Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2003? 2003
142?
4163
Original Article
ECOLOGICAL DIVERSITY IN
TRICHOMANES
(HYMENOPHYLLACEAE)
J.-Y. DUBUISSON
ET AL.
Botanical Journal of the Linnean Society, 2003, 142, 41–63. With 15 figures
Ecological diversity and adaptive tendencies in the
tropical fern Trichomanes L. (Hymenophyllaceae) with
special reference to climbing and epiphytic habits
JEAN-YVES DUBUISSON1*, SABINE HENNEQUIN1, FRANCE RAKOTONDRAINIBE2
and HARALD SCHNEIDER3
1
Equipe ‘Classification, Evolution et Biosystématique’, Laboratoire de Paléobotanique et Paléoécologie,
IFR 101 CNRS ‘Institut d’Ecologie Fondamentale et Appliquée’, Université Pierre et Marie Curie, 12 rue
Cuvier, F-75005 Paris, France
2
EPHE, Laboratoire de Phanérogamie, Muséum National d’Histoire Naturelle, F-75005 Paris, France
3
Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Abt. Systematische Botanik, Georg-AugustUniversität Göttingen, Untere Karspüle 2, 37073 Göttingen, Germany
Received July 2002; accepted for publication January 2003
Among the basal fern families, the Hymenophyllaceae, with more than 600 species, display a high diversity in terms
of their morphology and the habitats that they occupy. We have chosen to focus on Trichomanes L., a clearly defined
genus for which a phylogeny is presently being developed, to investigate the appearance of the climbing and epiphytic habits, as well as the related supposed adaptive characters. In this study we present the first review of the
different ecological types within the genus: terrestrial, climbing (divided into hemi-epiphytic forms and true lianas),
and epiphytic types. The study of several features concerning stem morphology and leaf size allows a proposal on
relationships between ecology and plant morphology. Terrestrial species display a thick monocaulous rhizome with
robust roots and short internodes. Climbing species are characterized by a branched, thick, creeping rhizome with
long internodes. Epiphytic species also exhibit long, creeping and branching stems with long internodes but the rhizome is fine to filiform. Under these circumstances, there is a reduction of root system and frond size leading to
dwarfism in numerous instances. This may be related to an extreme hygrophilous epiphytic strategy. Finally, hypotheses on the evolution of these habits and hence on the evolutionary relationships between ecology and characters are
presented and discussed. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003,
142, 41–63.
ADDITIONAL KEYWORDS: filmy ferns – hygrophilous – lianescence – pteridophytes – rain forests – vines.
INTRODUCTION
The Hymenophyllaceae are the largest and most speciose (more than 600 species) family of the basal ferns.
The oldest putative fossils are from the Triassic
(Axsmith, Krings & Taylor, 2001), and recent phylogenetic studies suggest close relationships with families of Palaeozoic origin such as Osmundaceae and
gleicheniaceous ferns including Gleicheniaceae,
Cheiropleuriaceae, Matoniaceae and Dipteridaceae
(Pryer, Smith & Skog, 1995; Pryer et al., 2001a).
Hymenophyllaceae have a pantropical distribution,
*Corresponding author. E-mail: jdubuiss@snv.jussieu.fr
and they are common ferns in all tropical rain forests.
In addition, they show a remarkable diversity in terms
of morphology (e.g. minute to large, simple to highly
divided, mono- or dimorphic fronds; short to long creeping stem with robust roots or rootless) and the habitats
that they occupy (reported as terrestrial, epiphytic and/
or epipetric, hemi-epiphytic, lianescent). Such a diversity is rarely found in any other extant groups of ferns
(Dubuisson, 1996, 1997a). Hymenophyllaceae (filmy
ferns or filmies) are an excellent model group for studying the evolution of ecology and related adaptive survival strategies in pteridophytes, especially of the
climbing or lianescent type; this latter is exceptional
and rarely studied in ferns (see Putz & Mooney, 1991).
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
41
42
J.-Y. DUBUISSON ET AL.
Infra-familial relationships among filmy ferns continue to be debated, as illustrated by numerous conflicting published classifications (Copeland, 1938,
1947; Morton, 1968; Pichi Sermolli, 1977; Iwatsuki,
1984, 1990; reviewed by Dubuisson, 1996, 1997a). A
recent molecular analysis confirms the existence of
two lineages, corresponding to the traditional bigeneric classification that recognizes Trichomanes sensu
lato and Hymenophyllum s.l. (Pryer et al., 2001b). Trichomanes s.l. (corresponding to the tribe Trichomaneae sensu Schneider, 2000) appears the best
delimited of the two, and it is also the most diverse
both morphologically and ecologically. The morphologically more uniform Hymenophyllum s.l. (involving
Morton’s genera Cardiomanes, Serpyllopsis, Hymenoglossum, Rosenstockia and Microtrichomanes; Hennequin et al. in press) includes only epiphytic and/or
epipetric taxa (exceptionally terrestrial). Strictly terrestrial and climbing/lianescent growth forms are
known only within Trichomanes. Preliminary phylogenetic works suggest that epiphytism has evolved
independently in the two lineages (Dubuisson, 1997b;
Pryer et al., 2001b). We have chosen, therefore, the
Trichomanes s.l. lineage (called here genus Trichomanes) as a model group for studying the evolution
and appearance of climbing habit, epiphytism and
related supposed adaptive characters in a monophyletic well-defined group of pteridophytes. A comparative analysis that uses a phylogenetic framework to
test relationships and to study the correlation
between character occurrence and ecology (as suggested by Harvey & Pagel, 1991) appears to be the
most appropriate approach. However, this type of
analysis needs a robust and complete phylogeny (still
in progress). We propose, therefore, to perform a first
descriptive study with the objectives (i) to clarify the
different extant ecological types among the genus (in
fact a global ecological review has not yet been published despite some attempts; Tryon & Tryon, 1982;
Iwatsuki, 1990; and others), and (ii) to observe more
precisely some morphological features which could
appear as good candidates for supposed ecological
adaptations. This work is necessary for providing
hypotheses which will be tested in subsequent phylogenetic and comparative studies. The study is
restricted to general morphological characters of the
sporophytic phase.
MATERIAL AND METHODS
TAXA
We selected 193 out of the 325 recognized living species of Trichomanes according to Morton (1968; see
Appendix), as a representative sample of the morphological and ecological diversity of the genus. In addi-
tion, all the sections defined by Morton, which are the
best-delimited infrageneric taxonomic units, are represented. Table 1 lists the 25 sections sensu Morton
with the corresponding subgenera, geographical distribution and number of recognized and selected species. Correspondences with section are also indicated
in the species list (Appendix).
ECOLOGY
A review of the precise ecological type or habitat of
each species was extracted from literature data, especially floras (Copeland, 1933, 1938, 1947; Baker &
Posthumuis, 1939; Tardieu-Blot, 1951; Wessels Boer,
1962; Tindale, 1963; Vareschi, 1968; Brownlie, 1969;
Hébant-Mauri, 1972; Kornas, 1976, 1994; Yoroi &
Iwatsuki, 1977; Tagawa & Iwatsuki, 1979; Jacobsen,
1983; Iwatsuki, 1984, 1985, 1991; Taylor, 1984;
Brownsey & Smith-Dodsworth, 1989; Proctor, 1989;
Burrows, 1990; Lellinger, 1991, 1994a, 1994b; Parris,
Beaman & Beaman, 1992; Prelli & Boudrie, 1992;
Windish, 1992; Farrar, 1993; Duncan & Isaac, 1994;
Pacheco, 1994; Smith, 1995; Stace, 1997; Bostock &
Spokes, 1998; Sanchez, 2000; Prelli, 2001, 1992), notes
on herbarium specimens deposited at Paris (P), The
Field Museum, Chicago (F), Berkeley (UC), Université
de Montpellier II (MPU) and Université de La
Réunion (REU), and personal field observations and
communications (including Bolivia, Borneo, Colombia,
Costa Rica, Ecuador, France (Normandy and Brittany), French Guiana, Germany (Palatina), Java,
Madagascar, Malay Peninsula, New Zealand, New
Caledonia, La Réunion, Venezuela).
SELECTED
STUDIED CHARACTERS
All the morphological observations were made on herbarium specimens from P, F, UC, MPU and REU (list
of vouchers available on request) and complemented
by data extracted from an exhaustive literature search
(see above references used for ecology).
To delimit the plant habit or growth form, which
depends mainly on the characters of rhizome or stem,
we selected several characters correlated with the rhizome (shoot): (i) the stem internode length; (ii) the
stem rhizome thickness; (iii) the stem branching pattern (that is supposed to be related to internode length
according to Hébant-Mauri, 1972); and (iv) the presence and structure of roots (fully studied by Schneider,
2000). Because of the problem of sampling homogeneity (i.e. number of available specimens per species)
and the fact that much data were culled from the literature, all these observations are qualitative.
