer was paraphyletic because C. introflexus
was nested within it. Molecular data suggested divergence between New and Old
World populations of C. pilifer, although the New World populations were paraphyletic. The Old World populations of C. pilifer were nested within the New
World populations (suggesting possible dispersal from the Old to the New
World), and C. introflexus was in turn nested within the Old World populations.
Using nucleotide sequences from the nuclear (ITS) and chloroplast (trnL–trnF)
genomes, Shaw & Allen (2000) found that groups of species defined by leaf
morphology within the aquatic moss genus Fontinalis are non-monophyletic.
Fontinalis antipyretica, a species found in both North America and Europe, is
paraphyletic because European populations are more closely related to another
European species (F. squamosa) than they are to North American populations of
F. antipyretica. Similarly, North American populations of F. antipyretica are more
closely related to other North American species (F. gigantea and F. chrysophylla)
than they are to the European populations of F. antipyretica. These observations
suggest that speciation in temperate Fontinalis species has been allopatric and
that widespread morphotypes may be old and non-monophyletic.
Several authors have used isozymes and DNA-based information to support
the description of new taxa. Flatberg & Thingsgaard (2003) showed that isozyme patterns corroborate morphological observations when they described
Sphagnum tundrae from Svalbard. So & Grolle (2000) provided evidence from
11 Bryophyte species and speciation
RAPD markers when they described Plagiochila detecta. Shaw & Goffinet (2000)
showed that Sphagnum ehyalinum is an intersectional hybrid when they described
it as new from Chile. The new species has cpDNA of section Subsecunda and
nuclear DNA of section Cuspidata. Shaw (2000c) found that a new species of
Schizymenium from California occurred sympatrically with morphologically similar plants of Mielichhoferia elongata. The two species have very similar gametophytes, differing mainly in sporophyte morphology. Primers were designed that
would only amplify the ribosomal DNA of M. elongata in order to survey and
identify ambiguous sterile plants from sites in the Sierra Nevada Mountains.
Pfeiffer et al. (2000) found that five putative species in the ‘‘Hypopterygium
tamarisci complex’’, a group that is widespread in the Southern Hemisphere,
could not be distinguished by about 300 nucleotides of cpDNA trnLUAA sequence.
A similar lack of differentiation between Patagonian and New Zealand populations of Weymouthia led Quandt et al. (2001) to conclude that putatively allopatric
species in this group should be synonymized. Their data was based on sequences
from the ITS2 region of nuclear DNA and longer cpDNA sequences that included
the trnL intron as well as the non-coding spacer between the trnL and trnF genes.
Goffinet et al. (2007) compared cpDNA sequences from two loci (trnL–trnF and
rps4) in a putative new species of Orthotrichum from Chile with those from the
morphologically similar Northern Hemisphere species O. alpestre. Although the
Chilean species (described as O. freyanum) is very similar in morphology to
O. alpestre, it turned out to be more closely related to a sympatric South American
species, O. assimile, which occurs in proximity to the new species on Nothofagus bark.
Stech & Frahm (1999a) compared 375 nucleotides of the trnL intron and 521
nucleotides of the ITS nuclear region in two specimens collected at the same site
in Germany. One specimen was typical Platyhypnidium riparioides and the other
was P. mutatum, a species recently described from plants collected at the site and
known only from there. Stech and Frahm found that the two plants had identical trnL intron sequences and differed by only one substitution in the ITS
region, and concluded that they were conspecific.
Budke & Goffinet (2006) sequenced one nuclear and two cpDNA regions to
test species concepts in the moss genus Timmia. Based on 27 samples, they
concluded that T. austriaca, T. megapolitana subsp. megapolitana, and T. megapolitana subsp. bavarica are demonstrably monophyletic, whereas the varieties of
T. norvegica were not, in part owing to the nested position of T. siberica; consequently they combined the two species taxonomically.
Feldberg & Heinrichs (2005, 2006) used the cpDNA trnL–trnF region and
nrITS for an analysis of Neotropical Herbertus species. This study is a very nice
example of a combined taxonomic revision, with keys, illustrations, descriptions, etc., and a molecular analysis of relationships within and among species.
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Partly on the basis of their molecular results, Feldman and Heinrichs combined
several previously recognized South American binomials under a single species,
H. juniperoideus. Their phylogenetic analysis demonstrated multiple dispersals
between the New and Old Worlds, involving plants presently found in Europe,
Africa, and South America. Groth et al. (2003, 2004) and Heinrichs et al. (2003,
2005, 2006) also demonstrated multiple dispersals in the leafy liverwort genus
Plagiochila between tropical America and Africa and/or Asia. Long-distance dispersal appears to be infrequent and speciation has occurred in disjunct regions
to produce geographically restricted species groups, but it is difficult to interpret the phylogeny of Plagiochila without hypothesizing occasional long-distance
range expansions, along with extinction in some areas. ITS sequences of
P. cambuena from Madagascar were very similar to those of P. corrugata from
Brazil, prompting the authors to synonymize them (Heinrichs et al. 2003).
Heinrichs et al. (2005) also found little divergence between South American
and African plants of P. boryana, P. punctata, and P. stricta, which they interpreted
as evidence of long-distance intercontinental dispersal. Based on their phylogenetic analyses, it appears that the direction of dispersal was from South America
to Africa.
11.4
Speciation mechanisms in bryophytes
Hybridization in natural populations can provide a window into evolutionary processes relevant to speciation; a thorough review of natural bryophyte
hybrids was provided by Natcheva & Cronberg (2004). Premolecular studies of
naturally occurring moss hybrids and mechanisms of reproductive isolation
were reviewed by Anderson & Snider (1982). Relatively few studies of hybridization in natural bryophyte populations based on genetic data have been
published.
Shaw (1994, 1998) documented viable recombinant gametophytes derived
from hybrids between Mielichhoferia elongata and M. mielichhoferiana, and found
that most recombinants were genetically closer to M. mielichhoferiana than
to M. elongata. Natcheva & Cronberg (2007a) found that interspecific recombinant gametophytes derived from hybrid sporophytes involving Sphagnum
capillifolium and S. quinquefarium consistently had the maternal cpDNA of
S. quinquefarium, but were closer to S. capillifolium in terms of nuclear ISSR
markers. The asymmetric nature of interspecific recombinants in terms of
nuclear DNA, observed by Shaw in Mielichhoferia and by Natcheva and
Cronberg in Sphagnum, could reflect back-crossing to one of the parental species,
or lower fitness of recombinants that have a more even contribution of genetic
material from the two parents. Recombinant sphagna grown from spores
11 Bryophyte species and speciation
exhibited the same asymmetry of parental contributions, supporting the latter
interpretation (Natcheva & Cronberg 2007a). These observations suggest that
genic interactions, perhaps involving organellar and nuclear loci, may be important in determining the result of interspecific hybridization and, conversely, the
evolution of reproductive isolation. In the case of S. capillifolium–S. quinquefarium
hybrids, experimentally grown recombinants were viable and performed well
under a range of environments (Natcheva 2006). These were the recombinants
that contained a preponderance of S. capillifolium nuclear markers.
Using microsatellite markers, van der Velde & Bijlsma (2004) found no
evidence of established interspecific recombinant gametophytes between
Polytrichum commune and P. uliginosum, which appear to be reproductively isolated. Within a sympatric population, however, hybrid, albeit abortive, sporophytes were found attached to P. uliginosum female gametophytes, but not on
P. commune females. Hybrid sporophytes produced few if any viable spores. It
appears that the mechanisms of reproductive isolation between these two
species is asymmetric: prezygotic or very early postzygotic when P. commune is
the female parent (i.e. hybrid sporophytes do not form or at least do not develop
to a visible stage) and postzygotic when P. uliginosum is the female parent (hybrid
sporophytes begin development but abort).
A first attempt to get at the genetic basis of hybrid breakdown was conducted
by McDaniel (2005) using a QTL (quantitative trait loci) approach. McDaniel
found that reduced protonemal growth in a cross between genetically divergent
populations of Ceratodon purpureus could be traced to multiple unlinked loci.
He also demonstrated that non-additive interactions among loci (i.e. epistasis)
contributed to reduced protonemal growth of inter-racial hybrids. McDaniel’s
analyses thus provide direct evidence of genic interactions affecting the outcome of mating between genetically differentiated plants.
New species of bryophytes undoubtedly originate in a variety of ways including the geographic subdivision of ancestral ranges (classic allopatric speciation),
through founder events associated with infrequent long-distance dispersal, and
through cytological mechanisms such as polyploidization. Many bryophytes
make good experimental organisms, yet the pioneering work of von Wettstein
(reviews: 1928, 1932) has not been followed up in recent years.
So what do we know about speciation mechanisms in bryophytes?
Unfortunately, not much. Anderson (1963) and Crum (1972) argued mainly
from biogeographical observations that many or most bryophyte species are
ancient, and that the broad geographic distributions characterizing many taxa
result from vicariance associated with continental drift. Crum (1972) argued
extensively that long-distance dispersal as a general explanation for the common intercontinental geographic distributions of many bryophytes is highly
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unlikely. It is now clear from experimental (van Zanten 1978), atmospheric
(Muñoz et al. 2004), and phylogenetic (see above) data that intercontinental
long-distance dispersal, while not common, has played an important role in
generating the geographic distributions of bryophyte species. Molecular analyses have corroborated taxonomic conclusions that many tropical species are
disjunct across several continents and such disjunctions appear to be especially
common between the Neotropics and Africa. It should nevertheless always be
kept in mind that finding a lack of divergence between disjunct populations is a
negative result and does not preclude the possibility that additional markers
will reveal differentiation. In the Northern Hemisphere temperate and boreal
zones, it is fair to generalize that most species have continuous or discontinuous
intercontinental ranges and there is little evidence from molecular markers of
significant intercontinental divergence. (See, however, isozyme evidence provided by Cronberg (1998) of divergence between British and Scandinavian populations of Sphagnum rubellum.)
So the question remains, how do we explain the broad geographic distributions of many bryophyte species without substantial morphological differentiation among widely disjunct populations, and in many cases, without obvious
genetic differentiation as well? Either there is sufficient intercontinental gene
flow to prevent differentiation, or divergence is slow indeed, as Crum (1972) and
others have suggested. Neither a level of gene flow sufficient to cause genetic
homogenization, nor such slow evolution that populations have not diverged
by genetic drift over millions of years, seem very likely, yet there appears to
be no other explanation! Stenøien & Saº stad (1999) interpreted the lack of
genetic differentiation between North American and European populations of
Sphagnum angustifolium as slow evolution, due to very large effective population
sizes that make genetic drift negligible. Whether this is true, is hard to test. It
seems clear that bryophytes are able to disperse effectively over both short and
long distances and such changes in distribution erase historical information
that might be used to make inferences about speciation modes. For this reason,
bryophytes are not always very good organisms for formulating and testing
hypotheses about speciation mechanisms thought to be common, such as allopatric divergence caused by drift or natural selection.
The most studied mode of speciation in bryophytes is through allopolyploid
formation. Wyatt et al. (1988) first demonstrated allopolyploidy in bryophytes, and since then allopolyploids have been documented in at least 12
genera (Table 11.2). Allopolyploids involve hybridization followed by chromosome doubling (polyploidization). Polyploidization in bryophytes was
assumed by early authors to result primarily from apospory: the regeneration
of diploid gametophytes from immature sporophyte tissues (e.g. Anderson
11 Bryophyte species and speciation
1980, Wyatt & Anderson 1984). Apospory has been reported in both mosses and
liverworts (Lal 1984). However, recent work suggests that diplospory – the
production of unreduced spores – might be as or more important a mechanism,
especially in the generation of stable allopolyploid species (Saº stad 2005,
Flatberg et al. 2006). Saº stad (2005) estimated that approximately 5%–10% of
liverwort species and 6%–19% of moss species are polyploids, and thus genome
duplication has been an important process in bryophyte evolution. Saº stad
(2005) argued that no well-established examples of autopolyploidy exist; all
polyploid species that have been studied genetically appear to be allopolyploids.
Infraspecific variation in chromosome numbers is common as well (Fritsch
1991), and autopolyploidy may also be important in bryophyte evolution.
There has been little study of genetic and phylogenetic relationships among
polyploid ‘‘races’’ within individual, morphologically defined species.
Consequently, Saº stad’s (2005) rejection of autopolyploidy as an important feature of bryophyte evolution may have been premature.
The primary evidence in favor of polyploid bryophytes being of hybrid origin
is the observation of fixed heterozygosity for molecular markers. That is, all
sampled gametophytes are heterozygous for codominant markers, suggesting
that the alleles do not segregate at meiosis to yield both homozygotes and
heterozygotes. Fixed heterozygosity occurs when the two haploid genomes
present in a diploid gametophyte are sufficiently differentiated that chromosomes do not pair properly and segregate. It is worth noting that the absence of
homozygotes in a population survey, while suggestive, provides only indirect
evidence that heterozygosity is fixed. Studies involving growth of gametophytes
from spores in order to test for segregation directly is the only way to demonstrate unequivocally that heterozygosity is really fixed. Inferences based on
population surveys require sufficient sample sizes to adequately demonstrate
that homozygotes were not simply missed.
Important questions addressed by studies on polyploid bryophyte species
are as follows. (1) Is the polyploid an allo- or autopolyploid? (2) What (is) are
the parental species? (3) If allopolyploid, what is the maternal parent and is
that species always the maternal parent? (4) How many times has the polyploid originated? (5) Is (are) the origin(s) recent or ancient? Once these
questions have been answered, then polyploids are valuable species for
addressing questions about molecular evolution following genome duplication (Wendel 2000).
11.4.1
Allopolyploidy in liverworts
The European species of Pellia are perhaps the most thoroughly studied
group of taxa, through a variety of molecular techniques. Isozymes and RAPDs
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have shown that both P. endiviifolia and P. epiphylla consist of at least two morphologically cryptic taxa (Szweykowski et al. 1981b, Zielinski 1984, 1987,
Szweykowski & Odrzykoski 1990). Moreover, the polyploid species, P. borealis,
is an allopolyploid with P. epiphylla ‘‘cryptic species N’’ and P. epiphylla ‘‘cryptic
species S’’ as the progenitors. Fixed heterozygosity for isozyme alleles in
P. borealis show that the cryptic species differ in significant genomic features
such that homeologous chromosome pairing and independent assortment are
precluded (Odrzykoski et al. 1996). Fiedorow et al. (2001) used a PCR–RFLP
technique to compare tRNALEU genes in the haploids and polyploids and found
an additive pattern in P. borealis. Sequences from the same region indicated that
P. borealis differs from the two progenitors only slightly. Pellia borealis is one of
only a few bryophyte allopolyploids in which male and female parentage has
been ascertained; P. epiphylla ‘‘cryptic species N’’ contributed the mt- and cpDNA
for all of 14 Polish populations of P. borealis sampled.
Reboulia hemisphaerica is traditionally considered to be the only species in this
genus, but Boisselier-Dubayle et al. (1998b) found that it consists of three genetically differentiated but morphologically cryptic haploid taxa (pairwise Nei’s
I ¼ 0.325–0.550). In addition, plants from New Zealand and Australia proved to
be polyploid. Only one isozyme locus, AAT, was heterozygous in the polyploids,
but the same heterozygous pattern was found in the two polyploid samples
analyzed, one from New Zealand and one from Australia. One of the alleles
present in the heterozygotes was also detected in the Japanese cryptic haploid
species of R. hemisphaerica (R. hemisphaerica var. japonica) and the other occurred in
European populations of R. hemisphaerica s. str. (R. hemisphaerica var. hemisphaerica). The polyploid was interpreted as an allopolyploid involving these two
parents. Polyploid colonies in New Zealand and Australia are genetically closer
to the European haploids but are morphologically more similar to the Japanese
haploids. Additional markers are needed to test the hypothesis that the whole
genome, rather than just the locus coding for AAT, is duplicated.
Boisselier-Dubayle & Bischler (1998) found that the complex thalloid liverwort genus Corsinia, previously considered monospecific, consists of at least
three morphologically cryptic taxa, one haploid and two diploid. Corsinia coriandrina (s. l.) is widespread though sporadic in southern Europe and Micronesia
and is also found in the U.S.A. and South America. One sample from Texas
proved to be diploid, as were some samples from the Mediterranean region.
New World and Old World diploids appear to have originated independently,
and were highly divergent. European diploids exhibited fixed heterozygosity at
six of eight enzyme systems assayed and some alleles could have been provided
by the sampled haploid form, but other alleles could not be accounted for, so an
additional unsampled parent is implied.
11 Bryophyte species and speciation
Porella baueri, with a chromosome number of N ¼ 16, is the only reported
polyploid in that genus (Boisselier-Dubayle et al. 1998a). The polyploid exhibits
fixed heterozygosity at four of 13 isozyme loci and alleles present at these and
the remaining homozygous loci occurred in either or both of the putative
haploid parents, P. cordeana and P. platyphylla. Populations of the polyploid,
P. baueri, from Western Europe tended to be morphologically and genetically
closer to P. cordaeana, whereas eastern European populations were closer to
the other parent, P. platyphylla. Jankowiak and Szwekowska-Kulinska (2004)
recently showed that P. cordaeana was the maternal parent, based on cpDNA
and mtDNA sequences. At least two origins of the polyploid were inferred from
the observation that two different alleles of phosphatase were detected in each
of the putative haploid parents, and both turned up in different polyploid
individuals. Porella baueri appears to be sexually fertile, and some preliminary
indication of recombination between sympatric haploids and diploids was
detected.
A more complex history was inferred for triploids in the thallose liverwort
genus Targionia (Boisselier-Dubayle & Bischler 1999). Targionia hypophylla (N ¼ 9)
and triploids known as T. lorbeeriana (N ¼ 27) are widespread in both the New and
Old Worlds. European and Macaronesian populations include both haploids and
triploids and the two cytotypes occur sympatrically and sometimes close
together, although apparently not in mixed colonies. Haploids appear to be
more common in northern Europe and triploids more common in southern
Europe. Triploids exhibited fixed heterozygosity at all of the seven isozyme loci
investigated. European triploids contain two sets of alleles from the European
haploids, while a third set of alleles was not detected in any haploid population
and the authors hypothesized that the other parent is extinct. They excluded
other allopatric species of Targionia as potential parents based on morphological
considerations. Based on limited sampling, African and Australasian triploids
had a highly divergent allelic profile so Boisselier-Dubayle & Bischler (1999)
interpreted them as independently derived. In total, a minimum of three origins
were hypothesized for triploid Targionia; two in Europe and one in Africa/
Australasia. Boisselier-Dubayle & Bischler (1999) hypothesized that triploids
originated by hybridization and chromosome doubling, followed by meiotic
non-disjunction.
Southern Hemisphere gametophytes of Plagiochasma rupestre are haploid
(N ¼ 9), but European samples are gametophytically diploid (Boisselier-Dubayle
et al. 1996). Although Boisselier-Dubayle et al. initially assumed the diploids were
derived by autopolyploidy, they assayed AAT isozymes from sporelings germinated from experimentally crossed plants and found no segregation of alleles.
Tetrasomic inheritance would have been expected if the autopolyploid
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hypothesis were correct, so these authors suggested that P. rupestre is an allopolyploid. This is the only published study in bryophytes that actually shows,
experimentally, that heterozygotes are fixed rather than segregating.
Buczkowska et al. (2004) assayed four enzyme systems in 223 Polish
samples of the leafy liverwort Calypogeia, representing six species. Only nine
multilocus haplotypes were detected, but three species, C. azurea, C. muelleriana,
and C. sphagnicola, were shown to be polyploid based on chromosome counts,
and exhibited apparent fixed heterozygosity for one or two enzymes. Although
the authors acknowledged that additional work is necessary to corroborate their
interpretation, they considered the latter three species to be allopolyploids. For
the enzyme TPI, variation in the allelic composition among polyploid species
suggests independent origins.
11.4.2
Allopolyploidy in mosses
Three species of Polytrichastrum, namely P. pallidisetum, P. sexangulare, and
P. ohioense, are allopolyploids based on fixed heterozygosity at five or six of eleven
isozyme loci screened from some 7000 shoots representing 304 populations
(Derda & Wyatt 2000). Isozyme profiles from the polyploids were sufficiently
differentiated from any haploid species sampled that parents could not be identified. It appears that the hybrids are derived from crosses between species in
different genera of Polytrichaceae, possibly involving Polytrichum, Polytrichastrum,
and Pogonatum. Monophyly of and phylogenetic relationships among these genera
are, however, incompletely resolved at present (Hyvönen et al. 2004). Haploid
species including Polytrichastrum appalachianum and Polytrichum commune have isozyme alleles that might indicate that they were involved in the parentage of one
or more of the polyploids, but other species could not be eliminated. Derda &
Wyatt (2000) speculated that polyploidization might have occurred so long ago
that precise parentage may never be uncovered.
Polytrichum longisetum also appears to be an allopolyploid based on fixed heterozygosity of four isozyme and 12 microsatellite loci (van der Velde & Bijlsma 2001).
Forty-three percent of the microsatellite loci assayed for P. longisetum exhibited a
single band, and therefore appeared to be homozygous. These authors, however,
argued that because microsatellite loci have very high mutation rates, these
seemingly homozygous loci were unlikely to result from indistinguishable alleles
in the two progenitor species. Rather, they thought the single banded patterns
reflected a failure to amplify one of the two alleles. They concluded from their
analyses that the haploid species, P. formosum, or a taxon very similar to it, was one
of the parents, but they could not identify the other parent. As in the case of
Polytrichastrum studied by Derda & Wyatt (2000), these results suggest that the
allopolyploid does not have a recent origin.
11 Bryophyte species and speciation
Rhizomnium pseudopunctatum is an allopolyploid of R. gracile of western North
America and northern Asia, and R. magnifolium of Europe (Wyatt et al. 1993b).
Although the two putative progenitor species are currently allopatric and their
ranges could not be much more disjunct, the genetic evidence is strong that they
gave rise to R. pseudopunctatum. If true, this observation provides a statement
about how current distributional ranges may be misleading in the formulation
of hypotheses about bryophyte speciation. Jankowiak et al. (2005) demonstrated
from cp- and mtDNA sequences sampled from the two parents and the allopolyploid that R. magnifolium is the maternal parent, assuming that organellar
inheritance is only through the female.
Plagiomnium medium is an allopolyploid derivative of P. ellipticum and P. insigne
(Wyatt et al. 1988, 1992). Isozyme alleles found in the allopolyploid were
detected in different individuals of the two parents, indicating multiple origins.
In addition, more than 30 different multilocus isozyme genotypes were detected
in P. medium, suggesting recombination among allopolyploid individuals subsequent to their origin(s). Restriction digests of cpDNA from the two parents and
P. medium indicate that P. insigne is the maternal parent. However, RFLP analysis
of whole chloroplast genomes is too crude to determine whether there is variation at the cpDNA sequence level within the polyploid or its parents.
Plagiomnium cuspidatum also appears to be an allopolyploid based on fixed or
nearly fixed heterozygosity at eight allozyme loci (Wyatt & Odrzykoski 1998).
The east-Asian P. acutum appears to be one parent but the other could not be
identified. During the course of their investigations, Wyatt & Odrzykoski (1998)
also uncovered genetic evidence of previously unrecognized species, one of
which was subsequently described (Wyatt et al. 1997).
Only two chromosome numbers have been reported in the genus Sphagnum,
N ¼ 19 and 38 (Fritsch 1991). Cronberg (1996) presented isozyme evidence that
S. russowii (N ¼ 38) is an allopolyploid with S. girgensohnii and either S. quinquefarium
or S. rubellum as progenitors. Shaw et al. (2005b) reported corroborating evidence
from nuclear and chloroplast DNA sequences, also suggesting that S. russowii has
originated multiple times, and one origin might have involved S. warnstorfii as
well. Flatberg et al. (2006) described hybrid sporophytes in a mixed population of
S. girgensohnii and S. russowii, derived from inter-ploidal backcrossing. The hybrid
sporophytes were found only on female S. girgensohnii gametophytes. Less than 5%
of the spores in hybrid capsules germinated but triploid plants were successfully
reared to at least a juvenile gametophyte stage. Hybrid sporophytes on female
S. girgensohnii gametophytes were reported by the authors from scattered
Scandinavian sites, and were also found at the same Norwegian site in multiple
years. The extent to which triploid hybrids between S. girgensohnii and S. russowii
persist in nature, or cross with either of the progenitors, is unknown.
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A. J. Shaw
N
S. tenellum
2N
S. troendelagicum
N
S. balticum
2N S. jensenii
S. cuspidatum
N
S. majus
2N
S. annulatum
N
Fig. 11.1. Hypothesized ancestry for allopolyploid species of Sphagnum section Cuspidata. Four
(gametophytically) haploid species (N), S. tenellum, S. balticum, S. cuspidatum, and S. annulatum,
have given rise to three allopolyploid species (2N), S. jensenii, S. majus, and S. troendelagicum with
overlapping parentage. Summarized from results of Saº stad et al. (1999a, 2000, 2001).
Flatberg et al. pointed out that because of the huge numbers of spores produced by
hybrid sporophytes, 5% germination could yield thousands of viable offspring.
