ZoologicalJournaloftheLinneanSociety(1981)73:261-287. With 1 figures
Snail-eatingfrogs from the Ethiopian
highlands :a new anuran specialization
ROBERT C. DREWES
Department @Herpetology, Calfornia Academy @Sciences,
Golden Gate Park, San Francisco, Calfornia 94 I 18, U S .A.
AND
BARRY R O T H
Department of Geology, Calfornia Academy
Calfornia 941 18, U.S.A.
of Sciences, Golden Gate Park, San Francisco,
Acceptedfor publication September 1980
Morphological studies and analysis of gut contents indicate that two species of montane Ethiopian
frogs are specialized for selective feeding on terrestrial gastropod mollusks. Certain bony elements
of the skull, such as the palatines and prevomers, are reduced and deflected dorsally, while lateral
elements of the maxillary arch, such as the quadratojugals and maxillaries, are expanded. The nasal
apparatus in both species is situated in an extreme anterior position. The two species are removed
from the genus Karrina Girard and placed in the genus Tom'erefla Ahl. Morphology of the head
suggests that these frogs grasp mollusks with their jaws, pull them from the substrate, and swallow
them whole. The sensoiy cues which trigger feeding are as yet unknown. Apparently, these frogs are
the first terrestrial vertebrates known to feed exclusivelyon whole mollusks, without crushing them
or removing the soft parts from the shell.
KEY WORDS :- Anura - Hyperoliidae - Kassina - Tom'erella - snail-eating - feeding specializations
- African frogs - montane species- Ethiopian highlands - Subulinidae - Succineidae- Urocyclidae.
CONTENTS
. . . .
Introduction
Stomach content analysis .
.
Skull form and structure
Tongue form and structure
. . .
Jawmusculature
Discussion
. . . . .
Acknowledgements
. .
References
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267
269
212
219
281
283
285
286
INTRODUCTION
Specialization for selective feeding on gastropod mollusks is rather uncommon
among the vertebrates, although snails are frequently found as fractions of
0024-4082/81/070267 + 21/$02.00/0
1s
26 7
0 198 1 The Linnean Society of London
268
R. C. DREWES AND 8. ROTH
vertebrate diets. A number of marine fishes are noted for crushing snails and
other mollusks, and certain cichlids from the Rift Valley lakes of Africa are
apparently specialized for biting the foot and extracting the soft parts from snail
shells (Vermeij, 1978). At least three birds of prey, the Everglades kite, the
hookbilled kite and the slenderbilled kite feed exclusively on snails, which are
extracted from the shell by means of specialized beaks (Bent, 1937; Brown &
Amadon, 1968). Old World ciconiid storks of the genus Anastomus have an oddly
shaped mandible which may serve to crush freshwater snails (Macworth-Praed &
Grant, 1970). The lower jaw of adult female turtles of certain species of the
emydid genus Graptemys becomes flattened for crushing, and their diet has been
shown to be made up primarily of freshwater snails (Ernst & Barbour, 1972).
Among the Squamata, the aquatic macroteid lizard, Dracuenu, has long been cited
as an example of feeding specialization, preying exclusively on snails, which it
crushes (Dalrymple, 1979). Rieppel & Labhardt (1979) have recently studied the
mandibular mechanics of the varanid lizard, Varanus niloticus, which shifts
ontogenetically from an insectivorous to a molluscivorous diet. Old and New
World snakes of the Family Dipsadidae possess non-kinetic lower jaws with
which they extract snails from their shells (Smith, 1943; Peters, 1960; Dunn,
195 1). We have found no reports of gastropod feeding specializations among
mammals.
With few exceptions, such as Rhinophrynus, and Myobatrachus, the majority of
frogs are believed to be generalized carnivores (Gadow, 1909 ; Cogger, 197 5),
ingesting virtually anything occurring in their niche of appropriate size which
moves in front of them (Noble, 1931; Frost, 1924). However, examination of
distinctive features of the skull, mouth, and musculature, and analysis of stomach
contents indicates that two species of the treefrog family Hyperoliidae, from
highland Ethiopia, are the first anurans discovered to be morphologically
specialized for feeding on gastropod mollusks.
Three ‘kassinoid’ hyperoliid frog forms inhabit the Ethiopian plateau. Kassina
senegalensis somalica (Scortecci) is a widely distributed lowland species usually
occurring below 1500 m. The other two are endemic highland forms referred to
by Largen (1975) as Kmsina obscuru obscura Boulenger and K . o. Rouniensis
(Mocquard). The former is found west of the Rift Valley at elevations between
1800 and 3000 m. The latter is restricted to localities east of the Rift between 2400
and 3000 m. Largen (19751, in his revision of Ethiopian Kussinu, referred both
highland species to that genus, and on the basis of external morphology
suggested that the two are distinct only at the subspecific level.
Examination of cleared and stained and dry skeletal specimens, plus
m ological characters strongly suggests that while these two highland species are
re ated to the genus Kussznu Girard, they both posses unique adaptations. These
adaptations, which are described below, represent a significant adaptive shift
(Inger, 1958) which is sufficient to warrant separate generic assignment for the
two species. The earliest available generic name appropriate for these species is
Tomierella Ahl. Its taxonomic status within the family Hyperoliidae will be treated
elsewhere (Drewes, in prep.).
