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SEAT

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Source : MNHN, Paris

AIRTTES

INTERNATIONAL JOURNAL OF BATRACHOLOGY

January 1995 Volume 12, N° 4

Alytes, 1995, 12 (4): 145-157. 145

Fossil tadpoles from the Miocene of Turkey

Richard J. WasseRsuG * & David B. WAKE **

* Department of Anatomy and Neurobiology,

Dalhousie University, Halifax, Nova Scotia, B3H 4H7, Canada

** Museum of Vertebrate Zoology and Department of Integrative Biology,

University of California, Berkeley, California 94720, U.S.A

We describe two exceptionally well-preserved anuran larvae from the

Middle Miocene of central Turkey. Among extant taxa from Europe and Asia

Minor, these specimens most closely resemble tadpoles of the genus Peloba-

tes. Many non-mineralized tissues, such as the keratinized beaks, are pre-

served. Some of these structures are ambiguous for taxonomic assignment,

and key diagnostic features, such as spiracular position and organization of

oral denticles, are not observable.

INTRODUCTION

In 1968, the Turkish-American botanist Baki KASAPLIGIL discovered a fossil-rich site

in the Gürcü Valley of Turkey, about 90 km north of Ankara (KASAPLIGIL, 1977, 1981).

On that and subsequent trips KASAPLIGIL and associates encountered an “‘abundance of

frustules of pennate fresh-water diatoms, Cyprinid fish fossils, frogs, salamanders,

mosquito larvae, Nematoceran flies, dragon flies, bees and beetles” (KASAPLIGIL, 1981:

97). Before his death in 1992, Dr. KASAPLIGIL asked us to study some remarkably

well-preserved fossil tadpoles from the site, and we present the results of our study here.

At first the site was listed as Pliocene (KASAPLIGIL, 1977), but later the age of the fossil

deposits was determined through K/Ar isotope analysis to be + 14.1 million years and

said to be Upper Miocene (KASAPLIGIL, 1981). However, the dating makes the site Middle

Miocene.

iothèque Centrale Muséum

LUI

3 3001 1SMPCB : MNHN, Paris

146 ALYTES 12 (4)

MATERIALS AND METHODS

There are two fossil tadpoles available for study; KASAPLIGIL knew of the existence

of more vertebrate remains but was unable to locate them. Both specimens have been

catalogued into the collection of the University of California Museum of Paleontology

(UCMP) in accord with the wishes of Dr. KAsAPLIGIL. The specimens are preserved in a

laminated diatomite. One specimen (UCMP 139183) is a ventral impression of a complete

tadpole, ventral side up. The matrix of this specimen is firm and dense. This specimen has

the following accompanying data: Ankara, Güven, Beskonak, Karga Creek, alt. 1300 m,

October 4, 1986. The other specimen (UCMP 139184) is a more fragmentary head and

body preserved as an impression and a counterpart. The soft matrix is fissile, and flakes

easily. Both parts are mounted on stiff board. They have the following accompanying data:

Güven, Gürcü Valley, Akoz Site, alt. 1200 m, August 30, 1976. We comment briefly on

one additional specimen available to us only in the form of a photograph.

DESCRIPTION OF FOSSIL TADPOLES

SPECIMEN UCMP 139183

External form and dimensions

This specimen is superbly preserved; it reveals the virtually complete form of a

tadpole, including head, body and tail (figs. 1-3). The specimen is preserved flat, with a

small amount of relief visible in oblique light. The ventral surface is up. The keratinized

beaks are conspicuous at the rostral end of the specimen. The maximum width of the

beaks is 3.5 mm. The beaks are relatively thin and the lower beak forms a very broad “U”

rather than a “V”.

The keratin of the beaks is extremely fragile and the margins of the beaks are not

adequately preserved to resolve serrations. Isolated specks of keratin around the beaks

may be fragments of the beaks or isolated denticles. However, in this specimen those

specks are neither sufficiently numerous nor symmetrically arranged so as to define

denticle rows.

Measurements (in mm): total length 69.2; head-body length 28.3; tail length 40.9 (as

much as 10 % of the terminal tip of the tail may be missing); maximum width of the body

at the abdomen 19.6; maximum length of thoracoabdominal portion 14.8; maximum width

of body at the branchial baskets 21.7; maximum width of specimen at level of eyes 18.4;

maximum diameter of eyes 2.7 (left) and 3.0 (right); interocular distance 10.6; internarial

distance ca. 3.9. Lee

Source : MNHN, Paris

WASSERSUG & WAKE 147

a 7 2 w9 £

Fig. 1. — A Miocene tadpole from Turkey (UCMP 139183).

BIBL. DU

MUSÉUM

PARG/

Source : MNHN, Paris

148 ALYTES 12 (4)

frontoparietal

parasphenoid

branchial arch

À otic capsule

vertebrae

intestine

Fig. 2. — An outline drawing of fig. 1, with prominent features discussed in the text indicated.

Source : MNHN, Paris

WASSERSUG & WAKE 149

Fig. 3. — Enlargement of the beak region of fig. 1. Note the fossilized keratinous beaks. Remnant

denticle rows are not visible in this illustration.

Skeletal elements

Although the specimen appears to be premetamorphic, some skeletal elements are

evident. Cartilage of the chondrocranium is represented as dark brown staining of the

underlying rock. The vague outline of the cranial base and ethmoidal region is visible.

More distinct are three obliquely oriented ceratobranchials on each side. These gill bars

define the branchial baskets, each of which is about 9 mm long and 8 mm wide.

The parasphenoid is well-developed and its outline is clear. The bone has the shape

of an inverted “T,” with the cultriform process gradually but continuously tapering

rostrally, to a sharp point. The alar processes are relatively narrow, parallel-sided, and

blunt-tipped. The parasphenoid is 7.6 mm long and 4.1 mm wide. The maximum width of

the cultriform process is 0.9 mm, and the maximum rostrocaudal dimension of the alar

processes is 1.1 mm. The caudal margin of the parasphenoid forms a shallow “V” on the

midline.

Elliptical ossifications of the prootic are evident. On the right side of the specimen the

prootic lies immediately lateral to the alar processes of the parasphenoïd, while on the left

Source : MNHN, Paris

150 ALYTES 12 (4)

the bone is displaced further laterally a short distance. The bones measure 2.3 mm

rostrocaudally and are 1.5 mm wide. The prootic ossification on the left is rotated with its

lateral portion facing rostrally. Each prootic has a hemispheric elevation filling the lateral

half, we interpret these thickened areas as mineral deposits in the endolymphatic sacs.

Paired frontoparietal bones are conspicuous lateral to the cultriform process of the

parasphenoid. These elongate elements taper to rostral points but are blunter posteriorly.

The bones are 5.0 mm long and 1.4 mm wide at the widest point (about three-fourths of

the distance back from their rostral tip). Each bone has a distinct elevated strip, now

facing laterally; this zone may represent matrix-filled evacuations, because they are

symmetrical and thus likely derive from the normal anatomy of the tadpole. They lie in

the middle third of each bone and are about 2 mm long and 0.5 mm wide. In life these

may have faced each other across the dorsal midline of the skull, delimiting a

frontoparietal fontanelle; if so, they have undergone postmortem rotation around their

longitudinal axis.

Preservation in the region of the craniovertebral joint is poor. Whereas each

exoccipital-first vertebral articulation can be discerned, resolution is insufficient to

interpret the shape of the condyles and cotyles.

A number of vertebrae are present, with the more anterior being better preserved,

probably because of more extensive ossification. À precise count is not possible because

of fragmentation. The first two vertebrae are slightly shifted off the midline, but the third

is displaced far to the left and somewhat rostrally, behind the prootic. What may be the

fourth and fifth vertebrae are fragments displaced to the right and left respectively. The

next five vertebrae are located in sequence and more or less along the midline. Thus, either

nine or ten vertebrae are present, depending on interpretation of the fragments. The first

three vertebrae display neural arch elements and centra; they are spool-shaped with

amphicoelous ends. Vertebrae six through ten are also spool-shaped, but they consist

mainly of neural arch elements, and these fade caudally so that the last element consists

only of paired, slightly concave impressions. Vertebrae six and seven appear to have

ossified centra.

No appendicular elements are observed. That feature, by itself, suggests that the

tadpole is at an early free-swimming stage. However, the fact that the parasphenoid,

exoccipital, prootic and many vertebral elements are ossified indicates that this tadpole

must be at a later stage of development. The ossification schedules of Xenopus (TRUEB &

HANKEN, 1992), Bombina (HANKEN & HALL, 1984, 1988), Rana (ERDMANN, 1933; KEMP &

HoyT, 1969), and Spea (WIENS, 1989) all suggest that this specimen is close to GOSNER’s

(1960) stages 36-38, i.e. a more mature but still premetamorphic larva.

Additional features

The eyes are clearly visible as two black spots, possibly resulting from retinal melanin.

They are located within the outline of the head but rather far laterally.

Elevations and depressions in the abdominal region (best seen with oblique lighting)

suggest intestinal coils. These are most evident as a weakly elevated and more lightly

Source : MNHN, Paris

WASSERSUG & WAKE 151

my we wa

“G

3.kasnPliqu# CO7C a.

Fig. 4. — A Miocene tadpole from Turkey (UCMP 139184). The photographs are oriented with the

snout of the specimen at 11 o’clock on both the cast and the counterpart. The eyes, beaks and

abdomen are easily visible on both parts. The greater width of the abdomen compared to the

head is probably a postmortem artifact.

stained area along the left margin of the specimen and an arched depression in the lower

left quadrant of the abdomen (i.e. on the anatomically right side of the specimen). The

depression first follows the curve of the abdomen but then bends caudally to the anal

region where it terminates. The topography suggests that the depression was produced by

the distal portions (colon and rectum) of the alimentary canal.

SPECIMEN UCMP 139184

External form and dimensions

This specimen consists of an imprint and a counterpart of the head and body of a

tadpole without the tail (fig. 4). The size of this specimen, the position of its eyes and

mouth, and the similarity of its skeletal elements to those of UCMP 139183 leaves little

doubt that the two are specimens of the same species at nearly the same stage of

development.

Measurements (in mm): maximum length of head + body 37.6; maximum width of

specimen (across abdomen) 28.3; maximum length of cranium 17.9; maximum width of

head at the eyes 18.5; maximum eye diameter 3.8.

Source : MNHN, Paris

152 ALYTES 12 (4)

Skeletal elements

In general this specimen displays fewer soft tissue features than the previous specimen,

but the bony elements present are more extensively ossified. No outline of the

chondrocranium can be seen. Our description focuses on features that distinguish this

specimen from UCMP 139183, and comparisons are to that specimen.

The imprint of the beak is more complete, and while most of the keratin has

deteriorated, the imprints show upper and lower beaks that are deeper in rostrocaudal

dimension. The maximum width of the beaks is 4.1 mm. The exterior surfaces of both

beaks have fine ridges and very finely serrated margins. Keratinized fragments of the beaks

and denticles are displaced both rostral and caudal to the beaks. Close to the beaks, both

rostrally and laterally, there are two to seven specks of keratin in tight rows. These appear

to be the keratinized remains of denticles, but the rows are so fragmentary as to preclude

determination of the number of rows present in life.

Neither the cultriform nor the alar processes of the parasphenoïid are fully intact, and

while the preserved portion of the bone measures 7.0 mm in length and 3.7 mm in width,

this element evidently was larger in life in this specimen than in the other. The relatively

large alar processes in this specimen, for example, have a maximum rostrocaudal

dimension of 1.7 mm and obscure the exoccipital region from view.

Prootic elements are not preserved, but circular impressions on both the primary cast

and the counterpart indicate the position of the mineral deposits in the endolymphatic sac.

Both sacs, with diameters of about 1.6 mm, are displaced rostrally, one sufficiently far

forward and lateral to contact the posterior edge of the eye.

The only other cranial elements preserved are the frontoparietals. These lie

approximately parallel to the long cultriform process of the parasphenoid, but they have

been subjected both to shear and torsion so that one is closer to the parasphenoid and

contacts it while the other is displaced laterally a third of the distance to the eye. The

maximum length of the frontoparietals is 5.8 mm; maximum width is 1.5 mm. These

elements are less well preserved than in the other specimen; they are wider posteriorly and

more ossified. The lateral emarginated zone described in the other specimen is not evident.

On the other hand, the frontoparietals in this specimen have a thickened ridge along their

lateral margins which we interpret as a flattened ventral ridge.

Parts of at least nine vertebrae are evident. The most fully preserved, in the middle

of the vertebral column, are rotated around the long axis of the body and display both

elements of the neural arch and the centrum. The more rostral vertebrae are displaced

laterally and appear to have been forced forward, partly under the skull, where they have

left impressions directly in the alar processes of the parasphenoid. The most caudal

vertebra is represented only by its split neural arch, one side more posterior than the other.

Remarkably, both the primary and counter impressions reveal the clear outline of the

notochord, which extends about two vertebral lengths (3.6 mm) behind the last vertebra.

It also can be seen continuing rostrally through the fragments of two vertebrae. The

notochordal impression is lost within the remains of the next most rostral vertebra but

then reappears and extends forward to within one vertebral length of the occiput.

Source : MNHN, Paris

WASSERSUG & WAKE 153

As in the other specimen, the greatest postmortem disturbance of the axial skeleton

is in the immediate postcranial region. Consequently, it is difficult to resolve critical

features in that anatomical region, such as a pectoral girdle or limb rudiments, which

would help stage this specimen. We also find no evidence of hind limbs or the pelvic girdle.