Several allopolyploid species have been documented in Sphagnum section
Cuspidata (Fig. 11.1). Saº stad et al. (2000) found that the boreal species, S. majus,
exhibits fixed heterozygosity at three out of nine isozyme loci assayed, while
two other loci were homo- or heterozygous in different individuals. Both alleles
detected at the loci characterized by fixed heterozygosity were found also in the
haploid species S. cuspidatum and S. annulatum. Six alleles found in the polyploid
were not detected in either putative parent. These authors suggested that a
relatively high frequency of orphan (or silenced) alleles in S. majus might indicate an ancient origin (and subsequent divergence from the ancestral allopolyploid(s)). In contrast, all alleles of another allopolyploid in section Cuspidata,
S. jensenii, were detected in one or both putative parents (S. balticum and
S. annulatum), suggesting a more recent origin (Saº stad et al. 1999a). Sphagnum
jensenii exhibited fixed heterozygosity at four out of nine isozyme loci assayed.
Different polyploid individuals had common MNR-1 alleles found in different
plants of S. balticum, suggesting at least two independent origins.
In contrast to the broad geographic ranges of Sphagnum majus and S. jensenii,
another allopolyploid Sphagnum, S. troendelagicum, is endemic to a relatively
small area of central Norway. Isozyme and RAPD data support an origin for
S. troendelagicum through hybridization between S. tenellum and S. balticum (Saº stad
et al. 2001). Fixed heterozygosity was observed at two loci in S. troendelagicum and
11 Bryophyte species and speciation
both alleles at each locus were also found in S. balticum and/or S. tenellum. The
allopolyploid exhibited limited polymorphism at isozyme loci but was highly
polymorphic for RAPD markers (Stenøien & Flatberg 2000, Saº stad et al. 2001).
Surprisingly, there was little or no linkage disequilibrium among RAPD markers
in three intensively sampled populations of S. troendelagicum (Stenøien &
Flatberg 2000). Sexual reproduction has never been observed in S. troendelagicum,
so even if the polyploid originated several times, strong linkage disequilibrium
would be expected. Recent, unpublished cpDNA sequences indicate that
S. tenellum is the chloroplast parent (Stengrunet et al., unpublished data).
Sphagnum balticum appears to have participated in the origin of at least two
allopolyploid species in section Cuspidata (S. jensenii and S. troendelagicum).
Similarly, S. annulatum appears to be one parent of both S. majus and S. jensenii.
These observations clearly indicate that species of section Cuspidata are able to
hybridize with related species and it may be that the high levels of phenotypic
variation characteristic of these species reflect hybridization in natural populations.
Allopolyploidy also appears to be common in Sphagnum section Subsecunda. Of
the species found in Europe and eastern North America, S. contortum, S. platyphyllum, and S. subsecundum appear to be consistently haploid whereas S. auriculatum, S. carolinianum, S. inundatum, and S. lescurii are polyploid (Fritsch 1991,
Melosik et al. 2005, A. J. Shaw, unpublished data). Here the evolutionary patterns
are complex and raise challenging taxonomic problems; many of the data are
currently unpublished but well-supported aspects of the story are briefly summarized. Sequence data from the chloroplast and nuclear genomes, and microsatellites, show that the North American polyploid species S. lescurii is distinct
from the European polyploid S. auriculatum. Furthermore, European S. inundatum
originated independently of North American S. inundatum and the two are
differentiated for both nuclear and chloroplast markers. On the other hand,
the North American polyploids S. carolinianum, S. lescurii, and (American populations of) S. inundatum cannot be distinguished by cpDNA or nuclear sequences
and differ only very slightly in microsatellite allele frequencies. Similarly,
European S. inundatum and S. auriculatum are undifferentiated for either
sequence-based or microsatellite markers. Sphagnum contortum and S. platyphyllum were eliminated as haploid parents; only S. subsecundum is implicated by
both cpDNA sequences and microsatellite markers. The other parent may be an
unsampled race of S. subsecundum or some other, perhaps extinct, species.
11.5
Tempo and mode of allopolyploid evolution
We do not have any way to know with confidence how old allopolyploid
bryophyte species are. In the absence of direct methods for dating allopolyploid
471
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A. J. Shaw
origins, we can infer that if all alleles found in the allopolyploid species can also
be detected in the parental haploids, the origin may have been relatively recent.
Examples include Sphagnum jensenii and S. troendelagicum. The latter species is
highly restricted in geographic distribution and presently occurs sympatrically
with the two parental haploids. It may be very recent. The allopolyploid Pellia
borealis may be a relatively recent derivative of two European, morphologically
cryptic haploid species. Similarly, the allelic profile of polyploid Porella baueri
can be completely accounted for by alleles found in two haploid species,
P. cordeana and P. platyphylla. Polyploid species of Polytrichastrum, in contrast,
may have originated so long ago that we cannot even identify the parental
haploids, which may be extinct. In Rhizomnium, the parental haploids can be
identified, but presently have widely disjunct allopatric distributions. Clearly
the allopolyploid is old enough that major range changes have occurred since
the haploids had opportunities to hybridize. When sufficient data have been
collected, it appears that some or perhaps most allopolyploid bryophyte species
originated multiple times. This is in keeping with what we know about allopolyploid origins in vascular plants (Soltis & Soltis 1999).
11.6
Reconciling evolutionary inferences from molecular
data with species concepts
To some extent the controversy over biological versus phylogenetic
species concepts is an artificial one. Phylogenetic concepts that define species
as the least inclusive group of populations/individuals that are hierarchically
related (Nixon & Wheeler 1990) are based on the fact that relationships below
the species level are reticulate rather than hierarchical because of recombination. Moreover, reciprocal monophyly of related species can only occur when
they have been reproductively isolated for sufficient time for allele coalescence
to occur within species. At least partial reproductive isolation is necessary, even
if not sufficient, for speciation to proceed. Thus, evolutionary biologists focused
on speciation mechanisms (e.g. Coyne & Orr 2004) tend to adopt a biological
species concept whereas those focused on defining and delimiting species prefer phylogenetic approaches.
Allopolyploids present special problems for taxonomists. It is now known
that most allopolyploid ‘‘species’’ have originated multiple times and in some
cases there is genetic evidence of more than ten origins for a single taxon (Soltis &
Soltis 1999). Such species are thus demonstrably polyphyletic; what is a
taxonomist to do? Inferences that polyphyletic allopolyploids go on to function
as biologically meaningful species come from evidence of genetic recombination among independently derived plants and animals (e.g. Wyatt et al. 1988,
11 Bryophyte species and speciation
1992, Doyle et al. 1999, Espinoza & Noor 2002). It is standard practice to recognize allopolyploids as species, even when known to be polyphyletic. Yet the
practice goes contrary to any phylogenetic species concept that requires monophyly. The alternative is to recognize two, three, . . . ten or more monophyletic
species that cannot be distinguished morphologically, and which in some cases
at least appear to function together as ‘‘evolutionarily significant units’’.
Molecular approaches to study polyploid formation have clarified some aspects of
bryophyte evolution, but have perhaps muddied the waters of bryophyte
taxonomy.
Acknowledgment
Preparation of this chapter was supported by NSF grant DEB-0515749.
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12
Conservation biology of bryophytes
a l a i n va n d e r p o o r t e n a n d t o m a s h a l l i n g b ä ck
12.1
Introduction
Conservation biology is a fairly new, multidisciplinary science that has
developed to deal with the crisis confronting biological diversity (Primack 1993).
As a crisis discipline, conservation biology arose in response to an increasingly
formulated political demand to face the dramatic loss of biodiversity and the
need to take steps to anticipate, prevent, and reverse the trend (Heywood &
Iriondo 2003). Subsequent ratification of the Convention on Biological Diversity
at the United Nation conference held in Rio in 1992 by most of the world’s
governments has placed the subject of biodiversity firmly on the political
agenda.
The past few years have witnessed a major evolution in our understanding of
conservation. The increasing need for performing tools has rendered conservation biology a truly multidisciplinary science, feeding on a variety of other areas,
including ecology, demography, population biology, population genetics, biogeography, landscape ecology, environmental management, and economics
(Heywood & Iriondo 2003). Conservation interest has also been progressively
enlarged to include a broad array of taxa that used to be completely overlooked.
Cryptogams were, for example, the focus of only about 4% of published
papers between 2000 and 2005 in leading conservation journals (Hylander &
Jonsson 2007). The situation has been most recently changing and there
has been an increasing awareness of the necessity to include cryptogams in
general, and bryophytes in particular, in conservation programs (Hylander &
Jonsson 2007).
The reasons for a late but growing interest in bryophyte conservation are
manifold. Although bryophytes are rarely the most conspicuous elements in the
Bryophyte Biology: Second Edition, ed. B. Goffinet & A. J. Shaw. Published by Cambridge University Press.
# Cambridge University Press 2008.
488
A. Vanderpoorten and T. Hallingbäck
landscape, they play important ecological roles in terms of water balance,
erosion control, or nitrogen budget, or simply by providing habitat for other
organisms (Longton 1992). Furthermore, bryophytes locally exhibit richness
levels that are comparable to or even higher than those of angiosperms. In
boreal forests, for example, bryophyte diversity often exceeds that of vascular
plants at a scale of 0.1 ha (Berglund & Jonsson 2001). In wet sclerophyll forest of
Tasmania, the ratio of the number of bryophyte to vascular plant species is often
5 : 1 (Pharo & Blanks 2000). Lastly, and perhaps most importantly, diversity
patterns in bryophytes do not necessarily follow the patterns present in other,
better-studied taxa (Sérgio et al. 2000, Pharo et al. 2005), so that an enlarged
concept of biodiversity has become increasingly necessary.
In this chapter, we review the tools that are available for assessing threat
levels in bryophytes and emphasize in particular how the IUCN classification
system can be applied to the specific case of bryophytes. We then provide an
overview of global threat levels and conservation needs and review the mechanisms by which bryophytes are, at least locally, severely threatened. Finally, we
discuss appropriate conservation strategies for preserving and managing bryophyte diversity. We conclude by some perspectives regarding the need for and
possibilities of implementation of a novel, evolutionary approach to biodiversity that may complement and, perhaps, eventually replace the traditional
approach focused on threat levels and phenetic species concept.
12.2
Levels of threats and the need for conservation
12.2.1
What to conserve? A hierarchical system of threat categories applied to bryophytes
The IUCN classification system
Conservation, ‘‘the philosophy of managing the environment in such a
way that does not despoil, exhaust, or extinguish it’’ (Jordan 1995), is by definition concerned with the threat of extinction of species, communities, or ecosystems due to human activities. To date, the number of species believed to be
under some degree of threat makes necessary the use of a system of classification that helps categorize species according to the risk of extinction they are
facing (Heywood & Iriondo 2003).
The likelihood of extinction of a species must be assessed against certain
criteria. This is the purpose of a red list. The most obvious option for bryophyte
species status assessment is to apply the most recent criteria and threat categories of the International Union for the Conservation of Nature and Natural
Resources (hereafter, IUCN) (IUCN 2001). The IUCN criteria have the advantages
that (a) they have been elaborated after much thought by a great number of
12 Conservation biology of bryophytes
Table 12.1 IUCN criteria of species threat categories
Criterion
Threshold
Declining population
30–90% population decline during a time period of
Rarity and decline
EOOa <20 000 km2 or AOOb <2000 km2 and severe
10 years or 3 generations, whichever is the longest
fragmentation, continuing decline, or extreme
fluctuations
Small population size and
Population size <250 reproductive individuals and
fragmentation, decline, or
continuing decline of >10% in 10 years or
fluctuations
3 generations
Very small population size or very
restricted distribution
Quantitative analysis of
extinction risk
Number of individuals <1000 or AOOb<20 km2
(or <5 locations)
Population viability analysis (Gärdenfors 2000) or any
other form of analysis estimating extinction
probability
a
Extent of Occurrence (EOO) is the geographical range, defined as the area contained within the
shortest continuous imaginary boundary that can be drawn to encompass all the known,
inferred, or projected sites of present occurrence of a taxon.
b
Area of Occupancy (AOO) is defined as the area, calculated by summing up all grid squares with
the mesh size of 2 km 2 km that are actually occupied by a taxon, excluding cases of vagrancy.
experts; (b) they carry international weight, so that any red list using these
criteria is much more powerful than a list using alternative criteria; and
(c) they have a clear, repeatable methodology, applicable in a wide range of
circumstances and geographical areas. The IUCN red listing system can be
used at different geographic scales. In September 2003, the Species Survival
Commission published the Guidelines for Application of IUCN Red List Criteria at
Regional Levels (IUCN 2003).
Five quantitative criteria are estimated to determine whether a taxon is
threatened or not (Table 12.1) and, if so, to which of the seven threat categories
it belongs to (Fig. 12.1, Box 12.1).
Application of the IUCN 2001 red listing system to bryophytes
Although the IUCN criteria are mainly adapted to animals, Hallingbäck
et al. (1998) showed how they could be used for bryophytes according to a
protocol that has now been adopted officially by IUCN. Assigning bryophytes
to a threat category is often associated with four main difficulties regarding the
definition of an individual and of the generation length, the assessment of a
fragmented distribution (see Section 12.3.2), and by the absence of proper
distribution data (Hallingbäck 2007).
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Box 12.1 The IUCN categories in brief
Extinct (EX): A taxon is Extinct when there is no reasonable doubt that the
last individual has died. For bryophytes, a species is considered EX or RE
when it has not been seen for the past 50 years throughout its entire
distribution range (EX) or in part of it, in which case the taxon can be
included in the ‘‘Regionally Extinct’’ category (RE). Alternatively, the taxon
must be confined to sites that have been thoroughly surveyed without
success in recent years, or where suitable habitat has disappeared. Example:
Neomacounia nitida (Lindb.) Irelanda
Critically Endangered (CR) corresponds to a 50% risk of extinction in
10 years or 3 generations. For bryophytes, the criterion based on the
distribution area (AOO) is most easy to use. The taxon must be known from a
single or several severely fragmented locationsb covering altogether
<10 km2 and experience a continuing decline. Decline in habitat size or
quality is most often used as a surrogate for actual population decline in the
lack of actual data on population trends. Example: Thamnobryum angustifolium
(Holt) Crundw.a
Endangered (EN) corresponds to a risk of extinction 20% in 20 years or 5
generations. The AOO must be <500 km2. In addition, the taxon must be
known from 5 locationsa (or >5 if these are severely fragmented; see IUCN
2001) and also have experienced a continuing decline. Example:
Caudalejeunea grolleana Gradst.a
Vulnerable (VU) corresponds to a risk of extinction 10% in 100 years.
The AOO must be <2000 km2. In addition, the taxon must be known from
10 locationsa (>10 if these are severely fragmented; see IUCN 2001) and
have experienced a continuing decline. Example: Hypnodontopsis apiculata
Z. Iwats. and Nog.a
Data Deficient (DD) is applied to taxa with insufficient data to categorize
them, but which are thought likely to qualify as Extinct, Critically
Endangered, Endangered or Vulnerable when they are better known.
Near Threatened (NT): A taxon is NT when it is close to qualifying for VU.
Least Concern (LC) is applied to taxa that do not qualify (and are not close
to qualifying) as threatened or near threatened.
a
b
See www.artdata.slu.se/guest/SSCBryo/WorldBryo.htm.
The term ‘‘location’’ defines a geographically or ecologically distinct
area in which a single threatening event can rapidly affect all
individuals of the taxon present (IUCN 2001).
12 Conservation biology of bryophytes
Fig. 12.1. Structure of the IUCN threat categories. See text and Box 12.1 for details.
(a) The concept of individual. The IUCN system defines an individual,
hereafter termed IUCN-individual, as a distinguishable entity that is
able to survive and reproduce. Although this definition is theoretically
and biologically sound, practical application of this principle is
impossible. One of its major drawbacks is that many bryophytes are
mostly clonal, with a broad array of ramet and genet sizes, plus different
survival and reproductive strategies (see Chapters 10 and 11, this
volume). What is the entity that best corresponds to discrete
individuals like animals? For most bryophyte species, no specific
information about the number of ramets is available, which means
that standardized templates have to be used to make population
estimates. For practical reasons, a purely pragmatic definition is
therefore used in the red list assessment process. For species that
depend on discrete substrate entities (such as tree trunks or
droppings), each substrate entity can be considered to contain one
or two IUCN-individuals. For bryophyte species growing on ground or
rocks, one IUCN-individual may be assumed to occupy a surface of 1 m2.
However, in the cases of some very small mosses (e.g. the genera Seligeria
and Tetrodontium), one individual should be associated with a surface of
0.1 m2.
(b) Generation length. IUCN has a definition of generation length, which
reflects the turnover (reproductive rate) of individuals/ramets in the
population. According to IUCN criteria, the population development
of a species should be assessed over a time period equivalent to one up
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A. Vanderpoorten and T. Hallingbäck
to three generations or at least ten years depending on what
subcriterion is applied. It is very difficult to apply the ‘‘generation
length’’ criterion to bryophytes. In theory, a species without sexual
reproduction might have a generation length equal to that of its
existence. For bryophytes, it is probably more relevant to estimate the
lowest normal generation length, i.e. the time normally required for a
diaspore or fragment to reach the state at which it produces new
offspring. We believe that a pragmatic approach should be applied,
using templates of 10, 25, 50 and 100-year periods for the time
windows. These stereotyped definitions may not reflect the true
picture but should be preferred to generalization and application of a
default 10-year time window to all bryophytes. We recommend
estimating these templates by means of a life history classification
(During 1992, Söderström 2002, Söderström & During 2005). The main
reason for using life history classification as a template for generation
length is that the different strategy classes typically have different
reproduction strategies; early (quick) vs. late (delayed) reproduction.
These strategies reflect natural turnover rates. Generally, species that
reproduce only after many years of growth exhibit the longest
generation length, and substantial evidence indicates that individual
mats or cushions may be very long-lived. A cushion may last for as long
as it takes for the substratum to decay, and the life span of a terricolous
moss bolster can be counted in decades and perhaps even centuries. For
instance, Bates (1989) estimated from growth rates the age of large
cushions of the terrestrial forest moss Leucobryum glaucum at about
85 years, and colonies of the strictly epiphytic moss Neckera pennata may
last as long as 50 years (Wiklund & Rydin 2004b). There is, however, an
enormous difference between the potential lifespan, achieved by very
few individuals, and the actual average generation length. Therefore, a
generation length of 50 years can be attributed to species with a longlived shuttle strategy and to stayers, i.e. species such as Leucobryum
glaucum, which often grow on stable ground or on rock. By contrast,
typical colonist species, e.g. Ceratodon purpureus, exhibit a much shorter
time span of less than 10 years. In the case of so-called short-lived shuttle
species (During 1992), a group that includes most epiphytes, a period of
25 years may be used as equivalent to three generations.
(c) Absence of proper past and present distribution data. Species’ extent of
occurrence (EOO) is relatively accurately assessed on the basis of
mapping schemes at the 2 km 2 km level of resolution (IUCN 2001)
and ecological niche modeling methods (see Section 12.4.2). Because
12 Conservation biology of bryophytes
frequency estimates are most often biased, owing to the existence of, for
example, under-recorded areas and easily overlooked taxa (Urmi &
Schnyder 2000), it can be useful to include an estimated level of
uncertainty in the assessments. An uncertainty value of 3, for
instance, means that we estimate that only 1/3 of the true number of
individuals or localities is known. Similarly, trends in frequency are
fairly easy to assess when historical data from systematic surveys of
species distributions are available (e.g. Bates 1995a). This is, however,
rarely the case, and herbarium-based methods have been proposed
to estimate, with a degree of uncertainty, past species distribution
frequencies (Hedenäs et al. 2002, Zechmeister et al. 2007). However,
detailed past and current distribution data are mostly only available in
some European countries with a long tradition of floristic mapping. The
limited information on species distribution and trends in countries
where taxonomic information and floras are scarce, or even lacking,
renders the implementation of the IUCN system difficult.
12.2.2
Level of threat in the bryophyte floras
At a worldwide scale, only 80 species (36 mosses, 43 liverworts and one
hornwort) are included in the IUCN World Red List of Bryophytes (www.iucnredlist.org/
or http://www.artdata.slu.se/guest/SSCBryo/WorldBryo.htm) on the basis of their
global threat level, occurrence in threatened habitats, and narrow distribution
range. This list is not yet comprehensive and the ‘‘narrow endemic’’ condition
precludes the inclusion of truly rare but widespread species with transoceanic
distributions, which is quite a common pattern among bryophytes (Shaw 2001).
In fact, despite a tendency for occupying wide distribution ranges, the vast
majority of bryophyte species are sparsely distributed, within a given area or
globally (Cleavitt 2005). Species frequency distributions are typically highly
skewed at a given geographic scale, with rare – and potentially threatened –
species representing the bulk of the flora (Longton & Hedderson 2000).
Table 12.2 shows the levels of threat at the national and regional scale in
different countries. Although this exercise is mostly focused on Europe owing
to the limited availability of precise data on species distributions and threat
levels on other continents, it nevertheless shows that rates of extinction in most
countries are already 2%–4% and that a substantial proportion of the flora is
threatened in the short term.
12.2.3
Implementation of threat levels in legislation
In view of the vulnerability of bryophytes, a logical step beyond the
recognition of highly threatened taxa is the implementation of threat levels into
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Table 12.2 Level of threat in the bryophyte flora of selected countries and areas
Mosses
Area or
country
Liverworts
% threatened Rates of
% threatened
Rates of
extinction (%)a speciesb
extinction (%)a speciesb
Czech
Republic
3.1
22.1
2.8
Estonia
Finland
Iberian
2.2
3.1
2.6
1.3
14.0
9.9
35.0
Kucera & Vana
2005
0.0
4.2
Ingerpuu 1998
3.7
0.0
20.5
11.7
Ulvinen et al. 2002
Sérgio et al.
13.0
Iwatsuki et al. 2000
1994
Peninsula
Japan
Luxembourg
New Zealand
Reference
—
0.2
0.0
9.0
—
34.5
5.3
5.3
0.0
36.1
8.6
Werner 2003
Glenny & Fife
—
—
14.8
—
—
0.8
9.9
15.5
Flatberg et al. 2006
Klama 2006
Rio de Janeiro —
12.1
—
19.2
Da Costa et al.
0.0
81.0
Sabovljevic et al.
2003
2005
Norway
Poland
state (Brazil)
Serbia and
Montenegro
2005
0.5
51.0
Slovakia
2.6
33.5
3.6
36.6
Sweden
1.9
9.3
1.2
9.3
Switzerland
1.4
34.0
1.2
47.2
Schnyder et al.
2004
The
3.0
29.0
2.0
31
Siebel et al.
Netherlands
U.K.
2.3
13.2
0.3
11.0
2006
Church et al. 2001
a
RE sensu IUCN.
b
Sensu IUCN (see Box 12.1).
Kubinská et al. 2001
Gärdenfors 2005
the legislation. Although the level of legal protection remains very low, bryophyte species have increasingly been included in legal texts regulating the
collection of selected species [e.g. the Swiss Nature and landscape protection
decree, appendix 2 (www.admin.ch/ch/f/rs/451_1/index.html); the Canadian
Species at Risk Act (McIntosh & Miles 2005); the European Annex V of the
Habitats Directive (http://ec.europa.eu/environment/nature/nature_conservation/
eu_nature_legislation/habitats_directive/index_en.htm); and Schedule 8 of the
British Wildlife and Countryside Act 1981 (www.jncc.gov.uk/)]. In the European
Union, for example, the habitat of 32 more or less threatened bryophyte
species are protected under Annex II of the Habitats Directive, which has
already led to the protection of more than 1000 localities included in the
Natura 2000 network (Hallingbäck 2003). In the U.K. similarly, bryophytes may
12 Conservation biology of bryophytes
be included within a Site of Special Scientific Interest (SSSI), and guidelines have
been produced to aid the selection of SSSI on the basis of the sum of species threat
levels, as defined in the British Red Data Book (www.jncc.gov.uk/).
12.3
Why are bryophytes threatened?
12.3.1
What biological properties make bryophytes vulnerable?
As Cleavitt (2005) summarizes, rarity – and vulnerability – are linked to
a series of intrinsic properties of bryophytes regarding dispersal ability, genetic
potential, habitat tolerances, competitive ability, reproduction and establishment, and survival rates, whose significance for conservation are briefly
reviewed below.
Dispersal
Low dispersal ability of rare species is a fundamental assumption in the
metapopulation theory framework (Cleavitt 2005, see also Chapter 10, this
volume). Demographic processes are especially crucial in fugitive species such
as epiphytes, for which substrate availability lasts for a limited amount of time.
Thus, epiphytes are critically dependent on their ability to disperse to new
patches, and metapopulation models predict that habitat density is the crucial
factor for their persistence (Hazell et al. 1998).
The dispersal ability of bryophytes has long been debated (see Shaw 2001 for
a review). Several pieces of evidence from spore durability experiments (Van
Zanten 1978, Van Zanten & Gradstein 1988), intercontinental transport of
spores on airplane wings via jetstreams (Van Zanten & Gradstein 1988), correlative analyses between species distributions and air currents (Muñoz et al.
2004), interpretation of species distributions in a phylogenetic context (e.g.
