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Botanical Journal of the Linnean Society, 2013, 173, 573–593. With 7 figures
Epiphytism, anatomy and regressive evolution in
trichomanoid filmy ferns (Hymenophyllaceae)
JEAN-YVES DUBUISSON1*, SOPHIE BARY1,2, ATSUSHI EBIHARA3,
EUGÉNIE CARNERO-DIAZ4, ELODIE BOUCHERON-DUBUISSON4 and
SABINE HENNEQUIN1
1
Université Pierre et Marie Curie, UMR 7207 CNRS-MNHN-UPMC, Centre de Recherche sur la
Paléobidoversité et les Paléoenvironnements, MNHN, Bâtiment de Géologie, CP48, 57 rue Cuvier,
F-75005 Paris, France
2
Département Systématique et Evolution, MNHN, 57 rue Cuvier, F-75005 Paris, France
3
Department of Botany, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba 305-0005,
Japan
4
Université Pierre et Marie Curie, UR5 Physiologie Cellulaire et Moléculaire des Plantes, Casier 156,
9 Quai St Bernard, F-75005 Paris, France
Received 17 December 2012; revised 28 June 2013; accepted for publication 13 August 2013
The few studies on the evolution of epiphytism in ferns have mostly focused on xerophytic and humus-collecting
strategies, neglecting hygrophytes that are abundant in rainforests, such as the trichomanoids (Hymenophyllaceae). Using a phylogenetic approach, we studied the acquisition of epiphytism in this lineage, with the aim of
identifying ecological anatomical adaptations and verifying the regressive epiphytic ‘bryophyte-like’ strategy
previously suggested for the group. Inferred evolution of anatomy and morphology, regression and ecology (more
particularly colonial epiphytism) were analysed and compared using a maximum likelihood approach. Regressive
evolution of anatomy and morphology is revealed in the three clades of colonial epiphytes, probably linked to the
selection of water acquisition by blades rather than by regressed roots. However, the ‘bryophyte-like’ strategy is
restricted to some taxa (especially Didymoglossum). Furthermore, a relationship is revealed between large
metaxylem and climbing habit. Diversification of colonial epiphytes (and some individual epiphytes) and hemiepiphytism would have occurred in the upper Cretaceous and Tertiary, in accordance with the timing of
diversification of modern ferns and the evolution of epiphytism in other fern families in the first angiospermdominated forests. This was here performed by selecting hygrophilous strategies that are unique in vascular
plants. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593.
ADDITIONAL KEYWORDS: bryophytes – comparative methods − ecology − phylogeny – Trichomanes.
INTRODUCTION
Epiphytes, including ferns, lycophytes and mosses,
are one of the main components of rainforest diversity
at the pantropical level, especially in montane cloud
forests, in which epiphyte diversity is highest (Gentry
& Dodson, 1987). However, studies on epiphytism and
related strategies in ferns are relatively scarce in
comparison with angiosperms (Benzing, 1990;
*Corresponding author. E-mail: [email protected]
Dubuisson, Hennequin & Schneider, 2009). With 29%
of the total number of fern species occupying this
habitat, ferns are nevertheless the second group of
vascular plants in terms of epiphyte diversity, after
monocots with 31% epiphytic species, mostly Orchidaceae. In addition, most ferns and lycophytes are
more diverse than orchids in many palaeotropical
rainforests, forming 36–72% of the total epiphytic
diversity (e.g. in Australia, New Zealand and the
Micronesian islands; Oliver, 1930; Hosokawa, 1943;
Wallace, 1981). Obligate epiphytic ferns are subjected
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
573
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J.-Y. DUBUISSON ET AL.
to the same environmental constraints as seed plants
and should also be naturally selectively adapted to
this habitat. The epiphytic habitat is quite constraining; the lack of relation to the soil implies a high risk
of desiccation and the obligatory capacity to use rainwater or air moisture quickly and directly and/or to
limit or compensate the water loss from evaporation.
Like the majority of epiphytic seed plants, strict epiphytic ferns, especially those belonging to Polypodiales (sensu Smith et al., 2006; Christenhusz, Zhang &
Schneider, 2011), generally display xeromorphic adaptive traits, enabling them to avoid and/or endure
drought (Schneider et al., 2004a; see reviews by
Dubuisson et al., 2009; Hietz, 2010). Other ferns
display growth habits allowing them to accumulate
humus and to entrap nutrients and water. These are
mesophile humus collectors, illustrated by the wellknown bird’s nest fern (Asplenium nidus L., Aspleniaceae), the drynarioid ferns [species of Drynaria
(Bory) J.Sm., Polypodiaceae; Janssen & Schneider,
2005] and the staghorn ferns (species of Platycerium
Desv., Polypodiaceae; Kreier & Schneider, 2006). The
humus-collecting strategy is sometimes combined
with a mutualistic interaction with ants, as in Microgramma bifrons (Hook.) Lellinger (Polypodiaceae) and
relatives (e.g. Lecanopteris Reinw. genus, Polypodiaceae; Haufler et al., 2003). The final type of epiphytic
fern, hygrophilous epiphytes or hygrophytes, lacks
both xerophytic traits and humus-collector strategies
(Dubuisson et al., 2009). Consequently, these epiphytes are restricted to humid environments.
As recently reviewed by Dubuisson et al. (2009,
2011), most members of Hymenophyllaceae, or filmy
ferns, are obligatory hygrophytes. They constitute a
pertinent group in which to investigate adaptive
strategies related to hygrophilous epiphytism in
ferns. Despite the strong limitations or constraints
related to the epiphytic habit, members of Hymenophyllaceae have succeeded in diversifying under
such constraints, with > 60% epiphytic species distributed worldwide on most continents and numerous oceanic islands. Several species of filmy ferns are
desiccation tolerant and have the capacity to survive
a period of dehydration and revive after rehydration,
similar to some species of epiphytic Polypodiaceae.
However, the dehydration is limited to a short period
(a few hours) (Hietz & Briones, 1998, 2001; Nitta,
2006) and is supposedly more problematic in an epiphytic context because plants do not have the possibility to absorb water directly from the soil to
compensate for dehydration. A regressive evolution
in morphology has been suggested previously for epiphytic trichomanoids, one of the two major clades in
the family and the most morphologically and ecologically diversified (Schneider, 2000; Dubuisson et al.,
2003). Trichomanoids here refer to the distinct clade
that traditionally corresponds to the genus Trichomanes L. s.l. and currently includes eight genera
(Abrodictyum C.Presl, Callistopteris Copel., Cephalomanes C.Presl, Crepidomanes C.Presl, Didymoglossum Desv., Polyphlebium Copel., Trichomanes and
Vandenboschia Copel.; Ebihara et al., 2006). The
regressive evolution in trichomanoids would illustrate tendencies towards a ‘bryophyte-like’ strategy,
allowing filmy ferns to reduce their requirements in
a constraining habitat. Recent phylogenetic and comparative analyses have revealed that regressive evolution in trichomanoids also concerns anatomy
(Dubuisson et al., 2011). The anatomical regression,
illustrated by the acquisition of subcollateral and
collateral types and related to reductions in stem
and stele size, was observed in three groups embedded in a clade clustering hemi-epiphytic and epiphytic taxa, each involving only colonial epiphytes
(i.e. individuals having the ability to colonize a broad
surface of substrate). Furthermore, Dubuisson et al.
(2011) have shown that not all epiphytes display
morphological and anatomical regression, especially
when non-colonial (i.e. individuals that do not have
the ability to colonize a broad surface of substrate).
Further phylogenetic comparative analyses are thus
needed to test the relationships between habit (here
hygrophilous epiphytism) and morphological and
anatomical regression.
The present study is analogous to and derived from
a previous study (Dubuisson et al., 2011). The aims of
this study are to infer the evolution of the ecology and
related morphological and anatomical changes in
trichomanoids, relying on an expanded molecular
phylogenetic analysis representing morphological,
ecological and geographical variability in the lineage,
and on adequate statistical tests. By completing an
existing dataset with additional anatomical and ecological data, we statistically test potential relationships among selected characters and between
characters and ecology, with the aim of proposing
hypotheses on adaptive strategies that have enabled
filmy ferns to colonize the epiphytic habitat of rainforests and to verify the ‘bryophyte-like’ strategy suggested previously.