Nevertheless, the amount of ossification suggests that this tadpole, like UCMP 139183,

was at GosnER’s (1960) developmental stage 36-38 when it died.

ADDITIONAL MATERIAL

According to information provided by Dr. KASAPLIGIL (pers. comm.) and his

published observations (KASAPLIGIL, 1977, 1981), there are additional fossil amphibian

specimens, both anuran and urodele, in the collections he made from the site reported

here. These have been unavailable to us. However, Dr. KASAPLIGIL provided us with a

photograph of one additional tadpole (labeled as B.K. 5629), possibly now in the

collection of the Natural History Museum of the Mineral Research and Exploration

Institute of Ankara. We present his photograph (fig. 5), with the following comments: in

terms of size, degree of ossification, and developmental stage, this specimen appears to be

taxonomically identical to the two specimens described above. However, the specimen is

preserved in a more lateral view, with the head missing anterior to the parasphenoid, and

the distal half of the tail is also missing. The parasphenoid is ossified. There are at least

eight, and possibly nine, vertebrae but, as in the other specimens, the preservation in the

immediate postcranial area is inadequate to permit a precise description of skeletal

elements in this region.

DISCUSSION

Fossils of tadpoles and adult frogs were reported from the Miocene of Turkey by

PAICHELER et al. (1978), also from the Gürcü Valley, near the site of the fossils described

herein. These authors figured a fossil tadpole and assigned their specimens to Pelobates sp.

However, their brief and general account contains no description and mentions no

diagnostic features other than size and the presence of a beak. We believe that these

specimens are from the same strata as those described here and are taxonomically

identical. Reasons for our taxonomic assignment are presented below.

TAXONOMIC CONSIDERATIONS

The keratinized mouthparts immediately preclude assignment of these fossils to the

Pipoidea or the Microhylidae. The fact that the botanical associates of these tadpoles are

largely genera present in modern-day Turkey (KAsAPLIGiL, 1977, 1981) suggests that these

fossil tadpoles are likely to be members of genera extant in Asia Minor or neighboring

regions. Among extant European and western Asian taxa (BAsoëLU & Ozeri, 1973), the

Source : MNHN, Paris

R. AASA Pl

À: NES629

Fig. 5. — Photograph of an additional Miocene tadpole from the same deposit as those shown in figs.

land 2 (B.K. 5629). This photograph was provided by B. KasaPLiGiL. The specimen itself was

not examined, but from the notes of B. KASAPLIGIL it seems likely that it may be in the collection

of the Natural History Museum of the Mineral Research and Exploration Institute of Ankara.

The tadpole is preserved on its side and in the photograph is oriented with the snout at 10

o’elock. This specimen closely resembles the specimens illustrated in figs. 1-4 in terms of size,

shape, and extent of ossification.

Source : MNHN, Paris

WASSERSUG & WAKE 155

large size of the fossil tadpoles precludes assignment to Pelodytes, Discoglossus, Bombina,

Bufo, or the brown frogs within the genus Rana (for comparison, see descriptions and

illustrations in BOULENGER, 1897, DELWIG, 1928 and GRILLITSCH et al., 1983). The other,

larger Rana (i.e. the green frog group) have proportionately narrower bodies and longer

tails than our most complete specimen UCMP 139183.

The remaining extant genera to be considered are A/ytes and Pelobates. Unfortunately

the diagnostic features of the denticles, spiracle, oral disc, anal tube position, tail fin shape,

etc., are not observable in our specimens. Accordingly we are unable to assign our

specimens with certainty to either of these genera. However, several lines of evidence lead

us to make a tentative assignment to Pelobates.

The lateral eyes and nearly terminal mouth of the complete tadpole are more typical

of Pelobates than of Alytes (see figures in BOULENGER, 1897). The general form of the body

resembles that of tadpoles of Pelobates fuscus (e.g. figures in GRILLITSCH et al., 1983;

ScHuLZE, 1892). The denticles of the fossils are simple in structure and are neither

multicusped nor cupped. If we assume that the few denticles retained in the specimens are

complete (as they appear to be), they more closely resemble those of Pelobates

(BOULENGER, 1897: fig. 43) than of Alytes.

Osteological features of the fossil tadpoles, especially the shape and arrangement of

the parasphenoid and frontoparietal bones, resemble those of Pelobates (ROËEK, 1980:

figs. 38 and 43) and metamorphic Spea (WiENs, 1989), a North American pelobatid, and

contrast with those of many other extant anurans (as illustrated by D'UELLMAN & TRUEB,

1985: figs. 13.17-18). The pointed, tapered cultriform process and the orthogonally

oriented, blunt-ended alar processes of the parasphenoid of the fossils closely match these

features of the parasphenoïd in Pelobates cultripes and Spea bombifrons as illustrated by

ROËEK (1980) and Wiens (1989), respectively. Furthermore, the spacing size and shape of

the frontoparietals of the fossils, including the ventral ridge, match those features in the

two extant pelobatids with which we have compared them. Taken together, these

resemblances support our tentative assignment of the Turkish fossils to the pelobatid

genus Pelobates. The fossil tadpoles are not identical to those of modern Pelobates in all

discernible features, however. For example, the wider and thinner beaks of specimen

UCMP 139183 are more like those of Pelodytes and Alytes than of Pelobates.

Pelobatid frogs are an ancient group; divergence of Pelobates from the Scaphiopus-

Spea group in North America has been estimated at more than 100 million years, but the

frogs retain great morphological similarity and have changed relatively little over vast

periods of time (reviewed by SAGE et al., 1982). Given the geological age of our specimens

and the absence of critical features used to discriminate tadpoles of living species, we

consider it premature to assign the specimens we have studied to any species.

TAPHONOMIC CONSIDERATIONS

The fossils occur in very fine grained, laminated diatomaceous earth that is soft and

crumbles readily. KASAPLIGIL (1977: 25) reports that “the laminated diatomaceous earth

Source : MNHN, Paris

156 ALYTES 12 (4)

was oriented vertically and the sheets of these spongy rocks were naturally split into

book-size platelets. Due to absorption of rainwater we could pull out any piece with great

ease, just like pulling out books from a library shelf”. Elsewhere he speculates that

fossilization occurred as a result of volcanic activity which poured lava and hot volcanic

ash into the lake, causing rapid sedimentation of diatomaceous frustules. These, along

with the accumulation of fine silt from streams flowing into the lake, formed the laminated

diatomites and paper shales (KASAPLIGIL, 1981).

Frogs in this part of the world would be expected to breed in the winter and early

spring (BasoëLu & Üzeri, 1973). Based on the size and developmental stage of the fossils,

we speculate that the tadpoles were killed in mid to late spring.

ECOLOGICAL CONSIDERATIONS

The particularly globose body and relatively short tail of specimen UCMP 139183

characterizes a generalized pond tadpole adapted to life in standing water. The terminal

mouth and position of the eyes (more lateral than dorsal) characterize anuran larvae that

are active in the water column and not strictly benthic. The large branchial baskets

furthermore suggest that this Miocene form was an effective suspension feeder in life. Our

interpretation of the morphology of the fossils is consistent with the taphonomy of these

fossils and the associate plant fossils.

ACKNOWLEDGEMENTS

We thank the late Baki KASAPLIGIL for inviting us to describe these fossils and making the

materials available for study. He also provided a photograph. Other photographs are by the Scientific

Photographic Laboratory, University of California at Berkeley. We thank J. HANKEN for comments

on the manuscript and Z. ROëEK for providing useful information. Research in the laboratory of

R.W. is supported by the Natural Science and Engineering Research Council of Canada, and of D.W.

by the National Science Foundation (U.S.A.) and the Gompertz Professorship.

LITERATURE CITED

BOULENGER, G. À., 1897. — The tailles batrachians of Europe. Part I. London, Ray Socie +

1-210.

BaçoëLu, M. & Üzeri, N., 1973. — Türkiye amfibileri. Ege Üniversitesi Fen Fakültesi Kitaplar Serisi,

50: 1-155.

DELwWiG, W., 1928. — Pelodytes caucasicus Blgr. Beschreibung der Larven nebst einigen Notizen über

Lebensweise und Fortpflanzung dieser Art. Zool. Anz., 76: 303-305.

DuELLMAN, W. E. & TRUEB, L., 1985. — The biology of amphibians. New York, McGraw-Hill: 1-670.

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WASSERSUG & WAKE 157

ERDMANN, K., 1933. — Zur Entwicklung des knochernen Skelets von Triton und Rana unter

besonderer Berucksichtigung der Zeitfolge der Ossifikationen. Z. Anat. Entwicklungsgeschichte,

101: 566-651.

Gosner, K. L., 1960. — A simplified table for staging anuran embryos and larvae with notes on

identification. Herpetologica, 16: 183-190.

GRILLITSCH, B., GRILLITSCH, H., HÂUPL, M & TIEDEMANN, F., 1983. — Lurche und Kriechtiere

Niederôsterreichs. Vienna, Facultas-Verlag: 1-176.

HANKEN, J. & HALL, B. K., 1984. — Variation and timing of the cranial ossification sequence of the

Oriental fire-bellied toad, Bombina orientalis (Amphibia, Discoglossidae). J. Morphol., 182:

245-255.

_— 1988. — Skull development during anuran metamorphosis. I. Early development of the first three

bones to form the exoccipital, the parasphenoïd, and the frontoparietal. J. Morphol., 195:

247-256.

KasaPLiGiL, B., 1977. — A late-Tertiary conifer-hardwood forest from the vicinity of Güven village,

near Kizilcahamam, Ankara. Bull. mineral Res. expl. Inst. Turkey, Foreign Edition, 88: 25-33

+ figs. 2-31.

—— 1981. — Past and present oaks of Turkey. Part I. Phytologia, 49: 95-146.

KemP, N. E. & HOYT, J. A., 1969. — Sequence of ossification in the skeleton of growing and

metamorphosing tadpoles of Rana pipiens. J. Morphol., 129: 415-444.

PAICHELER, J.-C., BROIN, F. DE, GAUDANT, J, MOURER-CHAUVIRÉ, C, RAGE, J.-C. & VERGNAUD-

GrAZZINI, C., 1978. — Le bassin lacustre Miocène de Bes-Konak (Anatolie, Turquie): géologie

et introduction à la paléontologie des vertébrés. Géobios, 11: 43-65.

ROËEK, Z., 1980. — Cranial anatomy of frogs of the family Pelobatidae Stannius, 1856, with outlines

of their phylogenies and systematics. Acta Universitatis Carolinae — Biologica, 1980: 1-164.

SAGE, R. D., PRAGER, E. M. & WAKE, D. B.. 1982. — A Cretaceous divergence time between pelobatid

frogs (Pelobates and Scaphiopus): immunological studies of serum albumin. J. Zool., Lond.,

198: 481-494.

Scnuzze, F. E., 1892. — Über die inneren Kiemen der Batrachierlarven. II. Mitteilung. Skelet,

Musculatur, Blutgefässe, Filterapparat, respiratorische Anhange, und Athmungsbewegungen

erwachsener Larven von Pelobates fuscus. Phys. Abh. Kônigl. Akad. Wiss. Berlin, 1892 (3): 1-66,

pl. I-VI.

Trurs, L. & HANKEN, J., 1992. — Skeletal development in Xenopus laevis (Anura: Pipidae). J.

Morphol., 214: 1-41.

WIENS, J. J., 1989. — Ontogeny of the skeleton of Spea bombifrons (Anura, Pelobatidae). J. Morphol.,

202: 29-51.

Corresponding editor: Alain DuBois.

Source : MNHN, Paris

Alytes, 1995, 12 (4): 158

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MODES OF PAYMENT

— In French Francs, by cheque drawn on a French bank payable to “ISSCA”, sent to:

ISSCA, Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire naturelle, 25

rue Cuvier, 75005 Paris, France.

— In French Francs, by direct postal transfer to the ISSCA postal account: “ISSCA”, Nr.

1-398-91 L, Paris.

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Oklahoma Museum of Natural History, University of Oklahoma, Norman, Oklahoma

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Source : MNHN, Paris

Alytes, 1995, 12 (4): 159-168. 159

Microscopia electrônica de barrido

del aparato bucal y de la cavidad oral

de la larva de Leptodactylus ocellatus

(Linnaeus, 1758) (Anura, Leptodactylidae)

Dinorah D. ECHEVERRIA

Facultad de Ciencias Exactas y Naturales (UBA), Departamento de Ciencias Biolôgicas,

Laboratorio de Vertebrados, 1428 Buenos Aires, Argentina

Scanning electron microscopy showed that the buccal apparatus of

Leptodactylus ocellatus lawwa has a well developed homny beak with teeth with

a main cusp. It has multicusped labial teeth with 6 to 8 denticles slightiy

marked neck and shows the tooth base (or homy sheath) as long as the paddle.

Larval intemal oral features are most similar to those of the L. fuscus group

(especially shape and location of the secretory pits, low number of buccal floor

arena papillae, 10 to 14 papillae on each side) and differ from them on the

presence of a prenarial channel on the buccal roof. The prenarial channel

could play a part in driving the feeding water with small food particles into the

buccal cavity and shunt the food then into the esophagus. The keratinized

buccal structures allow grazing activity on the periphyton. Planktonic diatoms

have been found in the foregut.

