Digital Pad Morphology in Torrent-living Ranid Frogs

12 Pages·1995·3.9 MB·

by  Annemarie Ohler

IJune 1995 Asiatic Herpetolo^ical Research Vol. 6, pp. 85-96
Digital Pad Morphology in Torrent-living Ranid Frogs
ANNEMARIE OHLER
Laboraloire desReptileselAmphibiens, Museumnationald'llistoire nalurelle,
25 rueCuvier, 75005 Paris,France
Abstract. -Digital pads of24 species ofranoid frogs (Raninae, Dicroglossinae, Ranixalinae, Rhacophorinae,
Hyperoliinae) were studied by scanning electron microscopy. In many species of Raninae the cells of the
adhesivepad are differentiated (elongated and wearing projections). Functional aspects ofcell morphology and
digital padexpansion arediscussed in relation with sticking condition in aquatic medium.
Keywords: Amphibia, Anura, morphology
Introduction lines could be distinguished by their digit
morphology. Ranines have digital pads
Digital pads occur in most of advanced with a latero-ventral groove, often separated
anuran families. This organ seems to be of terminally. Dicroglossines have digital pads
multiple origin and of difficult use in showing a dorso-terminal groove.
systematics (Noble and Jaeckle, 1928;
McAllister and Channing, 1982). Digital The histological structures of the digital
pads occur in arboreal anurans (Hyla), but pads were first described by Schuberg
they can also be observed in torrent-living (1895) and Siedlecki (1910). Noble and
frogs (Amolops), and in some fossorial Jaeckle (1928) undertook a comparative
species (Kaloula). In Asian and African histological analysis of 47 species of
frogs of the family Ranidae, several genera anurans. The fine structure ofthe epidermal
and species groups belonging to different cells in the digital pad has been observed by
subfamilies have fingers and toes bearing transmission electron microscope (Komnick
digital pads. and Stockem, 1969; Ernst, 1973 a-b).
Scanning electron microscopy has been used
There exists no strong hypothesis of to describe morphology of digital pads,
phylogeny of ranids as a whole. often in view of taxonomic utilisation or
Phylogenetic analyses were undertaken only functional interpretation (Welsch, Storch
for geographic and taxonomic limited and Fuchs, 1974; Green, 1979, 1980, 1981;
groups (Liem, 1970; Clarke, 1981; Hillis, Emerson and Diehl, 1980; Mc Allister and
1985; Emerson and Berigan, 1993). The Channing, 1983; Green and Simon, 1986;
broadly accepted classification (Frost, 1985) Green and Carson, 1988).
is based on Boulenger's works dating from
the beginning of this century (Boulenger, The epidermis of anurans has a
1882; 1920). Recently Dubois (1986, superficial layer ofhexagonal or pentagonal
1992) tried to review the entire group and squamosal cells, which are disposed in a
proposed a tentative classification which he regular way (Tyler and Miller, 1985).
sees as a working hypothesis. In this Differentiation ofthe pad leads to prismatic
hypothesis ranids are split into several epithelial cells. Their surface is usually
families, subfamilies and tribes (Dubois, hexagonal or pentagonal, as is that of
1992). Species that are enclosed in the generalized cells, but their height is more
genus "Rana" in Frost (1985) are in Dubois' important than in the latter. They are
classification distributed in several separated in their distal part forming deep
subfamilies (Table 1). crypts.
Results from study of skeleton showed In the dermis of amphibians both
several major lines in "Rana" (Deckert, mucous and venomous glands are present.
1938; Clarke, 1981). Study of the Their aperture is situated between the
morphology of the digital pads (Ohler and epithelial cells ofthe epidermis. On the pad
Dubois, 1989) confirmed that two of these
1995 byAsiaticHerpetologicalResearch
Vol. 6, p. 86 AsiaticHerpetologicalResearch June 1995
TABLE 1. Classification of Dicroglossinae and Raninae as proposed by Dubois (1992) and numbers of
species studied here. D: digital pad orexpanded digit tip present in some species at least; M: some species at
least in the genus Micrixalus in the classification given by Frost (1985); R: some species at least in the
genus Rana in the classification given by Frost (1985); the number indicates the number of species here
studiedby morphometry,external morphologyand/orscanningelectron microscopy.