Several Trichomanes species are dwarfish with
respect to their frond size (i.e. fronds less than 2 cm
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
43
Table 1. List of Morton’s subgenera and sections within Trichomanes with geographical distribution, number of reported
species (according to Morton) and number of selected species for the present study (see Appendix)
Subgenera
Sections
Geographical distribution
Number of
reported species
Number of
selected species*
Trichomanes
Trichomanes
Lacosteopsis
Gonocormus
Crepidomanes
Crepidium
Phlebiophyllum
Pleuromanes
Didymoglossum
Microgonium
Lecanium
Achomanes
Acarpacrium
Feea
Neurophyllum
Odontomanes
Homeotes
Trigonophyllum
Ragatelus
Lacostea
Pachychaetum
Cephalomanes
Davalliopsis
Callistopteris
Nesopteris
Abrodictyum
West Indies
Cosmopolitan
Palaeotropical
Palaeotropical
Asiatic†
Australia + New Zealand
Asiatic†
Neotropical‡
Palaeotropical‡
Neotropical
Neotropical§
Neotropical
Neotropical
Neotropical
Neotropical
Neotropical
Neotropical
Neotropical
Neotropical
Pantropical
Asiatic†
Neotropical
Asia-Pacific
Asia-Pacific
New Guinea + Philippines
1
58
15
29
8
1
3
19
20
1
38
9
4
2
3
1
2
1
4
30
16
1
5
6
1
1
34
7
14
5
1
2
17
20
1
19
6
5
3
1
1
4
1
4
27
11
1
3
4
1
Didymoglossum
Achomanes
Pachychaetum
*involving species not reported by Morton
can include Indian Ocean, Malaysian area and Pacific Ocean
‡
+ few palaeotropical species for Didymoglossum and few neotropical species for Microgonium
§
+ one single African species (T. crispiforme Alston)
†
long), and exhibit reduction in numerous anatomical
and morphological features (such as rootless filiform
stem). Prantl (1875), Giesenhagen (1890) and Copeland (1938) suggested that these features were
derived and not confined to primitive states. Tryon &
Tryon (1982) and Iwatsuki (1990) proposed that these
reductive tendencies could be adaptations to very wet
and moist environmental conditions. A first cladistic
study based on anatomy and morphology (Dubuisson,
1997a) and an anatomical comparative investigation
of the roots (Schneider, 2000) have suggested simplification in the evolution of several characters in Trichomanes, including especially frond size and root
system reduction. Extreme cases, such as the loss of
root system, seem indeed to be correlated with habitat
and especially epiphytism (Schneider, 2000). Consequently, we also recorded the average size of the mature
leaves (lamina + petiole). Root characters have been
presented previously and designation of different root
system types follows Schneider’s nomenclature.
EVOLUTIONARY
HYPOTHESES
In order to provide first hypotheses about possible
relationships between ecology and morphology, we
inferred first, on a phylogeny, the evolution of ecological types. The selected phylogeny was reconstructed
using an unequally weighted maximum parsimonious
analysis on chloroplast rbcL nucleotide sequences performed with PAUP* ver. 4b10 software (Swofford,
2002) on a Pentium4 2 GHZ PC, according to the taxonomic sampling, data-set and reconstruction methods described in Pryer et al. (2001b). We nevertheless
reduced the sister-genus Hymenophyllum sampling to
four representative species (H. tunbrigense (L.) Sm.,
H. fucoides (Sw.) Sw., H. hirsutum (L.) Sw. and Cardiomanes reniforme (G.Forst.) C.Presl.) and we added
three new Trichomanes species: the epiphyte
T. diaphanum Humb., Bonpl. & Kunth (already published sequence; see Dubuisson, 1997b); the epiphyte
T. polypodioides L. (new sequence, GenBank accession
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
44
J.-Y. DUBUISSON ET AL.
number AY175795) and the climbing T. ankersii
C.Parker (new sequence, GenBank accession number
AY175800). At least in the Trichomanes lineage, the
produced topology (a single most-parsimonious tree of
3117.70 steps with CI = 0.4151 and RI = 0.4719) is
similar to the phylogenies published in Dubuisson
(1997b) and Pryer et al. (2001b), except for the inclusion of both the additional new sequenced species (see
Fig. 12). Supports for the major nodes are discussed in
the cited papers. A posteriori evolution of habitats was
inferred using MacClade software (Maddison & Maddison, 1992). We tested both character evolution
optimization criterions: ACCTRAN (‘Accelerated
Transformations’) and DELTRAN (‘Delayed Transformations’) in the PAUP program. This allows provision
of alternative equally parsimonious scenarios if equivocal ancestral state is revealed on some branches
(Kitching et al., 1998: 71–73). Because the taxonomic
sampling remains reduced, especially within Trichomanes, no statistical comparative analyses are presented here.
elevations on the trunks, up to 15 m (rarely at
upper levels except in very moist forests) and probably rarely or never in the higher canopy, in contrast to numerous angiosperm epiphytes such as
orchids or bromeliads and other ferns such as polypods and davalloids. This distribution is probably
related to the decrease in water availability (as discussed later).
(iii) Climbing habit characterizes species that are
found mostly climbing on tree-trunks at the adult
stages, but in some cases they grow as terrestrials or
epiphytes. The latter corresponds to hemi-epiphytic
climbers. Trichomanes giganteum Bory (section Lacosteopsis) in Mare Longue forest (La Réunion) is a typical hemi-epiphytic taxon, able to colonize a wide
surface of the ground and also sometimes to climb on
tree trunks (Fig. 5). As discussed later, hemiepiphytism is distinct from true lianescence where
contact with the soil is obligatory. Lianas are thus,
indeed, terrestrial plants with climbing stems. Both
types of climbers (hemi-epiphytic or true liana) are
found in Trichomanes.
RESULTS
ECOLOGICAL
DIVERSITY
An ecological type for each taxon is reported in the
species list (Appendix). This review allows three principal types to be distinguished: (i) terrestrial, (ii) epiphytic, and (iii) climbing forms (hemi-epiphytes and
lianas).
(i) The terrestrial species are always rooted in the
ground and often located in very wet places and/or on
river or stream banks, sometimes along trekking
paths (Figs 1,3). In these latter places, the ferns can
sometimes also be epipetric if their roots have the
opportunity to fix themselves in small crevices (e.g.
Asiatic T. javanicum Blume, section Cephalomanes
and T. meifolium Bory, section Pachychaetum, widespread in rainy primary forests; e.g. Bebour and Mare
Longue Forests in La Réunion). In very wet forests
(e.g. Asiatic dipterocarp forests), ‘terrestrial’ species
are occasionally found on the base of trunks or on
emerged tree roots, and more often on fallen and/or
rotten logs. In La Réunion, T. meifolium is frequently
observed on fallen mossy trunks and T. javanicum can
also grow on rotten logs in the Asiatic dipterocarp forests. The widespread neotropical T. crispum L. (section Achomanes) is another example of a mostly
terrestrial species, often reported in numerous other
habitats (occasionally epiphytic).
(ii) The epiphytic species are never (or exceptionally) in contact with the ground, and the whole life
cycle is completed on the supporting plant. The
ferns grow mostly on tree trunks or on branches
(Figs 2,4). Nevertheless, they are mainly at low
ECOLOGY
AND
TRICHOMANES
TAXONOMY
Out of the 193 species studied, we found 78 terrestrials (40.5%), 88 epiphytes (45.6%), 16 hemi-epiphytes
(8.3%, including related temperate epipetric species,
see Discussion) and four true lianas (2%). Seven species (3.6%) were observed either as epiphytes or in terrestrial settings. We observed relative ecological
uniformity at the level of Morton’s section.
About half of the terrestrial species belong to the
neotropical subgenus Achomanes (sensu Morton)
which includes the sections Achomanes, Acarpacrium,
Trigonophyllum,
Neurophyllum,
Odontomanes,
Homeotes and Feea. Subgenus Achomanes contains a
few species that are mostly epiphytic (T. dactylites
Sodiro, T. steyermarkii P.G.Windisch & A.R.Smith,
and T. lucens Sw., section Achomanes) and at least one
obligate epiphyte (T. polypodioides L., section Acarpacrium). The remainder of the terrestrial species correspond
to
Morton’s
pantropical
subgenus
Pachychaetum, which includes the sections Pachychaetum, Cephalomanes, Davalliopsis, Callistopteris and
Nesopteris. There is a single strict epiphyte in this
group, the monotypic Abrodictyum. A few species of
section Pachychaetum (T. tamarisciforme Jacq.
(Fig. 2), T. flavo-fuscum Bosch, T. caudatum Brack.
and T. cellulosum Klotzsch) can also be found more
often as epiphytes growing on the base of mossy tree
trunks and on fallen logs than on the ground.