Shaw et al. 2003, Heinrichs et al. 2005, Hartmann et al. 2006), and genetic
inferences of dispersal (McDaniel & Shaw 2005), all point to an overall good
ability of bryophytes for long-distance dispersal. The capacity of bryophytes to
successfully and routinely disperse at the landscape scale, which is a crucial
feature for the successful long-term persistence of the populations, is, however,
poorly documented. Observations on the colonization of artificial habitats by
species far from their nearest natural distribution area (Bates 1995a,
Vanderpoorten & Engels 2003, Miller & McDaniel 2004) suggest that some
bryophytes may be capable of routine dispersal over distances of at least
5 km. However, some studies demonstrated a significant tendency for spatial
aggregation in epiphytes (Snäll et al. 2003, 2004b, 2005, Löbel et al. 2006; but
see Hazell et al. 1998 and Hedenäs et al. 2003). A significant degree of kinship,
derived from a genetic analysis of spatial structure, was furthermore found
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A. Vanderpoorten and T. Hallingbäck
among individuals up to 350 m apart. This further supports the idea that at
least some species have a restricted dispersal range (Snäll et al. 2004a). Limited
dispersal ability has been evoked to explain the rarity of dioicous, rarely fertile
species across a landscape apparently composed of favorable habitats
(Vanderpoorten et al. 2006). The successful transplantation of rare species
into potential habitats further demonstrates that many taxa are not limited
by the availability of suitable habitats but rather by their poor ability to
colonize them (Kooijman et al. 1994, Gunnarsson & Söderström 2007). The
reasons for the limited dispersal ability of such species remain, however,
poorly understood. For instance, sporophyte production is not lower in rare
monoicous mosses and liverworts than in common ones (Longton & Hedderson
2000, Laaka-Lindberg et al. 2000); rare species often produce asexual gemmae in
abundance; and the tolerance to dessication of gemmae is equivalent or even
higher in rare than in common species (Cleavitt 2002).
Ecological range
Rare species tend to occupy narrower ecological niches than common
ones (Cleavitt 2005). A typical example is the widespread but discrete occurrence of copper mosses on heavily contaminated soils, suggesting that habitat
exclusivity is, in itself, a cause of rarity. However, whereas patterns of habitat
specificity are well documented, the link to experimentally demonstrated physiological tolerances is often lacking (Cleavitt 2005). One of the key factors at
different stages of the bryophyte life cycle is water availability. Water availability is most important at the germination stage. In an experiment on the mosses
Buxbaumia viridis and Neckera pennata, spores had the capacity to germinate at
water potential as low as –2 MPa, a value at which most seeds fail to germinate,
but only if pH was >5 (Wiklund & Rydin 2004a). The interaction between pH and
water potential effects on germination suggests that high moisture facilitates
germination at suboptimal pH and vice versa. Further, pH and water potential
determine the length of the lag phase preceding germination. The number of
days needed for germination to start varied between 2 and 50 days depending on
pH and water availability (Wiklund & Rydin 2004a). This time effect is ecologically important because delayed spore germination increases the risk of dessication or disappearance of spores through wind or predation. Wiklund & Rydin
(2004a) therefore suggested the existence of a general trade-off between the
ability of moss spores to colonize substrates with low moisture-holding capacity
and low pH. This trade-off implies that substrata prone to fast desiccation (such
as bark) can be colonized only if they have a fairly high pH. By contrast, substrata
with a high water-holding capacity, such as wood in late stages of decay, or peat,
can be colonized despite low pH.
12 Conservation biology of bryophytes
At the gametophytic stage, the lack of roots and a thick cuticle renders the
plant water status more or less dependent to the humidity of the environment.
Bryophytes are poikilohydric (Chapter 6, this volume), which means that
they are physiologically active only when water is available. As a result, a
number of bryophytes are desiccation-intolerant. For instance, shade epiphytes,
which are characteristic of the understorey of dense primary forests, are considered to be less desiccation tolerant than sun epiphytes and generalists that
developed a series of putative adaptations, such as papillose cell walls, which
enhance the capillary absorption and speed-up the process of rehydration.
Shade epiphytes are therefore highly sensitive to deforestation (Gradstein
1992a,b, Gradstein et al. 2001, Acebey et al. 2003) and more likely threatened
(Gradstein et al. 2001).
Genetic potential and adaptation
The ability of species to successfully disperse is linked to their reproduction mode. The absence of sexual reproduction, which results in a lack of genetic
recombination, a severely limited genetic variability and a compromised capacity to adapt, may be the most important factor leading to rarity. In dioicous
species, but not in monoicous ones, rarity is significantly associated with
the absence of sporophyte production (Longton & Hedderson 2000, LaakaLindberg et al. 2000). Monoicous species would thus tend to become rare if selffertilization becomes obligate, while dioicous species tend to become rare if
they fail to produce sporophytes owing to limitations in sperm mobility
(Longton & Hedderson 2000). Population genetic studies, however, yielded conflicting results regarding the amount of genetic variation within rare species
(Wyatt 1992, Gunnarsson et al. 2005, Werner et al. 2005). Furthermore, as
Oostermeijer et al. (1995) indicated, there is an overall need to better integrate
genetic and ecological studies with the study of the processes that condition the
viability of the populations; for example, by testing that individuals with a
higher number of heterozygous loci display significantly higher fitnesses (e.g.
spore numbers, viability, more robust offspring, etc.). At present, while the
accumulation of data on the population genetics of bryophytes remains very
slow (see Pharo & Zartman 2007, for review), the integration of genetics into
population ecology is still completely lacking.
Competitive ability
A common assumption is that rare species are restricted to specific
habitat conditions by competition. At high carpet densities, individual shoots
are indeed deprived of light and may become overtopped by larger neighbors
(Frego & Carleton 1995). One solution for species with low competitive skills is
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to escape, either in space by dispersal to a new, uninvaded spot, or in time, by
resting in the diaspore bank until a disturbance event renders their growth
possible again. This is one of the ideas behind the concept of ‘‘life-strategies’’
(During 1992, Söderström & During 2005). However, the interactions among
individuals that shape the spatial structure of the populations can also have
positive effects (Okland & Bakkestuen 2004). At low to moderate shoot densities,
growth is constrained by water availability. Because moderately dense stands
dehydrate less rapidly than loose stands or individual shoots, bryophyte growth
is often positively related to carpet density. Conflicting conclusions on the
significance of interspecific competition in bryophytes have, therefore, been
repeateadly reported (McAlister 1995, Rydin 1997, Zamfir & Goldberg 2000,
Pedersen et al. 2001, Wiklund & Rydin 2004b). The effect of competition seems
complex and dependent on a range of factors, including growth stage and
habitat condition (see Chapter 10, this volume). As underlined by Cleavitt
(2005), further experiments are needed to test the impact of competition on
the survival of threatened species.
12.3.2
What mechanisms cause bryophytes to be threatened?
Direct threats: collecting and harvesting
Scientific collecting
Collecting of specimens for scientific purposes is usually highly selective and
seldom constitutes a real threat to the survival of species. The extinction of
species by a targeted over-collecting has, however, already been documented
(Church et al. 2001). Collecting is especially an issue in the case of unique species
known only from the type or a few localities. Typical examples include the
pleurocarp Donrichardsia macroneuron, a Texan endemic known from a few spring
areas (Wyatt & Stoneburner 1980) and the highly peculiar monotypic peatmoss
Ambuchanania. Ambuchanania is known from two localities including the
type locality, which has not been relocated nor revisited since the original collection. The species, whose abundance is unknown, was therefore placed on the rare
and endangered species list of Tasmania to protect it from overcollecting or,
worse, possible extinction (R. Seppelt, pers. comm.). Scientific collecting of
bryophytes is still essential for a number of reasons, including specimen identification, herbarium collections for taxonomic studies, and, more recently,
constitution of DNA libraries. When it comes to rare species, however, it is
recommended to (i) ensure that the material is not already available in herbarium
or other institutional collections; (ii) place all collected specimens in institutions
where they can be preserved and be made available to other scientists, thus
limiting the need for further collections; (iii) submit copies of reports and
12 Conservation biology of bryophytes
publications in a timely manner to permit-issuing agencies; and (iv) avoid making
public the exact geographical information of the actual localities.
Commercial harvest
The high water-holding capacity of bryophytes makes them a useful potting
medium, particularly favored by orchid growers and for wrapping flowers or
fruit tree rootstock for transportation. At present, although outdoor Sphagnum
nurseries is an interesting option for a new type of professional horticulture
(Rochefort & Lode 2006), all bryophyte harvesting is from natural populations.
Local regulations sometimes exist [for example, the EU Directive 92/43/EEC
(Habitats Directive) in Europe (http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?
uri=CELEX:52001DC0162(02):EN:HTML); the Flora and Fauna Guarantee in
Victoria, Australia) ], but this activity is globally seldom monitored and can result
in considerable ecological damage and decline in bryophyte diversity. Initially
mostly focused on Sphagnum (e.g. Whinam & Buxton 1997), commercial moss
harvesting has been increasing in several countries including the U.S.A., Mexico,
Venezuela, India, and China (Peck & Muir 2001, Leon & Ussher 2005, Muir et al.
2006). Although species richness may exceed preharvest levels because harvested
stands represent new windows of opportunities for establishment, a survey conducted on epiphytes of the Pacific Northwest area indicated that cover on vine
maple shrubs immediately following harvest was reduced by 5% and 16%–20% for
low- (c. 34 kg ha 1) and high-intensity harvest treatments (c. 112 kg ha 1), respectively (Peck & Christy 2006). Differences between the two treatments disappeared
after one or two years (Peck & Christy 2006), but a long-term evaluation of cover and
species richness following simulated commercial moss harvest indicates that cover
regrowth may require 20 years at a rate of 5% per year, and volume recovery even
longer (Peck 2006a). Slow rates of accumulation and the unwanted harvest of nontarget species (e.g. red listed species) provide the incentive to manage and monitor
the harvest in order to ensure sustainability and maintain diversity (Vance &
Kirkland 1997, Peck & Muir 2001). Commercial moss harvest should be managed
on rotations of several decades, and patchy harvest methods should be encouraged
over complete strip harvesting to ensure moss regeneration (Peck 2006a). For
example, forest stands may be leased to commercial moss harvesters according
to a rotating scheme ensuring sufficient recovery between harvest entries, under
the condition that the harvesters adhere to specific guidelines and improve the
control of illegal harvest in the lease area (Peck 2006b, Peck & Christy 2006).
Indirect threats: habitat destruction, degradation, and fragmentation
The distribution and abundance of communities are governed by demographic processes such as immigration, which maintain or increase species
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richness, and local ecological factors such as habitat modification and competitive exclusion, which promote extinction (Ricklefs 1987). Habitat modification,
which includes a range of factors (Table 12.3), affects populations in both the
short term, through local population decrease or extinction, and the long term,
through habitat fragmentation. In a fragmented landscape, small populations
increasingly isolated from each other are prone to edge effects as well as demographic, environmental (i.e. natural catastrophes and anthropogenic accidents
listed in Table 12.3), and genetic stochasticity (Chapter 10, this volume). The
latter, also termed genetic drift, involves the random loss of alleles from small
populations. Genetic drift may have severe long-term demographic consequences for self-incompatible or dioicous species owing to the fixation of a
single allele, gender, or morph, and limited adaptive potential for new environments. In the long term, reduced gene flow among fragmented populations may
also lead to increased inbreeding. Inbreeding, which involves the redistribution
of alleles from heterozygous to homozygous combinations, may lead to the
expression of deleterious recessive mutations and a resulting reduced fitness
(e.g. low germination rates, high mortality, and poor growth and reproductive
ability of the offspring), rendering the long-term persistence of the population
in a fragmented landscape questionable (Oostermeijer et al. 2003).
Fragmentation therefore appears as one of the key issues in biological conservation (Heywood & Iriondo 2003). Bryophytes, and epiphyllous liverworts
in particular, experience accelerated life cycles, high rates of local extinction,
and naturally patchy substrates, and therefore represent ideal models to test
metacommunity-based predictions associated with habitat fragmentation
(Zartman 2003, Pharo & Zartman 2007). Despite this, threat assessments on
the bryophyte floras have mostly focused on habitat disturbance, degradation
and destruction (Table 12.3), whereas a larger overview of the mechanisms of
those factors on the diversity and long-term life expectancy of communities that
have been fragmented in the landscape has only recently been approached
(Pharo et al. 2005).
Fragmented epiphytic bryophyte populations typically follow the island
model, which states that the number of occurrences of a given species is almost
always lower on small than on large remnants surrounded by a treeless matrix
(Moen & Jonsson 2003, Zartman 2003). Two competing hypotheses have been
proposed to explain this pattern.
The maintenance of an equilibrium between extinction and colonization,
which requires an area sufficiently large for the preservation of both inhabited
and potentially inhabitable patches, is one of the central predictions of the
metapopulation theory. Following this scheme, Zartman & Nascimento (2006)
observed that the reductions in mean epiphyll abundance was best predicted by
Table 12.3 Overview of the impact of disturbance-related factors on bryophytes
Factor
Effect
References
Land use
Agriculture
Physical
disturbance
Use of fertilizers
Ploughing and sowing right after crop harvest hamper the development Porley 2001
of winter annuals.
Bryophytes have the ability to utilize a range of compounds from
Brown 1992, Porley 2001, Zechmeister et al. 2003
commercial agricultural fertilizers, but eutrophication and
increased vascular plant competition are detrimental to
acrocarpous mosses and thalloid liverworts of arable lands
with low competitive skills.
Forestry
Short-rotation harvesting and clear-cutting cause sudden exposure
and a drastic decrease in the amount of dead wood and old trees.
Hyvönen et al. 1987, Gradstein et al. 2001, Hannerz &
Haº nell 1997, Boudreault et al. 2000, Cobb et al. 2001,
The resulting disturbance negatively impacts old-growth species
Berg et al. 2002, Newmaster & Bell 2002, Ross-Davis &
diversity and composition and favors the introduction and spread
Frego 2002, Acebey et al. 2003, Drehwald 2005,
of newcomers.
Dynesius & Hylander 2007
Hydrological and wetland alterations
Stream regulation
Enhanced substrate stability causes a decrease in riparian species
overgrown by angiosperm development but genuine aquatics increase
Muotka & Virtanen 1995, Englund et al. 1997,
Vanderpoorten & Klein 1999, Downes et al. 2003
on stable substitution habitats (weirs).
Drainage and water Spring bryophytes (e.g. Philonotis) decline in favor of other groups,
abstraction
Peat extraction
Heino et al. 2005
including Sphagnum.
Excavation for fuel in more than 50 countries (60–70 million tonnes
of oil equivalent in 2000, representing about 10% of energy use in
countries such as Ireland), gardening and horticulture, severely
threaten bog communities.
Hinrichsen 1981, Asplund 1996, Rydin & Jeglum 2006,
Rochefort & Lode 2006
Table 12.3 (cont.)
Factor
Effect
References
Global change and pollution
Nitrogen deposits
Eutrophication and increase in cover of vascular plants result in
substantial decrease in bryophyte biomass and diversity.
Acidification causes a shift in species composition towards
Bergamini & Pauli 2001, Berendse et al. 2001,
Pearce & van der Wal 2002
Kooijman 1992, Twenhöven 1992, Thiébaut et al. 1998
physiologically adapted species and tolerant taxa, including Sphagnum.
Heavy metals and
micro-pollutants
Lethal concentrations in large rivers formerly caused complete
Vanderpoorten 1999
extinctions, but recovery is taking place in the context of global
improvement of water quality.
Global warming
Ongoing northwards expansion of Mediterranean and subtropical
bryophyte species is attributed to global warming in temperate areas.
In the latter, the impact of simulated increased drought and
temperature on local communities seems limited, possibly because
bryophytes are able to withstand repeated desiccation without injury,
resuming normal metabolism within minutes or a few hours of
rehydration, or because sufficient tissue hydration can be attained by
dewfall. In alpine and arctic ecosystems by contrast, simulated
warming caused local decrease in species diversity and the southern
boundary of peatland ecosystems is predicted to experience a shift
780 km northwards in response to a two-fold increase in CO2
concentrations.
Frahm & Klaus 2001, Gignac et al. 1998, Dorrepaal et al.
2003, Bates et al. 2005, Jägerbrand et al. 2006
12 Conservation biology of bryophytes
Ab undance
60
100-ha fragment
continuous
forest
50
40
30
20
10
0
10-ha fragment
1-ha
fragment
0–
20
20–
40
0–
20
20– 40–
40
60
60– 80– >100
80
100
0–
20
20– 40–
40
60
60– 80– >100 >100
80
100
Distance from edg e (m)
Fig. 12.2. Frequency distribution of epiphyll mean number of species per 1 ha plot s.d. in
1–100 ha forest fragments and continuous forest as a function of proximity to forest border at
the Biological Dynamics of Forest Fragments Project in Manaus, Brazil (reproduced from
Zartman & Nascimento 2006, with permission of Elsevier).
changes in patch area independently from the distance to the edge (Fig. 12.2).
Isolation of rather small patches of 1–10 ha from the nearest suitable habitat by
an average distance of 380 m was apparently sufficient for disrupting epiphyll
dispersal. Experimental leaf patches in reserves of >100 ha experienced nearly
double (48%) the colonization probability observed in small reserves (27%),
suggesting that the proximate cause of epiphyll species loss in small fragments
(<10 ha) is reduced colonization (Zartman & Shaw 2006). Altogether, these
observations indicate that dispersal limitation, rather than compromised habitat quality due to edge effects, account for the alteration of the epiphyll community after fragmentation.
An increasing body of literature indeed points to a positive effect of connectivity and emphasizes the effects of dispersal limitation and metapopulation
dynamics on community species richness (Zartman & Shaw 2006, Pharo &
Zartman 2007, Virtanen & Oksanen 2007). This hypothesis is supported by the
fact that bryophytes often exhibit aggregated distribution patterns (Snäll et al.
2003, 2004b, Löbel et al. 2006). For example, epiphytes tend to colonize predominantly trees occurring in the vicinity of occupied trees (Snäll et al. 2005).
A recent genetic analysis further demonstrated that pairs of individuals separated by a distance up to 350 m tend to exhibit more genetic similarity than
503
A. Vanderpoorten and T. Hallingbäck
1000
Hepatic cover (cm2)
504
100
10
Small forested moraine hills
(0.7–1.0 ha)
Large f orested moraine hills
(3.8–5.6 ha)
1
0
20
40
60
80
Distance to edge (m)
100
120
Fig. 12.3. Edge effects on forest bryophytes. Total cover (cm2) of hepatics on fallen logs in
relation to distance to nearest edge (m) in a mosaic of forested moraine hills within a mire
matrix in Sweden. ‘‘Small’’ and ‘‘large’’ islands correspond to 0.7–1.0 and 3.8–5.6 ha forested
hills, respectively (reproduced, with permission, from Moen & Jonsson 2003).
individuals separated by a greater distance, suggesting that isolation by distance
operates at this scale (Snäll et al. 2004a).
As opposed to the restricted dispersal range hypothesis, Moen & Jonsson
(2003) invoked edge effects to account for the highly variable and often low
hepatic cover in small forest patches at a distance of <50 m from the edge,
whereas there was a fairly steady increase in cover on large islands when plots
were located at >50 m from the edge (Fig. 12.3). Similar observations of changes
in species composition in riparian buffer strips were also attributed to an altered
microclimate (Hylander et al. 2002, 2005). Experimental studies in two
Hylocomium species clearly showed that growth increase after three months
was strongly affected by the distance from edge and edge exposure (Hylander
2005). Growth on south-facing edges was indeed substantially slower than on
north-facing edges, but this effect progressively disappeared with distance from
edge, so that no growth difference between north-facing and south-facing edges
was observed from a distance from edge of about 40 m (Fig. 12.4). These observations clearly point to a decrease in habitat quality due to the edge effects.
Moen & Jonsson (2003) therefore suggested that many bryophytes have the
mobility to overcome dispersal problems posed by fragmented landscapes if
an appropriate habitat or substrate is available. Efficient dispersal at the landscape scale was further invoked by Pharo et al. (2004, 2005) to explain the lack of
relationship between fragmentation and commonly occurring, drought-tolerant
species with often small spores (<25 mm), whose mobility may render the species less sensitive to fragmentation than taxa exhibiting difficulties in navigating the ‘‘matrix’’. This interpretation is shared by Hazell et al. (1998), who
12 Conservation biology of bryophytes
North-facing edges
30
South-facing edges
25
Hylocomium splendens
20
15
Growth (mm)
10
5
35
30
Hylocomium umbratum
25
20
15
10
0
20
40
60
80
0
20
Distance from edge (m)
40
60
80
Fig. 12.4. Mean growth of Hylocomium splendens and H. umbratum after three months in relation
to distance from forest clear-cut edges and edge exposure (reproduced, with permission, from
Hylander 2005).
observed that colonization of aspens by epiphytes was not more effective within
clusters of aspen than among solitary trees, as if long-distance dispersal was
effective enough to obliterate the effects of fragmentation.
Although little doubt persists on fragmentation affecting the long-term viability of populations at the landscape scale, even if this impact can be buffered
by the dispersal ability of some species, the nature of its effects remains debated,
and it is likely that the respective importance of demographic and ecological
factors depends on local conditions.
12.4
Conservation strategies
12.4.1
Specificity of bryophyte patterns of diversity
The high levels of threat in the bryophyte floras, exacerbated by
immediate habitat destructions and degradations and longer-term effects of
habitat fragmentation, call for urgent conservation measures. Unfortunately,
most conservation areas have not been located in places that deserve the
highest protection level. It is only recently that attention has been focused on
a systematic conservation planning involving scientific prescriptions based on
biogeographical theory and mapping (Margules & Pressey 2000, Groves et al.
2002). We are still faced with the old problem of where to establish protected
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areas, with an increasing sense of urgency, leading to debates on how to
set priorities and searching for new approaches and tools for diagnosis and
decision-making in conservation and management (Heywood & Iriondo 2003).
In view of the impossibility of truly documenting global biodiversity patterns,
conservation criteria are mostly based on flagship taxa. For bryophytes in particular, conservation is mainly incidental and occurs through preservation of habitat
for other reasons (Cleavitt 2005). How effectively diversity in general, and bryophyte diversity in particular, is currently incorporated in the system, is generally
not known (Andelman & Fagan 2000, Pärtel et al. 2004, Schultze et al. 2004).
A macro-scale analysis of areas containing exceptional figures of angiosperm
and vertebrate species endemism and threat levels resulted in the identification
of 25 hot-spots worldwide (Myers et al. 2000). Because diversity patterns, rates of
endemism, and threat levels do not necessarily coincide (Orme et al. 2005),
bryophyte hot-spots were identified based on the single criterion of species
endemism rate, with a cut-off value arbitrarily set at 15%. Rates of endemism
were obtained from various sources listed in Fig. 12.5. The figure obtained must,
however, be interpreted with extreme caution and will definitely be altered in
the near future (R. Gradstein, personal communication). Indeed, the data reflect
a compromise between two opposite trends. In the absence of monographic
work for many tropical taxa, certain rates of endemism are definitely overestimated because the multiple descriptions of the same species in different
areas call for extensive synomizations. On the other hand, substantial numbers
of species definitely remain to be described, especially from poorly known
tropical areas. This last tendency is, perhaps, the most misleading because
cryptic speciation, i.e. the accumulation of genetic differences among morphologically similar taxa, has been increasingly documented in bryophytes (Shaw
2001) and might well be the rule rather than the exception, in particular in the
very numerous bryophytes species whose distribution range spans several
continents.
The overlap between the bryophyte hot-spots defined on these bases and
those identified by Myers et al. (2000) is only partial (Fig. 12.5). New Zealand, New
Caledonia, the Pacific Islands, and the Malesio-Indonesian part of eastern Asia
exhibit the highest rates of endemism in bryophytes. For example, endemism
rates reach up to 45% in the Hawaiian moss flora and 52% in the liverwort flora of
New Zealand. These areas, although listed by Myers et al. (2000), are not ranked
among the richest hot-spots for vertebrates and angiosperms. Shared hot-spots
between liverworts and vertebrate and angiosperms, but not mosses, include
the northern Andes and Madagascar. The Mediterranean and many tropical
areas, e.g. the Galapagos Islands, the Caribbean Islands, Amazonia, and
Equatorial Africa, are listed among the most important hot-spots for
12 Conservation biology of bryophytes
Fig. 12.5. Worldwide patterns of bryophyte hot-spots of endemism compared to
angiosperm and vertebrate hot-spots (Myers et al. 2000) in the background. Only areas
with endemism rates at the species level 15% are presented, and exact values are
provided for each region. Mosses: M1: Hawaii (Staples et al. 2004); M2: Pacific Northwest
(Schofield 1984); M3: Northern Andes (Gradstein, pers. comm.); M4: La Réunion (Ah-Peng &
Bardat 2005); M5: New Guinea (Koponen 1990); M6: New Caledonia (Streimann 2000); M7: New
Zealand (Glenny & Fife, pers. comm.). Liverworts and hornworts: L1: Samoa (von Konrat &
Hagborg, unpublished data); L2: Patagonia (von Konrat & Hagborg, unpublished data);
L3: St Helena (Wigginton, pers. comm.); L4: southern Africa (Wigginton, pers. comm.);
L5: Madagascar and Mascarene Islands (Wigginton, pers. comm.); L6: Borneo (von Konrat &
Hagborg, unpublished data); L7: Japan (Yamada & Iwatsuki 2006); L8: New Guinea and Bismarck
Islands (Wigginton, pers. comm.); L9: Vanuatu (von Konrat & Hagborg, unpublished data);
L10: New Caledonia (Wigginton, pers. comm.); L11: Tasmania (von Konrat & Hagborg,
unpublished data); L12: New Zealand (Glenny & Fife, pers. comm.).
angiosperms and vertebrates, but do not exhibit spectacular rates of
endemism in mosses nor liverworts. By contrast, several temperate areas,
including Japan, Patagonia, the northern part of the Pacific Northwest
region of the U.S.A. and Canada, and Tasmania, exhibit high rates of endemism in either their moss or liverwort flora, but are not listed as priority
areas for conservation with respect to their vertebrate fauna and angiosperm flora.
