Bo~anical.7obumalofthe Linnean Soriely (ZOOO), 132: 2 9 4 6 . With 6 figurcs
doi: 10.1006/bojl.1999.0277, available online at htto://www.idedibrary.com o n
I D E bl"
@
Morphology and anatomy of roots in the filmy
fern tribe Trichomaneae H. Schneider
(Hymenophyllaceae, Filicatae) and the evolution
of rootless taxa
HARALD SCHNEIDER
7 h e Field Museum, Chicago, Illinoh 60605-2496, USA
Received September 1998; accepted for publication May 1999
The filmy ferns of the tribe Trichomaneae, synonymous with Tichomanes d.,
show various
constructions of their root system that correspond to different growth forms as well as
ecology. Most terrestrial species possess a short erect shoot with numerous thick roots,
whereas epiphytic species have a long creeping rhizome that may develop a few thin roots.
An evolutionary progression from ferns with well-developed roots to ferns without roots is
postulated. Rootless species occur in two monophyletic groups, subgen. Cnpidomancr and
subgen. Didymoglossum. The results are summarized in a new classification for the tribe.
Secondary simplification, e.g. loss of roots, is discussed as an adaptive trait in epiphytic
plants. Transformed structures such as root-like shoots and adhesive hairs are observed in
rootless taxa and their evolutionary significance is briefly discussed. Climbing Nmy ferns are
recognized as possible closely related species based on the similarities in their root systems.
0 2000 The I.innean Society of London
ADDITIONAL KEY WORDS:-growth form - phylogeny - hairs - rhizoids
root hairs - secondary simplification - Ti-ihomanes.
~
rhizome -
CONTENTS
Introduction . . . . . . . . . . . . . . .
Material and methods . . . . . . . . . .
Results . . . . . . . . . . . . . . . .
Presence of roots on adult sporophyte . . . .
Comparison of hair types of Hymenophyllaceae
Root-like rhizomes of rootless species . . . .
Anatomy of roots . . . . . . . . . .
Discussion . . . . . . . . . . . . . . .
Ecology. . . . . . . . . . . . . . .
Morphology . . . . . . . . . . . . .
Systematics . . . . . . . . . . . . .
Evolution . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . .
References . . . . . . . . . . . . . . .
Appendix. . . . . . . . . . . . . . . .
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0 2000 The Linnean Society of I-ondon
30
H. SCHNEIDER
INTRODUCTION
The filmy ferns have often attracted the interest of pteridologists and other
biologists in the past because of their peculiar morphology. They are common plants
in tropical forests in which they prefer environments with extremely wet conditions
(e.g. foggy forests). Two or three monophyletic groups are distinguishable on
various characters (Tryon & Tryon, 1982; Iwatsuki, 1984, 1990; Schneider, 1996):
Cardiomanoideae and Hymenophylloideae with the two tribes Hymenophylleae
and Trichomaneae (classification according to Schneider, 1996). Classifications of
the Trichomaneae were proposed by Copeland (1933,1938), Morton (1968), and
Iwatsuki (1984, 1990).All recognized the Trichomaneae as a putative monophyletic
group, but the number of accepted genera varies between 18 genera (Copeland,
1938), one genus (Morton, 1968) or three genera (Iwatsuki, 1990). However Morton
and Iwatsuki accept most of Copeland’s genera as groups of various taxonomic
rank. The three classifications are compared in Dubuisson (1997a). Cladistic studies
based on morphological characters as well as rbcL nucleotide sequences (Dubuisson,
1997a, b) indicate two major branches and close relationships of the two epiphytic
subgenera Crepidomanes and Didymoglossum. Further studies including more taxa and
characters are required. Unfortunately some characters are known from only a few
species. This is the case in important character sets such as gametophytes (Yoroi,
1972; Dassler & Farrar, 1997) and spores (Tryon & Lugardon, 1990). More
comparative examinations similar to the studies of the growth forms given by
Htbant-Mauri (1972) are needed. Additional detailed descriptions of character states
can be found in older botanical literature (Mettenius, 1865; RUSSOW,
1872; Prantl,
1875; Giesenhagen, 1890),but it is often difFicult to recognize the valid name. Roots
as a valuable character complex are mostly ignored in recent discussions on the
systematics of the filmy ferns, although lack of roots in some epiphytic taxa has
been documented for more than a century (Mettenius, 1865; Russow, 1872;
Prantl, 1875; Lachmann, 1886; Troll & Wetter, 1952; Wessels-Boer, 1962). Recent
investigations by Schneider (1996) have shown the importance of root anatomy for
the systematics and phylogeny of ferns.
MATERIAL AND METHODS
Specimens of Hymenophyllaceae have been studied from the herbaria of Aarhus
(AAU), Berlin (B), Chicago (F),Kew (K), Leiden (L), Natural History Museum
London (BM), and Zurich (Z, ZT). H. Tuomisto (TUR) has kindly made available
some specimens of climbing filmy ferns collected in Peru. These specimens were
deposited in TUR and L. Fresh material was collected by the author on field trips
in Ecuador, Malaya Peninsula and Borneo and fixed in 70% ethyl alcohol. Specimens
of these were deposited in Z and L. Sections for anatomical studies were prepared
with a freezing-microtome and examined by optical microscopy using polarized
light and various stains (Phloroglucin-HC1, Sudan black, Km. Root material taken
from herbarium specimens for anatomical studies was softened in 10% Tinoventin
solution for 3 to 5 days. Material for scanning microscope studies (SEM) was fixed
and preserved in 70% ethyl alcohol. The samples were critical point dried and
sputter coated (Au-Pd). The micrographs were taken with a Cambridge S4 SEM at
20 kV.
ROOTS OF 7 7 U C H O W E S
31
TABLE
1. Root systems and their characters. Symbols: - absent; + present; (+) often but not always
present
Growth-form
Rhizome length
Dimorphic
rhizomes
Adhesive
roots
habitat
RS I
RS IIa
RS IIb
RS IIc
RS 111
RS IVa
RSIVb
erect
short
-
creeping
long
creeping
long
-
creeping
long
-
climbing
long
+
creeping
long
-
creeping
long
+
+
-
+
terrestrial
-
-
+
(+)
+
+
climbing
shoots
+
root-like
shoots
+
(+)
terrestrial, epiphytic or epiphytic or climbing on epiphytic or epiphytic or
epipetric
epiphytic or epipetric
epipetric
trees or
epipetric
rocks
epipetric
(+I
All species are listed under valid combinations of the genus Tnchomanes s.1. because
this facilitates finding them in literature. Names of genera, subgenera, and tribes
follow the classificationgiven in the Appendix. The classification is based on Iwatsuki
(1 984,1990) but modified to reflect the results of the studies of Dubuisson (1997a,
b) and the presented results. Dubuisson (1997a) provided a comparison of corresponding taxa in the classifications of Copeland (1938), Morton (1968) and
Iwatsuki (1984,1990). For example, Crepidomanessection Maiora (Iwatsuki, 1984,1990)
corresponds to kndenboschia (Copeland, 1938). The term rhizome is always used for
the shoot of Hymenophyllaceae even though the term shoot is also correct. It is
practice to call the creeping shoots of ferns rhizomes.