Half of the epiphytic species belong to Morton’s subgenus Didymoglossum, which comprises the sections
Didymoglossum, Microgonium and Lecanium. A second group of epiphytes corresponds to the mostly
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ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
45
Figures 1–3. Typical Trichomanes environments. Fig. 1. Typical cloud forest from La Réunion (Bebour forest, alt.
ª1350 m, photo J.-Y. Dubuisson), the annual rainfall is from 4000 to more than 10 000 mm (Takamaka locality), all the
trunks and branches (here principally Eugenia sp., Myrtaceae, Dombeya sp., Sterculiaceae, and tree ferns, Cyathea
borbonica Desv., C. excelsa Sw., C. glauca Bory, Cyatheaceae) are densely covered by epiphytes (mostly bryophytes, filmy
ferns, Peperomia sp. (Piperaceae) and orchids: mostly Bulbophyllum and Angraecoid species; and some Liliaceae such as
Cordyline mauritiana Macbride); there are a few localized terrestrial individuals (T. meifolium Bory), sometimes in open
places such as here by a trekking path; in contrast, terrestrial ferns from other families are abundant (e.g. Thelypteridaceae, Aspleniaceae). Fig. 2. Tree trunk fully covered by filmy ferns (T. tamarisciforme Jacq., Hymenophyllum hygrometricum (Poir.) Desv.) in the Bebour forest. Fig. 3. Stream in a mountain forest (Basse Vallée Crest, La Réunion, alt. ª1000 m,
photo J.-Y. Dubuisson), with mossy banks representing a typical place in which most terrestrial Trichomanes taxa are
found (here T. meifolium).
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
46
J.-Y. DUBUISSON ET AL.
Figure 4. Trichomanes borbonicum Bosch (section Lacosteopsis), medium-size epiphytic species with spreading
fronds on a tree branch (Bebour forest, La Réunion, photo
J.-Y. Dubuisson).
palaeotropical sections Crepidomanes, Crepidium,
Pleuromanes, Phlebiophyllum and Gonocormus (Morton’s subgenus Trichomanes). Hemi-epiphytic climbers belong to the pantropical section Lacosteopsis
(subgenus Trichomanes), which also contains epiphytic and epipetric species. True lianescence is
apparent only in the four species of the neotropical
section Lacostea: T. ankersii, T. pedicellatum Desv.,
T. tanaicum Hook. ex J.W.Sturm and T. tuerckheimii
H.Christ.
HABIT
AND ECOLOGY
Character states for each species are reported in the
Appendix. In Trichomanes, the rhizome is (i) short to
long-creeping or erect with short internodes (<1 cm)
and fronds mostly approximate, or (ii) long-creeping
with long to very long internodes (>1 cm) and fronds
always widely apart. Short internode stems exhibit
exceptional branching while long-creeping, with long
internode stems are always branched. The stem can
also be (i) quite thick (>1 cm), short or long-creeping,
or (ii) fine to filiform (£1 cm) and long-creeping. Short
to long creeping thick stems with short internodes
always bear numerous and robust roots (root system
RS of type I or IIa sensu Schneider). Long creeping filiform stems have few and thin roots (RS IIc) or are
rootless (RS IVa and IVb). Root-like shoots sensu
Schneider are also observed on some filiform stems.
Terrestrial species are characterized by a stout and
short unbranched rhizome fixed to the soil by numerous robust roots and bearing spirally arranged,
approximate fronds (Figs 6,10A). In addition, fronds
appear mostly erect because of a more or less rigid petiole. If the rhizome is creeping, the fronds are never
widely separated because of the relative short internodes. The phyllotaxis remains generally helical.
Epiphytic species always have branched, fine to filiform, long-creeping stems with a root system more or
less reduced or absent (except for T. cumingii C.Presl,
section Abrodictyum, which is probably related to terrestrial taxa, see above; this taxon shares with related
terrestrial species the same habit and rhizome features). The widely separated fronds with distichous
phyllotaxis are often spread on tree-trunks or
branches (see Figs 4,10B). The leaves are flattened on
the substrate in very small, simple forms such as
found for T. hildebrandtii Kuhn (section Microgonium) and are often mixed with epiphytic mosses. In
wet epipetric situations the habit is similar.
The hemi-epiphytic climbing Lacosteopsis (including T. scandens L.) can develop terrestrial stages with
long-creeping stout stems and numerous robust roots.
When climbing on a support, the long-creeping stout
stem may lack roots, at least in part, explaining the
numerous, mostly rootless herbarium specimens that
nearly always represent only trunk-borne rhizomes
(Figs 7,10C). In fact, these species are often reported
as epiphytes, but observations in situ demonstrate the
frequent presence of terrestrial parts (e.g.
T. giganteum, above). The fronds are never approximate and display a spiral or occasionally distichous
phyllotaxis, and a petiole that is more or less rigid,
hence the more or less erect and sometimes spreading
habit. These species are able to sever relations with
the soil without damage and are therefore also found
as strict epiphytes.
The Lacostea lianas have a terrestrial, perennial,
short-creeping, stout rhizome with short internodes
and numerous robust roots that are anatomically similar to those of the terrestrial species (Fig. 8; RS III).
Lacostea also grows by branching, long-creeping rootless stems with long internodes, climbing and scrambling on tree trunks (Figs 8,9,10D). In addition, the
climbing stem is thinner (ª 1 mm) than in most hemiepiphytic Lacosteopsis. The fronds are widely separated and often flattened on the support, or spreading
if the support is not wide enough (Fig. 9). Observations
in situ show that the climbing stems are sometimes not
perennial, dying after the production of spores, and
that their lengths rarely exceed 4–5 m, while the
growth of climbing Lacosteopsis appears indeterminate. The lianescent habit of Lacostea appears therefore potentially defined and limited. Unlike the hemiepiphytic Lacosteopsis, climbing stems are not capable
of losing their relationship to the ground.
All the observations are summarized in Table 2 and
Figure 10.
FROND
SIZE
The average frond size among the 193 selected species
of Trichomanes is quite variable, ranging from 0.3 cm
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ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
(T. nummularium (Bosch) C.Chr., section Didymoglossum) to 60 cm (T. aphlebioides H.Christ., section
Lacosteopsis) with a mean of 15.13 cm and a standard
deviation (SD) of 11.35 cm. Figure 11 shows the distribution of the number of species according to 40 size
47
classes, divided into epiphytic and non-epiphytic
forms. In accordance with recommendations cited in
the Material and Methods above, no statistical comparative test on non-independent objects (here = taxa)
has been performed, and thus all the observations are
Figure 5. Secondary hemi-epiphytic taxon, Trichomanes giganteum Bory, ‘epiphytic’ form climbing on a trunk in the Mare
Longue forest, La Réunion, alt. ª450 m (photo J.-Y. Dubuisson)
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
48
J.-Y. DUBUISSON ET AL.
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
only graphical. We note graphically a strong distinction between the distribution by size of epiphytic taxa
and the terrestrial ones. The average frond size of terrestrial taxa ranges from 6 cm (T. holopterum Kunze,
section Achomanes) to 55 cm (T. cristatum Kaulf., section Achomanes and T. polyanthum Hook., section
Callistopteris). Epiphytic species display a range of
average frond size from the minimum 0.3 to 25 cm
(T. acutum C.Presl, section Pleuromanes). In addition,
half of these species are less than 3 cm long. Nineteen
49
out of the 22 smallest sizes (to 1.5 cm) correspond to
species belonging to subgenus Didymoglossum (maximum size = 8 cm for T. gourlianum Grev.) while
species belonging to strict epiphytic Lacosteopsis and
sections Gonocormus, Crepidomanes, Pleuromanes,
Phlebiophyllum and Crepidium have a range of size
from 1.5 cm (T. latemarginale D.C.Eaton, section
Crepidomanes) to the maximum size of leaves (25 cm)
observed in epiphytes. The hemi-epiphytic Lacosteopsis display an average frond size ranging from 6.5 cm
(T. boschianum J.W.Sturm, in fact an epipetric temperate taxon) to the maximum of the genus (60 cm).
The four Lacostea lianas have, on average, smaller
sizes (5–8.5 cm) than hemi-epiphytes. All descriptive
statistical values are reported in Table 2.
INFERRED
EVOLUTION OF HABITATS IN
TRICHOMANES
The inferred evolution of habitats is presented in
Figure 12. There are two equally parsimonious scenarios for epiphytism: (1) all the species belonging to a
‘Hemi-epiphytic/Epiphytic’ (HE) clade may have an
epiphytic common ancestor (ACCTRAN optimization),
implying an ecological reversal in terrestrial Nesopteris (T. thysanostomum Makino); or (2) strict epiphytism may have appeared twice in the HE clade
(DELTRAN optimization). Whatever the optimization,
by convergence, epiphytism may also have appeared
in T. polypodioides. Hemi-epiphytism is restricted to
one clade (T. radicans Sw.–T. speciosum Willd.) and
may have derived from epiphytism (ACCTRAN optimization). True lianescence is here restricted to
T. ankersii.
DISCUSSION
TRICHOMANES
Figure 10. Different morphological types (gross morphology) observed in the genus Trichomanes according to ecology. (A) Terrestrial form; (B) epiphytic form; (C) hemiepiphytic climber; (D) true liana. rs = root-like shoot. Parts
are not to scale. Drawings modified from Schneider (2000).