Furthermore, the two forms are unquestionably distinct from one another at
the species level. Therefore, K . o. obscura Boulenger is here referred to Tomierella
obscura (Boulenger, 18941, and K . 0 . Rouniensis (Mocquard) is placed in Tornierella
kouniensis (Mocquard, 1905).
1
SNAIL-EATING FROGS
269
Tornierellu kouniensis and T . obscuru are robust, moderate-sized hyperoliids;
males of the former average about 40.3mm snout-vent length, females are
slightly larger (44.9mm average). Tornierellu obscuru is slightly smaller with males
averaging 37.2 mm and females, 39.6 mm snout-vent length. Largen (1975)
provides excellent descriptions of the coloration and habitus of both species to
whi.ch readers are referred.
Largen ( 1975) reported that during the breeding season, April to November,
the calls of Tornierellu could often be heard during the daytime. Both species have
vertical pupils, however, and it seems likely that along with K. senegulensis (with
which they are allied and which also frequently calls during the daytime),
Tornierellu obscuru and T . kouniensis are nocturnal.
Both T . kouniensis and T . obscuru inhabit high altitude grassland associated with
Eucalyptus and/or Juniperus plantations. Largen ( 1975) reported one population
of T . obscuru at a lower elevation at Jimma (7040fN, 3605SfE, 1800m) which
occurred on the edge of a tropical deciduous forest, but stated that most
individuals are larger and more abundant at higher elevations. Since Largen’s
publication, one British Museum (Natural History) specimen, BM 1976.1661,
has been collected at Godare, at an elevation of 825 m. This is the only record
of Tornierellu below 1800 m. We are uncertain whether open high altitude
grassland is a natural vegetation type or a disclimax resulting from clearing for
agricultural purposes. Largen ( 197 7 believed that at least the “open undulating
landscape” of Gojjam Province, which includes two known T . obscuru localities, is
essentially natural vegetation.
Montane grassland at altitudes of roughly 1880 to 2500m in Ethiopia is
composed of communities of grass of about 1 m in height and typically includes
Themedu triandru Forsk., Loudetiu simplex (Nees) C . E. Hubb, and Andropogon
distuchyus L. Above 2500 m, the grasses are much shorter and Festucu ubyssinicu
Hochst., Pentaschistis munnii C . E. Hubb, and Agrostis isopholis C . E. Hubb are
typical species represented (Keay, 1959).
Collection data indicate that T . obscuru and T . kouniensis are terrestrial, as would
be expected because of their stout habitus and lack of noticeably expanded toe
tips. Both Tornierellu species have been found under boulders, beneath stones in
gravel diggings, and in flooded meadows. They have also been collected during
the breeding season while calling from ponds, temporarily flooded hollows, or
ditches. Largen (1975) did not observe frogs of either species climbing in the
field, although one T . obscuru individual did so readily in captivity. One
specimen, BM 1976.1661, a male T . obscuru, was collected at Godare (825 m) by J.
M. McElligott at about noon from a tree branch, approximately 1.75 m above
the ground-this is the only known above-ground capture.
STOMACH CONTENT ANALYSIS
Stomach contents were examined from 42 specimens of Tonzierellu kouniensis
and 18 of T . obscuru housed in the collections of the British Museum (Natural
History), the National Museum of Kenya, the Field Museum of Natural History,
and the California Academy of Sciences. This number represents nearly 80% of
the known preserved specimens. Juveniles and adults of both sexes, collected
over a period of 49 years, were dissected and their stomach contents removed for
identification. The results are summarized in Tables 1 and 2.
270
R. C. DREWES AND B. ROTH
Of T . kouniknsis examined, 25 (60%)stomachs contained food items and/or
other identifiable matter. Twenty of these contained recognizable remains or
whole individual gastropod mollusks, including periostracum (the organic
external layer of the shell of snails), shell fragments, entire snails and slugs of the
families Subulinidae and Urocyclidae, and remains that we interpret as snail soft
anatomy (mantle, fragments of digestive gland, and perhaps parts of the
columellar musculature). Mites and cyperaceous, graminaceous and hepatic
plant material were also present, presumably ingested by chance or as part of the
stomach contents of the ingested mollusks.
The largest snail found in gmtro was approximately 5 by 8 mm, a prodigious
meal for a frog whose head was 15.4 mm wide by 5.7 mm deep (BM 1975.1878,
snout-vent length = 50 mm). This was a subulinid snail, possibly a juvenile
specimen of the genus Homorus Albers, members of which are characterized by
high spire, blunt nucleus, and brown, longitudinally streaked periostracum.
Juvenile T. Rouniensis (those examined ranged from 16 to 22mm snout-vent
length) also eat snails, but of smaller size. BM 1973.2154,a specimen of 19 mm
length, contained six subulinid snails which were about 2 x 5.5 mm each, so no
ontogenetic shift in diet is apparent. However, two juveniles of this species from
one locality were found to have eaten slugs; in fact, BM 1973.2151,a juvenile,
contained the whole range of gastropod’ forms found in this species: one
urocyclid snail, one subulinid snail, and one urocyclid semislug (snails with shell
present but so reduced that the animal cannot retreat within it (Fig. 1C)).It is
important to note here that, with one exception, no traces of arthropods or
arthropod exoskeletal remains were found. The only exception, BM 1975.1885,
contained remains of a subulinid snail but also one moth larva and parts of
another, both of the family Noctuidae (or perhaps, Agaristidae).