INTRODUCCION

En los anuros, la diagnosis de un taxôn especifico generalmente se basa en diversos

aspectos anatomicos y biolôgicos referidos a la forma adulta, mientras que al estadio

de larva sensu lato se le ha restado importancia. En el caso de Leptodactylus ocellatus

se ha estudiado el canto (BARRIO, 1964), la reproducciôn y el comportamiento aso-

ciado (Cr1, 1948, 1949; VAZ FERREIRA & GEHRAU, 1974, 1975), la serologia (Cet &

BERTINI, 1961), la bioecologia (GALLARDO, 1964) y la anatomia (LIMESES et al., 1972;

HEYER, 1968). Las larvas de Leptodactylus ocellatus han sido descritas por FERNANDEZ &

FERNANDEZ (1921) en los aspectos morfolôgicos generales. En la actualidad es posible

ampliar las descripciones de las larvas incluyendo en ellas, por ejemplo, la descripcion

del aparato bucal y de la cavidad oral realizada con microscopio electrénico de

barrido.

Las larvas de los leptodactilidos han sido ampliamente estudiadas en tal sentido por

WaASsERSUG & HEYER (1983, 1988). Estos autores han establecido pautas generales para la

caracterizaciôn morfolôgica de los renacuajos de aguas quietas (pond tadpole) y de aguas

corrientes (stream tadpole) que involucran relaciones fundamentales entre la anatomia

bucal y el medio ambiente en que se desarrollan.

Source : MNHN, Paris

160 ALYTES 12 (4)

El propésito de este trabajo es completar la caracterizaciôn anatémica de la boca y

de la cavidad bucal de las larvas de Leptodactylus ocellatus describiendo los caracteres

microanatémicos de las mismas y discutir las implicaciones ecolôgicas que surjan.

MATERIAL Y MÉTODOS

La muestra consté de cuarenta y seis larvas de Leptodactylus ocellatus que fueron

capturadas en cuerpos de agua semipermanentes de la provincia de Buenos Aires (en las

localidades de Magdalena, Del Viso, Pilar, San Miguel y José C. Paz), y en la provincia

de Misiones (Posadas). Las larvas forman parte de la coleccion de larvas depositadas en

el Laboratorio de Vertebrados bajo las siglas: LARV-DDE y LARV-DDE-MEB.

Los ejemplares corresponden a los estadios 31 al 38 segün la nomenclatura de GOSNER

(1960).

Las larvas fueron fijadas in toto en Ancel y Vitemberger (RoUGH, 1962) o formol al

10 %.

Las observaciones del aparato bucal y de la cavidad oral se efectuaron con

microscopio electrénico de barrido (MEB) y estereoscopico. Combinando ambos métodos

de observaciôn se compusieron las figuras 5a y 5b que integran los detalles del resto de las

figuras.

Para facilitar el estudio con MEB se procedié a separar la regin del disco oral del

resto del cuerpo. Para efectuar el exâmen de la cavidad oral se separaron las regiones del

techo y piso de la boca, segün la técnica aplicada por WASsERSUG (1980).

En el caso de utilizar el microscopio estereoscopico, se procedié a realzar la forma de

las papilas y püstulas dejando extender una gota de azul de metileno (en solucién acuosa

1%) o de hematoxilina de Carazzi, sobre cada pieza a examinar sumergida en formol al

4%.

El material utilizado para las observaciones con MEB fue deshidratado paulatina-

mente segün la técnica aplicada por FIORITO DE LÔPEZ & ECHEVERRIA (1984). La

metalizaciôn de las piezas se realizo en oro-paladio.

La nomenclatura aplicada para la descripcin del aparato bucal y de los dientes

cérneos se basé en las propuestas por VAN Duk (1966) y DEUNFF & BEAUMONT (1959)

respectivamente. En cuanto a la nomenclatura de la cavidad bucal se utilizé la propuesta

por VIERTEL (1982).

RESULTADOS

El borde papilar del disco oral presenta una brecha dorsal amplia (fig. 1). Las papilas

marginales se disponen en las zonas laterales y ventral del disco. Las papilas presentan

forma cônica, con el extremo liso y romo, siendo las de posicién mental las que presentan

Source : MNHN, Paris

ECHEVERRIA 161

Fig. 1. — Vista general del aparato bucal. A-1: primera hilera anterior; A-2: segunda hilera anterior;

P-1: primera hilera posterior; P-2: segunda hilera posterior; P-3: tercera hilera posterior; PI: parte

inferior del pico crneo; PS: parte superior del pico côrneo; m: papila marginal. Escala: 100 p.

Fig. 2. — Infrarostrodontos. Escala: 10 p.

Fig. 3. — Queratodontos en P-3. C: cono de la raiz o cubierta cornea; E: espätula. Escala: 10 p.

Fig. 4. — Queratodontos en A-1 desgastados. Aspecto modificado de la espätula (e) y cubierta côr-

nea (c). 1: del diente côrneo por desprenderse; 2: del diente côrneo emergiendo. Escala: 10 p.

mäs marcadamente este ültimo caräcter (fig. 1). En la region lateral del disco se hallan

varias hileras de papilas, mientras que en el borde papilar mental y angular superior

generalmente se hallan dos hileras alternadas con papilas de distinta altura.

El pico cérneo estä bien desarrollado y queratinizado. Los rostrodontos estän

dispuestos en empalizada; presentan una cüspide aguda o redondeada (fig. 2).

Los pliegues labiales se disponen en cinco hileras, dos anteriores y tres posteriores que

sostienen a los queratodontos. Esta disposiciôn determina la formula dentaria 2/3 en todos

los ejemplares de la muestra. Todas las hileras se extienden desde un extremo al otro de

Source : MNHN, Paris

162 ALYTES 12 (4)

las äreas marginales laterales. En algunos casos la P-1 puede presentar una escotadura

mediana dirigida hacia la regién bucal (fig. 1).

Los queratodontos presentan una espätula alargada, mäs larga que ancha, con

denticulos en nûmero de seis a ocho. El cuello es poco marcado. El cono de la raiz

generalmente alcanza el largo de la espâtula (fig. 3).

A medida que los dientes emergen, se puede observar que las camadas mâs antiguas

o distales pueden permanecer asociadas con la camada inmediata inferior que la sostiene.

Se observaron de una a tres camadas de dientes, la mâs distal con los dientes funcionales

desgastados mientras que de las restantes se observa solamente la cubierta cornea o cono

de la raiz donde se sostienen (fig. 4).

CAVIDAD BUCAL

Piso de la boca (fig. 5a)

El orificio de la boca se halla flanqueado por un par de papilas infralabiales (PI), con

dos ramas (papila bifurcada).

Sobre el esbozo lingual (L) se hallan tres a cuatro (estadios 31 al 33 en adelante,

respectivamente) papilas linguales (PL) conicas y altas.

La superficie del piso de la cavidad oral estä limitada por altas papilas periféricas

(PP), dispuestas en dos arcos laterales con 10 a 14 papilas en cada uno. Se pueden hallar

püstulas (papilas bajas, con el âpice romo, que apenas emergen del piso de la cavidad

bucal) sin orden aparente, pero que se hallan mäâs acumuladas en la region posterior de

la arena del piso de la boca (fig. 6).

Las hendiduras bucales (H) son alargadas, elipticas y estän orientadas con el extremo

interno dirigido hacia la region anterior de la cavidad oral.

El velo ventral (V) presenta proyecciones marginales (F) espaciadas y una escotadura

mediana (M) bien marcada.

Se hallan fosetas glandulares sobre las proyecciones marginales del velo y sobre los

bordes que las separan (fig. 7).

Techo de la boca (fig. 5b)

El ârea prenarial presenta un par de tabiques bajos dispuestos en forma de L invertida

(canal prenarial) (fig. 8).

Las coanas (C) elipticas estän dispuestas en posiciôn transversal, respecto de la

cavidad bucal. Las välvulas nasales (N) estän bien desarrolladas y presentan un borde

discontinuo (fig. 5b).

Bordeando el ârea postnarial se hallan tres pares de formaciones: (1) un par de papilas

postnasales (P) bien desarrolladas y alargadas, cuyo borde ventral se observa convexo y

discontinuo, levemente festoneado; (2) un par de papilas pre-pliegue (PG), es decir papilas

Source : MNHN, Paris

Fig. 5. — Cavidad oral. a: piso; b: techo. C: coana; CP: canal prenarial; F: proyecciôn marginal; G: regiôn glandular;

H: hendidura (0 bolsillo) bucal; L: esbozo lingual; LP: pliegue lateral; M: escotadura mediana; MP: pliegue mediano:

N: välvula nasal; P: papila postnasal; PG: papila pre-pliegue; PI: papila infralabial; PP: papilas periféricas del ârea del

piso de la boca; PM: papilas del märgen de la arena del techo de la boca; PL: papilas linguales, PLT: papilas laterales

del techo de la boca; V: velo. Escala: 100 y.

VRAI

€9l

Source : MNHN, Paris

164 ALYTES 12 (4)

Fig. 6. — Detalle de la arena del piso de la boca. Escala: 100 p.

Fig. 7. — Proyecciôn marginal del velo, con fosetas glandulares. Escala: 10 p.

g. 8. — Vista general de la regiôn anterior del techo de la cavidad bucal. CP: canal prenarial. Escala:

1000 p.

Fig. 9. — Grupo de papilas laterales del techo de la boca. Escala: 100 p.

de posiciôn anterior al pliegue lateral, que presentan escaso tamaño, aproximadamente 1/4

de la longitud de la papila postnasal; (3) un par de formaciones que constituyen el pliegue

lateral (LP). Cada proyeccion del pliegue lateral presenta el borde dorsal liso y convexo,

mientras que el borde ventral presenta seis a siete proyecciones o papilas, siendo mäs

prolongadas una o dos de las centrales.

El pliegue mediano, en forma de proyecciôn semicircular, presenta en el borde ventral

mediano, pequeños salientes o püstulas que se acentüan en los estadios 35. La cara

anterior muestra escasas püstulas y la cara posterior es lisa.

En la superficie del techo de la boca son notables las püstulas centrales rodeadas por

largas papilas cônicas y simples. Las papilas del techo de la boca pueden hallarse en

Source : MNHN, Paris

ECHEVERRIA 165

Fig. 10. — Diatomeas en el contenido del intestino anterior. 1: Fragilaria ulna; 2: Nitzschia sp. Escala:

lu.

nümero de diez a doce en cada lado. A los lados del techo de la boca se halla un grupo

de papilas laterales (fig. 9).

La regiôn glandular (G) se dispone en forma de V en una amplia banda posterior en

la que se hacen visibles las fosetas secretoras redondeadas semejantes a las halladas sobre

las proyecciones marginales del velo ventral. El velo dorsal presenta escasas proyecciones

marginales hacia la regiôn mediana.

Cabe destacar que se hallaron früstulos de Fragilaria ulna y Nitzschia sp. en las

coanas, entre las hileras dentarias y en el intestino anterior (fig. 10).

DIsCUSIÔN

Los estudios realizados por WASsERSUG & HEYER (1983, 1988) en larvas de

leptodactilidos sudamericanos Ilevan a estos autores a concluir que se podria establecer

una relaciôn directa entre la proliferaciôn o aumento de tamaño de ciertas estructuras de

la cavidad bucal y la forma de vida de los renacuajos de aguas en movimiento, aunque

comentan que, en algunos casos, no les fue posible asociar la anatomia bucal con el

microhabitat.

Source : MNHN, Paris

166 ALYTES 12 (4)

La mayoria de las larvas examinadas por WaAssERSUG & HEYER (1988) que

presentaron caracteres orobranquiales de renacuajos de aguas quietas fueron Leptodacty-

lus chaquensis, L. mystacinus, L. fuscus y L. gracilis.

En Leptodactylus ocellatus se hallaron algunos caracteres morfolégicos comunes con

las especies anteriormente mencionadas como son la presencia de tres o cuatro papilas

linguales; el bajo nümero de papilas postnariales; y la papilaciôn del pliegue lateral. Si bien

se diferencia de las especies mencionadas por los siguientes caracteres: (1) la presencia de

un reborde antero-posterior en la region prenarial, o canal prenarial; (2) la presencia de

papilas laterales simples, aisladas y agrupadas, bien desarrolladas; (3) los märgenes del

velo dorsal con papilas espaciadas y bien desarrolladas, que se hallan mäs abundantes

hacia la region mediana; (4) el desarrollo de las papilas del puente medio sobre el margen

ventral.

El canal prenarial propio de L. ocellatus muestra una disposiciôn parecida al relieve

que presentan en la cavidad oral las larvas de Colostethus nubicola, dendrobätido con boca

en embudo hallado en charcas de desbordes de las märgenes del Rio Aquabiena en Costa

Rica (WASsERSUG, 1980). Ademäs las larvas de L. ocellatus comparten con los hylodinos

de aguas corrientes la combinaciôn de caracteres referidos a la posicién, forma y desarrollo

de las papilas bucales y del velo. Estas caracteristicas son asociadas por WASSERSUG &

HEYER (1983, 1988) a la vida en aguas en movimiento, cuando en realidad el habitat mäs

frecuente en que se desarrollan las larvas de L. ocellatus son las aguas estancadas, con

mucha vegetacion, preponderantemente con macrofitos enraizados.

Es posible que el canal prenarial hallado en L. ocellatus contribuya a favorecer el

desarrollo de una corriente de succiôn del agua con el alimento en suspensin que podria

contribuir a conducir el alimento directamente hacia el interior de la cavidad bucal donde

se hallan las abundantes y conspicuas fosetas secretoras de mucus.