RESULTS
Presence of roots on adult sporoplyte
The species of Trichomaneae differ in their root systems as well as growth forms
described by HCbant-Mauri (1972).The growth forms of filmy ferns show differences
in the following features: rhizome (length and diameter), phyllotaxis (spiral or
distichous), and root (if present; number, position, size). Four major types of root
systems are defined as main growth forms (root system types RS I-RS IV),
occasionally with subtypes (Table 1). This classification differs partially from the
division of growth forms by Htbant-Mauri (1972), because her classification does
not consider the presence, number, and location of roots. However, the types
represent only main steps in a continuum of forms, and intermediates are found in
more thorough studies. This is especially the case in the transition of RS IIc to RS
IVa (Fig. 1).
RS 1. Ferns with an erect, semi-erect or rarely short creeping rhizome (more than
2mm thick), which possesses a large amount of thick roots (more than 0.5mm
thick). Leaves are arranged in a spiral phyllotaxis with internodes shorter than 5 mm.
The rhizome is covered with multicellular hairs. These ferns are normally terrestrial.
This growth form characterizes the greater part of Cephalomanes including subgenera
Abrodicpum, Callirtoptais, Cephalomanes, Davalliopsis, JVesopth, Paclyghna, and major
parts of Tihomanes.
H. SCHNEIDER
32
thick rhizome
root-like shoot
-;
thin rhizome
4 ;substrate
-
. ..... .
;root
- leaf
;soil
-- - -
;
postulate direction of evolution - 0
Figure 1. Scheme of transformation series of growth form in Trichomaneae.
RS IIa. Ferns with a long creeping rhizome (more than 2 mm thick), which possesses
many roots (more than 0.5 mm thick). There are often 2-6 (rarely 10) roots per
leaf. The leaves show spiral or distichous phyllotaxis with internodes more than
5 mm. The rhizome is covered with multicellular hairs. These ferns grow as epiphytes
or terrestrials on soil or rocks. Species with this growth form exist in Cephalomanes
(subgen. Macroghna) and Crepidomanes (subgen. Maiora sect. Maiora (pro parte).
ROOTS OF IRICHOALWES
33
RS ZZb. Ferns with a long creeping thin rhizome (not thicker than 2 mm) with more
than four roots per leaf. The roots are thin (0.2-0.4mm in diameter). The leaves
show distichous phyllotaxis with internodes more than 5 mm. Multicellular hairs
densely cover the rhizome. These ferns always grow as epiphytes on tree branches
densely covered by mosses. This type is found in Crepidomanes subgen. Pleuromanes,
Trichomanes (subgen. Trichomanes, sect. Acopricum), Hymenophylleae and Cardiomanes
(Schneider, 1996).
RS ZZc. Ferns with a long creeping thin rhizome (diameter not exceeding 1 mm) with
few, thin roots (0.2-0.4 mm thick). The leaves show distichous phyllotaxis with
internodes more than 5 mm. The rhizome is covered with adhesive hairs on each
side. Roots are restricted to parts of the rhizome. Therefore smaller specimens may
lack roots completely, but larger collections always show small parts of the shoot
with roots. The outgrowth of roots seems to correlate with the humidity of the
substrate (facultative root development). These ferns are epiphytic or sometimes
epipetric. This growth form is found only in Crepidomanes subgen. Maiora.
RS ZIZ. Ferns with a long climbing rhizome (more than 2 mm thick) with distichous
phyllotaxis and a terrestrial short rhizome with a spiral phyllotaxis. Normally the
climbing part of the rhizome is rootless and roots occur only in those parts of the
rhizome which grow in the soil. These roots are long, very thick (more than 0.5 mm)
and arranged as in RS I. The lower side (against substrate) of the climbing rhizome
is covered with adhesive hairs, whereas the often naked upper side of the shoot has
a green colour. They occur as climbing ferns on trees and occasionally on rocks in
wet tropical forests. This growth form occurs in Crepidomanes (subgen. Crepidomanes
sect. Lucostea and sect. Maiora pro parte).
RS IVa. Ferns with a long creeping thin rhizome (diameter not exceeding 1 mm),
without roots. The leaves are arranged in one or two rows (monostichous or
distichous). The rhizome is densely covered by adhesive hairs, which often consist
of only two or three cells. These ferns are usually epiphytic or occasionally epipetric.
This growth form characterizes Crepidomanes subgen. Didymoglossum and subgen.
Crepidomanes, but it is also found in a few species of subgen. Maiora sect. Maiora.
RS ZVb. Ferns with a long creeping thin rhizome (diameter less than 1 mm), which
possesses root-like shoots but not typical roots. The rhizome is densely covered with
adhesive hairs. These ferns are epiphytic and/or epipetric. This growth form occurs
in Crepidomanes subgen. Crepidomanes sect. Crepidium (e.g. T. humile), sect. Crepidomanes
(e.g. T. bilabiatum, T. bipunctatum, T. latemargianle), sect. Phlebiophyllum (e.g. T. venosum)
and subgen. Didymoglossum sect. Lecanium (e.g. T membranaceum).