MATERIAL AND METHODS
TAXONOMIC SAMPLING
Here, we follow the strategy selected in the previous
study (Dubuisson et al., 2011) with 50 trichomanoid
species representative of the morphological, anatomical and ecological variability of the lineage and of its
global geographical distribution. The selected species
are listed in Table 1 with details of their ecology,
growth forms and geographical distribution.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
E
E
E
E
E
E
P
IO
A
A
NT
P
IO
A
A
IO+A
IO
AF+IO
A
PT
A
A
A
IO
NT
Abrodictyum
Pachychaetum
Abrodictyum
Pachychaetum
Pachychaetum
Abrodictyum
Pachychaetum
Abrodictyum
Pachychaetum
–
–
Crepidomanes
Crepidomanes
Crepidomanes
Crepidomanes
Crepidomanes
Nesopteris
Nesopteris
Nesopteris
Microgonium
Microgonium
Didymoglossum A
Didymoglossum NT
Didymoglossum IO
Didymoglossum NT
Didymoglossum NT
Abrodictyum caudatum (Brack.) Ebihara & K.Iwats.
Abrodictyum elongatum (A.Cunn.) Ebihara &
K.Iwats.
Abrodictyum flavofuscum (Bosch) Ebihara & K.Iwats.
Abrodictyum meifolium (Bory ex Willd.) Ebihara &
K.Iwats.
Abrodictyum obscurum (Blume) Ebihara & K.Iwats.
Abrodictyum pluma (Hook.) Ebihara & K.Iwats.
Abrodictyum rigidum (Sw.) Ebihara & Dubuisson
Abrodictyum strictum (Menzies ex Hook. & Grev.)
Ebihara & K.Iwats.
Abrodictyum tamarisciforme (Jacq.) Ebihara &
Dubuisson
Callistopteris apiifolia (C.Presl) Copel.
Cephalomanes javanicum (Blume) C.Presl
Crepidomanes bipunctatum (Poir.) Copel.
Crepidomanes cf. bonapartei (C.Chr.) J.P.Roux
Crepidomanes fallax (H.Christ) Ebihara &
Dubuisson
Crepidomanes latealatum (Bosch) Copel.
Crepidomanes minutum (Blume) K.Iwats.
Crepidomanes aphlebioides (H.Christ) I.M.Turner
Crepidomanes intermedium (Bosch) Ebihara &
K.Iwats.
Crepidomanes thysanostomum (Makino) Ebihara &
K.Iwats.
Didymoglossum cuspidatum (Willd.) Ebihara &
Dubuisson
Didymoglossum ekmanii (Wess. Boer) Ebihara &
Dubuisson
Didymoglossum exiguum (Bedd.) Copel.
Didymoglossum gourlianum (Grev. ex J.Sm.) Pic.
Serm.
Didymoglossum hildebrandtii (Kuhn) Ebihara &
Dubuisson
Didymoglossum krausii (Hook. & Grev.) C.Presl
Didymoglossum membraceum (L.) Vareschi
E
T
E
E
HE
T
T
T
E
E
E
E
T
T
T
T
CE
T
CE
T
P
P
Subgenus
Taxon
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
C
C
C
C
C
C
C
I
C
C
C
I
I
I
C
C
C
I
I
I
I
I
I
I
I
I
D
D
D
D
M
D
D
L
D
D
L
L
L
L
D
D
M
L
L
L
L
L
L
L
L
L
R
R
R
R
R
R
R
D
R
R
D
D
D
D
R
R
R
D
D
D
D
D
D
D
D
D
Rg***
C-Rg
C
Rg***
Rg***
Rg***
Rg***
M
SC
Rg**
M
M
M
M
SC
SC to Rg
SC to Rg
M
M
M
M
M
M
M
M
M
Growth Blade
Root
Stele
Distribution Ecology form
length* system type
S
S
S
S
S
S
S
L
S
S
L
L
L
L
S
S
S
L
L
L
L
L
L
L
L
L
14.54
7.04
17.93
18.74
8.75
7.26
8.64
28.68
15.28
8.33
90.95
26.33
29.00
20.69
9.54
10.31
14.45
34.18
38.41
24.06
21.25
22.70
58.17
28.66
27.57
31.27
Metaxylem
Stele
diameter
diameter* (μm)
Table 1. List of selected taxa with geographical distribution, ecology, growth form, qualitative and quantitative characters of interest for morphology and anatomy
(see text)
EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
575
NT
P
NT
P
NT
NT
NT
NT
NT
NT
NT
NT
NT
NT
NT
NT
NT
Hawaii
IO
A
NT
NT
E
–
–
–
–
–
Trichomanes
Trichomanes
Trichomanes
Trichomanes
Feea
Trichomanes
Trichomanes
Trichomanes
Trichomanes
Trichomanes
Davalliopsis
Lacostea
Lacostea
Vandenboschia
Vandenboschia
Vandenboschia
Vandenboschia
Lacosteopsis
Vandenboschia
Polyphlebium borbonicum (Bosch) Ebihara &
Dubuisson
Polyphlebium capillaceum (L.) Ebihara & Dubuisson
Polyphlebium endlicherianum (C.Presl) Ebihara &
K.Iwats.
Polyphlebium hymenophylloides (Bosch) Ebihara &
Dubuisson
Polyphlebium venosum (R.Br.) Copel.
Trichomanes alatum Sw.
Trichomanes arbuscula Desv.
Trichomanes crispum L.
Trichomanes holopterum Kunze
Trichomanes osmundoides Poir.
Trichomanes pinnatum Hedw.
Trichomanes polypodioides L.
Trichomanes robustum E.Fourn.
Trichomanes scandens L.
Trichomanes trigonum Desv.
Trichomanes elegans Rich.
Trichomanes ankersii C.Parker ex Hook.
Trichomanes pedicellatum Desv.
Vandenboschia davallioides (Gaudich.) Copel.
Vandenboschia gigantea (Bory ex Willd.) Ebihara &
Dubuisson
Vandenboschia maxima (Blume) Copel.
Vandenboschia radicans (Sw.) Copel.
Vandenboschia rupestris (Raddi) Ebihara & K.Iwats.
Vandenboschia speciosa (Willd.) G.Kunkel
T
HE
HE
HE
E
E
T
E
T
T
T
E
T
HE
T
T
HE
HE
HE
HE
E
E
E
E
I
C
C
C
C
I
I
I
I
I
I
C
I
C
I
I
C
C
C
C
C
C
C
C
L
L
L
L
M
L
M
L
M
L
L
M
L
L
L
L
M
M
L
L
M
L
M
M
D
D
D
D
Rg
D
D
D
D
D
D
Rg
D
D
D
D
D
D
D
D
Rg
Rg
Rg
Rg
S
S
S
M
Re
Re
Re
Rg**
M
M
M
M
M
M
M
M
M
M
M
M
M
Re
Re
L
L
L
L
S
L
L
L
L
L
L
L
L
L
L
L
L
L
L
L
SC to Rg S
SC
Rg**
SC
37.60
54.19
50.91
44.20
12.52
24.25
32.48
34.99
23.64
21.63
26.30
20.81
33.43
46.07
38.66
40.21
34.14
68.55
85.74
44.09
6.37
14.03
8.99
10.58
Metaxylem
Stele
diameter
diameter* (μm)
Distribution: A, Asia and sometimes to Pacific; AF, tropical Africa; E, Europe; IO, Indian Ocean; NT, Neotropics; P, restricted to Australasia and/or Pacific islands;
PT, Palaeotropics.
Ecology: CE, climbing epiphyte; E, epiphyte; HE, hemi-epiphyte; T, terrestrial.
Growth form: C, colonial; I, individual (see text).
Blade length: D, small to dwarf; L, large; M, medium; (see text, *values are reported in Dubuisson et al., 2011).
Root system: D, developed and robust; R, rootless; Rg, present and regressed.
Stele type: C, collateral; M, massive; Re, reduced; Rg, regressed (**of the subcollateral type; ***of the collateral type); SC, subcollateral.
Stele diameter: L, large; S, small (see text, *values are reported in Dubuisson et al., 2011).
AF+IO*
Subgenus
Growth Blade
Root
Stele
Distribution Ecology form
length* system type
Taxon
Table 1. Continued
576
J.-Y. DUBUISSON ET AL.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
ANATOMICAL
DATA AND NEW QUANTITATIVE
CHARACTERS
The anatomical diversity was fully investigated by
Dubuisson et al. (2011). In that paper, four stele types
(massive, reduced, subcollateral, collateral) and two
cortex types (homogeneous and heterogeneous) are
defined and described. Quantitative measures were
performed on stem thickness and stele diameter, and
allowed us to define two classes for stele diameter
with a limit at 150 μm. Many trichomanoids are
climbing taxa (in a hemi-epiphytic context, see next
section) and Carlquist (1991) showed that, in angiosperm lianas, vessels are significantly larger than
those observed in non-climbing relatives, enabling
faster water conduction in long, climbing stems. In
the present study, we added data on metaxylem diameter in order to test its potential relationship with a
climbing habit. Following the recommendations
detailed in the previous study, for each species
studied, we performed measures on at least three
specimens collected from different localities and on
ten sections per specimen, collected at different positions on the stem, whenever possible, but especially
for colonial long-creeping taxa. In the case of rare,
short monocaulous species, measures were made on
ten sections from the single rhizome of one specimen.