GALLARDO (1974) y VAZ FERREIRA & GEHRAU (1971, 1974, 1975) han observado que

los renacuajos de L. ocellatus se reünen en cardümenes, que se alimentan de diatomeas y

algas cianoficeas y que en ciertas oportunidades raspan el dorso de los adultos para

conseguir alimento. Estas afirmaciones indicarian, en primera instancia, que los renacuajos

de L. ocellatus podrian implementar distintas estrategias de obtencion del alimento.

À juzgar por los grandes acümulos de früstulos de diatomeas como Fragilaria ulna

presentes en el plancton hallado en el exterior de la boca y en el intestino anterior de las

larvas de L. ocellatus examinadas, y considerando la tendencia de las mismas al

gregarismo, es posible que al desplazarse en el agua ondulando la cola, el cardumen podria

provocar una corriente de agua que movilice los microfitos (algas epiliticas y epifiticas) que

se hallaren a su alrededor, en el bentos y perifiton. Cada miembro del cardumen podria

lograr encauzarlos hacia el interior de la boca favorecidos por la presencia del canal

prenarial. Esta estrategia alimentaria no implica necesariamente la ausencia de dientes

corneos; de hecho, L. ocellatus los presenta espatulados y bien distribuidos, con una

férmula dentaria constante (2/3), lo que les permitiria, en otras oportunidades, raspar las

superficies de los macrofitos sumergidos. Esta acciôn podria ser ejercida escasamente por

las larvas cuando pueden obtener alimento de capturas en grupo. La presencia de varias

camadas de queratodontos sin desprenderse asi podria indicarlo. De acuerdo con las

observaciones de FIORITO DE LOPEZ & ECHEVERRIA (1989) en Bufo arenarum, si los dientes

Source : MNHN, Paris

ECHEVERRIA 167

labiales funcionales fueran sometidos frecuentemente a la acciôn de raspar, no podrian

sostenerse varias camadas en el exterior. Es posible que la existencia en L. ocellatus de una

combinaciôn de caracteres propios de larvas de estanque y de aguas en movimiento se

pueda atribuir a un fenémeno de convergencia adaptativa. Esto quizäs podria estar

apoyado por las estrategias alimentarias que utilizan y el tamaño de la particula de

alimento hallado mäs frecuentemente (diatomeas epifitas), que deberân concentrar para ser

ingeridos en grandes cantidades, sin utilizar directamente los queratodontos.

RESUMEN

Las observaciones del aparato bucal y de la cavidad oral con microscopio electrénico

de barrido de las larvas de Leptodactylus ocellatus revelaron que ellas poseen un pico

corneo bien desarrollado, con dientes que presentan una cüspide. Los dientes labiales son

multicuspidados, con 6 a 8 denticulos; y con un cuello levemente marcado.

La cavidad oral mostré caracteres similares a las larvas del grupo L. fuscus hasta el

momento estudiadas (especialmente en cuanto a la forma y localizaciôn de las fosetas

secretoras) y difieren de ellas por la presencia de un canal prenarial que se halla en el techo

bucal. El canal prenarial podria intervenir dirigiendo el flujo de agua con el alimento hacia

la cavidad bucal y permitir la circulacion del alimento hacia el esofago. Las estructuras

cérneas permiten también utilizar el perifiton como alimento.

En el intestino anterior se hallaron acmulos de früstulos de diatomeas planctnicas.

AGRADECIMIENTOS

Al señor Dante GIMENEZ del Servicio de Microscopia Electrônica de Barrido dependiente del

Instituto de Investigaciones Cientificas y Técnicas de las Fuerzas Armadas (CITEFA), por el apoyo

técnico brindado. À la Lic. Olga B. VACCARO por su contribuciôn con las larvas de la localidad de

Magdalena. À la Dra. Graciela B. ESNAL por facilitarme la utilizaciôn del microscopio estereoscépico

con cämara de dibujo.

LITERATURA CITADA

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Cincuentenario Mus. prov. Cienc. nat. F. Ameghino, S. Fé: 51-19

Cu, 3. M. 1948. — El ritmo estacional en los fenômenos ciclicos endôcrinosexuales de la rana criolla

Leptodactylus ocellatus (L.) del norte argentino. Acta zool. lilloana, 6: 283-331.

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Leptodactylus ocellatus (L.) de la Argentina. “Razas de temperatura” y sus relaciones con

algunas caracteristicas climâticas regionales. Acta zool. lilloana, 7: 113-134.

Cu, J. M. & Berri, F., 1961. — Serum proteins in allopatric and sympatric populations of

Leptodactylus ocellatus and L. chaquensis. Copeia, 1961: 336-340.

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DEUNFF, F. & BEAUMONT, A., 1959, — Histogénèse des dents et du bec cornés chez les larves de

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FioriTo DE LôPez, L. E. & ECHEVERRiA, D. D., 1984. — Morfogénesis de los dientes larvales y pico

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Zool., 13 (60): 573-578.

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Bufonidae). Cuad. Herp., 4 (2): 4-10.

GALLARDO, J. M., 1964. — Consideraciones sobre Leptodactylus ocellatus (L) (Amphibia, Anura) y

especies aliadas. Physis, 24 (68): 373-384.

—— 1974. — Anfibios de los alrededores de Buenos Aires. Buenos Aires, Eudeba: 1-231.

Gosner, K. L., 1960. — A simplified table for staging anuran embryos and larvae, with notes on

identification. Herpetologica, 16: 183-190.

Limeses, C. E., VIGnes, [. & Tio, M., 1972. — Las especies argentinas del género Leptodactylus

(Anura, Leptodactylidae). Algunos aspectos anatômicos de posible significaciôn taxonémica.

Parte II. Physis, 31 (83): 631-652.

LyncH, J. D., 1973. — The transition from archaic to advanced frogs. In: J. L. ViaL (red.),

Evolutionary biology of the anurans, Columbia, Univ. Missouri Press: 133-182.

Hever, W. R., 1968. — The proper name for the type-species of the genus Leptodactylus. Copeia, 1968

(1): 160-162.

— 1969. — The adaptive ecology of the species groups of the genus Leptodactylus (Amphibia,

Leptodactylidae). Evolution, 23 (3): 421-428.

ROUGH, R., 1962. — Experimental embryology. Techniques and procedures. Burguess Publishing Co.

Va Dux, D. E., 1966. — Systematic and field keys to the families, genera and described species of

the southern African anuran tadpoles. Ann. Natal. Mus., 18 (2): 231-286.

Vaz FERREIRA, R. & GEHRAU, À., 1971. — Agrupaciones y comportamiento social de renacuajos de

L. ocellatus (L). Resumen V Congreso Latinoamericano Zool.: 12-13.

1974. — Protecciôn de la prole en leptodactylidos. Revista Biol. Uruguay, 2 (1): 56-62.

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Leptodactylidae). I. Atenciôn de la cria y actividades alimentarias y agresivas relacionadas.

Physis, 34 C (88): 1-14.

VierreL, B., 1982. — The oral cavities of central european anuran larvae (Amphibia): morphology,

ontogenesis and generic diagnosis. Amphibia-Reptilia, 4: 327-360.

WASSERSUG, R., 1980. — Internal oral features of larvae of eight anuran families. Misc. Publ. Mus.

nat. Hist. Univ. Kansas, 68: 1-146.

WASSERSUG, R. & HEYER, W. R., 1983. — Morphological correlates of subaerial existence in

leptodactylid tadpoles associated with flowing water. Can. J. Zool., 61: 761-769.

1988. — A survey of internal oral features of leptodactylid larvae (Amphibia: Anura).

Smithsonian Contrib. Zool., 457: 1-99.

Corresponding editor: Marvalee H. WAKE.

Source : MNHN, Paris

Alytes, 1995, 12 (4): 169-174. 169

Notas sobre la miologia apendicular

de Phyllomedusa hypocondrialis

(Anura, Hylidae)

Adriana S. MANZANO & E. O. LAVILLA

Instituto de Herpetologia, Fundaciôn Miguel Lillo,

Miguel Lillo 251, 4000 Tucumän, Argentina

Phyllomedusa hypocondrialis is unusual among anurans in having areas of

the long bones of fore- and hindlimbs not covered by muscles. This situation

is due to three factors: (1) thin muscles; (2) unusual insertion of muscles;

(3) shortened muscles. There is no reduction in the number of muscles; on the

contrary, some have accessory slips, and some girdle and limb muscles are

reported for the first time among « hyloids » or even among all anurans.

INTRODUCCION

En el marco de un estudio mäs amplio sobre la musculatura de los miembros y

cinturas de las especies argentinas de Hylidae notamos una serie de caracteristicas

particulares en Phyllomedusa hypocondrialis, destacändose la existencia de regiones mäs o

menos amplias de los huesos largos no cubiertas por müsculos, asi como la presencia de

müsculos no reportados entre los “hyloideos”’ (Neobatrachia no Ranoïdea, “Bufonoidea”

en el sentido de FORD & CANNATELLA, 1993), y de otros no registrados aüûn en ningün

anuro conocido.

Estos hechos son significativos si tenemos en cuenta que los taxa del género

Phyllomedusa presentan una serie de caracteres morfolégicos y etolégicos de importancia

en relaciôn a sus miembros, entre los que se destacan la presencia de pulgares oponibles

en manos y patas, las extremidades muy largas en relaciôn al tamaño del cuerpo, la

locomociôn por braquiacion en ärboles, con saltos ocasionales, el acicalamiento, por

medio del cuäl esparcen secreciones cerosas por todo el cuerpo y la construcciôn de nidos

con hojas de ärboles. “

MATERIAL Y METODOS

Se estudiaron 2 hembras y 2 machos de Phyllomedusa hypocondrialis, Fundaciôn

Miguel Lillo (FML) 04286. Como material de comparaciôn se analizaron, ademäs,

2 ejemplares de Phyllomedusa sauvagii (FML 04899), 2 ejemplares de Phyllomedusa

boliviana (FML 02706) y 2 ejemplares de Scinax fuscovaria (FML 04635).

Source : MNHN, Paris

170 ALYTES 12 (4)

Para analizar la musculatura se empleé una combinacién de las técnicas de

WaASsERSUG (1976) y de Bock & SHEAR (1972), con la que se tiñen los huesos de rojo y los

cartilagos de azul de manera permanente, y los müsculos se resaltan transitoriamente en

castaño. De este modo se diferencian fâcilmente müsculos, fascias, aponeurosis, tendones,

huesos y cartilagos.

La nomenclatura empleada sigue las propuestas de DUELLMAN & TRUEB (1985),

DunLAP (1960), ECKER (1889) y NOBLE (1922).

RESULTADOS

LA MUSCULATURA DE LOS MIEMBROS Y SU RELACIÔN CON LAS ÂREAS EXPUESTAS DE HUESO

En los miembros anteriores de Phyllomedusa hypocondrialis se han registrado âreas de

hueso expuestas en las caras ventral y laterales del hümero (fig. 1a), y ésto es debido a dos

factores. Por una parte, los müsculos deltoides episternalis, pectoralis epicoracoideus

anterior y posterior, pectoralis abdominalis interno y externo, coracobrachialis longus

superficial y profundo y el coracoradialis, que se originan en la cara externa (ventral en

posiciôn fisiologica) de la cintura pectoral, muestran las âreas de insercion desplazadas

hacia la mitad proximal de la cara ventral del hümero. Este hecho deja la mitad distal de

la diäfisis humeral prâcticamente libre de inserciones musculares. Por su parte, los

müsculos triceps brachialis lateral interno, medio y lateral externo son muy delgados, y

sélo cubren la cara dorsal del hämero, sin desbordar hacia las regiones laterales.

En los miembros posteriores, las äreas de hueso expuestas se localizan en la cara

dorsal del fémur y a lo largo de tibia-fibula (fig. 1b).

Los responsables de la exposiciôn de porciones del fémur son los müsculos adductor

longus e ileofemoralis. El primero se encuentra adelgazado y no Ilega a hacer contacto

lateral con el sartorio, mientras que el segundo se encuentra acortado y adelgazado,

estando limitado a la regiôn proximal ventral del fémur.

En la tibia-fibula, los müsculos tibialis anticus longus, extensor cruris brevis y tibialis

anticus brevis estän muy adelgazados y limitados a la cara dorsal del hueso, y no

establecen contacto lateral con los müsculos plantaris longus y tibialis superficialis. Estos

dos ültimos elementos, por su parte, son también muy delgados y estän restringidos a la

cara ventral de la tibia-fibula. Conviene señalar, ademäs, que el müsculo plantaris longus

no alcanza a cubrir al tibialis superficialis.

NUEVOS REGISTROS MUSCULARES

En los miembros y cinturas de Phyllomedusa hypocondrialis se han registrado

müsculos previamente no reportados entre los “hyloideos”, asi como otros que se registran

por primera vez entre los anuros.

Source : MNHN, Paris

MANZANO & LAVILLA 171

Fig. 1. — Phyllomedusa hypocondrialis: (a) miembro anterior en vista ventral; (b) miembro posterior

en vista ventral.

Las äâreas de hueso expuestas se muestran en punteado oscuro.

CR: m. cruralis; CV: m. adductor magnus, caput ventral; DE: m. deltoides episternalis; EC:

m. extensor cruris brevis; GMA: m. gracilis major; GMI: m. gracilis minor; IS: m. ichiocutaneus;

PAE: m. pectoralis abdominalis externus; PEA: m. pectoralis epicoracoideus anterior;

PE: peroneus; PI: m. pectoralis abdominalis internus; PL: m. plantaris longs; PP: m. pectoralis

epicoracoideus posterior;, SA: m. sartorius; ST: m. semitendinosus; TA: m. tibialis anticus;

TP: m. tibialis posticus.