One half (9)of the T . obscura stomachs examined contained identifiable
material. These included snails of the families Succineidae and Subulinidae and
snail tissue fragments. One 30.1mm male, the head of which was 9.4mm wide by
4.8mm deep (BM 1969.1161), contained five succineid snails which were 6 to
7 mm long by about 4 m m wide (Fig. 1B). Another male, of 46.6 mm,
BM 1976.1661,contained the largest snail found in either species, a subulinid
(Hornorus?) about 8 x 14 mm, nearly twice the dimensions (eight times the
volume) of the largest snail found in T. kouniensis (Fig. 1A). The head of this frog
was 16.4mm wide by 6.7 mm deep. Again, no traces of arthropod remains were
found except in one specimen. BM 1969.1162, a male from Debre Marcos,
contained remains of noctuid moth larvae, as did the one exception of
T . kouniensis examined.
All of the gastropods found in the stomachs are terrestrial. Significantly, none
of the aquatic mollusk species reported by Wright 8c Brown (1962)and Brown
(1965)from the vicinity of Debre Marcos was found as stomach contents. The
family Succineidae is worldwide in distribution with members found from near
sea level to 2500 m, characteristically in marshy habitats. The succineids found in
the stomach of BM 1969.1161 (Debre Marcos, 2500 m) are at or near the upper
aItitude limit known for the family.
The high-spired snails found all appear to belong to the genus Homorus of the
Subulinidae, several species of which occur in the Ethiopian Region (Pilsbry,
1904-1905). The specimens at hand are too poorly preserved for specific
identification. Judging by the number of whorls, most are probably juveniles.
SNAIL-EATING FROGS
27 I
272
R C. DREWES AND B. ROTH
The Urocyclidae is a family of slugs and semislugs endemic to the Afrotropical
Region (Te, 1976). Urocyclid semislugs were identifiable by examination of shell
remnants and periostracum. Localities yielding semislug remains are within the
geographic range of the genus Degneria Verdcourt, which is confined to the
Ethiopian massif (Van Mol, 1970).
The true slugs found were all small (largest 4.5 mm long) and juvenile, lacking
the reproductive characters needed for firm generic assignment. The observable
characters are consistent with those of members of the urocyclid genus Atoxon
Simroth, which, in Ethiopia, is known from east of the Rift Valley (Van Goethem,
1977). In general, the land mollusk fauna of the Ethiopian highlands shows
strong relationship to that of the mountains of central Africa, one of the world’s
centres of slug and semislug diversity (Van Mol, 1970; Solem, 1974; Van
Goethem, 1977).
The condition of the snails found in the stomachs examined varied. Some were
essentially whole specimens, several others were intact except that the calcareous
shell was partially or completely dissolved beneath the periostracum. In only one
frog, a T . obscura male (BM 1976.1661), did the subulinid snail within its stomach
appear crushed. Thus the implication is that snails are ingested whole by these
frogs. In intact snails in which the periostracum was perforated or torn (possibly
by the frog’s teeth) differential dissolution of the calcareous shell beneath was
obvious.
The tissue remains that we interpret as snail anatomical fragments were
remarkable for their similarity in each gut and for maintaining their integrity
even while being removed from the gut with forceps (Fig. 1D). In both whole
mount and section, these agree fairly well with mantle, digestive gland, and
columellar muscle tissues dissected from other snails. One T. kouniensis and four
T. obscura stomachs contained only this material and no other gastropod remains.
In tive T . kouniensis stomachs the tissue was associated with other definite snail
remains (Table 1). If correctly identified, these tissues are the contents of the
upper and inner whorls of the shell; but it is not clear why these parts would
regularly persist in the stomachs while other presumably more resistant structures
(periostracum, radula, sole of the foot) do not.
Morphological correlates to feeding in am hibians are rare, and the
anatomical examination which follows revealel several features unique to
Tornierella. Throughout the morphological studies below, both Tornierella species
were compared with K. s. somulica, their closest relative on the Ethiopian plateau.
The observations are based on four cleared and double-stained specimens
(Dingerkus & Uhler, 1977), three skeletonized specimens, and partial or total
dissections of ten additional specimens. Osteological terminology follows that of
Trueb (1973).
SKULL FORM AND STRUCTURE
Among unique features of skulls of T . kouniensis are those associated with the
maxillary arch. The maxillary arch typically consists (from anterior to posterior)
of paired dermal premaxillaries, maxillaries and quadratojugals (Fig. 2A). The
last named elements are often reduced in anuran species and frequently lost in
many smaller frogs. Representatives of all presently recognized hyperoliid genera
have been examined (Liem, 1970) and with the exception of Tornierella, the
SNAIL-EATING FROGS
273
quatratojugals are reduced in all. Actual loss of this element within the
Hyperoliidae seems to be confined to certain species of the genus Afrixalus
(Laurent & Combaz, 19501, and a transformation series (i.e. from present and
complete to absent) can be demonstrated for this character (Drewes, in prep.).
In lateral view, the anterior part of each maxillary bears a facial flange, the
pars facialis. Size and shape of this flange vary greatly among hyperoliid species;
but posterior to it in all individuals the maxillary narrows to its point of
articulation with the quadratojugal. Ventrally, the maxillary consists of a dental
ledge, the pars dentalis, which bears teeth in all hyperoliids examined (Fig. 2A).
