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 © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 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 © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 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. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 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 © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 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- © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 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). © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 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. REFERENCES Axsmith BJ, Krings M, Taylor TN. 2001. A filmy fern from the upper Triassic of North Carolina (USA). American Journal of Botany 88: 1558–1567. Baker CA, Posthumuis O. 1939. Varenfora voor Java. Overzicht der op Java vookomende varens en varenchtig, hare verspeiding, oekologie en toepassingen. Buitenzorg: Archiepl Druckerij. Benzing DH. 1987. Vascular epiphytism: taxonomic participation and adaptive diversity. Annals of the Missouri Botanical Garden 74: 183–204. Benzing DH. 1990. Vascular epiphytes. Cambridge: Cambridge University Press. Benzing DH, Ott DW. 1981. Vegetative reduction in epiphytic Bromeliaceae and Orchidaceae: its origin and significance. 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The New World species of Trichomanes sect. Didymoglossum and Microgonium. Acta Botanica Neerlandica 11: 277–330. Windisch PG. 1992. Trichomanes crispum L. (Pteridophyta, Hymenophyllaceae) and allied species. Bradea 6: 78–117. Yoroi R, Iwatsuki K. 1977. An observation on the variation of Trichomanes minutum and allied species. Acta Phytotaxonomica et Geobotanica 28: 152–159. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 41–63 60 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