Source : MNHN, Paris

172 ALYTES 12 (4)

En la primera categoria se incluyen müsculos que hemos homologado por su

estructura y posicion a los müsculos ischiocutaneus (reportado por NoBLe, 1922, en

Scaphiopus, Bombina y Rhinophrynus) y subscapularis (mencionado por ECKER, 1889, para

Ranidae).

Entre los nuevos müsculos registrados en anuros, se señalan:

(1) En la cintura pectoral, un müsculo que Ilamamos epicoracoideus (fig. 2a) se origina

en el extremo proximal de los epicoracoides, en su punto de uniôn con las claviculas, y se

inserta en el extremo distal de los mismos. Es una banda muscular corta y angosta, y

recubre a los epicoracoides tanto externa- como internamente (caras ventral y dorsal en

posiciôn fisiolgica). Es independiente, y no presenta relaciones con los müsculos rectus

abdominis y sternohyoideus.

(2) En la cintura pélvica, un muüsculo que Ilamamos iliacus accesorius ventralis (fig. 2b)

se origina en la mitad proximal dorsal del cuerno iliaco y se inserta sobre la region

proximal del ilion, por medio de un tendén. Se trata de un par de muüsculos largos, que

corren paralelos al margen interno del cuerno iliaco. A pesar de su origen e inserciôn

dorsales, son visibles ventralmente.

(3) En los miembros posteriores, un müsculo que Ilamamos /emoralis (fig. 2c) se

origina en la cara dorsal de la mitad distal del fémur, y se inserta en la base del condilo

distal del mismo hueso. Es un elemento triangular y corto, ubicado préximo al müsculo

iliaco interno.

DISCUSION Y CONCLUSIONES

En la generalidad de los anuros conocidos, los miembros presentan una capa

profunda de müsculos, generalmente cortos y con origen e inserciôn en un mismo hueso,

y otra superficial, formada por müsculos mâs largos que pueden extenderse sobre mäs de

un hueso. Estas capas musculares revisten casi completamente a los elementos esqueléticos,

y las pocas âreas de hueso expuestas corresponden a las regiones articulares, donde se

observa la inserciôn de tendones, aponeurosis, fascias, etc.

Phyllomedusa hypocondrialis se aparta de este patron, y la existencia de äreas

expuestas en los huesos largos de los miembros se debe a un complejo de factores, entre

los que se destacan: (1) la existencia de müsculos muy delgados que no hacen contacto

lateral entre si; (2) la existencia de müsculos cuyos puntos de insercién se encuentran

desplazados hacia los extremos de los huesos; (3) la existencia de müsculos que combinan

los dos factores anteriores.

En contra de lo que se podria pensar, no se ha verificado la ausencia de müsculos si

comparamos a Phyllomedusa hypocondrialis con otras especies del género (por ejemplo:

Phyllomedusa sauvagii, MANZANO, 1994; Phyllomedusa boliviana, obs. pers.), y sin embargo

se ha verificado la presencia de müsculos con cabezas accesorias (por ejemplo el müsculo

adductor magnus, con tres ramas en lugar de las dos generalmente presentes; la tercera,

o caput accesoria, fue registrada por NoBLe, 1922, en los “anfibios mäs avanzados” y por

nosotros en Scinax) y de un müsculo nuevo para el orden, el müsculo femoral

Source : MNHN, Paris

MANZANO & LAVILLA 173

Fig. 2. — Phyllomedusa hypocondrialis: (a) musculatura de la region pectoral; (b) musculatura

profunda de los iliones; (c) musculatura profunda del fémur.

CO: m. coracoradialis; CR: m. cruralis; DE: m. deltoideus episternalis; E: m. epicoracoideus;

F: m. femoralis; IAV: m. iliacus accesorius ventralis; II: m. iliacus internus; PEA: m. pectoralis

epicoracoideus anterior; PEP: m. pectoralis epicoracoideus posterior; PES: m. pectoralis

esternalis.

Source : MNHN, Paris

174 ALYTES 12 (4)

A las particularidades señaladas de la miologia apendicular de Phyllomedusa hypocon-

drialis se debe agregar el registro de otros dos müsculos no reportados previamente en el

orden, el müsculo epicoracoideus en la cintura pectoral y el müsculo iliacus accesorius en

la cintura pélvica. El müsculo epicoracoideus no es mencionado en los trabajos cläsicos

sobre la miologia de anuros firmisternos (i.e. ECKER, 1889; GaupP, 1896) ni en los pocos

trabajos dedicados a formas arciferas (i.e. BIGALKE, 1927; JONES, 1933; LIMESES, 1968).

Analizando la literatura disponible, es evidente que el ünico otro anuro en el que se

ha reportado la existencia de äreas de huesos largos no cubiertas por müsculos es Cen-

trolene prosoblepon, que presenta la cara flexora del hümero descubierta (EATON, 1958).

Finalmente, es conveniente señalar que el müsculo epicoracoideus que acabamos de

describir no debe confundirse con el müsculo sterno-epicoracoideus, porciôn especializada

del müsculo rectus abdominis que fuera descripta por JONES (1933).

Pese a las diferencias miolôgicas señaladas, es notable que entre Phyllomedusa

hypocondrialis y los restantes miembros del género no existan, aparentemente, variaciones

de comportamiento.

LITERATURA CITADA

BIGALKE, R., 1927. — Zur Myologie der Erdkrôte (Bufo vulgaris, Laurenti). Z. Anat. Entw.-Gesch.,

82 (1): 286-353.

Bock, J. & SHEAR, S., 1972. — A stain method for gross dissection of vertebrate muscles. Anat. Anz.,

130: 222-227.

DuELLMAN, W. E. & TRUEB, L., 1985. — Biology of amphibians. New York, MeGraw-Hill: i-xix +

1-670.

Duntar, D. 1960. — The comparative myology of the pelvic appendage in the Salientia. J. Morphol.,

106: 1-76.

EATON, T.H., 1958. — An anatomical study of a neotropical tree frog, Centrolene prosoblepon

(Salientia: Centrolenidae). Univ. Kansas Sci. Bull., 39 (10): 459-472.

ECKER, A., 1889. — The anatomy of the frog. Oxford, Clarendon Press: i-xvi + 1-450.

Forb, L. S. & CANNATELLA, D. C., 1993. — The major clades of frogs. Herpet. Monogr., 7: 94-118.

Gaurr, E., 1896. — 4. Ecker's und R. Wiedershein's Anatomie des Frosches. 2 vols. Brawnschweg,

Friedrich Vieveg & Sohn.

JOnEs, E. [., 1933. — Pectoral musculature of Amphibia Salientia. Ann. Mag. nat. Hist., 12: 403-420.

LIMESEs, C., 1968. — Lepidobatrachus Budgett (Anura, Ceratophrynidae). Nota miolôgica comple-

mentaria. Physis, 28 (76): 127-134.

MANZANO, A. S., 1994. — Musculatura de los miembros de Phyllomedusa sauvagii (Anura: Hylidae).

Acta zool. lilloana, en prensa.

NoBLe, G. K., 1922. — The phylogeny of Salientia. [. The osteology and thigh musculature; their

bearing on classification and phylogeny. Bull. amer. Mus. nat. Hist., 46: 1-86.

TRUEB, L., 1973. — Bones, frogs, and evolution. /n: J. L. ViaL (red.), Evolutionary biology of the

anurans, Columbia, Univ. Missouri Press: 65-132.

WaASsERSUG, R. J., 1976. — A procedure for differential staining of cartilage and bone in whole

formalin-fixed vertebrates. Stain. Tech., 51 (2): 131-134.

Corresponding editor: W. Ronald HEYER.

Source : MNHN, Paris

Alytes, 1995, 12 (4): 175-182. 175

Reproductive cycle

of the Ozark zigzag salamander,

Plethodon dorsalis angusticlavius

(Caudata, Plethodontidae),

in north central Arkansas

Walter E. MESHAKA, Jr. * & Stanley E. TRAUTH **

* Archbold Biological Station, P. O. Box 2057,

Lake Placid, Florida 33852, U.S.A.

** Department of Biological Sciences,

“Arkansas State University,

State University, Arkansas 72467, U.S.A.

The reproductive cycle of the Ozark zigzag salamander, Plethodon dorsalis

angusticlavius, was studied from January to December 1987. Sexual maturity

was attained at the end of the second year of life (in early fall) for both sexes.

Unlike northem populations of small plethodons, seasonal reproduction was

annual for both sexes. Mean clutch size was 5.3 ova, and volked follicles were

present from January to May. The diameters of the vasa deferentia were

greatest from January to April. Only adult Ozark zigzag salamanders were

found on cedar glades and only during the mating season. Differential use of

the cedar glade during courtship was suggestive of a migration, a phenomenon

not previously reported for this species or its sibling species.

INTRODUCTION

Plethodon dorsalis angusticlavius is a small woodland salamander averaging 60-98 mm

in total adult length (CONANT & COLLINS, 1991) and occurs almost entirely within the

Ozark Mountains of the Interior Highlands region in the United States (DOWLING, 1956).

The geographic range of the nominotypical subspecies, P. d. dorsalis, is within the

northeastern United States and disjunct with that of P. d. angusticlavius (CONANT &

CoLuins, 1991). However, the range of P. d. dorsalis comes into contact with that

of its sibling species, P. websteri, of the southeastern United States (HIGHTON, 1979,

1985).

Reproductive characteristics of P. websteri reported by SEMLITSCH & WEST (1983) are

similar to those of P. d. angusticlavius from a location farther north than that of the

present study (WiLKkiNsoN et al., 1993). Little else has been published regarding the life

history of P. d. angusticlavius anywhere in its range, and the natural history of P. d.

dorsalis within its range remains unknown. In this study, we present data on the

reproductive cycle of P. d. angusticlavius in a different habitat located between those of

Source : MNHN, Paris

176 ALYTES 12 (4)

SEMLITSCH & WEsT’s (1983) study on P. websteri in South Carolina and WiLKINsON et al.”

(1993) study of P. d. angusticlavius in northern Arkansas.

MATERIALS AND METHODS

Salamanders were collected during the day from January to December 1987 at two

localities in north central Arkansas. City Rock Bluff (TI7N, R11, S31) in Stone County

and Calico Rock (TI7N, R11W, S28) in Izard County are comprised of cedar glades

bordered by oak-hickory forest, and each joins a system of rocky bluffs along the White

River which separates the sites by 3 km.

Salamanders were found under large rocks on the cedar glades and 100-150 m away

under wet leaf litter along the dripline of the rock formations at the bluffs. AII specimens

were killed in a dilute chloretone solution (20 %) within 24 hours of capture, fixed in 10 %

formalin, and stored in 70 % ethanol. All measurements were taken from specimens

preserved at least 30 days. Snout-vent length (SVL) was measured from the tip of the snout

to the anterior end of the vent to the nearest 0.1 mm with vernier calipers.

The number and diameters of follicles and the diameter of the anterior region of the

right testis and vas deferens were measured with a dissecting microscope and ocular

micrometer. Color of testes and the presence or absence of hypertrophied mental glands

were noted. Maximum number of eggs a female might lay was determined by counting the

largest set of follicles. Females were considered sexually immature if their ovaries

contained only white previtellogenic ova and if the females were smaller in body size than

the smallest females which contained vitellogenic ova.

The cloacal tissue containing the spermatheca of 45 females was excised and trimmed

for either transverse or sagittal sectioning (HUMASON, 1979). Relative amounts of sperm

present within the sections of spermathecal sacs were visually estimated as empty or at

least half-full. All specimens are deposited in the Arkansas State University Museum of

Zoology. Two standard errors (+ 2 SE) accompany mean measurements.

RESULTS

MALE REPRODUCTION

The testes and vasa deferentia of 54 males (SVL = 39.2 + 0.410 mm) exhibited

seasonal variation in size (Table I). Spermatogenic activity was probably greatest during

late summer prior to emergence of P. d. angusticlavius from summer retreats in October.

At that time the anterior region of the testes, swollen with sperm, was dark in color and

at maximum diameter (x = 1.7 + 0.063 mm). The anterior region of the testes began to

regress in December and was smallest in May (X = 0.616 + 0.055 mm).

Source : MNHN, Paris

MESHAKA & TRAUTH 177

Table I. — Monthly mean diameters (mm) of the anterior region of the right testes and

vasa deferentia in Plethodon dorsalis angusticlavius. Means are followed by 2 standard

errors. No salamanders were found from June to September.

Month Vasa deferentia

0.28 + 0.04

January

February

October

November

December

HHHHHHE

cocecces

Be di ei QD

DO IOG BR

1.02

1.00

0.9

0.8

0.5

1.7

1.6

1.4

DOLOI-N

Evacuation of sperm from testes in an antero-posterior direction was accompanied by

a concomitant increase in diameters of the vasa deferentia (Table I). By May the vasa

defcrentia had also reached their smallest diameter (X = 0.156 + 0.016 mm) and by

October they had enlarged slightly (& = 0.173 + 0.023 mm). Production of spermato-

phores occurs when the vasa deferentia are packed with sperm (FRANCIS, 1934). An

increase in the diameter of the vasa deferentia occurred from December through April.

From January through April, coinciding with mating, males were found almost exclusively

on the cedar glade habitat. After May mature males could not be found anywhere until

October.