Then, at least ten measures (of the largest diameter
for not fully cylindrical cells) were performed on the
ten largest metaxylem cells, if available. For small
steles with few tracheids and/or with less than ten
metaxylem cells, measures were made on all available
metaxylem cells. Although the absence of xylem has
been reported for a few species of Hymenophyllaceae
(Ogura, 1972), all specimens selected and studied
here had at least one tracheid. In the case of a single
tracheid, we measured this single cell. As explained in
the previous analysis, and as a result of heterogeneity
in the data acquisition procedure, intraspecific variability was not taken into account. We thus assume
that the data (means) used here are representative of
the taxon and are useful for interspecific comparative
studies, but do not reflect their entire natural
variability.
Correlations among selected anatomical characters
were graphically evaluated using a standard regression procedure to evidence potential clustering. This
approach enabled us to categorize quantitative characters and to formulate hypothetical correlations,
which were then phylogenetically tested.
PHYLOGENETIC
APPROACHES AND INFERRED
EVOLUTION OF SELECTED HABITS AND CHARACTERS
The choice of the phylogenetic framework and the
rooting strategy is explained in detail in our previous
577
related study (Dubuisson et al., 2011). Following
reviews on ecology in trichomanoids (Dubuisson et al.,
2003, 2009), we defined here four main ecological
types: terrestrials; climbing (hemi)-epiphytes; individual epiphytes; and colonial epiphytes. Terrestrials
correspond to taxa that complete their entire life cycle
rooted on soil or, possibly, in trichomanoids, on crevices of rocks in which humus accumulates. In terrestrial taxa, epiphytism is sometimes observed, but is
considered accidental and not obligatory. According to
Benzing (1990), hemi-epiphytes correspond to taxa
that occur in both habitats, firstly terrestrial and
secondarily epiphytic for secondary hemi-epiphytism,
and conversely for primary hemi-epiphytism. Some
trichomanoids are secondary hemi-epiphytes sensu
Benzing, beginning their growth terrestrially, then
climbing on trunks and secondarily becoming epiphytic. For example, Vandenboschia gigantea (Bory ex
Willd.) Ebihara & Dubuisson colonizes the forest
understorey before climbing on trunks (Dubuisson
et al., 2003). Other hemi-epiphytes, such as Vandenboschia collariata (Bosch) Ebihara & K.Iwats., begin
their growth at the bases of trees, developing roots in
the soil and climbing on trunks with long-scandent,
rootless stems. They are considered as primary hemiepiphytes, because the juvenile stage is epiphytic at
the bases of trees before roots reach the soil (Nitta &
Epps, 2009). The attribution of a precise hemiepiphytic category to every species requires further
field investigations, and the separation is not always
clear cut. In addition, Dubuisson et al. (2003) also
distinguished lianescence for Trichomanes subgenus
Lacostea Bosch, with species having a rooted terrestrial part and climbing rootless stems. Because strategies in Lacostea are comparable with those observed
in V. collariata and, in order to avoid confusion with
‘lianas’ (a term usually restricted to woody vines), we
decided to group here under ‘hemi-epiphytic habit’ s.l.
all trichomanoids that begin their growth terrestrially or at the bases of trees and complete their growth
as epiphytes after climbing on trunks. Uncertainty
remains as to the precise type of hemi-epiphytism for
several climbing taxa. Hemi-epiphytism therefore
concerns all Vandenboschia [except Vandenboschia
maxima (Blume) Copel.] and all Trichomanes subgenus Lacostea and some Trichomanes subgenus Trichomanes (e.g. Trichomanes scandens L.), and always
implies a climbing habit on a trunk for mature parts.
A particular case is formed by Abrodictyum caudatum
(Brack.) Ebihara & K.Iwats. and Abrodictyum flavofuscum (Bosch) Ebihara & K.Iwats. These taxa are
holo-epiphytic, living their entire lives as epiphytes
(see hereafter), but always display a robust longcreeping stem (with rare branching) that climbs vertically along tree trunks. We categorized such species
as climbing epiphytes. Our term epiphytes corre-
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
578
J.-Y. DUBUISSON ET AL.
sponds here to holo-epiphytes and concerns taxa that
obligatorily complete their entire life cycle on other
plants (phorophytes), especially trees or tree ferns.
This habit also involves the saxicolous habit, in which
constraints are similar in terms of accessibility to
water and nutrients, and because numerous species
(especially belonging to Crepidomanes and Didymoglossum) occur in both habitats. In previous studies
(Dubuisson et al., 2003, 2009, 2011), two types of
growth form were distinguished. The individual
growth form concerns taxa with erect to shortcreeping rhizomes that rarely branch, not allowing
individuals to colonize a large area. In contrast, the
colonial growth form concerns taxa with branched
long-creeping rhizomes, enabling individuals to colonize their substrate, sometimes over a relatively large
area (e.g. V. gigantea, see Dubuisson et al., 2003; and
Fig. 6 for colonial epiphytes). In addition to these two
main growth forms, a few species display longcreeping rhizomes that do not or only rarely branch,
and individuals do not colonize a large area (e.g.
A. caudatum, A. flavofuscum and Trichomanes robustum E.Fourn.). The growth form of these species
is thus considered here as individual. Most terrestrial
species display an individual growth form. All
hemi-epiphytes are colonial with branched longcreeping scandent rhizomes. If not (i.e. all remaining
epiphytes), the growth on phorophytes has, a priori,
no preferential direction. Holo-epiphytism (s.l.) can
thus be divided into individual (non-climbing) epiphytism, colonial (non-climbing) epiphytism and
climbing epiphytism. In our coding, climbing holoepiphytes (s.l.) are treated together with hemiepiphytes. Phylogenetic relationships between growth
form and anatomy are discussed in Dubuisson et al.
(2011).
We also used characters previously defined for the
blade length and anatomy (Dubuisson et al., 2011) as
follows. The blade length represents the plant size
and is divided into three classes: large plants (with
leaves longer than 12 cm), small to dwarf plants (with
leaves shorter than 6 cm) and medium-sized plants
(with leaves of 6–12 cm). The stele type was coded by
combining collateral with subcollateral types and
massive with reduced types. We defined two classes
for the stele diameter with a limit of 150 μm. As
already highlighted in our previous study, anatomical
regression of the stem also seems to be accompanied
by a regression in the adventitious root system in at
least four groups (Trichomanes polypodioides L.,
Polyphlebium, Didymoglossum and Crepidomanes
subgenus Crepidomanes), which are all colonial epiphytes. We also investigated the root system by defining two classes: developed root system and regressed
root system (to rootless). Coding for all characters is
reported in Table 1.
As for the previous study, the evolution of selected
characters was inferred from the consensus phylogenetic tree (including branch lengths) using the
maximum likelihood (ML) method as implemented
in the Mesquite package ver. 2.73 (Maddison &
Maddison, 2010). We tested two models implemented
in Mesquite. The first (MK1 for ‘Markov K-state oneparameter’) assumes equivalent probabilities for
forward (apomorphic) and backward (reversal)
changes for a single character. The second
(AsymmMK for ‘Asymmetrical Markov K-state twoparameter’) attributes distinct probabilities for reversal and apomorphic changes. This difference in
change rates appears to be more realistic, especially
in the case of regressive evolution, when reduction
and loss of characters are often irreversible (the irreversibility constraint is particular to the AsymmMK
model when the backward rate is constrained to be
low to negligible). However, the AsymmMK model can
only be selected for binary characters. For both
models, rates of changes are directly estimated based
on our data.
In accordance with previous hypotheses (Dubuisson
et al., 2011), we particularly propose here to test
correlations between morphological and anatomical
regression and epiphytism and between metaxylem
diameter and climbing habit of (hemi)-epiphytes.
Morphological and anatomical regression is represented by small to dwarf size (leaves shorter than
6 cm), regressed root system, small stele (< 150 μm)
and subcollateral and collateral stele types. We tested
correlations between characters on the phylogenetic
tree using the method of Pagel & Meade (2006) on
discrete data implemented in their BayesTraits
package (available from http://www.evolution.rdg
.ac.uk). For each pair of characters tested, the
program calculates the likelihood of the distribution
of character states expected on the trees under the
assumption that both characters are dependent (or
evolutionarily correlated), and the likelihood of the
expected distribution under the assumption that both
characters are independent (or not evolutionarily correlated). We used the ML method implemented in the
BayesTraits package. The analyses were performed
on a random sampling of 100 trees among the trees
produced by the Bayesian analysis used to reconstruct the phylogenetic tree. The resulting likelihoods
were compared using the likelihood ratio test statistic
(LR) (Felsenstein, 1981), where LR = 2[log-likelihood
(dependent
model) – log-likelihood
(independent
model)] is distributed as a χ2 with four degrees of
freedom. A significant χ2 value proposes that the
evolutionary correlation between the two characters
is statistically significant. The LR used here corresponds to the mean of the LR provided for each of the
100 sampled trees.