Dircoglossinae
June 1995 AsiaticHerpetologicalResearch Vol. 6, p. 87
FIG. 1. Generalized plan ofdigital pad. Leftdorsal view; rightventral view, c: cover; df: dorsal fold; tk:
terminal knuckle; eg: circumferential groove; p: pad; bg: basal groove.
MNHN
FIG. 2. Digital pad ofRaninae with latero-ventralgroove (Rana (Hylarana)erythraea, 1987.3343,
Thailand), a: dorsal viewoffingerIII; b: ventral view offingerIII; stippledareacorresponds tothepad with
prismatic cells.
only openings of mucous glands can be lizards differ substantially from amphibians
observed. in having a dry or setal adhesive system
(Green and Carson, 1988).
The first authors (Schuberg, 1895;
Siedlecki, 1910; Noble and Jaeckle, 1928) Emerson and Diehl (1980) and Green
supposed that the products of the mucous (1981) independently showed that surface
glands were implicated in sticking function. tension was mechanically responsible for the
To complete sticking the epidermal cells adhesive abilities oftreefrog digital pads.
would allow attachement to natural surfaces As the surfaces ofplants have usually a low
that are covered with irregularities (Welsch, surface tension, the structure ofthe pad cells
Storck and Fuchs, 1974), somehow close to assures humidification responsible for
the mechanism of clinging in lizards. But adhesion. The grooves surrounding the pad
Vol. 6, p. 88 AsiaticHerpetologicalResearch June 1995
FIG 3. Digital padofDicroglossinae with dorso-tcrminal groove (Limnonectes (Bourretia)doriae,MNHN
1987.3130, Thailand), a: dorsal view oftoe IV; b: ventral view oftoe IV; stippledareacorrespondsto the pad
with prismatic cells.
serve as a reservoir for the fluid wetting formalin fixed and all had been stored in 70
%
agent (McAllister and Channing, 1983). alcohol. Finger II or IV or toe III were
cut on the terminal articulation. Cleaned
Numerous frog species with enlarged with ultrasonic sounds, they were
digital tips have been studied (Hyperoliinae, dehydrated in alcohol. After critical point
Hylidae, Telmatobiinae, Rhacophorinae, drying, they were gold covered (2-4 A).
and others), as well as the digital tips of Specimens were observed with the Scanning
Osnolmye sspoemceiesspweictihesouotfetnhlearfgaemdildiygiRtaalnitdipase. eMlNecHtrNonSmEiMcrfoascicloitpiees.(JPShMot-o8g4r0a)phsofwetrhee
have been studied in this respect, including taken on 120 Ilford FP4 film.
only species without digital pad. Here I will Measurements were taken with a slide
present the structure of digital pads and caliper (SVL) or a binocular microscope
digital pad cells of subfamilies of ranoids (FW): SVL - snout-vent length; FW - third
aRcacnoirxdailnignateo,DuDbiocirso'gl(o1s99s2i)nacel,assRifainciantiaoen,, ffiinnggeerr).widTtho(emlaimxiinmautem wsiizdethfaocftotirp,oFfWthirids
Rhacophorinae and Hyperoliinae. They given as a ratio of SVL (per thousand).
include arboreal ("Hylarana") and torrent-
living frogs (Amolops) that have digital pads Terminology of digital pad
with grooves and modified cells. For the morphology (Fig. 1, 2, 3)
torrent-living frogs a mechanism of sticking
is proposed and the correlation of cell (1) The circumferential groove (Green and
morphology, digit tip enlargement and Simon, 1986) (Fig. 1) surrounds the digit
biology ofthese frogs is outlined. tip latero-terminally and separating a dorsal
part from a ventral part. The groove may be
Material and methods complete or open (with a distal zone of
contact between the dorsal and ventral part).
Specimens representing 15 of 34 genera This is the generalized groove that is
and subgenera, possessing digital pads, as modified in various manners according to
recognised by Dubois (1992) were chosen the group offrogs observed.
MNHN
in the collection of (see Table 1,
Appendix I). They had been generally
June 1995 Asiatic HerpetologicalResearch Vol. 6, p. 89
- »i
FIG. 4. Squamosal cells with short spinulae, FIG. 5. Squamosal cells with microridges, ventral
ventral view, proximalofpaMdNofHfNingerIII view,outsidethecircumfMerNenHtiNal grooveoffingerHI
(Batrachylodesvertebralis, 1970.1407, (Amolops marmoratus, 1988.2787, Nepal).