Indeed, in contrast with one of the few truly general patterns in biogeography, no significant latitudinal gradient of species diversity is evident in the
bryophyte flora (Shaw et al. 2005). The moss flora of tropical lowland forests is,
for example, notably depauperate (Churchill 1998), possibly because, in the
absence of fog, high air temperature and desiccation inhibit net photosynthesis
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(Gradstein 2006). High levels of bryophyte diversity are found in tropical mountains (Churchill et al. 1995, Gradstein 1995), but the numbers presently available
for mosses do not support the view that tropical mountains are obviously more
species-rich than other regions at higher latitudes (Shaw et al. 2005). In the large
leafy liverwort families Lophoziaceae and Scapaniaceae for example, species
diversity tends to follow a diversity gradient extending away from the equator
(Söderström et al. 2007). Although it is true that the current level of floristic
knowledge in tropical areas is far below that achieved in temperate areas, the
figures would have to change dramatically for a clear trend to emerge (Shaw
et al. 2005).
At the landscape scale, bryophyte species richness tends to be significantly
correlated with that of other taxonomic groups (Sauberer et al. 2004, Schulze
et al. 2004). However, few taxonomic groups/guilds turned out to be good predictors for others (Schulze et al. 2004, Nordén et al. 2007), and many groups of
organisms actually differ in their conservation demands (Heilman-Clausen et al.
2005). For example, Pharo et al. (2000) found that a set of sites that preserved 90%
of vascular plant species captured only 65% of bryophyte species, and that
vascular plant species richness was a poor predictor of bryophyte species diversity. On a local scale indeed, reserves selected for vascular plants can capture
large percentages of bryophytes, but individual sites important for bryophyte
conservation may not be important for vascular plant conservation. According
to our unpublished personal experience, many habitats, such as shaded rock
outcrops, crags, old quarries, waterfalls, etc. often display a very rich bryoflora,
whereas their interest for higher plants is extremely limited. Therefore, bryophyte conservation should deserve special attention in terms of selection of
reserves and management measures.
12.4.2
Circumscription of key areas for bryophyte conservation
The most straightforward approach to circumscribe key areas for bryophyte conservation involves comprehensive field surveys (e.g. Urmi 1992).
However, time and expertise are not always available and sharp differences in
the level of knowledge of species distributions are obvious among areas and
continents, resulting in a general under-documentation of bryophyte distributions (Cleavitt 2005). Even in well-prospected areas, mapping the diversity of
small and often inconspicuous plants, which, like the non-chlorophyllose, subterranean liverwort Cryptothallus mirabilis, can sometimes be extremely difficult
to find (Sergio et al. 2005), indeed remains a very challenging task.
Therefore, predictive models have been increasingly used to facilitate subsequent field investigations in order to document bryophyte diversity patterns at
the landscape scale. Initially launched under the ‘‘mesohabitat’’ concept (Vitt &
12 Conservation biology of bryophytes
Fig. 12.6. Distribution of Riccia sommieri in Portugal: actual range based on herbarium (n ¼ 76,
filled dots) and bibliographic (n ¼ 5, open dots) records and predicted range inferred from an
ecological niche model using environmental variables as predictors (reproduced from Sérgio
et al. 2007, with permission of Elsevier).
Belland 1997), predictive models have developed through the increasing availability of databases and computing facilities that take the complexity of conservation programs into account. Geographical Information Systems (GIS) are one of
the tools that allow the integration and analysis of large amounts of data sets. This
enables an increase in the input data to be used and in the output relationships
that can be established among the data (Draper et al. 2003). Potentially valuable
areas for conservation can be circumscribed by crossing information on predicted
habitat suitability for particular species (Sérgio et al. 2005, Vanderpoorten et al.
2006, Sérgio et al. 2007) (Fig. 12.6), sets of species, or global diversity patterns
(Vanderpoorten & Engels 2003, Vanderpoorten et al. 2005), with information on
the human (i.e., needs and capacities of land managers) and financial resources
that are available for conservation (Draper et al. 2003).
The factors identified by predictive models to determine bryophyte diversity
are multiple and vary from one area to another. For example, the high correspondence between high soil pH and plant diversity in boreal areas (Vitt et al.
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2003, Hylander & Dynesius 2006) does not necessarily hold true outside that
area, as regional evolutionary centers are rather located on acidic soils in the
tropics (Pärtel et al. 2004). A survey of the literature recurrently revealed that
high conservation value tends to be associated with habitat heterogeneity at
different spatial scales, from landscape complexity indices (Moser et al. 2002),
soil conditions and topography at the landscape scale (Bates 1995b, Draper et al.
2003, Vanderpoorten et al. 2005), and habitat structuring element, such as the
presence of rock outcrops and well-decayed logs and stumps (Humphrey et al
2002, Ohlson et al. 1997, Rambo 2001, Pharo et al. 2004, Heilman-Clausen et al.
2005, Löhmus et al. 2007) at the local scale.
12.4.3
Strategies for implementing a network of protected areas
Given the limitations of conservation possibilities, not all the areas
identified for their conservation relevance can be protected, and a restricted
set of potential areas must be hierarchically defined based on conservation
priorities. Pharo et al. (2005) used a cumulative algorithm to approximate a
minimum set of areas that represent all species at least once. The most
species-rich site is added first, and the remaining sites are then reassessed to
find the site that adds the most species. This procedure is repeated until all
species have been added to the set of reserved sites.
Such an approach is efficient to objectively design a network of reserves that
maximizes the capture of the present-day diversity. This procedure misses,
however, a longer view on the conservation of evolutionary processes.
Reductions in habitat availability caused by fragmentation indeed increase
local extinction risk by sharpening edge effects, lowering mean population
size and immigration potential, and, eventually, affecting population viability
and evolutionary potential. For instance, it has been suggested that, in a fragmented territory, small-scale protected areas of usually less than 2 ha, exhibiting a high concentration of endemic, rare or threatened species, can be
established in great numbers to complement larger, more conventional protected areas that are less easy to implement in legal and management terms
(Heywood & Iriondo 2003). Identifying core areas for sensitive organisms and
protecting them in small reserves has, for example, become common practice in
‘‘woodland key habitats’’ in Scandinavia (Hylander 2005). This approach is appropriate if, as suggested by Pharo et al. (2004, 2005), bryophytes have the mobility
to overcome dispersal problems posed by fragmented landscapes. However, substantial size effects on the persistence of species diversity, due either to the
break in the immigration/extinction balance due to disrupted dispersal
(Zartman 2003) or to compromised habitat quality due to an edge effect
(Moen & Jonsson 2003, Hylander et al. 2002, 2005, Hylander 2005), have been
12 Conservation biology of bryophytes
demonstrated. Moen & Jonsson (2003) found that the cover of epiphytic liverworts
on forest islands in a vast mire landscape experienced edge effects of about 50 m,
and therefore proposed that buffer areas of >50 m should be retained in addition
to the area of concern for conservation purposes if negative edge effects should be
avoided. Similarly, Hylander et al. (2002, 2005) observed that the species in most
need of protection (i.e. the red-listed species), were among the ones with strongest
declines in riparian buffer-strips 20 m wide, and hence suggested that increasing
the width of buffer strips at sites with known or potential value should be
considered a better strategy than using many narrow strips. If, as advocated by
Zartman (2003), reduced dispersal among fragmented patches distant of only
380 m, rather than compromised habitat quality, causes patch diversity to
decrease with time, much larger protected patch areas must be designed.
Zartman & Nascimento (2006) recommended that stands of at least 100 ha should
be conserved for the long-term existence of epiphylls in Amazonian rainforests.
Therefore, a sound conservation strategy must be based on both the identification
of key areas and an understanding of the processes that threaten the populations
(i.e. dispersal disruption vs. edge effects) in order to assign the appropriate
number and size of reserved areas in each case.
12.5
Managing bryophyte diversity
12.5.1
Management of protected areas
Biodiversity conservation has traditionally relied on the establishment
and maintenance of a network of protected areas. Once selected, protected areas
must be managed in order to ensure the long-term viability of species or communities that justified their conservation status. The vegetation dynamism and
sometimes rapid species turnover, however, raise such issues as to which state
or stage of the vegetation cycle should be preserved (Heywood & Iriondo 2003).
Therefore, the contradictory goal of conserving a biota that is dynamic and everchanging can only be solved when appropriate temporal and spatial scales are
set. The approach to protected areas has in fact changed considerably during the
past 20 years. The ‘‘fortress’’ concept, which dominated conservation philosophy in earlier decades, has progressively moved towards a much more interventionist approach involving the acceptance of a broad range of options and
techniques (Marrero-Gomez et al. 2003).
The most appropriate actions for recovering declining populations can be
determined by experiments that test the effects of different management
regimes derived from competing hypotheses about critical factors that limit
population growth. Except for Fennoscandia, where cryptogams are often taken
into account in managing plans for the boreal forests, reserves are almost never
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managed for cryptogams. Rather, the landscape is mostly managed in favor of a
suite of species perceived to be the most sensitive (‘‘focal-species’’ approach,
Lambeck 1997). The fundamental assumption is that if restoration efforts are
targeted towards a group of species, the needs of other taxa will also be met.
However, some authors have raised concerns about the conceptual, theoretical,
and practical basis of taxon-based surrogate schemes (Andelman & Fagan 2000,
Lindenmayer et al. 2000, 2002).
For example, most temperate dry grasslands are an anthropogenic, seminatural vegetation type of high biological value that has been threatened
owing to the loss of its agricultural usefulness in the middle of the twentieth
century. Many of them were therefore set aside as nature reserves, which have
to be actively managed to prevent a natural succession to woodland. The conservation of biological diversity in grasslands requires an integrated approach
covering the ecological demands of a multitude of organisms. In practice, however, the emphasis is often placed on the vascular flora. Bryophytes, which
include a number of rare species restricted to that habitat (During 1990), are
seldom considered in conservation and restoration programs, and the extent to
which management practices affect the bryophyte layer are largely unknown.
In calcareous grasslands, cessation of management results in the development of a tall and dense herb and shrub canopy that eventually causes bryophyte diversity to decrease (Van Tooren et al. 1991, During & Van Tooren 2002).
In order to prevent a natural succession to woodland, mowing is often implemented because of its positive effects for orchids. For bryophytes, however,
mowing is not an optimal strategy (Bergamini et al. 2001). Vanderpoorten et al.
(2004b) observed that mown plots were characterized by a dense bryophyte
layer mostly composed of the large Scleropodium purum, one of the rare species
termed as ‘‘competitors’’ among bryophytes (Grime et al. 1990) and likely to
outcompete typical grassland species. Alternatively, because bryophyte richness is inversely related to graminoid abundance (Yates et al. 2000, Klanderud
& Totland 2005, Pharo et al. 2005, Eskelinen & Oksanen 2006), grazing, which
opens the moss and grass layers, is likely to increase species richness, especially
that of gap-detecting colonists (Van Tooren et al. 1990). However, heavy grazing
is detrimental to the bryophyte layer (Eskelinen & Oksanen 2006), so that
intermediate disturbance levels are optimal for maintaining cryptogam diversity in temperate grassy ecosystems (Yates et al. 2000).
12.5.2
Integrated management measures in the context of sustainability
Although the whole concept of sustainable development and conservation outside strictly protected areas has sometimes been questioned (Soulé &
Sanjayan 1998), conservation in selected reserved areas increasingly appears as
12 Conservation biology of bryophytes
a necessary but not sufficient condition of the successful conservation of biodiversity (Huntley 1999). Indeed, not only does the greater part of biodiversity
exist outside any kind of formal protection, but the surroundings of a strictly
protected area may provide complementary habitats to those secured in protected areas themselves (Perfecto & Vandermeer 2002). We shall illustrate this
theory with two examples.
Bryophyte conservation and sustainable forest management
Forest and other wooded lands are by far the best-represented, extensively managed ecosystems worldwide. They display, even in highly managed
environments such as plantations (Andersson & Gradstein 2005), an important
role for conservation that has been recently emphasized and firmly placed on
the political agenda through several agreements promoting the sustainable
management of forest ecosystems and the conservation of their biodiversity
(e.g. the EEC directives 79/409 and 92/43, the Ministerial Conference on the
Protection of Forest in Europe, and the Convention on Biological Diversity,
Decision VI/22).
In forest ecosystems, the importance of ecological continuity and forest age
for species diversity is well recognized and supported by an extensive body of
literature mostly focused on temperate ecosystems (Rose 1992, Frisvoll & Prestø
1997, McCune et al. 2000, Cooper-Ellis 1998). In tropical forests, Holz & Gradstein
(2005) found that, although primary and secondary forests display similar
diversity patterns because harvested areas are rapidly invaded by sun epiphytes
(Hyvönen et al. 1987), the composition of their epiphytic assemblages differs
markedly. One third of primary forest species had not re-established in Costa
Rican secondary forests after 40 years of succession, indicating that a long time
is needed for the re-establishment of microhabitats and re-invasion of species
and communities adapted to differentiated niches (Holz & Gradstein 2005).
Ecological continuity is intimately associated with structural diversity. In
particular, the specific occurrence of a set of ‘‘shade epiphytes’’ in old-growths
or, alternatively, in the oldest stands of managed forests (Frisvoll & Prestø 1997,
Boudreault et al. 2000, McGee & Kimmerer 2002, Ross-Davis & Frego 2002,
Drehwald 2005, Botting & Fredeen 2006), and the significant relationship
observed between epiphyte diversity and tree age or diameter (Fig. 12.7) are
attributed to the fact that large, old trees provide a more complex environment,
especially considering bark structure, chemistry, and moisture conditions
(Hazell et al. 1998). Large, old trees are also available for a longer time for
colonization (Hazell et al. 1998, Snäll et al. 2004b), are a source of logs
(Heilmann-Clausen et al. 2005), and contribute, when windthrown, towards
providing a special habitat for cryptogams that grow on inorganic soil.
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Fig. 12.7. Relationship between epiphytic bryophyte species richness and diameter at breast
height of Eucalyptus obliqua. Encircled dots represent trees for which ages are known
(reproduced from Kantvilas & Jarman 2004, with permission of Elsevier).
Specialist species of this nature colonize the freshly exposed soil, enabling the
occurrence of species that would otherwise be outcompeted at ground level
(Heilmann-Clausen et al. 2005).
Several authors recently pointed out, however, that unmanaged, mesic forest
stands may not necessarily exhibit high diversities and specific communities, at
least in temperate areas where these studies were conducted, and emphasized
that factors of long continuity of woodland cover may not be crucial for maintaining bryophyte diversity (Ohlson et al. 1997, Humphrey et al. 2002, Heylen
et al. 2005). Heylen et al. (2005) found that the dominant tree age of an ecotope
may have on its own a significantly negative effect on total epiphyte diversity
and suggested that young trees have generally more to offer and should be
prominently present on ecotope level. Van der Pluijm (2001) indeed observed
that epiphytic-rich pioneer communities of an alluvial Rhine forest were
replaced by mats of a few dominant species when willows reached an age
of approximately 20 yr. Furthermore, a substantial proportion of epiphytes
found in mid-western Europe favors open, softwood stands rather than mature,
shaded hardwood stands (Hodgetts 1996, Klein & Vanderpoorten 1997,
Vanderpoorten & Engels 2002). In fact, while modern forestry tends to favor
fairly dense stands, ancient forests would have been open in the past owing to
the presence of considerable numbers of large grazing and browsing herbivores
12 Conservation biology of bryophytes
and recurrent fires (Esseen et al. 1992), so that the flora may have adapted to this
partly open environment over a period of perhaps millions of years (Rose 1992).
Hylander (2005) therefore proposed that edge habitats, although unsuitable for
shade epiphytes (see Section 12.3.2), may be, under certain circumstances, more
favorable than interior habitats because of a trade-off between moisture and
light requirements, making edges a species-rich refugium for a specific lightdemanding flora once typical of softwood, pioneer stands (Vanderpoorten et al.
2004a).
As a consequence, the diversity and composition of epiphytic assemblages is
linked to a series of forests of different composition, age, and structure. The
conservation of all the stages of the forest cycle is, however, extremely rarely
achieved. In fact, less than 1% of European forests can be termed as old-growth
and include natural senescent and rejuvenation phases (Norton 1996). Therefore,
the conservation of epiphytic bryophytes must also take place in managed
forests whose conservation value will be enhanced if a few conservationoriented measures can be taken. For instance, retained trees, or clusters of
trees, can form links during forest succession between young and old stands
after final harvest and are beneficial to at least some species considered to be
sensitive to forest operations (Hazell & Gustafsson 1999, Kantvilas & Jarman
2004, Fenton & Frego 2005). This is especially true of well-illuminated, pioneer
trees that often support a rich, specialized epiphytic flora. As these epiphytes
must switch from one host to another fairly frequently as their host will be
invaded by large mats of pleurocarpous assemblages and eventually die, the
conservation of such epiphytes relies on the conservation and dynamics of
regeneration of the phorophytes, through, for example, coppicing (Heylen
et al. 2005).
Bryophyte conservation and sustainable agriculture
Many native plant species have benefitted from agricultural activities
concomitant with forest removal, especially those growing in more open types
of landscapes, which now appear as refuges for plant species typical of once
dominant regional vegetation (Jobin et al. 1996, Boutin & Jobin 1998). Many
annual shuttle bryophyte species with short life cycles indeed rely on regular
soil disturbance (Zechmeister et al. 2002). In Europe for example, hornworts are
largely confined to crop fields (Bisang 1998). As a consequence, the highest
percentages of red list species in many European countries are found in dry
grasslands and places with bare soil such as arable fields (Schnyder et al. 2004),
which include up to 63% of the endangered species at a national scale
(Zechmeister et al. 2002). In tropical areas, cacao plantations with low and
moderate management intensity are also of high conservation relevance
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(Andersson & Gradstein 2005). They indeed serve as an important substitution
habitat and even currently represent the unique known habitat of the rare,
western Ecuadorian endemic liverwort Spruceanthus theobromae (Kautz &
Gradstein 2001).
With the intensification of land-use, however, the once positive contribution
to biodiversity of landscape diversification has progressively decreased, giving
rise to the intermediate disturbance hypothesis, according to which highest
levels of biodiversity are maintained at intermediate scales of disturbance.
The strong correlation between land use intensity and bryophyte richness
and conservation value is supported by an extensive body of literature (Kautz &
Gradstein 2001, Zechmeister & Moser 2001, Zechmeister et al. 2003, Andersson &
Gradstein 2005). In a study of Austrian agricultural landscapes, Zechmeister et al.
(2003) found that profit margin and variable costs correlated negatively with
plant species richness, and meadows that offered low or no profit margins
showed highest species richness. Zechmeister et al. (2003) and Schmitzberger
et al. (2005) concluded that, if plant species richness is to be maintained in
agricultural landscapes, farmers have to receive increased financial incentives
through agro-environmental subsidies for appropriate meadow management,
and these have to be linked to clearly defined measures.
12.6
Ex situ conservation and reintroduction
In complement to in situ conservation strategies described above, ex situ
conservation involves the medium- or long-term storage of selected samples of a
population’s genetic diversity intended for the possible reintroduction of rare
and endangered taxa into the wild.
Typical ex situ techniques involve the creation of living collections or diapaused
material such as seeds, spore banks, or cryopreserved material. Living collections
can be grown in greenhouses or axenic cultures. For example, Monosolenium
tenerum, the only species of the family Monosoleniaceae (Marchantiales) and
very rare in nature, is viable in greenhouses and widely cultivated as an aquarium
plant in Central Europe (Gradstein et al. 2003). Axenic cultures, although artificial,
provide a more uniform and secure method of maintaining plants in a tissue
culture collection without fungal, algal, and bacterial contaminants (Duckett
et al. 2004). However, axenic cultures might not be ideal for long-term conservation purposes. Indeed, the material is continually subcultured and is likely to
become adapted to growing in culture conditions over time. This is particularly
problematic for material retained for conservation purposes where reintroduction is a possible long-term objective. Alternatively, cryopreservation has been
shown to be an effective, convenient, and stable long-term storage technique for
12 Conservation biology of bryophytes
vascular plants. In bryophytes, the first experiments appear promising, although
desiccation-intolerant species did not survive either dehydration or freezing
(Burch 2003). A project for the ex situ conservation of endangered U.K. bryophytes
was launched in August 2000, at the Royal Botanic Gardens, Kew, with the
appointment of a dedicated bryophyte conservation officer. The aim is to provide
long-term basal storage of rare bryophyte material for use in future conservation
programs, and material of 18 endangered species is currently conserved (see
further details at http://rbgweb2.rbge.org.uk/bbs/Learning/exsitu/exsitu.htm).
The reintroduction of populations in areas from where they vanished has
been seldom, but increasingly, documented in bryophytes. Recent experiments
demonstrate the possibility of reintroduction from gametophyte fragments
(Kooijman et al. 1994, Gunnarsson & Söderström 2007, Mälson & Rydin 2007)
or cultured gametophytes (Fig. 12.8) (Rothero et al. 2006).
The success of the reintroduction trial is closely linked to a series of measures
to restore appropriate habitat conditions as in the case, for example, of mined
peat bogs (Rochefort & Lode 2006) and provide an appropriate protective cover.
Protective cover has a positive effect on the regeneration of shoot fragments
(Fig. 12.9) because it provides more humid conditions during summer drought
and prevents the development of micro-organisms such as algae during wet
periods, which transform into a potentially fatal hard crust upon drying (Mälson
& Rydin 2007).
This suggests that the possibility exists to increase the population size and/or
the number of populations by artificial introduction of diaspore. However, the
genetic variation of at least some bryophytes species is geographically highly
structured (Chapter 11, this volume), so that a minimal precaution in any
attempt of reintroduction therefore involves a detailed genetic study of the
source populations and their compatibility with the site to be recolonized.
12.7
Conclusion, issues, and perspectives
Interest in biodiversity and conservation biology is rapidly increasing,
including concern for lower plants. Bryophytes have been successfully introduced into the IUCN system and the legal protection of threatened species, and
their habitat, although still limited, is gaining attention in several countries.
Threats and mechanisms that make bryophytes vulnerable are being increasingly well perceived, even if additional experimental research is still needed to
better understand the causes of species rarity. Finally, increasingly practical
tools are becoming available to design and manage networks of conservation
areas for bryophytes, and promising new methods of ex situ conservation are
being developed.
517
Fig. 12.8. In vitro cultivation and reintroduction into the wild of rare and threatened bryophyte
species: the example of the moss Bryum schleicheri var. latifolium in the U.K. (a) Phytagel culture in
5 cm Petri-dishes. (b) Colony on a muslin bag six months after planting. (c) A well-grown colony
one year after planting (photographs by G. P. Rothero and J. G. Duckett).
12 Conservation biology of bryophytes
Fig. 12.9. Effect of cover treatment for survival of individual shoots during the first year of a
reintroduction experiment of four mosses of rich fens (Scorpidium scorpioides, S. cossonii,
Pseudocalliergon trifarium, and Campylium stellatum) in a Swedish mire complex (redrawn from
Mälson & Rydin 2007).
Future challenges include the necessity to perform long-term studies to
identify the causes of decline of so many species and develop networks between
scientists and land managers to improve the applicability of the results
(Hylander & Jonsson 2007).
The central question ‘‘what to conserve?’’ remains, furthermore, highly
debated. Biodiversity studies typically focus on the species as the unit for
comparison and global analyses often use community and regional endemism
as measures of the biodiversity in an area, which raises two issues. Firstly,
morphospecies polyphyly is the rule rather than the exception (Funk &
Omland 2003). This problem is especially acute in taxa with reduced morphologies such as bryophytes, wherein species circumscriptions have traditionally
relied on a few key characters whose taxonomic significance has been increasingly questioned (Vanderpoorten & Goffinet 2006). Secondly, species are not
equivalent in ‘‘biodiversity value’’ because, besides differences in rarity and
threat levels, they differ in phylogenetic history and current population
processes. Molecular studies have increasingly revealed striking intraspecific
levels of genetic variation that differ from one morphospecies to another. For
example, Shaw & Cox (2005) found that, in Sphagnum, morphologically defined
species are not equivalent with regard to molecular biodiversity because
519
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A. Vanderpoorten and T. Hallingbäck
morphospecies differ by the levels of nucleotide variation that they encompass
and their degree of phylogenetic separation from closely related species. In
extreme cases, genetic differentiation extends beyond the morphospecies
level to give ‘‘cryptic’’ species (see Shaw 2001 for a review). This raises the
question of whether conserving races or cryptic species within genetically
variable but morphologically uniform taxa might not be at least as valuable as
conserving some rare but uniform species that are closely related to common
ones (Longton & Hedderson 2000).
Recognition that units assigned the rank of species are often non-equivalent
has led to alternative metrics, such as phylogenetic diversity, for quantifying
levels of biodiversity (Faith 1992, Krajewski 1994, Barker 2002, Diniz 2004).