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EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
RESULTS
METAXYLEM
DIAMETER
Metaxylem diameters are reported in Table 1. With
the sampling used here, the metaxylem diameter
ranges from 6.37 to 90.95 μm (mean, 29.16 μm; SD,
18.99 μm). The metaxylem diameter appears to be
significantly correlated with the stele diameter
(R = 0.77, d.f. = 48, P < 0.001, Fig. 1), but the correlation is supported only for climbers (R = 0.82, d.f. = 9,
P < 0.01). Three clouds of points can be distinguished:
the first contains the colonial epiphytes, the second
clusters terrestrials, individual epiphytes and one
hemi-epiphyte (Trichomanes ankersii C.Parker ex
Hook.), and the third involves the remaining hemiepiphytes and one climbing epiphyte (A. flavofuscum).
Based on these results, we can graphically define
three classes for the metaxylem diameter with two
empirical limits of 20 and 41 μm, respectively. The
largest metaxylem (> 41 μm) would characterize
hemi-epiphytes and one climbing epiphyte (A. flavofuscum) (i.e. all climbing taxa except T. ankersii and
A. caudatum).
INFERRED
EVOLUTION OF ECOLOGY AND
CHARACTERS
Because some models used in the phylogenetic comparative method require that characters are binary,
ecological types were decomposed into four binary
characters: strict terrestrial and non-strict terrestrial
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(the latter, a priori, including all the other types);
non-climbing (hemi)-epiphyte and climbing (hemi)epiphyte; non-individual epiphyte and individual
epiphyte; and non-colonial epiphyte and colonial epiphyte. Ancestral state probabilities for the ecology of
some selected representative nodes are reported in
the Appendix, and the inferred evolution of ecology is
illustrated in Figure 2 for non-climbing epiphytism
and in Figure 5 for climbing habit. The terrestrial
state is inferred as ancestral in trichomanoids [by
combining the fact that the ecology for basal nodes is
neither epiphytic nor climbing (hemi)-epiphytic, see
Appendix]. Colonial epiphytism appeared at least four
times, independently in Polyphlebium, Didymoglossum, Crepidomanes subgenus Crepidomanes and
T. polypodioides (Fig. 2). Individual (non-climbing)
epiphytism is restricted, with our sampling, to three
isolated species (Abrodictyum tamarisciforme (Jacq.)
Ebihara & Dubuisson, Trichomanes alatum Sw. and
Trichomanes crispum L.). Climbing habit appeared at
least five times: climbing hemi-epiphytism in the
genus Vandenboschia with a reversal to the terrestrial state in V. maxima; in Crepidomanes aphlebioides (H.Christ) I.M.Turner; in T. scandens; in
Trichomanes subgenus Lacostea (represented here by
T. ankersii and Trichomanes pedicellatum Desv.);
and climbing epiphytism in the clade (A. caudatum–
A. flavofuscum) (Fig. 5). By separately treating nonclimbing epiphytism (i.e. all epiphytes except
A. caudatum and A. flavofuscum) and climbing habit
Figure 1. Graphical correlations between metaxylem diameter and stele diameter, depending on ecology. Clustering and
regressions are detailed and discussed in the text.
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Figure 2. Evolution of holo-epiphytism in trichomanoids inferred using maximum likelihood. We excluded here climbing
epiphytism that concerns only two taxa (Abrodictyum caudatum and A. flavofuscum) which are treated as climbers (see
Fig. 5). The arrow indicates the alternative inferred appearance of colonial epiphytism when ecology is treated involving
all the states (see text). The partial coloration of some internal nodes is proportional to the change probabilities (see
Appendix). On nodes, abbreviations correspond to representative clades also reported in the Appendix: Ab, Abrodictyum;
C, Crepidomanes subgenus Crepidomanes; Ca, Callistopteris; Ce, Cephalomanes; Cr, Crepidomanes; D, Trichomanes
subgenus Davalliopsis; Di, Didymoglossum; HE, ‘(Hemi)-Epiphytic’ clade (see text); L, Trichomanes subgenus Lacostea;
N, Crepidomanes subgenus Nesopteris; Po, Polyphlebium; Tr, Trichomanes; Va, Vandenboschia.
as detailed above, we do not reveal any relationship
between these two habits, suggesting that climbing
hemi-epiphytic or epiphytic taxa or clades would have
been derived directly and independently from terrestrial ancestors. When we treat ecology as one multistate character involving epiphytism and climbing
habit, colonial epiphytism is inferred to have
appeared in the common ancestor of the clade called
HE [as ‘(Hemi)-Epiphytic’ clade, because it involves
epiphytes and climbing (hemi)-epiphytes] with a prob-
ability of 0.71 (not detailed in Appendix, arrow in
Fig. 2). This result suggests that both hemiepiphytism in Vandenboschia and in Cr. aphlebioides
would have been independently derived from colonial
epiphytism with an additional reversal to terrestrial
habit in [Crepidomanes intermedium (Bosch) Ebihara
& K. Iwats.–Crepidomanes thysanostomum (Makino)
Ebihara & K.Iwats.] and V. maxima. Outside the HE
clade, the inferred changes are identical to those
revealed by the binary treatment.
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EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
We found similar evolutionary scenarios for all
binary characters, regardless of the model selected
(MK1 or AsymmMK, see Appendix). Consequently,
only the evolution with the MK1 model is presented
in Figures 3−5. Inferred evolutions of stele type and
stele diameter were detailed in the previous study
(Dubuisson et al., 2011) and are reported in Figure 3.
The evolution of blade length and root system is
shown in Figure 4. The large leaves are inferred as
ancestral in trichomanoids and dwarfism (i.e. appearance of small to dwarf leaves) evolved at least twice:
in Didymoglossum with a reversal to medium size in
Didymoglossum gourlianum (Grev. ex J. Sm.) Pic.
Serm.; and in Crepidomanes subgenus Crepidomanes
with a reversal to medium size in Crepidomanes
fallax (H.Christ) Ebihara & Dubuisson (Fig. 4).
Medium size appeared at least four times: in
Polyphlebium [excluding Polyphlebium capillaceum
(L.) Ebihara & Dubuisson]; in Trichomanes subgenus
Lacostea; in the clade (Trichomanes arbuscula Desv.–
Trichomanes holopterum Kunze); and in T. polypodioides. The evolution of the root system is fully
congruent with the appearance of colonial epiphytism
(Fig. 4). Metaxylem evolution (here the appearance of
large metaxylem) is reported in Figure 5. Large
metaxylem appeared (probably from medium-sized
metaxylem) five times: in Vandenboschia with a
reversal in V. maxima; in Cr. aphlebioides; in T. pedicellatum; in T. scandens; and in A. flavofuscum.
PHYLOGENETIC
COMPARATIVE ANALYSES
When treating ecology as a multistate character
(where the appearance of colonial epiphytism is
inferred in the common ancestor of the HE clade, see
Fig. 2), we demonstrated no significant phylogenetic
correlation between epiphytism and any morphological or anatomical character. Conversely, when applying a binary treatment for each ecological type,
graphics (Fig. 3A, B) and analyses clearly indicate a
significant phylogenetic correlation between colonial
epiphytism and small stele (LR = 22.542, P < 0.001),
and between colonial epiphytism and collateral/
subcollateral stele (LR = 18.608, P < 0.001). Furthermore, the inferred evolution of small metaxylem (not
shown here) is identical to the evolution of the
collateral/subcollateral stele; the correlation with
colonial epiphytism could therefore also be applied to
small metaxylem. Colonial epiphytism, root system
regression (which fully evolves in parallel with colonial epiphytism), stele diameter, stele type and small
metaxylem thus appear to be strongly evolutionarily
linked. Concerning dwarfism, we evidenced no phylogenetic correlation between small to dwarf sizes and
colonial epiphytism (LR = 9.338, P > 0.05), but the
graphics strongly show that dwarfism is restricted to
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two colonial epiphytic clades: Didymoglossum and
Crepidomanes subgenus Crepidomanes. However, if
we combine medium sizes with small to dwarf sizes,
the correlation between size and colonial epiphytism
becomes significant (LR = 16.552, P < 0.01), suggesting that colonial epiphytism is accompanied by a
reduction in size in the three colonial epiphytic clades
(by adding Polyphlebium) and in colonial epiphytic
T. polypodioides, and thus leads to dwarfism in only
two of the three colonial epiphytic clades, as developed above. We found no phylogenetic correlation
between individual epiphytism and any anatomical or
morphological character. The climbing habit appears
to be phylogenetically correlated only with large
metaxylem (Fig. 5; LR = 33.494, P < 0.001).
