Volume 7 • 1997

tailor

Ermi Zhao

Chengdu Institute of Biology, Academia Sinica, Chengdu. Sichuan, China

Associate Editors

J. Robert Maeey Theodore J. Papenfuss

Department of Bioloev. Washington University. St. Louis. Museum of Vertebrate Zoology. University of California.

Missouri, USA Berkeley. California. USA

Managing Editor

Valeurie E. Friedman

Berkeley, California, USA

Editorial Board

kraig Adler

Cornell University, Ithaca, New York, USA

Natalia B. Ananjeva

Zoological Institute. St. Petersburg. Russia

Steven C. Anderson

University of the Pacific. Stockton, California, USA

Ki ll.ii Autumn

Museum of Vertebrate Zoology. Universitj of California,

Berkeley. USA

Aaron Bauer

Villanova University. Villanova. Pennsylvania. USA

Leo Borkin

Zoological Institute. St. Petersburg. Russia

Bihui Chen

Anhui Normal University. Wuhu, Annul. China

Ilya Darevsky

Zoological Institute. St. Petersburg. Russia

Indraneil Das

Centre for Herpetology. Madras Crocodile Bank. Post Bag No. 4,

Mamallapuram-603 104, Tamilnadu, S. India

William E. Duellman

University of Kansas. Lawrence, Kansas, USA

Hajime Fukada

Sennyuji Sannaicho. Higashiyamaku. Kyoto. Japan

Carl Gans

University of Michigan. Ann Arbor, Michigan. USA

Hui-qingGu

Hangzhou Teacher's College. Hangzhou. Zhejiang. China

Robert F. Inger

Field Museum. Chicago. Illinois. USA

M.ihiiicniil Latifi

Institut d'Etat des serums el vacuus Ra/i. Teheran. Iran

kuangyang Lue

National Taiwan Normal University, Taipei. Taiwan, China

Ronald Marlow

University of Nevada. Las Vegas. Nevada. USA

Robert W. Murphy

Royal Ontario Museum. Toronto. Ontario, Canada

Goren Nilson

University of Goteborg. Goteborg. Sweden

Nikolai Orlov

Zoological Institute, St. Petersburg. Russia

Hidetoshi Ota

Department of Biology, University of the Ryukyus. Okinawa.

Japan

Jiong-hua Pan

South China Normal University. Guangzhou. Guangdong. China

Yun-xu Tong

Lanzhou University. Lanzhou. Gansu. China

Yehudah Werner

Hebrew University. Jerusalem. Israel

ke-ming Xu

Liaoning Normal University. Dalian. Liaoning. China

Yu-hua Yang

Sichuan University. Chengdu. Sichuan. China

ken-tang Zhao

Suzhou Railway Teacher's College, Suzhou, Jiangsu. China

Asiatic Herpetologkal Research is published by the Asiatic Herpetological Research Society (AHRS) and the Chinese So-

ciety for the Study of Amphibians and Reptiles (CSSAR) at the Museum of Vertebrate Zoology. University of California.

The editors encourage authors from all countries to submit articles concerning but not limited to Asian herpetology. All cor-

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Asiatic Herpetological Research Volume 7 succeeds Volume 6 published in 1995. Volume 5 published in 1993. Volume 4

published in 199^ Volume 3 published in 1990 and Chinese Herpetological Research Volume 2. which was published at

the Museum of Vertebrate Zoology, 1988-1989 as the journal for the Chinese Society for the Study of Amphibians and Rep-

tiles Volume 2 succeeded Chinese Herpetological Research 1987. published for the Chengdu Institute of Biology by the

Chongqing Branch Scientific and Technological Literature Press, Chongqing, Sichuan. China. Acta Herpetologica Sinica

ceased publication in June, 1988.

Cover: Bungarus multicinctus. Tarn Dao, northemVietnam. Photo by Nikolai Orlov.

1997

Asiatic Herperological Research

Vol. 7, pp. 1-5

Anurans Collected in West Malaysia

TOMAS CEDHAGEN

Department of Ecology and Genetics, Institute of Biological Sciences, University of'Aarlius, N\ Munkegade,

Building 540, DK-Aarhus C, Denmark

Abstract. - Distributional records and natural history notes are given for anurans collected in West Malaysia

1976. Rana baramica was observed when it was caught by an Aliaetulla nasuta (Serpentes: Colubridae).

Rhacophorus leucomystax, Limnonectes limnocharis and Microhyla heymonsi were all found at night on

September 16-17, when they were spawning in shallow ditches, formed by the wheels of a truck. Amolops

larutensis were day active and occurred in the shadow, among stones in a forest stream, particularly close to

water falls and rapids. Several white foam nests with a diameter of 5-7 cm were deposited on the same stones just

above the water surface on August 27. Other species observed were Bufo melanostictus, Bufo asper,

Leptobrachium hasseltii, Kaloula pulchra, Limnonectes laticeps, Limnonectes macrodon, Rana erythraea, Rana

glandulosa, Rana nicobariensis, and Rhacophorus prominanus.

Key words: Amphibia, Anura, West Malaysia.

Figure 1 . West Malaysia: The collecting sites are

marked with a dot (•). Scale bar = 100 km.

Introduction

The amphibian fauna of peninsular Malaysia is cov-

ered by some books (Berry 1975; Boulenger 1912:

Smith 1930) and articles published thereafter (e.g.,

Arak 1984; Dring 1979: Kiew 1979; Inger 1980a, b;

Lim 1990). New species have been described in the

area during the last decades, e.g., Kalophrynus palma-

tissimus Kiew, 1984b, Rana malesiana Kiew, 1984c

and Rhacophorus tunkui Kiew, 1987. which indicates

that much more work still remains to be done. Most of

the existing publications deal with systematics. The

fauna is rich and contains many interesting species,

however, most of them are not studied in detail

according to aspects of their distribution, natural his-

tory and ecology.

The nature in Malaysia is now undergoing radical

and large-scale changes. Most of them are effects of

an increasing human population, industrialization,

changes of the vegetation over large areas, and the

massive use of biocides (Aiken and Leigh 1992: Cran-

brook 1988; Cubitt and Payne 1990; Yussof 1987).

These factors probably threaten the amphibians (Kiew

1984a) in similar ways as, e.g., the fish fauna (M.

Zakaria-Ismail 1994: Ng et al. 1994; Rosier 1988). An

increased field work is therefore motivated, so that the

degree of habitat destruction is documented and nec-

essary conservation measures can be done. This con-

tribution contains some notes on the geographical

distribution and natural history of several amphibians

collected in Malaysia 1976.

Material and Methods

Collecting sites are listed in Table 1 , and marked on

the map (Fig. 1 ). The positions were plotted from the

map of Malaysia, published by the Director of

National Mapping. Malaysia, 1976, series 1307, edi-

tion 5-PPNM, sheet 1. scale 1:760.000. The speci-

mens were preserved in formalin, identified by the use

of Berry (1975). verified by Dr. Lim Boo-Liat. and

deposited at Department of Medical Ecology. Institute

Vol. 7. p. 2

Asiatic Herpetological Research

1997

Table 1. Sampling stations.

Field Study Center. University of Malaysia. Ulu Gombak, Selangor

Biological Field Station, Kota Tinggi. Johore

Kuala Brang. Trengganu

Kuin. about 4 miles SW of Marang, Trengganu

Bukit Besar, Kuala Trengganu, Trengganu

Malacca Youth Hostel. 9 miles north of Malacca city

Portugese settlement. Malacca

Kuala Lumpur Youth Hostel. Jalan Ipoh. Kuala Lumpur, Selangor

101°45'E;3°17'N

103°50'E; 1°50'N

103°0rE;5°04'N

103o10'E;5°09'N

103°07'E;5o20'N

102°10'E;2°14'N

102°17'E;2o10'N

101°44'E;3o09'N

for Medical Research in Kuala Lumpur, Malaysia.

The nomenclature follows Frost (1986) and later

changes summarized by Duellman ( 1993).

Results

Bufo melanostictus Schneider, 1799

Malacca Youth Hostel, July 29, 1976 (3 specimens);

Portugese settlement, Malacca, July 29, 1976 (1 spec-

imen); Kuala Lumpur Youth Hostel, August 5, 1976 ( 1

specimen), and September 29, 1976 (4 specimens).

All specimens were found in urban areas or other

environments affected by human activities.

Bufo asper Gravenhorst, 1829

Kuala Brang. August 27. 1976 ( 1 adult specimen), and

August 28, 1976. (1 juvenile specimen); Field Study

Center of the University of Malaysia. Gombak, Sep-

tember 14, 1976 (1 juvenile specimen). Several other

adult specimens, except the collected one, were

observed in the day, sitting on rocks 2-3 m above a

small river. They were very shy and jumped into the

water when disturbed, but returned to their rocks,

within 10-30 minutes. The juvenile specimens were

collected on the ground at night.

Leptobrachium ftasse/f/Tschudi, 1838

Kuin. August 24, 1976 ( 1 specimen). It was found on

the ground close to a stream in a primary forest.

Kaloula pulchra Gray, 1831

Kuala Lumpur Youth Hostel. August 6, 1976. ( 1 spec-

imen).

Microhyla heymonsiWogt, 1911

Kuala Brang, August 26, 1976 (l specimen); Field

Study Center of the University of Malaysia, Gombak,

September 17, 1976 (6 specimens). The specimen

from Kuala Brang was jumping in the leaf litter of an

open secondary forest. The specimens from Gombak

were 3 pairs in amplexus found in shallow ditches

between 8.30 and 10.30 p.m.

Amolops larutensis (Boulenger, 1899)

Kuala Brang. August 27. 1976 (13 specimens). The

frogs were active in the day, jumping in the shadow

between the stones (Fig. 2) in a rapid stream particu-

larly close to waterfalls (Fig. 4), and disappeared in

the water when disturbed. Several white foam nests

with a diameter of 5-7 cm were found on the same

stones, just above the water level (Fig. 3).

Limnonectes laticeps (Boulenger, 1882)

Field Study Center of the University of Malaysia.

Gombak. September 17, 1976 (1 specimen). It was

found in the day. jumping in the leaf litter in a primary

forest not far from a stream.

Limnonectes limnocharis (Boie, 1835)

Portugese Settlement, Malacca, July 30. 1976 (5 spec-

imens); Kuin, August 23, 1976 (3 specimens); Kuala

Brang, August 25, 1976 ( 1 specimen) and August 28.

1976 (3 specimens); Bukit Besar. Kuala Trengganu.

September 27. 1976 (1 specimens); Field Study Cen-

ter of the University of Malaysia, Gombak. September

17, 1976 (8 specimens); Biological Field Station,

Kota Tinggi, September 20. 1976 ( 1 specimens). They

were all found in areas affected by human activities.

The 8 specimens from Gombak were males, actively

croaking in water filled ditches.

1997

Asiatic Herpetological Research

Vol. 7. p. 3

Figure 2. Amolops larutensis, Kuala Brang. Treng-

ganu. The day active frog jumped in the shadow

among the stones in a stream.

Figure 3. Egg mass of Amolops larutensis, Kuala

Brang, Trengganu

Figure 5. Rana

macrodon, dor-

sal view, Treng-

ganu, Kuin.

Figure 4. Habitat for Amolops larutensis. Kuala Brang,

Trengganu.

Figure 6. Rana macrodon. lateral view, the same indi-

I vidual as in Fig. 5

Vol. 7, p. 4

Asiatic Herpetological Research

1997

Limnonectes macrodon (Dumeril and Bibron,

1841)

Kuin. August 23. 1976 (2 specimens). They were

found at night, sitting on stones in a small stream in a

primary forest (Figs. 5-6).

Rana baramica Boettger, 1901

Kuin. August 24, 1976 (1 specimen). The specimen

was observed when it was caught by the colubrid

snake Ahaetulla nasuta (Lacepede, 1789). in a pri-

mary forest close to a stream.

Rana erythraea (Schlegel, 1837)

Bukit Besar, Kuala Trengganu. August 29. 1976 (1

specimen), and September 27, 1976 (1 specimen);

Biological Field Station, Kota Tinggi, September 20,

1976 (4 specimens). All specimens were found in the

dense vegetation in shallow lakes, some of them also

populated with fish.

Rana glandulosa Boulenger, 1882

Biological Field Station, Kota Tinggi. September 20.

1976 (2 specimens). They were found in a logged,

swampy area with a dense, secondary vegetation.

Rana nicobariensis (Stoliczka, 1870)

Biological Field Station. Kota Tinggi, September 20,

1976 (2 specimens). They were found croaking at

night, in a logged, swampy area with dense, second-

ary vegetation. They climbed up in the vegetation.

0.5- 1 m above the ground.

Rhacophorus leucomystax (Boie, 1829)

Field Study Center of the University of Malaysia,

Gombak. September 16, 1976 (29 specimens), and

September 17, 1976 (34 specimens); Biological Field

Station, Kota Tinggi. September 21. 1976 (3 speci-

mens), and September 22. 1976 (1 specimen). The

specimens from Gombak were found in small water-

filled pits or wheel tracks, or in the vegetation above

them. Several pairs were found in amplexus, and yel-

low foam nests with whitish eggs were found on the

water surface, or on the vegetation about 10 cm above

the surface (Fig. 7).

Rhacophorus prominanus Smith, 1924

Kuala Brang, August 27, 1976 (1 specimen). It was

found in primary forest, close to a little river.

Discussion

The identity of Limnonectes macrodon has been

uncertain (Kiew 1978). Kiew (1984c) described a

closely related species. Rana malesiana (now Lim-

nonectes malesianus according to Duellman 1993)

earlier confused with L. macrodon. The species found

by me is L. macrodon (Kiew 1984c; Frost 1985) (Fig.

5-6).

Some aspects on the reproduction in Amolops

larutensis are mentioned, seemingly for the first time,

since no information was found in the literature. The

reproduction in Microhyla heymonsi is studied by

Berry ( 1964) in Singapore and occurs during all times

of the year. Additional Information is given by Pope

( 1931 ). The reproductive pattern of Rhacophorus leu-

comystax varies within its large distributional area.

Berry (1964) and Flower (1899) note that they seem

to breed at almost all times of the year in Singapore

and Malaysia, but Zeller (1960) reported a synchro-

nous periodicity in the reproduction in Java, and

Kiyasetuo and Khare (1986) found it to have an

annual breeding cycle, with spawning in June, in

northeastern India. The reproduction has also been

reported by Yorke (1983), Arak (1984), Feng and

Narins(1991).

Acknowledgments

I would like to express my sincere thanks to Dr. Kiew

Bong-Heang and Dr. Lim Boo-Liat, Kuala Lumpur,

for valuable help and advice. I am also most grateful

to Mr. Mohammad Zaharan bin Razak, B.Sc, Kuala

Trengganu, for the time we spent together in the

nature. Professor Immanuel Vigeland invited me to

the Biological Field Station, Kota Tinggi. Mr. Ragnar

Cedhagen kindly lent me a camera and provided film.

Dr. Mats Olsson, Goteborg. critically commented on

an earlier version of this manuscript.

Literature Cited

Aiken, S. R. and C. H. Leigh. 1992. Vanishing Rain

Forests. The Ecological Transition in Malaysia. Clar-

endon Press, Oxford, 194 pp.

Arak, A. 1984. Sex and song in Malaysian frogs and

toads. Malayan Naturalist 38( 1 ):20-24.

Berry, P. Y. 1964. The breeding patterns of seven spe-

cies of Singapore Anura. Journal of Animal Ecology

33:227-243.

Berry, P. Y. 1975. The Amphibian fauna of Peninsular

Malaysia. Tropical Press. Kuala Lumpur, x + 130 pp.

Boulenger, G. A. 1912. A vertebrate fauna of the

Malay Peninsula from the Isthmus of Kra to Sin-

gapore including the adjacent islands. Reptilia and

Batrachia. Taylor and Francis, London. 294 pp.

1 997

Asiatic Herpetological Research

Vol. 7. p. 5

Cranbrook, Earl of. 1 988. Key environments. Malay-

sia. Pergamon Press, Oxford. 3 1 7 pp.

Cubitt. G. and J. Payne. 1990. Wild Malaysia. The

wildlife and scenery of Peninsular Malaysia, Sarawak

and Sabah. New Holland Ltd. London. 208 pp.

Dring. J. C. M. 1979. Amphibians and reptiles from

northern Trengganu. Malaysia, with descriptions of

two new geckos: Cnemaspis and Cyrtodactylus. Bul-

letin of the British Museum (Natural History) Zool-

ogy series 34(1): 18 1-241.

Duellman, W. E. 1993. Amphibian species of the

world: additions and corrections. The University of

Kansas Museum of Natural History. Special Publica-

tion No. 21. 372 pp.

Feng. A. S. and P. M. Narins. 1991. Unusual mating

behaviour of Malaysian treefrogs. Polypedates leu-

comystax. Naturwissenschaften 78(8):362-365.

Flower. S. S. 1899. Notes on a second collection of

reptiles made in the Malay Peninsula and Siam. Pro-

ceedings of the zoological Society, London: 600-696

+ 885-916.

Frost. D. E. (ed) 1985. Amphibian species of the

world. Allen Press, Inc. and The Association of Sys-

tematic Collections, Lawrence, Kansas. 732 pp.

Inger. R. F. 1980a. Densities of floor-dwelling frogs

and lizards in lowland forests of southeast Asia and

Central America. The American Naturalist

115(61:761-770.

Inger, R. F. 1980b. Relative abundance of frogs and

lizards in forests of southeast Asia. Biotropica

12(1): 14-22.

Kiew, B. H. 1978. The nomenclature and identity of

the Javanese fro,!,' Rana macrodon Dumeril and

Bibron. Malayan Nature Journal 3 1(4):2 19-229.

Kiew, B. H. 1979. A note on the frogs and toads of

Batu Caves. Malayan Nature Journal 33( 1 ):67-69.

Kiew, B. H. 1984a. Conservation status of the Malay-

sian fauna. III. Malayan Naturalist 37(4):6-10.

Kiew. B. H. 1984b. A new species of sticky frog

{Kalophrynus palmatissimus n. sp.) from Peninsular

Malaysia. Malayan Nature Journal 37(3): 145-152.

Kiew. B. H. 1984c. Rana malesiana, a new frog from

the Sunda Region. Malayan Nature Journal

37(31:153-161.

Kiew, B. H. 1987. An Annotated Checklist of the Her-

petofauna of Ulu Endau. Johore. Malaysia. Malayan

Nature Journal 41(2-3):413-423.

Kiyasetuo and M. K. Khare. 1986. Annual Breeding

Cycle and Development of Rhacophorus leucomystax

(Kuhl). Pp. 417-422. In Rocek, Z. (ed.) Studies in

Herpetology. Proceedings of the European Herpeto-

logical Meeting (3rd ordinary general meeting of the

Societas Europea Herpetologica) Prague 1985.

Lim, K. K. P. 1990. The amphibian fauna of Ulu

Kinchin. Pahang, Malaysia. Malayan Nature Journal

43(4 1:322-325.

M. Zakaria-ismail 1994. Zoogeography and biodiver-

sity of the freshwater fishes of Southeast Asia. Hydro-

biologia 285:41-48.

Ng, P. K. L., J. B. Tay and K. K. P. Lim 1994. Diver-

sity and conservation of blackwater fishes in Peninsu-

lar Malaysia, particularly in the North Selangor peat

swamp forest. Hydrobiologia 285:203-218.

Pope, C. H. 1931. Notes on the Amphibians From

Fukien, Hainan, and Other Parts of China. Bulletin of

the American Museum of Natural History 61(8):397-

611.

Rosier, H. J. 1988. Malaysia - noch das gelobte Land?

Die Aquarien- und Terrarien-Zeitschrift 41(5): 111-

112.

Smith. M. A. 1930. The Reptilia and Amphibia of the

Malay Peninsula. Bulletin of the Raffles Museum

(3): 1-149.

Yorke, C. D. 1983. Survival of Embryos and Larvae of

the Frog Polypedates leucomystax in Malaysia. Jour-

nal of Herpetology 17(3):235-241.

Yussof, S. 1987. Conservation in Malaysia. Gua Anak

Takun revisited. Malayan Naturalist 40(3-4): 12- 16.

Zeller, C. 1960. Das periodische Eierlegen des Klet-

terfrosches Rhacophorus leucomystax. Revue Suisse

de zoologie 67:303-308.

1997

Asiatic Herpetological Research

Vol. 7, pp. 6-18

A Catalogue of Non-Metrical Variations in Skull Bones of Vipera lebetina

(Reptilia, Viperidae)

Yuri A. Chikin

Institute of Zoology, Uzbek Academy of Sciences, A. Niyazov Street, I , Tashkent 700095, Uzbekistan.

Abstract.- This paper presents a description, codes, and figures of 16 variations of non-metrical characters of 122

skull bones of Vipera (Macrovipera) lebetina inhabiting Central Asia and the Caucasus. Statistical characteristics

of the number of teeth on the pterigoideum and dental bones for several populations of the three subspecies of the

levantine viper are provided.

Kev words: Reptilia, Ophidia, Viperidae. Vipera lebetina obtitsa, V I. turanica, V I. cernovi, Uzbekistan,

Turkmenistan, Caucasus, osteology, skull bones.

Introduction

Currently, the use of non-metrical variation in cranial

structures for the identification of differences and the

determination of whether an individual belongs to

some populational group, subspecies or larger taxon,

is widely used in zoological studies (Berri. 1975;

Yaletsky, 1978: Shubin and Sedokova, 1982; Larina

and Eremina. 1988: Zerova and Chikin. 1992). While

working on a catalogue of non-metrical variations of

the cranial traits of Vipera lebetina L.. 1758, I

attempted to identify the range of variability, system-

atize the data, and unify techniques for distinguishing,

describing, and coding traits and their variations.

Material and Methods

An osteological collection in the Institute of Zoology

of the Uzbek Academy of Sciences as well as some

skulls from Moscow State University were the basis

for this work. A total of 268 skulls of the Levantine

viper of different ages and sexes from various locali-

ties in both Central Asia and Azerbaistan were used.

These populations are attributed by modern taxono-

mists to the following subspecies:

1. Vipera (Macrovipera) lebetina obtusa Dwigubsky.

1832, 35 specimens;

2. V. (M.) I. turanica Chernov. 1940. 175 specimens;

3. V. (M.) I. cernovi Chikin and Szczerbak, 1992. 58

specimens.

The ordinal numbers of the subspecies correspond

to those in the fourth column of Tables 1 and 2 of this

catalogue and in the first column of Tables 3 and 4.

Variations of the characters were revealed and

illustrated while comparing the bones using the binoc-

ular MBI-9 at different magnifications and with a

magnifier. The characters are arranged in groups to be

presented in the tables: the characters of the bony ele-

ments in Table 1 as foramenal characters in Table 2.

Table 3 provides statistical characteristics, calculated

using standard techniques (Lakin. 1990). of the num-

bers of the teeth in the pterigoideum and dental bones

separately for males and females, and their total: the

total number of teeth is given in Table 4. The popula-

tions of V. (M.) I. turanica — one from the eastern and

western parts of the Nuratau Ridges (EN, WN) and

Turkestan (T), the Malguzar Ridge (M), and Gobdun-

tau (G) — are characterized in Tables 3 and 4.

Names of bones and bony elements are given as

described by Gurtovoy et al. (1978), Groombridge

(1980), Mbrkevitch and Tatarko (1983). and Szyndlar

( 1984). The names of the characters are coded by the

letter symbols (initial letters of their Latin names).

Results

The following non-metrical variations are described

in this catalogue: (Table 1 ) variability in the shape of

most cranial bones, (Table 2) foramenal characters,

(Table 3) the number of teeth (and whether a subspe-

cies shows variations in this or that trait), and (Table

4) some schematic drawings (Figs. 1-16), illustrating

the variations described.

Some of the variations may be considered as insig-

nificant anomalies (rare phenes). which characterize

only individual populations of a subspecies. However,

the variations are common, i.e.. found in each of the

subspecies, and are "normal" for a species, though

their occurrence is different in each populational

group. Naturally-occurring heterogeneity of bilateral

structures is not reflected in the catalogue except the

characters Mcp and Fpa on the parietal bone. These

1997

Asiatic Herpetological Research

Vol. 7.

combinations, assessed by means of the values of

fluctuating asymmetry and observed even on a single

(nonpaired) bone, are independent characteristics of

stable development and its description is not supposed

here.

It is noteworthy that separate variations (Mpa.

Mcp). expanding the range of variability, can be in

fact considered as the age characteristics and it is this

case that necessitates a study on transformations of

the characters in ontogeny.

This catalogue cannot be considered comprehen-

sive and should be treated as a scheme, which, when

used by researchers, will enable them to amplify it in

the following:

( 1 ) description of variability of the other bones;

(2) incorporation of new traits and variations; and

(3) identification of known traits and variations to

individuals in various populational and taxonomic

groupings, both living and fossil.

Discussion

This publication of the Catalogue is a slightly

extended variant of my previous work (Chikin, 1993),

which, due to its limited distribution, is inaccessible

to most scientists. I will be grateful to my readers for

their remarks and glad to have followers.

Acknowledgments

The author is indebted to Galina A. Zerova for discus-

sions resulting in this work. My thanks are extended

to Valentina F. Orlova and Evgeny Dunayev (Zoologi-

cal Museum of Moscow State University) for the

specimens from their collection. Dzhavkhar

Khodzhaev for translation of the manuscript and

Kraig Adler for reviewing it.

Appendix I

Figures 1-16

J^tpb

1^1 TM

Mpcod

Figure 1 . Basioccipital bone. A, B and C are the location of the characters; the numbers of

variations correspond to those in Tables 1 and 2.

Vol. 7, p. 8

Asiatic Hevpetological Research

1997

Fed

Fed

Mepm

Figure 2. Supraoccipital bone (dorsal view). Location of the characters and their variations.

Figure 3. Parietal bone. A,

B. and C are the variations

of the form of the parietal

crest and posterior mar-

gin. D, E, and F are the

foramina and notches or

the anterior edge of the

descending part of the

bone.

Figure 4. Postfrontal

bone, showing the surface

that joins with the parietal

bone.

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Asiatic Herpetological Research

Vol. 7. p. 9

•iHLIzJi

Figure 5. Basiparasphenoid bone.

Location of the characters: A - infe-

rior; D - superior views; B, C. E, F -

variations.

7] Mppn^

Mtpp

1a 1b 1c 2a

2b

3a 3b 3o 3d

Figure 6. Premaxillary bone:

A - inferior, B - lateral views.

Location of the characters

and (C. D) variations

observed.

Mnav 2

Figure 7. Nasal bone. Variations in the form

of the anterior edge.

Figure 8. Variations of the anterior margin

of the ectopterygoid (A, B); C- external lat-

eral prominence.

Vol. 7. p. 10

Asiatic Herpetological Research

1997

Moml 1

Figure 9. Maxillary bone. A - anterior, B

lateral, C - dorsal views.

Figure 10. Articular bone, a Proximal part

from the external lateral view.

Meos 1 ; Fsp 1

Meos 2 j Fsp 2

Figure 1 1 . Angular bone. Variations in the form of the

anterior margin and foramina.

Figure 1 2. Splenial bone. Variations of the noch or the

dorsal part and of the openings.

Figure 1 3. Dental bone. A - external lateral side; the

position of the notch margin of the articular bone and

mental foramen. B - the internal lateral side, where

Mekkel's groove begins to expand. C- variations in the

form of the mental foramen. 1 - 5 - numbers of the

teeth.

Figure 14. Prooticum (left bone). Variations

of the foramina at the external lateral side.

1997

Asiatic Herpetological Research

Vol. 7, p. 1 1

F:

2HS

Figure 15. Palatal bone. Variations of the foramina at

the dorsal part of the Internal lateral surface.

Figure 16. Squamosum bone. A variant with the fora-

men.

Appendix II

Tables 1-4

TABLE 1 . Form of the skull bones in the Levantine Viper.

Character

Description of variations

Code

Sub-

species

The main occipital bone — basioccip-

itale (Fig. 1)

Margo terminationis processus hasio-

ccipitalis (Mtpb)

Margo prominentiae condyli occito-

condilaris, pars dorsalis (Mpcod)

Margo sinus prominentiae condili

on iti h ondilaris ( Mspco)

Supraoccipital bone — exoccipitale

(Fig. 2)

Fades exoccipitalis, pars dorsalis

(Fed)

Coral -shaped

Saw-shaped

V-shaped

Projection in the middle

Truncated

Roundish

Margin of prominence sharply extending

above the bone

Margin of prominence gently extending

above the bone

Groove absent

Groove chink shaped

Groove oval

Groove irregular

Surface is smooth or slightly wavy

Mtpb 1

Surface with hollows

Fed 1

Fed 2

1:3

(Continued)

Vol. 7. p. 12

Asiatic Herpetological Research

1997

Character

Description of variations

Code

Sub-

species

Mai go exoccipitalis posterior, pars

media/is ( Mepm )

Parietal bone — parietale (Fig. 3)

Margo parietal is anterior (Mpa)

Margo crista parietalis (Mcp)

Margo parietalis posterior ( Mpp )

Postfrontal bone — postfrontale

(Fig. 4)

Sunn a articuli ossis postfrontale

(Suap)

Basiparasphenoid bone — basiparas-

phenoid (Fig. 5)

Margo cristae basiparasphenoidis

(Mcb)

Margo processus suborbitalis et areae

lateralis (Mpsal)

Surface with deep grooves

Margin salient

Margin concave

Margin straight

Margin straight

Margin slightly concave

Crest absent

Crest reaches the posterior margin of the

bone

Crest does not reach the posterior margin of

the bone

Left and right parts of the crest join at acute

angles

Parts of the crest join at right angles

Parts of the crest do not join

Margin roundish

Margin right-angled

Margin obtuse-angled

Suture starts at the projection in midpart

Crest long with rounded top

Suborbital appendix is big. in the form of a

semicircle projecting beyond the line and

the margin of the lateral surface passes near

the line in the form of a concave arc

Suborbital appendix is small, projecting

beyond the line in the form of a small sector

of a circle or obtuse angle, and the margin

of the lateral line parallel with the line or on

it

Suborbital appendix small, parasphenoid

and suborbital appendices project beyond

the line, as well as most of the lateral line

Suap 1

Mcb 1

Mpsal 1

Mpsal 2

Mpsal 3

1:2:3

1; 2; 3

1;2

(Continued)

[997

Asiatic Herpetological Research

Vol. 7. p. 13

Character

Description of variations

Margo et directio processus basipteri-

goidis (Mdpb)

Pesten canalis minimis (Pcv)

Premaxillary bone — premaxilla

(Fig. 6)

Margo terminations processus palati-

ms (Mtpp)

Magnitude processus palatinus et pro-

cessus nasalis (Mppn)

Nasal bone — nasale (Fig. 7)

Margo nasalis anterior, pars verticalis

(Mnav)

Ectoptervgoid bone — ectoptervgoid

(Fig. 8)

Margo ectopterigoidis anterior (Mea)

Prominentia lateralis exterior (Pie)

Maxillary bone — maxillare (Fig. 9)

Margo corpus maxillare. pars lateralis

( Mcml )

Appendix sharp and directed upward and lo

the side

Appendix sharp and directed downward,

forming outer margin of deep groove

Appendix obtuse (not manifested), the

groove is shallow or absent

(rest absent

Crest present

Edge straight

Edee with notch

Margin with projection

Margin with projection and groove

Downward-turning projection

Bone expanded with large shoulder-shaped

projection

Mnav 1 1:2:3

Mnav 2 1

Mcml 1

1:2:3

(Continued)

Vol. 7. p. 14

Asiatic Herpetological Research

1997

Character

Description of variations

Code

Sub-

species

Sinus el crista transversus dorm salts,

pars interior (Scti)

Articular bone — articulare (Fig. 10)

Gracilis evolutionis processes media-

ns et processus lateralis (Gpml )

Angular bone — angulare (Fig. 11)

Margo exiguus ossis angulares

(Meoa)

Splenial bone — spleniale (Fig. 12)

Margo emarginaturae ossis spleniale

(Meos)

Dental bone — dentate (Fig. 13)

Magiutudo relativa emarginaturae

ossis articulare. pars lateralis exterior

(Mrel)

Initialio apertionis fissurae Mekkelii

(IafM)

Opening rectangular; crest well developed Scti

The medial process is significantly larger; Gpml 1

the lateral process is small and smooth

Margin even (no projection observed) Meoa 1

Notch not restricted by the projections

Notch posteriorly restricted by the projec-

tion

Notch anteriorly restricted by the projec-

tions

Notch both anteriorly and posteriorly

restricted by the projections

Margin of notch reaches 7th tooth

Margin reaches 8th tooth

Margin reaches 9th tooth

Margin reaches 10th tooth

Margin reaches 1 1th tooth

Margin reaches 1 2th tooth

Fissure opens under 7th tooth

Fissure opens under 8th tooth

Fissure opens under 9th tooth

Mrel 1

1:2:3

I; 2; 3

2; 3

] 997

Asiatic Herpetological Research

Vol. 7. p. 15

TABLE 2. Foramenal traits of the skull bones in Levantine Viper.

Character

Description of \ariations

Code

Sub-

species

The main occipital bone-

basioccipitale (Fig. 1)

Foramen ossis basioccipitale, part

ventrale (Fbv)

Prooticum bone-prooticum (Fig. 14)

Foramen ossis prooticum, pars lateralis

(Fpl)

Parietal bone-parietale ( Fig. 3)

Foramens et emarginaturas ossis pari-

etale, pars anterior (Fpa)

Foramen not present

One foramen

Two foramina

Three foramina

Four foramina

One foramen

Two foramina

Three foramina

Four foramina

Two completely closed foramina

One of the foramina is not closed

Two open foramina, rupture in the wall

smaller than the diameter of the foramen

Fbv 1

Fbv 2

Fbv 3

Fbv 4

Fbv 5

Fpl 1

Fpa 1

Fpa 2

Fpa 3

Two open foramina, rupture in the wall larger Fpa 4

than or equal to the diameter of the foramen

Basiparasphenoid bone-basiparasphe-

noid (Fig. 5)

Foramen et sulculus processes trabecu-

laris (Fspt)

Foramen anterior canal is vidianis

(Facv)

Premaxillary bone-premavilla (Fig. 6)

Of equal size on both sides

Both foramen and sulcus missing

Foramen present

Sulcus present

Both a groove and sulcus present

One fossa

Fpa 5

Fspt 1

Fspt 2

Fspt 3

Fspt 4

Facv 1

External edge of foramen not closed (partition Facv 2

has sulcus, canal)

2; 3

1 : 2; 3

1:2

1

2

2; 3

1:2; 3

2

1:2:3

1

1:2

1:3

(Continued)

Vol. 7, p. 16

Asiatic Herpetological Research

1997

Character

Description of variations

Code

Sub-

species

Foramen ossispremaxilla. pars ventralis Foramen not present

(Fpv)

One foramen

Two foramina

Three foramina

Four foramina

Palatine bone-palatinum (Fig. 15)

Foramen ossis palatinum, pars lateralis

interior (Fpli)

Squamose bone squamosum (Fig. 16)

Foramen squamosum (Fsq)

Angular bone-angulare (Fig. 11)

Foramen annulare (Fa)

Splenial bone spleniale (Fig. 12)

Foramen spleniale (Fsp)

Dental bone-dentale (F'ig.13)

Foramen mentale (date, fornix Fm)

Situs foramen mentale (Sifm)

Foramen not present

One foramen

Two foramina

Three foramina

No foramen

One foramen

No foramen

One foramen

Two foramina

No foramen

One foramen

One foramen, oval

One half-moon-shaped foramen

Two oval foramina

One foramen under 5th tooth

One foramen under 6th tooth

One foramen under 7th tooth

One foramen under 8th tooth

Two foramina under 4th and 7th teeth

Two under 5th and 6th teeth

Two under 5th and 7th teeth

Fpv 1

Fpv 2

Fpv 3

Fpv 4

Fpv 5

Fpli 1

2; 3

2: 3

2: 3

I; 2

1997

Asiatic Herpetological Research

Vol. 7, p. 17

Character

Description of variations

Code

Sub-

species

Two under 6th and 7th teeth

Two under 6th and 8th teeth

Two under 7th and Xth teeth

Sifm 8

Sifm 9

Sifm 10

2

2

2:1

The bones of the snakes of unknown sex were added: x - mean; Sx - Standard error; CV - coefficient of variation

Vol. 7, p. 18

Asiatic Herpetological Research

1997

TABLE 4. Total tooth number on the skull in the Levantine Viper.

Literature Cited

Berri, R. J. 1975. Islands and the evolution of Micro-

tias arvalis (Microtinae). Journal of Zoology. 177:

395-409.

Chikin, Y. A. and N. N. Szczerbak. 1992. [Vipera leb-

etina cernov ssp. n. (Reptilia. Viperidae), a new sub-

species from Central Asia]. Vestnik Zoology 6: 45-49

(In Russian).

Chikin, Y. A. 1993. [Catalogue of non-metrical varia-

tions of the skull bones of Levantine viper], p. 104-

120. In: Zoological Research, Vol. 1, University Press.

Tashkent (In Russian).

Groombridge, B. 1980. A Phyletic Analysis of Vipera

Snakes. Unpublished Ph.D. thesis. C.N.A.A., London.

249 pp.

Gurtovoi, N. N.. B. S. Matveev, and F. Ya. Dzerzhin-

sky. 1978. [Practical zootomy of vertebrates: amphibi-

ans, reptiles. A reference book for the university

specialists in biology]. Higher School Publishers,

Moscow. 407 pp. (In Russian).

Lakin, G. F. 1990. [Biometria]. Higher School Pub-

lishers, Moscow. 352 pp. (In Russian).

Larina, N. I., and I. V. Eremina. 1988. [Catalogue of

the main variations of cranial characters in rodents], p.

8-52. In: The Phenetics of Natural Populations.

Nauka. Moscow (In Russian).

Markevich A. P., and K. I. Tatarko. 1983. [Russian-

Ukranian-Latin Dictionary of Zoology]. Naukova

Dumka Publishing House, Kiev. 412 pp. (In Russian).

Shubin. N. G.. and M. L. Sedokova. 1982. [Epigenetic

polymorphism of the skull of Talpa altaica], p.269-

276. In: Phenetics of Populations. Nauka, Moscow.

(In Russian).

Szyndlar, Z. 1984. Fossil snakes from Poland. Acta

Zoologica Cracovensia. 28: 3-156.

Valetsky, A. V. 1978. [Non-metrical variations in the

skull texture in some Pinnipedia], p. 89-92. In: Physi-

ological and Populational Ecology of Animals. Sara-

tov University Press, Saratov. (In Russian).

Zerova. G. A., and Yu. A. Chikin. 1992. Polymor-

phism of the structure of the separate skull-bones in

Vipera (Daboia) lebetina, p. 497-500. In: Korsos, Z.

and Kiss. I. (eds.). Proceedings of the Sixth Ordinary

General Meeting Societas Europaea Herpetologica,

Budapest. 1991.

1997

Asiatic Herpetological Research

Vol. 7. pp. 19-22

A New Gecko of the Genus Gonydactylus (Sauria: Gekkonidae) with a Key to

the Species from Vietnam

ILYA S. DAREVSKY1 AND NIKOLAI N. SZCZERBAK2

Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034. Russia; 'Institute of Zoology

Ukranian Academy of Sciences, Kiev 252650, Ukraine

Abstract: Gonydactylus paradoxus sp. nov from a small off-shore island in South Vietnam distinctly differs from

all other known species of the genus Gonydactylus in the absence of preanal and femoral pores in males and

females. The occurrence in a new insular species of a feature so unusual for the genus Gonydactylus may be an

external manifestation of founder effect sensu E. Mayr ( 1942).

Key words: Lizards. Gekkonidae. Gonydactylus, femoral pores

Figure 1 . Lateral view of head (a) and preanal and

femoral areas (b) of a holotype of Gonydactylus para-

doxus sp. nov. Note the rows of enlarged preanal and

femoral scales.

Introduction

The validity of the genus Gonydactylus Kuhl et van

Hasselt. 1822. originally described at the beginning of

the last century and long regarded as a synonym of the

genus Cyrtodactylus Gray. 1827, has recently been

advocated by Kluge (1991). According to the latter

author and current literature Gonydactylus comprises

62 species widely distributed within the South and

South-Eastern Asia. Some of them have been only

recently described from the Borneo (Hikida. 1990)

and from Thailand (Ulber. 1993).

a b

Figure 2. Lower surface of the right manus (a) and

right pes (b) of a holotype of Gonydactylus paradoxus

sp. nov.

Among the most important diagnostic characters

in the genus are the pattern of disposition and number

of femoral and preanal pores, which are present in

specimens of all known species of Gonydactylus.

Some years ago on a small offshore island of South

Vietnam the first author collected a series of speci-

mens of a species of Gonydactylus totally devoid of

both femoral and preanal pores. A more detailed

examination has shown that these lizards constitute a

rare new species of the genus Gonydactylus. A

description of this form is provided below.

The following acronyms and abbreviations are

used: ZIL - Zoological Institute. Russian Academy of

Sciences. St. Petersburg; ZMK - Zoological Museum.

Ukranian Academy of Sciences, Kiev; SVL - snout-

vent length; TL - tail length.

Gonydactylus paradoxus sp. nov. (Figures 1-

3)

Holotype: ZIL 203 K), Hon Thorn Isle near south

point of Phu Quoc Island. Kieng Giang Province.

Vol. 7. p. 20

Asiatic Herpetological Research

1997

Figure 3. Dorsal coloration variability in six paratype specimens of Gonydactylus paradoxus sp. nov.

South Vietnam, coll. I. Darevsky, April 13, 1987. adult

male.

Paratypes: Z1L 20311-20315. 204-21. 20422,

20479-20481: ZMK Re 22. 23a (7 males. 6 females).

Same data as for holotype.

Etymology: The species name derives from the

Greek word "paradoxes" - unusual, strange: in the

present case referring to the lack of femoral and prea-

nal pores.

Diagnosis: A medium-sized species of Gonydactylus

with an adult body size of 45-84 mm in SVL: no prea-

nal groove, no preanal and femoral pores in males or

females; enlarged femoral scales distinct: 26-36 mid-

ventral scale rows between indistinct lateral folds; 17-

23 subdigital lamellae under fourth toe; a median

series of transversely widened subcaudal scales; irreg-

ular crossbands on the dorsum.