Anteriormost elements of the maxillary arch, the premaxillaries, are varied in
shape and ventrally possess partes dentales which articulate with the partes
dentales of the maxillaries, together forming the basic structural component of
the maxillary arch. In all hyperoliids examined, the premaxillaries also bear
teeth.
In lateral view, the maxillary arch of T . kouniensis individuals is deep compared
to other hyperoliids. The maxillary bone is stout. The pars facialis is deep and
rounded, and posterior to it, the maxillary is expanded, rather than gradually
narrowed, such that at its point of articulation with the quadratojugal it is
rounded and almost 75% of the height of the pars facialis (Fig 2B). Posterior
expansion of the maxillary is rather uncommon among frogs which lack
extensive cranial exostosis. For instance, Lynch, in his revision of the
Table 1. Stomach contents of Tornierella kouniensis
Museum no.
BM.1973.2133
1973.2144
Sex Locality
8 Kofole(2600m)
j 6'15'N, 3E045'E,
A
B
C
D
E
F
G
H
I
J
K
1
X
(2400+ m)
1973.2145
1973.2146
1973.2147
1973.2148
1973.2150
1973.2151
1973.2152
1973.2154
1973.2156
1973.2159
1973.2160
1974.2949
1975.1875
1975.1878
1975.1880
1975.1881
1975.1885
1975.1887
1975.1888
CAS 141875
145357
FMNH 12514
1
j
X
j
j
j
j
j
1
2
1
X
X
x
Dinshu, 4 km E (3000m)
X
Kebre Mengist, 'IOkmNW,
(26 7 0 m)
x
x 1
X
I
3
8
X
X
I
8
8
8
X
$?
x
1
6
$?
8
8
8
x
1
1
X
X
$?
8
X
4
j
j
j
j
9
X
1
X
1
1
1
1
Allata(2500m)
x
x
1
1
S
X
1
1
X
x
x
1
X
x
x
X
X
Key: A, animal tissue (unidentified); B, plant tissue; C, snail tissue; D, succineid snail; E, subulinid snail
(Hornorus?); F, urocyclid snail; G , urocyclid slug (Atoxon?);H, shell fragments; I, periostracum;J, mite; K,
noctuid larva. Numbers in columns indicate number of items. X, Indicates presence of material only.
274
R. C. DREWES AND B. ROTH
A
C
Figure 2. Schematic lateral view of skulls of A, Kassina sencgdmis samalica; B, Tornierella Lounierrtrs; C,
T. obrcura. Cartilagenous structures are not shown in detail. The premaxillaries of T . obsncra are not
visible in lateral view. Scale bar = 5 mm. Abbreviations for all Figs: a.m.e.l., adductor mandibulae
externus lateralis; a.m.p.1.. adductor mandibulae posterior longus; a.m.p.s., adductor mandibulae
posterior subexternus; at, annulus tympanicus; dm, depressor mandibulae; fm, foramen magnum;
fo,footplate; fp, frontoparietal; ih, interhyoideus; im, intermandibularis; mx, maxillary; na, nasal;
pa, palatine; pd, pars dentalis; pf, pars facialis of the maxillary; pp, pars palatina; ps, parasphenoid;
pt, pterygoid; pv, prevomer; px. premaxillary; qj, quadratojugal; sm, submentalis; sp,
sphenethrnoid; sq, squamosal.
SNAIL- EAT1NG FROGS
275
Table 2. Stomach contents of Tornierellu obscuru
Museum no.
Sex Locality
BM. 1969.1160
1969.1161
1969.1162
1973.2121
,j'
,j'
1973.2122
1973.2130
NMKA/116/1
BM.1975.1874
1976.1661
9
0
0
,j'
,j'
,j'
Debre Marcos (2500 m)
A
B
C
D
E
F
G
H
I
J
K
X
5
1
Enjiabara, 6kmN
(2700 m)
Dasse, 75kmN(2500m)
,j' Godare(825 m)
1
1
1
1
1
1
Key: A, animal tissue (unidentified); B, plant tissue; C, snail tissue; D, succineid snail; E, subulinid snail
(Hornorus?);F, urocyclid snail; G, urocyclid slug (Atoxon?);H, shell fragments; I , periostracum; J, mite;
K, noctuid larva. Numbers in columns indicate number of items. X, Indicates presence of material only.
Leptodactylidae (197 l ) , found only one genus (the monotypic Meguelosiu) with
members exhibiting this character state. Members of this genus also possess
long daggerlike teeth as in T. kouniensis (see below).
The quadratojugal of both Tornierella species is unique among hyperoliid
frogs, being greatly expanded posteriorly and dorsally. In T . kouniensis its height
is equal to or slightly greater than the pars facialis of the maxillary (Fig. 2B).Its
posterior edge is in broad contact with the basal half of the ventral ramus of the
squamosal, its anterior edge articulating broadly with the proximal part of the
maxillary. The squamosal is angled markedly forward (approximately 4 5 O 1.
Although expanded, the quadratojugal is so thin that in a skeletonized
preparation the free anterior and dorsal edges tend to curl inward when dried. In
undissected specimens, this structure is semitransparent and the adductor
musculature of the jaw can be seen through it.