Comparison o f hair gpes o f Hymenophyllaceae
Duckett et al. (1996) distinguished three hair types in the filmy ferns: “root hairs”,
“persistent multicellular, linear to stellate hairs”, and “short lived clavate bicellular,
glandular hairs”. The epidermis of the leaf and shoot is usually accepted as not
homologous to the rhizodermis (i.e. epidermis of the root). Root hairs are unicellular;
they develop by prolongation without any cell division of the trichoblast. In contrast,
hairs of the rhizome and leaf develop by a cell division of the trichoblast (Peterson
& Farquhar, 1996). Therefore the hair-like structures of the fern sporophyte can be
H. SCHNEIDER
34
TABLE
2. Comparison of root, adhesive, and other hairs
Criterion
Position
Connection Lo the epidermal cell
Internal divisions
Colour
Function
Root hairs
Adhesive hairs
Other hair types
root
rhizome and leaf
rhizome and leaf
non septate
septate
septate
none
0-3
0-3 or more
brown
colourless to black
brown to black
water and nutrient uptake
anchorage
other or unclear functions
divided into two non-homologous classes: (1) root hairs (hairs of the root); (2) hairs
(hairs of the leaf and rhizome) with the two subtypes according to Duckett et
al. (1996). To the latter a third subtype is added which has previously been
misinterpreted-hairs that consist of the basal cell and only one (rarely two or three)
hair cells (Table 2). These hairs look similar to root hairs (Fig. 6) and they may be
the hair type from which Duckett et al. (1996) described chloroplasts. The technical
term ‘adhesive hairs’ is suggested for these hairs because this name fits the origin
and character of the structure better than other suggested terms such as ‘Haarwurzeln’
(Mettenius, 1865)or rhizoids. Adhesive hairs are defined here as hairs of the rhizome
and petiole (occasionally rachis) that are developed by cell divisions of epidermal
cells and composed of one or more hair cells with a stiff texture. Their function is
to anchor the plant to the substrate. This is normally the function of roots, but not
of root hairs which have an unsuitable, soft texture. It is not known if these hairs
produce any mucilage coatings similar to that produced by root hairs or rhizoids
(Farrar & Wagner, 1968). Adhesive hairs are not structurally similar to rhizoids
of the gametophyte generation. However, gametophytic rhizoids share structural
similarities with root hairs, Adhesive hairs are found on the rhizome of rootless
species (RS IV), on the rhizome of epiphytic species with a thin rhizome (RS IIb),
and on the lower side of the climbing rhizome of climbing filmy ferns (RS III). They
are also present on the petiole and rachis of some epiphytic species that possess
adhesive hairs on the rhizome.
Root-like rhizomes of rootless species
Some larger rootless species possess short rhizomes (Ankersprosse)that show the
following characters (Figs 2, 6): dichotomous branching, plagiotropic growth, and
rarely reduced leaves or leaf buds. These rhizomes are very similar to roots in their
shape. These organs were first recognized by Mettenius (1865).Later Troll & Wetter
(1952) emphasized the similarities of root-like rhizomes and normal rhizomes. In
Table 3, criteria are listed for determination of root-like rhizomes including criteria
for rhizomes and roots. Root-like rhizomes fulfil mainly the criteria of rhizomes,
but they differ in their branching from the main rhizome. Additionally, position
and development indicate a homology between the root-like rhizome and the
rhizome. Intermediate forms between both are easily found in larger collections
which indicates the importance of environmental influences during the differentiation
of the rhizome. Root-like rhizomes are found in species, which lack true roots,
especially Crepidomanes subgen. Crepidomanes (T. humile, ‘I: latemaq$nale) and subgen.
Di&moglossum (T.membranaceum).
ROOTS OF 7RICHOM.4NES
35
2
Figures 2-5. Fig. 2. Root-like shoot of Tichomanes (C@idomnes) bipunctatum Poir., thin rhizome with
hairs, leaves and root-like shoot; s=shoot, l=leaf, -+ =root-like. shoot, Scale bar= 1 cm. Fig. 3. Crosssection of root of Tiichomanes (Cephalomanes) mazlium Bory, o =outer, i =inner cortex, e =endodermis,
r = rhizodermis. Scale bar =0.1 mm. Fig. 4.Cross-section of root of Tnchomanes fliichornanes) omundoides
DC., abbreviations as in Fig. 3. Scale bar=0.1 mm. Fig. 5. Cross-section of root of Tichomnes
(Cwpidomanes) pallidurn Blume, abbreviations as in Fig. 3. Scale bar =0.1 mm.
Anatomy of mots
Among taxa of Trichomaneae roots differ in the number of cell layers of the
cortex, stages of endodermis and numbers of protoxylem poles. The rhizodermis is
one cell layer thick and consists of relatively large cells that sometimes show slightly
thickened outer walls. The cortex is divided into two areas: an outer cortex with
1-3 layers of parenchymatous cells, and an inner cortex with 3-10 layers of
sclerenchymatous cells. In contrast to other ferns the outermost cell layer of the
H. SCHNEIDER
36
TABLE
3. Comparison of roots, rhizomes and root-like rhizomes. Note: An organ is interpreted as
associated with a leaf site if o n e leaf corresponds t o one rhizome or root. M o r e than o n e root is
developed p e r leaf and roots a r e not restricted t o just around the nodes. Although new branches of
the rhizomes are usually n o t developed in the mils of leaves, the branch is clearly connected to a leaf
in all Hymenophyllaceae
Criterion
root
root-like rhizome
rhizome
Initiation
endogenous
exogenous
exogenous
Position
not associated with leaf site
associated with leaf site
associated with leaf site
root like development of
lateral roots
dichotomous branching
with four cutting faces
with three cutting faces
dichotomous to strong
anisodichotomous
branching
with three cutting faces
Branching type
Apical cell
Presence of a root cap
Growth
Growth direction
lndumentum
Presence of leaves
present
absent
absent
positive geotropic or
negative heliotrope
plagiotropic
orthotropic or plagiotropic
f determinate
f determinate
It indeterminate
root hairs
adhesive hairs
multicellular hairs and/or
adhesive hairs
without leaves
without leaves but sometimes
with rudimentary leaf
primordia
with leaves
Position of protoxylem
exarch
Presence of chloroplasts
without
with chloroplasts
with chloroplasts
brown to black
green to black
green to black
half or less
equal to half
equal
allsent
present
present
Colour of the surface
Diameter in comparison
to main rhizome
Presence of cuticle
endarch to mesarch, rarely endarch to mesarch, rarely
exarch
exarch
inner cortex always possesses thicker cell walls than cells of other cell layers. The
thickness of the cell walls increases successively from the innermost to the outermost
cell layer of the inner cortex. Three types of root cortex (RC) are found in Tnchomanes
s.1. Cells of the cortex contain starch grains in some species, whereas silicate crystals
are only found in the outer cortex of Tichomanes osmundoides. They may be identical
to the crystals found in some cells of the leaf, the so-called ‘Deckzellen’ (Mettenius,
1865).
RC I. The cortex consists of an outer cortex with one to rarely two cell layers of
thin-walled, large cells and an inner cortex with one layer of thick-walled cells (Fig.
5). Roots of this structure are found in Pleuromanes and in some species of subgen.
Muioru. This root cortex characterizes Cardiomanes and Hymenophylleae (Schneider,
1996)
RC ZI. The cortex consists of an outer cortex with at least two or more cell layers
of thin-walled, large cells and an inner one with two or more layers of thick-walled
cells with a smaller diameter (Fig. 3). This anatomy is found in Cephalomanes (pro
park) and Maiora subgen. Maiora (pro park). The climbing filmy ferns generally show
this type of root cortex.