ECOLOGY
Trichomanes and other such ferns are generally
regarded as very delicate ferns with frond lamina one
cell thick (except for few species). They lack cuticle,
differentiated epidermis and stomata, as implied by
their vernacular English name (filmy fern). The
absence of differentiated blade tissues including epidermis and a well-developed cuticle causes a dependence on environmental moisture, because no barrier
exists to prevent unregulated loss of water (e.g. Haertel, 1940). Filmy ferns are therefore strongly hygro-
Figures 6–9. Representative terrestrial and climbing Trichomanes. Fig. 6. T. meifolium Bory (section Pachychaetum,
collected in Bebour forest, La Réunion, photo J.-Y. Dubuisson), terrestrial species with short, stout stem, robust roots and
erect approximate fronds, habitus. Fig. 7. T. collariatum Bosch (section Lacosteopsis, F specimen), hemi-epiphytic climber
with long-creeping stem and widely remote fronds, habitus. Fig. 8. T. tuerckheimii H.Christ (section Lacostea, F specimen),
true liana, habitus, the arrow shows the terrestrial part with robust roots from which have developed a climbing, longcreeping stem with widely separated, horizontally orientated fronds and a second small young one without blades. Fig. 9.
T. pedicellatum Desv. (section Lacostea, French Guiana, photo N. P. Rowe), in situ, the climbing part of the true liana on
a thin tree trunk. Scale bars = 2 cm.
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50
J.-Y. DUBUISSON ET AL.
Table 2. Summarized morphological observations in relation to habitats in Trichomanes (see text for quantitative details)
Terrestrial
Epiphytic or epipetric
Hemi-epiphytic*
True lianas†
Stem thickness
Thick
Filiform
Thick
Stem internodes
Short
Long
Long
Branching
Exceptional (stem
monocaulous)
Numerous and robust
Yes
Yes
Thick in terrestrial
part and fine in
climbing stems
Short if terrestrial
or long in
climbing stems
Yes
Few slender or absent
Frond disposition
More or less
approximate, never
widely separated,
always spiral
Widely separated,
mostly distichous
Numerous and
robust at least
in terrestrial
stages and
some climbing
parts
Widely
separated,
spiral to
distichous
Frond habit
Mostly erect
Frond size (cm)
Min: 6
Max: 55
Mean: 23.09
SD‡: 9.67
Mostly spreading or
flattened on
substrate
Min: 0.3
Max: 25
Mean: 4.61
SD: 3.20
Roots
Numerous and
robust in
terrestrial stages
only, unless
absent
More or less
erect
Widely separated
in climbing stems,
spiral in
terrestrial stems
to distichous in
climbing stems
Flattened on
support
Min: 6.5
Max: 60
Mean: 32.66
SD: 12.34
Min: 5
Max: 8.5
Mean: 7.25
SD: 1.25
*this
group corresponds to hemi-epiphytic climbing Lacosteopsis (see text)
section Lacostea
‡
SD = standard deviation.
†
philous and their growth is restricted to wet and moist
places (but never aquatic). Some species, especially in
the Hymenophyllum s.l. lineage, are relatively reviving, poikilohydric, and thus able to survive short periods of desiccation (Benzing, 1990; Iwatsuki, 1990). In
general, filmy ferns do not grow in environments with
long dry seasons such as savannas (unless in gallery
riverside forests) and in more or less dry biotopes, but
they are generally found in dense and dark forests
with a relative constant high degree of humidity. However, the shady condition does not appear to be obligatory. Trichomanes meifolium (Morton’s section
Pachychaetum) in Malaysia can grow on sandstone
rocks together with Syngramma borneensis (Hook.)
J.Sm. (Pteridaceae sensu lato, pers. observ.). The rocks
are open and exposed daily to sun for some time. In the
Bebour mountain forest and in Mare Longue lowland
forest (La Réunion), the same species is usually found
in wet shady locations and in relatively open places,
and sometimes along the trekking paths (pers.
observ.). In both Malaysian and Mascarenian exam-
ples, the ferns are nevertheless mostly close to waterfalls, streams, or very wet places (average annual
rainfall in the Mascarenian locations is from 4 to 6 m
with a record of 10 m in Takamaka). Other species
belonging to Morton’s subgenera Trichomanes (especially from the Crepidomanes and Gonocormus sections) occur quite often on rocks and tree branches in
high mountain forests, sometimes in cloud forests
(personal observations). It is not accurate to describe
these conditions as perpetually shady or dark because
plants are invariably exposed to direct sunlight for a
period each day (as also observed in La Réunion
Bebour and Mare Longue forests, see previous examples). It appears that all these species share the same
environmental requirement, which is uniform water
availability (humidity) throughout the year (waterfalls, daily fog, etc.), which could be, in fact, the limiting environmental constraint for filmy ferns.
If ecological parameters of terrestrial species (fixed
to soil or in crevices) are relatively easy to delimit,
those of epiphytes are less obvious, especially their
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
Number of species
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
24
22
20
18
16
14
12
10
8
6
4
2
0
51
Epiphytes (black)
Terrestrials (white)
0
3
6
9
12 15 18 21 24 27 30 33 36 39 42 45 48 51 54 57 60
Frond size (cm)
Number of species
Hemi-epiphytic Lacosteopsis (white)
True lianas Lacostea (grey)
22
20
18
16
14
12
10
8
6
4
2
0
0
3
6
9
12 15 18 21 24 27 30 33 36 39 42 45 48 51 54 57 60
Frond size (cm)
Figure 11. Distribution of the number of species per class of average frond size (values indicate the upper limit of the
corresponding class). Top: epiphytic and terrestrial taxa; Below: hemi-epiphytic climbers and true lianas.
vertical distribution. In fact, in rainforests, the limits
of filmy fern occurrence are unclear. A thorough investigation of high canopy examples has not yet been
undertaken. The presence of Hymenophyllum has
been indirectly observed in Madagascar on high
branches of fallen trees (pers. observ.). Some epiphytic
angiosperms grow in similar places to filmy ferns, for
example some Peperomia species (Piperaceae) and
numerous orchids (such as the neotropical Pleurothallinidae: Pleurothallis, Stelis, Dracula, Masdevallia
and related taxa often grow sympatrically with
Hymenophyllaceae; personal observations). In very
wet places, most epiphytic species can become
epipetric, often near waterfalls (but rarely within), on
mossy rocks overhanging rivers or streams and on wet
cliffs. In fact, under very wet environmental conditions, rocky substrates are subject to equivalent environmental constraints as tree trunks, explaining why
epiphytic taxa are often able to become epipetric. For
example, in Venezuelan Guayana, some species are
epiphytic in cloud forests from 1600 to 2300 m, and
epipetric on very wet high plateaux named ‘tepuies’
(higher than 2300 m) overhanging the forests and on
which no trees grow at all (Smith, 1995; pers. observ.).
A similar observation has also been made for Pleurothallinidae orchids. In Malaysia, the transition from
mountain to cloud forests is not very distinct and some
species of sections Crepidomanes and Gonocormus
appear to be very opportunistic, growing as epiphytes
and/or on rocks (pers. observ.).
If epiphytic species are confined to very wet places
and mostly to the cloud forests, terrestrial forms are
more widespread. They can be found in savannas,
where they are restricted to gallery riverside forests.
The ‘opportunistic’ T. crispum is often found as terrestrial and epipetric near rivers in the savanna of
Venezuelan Guayana (Gran Sabana). This is also the
case of T. rigidum Sw. (section Pachychaetum), and for
the less widespread T. egleri P.G.Windisch (section
Achomanes; Smith, 1995; pers. observ.).
The sharing of both habitats (terrestrial and epiphytism) by a single individual, which occurs in some
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52
J.-Y. DUBUISSON ET AL.
Figure 12. Inferred evolution of habitats within the genus Trichomanes. T. tamarisciforme is observed more often as an
epiphyte on the base of tree trunks than terrestrial, but it is here coded as terrestrial because it was selected as
representing the mostly terrestrial section Pachychaetum. The phylogeny (see text) includes the sister-genus (Hymenophyllum species) and non-Hymenophyllaceae fern extra-groups. The equivocal part is terrestrial with the DELTRAN
optimization and is epiphytic with the ACCTRAN optimization. For Trichomanes taxa, Morton’s sections are indicated in
parentheses. Letters above the taxa correspond to Trichomanes Morton’s subgenera: T = Trichomanes; D = Didymoglossum;
A = Achomanes; P = Pachychaetum. HE = ‘hemi-epiphytic/epiphytic’ clade (see Dubuisson, 1997b).