The partes dentales of the maxillaries and premaxillaries of T. kouniensis bear
long, sharp daggerlike teeth, all of which are curved strongly inward. The teeth
are pedicellate, equally spaced and subequal in size. The only other hyperoliid
among the examined material that has long sharp teeth is the arboreal West
African Leptopelis breuirostris (Werner), but its teeth are broader basally, almost
triangular, interspersed with smaller teeth, and not curved inward.
Overall, skulls of T. kouniensis are slightly broader than long (length:
width = 0.85, approximately; see Largen (1975) for external dimensions).
Dorsally, the paired frontoparietals are long and semi-rectangular, their anterior
width about equal to their width posteriorly, and almost in contact with the
posterior margins of the nasals. The nasals are-large, subtriangular and nearly in
contact with each other in the midline. Laterally the nasals are in contact with the
dorsal edge of the partes faciales of the maxillaries. The entire nasal apparatus
appears more compact and is more anteriorly positioned than in other
hyperoliids. It represents but 33% of the total length of the skull, while in K . s.
somalicu, this value is 45%.
Posteriorly, the otic (posterior) rami of the squamosals are curved inward and
broadly flanged to form an almost continuous shelf with the otic capsule, and
together with the zygomatic (anterior) rami, nearly parallel with the skull roof
(Fig. 3B).
In ventral aspect, the partes palatinae of the premaxillaries and maxillaries are
16
276
R. C. DREWES AND B. R O T H
A
R
c
Figure 3. Schematic dorsal view of skulls of A, K . 5. s d i c u ; B, T . Aouniensis; C, T . obrcuru.
Cartilagenous structures are not shown in detail. Note relative lengths of frontoparietals of both
T ~ m i t r t lspecies
l~
compared with those o f K . 5. s o d i c u . Abbreviations as in Fig. 2. Scale bar=5mm.
SNAIL-bATING FROGS
211
strongly developed lingually. At the anterior end of the maxilla, the visible part
of the pars palatina is twice as broad as the pars dentalis. The prevomers are
simple, reduced compared to other hyperoliids, and in the specimens examined
do not bear teeth. These bones are inclined dorsally giving thleroof of the skull a
vaulted appearance. The palatines are slender, widely spaced rods so small that
they are difficult to see in skeletonized specimens (Fig. 4B).
The anterior rami of the pterygoids articulate well forward on the maxillaries.
The distance between the anterior and posterior rami of the pterygoid is equal to
52% of the lateral head length (as defined by Trueb, 1977). This value is less (37%)
in K. s. somulica specimens. The anterior and posterior rami of the pterygoids are
bowed markedly inward.
The are two distinctive features of the skull in posterior aspect. The ventral
ramus of the squamosal is greatly expanded laterally. This flattening is on the
same plane as, and forms a continuous lateral plate with the enlarged quadratojugal. Medially, the angle formed by the articulation of the base of the squamosal
with the posterior ramus of the pterygoid is completely enclosed by a continuous
sheet of bone. This bony sheet is an expansion of both the medial and posterior
rami of the pterygoids (Fig. 7B).
The mandible of T . kouniensis is more robust and much deeper in lateral view
than that of K. s. somalica, and other hyperoliid frogs. The anterior portion of the
proximal element of the mandible, the angular, is more expanded mediodorsally
than in K . s. somalica, and functions as increased surface for insertion of the
massive adductor musculature described below.
Skulls of T. obscura are shorter and broader than those of T . kouniensis and are
bonier and more massive in appearance (length: width = 0.64, approximately).
The frontoparietals are similar in size and shape but diverge slightly at their
anterior end (Fig. 3C). The nasals are subtriangular (as in T . kouniensis), and in
close contact with each other medially and with the partes faciales of the
niaxillaries laterally. The otic rami of the squamosals are curved inward and
flanged as in T . kouniensis, but the flanges are more extensive medially. The
zygomatic rami are described for T . kouniensis.
The maxillary arch of T. obscura is even more highly modified than that of its
congener (Fig. 2C). The maxillaries are relatively shorter but deeper. The partes
faciales are higher, and the proximal ends of the maxillae are more expanded,
approximately 85% of the height of the former. The quadratojugals are
enormously expanded so that their dorsal extent is considerably greater than that
of the partes faciales, and they obscure the entire anterior margins of the ventral
rami and a portion of the ventral edge of the zygomatic rami of the squamosals.
The partes dentales of the maxillaries and premaxillaries bear inwarddirected, blunt, pegshaped teeth, unlike the fanglike teeth of T . kouniensis.
In ventral aspect, the most prominent feature of skulls of T . obscura is the
continuous shelf formed by the partes palatinae of the premaxillaries and
maxillaries (Fig. 4C). This shelf is expanded lingually to a greater degree than in
T. kouniensis, i.e. the partes palatinae of the premaxillaries are about three times
wider than the partes dentales. The prevomers are toothless and shaped as in
T . kouniensis but even smaller, so that they are greatly obscured by the partes
palatinae of the prenhxillaries. The prevomers of T . obscura are more dorsally
deflected than those of T. kouniensis, so that the oral cavity is more deeply vaulted.
The prevomers do not bear teeth. As in T. kouniensis, the palatines are greatly
278
R. C. DKEWES AND B. ROTH
P'
B
C
tigul-t 4 . Scliernatic ventral view of skulls of A, K . s. somalica; B, T . kouniensis; C, T . obscuru.
Cartilagenous structuresare not shown in detail. Abbreviations as in Fig. 2. Scale bar=5mm.