FEMALE REPRODUCTION

The ovarian follicles of 60 mature females (SVL = 41.3 + 0.501 mm) exhibited

seasonal variation in size (fig. 1). Ovarian follicles were smallest (X = 1.14 + 0.020 mm)

after emergence of females from summer retreats. Follicles steadily increased in size and

were largest in early May (% = 2.68 + 0.110 mm), after which time no females could be

found until October. The average number of follicles was 5.3 + 0.125 mm (range: 3-9;

N = 267), and clutch size did not significantly increase with SVL (r = 0.131, p > 0.05).

Histological sections of spermathecae from 45 females revealed a seasonal presence of

sperm from January through May (fig. 1), during which time adult females were found

almost exclusively on the cedar glade habitat. Spermatophores were detected in

histological sections of spermathecae in January and March. Most spermathecae were full

of sperm during May and none contained sperm from October to December. No sperm

was present in non-reproductive females indicating that insemination generally occurred

only in females containing follicles of at least 1.7 + 0.066 mm (TRAUTH, 1984).

Source : MNHN, Paris

178

mmSVL

ALYTES 12 (4)

6 7

MONTH

11 12

Fig. 1. — Seasonal variation in the presence of sperm in the spermatheca of mature female Plethodon

dorsalis angusticlavius. Squares represent mature females. Closed squares indicate the presence

of sperm. Asterisks represent nonreproductive females.

8288882888

mmsSVL

> >> mu

LEZ Ai, 42)

…

MONTH

Fig, 2. — Size distribution in Plethodon dorsalis angusticlavius. Closed triangles represent males.

Closed squares represent females. Asterisks represent immatures.

Source : MNHN, Paris

MESHAKA & TRAUTH 179

GROWTH AND MATURITY

The smallest P. d. angusticlavius had a SVL of 15.9 mm (in November), and it showed

no remnants of abdominal yolk. Inaccessibility of hatchlings prior to November precluded

an accurate estimation of growing dates; however, a conservative growth rate of

approximately 0.76 mm per month was estimated if at least 25 months were necessary to

grow 19.0 mm (from 16.0 mm at hatching to a minimum of 35.0 mm at maturity).

Salamanders reproduce for the first time beginning January during their third year of life

(fig. 2). Average SVL's of mature males and females were not significantly different (p >

0.05).

SEASONAL ACTIVITY

Immature and mature salamanders were abundant in the wet leaf litter at the base of

the bluffs in October. In November and December, mature salamanders began to appear

under stones on the cedar glades 100-150 m from the bluffs. From January to April, adults

were at the peak of reproductive readiness and presumably were courting. During this time

interval, adults were found almost exclusively on the cool, wet, cedar glades. Adults were

observed in groups of up to four individuals under the many flat stones of this habitat.

Plethodon albagula, occasionally encountered in the wet leaf litter, was never observed on

the cedar glade.

In May, a few adults were found on the cedar glades. By June, adults were absent

from the increasingly xeric and hot cedar glades but could be found in the leaf litter of the

bluffs. Juveniles were never found on the cedar glades throughout this study. From July

through September, salamanders of all sizes could not be found anywhere despite vigorous

searching (fig. 2).

DISCUSSION

Growth during the first year of life in Plethodon dorsalis angusticlavius was at least 9

mm in SVL and, as in P. websteri (SEMLITSCH & WEsT, 1983), individuals exhibited a low

juvenile growth rate when compared to larger plethodontids (Houcx, 1977). A long

growing season accompanied by small adult size allowed these individuals to reach sexual

maturity by the end of their second year. As in P. websteri (SEMLITSCH & WEST, 1983) and

more northern P. d. angusticlavius (WiLKkiNsoN et al., 1993), adult size at the onset of

sexual maturity was the same for both sexes.

Distinct gonadal cycles in both sexes and the absence of enlarged ovarian follicles in

less than 4 % of reproductively mature females was suggestive of a seasonal and annual

reproductive cycle. Both reproductive traits are found in P. websteri (SEMLITSCH & WEST,

1983) and presumably in more northern P. d. angusticlavius (WiLKiNsON et al., 1993) which

have long active seasons. In contrast, northern and western populations of large and small

Source : MNHN, Paris

180 ALYTES 12 (4)

plethodons, such as P. glutinosus (HIGHTON, 1962), P. cinereus (SAYLER, 1966), P.

richmondi (ANGLE, 1969), P. vehiculum (PEACOCK & NUSSBAUM, 1973), P. larselli

(HERRINGTON & LARSON, 1987) and P. ouachitae (TAYLOR et al., 1990), exhibit a biennial

pattern of reproduction. Further, both sexes of the smaller forms mentioned above possess

larger minimum body sizes at sexual maturity and mean adult body sizes at northern

latitudes where the growing season is shorter.

By December, vasa deferentia were packed with sperm which is associated with

production of spermatophores (FRANCIS, 1934). Although December matings were

possible, no sperm or spermatophores were detected within the cloacal chambers of

females until January. BLANCHARD (1928) stated that the spermatophore cap is expelled

soon after mating. Consequently, our data suggest that the mating season began in

January and terminated in April.

The courting season of P. d. angusticlavius was different than the fall or spring

courtship seasons of many northern Plethodon populations (HIGHTON, 1962; SAYLER, 1966;

ANGLE, 1969; PEACOCK & NUSSBAUM, 1973; HERRINGTON & LARSON, 1987). Winter-spring

courtship of P. d. angusticlavius was possible probably because of the mild, wet winters

with which southern plethodons are associated (SEMLITSCH & WEsT, 1983; CAMP, 1988;

WILKINSON et al., 1993; this study).

No hatchlings were collected until November in 1987, but the presence of some larger

hatchlings in November as well as the emergence of postreproductive females in October

indicated that emergence of adults and the smallest hatchlings could occur in October.

Visits to both collection sites in October 1988 yielded hatchlings and postreproductive

females in the leaf litter, which corroborated our suggestion of an October emergence. In

wetter years and/or sites, a September emergence is just as feasible.

Comparisons of our results corroborated no latitudinal differences in the reproductive

cycle or active season within the small range of this subspecies (WILKINSON et al., 1993)

nor with its sibling species of the Southeast (SEMLITSCH & WEST, 1983). However, we did

detect a difference in reproductive phenology with respect to an adjoining habitat which

was structurally unlike that associated with eastern small plethodons. Unlike those of P.

websteri (SEMLITSCH & WEST, 1983), courting adult P. d. angusticlavius of this study had

access to cedar glades, a distinct habitat 100-150 m from the rocky bluffs. This habitat was

differentially used concurrent to the mating season of P. d. angusticlavius. Because we did

not mark animals, we are not certain that a breeding migration to the adjoining cedar

glade habitat had taken place. However, two lines of evidence suggest that this

phenomenon had occurred. First, individuals present on the cedar glade habitat were

exclusively adults. Secondly, at the peak of the courting season, very few adults could be

found anywhere but the cedar glade habitat.

Although the proximate causes for the purported migration phenomenon are

unknown, one observation may yield some insight. During the seasonally cool wet months

corresponding with courtship, the microhabitat under the flat rocks of the cedar glade, like

the wet leaf litter, was amenable to the presence of salamanders. Two major differences

were observed between these two habitats. First, noticeably smaller numbers of predators

and numbers of predator species were found under the rocks on the cedar glade than in

the bluff system. Perhaps the cedar glade was a safer habitat for courtship activities.

Source : MNHN, Paris

MESHAKA & TRAUTH 181

Second, in contrast to the heavily-canopied bluff, the cedar glade received full exposure to

the sun. Warmth, held in the heated sandstone, may have created a preferred thermal

microhabitat for the courtship activities of this subspecies. Little detail is provided by

WILKINSON et al. (1993) regarding habitat characteristics of their site from a county less

than 300 km north of our two study sites. Thus, we cannot be certain if differential use

of the cedar glade habitat is unique to P. d. angusticlavius or just to some populations.

The reproductive cycle and seasonal activity of P. d. angusticlavius were almost

identical to that of another population of conspecifics and its sibling species, P. websteri.

Unlike P. websteri, adult P. d. angusticlavius in our study were found almost exclusively

in a different habitat during the courting season. Perhaps the seasonally predator-poor

nature of the crevice-like (i.e. surface rock-to-substrate interface) cedar glade habitat and

an amenable microhabitat beneath the sandstone may have been responsible for this

phenomenon.

RESUMEN

El ciclo reproductivo de la salamandra Plethodon dorsalis angusticlavius fue exami-

nado en el periodo desde enero hasta diciembre 1987. Madurez sexual fue alcanzada al

final del segundo año de vida (el principio del otoño) en los dos sexos. Contrario a

poblaciones nortenas de pequeños plethodons, la reproduction fue anual en los dos sexos.

El nümero medio de la puesta es de 5.3 huevas y huevas vitelogenicas fueron producidos

de enero a mayo. Los diametros de las vasa deferentia son mas grandes de enero a abril.

Solamente las salamandras adultas fueron encontradas en cedros herbosos y solamente

durante la epoca de reproduccién. El uso diferencial de cedros herbosos sugiere una

migracion, un fenémeno no previamente reportado en esta especie o en su especie

hermana, P. websteri.

ACKNOWLEDGMENTS

This manuscript was extracted from a thesis presented to Arkansas State University for partial

fulfillment of MS degree to WEM in 1988. WEM extends his appreciation to other committee

members V. R. MCDANIEL and J. K. BEADLES for their support throughout time spent at ASU.

Fondest appreciation goes to W. E. and R. A. MEsHakA who have been a constant source of

encouragement in the endeavors of the senior author. Both authors acknowledge B. P. BUTTERFIELD,

P. MCLARTY, and the late R. L. Cox for their camaraderie and assistance in the field. Ronn ALTIG

kindly reviewed an earlier version of this manuscript.

LITERATURE CITED

ANGL

, J. P., 1969. — The reproductive cycle of the northern ravine salamander, Plethodon richmondi

richmondi, in the valley and ridge province of Pennsylvania and Maryland. J. Wash. Acad. Sci.,

59: 192-202.

Source : MNHN, Paris

182 ALYTES 12 (4)

BLANCHARD, F. N., 1928. — Topics from the life history and habits of the red-backed salamander in

southern Michigan. Amer. Nat., 62: 156-164.

Camp, C. D., 1988. — Aspects of the life history of the southern red-back salamander Plethodon

serratus Grobman in the southeastern United states. 4mer. Midl. Nat., 119: 93-100.

CoNaANT, R. & COLLINS, J. T., 1991. — A field guide to reptiles and amphibians of eastern and central

North America. Boston, Houghton Mifflin Company: 1-450.

DowLiNG, H. G., 1956. — Geographic relations of Ozarkian amphibians and reptiles. Southw. Nat.,

4: 174-189.

FRANCIS, E. T., 1934. — The anatomy of the salamander. Oxford, The Clarendon Press: 1-60.

HERRINGTON, R. E. & LARSON, J. H., Jr., 1987. — Reproductive biology of the Larch Mountain

salamander (Plethodon larselli). J. Herpet., 21: 48-56.

HiGHTON, R. T., 1962. — Revision of the north american salamanders of the genus Plethodon. Bull.

Florida State Mus., 6: 235-367.

- 1979. — A new cryptic species of salamander of the genus Plethodon from the southeastern

United States (Amphibia: Plethodontidae). Brimleyana, 1: 31-36.

ee 1985. — The width of the contact zone between Plethodon dorsalis and P. websteri in Jefferson

County, Alabama. J. Herpet., 19: 544-546.

Houcx; L. D. 1977. — Life history patterns and reproductive biology of neotropical salamanders. /n:

D. H. TayLor & S. I. GUTTMAN (eds.), The reproductive biology of amphibians, New York,

Plenum Press: 43-72.

HUMASON, G. L. 1979. — Animal tissue techniques. San Francisco, Freeman: 1-478.

PEACOCK, R. L. & NUSSBAUM, R. A., 1973. — Reproductive biology and population structure of the

western red-backed salamander, Plethodon vehiculum (Cooper). J. Herpet., 7: 215-224.

SAYLER, A., 1966. — The reproductive ecology of the red-backed salamander, Plethodon cinereus, in

Maryland. Copeia, 1966: 183-193.

SemarscH, R. D. & Wsr, C., 1983. — Aspects of the life history and ecology of Webster's

salamander, Plethodon websteri. Copeia, 1983: 339-346.

TayLor, C. L., WiLKINSON, R. F., Jr. & PETERSON, C. L., 1990. — Reproductive patterns of five

plethodontid salamanders from the Oachita Mountains. Southw. Nat., 35: 468-472.

TRAUTH, S. E., 1984. — Spermathecal anatomy and the onset of mating in the slimy salamander

(Plethodon glutinosus) in Alabama. Herpetologica, 40: 314-321.

WILKINSON, R. F., PETERSON, C. L, Mozz, D. & HOLDER, T., 1993. — Reproductive biology of

Plethodon dorsalis in northwestern Arkansas. J. Herpet., 27: 85-87.

Corresponding editor: Günter GOLLMANN.

Source : MNHN, Paris

Alytes, 1995, 12 (4): 183-189. 183

The impact of Alpine newts (Triturus alpestris)

and minnows (Phoxinus phoxinus)

on the microcrustacean communities

of two high altitude karst lakes

Robert SCHABETSBERGER, Christian D. JERSABEK & Susanne BROZEK

Zoological Institute, University of Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria

The zooplankton communities in two neighboring high altitude karst

lakes of similar size and water chemistry were entirely different from each

other. In one lake Alpine newts (Triturus alpestris) exploited the food

resources during summer, in the other fish (European minnow, Phoxinus

phoxinus) were the top predators. The zooplankton community in the fishless

lake consisted of several big species of crustaceans, whereas rotifers domina-

ted in the other. Although the diet of the newts consisted mainly of

crustaceans, their predation pressure was low compared to that of the fish

population. Population size of adult newts was at least ten times smaller than

that of sexually mature fish (1570 newts versus 17420 minnows).