Bisang & Hedenäs (2000) advocated the use of a phylogenetic approach for
standardizing the choice of taxa that are separated by the highest number of
character state transitions. Both existing species and the process of speciation
should, however, be preserved (Longton & Hedderson 2000), and one could
argue that this method maximizes the capture of ancient diversification processes (represented as long branches on a phylogenetic tree) that led to extant
species rather than actual speciation processes (represented by radiative short
branches). It is also clear that we are in urgent need of an appropriate definition
and circumscription of the species. The ease with which this new species concept, largely influenced by the understanding of evolutionary processes, will be
compatible with our traditional knowledge of plant taxonomy, distribution, and
frequency patterns, which currently make up the bulk of the information
available for conservation, remains, however, largely unknown.
Acknowledgments
The authors sincerely thank Rob Gradstein, Tord Snäll, Bernard
Goffinet, and Emma Pharo for their very constructive comments on an earlier
draft of the manuscript, and Allan Fife, Lars Söderström, Brian O’Shea, Martin
Wigginton, Matt von Konrad, Benito Tan, Henk Siebel, and David Glenny for
their invaluable help regarding patterns of endemism and threats.
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bryophytes in Austrian agricultural landscapes. Biological Conservation, 103,
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Applied Vegetation Science, 10, 111–20.
533
Index
Entries in bold refer to figures
Acromastigum 44
allele replacement 219, 221
Acroporium 122
Allionellopsis 122
Abietinella 117
Acroschisma 86, 100
Allisonia 5, 21, 38
Abietinella abietina 398
Acroschisma wilsonii 86
Allisonia cockaynei –
abscisic acid (ABA) 260, 274,
Acroscyphella 46
3/2 self-thinning rule 405
275, 276, 279
acrotelm 357, 361, 363, 371,
gametophyte 12
Allisoniaceae 20, 38
Allisoniella 45
abscisic acid – Responsive
373, 374, 381
Elements (ABREs) 279
Actinodontium 115
allopatric speciation 463
Ac/Ds transposition 211
Actinothuidium 116
allopolyploid 451, 464
Acanthocoleus 41
active transport 301
allopolyploidy 446, 470
Acantholejeunea 41
Adelanthaceae 45
Alobiella 45
Acanthorrhynchium 122
Adelanthus 45
Alobiellopsis 45
Acaulon 107
Adelothecium 114
Aloinella 107
Acer platanoides 416, 418, 431
adenosine kinase 457
Aloinia 107
Achrophyllum 114
adk 457
Alophozia 101
acid phosphatase 321
Aerobryidium 119
Alsia 125
acidic peatlands 363, 369, 376
Aerobryopsis 119
aluminum (Al) 308, 324, 336,
Acidodontium 110
Aerobryum 118
Acritodon 119
Aerolindigia 118
Amazoopsis 44
Acrobolbaceae 46
AFLPs see Amplified Fragment
Amblyodon 109
Acrobolbus 46
Length Polymorphism
337, 338
Amblyolejeunea 41
acrocarpous mosses 394
Agrostis curtisii 426
Amblystegiaceae 116
Acrochila 45
Aitchisoniella 25, 36
Amblystegium 116, 452
Acrocladium 125
a-cellulose 372
Amblytropis 115
Acrolejeunea 41
Aligrimmia 104
Ambuchanania 73, 100, 498
Acrolophozia 47
alkaline peatlands 364
Ambuchananiaceae 100
535
536
Index
Ambuchananiales 100
Aneuraceae 21, 30, 40
Antitrichia 68, 123
ammonia (NH3) 308, 320
anhydrobiosis 225, 228
Antitrichia curtipendula 242, 418
ammonium (NH4þ) 301, 311,
Anisotachis 46
Aongstroemia 106
Anisothecium 106
Aongstroemiopsis 106
Amphicephalozia 45
annual shuttle 327, 515
Aphanolejeunea 41
Amphidium 106
Anoectangium 107
Aphanorhegma 103
Amphijubula 41
Anomacaulis 45
Aphanotropis 41
Amphilejeunea 42
Anomobryum 110
apical cell (see also under
Amphilophocolea 44
Anomobryum filiforme 247
liverwort, moss, and
Amplified Fragment Length
Anomoclada 45
hornwort) 1, 11, 177, 237,
321, 333
Polymorphism 456
Anomodon 126, 239
239, 247
Anacamptodon 116
Anomodon rostratus 425
Aplodon 109
Anacolia 110
Anomodon viticulosus 242,
Apomarsupella 47
Anacolia menziesii 452
255, 256
Apometzgeria 40
Anacolia webbii 452
desiccation 259
apophysis 335
Anastrepta 45
photosynthesis 255
apoplast water 241, 243
Anastrophyllum 45, 400
Anomodontaceae 125
Apotomanthus 45
Anastrophyllum hellerianum 332,
Anomomarsupella 47
Apotreubia 34
Anoplolejeunea 41
Aptychella 122
Anthelia 47
Aptychopsis 122
comparison 176,
Antheliaceae 8, 47
aquaporins 300
177, 178
antheridiophore 24
Arabidopsis 200, 205, 208,
399, 401
ancestor–descendant
Ancistrodes 114
antimony (Sb) 324
Andoa 119
Anthoceros 139, 140, 142, 144,
Andreaea 57, 63, 67, 80, 81,
85, 86, 87, 92, 94, 99,
100, 331
Andreaea alpina 242, 243, 337
Andreaea rothii 248, 256, 337
Andreaeaceae 100
155, 159, 161, 162, 166,
247, 302, 320
209, 211, 213, 217, 227,
230, 276
Arabidopsis thaliana 205,
227, 300
land plant phylogeny 187
Arachniopsis 44
& Nostoc 319
Arbusculohypopterygium 114
Anthoceros agrestis –
pyrenoid 148
archegoniate 154
archegoniophore 24
Anthoceros angustatus 159
Archeochaete 44
Andreaeobryaceae 101
pyrenoglobuli 149
Archeophylla 44
Andreaeobryales 101
pyrenoid 149
Archidiaceae 104
Andreaeales 100
Andreaeobryopsida 61, 97, 101
Anthoceros cavernosus 159
Andreaeobryum 57, 59, 80, 81,
Anthoceros fusiformis 142
Archidium 86, 88, 104
Anthoceros punctatus 142, 159
Archilejeunea 41
85, 86, 87, 99, 101
Archidiales 104
spore 161
Arctoa 106
97, 100
thallus anatomy 150
Arctoscyphus 46
Andrewsianthus 45
Anthoceros tuberculatus 159
Aneura 22, 26, 31, 40
Anthocerotaceae 142, 149
Aneura pinguis 452
Anthocerotales 141, 142
Arnellia 46
apical and slime cell 4
Anthocerotidae 142, 144
Arnelliaceae 46
gametophyte 13
Anthocerotophyta 142
arsenic (As) 324
sporophyte 27
Anthocerotopsida 142, 144
Arthrocormus 107
Andreaeopsida 60, 61, 63, 79,
area for CO2 uptake/projected
leaf area ratio 248
Index
Aschisma 107
Baldwiniella 124
Ascidiota 41
Barbella 119
ascorbate 278
Barbellopsis 119
Asterella 22, 24, 25, 27, 36
Barbilophozia 45
carbon accumulation 381
Asterella tenella –
Barbula 107
chemistry 362
Bardunovia 119
depth 370
carpocephalum 11
bog 358, 360, 360, 361,
363, 371, 376, 378,
379, 426
Astomiopsis 105
Bartramia 110
Athalamia 24, 36
Bartramiaceae 65,
bohemite 308
110, 247
boron (B) 324
atmospheric CO2 383
net primary production 380
atmospheric pollution 238
Bartramiales 110
Boulaya 117
ATP 286, 301
Bartramiopsis 101
boundary layer 245
Atractylocarpus 107
basic 369
Brachelyma 115
Atrichopsis 101
Bazzania 44
Brachiolejeunea 41
Atrichum 101
Bazzania novae-zelandiae –
Brachydontium 104
gametophyte 14
Brachymeniopsis 103
Atrichum androgynum 273,
Bazzania trilobata 242, 243
Brachymenium 110
Atrichum angustatum 398
Beeveria 114
Brachymenium leptophyllum 94
Atrichum undulatum – CO2
Bellibarbula 107
Brachytheciaceae 118, 329
uptake 249
Benitotania 114
Brachytheciastrum 118
Aulacomniaceae 112
Bescherellia 113
Brachythecium 64, 82, 118, 313
Aulacomnium 63, 112, 370
Bestia 125
Brachythecium praelongum 404
Aulacomnium palustre 248, 367,
Betula 329
Brachythecium reflexum 426
Betula pendula 431
Brachythecium rutabulum 250,
277, 279
379, 422, 425
Aulacopilum 105
bioaccumulate 323
Aureolejeunea 41
biolistic transformation 220
Brachythecium starkei 332, 426
Austinia 119
biological glass 276
Bragginsella 46
Austrofossombronia 38
biological species concept
Braithwaitea 112
Austrofossombronia peruviana –
448, 472
313, 314, 316, 332
Braithwaiteaceae 112
biomineralization 307
Braunfelsia 106
bismuth (Bi) 324
Braunia 111
Austrolembidium 44
Bissetia 107, 124
Breidleria 119
Austrolophozia 46
black spruce 379
Breutelia 110
Austrometzgeria 40
Blasia 26, 32, 35, 319
Brevianthaceae 45
cells and oil bodies 8
Austrolejeunea 41
Austrophilibertiella 105
Austroscyphus 46
auxin 72
and Nostoc 319
Blasia pusilla – cells and oil
bodies 8
Brevianthus 45
Bromeliophila 41
Brothera 107
Blasiaceae 8, 20, 35
Brotherella 122
Blasiales 9, 22, 29, 31, 35
Brotherobryum 106
Blasiidae 21, 34
brown moss 362, 363, 364
BAC clone 207
Blepharidophyllaceae 46
Bruchia 105
Balantiopsidaceae 29, 46
Blepharidophyllum 46
Bruchia flexuosa 91
Balantiopsis 46
Blepharolejeunea 41
Bruchiaceae 105
Balantiopsis rosea –
Blepharostoma 18, 44
Bryaceae 58, 67, 84, 109
Blindia 104
Bryales 109
Aytoniaceae 24, 25, 29, 30, 31,
36, 46
gametophyte 14
537
538
Index
Bryanae 99, 108
Bryoxiphiaceae 103
Calycularia radiculosa 5
Bryhnia 118
Bryoxiphiales 103
Calyculariaceae 20, 38
Bryidae 97, 108
Bryoxiphium 65, 69, 103
Calyculariineae 38
Brymela 115
Bryum 64, 80, 110, 333, 336
Calymperaceae 64, 66, 69,
Brymela websteri 59
Bryum argenteum 333, 398
Bryoandersonia 118
Bryum bicolor 327
Calymperastrum 107
Bryobartramia 93, 102
Bryum caespiticium 95
Calymperes 107
Bryobartramiaceae 102
Bryum schleicheri var.
Calypogeia 7, 46, 367, 452, 454,
Bryobeckettia 103
latifolium – culture 518
71, 107
455, 468
Bryobrittonia 103
Bucegia 24, 36
Calypogeia azurea 455, 468
Bryobrothera 114
Buckiella 119
Calypogeia muelleriana 455, 468
Bryoceuthospora 107
Bucklandiella 104
Bryochenea 116
bulk elastic modulus 241, 243
Bryocrumia 119
Buxbaumia 64, 67, 76, 84, 85,
Bryoerythrophyllum 107
Bryohumbertia 107
Bryolawtonia 124
86, 94, 102
Buxbaumia viridis 328, 396,
402, 496
cells and oil bodies 8
Calypogeia sphagnicola 455, 468
Calypogeiaceae 18, 46
Calyptopogon 107
Calyptothecium 123
Calyptrochaeta 82, 114
Bryomanginia 105
Buxbaumiaceae 82, 102
Calyptrocolea 45
Bryonorrisia 126
Buxbaumiales 97, 102
Campanocolea 44
Bryophyta 100
Buxbaumiidae 102
Camptochaete 125
Camptodontium 106
bryophyte – diversity in
vegetation 394
ecological significance of
life history features 395
ecological significance of
cadmium (Cd) 322, 324, 325
Campyliadelphus 116
Caduciella 124
Campylidium 119
Calatholejeunea 42
Campylium 116, 370
calcium (Ca) 301, 302, 304,
Campylium stellatum 364
fen restoration 519
morphological
305, 307, 311, 317, 323,
features 395
324, 333, 337, 338, 340,
Campylophyllopsis 119
361, 375
Campylophyllum 119
ecological significance of
physiological
features 395
life history diversity in
spore bank 403
calcium carbonate (CaCO3)
336, 360
Campylopodiella 107
Campylopodium 106
calcium:sodium (Ca:Na) 340
Campylopus 82, 107, 460
Callicladium 119
Campylopus introflexus 334,
mitochondrial genome 180
Callicostella 115
paraphyly 180
Callicostellopsis 115
sperm 178
Calliergon 116
Campylopus pilifer 452, 460
Calliergonaceae 116
Campylostelium 104
Bryopsida 61, 62, 64, 71, 94,
427, 452, 460
Campylopus paradoxus 334
Calliergonella 119
Canalohypopterygium 62, 74, 114
Bryopteris 17, 41, 447
Calliergonella cuspidata 310,
capillary space 239
Bryopteris diffusa 447
321, 338, 364, 425
capillary water 240
97, 101
Bryopteris filicina 447
Calluna vulgaris 334, 427
Capillolejeunea 42
Bryopteris gaudichaudii 447
Calluna 334
carbon accumulation in
Bryostreimannia 116
Calobryales 34
Bryotestua 106
Calomnion 112
Bryowijkia 111
Calycularia 5, 22, 38
bog 381
carbon concentrating
mechanism 165, 261
Index
carbonates 308, 375
Cephaloziellaceae 28, 45
carboxylic 374
Cephaloziineae 45
Cardotiella 111
Cephaloziopsis 45
infA gene 196
Carex 362
Ceratodon 105
inversion 196
Caribaeohypnum 119
Ceratodon purpureus 200, 225,
inverted repeat 187–8
carotenoid:chlorophyll
ratio 250
333, 334, 336, 341, 492
Ceratolejeunea 42
Genbank accessions
183
inverted repeat a 196
inverted repeat b 196
carpets 361, 367
cesium (Cs) 313
matK gene 196
carpocephalum 24
Ceuthotheca 111
ndh genes 196
Catagoniaceae 120
Chaetocolea 44
odpB gene 196
Catagoniopsis 118
Chaetomitriopsis 121
pet genes 196
Catagonium 113, 120
Chaetomitrium 121
psb genes 196
Catharomnion 62, 114
Chaetophyllopsidaceae 45
pseudogene 182, 197
cation-exchange 304, 305,
Chaetophyllopsis 45
rpl genes 196
305, 306, 307, 312, 312,
Chamaeobryum 102
rpo genes 196
337, 376
Chandonanthus 45
rps genes 196
ability 337, 374
Chara 184
tRNA gene 182, 196
capacity (CEC) 304, 337
Characeae 301, 302
ycf genes 196
complex 318
Charophyaceae 177
ycf3 intron loss 187
chloroplast stabilizing
Catoscopiaceae 109
charophyte 147
Catoscopium 109, 370
Cheilolejeunea 42
Catoscopium nigritum 367
Cheilothela 105
Chondriolejeunea 42
proteins 275
catotelm 357, 373
Chenia 107
Chonecolea 45
Caudalejeunea 42
Chiastocaulon 45
Chonecoleaceae 45
Caudalejeunea grolleana 490
Chileobryon 126
Chorisodontium 106
Cavicularia 21, 26, 35
Chiloscyphus 17, 21
chromium (Cr) 322, 324
cDNA microarray 288
Chiloscyphus polyanthos 338
Chrysoblastella 105
cell electrophysiology 300
Chinostomum 122
Chrysocladium 119
cell wall and water movement
Chionoloma 107
Chryso-hypnum 119
chloramphenicol 257
Cinclidium 110
241, 243
cell water potential 240
Chloranthelia 44
Cinclidotus 93, 107, 452
cellular protection
chloride (Cl) 302
Cirriphyllum 118
chlorophyll a/b ratio 250
citrate 338
chlorophyll fluorescence 248,
Cladastomum 105
processes 274
cellulose 357
central strand of the seta 308
250, 251, 253, 257,
Cephalantholejeunea 42
259, 280
Cephalojonesia 45
Cephalolejeunea 42
chlorophyll: dry weight
ratio 250
Cladina – net primary
production 380
Cladina mitis 377
Cladolejeunea 42
Cephalolobus 45
chloroplast 281, 282, 285, 286
Cladomnion 113
Cephalomitrion 45
chloroplast genome 181
Cladomniopsis 113
Cephalozia 16, 18, 45, 367
atbF gene 197
Cladonia 332, 414
Cephaloziaceae 8, 14, 18, 28,
atpF gene 196
Cladonia uncialis 377
chl genes 196
Cladophascum 105
clpP2 gene 197
Cladopodanthus 107
31, 45
Cephaloziella 15, 45
539
540
Index
Cladopodiella 45
competitive exclusion 419
Crossidium 107
Clandarium 46
complementation 208, 223
Crossomitrium 114
Claopodium 117
complementation group 208
Crossotolejeunea 42
Clasmatocolea 44
complex thalloid (see
Crumia 107
Clasmatodon 118
Marchantiopsida)
Crumuscus 105
Clastobryella 122
Conardia 116
Cryphaea 122
Clastobryophilum 122
conductivity 360
Cryphaeaceae 122
Clastobryopsis 122
conifers 329
Cryphaeophilium 122
Clastobryum 122
connectivity 410, 413
Cryphidium 122
Clavitheca 103
Conocephalaceae 36
cryptic speciation 446, 506
Cleistocarpidium 105
Conocephalum 23, 24, 25, 31,
cryptic species 451, 460, 466
Cleveaceae 24, 25, 36
Climaciaceae 115
Climacium 116, 454
36, 454
Conocephalum conicum 30, 242,
302, 422, 425, 452
Climacium americanum 452
carpocephalum 11
Climacium dendroides 452
photosynthesis 244
Cryptochila 45
Cryptocolea 46
Cryptocoleopsis 46
Cryptodicranum 106
Cryptogonium 123
Climacium kindbergii 452
Conoscyphus 44
Cryptogynolejeunea 42
clonal growth 73
Conostomum 65, 110
Cryptoleptodon 124
cloud forest 329
conservation – cultivation 518
Cryptomitrium 36
Cnestrum 106
cobalt (Co) 305, 324
CO2 diffusion 249
disturbance related
factors 501
Cryptopapillaria 119
Cryptopodium 112
threat levels 494
cryptospore 97
constitutive cellular
Cryptostipula 46
coalescence 449, 450
protection
Cryptothallus 40
Codonoblepharon 111
mechanism 273
Cryptothallus mirabilis 508
CO2 uptake 247, 248, 249
Codriophorus 104
Coelochaete 155, 157
copper (Cu) 305, 322,
324, 341
Ctenidiadelphus 119
Ctenidium 121
Colobodontium 122
copper mosses 341
Ctenidium molluscum 337, 425
Cololejeunea 42
coprophiles 334
Curvicladium 124
colonists 327
cordifolia 322
Curviramea 126
columella 1
Corsinia 24, 25, 27, 36,
Cuspidatula 45
Colura 15, 42
combinatorial
mutagenesis 223
comparative chloroplast
genomics 181–8
455, 466
Corsinia coriandrina 455, 466
Corsiniaceae 25, 36
cuticle (see under liverwort,
moss, and hornwort) 1,
11, 177, 237, 239, 247
Costesia 102
Cyanolophocolea 44
co-transformation 224
Cyathodiaceae 24, 25, 36
homoplasty 186–7, 188
Crassiphyllum 124
Cyathophorum 114
land plant phylogeny
Craterostigma plantagineum 275
Cyathophorum tahitense 66
Cratoneuron 116
Cyathothecium 93, 120
Cratoneuron filicinum 338
cyclization recombination 224
Cratoneuropsis 116
Cyclodictyon 115
Crepidophyllum 119
cyclohexamide 257
Cronisia 24, 25, 36
Cyclolejeunea 42
Crosbya 114
Cygnicollum 103
184–8
retention index 186
comparative genomics
175, 178
comparative genomics –
synteny 182, 189
Index
Cygniella 105
Cylindrocolea 45
Dendroceros tubercularis –
antheridium 154
requirements 258
seed 178, 245
Cynodontium 106
gametophyte 146
Selaginella 178
Cyptodon 122
mucilage cleft 146
vegetative 178
Cyptodontopsis 122
pyrenoid 149
vegetative in hornwort 270
Cyrto-hypnum 117
rhizoid 146
vegetative in liverwort 270
Cyrtolejeunea 42
Dendrocerotaceae 143
Cyrtomnium 110
Dendrocerotales 141, 143, 144
Cyrtopodendron 113
Dendrocerotidae 143, 144
Cyrtopus 113
Dendrocerotoideae 143, 159
Cystolejeunea 42
Dendrocryphaea 122
cytoplasm 277
Dendrocyathophorum 114
bryophytes 271, 272, 273,
Dendro-hypnum 113
276, 277
D1 protein 277
Dendrohypopterygium 114
Dactylolejeunea 42
Dendrohypopterygium arbuscula
Dactylophorella 42
66, 73
vegetative in moss
178, 270
vegetative in
tracheophyte 178
desiccation-tolerant
desiccation-tolerant
plants 276
desiccation-tolerant
Daltonia 82, 114
Dendrolejeunea 42
Daltoniaceae 114
Dendroligotrichum 101
Desmotheca 111
Dawsonia 70, 92, 101, 239
Dendroligotrichum dendroides –
deterministic extinctions 417
Dawsonia laevigata 88
CO2 uptake 249
protoplasm 272
Dialytrichia 107
Dawsonia superba 64
Dendromastigophora 44
Diaphanodon 119
dehydration 269, 271,
Dendropogonella 122
diaspore bank 328
272, 274, 277, 283,
Denotarisia 45
Dichelodontium 113
302, 498
density-dependent
Dichelyma 115
dehydration tolerance
population model 405
Dichodontium 106
270, 289
density-effects 409
Dicladolejeunea 42
dehydrin 276, 280
desert species 273
Dicnemon 106
Delavayella 14, 46
desiccation 270, 271, 272,
Dicranaceae 58, 69, 71,
Delavayellaceae 14, 46
Dendroalsia 122
Dendrobazzania 44
276, 279, 281
desiccation–rehydration
cycles 314
99, 106
Dicranales 84, 91, 104
Dicranella 106
desiccation tolerance 177, 178,
Dicranella palustris 278
145, 147, 149, 150, 157,
225, 228, 238, 243, 252–60,
Dicranidae 90, 97, 103
159, 162, 163, 164, 166
255, 258, 260, 269, 270,
Dicranodontium 107
271, 272, 274, 275, 282,
Dicranolejeunea 42
Dendroceros 139, 140, 143, 144,
apical cell 147
Dendroceros cavernosus – apical
283, 289, 290
Dicranoloma 106, 452
angiosperms 178
Dicranoweisia 106
cDNA library 178
Dicranoweisia cirrata 337
constitutive 275, 280, 282
Dicranum 64, 69, 91, 106, 320
Dendroceros crispus 159
evolution 254
Dicranum flagellare (see also
Dendroceros granulatus – spore
expressed sequence
cell 147
Dendroceros crispatus –
sporophyte epidermis 158
160, 161
Dendroceros japonicus –
archegonium 153
tags 178
Orthodicranum)
332, 421
ferns 178
Dicranum majus 242, 243
rate of drying 260
Dicranum polysetum 399
541
542
Index
Dicranum scoparium 332, 401
Donrichardsia 118
Elharveya 120
Dicranum undulatum 367
Donrichardsia macroneuron 498
Elmeriobryum 120
Didymodon 107
dormancy 402
embryophyte 139, 152,
diffuse mass transfer 237
Douinia 45
diffusion resistance 237
Douinia ovata 247
Dimerodontium 119
Dozya 106, 123
Dimorphocladon 121
Drepanocladus 116, 370
Encalyptaceae 91, 102
Diobelonella 106
Drepanocladus aduncus 364
Encalyptales 97, 99, 102
dioicy 394, 396
Drepanocladus fluitans
endemism 506, 507
157, 177
Encalypta 71, 84, 95,
103, 239
(see also Warnstorfia) 308
endemism and hot spots 507
Diphysciales 97, 102
Drepanocladus unciniatus 332
endogenous mismatch repair
Diphysciidae 102
Drepanolejeunea 42
Diphyscium 64, 77, 80,
Drosera 427
endohydry 239, 406
Diphysciaceae 102
mechanism 223
Drosera rotundifolia 427
endosymbiosis 1
Diplasiolejeunea 42
drought stress 245
Endotrichellopsis 113
Diplocolea 46
drought tolerance 245, 260
Enigmella 46
Diploneuron 115
Drucella 44
Entodon 121
Diplophyllum 45
Drummondia 103
Entodontaceae 121
Disceliaceae 103
Drummondiaceae 103
Entodontella 120
Discelium 103
Dryptodon 104
Entodontopsis 118
discrimination of
Dumortiera 23, 24, 25, 31, 37
entomophiles 335
Dumortiera hirsuta 242
Entosthodon 103
94, 102
photosynthesis
13
Dumortieraceae 37
environmental stresses 307
dispersal 269
dung-moss 335
Eobruchia 105
dissolved organic carbon
Duthiella 119
Eocalypogeia 46
against
C 247
Eoisotachis 46
(DOC) 374
Distichium 65, 105
Distichophyllidium 114
early light-inducible protein
Eoleucodon 123
(ELIPs) 280, 286, 287
Eopleurozia 40
Distichophyllum 114
Eccremidium 105
Eotrichocolea 44
dithiothreitol 257
Echinocolea 42
Ephemeraceae 95
Ditrichaceae 93, 105
Echinodiaceae 125
Ephemeropsis 114
Ditrichopsis 105
Echinodium 125
Ephemerum 99, 107, 328
Ditrichum 105
Echinolejeunea 42
Epipterygium 66, 110
divergence time 2
ecological niche model 509
epixylic 332
Dixonia 124
ectohydry 239, 406
Eremonotus 47
DNA damage 213
Ectropotheciella 120
Eriodon 118
DNA repair 213–17
Ectropotheciopsis 120
Erpodiaceae 105
DNA repair model 215
Ectropothecium 120
Erpodium 105
Dolichomitra 124
edge effect 504, 510
Erythrodontium 121
Dolichomitriopsis 125
on cover 504
Erythrophyllopsis 107
Dolotortula 107
on growth 505
Eucalyptus 329, 333
dominance control 424
dominants 328
Donnellia 122
effective quantum yield
251, 252
elasticity 409
Eucamptodon 106
Eucamptodontopsis 106
Eucladium 107
Index
Eulacophyllum 118
Felipponea 123
founder control 424
Eumyurium 125
fen 358, 360, 371, 425
FPSII 251
Euptychium 113, 447
chemistry 362
Franciella 113
Eurhynchiadelphus 118
depth 370
Fraxinus excelsior 418, 431
Eurhynchiastrum 118
ferrihydrite 308
frequency distribution of
Eurhynchiella 118
Festuca ovina 427
Eurhynchium 68, 118, 452
Fifea 125
frost mounds 378
Eurhynchium crassivervium 452
Fissidens 33, 56, 67, 104
Frullania 11, 17, 41, 329, 330
Eurhynchium praelongum 332
Fissidens cristatus 338
Frullania tamarisci 242, 256
Eurohypnum 120
Fissidens obtusifolius 422, 425
Frullaniaceae 15, 16, 30, 41
Eustichia 105
Fissidentaceae 104
Frullanoides 42
Eustichiaceae 105
Flabellidium 118
fugitive 327
eutrophic 358
flarks 361
Fulfordianthus 42
Evansianthus 44
Fleischerobryum 110
full turgor water content
Evansiolejeunea 42
FLO/LFY gene 230, 457
evaporation 237, 254
Floribundaria 119
Funaria 65, 82, 86, 91, 103
Exodictyon 107
Florschuetziella 111
Funaria hygrometrica 81, 96,
Exormotheca 25, 36, 249
Flowersia 110
Exormotheca holstii 260
Folioceros 139, 142, 144, 157,
Exormothecaceae 36
Exostratum 107
expressed sequence tag (EST)
179, 202, 205, 206, 286
expression profile analysis 284
external capillary water
243, 244
external water 243, 260
159, 161, 166
Folioceros appendiculatus –
placenta 156
spore 160
Folioceros fuciformis 142
species 503
243, 260
200, 204, 260, 279, 302,
308, 327, 333, 341
habit 83
peristome 89
Funariaceae 58, 87, 91, 103
Funariales 97, 99, 103
Funariella 103
placenta 156
Funariidae 97, 102
pyrenoid 148
Fuscocephaloziopsis 45
spore 160
extinction 488
Folioceros incurvus 142
Gackstroemia 41
extreme temperature
Fontinalaceae 115
gallium (Ga) 324
Fontinalis 93, 115, 459, 460
gametangia 273
Fontinalis antipyretica 247, 303,
gametophytic generation 273
tolerance 256
extreme-rich fens 360
308, 322, 452, 460
Gammiella 120
Fabronia 119
Fontinalis chrysophylla 460
Ganguleea 107
Fabronia ciliata –
Fontinalis dalecarlica 339
Garckea 105
Fontinalis gigantea 460
Garovaglia 113, 447
Fontinalis squamosa 460
gas exchange 247, 248, 252,
photosynthesis 253
Fabronia pusilla –
photosynthesis 253
Foreauella 120
253, 257
Fabroniaceae 119
Forsstroemia 125
gemmae 327, 332, 401, 429
Fabronidium 117
fossil 2, 177, 181, 237
gemmae cups 303
facilitated diffusion 300
Fossombronia 5, 6, 16, 18, 19,
gene duplication 179, 182,
Fallaciella 125
23, 29, 31, 38
Fauriella 117
Fossombroniaceae 38
gene function 199, 201
feather mosses – net primary
Fossombroniales 37
gene knock-in 213,
production 380
Fossombroniineae 38
229
218, 225
543
544
Index
gene knock-out 213, 217, 218,
219, 222, 223
glyceraldehyde 3-phosphate
Gymnostomiella 107
dehydrogenase 457
Gymnostomum 107
gene tagging 211
glycine-betaine 245
Gyrothyra 47
gene targeting 201, 208, 212,
Glyphomitrium 106
Gyrothyraceae 47
213, 214, 219, 220, 221,
Glyphotheciopsis 113
Gyroweisia 107
225, 227
Glyphothecium 113
gene targeting – method 218
GO (genome ontology) 287
Habitats Directive 494
generation length 491
Goebeliella 16, 41
Habrodon 120
genet 491
Goebeliellaceae 41
Haesselia 45
genetic drift 500
Goebelobryum 46
Hageniella 120
genetic identity 454
Gollania 120
halophyte 339
genetic linkage map 207
Gongylanthus 46
halophytic ecotypes 339
genetic transformation
Goniobryum 112
Hamatocaulis 116
Goniomitrium 99, 103
Hamatocaulis lapponicus
201, 209
genome alignment 182
Gottschea 43
genome inversion 182,
Gottschelia 46
Hamatocaulis vernicosus 364
364, 367
gpd 457
Hampeella 113
genome ontology 287
Gradsteinia 116
Handeliobryum 124
genomic character 174, 180,
green alga 139
Haplocladium 117
green cells 368
Haplohymenium 126
Greeneothallus 23, 39
Haplolejeunea 42
Grimmia 68, 104, 331, 366
Haplomitriaceae 2, 34
186, 188
181, 188
genomic character
coding 182
Grimmia atrata 341
Haplomitriidae 34
phylogenetic
Grimmia doniana 337
Haplomitriopsida –
significance 188
Grimmia laevigata 273,
genomic character –
genomic characters –
315, 331
matrix 185
Grimmia maritima 339
genotoxic stress 214
Grimmia orbicularis 311
Geocalycaceae 46
Grimmia pulvinata 246, 248,
gametophytes 10
Haplomitriopsida 2, 5, 18, 19,
30, 33
Haplomitrium 6, 7, 9, 12, 15, 16,
18, 19, 29, 30, 31, 32, 34
256, 340
Haplomitrium blumii 31
geogenous bogs 359
Grimmiaceae 104
Haplomitrium gibbsiae –
Geographical Information
Grimmiales 103
Geocalyx 46
Systems (GIS) 509
Grollea 44
Geothallus 35
Grolleaceae 44
Gerhildiella 45
Group 3 LEA proteins 277
Gertrudiella 107
Groutiella 111
gibbsite 308
growth forms and
Gigaspermaceae 73, 99, 102
ecophysiology 246
gametophyte 10
Haplomitrium hookeri – apical
cell 4
gametophyte 10
Haplomitrium mnioides –
gametophyte 10
Haplomitrium subg.