DISCUSSION
EVOLUTION
OF ECOLOGY IN TRICHOMANOIDS
Two distinct inferences of the appearance of colonial
epiphytism were obtained depending on the treatment of ecology as a multistate character (colonial
epiphytism ancestral in HE clade, but with weak
support; probability 0.71) or as a binary character
(three occurrences in the HE clade, see Fig. 2; change
probabilities > 0.92). As already discussed in the previous study (Dubuisson et al., 2011), the result
obtained with the multistate treatment is also statistically expected. Indeed, colonial epiphytism is the
most frequently observed state in terminal taxa of the
HE clade and therefore has a higher probability to be
inferred for the common ancestor of the HE clade
than has hemi-epiphytism, which is less frequent in
terminal taxa and concentrated in the subclade corresponding to Vandenboschia. Biologically, the observation in a broad clade of a characteristic shared by
the majority of species does not necessarily imply that
the other, less frequent traits observed in the same
clade evolved first. This is especially true if the most
common trait illustrates one or several recent events
of rapid and high diversification subsequent to the
occurrence of the other characters, leading to an overrepresentation in extant taxa. We could suggest an
equivalent bias in the study by Hennequin et al.
(2008), which proposed a similar evolutionary pattern
for epiphytism s.l. in trichomanoids. Therefore, we
prefer to select here the evolutionary hypothesis provided with the binary treatment, where change probabilities (here the appearance of colonial epiphytism)
are also the highest. The choice of this scenario is also
reinforced as being the unique hypothesis revealing a
significant correlation between a habit (colonial epiphytism) and important changes in morphology
(reduction in size, regression in root system) and
anatomy (acquisition of subcollateral/collateral types,
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Figure 3. Comparative evolution of characters in trichomanoids inferred using maximum likelihood. A, Comparative
evolution of colonial epiphytism (black) and small stele (black) [‘Markov K-state one-parameter’ (MK1) model]; small stele
corresponds to diameter smaller than 150 μm (see text). B, Comparative evolution of colonial epiphytism (black) and stele
type (white, massive/reduced; black, subcollateral/collateral) (MK1 model). In both figures, the coloration of internal nodes
is proportional to the change probabilities (see Appendix). The statistical test result is reported with the likelihood ratio
test statistic (LR) value and the probability suggesting a significant correlation between the compared characters (see
text). On nodes, abbreviations correspond to representative clades as also reported in the Appendix: Ab, Abrodictyum; C,
Crepidomanes subgenus Crepidomanes; Ca, Callistopteris; Ce, Cephalomanes; Cr, Crepidomanes; D, Trichomanes subgenus Davalliopsis; Di, Didymoglossum; HE, ‘(Hemi)-Epiphytic’ clade (see text); L, Trichomanes subgenus Lacostea; N,
Crepidomanes subgenus Nesopteris; Po, Polyphlebium; Tr, Trichomanes; Va, Vandenboschia.
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EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
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Figure 4. Comparative evolution of blade length, root system and colonial epiphytism in trichomanoids inferred using
maximum likelihood [‘Markov K-state one-parameter’ (MK1) model]. The coloration of internal nodes is proportional to
the change probabilities (see Appendix). The statistical test shows no significant correlation between small to dwarf size,
regression in root system and colonial epiphytism (LR = 9.338, P > 0.05). A significant correlation is nevertheless revealed
if small to dwarf size is combined with medium size (LR = 16.552, P < 0.01). On nodes, abbreviations correspond to
representative clades as also reported in the Appendix: Ab, Abrodictyum; C, Crepidomanes subgenus Crepidomanes; Ca,
Callistopteris; Ce, Cephalomanes; Cr, Crepidomanes; D, Trichomanes subgenus Davalliopsis; Di, Didymoglossum; HE,
‘(Hemi)-Epiphytic’ clade (see text); L, Trichomanes subgenus Lacostea; N, Crepidomanes subgenus Nesopteris; Po,
Polyphlebium; Tr, Trichomanes; Va, Vandenboschia.
reduction in stele diameter and appearance of small
metaxylem). These changes could illustrate a regressive evolution linked to an ecological specialization, as
discussed later.
INDIVIDUAL
EPIPHYTISM
Even in rainforest, a significant decrease in relative
air hygrometry is often possible during a few hours a
day, generating water loss in plants. Under relative
drought conditions, even for a short period, terrestrial
and climbing hygrophilous species are supposed to be
able to compensate for water loss by absorbing water
via roots anchored in an ever-wet soil. Terrestrial
hygrophilous species are often observed near waterfalls, along streams or on shady crevices below rocks
in forests, where the soil is never dry, and some
species, such as the Neotropical Trichomanes pinnatum Hedw. and the Asiatic Cephalomanes javanicum
(Blume) C.Presl, often grow in temporarily flooded
areas. A decrease in relative air hygrometry is more
problematic for epiphytic species that have no direct
connection to the soil and rely on selected alternative
adaptations to endure water loss. Nitta (2006)
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Figure 5. Comparative evolution of climbing habit (black) and large metaxylem (black) in trichomanoids inferred using
maximum likelihood [‘Markov K-state one-parameter’ (MK1) model]. Large metaxylem corresponds to diameter larger
than 41 μm (see text). The coloration of internal nodes is proportional to the change probabilities (see Appendix). The
statistical test result is reported with the likelihood ratio test statistic (LR) value and the probability, suggesting a
significant correlation between the compared characters (see text). On nodes, abbreviations correspond to representative
clades as also reported in the Appendix: Ab, Abrodictyum; C, Crepidomanes subgenus Crepidomanes; Ca, Callistopteris;
Ce, Cephalomanes; Cr, Crepidomanes; D, Trichomanes subgenus Davalliopsis; Di, Didymoglossum; HE, ‘(Hemi)-Epiphytic’
clade (see text); L, Trichomanes subgenus Lacostea; N, Crepidomanes subgenus Nesopteris; Po, Polyphlebium; Tr,
Trichomanes; Va, Vandenboschia.
demonstrated on a restricted and local sample that
colonial epiphytic members of Hymenophyllaceae
were more drought tolerant than terrestrial types. In
forests in which it rains daily, rapid rehydration is
also facilitated by the absorption of rainwater directly
by the lamina that lacks a cuticle, regardless of
the ecology and growth form. Individual epiphytes
(A. caudatum, A. flavofuscum, A. tamarisciforme,
T. crispum and T. alatum) exhibit a morphology and
anatomy similar to those of terrestrial relatives and,
a priori, no particular adaptation to epiphytism.
These species are found in wet areas where the risk
of drought is low. Epiphytic A. tamarisciforme occurs
on La Réunion Island above 1000 m where annual
rainfall exceeds 6000 mm without a significant dry
season, whereas the terrestrial sister species Abrodictyum meifolium (Bory ex Willd.) Ebihara & K.Iwats.
occurs above 300 m where annual rainfall can be
below 3000–4000 mm (Grangaud, 2010; J.-Y. Dubuisson, pers. observ.). Furthermore, except for the widespread T. crispum that appears to be opportunistic
(Proctor, 1977; Lellinger, 1994; J.-Y. Dubuisson, pers.
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EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
observ.), all individual epiphytes are mostly observed
on tree fern trunks (Cyatheaceae; Brownlie, 1969;
Proctor, 1977; Ebihara, 2002; Grangaud, 2010; J.-Y.
Dubuisson, pers. observ.) with their stems and root
system embedded in the adventitious root mantle
covering the tree fern trunk, but there does not
appear to be a strict specific relationship. This substrate is likely to retain more water than smooth
bark, where such species are not or rarely observed.