INTRODUCTION

The shift in a zooplankton community from big crustaceans towards smaller species

due to size selective predation of fish was first described by HRBACEK (1962) and BROOKS

& Dopson (1965). Since then these ideas have been confirmed in many studies (GULATI et

al, 1990, and references therein). Less information is available about the impact of

zooplanktivorous urodele amphibians. Early studies with Ambystoma tigrinum in shallow

Colorado Alpine ponds have shown that this species exploited the available resources in

a manner nearly identical to fish (Dobson, 1970; ZARET, 1980). On the other hand, detailed

studies about community effects of zooplanktivorous urodeles have shown a weaker

impact (Morin et al., 1983; Morin, 1987; TAYLOR et al., 1988; STROHMEIER & CROWLEY,

1989). Whereas ZARET (1980) described Ambystoma as a “fish in amphibians garments”,

STROHMEIER & CROWLEY (1989) anticipated a low predation pressure of Notophthalmus

viridescens on invertebrates compared to foraging fish.

In the Alps, Triturus alpestris is the only urodele species inhabiting high altitude water

bodies. In Alpine ponds and lakes, Triturus alpestris is normally associated with big,

planktonic daphniids or diaptomid copepods, whereas, in lakes that contain introduced

fish, rotifers and small benthic crustaceans dominate the zooplankton (authors’ unpubli-

shed observations). In a detailed study we were able to show that daily food consumption

of Alpine newts is less than in salmonid fishes (SCHABETSBERGER & JERSABEK, in

press).

Source : MNHN, Paris

184 ALYTES 12 (4)

TABLE I. — Morphometric parameters and abiotic conditions of lakes GroBer Feichtauer-

see and Kleiner Feichtauersee.

Groker Feichtauersee Kleiner Feichtauersee

Altitude 1400 m 1390 m

Surface area 11344 m° 5174 m

Volume 30550 m° 7021 m°

Max. length 172 m 98 m

Max. depth 11.8m 41m

Max. surface 19.2 °C 212

temperature :

pH 7.55 - 8.64 7.30 - 8.42

Conductivity (25 °C) 137-235 uS 125-192 uS

In this study, we present data about zooplankton communities of the two neighboring

lakes GroBer Feichtauersee (Lake 1) and Kleiner Feichtauersee (Lake 2). Lake 1 contains

the European minnow (Phoxinus phoxinus) and in Lake 2 Alpine newts are the top

predators.

MATERIAL AND METHODS

Lakes 1 and 2 are situated in the North Eastern calcareous Alps of Austria. Both

lakes are just 50 m apart from each other and get their water from underground karst

springs. Whereas Lake 1 maintained its water level throughout the year, Lake 2 lost over

90 % of its spring water content during summer. In very dry summers Lake 2 can dry out.

Apart from this differences in hydrology, abiotic conditions of both lakes were very similar

(Tab. I). Both lakes were supersaturated with oxygen during summer. In winter the lakes

were covered with a 1.5 to 3 m thick ice-cover, which caused an oxygen depletion down

to 50 % saturation directly under the ice. Nevertheless, no anoxic conditions could be

found.

Water chemistry was analyzed following standard methods in a professional

hydrochemical laboratory (Forschungsstelle Nationalpark Kalkalpen, 4591 Molln, Aus-

tria). Zooplankton samples were taken with a Schindler-Patalas plankton trap (5 1) in

monthly intervals.

Adult newts were caught by scuba diving, anaesthetized with MS 222 and marked

individually (121 males; 89 females) by tattooing with Alcian Blue according to JoLy &

MiauD (1990). Population size was estimated with a multiple mark recapture method

(Jolly-Seber method, in KREBs, 1989).

Source : MNHN, Paris

SCHABETSBERGER, JERSABEK & BROSEK 185

Stomach contents were secured with a stomach flushing technique and preserved

in 4% formaldehyde. Prey items were determined and counted for diet analysis.

Stomach contents were divided into 8 prey categories: Amphipoda (Niphargus sp.)

(micro-) crustaceans (mainly Daphnia rosea and Arctodiaptomus alpinus); Hemiptera

(Sigara carinata), terrestrial prey (different Pterygota); Mollusca (Pisidium sp. and

Bythinia tentaculata); Coleoptera larvae (Agabus solieri and Hydroporus palustris);

Trichoptera larvae (Limnephilus sp.); skin sloughs. Prey categories were pooled for

each sex and sampling date, dried to constant weight at 60°C and weighed to the nearest

10 ug.

The “Index of relative importance” (IRI) was calculated for the different food

categories at consecutive sampling occasions (PINKAS et al., 1971):

IRI = (% N + % W) x % O,

where:

% N = prey category as percent of total number of ingested prey;

% W = prey category as percent of total weight of ingested prey;

% O = percent of stomachs containing prey category.

Sexually mature minnows were collected in the littoral zone by electro-fishing. They

were anaesthetized with a dilute solution of MS 222 and marked with one blue spot

ventrocaudal of the anal fin, using the same technique as described for the newts. After the

marking procedure, the fish were rinsed in a commercial antiseptic solution (Tetramin) to

prevent infection with Fungi or Protozoa.

Population size was estimated with a multiple mark recapture model (Schuhmacher

method in KREBs, 1989). In total, 2891 minnows were marked on four different sampling

occasions (17.06, 2.07, 19.07, 2.08.1992).

RESULTS

Big crustacean species like the cladoceran Daphnia rosea and the calanoid copepod

Arctodiaptomus alpinus dominate the zooplankton in Lake 2. In addition, benthic species

like Macrocyclops fuscus, Megacyclops viridis and Eucyclops serrulatus could be found in

the open water. The size (body length) of adult crustaceans ranged from 1.5 to 3 mm.

In contrast, only small rotifers and small developmental stages of cyclopoid copepods

occur in the pelagial zone of Lake 1. Cold stenotherm species like Keratella hiemalis,

Notholca squamula, Polyarthra dolichoptera, Synchaeta lakowitziana, Anuraeopsis mira-

cleae and Filinia hofmanni are present in the lake throughout the year. Further, the

eurytherm species Synchaeta pectinata, Polyarthra remata and Ascomorpha ecaudis

colonize the open water. All of these zooplankton species are smaller than 0.5 mm.

There was no evidence that differences in chemistry or hydrology are solely

responsible for the differences between the two zooplankton communities. In fact, the

deeper Lake 1 would be an ideal habitat for the crustacean species occurring in Lake 2.

Source : MNHN, Paris

186 ALYTES 12 (4)

Le]

6 à

a ©

£ o©

“10

&© +

+ ©

L02

June | July I August

Fig 1. — Temporal changes in the diet of adult Triturus alpestris. “Index of relative importance” of

different prey categories as percent of total scores.

Total population size of Alpine newts in Lake 2 was estimated to reach 1570 adults

(95 % confidence interval: 206-16777) at the beginning of their aquatic period (04.07.1992).

No marked animals were caught at the second sampling occasion resulting in poor

confidence limits and probably in an overestimation of population size. After 2 weeks

(18.07.1992), population size had dropped to a more reliable number of 270 animals

(84-1046).

Total population size of sexually mature minnows in Lake 1 was estimated to be

17422 individuals (16638-18570). Confidence limits were narrow, as approximately 13 %

of the total population were marked. The abundance of adult Alpine newts was at least

ten times less than that of minnows.

Alpine newts did use crustaceans as a major food resource (fig. 1). At the end of July,

Daphnia rosea constituted more than 98 % of all ingested food organisms. This resulted

from an interesting feeding strategy of newts. Daphnia rosea reached very high densities in

the shadows of rocks. Adult newts struck upwards into these aggregations with their anterior

legs up and their mouth open. They probably ingested several individuals with one stroke.

DisCUSSION

In Alpine lakes, calanoid copepods usually produce only resting eggs during summer.

The eggs sink to the lake bottom and hatching of nauplii occurs in the next spring

Source : MNHN, Paris

SCHABETSBERGER, JERSABEK & BROSEK 187

(univoltine reproduction). This strategy of reproduction makes these species more

vulnerable to predation compared to species producing several generations during one

season. Bright red coloration in some high altitude calanoid copepods is another

disadvantage when optically oriented predator fish are introduced into the lakes.

Daphniids in high altitude water bodies are usually large species and have fewer

generations than species in lowland lakes. Although the newts did use crustaceans as a

major food resource, their predation pressure seems not to be sufficient to eliminate these

populations. Daily food consumption of Alpine newts is less than that of fish of

comparable body weight due to lower gastric evacuation rates in newts (SCHABETSBERGER,

1994; SCHABETSBERGER & JERSABEK, in press). Further, the newts are restricted to feeding

near the sediment and adults exploit the habitat only during the summer months. Newt

larvae also use these crustaceans as prey (SCHABETSBERGER, 1993). The larvae often die

under the long ice cover of Alpine water bodies (BRAND & GROSSENBACHER, 1979). If they

can survive, low temperatures cause low gastric evacuation rates and a smaller impact on

prey communities compared to teleost fishes (SCHABETSBERGER, 1994).

On the other hand, minnows seemed to have eliminated one of their own food

resources. All size classes are facultative zooplanktivorous predators (LAZZARO, 1987).

There is no plausible explanation for the total absence of big crustaceans in the

zooplankton community of Lake 1 other than that of extinction due to predation by fish.

Most likely the minnows were introduced into Lake 1 long ago, either for cooking

purposes (FROST, 1943), or as bait-fish for salmonids. The Alpine pasture near the lakes

have been used for cattle farming for hundreds of years. Minnows were found to survive

in lakes where oxygen depletion in winter prevents survival of salmonids. Since the outflow

of Lake 1 falls over several cascades, a colonization by anadromous fish is impossible. In

other respects, a passive transport of fish eggs in the plumage of water fowl is extremely

unlikely.

Total population size of minnows is usually bigger than that of Alpine newts, because

the fish have higher fecundity when the lake is suitable for reproduction. Often salmonid

fish are introduced in large numbers and compete for the scarce resources in the

oligotrophic Alpine lakes. The population size of Alpine newts in high altitude lakes seems

to be limited by factors such as high mortality rates during metamorphosis and migration

(SCHABETSBERGER & GOLDSCHMID, 1994).

Fish stocking in Alpine lakes causes irreversible changes in zooplankton communities,

because the prey species are not adapted to actively foraging fish. Beside these changes in

zooplankton, amphibian populations usually disappear shortly after fish introduction,

because predatory fish prey heavily on their eggs and larvae (GiAcoMA, 1989). In Austria,

the introduction of fish into fishless high altitude lakes dates back into the middle ages

(PECHLANER, 1966) and is today encouraged by some fishery biologists, as stocking has

become easier with the use of helicopters.

The native Arctic charr (Salvelinus alpinus salvelinus) has become an endangered

species in the Alpine lowland lakes of Austria due to mismanagement and the introduction

of North American salmonids as competitors (JAGSCH, 1987). Fishery biologists have

argued to introduce Arctic charr into fishless Alpine lakes for conservation of a gene-pool

of this endemic subspecies in the Alps (STEINER, 1987). Often other North American charr

Source : MNHN, Paris

188 ALYTES 12 (4)

species or different charr hybrids are introduced instead of Arctic charr, as these fish are

more easily available from commercial hatcheries. Since the introduction of fish causes a

degradation of these ecosystems, we strongly recommend the protection of fish species by

better management in their natural habitats. Although many of these high altitude lakes

are situated in existing or planned national parks, Austrian fishery law still allows these

stocking activities. The introduction of alien North American charr as well as the

degradation of the natural amphibian and zooplankton communities conflicts with the

principles of a national park.

RÉSUMÉ

Les communautés zooplanctoniques de deux lacs karstiques alpins voisins l’un de

l’autre, similaires par leurs dimensions et leurs caractéristiques abiotiques, s'avèrent

différer beaucoup l’une de l’autre. Dans le premier des deux lacs, le triton alpestre (Triturus

alpestris) exploite les ressources nutritives pendant l'été, tandis que dans l’autre, un poisson

(le vairon européen, Phoxinus phoxinus) est le super-prédateur. La communauté zooplanc-

tonique du lac sans poissons se compose de quelques grandes espèces de crustacés, alors

que dans l’autre lac les rotifères dominent. Bien que la nourriture des tritons se compose

surtout de crustacés, leur pression prédatrice est moindre que celle des poissons. L’effectif

de la population des tritons adultes est au moins dix fois inférieur à celui des poissons

sexuellement mûrs (1570 tritons contre 17420 vairons).

ACKNOWLEDGEMENTS

We wish to thank the Austrian Ministry for the Environment, Youth and Family for funds and

facilities. Two anonymous referees and Günter GOLLMANN provided numerous constructive

comments that improved the manuscript.

LITERATURE CITED

BRAND, M. & GROSSENBACHER, K., 1979. — Untersuchungen zur Entwicklungsgeschwindigkeit der

Larven von Triturus a. alpestris (Laurenti 1768), Bufo b. bufo (Linnaeus 1758) und Rana t.

temporaria ( Linnaeus 1758) aus Populationen verschiedener Hôhenstufen in den schweizer Alpen.

Dissertation, Universität Bern: 1-260.

Brooks, J. L. & Dopson, S. [., 1965. — Predation, body size, and composition of plankton. Science,

150: 28-35.