Calobryum 19
Gigaspermales 97, 102
guerrilla 404
Gigaspermum 93
Gymnocolea 45
Giraldiella 120
Gymnocoleopsis 45
Globulinella 107
Gymnomitriaceae 47
hardening 260, 271, 279
glomeromycete 33
Gymnomitrion 47, 331
hardening/dehardening 273
glutathione (GHS) 278
Gymnomitrium obtusum 247
Harpalejeunea 42
Haplomitrium subg.
Haplomitrium 19
Index
Harpanthus 46
Heterophyllium 122
Hattoria 45
Heteroscyphus 44
Hattorianthus 21, 39
Hildebrandtiella 123
antheridium 152–3, 166, 167
Hattoriella 46
Hilpertia 107
apical cell 145, 147, 150,
Hattorioceros 139, 143, 144,
Himantocladium 124
159, 161
Hattorioceros striatisporus –
antheridial number
evolution 165
152, 164
Höfler diagram 239, 240, 240
archegonium 149, 152, 155
holocellulose 372
asexual reproduction 152
spore 160
Holodontium 106
basal meristem 155,
Hattoriolejeunea 42
Holomitriopsis 106
heat shock proteins 277
Holomitrium 106
bicentriole 154
heavy metal cations 305
Homalia 124
callose 152
heavy metal pollutants 303
Homaliadelphus 124
centrosome 147
heavy metals 323
Homaliodendron 124
chloroplast 147, 149, 152,
Hebantia 101
Homalotheciella 118
Hedwigia 95, 111
Homalothecium 118
chromoplast 153
Hedwigia ciliata 68
Homalothecium lutescens 242, 243
cingulum 162
Hedwigiaceae 111
Homalothecium sericeum
classification 140
Hedwigiales 111
308, 337
157, 167
157, 161, 165–6, 167
columella 155, 157, 162
Hedwigidium 111
homeologous targeting 223
desiccation 159, 166
Helicoblepharum 115
homoeotic gene 230
development 145
Helicodontium 118
homoiohydry 245
embryo 155
Helicophyllaceae 111
homologous recombination
endothecium 155
Helicophyllum 70, 111
201, 213–17, 218, 220,
exine 162
Helodiaceae 116
221, 221, 222
extinction 163
Helodium 116
history 207–13
food transport 149
hemicellulose 357, 372
mediate repair 214
foot 149, 155
Hemiragis 115
pathway 216
fossil 139, 163
Henicodium 123
Homomallium 120
gametangium 152, 167
Hennediella 107
Hondaella 120
growth form 145
Hepatostolonophora 44
Hookeria 114
haustorium 155
Herbertaceae 44
Hookeria lucens 242, 243, 308
intine 162
Herbertus 11, 15, 16, 44,
Hookeriaceae 67, 114
involucre 155, 164
Hookeriales 98, 113
lipid 152
452, 461
Herbertus borealis 452
Hookeriopsis 115
microtubule 161, 167
Herbertus juniperoideus 462
Horikawaea 123
monoplastidic meiosis
Herbertus sendtneri 452
Horikawaella 46
herbivore 8
hormogonium-repressing
Herpetineuron 126
Herzogianthaceae 43
factor (HRF) 320
hornwort
147, 161
morphological reduction
164, 166
mucilage 145, 149, 152,
Herzogianthus 16, 43
amphithecium 155
Herzogiara 9, 44
amyloplast 157
mucilage clefts 149
Herzogiella 120
anatomy 145
mycorrhizae 149
Herzogobryum 47
antheridial jacket cell
Nostoc 145, 149, 150,
Heterocladium 120
evolution 165
159, 164, 167
164, 167
545
546
Index
hybridization 446, 456
Hyophiladelphus 107
oil 159
hydrins 284
Hypnaceae 119, 329
perine 162
Hydrocryphaea 124
Hypnales 66, 84, 98, 115
phylogeny 140, 141, 165
hydrogen ions (Hþ) 302, 374
Hypnanae 93, 98, 99, 112
hornwort (cont.)
placenta 156, 157, 167
hydroid 239
Hypnella 115
polar bodies 147
hydrophytic vegetation 358
Hypnobartlettia 116
pseudoelater 159, 162
Hydropogon 122
Hypnobartlettia fontana 452
pyrenoid 147, 164, 165–6
Hydropogonella 122
Hypnodendraceae 113, 447
pyrenoid evolution 165
Hygroamblystegium 116
Hypnodendrales 112
rhizoid 149
Hygrobiella 45
Hypnodendron 113
RUBISCO 147, 165
Hygrodicranum 106
Hypnodontopsis 105
sculptoderm 159
Hygrohypnella 116
Hypnodontopsis apiculata 490
slime papillae 167
Hygrohypnum 116
Hypnodontopsis mexicana 446
sperm cell 154–5, 166–7
Hygrolembidium 44
Hypnum 95, 120
spermatogenesis 153,
Hylocomiaceae 120
Hypnum cupressiforme 318
Hylocomiastrum 121
Hypnum imponens 73
spore aperture 162
Hylocomiopsis 117
Hypnum jutlandicum 334,
spore color 159–62
Hylocomium 121, 401, 408,
166–7
spore germination 162
spore maturation 157
spore ornamentation 159,
163, 164
409, 504
Hylocomium splendens 256,
405, 425
Hypodontiaceae 104
Hypodontium 104
304, 305, 307, 309, 311,
Hypoisotachis 46
314, 315, 316, 318, 320,
Hypopterygiaceae 63,
66, 113
spore shape 159, 164
323, 327, 332, 333, 334,
spore wall 159, 162, 163
377, 396, 399, 400, 401,
Hypopterygium 114
sporogenesis 161, 167
404, 405, 407, 408, 425,
Hypopterygium rosulatum 452
sporogenous tissue 155, 157
426
Hypopterygium tamarisci
sporophyte dehiscence 162
cation exchange 305
sporophyte development
growth 505
155–7
sporopollelin 162
sporopollenin 161
stomata evolution 165
stomata 149, 157, 164
452, 461
life cycle transition 408
incubous leaves 15
metal concentration 324
inducible 280
nutrient concentration 307
Indusiella 104
Hylocomium umbratum –
growth 505
insertional mutagenesis
208, 211
thylakoid 147
Hymenodon 112
internal lawns 378
transfer cell 156
Hymenodontopsis 112
internal transcribed spacer
trilete ridge 162
Hymenoloma 106
tubers 149, 152, 164
Hymenolomopsis 104
ventral cleft 164
Hymenophytaceae 20, 21, 39
Conservation of Nature
zygote 155
Hymenophyton 20, 21, 22,
and Natural Resources
Horridohypnum 120
39, 452
(ITS) 457
International Union for the
(IUCN) 488
HVA1 276
Hymenostyliella 107
IUCN categories 490
hyaline cells 368, 369
Hymenostylium 107
IUCN criteria 489
hyalodermis 368
Hyocomium 120
inter-simple sequence repeats
Hyalolepidozia 44
Hyophila 107
(see also ISSR) 456
Index
Jubula hutchinsiae 242, 243
lanthanum (La) 304, 324
conduction 301
Jubulaceae 30, 41
Late Embryogenesis
intron 180, 182, 187
Jubulineae 25, 41
Abundant protein (LEA)
invermectins 336
Jubulopsis 41
178, 225, 228, 275, 276,
inverse PCR 209, 210
Juncus 362
Invisocaulis 46
Jungermannia 6, 16, 46
latent heat evaporation 245
ion channels 300
Jungermannia caespiticia 22
law of constant final yield
ion uptake 300
Jungermannia exsertifolia 322
Irelandia 120
Jungermannia vulcanicola 326
lawns 361
iron (Fe) 308, 322, 324, 326,
Jungermanniaceae 12, 46
lead (Pb) 305, 308, 322, 324,
intracellular (symplastic)
336, 337, 338
Jungermanniales 13, 20, 43
287, 288
404, 405
325, 372
Ischyrodon 119
Jungermanniidae 2, 5, 6, 9, 12,
Isocladiella 122
18, 19, 20, 22, 26, 31,
leaf-area index (LAI) 246
40, 46
leaves of bryophytes 271
Isodrepanium 124
isolation by distance 504
Isolembidium 44
Jungermanniidae –
gametophyte 14
dating 378
leaves – liverwort 5–6, 9–16
Leiocolea 46
Isopaches 45
Jungermanniineae 46
Leiodontium 120
Isophyllaria 44
Jungermanniopsida 2, 7, 8,
Leiolejeunea 42
isophylly 15
28, 29, 30, 31, 37, 447
Leiomela 110
Isopterygiopsis 120
Juratzkaea 118
Leiomitra 44
Isopterygium 122
Juratzkaeella 118
Leiomitrium 111
Leiomylia 46
Isotachis 26, 46
Isostachis lyellii –
gametophyte 14
Kiaeria 106
Leiomylia (Mylia) anomala 364
Kindbergia 118
Leiosporoceros 139, 140, 142,
Isothecium 125, 452
Kleioweisiopsis 93, 105
ISSRs 456, 458
Km, Vmax 304
Itatiella 101
KNOX gene family 179
ITS 457
Koponenia 116
IUCN 488
Krunodiplophyllum 45
antheridium 154
Iwatsukia 45
Kurzia 44
apical cell 151
Iwatsukiella 120
Kymatocalyx 45
chloroplast 149
Kymatolejeunea 42
gametophyte 146
144, 147, 150, 155, 159,
161, 162, 163, 164, 166
Leiosporoceros dussii –
antheridia 146
Nostoc 151
Jackiella 28, 46
Jackiellaceae 46
Lamellocolea 44
Nostoc canal 146, 151
Jaegerina 123
laminar atmospheric
placenta 156
Jaffueliobryum 104
Jamesoniella 45
Jamesoniellaceae 45
jarosite 308
boundary layer 245
spore 160, 161
laminar boundary layer 237,
spore wall 161
245, 260
land plant 78, 87, 139, 145,
sporophyte 146
sporophyte anatomy
Jensenia 20, 21, 39, 452
147, 166, 175, 177, 178,
156, 158
Jensenia connivens –
179, 180, 181, 200, 229,
stomata 158
gametophyte 12
238, 269
Jonesiobryum 105
evolution 270
Jubula 28, 41
phylogeny 184–8, 186, 187
Leiosporocerotaceae 142
Leiosporocerotales
141, 142
547
548
Index
Lepyrodontopsis 119
Lindigianthus 42
Leratia 82, 111
Liochlaena 46
Lejeunea 16, 42
Lescuraea 117
lipids – in liverwort (see also
Lejeuneaceae 14, 16, 19, 28,
Leskea 117
Leiosporocerotopsida 58,
142, 144
oil bodies) 30
30, 31, 41, 329, 330, 445,
Leskeaceae 117
Liriodendron 313
446, 447
Leskeadelphus 117
liverwort 139, 145, 155
Lembidium 44
Leskeella 117
acrogyny 12, 19, 22
Lembophyllaceae 125
Leskeodon 114
adventive branches 18
Lembophyllum 125
Leskeodontopsis 114
air chambers 23, 24
Lepicolea 26, 44
Lethocolea 46
air pores 23, 24
Lepicoleaceae 44
Leucobryaceae 69, 71, 106
amphigastria 9
lepidocrocite 308
Leucobryum 67, 107, 452
anacrogyny 19, 22
Lepidogyna 41
Leucobryum albidum 406, 425,
androecium 19, 21
Lepidolaena 41
452, 458, 492
antheridiophore 24
Lepidolaenaceae 15, 41
Leucobryum glaucum 458
antheridium 18–19, 21, 24
Lepidolejeunea 42
Leucodon 123, 452
apical cell 3, 22, 23, 32
Lepidopilidium 115
Leucodon sciuroides 311
archegonium 18, 19–20,
Lepidopilum 115
Leucodontaceae 123
Lepidozia 6, 44
Leucolejeunea 42
Lepidozia reptans 332
Leucolepis 110
Lepidoziaceae 8, 13, 18, 44
Leucoloma 106
auxin 28
Leptobarbula 107
Leucomiaceae 114
bract 19, 20, 26
Leptobryum 109
Leucomium 115
bracteoles 19, 20, 26
Leptocladiella 121
Leucoperichaetium 104
branch types 17, 18, 23
Leptocladium 117
Leucophanes 107
branching 16–18, 21
Leptodictyum 116
Levierella 119
calyptra 25, 26
Leptodon 125
life forms and
capsule 29
Leptodontaceae 125
Leptodontiella 107
Leptodontium 108
Leptohymenium 121
ecophysiology 246
life-strategies 327, 396
annual shuttle 327,
398, 403
22, 25
asexual diaspore 20,
22–3, 25
carpocephalum 25
caulocalyx 22, 26
coelocaule 25–6, 28
columella 1
Leptoischyrodon 120
colonist 327, 398, 403
cuticle 1, 11
Leptolejeunea 42
dominant 327
dehiscence 29
Leptophyllopsis 44
fugitive 327, 398
divergence time 2
Leptopterigynandrum 117
long-lived shuttle 398, 403
domatia 34
Leptoscyphopsis 44
medium shuttle 327
elater 29, 30
Leptoscyphus 44
perennial 327, 398, 403
elatophore 30
Leptostomataceae 110
short-lived shuttle 398, 403
embryology 25
Leptostomopsis 110
shuttle 398
endospory 30, 31
Leptostomum 110
lignin 61, 357, 372
endosymbiosis 1
Leptotheca 112
Limbella 116
epigonium 25
Leptotrichella 106
Limprichtia 116
epiphylls 330
Lepyrodon 124
Lindbergia 117
foot 25, 28
Lepyrodontaceae 124
Lindigia 118
fossil 2
Index
gametangia 18–20, 24–5
sporangium 28
gametangiophore 11
spore 31
geocauly 26
spore germination 31–2
Lyellia 101
germ tube 32
spore:elater ratio 30
Lyophyllum palustre 321
lycophyte – chloroplast
genome 180
gynoecium 19, 22, 26
sporocyte 30, 31
haustorium 28
sporogenesis 28, 29
Macgregorella 119
heteroblasty 16
sporophyte 27
Macrocolura 42
homoplasy 32
stem anatomy 16
Macrocoma 111
intercalary branches 18
stem perigynium 26
Macrodictyum 106
involucellum 28
stomata 1
Macrodiplophyllum 46
involucre 11, 22, 26
tapetum 30
Macrohymenium 122
isospory 31
transfer cells 28
Macrolejeunea 42
leaves 5–6, 9–16
trigone 21
Macromitrium 65, 73, 82, 111
marsupium 26, 28
underleaves 9, 15, 18
Macrothamniella 120
merophyte 3, 16, 17
ventral scales 23, 24
Macrothamnium 121
metamer 3
water conduction 11, 13,
Macvicaria 41
module 3, 16, 19, 22
monoplastidic meiosis 31
15, 20, 24
water retention 15, 21
MADS-box gene 179,
229, 230
mucilage 33
Lobatiriccardia 40
mucilage cavities 24
local dynamics 410
307, 311, 314, 317, 324,
mycorrhizae 16, 24
local extinction 410
333, 361
nurse cells 30
local population 410
Mahua 120
nutrient transfer 28
Loeskeobryum 121
Makinoa 5, 38
oil bodies 6–8, 8
Loeskypnum 116
Makinoaceae 20, 38
operculum 29
Loiseaubryum 103
Makinoineae 38
paraphyllia 19
long-distance dispersal 495
malate 338
perianth 20, 22, 26
long-lived shuttle 328
Mamillariella 117
perigynium 25
Lophochaete 44
Mandoniella 118
photosynthesis 1
Lophocolea 6, 44
manganese (Mn) 305, 308,
phylogeny 32–3
Lophocoleaceae 14, 44
polyplastidic meiosis 31
Lophocoleineae 43
Mannia 24, 36
protonema 31–2
Lopholejeunea 42
map-based cloning 208
pseudoperianth 11, 12, 22,
Lophonardia 47
mapping 287
Lophozia 45, 332, 367
Marchantia 24, 25, 31, 32,
25, 26, 27
quadripolar microtubular
system (QMS) 30
Lophoziaceae 45, 508
Lopidium 114
rhizoid 16, 20, 23, 24, 32
Lorentziella 102
seta 26, 28–9
Luisierella 108
sexual dimorphism 21
Lunularia 24, 25, 31,
shoot calyptra 25, 26
36, 452
slime cell 4
Lunularia cruciata 260, 279
slime hairs 19, 20, 21, 22
Lunulariaceae 36
slime papillae 20, 21, 22, 24
Lunulariales 33, 36
spermatid 33
Luteolejeunea 42
magnesium (Mg) 305, 306,
322, 338
36, 454
land plant phylogeny 187
Marchantia polymorpha 242,
248, 302, 303, 341, 452
antheridiophore 11
archegoniophore 11
idioblastic oil cell 8
nuclear genome 189
Marchantiaceae 23, 24, 25, 28,
33, 36
549
550
Index
Marchantiales 9, 36, 248,
252, 261
Megalembidium insulanum –
gametophyte 14
Microbryum 108
Microcampylopus 107
Megalembidium 16, 17
Microctenidium 120
Meiotheciella 122
Microlejeunea 42
Marchantiophyta 7, 22, 30
Meiothecium 101, 122
Micromitrium 108
Marchantiopsida 2, 5, 7, 8, 9,
membranes 277
Micropterygium 44
12, 19, 21, 22, 26, 28, 30,
merophyte 5–6
microsatellite size
31, 32, 34, 152, 239,
mercury (Hg) 322, 324
Marchantiidae 9, 22, 28, 29,
30, 31, 32, 33
243, 447
Marchantiopsida –
gametophyte 11
(HgS) 326
homoplasy 456
Microtheciella 126
Merrilliobryum 119
Microtheciellaceae 126
Mesoceros 139, 143, 161
microtubular cytoskeleton
Marchesinia 42
Mesochaete 112
Marsupella 26, 47, 331
Mesonodon 121
Mielichhoferia 110, 341, 462
Marsupella emarginata 338
Mesoptychia 46
Mielichhoferia elongata 452,
Marsupella marginata – cells
Mesoptychiaceae 46
and oil bodies 8
mesotrophic 359
257, 282
459, 461, 462
Mielichhoferia mielichhoferiana
Marsupidium 46
Mesotus 106
mass effect 428
Metacalypogeia 46
mineral input 317
Mastigolejeunea 42
Metadistichophyllum 114
mineral nutrition 238
Mastigopelma 44
Metahygrobiella 45
mineralization 366
Mastigophora 44
metal concentration 313, 324
minerotrophic 359
Mastigophoraceae 44
metal tolerance 341
mires 358
Mastopoma 122
Metalejeunea 42
Mironia 108
maternal inheritance 77
Metaneckera 124
mitochondria 282
matrotrophy 63, 80
metapopulation 393, 410
Mitrobryum 106
Matteria 111
metapopulation
Mittenia 91, 108
Meesia 109, 370
extinctions 417
452, 459, 462
Mitteniaceae 108
Mittenothamnium 120
Meesiaceae 109
Meteoriaceae 118
Megaceros 139, 140, 143,
Meteoridium 118
Mitthyridium 107, 446, 452
144, 147, 149, 150,
Meteoriella 121
Miyabea 117
155, 157, 159, 161,
Meteoriopsis 119
Mizutania 20, 40
162, 163, 164, 166
Meteorium 119, 254
Mizutaniaceae 40
Metzgeria 23, 40
Mniaceae 66, 68, 110, 239
chloroplast 149
Metzgeria furcata 242, 243
Mniobryoides 110
mucilage cleft 150
Metzgeria leptoneura –
Mniodendron 113
Megaceros aenigmaticus 152
thallus anatomy 150
gametophyte 13
Megaceros cf. vincentianus –
Metzgeriaceae 8, 20, 21,
pyrenoid 148
31, 40
Mnioloma 46
Mniomalia 110
Mnium 69, 110
Megaceros gracilis – spore 160
Metzgeriales 5, 22, 32, 40
Mnium arizonicum 425
Megaceros pellucidus –
Metzgeriidae 2, 5, 9, 20, 22,
Mnium hornum 242, 246, 452
sporophyte
anatomy 158
31, 39
gametophyte 13
Mnium orientale 452
Mnium thomsonii – peristome 90
Megaceros vincentianus 144
Metzgeriopsis 42
moderate-rich fens 360
Megalembidium 44
Micralsopsis 123
Moerckia 5, 21, 22, 39
Index
Moerckiaceae 20, 39
archegonium dehiscence 76
deuter 68
molecular diffusion 246
arthrodontous mosses 92, 99
development 202
Molendoa 108
arthrodontous peristome 88
dextrorse seta 82
molybdenum (Mo) 324
asexual diaspore 95
diaspore 78
Monocarpaceae 36
asexual reproduction 77–8
diaspore abscission 78
Monocarpus 23, 24, 27, 36
autoicy 74, 75
diaspore type 78
Monoclea 9, 20, 21, 25, 26, 31, 37
auxin 203, 206
dioicy 75, 95
Monoclea gottschei – oil cells 11
axillary hair 58, 59, 60, 77
diploidy 95
Monocleaceae 37
basitonous branching 72
diplolepideous alternate
Monodactylopsis 44
branch initial 56, 57, 60,
monoicy 396
71, 73
peristome 91
diplolepideous mosses
Monosoleniaceae 36, 516
brood bodies 63
Monosolenium 9, 21, 24, 36
bud 60, 204
91, 99
Monosolenium tenerum 516
bud initial 203
monosporangiate 157, 163
calyptra 59, 81, 83, 92
Moseniella 109
calyptra removal 81
moss
calyptra shape 81
distichy 65
diversification 98
diplolepideous opposite
peristome 91
diplolepideous peristome
89, 90
aborted spore 88
capsule 59, 79, 84, 94
abortion 79
capsule shape 84
dwarf male 73, 88
abscisic acid (ABA) 206
cauline cortex 58, 61
embryo protection 80–2
acrandry 76
caulonema 94, 203, 203
embryo 79, 80, 81
acrocarpous mosses 99
cell cycle 214
embryogenesis 79, 84
acrocarpy 75
cell shape 200
endospory 94
acrogyny 75
character evolution 98
endostome 90, 90
acrotonous branching 72
chloronema 94, 95, 202,
endothecium 86
alternate peristome 90
amphigastrium 66
amphithecium 86,
203, 220
chloroplast 202, 203, 204,
205, 213
entomophily 84, 86, 93
epibasal cell 79
epigonium 81
chloroplast genome 180
epiphragm 92
anemophily 98
cladocarpy 75
evolution 96–8
anisophylly 65
cleistocarpy 92, 93
exine 87, 93, 202
anisospory 88
clonal reproduction 95
exospory 94
annulus 86
clone 78
exostome 90
antheridium 76, 203, 204
CO2 absorption 69, 70
exostome tooth 59
antheridium dehiscence 77
columella 86, 92
fertilization 204
aperture 87, 93
complanate leaves 65
food-conducting cell 62, 68
apical cell 56, 60, 64, 71, 75,
costa 68–9
food conduction 83, 94
costal lamellae 69
foot 79, 80
apical dominance 72
cryptoporous stomata 85
fossil 96
88, 98
78, 202, 203, 217
apogamy 81, 95–6
cucullate calyptra 82
function of calyptra 81
apophysis 84
cuticle 67, 70, 83, 85
gametangia 204
apospory 95–6
cytokinin 204, 206
gametophyte 57–78, 59, 200
archegonium 75, 79, 81, 96,
decay resistance 93
gametophyte development
203, 204
dehiscence 81, 86, 91, 98, 99
93–5
551
552
Index
moss (cont.)