Most individual epiphytes are rarely observed above
10 m on trunks, especially if they grow on tree ferns
(exceptionally > 20 m for Cyatheaceae in the Indian
Ocean; Janssen & Rakotondrainibe, 2008). Lower on
tree fern trunks, the environment of epiphytes is
similar to conditions of the understorey with low
hygrometric fluctuations compared with higher up in
the canopy. This environment is thus favourable for
epiphytic hygrophytes that are also named ‘understorey epiphytes’. In Madagascar and the Mascarene
Islands, A. tamarisciforme is found on various tree
fern species, but not exclusively (Grangaud, 2010;
J.-Y. Dubuisson, pers. observ.). In the area, tree ferns
radiated quite recently in the upper Tertiary (Pliocene) according to Janssen et al. (2008). We therefore
suggest that individual epiphytism may thus have
appeared several times by parallelism from terrestrial clades, probably at least in the Tertiary (see
Fig. 7), and that it does not illustrate any ecological
diversification, radiation or ‘success’, contrary to colonial epiphytism as discussed below. The presence of
these species as epiphytes on tree ferns rather than in
a terrestrial habitat, as displayed by their close relatives, could be conditioned by preferences of the
gametophyte.
COLONIAL
EPIPHYTISM
All colonial epiphytic species belonging to Didymoglossum, Polyphlebium and Crepidomanes subgenus
Crepidomanes share regressive morphology and
anatomy (reduction in size, stem thickness, stele type
and diameter, metaxylem diameter and reduction in
root system to rootless type). These regressive tendencies appear to be statistically well related to
colonial epiphytism acquisition (see Figs 3 and 4). As
for individual climbing and non-climbing epiphytes,
they are understorey epiphytes and not or only rarely
observed in canopy situations. Some species are generalist and found on various substrates [such as
Didymoglossum cuspidatum (Willd.) Ebihara &
Dubuisson observed on tree trunks and branches,
emerging roots, wet rocks or stumps; Grangaud, 2010;
J.-Y. Dubuisson, pers. obs.], whereas others seem to
be more specialized [such as Didymoglossum godmanii (Hook.) Ebihara & Dubuisson, mostly occurring on
the palm Welfia georgii H.Wendl.; Moran & Russel,
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2004], even though they are phylogenetically related
(D. godmanii was not sampled here but belongs to the
same subgenus, Microgonium C.Presl, as D. cuspidatum). Colonial epiphytic species have the ability to
colonize a broad surface with their highly branched
and long-creeping filiform rhizomes (see Fig. 6), and
to adhere to smooth bark and hard substrates (including rocks) by using a dense cauline indumentum in
addition to branched root-like shoots for rootless taxa
(sensu Schneider, 2000), rather than their few roots if
present.
On vertical substrates, leaves are pendant or
appressed to the substrate. In Polyphlebium, pendant
leaves of various sizes are always dissected and sometimes have capillary segments (e.g. P. capillaceum). In
subgenus Crepidomanes, pendant leaves are always
dissected (Fig. 6A), even in the smallest species, such
as Crepidomanes minutum (Blume) K.Iwats., which
often exhibits a finely dissected flabellate lamina
(Fig. 6B). In Didymoglossum, a few species [e.g.
D. gourlianum and Didymoglossum krausii (Hook. &
Grev.) C.Presl] are pinnatifid with pendant leaves;
most other species display lobed to rounded lamina
that are pendant or appressed to substrates, especially the smallest ones (Fig. 6C). Didymoglossum
hildebrandtii (Kuhn) Ebihara & Dubuisson from the
Western Indian Ocean Islands and Didymoglossum
tahitense (Nadeaud) Ebihara & K.Iwats. from Polynesia are related species (Ebihara et al., 2007), and
are characterized by rounded to peltate leaves tightly
appressed on the smooth barks of tree trunks
(Fig. 6D, E), resulting in a habit that is unusual for
ferns and more frequently observed in thallose liverworts and hornworts. Regardless of leaf architecture
and size, all colonial epiphytes, with their large colonies of pendant or appressed thin blades lacking a
cuticle, have the capacity to capture rainwater
directly via the lamina rather than via their reduced
root system. They especially capture the rainwater
flowing along vertical substrates during and after
daily rainfall. This could enable fast rehydration in
the case of short periods of drought. The preferential
use of leaves for water absorption, probably by diffusion, could explain the reduction in the root system
and in vascular tissues in the stems, which would
have been counter-selected.
EPIPHYTISM
AND DWARFISM
Dwarfism, here defined as the reduction in leaf size,
for epiphytic filmy ferns is preponderant only in
Didymoglossum and Crepidomanes subgenus Crepidomanes, and the smallest species are observed in
Didymoglossum (with Didymoglossum nummularium
Bosch displaying leaves that do not exceed 0.3 cm
in length). This contrasts with one of the largest
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Figure 6. Representative colonial epiphytic trichomanoids in situ. A, Crepidomanes bipunctatum (Poir.) Copel., colonizing
a tree trunk in Mauritius rainforest, with pendant highly dissected leaves that can attain 5–6 cm in length (photograph
by J.-Y. Dubuisson). B, Crepidomanes minutum (Blume) K.Iwats., minute species growing on a tree trunk in Mauritius
rainforest; detail of two leaves of a colony that can colonize a broad surface; the largest leaf illustrated here bears two
sori on a flabellate dissected lamina; leaves of this species rarely exceed 2.5 cm in length in Mascarenes (photograph by
J.-Y. Dubuisson). C, Didymoglossum barklianum (Hook. ex Baker) J.P.Roux, dwarf species colonizing a tree trunk in
Mauritian rainforest with simple leaves that do not exceed 0.8 cm in length, mostly pendant or appressed on the substrate
(photograph by J.-Y. Dubuisson). D, Didymoglossum hildebrandtii (Kuhn) Ebihara & Dubuisson colonizing a stump in a
rainforest on Grande Comore (Comoros Islands) (photograph by G. Rouhan). E, Detail of D. hildebrandti, rounded and
peltate leaves, strongly appressed on tree bark, the central one bearing many marginal sori, leaves rarely exceeding 3 cm
in length (photograph by G. Rouhan).
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EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
trichomanoid species, Callistopteris polyantha (Hook.)
Copel., a terrestrial taxon that shows highly divided,
erect leaves exceeding 50 cm in length (Dubuisson
et al., 2003). The gross morphological resemblance to
bryophytes, especially to thallose liverworts, is mostly
observed in Didymoglossum (see Fig. 6D, E). This
resemblance is, of course, superficial; dwarf filmy
ferns are still vascular plants (even with regressed
conducting tissues). The lobed to rounded leaf that
reinforces this gross resemblance in Didymoglossum
could be the consequence of developmental constraints linked to sorus position. Members of Hymenophyllaceae are characterized by sori produced
marginally in the continuity of a single vein. In
species with highly dissected leaves, the ultimate
segments contain a unique vein, resulting in a single
sorus per segment. Polyphlebium and Crepidomanes
species display an anadromous venation combined
with marginal sori always localized on lateral veins,
rarely also on the terminal ones, whereas Didymoglossum species have catadromous venation combined
with marginal sori that always develop on terminal
veins and sometimes on the lateral ones (Dubuisson,
1997). This implies that Polyphlebium and Crepidomanes species always have dissected leaves with
single-veined segments. Consequently, the leaf of the
smallest Crepidomanes species is reduced to a single
or few segments with a limited number of sori (as
observed in Cr. minutum, see Fig. 6B, Crepidomanes
intramarginale (Hook. & Grev.) Copel., or Crepidomanes kurzii (Bedd.) Tagawa & K. Iwatsuki). In
Didymoglossum, the obligatory terminal sorus position seems to be accompanied by the ability to ‘laterally’ develop a lamina involving more than one vein
and often additional false veins (Dubuisson, 1997),
allowing the leaf to acquire a rounded to peltate
architecture and to bear many sori on the largest
leaves (see Fig. 6E).
The ontogeny of fern sporophytes is well documented
and it has been shown that, in species with highly
dissected mature leaves, the first (or juvenile) leaves of
the sporophyte are generally less dissected than the
following ones, thus indicating an increase in leaf
dissection with age, defined as a heteroblastic development (Bower, 1963; Allsopp, 1965). Didymoglossum
species, with their lobed to rounded leaves, could
illustrate a developmental heterochronic process, and
especially paedomorphy (here neoteny; as defined by
Gould, 1988), with mature fertile individuals retaining
the morphology of a young sporophyte. Developmental
constraints related to the sorus position and the heterochronic process hypothesis could explain why
dwarfism and the gross morphological resemblance to
thallose liverworts are exacerbated in catadromous
Didymoglossum. The gross resemblance to thallose
liverworts, as a consequence of regressive evolution in
587
morphology and anatomy leading to dwarfism, combined with probable preferential water absorption by
the lamina, seems to have been selected for Didymoglossum. It is therefore not unexpected to observe the
dwarf species sympatrically and often mixed with
liverworts and mosses.