Trichomanes, corresponds to hemi-epiphytism according to Benzing (1987, 1990). Some climbing species of
Trichomanes are, in fact, secondary hemi-epiphytes
sensu Benzing, beginning their growth fixed to the
soil and growing as epiphytes secondarily. By contrast, primary hemi-epiphytism sensu Benzing characterizes organisms that are first epiphytic and grow
secondarily as terrestrial by the development of very
long adventitious roots penetrating the soil. This
occurs in angiosperms such as the strangling figs
(Ficus sp., Moraceae), but has not been reported in
pteridophytes. We also defined above true lianas as
plants climbing vertically on a support (mostly a tree
trunk) and keeping an obligatory attachment to the
soil. This habitat, distinct from hemi-epiphytism as
described previously, is not restricted to woody
angiosperms, as often implied by authors focusing
their work on dicotyledonous flowering plants (see
Putz & Mooney, 1991). Our definition of the lianescent habit can be applied to all vascular plant groups,
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
including also monocotyledonous vines such as
Vanilla (Orchidaceae), and is thus understood in a
broad sense. The true lianescence habitat with a
permanent terrestrial part and a potentially nonperennial climbing one, is also therefore well
observed in Trichomanes.
TAXONOMY
AND ECOLOGY
The relative good correlation between habitat and
Morton’s infrageneric clusters needs to be evaluated
using a phylogenetic approach. Preliminary phylogenetic studies confirm the monophyly of the mostly
terrestrial subgenus Achomanes (excluding Lacostea,
Dubuisson, 1997a, 1997b; Fig. 12). Because of the
presence of several species reported occasionally as
epiphytes (mostly on the base of trunks or on fallen,
mossy logs and thus not considered as true epiphytes), subgenus Achomanes indeed shows relative
‘flexibility’ or ‘opportunism’ in habitat. The delimitation of the second, mostly terrestrial group (subgenus Pachychaetum) is less clear. Subgenus
Pachychaetum is considered as heterogeneous and
probably polyphyletic (Braithwaite, 1969, 1975;
Dubuisson, 1997a, 1997b; Fig. 12) and cannot be
defined as a possible second ‘terrestrial’ clade. Subgenus Didymoglossum appears to include only epiphytic or epipetric taxa. This pantropical group is
probably monophyletic (Dubuisson, 1997a, 1997b;
Fig. 12) and comprises species that seem the most
strongly adapted to the epiphytic habitat. The monophyly of the second, mostly epiphytic–epipetric
group including hemi-epiphytic climbers (subgenus
Trichomanes) is not retrieved and this group actually appears paraphyletic within a clade involving
the Didymoglossum group and the terrestrial section Nesopteris (Dubuisson, 1997b; Pryer et al.,
2001b; Fig. 12). This suggests a probable common
history for hemi-epiphytism and epiphytism among
the genus, as discussed later. The widespread section Lacosteopsis (subgenus Trichomanes) clusters
together epiphytic, hemi-epiphytic climbers, and few
strict epipetric taxa. Nevertheless, as Copeland
(1933) suggested, it could be divided into two subgroups:
the
‘T. radicans
group’
(including
T. scandens,
section
Trichomanes)
and
the
‘T. pyxidiferum L. group’. This dichotomy could be
validated by molecular data (Dubuisson, 1997b;
Fig. 12). In fact, the species belonging to the second
association are strict epiphytes (e.g. T. diaphanum)
while the first cluster comprises tropical hemi-epiphytic climbers and the epipetric rare temperate
species (European T. speciosum and North American
T. boschianum). Trichomanes boschianum may in
fact be a northern temperate dwarfish form of the
widespread pantropical T. radicans (A. R. Smith,
pers. comm.). Traditionally placed into the subgenus
53
Achomanes, the systematic position of Lacostea true
lianas has been debated (Dubuisson, 1996, 1997a).
New molecular data would suggest a close affinity to
the terrestrial neotropical section Davalliopsis and
its single species T. elegans Rich. (Fig. 12).
EVOLUTIONARY
HYPOTHESES
(i) Epiphytism
Epiphytism is well represented in the genus Trichomanes. At least 45% of species are epiphytic, and
this ecological type occurs mostly in two taxonomic
units (subgenera Trichomanes pro parte and Didymoglossum) which are closely related in a ‘Hemi-epiphytic/Epiphytic’ (HE) clade (Dubuisson, 1997b;
Fig. 12). All the epiphytic species share the same
habit, fine to filiform, long-creeping rhizome with long
internodes, and thin roots to rootless, which is not
exhibited by any terrestrial Trichomanes. These
characters are nevertheless also shared by
T. polypodioides (section Acarpacrium), an epiphytic
exception included in a terrestrial clade, the subgenus
Achomanes (Lellinger, 1994a, 1994b; Fig. 12). Some
other non-selected species (undoubtedly belonging to
subgenus Achomanes) are also strict epiphytes with a
filiform long-creeping stem, such as T. anadromum
Rosenst. and T. paucisorum R.C.Moran & B.Ollg (A. R.
Smith, pers. comm.). If subgenus Achomanes and epiphytic groups (subgenus Didymoglossum and subgenus Trichomanes pro parte) are not closely related as
suggested by preliminary phylogenetic studies, these
observations are in agreement with at least two independent appearances of epiphytism within the genus
Trichomanes, whatever the character evolution optimization: at least once (and perhaps twice) in the HE
clade and at least once in the subgenus Achomanes. It
may therefore imply ecological convergence in the
stem habit (filiform long-creeping stem). Some other
predominantly epiphytic species, such as T. cumingii,
some Achomanes (e.g. T. steyermarkii) and Pachychaetum (e.g. T. tamarisciforme, T. flavo-fuscum), possess
stem and/or leaf characteristics more usually associated with terrestrial species. The epiphytic habitat for
these taxa could be considered exceptional, and might
be explained by a preferential growing of the longlived gametophytic stage in an epiphytic context. The
importance of filmy ferns’ gametophyte ecology has
been investigated by Dassler & Farrar (1997) on a few
Trichomanes species and needs to be tested for other
taxa.
(ii) Climbing habit
We suggest that hemi-epiphytism may have evolved
at least once with respect to the monophyly of the
climbing Lacosteopsis, illustrated here by two repre-
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54
J.-Y. DUBUISSON ET AL.
sentative species (T. speciosum and T. radicans,
Fig. 12). This hemi-epiphytism may be closely related
to strict epiphytism because hemi-epiphytic Lacosteopsis and epiphytic taxa also appear closely related
in phylogenies (the HE clade). Furthermore, the
ACCTRAN optimization suggests that hemiepiphytism may have derived once from epiphytism.
However, true lianescence may also have evolved
once, independently from hemi-epiphytism, in the
Lacostea group closely related to terrestrial taxa in
phylogenies (Fig. 12). Differences between hemiepiphytes and true lianas are revealed by the leaf
size. The frond size distribution of hemi-epiphytic
Lacosteopsis is almost included into the distribution
corresponding to terrestrial taxa, while sizes of
Lacostea are more closely related to values measured
from epiphytes (Fig. 11). This indicates two classes of
frond size in climbers sensu lato, each one related to
one taxonomic association. Furthermore it shows
that expanded phylogenetic investigations are
needed to study precisely the distribution of the
frond size within Trichomanes. Lacosteopsis hemiepiphytism and Lacostea lianescence may not have a
common history. The shared long-creeping rhizome
with long internodes may therefore be an ecological
convergence.
(iii) Internode length and branched long-creeping stem
Filmy ferns excepted, all extant basal lineages of
leptosporangiate ferns are terrestrial. The most
basal lineage Osmundaceae (Pryer, Smith & Skog,
1995; Pryer et al., 2001a), which is sister to a clade
including filmy ferns and all other extant leptosporangiate ferns, have unbranched, often massive,
erect to trunk-like stems (Bower, 1963; Tryon &
Tryon, 1982). The next most basal fern lineage, sister to filmy ferns, includes the gleicheniaceous ferns
(Cheiropleuriaceae, Dipteridaceae, Gleicheniaceae,
Matoniaceae), which have long-creeping, branched
rhizomes. Figure 13 presents the inferred evolution
of internode length from the phylogeny used for the
evolution of habitats (see above). The ancestral condition of filmy ferns possibly related to the terrestrial habitat is therefore equivocal and may be
either plesiomorphic, unbranched rhizomes with
short internodes (DELTRAN optimization, Fig. 13,
top) or apomorphic, long-creeping branched rhizomes (ACCTRAN optimization, Fig. 13, below). We
nevertheless suggest that, at least in the Trichomanes lineage, because of the basal position of
the terrestrial taxa as sister-group of a clade
including hemi-epiphytes and epiphytes (the HE
clade), long internodes may have evolved from short
internodes, regardless of the character evolution
optimization (Fig. 13). Short internodes in Trichomanes can thus be interpreted as either a con-
served plesiomorphic feature or the result of
evolutionary reversal. By selecting the hypothesis of
hemi-epiphytism as derived from terrestrial habitat, the climbing habit seems to be accompanied
only twice (in climbing Lacosteopsis and in
Lacostea) by increase both of the internode length
and branching. In addition, we note a reversal to
short internodes in Nesopteris, probably related to
its terrestrial habitat. This scenario may be in
accordance with the hypothesis of ecological reversal in Nesopteris. The long internodes are a ‘climbing’ feature (see also Putz & Mooney, 1991). The
climbing habit is not common in pteridophytes. It
has evolved independently several times and occurs
only in few other families, such as Schizaeaceae
(e.g. Lygodium japonicum (Thunb.) Sw. and related
species), lindsaeoid ferns (Lindsaea subg. Ondoloma pro parte), oleandroid ferns (Arthropteris, Oleandra, Psammiosorus), dryopteridoid ferns (e.g.