ROOTS OF ~UCHOMAJVES
37
Figure 6. Apex of root-like shoot of Trichomanes (Cmpidomanes) bipunctatum Poir., the apex is naked and
the first hairs are developed near to the apex. Scale bar=0.05 mm.
RC ZZZ.The cortex consists of an outer cortex with one cell layer of thin-walled cells
and an inner cortex with two or many layers of thick-walled cells with a smaller
cross-section (Fig. 4). Roots of this anatomy characterize subgen. T'richomanes and
subgen. Feea, but it is also found in the genus Cephalomanes.
The central cylinder is delimited by the endodermis which consists of one celllayer of cells with a suberin lamella in terrestrial species of T'richomanes (Schneider,
1996). Thin roots of Crepidomanes and T'richomanes often lack a suberin lamella, but
larger species often possess cells with this structure. The lack of a suberin lamella
correlates with the reduction of roots. The number of protoxylem poles varies among
species. Some species with very thin roots contain only one protoxylem pole, whereas
roots of Hymenophylleae always possess two. In Trichomaneae thicker roots often
have three or four protoxylem strands, but sometimes roots with 5 or 7 are found.
Russow (1872) have observed up to nine strands for roots of T'richomanes radicans.
DISCUSSION
Ecology
The filmy ferns are characterized by a mostly one-cell thick lamina and often
lack a cuticle. The lack of this protective coat restricts the filmy ferns to environments
with high humidity during most of the growing season. However, many species can
withstand repeated desiccation and revive with moisture much like bryophytes.
Therefore filmy ferns have the highest diversity in foggy forests in tropical mountains
or similar environments. The growth form (including root systems), as shown in
38
H. SCHNEIDER
Figure 1, is correlated with the ecology as expressed by Holloway (1923) and other
authors because a balance between water-uptake and transpiration can support each
growth form in one or more habitats. Terrestrial species mainly have the growth
form RS I but sometimes RS IIa. They most often occur near streams where their
large root systems can absorb enough water. Additionally these ferns show welldeveloped vascular tissue in roots and rhizomes. Occasionally these ferns also grow
on rock faces and very rarely as epiphytes.
The remaining growth forms are characterized by reduced root systems and a
transfer of root functions to other organs. In many, leaves can directly take up water
and nutrients due to the lack of a thick cuticle (Haertel, 1940).In others, the rhizome
may absorb the water. The cuticle is thin or nearly absent in the rhizomes and the
dense indumentum may attract and hold water by capillary attraction. Similarly the
anchorage function becomes a primary function of the creeping rhizomes and its
indumentum. Thus in small epiphytic species, roots would be more or less superfluous.
However, roots perform well as anchoring if enough root-space is available. Otherwise, hairs may act better as adhesive organs on very smooth substrates. Some of
the rootless species of Tiichomunes are found on very smooth barks with none or few
depressions. The anchoring capacity of a rootless plant is increased by increase in
surface area covered by adhesive hairs. Root-like rhizomes offer the advantage of
increasing the surface area and consequently the anchoring capacity of a rootless
plant. Rootless filmy ferns share their habitat with mosses (Giesenhagen, 1890;
Kuerschner, 1990)and competition with these may be a relevant evolutionary factor.
Climbing filmy ferns with terrestrial root systems (RS III) combine the possibility of
water uptake in the soil with water uptake from the host substrate and from the
atmosphere. The young plants grow as terrestrials with a root system similar to RS
I, which also supply water to the long-climbing rhizomes of the adult plant. This
may explain why these ferns possess the largest amount of vascular tissue in their
roots and rhizomes of all filmy ferns (Russow, 1872).
Morphology
Root-like rhizomes do not correspond completely with the classical root-shoot
model of vascular plants (CRS model). Structures not fitting the CRS model are
often called misfits (Rutishauser & Sattler, 1989)which are more adequately described
in terms of fuzzy morphology (Rutishauser, 1995) and/or process morphology
(Sattler, 1992, 1994).The root-like rhizomes possess a combination of characters of
the rhizome (i.e. shoot) and root. Therefore they are often misunderstood in
descriptions based on a fixed concept of three organs. Root-like rhizomes can best
be described as partially analogous to roots, but homologous to shoots and retaining
a dominance of shoot characters. Similarities to roots reflect functional constraints,
whereas similarities to shoots are based on identity of developmental processes.
Anchoring with hairs is an alternative trait to root systems but they are less efficient
than roots. The increase of the rhizome surface compensates partly for the limitations
of mechanical resistance of this anchoring system. Both types of anchoring systems
are located on independent adaptive peaks in the image of an adaptive landscape
(Wright, 1932; Waddington, 1966). Plants capable of securing an adequate supply
of water without roots can explore the potentials of growth forms without roots.
Rootless plants are either floating aquatics such as Sulviniu or they grow epiphytic/
39
ROOTS OF TRICHOMA.NES
TABLE 4. Occurrence of root system, adhesive hairs, root-like shoots, and root anatomical features in
the genera of Trichomaneae (according to the classification of lwatsuki, 1990). Symbols: growth forms
(RS) classification as given above; root cortex classification as given above; - absent; + present; ( +}
often but not always present
Taxa
Root systems
(RS)
Adhesive
hairs
lib
+
Ila-IIc-III
III
+I-
IVa
IVa-IVb
IVa-IVb
IVb
IVa-IVb
+
+
+
+
+
Root-like
rhizomes
Root cortex
(RC)
Number of Starch in the
PX-poles
root cortex
Crepidomanes
Subgen. Pleuromanes
Subgen. Maiora
Sect. Maiora
Sect. Lacostea
Subgen. Crepidomanes
Sect. Gonocormus
Sect. Crepidium
Sect. Crepidomanes
Sect. Phlebiophyllum
Subgen. Didymoglossum
Cephalomanes
Subgen.Abrodicryum
Subgen. Pachychaetum
Subgen. Macroglena
Subgen. Callistopteris
Subgen. Nesopteris
Subgen. Cephalomanes
Subgen. Davalliopsis
Trichomanes
I, II, III
II
+
+I+I-
4
+
+
+
(+)
+
+
+
(+)
II
II
II, III
II
II
II, III
II
I
I
I
I
I
I
I
I (-IIa)
H(9)
5-9
+I-
III
3--4
4--7
3
6
+
4--7
6
+I-
3--5
+I-
epipetric. Rootless epiphytes exist in various groups of vascular plants such as
Psilotaceae, Hymenophyllaceae (pro parte) and Bromeliaceae (pro parte). Benzig & Ott
(1981) discussed enhanced nutrient economy as the advantage of rootless species of
Ttllandsia. This may be partly true in filmy ferns with mosses as potential competitors.