Because medium-sized to large colonial epiphytes
(as observed in Polyphlebium) are, a priori, not less
efficient at growing in similar habitats and in capturing rainwater than minute taxa, the selection of
dwarfism in filmy ferns should be explained by additional factors. The smallest species of Didymoglossum
and Crepidomanes are found mostly in the shadiest
places, at the base of trunks and under large
branches, or on very wet rocks, and always close to
the substrate and mostly mixed with bryophytes.
These represent potentially various microhabitats in
which high levels of hygrometry are maintained
throughout the year. These conditions are required
for hygrophilous mosses and, especially, liverworts to
limit water loss. We suggest that dwarf epiphytic
species of filmy ferns could be less drought tolerant
than the largest ones, hence their colonization of the
bryophyte-dominated microhabitats. However, this
hypothesis remains speculative in the absence of
studies on the drought tolerance of dwarf trichomanoids. Dwarfism related to epiphytism is not rare in
other groups of plants, but it always involves xerophyte strategies (e.g. succulent blades in small Lemmaphyllum C. Presl and Microgramma C. Presl
species, Polypodiaceae; dwarfism in orchids and bromeliads; see Benzing & Ott, 1981). The ‘bryophytelike’ ecology of dwarf filmy fern species appears in
accordance with an epiphytic ‘bryophyte-like’ strategy
that is unique in vascular plants, but which is not the
unique epiphytism strategy in general selected for
Hymenophyllaceae.
DIVERSIFICATION
OF EPIPHYTISM IN TRICHOMANOIDS
The few colonial epiphytes outside of the HE clade
include T. polypodioides (in subgenus Trichomanes),
often observed on tree fern trunks and having thin
branched creeping stems with a small stele, pendant
leaves of medium size and filiform roots (Proctor,
1977; Lellinger, 1994; J.-Y. Dubuisson, pers. observ.).
This species has a massive stele, a character also
present in its terrestrial relatives. Other colonial epiphytes, such as Trichomanes anadromum Rosenst.
and Trichomanes paucisorum R.C.Moran & B.Øllg.
(Moran & Øllgaard, 1998), were not available for this
study, but they have filiform long-creeping stems and
undoubtedly belong to Trichomanes subgenus Trichomanes. If a close relationship was to be confirmed
between T. polypodioides and these taxa, this would
suggest a colonial epiphytic specialization in a small
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
588
J.-Y. DUBUISSON ET AL.
Figure 7. Synthesized evolutionary hypotheses on ecology, growth form, morphology and anatomy in trichomanoids. The
figure (completed and modified from Dubuisson et al., 2009) reports the inferred appearances of climbing habit,
epiphytism (colonial and individual), colonial growth form, heterogeneous cortex and anatomy regression (with potential
reversals if present). Evolutionary correlations between ecology, morphology, growth form and anatomy are detailed and
discussed in the text. Divergence time estimates are from Hennequin et al. (2008). The age values selected for the nodes
are means calculated from the single gene analysis and are reported with standard deviation (SD) in Hennequin et al.
(2008: table 2). Left vertical line (in Cretaceous) and grey portion of the time scale indicate the diversification of modern
fern families providing more than 80% of living species, in parallel with the angiosperm diversification (according to
Schuettpelz, 2007). Abbreviations on the right correspond to representative clades: Ab, Abrodictyum; C, Crepidomanes
subgenus Crepidomanes; Ca, Callistopteris; Ce, Cephalomanes; Cr, Crepidomanes; D, Trichomanes subgenus Davalliopsis;
Di, Didymoglossum; F, Trichomanes subgenus Feea; L, Trichomanes subgenus Lacostea; N, Crepidomanes subgenus
Nesopteris; Po, Polyphlebium; T, Trichomanes subgenus Trichomanes, Tr, Trichomanes; Va, Vandenboschia.
clade in Trichomanes, rather than independently in a
few isolated species.
The independent appearance of colonial epiphytism
in three major clades at the end of the Cretaceous and
in the Tertiary, according to molecular dating performed by Hennequin et al. (2008) (see Fig. 7), is in
agreement with the hypothesis that most extant epi-
phytic ferns would have diversified during these
periods (Schuettpelz, 2007; Schuettpelz & Pryer,
2009). This result corroborates the preliminary
hypothesis suggested for Hymenophyllaceae of a
diversification of epiphytic filmy ferns at least in the
Late Cretaceous (Dubuisson et al., 2009). In the same
context, the localized occurrence of colonial epiphyt-
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
ism in Trichomanes subgenus Trichomanes (T. polypodioides, see Fig. 2), localized occurrences of individual
epiphytism (A. tamarisciforme, T. alatum, T. crispum,
see Fig. 2) and multiple acquisitions of a climbing
habit (see Fig. 5) could also be dated back to the
Tertiary (Hennequin et al., 2008) during the development of current tropical rainforests dominated by
angiosperms. These Tertiary tropical rainforests probably provided ecological facilities for the appearance
of such habits and for the diversification of colonial
epiphytes (Behrensmeyer et al., 1992; Willis &
McElwain, 2002; Schuettpelz & Pryer, 2009).
ANATOMY
AND CLIMBING HABIT
Concerning the climbing habit, our analysis strongly
suggests that, by convergence with angiosperm lianas,
as demonstrated by Carlquist (1991), the largest size
for equivalent conducting tissues (here tracheids)
would have been selected in climbing trichomanoid
taxa, with the consequence of a potentially higher
efficiency of water conduction in the long robust stems
of these species. Extant hemi-epiphytic climbing filmy
ferns produce medium-sized to large fertile leaves a
few metres above the ground (to maximize spore
dispersion) under conditions in which water loss, as for
strict epiphytes, is not negligible. By keeping a relationship to the ground via a developed root system,
hemi-epiphytes have the possibility to absorb groundwater, the conduction of which to more distant leaves
may be facilitated by the large stele and metaxylem. In
contrast, colonial non-climbing holo-epiphytes have
long-creeping, lax and filiform rhizomes with reduced
conducting tissues that are sufficient for a colonial
strategy on the epiphytic substrate. Dubuisson et al.
(2011) showed that climbing taxa outside the HE clade
and all taxa belonging to the HE clade have a heterogeneous cortex, which appears to be significantly
related to a colonial strategy and is conserved in
colonial epiphytes. The present study infers the
common ancestor of the HE clade as an individual
terrestrial. However, as already proposed in the previous study, we cannot reject the possibility that this
ancestor would have been hemi-epiphytic, because
inference is strongly conditioned by the current underrepresentation of hemi-epiphytic taxa in the HE clade.
The extant distribution of hemi-epiphytism in the HE
clade is limited to two subclades and a few isolated
taxa in trichomanoids (Dubuisson et al., 2011), but this
could hide the possibility that hemi-epiphytic taxa
were dominant during the clade diversification, estimated to have occurred during the Cretaceous in the
understorey of early angiosperm-dominated forests.
With this alternative hypothesis, regressed colonial
epiphytes would have derived from robust hemiepiphytes in the HE clade.
IMPORTANCE
589
OF THE GAMETOPHYTE GENERATION
In ferns, the sporophyte ecology is strongly linked to
the gametophyte habitat, which determines where
the sporophyte will grow, but fern gametophyte
ecology has not yet been studied in sufficient detail. In
trichomanoids, one study has suggested that the
recruitment and growth habit of the hemi-epiphytic
V. collariata depends on the habitat of the gametophytes, which seems to be restricted to the bases of
trees (Nitta & Epps, 2009). The few studies performed
on the subject have provided promising insights, such
as strong differences in ecological preferences and
biology of the gametophyte generation between terrestrial, epiphytic and climbing species. Dassler &
Farrar (2001) suggested that the success of epiphytic
ferns, especially in long-distance dispersal and colonization, could be related to the perennial and longlived strategy of epiphytic gametophytes, compared
with short-lived terrestrial ones (at least in Polypodiales). Watkins, Mack & Mulkey (2007) and Watkins
et al. (2007) further showed that epiphytic gametophytes are more drought tolerant than terrestrial
ones. The long-lived strategy and relative drought
tolerance of epiphytic gametophytes could also be
related to competition with epiphytic bryophytes and
to the increase in the outcrossing probability in a
habitat in which gametophyte establishment from
spores is limited (see also the review of Farrar et al.,
2008). Members of Hymenophyllaceae are characterized by perennial, long-lived and colonial gametophytes, and some populations, especially in temperate
areas, are also known to subsist only as gametophytes
reproducing asexually by gemmae (Farrar, 1990,
1992; Rumsey et al., 1999). The gametophytes of filmy
ferns thus appear (pre-)adapted to epiphytic habitats.
In this sense, we disagree with Farrar et al. (2008),
who proposed that gametophytes of terrestrial Hymenophyllaceae [citing Abrodictyum rigidum (Sw.)