Description of the holotype: Adult male. 80 mm

SVL; 95 mm TL; head oviform; forehead concave;

snout obtusely pointed; ear opening oval; eye with

vertical Gekko-type pupil; rostral large, quadrangular,

partially split by a median vertical cleft, contacting

nostrils, first upper labials and three enlarged interna-

sals; first upper labial, two postnasals, supranasal and

rostral forming border of nostril; scales on snout three

or more times larger than on occiput or interorbital

area; approximately 44 granules between palpebral

borders of eyelids at the middle of the orbits; granules

on the back of the head intermixed with few small

conical scales; 10/9 supralabials; mental triangular

with labial border wider than labial border of rostral;

9/9 lower labials; one large pair of postmental about

1/2 the size of the first; four gular scales bordering

first postmentals between second postmentals fol-

lowed by small gular granules. Dorsal surface of the

body with fine scales mixed with about 16 irregular

rows of small rounded conical or trihedral tubercles;

small tubercles developed on dorsal part of legs; vent-

rolateral folds feebly indicated by low rounded tuber-

cles; ventral scales small, cycloid, equal in size; about

30 scalerows between ventrolateral folds; approxi-

mately 135 scales in a row from chin shields to vent at

medial ventral line; one row of enlarged smooth fem-

oral scales on underside of thighs; no femoral and pre-

anal pores; tail round in cross-section, verticilate,

covered dorsally and laterally with small granules,

with 4-6 low tubercles near posterior part of each seg-

ment; a median series of transversely widened sub-

caudals.

Color (in life): Head and body yellow-brown above,

lighter below; back with seven brown-bordered light

undulating transverse bands, divided by a narrow Ion-

1997

Asiatic Herpetological Research

Vol. 7, p. 21

Figure 4. Type locality (Indicated by arrow) of Gony-

dactylus paradoxus sp. nov. at Thorn Island, Kien

Giang Province. South Vietnam.

gitudinal vertebral stripe; tail with dark rings sepa-

rated by narrow light interspaces.

Variation: The paratype specimens resemble the

holotype in all major characters. SVL of seven

mature males 41.0-84.0 mm and 50.3-78.0 mm for

mature females; scale rows between ventrolateral

folds 30-34; scales in a row from chin shields to vent

188-144. Variations in dorsal coloration are shown in

Fig. 3.

Distribution: All specimens are known only from the

type locality on Hon Tom Island in South Vietnam

(Fig. 4). It can be assumed that this island species

also occurs one some of the neighboring small islands

in the Gulf of Siam.

Field notes: All specimens from the type series were

collected at night on dry rocks under the canopy of a

secondary dipterocarp forest. By day, however, no

geckos were detected at the same place.

Reproduction: Four females kept in terraria laid 2

eggs repeatedly. Following about 55 days of incuba-

tion, young geckos 45-47 mm in total length were

hatched. A peculiar coloration of the young involves

the presence of bright white transverse rings on the

tail, which are hardly noticed in the adults.

Comparative notes: The intrageneric systematics of

the genus Gonydactylus has been largely based on the

pattern of scuttelation of the preanal and femoral

areas. The presence of more or less well developed

preanal or femoral pores is characteristic of all of pre-

viously-described representatives of the genus, the

number and disposition of these pores significantly

varying in different species. The pores are commonly

present in males only, although these may occasion-

ally be distinguishable in females too. Some species

display both femoral and preanal pores, whereas oth-

ers possess either the former or the latter.

There are 15 species of Gonydactylus in Indoch-

ina, four of which are known from Vietnam. All of

them, with the exception of G. paradoxus exhibits the

presence of preanal pores. As mentioned above, this

new species has no pores at all. and thus differs from

other representatives of the genus. In this regard G.

paradoxus exhibits some similarity to some Thai

specimens of G. oldhami whose males have generally

1-4 preanal pores, but which may lack pores entirely

(Smith. 1935; Taylor, 1963; Ulber, 1993). However,

G. oldhami definitely differs from G. paradoxus in a

number of other characters, particularly in possessing

a non-segmented tail and characteristic white spots on

the back. Among other Indochinese species, the new

species, according to its coloration and some other

markers, seems to be somewhat close to G. annularis

Smith from south Thailand, but differs from it in some

characters, in particular in a larger number (40-48) of

ventral scale rows between a ventrolateral folds (ver-

sus 30-34 in G. paradoxus). On the basis of the

majority of its characters the newly described species

obviously also differs from G. condorensis (Smith,

1921). a Vietnamese endemic insular species from

Pulo Condore (Con Dao) Island in the South China

Sea. Literature records (Bobrov. 1995) citing G. phil-

ippinicus from Vietnam are not confirmed by voucher

material and seem to be erroneous.

As is generally known, insular animals, in particu-

lar some reptile species, often display unusual mor-

phological characters (Mertens, 1934), which may be

regarded as a manifestation of the so called "founder

effect", originally formulated by E. Mayr (1942).

This principle attributes genetic uniformity and phe-

notypic specificy of specimens within an isolated pop-

ulation to an origin from a small founding population,

perhaps a single fertilized female, which might pos-

sess certain features not characteristic of the species.

It is assumed that the insular population of Gonydac-

tylus on Hon Thorn may have originated from an acci-

Vol. 7, p. 22

Asiatic Herpetological Research

1997

dentally introduced female having some genes

controlling the formation in ontogeny of femoral or

preanal pores (Darevsky et al., 1991 ).

Key to the species of Gonydactylus in Viet-

nam

1 (6) Underside of tail with transversely enlarged

plates.

2(3) Body handed with four distinct dark light-edged

dorsal cross-bars G. intermedins Smith.

3 (2) Body without distinct banded pattern.

4 (5) Males with a group of 4 to 7 preanal pores; 35-

40 scales across the belly G. condorensis Smith.

5 (4) Males and females without preanal pores: 30-34

scales across the belly G. paradoxus sp. nov.

6(1) Underside of tail with numerous roundish scales

G. irregularis Smith.

Acknowledgments

We are grateful to the participants of the Soviet-Viet-

namese expedition within Project No. 7 of the

UNESCO ("Ecology and rational exploration of island

ecosystems") for help during field work on Vietnam-

ese offshore islands.

Literature Cited

Bobrov, V V. 1995. Checklist and bibliography of

the lizards of Vietnam. Smithsonian Herpetological

Information Service. No. 105:1-28.

Darevsky, I. S. 1990. Notes on the reptiles (Squa-

mata) of some offshore island along the coast of Viet-

nam. Pp. 125-129 In: Peters G. and R. Hutterer (eds.).

Vertebrates in the Tropics. Proc. Int. Symp. Biogeog-

raphy and Systematics in the Tropics. Bonn.

Darevsky, I. S., A. G. Ponomarenko. and G. V

Kuznetzov. 1 99 1 . [Zoogeography of offshore island

of Vietnam]. Priroda, Moscow, 9:42-48. (In Rus-

sian).

Hikida. T 1990. Bornean Gekkonid Lizards of the

Genus Cyrtodactylus (Lacertilia: Gekkonidae) with

Description of Three New Species. Japanese Journal

of Herpetology 13:91-107.

Kluge, A. G. 1991. Checklist of Gekkonid Lizards.

Smithsonian Herpetological Information Service. No.

85:1-35.

Mayr. E. 1942. Systematics and the origin of species.

Columbia University Press, N.Y.

Martens. R. 1934. Die Insel-Reptilien. ihre Ausbere-

itung. Variation and Artbildung. Zoologica 32: 1 -209.

Smith. M .A. 1935. The Fauna of British India,

including Ceylon and Burma. Reptilia and Amphibia.

Vol. II. Sauria: 1-440.

Taylor. E. H. 1963. The Lizards of Thailand. Univer-

sity of Kansas Science Bulletin XLIV: 1-1077.

Ulber. T. 1993. Bemerkungen uber cyrtodactyline

Geckos aus Thailand nebst eshreibungen von zwei

neuen Arten (Reptilia: Gekkonidae). Mitt. Zool. Mus.

Berl. 69:187-200.

1997

Asiatic Herpetological Research

Vol. 7, pp. 23-26

Rediscovery of Lipinia macrotympanum (Stoliczka, 1873) from

the Nicobar Islands, India

INDRANEIL DAS

Centre for Herpetology, Madras Crocodile Bank, Post Ban No. 4, Mamallapuram-603 104, Tamilnadu, S. India

Abstract.- Stoliczka's (1873) Mocoa macrotympanum, known from the holotype collected over 120 years ago

from the Andaman Islands, India, is redescrihed on the basis of two specimens from Little and Great Nicobar

Islands. India. The species is diagnosed by: small body size (SVL up to 38.1 mm); tympanum exposed; disk on

lower eyelid translucent; prefrontals separate; the failure of the adpressed hind limbs to meet the fore limbs; 21-

23 smooth midbody scale rows; 15-17 subdigital scansors under toe IV; three pairs of nuchals; four supraoculars;

seven supralabials (supralabial V in midorbit position); six infralabials; and lateral bands starting from the

nostrils.

Key words.- Lipinia macrotympanum, Sauria. Scincidae. Great Nicobar. Little Nicobar, India.

Figure 1 . Lipinia macrotympanum (MCZ R-1 76760) from Pulo Ulan (07 03'N; 93 35'E), Little Nicobar, India,

in life.

Introduction

Mocoa macrotympanum was described by Stoliczka

( 1873), based on a single example from "South Anda-

man....on a sandy beach in Macpherson's Straits" (II"

31'N; 92- 39'E), which lie between South Andamans

and Rutland Island, that was deposited in the collec-

tion of the Asiatic Society of Bengal, in Calcutta. The

holotype is now in the collection of the Zoological

Survey of India (ZSI 5571). No further examples of

this distinctive species have come to light. In Mittle-

man's (1952) synopsis of scincids, the species was

assigned to the genus Scincella, although Greer

(1974) subsequently placed Stoliczka's species in the

genus Lipinia. now known to include 20 nominal spe-

cies (Austin, 1995; Greer. 1974; Greer and Mys,

1987) that are diagnosable by their small (SVL 56

mm) size, generally slender body, lack of a postorbital

bone and a dorsal color pattern of striking light, and

dark longitudinal stripes. Their distribution includes

the insular regions of south-east Asia, including the

Sundas east to the Philippines, New Guinea, with one

species (L. noctua) reaching Polynesia, further east

(see Fig. 45 in Greer, 1974. and Fig. 8 in Zweifel.

1979) that is suspected to be spread through human

agencies (Greer. 1989). Only one species (L. vittig-

era) has been recorded from the Asian mainland

(Greer, 1974).

The collection of an example (Fig. 1) of Lipinia

macrotympanum during field work conducted in the

Nicobars in 1994 and an examination of another

Nicobarese specimen (from Great Nicobar), referred

to Sphenomorphus quadrivittatum, although with

some hesitation, by Biswas and Sanyal (1977). pro-

vide an opportunity to both enlarge the description of

Vol. 7, p. 24

Asiatic Herpetological Research

1997

the species based on the two Nicobarese specimens

and announce its rediscovery after over 120 years.

Material and Methods

The material from Little Nicobar was fixed in 10%

formalin for two weeks, soaked in distilled water to

remove the formalin for a day and finally preserved in

70% ethanol. The following measurements were taken

13-14 months (for the material from Little Nicobar)

and 29 years (the material from Great Nicobars) after

collection, with dial vernier caliper (to the nearest 0.1

mm): snout-vent length (SVL; from the tip of the

snout to the vent), tail length (TL; from the vent to the

tip of the unregenerated tail), tail width (TW; mea-

sured at the base of the tail); head length (HL; the dis-

tance between the angle of the jaws and the snout-tip),

head width (HW: measured at the angle of the jaws),

head depth (HD; the maximum height of the head,

from the forehead to the throat), tympanum diameter

(TYD; the greatest [vertical] diameter of the tympa-

num), body width (BW; the greatest width of the

body), axilla to groin length (A-G; the distance

between the posterior edge of the fore limb and the

anterior edge of the hind limb), eye diameter (ED; the

greatest diameter of the orbit), eye to nostril distance

(E-N; the distance between the anterior-most point of

the eyes and the nostrils), eye to snout distance (E-S;

the distance between the anterior-most point of the

eyes and the tip of the snout), eye to ear distance (E-E;

the distance from the anterior edge of the ear opening

to the posterior corner of the eyes), greatest ear length

(EL; the greatest diameter of the ear opening), inter-

narial distance (IN; the distance between the upper

eyelids), fore limb length (FOL; the length of the out-

stretched fore limb, from axilla to the tip of its longest

finger), and hind limb length (HIL; the length of the

outstretched hind limbs, from vent to the tip of its

longest toe).

Institutional abbreviations follow Leviton et al.

(1985). Color nomenclature is that suggested by

Smith ( 1974; 1981 ) and taken from Kodak Gold film.

Nomenclature of dorsal striping is after Storr et al.

(1981).

Lipinia macrotympanum (Stoliczka, 1873)

Material examined: MCZ R- 176760. Pulo Ulan (07

03-N; 93 35'E), Little Nicobar, India. Coll. Indraneil

Das and Satish Bhaskar. 31 March. 1994: ZSI 22508,

Campbell Bay (06 50'N; 93 50-E). Great Nicobar,

India. Coll. A. Daniel, Great Nicobar Expedition.

1966.

Diagnosis.- A member of the genus Lipinia (fide

Greer, 1974), differentiable from congeneric species

in possessing the following suite of characteristics:

small body size (SVL up to 38.1 mm); tympanum

exposed; disk on lower eyelid translucent; prefrontals

separate; failure of the adpressed hind limbs to meet

the fore limbs; 21-23 smooth midbody scale rows; 15-

17 subdigital scansors under toe IV; three pairs of

nuchals: four supraoculars; seven supralabials

(supralabial V in midorbit position); six infralabials;

and lateral bands starting from the nostrils.

Redescription.- In general form, a supple skink, the

body elongated with fairly well-developed limbs.

Head relatively small (HL/SVL ratios 0.15 and 0.16),

snout acute, the sides converging to a distinctly

rounded tip; head relatively more slender than the

body, with a distinct neck, and longer than wide; head

and body slightly depressed dorso-ventrally; tail long

(TL/SVL ratios 1.20 and 1.41 ), rounded in cross sec-

tion and tapering to a sharp point.

Rostral enlarged and visible dorsally. broader than

high, forming a straight suture with frontonasal;

supranasals absent; postnasals contact supralabial II;

two loreals contact supralabials II and III; two preocu-

lars, smaller (preocular I) in contact with supralabial

IV; supralabials seven; infralabials eight; presubocu-

lar in contact with both supralabials IV and V;

supralabial IV in midorbital position; last supralabials

horizontally split: frontonasal broader than long,

broadly in contact with the rostral anteriorly and with

the prefrontals posteriorly; prefrontals not in contact

with each other; supraoculars four; frontal long,

spear-shaped, in contact with supraoculars I and II:

fused fronto-parietals; interparietal triangular, with

apex partially dividing parietals. and covering a rela-

tively large and distinct parietal eye; supracilliaries

10; two pre-temporals; two primary temporals; two

secondary temporals; three pairs of smooth nuchals;

mental wider than long, in contact with infralabials I

and II: postmental longer than wide, in contact with

infralabials II and III; three pairs of chin shields fol-

low the postmental on each side, the first pair in con-

tact with each other, the second pair divided medially

by the a single row of ventral scale, and the third pair

separated by three rows of ventral scales; tympanum

exposed, longer vertically, its greatest length more

than half eye diameter (ED/EL ratios 1.30 and 1.64),

shallow, lacking lobules.

Body slender (BW/SVL ratios 0.12 and 0.13); fore

and hind limbs well developed (FOL/SVL and HIL/

SVL ratios 0.22 and 0.23, and 0.32 and 0.33, respec-

tively), adpressed hind limbs fail to touch fore limbs.

Dorsally, the scales on body, limbs and tail are

smooth; ventrally, scales imbricate with three to four

very fine striations; midbody scale rows 21 and 23;

1997

Asiatic Herpetological Research

Vol. 7, p. 25

Table 1 . Meristic data (in mm) on the two Nicobarese specimens of

Lipinia macrotympanum

ventral scale rows (postmental to anal) 62; preanals

not enlarged; tripartite, the inner scales overlapping

the outer; ventrally, tail scales smooth, with imbricate

scales, the median series not being enlarged; scales on

palms and soles flattened and rounded. Subdigital

lamellae (MCZ R-176760) are as follows: (right fore

limb) finger I; 5; finger II: 9; finger III: 1 1; finger IV:

1 1; finger V: 7; (right hind limb) toe I: 7; toe II: 12;

toe III: 13; toe IV: 16; toe V: 11. transversely

enlarged, pad-like.

Measurements (in mm) of the two Nicobarese

specimens are in Table 1 . Subdigital formulae: 4 > 3 >

2 > 5 > 1 (manus); 4>3>2>5>1 (pes).

Color.- Vertebral stripe trogon yellow; paravertebral

stripes blackish neutral gray; dorsals trogon yellow;

dorsolateral stripes blackish neutral gray; snout cinna-

mon; ventrally. the body is an unpatterned cream; tail

beyond cloaca burnt orange both dorsally and ven-

trally: upper surfaces of limbs Pratt's rufous; under-

surface of manus and pes gray-brown (in

preservative).

Ecological notes.- Of the specimen from Great Nico-

bars, no field data are on record. Stoliczka's type was

taken from a beach, as was MCZ R-176760, which

was found moving with great agility over sand, into

which it made no attempts to burrow. Anecdotal notes,

and in certain cases, more detailed observations on

most of its congeners suggest however that members

of the genus Lipinia are largely arboreal (e.g.. Brown

and Fehlmann, 1958. for L. leptosoma; Loveridge.

1948:360, for L. miotis; Brown and Alcala. 1980:95-

96, for L. pulchella. Brown and Alcala, 1980:87. for

L. quadrivittata, Greer and Mys, 1987, for L. rouxi;

Brown and Alcala, 1980:100, for L. semperi. Brown

and Alcala, 1980:89, for L. subvittata Smith. 1930:36;

1935:307, forL. vittigera), although L. noctua, which

is arboreal elsewhere (Greer and Mys, 1987; Lover-

idge. 1948:358). is substrate dwelling on some of the

Vol. 7, p. 26

Asiatic Herpetological Research

1997

islands of Fiji (Zug, 1991) and Hawaii (Oliver and

Shaw. 1953; McMorris, 1970). The holotype of

Lipinia macrotympanum contained two eggs (Smith.

1935).

Variation.- The differences between the holotype and

hitherto only known specimen, as given by Stoliczka

( 1 873 ) and the fresh material from the Nicobars are

understandable, given the distance between the two

island groups. The holotype showed 15 lamellae

under the fourth toe (as opposed to 16 and 17) and 22

midbody scale rows (vs 21 and 22 in the Nicobarese

material). In addition, the color notes taken by Stolic-

zka (1873) indicate that the ventral surface of his

specimen (a gravid female) was livid carneous tinged

with orange, while the Nicobarese specimens have an

unpatterned cream belly.

Acknowledgments

Supported by the Royal Netherlands Embassy, Centre

for Herpetology, Madras Crocodile Bank Trust. Brit-

ish Council and a Fulbright Fellowship. I thank

Romulus Whitaker for support and Satish Bhaskar for

assistance during Held work in the Nicobars. For per-

mission and facilities to examine comparative mate-

rial, I thank E. N. Arnold and Colin J. McCarthy

(BMNH). John Cadle and Jose Rosado (MCZ). and

Shyamal Kumar Chanda and B. Dattagupta (ZSI).

Kraig Adler and Allen Greer offered comments on a

draft of the manuscript.

Literature Cited

Austin. C. C. 1995. Molecular and morphological

evolution in South Pacific scincid lizards: morpholog-

ical conservatism and phylogenetic relationships of

Papuan Lipinia (Scincidae). Herpetologica 51:291-

300.

Biswas, S. and D. P. Sanyal. 1977. Notes on the Rep-

tilia collection from the Great Nicobar Island during

the Great Nicobar Expedition in 1966. Records of the

Zoological Survey of India 72:107-124.

Brown. W. C. and A. C. Alcala. 1980. Philippine liz-

ards of the family Scincidae. Silliman University,

Dumaguete City, xi + 264 pp.

Brown, W. C. and A. Fehlmann. 1958. A new genus

and species of aboreal scincid lizards from the Palau

Islands. Occasional Papers of the Natural History

Museum, Stanford University (6): 1-7.

Greer. A. E. 1974. The generic relationships of the

scincid lizard genus Leiolopisma and its relatives.

Australian Journal of Zoology (Supplement Series)

31:1-67.

Greer. A. E. 1989. The biology and evolution of Aus-

tralian lizards. Surrey Beatty and Sons Pty Limited.

Chipping Norton, xvi + 264 pp.

Greer. A. E. and B. Mys. 1987. Resurrection of

Lipinia rouxi (Hediger. 1934)(Reptilia: Lacertilia:

Scincidae). another skink to have lost the left oviduct.

Amphibia-Reptilia 8:417-418.

Leviton, A. E.. R. H. Gibbs. Jr.. E. Heal and C. E.

Dawson. 1985. Standards in herpetology and ichthy-

ology: Part I. Standard symbolic codes for institu-

tional resource collections in herpetology and

ichthyology. Copeia 1985: 802-832.

Loveridge, A. 1948. New Guinea reptiles and amphib-

ians in the Museum of Comparative Zoology and

United States National Museum. Bulletin of the

Museum of Comparative Zoology 101:305-383 + 2

pi.

McMorris. J. R. 1970. Herpetological distribution and

life history notes for Hawaii and western North Amer-

ica. Great Basin Naturalist 30: 106-107.

Mittleman. M. B. 1952. A generic synopsis of the liz-

ards of the subfamily Lygosominae. Smithsonian Mis-

cellaneous Collections 1 17 (17): 1-35.

Oliver. J. A. and C. E. Shaw. 1953. The amphibians

and reptiles of the Hawaiian islands. Zoologica 38:

65-95.

Smith. F. B. 1974. Naturalist's color guide. Parts I and

II. The American Museum of Natural History. New

York.

Smith. F. B. 1981. Naturalist's color guide. Part III.

The American Museum of Natural History. New York.

Smith. M. A. 1930. The reptiles and Amphibia of the

Malay Peninsula. Bulletin of the Raffles Museum (3):

xviii+ 1-149.

Smith. M. A. 1935. The fauna of British India, includ-

ing Ceylon and Burma. Reptilia and Amphibia. Vol.

II- Sauria. Taylor and Francis. London, xiii + 440 pp +

lpl.

Stoliczka, F 1873. Notes on some Andamanese and

Nicobarese reptiles, with the descriptions of three new

species of lizards. Journal of the Asiatic Society of

Bengal 42(2): 162- 169.

Storr, G. M.. L. A. Smith and R. E. Johnstone. 1981.

Lizards of Western Australia. I. Skinks. Western Aus-

tralian Museum. Perth, xii + 200 pp.

Zug, G. R. 1991. The lizards of Fiji: Natural history

and systematics. Bishop Museum Bulletin in Zoology

(2): i-xii+ 1-136.

Zweifel. R. G. 1979. Variation in the scincid lizard

Lipinia noctua and notes on other Lipinia from the

New Guinea region. American Museum Novitates

(2676): 1-12.

1997

Asiatic Herpetological Research

Vol. 7, pp. 27-31

On the Distribution of Diploid and Tetraploid Green Toads of the Bufo Viridis

Complex (Anura; Bufonidae) in Southern Kazakhstan

Tatjaina Dujsebayeva1, Sergio Castellano2. Cristina Giacoma2, Emilio Balletto2,

AND GAETANO ODIERNA

3

Department of Biology, Kazakh State University. Timirjaseva Street, 46. Almaty, 480121 . Kazakhstan;

-Department of Animal Biology, University of Torino, \ ia Accademia Alhertina 1 7. 1-10123. Torino, Italy;

■Department of Comparative and Evolutionary Biology, University ofNapoli. Via Mezzocannone 8, ISO 1 34,

Napoli, Italy

Abstract. -115 specimens of Green Toads belonging to the Bufo viridis complex were sampled from 8

populations in south Kazakhstan during the breeding seasons of 1994 and 1995. Subsequent karyological

analysis revealed a single diploid population (Kopa) with a 2n=22 karyotype and large snout-vent length. All

other seven populations proved tetraploid with a 4n=44 karyotype and smaller size. Information on the

distribution of diploid and tetraploid toads in southern Kazakhstan is discussed in connection with previous data.

Key words: Amphibia. Bufonidae. diploid Bufo viridis, tetraploid Bufo danatensis Kazakhstan, geographic

distribution.

Introduction

Following the discovery of some polyploid Asiatic

Green Toad populations (Masik et al. 1976) and the

description of a new species, Bufo danatensis Pisanetz

(Pisanetz 1978). two distinct species, diploid Bufo vir-

idis and tetraploid Bufo danatensis. have been known

to occur in ex Soviet central Asia, where only Bufo

viridis Laurenti, 1768 was formerly recognized.

Using literature data on a number of populations

(Bachmann et al. 1978; Pisanetz 1978; Pisanetz and

Szczerbak 1979; Pisanetz et al. 1985; Toktosunov

1984). as well as their own data. Borkin et al. (1986a)

have drawn a preliminary map of the distribution of

diploid and tetraploid Green Toads of the Bufo viridis

complex in the territory of the ex Soviet Union. Only

3 records of tetraploid Bufo danatensis were known

for Kazakhstan at the time, whereas diploid Bufo viri-

dis had not yet been reported from this region (Borkin

etal. 1986a. p. 141).

During the following nine years many more data

became available on the distribution of diploid and

tetraploid Green Toads in Middle Asia, including

Kazakhstan and its bordering countries (China. Mon-

golia) (Borkin et al. 1986a, 1986b. 1986c, 1996; Fich-

tman 1989; Orlova and Terbish 1986: Orlova and

Uteshev 1986: Schneider and Egiasaryan 1995; Wu

Min and Zhao Yajiang 1987; Fichtman 1989; Zhao Er-

mi 1995). Although some of these data relate to

Kazakhstan, however, the vast territory of this Repub-

lic is still very poor studied in this respect.

In 1994-1995 a combined expedition by the

Department of Animal Biology of the University of

Torino (Italy) and the Department of Biology of

Kazakh State University at Almaty (Kazakhstan) car-

ried out some field work on the Bufo viridis complex

in south Kazakhstan. One of the aims of this expedi-

tion was to obtain new data on the geographic distri-

bution of diploid and tetraploid toads in this territory.

Materials and Methods

1 15 Green Toads were sampled from 8 populations in

South Kazakhstan (Fig. 1) during the breeding sea-

sons (May-June) of 1994 and 1995. Preliminary spe-

cies identification was based on morphometric

comparisons and records of mating calls. In order to

obtain the exact determination of the ploidy level of

each specimen a karyological analysis was subse-

quently carried out at Naples University. From each

specimens 100-200 u.1 of venous blood were incu-

bated for 4 days at 25* C in MEM (Minimal Eagle

Medium. GIBCO) with 20% calf serum and 3% Phy-

toaemogglutinin M. Chromosome preparations were

produced by conventional air-drying method, using

KC1 0.075 M as hypotonic solution. Standard stain-

ing method were performed using Giemsa 5% in

phosphate buffer pH 7.

Vol. 7, p. 28

Asiatic Herpetological Research

1997

Figure 1 . Known localities of diploid and tatraploid green toads. Bufo viridis complex in Kazakhstan. [Circle = date

from literature; Square = our own findings. Dark = Bufo danatensis (4n); light = Bufo viridis (2n); hemidark = sympa-

tic locality of Bufo danatensis and Bufo viridis. ? = attibution not supported by karyological analysis]

Bufo danatensis: 1 - Kapchagai, Hi River (Borkin et al.. 1986a); 2 - desert near Burubaital Village, to the soutwest of

the Balkhash Lake (Egemberdieva. 1983); 3 - Aksiir Farm, 12 km to the northwest of the Maikapchagay Village,

Zaissan Depression (Szczerbak, Golubev, 1981 ); 4 - Chindzhaly River near Andreyevka Village, Taldy-Kurgan

Region (Golubev, 1990); 5 - Chimkent Town, Chimkent Region (Mezherin, Pisanetz, 1991); 6, 7 - Almaty (Borkin et

al., 1996; our data); 8 - Baschii Village, 1 km to the south of the Altyn-Emel Mountain Range (44 10'N; 78 45'E),

Taldy-Kurgan Region (Borkin et al., 1996); 9 - Koyandytau Mountain Range, Taldy-Kurgan Region (Borkin et al.,

1996); 10 - Ayan-Saz Point, the Borokhudzir River Valley, Taldy-Kurgan Region (Borkin et al., 1996); 1 1 - Big Almaty

Lake, Zailijsky Alatau Range; 12 - Karaoj Village, to the south of the Balkhasn Lake; 13 - Zhidely Channel. Hi River

delta; 14 - Kizilkum Desert, 50 km to the southwest of the Bairkum Village, Chimkent Region; 15 - Jabagly Village,

Chimkent Region (1 1 -1 5, our data).

Bufo viridis viridis: 16 - Chornaya Rechka near Guryev Town, Guryev Region (Schneider, Egiasaryan, 1995).

Bufo viridis turanensis: 17 - Almaty (Mezherin, Pisanetz, 1991); 18 - Chindzhaly River near Andreyevka Village,

Taldy-Kurgan Region (Golubev, 1 990); 1 9 - a point in 20 km to the south of the Kopa Station, Almaty Region (our

data).

1997

Asiatic Herpetological Research

Vol. 7. p. 29

Table 1 . Some preliminary results of the study of green toad of Bufo viridis complex in South Kazakhstan. In 1 994

and 1995. specimens have been collected in two different regions of Almaty town and are. therefore, considered

as distinct samples

Locality Year Longitude Latitude

Altitude

(m)

Sample size

males/females

Karyotype

SVL min-max

mm

A map of the distribution of diploid and tetraploid

Green Toads of the Bufo viridis complex was made by

program Automap 1.1 (programmers V Dubjansky

and A. Kazimirov). Since the main purpose of this

paper is to present some new information on the dis-

tribution of diploid and tetraploid toads in Kazakh-

stan, only a brief review of other results obtained has

been summarized in Table 1 .

Results and Discussion

Of 8 populations, only one. sampled near Kopa. in

south eastern Kazakhstan, proved to have a diploid

karyotype. As it is normally the case, this population

also shows the largest snout-vent length (see Table I ).

Until now, diploid Green Toads were reported for

the territory of Kazakhstan from 3 localities only, but

only Mezherin and Pisanetz (1991) and Pisanetz

( 1991 ) supported the occurrence of Bufo viridis luran-

ensis at Almaty with a karyological study. The record

by Golubev ( 1990) of the presence of Bufo viridis in

cohabitation with Bufo danatensis on the Chindzhily

River, near the village of Andreyevka (eastern Kaza-

khstan) (Fig. 1) was based on differences in the breed-

ing behaviour of two groups of specimens and lacks

any karyological confirmation. Finally. Schneider and

Egiasaryan (1995) cited Bufo viridis viridis from

Chornaya Rechka. near the town of Guryev (north

western Kazakhstan, Fig. 1 ) on the basis of some

advertisement-call characters. Although the mating

calls and behaviour of some populations of Bufo viri-

dis have been studied in full detail, a karyological

analysis remains necessary for exact determination.

Records of tetraploid toads in Kazakhstan are

more numerous (Fig. 1). Two of them, however,

respectively from the Zaissan region (Szczerbak and

Golubev 1979) and the Chindzhily River, near

Andreyevka Village (Golubev 1990) need karyologi-

cal confirmation.

Our karyological data show that, apart from a sin-

gle locality (Kopa), all other populations examined

consist of tetraploid specimens. The finding of tetrap-

loid toad populations at the Zhidely Canal of the Hi

River delta and at Karaoj Village concurs with data

by Borkin et al. (1986a; 1996) in that the territory

south of Lake Balkhash and the area along the Hi

River are inhabited by tetraploid toads only (Fig. 1).

Specimens from Zhidely Canal and Karaoj also show

the smallest snout-vent lengths in comparison with

toads from all other populations sampled in 1994 and

1995 (Table 1).

Vol. 7, p. 30

Asiatic Herpetological Research

1997

Our record of tetraploid toads within the town of

Almaty (Table 1 ) is in an agreement with data by Bor-

kin et al. (1996). who identified a tetraploid popula-

tion in the same area by flow cytometry analysis, but

may contradict data of Mezherin and Pisanetz

(Mezherin and Pisanetz 1991: Pisanetz 1991, see

above) who reported the presence of diploid Bufo viri-

dis turanensis from Almaty. A high mountain popula-

tion from the Big Almaty Lake (Transvalley Alatau

Range. 2300 in) also has a tetraploid 4n=44 karyotype

(Table 1 ). For the time being, however, we cannot

exclude the possibility of the presence in the Almaty

region of diploid and tetraploid synthopic populations

and further investigations are necessary in order to

settle this point.

Mezherin and Pisanetz (1991) were first to report

on the presence of a tetraploid population in the

southeast region of Kazakhstan, near the town of

Chimkent. All specimens from the south east exam-

ined by us (Kizilkum Desert and Jabagly Village. Fig.

1 ) are indeed tetraploid. They share a similar snout-

vent length (Table 1 ) but inhabit ecologically different

biotopes. At Kizilkum. toads were found at a pond

located in a sand-dunes area and formed by water

overflowing from a water hole (altitude 250 m). At

Jabagly. toads were caught in small ponds and in a

stream, by a mountain village, at an altitude of 1100

m.

Acknowledgments

We are very grateful to Vladimir Dubyansky for pro-

viding technical assistance in preparing this manu-

script and for using program Automap 1.1.

Literature Cited

Bachmann, K.. A. Konrad. E. Oeldorf. and H. Hem-

mer. 1978. Genome size in the green toad (Bufo viri-

dis) group. Experientia 34:331-332.

Borkin, L. J.. I. A. Caune, E. M. Pisanetz. and Y. M.

Rozanov. 1986a. Karyotype and genome size in the

Bufo viridis group. Pp. 137-142. In Z. Rocek (Ed.),

Studies in Herpetology. Prague.

Borkin. L. J.. Y. M. Rozanov, H. Terbish. and I. M.

Caune. 1986b. [The distribution, karyology, taxon-

omy and variability of the toad of Bufo viridis group

in Mongolia]. Pp. 120-143. In Herpetological

researches in MNR. (In Russian).

Borkin, L. J.. H. Terbish, and I. A. Caune. 1986c.

[Tetraploid and diploid populations of the toad of

Bufo viridis group from Mongolia]. Doklades of

Academy of Sciences USSR 287(3 ):760-764. (In

Russian).

Borkin. L.J. . and S. L. Kuzmin. 1988. [The Amphib-

ians of Mongolia]. Pp. 30-197. In Amphibians and

reptiles of MNR. Moscow, Nauka. (In Russian).

Borkin. L. J., A. E. Vinogradov, Z. K. Brushko., and

S. L. Kuzmin. 1996. New records of tetraploid toads

{Bufo viridis group) from Alma-Ata and Taldy-Kur-

gan region, Kazakhstan. Russian Journal of Herpetol-

ogy 2 (2): 174-175.

Egemberdieva, G. Ch. 1983. [Differenciruyushchaya

rol izolyacii v izmenchivosti pozvonochnykh zhivot-

nykh]. Pp. 81-1 14. In Ecologo-geneticheskie osnovy

izmenchivosti pozvonochnykh zhivotnykh. Frunze.

(In Russian).

Fichtman. B.S. 1989. [On the diagnosis of the green

toad of Bufo viridis complex in Kirgizia]. Pp. 263-

264. In Problems of Herpetology. Kiev, Naukova

dumka. (In Russian).

Golubev, M. L. 1990. [New records of amphibians

and reptiles in the territory of Kazakhstan], Vestnik

Zoologii, Kiev 5:76-78. (In Russian with English

summary).

Masik, E. J., B. K. Kadyrova, A. T. Toktosunov. 1976.

[Karyotype pattern in the green toad Bufo viridis in

Kirgizia], Zoologichesky Zhurnal 55:1740-1742. (In

Russian with English summary).

Mezherin. S. V, and E. M. Pisanetz. 1990. [Genetic

structure and origin of asiatic tetraploid toad. Bufo

danatensis Pisanetz, 1978). Doklades of Ukrainian

Academy of Sciences 3B(8):71-73. (In Russian with

English summary).

Mezherin, E. J., and E. M. Pisanetz. 1991. [Genetic

divergence of green toads of Bufo viridis complex of

USSR fauna]. Doklades of Academy of Sciences of

USSR 3 1 7( 10):222-226. ( In Russian ).

Orlova, V F. and H. Terbish. 1986. [Materials on

Dzhungarian Gobi Herpetofauna]. Pp. 95-110. In

Herpetological Researches in MNR. Moscow. (In

Russian).

Orlova, V. F, and V Uteshev. 1986. The tetraploid

toad of Bufo viridis group from Dzhungarian Gobi,

Mongolia. Pp. 143-146. In Z. Rocek (ed.). Studies in

Herpetology. Prague.

Pisanetz, E. M. 1978. [On new polyploid species of

the toad. Bufo danatensis Pisanetz sp. n. from Turk-

menia], Doklades of Ukrainian Academy of Sciences

3B( 3 1:280-284. (In Russian or Ukrainian).

Pisanetz, E. M. 1991. [The new dates of karyology

Bufo viridis-complex (Amphibia. Bufonidae) and the

questions of origin of asiatic tetraploid toads]. Herpe-

tological Researches, Leningrad 1991( l):41-50. (In

Russian with English summary).

1997

Asiatic Herpetological Research

Vol. 7, p. 31

Pisanetz, E. M. 1992. Evidence of hybridization

between di- and tetraploid toads {Bujo viridis com-

plex) from Eurasia (Anura: Bufonidae). Pp. 357-360.

In Z. Korsos and I. Kiss, (eds.), Proc. Sixth Ord. Gen.

Meet. S.E. Budapest.

Pisanetz, E. M.. and N. N. Szczerbak. 1979. [Taxon-

omy of the green toads (Amphibia. Anura) from the

USSR fauna]. Vestnik Zoologii 4:1 1-16. (In Russian

with English summary).

Schneider. H.. and E. M.Egiasaryan. 1995. The mat-

ing call of the green toad. Bufo viridis viridis (Anura.

Amphibia) in Kazakhstan. Russian Journal of Herpe-

tology 2(1): 1-4.

Toktosunov. A. T 1984. [Ecological basis of altitude

adaptation of the vertebrates of Tien-Shan]. Lenin-

grad. Nauka. (In Russian).

Wu Min. and Zhao Yajiang. 1987. [Preliminary study

of the karyotype of green toad from Sinzsjan]. Zoo-

logical Researches 4:339-342. (In Chinese).

Zhao Er-mi. 1995. [A checklist of Chinese amphibi-

ans and their distribution]. Pp. 1-15. In Er-mi Zhao

(Ed.). Amphibian Zoogeographic Division of China.

1995 Supplement: Sichuan Journal of Zoology.

Chengdu, Sichuan. China. (In Chinese).

1997

Asiatic Herpetological Research

Vol. 7, pp. 32-37

Phylogeny of Genus Scutiger (Amphibia: Megophryidae): A Re-evaluation

Jinzhong Fu, Amy Lathrop, and Robert W. Murphy

Department of Ichthyology and Herpetology, Royal Ontario Museum, 100 Queen's Park, Toronto. Ontario,

Canada M5S 2C6, and Department of Zoology, University of Toronto

Abstract. - A re-analysis of a published data set from Ye et al. ( 1992) indicates that their phylogeny for the genus

Scutiger does not reflect the most parsimonious explanation of the data. The consensus of the resulting trees

from the original data set is a "bush" with only three resolved nodes. A re-evaluation of the character states, and

their respective polarizations, resulted in alternative phylogenetic hypotheses. However, measures of homoplasy

and data consistency for the re-evaluated topologies were relatively low, suggesting that little confidence could

be obtained in these relationships. More data are needed to generate a defensible hypothesis of the relationships

within the genus Scutiger.

Key words: Amphibia. Anura, Pelobatoidea. Megophryidae, Scutiger, morphology, phylogeny, parsimony

Character 27

Linea musculinae

absent (0); present (1)

1 ancestral state for Oreolalax

Figure 1 . Phylogeny of Oreolalax with the character

states of linea musculinae optimized on the tree. The

primitive condition of linea musculinae for the phylog-

eny of Scutiger is 1.

Introduction

Frogs in the family Megophryidae have long capti-

vated many herpetologists, especially Chinese col-

leagues, partly because of their supposed transitional

position between "primitive" and "advanced" frogs

(Lynch, 1973, Ford and Cannatella, 1992) and also

because of asthetic appeal. The phylogeny of peloba-

toids is largely unknown, and we now realize that the

concepts of "primitive" and "advanced" taxa are phy-

logenetically flawed and hence unacceptable: only

character states have these attributes.

Thirty-two species of Scutiger occur in the high

altitudes of the Tibet Plateau in southwestern China.

Burma. Nepal, and northern India. A phylogeny of

this group has been wanting. The genealogical rela-

tionships of this group would be useful for assessing

theories of the geologic events that have been linked

with the uplift of this region. Recently, Fei and Ye

(1990) and Xu et al. ( 1992) investigated the relation-

ships of megophryids. Of particular interest. Ye et al.

(1992) presented a phylogeny of genus Scutiger using

29 morphological characters. Unfortunately, some

invalid methods were employed in both the character

analysis and tree selection, and these nullify their

hypothesis. We performed a re-evaluation of the Ye et

al. (1992) data, and examined their proposed phylog-

eny of Scutiger.

Methods

The data of Ye et al. (1992) consisted of 29 morpho-

logical characters for 16 species of Scutiger, and one

outgroup taxon (Appendix I). Initially, we analyzed

these data without modification. Following Ye et al.

( 1992), five species, Scutiger ningshanensis, S. macu-

latus. S. nepalensis. S. occidentalis, and S. adungen-

sis, were excluded from the analysis owing to many

unknown character states (Appendix II). We used

outgroup analysis (Maddison et al., 1984) to reassess

character state polarizations. Oreolalax was used as

the outgroup and polarizations of the character states

were determined from previous work (Fu and Mur-

phy, in press). From this phylogeny, we were able to

identify pleisomorphic character states for Oreolalax,

which were then used to polarize the character states

for scutigers. For example following Maddison et al.

(1984) and Wiley et al. ( 1991 ). we assigned character

states for the terminal branches down the tree until

reaching the root node (see Fig. 1 for the optimization

of Linea Musculinae).

1997

Asiatic Herpetological Research

Vol. 7. p. 33

Hypothetical ancestor

S Itupanonsis

s chlntlngmnsla

S. pingwuensts

S boutongon

S. nytngchlansls

S sikklmansts

S. brovipas

S mammatus

S. tuberculatus

S gongshanosis

Figure 2. Strict consensus tree of the phylogeny of

Scutiger, derived from our reanalysis of Ye et al.'s

(1992) original data.