Polybotrya),
lomarioid
ferns
(Lomariopsis,
Lomagramma, Teratophyllum, Thysanosoria), and
blechnoid ferns (e.g. Stenochlaena). In most of these
examples (including Trichomanes), the climbing
part of the plant is the long-creeping stem. In the
schizaeoid fern Lygodium the climbing is performed by a quite unusual, indeterminate growing
rachis (Bower, 1963; Tryon & Tryon, 1982: 71–73).
A long-creeping stem with long internodes also
characterizes the other non-pteridophyte climbers,
such as the extinct Palaeozoic pteridospermaphyte
lianas (Kerp & Krings, 1998) and the extant gymnosperm (Gnetum) and angiosperm vines (Putz &
Mooney, 1991). We have here a morphological convergence, allowing the plant to colonize ‘rapidly’ its
vertical support and thus to climb and, in some
cases, to be secondarily epiphytic. Lacostea lianas
have smaller fronds and finer stems than climbing
Lacosteopsis and a peculiar vining growth. Because
of absence of special hanging features (except maybe
deciduous scales?) such as spines, prickles, and tendrils, the contact and clinging of the climbing stem
of filmy ferns on the substrate is probably mostly
biomechanical and/or resulting from a scrambling
growth. In Lacostea, the flattened fronds could also
facilitate climbing growth, also explaining the relative small size of the blades. In addition, as suggested by Schneider (2000), the terrestrial part of
these true lianas must supply water to the climbing
stem. Despite the tiny shoot diameter, vascular
strands of the stem are well developed (Dubuisson,
1997a: 281), thus aiding water conduction in long
vertical axes. As reviewed by Carlquist (in Putz &
Mooney, 1991), wide vessels can contribute to
improve water conduction in long climbing stems of
vines and lianas. Vessel-like cells have been
observed in the xylem of numerous pteridophyte
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
55
Figure 13. Inferred evolution of stem internode length within the genus Trichomanes. Top: DELTRAN optimization;
below: ACCTRAN optimization. The phylogeny (see text) includes the sister-genus (Hymenophyllum taxa) and nonHymenophyllaceae fern extra-groups. For Trichomanes taxa, Morton’s sections are indicated in parentheses. HE = ‘hemiepiphytic/epiphytic’ clade (see Dubuisson, 1997b).
groups including Hymenophyllaceae (Carlquist &
Schneider, 2001). The presence of vessels, the comparison of their diameter and the possible relationships between habits and vessels need to be further
investigated among filmy ferns.
Under the assumption that strict epiphytism is the
most derived habitat, at least in the genus Trichomanes, the long internode may also be related to
the acquisition of epiphytism. In fact, short internodes
are not confined to terrestrial habitats and numerous
epiphytic angiosperms (e.g. bromeliads) and pterido-
phytes (e.g. some Aspleniaceae, some Grammitidacae,
some Polypodiaceae and some Vittariaceae) exhibit a
short, monocaulous stem and approximate blades.
However most epiphytic ferns have long-creeping rhizomes. In an epiphytic context, long-creeping rhizomes permit plants to colonize the support too. Hairy,
long-creeping stems of epiphytes are simply in contact
with the support, often mixed with mosses or overlapped in tree bark crevices. These features may have
also appeared by convergence in the mostly epiphytic
sister-lineage Hymenophyllum s.l. (Fig. 13).
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56
J.-Y. DUBUISSON ET AL.
TENDENCIES
TOWARD DWARFISM AND BRYOPHYTIC
CONVERGENCE
In Trichomanes, epiphytes are, on average, smaller
than terrestrial forms and hemi-epiphytic taxa,
and true lianas are of intermediate size (Fig. 11).
As already proposed, the terrestrial habitat may
be ancestral, from which epiphytism may have
been derived. According to this hypothesis, frond
size and root system show tendencies toward
dwarfism and simplification, which may be related
to the acquisition of epiphytism, confirming
Dubuisson (1997a) and Schneiders’ (2000) assumptions. This is also observed in the Hymenophyllum s.l. lineage.
One major tendency in epiphytes is therefore a
diminution in size, a phenomenon that reaches
extreme proportions in subgenus Didymoglossum,
which has numerous dwarf species (fronds less
than 1.5 cm long; Fig. 14). In addition, Didymoglossum exhibits pinnatifid (for the largest species such
as T. gourlianum) to simple, sometimes oval fronds
(Fig. 14), while the (on average) larger epiphytic
species of the subgenus Trichomanes always have
divided fronds, whatever their size. Didymoglossum may have developed an unexpected morphological convergence with bryophytes (especially
Hepaticae) with which they are often mixed on tree
trunks and branches. The epiphytic habitat is in
fact quite a restricting environment, particularly
because of the problem of water availability. Vascular plants can respond to these constraints in two
principal ways: (i) develop xerophytic properties for
resisting desiccation and/or storing water (e.g. bromeliads, orchids, and some polypods), or (ii) be
hygrophilous and confined to very wet places (Benzing, 1987, 1990). Because of their delicate frond
morphology, filmy ferns are essentially hygrophilous and can grow as epiphytes (and epipetrics) only
under very humid environmental conditions. It is
likely that absorption of water (here humidity) is
mostly performed by diffusion through the filmy
lamina (as in bryophytes; Hébant, 1977), less often
by rootless stems and sometimes by specialized
root-like shoots (Schneider, 2000). In addition,
reduction in size may contribute to decrease water
loss, a favourable strategy in a constraining epiphytic context. In contrast, terrestrial and climbing taxa maintain contact with the soil, and have
robust functional roots and stout and vascularized
stems supplying water to large and/or widely
spaced fronds.
Terrestrial taxa may thus have an ‘Osmundaceaelike habit’. Hemi-epiphytic climbers are characterized
by a long creeping stem with long internodes, and epiphytes have a tendency to reduce their blade size to
decrease constraints due to the water availability.
Dwarfism in epiphytic forms has appeared independently in several fern families, such as Vittariaceae
(e.g. Hecistopteris and Monogramme, the latter is
among the smallest vascular epiphytes) and Polypodiaceae (e.g. Microgramma pro parte and Lemmaphyllum), but in these groups plants have welldifferentiated epidermal layers with more or less thick
cuticles, and they are not so delicate and hygrophilous.
The ‘resemblance’ to bryophytes, including hygrophily
and reduction of main parts of the vascular plant body
(epidermis, roots), is a unique feature of filmy ferns
even though dwarfism may be more common among
vascular pteridophyte epiphytes (Bower, 1963; Tryon
& Tryon, 1982; Benzing, 1990).
Evolutionary hypotheses are summarized in
Figure 15.
EPIPHYTISM
Figure 14. Trichomanes kapplerianum J.W.Sturm (section Microgonium), dwarfish epiphytic species with filiform
rootless stem bearing simple fronds, the 1/2 French Franc
has a diameter of ª 20 mm (specimen collected in French
Guiana, photo J.-Y. Dubuisson).