Ebihara & Dubuisson and Trichomanes osmundoides
Poir.] would have retained the form of their epiphytic
relatives, assuming terrestrial species to be derived in
the family. We propose, instead, that gametophytes of
terrestrial species probably exhibit the ancestral
state, because terrestrial habitat is inferred as ancestral. Epiphytic sporophytes, as in Didymoglossum,
would have more or less retained the properties of
their gametophytes, probably in a competitive context
with liverworts and other mosses. A precise comparative study on the ecological preferences, biology and
drought tolerance of gametophytes of terrestrial,
hemi-epiphytes and individual or colonial epiphytes
in Hymenophyllaceae using phylogenetic analysis is
therefore needed. The ecological preference of the
gametophyte could also explain why some species
are opportunistic and some specialized (e.g. how
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
590
J.-Y. DUBUISSON ET AL.
individual climbing or non-climbing epiphytes are
mostly observed on tree ferns, whereas their relatives
are terrestrial). Filmy ferns are a pertinent model for
the study of ecology evolution, not only of the fern
sporophyte, but also of the gametophyte, one of the
future directions of study in fern ecology proposed by
Walker, Mehltreter & Sharpe (2010).
CONCLUSIONS AND PROSPECTIVE WORK
Evolutionary scenarios of ecology, growth forms
(according to our previous study; Dubuisson et al.,
2011), gross morphology and anatomy for the trichomanoids are summarized in Figure 7, with a proposed
time scale following Hennequin et al. (2008). The first
trichomanoids were inferred as terrestrial, probably
robust plants displaying individual growth, standard
well-developed protosteles, developed root systems
and erect leaves (as observed for all extant terrestrial
trichomanoids). A colonial growth form appears to
have been selected in a clade during the lower Cretaceous, probably in the understorey of the first
angiosperm-dominated forests. Although our analyses
did not statistically propose that these first colonial
filmy ferns would be climbing hemi-epiphytes, the
hypothesis of a hemi-epiphytic appearance related to
coloniality in the HE clade is not fully rejected, as
suggested by the heterogeneous cortex that may
have been selected in relation to a climbing habit
(Dubuisson et al., 2011). Colonial epiphytism could
have appeared in the HE clade, maybe from hemiepiphytism, at least in three clades that diversified
during the upper Cretaceous or the Tertiary. This first
period corresponds to the time estimated for the
diversification of most modern fern lineages in the
‘shadow’ of the angiosperms (Schneider et al., 2004b),
and the second period corresponds to epiphytism
acquisition in other fern families (Schuettpelz, 2007;
Schuettpelz & Pryer, 2009). Morphological and anatomical regression is observed in these three colonial
epiphytic clades and would be related to water acquisition by the pendant or appressed blades rather
than by a root system. A ‘bryophyte-like’ strategy is
observed in one clade (Didymoglossum). Outside the
HE clade, parallel acquisition of climbing habit and
epiphytism (individual and colonial) could probably
have occurred more or less recently in the Tertiary.
This study deliberately excluded the Hymenophyllum sister clade, most members of which are colonial
epiphytic or epilithic species with pendant leaves
(with few individual epiphytic exceptions), which
would have diversified in parallel with trichomanoid
colonial epiphytic clades (Hennequin et al., 2008).
This genus differs from the trichomanoids in anatomical diversity [with three stele types: reduced;
subcollateral (rarely collateral); and dorsiventral:
Hennequin et al., 2006] and in the absence of clades
comprising dwarf forms resembling thallose liverworts. An analogous comparative study in this lineage
is required to provide hypotheses on the strategies
that allowed Hymenophyllum to succeed in diversifying in the epiphytic habitat at the pantropical level
with similar species richness, and to reveal potential
parallel evolution or distinct strategies in the two
lineages at the family level.
ACKNOWLEDGEMENTS
This work, and especially the field trips for specimen
acquisition, was supported by UMR 7207 ‘Centre de
Recherche sur la Paléobiodiversité et les Paléoenvironnements‘, IFR 101 ‘Institut d’Ecologie, Biodiversité, Evolution, Environnement‘ and the PPF MNHN
‘Etat et Structure Phylogénétique de la Biodiversité
Actuelle et Fossile’. The molecular work for providing
the phylogenetic framework was partly supported by
JSPS fellowship for A. Ebihara. We thank G. Rouhan,
F. Rakotondrainibe and J.-N. Labat for the use of P
herbarium specimens, C. Chaussidon, G. Rouhan, F.
Rakotondrainibe, C. Reeb, E. Grangaud, A. Le
Thomas and H. Schneider for discussions on filmy
fern anatomy, biology and ecology, and T. Dufour, N.
Salel and E. Watroba for precious help in anatomy
investigations. We also thank two anonymous reviewers for their pertinent commentaries, suggestions and
corrections.
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0
0
0
0
0
0.01
0
0
0
0
0
0.01
0
0.01
0
0
0
0
Not epiphyte
1
1
1
1
1
0.99
1
1
0.74
0.01
0.74
0.08
0.80
0.76
0.98
1
0.06
0.99
Clade
(Ca–Ce)
Ab
(A. caudatum–A. flavofuscum)
(Tr–HE)
Tr
(T. scandens–T. polypodioides–
T. alatum)
D–L
L
HE
Po
(Cr–Va–Di)
Di
(Cr–Va)
Cr
N
(Cr. thysanostomum–Cr. intermedium)
C
Va
Individual
epiphyte
0
0
0.26
0.99
0.26
0.91
0.20
0.23
0.02
0
0.94
0.01
0
0
0
0
0
0
Colonial
epiphyte
Non-climbing holo-epiphytism
(Fig. 2)
1-1
1-1
0.73-0.88
0.01-0.01
0.73-0.88
0.08-0.11
0.79-0.92
0.76-0.89
0.98-0.99
1-1
0.06-0.08
0.99-1
1-1
1-1
1-1
1-1
1-1
1-1
No
0
0
0.27-0.12
0.99-0.99
0.27-0.12
0.92-0.89
0.21-0.08
0.24-0.11
0.02-0.01
0
0.94-0.92
0.01-0
0
0
0
0
0
0
Yes
Colonial epiphytism (binary
coding) (Figs 3, 4)
0.93-0.81
0.02-0.03
0.99-0.81
1-0.97
0.98-0.75
0.99-0.88
0.91-0.62
0.93-0.72
0.84-0.70
0.99-0.95
0.99-0.90
0.11-0.15
0.99-0.89
1-0.90
0.01-0.01
1-0.88
1-0.90
1-0.89
No
0.07-0.19
0.98-0.97
0.01-0.19
0-0.03
0.02-0.25
0.01-0.12
0.09-0.38
0.07-0.28
0.16-0.3
0.01-0.05
0.01-0.1
0.89-0.85
0.01-0.11
0-0.10
0.99-0.99
0-0.12
0-0.10
0-0.11
Yes
Climbing habit (binary
coding) (Fig. 5)
0.99-0.92
0.92-0.74
1-0.82
1-0.95
0.98-0.77
0.99-0.87
0.91-0.68
0.94-0.77
0.85-0.77
0.99-0.95
0.99-0.89
0.11-0.26
0.99-0.88
1-0.93
0.98-0.79
1-0.89
1-0.90
1-0.78
Small
0.01-0.08
0.08-0.26
0-0.18
0-0.05
0.02-0.23
0.01-0.13
0.09-0.32
0.06-0.23
0.15-0.23
0.01-0.05
0.01-0.11
0.89-0.74
0.01-0.12
0-0.07
0.02-0.21
0-0.11
0-0.10
0-0.22
Large
Metaxylem diameter
(Fig. 5)
Probabilities of inferred ancestral states for ecology and metaxylem diameter for representative trichomanoid clades. The values correspond to the
probability of each state on selected clades according to an MK1 (‘Markov K-state one-parameter’) model (single value) or to an MK1 model and an
AsymmMK (‘Asymmetrical Markov K-state two-parameter’) model (two values; for colonial epiphytism, climbing habit and metaxylem diameter).
Highest probabilities are highlighted in bold. Clades (also reported in Figs 2–5): Ca, Callistopteris; Ce, Cephalomanes; Ab, Abrodictyum; Tr,
Trichomanes; D, Trichomanes subgenus Davalliopsis; L, Trichomanes subgenus Lacostea (T. ankersii–T. pedicellatum); HE, ‘(hemi)-epiphytic’ clade
(see text); Po, Polyphlebium; Cr, Crepidomanes; Va, Vandenboschia; Di, Didymoglossum; N, Crepidomanes subgenus Nesopteris; C, Crepidomanes
subgenus Crepidomanes.
APPENDIX
EPIPHYTISM EVOLUTION IN TRICHOMANOID FERNS
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 573–593
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