I 5

I 2

2

D

Hypothetical ancestor

S Itupanonsis

S plngwu&nsls

S chintingensis

S Oouleng&n

S. muli&nsts

S brevipes

S tuberculatus

S gongshanasls

S nytngchiensis

S sikkimensfs

Figure 3. One of 20 MPTs depicting the phylogeny of

Scutlgerthai was derived from our reanalysis of Ye et

al.'s (1 992) original data. When the outgroup condition

was not known, the original character state polariza-

tions of Ye et al. were used. This topology was

reached by successive approximations (Farris. 1969);

numbers indicate unambiguous synapomorphies

occuring at each corresponding node.

Phylogenetic analyses were conducted using

(PAUP) version 3.1.1 (Swofford, 1993) and employ-

ing an heuristic search with stepwise addition. Tree

optimization was performed using the tree bisection-

reconnection branch swapping option, steepest

descent, and retaining all most parsimonious trees.

Tree topologies were analyzed in MacClade 3.04

(Maddison and Maddison, 1992). To choose among

the most parsimonious trees, we employed successive

approximations (Farris. 1969). Decay analysis

(Bremer. 1988) was used to assess nodal stability.

Results

Our initial evaluation of the phylogeny of Scutiger

using the unmodified original data of Ye et al. (1992)

resulted in 20 most parsimonious trees (MPTs), each

with a consistency index (ci) of 0.46, retention index

(ri) of 0.53 and a length of 62 steps. A strict consen-

sus tree revealed only three consistent nodes (Fig. 2).

Scutiger gongshanensis with S. tuberculatus were

resolved as sister species, as were S. pingwuensis and

S. chintingensis. Only the latter relationship and the

association of S. mammatus. S. brevipes, S. muliensis.

Orootelax

S chintingensis

S. sikhimensis

S pingwuensis

S tiupanensis

S beulengen

S nymgchiensis

S tuberculatus

S- gongshanests

S brevipes

S mammatus

S muliensis

Figure 4. Phylogeny of Scutiger. One of 16 MPTs

derived from Ye et al.'s (1 992) data using Oreolalax as

the outgroup. When the outgroup condition was not

known, the original character state polarizations of Ye

et al. were used. This topology was reached by suc-

cessive approximations; numbers indicate unambigu-

ous synapomorphies occuring at each corresponding

node.

.S\ tuberculatus and S. gongshanensis were resolved

by Ye et al. (1992). Excluding these relationships, all

others were ambiguous. The topology of Ye et al.

requires 63 steps to explain the data, one steps longer

than our most parsimonious tree. A successive

approximations evaluation resolved a single tree, one

of the original 20 MPTs (Fig. 3).

Re-examination of the character polarizations of

Ye et al. (1992) shows that characters 3 and 27 were

incorrectly polarized in the original work. We were

unable to polarize character 25 because both states

occur in the outgroup; the presence or absence of spi-

nal patches on the forelimbs are equally probable as a

plesiomorphy for Scutiger. Characters 1 and 26 have

autapormorphic states only, making them phylogenet-

ically uninformative; they were excluded from subse-

quent analyses. Polarization of characters 7, 8, 9, 10,

II. 15. and 17 was not possible using outgroup crite-

rion because the state(s) in the outgroup are not

known. These characters were treated both using the

original polarizations of Ye et al. (1992). and subse-

quently by treating them as missing data in the out-

group.

Our analysis using the polarizations of Ye et al.

(1992) for characters 7-1 1, 15, and 17 resulted in 16

MPTs, 60 steps in length (ci = 0.45. ri = 0.53). The

strict consensus tree is identical to that of the original

analysis with only three nodes resolved. Using suc-

cessive weighting resulted in a single MPT which is

one of the 16 MPTs (Fig. 4). When supporting charac-

ters were mapped on the phylogeny, most of the nodes

received very little unambiguous support from these

data.

The alternative approach treated character states

that were unknown in the outgroup as missing data.

This resulted in 1 most parsimonious tree (Fig. 5), ci =

Vol. 7, p. 34

Asiatic Herpetological Research

1997

2_

0_

5

i

2

4

2

Oreolalax

S sikkimensis

S nyingchiensis

S boulengen

S. liupanensis

S chmtmgensis

S pingwuensis

S tuberculatus

S gongshanesis

S brevipes

S mammatus

S muliensis

Figure 5. A single MPT for the relationships of Scuti-

ger. The data in which unknown states for the out-

group are left as missing. Numbers indicate

unambiguous synapomorphies occuring at each node.

- Oreolalax

- S llupan-

- S pingwuensis

- S. chintlngensts

- S. Doulengen

- S nyingchiensis

- S sikktmensis

- B muliensis

• S gongshane

Figure 6. The resulting strict consensus tree of Scuti-

ger after saving all trees one step longer than the

shortest tree, from the data set where unknown out-

group states were left as missing.

0.49, ri = 0.57 and 59 steps. In this topology, like the

others, few unambiguous changes have occurred.

Discussion

Ye et al. (1992). recognized two subgenera in the

genus Scutiger. Scutiger and Aelurophryne. They

identified three synapomorphies for the latter, and

based on the derived relationships and current distri-

butions, drew conclusions about the origin of the

scutigers.

Our results show that the phylogeny of Ye et al.

(1992) was not the most parsimonious explanation of

their data. We resolved 20 trees that were more parsi-

monious. A strict consensus of our shortest trees

resulted in a tree with only three nodes resolved. As

was true in Ye et al.'s tree, Aelurophryne was mono-

phyletic and supported by three synapomorphies.

Within this clade the sister relationships of only two

species, S. tuberculatus and S. gongshanensis, could

be unambiguously resolved. The remaining scutigers

formed a single basal polytomy with the

Aelurophryne. but two species were resolved. S. chint-

ingensis and S. pingwuensis. This sister relationship

was also seen in Ye et al.'s tree, our analysis did not

resolve the subgenus Scutiger as a monphyletic group.

Ye et al. (1992) apparently used a hypothetical

ancestor rather than Oreolalax as the outgroup. some

characters were incorrectly polarized. Consequently,

we believe that any conclusions derived from either

their phylogeny or our reanalysis of the original data

set are invalid.

The proper ordering and polarizations of character

states using the outgroup criterion proved very impor-

tant. Failure to defensibly order states of multistate

characters resulted in the resolution of less parsimoni-

ous solutions. Even though we changed the polariza-

tions of two characters, seven other characters could

not be polarized. Consequently, subsequent analyses

either left the polarization as assumed by Ye et al

(1992). or we treated the outgroup states as missing,

thereby treating the characters as unpolarized. The

former analysis resulted in 16 MPTs in which the

strict consensus tree was identical to our first analysis.

The latter analysis resulted in one tree depicting

Aelurophyrne as monophyletic. and S. chintingensis

and S. pingwuensis as sister species. It did not resolve

the subgenus Scutiger as a monophyletic assemblage.

It is desirable to assess the support for individual

nodes and the entire phylogeny. Several methods have

been proposed. One procedure, bootstrap (BS) analy-

sis (Felsenstein. 1985), assesses relative support for

each node of a phylogeny (for criticisms of the

method see Carpenter, 1992; Hillis and Bull, 1993;

Kluge and Wolf. 1993; Trueman, 1993). One prereq-

uisite to a BS analysis often overlooked, is that a min-

imum three characters per node is required to obtain a

statistically significant BS value. Unfortunately, our

MPTs do not have enough unambiguous character

changes at each node to generate statistically mean-

ingful BS values.

Decay analysis (Bremer. 1988). an alternative

method, keeps all trees that are a specified length

longer than the MPTs. It permits the assessment of

nodal support by identifying only those monophyletic

groups that are common to all of the possible trees.

This method presumes that all relationships receiving

sound support from these data will be present in a

strict consensus tree of all trees one or two steps

longer. When we held all MPT plus those one step

longer, 241 trees were retained. The resulting strict

consensus tree showed no resolution; all of the

ingroup taxa were resolved from a single node. How-

ever, when the ambiguously polarized states were

coded as missing data in the outgroup, the MPTs and

those one step longer included 27 trees, and the strict

consensus tree broke into one ingroup clade,

Aelurophiyne (Fig. 6). Holding all trees two steps

longer resulted in 362 trees and a single polytomy.

1997

Asiatic Herpetological Research

Vol. 7, p. 35

The status of the subgenera Aelurophryne and

Scutiger has been debated (Myers and Leviton, 1462;

Noble. 1931; Pope and Boring. 1940; Liu. 1950) and

Aelurophryne was previously diagnosed by the

absence of maxillary teeth. Meyers and Leviton

(1962) stated that the absence of teeth actually

reflected a graded trend within the genus Scutiger, and

could not be used to separate Scutiger from

Aelurophryne. This is also true for two of the three

characters used by Ye et al. (1992) to define

Aelurophryne. However, the presence of a robust

metacarpal bone can be used to distinguish

Aelurophryne from other scutigers.

Ye et al. (1992). used their phylogeny to discuss

the evolution and specialization of Aelurophryne.

They described the subgenus as having become more

specialized for an aquatic lifestyle, and recognize

three synapomorphies: robust metacarpal bone, thick

humerus, and the no keritanized spines on the dorsum.

Two problems exist. First, the latter two synapomor-

phies are also derived in S. nyingchiensis. Second, one

synapomorphy, no keritanized spines, is an actual loss

of a character. It is more preferable when reconstruct-

ing phylogenies to use characters that are uniquely

derived and not represented by the absence of charac-

ters. Moreover, characterizing a group based on the

absence of traits should be avoided. Numerous sce-

narios can be developed to explain the loss of a char-

acter and its homologue can never be identified with

certainty. However, the presence of a character may

be scrutinized at a greater detail, often making it pos-

sible to recognize homologous counterparts.

Because the subgenus Scutiger cannot be diag-

nosed, it is possible, if not likely that this subgenus is

a polyphyletic assemblage of species. Therefore, our

analysis requires that the subgenus Aelurophryne not

be recognized if a holophyletic classification is to be

maintained.

One problem that permeates the data base is the

selection of highly homoplastic characters.

Homoplastic characters tend to provide no definitive

resolution. However, we cannot comment on the

quality of characters until we can see how they per-

form during a defensible phyletic estimation. We are

certain that too few characters were used to generate

support for any of the relationships on the phylogeny.

The information summarized by Ye et al. (1992)

forms the initial ground work for understanding the

evolutionary relationships Scutiger. Given that so lit-

tle is known about these frogs, any advances should

be deemed valuable. However, additional data are

required to confidently resolve the phyletic relation-

ships of scutigers. and to identify the corresponding

plesiomorphic condition in Oreolalax. Once a sound

phylogeny of the genus has been achieved, it will be

possible to address biogeographical, ecological, and

behavioral questions.

Acknowledgments

Many thanks to D. Upton, whose comments greatly

improved the quality of this paper. This work is sup-

ported by Natural Sciences and Engineering Research

Council of Canada grant No. A3 148 to RWM, and

No. OGP46464 to K. Coates. This is contribution

XXX from the Centre for Biodiversity and Conserva-

tion Biology of the Royal Ontario Museum.

Literature Cited

Bremer. K. 1988. The limits of amino acid sequence

data in angiosperm phylogenetic reconstruction. Evo-

lution. 42:795-803.

Carpenter. J. M. 1992. Random Cladistics. Cladistics

8:147-153.

Farris, J. S. 1969. A successive approximations

approach to character weighting. Systematic Zoology

18:374-385.

Fei. L. and C. Ye. 1990. Intergenetic relationships and

diversification of the high-altitude pelobatid toads in

Asia and their relation with the formation of Qinghai-

Xizang Plateau (Amphibia: Pelobatidae). Acta Zoo-

logica Sinica 36:420-428 [In Chinese].

Felsenstein. J. 1985. Confidence limits on phyloge-

nies: an approach using the bootstrap. Evolution

39:783-791.

Ford. L. S. and D. C. Cannatella. 1993. The Major

clades of frogs. Herpetological Monographs 7:94-

117.

Fu, J. and R.W. Murphy. 1997. Phylogeny of Chinese

Oreolalax and the use of functional outgroups to

select among multiple equally parsimonious trees.

Asiatic Herptological Research.

Hillis, D.M. and J. J. Bull. 1993. An empirical test of

bootstrapping as a method for assessing confidence in

phylogenetic analysis. Systematic Biology 42:182-

192.

Kluge, A. G. and A. J. Wolf. 1993. Cladistics: What's

in a word? Cladistics 9:183-199.

Liu. C-c. 1950. Amphibians of western China. Field-

iana: Zoology, Memoirs 2: —100.

Lynch, J. D. 1973. The transition from archaic to

advanced frogs, pp 133-182. In Evolutionary biology

of the Anurans: Contemporary research on major

problems. Columbia. University of Missouri Press.

Vol. 7. p. 36

Asiatic Herpetological Research

1997

Maddison. W. P. and D. R. Maddison. 1992. Mac-

Clade: analysis of phylogeny and character evolution,

version 3.04. Sinauer Associates Inc. Sunderland.

Massachusetts.

Maddison. W.P.. M.J. Donoghue. and D.R. Maddison.

1984. Outgroup analysis and parsimony. Systematic

Zoology 33:83-103.

Myers. G.S.. A. E. Leviton. 1962. Generic classifica-

tion of the high-altitude pelobatid toads of Asia

(Scutiger, Aelurophryne, and Oreolalax). Copeia

1962:287-291.

Noble, G. K. 1931. Biology of the Amphibians.

McGraw-Hill Book Co., New York. 577 pp.

Pope. C. H. and A. M. Boring. 1940. A survey of

Chinese Amphibia. Peking Natural History Bulletin

15: 13-86.

Swofford, D. L. ( 1993). PAUP: Phylogenetic analysis

using parsimony, version 3.1. program and documen-

tation. Illinois Natural History Survey. Champaign.

Trueman, J. W. H. 1993. Randomizations con-

founded: a response to Carpenter. Cladistics 9: 101-

109.

Wiley. E. O.. D. Siegel-Causey. D. R. Brooks and V.

A. Funk. 1991. The compleat cladist: a primer of phy-

logenetic procedures. The University of Kansas

Museum of Natural History Special Publication No.

19. 158 pp.

Xu. N.. G. Wei. L. Fei, C. Ye. D. Li. 1992. Study on

the phylogenetic relationship between species of

genus Oreolalax (Amphibia: Pelobatidae). Acta Her-

petologica Sinica Vol. 1 and 2: 40-49 [In Chinese].

Ye. C, L. Fei, G. Wi. N. Xu. 1992. Study on the phy-

logenetic relationship between species of Scutiger

genus in Qinghai-Xizang Plateau (Amphibia: Pelo-

batidae). Acta Herpetologica Sinica Vol.1 and 2:27-39

[In Chinese].

Appendix I

Modified data set ofYe et al (1992). Characters were polarized using Oreolalax as the outgroup. Those characters

in bold were omitted from the analysis because they are apomorphic.

Character

number

1 11111 11112 22222 2222

12345 67890 12345 67890 12345 6789

Oreolalax

S. liupanensis

S. pingwuensis

S. chintingensis

S. boulengeri

S. nyingchiensis

S. sikkimensis

S. mammatus

S. brevipes

S. tuberculatus

S. muliensis

S. gongshanensis

001 00 00000 00000 00000 0000- 01 00

11101 00011 10101 01101 110100000

01111 00111 10001 00101 11011 0011

00111 01101 00001 01001 11001 0011

01101 10000 10100 01100 11010 0000

01 001 00001 01 000 1 1 01 1 1 0000 0001

01 1 00 1 1 1 1 1 00000 01111 1 1 000 1 001

01001 10010 01110 10100 10100 0001

01101 10000 01110 10101 10000 0001

01011 10000 01110 11101 10000 0011

01011 10000 01110 10101 10100 0001

00111 10011 11110 1111000000 0111

1997

Asiatic Herpetological Research

Vol. 7, p. 37

Appendix II

Character used by Ye et al (1992).

1 . Head width to length

0: width > length. 1 : width < length

2. Maxillary teeth

0: well developed. 1: very small or absent

3. Nasal and sphenethmoid

0: articulated, 1: seperated

4. Columella

0: present 1 : absent

5. Quadratojugal

0: long, articulated or overlapped with maxilla,

1 : short, wildly seperated from maxilla

6. Prootic and exoccipital bone

0: seperated. 1 : fused

7. Hyoid plate plus anterior process (HPAP) and the

distance between the out flank of the anterior process

(DFAP)

0: HPAP < DFAP. 1: HPAP > DFAP

8. Hyoid fenestra

0: present 1 : absent

9. Cricoid cartilage

0: complete circle. 1 : circle incomplete

10. Omosternum and xiphisternum

0: Width of omosternum < width of xiphister-

num. 1: width of episternum >width of xiphis-

ternum

1 1 . Omosternum

0: partially ossified. 1: entirely cartilage

12. Humerus in male

0: length/width > 4. 1 : length/width < 4

13. Inner crest of radioulna in male

0: absent. 1 : present

14. Inner two metacarpals and phalanges in male

0: normal. 1: robust

15. Prepollex

0: ossified, 1: cartilage

16. Dorsal skin

0: with homy spines, I : without horny spines

17. Large warts near vent

0: absent. 1 : present

18. Post-femoral gland

0: present. 1 : absent

19. Webbing between toes

0: present, 1: absent

20. Metatarsal tubercle

0: absent, 1: present

2 1 . Vocal sac

0: present, 1 : absent

22. Spiney patches on the chest

0: one pair. 1 : two pair

23. Spines on the chest

0: small. 1: big

24. Spinal warts on belly

0: absent, 1: present

25. Spinal patches of forelimb

0: absent. 1: present

26. Nuptial spines

0: small. 1: big

27. Linea musculinae

0: absent. 1: present

28. Labial margin of tadpole

0: narrow, with many tubercles, 1 : wide, with

few or no tubercles

29. Labial teeth formula of tadpole. Number of tooth

rows

0: >I:5-5/I:5-5, 1: < 1:5-5/1:5-5.

1997

Asiatic Herpetological Research

Vol. 7. pp. 38^3

Phylogeny of Chinese Oreolalax and the Use of Functional Outgroups to Select

Among Multiple Equally Parsimonious Trees

JlNZHONG FU AND ROBERT W. MURPHY

Department of Ichthyology and Herpetology, Royal Ontario Museum, 100 Queen's Park. Toronto, Out. M5S 2C6,

Canada and Department of Zoology, University of Toronto

Abstract. -Re-analysis of a published data set from Xu et al. (1992) reveals that their proposed phylogenetic tree

is not the most parsimonious explanation. Ten shorter, most parsimonious solutions are derived from these data.

The progressive functional outgroup approach found a single tree from among the ten to be the best explanation

of the data. Such an approach may prove to be a powerful method for dealing with multiple equally parsimonious

trees.

Key words: Amphibia. Anura. Oreolalax. China. Phylogeny, Functional outgroups

Figure 1. Phylogenetic Cladogram of Oreolalax pro-

posed by Xu et al. (1992).

Introduction

Although considerable interest has been shown in the

evolution of pelobatid frogs relatively recently, the

phylogeny of many pelobatids remains largely enig-

matic. Xu et al. ( 1992) proposed a phylogeny for four-

teen species of Oreolalax (Fig. 1). This genus of

pelobatid frogs is endemic to China and most of the

15 described species occur at high elevations (1500 to

3300m). Xu et al. used 29 morphological characters in

their analysis (Appendix I), and these were gathered

for the 14 species known at the time of their analysis.

Subsequent to the proposed phylogeny. a new species,

O. multipunctatus, was described (Wu et al.. 1993).

However, the phylogenetic relationships of this new

species were not considered in the description; its

position among the other species remained uncertain.

Consequently, we undertook a re-examination of the

phylogeny of Oreolalax using data provided by Xu et

al. (1992) and Wu et al. (1993).

Our initial examination of Xu et al. (1992) showed

several problems in their analysis potentially invali-

dating their conclusions. Because of this, we first pur-

sued a re-evaluation of their data, and subsequently

incorporated the new species into our analysis to

obtain a more defensible phylogenetic estimation for

the genus Oreolalax.

Materials and Methods

The data set from Xu at al. ( 1 992 ) was used in our ini-

tial analysis (Appendix II). Our phylogenetic analysis

was undertaken using Hennig86 (version 1.5: Farris

1988). Random Cladistics (version 2.0: Siddall 1994)

and PAUP ( version 3.1.1. Swofford 1 993 ). Branch and

bound algorithm (Hendy and Penny 1982) as provided

in these software packages was used for all tree

searching. The resulting trees were rooted initially by

a hypothetical ancestor scored plesiomorphic for all

characters based on the hypotheses of Xu et al.

(1992). Using Random Cladistics. a permutation tail

probability test (PTP; Faith and Cranston 1991) was

used for assessing the presence of pattern in the data

set. which we assume to represent phylogenetic struc-

ture. Bootstrap values (BS: Felsenstein 1985) were

used for assessing the relative strength of support for

monophyletic groups. Examination of character state

distributions on trees was accomplished using Mac-

Clade (version 3.04; Maddison and Maddison 1992).

Initial estimations of phylogenetic analysis were

accomplished using the unaltered data of Xu et al.

(1992). Three methods were exploited for dealing

with multiple most parsimonious trees (MPTs): con-

1997

Asiatic Herpetological Research

Vol. 7. p. 39

Figure 2. A: Strict consensus tree of 1 0 MPTs resulting

from the original analysis with 7 unresolved nodes. B:

50% majority rule consensus tree with 2 unresolved

nodes: 6=0.6; 9=0.9; 1 =1 .0. C: Adams consensus tree

with 4 unresolved nodes.

sensus evaluation, successive approximations weight-

ing (SAW; Fams 1969. 1988), and functional

outgroup approach (FOG) modified from Watrous and

Wheeler (1981). Following resolution of the tree for

the initial 14 species treated by Xu et al., the position

of Oreolalax multipunctatus relative to the other spe-

cies was estimated.

Results

Our PTP test showed the data set of Xu et al. has pat-

tern which is significantly different from random. A

PTP value of p<0.001 was obtained based on 999 ran-

domized data sets. The minimum length tree derived

from the randomized data was 64 steps whereas the

minimum length tree from the original data was 58

steps. We interpret this pattern to reflect the presence

of phylogenetic structure.

Ten MPTs of 58 steps were found, each with a

consistency index (CI; Kluge and Farris 1969) of CI =

0.50, and a retention index (RI; Farris 1989) of RI =

0.59. When the data are mapped onto the tree of Xu et

al.. their tree was observed to have a length of 61 steps

(CI = 0.47; RI = 0.54). Using PAUP, we found no

Figure 3. Three MPTs resulting from successive

approximations weighting. The unstable position of O.

omeimontis and O. popei is responsible for the three

trees.

fewer than 7000 equally or more parsimonious solu-

tions having 61 steps; we terminated the program

after 30 minutes analysis.

A strict consensus tree, Adams consensus tree

(Adams 1972), and 50% majority consensus tree were

generated from the ten MPTs respectively. The strict

consensus tree (Fig. 2a) showed low resolving power.

Only seven of 13 nodes were resolved demonstrating

much conflict among various patterns of relationships.

The Adams consensus tree (Fig. 2b) gave a slightly

better resolution with four nodes unresolved. Finally,

the 50% majority consensus tree (Fig. 2c) left only

two nodes unresolved. In all analyses, O. rhodostig-

matiis always appeared at the base of the ten MPTs.

As another means of selecting a preferred tree

from among the ten MPTs, we used SAW. Following

the successive re-weighting of characters based on the

RI. three trees were found. When the character

weights were re-set to 1, each tree had a length of 58

steps, and thus all fall within the suite of initial MPTs.

Among the three trees, the position of O. omeimontis

and O. popei were unstable, accounting for three

alternative trees, and two other nodes were resolved as

polytomys (Fig. 3).

We had concern that the plesiomorphic states may

not have been correctly identified as no outgroup was

used in the analysis, although the ancestral states the-

oretically represent the conditions observed in Lepto-

brachium. Given this, and the observation that, in

general, the closer the outgroup is to the ingroup the

more likely the polarization of character states will be

accurately determined, we used a functional outgroup

(FOG) approach (Watrous and Wheeler 1981) to

Vol. 7. p. 40

Asiatic Herpetological Research

1997

Figure 4. Strict consensus tree of 2 MPTs resulting

from using Oreoialax rhodostigmatus as functional out-

group.

Figure 5. Resulting tree using Oreoialax lichuanensis

as functional outgroup.

examine the data. Because O. rhodostigmatus always

appeared at the base of the ten MPTs. this species was

used as our FOG. We excluded the hypothetical

ancestor from our secondary and subsequent analyses.

Our FOG approach revealed two equally parsimo-

nious trees, each with 53 steps (=58 steps with HA; CI

= 0.54, RI = 0.60). Neither tree was the same as

resolved from our SAW evaluation but both were

among our original ten MPTs. The strict consensus

tree shows two unresolved nodes (Fig. 4). For resolv-

ing the ambiguous nodes, a closer FOG, Oreoialax

lichuanensis, was selected. Taxa below the FOG (O.

rhodostigmatus. O. popei and O. omeimontis) were

excluded from this analysis. A single MPT with 37

steps was found (=58 steps with the deleted taxa; CI =

0.67, RI = 0.70) (. 5). It is one of the ten MPTs from

the original analysis. Examination of character state

distributions on this tree showed no potential for fur-

ther resolution to the relationships of O. chuanbeien-

sis, O. liangheiensis and more terminal taxa.

Combining the results of our progressive FOG analy-

sis, a single cladogram emerged as our preferred tree

(Fig. 6). Thus, our tree is left with one unresolved

polytomy.

Bootstrap (BS; Felsenstein 1985: Siddall 1994)

was used to assess strength of support of monophyl-

etic groups. The BS value based on 999 randomized

data sets was mapped on the resulting tree (Fig. 6).

Three nodes were shown to be well supported by BS

that have values over 0.5. The O. schmidti and O. pu.x-

iongensis clade has a highest value of 0.840. while the

O. jingdongensis, O.rugosus and O. granulosus clade

has the second highest value of 0.732. The ingroup

member excluding O. rhodostigmatus from the clade

and has a high value of 0.634. The weakest support

from BS is the O. popei and O. omeimontis clade that

has a value as low as 0.06 1 .

Finally, the data for Oreoialax multipunctatus

were combined with those of Xu et al. (1992: Appen-

dix 11). From the characters available for all ingroup

taxa, O. multipunctatus was resolved as either the sis-

ter group of O. schmidti or O. puxiongensi, both of

which were most frequently resolved as sister taxa.

The missing data were responsible for the ambiguity.

Discussion

Phylogeny of Oreoialax

Oreoialax rhodostigmatus was consistently resolved

as the sister of all other species in the genus. Three

characters (8, 10, 18; Appendix I) separate it from

other species. A BS value of 0.634 was calculated for

the node excluding O. rhodostigmatus. The rugosus

group of Xu et al. (1992) also appears to be mono-

phyletic and received a relatively high BS value

(=0.732). Zhao and Adler (1993) regarded O. puxion-

gensis as a synonym of O. schmidti. Here, the highest

BS value observed from the data, BS = 0.840, shows

that these two taxa are very similar. Although further

detailed work is needed to determine the status of O.

puxiongensis. because O. multipunctatus is resolved

as the sister species of either O. puxiongensis or O.

schmidti, synonymization of these latter two taxa

would also require synonymization of O. multipuncta-

tus if a holophyletic classification is to be maintained.

Thus, we recommend recognition of all three species

until far more detailed evaluations can be made.

1997

Asiatic Herpetological Research

Vol. 7, p. 41

0 431

0.634

Figure 6. Phylogeny of Oreolalax as resolved by using

our progressive functional outgroup analysis. One

node remains unresolved. Bootstrap values are pro-

vided for each node.

Although O. popei and O. omeimontis are grouped

together on our preferred tree (ure 6). the BS analysis

shows a very low value of 0.06 1. They shared five

characters (8, 10, 18. 21, 29). Optimizing these char-

acters on the preferred tree shows that character 8, 10

and 18 are shared by all ingroup members excluding

O. rhodostigmatus, with 1 or 2 independent reversals.

Characters 21 and 29 are shared by all ingroup mem-

bers with more than 2 independent reversals. These

two taxa do not share any uniquely derived characters.

We believe that this association should be considered

tenuous because of the low BS value, and the resolu-

tion of a different set of relationships for these two

taxa in our SAW evaluation (Fig. 3). More work is

needed to determine the relationships of these species

with the others.

The relationships of O. chuanbeiensis, O. liang-

heiensis and the rugosus group are unresolved. There

are no unambiguous characters to support any resolu-

tion of these three taxa. More characters are required

for the resolution of this polytomy.

Most species of Oreolalax are distributed along

the east edge of the Qinghai-Tibet Plateau. Oreolalax

rhodostigmatus occurs in the far east of the Qinghai-

Tibet Plateau and is almost allopatric in distribution

from all other species. The rugosus group occurs at

the highest elevations. 2100-3300m. This suggests

that their common ancestor was adapted for the rigors

of alpine life. The speciation within the rugosus group

appears to be closely associated with the uplift of the

Qinghai-Tibet Plateau.

Functional Outgroup Method

Our progressive functional outgroup method may

prove to be a powerful method for dealing with multi-

ple equally parsimonious trees, especially when levels

of homoplasy are relatively great, and the outgroup is

so distant from the in-group that mispolarization of

the character states is commonplace. When diver-

gences are great, and characters are constrained to

only a few possible alternative states, homoplasy may

be so rampant that there is very little resolving power

to the data when a taxonomic outgroup is used to

polarize character states. Selecting a closer sister

group, as in the use of FOGs, may prove particularly

beneficial for reducing this problem. Thus, the use of

FOGs might possibly result in the defensible selection

of a single most parsimonious tree when, otherwise, a

suite of equally parsimonious trees would be found.

The application of consensus tree methods has not

been recommended as a way of selecting among

equally parsimonious solutions, although this stance

has not been universally accepted (e.g., Wilkinson

1994). Our trial of this approach with the Oreolalax

data did not demonstrate high resolving power. The

strict consensus tree seeks the unambiguous nodes

appearing on all MPTs. It often results in a large num-

ber of unresolved nodes. A single taxon with ambigu-

ous relationships may cause the whole consensus tree

to be a total "bush". The Adams consensus method

improves this problem, but in both our case and in

others, it still frequently resolves ambiguous nodes. In

our case, strict and Adams consensus left 6 and 5

nodes unresolved respectively. Although the majority

rule consensus method often gives a more complete

solution, the percentage is arbitrary and it is doubtful

that all nodes reflect phylogeny.

Successive approximations weighting (Farris

1969) often reduces the number of cladograms to be

considered by restricting attention to the most consis-

tent characters, and hence the "best" evidence (Car-

penter 1988). Consequently, some ambiguous nodes

that are supported by the "best" evidence may get

resolved. However, the ambiguous nodes not sup-

ported by the suite of consistent characters will

remain unresolved. In our trials, SAW resolved three

equally parsimonious solutions. The ambiguous posi-

tion of O. popei and O. omeimontis is responsible for

these three trees. Character 28, which clusters these

two taxa together under FOG analysis, was not

included in the "best" evidence; It received a weight-

ing value of 0 from the SAW analysis.

In our case, the high resolving power of FOG

analysis results from the changing of the character

state polarizations. Some symplesiomorphies which

Vol. 7. p. 42

Asiatic Herpetological Research

1997

are useless in providing evidence of common ancestry

became synapomorphies after re-polarization. How-

ever, we believe that the revised data result in a better

solution. For example, the polarity of the states of

Character 28, changes after using O. rhodostigmatus

as the FOG. Unlike in our initial analysis, a derived

state united O. popei. O. omeimontis and O. liang-

beiensis. Similarly, after using O. lichuanensis as our

FOG, the polarities of the states of Character 24

changed such that a synapomorphy united O. schmidti

and O. puxiongensis with O. major.

Evolution of the Characters

Among the 29 characters used by Xu et al., 10 con-

tributed no information to the phylogeny. Characters

7. 11. 1 2. 22 have autapomorphic states and hence are

phylogenetically uninformative. The derived states of

characters 1. 13. 20. 23. and 24 were resolved as inde-

pendent "gains" (parallelism). Character 28 was inter-

preted to be two independent reversals. Conversely.

19 characters showed clear evolutionary trends when

mapped on our preferred tree. However, although

characters 2, 3, 4. 5. 6. 8. 9. 10. 14. 15. 16. 18. 19, 21,

26, and 27 evolved from state 0 to 1, characters 17,

25, 29 show a progression from state 1 to 0. These lat-

ter three characters are undoubtedly mispolarized by

Xu et al. if our tree reflects the genealogical relation-

ships of the taxa.

Acknowledgments

This work is supported by Natural Sciences and Engi-

neering Research Council of Canada grant No. A3 148

to RWM, and No. OGP46464 to K. Coates. Amy

Lathrop generously assisted with the preparation of

the figures.

Appendix I

The Characters used by Xu et al (1992)

1. Quadratojugal either long, overlapping with max-

illa (O). or short, not overlapping the maxilla.

2. Spoon-like cartilage either present (0), or absent

(1).

3. Columella either long (0). or reduced as a small

projection ( 1 ).

4. Tympanum either present (0). or absent ( 1 ).

5. Tympanic annulus either large. diameter>1.9 mm

(0), or either small, diameter<1.3 mm, or absent

(1).

6. Post-otic projection of squamosal either present (0),

or absent ( 1 ).

7. Ilium either short (0), or long ( 1 ).

8. Body length of males either greater than 65 mm (0),

or less then 56 mm ( 1 ).

9. Opening of Eustachian tube either large (0), or

small ( 1 ).

10. Tympanic status either obvious (0), or hidden

(1).

1 1. Dorsal skin either smooth (0). or warty and granu-

lar ( 1 ).

12. Skin groove along posterior area of the dorsum

either absent (0), or present ( 1 ).

13. Belly skin either smooth (0), or granular ( 1 ).

14. Colour pattern on belly either present (0). or

absent ( 1 ).

15. Triangular pattern between eyes either absent (0),

or present ( 1 ).

16. Toes either webbed (0), or either not webbed or

only a trace ( 1 ).

17. Vocal sac either present (0), or absent ( 1 ).

18. Spines in lip margins either absent (0), or present

(1).

19. Spinal patches on the chest either small (0), or

large ( 1 ).

20. Spines on the chest either small (0). or large ( 1 ).

21. Nuptial spines on fingers either small (0), or large

(1).

22. Spinal patches on the ventral surface at the base of

the upper arm either absent (0), or present ( 1 1.

23. Spinal patches on the inner side of the lower arm

either absent (0). or present ( 1 ).

24. Spinal patches on the back of the upper arm either

absent (0). or present ( 1 ).

25. Linea musculinae either absent (0), or present ( 1 ).

26. Labial tooth formula of tadpole either 1:7-7/1:7-7

or more (0), or 1 :6-6/l :6-6 or less ( 1 ).

27. Papillae of tadpole nostril more than one circle

clear (0), or only half circle clear ( 1 ).

28. Number of eggs laid either more than 280 (0), or

less than 220 ( 1 ).

29. Egg pigment, either present (0), or absent ( 1 ).

1997

Asiatic Herpetological Research

Vol. 7. p. 43

Apendix II

Coded Data set from Xu et al. (1992). A hypothetical ancestor (HA) was added for analysis.

HA

O. popei

<> chuanbeiensis

O. major

O. schmidti

O. omeimontis

O. puxiongensis

O. lichuanensis

0. rhodostigmatus

O. liangbeiensis

O. pingii

O. ntgosus

O. xiangchengensis

O.jingdongensis

O granulosus

00000 00000 00000 00000 00000 0000

10000 001 II 0000001 Kil 10000 0001

00001 001 1 I 00010 01 100 00010 101 I

00000 00011 001 10 01 I HI 00000 1111

10000 001 1 1 0001 1 1 1000 10001 1 I 1 1

00000 00101 00001 10100 10101 0001

00000 00111 00111 11000 11001 1110

oooooooioioooooonoi loin mi

00000 01000 00000 01000 10001 001 1

00001 00111 00010 01 100 00000 1101

oooooooin lioioonoo loon mi

01111 10111 00000 01100 00000 11-0

01111 ooill 0000001110 00000 1110

0101 1 101 1 1 00001 01 101 10000 1 I 10

01 I II 10111 00000 01110 00010 1011

Literature Cited

Adams. E. N. 1972. Consensus techniques and the

comparison of taxonomic trees. Systematic Zoology

21:390-397.

Carpenter. J. M. 1988. Choosing among multiple

equally parsimonious cladograms. Cladistics 4:291-

296.

Faith, D. P.. and P. S. Cranston. 1991. Could a da-

tagram this short have arisen by chance alone?: On

permutation tests for cladistic structure. Cladistics

7:1-28.

Farris, J. S. 1969. A successive approximations

approach to character weighting. Systematic Zoology

18:374-385.

Farris. J. S. 1988. Hennig86, version 1.5. Distrib-

uted by the author. Port Jefferson Station. N. Y.

Farris. J. S. 1989. The retention index and rescaled

consistency index. Cladistics 5:417-419.

Felsenstein. J. 1985. Confidence limits on phytoge-

nies: an approach using the bootstrap. Evolution

39:783-791.

Hendy. M. D., and D. Penny. 1982. Branch and

bound algorithms to determine minimal evolutionary

trees. Mathematical Biosciences 59: 277-290.

Kluge, A. G.. and J. S. Farris. 1969. Quantitative

phyletics and the evolution of anurans. Systematic

Zoology 18:1-32.

Maddison, W. P.. and D. R. Maddison. 1992. Mac-

Clade: Analysis of Phylogeny and character evolution.

Sinauer, Sunderland. Massachusetts.

Watrous. L. E.. and Q. D. Wheeler. 1981. The out-

group comparison method of character analysis. Sys-

tematic Zoology 30: 1-11.

Wilkinson. M. 1994. Common cladistic information

and its consensus representation: reduced Adams and

reduced cladistic consensus trees and profiles. Sys-

tematic Biology 43:343-368.

Wu, G.. E. Zhao. R. F. Inger and H. B. Shaffer. 1993.

A new frog of the Genus Oreolalax (Pelobatidae)

from Sichuan. China. Journal of Herpetology 27:410-

413.

Xu. N.. G.Wei. L. Fei. C. Ye and D. Li. 1992. [Study

on the phylogenetic relationship between species of

genus Oreolalax (Amphibian: Pelobatidae)]. Acta

Herpetologica Sinica Vol. 1 and 2:40-49 (In Chinese).

Zhao. E.. and K. Adler. 1993. Herpetology of China.

Society for the Study of Amphibians and Reptiles.

522 pp.

1997

Asiatic Herpetological Research

Vol. 7, pp. 44-^7

Helminths of Tago's Brown Frog, Rana tagoi tagoi (Ranidae), from Japan

Stephen R. Goldberg1, Charles R. Bursey2 and Quynh A. Truong1

1 Department of Biology, Whittier College, Whittier, California 90608, USA

2 Department of Biology. Pennsylvania State University, Shenango Valley Campus. 147 Shenango Avenue,

Sharon, Pennsylvania 16146, USA

Abstract. -Of 32 Rana tagoi tagoi. 22 (69% prevalence) harbored helminths. One cestode Cylindrotaenia

japonica (prevalence 25%, mean intensity 3.4). three nematodes Cosmocerca japonica (prevalence 53%, mean

intensity 3.1), Oswaldocruzia socialis (prevalence 3%. mean intensity 1.0), Rhahdias nipponica (prevalence

22%, mean intensity 2.9) and an acanthocephalan, Acanthocephalus lucidus (prevalence 22%, mean intensity

4.7) were found. Rana tagoi tagoi represents a new host record for Cylindrotaenia japonica. Cosmocerca

japonica. Oswaldocruzia socialis and Rhahdias nipponica.

Ke\ words: Rana tagoi tagoi. Ranidae. Cylindrotaenia japonica. Cosmocerca japonica. Oswaldocruzia socialis.

Rhahdias nipponica. Acanthocephalus lucidis. Japan

Introduction

Tago's brown frog, Rana tagoi tagoi Okada, 1928 is

known from Honshu. Shikoku. Kyushu Islands, Japan

where it lives in montane regions (Maeda and Matsui.

1990). To date the only helminth known from R. t.

tagoi is the acanthocephalan, Acanthocephalus luci-

dus Van Cleave, 1925 reported by Uchida (1975).

With world-wide concern over declining amphibian

populations (Heyer et al.. 1994). possible negative

effects of parasites on frogs has become a topic of

interest; however, the helminth fauna are incompletely

known or has yet to be studied in many species of

amphibians. The purpose of this note is to report the

results of a helminth survey of R. t. tagoi.

Materials and Methods

Thirty two (25 males, 7 females) Rana tagoi tagoi

(mean snout- vent length 40.9 ± 6.2 SD. range 26-54)

were examined. Specimens were collected on Hon-

shu Island during the period June 1988-May 1995

between elevations of 160-800 m. Twenty-nine were

from Kanagawa Prefecture; seventeen from Tanzawa

(35°28"N, 139°10,E). eight from Hakone (35°12'N,

139°02"E), two from Hadano (35°22'N, 139°14"E)

and two from Kiyokawa (36°12'N, 138°30"E). Two

were from Shizuoka Prefecture; Gotemba (35°18"N.

138°56"E) and one was from Fukushima Prefecture,

Hinoemata (37°02-N. 139°24"E).

The body cavity was opened ventrally and the

esophagus, stomach, small intestine, large intestine.

lungs and urinary bladder were slit longitudinally and

examined under a dissecting microscope. The liver

and body cavity were also examined for helminths.

All helminths were identified utilizing a glycerol wet

mount. Selected cestodes were stained with hematox-

ylin and mounted whole in Canada Balsam. Frogs

were deposited in the herpetology collection of the

Natural History Museum of Los Angeles County

(LACM): Fukushima Prefecture LACM 141442;

Kanagawa Prefecture 141247-141251; 141426-

141440: 141443-141447; 141916; 141918-141920;

Shizuoka Prefecture 141441; 141917. Helminths

were deposited in the U.S. National Parasite Collec-

tion (Beltsville, Maryland 20705): Cylindrotaenia

japonica. 85329; Acanthocephalis lucidus, 85333;

Cosmocerca japonica, 85330; Oswaldocruzia socia-

lis. 85332; Rhahdias nipponica. 85331. Terminology

usage is in accordance with Margolis et al. ( 1982).