Salomon
Islands).
r "V* '.J* tf"SS
FIG. 6. Squamosal cells with spongious FIG. 7. Sqamosal cells with hallow tubercles,
structures, dorsall view, on subunguis close to the ventralviw,proximal ofpadoffingerIII {Ingerana
MNHN
dorso-tenninalfoldoffingerIII(Ingeranatasanae, tasanae, 1987.2002,Thailand).
MNHN
1987.2002, Thailand).
(2) The basalgroove (Fig. 1) is the basal
(a) The latero-ventralgrooves (Ohler limit of the digital pad. Fusion of this with
and Dubois, 1989) (Fig. 2) close the pad, the circumferential groove results in a
that is oftriangular shape, laterally. In some circumplantar groove. The latter is not
species they join distally and close to a present in all digital pad types.
unique groove arround an oval or rounded
pad. (3) The ventral part is the proper
adhesive organ, the pad (Savage, 1987)
(b) The dorso-terminal groove (Fig. 1). Its latero-terminal limits are
(Ohler and Dubois, 1989) folds on the usually distinct formed by the groove. Its
dorsal part of the digit. The pad is of oval basal limit is intergrading, and the basal
or rounded form. In species where the groove, if present, is not the limit of the
groove is more pronounced its lateral parts functional part as indicated by presence of
can be observed ventrally (Fig. 3). modified cells still beyond this limitdistally.
Vol. 6, p. 90 AsiaticHerpetologicalResearch June 1995
TABLE
2. Distribution ofprismatic cell types and relative width oftip ofthird finger in ranoid frogs. - Cell
differentiation: L: elongated prismatic cells; R: regularly outshaped prismatic cells; H: cells ofheterogeneous
shape; P: projections on proximal border of prismatic cellls; S: small projections on proximal border of
prismatic cells; N - noprojections on prismatic cells; -: no prismatic cells in the digit tip. - Relative width of
tip ofthird finger, measured by FW/SVL: x: mean; s: standard deviation; n: number ofspecimens measured;
EV: extreme values ofratioFW/SVL in group.
Species studied
June 1995 Asiatic HerpetologicalResearch Vol.6, p. 91
FIG. 8. Regularoutshaped prismatic cells with FIG. 9. Elongated prismatic cells with disatal
mucousgland poreonpadoffinger III (Hyperolius projections on pad offinger III {Amolops sp. 1,
MNHN MNHN
viridiflavuskarissimbiensis, 1988.1055, 1987.2163,Thailand).
Rwanda).
FIG. 10. Elongated prismatic cells with distal FIG. 1 1. Elongated prismatic cells with small
projections on pad offinger III {Amolops sp. 3, distal projectionson pad offingerIII {Amolops
MNHN MNHN
1987.2140,Thailand). marmoratus, 1988.2787,Nepal).
FIG. 12. Orientation and distribution ofprismatic FIG. 13. Distribution ofprismatic and sqamosal
cells on distal partofthedigitalpadoffingerIIIof cellson theextremedistalpartofthedigital padof
Rana(Odorrana)andersoni(MNHN 1938.57, fingerIII ofRana (Sylvirana) sp. (MNHN
Vietnam). 1987.3471,Thailand).
Vol. 6, p. 92 AsiaticHerpetologicalResearch June 1995
The epidermal cells In the species of the genus Amolops,
this kind of cells is present with well
On the tips of the digits one observes developed projections (Fig. 9, 10). These
two major cell types (squamosal cells and were also observed in different "subgenera"
prismatic cells) with intermediary cells that of the genus Rana (Odorrana, Amnirana,
occur in high numbers in the proximal pad Hylarana, Chalcorana) and in Indirana
zone. gundia (Ranixalinae). The prismatic cells of
these species vary in their elongation, in the
(1) Squamosal cells. This is the size of the projection, and in the degree of
generalized cell type, covering the body of regularity. They are often rather regularly
amphibians (Tyler and Miller, 1985). The hexagonal, rounded proximally, with small
cells often show short spinulae (Fig. 4) or distal projections, as in Rana (Chalcorana)
structures called microridges (Fig. 5). In chalconota and in Ingerana tasanae. In some
Ingerana tasanae the surface of the species the prismatic cells are elongated,
squamosal cells is extremely rough and can rounded proximally without projections
show spongious structures (Fig. 6). On {Rana (Hylarana) erythraea). In other
other parts of the epiderm the surface ofthe species outlines are very variable among
squamosal cells ofIngerana tasanae shows neigbouring cells; the cells are elongated
hallow tubercles (Fig. 7). The squamosal forming a somehow triangular outshape
cells cover fingers and toes outside the pad. wearing a single or two distal projections
The groove is generally the border, but (Fig. 11). In all species ofAmolops of this
sometimes the squamosal cells are present study, this kind of elongated cells with
on the border of the pad {Rhacophorus heterogeneous outlines was observed.