Similarly the classification of hairs is quite difficult and needs further detailed
studies. Adhesive hairs are modified hairs which do not share any specific similarity
to root hairs and rhizoids of gametophytes. However, the term rhizoid is often used
for hair or hair-like structures with the function of anchorage or absorption. It may
be useful to reserve the term 'rhizoids' in higher vascular plants for hairs of the
gametophytes. However, it is not known if the same genes regulate the development
of hair-like structure in the gametophytic and sporophytic generation.
Systematics
Few conclusions can be drawn regarding systematic implications of the root
anatomy because only a few species have been examined. From studies thus far,
two main groups may be distinguished in the construction of the root cortex (Table
4). The genus Trichomanes (sensu lwatsuki) has roots of the RC III-type whereas roots
of the RC II-type mainly occur in Cephalomanes and Crepidomanes subgen. Maiora.
However, some species in the latter two genera possess roots of the former type
(RC III). Roots of the RC II-type are also found in Lacostea suggesting a relationship
to subgen. Maiora, which is also seen in cladistic analysis (Dubuisson, 1997a) based
on anatomical and morphological data. Further investigations are needed to test
40
H.SCHNEIDER
whether Cephalomanes and the primitive members of Maiora are related, especially to
subgenera M a m g h a and AbrodicQum. The second taxon is placed in the Crepidomanes
group by Dubuisson (199713) based on the rbcL- nucleotide sequences. A second
question is whether the reduced RC I-type represents a primitive character state in
the Hymenophyllaceae or an advanced state, which has evolved independently in
Hymenophylleae and Trichomaneae. However, in Trichomaneae roots of the RC
I-type occur only in Phlebiophyllum and some epiphytic species of Maiora, which may
indicate that this character state is advanced.
Of more relevance are the root systems because a large set of species have been
investigated (Table 4). The principal subgenera and tribes are very constant in the
structure of their root systems. The two subgenera Didymoglossum and Crepidomanes
are always rootless, but the lack of an embryonic root pole has been demonstrated
only for T uenosum (Stone, 1958). If both subgenera are derived from the same
ancestor the proposed close affinities of Didymoglossum to Tiichomanes S.S. (Iwatsuki
1984, 1990) will be rejected. A progression from rooted to rootless forms is found
in sect. Maiora, which is closely related to subgen. Crepidomanes. This relationship is
reasonably congruent with the tree topology in cladistic analysis (Dubuisson, 1997a,
b). Similarities of root systems support a close relationship between two groups of
climbing filmy ferns, sect. Maiora (e.g. Lacosteopsis) and sect. Lmostea. This stands in
contrast to older classification proposing separate origins of these growth forms
(Morton, 1968).The variation in root systems of sect. Maiora is in need of ontogenetic
studies. It is possible that species possessing root systems with thick long-creeping
rhizomes (RC II) are primitive relative to those developing roots only on short parts
of the rhizome. The latter forms with facultative developed root systems are epiphytes
or climbing ferns, indicating possible relations of Maiora to Lacostea and Crepidomanes.
Differences in root systems support the separation of Macroglena and Selenodesmium.
Small differences among the sections of Trichomanes may have importance in phylogenetic analysis of this genus. Comparative studies of development of roots and
rhizomes may produce a better view of the evolution of this group.
Evolution
The filmy ferns are characterized by the decline of morphological and anatomical
complexity such as reduction of the number of cell layers of the lamina and thickness
or presence of a cuticle, Additionally, morphological variation in the gametophytic
generation including the capability of vegetative propagation is more prominent in
filmy ferns when compared to most other ferns (Farrar, 1985; Dassler & Farrar,
1997). Because little is known about the reproductive biology and ecology of tropical
filmy ferns (Dassler& Farrar, 1997),detailed examination of morphological characters
may give a better insight into the evolutionary trends in this family. The results
presented here document a continuum in reduction of complexity in a proposed
evolutionary series of character states from obligate rooted species, to facultative
rootless species, to completely rootless species, and finally to species with root-like
rhizomes. Additionally, this reduction of complexity is combined with a blurring of
organ distinction. A more complete analysis of this reduction series may result from
studies of the embryo and the first stages of the sporophytes. The only described
embryo of a rootless species, Trichomanes uenosum (Stone, 1958), does not develop a
root pole similar to the embryo of the rootless, aquatic fern Salvinia (Guttenberg,
ROOTS OF TMCHOhMNES
41
1968).In other species of Tichomanes a secondary loss of roots during the development
is possible. The embryo of Tichomanes alatum, the only other species with well-studied
early development, possesses well-developed roots but this species has the growth
form RS I. As mentioned above, it is quite unclear whether the most primitive state
is RS I or RS IIb. The most closely related genera, Cardiomanes and Hymenophyllum
have growth forms of RS IIb, which could be interpreted as the primitive state.
However, RS I seems more primitive in an ontogenetic view and From the fact that
some basal families of ferns have mainly erect rhizomes with large, well developed
root systems (Schneider, 1996). Two evolutionary scenarios are thus possible; RS I
is primitive with a continuous progression leading to RS IV,or RS IIb is primitive
with two progression lines. In both, RS I11 is a separate line with a possible origin
in RS 11.
The described continuous reduction series between species with roots and without
roots is helpful in understanding the evolution of taxa with a loss of complexity.
Convergent simplification leads to confusion in taxonomy and classification in this
group as well as other groups of ferns such as Vittariaceae (Crane, Farrar & Wendel,
1995). Organisms with reduced complexity often show organs, which are partially
different from the typical organ. The ‘non-appendicular leaf of the rootless section
Gonoconnus is a further example of ‘misfits’ in filmy ferns (Bierhorst, 1973, 1974;
HCbant-Mauri, 1990). Furthermore losses of complex structures are often combined
with the transfer of functions to other organs. Acquisition or waste of functions may
lead to transformation of the ontogeny and structure of an organ. Finally, the filmy
ferns are an outstanding example for exploring the role of secondary simplification
(Bateman, 1996) in plant evolution because the nearly complete transformation
series is living today.
ACKNOWLEDGEMENTS
For valuable comments I am very grateful to A. Miller (Chicago),R. Rutishauser
(Zurich) and an anonymous reviewer. Furthermore I want to thank the keepers of
the herbaria for permission to use their collections (B, BM, F, K, L, Z, ZT), F.