AND COLONIALITY
One principal consequence of the stem branching
in hemi-epiphytic and epiphytic forms is the multiplication of shoot apices. Terrestrial individuals,
because of their monocaulous growth, have a single apex which in general gives rise to a small,
living stem that is unable to cover large areas of
the substrate. They are thus not well placed to
occupy a broad area. The plants are also more
sensitive to herbivory, and the destruction of the
apex is generally fatal. On the other hand, epiphytes with many apical meristems can form
extensive colonies. Individuals are also less sensitive to destruction through herbivory or fungal
parasites. In fact, the loss of some apices is rarely
prejudicial because growth will continue from the
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
57
Figure 15. Different habits observed among Trichomanes according to ecology (vertical) and frond size (horizontal) and
proposed evolutionary transitions. (1) Terrestrial taxa (mostly subgenera Achomanes and Pachychaetum). (2) Hemiepiphytic climbers (section Lacosteopsis in part + T. scandens L.). (3) True lianas (section Lacostea). (4) Small epiphytes
(epiphytic Lacosteopsis + other sections of the subgenus Trichomanes and some species of the subgenus Didymoglossum
+ few Achomanes species), rs = root-like shoot (see text). (5) Dwarfish reduced epiphytes (most species of the subgenus
Didymoglossum). We propose as a probable evolution: (i) one ancestral terrestrial habit (1); (ii) increase of the stem
internode length in hemi-epiphytes, lianas and epiphytes (2, 3, 4) and (iii) tendencies toward reduction in size in epiphytes
(4 + 5). See text for details. Parts are not to scale. Drawings modified from Schneider (2000).
remaining shoots. The tendency to form colonies
seems to be most prevalent in the smaller-leaved
forms. In this case, because of the very reduced
stem anatomy and the absorption of water principally through the lamina, each individual may be
considered as a ‘frond colony’. Each frond may
grow more or less independently from the others,
and its growth may depend on very local microenvironmental conditions (especially in the Gonocormus section and the very minute Crepidomanes
and Didymoglossum). This could explain the high
polymorphism in frond form and size observed at
the infra-individual level or within a colony. The
tendency to form colonies in a hygrophilous epiphytic context favours a convergence on bryophyte morphologies (i.e. minute blades). Longcreeping branched stems facilitate colony formation. It has facilitated the acquisition of hemi-epiphytism, and it has been fully exploited by
epiphytes. The strategy of long-creeping, branched
colonizing stems is also shown in evolutionaryclose terrestrial gleicheniaceous ferns, but it
occurs mainly in ‘modern’ (i.e. more recent) families among the polypodioids. In these latter
groups, plants are nearly always colonial (Polypodiaceae sensu stricto excluding Grammitidaceae)
but some are not (e.g. Dryopteris sensu lato, terrestrial genus, Dryopteridaceae). Both strategies
are thus found in all lineages of leptosporangiate
ferns. Hymenophyllaceae, and particularly the
genus Trichomanes, appear therefore as a spectacular group of very diversified ferns, which has
developed numerous habits and strategies, and
especially a ‘bryophytic colonial strategy’.
CONCLUSIONS
This first review of the ecological diversity of the
genus Trichomanes clarifies the existence of three
principal ecological types: (i) terrestrial, (ii) climbers,
and (iii) epiphyte. In addition, this study allows us to
divide climbers into hemi-epiphytic forms and true
lianas, the latter distinguishable from the former by
their particular limited climbing growth. The principal results are the observed relationships of ecology to
different habits.
Increase of internode length related to the climbing habit is not an unexpected result. This character has probably appeared and contributed to the
climbing habit within the vascular plants several
times. On the other hand, the tendencies toward
dwarfism combined with a hygrophilous biology in
Trichomanes are very rare in vascular plant epiphytes (Benzing, 1990). Dwarfism also occurs in
numerous epiphytic orchids, but it is mostly accompanied by xerophytic features, such as roots with a
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
58
J.-Y. DUBUISSON ET AL.
developed velamen, coriaceous blades and/or
pseudobulbs (Benzing & Ott, 1981; Dressler, 1993).
The ecological and evolutionary hypotheses developed on Trichomanes can be further tested with a
more complete phylogeny of the genus. In addition,
studies need to be extended to the sister-genus
Hymenophyllum s.l.
ACKNOWLEDGEMENTS
Funding for this work was provided by the ‘Institut
d’Ecologie Fondamentale et Appliquée’ (IFR CNRS
101), Université Pierre et Marie Curie, Paris and the
‘Laboratoire de Fonctionnement et Evolution des
Systèmes Ecologiques’ (UMR CNRS 7625), Université
Pierre et Marie Curie, Paris. We are grateful to Isabelle Dajoz (UMR CNRS 7625), Thierry Pailler and
Dominique Strasberg (Laboratoire de Botanique, Université de La Réunion), Edmond Grangaud (La
Réunion), Rose Hébant-Mauri (Université Montpellier
2), Jérôme Munzinger (MNHN, Paris), Alan Smith
(UC Herbarium, USA), Robbin Moran (NYBG, USA)
and Kunio Iwatsuki (University on Air, Chiba, Japan)
for their helpful information and discussion on the
ecology of filmy ferns. The authors would also like to
thank the staff of the different visited herbarium collections (P, F, UC, MPU, REU) who kindly helped us
during the visits, Christine Müller-Graf and JeanChristophe (Hans) Etienne for their pertinent comments on the manuscript and an anonymous reviewer
for his quite useful corrections.
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J.-Y. DUBUISSON ET AL.
APPENDIX
List of the 193 selected species with Morton’s corresponding section, ecology, average frond size (in cm) and morphological
observations. Ecology: E = strictly epiphytic and/or epipetric (exceptionally terrestrial); T = strictly terrestrial, occasionally
epipetric or epiphytic (T/E = mostly epiphytic and occasionally terrestrial); H = hemi-epiphytic climber; L = true liana.
Stem thickness: f = filiform to filamentous (<1 mm); F = fine (ª 1 mm); S = stout (>1 mm). IN (internode length): L = long
(>1 cm); s = short (<1 cm). Branching (of the stem): Y = usual to numerous; N = exceptional. Note: taxa are ranked by
ecology and size.