leucomystax) or in the contrary they are
pushed back by the prismatic cells even The prismatic cells are present outside
Rana
outside the groove (Amolops). the latero-ventral grooves in
(Odorrana) andersoni and in Amolops sp. 3.
(2) Prismatic cells. The prismatic cells Observation of direction of the channels
are present on the pad. They are of regular formed by the prismatic cells shows a
outline in all the species already studied generalized alignement in the direction ofthe
(Green, 1979; Green and Simon, 1986; space between the pair of lateral grooves
McAllister and Channing, 1982; Richards et (Fig. 12). In other species the border ofpad
al., 1977; Welsch, Strock, and Fuchs, is formed by squamosal cells, but a contact
1974). Among the species studied here, between the ventral and dorsal part ofdigital
Hyperolius vividiflavus karissimbiensis and tip remains (ex. Rana (Sylvirana) sp., Fig.
Rhacophorus leucomystax have prismatic 13).
cells of regular outline (Fig. 8) like those
found by previous authors. Also some The development ofthe toe pad
other species of ranids (Limnonectes
(Bourretia) doriae, Batrachylodes The measurements of the digital width
vertebralis) have this kind ofprismatic cells. (Table 2) show an important variation that
However, in most of the ranid species can be divided in several units. The species
investigated (Table 2) in this study, the Amolops formosus and Amolops
prismatic cells are not ofregular outline but marmoratus show the most enlarged finger
elongated. Their long axis is oriented in the pads (FW/SVL = 68 p.m.). Other species
proximo-distal direction on the digital pad. of Amolops, but also Rana (Chalcorana),
The ratio of the width to the length of these Ingerana tasanae and Rhacophorus
cells is smaller than 60%, while in normal leucomystax have very well developed
prismatic cells this ratio is over 80%, often digital pads (FW/SVL = 47-57 p.m.). The
close to 100%. On their narrow distal side, frogs ofthe subgeneraRana (Amnirana) and
the elongated cells have more or less Rana (Odorrana) show moderately enlarged
developed projections. digital pads (FW/SVL = 35-43 p.m.). The
species of Rana (Sylvirana) and Rana
(Hylarana), as the species of the subgenus
June 1995 Asiatic HerpetologicalResearch Vol. 6, p. 93
FIG. 14. Schemeofliquid fluid on adigital pad withregularoutshapedcells (left) and with elongatedcells
(right).
Limnonectes (Bourretia) have very little (Sylvirana), and Rana (Chalcorana); (5)
enlarged finger pads (FW/SVL = 22-28 arboreal frogs (Hyperolius, Rhacophorus).
p.m.). The species studied that show no
digital pad formation have the lowest ratios Actually the Raninae, the Dicroglossinae
(FW/SVL = 17-20 p.m.). and the Ranixalinae do not include strictly
arboreal species. The closest group of
Discussion treefrogs are the Rhacophorinae, an other
subfamily of Ranidae. Hyperolius
The elongated cells here described in viridiflavus karissimbiensis is another
some species of Ranidae have not been ranoid treefrog studied. Rhacophorus
described in other anuran families. In fact leucomystax, Hyperolius viridiflavus
the species that have been studied until now karissimbiensis and the species studies by
are "treefrogs", and no torrent-living frogs the previous authors (Green, 1979; Green
have yet been investigated. Considering the and Simon, 1986; Richards et al., 1977;
ecology of the studied species, five types McAllister and Channing, 1982; Welsch,
can be distinguished: (1) torrent-living frogs Strock, and Fuchs, 1974) have prismatic
ofthe genus Amolops, Rana (Odorrana) (the cells of regular outshape. This kind of
possible sister-group ofAmolops) and Rana regular cells was here also observed in
(Amnirana); Ingerana tasanae should be Limnonectes (Bourretia) doriae and
placed in this group; (2) aquatic frogs, like Limnonectes (Bourretia) pileata, two
Limnonectes (Limnonectes) kuhlii and terrestial species. Elongation ofdigital pad
Phrynoglossus laevis; (3) terrestrial frogs of cells in Amolops, Rana (Odorrana), and
the genus Limnonectes (Bourretia) andRana Rana (Amnirana) might be in relationship
(Hydrophylax); (4) ground/vegetation living with their mode of life. The presence of
frogs of the genera Rana (Hylarana), Rana elongated cells in Rana (Hylarana) and in
Rana (Sylvirana) might indicate
Vol. 6, p. 94 AsiaticHerpetologicalResearch June 1995
phylogenetic relationship to Amolops. The use of liquid (Fig. 14). The elongated cells
heterogeneous cells in some ofthese species of Amolops guide the liquid in the disto-
might indicate a regression in comparison to proximal direction. The digital pad is not
the elongated cells with projections in closed posteriorly and often also anteriorly
Amolops. The functional analysis of cell by a groove, and prismatic cells are not
morphology underlines this interpretation. restricted to the pad surface, but are also
present in the groove and outside to it.