Rumsey (NHM, London) for information about Tichomanes speciosum, and especially
H. Tuomisto (Turku) for excellent collections of climbing filmy ferns from Peru.
The technical assistance (SEM) of U. Jauch (Institute of Plant Biology of the
University of Zurich) is gratefully acknowledged. Finally, I acknowledge the financial
support from the G. & A. Claraz Foundation (Switzerland) for a collecting trip
to Ecuador (1994) and from the European Commission (Grant NR
ERBFMBICT960900) for a collecting trip to Borneo (1997).
REFERENCES
Bateman RM. 1996. Nonfloral homoplasy and evolutionary scenarios in living and fossil land plants.
In: Sanderson MJ, Hofford L, eds. f f o m o p h q 7he recurrence of similnng in euolution. San Diego:
Academic Press, 9 I - 1 30.
Benzig DH, Ott DW. 1981. Vegetative reduction in epiphytic Bromeliaceae and Orchidaceae: Its
origin and significance. Biotmpica 1 3 131-140.
Bierhorst DW. 1973. Non-appendicularfronds in the Filicopsida. In:Jermy AC, CrabbeJA, Thomas
42
H.SCHNEIDER
BA, eds. The phylogeny and classification of the ferns. BotanicalJournal ofthe Linnean Socieb 67: suppl.
1: 45-58.
Bierhorst DW. 1974. Variable expression of the appendicular status of the megaphylls in extant ferns
with particular reference to the Hymenophyllaceae.Annals ofthe Missouri Botanic Gardens 61: 40&420.
Copeland C. 1933. Trichomanes. PhilippineJoumal ofscience 51: 11S280.
Copeland C. 1938. Genera Hymenophyllacearum. Phili&~ineJournal of Science 67: 1-1 10.
Crane EH, Farrar DRYWendelJF. 1995. Phylogeny of the Vittariaceae: Convergent simplification
leads to a polyphyletic Vittaria. Ameriian Fern Journal 85: 83-305.
Dassler CL, Farrar DR. 1997. Significance of form in fern gametophytes: clonal, gemmiferous
gametophytes of Callistopteris baueriana (Hymenophyllaceae). Inhational Journal Plant Science 158
622439.
Dubuisson JY. 1997a. Systematic relationships within the genus Tihomanes sensu lato (Hymenophyllaceae, Filicopsida): a cladistic analysis based on anatomical and morphological data. Botanical
Journal ofthe Linnean Sociep 123: 265-296.
DubuissonJY. 1997b. rbcL Sequences: A promising tool for the molecular systematics of the fern
genus Trichomanes (Hymenophyllaceae)?Molecular Phyolgmetics and Evolution 8: 128- 138.
Duckett JG. 1996. Trichomes in the Hymenophyllaceae. In: CarnusJM, Gibby M, Johns RJ, eds.
pteridology in perspective. Kew: Royal Botanic Gardens, 5 1 1-5 14.
Farrar DR, Wagner WH. 1968. The gametophyte of Trichomanes holophm Kuze. The Botanical Gazette
129: 210-219.
Farrar DR. 1985. Independent fern gametophytes in the wild. In: Dyer AF, Page CN, eds. Biology
of Pteridophyta. Pmceedings Royal So&& Edinburgh ser B 86: 361-369.
Giesenhagen C. 1890. Die Hymenophyllaceae. Flora n.x 48: 41 1-464, pl. 14-17.
Guttenberg H von. 1968. Histogenese der Pteridophyten. In: Handbuch do lj’lanzenanatomie vol. 7, 2.
Berlin: Borntrager.
Haertel 0. 1940. Physiologische Studien an Hymenophyllaceae. 11. Wasserhaushalt und Resistenz.
Protoplasma 4 489-5 14.
Hkbant-Mauri R. 1972. Le genre Thomanes L. (fougkres leptosporangikes). Adansonia sir 2, 12:
469-495.
HCbant-Mad R. 1990. The branching of Tihomanes pmlijkum (Hymenophyllaceae).CanadianJournal
ofB0tany 6 8 1091-1097.
Holloway JE. 1923. Studies in the New Zealand Hymenophyllaceae. Part 1. The distribution of the
species in Westland, and their growth-forms. Eansmtions Nm zealand Institutes 54: 577-618.
Iwatsuki K. 1984. Studies in the systematics of filmy ferns VII. A scheme of classification based
chiefly on the Asiatic species. Acta Phytotavonomy and Geobotany. 35: 165-179.
Iwatsuki K. 1990. Hymenophyllaceae. In: Kramer KU, Green PS, eds. The families and genera of
vascular plants. Vol. I. Plnidophyta and Oymnospm New York Springer.
Kuerschner H. 1990. Die epiphytischen Moosgesellschaften am Mt. Kinabalu (Nord-Borneo,Sabah,
Malaysia). Nova H e d M 51: 1-75.
Lachmann P. 1886. Observations sur la structure de la racine des Hymenophyllacees. Bulbtin Socip
Botanic &on sh 2,4: 42-46.
Mettenius G. 1865. Ueber die Hymenophyllaceae.Abhandlungen der Koen$ichm saechsischen Gesellschaft
der Wusenschajh 11: 403-504, pl. 1-5.
Morton CV. 1968. The genera, subgenera, and sections of the Hymenophyllaceae. Contributions US.
National Herbarium 38: 153-2 14.
Peterson RL, Farquhar ML. 1996. Root hairs: specialized tubular cells extending root surfaces.
The Botanical Review 62: 1-40.
Prantl K. 1975. Untersuchungm zur Morphologie der Gefdkvyptogamen. I. Hymenophyllaceae. Leipzig:
Engelmann.
Russow E. 1872. Vergleichende Untersuchungen betreffs die Histologie der Leitbiindel-kryptogamen.
Mhoirs de I’Academy de Sociep St. Petersbourgh. sh. 29: 1-95.
Rutishauser R. 1995. Developmental patterns of leaves in Podostemataceae as compared to more
typical flowering plants: saltational evolution and fuzzy morphology. Canadian Journal of Botany 73:
1305-1 3 17.
Rutishauser R, Sattler R. 1989. Cornplernentarily and heuristic value of contrasting models in
structural botany: 111. Case study on shoot-like “leaves” and leaf-like “shoots” in Uhicularia macmrhba
and LJ. purpurea (Lentibulariaceae).BotanischeJahrbiicher der @stematik 111: 121-137.
Sattler R. 1992. Process morphology: structural dynamics in development and evolution. Canadian
Journal ofBotany 70: 70Ck714.
ROOTS OF TRICHOhwNES
+3
Sattler R. 1994. Homology, homeosis, and process morphology in plants. In: Hall BK, ed. Homology.
llte hierarchical basis of comparative bwlogr. San Diego: Academic Press, 423475.