Results and Discussion

Twenty two of 32 (69% prevalence) frogs were

infected by helminths (Table 1 ): 19 of 25 males (76%

prevalence) and 3 of 7 females (43% prevalence).

However, there was no significant difference for prev-

alence of infection between males and females (Chi-

square statistic = 0.58, 1 df, P > 0.05). None of these

parasites are unique to R. t. tagoi.

Cylindrotaenia japonica (Yamaguti, 1938) Jones,

1987, a parasite of the small intestine, has been

reported only from anurans of the Japanese Archipel-

ago. Although nothing is known of its life cycle, Joy-

1997

Asiatic Herpetological Research

Vol. 7. p. 45

Table 1 . Helminth parasites of Tago's brown frog, Rana tagoi tagoi, from Japan.

Parasite

Prevalence Mean intensity Location

(%) (range)

Cestoda

Cylindrotaenia japonica

Nematoda

Cosmocerca japonica

Oswaldocruzia socialis

Rhabdias nipponica

Acanthocephala

Acanthocephalus lucidus

25

22

3.4(1-6)

4.7(2-8)

b

a

c

a = small intestine, b = large intestine, c = lungs.

eux (1924) considers the life cycle of Cylindrotaenia

americana Jewell. 1916 to be direct with infection

ocurring when a contaminated fecal pellet is swal-

lowed by a frog. Other hosts include Hyla japonica,

Rana japonica. Rana ornativentris, Rhacophorus

schlegelii and Rhacophorus viridis (Goldberg et al..

1994; Jones, 1987; Uchida. 1975).

Cosmocerca japonica Yamaguti, 1938, a parasite

of the rectum, has been reported in amphibians from

the Palearctic biogeographic realm. Hasegawa ( 1989)

suggested a synonymy of Cosmocerca japonica with

C. ornata (Dujardin, 1845) Diesing, 1861, which has

been found in all biogeographic realms except the

Nearctic and Australian; but further review is neces-

sary before this synonymy can be accepted. The life

cycle of C. japonica is not known; however, the life

cycle of Cosmocerca commutata (Diesing, 1851)

Diesing. 1861 was studied by Fotedar and Tikoo

(1968). Eggs hatched in 2-4 hours. Larvae penetrated

the skin of the host and migrated through the viscera

to reach the lungs 3 days postinfection and the rectum

10-14 days postinfection. Other hosts include Buer-

geria japonica, Bufo japonicus, Bufo melanostictus,

Cynops ensicauda, Hyla japonica, Microhyla ornata,

Polypedates leucomystax, Rana ishikawae, Rana

japonica, Rana linwocharis. Rami narina, Rana

nigromaculata, Rana ornativentris, Rana rugosa from

Japan (Goldberg et al., 1994; Hasegawa. 1989;

Uchida, 1975; Yamaguti. 1938; 1954): Bufo biporca-

tus, Limnonectes macrodon, Phrynoglossus laevis,

Rana cancrivora, Rana limnocharis, from the Philip-

pines (Schmidt and Kuntz. 1969); Bufo bufo, Bufo

melanostictus from Taiwan (Yamaguti and Mitunaga.

1943; Myers and Kuntz. 1970); Rana limnocharis

from Okinawa (Hasegawa, 1984); Rana kuhlii, Rana

limnocharis, Rana rugulosa from North Viet Nam

(Moravec and Sey, 1985).

Oswaldocruzia socialis Morishita. 1926. a para-

site of the small intestine, is apparently restricted to

Japan. Travassos (1937) synonymized O. insulae

Morishita. 1926 and O. socialis with O. filiformis

(Goeze. 1782) Travassos, 1917 which has wide distri-

bution in Europe: but further review is necessary

before this synonymy can be accepted. The life cycle

of O. insulae is not known, however Baker (1978)

reported that Oswaldocruzia pipiens Walton, 1929.

development to infective larvae occurred in fecal pel-

lets with transmission to new hosts by skin penetra-

tion. Other hosts include Rami japonica, Rana

nigromaculata (Uchida, 1975).

Rhabdias nipponica Yamaguti. 1935. a parasite of

the lungs, is known from Japan. South China and Viet

Nam. The life cycle of Rhabdias nipponica is not

known, but Baker ( 1979) has studied the life cycle of

Rhabdias americanus. Development of larvae to the

infective third stage was by matricidal endotoky.

Infection occured by skin penetration followed by

migration through tissue to body cavity and lungs.

Vol. 7. p. 46

Asiatic Herpetological Research

1997

Adults appeared 7-9 days postinfection. Other hosts

include Rana nigromaculata, Rana rugosa from

Japan (Uchida, 1975): Rana guentheri, Rana limno-

charis, Rana nigromaculata from South China (Kung

and Wu, 1945: Wang et al.. 1978): Rana rugulosa

from Viet Nam (Moravec and Sey, 1985).

Acanthocephalus lucidus, a parasite of the small

intestine, is apparently restricted to Japan. The life

cycle of Acanthocephalus lucidus has not been stud-

ied, but infection is most likely acquired by consump-

tion of an intermediate host, probably an insect

(Petrochenko, 1956). Other hosts include Bufo

japonicus, Buergeria buergeri, Rana japonica, Rana

nigromaculata, Rana ornativentris, Megalobatrachus

japonicus (Petrochenko. 1956: Uchida, 1975).

Uchida (1975) lists 15 anurans from Japan harbor-

ing on average 7.7 species of helminths: helminth

diversity ranges from a minimum of 1 species in Hop-

lohatrachus tigerinus to 26 species in Rana nigromac-

ulata. With 5 helminth species present, R. t. tagoi is

near the lower end of the diversity scale for Japanese

frogs. Subsequent examinations of/?, t. tagoi will be

needed before the full extent and impact of helminth

parasitism in this species is known.

Acknowledgments

We thank Tatsuo Ishihara (Hakone Woodland

Museum, Hakone) for the collection of/?, t. tagoi.

Literature Cited

Baker. M. R. 1978. Development and transmission of

Oswaldocruzia pipiens Walton. 1929 (Nematoda: Tri-

chostrongylidae) in amphibians. Canadian Journal of

Zoology 56:1026-1031.

Baker. M. R. 1979. The free-living and parasitic

development of Rhabdias spp. (Nematoda: Rhabdi-

asidae) in amphibians. Canadian Journal of Zoology

57:161-178.

Fotedar, D. N., And R. Tikoo. 1968. Studies on the

life cycle of Cosmocerca kashmirensis Fotedar. 1959.

common oxyurid nematode parasite of Bufo viridis in

Kashmir. Indian Science Congress Association Pro-

ceedings 55:460.

Goldberg. S. R.. C. R. Bursey, And I. Ramos. 1994.

Gastrointestinal helminths of the Japanese treefrog,

Hyla japonica (Anura: Hylidae), from Japan. Journal

of the Helminthological Society of Washington

61:225-227.

Hasegawa, H. 1984. Helminth fauna of five Oki-

nawan amphibian species. Biological Magazine Oki-

nawa 22:1 1-22.

Hasegawa, H. 1989. Nematodes of Okinawan

amphibians and their host-parasite relationship. Pp.

205-217. In M. Matsui, T Hikida. and R. C. Goris,

eds. Current Herpetology in East Asia. Herpetologi-

cal Society of Japan, Kyoto.

Heyer, W. R., M. A. Donnelly, R. W. Mcdiarmid. L. C.

Hayek. And M. S. Foster (Editors). 1994. Measuring

and monitoring biological diversity. Standard meth-

ods for amphibians. Smithsonian Institution Press,

Washington. D.C. 364 pp.

Jones, M. K. 1987. A taxonomic revision of the

Nematotaeniidae Luhe. 1910 (Cestoda: Cyclophyl-

lidea). Systematic Parasitology 10:165-245.

Joyeux, C. E. 1924. Recherches sur le cycle evolutif

des Cylindrotaenia. Annales de Parasitologic

Humaine et Comparee 2:74-81.

Kung. C. C. And H. W. Wu. 1945. Parasitic nema-

todes of amphibians from Pehpei Szechwan, China.

Sinensia 16:73-83.

Maeda. N. And M. Matsui. 1990. Frogs and toads of

Japan. Bun-Iehi Sogo Shuppan Co.. Ltd. Tokyo.

Japan. 207 pp.

Margolis. L.. G. W. Esch. J. C. Holmes. A. M. Kuris,

And G. A. Schad. 1982. The use of ecological terms

in parasitology (report of an ad hoc committee of the

American Society of Parasitologists). Journal of Par-

asitology 68:131-133.

Moravec, F, And O. Sey. 1985. Some nematode par-

asites of frogs {Rana spp.) from North Viet Nam. Par-

asitologica Hungarica 18:63-77.

Myers, B. J., And R. E. Kuntz. 1970. Nematode par-

asites of amphibians taken on Taiwan (Formosa).

Srivastava Communications p. 151-154.

Petrochenko. V I. 1956. Acanthocephala of domestic

and wild animals. Vol. 1. Translated from Russian by

Israel Program for Scientific Translations. Jerusalem,

1971.465 pp.

Schmidt. G. D.. And R. E. Kuntz. 1969. Nematode

parasites of Oceania. VI. Foleyella confusa sp. nov.,

Icosiella hoogstraali sp. nov. (Filarioidea). and other

species from Philippine amphibians. Parasitology

59:885-889.

Travassos, L. 1937. Revisao da familia Trichos-

trongylidae Leiper 1912. Monographias do Instituto

OswaldoCruz 1:1-512.

Uchida, A. 1975. Check list of the helminth parasites

of Japanese amphibians. Bulletin of the Azabu Veter-

inary Colleae 30:63-81.

1997

Asiatic Herpetological Research

Vol. 7, p. 47

Wang. P. Q.. Y. Zhao, And C. Chen. 1978. (On some

nematodes from vertebrates in South China.] Fujian

Shida Xuebao 2:75-90. (In Chinese).

Yamaguti. S. 1938. Studies on the helminth fauna of

Japan. Part 23. Two new species of amphibian nema-

todes. Japanese Journal of Zoology 7:603-607.

Yamaguti, S. 1954. Helminth fauna of Mt. Ontake.

Part 1 . Nematoda and Acanthocephala. Acta Medica

Okayama 8:386-392.

Yamaguti. S., and Y Mitunaga. 1943. Intestinal hel-

minths from Bitfo melanostictus of Formosa. Trans-

actions of the Natural History Society of Taiwan

33:142-154.

1997

Asiatic Herpetological Research

Vol. 7. pp. 48-50

A New Species Of Leptolalax (Anura: Megophryidae) from Borneo

Robert F. Inger1, Maklarin Lakim2, Alim Biun2, and Paul Yambun2

'Field Museum of Natural History, Chicago, Illinois 60605. USA; 2Sabah Parks, P.O. Box 10626, 88806 Kota

Kinabalu, Sabah, Malaysia

Abstract.- A new species of frog of the genus Leptolalax is described from high elevation in Sabah. northern

Borneo. The new species is remarkable for its small size and the large size of its ova.

Key words: Borneo. Amphibia. Salientia, Leptolalax

ft mm

Figure 1 . Dorsal view of holotype of Leptolalax mau-

rus, new species. The scale line equals 10 mm.

Introduction

Sabah Parks (Sabah. Malaysia) has initiated a pro-

gram monitoring populations of amphibians at three

sites at differing elevations in Kinabalu Park. One of

these sites is at Mesilau (1850-1950 m, 6°04'N/

1 16°34'E), southeast of the peaks. At this elevation,

the vegetation changes from lower montane to upper

montane and the climate is temperate in Koppen's sys-

tem with mean temperature near 16.5° (Kitayama,

1992).

During the course of our initial survey at this site,

we collected a gravid female, which we describe

below as the holotype of a new species of Leptolalax.

On our next visit to the same site, we found an addi-

tional adult, one juvenile and two metamorphosing

individuals of the same species. This is not the first

Leptolalax to be found at montane elevations in

Borneo. Leptolalax dringi Dubois was collected at

1800 m on Mt. Mulu. Sarawak (Dubois. 1987). and L.

dringi and L. pictus Malkmus at 1230-1560 m in

Sabah (Inger et al., 1995). However, as will be

detailed below, the Mesilau species is smaller than

any other yet found in Borneo, has larger ova and

smaller clutch than females of other Bomean species,

and has a distinct coloration.

Material and Methods

The specimens were preserved in 10% formalin after

being euthanized and transferred to 70% ethanol after

four days. Comparisons with other species of Lepto-

lalax were made using the collections of Field

Museum (FMNH) and by reference to Dubois ( 1983.

1987). We use the following abbreviations: SVL.

snout-vent length; T, tibia length: HW. head width:

HL, head length; TYM. diameter of tympanum.

Leptolalax maurus new species

Material examined. -Holotype: Sabah Parks 2531, an

adult female, collected by the authors July 1, 1995, at

Mesilau Station. 1860 m. Kinabalu Park. Sabah, in

floor litter of oak-chestnut forest (Fig. 1 ).

Paratypes: FMNH 252425-26, Sabah Parks 2305-06,

one male, one juvenile, and two stage 45 metamor-

phic individuals.

Diagnosis. -A small species of Leptolalax. adult

female 32 mm, male 26 mm SVL: dorsal and ventral

surfaces dark, dorsally without visible pattern, belly

with narrow network of small light spots; underside of

hind limb dark; a superficial, round pectoral gland.

Description-Habitus moderately stocky, width of

head and body subequal. Snout obtusely pointed,

rounded in profile, not projecting; nostril lateral.

slightly nearer tip of snout than to eye; canthi distinct,

weakly constricted; lores weakly sloping, concave;

diameter of eye slightly longer than length of snout:

interorbital equal to eyelid, slightly wider than inter-

narial: tympanum visible, slightly more than half

diameter of eye; no vomerine teeth. Finger tips

1997

Asiatic Herpetological Research

Vol. 7, p. 49

rounded; first finger shorter than second; no subarticu-

lar tubercles, but long cornified strips under fingers, a

large inner palmar tubercle, a much smaller one at

base of fourth finger. Tips of toes like those of fin-

gers; third toe longer than fifth; toes webbed at base

only; subarticular tubercles replaced by long strips of

cornified tissue; low, oval inner metatarsal tubercle,

no outer one; heels overlapping when limbs are

flexed. Back with many low. rounded tubercles,

homogeneous in shape and size; sides with more ele-

vated, round tubercles: similar but smaller tubercles

on limbs; a strong angular supratympanic fold: ventral

surfaces smooth; a large superficial, circular, pectoral

gland on each side, gland diameter 1.8-2.5 mm.

Color in life almost black without visible pattern

dorsally; limbs slightly lighter, with dark crossbars;

sides black with light dots, reddish ventrolateral^ in

one individual; venter black or dark gray brown, with

indistinct small light areas; limbs ventrally dark olive

brown to black. In preservative dark purplish brown

dorsally. without visible pattern; obscure crossbars on

calf; sides dark brown, with small light spots (ca. size

of finger tips); venter dark brown with narrow net-

work of small light spots on belly; entire underside of

hind limb dark brown.

Measurements (mm) of holotype: SVL 31.8, T

15.9. HW 10.7, HL 13.0. TYM 2.7. interorbital 3.3.

Variation.-Male paratype: SVL 26.1. T 12.3. TYM

2.2, interorbital 3.3. Male with very large testis, but

no vocal sac opening visible. Newly transformed

frog: SVL 20.6, Tl 1.0, HW 7.4. HL 8.2. Metamor-

phosing individuals in stage 45: 20.4. 22.0. tail

lengths 27.0, 18.2. respectively. The light network on

the venter of the stage 45 frogs is wider than in the

others, but still occupies less than 20% of the total

area.

Female with 45 large, white ova in left ovary; ova

1.83-2.33 mm (13 measured).

Etymology. -maur us, from mauros, Greek, meaning

dark.

Comparisons -The new species differs from all pre-

viously known Bornean Leptolalax in size, skin sur-

face, coloration, pectoral gland, and size and number

of ova. The size range of females of other Bornean

species is 36.1-48.3 mm (n=77) and of males 28.7-

38.9 m (n=136) (Inger et al., 1995). compared to 31.8

(female) and 26.1 (male) in L. maurus. The back and

sides of L. maurus are covered with homogeneous,

round tubercles; in two of the other Bornean species

[L. pictus and "unspotted Sarawak" (Inger el al.,

1995)] the dorsal skin is smooth and in the two others

(L. gracilis and L. dringi) the dorsal tubercles are het-

erogeneous in size and smaller than those on the

sides.

Leptolalax maurus is the darkest of the Bornean

species of the genus. It is the only species that is uni-

formly dark brown on the ventral surface of the head

and hind limbs, and the only one in which no dark

pattern is evident on some portion of the dorsal sur-

face. It is also the only Bornean species with a con-

spicuous, superficial, round pectoral gland. A

pectoral gland is usually present in the other species,

but the skin must be cut and rolled over before the

gland becomes visible on the interior surface.

Leptolalax maurus also differs from the three cur-

rently recognized species (Dubois, 1983) from South-

east Asia. L. pelodytoides (Boulenger), L. heteropus

(Boulenger), and L. bourreti Dubois, in having a very

heavily pigmented belly and in lacking distinct dorsal

markings. The new species is much smaller than L.

bourreti I SVL males 36 mm, females 42-45 (Dubois,

1983), but similar to the other two in size.

The enlarged but not yet ovulated ova of L. mau-

rus are distinctly white; ova in the same stage of

development are yellow in the other Bornean species

and in L. pelodytoides. The left ovary of L. maurus

had 45 enlarged ova, compared to 1 12-210 in L. gra-

cilis (n= 1 ). dringi (2), pelodytoides ( 1 ) and pictus (2).

Mean diameter of 10 large ova in each of the last four

species ranged from 1.60±0.027 to 1.78±0.050 mm;

in L. maurus the mean of 13 ova was 2.0±0.049. The

volume of ova in the left ovary (ovum volume, based

on mean ovum diameter, times number of ova) for L.

gracilis, dringi. pelodytoides. and pictus varied from

255.5 to 542.3 mm3, but only 188.5 mm3 in L. mau-

rus. However, if the cube root of ovarian volume is

divided by SVL of females to obtain a relative mea-

sure of ovarian volume, there is very little difference

among the species; the ratio of cube root of ovarian

volume to SVL varies from 0. 1 52 to 0. 1 79 in L. graci-

lis, dringi. pelodytoides. and pictus and 0.180 in mau-

rus. Although relative reproductive effort measured in

this manner is approximately the same in all these

species, the division of the material into ova is quite

different in L. maurus. The enlargement of ova in the

high altitude species L. maurus is consistent with the

general trend in other Bornean anurans. The montane

frogs listed by Inger and Stuebing (1992) include a

high proportion with enlarged ova: species of Philau-

tus and Pelophryne with direct development and spe-

cies of Ansonia with normal larval development.

Together, species of those three groups compose 50%

of the montane frog fauna of northwestern Borneo.

Vol. 7, p. 50

Asiatic Herpetological Research

1997

Acknowledgments

We are grateful to Tan Fui Lian for preparing the illus-

tration. Field work was supported by Sabah Parks and

a grant from the John D. and Catherine T. MacArthur

Foundation.

Literature Cited

Dubois, A. 1983. Note preliminaire sur le genre Lep-

tolalax Dubois, 1980 (Amphibiens, Anoures), avec

diagnose d'une espece nouvelle du Vietnam. Alytes

4:147-153.

Dubois. A. 1987. Miscellanea taxinomica batracho-

logica(I). Alytes 5:7-95.

Inger. R. F. and R. B. Stuebing. 1992. The montane

amphibian fauna of northwestern Borneo. Malayan

Nature Journal 46:4 1-51.

Inger. R. F. R. B. Stuebing. and Tan F.-L. 1995. New

species and new records of anurans from Borneo.

Raffles Bulletin of Zoology 43: 1 1 5- 131.

Kitayama. K. 1992. An altitudinal transect study of

the vegetation on Mount Kinabalu. Borneo. Vegetatio

102:149-171.

1997

Asiatic Herpetological Research

Vol. 7, pp. 51-60

Taxonomic Notes on Pakistani Snakes of the Coluber karelini-rhodorachis-

ventromaculatus Species Complex: A New Approach to the Problem

Muhammad S. Khan

Herp Laboratory, 15/6 Darul Saddar North. Rabwah 35460, Pakistan.

Abstract. -Taxonomic characters used for definition of Pakistani species of Coluber snakes are analyzed and

discussed. New combinations of characters are used to devise a key for identification of Pakistani snakes of the

genus Coluber. Zoogeographical distribution is discussed.

Kev words: Taxonomy, Coluber karelini-rhodorachis-ventromaculatus species complex, Pakistan.

Introduction

The taxonomic status of Pakistani racers belonging to

the genus Coluber (C. ventromaculatus Gray and

Hardwicke 1834, C. karelini Brandt 1838 and C.

rhodorachis) Jan 1865, has long remained enigmatic

to herpetologists (Minton, 1966; Mertens, 1969; Khan

1982). Despite the problematic taxonomy of C.

ravergieri in the circum-Mediterranean region (Bou-

lenger, 1893; F. Werner, 1905; Mertens. 1952; Baran.

1976; Bannikov et al., 1977; Schatti and Agasian,

1985), it is readily differentiated from its Pakistani

congeners by 21 midbody scale rows (Khan. 1982).

However, C. karelini. C. rhodorachis and C. ventro-

maculatus. due to their dubious color variations and

overlapping scale counts, have always posed taxo-

nomic problems to the herpetologists working in Mid-

dle East and southeast Asia (Clark et al., 1969;

Leviton, 1959; Leviton and S. Anderson. 1969, 1970;

Minton, 1966; Mertens, 1969; Haas and Y. Werner,

1969; Khan. 1977, 1982; Latifi, 1991; Tiedemann.

1991; Leviton et al., 1992).

The present work has been undertaken to assess

the validity of various morphological characters

which have usually been used to define these colubrid

taxa. New combinations of readily observable mor-

phological characters are suggested for identification

of these species, gathered from the material coming

from different parts of Pakistan and Azad Kashmir.

Materials and Methods

For this study a total of 27 C karelini. 92 C. rhodora-

chis and 142 C. ventromaculatus. from different parts

of Pakistan and Azad Kashmir, were available. States

of the following morphological characters, usually

used in the taxonomic determination of these snakes,

were recorded for each species: i. Measurements:

total length (from anterior tip of snout to the posterior

tip of tail); body or snout-vent length (from anterior

tip of snout to anterior lip of anal aperture); tail length

(from posterior lip of anal aperture to the tip of tail);

head length (from anterior tip of snout to posterior

margin of the last supralabial); head width (at the

level of last supralabials across head), were recorded

to the nearest 0.1 mm. ii. Snakes under 500 mm total

length are taken as juveniles, up to 750 mm subadults,

and above, adults, iii. Scutellation: number of scale

rows at midbody and just anterior to vent were

counted on both sides of the same ventral; pre- and

postsuboculars lie below the level of eye; first broader

than long scale in the gular region was counted as the

first ventral, and the preanal scale is not counted, iv.

Color pattern: For description of dorsal body pattern,

formed by the deposition of sooty pigment. Fig. 1 1

and 1 A (Peters, 1964) and Fig. 27 (Khan, 1993a) were

followed, v. For hemipeneal study three Coluber ven-

tromaculatus , one C. rhodorachis are available with

fully everted hemipenes. However, for additional

comparative material for these species and for C.

karelini, the technique suggested by Pesantes (1994)

was used to evert the organ of preserved specimens.

Description of the organ follows Dowling and Savage

(1960) and Khan (1993b).

Characteristics of Pakistani Coluber snakes

Long, narrow, cylindrical body with distinct elongated

head, long tail with very gradual taper with a fine tip.

Head with large, symmetrically arranged scales; ros-

tral strongly hollowed underneath, a pair of interna-

sals and prefrontals; single supraorbital and frontal, a

pair of parietals, single loreal, 1-2 pre- and postocu-

lars. 1-2 pre- and postsubocular, upper preocular in

contact with frontal; 9 supralabials, 1-2 in contact

with eye; frontal broad, elongated, parietals broad and

elongated; temporals 2+3 or 3+3. Genials 2, posterior

longer, separated from each other by small scales;

Vol. 7, p. 52

Asiatic Herpetological Research

1997

Figure 1. Coluber karelini. A. Dorsal head scales; B.

Lateral head scales.

eyes large, with distinct round pupil. Snout project-

ing, distinct canthus, a pair of nasals. Body scales

smooth, 19-21 at midbody. reduced to 11-13 at vent,

anal divided; ventrals rounded, ranging 192-277; sub-

caudals paired, ranging 82-145; hemipenis is simple

with single sulcus spermaticus, distal portion calcu-

late, proximally spinose, spines enlarged.

Evaluation of Characters used in Coluber tax-

onomy

Various morphological characters have been used in

different combinations for Taxonomic determination

of Pakistani Coluber racers. In the following section

these characters are examined in the light of the data

collected from present collections:

i. Circumocular scales: Basic circumocular scalation

consists of one supraocular, one preocular and two

postoculars. Usually one supralabial. the fifth,

touches orbit in C. karelini (Fig. lb), while two

supralabials, 5th and 6th (rarely 4th and 5th) touch the

orbit in both C. rhodorachis and C. ventromaculatus.

Circumocular conditions are complicated by the

appearance of a presubocular or a postsubocular scale

preventing either 4th or 5th, rarely 6th supraocular to

come in contact with orbit, so that one. two, three, or

none of the supralabials comes in contact with orbit

and conditions like that seen in C. karelini may appear

in C. rhodorachis and C. ventromaculatus (Bannikov

et al., 1977; Gasperetti, 1988). Rarely, presubocular

and postsubocular are fragmented in 3-4 scales at

loreal and postocular region.

Table 1 summarizes different circumocular states

observed in the present collection: in 97% C. karelini

5th supralabial is in contact with orbit on both sides,

Table 1 . Variations in circumocular scutellation of

Pakistani colubrid snakes: (1= C. karelini; 2= C.

rhodorachis; 3= C. ventromaculatus. Note: fig-

ures with oblique represent bilateral configura-

tions, while those in parentheses represent

number of specimens of each species present in

present collection).

3% have 5th on one side and 5th and 6th on the other,

one specimen has none in contact on one side, one on

the other. More variation is observed in C. rhodora-

chis and in C. ventromaculatus.

ii. Number of ventrals and suhcaudals: Ventral and

subcaudal counts overlap in these snakes; however, C.

rhodorachis is recognized due to its high subcaudal

counts ( 139-144). well above range of C. karelini and

C. ventromaculatus. To make ventral and subcaudal

counts taxonomically more meaningful. Mertens

( 1969) and Leviton ( 1986) computed ventrals together

with subcaudals to single out C. rhodorachis. where

low ventral counts for this species may overlap high

counts for the other two species (Table 2).

iii. Number of dorsals anterior to vent: Nineteen mid-

body scale rows, in C. karelini and C. ventromacula-

tus, are reduced to 13 just anterior to vent and 10-13

in C. rhodorachis. A clear distinction between these

taxa, on this basis, is not possible.

iv. Loreal scale: Shape of loreal scale has been con-

sidered a taxonomically important character (Smith,

1943; Khalaf, 1959). In C. karelini the loreal scale is

almost squarish to triangular (Fig. lb), while in C.

rhodorachis and C. ventromaculatus it is usually

longer than high, rarely squarish.

v. Hemipenial morphology: Typically, the hemipenis

is a simple single-lobed cylindrical organ, with a

1997

Asiatic Herpetological Research

Vol. 7, p. 53

Table 2. Range of ventral (V) and subcaudal (Scd) counts in Coluber species in present collection.

Taxon

Scd

V+Scd

90-11

139-144

82-119

282-317

344-42 1

277-339

Table 3. Distribution of sex in a collection of C. karelini, C. rhodorachis, and C. ventromaculatus from

Pakistan.

Sex

C. ventromaculatus

Sample size

Males

Females

Undetermined:

Juveniles

Damaged

142

95

32

median sulcus spermaticus. Distally, the organ is

calyculated with deeply scalloped cups fringed with

spines, while the proximal portion is spinose with sev-

eral rows of large proximally curved spines extending

to the organ's base, with several transverse rows of

much smaller scales at the middle. In C. karelini the

calyculated part is more extended, and cups are much

longer than broad, more deeply scalloped, and are

fringed with much longer spines. The proximal spiny

half of the organ merges abruptly into the distal caly-

culated half. On the other hand, cups in C. rhodora-

chis and C. ventromaculatus are shallower, squarish,

fringed with smaller spines and the proximal spiny

portion gradually merges with the scalloped distal

part through spines, which gradually decrease in size.

Males predominate in our collections of these

snakes from Pakistan (Table 3).

vi. Extension of rostral scale: The dorsal part of the

rostral scale is more acutely pointed behind and raised

in C. ventromaculatus, and extends between interna-

sal scales to almost 1/4 of the internasal suture, while

in C. karelini and C. rhodorachis it is not raised and is

broadly rounded off, just touching the internasal

suture (Fig. la).

vii. Number of temporals: Usually the temporal for-

mula for these snakes is 2+3+3, however. 1+2+3.

2+2+3 and 1+3+3 temporal counts unilaterally or

bilaterally are recorded in all the species.

viii. Dorsal body pattern: There is no marked differ-

ence between adult and juvenile patterns in C. karelini

and C. ventromaculatus except size of spots and

blotches; however, adult/juvenile differences are quite

marked in C. rhodorachis.

The head of C. karelini is relatively light in color,

with slight darkening of supralabials and internasals,

while the head of C. rhodorachis is more melanistic

and dark mottling is not discernible. The head of C.

ventromaculatus is lighter with distinct dark-brown

mottlings at the supralabials. frontal and parietals.

The suboculo-labial and a postoculo-temporal stripe

is vividly marked in C. karelini (Fig. 1A, B), hardly

discernible in C. rhodorachis and well marked in C.

ventromaculatus.

Grayish, pale-gray, buff, sandy, pale, reddish-

brown, brownish and greenish body hues have been

reported for these snakes by different herpetologists.

The basic body color is due to the deposition of

minute dots of different colors, to which additional

sooty-black pigment is deposited in three specific pat-

terns (Khan, 1993a).

In C. karelini the sooty pigment is uniformly

deposited on the whole scale, resulting in the vivid

dorsal pattern in this snake. It consists of a median

Vol. 7, p. 54

Asiatic Herpetological Research

1997

Figure 2. Pigmentation of dorsal pattern. A. Coluber

karelini; B. Coluber rhodorachis; C. Coluber ventro-

maculatus

Figure 3. Coluber karelini

Figure 4. Coluber rhodorachis

Figure 5. Coluber ventromaculatus

row of vivid sooty-black transverse bars extending

from nape to base of tail. In the anterior half of the

body, the bars are 2-3 scales thick, narrower than

interspaces, occupying 10-11 median rows of dorsals,

alternating with a transversely enlarged lateral row of

spots, the bases of which touch tips of adjacent ven-

trals (Fig.2A). Ventrum is spotless ivory.

In C. ventromaculatus the fine dark brown dots are

uniformly deposited on the scales, more densely on

scales of dorsal pattern while sooty pigment is rare. A

median row of squarish or rectangular blotches or sad-

1 997

Asiatic Herpetological Research

Vol. 7, p. 55

Figure 6. Geographic distribution of Coluber ravergieri ( + ), Coluber karelini (o). Coluber rhodorachis (O).

Coluber ventromaculatus ( )

dies is characteristic of this species. The blotches are

broader than interspaces, occupying 8-9 median dor-

sal scale rows, alternating with a pair of lateral rows

of spots, the outermost row is just of dark specks

which occasionally touch edges of corresponding

ventrals. Here the sooty pigment is deposited on the

periphery of the scales, leaving their centers clear,

resulting in a dull pattern (Fig. 2C). A distinct 6-9-

scale long. 2-4-scale thick nuchal blotch or stripe is

characteristic of this species, this mark generally

flanked by a large blotch on temporals. In specimens

from the Middle East, the nuchal stripe is long and

thin, occupying half scales of the median dorsal pair

of scales. Ventrum is ivory white, with occasional lat-

eral spots on ventrals.

In juvenile C. rhodorachis, the anterior half of the

body is lighter with distinct 4-5 alternating rows of

dark irregular blotches or spots, replaced in the poste-

rior, darker half by a mosaic of close-set vertical nar-

row, dark streaks. The streaked pattern is due to a

concentration of pigment between adjacent rows of

scales, creating a light/dark zigzag mosaic pattern

(Fig. 2B), ventrum melanistic, due to deposition of

pigment between ventrals.

Adult C. rhodorachis are more melanistic anteri-

orly, while the posterior half, which appeared darker

in juveniles, now appears lighter. Juvenile spotted

pattern is either lost altogether in darker adult speci-

mens as is usual in snakes from Kashmir (Khan,

unpublished data: Murthy and Sherma. 1976; 1979),

or is replaced by fine light/dark streaked mosaic pat-

tern as in snakes from Baluchistan (Mertens.

1969. Fig. 17). Ventrals, in adults, are ivory, except for

occasional lateral spottings.

ix. Geographical distribution (Fig. 6): Racers are noc-

turnal, alert and shy snakes. They generally prefer

Vol. 7, p. 56

Asiatic Herpetological Research

1997

open semidesert country with sparse grass and

scrubby vegetation. They are widely distributed from

Transcaspia to Transcaucasia in the north, to the Afri-

can Sahara in the west, extending in the east to Kash-

mir and Nepal, and descending through the Indo-

Gangetic plains into the Indian peninsula in the south.

Coluber ravergieri is a wide-ranging Central

Asian species, extending from the Turanian Plateau to

the Anatolian highlands in the west, through Turkey.

Israel. Jordan, northern Egypt, Iraq. Iran, and Afghan-

istan. It reaches the western border of Pakistan at its

eastern limit of distribution.

Coluber karelini is widely distributed in the Mid-

dle East, from the Turanian Plateau to the Kazakh

uplands in the north, entering Afghanistan, and

extending south to the low hills of the Quetta-Pishin

area in Baluchistan (Khan. 1980. 1987).

Coluber rhodorachis is the most wide-ranging

Saharo-Sindian racer, extending from Algeria to the

western and northwestern highlands of Pakistan

through Egypt, Ethiopia. Arabian Peninsula. Iraq.

Kuwait, Iran, and extending northwards to the Aralo-

Caspian region and Afghanistan. In Pakistan it is

widely distributed in Baluchistan to the Makran coast,

extending through Waziristan into the Siwaliks in

Kashmir, Utter Pardesh. India to Nepal.

Coluber ventromaculatus is primarily an Indian

species. It is widely distributed in the Indo-Gangetic

plains and does not extend west of the Indus. I regard

all reports of this snake from Iran and Iraq as pertain-

ing to local races of C. rhodorachis with low ventral

and subcaudal counts.

Coluber karelini, C. ravergieri, and C. rhodora-

chis are sympatric in most of their northern Caucaso-

Turanian and Afghanistan range. However, in the

Saharo-Sindian belt C. ravergieri is primarily a north-

ern species, while C. rhodorachis is a southern form

extending to northern Somalia. In Pakistan C. kare-

lini is sympatric with C. ravergieri and C. rhodora-

chis in western Baluchistan, while C. ventromaculatus

is in sympatry with C. rhodorachis in northern, north-

western and coastal foothills (Fig. 6).

Diagnoses of Pakistani species of Coluber

Coluber ravergieri Menetries, 1832

Diagnosis:

i. Midbody scale rows 21, reduction to 15 just anterior

to vent.

ii. Dorsum buff or grayish with a dorsal series of dark

rhomboidal spots or narrow cross-bars alternating

with a series of smaller spots on sides.

iii. Temporals 3+3.

iv. Ventrals 197-234. subcaudals 82-101.

Distribution in Pakistan (Figure 6): Central Asian:

reaches western Baluchistan and northwestern hills in

N.W.F.P. collected at 3.000 to 5,000 m elevation.

Coluber karelini Brandt. 1838 (Figures 2 A, 3)

Diagnosis:

i. Midbody scale rows 19. reduction to 12-13 just

anterior to vent.

ii. Vivid sooty pigment is uniformly deposited on

scales of the dorsal pattern (Fig. 2A).

iii. Dorsal pattern vivid, consisting of a median row

of black crossbars, narrower than interspaces, alter-

nating with a lateral row of spots touching ventrals.

iv. Vivid oculo-labia] and oculo-temporal stripes

always present.

v. Almost always 5th (rarely 6th or 5th. 6th, or none)

supralabial in contact with orbit.

vi. Ventrals 192-207. subcaudals 90-1 10.

Distribution in Pakistan (Fig. 6): From Transcaspia

to low hills of Quetta-Peshin area, at an elevation of

1600-1840 m; does not extend eastward into Sind and

Punjab.

Remarks: Often C. rhodorachis is confused with this

taxon due to occasional occurrence of C. rhodorachis

with one supralabial in orbit and dorsal row of lighter

cross bars. Specimens are illustrated by Gasperetti

(1988. Fig. 29) from Afghanistan and Nushki (Bal-

uchistan); specimens from this region have neither

dorsal pattern nor orbito-labial and temporal stripes as

vivid as observed in C. karelini from Quetta-Peshin,

Baluchistan. Mertens (1969) erected his C. karelini

mintonorum on similar C . rhodorachis from the Bal-

uchistan highland. In southern Turkmenistan, C.

karelini is known to hybridize with C. rhodorachis

(Bannikovetal.. 1977).

Coluber rhodorachis Jan, 1865 (Figures 2B, 4)

Diagnosis:

i. Midbody scale counts 19. reduced to 11-13 at the

level of vent.

ii. Colored dots are uniformly deposited on dorsal

scales, while the dorsal pattern is formed by concen-

tration of colored dots, however, melanicity of older

snakes is due to additional deposition of sooty pig-

ment (Fig. 2B).

iii. Juvenile pattern is of spots on anterior part of

body, unicolor or streaked posteriorly; venter melanis-

tic. Adults become melanistic anteriorly, losing spots,

sometimes having fine, streaked pattern anteriorly and

1997

Asiatic Herpetological Research

Vol. 7, p. 57

are unicolor posteriorly. Venter ivory, with sides of

ventrals darkly smudged.

iv. Usually two, 5th and 6th (rarely 4th and 5th or 5th

or three. 4th. 5th. and 6th) supralabials touching orbit.

v. Ventrals 205-277. subcaudals 139-144.

vi. Distinct oculo-labial stripe, indistinct oculo-tem-

poral stripe.

Distribution in Pakistan (Figure 6): Widely dis-

tributed in Baluchistan, western and northern sub-

Himalayan (N.W.F.P. ) highland and inland low ranges

(Punjab and Sind). From sea level (along Makran

coast) to about 2300 m. It does not extend onto

plains.

Remarks: Unaware of Jan's (1865) erection of the

nominal taxon. J. Anderson ( 1871 ) described Zamnis

ladacensis from Ladakh, Baltistan. Later, he (1895)

compared rhodorachis with ladacensis and found

them identical. Despite proven conspecificity, a

rhodorachis with a median dorsal pinkish-red (Nikol-

skii, 1916). drab (Corkill and Cochran. 1965). light

orange to vermilion (Minton, 1966), red (Mertens,

1969) vertebral line has been regarded as ladacensis.

The so-called "colored vertebral line" is discernible

only in living snakes, as it is soon lost on preservation,

especially in formalin. This is why the validity of

ladacensis as a separate taxon has frequently been

questioned (Mertens. 1956; Kramer and Schnurren-

berger, 1963; Leviton and S. Anderson, 1961; Krai.

1969;Ataev, 1985).

Coluber rhodorachis from southern Israel (F.

Werner, 1896, Fig. 2 A. B) has more close-set (2 scales

wide) transverse stripes which are much broader than

interspaces. Leviton et al., ( 1992, Plate 15) show two

color morphs of C. rhodorachis from the Arabian pen-

insula: Fig. C. from Tabuk Emirate, anterior half of

body spotted, posterior unicolor; Fig. D, from Taif,

Makkah Emirate, is unicolor melanistic. while Fig. E.

from Khuzistan Province, Iran, is a banded form, the

bands broader than interspaces. Latiri (1991, Plate

16) shows two more color morphs from Iran: Fig. 41

unicolor and Fig. 42 spotted, the spots are more like

broken transverse bands. C. rhodorachis is known to

exhibit high variability of color and pattern through-

out its range (Y. Werner. 1971).

Coluber ventromaculatus Gray and Hardwicke,

1834 (Figures 2C, 5)

Diagnosis:

i. Midbody scale rows 19, reduced to 13 at level of

vent.

ii. The sooty pigment is confined to each scale's

periphery in dorsal body pattern (Fig. 2C).

iii. Dorsal pattern consists of a median row of rhombs

or saddles, broader than interspaces, alternating with a

lateral row of spots, usually touching ventrals.

iv. Two supralabials. 5th and 6th or 4th and 5th. touch

orbit.

v. Ventrals 195-220. subcaudals 82-1 19.

vi. Loreal scale longer than high.

Distribution in Pakistan: Plains of Punjab and Sind:

rarely extends above 300 m elevation. (Fig. 6).

Remarks: This taxon is based on Plate 80, Fig. 1 . a.

b of Gray and Hardwicke (1834), with only the

inscription, "spotted bellied snake Coluber ventro-

maculatus"; no description or type locality is given.

The figured snake has approximately 220 ventrals, 70

subcaudals, with a median row of more than 60. 1-2-

scale-wide narrow cross bands, replaced on tail by

narrow transverse streaks formed of dark edges of lat-

eral scales, distinct orbito-labial and temporal

stripes. Figure la shows an irregular cross band

between the orbits and a few spots on temporals and a

distinct median dorsal one-scale-narrow nuchal

streak. The lower jaw is shown distinctly counter-

sunk, abnormal for this species.

Schmidt (1939) restricted the type locality to Ben-

gal, since, according to Smith (1931). Hardwicke

mostly collected from the region. A comparison with

Pakistani snakes of this taxon shows differences in

dorsal pattern, which usually consists of 3-4-scale-

wide diamonds or saddles, obscure oculo-temporal

bar, 2-4-scale-wide nuchal streak always flanked by

larger temporal blotches obscuring oculo-temporal

streak: pigment is peripherally deposited on scales.

head with indistinct dark mottling. However, a pair of

snakes from southeastern Thar Pakar, Sind, has a sin-

gle scale-wide uninterrupted median nuchal streak,

running to the midbody. passing through dorsal sad-

dles, while snakes from Punjab and most of Sind have

a short, 2-4-scale-wide and 5-6-scale-long streak or

blotch, which seldom extends between saddles.