SNAIL-EAHNG FROGS
219
reduced and deflected dorsally. The nasal apparatus is positioned even more
anteriorly, and constitutes only 28%of the total length of the skull. The anterior
rami of the pterygoids articulate with the maxillae at a position well forward of
the same articulation in T. Kouniensis; the distance between the anterior and
posterior rami is 55% of the lateral head length.
The posterior portion of the skull is similar to that of T. Kouniensis; the ventral
rami of the squamosals are laterally flattened, almost horizontal, and there is a
continuous sheet of bone across the angle formed by these elements and the
posterior rami of the pterygoids.
The mandible of T. obscura is similar to that of T. kouniensis in appearance and
bears an even more greatly expanded mediodorsal flange of the angular.
TONGUE FORM AND STRUCTURE
The tongues of Tornierella kouniensis and T. obscuru are unique within the
Hyperoliidae, and also differ markedly from each other. Tongues of most
hyperoliids, as exemplified by Kmsina s. somalica (Fig. 5A), are typically large and
emarginate posteriorly, more or less heartshaped. In many hyperoliids (e.g.
some Leptopelis and Acanthixalus), tongues are large enough completely to occupy
the floor of the mouth. Tongues of most advanced frogs are attached to the floor
of the buccal cavity anteroventrally, leaving the major portion free posteriorly.
Relative to other hyperoliids, a T. Kouniensis tongue is minute. It is uniformly
round (non-emarginate),with its diameter equal to or less than the diameter of
the eye (the largest T. Kouniensis tongue measured had a diameter of 2.7 mm; in
all other Hyperoliidae examined, the tongue is much larger than the diameter of
the eye). The tongue is situated in an extreme anterior position and firmly
attached to the floor of the buccal cavity along its ventral two-thirds, leaving only
a small portion free posteriorly. The surface of the tongue is covered by round,
flattened, equally spaced nodules which are subequal in size and separated by
small granules (Fig. 5B).
A T . obscuru tongue is similarly round but somewhat larger, its diameter being
slightly greater than the diameter of the eye in most individuals (Fig. 5C).The
anteroventral attachment is the same as in T. kouniensis. Its dorsal surface is
smoother (as in other hyperoliids), except some individuals from various localities (BritishMuseum specimens)in which there are a fav nodules on the extreme
anterior portion of the tongue but none posteriorly (Barry Clarke, pers. commn).
Viewed anteriorly, tongues of T. obscuru and T. kouniensis are similar to those of
certain plethodontid salamanders figured by Lombard & Wake (1977), such as
Bolitoglossa subpalmata and Eurycea longicauda guttolineata, respectively. The protractor/retractor musculature of Tornierella tongues has not been examined in
detail, but it is possible that the tongues may be of the projectile type described by
the former investigators.
The method by which frog tongues are extruded for prey capture has been
described for a number of species (Magimel-Pelonnier, 1924; Regal & Gans,
1976). It is difficult to imagine, however, Tornierellu tongues being extruded in the
manner of any of the frogs described, especially in light of the extent of their
anteroventral attachment.
We suspected that the nodules of T. Kouniensis tongues might have some
sensory function and therefore compared sections of these tongues with sections
280
K. C . DKEWES A N D B. ROTH
A
B
C
biglire 5 . Tongues of A, K . J. sornalica; B, T . kountmsk; C, 7'. obscura. In B and C, musculature of the
Iloor of tlic mouth has been excised so that the lower jaw is not shown. Scale bar = 3 mm.
SNAIL-EATING FROGS
28 1
of T. obscura and K. 5. somalica tongues. Study of the sections revealed that the
nodules in T. kouniensis lack pores, invaginated cells or separate innervation; thus
a sensory function seems unlikely. The nodules are similar to the fungiform
papillae described in Rana catesbeiana by Hammerman (1969). The tongues of
both Tornierella species are highly glandular. The glands resemble the mucoserous glands described for certain salamanders by Fahrmann (1974). They are
large, tubular, thick-walled and basophilic, but their contents appear granular.
The lingual glands of K. 5. somalica, however, appear to be typical serous glands
such as found in the dermis of the integument (Gaupp, 1907). No classic mucous
glands were found in the sections.
JAW MUSCULATURE
I t is assumed that the strikingly modified portions of the maxillary arches of
Tornierella are adaptations to increase surface area for muscle attachment. The
depressor and adductor musculatures of the jaws were dissected to test this
assumption. Starrett’s (1968) work on Rana catesbeiana was used as a standard for
comparison with both Tornierella and K. 5. somalica.
In T. kouniensis, the depressor mandibulae musculature consists of two distinct
slips much as described for R a w catesbeiana (Fig. 6A). The two slips are widely
separated, however, and fuse just above the point of insertion on the posterior
angle of the jaw. The much smaller anterior portion originates on the posterior
and ventral perimeter of the annulus tympanicus. The squamosal is not involved
with the origin of the slip. The posterior slip is fan-shaped and its origin is
entirely on the dorsal fascia overlying the m. dorsalis scapulae. The insertions are
as described for R. catesbeiana. Between and deep to these two slips in male
specimens is a long, dorsally directed, third slip which also originates on dorsal
fascia. O n first inspection it appears to be part of the depressor musculature, but
is in fact a posterior elongation of the m. interhyoideus of the vocal sac
complex-a feature unique among the Hyperoliidae (Fig. 6A, C).The slip is also
present in T. obscura. We have been unable to determine whether or not its
presence and configuration are correlated with gastropod-eating.