Schneider H. 1996. Vqlleichende Wur<elanatornie der Fame. Aachen: Shaker.
Stone IG. 1958. The gametophyte and embryo of Po!yphlebium venosum (R.Br.) Copeland (Hymrnophyllaceae). Australian Journal ofBotany 6 183-203.
Troll W, Wetter C. 1952. Beitraege zur Kenntnis der Radficationsverhaeltnisse von Farnen.
Abhandlungen der Akademie der WusenschaJten und Literature Main~jNatunuissensch~~liche
Klasse 1: 1-84.
Tryon AF, Lugardon B. 1990. Spores ofthe pteridophyta. New York Springer.
Tryon RM, Tryon AF. 1982. F m and allied plants with special refmce to tropical America. New York:
Springer.
Waddington CH. 1966. Principles of development and dtffmntiation. New York MacMillan.
Wessels Boer JG. 1962. The New World species of Trichomanes sect. Llidymoglossum and Micmgonium.
Acta Botanica Neerlandica. 11: 277-330.
Wright S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Pmctedings
ofthe Sixth International Congress of Genetics 1: 356-366,
Yoroi R 1972. Studies on spore germination and gametophyte of Japanese Hymenophyllaceae.Srience
Reporb ofthe 7olfyo Xyoika Dingaku B 15: 8 1- 1 10.
APPENDIX
List
of obsmed species includitg notes on the gmuithforms and mot cortex structure
All studied species are listed with the notation of the construction of the growth forms (RS X) and
the root cortex structure (RC Y), if these have been examined. Both follow the classification given in
the text. The classification of genera is based mainly on Iwatsuki (1 984, 1990) but has been modified
according to results of Dubuisson (1997 a, b). Additionally the sections of Morton (1968) have been
recognized for the genus Tichornanes. Tichomanes cn$um L. is accepted as the type species of T'richomanes.
In the text of this publication all species are named as species of the genus Tihamanes because it is
more practical for comparisons with other classifications.
Tribe Trichomaneae H. Schneider
Genus Ckepidomanes C.Pres1
Subgenus Maiora (Prantl) K. Iwat
Section Maiora Prantl
7: abmtan$lium Bosch RS IIc, 7: mutilobum Ching RS IIc, 7: ajzcanum Christ RS IIc, 7: ambile
Nakai RS IIc, 7: anptatum Carmich. RS IIc, 7:aphlebiodes Christ RS IIa, RC 11, 7: auriru/atum Blume
RS 111, 7: birmanicum Bedd. RS IIa, RC 11, 7: boschianum Sturm RS IIc, 7: brachyblastos Mett. RS I-IIa,
7: capilheum L. RS IIc, RC I, 7: cellulosurn Klotzsch RS I, RC 111, 7: chevalim' Christ RS IIc, 7:
clathraturn Tagawa RC Wa, T c o h s o i Hook.F. RC IIc, T collariaturn Bosch RC 111, RC 11, 7: cyrtohcn
Hillebr. RS IIb-IIc, 7: davallioides Gaudich. RS IIa-111, 7: diaphanum Humb., Bonapl. Et Kunth RS
IIc, RC I, 7: draytonianum Brack. RS IVa, 7: exsecturn Kunze RS IIc, 7:&llau Christ RS IV, 7:fargesii
Christ RS 111, 7: &anteurn Bory RS IIa, 7: herzogii Rosenst. RS IIc, 7: hpenophylloides Bosch RS IIc,
7:johnstonme F.M.Bailey RS IIc, 7: inopinnatum (PicSerm.) J.E.Burrows RS IIc, 7: liukiumse Y.Yabe
RS IIa, 7: maximum Blume RS IIa, 7: melanotnchiurn Schltdl. RS IVa, 7: mettmii C.Chr. RS IVa, I:
orientalis C.Chr. RS IIa, 7: Philippianurn Sturm RS I, I: pyxid@twn L. RS IIc, 7: radicam SW. RS IIa111, 7: ncpestre (Raddi) Bosch RS Ilc, I: scandm L. RS IIa, I: schrnidianum Zenker RS IIc, I: speciosurn
Willd. RS IIa, RC 11, 7: sho$hon Christ RS IIc, 7: subclathraturn (K.Iwats,) Morton RS IIc, 7: tenerum
Spreng. RS IIc, 7: titibuensis H.Ito RS IVa.
Section Lacostea (Bosch) Christ
7:ankersii C.Parker RS 111, RC 11, 7: pedicellatum Desv. RS 111, 7: lanaicum Baker RS 111, RC 11, 7:
tumkheimii Christ RS 111, RS 11.
14
H. SCHNEIDER
Subgenus Pleummanes (C.Pres1) K.Iwats
7: acutum C.Pres1 RS IIb, T. album Blume RS IIb, T. retusum (Copel.) Morton RS IIb, 7: pallidum
Blume RS IIb, RC I.
Subgenus Crepidomanes (C.Pres1)Prantl
Section Crepidomanes (C.Pres1) Prantl (including Taschneria C.Chr.)
T. bilabiatum Nees Et Blume RS IVb, T. bipuncbtum Poir. RS IVb, 7: bnv$es (C.Pres1) Baker RS N b ,
T. christii Copel. RS IVb, T. clurenceanum F.Ballard RS N a , 7: instgne Bedd. RS IVa, T. intramagnatum
Hook. Et Grev. RS IVb, T. kurzii Bedd. RS IVa, T. latealatum (Bosch) Christ RS IVb, 7: latemaginab
D.C.Eaton RS Nb, 7: majorae Watt RS IVa, T. makinoi C.Chr. RS Ik,T. megistostomum Copel. RS Nb,
T. plicatum (Bosch) Bedd, RS Ab,7: pmenulosum Alderw. RS IVa, T. mthertii Alderw. RS IVa, T.
rupicolum Racib. RS IVa, I: sarawakensis (K.Iwats.) Croxall RS IVb, T wallen' Watt RS IVa, T. venulosum
(Roscnst.) Copel. RS IVb.
Section Crepidium (C.Resl) comb. nov.
T. endlicherianum C.Presl RS IVa, T. humile G.Forst. RS Nb, I:gracillimum Copel. RS IVa, T. samome
C.Chr. RS N a , T. uieilhrdii Bosch RS IVb, T. w e m ' Rosenst. RS IVa.
Section Phlebiophyllum (Bosch) comb. nov.
7: venosum R.Br. RS IVb.