The major sticking force of tree frogs is Water can flow out of the pad and distance
surface tension (Emerson and Diehl, 1980; from pad to sticking surface is minimized,
Green, 1981). It is a kind of wet adhesion, thus increasing the sticking force inversely.
where two surfaces are hold together by an
interlaying liquid. The prismatic cells, the It would be interesting to compare the
channels and the mucous glands are required cell morphology of torrent-living frogs of
in the humidification mechanism necessary other anuran families, like Ansonia
for sticking. For torrent-living frogs the (Bufonidae), Petropedetes
surfaces to stick to are already humid or in a (Phrynobatrachidae), some Litoria and Hyla
liquid medium. In liquid the force is no (Hylidae) and Heleophryne
more proportional to the surface, but to the (Heleophrynidae) to what is here described
squared surface which reduces the sticking in Raninae. A more detailed morphological
force to its square root (Emerson and Diehl, analysis of surface ofdigital pads should be
1980). When sticking to glass at an angle of undertaken to compare sticking surface in
90 to 180 , a treefrog is inmerged in water, tree and torrent-living frogs.
it will separate almost immediately (Emerson
and Diehl, 1980). The force of attachment Acknowledgments
in liquid medium is inversely proportional to
the distance of the two surfaces, separated The photos of this work were realized
by the liquid. with the precious help ofJean Menier in the
facilities of the "Service Commun de
To provide a good sticking in water, the Microscopie electronique" of the Museum
surface of the pads should be enlarged. national d'Histoire naturelle of Paris. I
Some of the species of Amolops, as express my gratitude to Alain Dubois for
Amolopsformosus orAmolops marmoratus advice and discussion.
have in fact very much enlarged digital pads
(Table 2). A correlation between the digital Literature Cited
pad development, as defined by the groups
A, B, C, D and E see Table 2), and the BOULENGER, G. A. 1882. Catalogue of the
ecology of the species may be found. The Batrachia Salientia s.Ecaudata in the collection of
terrestial species and the aquatic frogs the British Museum. London, Taylorand Francis: i-
belong to the group A. The group B xvi+ 1-503, pi. I-XXX.
Tinhcelutdoersrengtr-oluinvdin/gvefgreotgastiaorne-ldiisvtirnigbuftreodgsi.n BOULENGER, G. A. 1920. A monograph of the
three grDoups: C {Odorrana, AmnEirana and fSroougtshoAfsitahen,gePnaupsuaRna,naM.elaRneecs.iaInn,diaanndMAuuss.tra2l0i:a1n-
Huia), (Amolops, Ingerana), (Amolops
126.
formosus and Amolops marmoratus). The
treefrogs (Rhacophorus, Hyperolius) are all CLARKE, B. T. 1981. Comparative osteology and
members of the group D, thus not the evolutionary relationship in the African Raninae
species with the largest digital pads. (Anura Ranidae). Monit. zool. ital. (n. s. ) 15
suppl. :285-331.
Elimination of the distance between the
pad and the surface to stick to will increase DECKERT, K. 1938. Beitrage zur Osteologie und
attachment force equally and more distinctly. Systematic ranider Froschlurche. Sber. Ges. naturf.
FreundeBerl. 1938:127-184.
In treefrogs the regular cells guide the fluids
in all directions, thus humidifying the whole
pad in a regular manner and optimizing the