Leviton et al., (1992, PI. 15) illustrate two snakes

as C. ventromaculatus: Fig. F, from Sabiya Peninsula,

near Kuwait City, with a long narrow nuchal streak

and transverse bands, broader than interspaces, and a

row of lateral spots, while Fig. H. from Ghizri. Kara-

chi, with indistinct spottings on anterior half of body,

is just like snakes mostly from Baluchistan.

Coluber ventromaculatus and C. rhodorachis

sometimes indistinguishably intergrade into each

other in appearance, scale counts and dorsal body pat-

tern. For a long time. Russian herpetologists con-

fused C. rhodorachis with C. ventromaculatus

(Nikolskii. 1916; Terentev and Chernov. 1949; Levi-

Vol. 7, p. 58

Asiatic Herpetological Research

1997

ton. 1959; Leviton and S. Anderson. 1970). and still

this confusion exists (Baran. 1982). I am inclined to

believe that all C. ventromaculatus reported from west

of the Indus (Fig. 6) are actually color morphs of C.

rhodorachis, and C. ventromaculatus does not extend

westward beyond the Indus. Reports of this species

from Chitral, Dir and Swat (McMahon, 1901a,b).

actually pertain to C. rhodorachis. Mostly, the confu-

sion between these taxa is created by dorsal pattern

figured in the type. Fig. 1. Plate 80 (Gray and Hard-

wicki. Vol. II, 1834). Famous Indian ophiologist Wall

(1923) found no option but to unite C. ventromacula-

tus with C. rhodorachis to settle this taxonomic tan-

gle.

Key to Pakistani Snakes of the Genus

Coluber

A satisfactory key for identification of Pakistani Co/u-

ber has long been needed. The following key is based

on diagnostic characteristics gathered from the

present collection, satisfactorily helping in diagnosis

of these taxa (Khan 1993):

la. Midbody scale rows 21; collected from Chitral

and northern Baluchistan C.ravergieri

lb. Midbody scale rows 19 2

2a. Subcaudals 125-144; unicolor, spotty, or with

close-set transverse striations; sooty pigment depos-

ited between scales, main dorsal pattern formed by

concentration of tiny dots; collected from western and

northern highland and Salt Range, Punjab

C. rhodorachis

2b. Subcaudals 80-120; dorsal pattern of saddles, dia-

monds, or transverse bars 3

3a. One (5th, rarely 6th. or none) supralabial in con-

tact with orbit: dorsal pattern of vivid black transverse

bars, narrower than interspaces: sooty pigment depos-

ited uniformly on scales; collected from western Bal-

uchistan C.karelini

3b. Two (5th and 6th) supralabials in contact with

orbit; dorsal pattern a median row of saddles or dia-

monds, broader than interspaces; sooty pigment

deposited on periphery of scales; collected from Pun-

jab and Sind plains C. ventromaculatus

Acknowledgments

I wish to thank Mr. Shahid Hussain Malik, who has

been my constant companion during various collec-

tion tours to different parts of Pakistan: Azad Kash-

mir. Punjab, N.W.F.P.. Baluchistan and Sind. during

which most of the material for the present study was

collected. Special thanks are due to Messers Naeem

Ahmed. Basharat Ahmed and Mr. Shoib Ahmed for

helping in arranging our stay while we collected in

Baluchistan. Master Muhammad Sadiq (Goi), Dr.

Shah Muhammad (Kotli) for helping in different ways

in our collections from Azad Kashmir.

I am deeply indebted to Dr. Sherman A. Minton,

Jr.. Indiana University, USA, for advise and pholi-

dosic data from his colubrid collection, and Dr. Zug,

National Museum of Natural History. Washington.

D.C.. USA, for supplying pertinent literature.

Appendix I

Snakes for this study were collected from within a

radius of 5-10 km around the following localities in

Pakistan and Azad Kashmir. Figures in parentheses

indicate the number of snakes collected from each

locality.

Coluber ravergien.'Baluchistan: Boostan ( 1 ): Sha-

dezai(2).

Coluber karelini: Baluchistan: Punj Pai (4); Quetta

(4); Peshin (6); Boostan (3): Chaman (4); Loi

Banda. Zob (4); Muslim Bazar. Zob (2).

Coluber rhodorachis: Baluchistan: Punjpai (2)

Quetta (3); Peshin (2): Boostan (1); Chaman (2)

Loi Banda, Zob (1): Muslim Bazar, Zob (1)

Khuzdar (3); Kama. Khuzdar (2); Waddh, Khuz-

dar (3): Arnachh, Khuzdar (1); Naal, Khuzdar

(2); Nushki ( 1 ); Kalat ( 1 ); Mastung (5).

Northwestern Frontier Province: Wana ( 1 ); Tank

(1): Bannu (1): Kohat (1); Nowshera (3);

Peshawer (4): Mardan (2); Manshera (2); Dadar

(1); Abbottabad (2): Ghan Habibullah (2); Swat

(2); Kalam(2).

Punjab: Rohtas Fort (2); Islamabad (2): Chattar

(2); Attock (1); Pir peahai (2); Pind Dadan Khan

(2); Dandot ( 1 ); Khewara (2); Choa Saidan Shah

(2).

Sind: Chauki ( 1 ); Band Murad Khan ( 1 ); Karachi

(2); Thatta (1).

Azad Kashmir: Mirpur ( 1 ); Bhimbar (2); Dulaih

Jattan (1): Kotli (3); Goi Madan (8); Aram Bari

(2); Palandri ( 1 ). Punch ( 1 ); Bagh ( 1 ); Muzaffara-

bad (3).

Coluber ventromaculatus: Punjab: Jhelum (2); Lala

Musa ( 1 ); Gujrat (2); Wazirabad ( 1 ): Sialkot (3);

Gujranwala (1); Lalian (3); Rabwah (25); Chiniot

(14); Sargodha (4); Mianwali (5); Khushab (10);

Nurpur (12); Bhakkar (4); Leiah (3); Toba Tek

Singh (2); Multan (5); Dera Ghazi Khan (6);

Rajanpur (3); Bahawalnagar (3); Fort Marot (2);

Rahimyar Khan (4);

1997

Asiatic Herpetological Research

Vol. 7, p. 59

Sind: Sukkur (2); Sehwan (3); Larkaa (2):

Nawab Shah (3); Dadu (3); Hyderabad ( 1 ); Mithi

(2); Diplo (3).

Literature Cited

Anderson. J. 1871. A list of the reptilian aeeession to

the Indian Museum. Calcutta, from 1865 to 1870.

with a description of some new species. Journal of

Asiatic Society of Bengal 40: 12-39.

Anderson. J. 1895. On a collection of reptiles and

batrachians made by Colonel Yerbury at Aden and its

neighbourhood. Proceedings of Zoological Society of

London 1872:371-404.

Anderson. S. C. 1963. Amphibians and reptiles from

Iran. Proceedings of the California Academy of Sci-

ences, Series 4 3 1 :4 1 7-498.

Ataev. Ch. A. 1985. Reptiles of mountainous Turk-

menistan. Ashkabad Ilym, pp.410. (In Russian).

Bannikov. A. G.. I. S. Darevski, V. G. Ischenko. A. K.

Rustamov and N. N. Szczerbak. 1977. Catalogue of

amphibians and reptiles of the USSR. Moscow,

pp.410. (In Russian).

Baran. I. 1976. Turkiye yilanlarinin taksonomik

revizyonu ve cografi dagilislari. TUBITAK Yayinlan

309:1-177. Ankra. (In Turkish).

Baran. I. 1982. Zur taxonomie der Schlangen in

siidost-und ost Anatolia. Spixiana 5:51-59. (In Turk-

ish).

Boulenger. G. A. 1890. Fauna of British India,

including Ceylon and Burma. Reptilia and Batrachia.

London.

Boulenger. G. A. 1893. Catalogue of the snakes in

the British Museum. London. Vol. 1 .

Brandt. M. 1838. Note sur quatre nouvelles especes

des serpentes de la cote occidentale de la mer Caspi-

enne et de la Perse septentrionale, decouvertes par M.

karelini. Bulletin Science. Academy Imperial Science

St. Petersbourg, 111:243-244. Zoology, 32:201-244.

Clark. R. J.. E. D. Clark. S. C. Anderson and A.E.

Leviton. 1969. Report on a collection of amphibians

and reptiles from Afghanistan. Proceedings of Cali-

fornia Academy of Sciences series 4 36:279-3 1 6.

Dowling. H. G. 1967. Hemipenes and other charac-

ters in colubrid classification. Herpetologica 2:138-

142.

Dowling. H. G., And J. M. Savage. 1960. A guide to

the snake hemipenis: a survey of basic stucture and

systematic characteristics. Zoologica 45:17-28.

Gray, J. E.. And T. Hardwicke. 1834. Illustrations of

Indian zoology: chiefly selected from the collection

of Major General Hardwicke. II: Plate 80. British

Museum (N.H.), London.

Haas. G., And Y. L. Werner. 1969. Lizards and

snakes from southwestern Asia, collected by Henry

Field. Bulletin Museum Comparative Zoology

138:327-406.

Khalaf, K. T. 1959. Reptiles of Iraq with some notes

on the amphibians. Ar-Rabitta Press, Baghdad, pp 96.

Khan, M. S. 1 977. Checklist and key to the snakes of

Jhang District. Punjab, Pakistan. Biologia (Lahore)

23:145-157.

Khan. M. S. 1980. Affinities and Zoogeography of

herpetiles of Pakistan. Biologia (Lhore) 26:1 13-171.

Khan. M. S. 1982. An annotated checklist and key to

the reptiles of Pakistan. Part III: Serpentes (Ophidia).

Biologia (Lahore) 28:215-254.

Khan. M. S. 1986. A noteworthy collection of

amphibians and reptiles from northwestern Punjab.

Pakistan. The Snake 1 8: 1 1 8- 1 25.

Khan. M. S. 1987. Checklist, distribution and zoo-

geographical affinities of herpetofauna of

Balochistan. Proceedings of 7th Pakistan Congress of

Zoology 1987:105-112.

Khan, M. S. 1993a. Sarzameen-a-Pakistan kay

saamp (Snakes of Pakistan). Urdu Science Board.

299 Upper Mall. Lahore. 208 pp. (In Urdu).

Khan. M. S. 1993b. Hemipenial morphology of

Varanus flavescens (Hardwicke and Gray. 1927), and

its phylogenetic implications. Pakistan Journal of

Zoology 25:135-138.

Khan, M. S. 1994. Key for identification of amphibi-

ans and reptiles of Pakistan. Pakistan Journal of Zool-

ogy 26:249-255.

Khan. M. S. and N.Ahmed. 1987. On a collection of

amphibians and reptiles from Baluchistan, Pakistan.

Pakistan Journal of Zoology 19:361-370.

Krai, B. 1969. Notes on the herpetofauna of certain

provinces of Afghanistan. Zoology listy. 1:55-66.

Kramer, E., and H. Schnurrenberger. 1963 . Systema-

tic Verbreitung und Okologie der libyschen Schlan-

gen. Revue Suisse Zoologie 70:453-568.

Latifi. M. 1991(1985). The snakes of Iran. Transla-

tion. Society for the Study of Amphibians and Rep-

tiles. USA, pp.159.

Leviton. A. E. 1959. Report on a collection of rep-

tiles from Afghanistan. Proceedings of the California

Academy of Sciences. (4th Series) 29:445-463.

Leviton, A. E. 1986. Description of a new species of

Coluber (Reptilia: Colubridae) from the southern

Tihama of Saudi Arabia, with comments on the bioge-

Vol. 7, p. 60

Asiatic Herpetological Research

1997

ography of southwestern Arabia. Fauna Saudi Arabia

8:436-446.

Leviton, A. E. and S. C. Anderson. 1961. Further

remarks on the amphibians and reptiles of Afghani-

stan. Wasmann Journal of Biology 19:269-276.

Leviton, A. E. and S. C. Anderson. 1963. Third con-

tribution to the herpetology of Afghanistan. Proceed-

ings of the California Academy of Sciences, (4th

Series) 31:329-339.

Leviton, A. E. and S. C. Anderson. 1970. The

amphibians and reptiles of Afghanistan, a checklist

and key to the herpetofauna. Proceedings of the Cali-

fornia Academy of Sciences. (4th Series) 38: 163-206.

Leviton. A. E., S. C. Anderson, K. Adler, and S. A.

Minton. 1992. Handbook to Middle East amphibians

and reptiles. Society for the Study of Amphibians and

Reptiles, USA, 252 pp.

McMahan. A. H. 1901a. Notes on the fauna of Chi-

tral. Journal of the Asiatic Society of Bengal 70: 1-7.

McMahan. A. H. 1901b. Notes on the fauna of Dir

and Swat. Journal of the Asiatic Society of Bengal

70:7-12.

Menetries, E. 1832. Catalogue raissone des objects

die zoologie recuillis dans un voyage au Caucase. St.

Petersbourg 32:1-273.

Mertens, R. 1952. Amphibien und reptilien aus der

Tiirkei. Rev. Fas. Science University Istanbul 17:41-

75.

Mertens. R. 1969. Die Amphibien und Reptilien

West-Pakistans. Stiittgarter Beitriige zur Naturkunde

197:1-96.

Minton, S. A.. Jr. 1962. An annotated key to the

amphibians and reptiles of Sind and Las Bela, West

Pakistan. American Museum Novitates. No. 2081:1-

21.

Minton, S. A., Jr. 1966. A contribution to the herpe-

tology of West Pakistan. Bulletin of the American

Museum of Natural History 134:31-184.

Murthy. T. S. N. and B. D. Sharma. 1976. A contri-

bution to the herpetology of Jammu and Kashmir.

British Journal of Herpetology 5:533-538.

Murthy. T. S. N. and B. D. Sharma. 1979. Second

report on the herpetofauna of Jammu and Kashmir.

India. The Snake 11:234-241.

Nilson G. and C. Andren. 1983. Die Herpetofauna

des Kavir-Schiitzgebietes, Kavir-Wiiste, Iran.

Salamndra 17:130-146.

Nikolskii, A. M. 1916. Fauna of Russia: Reptiles.

Petrograd 2:1-349. (Israel Programme of Transla-

tions, Jerusalem).

Pesantes, O. S. 1994. A method for prepration of the

hemipenis of preserved snakes. Journal of Herpetol-

ogy 28:93-95.

Schatti. B, and A. Agasian. 1985. Ein neues Konzept

fur den Coluber ravergieri-C . nummifer -Komplex

(Reptilia, Colubridae). Zoologische Abhandlungen

Staatliches Museum fur Tierkunde. Dresden 40:109-

123.

Schatti. B. and L. D. Wilson. 1986. Coluber Lin-

naeus. Holarctic racers. Catalogue American

Amphibians and Reptiles: 399.1-399.4.

Schmidt. K. P. 1939. Reptiles and amphibians from

Southwest Asia. Field Museum of Natural History.

Zoology Series 24:49-92.

Schmidt. K. P. 1941. Reptiles and amphibians from

Central Arabia. Field Museum Natural History, Zool-

ogy Series 24:161-165.

Schmidt, K. P. and H. Marx. 1956. The Herpetology

of Sinai. Fieldina: Zoology 39:21-40.

Smith, M. A. 1943. The fauna of British India. Cey-

lon and Burma. Reptilia and Amphibia. Vol. Ill: Ser-

pentes. Taylor and Francis. London. 583 pp.

Strauch. A. 1873. Die Schlangen des russischen

Reiches. Memoires Academy of Science. St. Peters-

bourg 21:1-122.

Tiedemann. F. 1991. First record of Acanthodactylus

opheodurus Arnold, 1980, and Coluber ventromacu-

latus Gray, 1834 (Squamata: Lacertidae, Colubridae)

from the United Arab Emirates. Herpetozoa 4:167-

175.

Terentev. P. V and S. A. Chernov. 1949. Key to the

amphibians and reptiles. 3rd ed. (Isreal Programme

of Translations. Jerusalem) 1-315.

Wall. F. 1923. A handlist of the snakes of the Indian

Empire. Part II. Journal of the Bombay Natural His-

tory Society 19:598-632.

Werner, F. 1905. Einige fur Kleinasien neue Rep-

tilien. Zool.Anz. 29:411-413.

Werner. Y. L. 1971. Lizards and snakes from Trans-

Jordan, recently acquired by the British Museum

(Nat. Hist.). Zoology 21:215-256.

Werner, Y. L. 1986. Evolutionary implications of

occasional (non-mimetic) behavioural triangulation of

the head in snakes (Coluber rhodorachis and Malpo-

lon monspessulamis). The Snake 18:37-41.

1997

Asiatic Herpetological Research

Vol. 7, pp. 61-67

A New skink from the Thai Desert of Pakistan

Muhammad S. Khan and Muhammad R. Z. Khan

Herp Laboratory, 15/6 Darul Saddar North, Rahwah 35460, Pakistan.

Abstract. - A new skink belonging to the genus Eumeces is morphologically described and compared with its

Pakistani congeners.

Key words: Eumeces indothalensis new species, description. Sauria, Scincidae, Eumeces

Figurel . The distribution of lizards of the genus Eumeces in Pakistan

Vol. 7. p. 6:

Asiatic Herpetological Research

1997

Figure 2A (top) and B (bottom). Eumeces indothalen-

sis new species.

Introduction

In early summer. 1984. the senior author picked up a

pair of eviscerated skinks with a vivid dorsal striped

pattern from a heap of E. taeniolatus skinks. Mr.

Nazar Muhammad, an animal and plant collector for

local Hakims (physicians), was eviscerating almost a

sackful of living mass of writhing and struggling

Eumeces taeniolatus skinks. He had collected the ani-

mals from the roots of common reed-bush. Sach-

harum moonja, close to village Bar Ganga. 9 km SW

of Bakkhar. District Mianwali, western Punjab. Paki-

stan. The eviscerated lizards were to be sun-dried and

sold in the market as reg mahi at Rs. 500-800 per 500

gram. Dried skinks are in great demand since the

stuff is used in several aphrodisiac preparations

(Khan. 1991. in press).

Laboratory examination of the striped pair of

skinks proved that they belong to a new species,

which is being described here.

Abbreviations used: BMNH=Bntish Museum

(Natural History). London; MCZ=Museum of Com-

parative Zoology, Harvard University. Cambridge.

USA; MSK=Herp Laboratory. 15/6 Darul Saddar

North, Rabwah 35460, Pakistan.

Taxonomic Considerations

The cosmopolitan genus Eumeces is represented by

three species in Pakistan: E. taeniolatus (Blvth.

1854), E. blythianus (J. Anderson. 1871) and E.

zarudnyi Nikolsky. 1899 (Minton. 1966; Mertens,

1969; Khan and Mirza, 1977) (Fig. 1). Taylor (1935)

revised the genus Eumeces distinguishing it into sev-

eral species groups: placing E. taeniolatus in the Tae-

niolatus Group, which is characterized by the

presence of a postnasal, frontal in contact with inter-

parietal, a single row of median dorsal much widened

scales, dorsum solden yellowish with light and dark

flecks which extend on limbs and tail. While both E.

zarudnyi and E. blythianus are included in the

schneiderii group, which has no postnasal scale, fron-

tal is not in contact with interparietals, has a pair of

median dorsal row of wider scales on dorsum with

striped or unicolour pattern. However. Mertens

( 1946) gives E. zarudnyi and E. blythianus subspecies

status of the widely distributed Saharo-Sindhian E.

schneiderii. The new species has strong affinities

with E. schneiderii.

Eumeces indothalensis, sp. nov.

Holotype: BMNH 1990.6 (MSK 0423.85, Fig. 2. A).

a young male. from under roots of a common reed

plant, Sachharum moonja, near village Bar Ginga, 9

Km SW of Bakkar. midwestern Punjab. Pakistan.

32°.50' N. 7 1 ° E, along west bank of Indus River, ele-

vation 75 m. Nazar Muhammad collector, 16 July,

1984.

Paratype: (1): MSK 0422.85. (Fig. 2, B). an adult

male, data as holotype, except 17 July, 1984.

Diagnosis: Medium sized skink, with dorsal pattern

of 5-7 dark brown stripes separated by alternating

light narrower stripes, extending on to the tail, no

scattered scales of different colour on the body and

limbs; nasal scale resting on first supralabial; nasal

suture horizontal; no postnasal; interparietal about

half the size of frontal and is of the same shape: two

azygos postmentals: 52-56 scales in paired middorsal

row of wider scales; posterior loreal and presubocu-

lars longer than deep; no intercalary scales between

subdigital lamellae.

Description of holotype: Rostral as high as

broad.triangular. its part visible from above distinctly

narrower than frontonasal, broadly truncate posteri-

orly. Supranasals lateral, about thrice as long as

broad, reaching mesially to form a suture above

nasals, the length of which equals the breadth of the

rostral visible from above. Frontonasal transverse,

much smaller than prefrontals, extend considerably

forward between supranasals. laterally contacting

anterior loreal. Prefrontals two. hexagonal, forming a

median suture, contacting on sides with both loreals

and first supraciliary. Frontal as long as its distance

from rostral tip. abruptly truncated to a median point

at anterior and posterior end, its length about twice its

greatest breadth, in contact with three supraorbitals.

Frontoparietals hexagonal, forming a median suture

which is in line with that of prefrontals.

Interprietal longer than broad, about half the

length of frontal and of the same shape, much longer

than frontoparietals, abruptly truncated at both ends,

posteriorly bordered by first pair of nuchals. Parietal,

1997

Asiatic Herpetological Research

Vol. 7, p. 63

Table 1 . Pholidosic counts and measurements of the type series of the new species Eumeces indothalensis

(br=broken).

longer than broad, produced anterolaterally to contact

the fourth postocular. A single pair of much broad

nuchals. meeting at the posterior pointed tip of inter-

parietal, an azygos nuchal on left side. Nasal slightly

longer than broad, lies exactly on first supralabial not

touching second, nasal suture horizontal, passing

above naris, meeting rostral at its midlateral side,

lower nasal larger bears major part of postero-lateral

naris which lies posterior to nasorostral suture. Ante-

rior loreal rectangular, oblique, about thrice as long as

broad, higher than posterior, touching prefrontal, pos-

terior loreal longer than high narrowing posteriorly to

come in contact broad, forms a continuous subocular

series with 8 postsuboculars, fifth is broadest, seventh

longest: second presubocular longer than broad,

smaller than anterior. A distinct small triangular pre-

ocular with two posterior smaller ones form a series

with several more or less longer scales extending on

Vol. 7, p. 64

Asiatic Herpetological Research

1997

to the posterior of eye, separating supraciliaries from

pelpebral scales.

A series of 7 supraciliaries. first largest, a little

smaller than first supraocular, extending on to head

top to contact with prefrontal, second longest, while

seventh about as high as first but half of its size. A

pair of small postoculars and three oblique rows of

granular scales touching lower palpebrals. Supraocu-

lars 4, first three in contact with frontal, parietal sepa-

rates fourth from upper secondary temporal. A single

primary temporal, quadrangular, oblique; secondary

temporals two, upper as broad as parietal, lower verti-

cal, produced anteriorly to touch primary temporal.

Two tertiary temporals, upper smaller, lower vertical,

about twice as long as broad.

Eight supralabials, first five anterior to eye, sixth

subocular about twice as long as high, first smallest,

subtriangular, narrower along oral orifice. 7th and 8th

subequal and largest, 8th supralabial separated from

ear by four scales occupying a space equaling the

width of 8th supralabial. A slightly distinct preocular

from pelpebral scales. Ear opening vertical, oval,

preauricular lobes 3/3, upper two broad reaching to

the middle of the auditory meatus, third very small.

Mental scale broader than rostral. A pair of azygos

postmentals, first as broad and as long as mental, sec-

ond about twice broader than first, mesially produced

backwards between first pair of chin shields; chin

shields three pairs, first in contact, second separated

from each other by a scale while third by three scales.

Infralabials seven, 7th largest.

Body scales smooth, polished, imbricate, regular,

arranged in parallel longitudinal rows; scales of

median dorsal two rows 3-4 times broader than long,

52. from parietal to the level of vent. All ventrals sim-

ilar except abdominals which are slightly larger; mid-

ventrals 60, from postmental to the level of vent; 33

around neck, axilla 41: mid-abdomen 26, around

groin 29 and 51 from armpit to groin.

Median dorsal pair of enlarged scales extends on

the tail dorsum. At base, the tail squarish in cross sec-

tion, becoming round at middle, with a very gradual

taper to its pointed tip. A median ventral series of

transversely enlarged subcaudals, 33 in holotype, as

tail is broken. A pair of large median preanal scale

suiTounded anterolaterally by 8 smaller scales, over-

lapped later ally by the median large scales; a distinct

tubercular large scale on each side of the anal slit;

four postanal transverse rows of smaller scales, with a

shallow transverse postanal pit; 22 scales round the

tail base just posterior to the lateral anal tubercular

scale.

Limbs short, anterior when stretched forward

claws reaching to eye, posterior reaching to the level

of mid-abdomen; when thighs are bent at right angle

to the body, toes freely overlap. Limbs with smooth

cycloid scales in parallel longitudinal rows, 17 at mid-

upper arm. 14 mid-fore arm. mid-thigh 22 and 14

rows scales, no intercalary scales. Claws strong with

a basal solid part and long sharp broader tip.

Color (in formalin): Seven vivid dark brown longi-

tudinal stripes on body: a single median dorsal starts

from behind inter parietal and extends to the level of

vent; second dorsal, paired, from behind parietals to

the level of vent, join each other at the level of vent,

do not extend on tail; third pair, from behind eye

extends laterally to groin than along lateroventral side

of tail; fourth pair from behind ear above shoulder to

groin. The dark brown stripes separated from each

other by narrower lighter stripes, making the pattern

distinct. Head uniform brownish, lips, chin and ven-

trum light yellowish. Measurements (in mm): Snout

vent length (SVL) 57. tail length (TL) 40 (broken),

snout to eye 4, snout to ear 13 snout to fore limb 21,

axilla to groin 30. head length 13, head breadth 9.

Variation: Table 1 summarizes pholidosic and mea-

surement variations in the type series. Both specimen

have broken tails, MSK 0422.84 after I Ith subcaudal

while holotype after 33rd. Snout region of MSK

0422.84 is injured, not allowing detailed morphologi-

cal study. A part differences in snout-vent length and

some minor differences in scale counts the type series

is consistent in other pholidosic characteristics, how-

ever. MSK 0422.84 has 9 stripes on dorsum, while

there are seven in holotype.

Head uniform brownish in both specimens, how-

ever, supralabials and preauricular lobules are with

brownish specks in the paratype.

Etymology: The name indothalensis refers to the

part of the Thai Desert lying on the western bank of

Indus River, northwestern Punjab. Pakistan, from

where the new species was collected.

Comparison: According to the collector, Mr. Nazar

Muhammad. Eumeces taeniolatus is sympatric with

the new species in the type locality and is much more

common. E. taeniolatus differs from the new species

in having a postnasal, single row of broadened median

dorsals, frontal in contact with interparietal, dorsum

pale grey to bronze, speckled with creamy specks,

three dark brown stripes on dorsum with pale specks,

tail and limbs similarly speckled. On the other hand

absence of postnasal scale, median dorsal double row

of broadened scales, a pair of azygos postmentals and

separation of frontal from inteiparietal warrant inclu-

sion of the new species in the Schneiderii Group (Tay-

lor, 1935).

1997

Asiatic Herpetological Research

Vol. 7, p. 65

Table 2. Comparison of pholidosic and measurement data of Eumeces indothalensis new species with its con-

geners; br=broken. (Data except of type series and E.zarudnyi from Taylor, 1935. Data for E. zarudnyi partially

through courtesy Dr. Rosaldo [per. comm.] for material in Museum of Comparative Zoology collected by Loveridge

[1959] from Balochistan).

Vol. 7, p. 66

Asiatic Herpetological Research

1997

Table 2 summarizes comparison of the new spe-

cies, E. indothalensis with its congeners of the

Schneiderii Group: E. blythianus (Anderson) known

from Punjab, differs from the new species in having a

single postmental, 30 scales round midbody, 50-60

scales from occiput to above anus, 3 pairs of nuchals.

Taylor (1935, Plate 6) illustrates E blythianus

(BMNH 98.7.12.1) from Afridi country (Waziristan.

southern borderline of N.W.F.P. with Afghanistan,

similarly Finn (1898) has also reported it from the

area. Taylor's photograph shows dorsal pattern of lon-

gitudinal stripes on olive-brown dorsum separated by

narrower light stripes exactly matching with the dor-

sal pattern of the new species (Fig. 2,A,B). A similar

striped young E. blythianus from Karachi (Minton.

1966, plate 19, 2). is reported to have unicolour pink

adult phase (Fig. 2). Mertens (1969) reports similar

lizards from Astola Island off the Karachi coast. A

pinkish unicolour skink has been reported from

Sheikh Manda near Quetta. Balochistan by Khan and

Ahmed ( 1987). E. princeps also has a striped adult

pattern, however, its juveniles are pattemless

(Mertens, 1969).

The second species. E. zarudnyi, nikolsky, from

southwestern Iran and southern Balochistan (Lover-

idge. 1959), differs from the new species in having 5-

6 preauricular lobules, wider head, and uniform grey

dorsum. While the wide ranging Saharo-Sindhian

skink E. schneiderii which is known from Mekran to

Waziristan, differs from E. indothalensis in having 66

scales in the mid dorsal row. 24 scales around mid-

body, subocular as wide as high, dorsum brown or

olive, median dorsal rows shaded dark with light

spots, a very dim dorsolateral line and spotted hind

limbs.

The new species, Eumeces indothalensis, is

unique among Pakistani eumecid lizards in having the

nasal scale resting exactly on the first supralabial

which is triangular and does not touch second labial;

horizontal nasal suture which passes above nostril, the

nostril lies posterior to rostral-labial suture: dorsal

part of rostral much narrower than frontonasal; suboc-

ular longer than broad, its ocular side longer than

labial side; second loreal longer than broad; presuboc-

ular much longer than broad; interparietal as long as

parietals, exactly of the shape of frontal but half of its

size; three preauricular lobules, upper two much

broader than long, third much smaller; 1-2 pairs of

nuchals with an additional azygos nuchal; no interca-

lary scales between subdigital lamellae; dorsum with

seven dark brown stripes, which increase to nine in

adult (paratype) rather to disappear and become uni-

colour as in E. blxthianus (Minton. 1966).

Acknowledgments

Our special thanks are due to Mr. Jose P. Rosado,

Curatorial Associate. Department of Herpetology,

Museum of Comparative Zoology. Harvard Univer-

sity, Cambridge. USA. for providing photographs,

measurements and scale counts of the skinks col-

lected by Dr. Loveridge from Balocistan ( 1959). Our

thanks are also due to Dr. Robert W. Murphy, Royal

Ontario Museum Toronto, Canada, for exchange of

ideas and providing pertinent literature which made

this study possible.

Literature Cited

Finn, F. 1 898. Notes on a specimen of the rare scin-

coid lizard Eumeces blythianus (Anderson) from the

Afridi country, with exhibition of the type-specimens.

Proceedings of Asiatic Society of Bengal: 1 89.

Ingoldby. C. M. and J. B. Proctor. 1923. Notes on a

collection of reptilia from Waziristan and the adjoin-

ing portion of the N. W. Frontier Province. Journal

Bombay Natural History Society 29: 117-1 30.

Khan. M. S. 1987. Checklist, distribution and zoo-

geographical affinities of amphibian and reptiles of

Baluchistan. Proceedings of 7th Pakistan Zoological

Congress 1987:105-112.

Khan. M.S. 1991 . Endangered species of reptiles of

Pakistan and suggested conservation measures.

Handbook Pakistan Wildlife Conservation Founda-

tion, Islamabad 42-45

Khan. M. S. in press. Colour guide to the Reptiles

and Amphibians of Pakistan. Robert E. Krieger. Pub-

lishing Company. Melbourne. Florida.

Khan. M. S. and Mirza, M. R. 1977. An annotated

checklist and key to the reptiles of Pakistan. Part II:

Sauria (Lacertilia). Biologia (Lahore) 23:41-64.

Khan, M. S. and Naeem Ahmed. 1987. On a collec-

tion of amphibians and reptiles from Baluchistan.

Pakistan. Pakistan Journal of Zoology 19:361-370.

Loveridge, A. 1959. Reptiles and amphibians col-

lected by the expedition in Saudi Arabia and in Bal-

uchistan and Bahawalpur, West-Pakistan. Paper

Peabody Museum Arch. Ethnol. Harvard University

52:226-227.

Mertens. R. 1946. Dritte Mitteilung ber der Rassen

dir glattechse Eumeces schneiderii. Senckenbergiana

biology, Frankfurt a.M. 27:53-62.

Mertens, R. 1959. Ber einiuge seltene Eidechsen aus

West-Pakistan. Aquar-Terra-Zeits. 12:307-310.

1997

Asiatic Herpetological Research

Vol. 7, p. 67

Mortens. R. 1969. Die Amphibien unci Reptilien

West-Pakistans. Stuttgarter Beitrage zur Naturkunde

197:1-96.

Minton. S. A. 1966. A contribution to the herpetol-

ogy of west Pakistan. Bulletin American Museum

Natural History 134(21:31-184.

Taylor. E. H. 1935. A taxonomic study of the cosmo-

politan scincoid lizards of the genus Eumeces with an

account of the distribution and relationships of its spe-

cies. Bulletin University of Kansas 36 (14): 1-643.

[997

Asiatic Herpetological Research

Vol. 7. pp. 68-79

Taxonomic Review of the Megophryid Frogs (Anura: Pelobatoidea)

Amy Lathrop

Centre for Biodiversity and Conservation Biology of the Royal Ontario Museum, 100 Queen's Park, Toronto.

Ontario, Canada M5S 2C6 and Department of Zoology, University of Toronto

Abstract.- The family Pelobatidae has recently undergone notable reorganization. Once composed of two

subfamilies, Pelobatinae and Megophryinae. it now consists of only the former. The family Megophryidae has

recently been elevated to represent Asian members once in the family Pelobatidae; megophryids are diagnosed

by three synapomorphies.

A phylogenetic analysis of the Archeaobatrachia by Cannatella (1985) included three species from two

genera within Megophryidae. Paraphyly in the genus Megophrys was supported by one character, the articulation

of the urosacrum. A re-analysis of Cannatella's (1985) data indicated that alternative patterns of the relationships

among megophryids were plausible and that the homology of the urosacral articulation should be examined in

more detail.

Key words: Amphibia, Anura, Pelobatoidea. Megophryidae, taxonomy

Introduction

The classification of anurans has been a matter of

much recent debate. Several different opinions exist

about their relationships (see Ford and Cannatella.

1993 for a review of the recent work on anuran rela-

tionships), and no fewer than three different taxono-

mies are currently in use (Duellman and Trueb, 1986;

Dubois 1985, 1986; Ford and Cannatella, 1993). Pre-

vious classifications (prior to Duellman. 1975) have

been based on a single complex of characters. As a

result, when alternative character schemes were

derived, earlier classifications were found to be incon-

gruent.

The source of the incongruities have been the

choice of characters used to construct each classifica-

tion (Noble [1922, 1931] vertebral centrum, pectoral

girdle, thigh musculature, and dentition; Griffiths

[1963] hyolaryngeal structures, skull and limb mor-

phology, and reproduction and development, vertebral

column; Hecht [1963] and Starrett [1973] tadpole

types). Each classification directly reflected the char-

acters used in the particular study. For example, the

classification proposed by Hecht (1963) in which

Orton*s (1957) larval characters were used to con-

struct a classification that differed markedly from one

developed the same year based on adult morphology

(Griffiths, 1963). The history of these characters and

their role in the classification of anurans is reviewed

in the works of Lynch (1973) and Duellman (1975).

Noble (1922), reflected on the problems involved

with constructing a classification based on either a

single character or a complex of characters. However,

the trend continued until Tihen (1965) and Inger

(1967) provided classifications based on multiple

characters. Subsequently, others have adopted a simi-

lar approach to the classification of anurans (Kluge

andFarris, 1969; Lynch, 1973; Duellman, 1975; Lau-

rent. 1979; Dubois. 1986). More recently. Ford ( 1989,

1993) undertook an analysis of the Neobatrachia, in

an attempt to identify the phylogenetic position of

Dendrobatidae among all anurans. Similarly, Canna-

tella (1985) generated a phylogeny for the Archaeo-

batrachia. Both of these thorough phylogenetic

analyses culminated in a phylogeny for all major

groups of frogs (Ford and Cannatella. 1993). They

have applied contemporary techniques to generate a

taxonomy reflecting natural groupings (de Queiroz

and Gauthier. 1992). i.e., evolutionary history.

Anuran classification has progressed since Reig

(1958) divided the Anura into four suborders: Amphi-

coela, Aglossa, Archaeobatrachia. and Neobatrachia.

Based on the analysis of Ford and Cannatella ( 1993),

the Amphicoela and Archaeobatrachia are artificial

groupings. However. Neobatrachia and Aglossa

reflect natural groupings (the latter now called

Pipoidea). They confirmed Lynch *s (1973) observa-

tion that members of Pelobatidae represent a transi-

tional group between the basal anurans and

1997

Asiatic Herpetological Research

Vol. 7, p. 69

Table 1 . Characters that support the family Pelo-

batidae (Duellman and Trueb, 1986), superfamily

Pelobatoidea (Ford and Cannetella. 1992) which

includes pelobatines and megophryines and the

genus Pelodytes.

ossified intervertebral discs present

procoelous centrum

presacrals I and II not fused

atlantal cotyles of Presacral I closely juxta-

posed

ribs absent

sacral diapophysis greatly expanded

sacrum fused to coccyx (moncondylar articula-

tion with the coccyx in megophryine and some

eopelobatines)

transverse processes on the proximal part of

the coccyx (often incorporated into the sacral

diapophysis)

pectoral girdle arciferal

cartilaginous omosternum

osseous sternum

scapula not overlain by the clavicle

parahyoid absent

cricoid ring incomplete dorsally

astragalus and calcanium are fused only proxi-

mally and distally

two tarsalia

m. sartorius is not discrete from the m. semi-

tendinosus and the end of the latter inserts

ventral to the m. gracilis

m. glutaeus magnus has an accessory tendon

m. adductor magnus lacks an accessory head

pupil vertical

amplexus is inguinal

type IV larvae

trigeminal and facial ganglia are fused

diploid number of chromosomes is 26 (24 in

Leptolalax pelodytoides)

Neobatrachia; this implies that they possess an inter-

mediate number of primitive character states.

Cannatella (1985) found that the family Pelo-

batidae. composed of two subfamilies. Megophryinae

and Pelobatinae. represented an artificial grouping,

and that each subfamily must be elevated to familial

status to remove the conflict. Currently the two fami-

lies are placed in a superfamily, Mesobatrachia (Can-

natella. 1985). and is composed of pelobatoids

(Pelobatidae. Pelodytidae, and Megophryidae) and

pipoids (Rhinophrynidae and Pipidae).

To date, the evolutionary relationships of the

Mesobatrachia have been addressed only in the phylo-

genetic analysis of Cannatella ( 1985. Ford and Canna-

tella, 1993). Within the Mesobatrachia. the

relationships of Pelobatidae (Scaphiopus and Spea)

have been partially resolved by Cannatella (1985).

However, within the Megophryidae, only genealogi-

cal relationships of Scutiger (Yea et al.. 1992), and

Scutiger with Oreolala.x (Yang and He, 1980) has

been examined. In Cannatella"s ( 1985) analysis of the

Archaeobatrachia (hereafter referred to as DCC for

ease of discussion), conclusions were made regarding

the relationships of two genera of Megophryidae,

Megophrys and Leptobrachium. However, there were

errors in the coding of the characters in DCC's analy-

sis that have serious implications on the composition

of the family. Consequently, herein. I will review the

taxonomic history of the family Megophryidae, and

provide a re-analysis of Cannatella's data relevant to

Pelobatoidea (Pelodytidae, Pelobatidae. Megophry-

idae). I conclude, by discussing the need for a phylo-

genetic classification that includes all the genera of

Megophryidae.

Taxonomic History of Megophryidae

The first megophryid, Megophrys montana, was

described by Kuhl and Van Hasselt (1822). Only four

species of megophryids were known at the time of

Boulenger's ( 1882) comprehensive account of known

amphibians. Since then, 78 additional species have

been described, and undoubtably more will be added

as southeast Asia is more thoroughly investigated.

The first efforts to classify anurans was Cope

( 1865). He grouped taxa on the condition of the pec-

toral girdle and the vertebral column. In the taxo-

nomic practices of the past, grouping of organisms

were based on similarity, often creating polyphyletic

assemblages of taxa. The family Asterophrydidae

Gunther 1859. a polyphyletic group, was the first fam-

ily that included a megophryid. Members of this fam-

ily included three genera of megophryids

Vol. 7. p. 70

Asiatic Herpetological Research

1997

{Megalophrys, Xenophrys, and Leptobrachium), as

well as a microhylid, and a myobatrachid.

Noble (1922, 1931) provided groupings based on

multiple characters of the adult morphology;

megophryids were placed in the suborder Anomo-

coela, family Pelobatidae. In these works, the family

Pelobatidae included three subfamilies: Megophryi-

nae (Megophrys, Leptobrachium, Nesobia, Scutiger,

Aelurophryne, Leptobrachella), Pelobatinae (Scaphi-

opus, Spea, Pelobates. Peladytes), and Sooglossinae

(Nesomantis and Sooglossus). Noble (1926) believed

that the Sooglossinae possessed all the evolutionary

significant pelobatid characteristics (maxillary teeth,

arciferal pectoral girdle, procoelous vertebrae, a sin-

gle coccygeal condyle, and the particular arrangement

of the pectoral muscles). However, it showed a differ-

ent arrangement of the thigh musculature thought to

be derived with respect to Asian pelobatids. Not satis-

fied with the characters used by Noble, Griffiths

(1959) removed Sooglossinae from the family Pelo-

batidae and placed it in its own family, Sooglossidae.

The classification of the Pelobatidae (viz. Peloba-

tinae, Megophryinae. and Pelodytinae) was main-

tained for nearly 40 years. Lynch (1973) removed

Peladytes from the family Pelobatidae, and erected a

new family for this one genus (Pelodytidae) on the

basis of limb characteristics that were derived inde-

pendently from those of pelobatids.

Duellman and Trueb (1986) provided a phyloge-

netic tree that placed megophryids within Pelobatidae,

as the sister group to Pelodytidae (see Table 1 for a list

of synapomorphies uniting Pelodytidae and Pelo-

batidae). This arrangement has been the convention

since Lynch's (1973) work.