life strategies 398
phaneroporous stomata 85
gemmae 95
light 204
phyllodioicy 73, 75, 88
gemmae germination 78
lipid 61, 63, 64, 77, 93
phyllotaxy 64
genome 205, 211, 216
meiosis 87, 96, 204
placenta 63, 80
genome size 205, 207
metamer 56, 59, 60, 64,
plasmodesmata 62, 94
germ tube 87, 93, 94, 202
66, 71
plastid 87
guide cell 68
mitrate calyptra 82
pleurocarpous mosses 99
hair points and water loss 246
module 56, 60, 63, 71
pleurocarpy 75
haplolepideous mosses
monoicy 75
polar cell growth 201
monopodial branching
polyphenol 61
91, 99
haplolepideous peristome
89, 90
72, 72
polysaccharide 87
morphogenesis 200
polysety 79
haustorium 64, 80
mucilage 58, 204
polysporangy 84
heteroblasty 65, 75
mucilaginous leaves 59
pore 62
heterophylly 65
neck 84
primary peristomial layer
heterospory 88
nematodontous mosses 92,
hyalocyst (see also hyaline
cell) 58, 70
hyalodermis 58
97, 99
nematodontous
peristome 88
(PPL) 88, 89
primordium 60, 71
prosenchymatous cell
61, 66
hydroid 61, 62, 68, 83, 98
nematogens 57
protein reserve 93
protonema 94, 95, 96, 202,
hydrome 61, 83, 84
nutrient transfer 80
hygrogastique peristome 93
nutrient transport 80
hypobasal cell 79
oil 202
protonemal gemmae 95
hypophysis 84
operculum 59, 84, 85, 86,
pseudoautoicy 75
inner peristomial layer (IPL)
88, 89
intercellular gas space 85
intine 87, 202
92, 98
206, 217, 227, 260
pseudocolumella 93
opposite peristome 90
pseudodioicy 75
outer peristomial layer
pseudoparaphyllia 60
(OPL) 88, 89
pseudopodium 99
IPL asymmetric division 91
pachydermous leaves 68
pseudostomata 85, 92
IPL symmetric division 91
papillae 69, 239, 247
quadripolar microtubule
isospory 88
paraphyllia 58, 60, 239
juvenile leaf 65
paraphysis 74, 77
lamellae 248, 249
parenchymatous cell 61, 66
lamellae and CO2
paroicy 75
reverse evolution 98
parthenogenesis 84
rheophily 69
uptake 249
system 87
residual primary
meristem 79
leaf initial 56, 60, 64, 66, 71
pectin 87
rhizoid 57–8, 94, 204, 239
leaf traces 62
perichaetium 75, 79
rhizoidal gemmae 57
leptoid 62, 83, 94
perine 87, 202
rhizoidal pegs 58
leptoma 87
peristome 88, 89, 98
rhizoidal tuber 57
leucocyst 70, 71
peristome cilia 90, 90, 91
rhizome 73
life cycle 202, 203
peristome segments 90
scaly leaves 60
life cycle stage
peristome trellis 93
self-fertilization 204
peristome types 88
selfing 78
petiole 64
seta 59, 79, 82, 95, 204
transition 408
life form 71
Index
seta anatomy 82
struma 84
Myurium 125
seta meristem 79, 83
subapical meristem 56
Myurium hochstetteri 247
sex expression 96
superclass 99
Myuroclada 118
sexual dimorphism 73,
sympodial branching 72, 73
synoicy 75, 96
Nanomarsupella 47
sinistrorse seta 82
teniolae 69
Nanomitriella 103
slime papillae 59
tetraploid 96
Nanomitriopsis 108
sperm 204
tmema cell 78
Nanothecium 120
splash cups 77
transfer cells 64
Nardia 26, 46
sporangium 82, 88
trichomes 59
Natura 149, 494
spore 87–8, 203
trilete mark 87
Neckera 124, 402, 416, 453, 454
spore dispersal 82, 91
urn 84, 85
Neckera crispa 242, 243
spore dormancy 205
vaginant laminae 67
Neckera pennata 328, 402, 416,
75, 88
spore germination 93, 202
vaginula 80, 81, 82
spore maturation 93
vegetative diaspore 78
417, 429, 492, 496
population size 416
spore wall 87, 93
water absorption 69, 70
Neckeraceae 63, 124
spore wall development 87
water-conducting cell 62
Neckeropsis 63, 124
sporeling 94, 203
water conduction 57, 58,
NEE 381
sporeling types 94
68, 69, 71, 80, 83
Neesioscyphus 46
sporocyte 87
water retention 71
Nematocladia 119
sporogenesis 87, 96,
xerocastique peristome 93
Neobarbella 125
young leaf 65
Neodicladiella 104, 119
sporogenesis stages 87
young sporophyte 203
Neodolichomitra 121
sporogonium 79
zygote 79, 204
Neogrollea 44
sporophyte 79–93, 204
moss bags 323, 325
Neohattoria 41
sporophyte abortion 78, 257
most recent common
202, 204
sporophyte apical cell 79, 84
ancestor (MRCA) 449
Neohodgsonia 23, 24, 25, 27, 35
Neohodgsoniaceae 35
sporophyte apical growth 79
mRNA knock-down 224
Neohodgsoniales 33, 35
sporophyte
MRN complex 216
Neohypnella 115
Muellerobryum 123
Neolindbergia 123
sporophyte geotropism 81
multigene family 223–5
Neomacounia 124
sporophyte intercalary
Muscoherzogia 106
Neomacounia nitida 490
mutagenesis 200, 209, 211
Neomeesia 109
mutant phenotype 200, 201,
Neonoguchia 119
architecture 82–7
growth 79
sporophyte meristem 79
sporopollenin 87, 93, 202
208, 216, 222–3
Neophoenix 108
starch 61
Mylia 46
Neopotamolejeunea 42
starch reserve 93
Myliaceae 46
Neorutenbergia 115
stem anatomy 58
Myrinia 119
Neosharpiella 110
stereid 61, 68
Myriniaceae 119
Neotrichocolea 15, 43
stolon 73
Myriocolea 42
Neotrichocoleaceae 14, 15, 43
stoma shape 85
Myriocoleopsis 42
Nephelolejeunea 42
stomata 58, 67, 82, 85, 86,
Mytilopsis 44
net photosynthesis 244, 255
Myurella 120
net primary production 380
Myuriaceae 125
Neurolejeunea 42
96, 98
stomata evolution 85
553
554
Index
neutrocline 336
Nothogymnomitrion 47
Oedipodiopsida 101
niches 270
Nothostrepta 45
Oedipodium 68, 86, 94,
nickel (Ni) 305, 322, 323, 324
Notoligotrichum 101
Niphotrichum 104
Notoscyphus 46
oil bodies 6–8
Nipponolejeunea 41
Notothyladaceae 142
oil bodies – Bazzania-type 7
nitrate (NO3−) 301, 310, 314,
Notothyladales 141, 142, 144
oil bodies – Massula-type 7
Notothyladoideae 142, 144
oil droplets 277
Notothylas 139, 140, 142, 144,
Okamuraea 118
317, 333
nitrate reductase 310, 314
97, 101
nitrite (NO2) 308
155, 157, 161, 162, 163,
oleosome 7
nitrogen (see also ammonia/
164, 166
Olgantha 44
ammonium) 307, 311,
Notothylas dissecta 142
Oligotrichum 101
314, 315, 316, 317,
Notothylas javanica 142
oligotrophic 359
319–21, 326, 361,
Notothylas nepalensis 142
ombrogenous bogs 359, 364
365, 399
Notothylas orbicularis 142
Ombronesus 113
nitrogen (15N) 316
antheridium 154
ombrotrophic 359
nitrogen (d15N ratio) 326
spore 161
Omphalanthus 42
nitrogen inputs 319
nitrogen NPK 314
Notothylas temperata 162
spore 161
Oncophorus 106
oomycete 58
nitrogen NPS 302
Notothylatidae 142, 144
opal 308
nitrogen – deposition 365
Nowellia 14, 45
Oreas 106
nitrogen – fixation 317,
Nowellia curvifolia 247
Oreoweisia 106
nutrient accumulation 317
organellar membranes 273
nutrient capture 299
Orontobryum 121
nutrient concentration 307
Orthoamblystegium 117
319, 333
nitrogen – invertebrates and
liverworts 15
nitrogen – mineralization 358
nutrient movement model 309
Orthodicranum 106, 120
Nobregaea 118
nutrient transport (see
Orthodicranum flagellare 74
Noguchiodendron 124
under liverwort and
Orthodontiaceae 112
non-homologous end joining
moss) 238
Orthodontium 112
(NHEJ) 214
non-osmotic water 241
nutrient triangle
experiments 302
Orthodontium lineare 412
Orthodontopsis 112
Orthomnion 110
non-photochemical
quenching (NPQ) 251,
occupancy 410
Orthorrhynchiaceae 124
252, 253, 258, 259, 260
ocelli 11
Orthorrhynchidium 123
Ochiobryum 110
Orthorrhynchium 124
Ochrobryum 107
Orthostichella 125
Noteroclada 5, 6, 19, 23, 37
Ochyraea 116
Orthostichidium 123
Noteroclada confluens –
Octoblepharum 107
Orthostichopsis 123
Odontolejeunea 42
Orthothecium 120
Odontoschisma 45
Orthotrichaceae 86, 91,
Nostoc 319, 320, 393
in liverworts 21, 34
gametophyte 12
Nothoceros 139, 140, 144, 145,
159, 161, 164, 166
Odontoseries 44
Nothoceros endiviaefolius 144
Oedicladium 125
Orthotrichales 95, 111
Nothoceros giganteus – cell
Oedipodiaceae 101
Orthotrichum 65, 68, 82, 83,
wall 150
Nothofagus 461
Oedipodiales 101
Oedipodiella 102
111, 329
111, 366, 461
Orthotrichum alpestre 461
Index
Pellia 20, 21, 22, 37, 453, 454,
Orthotrichum cupulatum 337
connectivity 415, 416
Orthotrichum freyanum 453, 461
duration 418
Oryzolejeunea 42
quality 418
Pellia borealis 455, 466, 472
Osculatia 110
size 418
Pellia endiviifolia 5, 453, 466
osmotic potential 239,
240, 240
Osterwaldiella 123
Otolejeunea 42
patterned fen 360
peat 357, 366, 373, 380,
393, 426
peatland 360, 425
455, 465
Pellia epiphylla 5, 22, 30, 242,
453, 455, 457, 466
apical and slime cell 4
gametophyte 12
oxidative damage 278
alkalinity 362, 375
Pellia neesiana 457
Oxymitra 24, 25, 36
ammonium 362
Pelliaceae 30, 37
Oxymitraceae 36
bicarbonates 375
Pelliales 37
Oxyrrhynchium 118
bulk-density 383
Pelliidae 5, 9, 12, 19, 22, 28,
calcium 362, 375
Pachyglossa 9, 44
Pachyneuropsis 108
carbon cycle – correlation
383
29, 31, 37
gametophyte 12
Peltolepis 36
Pachyschistochila 43
chlorine 375
Pendulothecium 125
Palamocladium 118
climate – correlation 383
Pentastichella 111
Palisadula 125
conductivity 362
Penzigiella 123
Pallavicinia 21, 22
dating 383
Perdusenia 44
Pallavicinia ambigua – apical
dissolved organic
perennial stayers 327
cell 4
carbon 375
permafrost 377, 378
Pallaviciniaceae 20, 21, 39
fen restoration 519
Perssonia 110
Pallaviciniales 20, 21, 38
little ice age 383
Perssoniella 43
Pallaviciniineae 39
magnesium 375
Perssoniellaceae 43
Paludella 109
net primary
Perssoniellineae 43
paludification 369
production 367
Petalophyllaceae 20, 23, 38
Palustriella 116
nitrate 362
Petalophyllum 5, 38
papillae 11
nutrients 362
pH 328, 329, 333, 335, 338, 360,
Papillidiopsis 122
organic mass 373
Paracromastigum 44
peat accumulation 383
Paracromastigum bifidum –
peat mass 371
sporophyte 27
pH 362, 375
376, 415, 424, 496, 509
Phaeoceros 139, 140, 143, 144,
155, 157, 159, 161, 163,
164, 166, 247
Phaeoceros carolinianus 143
Paraleucobryum 106
phosphorus 362
Paramomitrion 47
reduced conductivity 375
apical cell 146
Paranapiacabaea 122
sodium 375
archegonium 153
Paraphymatoceros 139, 140,
total dissolved
chloroplast 147
143, 144, 161
phosphorus 375
Nostoc 151
Paraphymatoceros diadematus 143
total dissolved solids 375
pyrenoid 147
Paraphymatoceros hallii 143, 144
total Kjehldahl nitrogen 375
spore 160
Pararhacocarpus 111
total potassium 375
sporophyte anatomy 158
Paraschistochila 43
vegetation 364
stomata 158
Parisia 106
Pedinophyllopsis 45
Phaeoceros himalayensis 143
patch 410
Pedinophyllum 45
Phaeoceros laevis 143
Pelekium 117
Phaeoceros pearsonii 143, 144
configuration 418
555
556
Index
Phaeocerotoideae 142, 144
Phyllothalliaceae 39
Pilotrichum 68, 115
Phaeolejeunea 42
Phyllothalliineae 39
Pinnatella 125
Phaeomegaceros 139, 140,
phylogenetic contrast 175
Pinus sylvestris 427
144, 150, 155, 159, 161,
phylogenetic reasoning 176
Pireella 123
163, 166
phylogeny of land plants 269
pirolusite 308
Phymatocerales 143, 144
Pisanoa 45
Phymatoceros 139, 140, 143,
Plagiochasma 24, 36, 455
Phaeomegaceros fimbriatus –
haustorium 156
spore 160
sporophyte anatomy 156
Phaeomegaceros hirticalyx 166
sperm cell 154
159, 161, 164
Phymatoceros bulbiculosus 143
and Nostoc 151
Phymatoceros phymatodes 143
Plagiochasma rupestre 455, 467
Plagiochila 16, 45, 330, 453, 462
Plagiochila boryana 462
Plagiochila cambuena 462
Phaeomegacerotoideae 144
spore 160
Plagiochila carringtonii 453
phalanx 404
tuber 150
Plagiochila corrugata 462
Phanerochaete velutina 318
Phymatocerotaceae 143
Plagiochila cucullifolia 453
Phascopsis 108
Phymatocerotales 141
Plagiochila cucullifolia var.
Phascum cuspidatum 96
Physantholejeunea 42
Philonotis 110, 239, 453, 501
Physcomitrella 81, 84, 103, 199,
anomala 453
Plagiochila detecta 453, 461
Philonotis calcarea 248
200, 201, 204, 205, 206,
Plagiochila punctata 462
Philophyllum 115
207, 209, 211, 212, 213,
Plagiochila stricta 462
phloem 238
214, 217, 219, 220, 223,
Plagiochila virginica 453
phorophyte 328, 329
224, 225, 227, 230
phosphatase 322
Physcomitrella patens 199, 200,
Plagiochilaceae 12, 19, 45
Plagiochilidium 45
phosphomonoesterase 322
202, 203, 207, 279, 287,
Plagiochilion 45
phosphorus (P) 307, 311, 313,
289, 300, 307
Plagiomnium 110, 455
317, 318, 321, 322, 333,
nuclear genome 189, 300
Plagiomnium acutum 455, 469
Physcomitrellopsis 103
Plagiomnium curvatulum 455
Physcomitrium 84, 103
Plagiomnium cuspidatum 455, 469
phosphate (H2PO4 ) 301
Physcomitrium pyriforme 81, 200
Plagiomnium elatum 455
photoprotection 252, 259
Physotheca 44
Plagiomnium ellipticum 455, 469
photorespiration 248, 252
phytochrome 457
Plagiomnium insigne 455, 469
photosynthesis 1, 251, 253
Picea abies 431
Plagiomnium medium 455, 469
Photosystem II 251, 277,
Picea mariana 318, 333
Plagiopus 110
Pictolejeunea 42
Plagioracelopus 101
phy 457
Pictus 116
Plagiotheciaceae 121
Phycolepidozia 44
Pigafettoa 44
Plagiotheciopsis 120
Phycolepidoziaceae 44
Piloecium 122
Plagiothecium 65, 121
Phyllodon 120
Pilopogon 107
Plagiothecium denticulatum
Phyllodrepaniaceae 110
Pilosium 118
Phyllogoniaceae 123
Pilotrichaceae 115
Phyllogonium 124, 254
Pilotrichella 125, 239,
334, 361, 365, 399, 401
(32P) 308, 318
280, 285
Phyllothallia 5, 19, 39
Phyllothallia nivicola – apical
and slime cell 4
gametophyte 12
247, 254
332, 426
Plagiothecium undulatum
256
plasmalemma 300
Pilotrichella ampullacea 244
plasma-membrane 273
Pilotrichidium 115
plasmodesmata 61, 315
Pilotrichopsis 122
plasmolysis 243
Index
Plasteurhynchium 118
Poeltia 47
plastoglobules 7
Pogonatum 101, 468
315, 398, 422, 453, 454,
plastome 180, 182
Pogonatum dentatum 402
455, 468
Platycaulis 44
Pogonatum pensylvanicum 95
Platydictya 120
Pogonatum perichaetiale – CO2
Platygyriella 120
Platygyrium 122
Platygyrium repens 74, 425
uptake 249
Pogonatum semipellucidum –
CO2 uptake 249
Platyhypnidium 118, 453
Pohlia 68, 110, 336
Platyhypnidium mutatum 461
Pohlia cruda 247
Platyhypnidium riparioides 461
Pohlia wahlenbergii 247
Platyhypnidium riparioides –
poikilohydric plants 301
P. mutatum 453
poikilohydry 177, 238,
Platylomella 117
239, 245, 250, 260, 302,
Platyneuron 106
406, 497
Polytrichum 76, 101, 239,
CO2 uptake 249
Polytrichum alpestre 405
Polytrichum commune 242, 243,
316, 320, 321, 426, 453,
463, 468
Polytrichum formosum 256, 257,
282, 406, 455, 468
desiccation 259
Polytrichum juniperinum 317,
333, 334
CO2 uptake 249
Polytrichum longisetum 455, 468
Plaubelia 108
pollen 270
Polytrichum ohioense 468
Plectocolea 46
pollution 238
Polytrichum pallidisetum 468
Pleuridium 105
polyethylene glycol
Polytrichum piliferum 76, 249,
Pleurochaete 108
208, 219
317, 334
Polytrichum sexangulare 468
Pleurocladopsis 43
Polymerodon 106
Pleurocladula 45
polyphenols 29
Polytrichum strictum 367, 379
Pleurophascaceae 108
polyploidization 463, 464
Polytrichum uliginosum
Pleurophascum 84, 93,
polyploidy 456
99, 108
Pleurorthotrichum 39, 111
Pleurozia 5, 6, 15, 16, 18, 19,
32, 40
Pleurozia acinosa –
gametophyte 13
Pleuroziaceae 40
453, 463
Polypodium virginianum 275
poor fens 360, 361, 363
Polysporangiophyta 79, 85,
population – colonization 421
97, 157, 163
Polytrichaceae 57, 58, 62,
competition 425, 433
connectivity 416
63, 64, 65, 66, 69, 70,
density 405
73, 81, 83, 88, 101, 249,
diaspore output 411
406, 422
diaspore rain 411
Pleuroziales 39
CO2 uptake 249
disturbance 421
Pleuroziopsis 116
Polytrichadelphus 101
edge effect 504
Pleurozium 121
Pleurozium schreberi 247, 311,
320, 323, 325, 332, 333,
334, 377, 393, 401, 405,
423, 425
permafrost 378
CO2 uptake 249
Polytrichales 62, 97, 101, 248,
252, 261
Polytrichastrum 101, 455,
468, 472
Polytrichastrum
equilibrium theories 433
growth rate, l 407
herbivory 433
immigration 411
long-range dispersal 433
metapopulation
Plicanthus 46
appalachianum 468
Pluvianthus 42
Polytrichastrum ohioense 455
PMEase 322
Polytrichastrum pallidisetum 455
Pocsiella 106
Polytrichastrum sexangulare 455
shift in reproduction 421
Podomitrium 21, 22, 39
Polytrichopsida 60, 61, 66, 88,
size 411, 416
Podperaea 120
92, 101
occupancy 412
non-equilibrium
theories 433
species association 420
557
558
Index
population – colonization
Prionodontaceae 123
Pseudoracelopus 101
(cont.)