Taxa
Morton’s sections
Ecology
T. nummularium (Bosch) C.Chr.
T. motleyi Bosch
T. wallii Thwaites
T. angustifrons (Fée) Wess.Boer
T. liberiense Copel.
T. pinnatinervium Jenman
T. ovale (E.Fourn.) Wess.Boer
T. exiguum (Bedd.) Baker
T. ballardianum Alston
T. rhipidophyllum Sloss.
T. petersii A.Gray
T. bimarginatum Bosch
T. punctatum Poir. in Lam.
T. cultratum Baker
T. kapplerianum J.W.Sturm
T. craspedoneurum Copel.
T. latemarginale D.C.Eaton
T. nymanii H.Christ
T. pervenulosum Alderw.
T. henzaianum Parish
T. chamaedrys Taton
T. tahitense Nadeaud
T. curtii Rosenst.
T. cuspidatum Willd.
T. megistostomum Copel.
T. montanum Hook.*
T. chevalieri H.Christ
T. clarenceanum F.Ballard
T. hymenoides Hedw.
T. mindorense H.Christ
T. vieillardii Bosch
T. omphalodes (Vieill.) C.Chr.
T. rupicola Racib.
T. sublimbatum K.Müll.
T. ruwenzoriense Taton
T. ekmanii Wess.Boer
T. pusillum Sw.
T. godmanii Hook. in Baker
T. hildebrandtii Kuhn
T. mettenii C.Chr.
T. saxifragoides C.Presl
T. mannii Hook.
T. minutum Blume
T. intramarginale Hook. & Grev.
T. africanum H.Christ
T. lineolatum (Bosch) Hook.
T. parvum Copel.
Didymoglossum
Microgonium
Didymoglossum
Didymoglossum
Didymoglossum
Didymoglossum
Didymoglossum
Didymoglossum
Microgonium
Didymoglossum
Didymoglossum
Microgonium
Didymoglossum
Microgonium
Microgonium
Microgonium
Crepidomanes
Crepidomanes
Crepidomanes
Microgonium
Microgonium
Microgonium
Didymoglossum
Microgonium
Crepidomanes
Didymoglossum
Lacosteopsis
Crepidomanes
Didymoglossum
Microgonium
Crepidium
Microgonium
Crepidomanes
Microgonium
Gonocormus
Microgonium
Didymoglossum
Microgonium
Microgonium
Lacosteopsis
Gonocormus
Gonocormus
Gonocormus
Crepidomanes
Lacosteopsis
Didymoglossum
Lacosteopsis
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
Size
0.3
0.35
0.5
0.6
0.6
0.65
0.75
0.75
0.8
1
1.2
1.25
1.25
1.25
1.25
1.5
1.5
1.5
1.5
1.5
1.5
1.5
1.6
1.75
1.75
1.75
2
2
2
2
2
2
2
2
2
2.25
2.25
2.3
2.5
2.5
2.5
2.75
3
3
3.5
3.5
3.5
Stem thickness
IN
Branching
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
61
APPENDIX Continued
Taxa
Morton’s sections
Ecology
Size
Stem thickness
IN
Branching
T. werneri Rosenst.
T. assimile Mett. in Kuhn
T. bipunctatum Poir.
T. diaphanum Humb., Bonpl. & Kunth
T. erosum Willd.
T. krausii Hook. & Grev.
T. membranaceum L.
T. schmidtianum Zenker
T. hookeri C.Presl
T. reptans Sw.
T. latealatum (Bosch) H.Christ
T. melanopus Baker
T. makinoi C.Chr.
T. rothertii Alderw.
T. gracillimum Copel.
T. humile G.Forst.
T. alagense H.Christ
T. draytonianum Brack.
T. stenosiphon H.Christ
T. christii Copel.
T. venosum Brown
T. venulosum (Rosenst.) Copel.
T. endlicherianum C.Presl
T. hymenophylloides Bosch
T. gourlianum Grev.
T. frappieri Cordem.
T. melanotrichum Schlecht.
T. teysmannii Bosch
T. pyxidiferum L.
T. borbonicum Bosch
T. fallax H.Christ
T. inopinatum (Pic.Serm.) J.E.Burrows
T. colensoi Hook.
T. angustatum Carmich.
T. latifrons Bosch
T. polypodioides L.
T. brevipes (C.Presl) Baker
T. cumingii C.Presl
T. capillaceum L.
T. pallidum Blume
T. acutum C.Presl.
T. boschianum J.W.Sturm
T. rupestre (Raddi) Bosch
T. birmanicum Bedd.
T. kunzeanum Hook.
T. speciosum Willd.
T. johnstonense Bailey
T. cyrthoteca Hildebr.
T. collariatum Bosch
T. auriculatum Blume
T. scandens L.
T. radicans Sw.
T. davallioides Gaudich.
Crepidium
Gonocormus
Crepidomanes
Lacosteopsis
Microgonium
Didymoglossum
Lecanium
Lacosteopsis
Microgonium
Didymoglossum
Crepidomanes
Didymoglossum
Crepidomanes
Crepidomanes
Crepidium
Crepidium
Gonocormus
Lacosteopsis
Lacosteopsis
Crepidomanes
Phlebiophyllum
Crepidomanes
Crepidium
Lacosteopsis
Didymoglossum
Lacosteopsis
Lacosteopsis
Gonocormus
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Acarpacrium
Crepidomanes
Abrodictyum
Lacosteopsis
Pleuromanes
Pleuromanes
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Trichomanes
Lacosteopsis
Lacosteopsis
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
H†
H
H
H
H†
H
H
H
H
H
H
H
3.5
4
4
4
4
4
4
4
4.5
4.5
4.5
5
5
5
5.5
5.5
5.5
6
6
7
7
7.5
7.5
7.8
8
8.75
9
9
9.25
10
10
10.5
10.5
11
12
12
12
13
14
15
25
6.5
15
18
20
20
21
30
32
35
35
40
40
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
f
S
f
F
F
F
F
S
S
S
S
S
S
S
S
S
S
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
s
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
N
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
62
J.-Y. DUBUISSON ET AL.
APPENDIX Continued
Taxa
Morton’s sections
Ecology
Size
Stem thickness
IN
Branching
T. giganteum Bory
T. maximum Blume
T. superbum Backh.
T. aphlebioides H.Christ
T. tuerckheimii H.Christ
T. tanaicum Hook. ex J.W.Sturm
T. ankersii C.Parker
T. pedicellatum Desv.
T. holopterum Kunze
T. mougeotii Bosch
T. bicorne Hook.
T. kingii Copel.
T. botryoides Kaulf.
T. ianum Lellinger
T. macilentum Bosch
T. arbuscula Desv.
T. parviflorum Poir.‡
T. roraimense Jenm.
T. anomalum Maxon & C.V.Morton in Maguire
T. egleri P.G.Windisch
T. jenmanii Lellinger
T. acrosorum Copel.
T. tereticaulum Ching
T. boryanum Kunze
T. humboldtii (Bosch) Lellinger
T. diversifrons (Bory) Mett. ex Sadeb.
T. trollii Bergdolt
T. hostmannianum (Klotzsch) Kunze
T. galeottii E.Fourn.
T. vandenboschii P.G.Windisch
T. extravagans Copel.
T. setaceum Bosch
T. angustimarginatum Bonap.
T. currani Weath.
T. osmundoides DC.
T. guidoi P.G.Windisch
T. crinitum Sw.
T. crispum L.
T. guineense Afzel. ex Sw.
T. laetum Bosch
T. asa-grayi Bosch
T. bancroftii Hook & Grev.
T. vittaria DC. ex Poir.
T. strictum Menzies
T. alatum Sw.
T. javanicum Blume
T. obscurum Blume
T. pachyphlebium Chr.
T. singaporianum (Bosch) Alderw.
T. sumatranum Alderw.
T. gemmatum J.Sm.
T. martiusii C.Presl
T. atrovirens (C.Presl) Kunze
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacosteopsis
Lacostea
Lacostea
Lacostea
Lacostea
Achomanes
Feea
Trigonophyllum
Cephalomanes
Feea
Pachychaetum
Trigonophyllum
Trigonophyllum
Pachychaetum
Achomanes
Achomanes
Achomanes
Neurophyllum
Cephalomanes
Pachychaetum
Cephalomanes
Homeotes
Feea
Feea
Odontomanes
Achomanes
Achomanes
Pachychaetum
Pachychaetum
Pachychaetum
Acarpacrium
Feea
Achomanes
Ragatelus
Achomanes
Pachychaetum
Pachychaetum
Pachychaetum
Trigonophyllum
Neurophyllum
Pachychaetum
Acarpacrium
Cephalomanes
Pachychaetum
Pachychaetum
Cephalomanes
Cephalomanes
Pachychaetum
Achomanes
Cephalomanes
H
H
H
H
L
L
L
L
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
50
50
50
60
5
7
8.5
8.5
6
7
7.5
8
8.5
8.5
8.5
9
9
9.5
10
10
10
10
10
10
12
12
12
13
15
15
15
15
16
16
16
16
18
18
18
18
18
19
19
19
20
20
20
20
20
20
20
21
22
S
S
S
S
S/F
S/F
S/F
S/F
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
L
s
L
L
L
L
L
L
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
Y
Y
Y
Y
Y
Y
Y
Y
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63
ECOLOGICAL DIVERSITY IN TRICHOMANES (HYMENOPHYLLACEAE)
63
APPENDIX Continued
Taxa
Morton’s sections
Ecology
Size
Stem thickness
IN
Branching
T. caliginum Lellinger
T. boivini Bosch
T. crispiforme Alston
T. longicollum Bosch.
T. rigidum Sw.
T. accedens C.Presl.
T. cupressoides Desv.
T. meifolium Bory
T. pellucens Kunze
T. thysanostomum Makino
T. elongatum A.Cunn.
T. madagascariense T. Moore
T. asplenioides C.Presl
T. densinervium Copel.
T. dentatum Bosch
T. baldwinii D.C.Eaton
T. batrachoglossum Copel.
T. trigonum Desv.
T. fimbriatum Backh. ex T.Moore
T. compactum Alderw.
T. schlechteri Brause
T. intermedium Bosch
T. apiifolium C.Presl
T. crassum Copel.
T. plumosum Kunze
T. robustum E. Fourn.
T. pinnatum Hedw.
T. elegans Rich.
T. grande Copel.
T. lambertianum Hook.
T. blepharistomum Copel.
T. cristatum Kaulf.
T. polyanthum Hook.
T. cellulosum Klotzsch
T. caudatum Brack.
T. flavo-fuscum Bosch
T. steyermarkii P.G.Windisch & A.R.Smith
T. tamarisciforme Jacq.
T. lucens Sw.
T. dactylites Sodiro
Acarpacrium
Pachychaetum
Achomanes
Pachychaetum
Pachychaetum
Achomanes
Pachychaetum
Pachychaetum
Achomanes
Nesopteris
Pachychaetum
Cephalomanes
Cephalomanes
Cephalomanes
Pachychaetum
Callistopteris
Pachychaetum
Acarpacrium
Acarpacrium
Pachychaetum
Pachychaetum
Nesopteris
Callistopteris
Cephalomanes
Achomanes
Achomanes
Neurophyllum
Davalliopsis
Nesopteris
Achomanes
Nesopteris
Achomanes
Callistopteris
Pachychaetum
Pachychaetum
Pachychaetum
Achomanes
Pachychaetum
Achomanes
Achomanes
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T/E
T/E
T/E
T/E
T/E
T/E
T/E
22
23
23
23
23
25
25
25
25
25
25
26
28
28
30
30
30
30
35
35
35
37
40
40
40
45
45
50
50
50
50
55
55
8.5
23
25
25
30
39
40
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
s
L
s
s
s
s
s
s
s
s
L
L
s
s
s
s
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
*A
heterotypic synonym of neotropical T. reptans, the present taxon corresponds to Malagasian specimens named
T. montanum by Tardieu-Blot (1951)
†Mostly temperate epipetric taxa
‡
Close to T. meifolium and probably a small form of this species (pers. observ. on P specimens). As observed in the field (La
Réunion Mare Longue and Bebour forests), T. meifolium appears greatly polymorphic even at the population level. The
splitting into different taxa is debatable as it has been made only on herbarium specimens (e.g. Tardieu-Blot’s work at P)
on the basis of the segment width and pinna orientation (planar or more or less horizontal). A taxonomic revision is
therefore needed.
© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63