Cannatella ( 1985) performed a phylogenetic anal-

ysis of the Archaeobatrachia and found that Pelo-

batidae (Megophryinae and Pelobatinae) was

paraphyletic with respect to Pelodytidae and thus

removed megophryids from Pelobatidae and erected a

new family, Megophryidae. Despite a recent effort to

disseminate this information (Ford and Cannatella.

1993), with the exception of Trueb ( 1991 ) and Fu et

al., (submitted), the application has not received wide

acceptance. Recent taxonomic accounts have grouped

megophryids as a subfamily of Pelobatidae (Dubois.

1986; Duellman. 1993; Fang. 1985; Yea. et al., 1992:

Fei and Yea, 1990, 1983; Frost, 1985; Guan-Fu, et al.,

1993; Inger and Stuebing. 1991; Huang, 1985; Kuo,

1985; Wu, et al.. 1993; Zhao and Adler. 1993; and

others).

Taxonomic History of the Genera

The generic taxonomy of Megophryidae suffers from

a convoluted history and temporal instability of its

genera. The first generic name was proposed for the

type species. Megophrys montana Kuhl and van Has-

selt 1822. Shortly thereafter, Wagler (1830) published

the generic name as Megalophrys for the genus

Megophrys. This spelling continued for a century, and

appeared as the original generic name for seven spe-

cies in monographic reviews of anuran taxonomy

(Boulenger, 1908; van Kampen, 1923). In his review

of reptiles and amphibians of the Malay Peninsula.

Smith (1930) corrected this unjustified emendation

but without comment to the previous error.

From this single genus. Megophrys (Meg-

alophrys). Boulenger (1882) recognized three forms

on the basis of the presence or absence of vomerine

teeth and the type of vertebrae (procoelous or opistho-

coelous). He split the group into three genera:

Xenophrys (Giinther. 1865), Megalophrys (Wagler.

1830), and Leptobrachium Tschudi. 1838. Boulenger

(1908) later regrouped all three into the genus

Megophrys because the characters that he previously

had used to separate them varied intergenerically and

were not useful for distinguishing the genera.

Ceratophrys Gravenhorst. 1829. was used to

describe another form of Megophrys montana. Cer-

atophrys. a genus of large-headed leptodactylid.

occurs exclusively in South America and bears only a

superficial resemblance to Megophrys. Other junior

synonyms of Megophrys are Ixalus (Anderson. 1871 ),

once a genus of Rhacophoridae. The description of

the species was based on juvenile material of

Megophrys lateralis (Boulenger, 1908); Gorham

( 1966) considered this species a nomen dubium. Bed-

dard ( 1 907 ) placed Megophrys montana in a mono-

typic genus. Pelobatrachus. However, he did not

provide any unique characters to distinguish it from

the other known megophryid genera (Xenophrys.

Megalophrys. Leptobrachium). Therefore, it was

returned to Megophrys (Boulenger, 1908). Brachytar-

sophrys and Atympanophrys, were described by Tian

and Hu (1983). The latter. Atympanophrys, (Greek

[atympano = without tympanum]), was a monotypic

genus described from a specimen of Megophrys shap-

ingenesis in which the authors report that all struc-

tures associated with the middle ear (stapes, tympanic

annulus) were absent. Brachytarsophrys was thought

to be distinct because of its peculiar shaped head and

high neural spines of the vertebrae. Dubois (1986)

reviewed the three genera, Megophrys. Brachytar-

sophrys. and Atympanophrys. He concluded that the

three different evolutionary states that Tian and Hu

1997

Asiatic Herpetological Research

Vol. 7. p. 71

(19S3) referred to were neither sufficient nor impor-

tant enough to deserve generic ranking and thus made

them subgenera of Megophrys. A later investigation of

the type series of Atympanophrys revealed that all

structures of the middle ear were present and that the

absence of the middle ear in one specimen

(SM00042) was a result of improper handling of the

type (Fei et al., 1991, p. 4). The genus Atympanophrys

was considered a junior synonym of Megophrys (Fei

et al., 1991 ). Brachytarsophrys is still recognized as a

subgenus of Megophrys (Duellman, 1993).

Boulenger (1887, p. 405) reported that Scutiger

Theobald, 1868 (Chinese megophryids), as a genus of

Amphibia, is preoccupied by an earlier name, Scutig-

era Latreille. 1802, for a genus of centipede. As a

result, Boulenger erected a new generic name. Coph-

ophryne, for these forms. He also pointed out that

many of the characters of Cophophryne appear to be

intermediate between pelobatids and bufonids (viz.

absence of maxillary teeth, expanded sacral diapophy-

ses). Because of these characteristics, it was consid-

ered a member of the family Bufonidae.

Boulenger (1919) erected Aelurophryne for a sin-

gle species, A. mammata (= Bufo mammata Giinther.

1896) that could be distinguished from Cophophryne

by the absence of a posteriorly-notched tongue. These

two genera (Aelurophryne and Cophophryne) could

be distinguished from bufonids by the presence of

vertical pupils (a character found in many pelobatids).

Thus, Boulenger (1919) placed these two genera in

the Pelobatidae. Procter (1922) followed Boulenger's

(1919) familial arrangement. However, he considered

Cophophryne and Aelurophryne to be congeneric, and

place Cophophryne as a junior synonym of

Aelurophryne.

Noble (1931) recognized both Scutiger Theobald

(= Cophophryne Boulenger) and Aelurophryne (Bou-

lenger, 1919). He distinguished the two by the pres-

ence of short maxillary teeth in Scutiger and the

absence of dentition in Aelurophryne. Pope and Bor-

ing (1940) and Liu (1950) also recognized

Aelurophryne in their surveys of Chinese amphibians.

Liu ( 1 950) further characterized the two genera by the

presence of a tympanum and a small opening for the

eustachian tube in Aelurophryne. and the absence of

these characters in Scutiger. After having re-examined

four species fastigiate described by Liu (1950). Myers

and Leviton (1962) argued that Scutiger and

Aelurophryne could not be distinguished in the way of

Liu, Pope and Boring, and Noble had proposed. They

found that three of the four Scutiger forms possessed

a combination of characteristics that were supposed to

be present in either Scutiger or Aelurophryne (e.g..

presence of a deeply notched tongue, teeth, a tympa-

num which was concealed under the skin, and a dis-

tinct openings for the eustachian tubes).

Consequently. Myers and Leviton (1962) adopted

Procter's (1922) taxonomy, but because Scutiger pre-

ceded Aelurophryne. all Himalayan megophryids

were placed in Scutiger.

Ophryophryne, a genus described by Boulenger

(1903), was originally placed in the Bufonidae

because it possessed similar external characteristics

(horizontal pupil and an edentate maxilla). Boulenger

(1903) suggested that Ophryophryne was the evolu-

tionary link between the pelobatids and bufonids.

However, Noble (1926) examined the thigh muscula-

ture of two species of Ophryophryne and concluded

that they were diminutive Megophrys. Ophryophryne

remained a distinct genus, because most of the varia-

tion between Megophrys and Ophryophryne is in the

head region. Dubois (1980) stated that ". . . the strong

resemblance between Megophrys and Ophryophryne

(to the point that it is probably impossible to deter-

mine to which group one would place the specimen

without the head!) indicates that they probably do not

merit the status of distinct genera"1. In this work,

Dubois relegated Ophryophryne to the status of sub-

genus of Megophrys. Dubois (1986) re-examined his

earlier comparisons (Dubois, 1980) and considered

the differences to be distinctly different, thus return-

ing generic status to Ophryophryne.

Liu ( 1950) placed some species of Leptohrachium

in a new genus, Vibrissaphora. to represent a small

group that possessed keritanized nuptial excrescences

along the margin of the maxilla. Liu et al. (1973)

examined members of Vibrissaphora and Leptohrach-

ium hasseltii and found that the only difference

between the two genera was the presence of the max-

illary spine in Vibrissaphora. This character did not

seem significant enough to warrant two separate gen-

era. Therefore, Vibrissaphora was returned to Lepto-

hrachium (Dubois, 1980). Some authors still

recognize Vibrissaphora as a distinct genus (Zhao and

Adler. 1993).

Nesobia (van Kampen. 1923) was a name given to

small species that possess horizontal pupils and

inhabit Natuna Island. The taxonomic status of this

genus was not questioned by Dubois (1980) because

material was not available for examination. However,

because the name Nesobia was preoccupied, a genus

of molluscs, a new name was applied to this group

(Leptobrachella Smith 1925).

English translation of the original text in French.

Vol. 7. p. 72

Asiatic Herpetological Research

1997

Table 2. Genera of Megophryidae and their known synapomorphies.

Leptobrachella (Borneo and the Bunguran [=Natuna]

Islands)

very reduced sternum

pointed expansion at tips of digits

ventral skin of digits sharply delimited

no denticles on larval oral disc

nuptial excrescences absent

*vertical pupil

Leptobrachium (Southern China to the Philippines,

Indochina, and Sunda Is. to Bali)

♦vomerine teeth absent

snout not extending beyond lower jaw

tongue strongly notched posteriorly

two well developed metacarpal tubercles

vertebrae proceolous

omosternum cartilaginous

sternum with a bony style

*horizontal pupil

Leptolalax (Burma and southern China through Thai-

land and Vietnam to Malaya and Borneo)

(no unique synapomorphies)

Ophryophryne ( northern Vietnam and southern

China)

*maxillary teeth absent

horizontal pupil

♦vomerine teeth absent

Megophrys (southern, eastern, and southeastern Asia)

tadpole with funnel-shaped oral disc

larvae with median anal tube

♦vertical pupil

Scutiger (high altitudes of southwestern China, north-

ern Burma. Mepal, and northern India)

♦maxillary teeth reduced or absent

rough skin

tympanum obscured

♦vertical pupil

♦ character is not unique to the genus

Hu et al., erected Carpophrys (Sichuan Institute of

Biology, 1977) as a generic name for a single species,

Leptobrachium oshanensis. In a draft of the second

edition (1977) of the Chinese amphibians (Liu, et al.,

1966). Liu described three species of Leptobrachium

that were distinct in which he placed them in a new

genus. Carpophrys.

In this document Liu included a diagnosis of Car-

pophrys and the type species for the genus (Lepto-

brachium pelodytoides). This draft was distributed

among Chinese colleagues and has been cited in sev-

eral Chinese publications (after 1977), (personal com-

munication. Jinzhong Fu. 1995). Dubois (1980)

reviewed the status of Leptobrachium and agreed with

Liu that three species (L. gracile, L. pelodytoides, and

L. oshanensis') were distinct from other species of

Leptobrachium based on the position of the axillary

glands, appearance of the skin on the dorsum, unpig-

mented eggs, and other relative proportions of the

body. He thought these three species were likely to be

: Dubois ( 1980) used the specific epithet oshanense

because as he noted (B.G. 476 in a footnote) that the

original genus name. Leptobrachium, is neuter in gen-

der, and must be amended to agree with Leptolalax.

closely related to the larger subset of Leptobrachium.

but distinct. Dubois ( 1981 ) pointed out that the genus

name Carpophrys was not valid because the original

description was published anonymously and the type

species for the genus was not designated (following

Art. 13b, Art. 14. International Code of Zoological

Nomenclature, 1985). Thus, he created two subgenera

for the groups — Leptolalax for the three species, and

Leptobrachium for the larger subset (in the genus

Leptobrachium). Later, Dubois (1983) elevated Lep-

tolalax to generic status. Fei and Ye (1992) investi-

gated the validity of the two generic names.

Carpophrys and Leptolalax. and concluded that

although a description of the genus existed and a type

species was designated, Leptolalax is valid because

Carpophrys was not published in an official publica-

tion (Art. 8a. 1, International Code of Zoological

Nomenclature, 1985).

Currently, the family Megophryidae consists of 83

species divided into six genera (Leptobrachella, Lep-

tobrachium. Leptolalax, Ophryophryne, Megophrys,

and Scutiger). Each genus is supported by a set of

unique synapomorphies (Table 2) except for Leptola-

lax. My investigation into the literature has provided

no unique synapomorphies for Leptolalax. An addi-

1997

Asiatic Herpetological Research

Vol. 7. p. 73

Majority rule

100

100

100

100

100

67

100

100

67

100

100

100

100

Leiopelma

Discoglossidae

Leptobrachium

Megophrys aceras

Megophrys montana

Pelobates cultripes

Pelobates syriacus

Pelobatesfuscus

Pelobates varaldii

Spea bombifrons

Spea hammondii

Spea intermontana

Spea multiplicata

Scaphiopus couchii

Scaphiopus holbrookii

Scaphiopus hurterii

Pelodytes

Figure 1 . Majority rule consensus tree depicting the relationships of Pelobatoidea. In this phylogeny, Megophrys is

monophyletic and multiple trees result from the ambiguous relationships of Pelobates. The clade, Megophryidae is

bolded.

tional genus, Oreolcdax, erected by Myers and Levi-

ton (1962) to represent Chinese Scutiger-iike forms

that possess maxillary teeth. Recently. Fei and Ye

(1989) provided additional evidence to distinguish

Oreolalax from Scutiger, and this motion has been

followed by some authors (Fu and Murphy, in press;

Wu et al.. 1993; Guan-Fu et al., 1993; Fei and Yea,

1990). Other sources do not recognize the genus Ore-

olalax (Dubois. 1979. 1986; Duellman, 1993; Frost,

1985).

Evidence of Monophyly and OutgroupTaxa

The association of megophryids with pelobatids and

Pelodytes (= Pelobatoidea of Cannatella. 1985) has

gone largely unchallenged through the history of anu-

ran taxonomy. Previously recognized as Pelobatidae

(authors prior to 1973) or Pelobatidae plus Pelo-

dytidae (Lynch, 1973), the group is supported by sev-

eral synapomorphies (Table 1 ).

Although DCC was fairly confident about the

definitive synapomorphies of the Pelobatoidea. the

monophyletic nature of megophryids does not remain

incontestable. The results published in his thesis list

ten synapomorphies for the group; four are reversals

to the plesiomorphic condition, four represent conver-

gences with other anuran groups, and two were con-

sidered to be uniquely derived: loss of most of the

hyale of the hyoid and an ossified episternum. For

unknown reasons, the latter character was not

included as a synapomorphy by Ford and Cannatella

(1993).

Among the 83 species of megophryids, DCC

included only three species from two of the six gen-

era. He reported that "relationships within the mego-

phyrines are poorly defined . . . because few taxa were

available to study" (p 275). He went on to say that his

results suggest that Megophrys was paraphyletic with

the single species of Leptobrachium used in his analy-

sis; this was defined by a single character (the articu-

lation of the sacrum and the coccyx). The character

was said to be a reversal to the plesiomorphic condi-

tion in one species of Megophrys. Coding of this char-

acter is ambiguous at best, the character state is

probably not homologous to the primitive condition

found in discoglossids and Ascaphus. Cannatella

alluded to this problem in his section on character

analysis (p. 127).

Because the results of DCC's analysis have

brought into question the monophyly of Megophrys, I

re-investigated the issue.

Vol. 7, p. 74

Asiatic Herpetological Research

1997

Leiopelma

Discoglossidae

Leptobrachium

Megophrys aceras

Megophrys montana

Pelobates culthpes

Pelobates syriacus

Pelobates varaldii

Pelobatesfuscus

Spea bombifrons

Spea hammondii

Spea intermontana

Spea multiplicata

Scaphiopus couchii

Scaphiopus holbrookii

Scaphiopus hurterii

Pelodytes

Figure 2. Phylogeny of Pelobatoidea. The relationships of Pelobates is unresolved. The character UROSACRM

when evaluated as ordered with its original four states (Cannatella, 1985) constrains Megophrys to be paraphyletic

with Leptobrachium. The clade. Megophryidae is bolded.

Materials and Methods

I examined the data set of Cannatella ( 1985) in order

to understand the evolution of the morphological

character within pelobatoids. My evaluation of the

taxa in the clade Pelobatoidea (viz. Leptobrachium,

Megophrys. Pelobates, Pelodytes, Scaphiopus. and

Spea) included 43 of 181 characters for 17 of 42 taxa

of archaeobatrachians. Two characters associated with

the stapes: COLUMEL1 (0, absent; 1, present; 2,

greatly elongated) and COLUMEL2 (0, normal size;

1. reduced) were combined to removed inapplicable

character states. The character COLUMEL was coded

as follows (0. absent; 1. present, normal, extending

entire length of ear cavity; 2, greatly elongated; 3,

reduced). Uninformative characters at this level of the

analysis were removed; of the 181 characters. 137

characters were not informative in the analysis of

Pelobatoidea (Appendix I). Phylogenetic analyses

were performed using Swofford's (1993) Phyloge-

netic Analysis Using Parsimony program (PAUP). A

heuristic search was performed using simple stepwise

addition only minimal trees were retained and trees

were constructed using branch swapping option of

tree bisection-reconnection. steepest descent, and

holding all most parsimonious trees. Characters were

ordered and polarized by outgroup comparison

( Watrous and Wheeler, 1981) using the outgroup Dis-

coglossus, the sister species of the clade Pelobatoidea.

and Leiopelma as a secondary outgroup.

Results

Three most parsimonious trees (MPTs) were resolved

when the data were run as unordered (65 steps; CI -

.723; RI = .860; Fig. 1 ). In all cases, Megophrys was

monophyletic, with Leptobrachium as its sister group.

Differences among the MPTs occurred within the

clade of Pelobates. Character states for Pelobates

were invariant, except for the COLUMELLA and the

CRICOID, both of which were autapomorphic for P.

veraldii and P. fuscus. respectively. These autoapo-

morphies were responsible for the differing topologies

among Pelobates. When all the characters were

treated as ordered, as in the DCC analysis, six MPTs

were resolved, each 73 steps long (CI = .699; RI =

.850). Three of trees were identical to those in the

unordered analysis (Fig. 1). Among the other three

topologies, Megophrys is paraphyletic with Lepto-

brachium. and the relationships of Pelobates were not

resolved (Fig. 2).

One character used by DCC was the articulation

of the sacrum and the coccyx (UROSACRM). DCC

had doubts about the polarity and homology of this

character. Although similar in configuration, he ques-

1 997

Asiatic Herpetological Research

Vol. 7. p. 75

tioned whether the condition in Megophrys montana

was homologous to that of Leiopelma. Cannatella

coded this character as homologous, but with reserva-

tion. When the character was either left unordered or

removed completely from the analysis. Megophrys

was resolved as a monoprn letic group and the result-

ing three topologies were identical to those Fig. 1 .

If the articulation of the sacrum in Megophrys

montana is not homologous to that of Leiopelma, and

different from that seen in Megophrys aceras, then 5

character states are required to describe the variation

in UROSACRM. rather than the original 4 states as in

DCC. When UROSACRM was coded as five ordered

or unordered character states (Appendix 1 ) the analy-

sis resulted in three trees identical to those of the pre-

vious unordered analysis of the original data set

(ordered = 73 steps; CI = .712: Rl = .854; unordered =

66 steps; CI = .727; RI = .859).

Discussion

DCC's phylogeny depicts the two species of

Megophrys as paraphyletic with respect to Lepto-

brachium. However, my re-analysis demonstrates that

there is an alternative arrangement in which

Megophrys is monophyletic. The condition of the

UROSACRUM (e.g.. syncondrotic or synovial, mono-

condylar or bicondylar) has been used as a diagnostic

character for some groups of anurans (Nicholls, 1916;

Griffiths. 1963; Lynch. 1973; Cannatella. 1985: Ford.

1989) and avoided by others (Duellman and Trueb.

1986). Noble (1922) cautioned against its utility as a

diagnostic character for pelobatids (Megophryidae.

Pelobatidae. and Pelodytidae). Furthermore, within

the Megophryidae, specifically Megophrys, there has

been several reports of variation in the urosacral

fusion (Kluge, 1966). Thus, because UROSACRM

has the ability to make Megophrys paraphyletic, the

articulation of the coccyx to the sacrum must be

examined more closely to determine its true homol-

ogy.

Wiens (1989) illustrated the difference in develop-

ment between a fused bicondylar articulation and one

that is not fused, and suggested that these arrange-

ments may have arisen via several different develop-

mental pathways. What appears to be two different

conditions in the Megophryidae — sacrum and uro-

style separate; joint synchondrotic in Megophrys

montana and Leptobrachium hasseltii; sacral fusion

in Megophrys aceras — may have been formed from

two very similar developmental pathways. Ontoge-

netic studies of the formation of the sacrum and the

coccyx may reveal homologous states that would not

be identified by examining just the adult condition.

The systematics of megophryids is poorly under-

stood. Our ideas of the relationships within the family

have not changed much since Noble's (1926) evolu-

tionary hypothesis. Without a comprehensive phylo-

genetic hypothesis from which we can base a

classification, the resulting taxonomy will likely

prove to be unstable; it may include paraphyletic

groupings. Although Dubois (1980) constructed a

classification to serve as a starting point for future

studies, his conservative scheme is not based on a

phylogeny, but primarily on phenetic clusterings with-

out regard for evolution of the characters.

To understand the relationships between the gen-

era of Megophryidae, and the placement of

megophryids within the pelobatoids. a thorough phy-

logenetic analysis of the family is necessary. This

analysis should be performed in a similar manner as

Cannatella's (1985) study, and the classification

should be derived directly from the phylogeny (Wiley.

1981 ). Employing a phylogenetic classification would

ensure that the taxonomy was consistent, functional,

and maximized information content. In this way, the

knowledge that is gained from this interesting group

of frogs will produce a useful classification that

clearly reflects the evolutionary paths of each species.

Acknowledgments

I am grateful to J. R Bogart. for his loan of literature

on short notice. R. MacCulloch helped translate the

French. J. Fu translated, discussed, and clarified much

of the Chinese literature that would still continue to be

a mystery to me. C. Huang was kind enough to allow

me to use her draft translation of Fei et al.,'s (1991)

Key to Amphibians of China. I am grateful to S.

Monks, R. Murphy, and D. Upton for their helpful

suggestions which have improved the quality of this

paper. This study was supported by the Natural Sci-

ences and Engineering Research Council (NSERC) of

Canada Grant A3 148 awarded to R. W. Murphy. This

is contribution XXX from the Centre for Biodiversity

and Conservation Biology of the Royal Ontario

Museum.

Vol. 7. p. 76

Asiatic Herpetological Research

1997

Appendix I

Data matrix of characters from Cannatella ( 1985) to include only Pelobatoidae and the outgroup taxa, Leiopelma

and Discoglossus. (A) Leiopelma, (B) Discoglossus pictus, (C) Leptobrachium. (D) Megophrys aceras, (E) M.

montana, (F) Pelobates cultripes, (G) P. syriacus. (H) P. varaldii, (I) P. fuscus, (J) Spea bomifrons, (K) S. ham-

mondii, (L) S. intermontana. (M) S. multiplicata. (N) Scaphiopus couchii. (O) S. holbrookii. (P) S. hurterii. (Q)

Pelodaytes punctatus. See original work (Cannatella. 1985) for character coding.

characters taxa

ABCDEFGHI J KLM

(Continued)

a. UROSACRM is coded as 0 in Cannatella (1985).

Literature Cited

Beddard. F. E. 1907. Contributions to the knowledge

of the anatomy of the batrachian family Pelobatidae.

Proceedings of the Zoological Society of London

1907:871-911.

Boulenger, G. A. 1882. Catalogue of the Batrachia

Salientia s. Ecaudata in the collection of the British

Museum. London 2nd ed. 503 pp.

Boulenger. G. A. 1887. On a rare Himalayan toad.

Cophophryne sikkimmensis Blyth. Annual Magazine

of Natural History, ser. 5, 19:405-407.

Boulenger. G. A. 1903. Descriptions of three new

batrachians from Tonkin. Annual Magazine of Natural

History. 7 (12):186-188.

Boulenger. G. A. 1908. A revision of the Oriental

pelobatid batrachians (genus Megalophrys). Proceed-

ings of the Zoological Society, London 1908:407-430.

Boulenger. G. A. 1919. On Aelurophryne mammata,

Gunther.. an addition to the batrachian fauna of Kash-

mir. Records of the Indian Museum. Calcutta. 16:

469-470.

Cannatella, D. C. 1985. A phylogeny of primitive

frogs (Archaeobatrachians). Ph.D. Thesis. University

of Kansas. 403 pp.

Cope. E. D. 1865. Sketch of the primary groups of

Batrachia Salientia. Natural History Review 1865:97-

120.

de Queiroz, K.. and J. Gauthier. 1992. Phylogenetic

taxonomy. Annual Review of Ecology and Systemat-

ics 23:449-480.

Dubois. A. 1979. Une espece nouvelle de Scutiger

Theobald. 1868, (Amphibiens, Anoures) du nord de la

Birmanie. Rev. Suisse Zool., 86:631-640.

Dubois. A. 1980. Notes sur la systematique et reparti-

tion des amphibiens anoures de Chine et des regions

avoisinantes. IV. Classification generique et subgene-

rique des Pelobatidae Megophryinae. Bulletin Men-

suel de la Societe Linnenne de Lyon 49(8):469-482.

[In French].

Dubois. A. 1981. Notes sur la systematique et la rep-

artition des amphibiens anoures de Chine et des

regions avoisinantes. V. Megophrys oshanensis Liu.

1950 et Leptobrachium minimum Taylor. 1962.. Bul-

letin Mensuel de la Societe Linnenne de Lyon 51:183-

192. [In French | .

Dubois, A. 1983. Note preliminaire sur le genre Lep-

tolalax Dubois, 1980 (Amphibiens, Anoures), avec

diagnose d'une espece nouvelle du Vietnam. Alytes

2(4): 147-153. [InFrench|.

Dubois, A. 1985. Miscellanea nomenclatorica batra-

chologica (VII). Alytes 4:61-78.

Dubois, A. 1986. Miscellanea taxinomica batracho-

logica (I). Alytes 5( l-2):7-95. [In French!.

Duellman. W. E. 1975. On the classification of frogs.

Occasional Papers of the Museum of Natural History,

The University of Kansas, Lawrence. Kansas. 42: 1-

14.

Duellman. W. E. 1993. Amphibian species of the

world: additions and corrections. University of Kan-

sas Publications, Museum of Natural History 21:1-

372.

Duellman. W. E. and L. Trueb 1986. Biology of

Amphibians. McGraw-Hill. Inc. New York. 670 pp.

Fang, R.-s. 1985. A new species of Scutiger from

Shaanxi. China. Acta Herpetologica Sinica 4(4):305-

307. | In Chinese].

Fei, L., and C. Ye. 1983. Two new subspecies of

Megophrxs omeimontis Liu from China (Amphibia:

Pelobatidae). Acta Herpetologica Sinica 2:49-52.

Fei. L., and C. Ye. 1989. Geographical distribution,

origin and evolution, and centre of differentiation of

high-altitude pelobatid toads in Asia (Amphibia: Pelo-

batidae) Zoological Research. Kunming 109(4): 295-

302. [In Chinese].

Fei, L.. and C. Ye. 1990. Intergeneric relationships

and diversification of the high-altitude peobatid toads

in Asia and their relation with the formation of Qing-

hai-Xiz and Plateau (Amphibia: Pelobatidae). Acta

Vol. 7. p. 78

Asiatic Herpetological Research

1997

Zoologica Sinica, Beijing, 36(41:420-428 [In Chi-

nese].

Fei. L., and C. Ye. 1992. Comments on the taxonomy

of pelobatid toads of genus Leptolalax (Carpophrys)

with description of a new species. Acta Zoologica

Sinica 38(3): 245-253. [In Chinese].

Fei, L., C. Ye, and Y Huang. 1991. Key to Chinese

Amphibia. Chongqing Branch. Science and Technol-

ogy Literature Publishing House, Chongqing

(Sichuan). 364 pp. [In Chinese].

Ford, L. S. (1989). The phylogenetic position of poi-

son-dart frogs (Dendrobatidae): reassessment of the

neobatrachian phylogeny with commentary on com-

plex character systems. Ph.D. Thesis. University of

Kansas. 307 pp.

Ford. L. S. 1993. The phylogenetic position of the

dart-poison frogs (Dendrobatidae) among anurans: an

examination of the competing hypotheses and their

characters. Ethology Ecology and Evolution 5:219-

231.

Ford, L. S., and D. C. Cannatella. 1993. The Major

clades of frogs. Herpetological Monographs 7:94-

117.

Frost, D. R. 1985. Amphibian species of the world.

The Association of Systematic Collections, Lawrence,

Kansas, 732 p.

Fu. J.. A. Lathrop. and R. W. Murphy. 1997. Phylog-

eny of Genus Scutiger (Amphibia: Megophryidae) —

A Reevaluation. Asiatic Herpetological Research.

Fu. J. and R. W. Murphy. 1997. Phylogeny of Chinese

Oreolalax and the use of functional outgroups to

select among multiple equally parsimonious trees.

Asiatic Herpetological Research.

Gorham. S. W. 1966. Liste der rezenten Amphibien

und Reptilien. Ascaphidae, Leiopelmatidea (sic). Pip-

idae. Discoglossidae. Pelobatidae. Leptodactlylidae.

Rhinophrynidae. Das Tierreich. 85:1-222. [In Ger-

man].

Griffiths. I. 1959. The phylogeny of Sminthillus lim-

batus and the status of the brachycephalidae

(Amphibia Salientia). Proceedings of the Zoological

Society, London 132:457-487.

Griffiths, I. 1963. The phylogeny of the Salientia.

Biology Review 38: 241-292.

Hecht. M. K. 1963. A reevaluation of the early history

of the frogs, part II. Systematic Zoology. 12( 1 ):20-35.

Huang. Y.-z. 1985. A new species of pelobatid toads

(Amphibia,: Pelobatidae) from Ningxia Hyi Autono-

mous Region. Acta Biologica Plateau Sinica. Xining

1985:77-81. fin Chinese!.

Inger, R. F. 1967. The development of a phylogeny of

frogs. Evolution 21(21:369-384.

Inger, R. F. and R. B. Stuebing. 1991. A new species

of frog of the genus Leptobrachclla Smith (Anura:

Pelobatidae), with a key to the species from Borneo.

Raffles Bulletin of Zoology 39(1): 99-103.

International code of zoological nomenclature. 1985.

International code of zoological nomenclature 3rd ed..

International Trust for Zoological Nomenclature,

London. 338 pp.

Kluge. A. G. (1966). A new pelobatine frog from the

lower miocene of South Dakota with a discussion of

the evolution of the Scaphiopus-Spea complex. Con-

tributions in Sciences, Los Angeles County Museum.

113: 1-26.

Kluge. A. G.. and J. S. Farris. 1969. Quantitative phyl-

etics and the evolution of anurans. Systematic Zool-

ogy 18:1-32.

Kuhl. H.. and J. C. v. Hasselt. 1822. Uittreksels uit

brieven van de heeren Kuhl en van Hasselt. aan de

heeren C. J. Temminck. Th. van Swinderen en W. de

Haan. geschreven in de Straat Sunda, den 17 den

December 1820 [parts 1-3]. Algemeene Konst- en

Letter-Bode, Haarlem 7:82—88, 99—104. 149—153.

Kuo, Z.-T. 1985. A new species of Ophryophryne

from Yunnan. Acta Herpetologica Sinica 4(4):41-43

[In Chinese].

Laurent. R. F 1979. Esquisse d'une phylogenese des

anoures. Bulletin Society of Zoology. France 104:

397422 [In French].

Liu C. C. 1950. Amphibians of western China. Fieldi-

ana: Zoology, mem. 2:1-400.

Liu, C. C. S-c Hu. L. Fei. and C-c Huang 1973. On

collections of amphibians from Hainan Island. Acta

Zoologica Sinica, Beijing. 19(14): 385-104 [In Chi-

nese].

Liu. C-c. S-c Hu. and H-b Ding 1966. Atlas of Chi-

nese animals — Amphibians (1st ed.). Science Press,

Beijing, 29pp.

Lynch, J. D. 1973. The transition from archaic to

advanced frogs In Evolutionary biology of the

Anurans: Contemporary research on major problems.

Vial. J. L. (ed.). University of Missouri Press, Colum-

bia, pp. 133-182.

Myers, G. S., and A. E. Leviton (1962). Generic clas-

sification of the high-altitude pelobatid toads of Asia

(Scutiger, Aelurophryne, and Oreolalax). Copeia

1962(2): 287-291.

Nicholls. G. C. (1916). The structure of the vertebral

column in the anura Phaneroglossa and its importance

1997

Asiatic Herpetological Research

Vol. 7, p. 79

as a basis of classification. Proceeding of the Lin-

nean Society of London. 128: 80-92.

Noble. G. K. 1922. The phylogeny of the Salientia. I.

The osteology and the thigh musculature; their bear-

ing on classification and phylogeny. Bulletin of the

American Museum of Natural History 46: 1 -87.

Noble. G. K. 1926. An analysis of the remarkable

cases of the distribution among the Amphibia, with

descriptions of new genera. American Museum Novi-

tates 212:1-24.

Noble. G. K. 1931. Biology of the Amphibians.

McGraw-Hill Book Co.. New York. 577 pp.

Orton. G. L. 1957. The bearing of larval evolution on

some problems in frog classification. Systematic

Zoology 6(2):79-86.

Pope, C. H.. and A. M. Boring. 1940. A survey of Chi-

nese Amphibia. Peking Natural History Bulletin

15:13-86.

Procter. J. B. 1922. On a new toad. Cophophryne alti-

cola, collected on the Mt. Everest Reconnaissance

Expedition. 1921. Annual Magazine of Natural His-

tory ser. 9:583-587.

Reig. O. A. 1958. Proposiciones para una neuva mac-

rosistematica de los anuros. Nota preliminar. Physis

21:109-118.

Sichuan Institute of Biology (Hu. S.-q. C.-y. Ye. and

L. Fei). 1977. Systematic Key to Amphibians of

China. Science Press. Beijing 93pp [In Chinese].

Smith. M. A. 1930. The Reptilia and Amphibia of the

Malay Peninsula from the Isthmus of Kra to Sin-

gapore including the adjacent islands. Bulletin of the

Rattles Museum, Singapore 3:1-149.

Starred. P. H. 1973. Evolutionary patterns in larval

morphology In Evolutionary biology of the Anurans:

Contemporary research on major problems. Vial. J. L.

(eds.). University of Missouri Press, Columbia, pp.

251-271.

Swofford. D. L. 1993. PAUP: Phylogenetic analysis

using parsimony, version 3.1. Illinois Natural History

Survey, Champaign.

Tian. W.-s.. and Q. Hu. 1983. Taxonomic study on

genus Megophrys, with description of two new gen-

era. Acta Herpetologica Sinica. Chengdu, new ser..

2(2):41-48. | In Chinese].

Tihen. J. A. 1965. Evolutionary trends in frogs. Amer-

ican Zoologist. 5:309-318.

Trueb, L. 1991. Patterns of cranial diversity in Lissa-

mphibia. In The skull. Hanken. J., and B. K. Hall

(eds.) The skull: Patterns of structural diversity Vol-

ume 2. University of Chicago Press. Chicago, pp.

255-343.

van Kampen, P. N. 1923. The Amphibia of the Indo-

Australian Archipelago. Leiden, E. J. Brill, Ltd. 304

PP-

Wagler, J. 1830. Naturliches system der amphibien.

mit vorangehender classification der Saughiere und

Vogel. Miinchen, Cotta, 354 p.

Watrous. L. E.. and Q. D. Wheeler. 1981. The out-

group comparison method of character analysis. Sys-

tematic Zoology 30(1): 1- 1 1.

Wiens. J. J. ( 1989). Ontogeny of the skeleton of Spea

bombifrons (Anura: Pelobatidae). Journal of Mor-

phology. 202: 29-5 1 .

Wiley. E. O. 1981. Phylogenetics: The theory and

practice of phylogenetic systematics. Wiley Inter-

science, New York, 439 p.

Wu. G.-F., E.-m. Zhao, R. F. Inger, and H. B. Shaffer.

1993. A new frog of the genus Oreolalax (Pelo-

batidae) from Sichuan, China. Journal of Herpetology

27(4):410-413.

Yang. D-t. and Y-h He. 1990. Relationship between

species within tympanumless toad group of Scutiger

(Oreolalax) from Southwest China. Pp. 204-209. In

E-m. Zhao (ed.): From Water onto Land. China For-

estry Press, Beijing. [In Chinese].

Ye. C, L. Fei. G. Wei. and N. Xu. 1992. Study on the

phylogenetic relationship between species of Scutiger

genus in Qinghai-xizang Plateau (Amphibian: Pelo-

batidae). Acta Herpetologica Sinica, Guiyang (1 and

2): 27-39. [In Chinese].

Zhao. E.-m., and K. Adler. 1993. Herpetology of

China. Published by Society for the study of Amphib-

ians and Reptiles, in cooperation with Chinese Soci-

ety for the Study of Amphibians and Reptiles.

Contributions to Herpetology, 10:1-522.

1997

Asiatic Herpetological Research

Vol. 7. pp. 80-84

A Brief Herpetological Excursion To Wai Ling Ding, Wanshan Islands, South

China Sea

James Lazell.1 Michael Lau,2 and Wenhua Lu1

The Conservation Agency, 6 Swinburne St., Jamestown, RI 02835, U.S.A.; Department of Ecology and

Biodiversity, University of Hong Kong, Pokfulam Rd.. Hong Kong.

Abstract. - Two frogs and three lizards are recorded from Wai Ling Ding, one of the larger Wanshan Islands

southwest of Hong Kong, in Guangdong Province. China (the number of additional unpublished records for

islands within Hong Kong Territory for both frogs in parentheses): Kaloula p. pulchra (7), Rhacophorus

leucomystax or "Polypeddtes megacephalus" {7), Hemidactylus bowringi, Eumeces quadrilineatus, and

Scincella modesta. Ours is the first record for S. modesta in Guangdong Province; ontogenetic and elevational

data are presented for this species.

Key words: Biogeography, Wanshan. Hong Kong, Anura. Kaloula. Rhacophorus. Polypeddtes, Squamata,

Hemidactylus, Eumeces, Scincella modesta.

^

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Figure 1 . The Wanshan Islands and adjacent portions of Hong Kong Territory. 1 . Da and Xiao Wanshan

(the "Ladrones"); 2, Zhizhou; 3, Dangan; 4, Jiapeng; 5, Lantau (Tai Yue Shan); and 6, Hong Kong Island.

Arrow indicates Wai Ling Ding. Dashed line indicates part of the southern and western border of Hong

Kong Territory. Bar, top left, is 5 km.

1997

Asiatic Herpetological Research

Vol. 7, p. 81

O

o

«3

Figure 2. Island localities for Kaloula p. pulchra vouchered by MCZ specimens (solid dots) or from Karsen

et al., 1 986 (open circles). 1 , Hong Kong; 2, Cheung Chau; 3. Chek Lap Kok (now blasted away); 4. Siu-A-

Chau, Soko Islands; 5, Po Toi; 6. Yim Tin Tsai; 7, Peng Chau; 8 Tai Lei; 9, Lamma; and 1 0, Lantau (Tai Yue

Shan). Star is Wai Ling Ding. Bar, bottom right, is 5 km.

Introduction

More than 40 vegetated islands lie south and west of

the British Territory of Hong Kong, on the inundated

continental shelf of the South China Sea. within

Guangdong Province. Collectively, the group is

called Wanshan; two of the larger islands, in the

extreme southwest, were well known historically as

the Ladrones: DaWanshan and XiaoWanshan today

(Empson 1992). To the north lies the Zhizhou cluster,

and to the east and southeast lie the Dangan and Jiap-

eng groups, respectively. Centrally located is the San-

men complex, the largest of which is Wai Ling Ding,

ca 3.3 km" and 310 m above sealevel, some 25 km

southwest of Hong Kong (Fig. 1 ).

Access to these islands has heretofore been very

limited (Pan et al.. 1985), while the 100 or more

islands within Hong Kong Territory have received

considerable attention (Karsen et al.. 1986: Zhao and

Adler 1993). In an attempt to develop commerce,

Chinese authorities now permit regular tourist access

to at least Wai Ling Ding from Hong Kong. We made

the trip on 20 July 1994.

Results

We were able to collect for only two hours during

overcast weather with intermittent showers. Heavy

rain developed at midday and soon terminated our

efforts. Only five species were vouchered. All speci-

mens are in the Museum of Comparative Zoology

(MCZ).

1. Kaloula p. pulchra (Anura: Microhylidae). MCZ

1 16225. Found under debris on a hillside, ca 60 m

above sealevel. A second individual was not col-

lected. This abundant species is widespread on

coastal islands including Hong Kong and Cheung

Chau (Karsen et al.. 1986), Chek Lap Kok (MCZ

115497-502; population now extirpated by destruc-

tion of the island), Siu-A-Chau in the Soko Islands

(Lazell 1988a; MCZ 109400). Po Toi (MCZ 1 16089),

Yim Tin Tsai (MCZ 117716-8), Peng Chau (MCZ

109403). Lamma (MCZ 109402), many localities on

Lantau (e.g. MCZ 1 16081-8. Shui Hau). and even tiny

Tai Lei off Peng Chau, area 2.9 ha (MCZ 1 10964-5).

See Fig. 2.

2. Rhacophorus leucomystax ("Polypedates mega-

cephalus") (Anura: Ranidae or "Rhacophoridae"),

Vol. 7, p. 82

Asiatic Herpetological Research

1997

Figure 3. Localities for Rhacophorus leucomystax or " Polypedates megacephalus" vouchered by MCZ

specimens (solid dots). 1 , Hong Kong; 2, Chek Lap Kok (now blasted away): 3. Tai-A-Chau, and 4, Siu-A-

Chau, Soko Islands; 5, Ma Wan; 6 Yim Tin Tsai; 7, Peng Chau; 8. Kau Sai Chau; 9, Lamma; and 1 0, Lantau

(Tai Yue Shan). Star is Wai Ling Ding. Bar. bottom right, is 5 km.

MCZ 116226. Tadpoles were also collected for the

Department of Zoology, University of Hong Kong.

The voucher is a metamorph. All specimens were

found in rain water pools on the hillside above the vil-

lage at about 70 m elevation.

The nomenclature for this frog is unsettled. Zhao

and Adler ( 1993: 74) notwithstanding, the sole consis-

tent character given by Liem (1970) separating

"Polypedates" from Rhacophorus is the diplasio-

coelous vertebra of the former. One of us (JL) finds

this character prone to individual variation in adult

frogs and questions whether any genus founded on

such a single character could be monophyletic. Zhao

and Adler (1993: 156) accepted the notion of Matsui

et al. ( 1986) that Chinese specimens should be called

megacephalus (type locality Hong Kong: Hallowell.