The six muscles which typically make up the adductor complex in frogs are all
present and comparable to those in R. catesbeiana. Curiously, the greatly enlarged
quadratojugal does not serve for adductor origin, except for one of the external
members, the adductor mandibulae externus lateralis (as in R. catesbeiana).
Otherwise, no muscles originate on the quadratojugal at any point, and its inner
surface and dorsal and anterior edges are free.
In T. kouniensis, the two deepest adductors, the a. m. posterior longus and the
a . m . anterior internus, are much broader and more massive than in K. s.
somalica, but otherwise these and the other adductors are similar in origin and
insertion to those of both K. 5. somalica and R. catesbeiana.
Jaw musculature of T. obscura is somewhat different from T . kouniensis. The
depressor musculature is single, rather than divided into two distinct slips as in
T. kouniensis (Fig. 6B). The shorter anterior portion originates from the ventral
and posterior rim of the annulus tympanicus but overlies and obscures the
posterior third to half of the structure. The longer proximal fibres originate from
dorsal fascia as in T . Rouniensis, and similarly, there is no squamosal component
in their origin. A deep medial extension of the interhyoideus is present in males
K L. D K t - l V t S A N D B. KOTH
.I
-I
L
rn
rn
ih
C
Figuw 6. Jaw musculature: A, dorsal aspect of T . kounzensis; B, lateral view of T . obscura; C, ventral
iew o f f . kuuriremis with suprarnandibular slip of interhyoideus removed from origin and spread
laterall\. Note anterior origin of m. interhyoideus o n adductor mandibulae posterior longus in T.
o b ~ u r uAbbreviations
.
as in Fig. 2.
but dit’f’ersin length and origin from that of the congener (Fig. 6B). Overall, the
depressor musculatures of both species do not appear particularly modified; they
are similar to inany described by Starrett (1968).
The adductor complex of T. obscura is more elaborate than in T. kouniensis. The
origin of the a. m. externus lateralis is similar to T. kouniensis, and the deep a. m.
posterior longus and a. m. anterior internus are even more massive and broader
than in K. s. somalica. The primary difference lies in the a. m. posterior
subexternus, which, in R. catesbeiana and K. 5 . somalica, originates on the ventral
surface of the zygomatic ramus of the squamosal and inserts on the lateral face of
the mandible, deep to the a. m. externus superficialis. In T. obscura, this muscle
has an expanded origin which includes the squamosal and also the entire dorsal
edge of the quadratojugal. The origin of the muscle is deeper as well, so that the
dorsal fifth of the quadratojugal including the anterior edge is broadly involved
in its origin (Fig. 7A).
\NAII,-tAI I N G FROGS
283
5
o mps
A
mx
B
Figure 7 . A. Lateral view of skull of T . obscuru illustrating origin of m. adductor mandibulae
posterior subexternus. Stippled area indicates expanded origin on quadratojugal; dotted line
indicates path of this muscle behind quadratojugal. B. Posterior view of left half of skull of T .
kouniensis. Stippled area indicates bony expansion of pterygoid enclosing pterygoidhquamosal angle
present in both species of Tonierellu.
DISCUSSION
Analysis of stomach contents strongly suggests that T. kouniensis selectively feed
on snails and semislugs (and as juveniles, also on slugs), while T. obscura feed
exclusively on snails and can eat individuals of larger size. The absence of
arthropod exoskeletal remains from stomach samples is strong evidence against
other conclusions. Frogs of both species appear to feed exclusively on land. All of
the gastropods and identifiable plant material found in their gut contents are
strictly terrestrial. Although one stomach contained hepatic plant material
(liverwort), its seems likely this was ingested by chance or was in the stomach of a
mollusk.
Specimens containing gastropods were collected in March, April, September,
October and December; thus, there is no obvious correlation with the AprilNovember season of maximum rainfall in highland Ethiopia (Wernstedt, 1972).
284
K C D K t W t S 4 N D B ROTH
This, coupled with the fact that specimens with molluscan remains in their
stomachs were collected over a 49-year period, suggests that gastropod-eating is
not a seasonal or temporary phenomenon.
Morphological observations support the view that both frog species are
uniquely adapted for selective feeding on gastropods, primarily snails. Reduction
and dorsal deflection of the palatines and prevomers in the two Tomierellu species
niay be a response to the necessity of enlarging the buccal cavity for the ingestion
of large, round snails. Any structural support lost by the modification of these
elements may be regained internally by the expansion of the partes palatinae of
the niaxillaries and premaxillaries, externally by the breadth and close proximity
of the bones of the skull roof, and laterally by the expanded pars facialis and
proximal portions of the maxillary and the quadratojugal, and the widely
separated articulations of the rami of the pterygoid with the upper jaw. The
medial bowing of the latter may also serve to permit contraction of the massive
adductor musculature. The massiveness of the posterior part of the skulls in both
species-including the lateral expansion of the ventral ramus of the squamosal,
the bony sheets enclosing the angle between that element and the posterior
rdmus of the pterygoid, and the greatly enlarged quadratojugal-may serve to
strengthen that area as a fulcrum for the increased force generated by the
contraction of the adductor musculature (which includes the broadened a. m.
posterior subexternus). This extra force may be necessary to overcome the
adhesion of a large snail to its substrate. The nearly horizontal zygomatic rami of
the squarnosals would seem to be associated with a lengthening of the adductor
musculature which originates on them.