Dopson, S. 1, 1970. — Complementary feeding niches sustained by size-selective predation. Limnol.

& Oceanog., 15: 131-137.

FRosT, W. E., 1943. — The natural history of the minnow, Phoxinus phoxinus. J. anim. Ecol., 12:

139-162.

Gracoma, C., 1988. — The ecology and distribution of newts in Italy. Annuar. Ist. Mus. Zool. Univ.

Napoli, 26: 49-84.

Source : MNHN, Paris

SCHABETSBERGER, JERSABEK & BROSEK 189

GuLATI, R. D., LAMMENS, E. H. R. R., MEuER, M.-L. & VAN Donk, E. (eds.), 1990. —

Biomanipulation — tool for water management. Proceedings of an international conference

held in Amsterdam, The Netherlands, 8-11 August, 1989. Developments in Hydrobiology,

Dordrecht, Kluwer Acad. Publishers, 61: 1-628. (Reprinted from Hydrobiologia 200/201).

HRBACEK, J., 1962. — Species composition and the amount of zooplankton in relation to the fish

stock. Rozpr. cesk. Akad. Ved. Rada. Mat. Prir., 72: 1-117.

JaGscH, A., 1987. — Arctic charr in some of the lakes of the eastern Alps (Austria). Proc. Fourth

ISACF Workshop on Arctic Charr, 1986, Sweden, Institute of Freshwater Research Drottning-

holm: 64-72.

JoLy, P. & Miaun, C., 1990. — Tattooing as an individual marking technique in urodeles. Alytes, 8:

11-16.

Kkess, C. J., 1989. — Ecological methodology. New York, Harper & Row Publishers: 1-652.

LazzaRo, X., 1987. — A review of planktivorous fishes: their evolution, feeding behaviours,

selectivities, and impacts. Hydrobiologia, 146: 97-167.

Miaun, C., 1990. — La dynamique des populations subdivisées: étude comparative chez trois amphibiens

urodèles (Triturus alpestris, T. helveticus er T. cristatus). Thèse de Doctorat, Univ. Claude

Bernard Lyon I: 1-205.

MORIN, P. J., 1987. — Salamander predation, prey facilitation, and seasonal succession in

microcrustacean communities. In: W. C. KERFOOT & A. SiH (eds.), Predation: direct and indirect

impacts on aquatic communities, Hanover, New Hampshire, Univ. Press of New England:

174-188.

Morin, P. J., WiLBuR, H. M. & HaRis, R. D., 1983. — Salamander predation and the structure of

experimental communities: responses of Notophthalmus and microcrustacea. Ecology, 64:

1430-1436.

PECHLANER, R., 1966. — Salmonideneinsätze in Hochgebirgsseen und -tümpel der Ostalpen. Verh.

internat. Verein. Limnol., 16: 1182-1191.

PINKAS, L., OLIPHANT, M. S. & IVERSON, I. L. K., 1971. — Food habits of albacore, bluefin tuna and

bonito in Californian waters. Calif. Fish Game, 152: 1-105.

SCHABETSBERGER, R., 1993. — Der Bergmolch (Triturus alpestris, Laurenti) als Endkonsument in

einem alpinen Karstsee (Dreibrüdersee, 1643 m, Totes Gebirge). Dissertation, Universität

Salzburg: 1-129.

--- 1994. — Gastric evacuation rates of adult and larval Alpine newts (Triturus alpestris) under

laboratory and field conditions. Freshwater Biol., 31: 143-151.

SCHABETSRERGER, R. & GOLDSCHMID, A., 1994. — Age structure and survival rate in Alpine newts

(Triturus alpestris) at high altitude. Alytes, 12: 41-47.

SCHABETSBERGER, R. & JERSABEK, C. D., in press. — Alpine newts (Triturus alpestris) as top predators

in a high altitude karst lake: daily food consumption and impact on the copepod

Arctodiaptomus alpinus. Freshwater Biol., in press.

Sreiner, V., 1987. — Die Hochgebirgsseen Tirols aus fischereilicher Sicht. Teil 1. Bestandsaufnahme

1980-1985. Innsbruck, Studie im Auftrag des Amtes der Tiroler Landesregierung: 1-213.

STROHMEIER, K. L. & CROWLEY, H., 1989. — Effects of red-spotted newts (Notophthalmus viridescens)

on the densities of invertebrates in a permanent, fish free pond: a one month enclosure

experiment. J. Freshwater Ecol., 5: 53-65.

TAYLOR, B. E., ESTES, R. A., PECHMANN, J. H. K. & SEMLITSCH, R. D., 1988. — Trophic relations in

a temporary pond: larval salamanders and their microinvertebrate prey. Can. J. Zool., 66:

2191-2198.

ZaRET, T. M., 1980. — Predation and freshwater communities. New Haven & London, Yale University

Press: 1-187.

Corresponding editor: Günter GOLLMANN.

Source : MNHN, Paris

Alytes, 1995, 12 (4): 190.

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Alytes, 1995, 12 (4): 191-192. 191

Neotropical frog Leptodactylus pentadactylus

eats scorpions

Wilson R. LOURENÇO * & Orlando CUELLAR **

* Université Pierre et Marie Curie, U.F.R. des Sciences de la Vie, 4 place Jussieu,

75252 Paris Cedex 05, France

** Department of Biology, University of Utah, Salt Lake City, Utah 84112, U.S.A.

Dietary examination of preserved frogs from Ecuador at the Genève

Museum revealed the presence of scorpions in four specimens of Leptodacty-

lus pentadactylus. This observation is of particular interest because it

represents the first known case of frog predation on scorpions in the New

World tropics.

Scorpion predators have been described in detail by PoLis et al. (1981) and

McCormick & PoLis (1990). They include approximately 150 taxa, the majority of which

are vertebrates. According to McCormick & PoLis (1990), vertebrate predators include

birds (37 %), lizards (34 %), mammals (18 %), frogs and toads (6 %) and snakes (5 %).

In their table of predators, PoLis et al. (1981) presented only seven species of anuran

amphibians: Bufo cognatus (Oklahoma, U.S.A.), B. compactilis (Oklahoma, U.S.A.), B.

melanostictus (Singapore), B. regularis (South Africa), B. terrestris americanus (Oklahoma,

U.S.A.), Pyxicephalus adspersus (South Africa) and Scaphiopus couchii (southwestern

USA).

In this note we identify a new amphibian predator of scorpions, the South American

frog Leptodactylus pentadactylus. This is the first known case of this frog preying on

scorpions, and the first one reported for South American species. During a review of the

scorpions of Ecuador at the Genève Museum (Switzerland), the remains of single

scorpions were found in the stomach contents of four adult specimens of the frog L.

pentadactylus. Although most of the bodies had been digested, taxonomic identification

was made possible by analyzing the more durable pedipalps and metasoma. In all four

cases, the scorpions were adult females of Tityus bastosi Lourenço, 1984 (Buthidae),

previously described from the Amazonian region of Ecuador. The frogs had been collected

in the region of San Pablo, Napo Province in Ecuador. This new documentation of

scorpion predation is of great interest because: (1) it represents the first known case of

Neotropical frog preying on scorpions in the Amazon region; (2) all four scorpion

specimens belonged to the same species; (3) all were found in the same predator species,

suggesting that this frog may feed extensively on scorpions, and specifically on Tityus

bastosi.

Source : MNHN, Paris

192 ALYTES 12 (4)

Tityus bastosi is a small scorpion ranging from 30 to 35 mm in length (LOURENÇO,

1992), whereas adult L. pentadactylus average about 85 mm in snout-vent length. When

disturbed T. bastosi displays a temporary lethargic behavior, which possibly may have

evolved in reponse to frog predation. Frogs typically feed on moving prey. If the first

attack is unsuccessful, freezing behavior would be highly advantageous, since the frog may

not easily distinguish the scorpion from its background. At least juvenile forms of several

other species of scorpions from this region, such as Tityus asthenes Pocock, T. silvestris

Pocock, T. jussarae Lourenço and T. gasci Lourenço (LOURENÇO, 1988), could also be prey

for L. pentadactylus. Because scorpions and frogs are predominantly nocturnal, most of

the predation probably occurs at night. Some tropical scorpions, such as Tityus serrulatus

from Brazil, are extremely venomous and pose an important sanitary problem due to their

lethal venom and habit of living in human communities (LOURENÇO & CUELLAR, 1994).

With the alarming decline of amphibian populations worldwide (BARINAGA, 1990;

PHizuips, 1990; Wake et al., 1991), scorpions may be losing some of their most effective

predators and effective means of population control. Urgent studies are needed to verify

the amount of frog predation on scorpions, and to assess the status of frog populations

in the neotropics.

ACKNOWLEDGEMENTS

We are grateful to Dr. V. MauNERT of the Natural History Museum of Genève for allowing us

to examine the material used in this study.

LITERATURE CITED

BARINAGA, M., 1990. — Where have all the frogies gone? Science, 247: 1033-1034.

LOURENÇO, W. R., 1988. — La faune des scorpions de l'Equateur. I. Les Buthidae. Systématique et

biogéographie. Rev. suisse Zool., 95 (3): 681-687.

Las 1992. — Biogéographie des espèces du groupe naturel “Titpus clathratus” (Chelicerata,

Scorpiones, Buthidae). Bull. Mus. nat. Hist. nat., (4), 14 (A2): 473-481.

LOURENGÇO, W. R. & CUELLAR, O., 1994. — Notes on the geography of parthenogenetic scorpions.

Biogeographica, 70 (1): 19-23.

MCCoRMICK, S. J. & PoLis, G. A., 1990. — Prey, predators, and parasites. /n: G. A. PoLis (ed.), The

biology of scorpions, Stanford, Stanford Univ. Press: 294-320.

Pizuips, K., 1990. — Where have all the frogs and toads gone? BioScience, 40: 422-424.

Pouis, G. A., Sissom, W. D. & MCCORMICK, S. J., 1981. — Predators of scorpions: field da

review. J. arid Envir., 4: 309-326.

Wake, D. B., MOROWITZ, H. J., BLAUSTEIN, A., BRADFORD, D., BURY, R. B., CALDWELL, J., CORN,

P.S., Dumois, A., HARTE, J., HAYES, M., INGER, R., NETTMANN, H. RAND, A. S., SMITH,

D., TvLer, M. & Vrrr, L., 1991. — Declining amphibian populations — a global phenomenon?

Findings and recommendations. Alytes, 9: 33-42.

and a

Corresponding editor: Ulrich SINSCH.

| BIBL. DU

| MUSÉUM

\| PARIS

\«

Source : MNHN, Paris

AINTTES

International Journal of Batrachology

published by ISSCA

EDITORIAL BOARD FOR 1994

Chief Editor: Alain Dusois (Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire

naturelle, 25 rue Cuvier, 75005 Paris, France).

Deputy Editor: Günter GOLLMANN (Institut für Zoologie, Universität Wien, AlthanstraBe 14, 1090

Wien, Austria).

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Italy); Alain COLLENOT (Paris, France); Tim HALLIDAY (Milton Keynes, United Kingdom);

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ix + 1-547, pl. I-IV.

GRAF, J.-D. & PoLLs PELAZ, M., 1989. - Evolutionary genetics of the Rana esculenta complex. In:

R. M. DAWLEY & J. P. BOGART (eds.), Evolution and ecology of unisexual vertebrates, Albany, The

New York State Museum: 289-302.

INGER, R. F., Voris, H. K. & Voris, H. H., 1974. - Genetic variation and population ecology of some

Southeast Asian frogs of the genera Bufo and Rana. Biochem. Genet., 12: 121-145

Manuscripts should be submitted in triplicate either to Alain Duois (address above) if dealing

with amphibian morphology, systematics, biogeography, evolution, genetics or developmental

biology, or to Günter GOLLMANN (address above) if dealing with amphibian population genetics,

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Acceptance for publication will be decided by the editors following review by at least two

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Published with the support of AALRAM

(Association des Amis du Laboratoire des Reptiles et Amphibiens

du Muséum National d'Histoire Naturelle, Paris, France).

Directeur de la Publication: Alain DuBois.

Numéro de Commission Paritaire: 64851.

Alytes, 1995, 12 (4): 145-192.

Contents

Richard J. WassERsUG & David B. WAKE

Fossil tadpoles from the Miocene of Turkey ....................... 145-157

Dinorah D. ECHEVERRIA

Microscopia electrénica de barrido del aparato bucal

y de la cavidad oral de la larva de Leptodactylus ocellatus

(Linnaeus, 1758) (Anura, Leptodactylidae) ......................... 159-168

Adriana $S. MANZANO & E. O. LAVILLA

Notas sobre la miologia apendicular de

Phyllomedusa hypocondrialis (Anura, Hylidae)...................... 169-174

Walter E. MESHAKA, Jr. & Stanley E. TRAUTH

Reproductive cycle of the Ozark zigzag salamander,

Plethodon dorsalis angusticlavius (Caudata, Plethodontidae),

in north central Arkansas. ................................,.... 175-182

Robert SCHABETSBERGER, Christian D. JERSABEK & Susanne BROZEK

The impact of Alpine newts (Triturus alpestris)

and minnows (Phoxinus phonixus) on the microcrustacean

communities of two high altitude karst lakes....................... 183-189

Wilson R. LOURENÇO & Orlando CUELLAR

Neotropical frog Leptodactylus pentadactylus eats scorpions ........ 191-192

Announcements

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Sciences, Pascal, Referativny Zhurnal and The Zoological Record.

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Dépôt légal: 1° trimestre 1995.

Source : MNHN, Paris