1861) "based on comparisons of Taiwanese and

Bornean specimens." Taiwan and Borneo are both

continental shelf islands. Borneo is more than twice

as far from Wai Ling Ding (and Hong Kong) as is Tai-

wan, but we see no rationale for assigning populations

on that basis, and opine that this species, abundant at

Hong Kong (Karsen et al., 1986: 31), should be

judged on evaluation of topotypic material. Nor do

we believe the minor differences noted by Matsui et

al. ( 1986) necessarily imply species-level distinction.

Karyotypes often vary within species (e.g. Schmid et

al., 1994). A demonstration of sympatry would be

convincing.

In addition to the New Territories mainland and

Hong Kong Island, noted by Karsen et al. (1986), this

species has been vouchered on Chek Lap Kok (MCZ

1 15709-36; population now extirpated by destruction

of the island), Siu-A-Chau (Lazell 1988a: MCZ

109426-30) and Tai-A-Chau (Lazell 1988a; MCZ

110969-71) in the Soko Islands. Peng Chau (MCZ

109425), Ma Wan (MCZ 1 15737-40). Lamma (MCZ

109437), Yim Tin Tsai (MCZ 109437) and Kau Sai

Chau (MCZ 116227) in the Port Shelter Islands, and

several localities on Lantau (e.g. Shui Hau, MCZ

115742-4). See Fig. 3.

3. Hemidactylus bowringi (Squamata: Gekkonidae).

MCZ 179462-3. Both were collected under debris in

the village area at the northwest of the Island. Sev-

eral others were seen. This is probably the most ubiq-

uitous and widespread member of the Hong Kong

39207 Hong Kong: The Peak

172779 Lantau: Tei Tong Tsai

1 72780 Lantau: Tei Tong Tsai

172781 Lantau: Keung Shan

176240 Lantau: Ngong Ping

176241 Lantau: Ngong Ping

1 76242 Lantau: Ngong Ping

1 76243 Lantau: Tai Tung Shan

176244 Lantau: Keung Shan

1 76245 Hong Kong: Pokfulam

176246 Mainland New Territories: Pat Sin Leng

176746 Guangdong: Wanshan: Wai Ling Ding

550

360

360

100

420

420

490

320

100

190

200

60

JFMAMJJASOND

Figure 4. Ontograph of MCZ specimens of Scincella

modesta from Guangdong and Hong Kong. Lines indi-

cate the size/time zone in which we expect specimens

to occur in this tropical, monsoonal region.

herpetofauna (Karsen et al.. 1986; Lazell 1988a) and

is to be expected on all continental shelf islands with

more than herb stage vegetation in the South China

Sea.

4. Eumeces quadrilineatus (Squamata: Scincidae),

MCZ 179461. This, the only individual seen, was

found under debris inside an abandoned hut at the vil-

lage periphery at about 60 m. This spectacular spe-

cies is widespread but not especially common in the

region. Karsen et al. (1986) record it from Hong

Kong, Lantau. and Cheung Chau islands: Lazell

(1988a) added Tai-A-Chau in the Soko group (MCZ

173399-100). An ontogenetic and biogeographic

study of this species is underway ( JL).

5. Scincella modesta (Squamata: Scincidae), MCZ

176746. This individual was found under debris

inside an abandoned hut above the village at ca 60 m.

S. modesta on Wai Ling Ding is our most notable find.

Nowhere common in this region, the species has here-

tofore been recorded only on Hong Kong. Lantau, and

Cheung Chau islands off the mainland, and is usually

encountered at moderate to high elevation (Karsen et

al.. 1986: Table 1 ). Karsen (pers. comm.) informs us

that the Cheung Chau record is not based on a speci-

men, but sight only. He suspects it may have been

Scincella reevesi.

Zhao and Adler ( 1993) recognized two subspecies

of S. modesta but did not admit to either occurring in

South China. Hong Kong, or on any islands. The

identity of these tropical skinks, widely disjunct from

their relatives to the north, was not considered by

Zhao and Adler and remains open to question. Onto-

genetic data are provided in Fig. 4.

Vol. 7. p. 84

Asiatic Herpetological Research

1997

Discussion

In addition to our five species. Pan et al. (1985) record

three species of frogs: Rana guentheri, R. limno-

charis, and R. rugulosa. Li and Pan (1995) added

Kaloula pulchra.

We saw only the extreme northwest portion of Wai

Ling Ding. The village where we landed had all the

appearances and aromas of a typical, impoverished,

fishing community burdened by an influx of workers

attempting to construct a facade attractive to tourists.

This community was called simply "Ling Ding

Tsuen" (Nowhere Alone Town). The area we saw was

extremely ecologically degraded with vast areas of

barren rock interspersed with cutgrass {Panicum

sp.). There were clumps and strips of scrub vegeta-

tion largely consisting of native species such as

Melastoma sp., Dicranopteris sp., and Rhodomyrtus

tomentosa. The trees, however, were exotic species:

Acacia confusa, Casaurina sp.. and unidentified euca-

lypts.

In view of the number of endemic species known

from Hong Kong islands, including some found at low

elevation such as Philautus romeri, Megophrys

brachykolos, and Dibamus bogadeki, the Wanshan

Islands will repay a thorough investigation.

Acknowledgments

We are indebted to ornithologist Dr. Martin Williams,

of Cheung Chau. Hong Kong, for arranging our trip,

and to Nick Goodyer. Brian Moseley. and Eddie Wu

Chon Wai for assistance in the field. Our trip was

sponsored in part by The Conservation Agency and

the Explorers Club.

Literature Cited

Empson. H. 1992. Mapping Hong Kong: A historical

atlas. Government Information Services, Hong Kong.

249 pp.

Hallowell, E. 1861 ("1860"). Report upon the Rep-

tilia of the North Pacific exploring expedition, under

command of Capt. John Rogers, U.S.N. Proceedings

of the Academy of Natural Sciences of Philadelphia

12:480-510.

Karsen. S„ M. Lau, and A. Bogadek. 1986. Hong

Kong amphibians and reptiles. Urban Council, Hong

Kong. 136 pp.

Lazell. J. 1988a. Soko Islands, South China Sea.

Explorers Journal 66(2):80-85.

Lazell, J. 1988b. Herpetology in South China. Her-

petological Review L9(3):49-51.

Li, Z.. and J. Pan. 1995. Guangdong Province

amphibians: fauna] regions and biogeography. Chi-

nese Amphibian Biogeography. Herpetological Series

8:125-130.

Liem. D. 1970. The morphology, systematics. and

evolution of the Old World treefrogs (Rhacophoridae

and Hyperoliidae). Fieldiana Zoology 57(1107): vii+

145 pp.

Matsui. M., T. Seto, and T Utsunomiya. 1986.

Acoustic and karyotypic evidence for specific separa-

tion of Pohpedates megacephalus from P. leucomys-

tax. Journal of Herpetology 20(4):483-489.

Pan, C. Liu, and X. Qian. 1985 Studies on amphib-

ian fauna of the mainland and some adjacent islands

of Guangdong Province. Acta Herpetologica Sinica

4(3):200-208.

Schmid. M.. W. Feichtinger, I. Nanda, R. Schakowski.

R. Visbal Garcia. J. Manzanilla Puppo, and A.

Fernandez Badillo. 1994. An extraordinarily low dip-

loid chromosome number in the reptile Gonatodes

taniae (Squamata. Gekkonidae). Journal of Heredity

85:255-260.

Zhao. E. and K. Adler. 1993. Herpetology of China.

Society for the Study of Amphibians and Reptiles

10:522 pp.

(997

Asiatic Herpetological Research

Vol. 7. pp. 85-86

Captive propagation of the Mandarin Rat Snake {Elaphe mandarina)

at Moscow Zoo

Sergei Mamet and Sergei Kudryavtsev

Department of Herpetology, Moscow Zoo, B.Gruzinskaya I , 123242 Moscow, Russia

Abstract. -Some results of a long-term breeding project aimed at captive propagation of the Mandarin Rat Snake

(Elaphe mandarina) are presented. Data on breeding periods, clutch size, number of young and their sizes are

given.

Key words: Reptilia. Serpentes, Elaphe mandarina, captive reproduction.

Introduction

The Mandarin Rat Snake {Elaphe mandarina) is dis-

tributed in south-eastern Asia from upper Burma

(Myanmar) through southern China to northern Viet-

nam, inhabiting mountain forests and rocky slopes

covered with bushes. It probably is one of the most

sought after species of the genus, for a large part due

to it's unusual and quite colorful coloration. How-

ever, these snakes are rather difficult to maintain, as

most of those becoming available are wild-caught and

usually arrive very stressed and in a poor shape after

prolonged transportation and transfers. Also, one of

the main reasons for a low percent of success when

trying to adapt a newly received wild-caught Manda-

rin Rat Snake is a nearly obligatory and quite heavy

parasite infestation, including both subcutaneous and

internal helminths. From more than a dozen of wild-

caught Mandarin Rat Snakes, that have been in our

possession in course of about 10 years, only three sur-

vived and adapted to captivity, mainly because of

prompt and extensive medical treatment of the above

mentioned problems. Lately, as a routine, we treat all

newly arrived snakes with Metronidasol (Flagyl) 250

mg/kg. repeated after 10 days; 2,59c Albendasol ( Val-

basen) 0,2-0,4 ml/kg, repeated twice every 7 days if

symptoms persist; Prasiquantel (Baytril) 5mg/kg

every 24 hours for 3-5 days, administered either per

os or subcutaneous, depending on clinical signs.

Another traditional mistake made when dealing with

this species is over-heating which also can (and usu-

ally does) cause health problems. Thus, probably the

largest chances for success are with either captive-

born or very young wild-caught animals, provided the

general care is correct.

Husbandry and Reproduction

In 1989. a pair of new-born Mandarin Rat Snakes was

received from probably the first breeder of this spe-

cies, Mr. Munzenmaier. The animals were 290+65

mm and 330+68 mm long (body length + tail length,

male and female, respectively) and weighed 13.3 and

13.9 g. They were housed together in a glass enclo-

sure, measuring 40 x 25 x 25 cm (L x W x H) with

typical assortment of water basin, several shelters,

moisture chamber (which they frequented eagerly),

etc. An incandescent heating bulb was present in the

terrarium, however, for the most part it was switched

off, as the preferred temperatures for these snakes

apparently were 22-26°C during daytime and 16-18°C

at night (both according to previous owner's and to

our own observations). Humidity was maintained at a

rather high level, by daily sprinkling with warm water.

Rations included pink mice and. eventually, adult

mice and small rats (even as adult, the male prefers

pink mice to any other food), offered at first twice a

week and then, as the snakes grew, weekly. Chicken

and frogs were offered as well, but without any suc-

cess. The snakes grew fast and eventually were

housed separately, in glass enclosures 60 x 40 x 40

cm.

By October, 1992, the snakes measured 734+175

and 742+154 mm and weighed 231.8 and 327.7 g

(male and female, respectively) and were considered

mature. After a preparatory period of 30 days they

were put to hibernation at 1 1-14°C for approximately

3 months. After hibernation, in February-March, the

snakes were housed separately and were offered food

more often than prior to hibernation, i.e. twice a week.

No vitamins were added and no UV radiation was

present.

On 1 April. 1993, the female was introduced to the

male's enclosure, with male showing immediate inter-

est and beginning to purchase the female at once.

Approximately two hours later, first copulation was

observed, lasting for 28 minutes, during which period

the male was holding the female by the "neck" with

Vol. 7, p. 86

Asiatic Herpetological Research

1997

Table 1 . Egg measurements of clutch from 1993.

*all eggs were glued together and no individual

weights were taken.

Table 2. Measurements of the young.

his teeth. Several hours after they parted, the snakes

were separated again. This routine continued for

three weeks, with at least 5 copulation occurring

(sometimes the snakes were left together for the night

and no observations were made on their behavior).

By mid-May. 1993 the female looked obviously

gravid and 5 eggs could be palpated. Starting from

about that time, she refused food and in the morning

of 5 June laid 5 large eggs (see Table 1 ). The eggs

were placed in an incubator, at 25-28°C and very high

humidity, with sphagnum moss for a substrate. Incu-

bation period consisted continued for 48 days and the

first egg hatched on 22 July, with the young emerging

on the same day. Of 5 eggs 4 hatched, with the last

young emerging on 24 July. Measurements of the

young are presented at Table 2. For the first time they

shed on 8-1 1th day and started to feed on pink mice

soon after. There were no real problems with their

feeding as all young were very aggressive and bit their

preys at the slightest provocation, after which usually

strangled and swallowed them. The same as their par-

ents, young Mandarin Rat Snakes grew fast and by

December they were about 1.5 times their hatching

size.

Starting from 1993 , the same pair of snakes pro-

duced three clutches from which more than 15 young

hatched. The general incubating routine was more or

less the same and most eggs hatched successfully,

with typical sex ratio being 2:1 (males:females).

Conclusions

Basing upon our 6-year experience with Mandarin

Rat Snakes, we consider this species not as difficult to

maintain and to breed in captivity as the general pub-

lic perception believes it to be, of course, provided the

animals are either captive bred or. if they are wild-

caught, are treated for parasites immediately upon

arrival. Antibiotic prophylaxis is also very advis-

able. Temperature requirements are of vital impor-

tance as, if overheated, these snakes tend to become ill

and die rather fast. It also should be noted that Man-

darin Rat Snakes are easily stressed and for successful

husbandry they should be provided with enough shel-

ters and better are kept separately.

Literature Cited

Fleck. J. 1985. Bemerkungen zur Haltung von

Elaphe mandarinus (Cantor, 1842) (Serpentes:Colu-

bridae). Salamandra 21 (2/3): 157-160.

Trutnau. L. 1980. Schlangen 1. Stuttgart

(Ulmer):185-186.

1997

Asiatic Herpetological Research

Vol. 7, pp. 87-92

Population Dynamics and Growth in a Natural Population of

Limnonectes limnocharis ( Anura: Ranidae)

ASHIS. K. MOHANTY1, NlNA SlNGH2 AND SUSHIL K. DUTTA2

/College of Basic Sciences and Humanities, Orissa University of Agriculture and Technology. Bhubaneswar,

Orissa, India; IDepartment of Zoology, Utkal University, Bhubaneswar-751004, Orissa, India

Abstract. -The study is based on measurement of specimen, collected from nature over a period of 12 months,

during 1987-88. Based on the size, the juveniles, mature males and gravid females were divided into various size

groups. Except the juveniles, the female size groups were comparable with the males. In addition, the females

are comparatively larger than the males of the same age group. The availability of various size groups during

different months of a year, is attributed to the continuous growth of the species in natural population

Ke\ words: Anura. Limnonectes limnocharis. population, growth.

Introduction

The first available information on growth study of

anurans was by Wright (1914), who analyzed growth

pattern of Rana pipiens and Rami catesbeiana. Since

then, several other studies (Wright. 1920; Flower,

1925; 1936: Force. 1933; Hamilton. 1934; 1955;

Raney and Ingram, 1941; Cowan, 1941; Raney and

Lachner, 1947; Wilson, 1950: Ting. 1951: Ryan,

1953; Fitch, 1956a; 1956b; Jameson. 1956; Martof,

1956; Cohen and Howard. 1958: Durham and Ben-

nett, 1963; Schroeder and Baskett, 1968) reported the

growth pattern of anurans either in captivity or in nat-

ural environment by analyzing individuals. Turner

(1960) reviewed all the above literature on anuran

growth and since then additional data has become

available for Bufo hemiophrys (Breckenridge and

Tester. 1961), Rana sylvatica (Bellis, 1961). Rana

arvalis (van Gelder. 1973; van Gelder and Oomen.

1970). Rana erythraea (Brown and Alcala, 1970),

Rana septentrionalis (Hedeen. 1972), Bufo boreas

(Lillywhite et al., 1973) and Bufo woodhousei fowleri

(Clarke. 1974). All the above studies (except Brown

and Alcala, 1970) deal with anurans from temperate

zones. The present study is the second one for any

Indian anurans. The first study was conducted by

Sahoo ( 1991 ) on Bufo melanostictus.

Materials and Methods

A total of 962 specimens (388 males. 267 females and

307 juveniles were collected over a period of 12

months, from a perennial pond near village Chakei-

sani, Bhubaneswar. India. Specimens ranging from

17.0-38.0 mm snout-vent length (SVL). were sexed

and the rest were treated as juveniles.

Results

Out of 962 specimens sampled, the lowest (43) and

the highest (110) captures were during March and

September respectively. The ratio of male to female

for each month

indicated more males than females, except during

the month of February, when the number of males

were slightly less than that of the females. Cumula-

tive ratio was also indicative of more males. The pop-

ulation dynamics of juveniles indicated maximum

(53) during the month of June (Table 1). Further,

juvenile population decreased drastically from

December through January and no juveniles were col-

lected during February and March. The low popula-

tion density of juveniles during December and

January and non-availability during February and

March is associated with non-breeding season,

because, basically the species breeds during monsoon

period (June-August) when the number of juveniles in

the natural population is more than non-breeding

months.

To analyze the growth pattern in natural popula-

tion, size range of juvenile (J), males (M) and females

(F) were recorded (Table-2) and divided into various

size groups (Table-3). Specimens measuring a maxi-

mum of 16.0 mm were not sexed and were considered

as juveniles. The lowest SVL (8.0 mm) of juveniles

from April through September is attributed to meta-

morphosis time of the species during these months,

because the metamorphosing froglets were found to

be with a SVL of about 8.0 mm. Based on SVL, the

juveniles were divided into two size groups (8.0-11.0

mm and 12.0-16.0 mm). Both the size groups were

found from May to October and the former was also

Vol. 7, p.

Asiatic Herpetological Research

1997

available during April. This is indicative of early

breeding of the species, because metamorphosed fro-

glets were found during this month. From November

until January, the larger size group juveniles were

found and this indicated growth in size.

A total of 388 males were collected over a period

of 12 months (Table 1) and the SVL ranged from 17.0-

36.0 mm. All the males were grouped into three size

groups (17.0-22.0 mm: 23.0-30.0 mm and 31.0-36.0

mm) and the first two size groups were available dur-

ing all the months (except three specimens of the third

group which were collected during May). The above

data indicated that both the juvenile, maturing and

mature males of various sizes were found in nature.

The data on female population is comparable with

males, except the lower number (267) of the former,

which is typical for the species. Like males, the

females were also grouped into three similar size

groups and all the size groups were available through-

out the year. However, the number of two smaller size

groups were less than the largest size group of

females. The above population trend and size range is

also indicative of continuous growth of the species in

natural environment.

Discussion

Several previous studies (refer to introduction)

reported the growth pattern of temperate climate spe-

cies of anurans and some of these studies (Wright,

1914; Breckenridge and Tester, 1961; Bellis, 1961;

Hedeen, 1972: Lillywhite et al.. 1973; Clarke, 1974)

provide data on specific species. Turner's (1960)

review of available data on anuran growth pattern sug-

gested that most of the studies have either been con-

ducted in captivity or in natural populations, by

analyzing marked individuals.

In general, growth rates of anurans have been

determined in three ways, depending on measurement

of 1. preserved materials. 2. captive individuals and 3.

individuals either marked or samples taken from the

same natural population at different times during the

same growing season (Turner. 1960). The present

analysis of growth pattern ofL. limnocharis fits to the

third category, because specimens of L. limnocharis

were collected from their natural population over a

period of 12 months. Further, the sampling method

adopted was random. A total of 962 specimens (307

juveniles, 388 males and 267 females) were sampled

and the data indicated maximum number of juveniles

collected during the month of June (Table 1). This

could obviously be due to metamorphic event of the

species during June. Dash and Mahanta ( 1993). while

studying the community structure of ten anurans in

natural populations, reported that L. limnocharis is the

dominant anuran in paddy fields. Hence, the avail-

ability of more juveniles than males and females dur-

ing May-September could be compared with

population dynamics data of the species reported by

Dash and Mahanta (1993).

Acknowledgments

We would like to express our sincere gratitude to Mr.

N. K. Acharya for statistical analysis of data and prep-

aration of illustrations. Financial assistance from the

CSIR, New Delhi (Grant No. 37 (0843)/94/EMR-II )

to S. K. D. is gratefully acknowledged.

Appendix I

Tables 1-3

Table 1. Cumulative data on population size of specimens of L. limnocharis collected for 12 months.

(Continued)

1997

Asiatic Herpetological Research

Vol. 7, p. 89

Table 2. Cumulative data on size range, mean and Standard Deviation of specimens of L. limnocharis

collected for 12 months.

Year/Month

Sex

SVL Range (mm)

Mean±SD(mm)

1987

April

May.

June

July

August

September

J

M

F

J

M

F

J

M

F

J

M

F

J

M

F

J

M

F

8.0- 10.0

20.0 - 29.0

31.0-38.0

8.0- 16.0

18.0-36.0

21.0-36.0

8.0- 16.0

18.0-28.0

27.0 - 38.0

8.0- 16.0

18.0-30.0

18.0-35.0

10.0- 16.0

18.0-29.0

18.0-34.0

8.0- 16.0

17.0-30.0

17.0-38.0

8.625 + 0.719

25.455 ± 2.559

34.750 ± 2.543

10.568 ± 2.526

25.645 ± 4.742

31.933 ±5.284

1 1.528 ±2.2fl7

23.621 ±3.201

31.18213.842

U.619±2.214

22.83913.928

26.423 ± 5.934

12.612 ± 1.850

24.793 ± 2.920

27.828 ±4. 167

11.773 ±2.530

23.262 ±3.818

31.333 ±7.516

(Continued)

10.0- 16.0

17.0-28.0

29.0 - 38.0

14.0- 16.0

17.0-27.0

18.0-36.0

15.0- 16.0

17.0-24.0

18.0-36.0

16.0

18.0-30.0

18.0-38.0

19.0-29.0

19.0-36.0

20.0 - 28.0

20.0-35.0

12.96 ± 1.670

23.71A + 3.266

32.333 ± 3.068

14.909 ±0.750

22.543 ±2.941

29.44R ± 5.736

15.889 ±0.333

19.667 ± 1.795

26.167 ±6.635

16.000 ±0.0

23. 125 ±4.098

27.032 ±7,276

22.903 ±4.2 1 5

24.667 ± 6.623

22.923 ±2.481

26.000 ±5.612

Literature Cited

Bellis. E. D. 1961. Growth of the wood frog. Rana

sylvatica. Copeia 1961:74-77.

Breckenridge. W. J. and J. R. Tester. 1961. Growth,

local movements and hibernation of the Manitoba

toad, Bufo hemiophrys. Ecology 42:637-646.

Brown. W. C. and A. C. Alcala. 1970. Population

ecology of the frog Rcma erythraea in southern

Negros. Philippines. Copeia 1970:611-622.

Clarke. R. D. 1974. Post-metamorphic growth rates

in natural population of Fowler's toad, Bufo wood-

housei fowleri. Canadian Journal of Zoology

52(12): 1489-1498.

Cohen. N. W. and W. P. Howard. 1958. Bull frog

food and growth at the San Joaquin Experimental

Range, California. Copeia 1958:223-225.

Cowan, I. M. 1941. Longevity of the red-legged frog.

Copeia 1941(1 ):48.

Dash, M. C. and J. K. Mahanta. 1993. Quantitative

analysis of the community structure of tropical

amphibian assemblages and its significance to conser-

vation. Journal of Bioscience 18(1 1:121-139.

Fitch, H. S. 1956a. A field study of the Kansas ant

eating frog, Gastrophryne olivacea. University of

Kansas. Publications. Museum of Natural Hististory

8(4):275-307.

Fitch. H. S. 1956b. Early sexual maturity and lon-

gevity under natural conditions in the Great Plains

narrow-mouthed frog. Herpetologica 12:281-282.

Flower, S. S. 1925. Contributions to our knowledge

of the duration of life in vertebrate animals-II. Batra-

chians. Proceedings of the Zoological Society of

London 1925:269-289.

Flower. S. S. 1936 Further notes on the duration of

life in animals-II. Amphibians. Proceedings of the

Zoological Society of London 1936:369-394.

Force, E. R. 1933. The age of attainment of sexual

maturity of the leopard frog, Rcma pipiens in north

Michigan. Copeia 1933(31:128-131.

Hamilton, W. F, Jr. 1934. The rate of growth of the

toad (Bufo americanus americanus) under natural

conditions. Copeia 1934(2):88-90.

Hamilton. W. F. Jr. 1955. Notes on the ecology of

the Oak toad in Florida. Herpetologica 1 1:205-210.

Hedeen. S. B. 1972. Postmetamorphic growth and

reproduction in the mink frog. Rana septentrionalis

Baird. Copeia 1972:169-175.

Jameson, D. L. 1956. Growth, dispersal and survival

of the Pacific tree frog. Copeia 1956( 1 ):25- 29.

Lillywhite. H. B., P. Licht and P. Chelgren. 1973.

The role of behavioral thermoregulation in the growth

energetics of the toad. Bufo boreas. Ecology 54:375-

383.

Martof. B. M. 1956. Growth and development of the

green frog, Rana clamitans, under natural condi-

tions. American Midland Naturalist 55( 1 ): 101-1 17.

Raney, F. S. and W. M. Ingram. 1941. Growth of

tagged frogs (Rana catesbeiana Shaw and Rana clam-

itans Daudin) under natural conditions. American

Midland Naturalist 26( 1 ):20 1 -206.

Raney, F. S. and E. A. Lachner. 1947. Studies on the

growth of tagged toads (Bufo terrestris americanus).

Copeia 1947(2): 1 13-1 16.

Ryan. R. A. 1953. Growth rates of some ranids under

natural conditions Copeia 1953(21:73-80.

Vol. 7, p. 92

Asiatic Herpetological Research

1997

Sahoo, G. 1991. Growth in natural population of

Bufo melanostictus. M. Phil, dissertation. Utkal Uni-

versity.

Ting. Han-Po. 1951. Duration of the tadpole stage of

the green frog. Rana clamitans. Copeia 195K 1 ):82.

Turner. F. B. 1960. Post metamorphic growth in

anurans. American Midland Naturalist 64(2):327-

338.

Van Gelder.T. J. 1973. Ecological observations on

Amphibia in the Netherlands II. Triturus helveticus:

migration, hibernation and neoteny. Netherlands

Journal of Zoology 23( 1 ):86-108.

Van Gelder, J. J. And H. C. J. Oomen. 1970. Ecolog-

ical observations on Amphibia in the Netherlands. I.

Rana arvalis Nilsson: Reproduction, growth, migra-

tion and population fluctuations. Netherlands Journal

of Zoology 20(2):238-252.

Wilson, M. A. 1950. Duration of life in Rana tempo-

raria. British Journal of Herpetology 3:66-68.

Wright. A. H. 1914. Life histories of the Anura of

Ithaca, New York. Carnegie Institute Publication

197:1-98.

Wright. A. H. 1920. Frogs: their natural history and

utilization. U. S. Bureau of Fisheries Document

888:1-44.

997

Asiatic Herpetological Research

Vol. 7, pp. 93-102

The Karyotypes of Megophryinae (Pelobatidae) with a Discussion on their

Classification and Phylogenetic Relationships

Ding-Qi Rao And Da-Tong Yang

Kunming Institute of Zoology, Academia Sinica, Kunming 650223, China

Abstract. -The karyotypes of nine Megophryinae species from China were studied. Megophrys omeimontis Liu

has 2n=26 with 5 large, 1 moderate and 7 small pairs. 8M+3SM+2ST. NF=52, 1 secondary constriction in 6p.

Megophrys giganticus Liu has 2n=26 with 5 large and 8 small pairs. 5M+5SM+2ST+1T, NF=48. Megophrys

minor Stejneger has two different forms. One is 2n=26 with 6 large and 7 small pairs. 8M+2SM+2ST. NF=52;

the other is 2n=30 with 6 large and 9 small pairs. The large group is identical to that of the 2n=26 form.

8M+2SM+3ST+2t, NF=56. Megophrys kuatunensis Pope has 2n=24 with 6 large and 6 small pairs.

5M+2M(SM)+2SM+3ST. Megophrys lateralis (Anderson) from Tengchong. Yunnan has 2n=26 with 6 large and

7 small pairs, 8M+3SM+2ST, NF=52. Megophrys lateralis (Anderson) from Hekou, Yunnan has 2n=26 with 6

large and 7 small pairs, 5M+1M(SM)+4SM+2ST+1T Megophrys parva Boulenger has 2n=26 with 6 large and

7 small pairs, 4M+5SM+1SM(ST)+3T, one secondary constriction 1Q; few metaphases with 2n=26+l and 4 pair

of T chromosomes. Megophrys palpebralespinosa Bourret has 2n+26 with 5 large and 8 small pairs,

5M+4SM+1SM(ST)+2ST+1ST(T). Megophrys daweimontis sp. nov. Has 2n=26, 5 large and 8 small pairs,

6M+3SM+1SM(ST)+1ST+1ST(T), one secondary constriction in 6Q. Ophryophryne microstoma Boulenger has

2n=26 with 6 large and 7 small pairs, 7M+1M(SM)+2SM+1ST+T. The karyotype of O pachyprocta Kou

resembles that of O. microstoma.

Karyotypes of the Megophryinae can be divided into 5+8 and 6+7 types. The karyotype of M. omeimontis

appears to be an intermediate between 5+8 and 6+7. Combining the cytological, morphological and ecological

characters, the classification of Megophryinae can be reviewed. The genus Atympanophrys is probable only

needed to verify its main generic character. Brachytarsophrys and Ophryophryne are valid genera. Megophrxs

can be divided into four groups: 1. M. giganticus, II. M. montana and M. nasuta, III. M. palpebralespinosa and

M. daweimontis sp. nov., IV. Other species generally with small-sized bodies and 6+7 karyotypes. M. giganticus

should probable belong to the genus Atympanophrys; a new genus should be erected for groups III and IV.

whereas Megophrys should refer only to group II. A new species, M. daweimontis. is described below.

Key words: Megophryinae, Brachytarsophrys. Megophrys. Ophryophryne. karyotype, classification,

phylogenetic relationships, Megophrys daweimontis sp. nov.

Materials and Methods

Megophrys lateralis were collected from Tengchong.

Yunnan in 1991 and Hekou. Yunnan in 1993; M. ome-

imontis and M. minor from Jingdong, Yunnan in June.

1990 and May, 1991; M. giganticus from Jingdong in

May, 1991; M. palpebralespinosa and M. daweimon-

tis sp. nov. From Kekou, Yunnan in July 1993; M.

parva and Ophryophryne pachyprocta from Mengla,

Yunnan in May 1993; M. kuatunensis from Chongan

and Dehua, Fujian; . O. microstoma from Hekou.

Yunnan in June 1992 and July, 1993. All the speci-

mens were brought alive to the laboratory for karyo-

typing.

Specimens were injected intraperitoneally with

colchicine at a dosage of 20 ug/g body-weight. After

24 to 36 hours the femur and tibia bones were

removed and the ends cut off. The marrow cells were

then washed out with \c/c tri-sodium citrate solution,

ground in hypotonic 0.64% KG solution and fixed in

3: 1 solution of methanol;acetic acid for two periods of

20 minutes each. Slides were prepared by the air-dry-

ing method and stained with 10% Giemsa PBS for

about 20 minutes.

Chromosomes were divided into 4 groups accord-

ing to the ratio of long arm/short arm in length: M=

metacentric, the ratio is 1-1.7; SM= submetacentric.

1.7-3.0; ST= subtelocentric. 3.0-7.0; T= telocentric,

more than 7.0. Chromosomes designated M, SM and

ST possess 2 arms and those designated T possess

only 1 arm. The fundamental number (NF) represents

the total arm numbers for all chromosomes in one

karyotype.

Vol. 7, p. 94

Asiatic Herpetological Research

1997

Results

The karyotype of M. lateralis from Tengchong, north-

west Yunnan has 2n=26; 6 large and 7 small pairs;

Nos. 3. 1 1 and 12 are SM, Nos. 8 and 13 are ST. the

rest are M and NF=52. There are no satellite or sec-

ondary constrictions (Fig. 3c). This karyotype mostly

agrees with that recorded by Wu ( 1987) for M. latera-

lis.

The karyotype of M. lateralis (Anderson) from

Hekou. Yunnan is 2n=26; 6 large and 7 small pairs;

Nos. 1.5, 6. 10 and 1 1 are M, Nos. 2. 3, 7. and 12 are

SM, Nos. 8 and 9 are ST, No. 13 is T No. 4 can be M

or SM and NF=52. Sometimes one secondary con-

striction is close to the centromere of the short arm of

No. 2 (Fig. 3). This karyotype is different from that of

specimens from Tengchong. Yunnan, especially in

Nos. 2, 7, 9, and 13, and the location of the secondary

constriction (it is in 5p in the results of Wu. 1987).

We think that a morphological comparison should be

made between the two populations as part of any eval-

uation of their specific status.

The karyotype of M. omeimontis from Jingdong,

Yunnan has 2n=26; 5 large, 1 moderate, and 7 small

pairs; Nos. 3. 7 and 12 are SM. Nos. 8 and 13 are ST.

the rest are M and NF=52. One secondary constric-

tion was near the base of the short arm of No. 6; there

is no satellite (Fig. 3d). This karyotype agrees with

that reported by Zheng and Wu (1989) for M. omei-

montis based upon a population from Mt. Omei in

Sichuan, but their results indicate that the secondary

constriction was in the long arm of No. 6.

The karyotype of M. giganticus is 2n=26; 5 large

and 8 small pairs are obvious; Nos. 2. 3. 4. 7 and 12

are SM, Nos. 9 and 1 3 are ST. No. 8 is T the rest are

M and NF=48. No satellite or secondary constrictions

were found (Fig. 3e). This karyotype is not the same

as that recorded by Li et al.. ( 1993) for M. giganticus.

Recognition of 5 large and 8 small pairs is the same as

the karyotypes of Brachytarsophrys.

The karyotype of M. minor is variable in speci-

mens from the same locality in Jingdong. One karyo-

type is 2n=26; 6 large and 7 small pairs; Nos. 7 and 13

are SM, Nos 8 and 12 are ST, the rest are M and

NF=52. No satellite or secondary constrictions were

found (Fig. 3a). The second karyotype is 2n=30; 6

large and 9 small pairs. The large chromosomes are

identical to those of the 2n=26 form, but the small

ones are different. Among them Nos. 7 and 10 are

SM, Nos. 8, 12 and 13 are ST, Nos. 14 and 15 are T.

the rest are M and NF=56 (Fig. 3b).

The karyotype of M. kuatunensis Pope is 2n=24; 6

large and 6 small pairs; Nos. 1, 2, 6, 10 and 1 1 are M,

Nos. 5 and 8 are SM, Nos. 7, 9 and 12 are ST, Nos. 3

and 4 can be M or SM and NF=48. No satellites or

secondary constrictions were found. It is the only

karyotype where 2n=24 in the Megophryinae. Further

study is needed to evaluate the taxonomy of this spe-

cies (Fig. 3j).

We found the karyotype of M. parva Boulenger to

be 2n=26; 6 large and 7 small pairs: Nos. 1, 2. 3. 4 and

5 are SM, Nos. 6, 7, 8 and 10 are M, Nos. 1 1. 12 and

13 are T, No. 9 varies between SM and ST and

NF=46. One secondary constriction is near the cen-

tromere of the long arm of No. 1 (Fig. 3h). A few

metaphases with 2n=26+l and 4 pair of T chromo-

somes were found. This karyotype is different than

that recorded by Li et al. ( 1993) from the same locali-

ties, especially in the arm length for large chromo-

somes, and the location of the secondary constriction

(5q in the Li et al. result).

The karyotype of M . palpebralespinosa Bourret is

2n=26; 5 large and 8 small pairs; Nos. 1, 2, 4. 5 and

12 are M, Nos. 3, 6, 8 and 10 are SM, Nos. 7 and 13

are ST, No. 9 varies between ST and T No. 1 1 can be

SM or ST and NF=52 or 50. No satellites and second-

ary constrictions were found (Fig. 3g).

The karyotype of M. daweimontis sp. Nov. Is

2n=26; 5 large and 8 small pairs; Nos. 1, 2, 4, 5, 9 and

13 are M. Nos. 3. 6 and 8 are SM, No. 12 is ST, No. 7

varies between ST and T and No. 10 can be SM or ST

and NF -52 or 50. One secondary constriction is close

to the centromere of the long arm of No. 6.; This kary-

otype is similar to that of M. palpebralespinosa (Fig.

3f).

The Karyotype of Ophryophryne microstoma

Boulenger is 2n=26; 6 large and 7 small pairs; Nos. 1,

2. 4, 5, 6. 8 and 10 are M, Nos. 3 and 7 are SM, No. 9

is ST, Nos. 12 and 13 are T, No. 1 1 can be M or SM

and NF=48. No satellites and secondary constrictions

were found (Fig. 3k). This karyotype is similar to the

6+7 type of some Megophrys species.

The karyotype of Ophryophryne pachyprocta Kou

resembles most closely that of O. microstoma: 2n=26;

6 large and 7 small pairs. The metaphase preparation

for O. pachyprocta is not good enough to provide a

plate here.

Discussion

Although Megophrys omeimontis is widely distrib-

uted in southwestern China, its type locality is Mt.

Omei. Sichuan. In Table 1, its karyotypes come from

two populations (Mt. Omei and Mt. Wuliang) and

they are very similar: all are with 5 large, one moder-

ate and 7 small pairs. One secondary constriction

1997

Asiatic Herpetological Research

Vol. 7, p. 95

occurs in the moderate sized No. 6. Two differences

exist. Zheng and Wu (1989) considered No. 6 large,

but it should be called moderate according to the rela-

tive length which they measured. The secondary con-

striction is in a short arm. Probably the two

populations from Mt. Omei and Mt. Wuliang belong

to one species. Fei et al. ( 1990) recognized the popu-

lation from Mt. Wuliang as a separate species, M.

jingdongensis.

The karyotype of Megophrys giganticus is of the

5+8 type, the same as those of the Brachytarsophrys

species and Atympanophrys shapingensis. Further

research is needed on the systematic positions of M.

giganticus and A. shapingensis.

Megophrys kuatunensis is the only Megophryinae

species discovered which has 2n=24. This karyotype

is the 6+7 type since it has 6 large pairs of chromo-

somes. This species only occurs on Mt. Chongan and

Mt. Daiyun. Dehua. Fujian Province, China, at the

eastern edge of the distribution of the Megophryinae.

Three karyotypes occur in M. lateralis (see Table

1 ). Form I and II, based on the specimens from

Tengchong, northwest Yunnan, are generally identical,

but both of them are different from Form III in chro-

mosome No. 2 and chromosome No. 13, and the loca-

tion of the secondary constriction which is in the

terminal short arm of chromosome No. 5 in form I,

but in the base of the short arm of No. 2 in form III.

Form III is based on the specimens from Hekou.

southeast Yunnan, far away from Tengchong. The

taxonomic status of the Hekou population needs addi-

tional attention after comparing their morphology to

other populations.

Table 1. Karyotypes of some Megophryinae species.

(Continued)

Vol. 7, p. 96

Asiatic Herpetological Research

1997

Groups

Large Group

Smalll Group

* M. lateralis (II) and M. shapingensis are from Wu (1987); M. boettgen from Gao et al. 1990; B. sp. nov. (II) from

Tan et al. (1987, as B. carinensis); M. omeimontis (II) from Zheng and Wu (1989); M. giganticus (II) and M. parva

(II) from Li et al. (1993); M. nasuta (I) and M. monticola (synonym of M. montana) from Morescalchi et al. (1977);

M. nasuta (II) from Schmid et al. (1987). M. lateralis (II) based on specimens from Tengchong, Yunnan; M. latera-

lis (III) based on specimens from Hekou, Yunnan; M. giganticus (I), B. sp. nov (I) and B. feae are from Rao and

Yang (in press).

Two different forms of karyotypes of Megophrys

parva are also shown in Table I; forms I and II are

based on the specimens from Mengla. Yunnan. This

species is more primitive in that it has 3 pairs of T

chromosomes in both forms. It may be primitive

because it is widely distributed in upper Burma and

southwest Yunnan.

Although Megophrys palpebralespinosa occurs

in Hekou, Yunnan, it is very close to M. hoettgeri of

Fujian in skin and color characters. They are very dif-

ferent in karyotype: the former has a 5+8 type karyo-

type while the later has a 6+7 type. M.

palpebralespinosa has tubercles on the outer edge of

the upper eyelids, folds on the back and a reddish

inner palm tubercles, while M. hoettgeri does not.

They are geographically widely separated. This sug-

gests that they are not closely related.

Megophrys daweimontis sp. nov. is like M. palpe-

bralespinosa in having a 5+8 karyotype, tubercled

upper eyelids and reddish inner palm tubercles, and

both occur on Mt. Dawei.

It is interesting that Megophrys palpebralespinosa

and M. daweimontis sp. nov. Have 5+8 type karyo-

types. Generally the 5+8 type karyotype occur in spe-

cies which are large-sized and possess a hidden

tympanum, such as M. nasuta. M. monticola (syn-

onym of M. montana), M. giganticus, M. shapingensis

and Brachytarsophrys species. Species with small-

sized bodies and a distinct tympanum generally have

6+7 karyotypes common in the Megophryinae. M.

palpebralespinosa and M. daweimontis sp. nov. are

relative small; body length is about 35 mm. In males

and 40 mm. In females. Additional study of their tax-

onomic position is needed.

Karyotypes of Ophryophryne microstoma and O.

pachyprocta are of the 6+7 type, the same as those of

Megophrys species which are generally small-sized.

These observations agree with Dubois (1980) who

considered Ophryophryne a subgenus of Megophrys.

However, on the basis of other characters, habitats and

habits, which are different from other Megophryinae

species, we recognize this genus as valid and separate.

According to Kou (1985), O. pachyprocta has a bump

above the anus. We think this bump is probably the

protruding coccyx and O. microstoma also has a pro-

truding coccyx. On the basis of this character, we

think that the two species should be recognized as a

single species.

The main differences among the species are

shown in Table 1. But another should be noted:

Megophrys hoettgeri has a secondary constriction in

6q and M. shapingensis also has one near the cen-

tromere of 1 q.

1997

Asiatic Herpetological Research

Vol. 7, p. 97

Megophrys minor from Jingdong, Yunnan has var-

ious karyotypes, but we can't find anatomical differ-

ences between the different specimens with different

karyotypes. Karyotype variation is common in Pelo-

batidae. such as Leptolaylax pelodytoides (Li et al..