The role of the teeth and tongue in T. obscura is uncertain. The teeth are
directed inward but are blunt. The surface of the tongue is not elaborate and its
area is probably too small to effect capture of a large snail, even if the ventral
attachment were such that it could be extruded in the manner typical of other
advdnced frogs. Perhaps the tongue and teeth act together to orient the snail
prior to swallowing.
The same modifications seen in skulls of T . obscura are present in T . kouniensis
but in each case, they are less extreme. Because the latter may eat smaller snails
than the former, less force would be required to remove them and therefore, less
structural support would be necessary to strengthen the back of the jaw.
Presumably for the same reason, the expansion of the a . m . posterior
subexternus is absent from this species.
The sharp daggerlike teeth, and the glandular nature and elaborate surface of
the tongue in T . kouniensis may be adaptations for the capture of slugs. The teeth
may be able to grasp slugs by penetrating their slippery mucous integument.
Another function may be to perforate the periostracum of snail shells to speed
dissolution of the calcareous layers beneath.
The elaborate surface of the tongue probably enhances the spread of the
secretory products of the lingual glands, much as the verrucae hydrophilica of
the ventral skin of many treefrogs apparently enhance the capillary spread of
water to aid in cutaneous uptake (Drewes et al., 1977).As noted above, the glands
of the tongue are predominantly of the muco-serous type described by
F2ihrmann ( 1974). Typical mucous glands are absent. We have not tested for the
presence of mucins, but it is possible that the surface of the tongue may not be
sticky, but instead may be coated with a substance to aid in the breakdown of the
SNAIL-EATING FROGS
285
mucous coat of slugs, thereby facilitating ingestion or digestion. Fahrmann
(1974) suggested an enzymatic function for the secretions of the muco-serous
lingual glands of the salamanders he studied. Perhaps the secretions of the
lingual glands of Tornierellu serve as an irritant to gastropods, breaking the
adhesion of the foot to the substrate.
The hyobranchial feeding mechanism of aquatic tongueless frogs has been
described by Sokol (19691, and the works by Magimel-Pelonnier (1924) and
Regal & Gans (1976) discuss the feeding mechanisms of many terrestrial
phaneroglossan species. In the latter, the tongue is extruded (in one way or
another), immobilizes the prey, and then by contraction of retractor muscles, the
prey item is brought into the buccal cavity for ingestion. Neither of these
mechanisms is appropriate for Tornierellu. The former is inapplicable! because
Tornierellu are not aquatic. The latter is unlikely because of the anteroventral
attachment of Tornierellu tongues, their size relative to the size of many of the
snails found as gut contents, and especially in light of the adhesive properties of
the foot of a snail, moving or at rest.
Repeated attempts by the senior author to obtain living material for
behavioral studies have been unsuccessful. However, we suggest the following
feeding model based on the data at hand. In order to ingest a snail, a Tornierellu
must first engulf the prey item within its jaws, then apply pressure against the
substrate with its stout muscular forelimbs, thereby freeing the snail from the
substrate. The snail is then swallowed whole. In the extreme, this task is
analogous to attempting to pick up with one’s mouth a football which has been
glued to the floor. If confirmed by observations of living frogs, this method of
feeding will represent a new mechanism among those described for the Anura.
Furthermore, these frogs are apparently the first vertebrates known to be
specialized to ingest snails whole; all of the other snail-eating species known to us
either crush the mollusks or remove the soft parts from the shell.
While most frogs feed in response to visual cues, the sensory triggers to feeding
in Tornierellu are not known. The presence of moth larvae in one specimen each
of both frog species is probably a chance result, but it is also possible that some
features of the larvae elicit the appropriate response. Feeding lepidopteran larvae
are not dissimilar in appearance to feeding slugs.
ACKNOWLEDGMENTS
The authors are grateful to Alex Duff-MacKay and Richard E. Leakey of the
National Museum of Kenya (NMK), Harold K. Voris of the Field Museum of
Natural History (FMNH), and especially to A. G. C. Grandison of the British
Museum (Natural History) (BM) for the loan of specimens in their care and
permission to dissect certain of them. Paul Tuskes of the University of California,
Berkeley, identified the moth larvae; Frank Almeda, Jr. of the California
Academy of Sciences (CAS) kindly examined the plant material, and David H.
Kavanaugh (CAS)identified the mites, examined the first stomach contents ( a bit
of periostracum) and suggested that they “might be from a snail.” Tongue
sections were kindly provided by Malcolm R. Miller, University of California
Medical Center, San Francisco, and sections of snail tissue were prepared by
Daphne F. Dunn of the California Academy of Sciences. Valuable criticism and
suggestions came from discussions with A. G. C. Grandison, Barry Clarke,
286
R. C. DREWES AND B. ROTH
Malcolm R. Miller, Sidney Raffel of Stanford University, David B. Wake,
Marvalee H. Wake, and Harry W. Greene of the University of California,
Berkeley, Linda Trueb of the University of Kansas, Otto M. Sokol of the
University of South Alabama, and William N. Eschmeyer, Tomio Iwamoto,
Dennis E. Breedlove, Laurence C. Binford, Alan E. Leviton and John E.
Simmons of the California Academy of Sciences. Illustrations were drawn by
Peggie L. Phillips.
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