Prionolejeunea 42
Pseudoscleropodium 118
Pseudoscleropodium purum 311,
species composition 433
proline 245
species diversity 433
Proskauera 45
species richness 430
Proskauera pleurata –
spore establishment 412
gametophyte 14
313, 314, 316, 336, 426
cation exchange 312
nutrient concentration 313
Populus 431
Proteaceae 319
Populus tremula 416, 430
protective proteins 275
Pseudospiridentopsis 119
Porella 6, 13, 41, 453, 455
protein synthesis 257, 258
Pseudosymblepharis 108
Porella baueri 455, 467, 472
Protocephalozia 44
Pseudotaxiphyllum 120
Porella cordeana 455, 467, 472
Protomarsupella 45
Pseudotrachypus 119
Porella obtusa 256
protonema 279
Pseudotrismegistia 122
Porella platyphylla 242, 243, 256,
protoplasm 272
Psiloclada 44
protoplast 208, 209, 214,
Psilopilum 101
315, 453, 455, 467, 472
apical cell 4
peristome 90
219, 221
pteridophyte 145, 155
sporophyte 27
Protosyzygiella 45
Pterigynandraceae 120
turgor pressure 241
Pseudatrichum 101
Pterigynandrum 120
water potential 240
Pseudephemerum 106
Pterobryaceae 123
Porellaceae 41
Pseudobraunia 111
Pterobryella 113
Porellales 13, 15, 16, 18, 19,
Pseudobryum 110
Pterobryellaceae 112
Pseudocalliergon 116
Pterobryidium 123
Pseudocalliergon trifarium – fen
Pterobryon 123
20, 28, 31, 40
Porellineae 41
pores in conducting cells 61
restoration 519
Pterobryopsis 123
Porotrichodendron 125
Pseudocephalozia 44
Pterogonidium 122
Porotrichopsis 125
Pseudocephaloziella 46
Pterogoniopsis 122
Porotrichum 125
Pseudochorisodontium 106
Pterogonium 123
Potamium 122
Pseudocrossidium 108
Pteropsiella 9, 44
Potamolejeunea 42
Pseudocryphaea 115
Pterygoneurum 108
potassium (K) 301, 302, 305,
Pseudoditrichaceae 110
Ptilidiaceae 43
306, 307, 311, 314, 317,
Pseudoditrichum 110
Ptilidiales 15, 42
323, 333, 340, 361, 399
Pseudohygrohypnum 116
Ptilidiineae 43
K : Ca : Mg 302
Pseudohyophila 106
Ptilidium 43, 120, 453
KH2PO4 322
Pseudohypnella 120
Ptilidium pulcherrimum 332, 432
Pottiaceae 58, 71, 107
Pseudolepicolea 44
Ptilium 120
Pottiales 107
Pseudolepicoleaceae 44
Ptilium crista-castrensis 60,
Pottiopsis 108
Pseudoleskea 117
Powellia 112
Pseudoleskeella 117
Ptychanthus 42
Prasanthus 47
Pseudoleskeopsis 117
Ptychodium 117
Preissia 36
Pseudolophocolea 44
Ptychomitriaceae 104
Preissia quadrata 453
Pseudomarsupidium 45
Ptychomitriopsis 104
pressure–volume curve 241
Pseudopleuropus 118
Ptychomitrium 95, 104
pressure–volume diagram 241
pseudopodium 63
Ptychomitrium polyphyllum 337
Pringleella 105
Pseudopohlia 110
Ptychomniaceae 113
Prionodon 123
Pseudopterobryum 123
Ptychomniales 98, 113
332, 333
Index
Ptychomniella 113
random amplified
Rhachithecium 105
Ptychomnion 113
polymorphic DNA (RAPD)
Rhacocarpaceae 111
Ptychostomum 110
456, 457
Rhacocarpus 111
Puiggariopsis 121
Rauiella 117
Rhacopilopsis 120
Pulchrinodaceae 109
reactive oxygen species (ROS)
Rhamphidium 105
Pulchrinodus 109
272, 275, 277, 278, 280
Rhaphidolejeunea 42
Pycnolejeunea 42
Reboulia 24, 36, 453, 454, 455
Rhaphidostichum 122
Pylaisia 120
Reboulia hemisphaerica 455, 466
Rhexophyllum 108
Pylaisia polyantha 257
Reboulia hemisphaerica var.
Rhizobium 319
Pylaisiadelpha 122
Pylaisiadelphaceae 122
Pylaisiobryum 121
Pyramidula 81, 103
Pyrrhobryum 112
Pyrrhobryum mnioides 453
hemisphaerica 455
Reboulia hemisphaerica var.
japonica 466
Reboulia hemisphaerica var.
orientalis 455
Rectolejeunea 42
regeneration niche 421
Quaesticula 108
Regmatodon 117
quantum efficiency 340
Regmatodontaceae 117
Quercus robur 431
rehydration 271, 272, 276,
Racelopodopsis 101
Rhizohypnella 120
rhizoid (see under liverwort,
moss, and hornwort) 16,
239
rhizoidal tubers 327
Rhizomnium 110, 455, 472
Rhizomnium magnifolium 455,
Racomitrium 62, 104, 331
Reimersia 108
relative electron transport
337, 406
Rhizogonium 112
302, 314, 315
Racomitrium aquaticum 248, 256
243, 248, 256, 257, 326,
Rhizogoniales 111
Rhizomnium gracile 455, 469
rehydrin 284, 285, 286, 287
Racomitrium lanuginosum 242,
Rhizogoniaceae 112
279, 280, 281, 284, 287,
Racelopus 101
Racomitrium fasciculare 337
Rhizofabronia 119
rate 253
469
Rhizomnium pseudopunctatum
455, 469
Rhizomnium queenslandica 455
relative humidity 271
Rhodobryum 110
relative water content (RWC)
Rhodobryum roseum 66
240, 241, 241, 243, 244
Rhodoplagiochila 45
Remyella 118
Rhynchostegiella 118, 452, 453
Racopilaceae 112, 447
Renauldia 123
Rhynchostegiopsis 115
Racopilum 66, 82, 112, 447, 453
reporter gene 213, 218,
Rhynchostegium 117,
desiccation 258
Rad51 gene 216
225, 227
118, 452
Rhynchostegium riparioides 322,
Rad52 epistasis group 216
restoration 512
Rad52 gene 217
retrotransformation 224
radionuclides 303
retrotransposon 223
Rhytidiaceae 121
Radula 13, 16, 18, 28, 31, 41, 330
reverse genetics 201, 213,
Rhytidiadelphus 121, 453, 458
217, 218, 225, 230
Rhytidiadelphus japonicus 458
Radula flaccida 331
Radula obconica – cells and oil
bodies 8
338
reverse transcriptase 205
Rhytidiadelphus loreus 242, 458
Rhabdodontium 123
Rhytidiadelphus squarrosus
Rhabdoweisia 106
304, 315, 320, 336,
Radulaceae 31, 41
Rhabdoweisiaceae 99, 106
426, 458
Radulina 122
Rhachitheciaceae 87, 91, 105
Rhytidiadelphus subpinnatus 458
Radulineae 41
Rhachitheciopsis 105
Rhytidiadelphus triquetrus 242,
ramet 491
Rhachitheciopsis tisserantii 82
sporophyte 27
313, 398, 406, 458
559
560
Index
Rhytidiopsis 121
Saulomataceae 114
Sciuroleskea 118
Rhytidium 121
Sauteria 36
Sclerodontium 106
ribosomal proteins 287
Scabridens 123
Sclerohypnum 120
Riccardia 20, 40
Scapania 46
Scleropodium 118, 239, 247
Riccia 23, 24, 25, 31, 36, 328,
Scapania undulata 325,
Scleropodium purum 512
453, 454
Riccia sommieri –
distribution 509
Ricciaceae 8, 25, 27,
28, 36
326, 338
Scopelophila 108
Scapaniaceae 13, 16, 45, 508
Scopelophila cataractae 341
Scapaniella 46
Scorpidium 57, 116, 370
Scaphophyllum 46
Scorpidium cossonii – fen
Schiffneria 9, 45
restoration 519
Ricciocarpos 23, 24, 25, 36
Schiffneriolejeunea 42
rich fens 359, 361, 363
Schimperella 118
Riella 35
Schimperobryaceae 114
Riellaceae 35
Schimperobryum 114
Scorpiurium 118
Rigodiaceae 116
Schistidium 104
Scouleria 103
Rigodiadelphus 117
Schistidium apocarpum 337
Scouleriaceae 103
Rigodium 117
Schistidium maritimum 339,
Scouleriales 103
RNAi-interference 224
Roellia 110
339, 340, 341
Schistidium maritimum –
Roivainenia 46
quantum
Rosulabryum 110
efficiency 340
Scorpidium scorpioides 248, 364,
367, 377, 382, 384, 425
fen restoration 519
Sehnemobryum 111
Selaginella lepidophylla
272, 282
selection cassette 219,
Rozea 117
Schistochila 16, 18, 28, 43
RUBISCO (see also hornwort
Schistochilaceae 13, 19, 43
selenium (Se) 322
Schistochilopsis 46
self-thinning 404
RUBISCO) 247
220, 224
Ruizanthus 46
Schistomitrium 107
Seligeria 104, 491
Rutenbergia 115
Schistostega 65, 67, 105
Seligeriaceae 104
Rutenbergiaceae 115
Schistostegaceae 105
Sematophyllaceae 69, 122
Schizymenium 110, 461
Sematophyllum 122
Saccogyna 46
Schizymenium shevockii 453
Seppeltia 39
Saccogynidium 46
Schliephackea 106
Serpoleskea 116
Saelania 105
Schlotheimia 82, 111
Serpotortella 108
Saelania glaucescens 247
Schoenobryum 122
Serpotortellaceae 108
Sagenotortula 108
Schofieldia 45
Sewardiella 5, 38
Saitobryum 108
Schofieldiella 121
sex chromosome 74
Sambucus nigra 329
Schraderella 122
short-lived shuttle 328
Sandeothallaceae 39
Schroeterella 122
shot-gun sequencing 206
Sandeothallus 5, 39
Schusterella 41
shuttle 330
Sandeothallus radiculosus 5
Schusterolejeunea 42
shuttle species 492
Sanionia 116
Schwetschkea 117
sieve cell 62
Sarconeurum 108
Schwetschkeopsis 126
signal transduction 226, 275
Sasaokaea 116
Sciadocladus 113
sink population 411
saturation irradiance 248,
Sciaromiella 116
Sinocalliergon 116
Sciaromiopsis 116
Sinskea 119
Sciuro-hypnum 118
Siphonolejeunea 42
249, 250, 260
Sauloma 114
Index
Sphagnum girgensohnii 455, 469
sister-group contrast 175, 178
406, 407, 414, 422, 424,
Site of Special Scientific
425, 426, 427, 428, 454,
Sphagnum inundatum 455, 471
455, 457, 459, 462, 469,
Sphagnum isoviitae 457, 458
470, 471, 499, 501, 519
Sphagnum jensenii 364, 378,
Interest 495
Skottsbergia 105
slugs 332
sodium (Na) 301, 304, 305,
317, 324, 326, 340, 361
sodium-entry 340
Solenostoma 46
Solenostoma crenulata 341
Solmsiella 105
net primary production 380
Sphagnum sect. Acutifolia
454, 459
Sphagnum sect. Cuspidata 461,
470, 470
Sphagnum sect. Subsecunda
454, 459, 471
somaclonal variation 223
Sphagnum andersonianum 459
somatic hybrid 208
Sphagnum angustifolium 364,
Sorapilla 69, 126
368, 369, 377, 379, 457,
Sorapillaceae 126
458, 464
source populations 411
Southbya 46
species diversity 508
species richness and diameter
at breast height 514
sperm dispersal 77
Sphaerocarpaceae 8, 35
Sphaerocarpales 19, 27, 30,
33, 35
Sphaerocarpos 19, 31, 32, 35, 58
Sphagnum annulatum 455,
470, 471
Sphagnum annulatum –
allopolyploidy 470
Sphagnum balticum –
Sphagnum majus 364, 378, 455,
470, 471
Sphagnum majus –
allopolyploidy 470
Sphagnum mirum 454
Sphagnum molle 401
Sphagnum papillosum 364, 368
Sphagnum platyphyllum 471
allopolyploidy 364, 455,
Sphagnum pylaesii 454, 459
470, 470, 471
Sphagnum quinquefarium 454,
338, 364, 368, 453, 454,
459, 462
Sphaerothecium 106
Sphagnum carolinianum 455, 471
Sphagnaceae 100
Sphagnum contortum 471
Sphagnales 100
Sphagnum cribrosum 454, 459
Sphagnopsida 61, 63, 79, 86,
Sphagnum cuspidatum 247, 364,
367, 453, 455, 470
Sphagnum cuspidatum –
68, 70, 71, 73, 75, 76, 77,
allopolyploidy 470
80, 81, 83, 84, 85, 86, 87,
Sphagnum ehyalinum 71,
94, 95, 97, 99, 100, 101,
369, 377, 425
Sphagnum obtusum 378
455, 471
Sphagnum capillifolium 316,
91, 100
454, 459
Sphagnum magellanicum 364,
Sphagnum nemoreum 318
Sphaerosporoceros 139, 142,
Sphagnum 56, 57, 62, 63, 64,
401, 457
Sphagnum macrophyllum
Sphagnum auriculatum
Sphagnum brevifolium 458
144, 159, 161, 164, 166
Sphagnum lescurii 455, 471
Sphagnum lindbergii 364, 378,
Sphagnum aongstroemii 401
Sphaerolejeunea 42
Sphaerotheciella 122
455, 470, 470, 471
Sphagnum lenense 364
454, 461
455, 462, 469
Sphagnum recurvum 315, 458,
454
Sphagnum recurvum
complex 458
Sphagnum riparium 364,
378, 378
Sphagnum rubellum 364, 453,
455, 459, 464, 469
Sphagnum russowii 304,
455, 469
Sphagnum squarrosum 321,
338, 425
155, 200, 306, 310, 317,
Sphagnum fallax 425, 457, 458
Sphagnum subnitens 425
320, 321, 325, 328, 338,
Sphagnum flexuosum 458
Sphagnum subsecundum 364,
361, 363, 365, 366, 368,
Sphagnum fuscum 310, 364,
369, 370, 371, 374, 376,
379, 393, 396, 398, 399,
400, 401, 402, 403, 404,
368, 369, 371, 377, 424
Sphagnum fuscum – nitrate
reductase 310
453, 455, 459, 471
Sphagnum subtile 459
Sphagnum tenellum 406,
455, 470
561
562
Index
Steereobryon 101
Superclass IV 101
Steereochila 45
Superclass V 86, 101
Sphagnum tenerum 459
Stegonia 108
surface tension 237, 247
Sphagnum teres 364
Stenocarpidiopsis 118
Symbiezidium 42
Sphagnum troendelagicum 455,
Stenocarpidium 118
Symblepharis 106
Stenodesmus 115
Symphogyna 454
Stenodictyon 115
Symphyodon 121
Stenolejeunea 42
Symphyodontaceae 121
Sphagnum tundrae 454, 460
stenophylls 66
Symphyogyna 5, 26, 39
Sphagnum viride 453
Stenorrhipis 45
Symphyogynopsis 39
Sphagnum warnstorfii 364,
Stenotheciopsis 120
Symphysodon 123
Stephaniella 46
Symphysodontella 123
Stephaniellidium 46
symplast pathway 315
Sphagnum tenellum –
allopolyploidy 470
470, 471
Sphagnum troenlandicum –
allopolyploidy 470
455, 469
Sphagnum-dominated
Stephensoniella 36
symplast water 243, 244
Sphenolobopsis 46
Stereodon 120
Synthetodontium 110
Sphenolobus 46
Stereodontopsis 120
Syntrichia 108, 248, 366
Spinacia oleracea –
Stereophyllaceae 117
peatlands 363
photosynthesis 244
Stereophyllum 118
desiccation tolerance 178
Syntrichia caninervis 399
Spiridens 113
Steyermarkiella 69, 106
Spiridentopsis 123
Stictolejeunea 42
Syntrichia intermedia 246
Splachnaceae 84, 86, 93,
desiccation tolerance 178
stochasticity 500
Syntrichia laevipila 454
109, 334, 335, 336,
Stolonivector 44
Syntrichia norvegica –
401, 413, 415
stomata (see also under
Splachnales 109
liverwort, moss, and
Splachnobryum 108
hornwort) 1, 177, 237,
Splachnobryum obtusum 75
239, 249
desiccation
tolerance 178
Syntrichia ruralis (see also Tortula
ruralis) 248, 254, 256
Stonea 108
Syringothecium 120
Stoneobryum 83, 111
Syrrhopodon 107
Straminergon 116
Syrrhopodon prolifer 71
335, 336, 414
Streptocalypta 108
Syzygiella 45
Splachnum luteum 335,
Streptopogon 108
Szweykowskia 45
Splachnum 86, 109, 328,
334, 414
Splachnum ampullaceum 248,
335, 414
Streptotrichum 108
Splachnum rubrum 335
Strombulidens 105
Taiwanobryum 125
splash-cup 398
strontium (90Sr) 311,
Takakia 57, 59, 61, 63, 67,
spores 269, 274
322, 324
80, 85, 86, 92, 94, 97,
Sporogonites 97
Struckia 121
sporophytes 273
subfunctionalization 229
Takakia lepidozioides 56
Spruceanthus 42
succubous leaves 15
Takakiaceae 100
Spruceanthus theobromae 516
sucrose 276
Takakiales 100
Sprucella 44
sulfur (SO2) 308
Takakiopsida 100
Squamidium 118
sulfur (SO42−) 301
targeted gene replacement
starch – in liverwort 30
Superclass I 100
Steerea 41
Superclass II 100, 121
Steereella 40
Superclass III 100
99, 100
(TGR) 221, 222, 223, 224
targeted insertion 221,
222–3, 222
Index
Targionia 24, 25, 36, 454,
455, 467
Thelia 68, 126
Tortula ruraliformis 278
Theliaceae 126
Tortula ruralis (see also Syntrichia
Targionia hypophylla 242, 467
Thuidiaceae 117
ruralis) 200, 225, 242,
Targionia hypophyllax 455
Thuidiopsis 117
270, 271, 272, 273, 274,
Targionia lorbeeriana
Thuidium 117, 239
275, 276, 277, 278, 280,
Thuidium delicatulum 72
281, 282, 283, 284, 285,
Targioniaceae 36
Thuidium tamariscinum 404
286, 287, 288, 315, 325,
Taxilejeunea 42
thylakoid 282
Taxiphyllopsis 120
Thysananthus 42
455, 467
337
Tortula schimperi 460
Taxiphyllum 120
Timmia 91, 97, 102, 454, 461
Tortula subulata 454, 460
Taxitheliella 122
Timmia austriaca 461
totipotency 220, 227
Taxithelium 122
Timmia megapolitana –
Touwia 125
Tayloria 109, 334
Tayloria lingulata 334
Tayloria tenuis 405
Telaranea 44
Temnoma 44
peristome 89
Timmia megapolitana subsp.
bavarica 461
Timmia megapolitana subsp.
megapolitana 461
Teniolophora 108
Timmiaceae 102
terpenoids 6, 8
Timmiales 102
Tetracoscinodon 108
Timmiella 108
Touwiodendron 113
Tr288 287
Tr288 288
Trabacellula 45
tracheid 61, 238
tracheophyte 139, 145, 163,
177, 181
chloroplast genome 180
Tetracymbaliella 14, 44
Timmiidae 102
endospory 178
Tetralophozia 45
Timotimius 122
Trachycarpidium 108
Tetraphidaceae 101
Tisserantiella 105
Trachycladiella 119
Tetraphidales 97, 101
titanium (Ti) 322
Trachycystis 110
Tetraphidopsida 88, 101
Toloxis 119
Trachylejeunea 42
Tetraphidopsis 113
Tomenthypnum 118, 370
Trachyloma 115
Tetraphis 66, 88, 92,
Tomenthypnum falcifolium
Trachylomataceae 115
94, 95
Tetraphis pellucida 332, 421
population dynamic 421
364, 367
Tomenthypnum nitens 70, 364,
367, 370, 371
Trachyodontium 108
Trachyphyllum 120
Trachypodopsis 117, 119
Tetraplodon 109, 334, 414
tonoplast 300, 301
Trachypus 119
Tetraplodon angustatus 414
Tortella 108
Trachythecium 121
Tetraplodon mnioides 334,
Tortella flavovirens 339
Trachyxiphium 115
Tortella tortuosa 337
transcription 274, 284, 285
Tetraplodon paradoxus 93
Tortula 65, 108, 271, 287
transcription factor 226, 229
Tetrapterum 108
Tortula caninervis (see also
transcriptional network
335, 414
Tetrastichium 115
Syntrichia caninervis) 271,
Tetrodontium 85, 101, 491
273
228–30
transcripts 274
thallium (Tl) 324
Tortula inermis 257, 273, 460
transfer cells 301, 308
Thamniopsis 115
Tortula intermedia –
transformation 209, 211, 212,
Thamnobryum 125
photosynthesis 253
214, 219, 220
Thamnobryum alopecurum 338
Tortula mucronifolia 460
transgenic line 221
Thamnobryum angustifolium
Tortula norvegica 273
transition to land 97
Tortula plinthobia – peristome 90
translation 284, 285
490
563
564
Index
transport systems 237
turgor – loss 241, 243
vittae 11
transporter proteins 301
turgor – loss point
Vittia 68, 116
240, 241
Voitia 93, 109
transporter-like
proteins 307
Tuyamaella 42
transposon 209, 211
Tuzibeanthus 42
Warburgiella 122
Trematodon 105
Tylimanthus 46, 458
Wardia 106
Treubia 6, 7, 9, 19, 29,
Tylimanthus saccatus –
Warnstorfia 116
32, 34
gametophyte 14
Treubia lacunosa –
gametophyte 10
Warnstorfia exannulata
364, 367
Uleastrum 105
Warnstorfia fluitans 364
Uleobryum 108
water conduction 239, 247
Ulmus 329
water deficits 269
Treubiales 34, 114
Ulota 69, 70, 111, 257
water loss 245, 246, 248
Treubiidae 33
Ulota crispa 415
water potential 239, 241,
Triandrophyllum 44
Ulota phyllantha 339
Trichocolea 26, 44
Unclejackia 121
water relations 239–45
Trichocoleaceae 44
Urtica dioica 332
water repellent 249
Treubiaceae 2, 16, 19,
22, 34
Trichocoleopsis 14, 31, 43
272, 273
water sac 14–15
Trichodon 105
vaginula 63
water sac – Frullania-type 14
Trichosteleum 122
vanadium (V) 322, 324
water sac – Lejeunia-type 14
Trichostomum 108
Vanaea 45
water storage 244,
Trichotemnoma 46
Vandiemenia 40
Trichotemnomataceae 46
Vandiemeniaceae 40
Tricocholea 12
vascular tissue 177
Tridontium 103
vegetative desiccation
triglyceraldehydes 7
trigones 11
trimeric replication
protein A (RPA complex)
270
vegetative desiccation
247, 254
water transport (see
under liverwort and moss)
238, 239
Weisiopsis 108
Weissia 108
tolerance 269, 270,
Weissia controversa 458
274, 277
Weissia wimmeriana 454
Venturiella 105
Weissiodicranum 108
Tripterocladium 120
Verdoornia 21, 22, 40
Werneriobryum 106
Triquetrella 108
Verdoornia succulenta –
wetland classes 359
Trismegistia 122
gametophyte 13
216
Wettsteinia 45
Tristichium 105
Verdoornianthus 42
Tritomaria 46
Verrucidens 106
Trochobryum 104
Vesicularia 120
Weymouthia mollis 256
Trocholejeunea 42
Vesiculariopsis 114
Wiesnerella 24, 25,
Trolliella 122
vessel 238
Tuerckheimia 108
Vetaforma 44
Wiesnerellaceae 36
turgidity 271
Vetaformataceae 44
Wijkia 122
turgor osmotic
Viridivelleraceae 106
Wijkiella 120
Viridivellus 106
Wildia 105
Vitalianthus 42
Willia 108
vitrification 276, 278
Wilsoniella 105
potential 241
turgor pressure
239, 240
Weymouthia 125, 247, 254,
454, 461
31, 36
Index
xanthophyll 278
xylans 61
Zelometeorium 118
Xenocephalozia 44
xylem 238, 239
zinc (Zn) 304, 305,
Xenochila 45
Xylolejeunea 42
Xenothallus 22, 26, 39
Xenothallus vulcanicola –
yttrium (Y) 324
Zoopsidella 44
Zoopsis 44
sporophyte 27
Pleuriditrichum 105
308, 322,
324, 325
Zanderia 105
Zygodon 82, 111
565