Section Conoconnw (Bosch) Christ
7: alagensis Christ RS IVa, T. assimile Mett. RS IVa, T. boninicolum Nakai RS IVa, I: d$ium Blume
RS IVa, T. mannii Hook. RS IVa, T. matthewi Christ RS N a , T. minutum Blume RS N a , T. novoguinme
Brause RS IVa, T. p m l f m m Blume RS IVa, T. trinente Baker RS IVa, T. tgmannii Bosch RS N a .
Subgenus Didymoglossurn (Desv.) C.Chr.
Section Didymoglossum (Desv.) Morton
T. angurtzjivns (Fee) Wess. Boer RS IVa, 7: curtii Rosenst. RS IVa, 7: exiguum (Bedd.) Baker RS N a ,
T.gourlianum Grev. RS IVa, T. hymenoides Hedw. RS N a , T. krausii Hook. Et Grev. RS IVa, T. liberiense
Copel. RS IVa, T. lineolatum (Bosch) Hook, RS IVa, T. nummularium (Bosch) C.Chr. RS IVa, T. reptans
Sw. RS N a , T. ovale (Fourn.) Wess.Broer RS IVa, T. pinnatineroumJENM. RS IVa, T. puncatum POIR.
RS IVa, T.pussilum SW. RS IVa, T. petersii A.Gray RS N a .
Section Minogonium (C.Presl) Christ
T. ballaridanum Alston RS IVa, 7: beccarianum Ces. RS IVa, 7: bimalginaturn Bosch RS N a , T. cuqidatum
Willd, RS IVa, 'I: ekmanii Wess.Boer RS IVa, T. msum Willd, RS IVa T.@lgens C.Chr. RS IVa, T.
henzaianum Parish RS IVa, T. hooken' C.Presl RS IVa, 7: kappearianum Sturm RS IVa, 7:mollyi Bosch
RS IVa, 7:sublimbatum MueLHal. RS IVa.
Section Lecanium (C.Pres1) Christ
T. membranacnrm L. RS IVb.
ROOTS OF 7RICHOAUNES
45
Genus Cephalomanes C.Presl
Subgenus Cephalomanes (C.Presl.) K.Iwats
7: atlouirens (C.Pres1) Kunze RS I, RC 2, 7: cramrn Copel. RS 1, 7: densinervum Copel. RS I , 7:
javanicum Blume RS I , RC 3, 7:madagascanensk T.Moore RS I , 7:preselii Morton RS I , 7:singaporeana
(Bosch) Alderw. RS I.
Subgenus Macoglena (C.Pres1) K.Iwats
7: ma-grqi Bosch RS I , RC 111, 7: caudatum Brack. RS IIa, 7: compactum A l d m . RS I, 7:.pavofiucum
Bosch RS IIa, 7:gemmatum J.SM. RS I-IIa, 7: indoneum Morton RS I-IIa, 7: laetum Bosch RS I, 7:
me@lium Bory RS IIa, RC 11, 7:parvflorum Poir. RS I , 7:schlechkri Brause RS I, 7:schultzii Brause RS
IIa, 7:setaceum Bosch RS I, 7:strictum Menzies RS I-IIa, ?: trichophyllum Moore RS I.
Subgenus Selenodesmium (Prantl) K.Iwats
7:cupressoides Desv. RS I, 7:dentatum Bosch RS I , 7:elongatum A.Cunn. RS I , 7:f i n e u m E.Fourn.
RS I , 7: obscurum Blume RS I, RC 11, 7: rigdum SW. RS I , RC 111, 7: sblosum Poir RS I-Ha, 7:
tamarisc@nneJacq. RS I , 7:tereticaulum Ching RS I .
Subgenus Davalliopsis (Bosch) K.Iwats
7: elegans Rich. RS I, RC 11.
Subgenus Callktopt&ris (Copel.) K h a t s
7:api@lium C.Presl. RS I, RC 11, 7: bauerianum Endl. RS I .
Subgenus Nesopt& (Copel.) K.Iwats
7:blepha~kmonCopel. RS I , 7:grande Copel. RS I , 7:intermedium Bosch RS I , 7:pseudoblephanstomum
Tagawa RS I, 7:superbum Backh. RS I, 7: thyanostomum Makino RS I , RC ID.
Subgenus Abmdictyum (C.Pres1) K.Iwats
7:cuminghii (C.Presl) C.Chr. RS I, RS 11.
Genus Tnchomanes L.
Section Achomanes C.Pres1
7: accedens C.Presl$!!-I I, RC 111, 7: adscendens Kunze RS I , 7: corcovadense Bosch RS I, 7: crkpijonne
Alston RS I, 7: crkpum L. RS I , RC 111, 7: Mistaturn KauK RS I, 7: delicatum Bosch RS I, 7: egleri
Windish RS I, 7:galeottii E.Fourn. RS I , 7:gardnm' Bosch RS I , 7:guianense Sturm RS I , 7:holoptmm
Kunze RS I , RC 111, 7:kalbrym' Baker RS I, 7: 1ucen.q SW. RS I , 7: ludovirianum Rosenst. RS I , 7:
macilentum Bosch RS Ila, 7:martiusii C.Pres1 RS I , 7:micayense Kunze RS I , 7:pe1lucen.s Kunze RS I ,
7:pilosum Raddi RS I , 7:plumosum Kunze RS I, 7: lobusturn Fourn. RS I, RC 111, 7: mraimense Jenm.
RS IIa, 7:sellowianum C.Pres1 RS IIa.
46
H. SCHNEIDER
Section Neumphyllum (C.Pres1) Moore
I: pinnatum Hedw. RS I, RC 111, I: uittaria DC. RS I.
Scction Odontosom (C.Presl) C.Chr
7: hostmannianum (Klotzsch)Kunze RS I.
Scction Trigono~hyllum(Prantl) C.CHR
I: arbuscula DESV. RS I, RC 111, 7: bicorne HOOK. RS I, RC 111.
Section Homeotes (Presl) C.Chr
I: humboldii (Bosch) Lelliiger RS IIa, I: spruceanurn Hook. RS IIa.
Section Feea (Boty) Christ
7: boQoides Kaulf. RS I, RC 111, I:diverrtfmns (Bory)Mett. RS I, I:mougeotii Bosch RS I, T ostnundoidcs
DC. RS I, RC 111, I: lmllii Bergdol RS I.
Section Raguteluv (C.Pres1) C.Chr.
I: crinitum SW. RS I, RC 111.
Section Acaparicum (Prantl) C.Chr
7: alatum SW. RS I, RC 111, T curranii WEATH. RS I, I:jrnbriatutn B A C W . RS I, I: pinnahifidum
BOSCH. RS I, T: po&odioide.r L. RS IIb, I: trigonum DESV. RS I.