1991). Because there are various karyotypes in the

same species, it is difficult to identify a species

according to its karyotype, especially for some widely

distributed species, such as M. lateralis, M. omeimon-

tis and M. minor. In contrast, some Pelobatidae have

very stable karyotypes with simple chromosome

arrangements and secondary constrictions, such as

Oreolaxax, Scntiger and Yibrissaphora. The karyo-

types of some genera are variable, such as Leptolaylax

and some Megophrys species. Thus, karyotypes can

be used to resolve some taxonomic problems in some

genera, but not in others. In general, karyotypic varia-

tion in Megophryinae occur among small chromo-

somes, while the large chromosomes are relatively

invariable. The karyotypes of Megophryinae species,

which are similar in morphology and habitats, are rel-

atively similar. So karyotypic characters can be used

for taxonomic purposes to separate genera and for

evolutionary analyses.

Up to now, karyotypes of 16 species (about 2/3 of

total) of Megophryinae have been obtained (Table 1).

They can be generally divided into two types on the

basis of the numbers of large and small chromosomes:

6+7 and 5+8. Brachytarsophrys feae, B. sp. nov.,

Megophrys shapingensis (previously Atympanophrys

shapingensis), M. giganticus, M. nasuta, M. monti-

cola (synonym of M. montana), M. daweimontis sp.

nov.. and M. palpehralespinosa have the 6+7 pattern,

whereas M. parva, M. lateralis, M. minor, M. boet-

tgeri, Ophryophryne microstoma and O. pachyprocta

have the 6+7 pattern. Although M. kuatunensis has 6

large and 6 small pairs it belongs to the 6+7 type. M.

omeimontis has 5 large. 1 moderate and 7 small pairs.

Thus it seems this pattern is intermediate between 5+8

and 6+7 types. In morphology M. omeimontis is sim-

ilar to species which share the 5+8 pattern.

Morescalchi (1973, 1977) thought that the 5+8

pattern was derived from the 6+7 pattern through the

lose of a fragment from one of its large chromosomes

(usually No. 6).

The No. 6 chromosome of M. omeimontis is pecu-

liar (see Fig. 3d). It seems that this chromosome is

easily broken at the site of secondary constriction in

the short arm and becomes 5+8 if the separated part is

lost. This hypothesis supports the conclusion of

Morescalchi with respect to the evolution of karyo-

types in Pelobatidae. The karyotype of M. omeimon-

tis should be considered derived from the 6+7 type.

We suggest that one of the large chromosomes trans-

ferred a fragment to a small chromosome and the

large one became small. The small one (T or ST chro-

mosome) became the No. 6. The transferred fragment

is the satellite on the short arm of No. 6 and it retains

the former body type in morphology because the frag-

ment is not lost. If the chromosomal fragment was

lost, then the karyotype would have resembled the

5+8 pattern.

All the large sized species have 5+8 type karyo-

types. While the species which are generally small

sized have two karyotypic patterns. Megophrys

palpehralespinosa and M. daweimontis sp. Nov. Have

a 5+8 pattern, and the other Megophrys and

Ophryophryne species have a 6+7 pattern.

It is interesting that M. giganticus, Atympanophrys

shapingensis, Brachytarsophrys species. M. nasuta

and M. monticola have not only the same type (5+8)

of karyotype, but also similar morphological charac-

ters and habitats; i. e. very large bodies; very large,

wide and flat heads; a hidden tympanum, round digi-

tal tips; and usually sit under stones at the edges of

streams during the breeding season (Bourret. 1942;

Inger, 1954; ^966; Liu and Hu, 1961; Tian et al..

1986; Yang et al.. 1991).

The Classification of Megophryinae

The megophryinae is currently divided into 4 genera:

Atympanophrys, Brachytarsophrys, Megophrys, ami

Ophryophryne. Some recent researchers think that

the genus Atympanophrys is not valid because its

main distinguishing character (no tympanum) is

wrong and this genus should be a synonym of

Megophrys (Fei et al. 1990). A. shapingensis has a

unique karyotype as well as other morphological

characters. This genus has a 5+8 karyotype, relatively

large sized body, relatively flat and wide head, a hid-

den tympanum and round digital tips. It occurs

always under stones at the sides of streams.

Brachytarsophrys includes three species (Rao and

Yang, in press): B.feae (previously M.fcae), B. carin-

ensis and a new species from China. B. feae and the

new species have 5+8 karyotypes. It is probable that

B. carinensis also have this kind of karyotype. All the

species in this genus have very large sized bodies,

widened and flattened heads, a hidden tympanum,

shortened legs and horny-bearing eyelids. They occur

under stones at the sides of streams. In our opinion,

this genus is valid.

Ophryophryne has three species: O. microstoma,

O. pachyprocta and O. pollard. The former two have

6+7 karyotypes. All the species in this genus have

small bodies, marrow mouths, small high heads, a dis-

Vol. 7, p. 98

Asiatic Herpetological Research

1997

tinct tympanum, and tubercled eyelids. They are usu-

ally found on grass and leaves beside very small

streams (this is unique among the Megophryinae).

This genus is valid, and it is related to the species of

Megophrys which have 6+7 karyotypes.

Megophiys is a large genus, with about 22 species.

Their body forms are varied. The karyotype patterns

differ. M. giganticus is very large, it has 5+8 karyo-

type, an obviously wide and flat head, a hidden tym-

panum, and round digital tips. The habitats and habits

for this species are similar to those of Brachytar-

sophrys and A. shapingensis. M. montana (including

former M. monticola), and M. nasuta all have 5+8

karyotypes, broad heads, relatively short legs, an

indistinct or hidden tympanum similar to Brachytar-

sophrys. However, they have elongate free dermal

flaps on the snout and long soft horn-like appendages

on the eyelids. Their habitats and habits are similar to

Brachytarsophrys. The genus Megophrys was first

described on the basis of the type, M. montana.

Megophrys palpebralespinosa and M. daweimon-

tis sp. nov. have 5+8 karyotypes, a small sized body

tubercled eyelids, reddish inner palm tubercles, and

widened and sucker-like digital tips. They are usually

found on grass at the sides of small streams. The rest

of Megophrys. including M. lateralis, M. minor, M.

kuatunensis, M. parva and M. hoettgeri have 6+7

karyotypes, are generally moderate or small in body

size, with regular body forms and head, a distinct

tympanum, no tubercles on the eyelids, and widened

and sucker-like digital tips. They are found on stones

or roots at the sides of streams or rivers. Although M.

otneimontis seems to be intermediate between the 5+8

and 6+7 karyotype, it is similar to M. lateralis M.

parva in morphology, habitats and habits.

Thus, the species of Megophrys may be divided

into four groups according to their karyotypes, mor-

phology, habitats and habits: 1). M. montana and M.

nasuta: 2). M. giganticus; 3. M. palpebralespinosa

and P. daweimontis sp. nov.; 4). M. lateralis, M. omei-

montis, M. pan'a, M. minor, M. kuatunensis, M. boet-

tgeri and probably including M. uankianensis, M.

kempii, M. baluensis, M. aceras, M. brachykolos and

M. robust a.

Because of these differences in karyotype and

morphology, we recognize a new genus for the M. lat-

eralis and the M. omeimontis group. Megophrys

should be restricted to the M. montana and M. nasuta

group. The M. lateralis group is generally small in

size, the heads are not wide, tympanum is present,

legs long, digital tips flat and sucker-like, temporal

fold thin and bent, and a 6+7 karyotype. Frogs of this

group are usually found sitting on rocks next to rivers.

The M. montana group is somewhat similar to

Brachytarsophrys in cytology, morphology and habi-

tats: 5+8 karyotype, very large body, wide and flat

head, a hidden tympanum, straight and thick temporal

fold, transverse shoulder groove, and short legs: but it

is different in lacking tubercles on the upper eye-lid.

As for M. giganticus, it is narrowly distributed in

Jingdong and Yondge. Yunnan. It is similar in mor-

phology to A. shapingensis with digital tips round,

hidden tympanum, wide and flat hear, straight and

thick temporal folds, and 5+8 karyotype. M. giganti-

cus is different than Brachytarsophrys and the M.

montana group in having much longer legs, lacking

any elongated tubercle on the upper eye-lid and no

transverse groove on the shoulder. We suggest that M.

giganticus should be placed in the genus Atympa-

nophrys along with A. shapingensis.

Megophrys palpebralespinosa and M. daweimon-

tis sp. nov. are more similar to the M. lateralis group

even though they have 5+8 karyotypes. But they have

tubercles on the upper eye-lid and reddish inner palm

tubercles, which is different from the M. lateralis

group. These species may be derived from an ances-

tor with 6+7 karyotype.

Based on the above information. Megophryinae is

reviewed below:

1 . The genus Brachytarsophrys is valid and it contains

three species: B. carinensis, B. feae and B. sp. nov.

(Rao and Yang. 1996). The type species if B. feae.

2. The genus Ophryophryne is valid and it contains

three species: O. microstoma. O. pachyprocta and O.

poilani. The type species is O. microstoma.

3. The genus Megophrys should be confined to the M.

montana group. It includes two species: M. montana

and M. nasuta. The type species if M. montana.

4. Atympanophrys should be re-named and its diagno-

sis should be revised. The genus should include M.

giganticus.

5. A new genus Panophrys should be recognized for

the Megophrys lateralis and M. omeimontis group. Its

type species is P. omeimontis. This new genus can be

distinguished on the basis of small size, tympanum

present, head not very wide and flat, long legs, upper

eye-lids tubercles absent (except for P. palpebralespi-

nosa and P. daweimontis). temporal fold thin and

bent, digital tips flat and sucker-like. They are usually

found on rocks.

As for the relationships of this subfamily, two

branches are recognized (Fig. 1): one for Brachytar-

sophrys, Megophrys, and Atympanophrys and

another for Panophrys and Ophryophryne. The two

1997

Asiatic Herpetological Research

Vol. 7, p. 99

E

2-

Figure 1 . Evolutionary tree of Megophrymae.

Figure 2. Megophrys daweimontis sp. nov. female

X 1.

branches diverged early in megophryine evolutionary

history. Both branches share almost the same distri-

bution.

Description of a New Species

The specimens collected from Mt. Dawei, Pingbian

County, southeast Yunnan are similar to specimens of

M. brachykolos, M. parva and M. longipes., but they

have horn-like tubercles on the eyelids and the head is

not flattened. In this character they can be distin-

guished from M. parva. The Mt. Dawei specimens

have relatively long legs where the heals can overlap

when the flexed legs are held at right angles to the

body axis. The specimens have markings on the

backs for heads and trunks, which are different from

those of M. brachykolos. These markings are similar

to those similar to those of M. longipes. According to

Taylor (1962), M. longipes has rudimentary webs

between the toes, no metatarsal tubercles, upper eye-

lids with small horn-like tubercles, and a body length

of 47 mm in males and 65 mm in females: whereas

the specimens from Mr., Dawei lack metatarsal tuber-

cles, have smaller tubercles on the eyelids, lack webs

between the toes, and are shorter (37 mm in males and

45 mm in females). Therefore we recognize the spec-

imens from Mt. Dawei as a separate species.

Megophrys daweimontis sp. nov. (Fig. 2)

Holotype: KIZ 93088, adult male, collected from Mt.

Dawei, Pingbian County, southeast Yunnan, China.,

altitude 1900 m.. July, 1993.

Paratypes: 17 adult males (KIZ 93069-KIZ 93085)

and 3 adult females (KIZ 93086, KIZ 93087, KIZ

93089) collected at the same place and time as the

holotype.

Diagnosis: A small tubercle on outer edge of upper

eyelid; vomerine teeth present; snout projecting

beyond jaw; tibiotarsal articulation reaching tip of

snout; vocal sac in male; toes without rudiment of

web; an inner palm tubercle and very small outer

palm tubercle, a reddish inner metatarsal tubercle;

body length from stiout to vent 34-37 mm in males

and 40-46 mm in females.

Description: Tongue pyriform; vomerine teeth

present; head slightly wider than long, depressed;

snout very short; interorbital space concave; tympa-

num distinct, round. Arms long and slender, the first

finger extending beyond second; palm tubercles red-

dish, the inner tubercle is very large and the outer very

small. Legs long, the distal end of femur reaching

shoulder; tibiotarsal articulation reaching tip of snout;

toes slender, swollen at tips, completely without web-

bing. Superarticular tubercles lacking; a reddish outer

metatarsal tubercle.

Skin smooth above, with small warts on flanks and

sides of body; two pairs of delicate oblique folds on

the scapular region extending posteriorly to waist, a

pair of folds on the back-side; fold extending from eye

above tympanum to shoulder; upper eyelid with very

small tubercle on outer edge; lower surfaces smooth.

Olive-brown above, a triangular marking between

eyes, followed with V-shaped marking above shoul-

der, or X-shaped marking on the back of trunk; black

marking beneath the vent and behind heel; transverse

lines above thigh: inner lower surface of legs reddish.

Vol. 7, p. 100

Asiatic Herpetological Research

1997

Measurements of holotype are: 33.5 mm snout-

vent; 12.5 mm head length; 12.5 mm head width; 52.5

mm hind leg; 18 mm tibia.

Distribution: Known only from type locality.

Variation: Body length 33-37 mm in males and 40-

46 mm in females.

Literature Cited

Bourret, R. 1942. Les Batrachiens de l'Indochine.

Memoires de l'lnstitut Oceanographie de l'Indochine.

Hanoi 6:1-517.

Dubois, A. 1980. Notes sur la systematique et la rep-

arition des amphibiens anoures de Chine et des

regions avoisinantes. IV. Classification generique et

subgenerique des Pelobatidae Megophryinae. Bulle-

tin Mensuel Societe Linneenne Lyon 49(8):469-482.

Gao.J. M..B. R. Geng and M. Z. Cai. 1990. [Akary-

otypic study of Megophrys lateralis (Boulenger)].

Journal of Fujian Normal University (Natural Sci-

ence), Fuzhou, 6( 1 ):8 1 -84. ( In Chinese).

Inger, R. F. 1954. Systematics and zoogeography of

Philippine Amphibia. Fieldania: Zoology, Chicago

33(4): 181-531.

Inger, R. F. 1966. The systematics and zoogeography

of the Amphiba of Borneo. Fieldiana: Zoology, Chi-

cago 52:1-402.

Kou, Z. T. 1985. [A new species of genus

Ophryophryne- O. pachyprocta]. Acta Herpetologica

Sinica 4(l):41-43. (In Chinese).

Li, S. S.. L. Fei and C. Y. Ye. 1991. [Cytogenetic

studies on two Leptolala.x pelobatoids (Pelobatidae.

Anura) from China]. Acta Genetica Sinica 18(6):495-

499. (In Chinese).

Li, S. S., L. Fei and C. Y Ye. 1993. [a cytogenetic

study of three Megophrys species from Yunnan Prov-

ince]. Acta Genetica Sinica 20( 1 ):26-32. (In Chi-

nese).

Liu, C. C. and S. Q. Hu. [Tailless amphibians of

China]. Science Press, Beijing. 364 pp. (In Chi-

nese).

Morescalchi. A. 1973. Amphibia. Pp. 233-348 In A.

B. Chiarelli and C. Capanna (eds). Cytotaxonomy

and vertebrate evolution. Academic Press, New York.

Morescalchi, A., E. Olmo, and V. Stigo. 1977. Trends

of karyological evolution in pelobatoid frogs. Experi-

entia 33( 1 2 ): 1 577-1 567.

Schmid. M., L. Vitelli, and R. Batistoni. 1987. Chro-

mosome banding in Amphibia, XI. Constitutive het-

erochromatin. nucleolus organizers, 18S+28S and 5S

ribosomal RNA genes in Ascaphidae. Pipidae, Disco-

glossidae and Pelobatidae. Chromosoma (Berlin)

95:271-284.

Tan. A. M.. X. M. Zeng. G. F Wu. and E. M. Zhao.

1987. Cytotaxonomical studies on Chinese pelo-

batids, I. A preliminary study on the karyotype of

Brachytarsophrys carinensis and the variation in their

chromosome number]. Acta Herpetologica Sinica

6(2): 1-4. (In Chinese).

Taylor E. H. 1962. The Amphibia fauna of Thailand.

The University of Kansas Science Bulletin 63(8): 1-

599.

Tian, W. S. and Y M. Jiang (editors), assisted by G. F.

Wu. Q. X. Hu, E. M. Zhao and Q. Y Huang. 1986.

[Identification manual for Chinese amphibians and

reptiles]. Science Press, Beijing. 164 pp. (In Chi-

nese).

Wu, G. F 1987. [Cytotaxonomical studies on Chi-

nese pelobatids. III. The analysis of the karyotypes of

Megophrys lateralis and Atympanophrys shapingen-

sis]. Acta Herpetologica Sinica 6(3):45-48. (In Chi-

nese).

Yang. D. T. S. M. Li, W. Z. Liu, and S. Q. Lu. 1991.

[The Amphibia-fauna of Yunnan]. China Forestry

Publishing House, Beijing. 259 pp. (In Chinese).

Zheng, X. M. and G. F Wu. 1989. Cytotaxonomical

studies on Chinese pelobatids, V. The karyotypes, C-

bands and Ag-NORs of Megophrys omeimontis and

Oreolalax schmidti. Chinese Herpetological

Research 2(2):37-45.

1997 Asiatic Herpetological Research Vol. 7. p. 101

Appendix I

Figure 3. The karyotypes of Megophryinae species: A-B. Megopkrys minor: C. M. lateralis (Tengchong); D. M.

omeimontis; E. M. giganticus; F. M. daweimontis sp. nov.; G. M. palpebralespinosa; H. M. parva; I. M. latera-

lis (Hekou): J. M. kuatunensis; K. Ophryophryne microstoma.

A.

M n ii » it n

I0M

ti it an *• ii •*

J)|i(J|IW:i

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Vol. 7, p. 102 Asiatic Herpetological Research 1997

M II II If IX

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1997 Asiatic Herpetologu at Research Vol . 7, pp. 1 03- 1 07

The Variation in Karyotypes of Brachytarsophrys from China with a Discussion

of the Classification of the Genus

Ding-Qi Rao and Da-Tong Yang

Kunming Institute of Zoology, Accidentia Sinica, Kunming 650223. China

Abstract. -Different karyotypic forms of Brachytarsophrys occur in populations from Jingdong and Dayao,

Yunnan. These forms, along with morphological evidence, suggest that Brachytarsophrys should be divided into

two different species. The Jingdong population is identified as B.feae (previously Megophrxs feae). The Dayao

population is a new species, resembling in morphology, B. carinensis which occurs in south Burma and Thailand.

The Dayao population is geographically far removed from B. carinensis. A valid sister species. B.feae, is found

between the distribution of the Dayao population and B. carinensis. The new species is found in a different

climatic zone and in different habitats than B. carinensis. B. intermedins in south Vietnam probably is not a valid

species because it is more similar to B. carinensis in morphology and shares the same climatic zone and habitats.

Key words: Brachytarsophrys. B. platyparietus sp. nov.. B.feae. karyotype, biogeography, classification

ii ii ii ii u

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II II II 11

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Vol. 7. p. 104

Asiatic Herpetological Research

1997

Introduction

Brachytarsophrys in China were considered to be

only B. carinensis until Ye and Fei (1992)

described a second species, B.feae. Our studies of

cytology and morphology agree with Ye and Fei that

Brachytarsophrys in China belong to two different

species. The Jingdong population we studied

belongs to B.feae. We do not agree with them with

respect to the Dayao population, which they identi-

fied as B. carinensis.

Materials and Methods

Specimens used in cytological research were col-

lected respectively from Jingdong. Yunnan in June,

1990 and May, 1991, and Dayao, Yunnan in May,

1990. All specimens were taken to the laboratory

before processing. Karyotypes were prepared using

the method of colchicine-hypotonic-air drying:

specimens were injected intraperitoneally with

colchicine at a dosage of 20 ug/g body weight for

about 24-36 hours, then the femur and tibia were cut

off at their two ends. The marrow cells were

washed out with 1% tri-sodium citrate solution,

ground, then placed in a hypotonic solution of

0.64% KC1 and fixed in 3:1 solution of metha-

nohacetic acid for two periods of 20 minutes each.

Slides were air-dried and stained with 10% Giemsa

PBS for about 15 minutes. Specimens from middle,

southern, southwestern, northwestern and northern

Yunnan were examined and some from Jingdong,

Menglian, Tengchong, and Xishuanbanna were dis-

sected.

Cytological Results

The karyotypic form of the specimens from Jing-

dong is 2n=26, 5 large and 8 small pairs, Nos. 1, 3.

4. 5. 7. 8, 11. are M (metacentric): Nos. 2. 6, 9. and

13 are SM (submetacentric): only No. 10 is T (telo-

centric). The NF (fundamental number) is 50. One

secondary constriction is found in the near base of

the short arm of No. 1 ; no satellite was found. The

karyotypic form of the specimens from Dayao is

mostly 2n=28, 5 large and 9 small pairs, Nos. 1, 3,

4, 5, 6, 7, 1 1, and 12 are M; Nos. 2 and 8 are SM

and Nos. 9, 10, 13, and 14 are T chromosomes,

NF=48. No satellite or secondary constrictions

were found. We also found a third karyotypic form

with 2n=30 in Dayao specimens, with 5 large and

10 small pairs, Nos. 2, 7, and 8 are SM. Nos 9 and

13 are ST and Nos. 11. 12. 14. and 15 are T; the rest

are SM chromosomes, NF=48. No secondary con-

strictions and satellites were found. A few speci-

mens had 2n-26, as reported by Tan et al. (1987) for

specimens from Miyi and Huili. Sichuan (omitted

from this article. Table 1 ).

1 W7

Asiatic Herpetological Research

Vol. 7. p. 105

Discussion of Karyotypes

Table I shows that the large chromosomes are similar

in the three populations examined, but the small chro-

mosomes vary. The karyotype of the specimens from

Dayao is closer to that from Sichuan than that from

Jingdong. The karyotype of the population from Jing-

dong has 2n=26, NF 50, an obvious secondary con-

striction in lp, only 1 telocentric pair (No. 10) of

chromosomes, 3 pairs of SM chromosomes (Nos. 6, 9,

13). Small chromosomes are more numerous in this

population than in the other two populations. The

karyotype of the Dayao population is 2n=28, NF=48,

no secondary constriction was found, only 1 SM chro-

mosome (No. 8), and 4 small T chromosomes (No. 9.

10. 13. 14). This is more than the Jingdong. Sichuan

population karyotypes which were mainly 2n=26.

NF=44, 1 secondary constriction in each of two T

chromosomes (No. 9, 11), no SM chromosomes, and

4 T chromosomes (No. 9. 11. 12. 13) (Tan. et al..

1987). Because of these differences in karyotype, the

populations of Jingdong and Dayao should be recog-

nized as two different species.

Morphological Results

The specimens from northeastern Yunnan (Lijiang,

Yangbi, Bianchuan, Dayao, Yuxi, Kunming. Shuang-

bai, Shiping and Xinping), from Sichuan (Miyi,

Huili), and from Guizhou (Leishan. Anlong) (Wu et

al.. 1986) are probably the same as those from

Guangxi (Longsheng, Jinxui). from Hunan (Yizhang),

and from Jiangxi (Jingganshan). The toes are obvi-

ously webbed and the web may reach or exceed 1/3 of

the toes. The tops of the skulls in specimens from

middle and northern Yunnan are very flat. Specimens

from southwestern Yunnan (Jingdong. Meghan.

Xishuanbanna, Tengchong, Yongde and Longchuan,

near the type locality of Megophrys feae) are nearly

free of webbing or with a mere rudiment of a web.

The tops of their skulls are obviously depressed.

These differences suggest that these forms be recog-

nized as two different species.

Bourret (1942) and Taylor (1962) described B.

carinensis (previously Megophrys carinensis) as fol-

lows: eyelid with two to four pointed tubercles near

edge, vomerine teeth normally present, heel reaches to

shoulder or jaw-angle, skin with bony deposits above

head and anterior part of body, a vocal sac, paired

elongate glandular folds of back, male 1 23 mm and

female 150 mm, and toes about 1/3 webbed. It is dis-

tributed in Thailand (Chang Mai, Lampang provinces

and Mergui) and south Burma (type locality is Karen

Hills in southwestern Burma).

B. feae (M. feae) is characterized by eyelids with

small tubercles, one much more elongate than the oth-

ers, no longitudinal glandular folds on dorsum, a

vocal sac. tibiotarsal articulation which reaches near

jaw-angle, bony deposits on head, length 106 mm.

head depressed, and toes free or with a mere rudiment

of web. It is distributed in north Burma and the type

locality is Kakhien Hills, Burma which is near Long-

chuan and Tengchong, Yunnan, China.

The population of southwestern Yunnan is here

assigned to B.feae and is not B. carinensis. The pop-

ulations of northeastern Yunnan and Sichuan are simi-

lar to B. carinensis, but lack paired glandular folds.

Discussion

The populations from north and middle Yunnan,

including the Dayao population, are similar to B. car-

inensis in possessing eyelids and toe-webs, but they

obviously lack paired elongate granular folds on the

back that are present in B. carinensis (Bourret, 1942;

Taylor, 1962). Also these Yunnan populations are

geographically widely separated from B. carinensis

and are found in different habitats and climate zones.

B. carinensis occurs in tropical habitats whereas pop-

ulations of northeastern Yunnan occur in temperate

zones, and are separated from B. carinensis by a valid

sister species. B.feae.

Physiological characteristics limit amphibian abil-

ity to disperse. Distributions should be continuous

and presently discontinuous distributions should be

vestiges of a once continuous range. The distribution

of a species should be continuous, and even when

populations are separated by a valid sister species or

different climatic zones, such populations should be

widely separated. We think that the population of

northeastern Yunnan, Sichuan and nearby localities

should be a new species and not recognized as B. car-

inensis.

B. intermedins in south Vietnam (Lang Bian) has

paired elongate folds; it is similar to B. carinensis.

and inhabits the same climatic zone (tropical). It is

probably a population of B. carinensis.

Karyotypic and morphological evidence and geo-

graphical distribution (Liu and Hu. 1961; Yang et al.,

1991; Wu et al.. 1986; Tian and Jiang. 1986). suggest

that the population from Jingdong (including those of

southwestern Yunnan) is B. feae. The populations

from Dayao (including northeastern Yunnan. Sichuan.

Guizhou. Guangxi. Hunan and Jiangxi) is a new spe-

cies and not a population of B. carinensis. B. carinen-

sis is distributed in southwestern Burma (type

locality) and north Thailand. Megophrys intermedins

Vol. 7, p. 106

Asiatic Herpetological Research

1997

W^

•=. platyparietus feae

Figure 2. The distribution of the genus Brachytarsophrys.

intermedius

Figure 3. Brachytarsophrys platyparietus sp. nov.

Holotype (KIZ 90275). adult male X 1 .

Smith (1921) in south Vietnam (Annam) is a popula-

tion of B. carinensis. We recognize three species in

the genus Brachytarsophrys: B. carinensis in south-

western Burma. Thailand and south Vietnam; B. feae

in north Burma and southwestern Yunnan; and a new

species in northeastern Yunnan, southern Sichuan.

Guizhou. Guangxi, Hunan and Jiangxi (Fig. 2).

Taxonomic Account

Brachytarsophrys platyparietus sp. nov. (Fig. 3)

Holotype. KIZ 90275. adult male, collected from

Duo-Di-He, San-Tai, Da-Yao. Yunnan, China, altitude

2100 meters.

Paratypes: 1 adult male (KIZ 90274) and adult

female (KIZ 90276), from the same locality as the

holotype.

Diagnosis: Body very large, male may reach 1 16 mm

from snout to vent, female 131 mm; eyelids with three

circular tubercles in a line, the middle longest, and not

very sharp; tympanum hidden; arched diagonal fold

from eyelid to above arm insertion: toes widely

fringed and obviously webbed (at least extending to 1/

3 toes); the top of skull obviously very flat; no longi-

tudinal granular folds on the body side; no subarticui-

lar tubercles. The karyotype with 2n=28. few are 26

or 30; 5 pairs of large chromosomes, always with 4

pairs of small telocentric chromosomes, no secondary

constriction in the No. 1 chromosome.

Description of Holotype: Head large, flat and wide,

length nine-tenths of width; snout obtuse, very short.

1 997

Asiatic Herpetological Research

Vol. 7, p. 107

its length in front of the level of eyes 12 mm; distance

between nostrils 1 1 mm; canthus rostralis not very

sharp; loreal region only slightly diagonal; eyelid ele-

vated, projecting, bearing three elongate and circular

tubercles in a line, among which the middle one is

longer than the other two. and with much smaller

tubercles (3-4) behind them; tongue broad, nearly

round, mostly free behind, free on sides, one notch in

front; chaoanae partly concealed by maxillary

shelves; vomerine teeth present; arm rather long in

proportion to leg; first finger shorter than second;

third longest; no web between fingers and no fringe;

legs relatively short, tibiotarsal articulation reaching

to back of skull; toes about one-third (or more)

webbed and widely fringed; a large flat inner metatar-

sal tubercle, as long as first toe; no tarsal fold; digits

without widened tips; heels separated by about 20 mm

when legs are folded; no subarticular tubercles.

Skin above generally smooth, but laterally with

numerous flat tubercles; a strong fold from edge of

eyelid to above arm insertion on each side, the folds

are arched; back without pair of curving ridges from

head to shoulders, and without any dorso-lateral

ridges on dorsal side and above groin; no paired coni-

cal symmetrical tubercles in front of shoulders; no

sharp ridges and tubercles on sides; tibia without any

ridges. Body length 113 mm, head length 47 mm,

width of head 57 mm.

Variation: One female (KIZ 90276) with body

length 131 mm, head length 52.5 mm, head width 61

mm.

Distribution: Yunnan (Yangbi. Lijiang. Bianchuan.

Dayao. Kunming. Yuxi); Sichuan (Miyi. Huili, Duko.

M nil, Jiulong); Guizhou (Anlong. Leishan); Guangxi

(Longshen, Jinxiu); Hunan (Yichang): and Jiangxi

(Jingganshan).

Comparisons: B.feae is only very narrowly fringed

and not webbed in the toes. The top of the skull is

obviously depressed and the eyelid tubercle is very

long and sharp. The karyotype is 2n=26 with five

large pairs, only one pair of small telocentric chromo-

somes, and a secondary constriction in the short arm

of the No. 1 chromosome. B. carinensis has webbed

toes, obvious granular folds on the back and above the

groin. The eyelids have three sharp pointed flattened

tubercles. B. intermedins from south Vietnam is very

similar to B. carinensis. It also has longitudinal gran-

ular folds on the back. We suggest that it should be

considered a synonym of B. carinensis.

Literature Cited

Bourret, R. 1942. Les Batrachiens de l'lndochine.

Memoires de l'lnstitut Oceanographie de l'lndochine.

Hanoi 6:1-517.

Liu, C. C. and S. Q. Hu. 1961.0 [Tailless amphibians

of China]. Science Press. Beijing. 364 pp. (In Chi-

nese).

Tan. A. M„ X. M. Zeng. G. F. Wu. and E. M. Zhao.

1987. Cytotaxonomical studies on Chinese pelo-

batids, I. A preliminary study on the karyotype of

Brachytarsophrys carinensis and the variation in their

chromosome number]. Acta Herpetologica Sinica

6(2): 1-4. (In Chinese).

Taylor E. H. 1962. The Amphibia fauna of Thailand.

The University of Kansas Science Bulletin 63(8): 1-

599.

Tian, W. S. and Y. M. Jiang (editors), assisted by G. F.

Wu, Q. X. Hu, E. M. Zhao and Q. Y Huang. 1986.

[Identification manual for Chinese amphibians and

reptiles]. Science Press. Beijing. 164 pp. (In Chi-

nese).

Wu. L.. Qing. D.. and R. H. Xu. 1986. [The

Amphibia-fauna of Guizhou]. Guizhou People's

Press, Guiyan, Guizhou. 192 pp. (In Chinese).

Yang, D. T. S. M. Li. W. Z. Liu, and S. Q. Lu. 1991.

[The Amphibia-fauna of Yunnan], China Forestry

Publishing House, Beijing. 259 pp. (In Chinese).

Ye. C. Y. and L. Fei. 1992. [Taxonomic study of pelo-

batid toads, genus Brachytarsophrys of China.] Acta

Herpetologica Sinica ( 1 . 2):58-62. (In Chinese).

1997

Asiatic Herpetological Research

Vol. 7, pp. 108-130

Behavior of Varanus griseus during Encounters with Conspecif ics

ALEXEY YU.TSELLARIUS AND ELENA YU.TSELLARIUS

Program VARAN, Dept. Herpetology, Zoological Institute. 199034. St. Petersburg. Russia

Abstract. - In 1990-1993 in the western region of the deserts of Kyzylkum (Uzbekistan), constant observations of

a group of desert monitors in natural conditions were conducted. Described are manifestations of various

emotional states of monitors, and common types of monitor interaction. Given are detailed descriptions of the

course of contacts between the animals, illustrated by photographs. Fights were rarely noted and only between

unfamiliar lizards. It is proposed that ritual combat arises from displays of dominance and not from a

ntualization of the fight. The behavior of monitors during contacts is highly varied and not stereotypical. Data

from observations attests to the existence of a complex, mammal-like social structure in the population.

Considered are probable mechanisms of intraspecific communication of monitor lizards.

Key words: social behavior, social relations. Reptilia. Sauria, Varanus griseus

Introduction

In the article at hand we have made an attempt to

reveal the communicational function of common

behavioral acts of desert monitor. We have made also

an attempt to describe some types of interactions

between monitors and the role of these interactions in

social organization of population. We will not touch

upon behavior connected with courtship and mating

in the present article.

In 1989. when a program for the study of endan-

gered species of reptiles was developed by us, the

principal emphasis was put upon their ecology.

When we stumbled onto the fact, that the behavior of

the monitor lizard is much more complex than was

imagined, we no longer had the opportunity to alter

the program of study. Hence, the gathering of etio-

logical material had to be conducted at the same time

as the primary tasks. Although we are aware of the

incompleteness of our data and the necessarily sche-

matic and fragmentary nature of our description, we

do not consider its publication to be in vain. This

issue has not only theoretical but practical signifi-

cance since desert monitor populations arouse serious

apprehension in many regions of Middle Asia

(Darevsky,Orlov 1988. Khodzhaev 1989)

There exists a vast literature dedicated to the ele-

mentary behavioral acts of lizards (see the survey of

Carpenter. Ferguson 1977). The behavior of some

species of monitor lizards has also been described in

some detail (Auffenberg 1981a; 1981b: 1983: 1988;

Carter; 1990; Davis et al. 1986; Deraniyagala 1958;

Gaulke 1989; Horn et al. 1994; Mertens: 1946). But

in the most of herpetological papers the social motives

and purposes of behavioral acts are not examined.

Behavior of animals during intraspecific contacts is

usually considered as a succession of behavioral acts,

but not as a social interaction directed at the mainte-

nance of long-term interrelations within a socium.

The analysis of behavior is reduced to statistical anal-

ysis of the sequence of the behavioral acts of contac-

tants. Generally, the task of the analysis is limited to

discovery of the most probable response of a lizard to

the acts of another lizard. In analysis one seldom

allows for the circumstances, under which the interac-

tion took place. The history of interrelations of con-

tactants, as a rule, is not taken into account at all.

Actually, the social interaction is considered as a

closed system with internal self-regulation, indepen-

dent of the structure of the socium.

Viability of the population (the ability for bal-

anced reproduction in particular) is to a considerable

extent determined by its social structure. The social

structure of many species is rather impressed by envi-

ronmental conditions and the reptiles are not an

exception (Panov, Zykova, 1985; Poly nova, Panyush-

kin 1982; Polynova, 1990; Stamps; 1977). A social

response of population to environmental changes is

often species-specific (Polynova, 1990) and is not

necessarily adaptive (Plyusnin, 1990). Peculiarities of

response of socium to the external influences are

determined for the most part by two closely interde-

pendent, species-specific systems of animal activity:

a) a production of the signals which carry information

about the animal and its circumstances; b) a percep-

tion, processing and analysis of these signals in con-

junction with others external and internal irritants.

The principles of organization of these processes may

be termed as a "language" and a "mentality" of a spe-

cies. This issue is closely linked to the problem of

1997

Asiatic Herpetological Research

Vol. 7, p. 109

management of populations and demands careful

study.

The Region of Studies

The studies were conducted in the western area of the

sand deserts of Kyzylkum. Uzbekistan. The coordi-

nates of our permanent camp were 40° 40' N and 62°

08' E. The landscape in this region is typical of the

Kyzylkum -- sandy ridges, bushy undergrowths

(mainly Haloxylon persiewn, and Calligonum sp.),

and sparse grass (Care.x physodes predominates) (Fig.

1 ). In the region of studies there is a rather high abun-

dance of rodents, for the most part Rhombomys opi-

mus and Spermophylopsis leptodactylus. Both

inhabited and abandoned colonies of Rh. opiums —

with their complex system of underground passages

and location not farther than 150-200 meters from one

another -- serve the monitors as refuges and hunting

grounds.

Materials and Methods

Observations were conducted from 1990 to 1993 for

periods of four to seven months annually. In all,

observations were made for a duration of more than

20 months. In the beginning of April, the period in

which monitor lizards come out of hibernation, they

were caught, measured, weighed, marked, and

released at the site of their capture - usually in the

course of a few hours after being caught. A special

mark permitted us to identify the animals by their

tracks (Tsellarius and Cherlin, 1991 ). Henceforth, for

the greater part of the season of monitor lizard activity

we conducted continuous observations of the animals

— following their tracks and observing them visually

from camouflaged holes situated in the places where

the appearance of monitors was most probable. In

order to determine age, we amputated the last phalanx

from one of the fingers of a number of the monitor liz-

ards. The specimen was processed by E M. Smirina

(Moscow) to whom we owe our sincere gratitude.

The region of operations was regularly inspected and

all points at which a tracks of the marked animals was

apparent were plotted on a chart. As a result, we have

at our disposal data on age, the location of home

ranges, and the nature of the interrelations between

the majority of the mature individuals settled in the

region of operations.

Indirect exchange of information predominates in

the population (Tsellarius and Men'shikov, 1994).

The monitor lizards comparatively rarely enter into

direct contacts. A possibility of observations of con-

tacts is all the more rare. Therefore, in order to gather

sufficient data, we provoked contacts. To this end. the

monitor lizard was specially caught, usually in the

morning hours. In the evening of that same day we

attempted to establish from tracks the site where

another monitor would spend the night. At dusk we

released the monitor captured earlier into a nearby

burrow. In the morning, as the monitors emerged

from their overnight shelters, encounter was inevita-

ble. It was only possible to perform these operations

from time to time so as not to disturb the lizards and

disrupt the normal course of their lives. In some

instances discussed in this article, data from tracking

was also used when it was possible to precisely and

fully reconstruct the course of events from the tracks.

During observations from hiding, detailed steno-

graphic notes were taken which were deciphered

immediately after observations were concluded.

Some of the encounters were photographed (from 5 to

16 frames per encounter). Unfortunately, a lack of

means prevented us from employing photographic

documentation to the extent that was necessary. In all.

we observed 37 instances of contact between males, 8

instances of contact between females, and 21

instances of contact between the sexes.

Results

The Spatial Structure of the Population and

Annual Dynamics of Activity

Data pertaining to the spatial structure of the popula-

tion is currently being readied for publication in a sep-

arate article. Here, however, it is only necessary to

address a few words to this issue. The number of

monitor lizards in the region of studies consisted on

the average of four adult individuals per square kilo-

meter. The monitors were, however, distributed over

the space unevenly: areas of high concentration alter-

nating with thinly populated areas. Areas in which

populations were more densely concentrated (settle-

ments) measure nearly 100-150 hectares. The dis-

tance between the centers of neighboring settlements

ranges from 3-5 kilometers. Each settlement is

formed from a group of adult settled individuals con-

sisting of five to six males of various ages and three to

four females. In each of two settlements which were

under constant surveillance, only one female took part

in reproduction. The rest of the females were not

impregnated over the entire period of observations

although they were in fact courted by the males. The

home ranges of all of the animals in a settlement

almost fully overlap each other. In the sparsely settled

areas between settlements, home ranges may, to a

varying degree, either overlap or be located at certain

distance from one another. The home ranges of set-

Vol. 7, p. 110

Asiatic Herpetological Research

1997

tied animals range from 30 to 200 hectares in size.

From time to time, each of the males makes brief, dis-

tant excursions beyond the borders of his home range,

during which time he may visit the territory of a

neighboring settlement. It should be kept in mind that

this is a simplified scheme. The real picture is com-

plicated by the presence of stray and nomadic individ-

uals among the settled ones, altering the make-up of

the settlements and so forth. The area of a settlement

amounts to a kind of "public property" for settled

inhabitants of this settlement. It is not specially

guarded. We did not observe any territorial behavior

either between settlements or within them. The

degree of unrest and aggressiveness during encounters

with acquaintances was. however, incontrovertibly

lower than during encounters with strangers (Tsellar-

ius and Men'shikov 1994) and made the incorporation

of newcomers into the settlement difficult. The

majority of the animals mentioned in this article were

members of one of two adjacent settlements which

were under constant surveillance.

In the region of research the hibernation lasts

approximately from the beginning of October to the

beginning of April. During 1.5-2.0 months after

emergence from hibernation, monitors widely travel

within their home ranges and intensively forage. In

this period the social activity of monitors is high

enough: they readily enter into contacts with conspe-

cifics and show great interest in their tracks, but males

do not make any attempts to court the females in this

period (Tsellarius and Men'shikov 1994). Mating

period continues for a short time, it starts from the

first days of June and comes to end till the twentieth

of June. Females, which have taken part in mating,

dig the nest burrows in the end of June or beginning of

July, and diligently protect the clutch during 1-3

months after deposition (Tsellarius and Men'shikov

1995). Social activity of other animals rapidly

decreases during 1-2 weeks after the end of mating

period. Mobility and activity of the foraging of moni-

tors (females with clutches excluded) also decrease.

In the end of July the range, daily inspected by a mon-

itor, is a third or quarter of daily range in May. In

addition, in the second part of the summer lizards

may, from time to time, spend several days in burrows

without emerging to the surface.

The Most Ordinary Behavioral Acts of Desert

Monitor

"Confident gait". The animal moves calmly, carry-

ing his body high over the earth (Fig. 2). The monitor

lizard holds his head and tail horizontally and some-

times the tip of the tail draws upon the earth while he

is in motion. When the monitor examines any object

with its tongue (e.g. tracks of other animals, burrow

entrances and so forth), the lizard slightly lowers his

head.

In ordinary conditions these behavior and body

posture were observed during the most part of period

of monitor's activity when for example the hunting

monitor travels over familiar area. "Confident gait"

may be generally characterized as a pose of routine

activity. In this time the animal is in a state of psycho-

logical comfort. A conflict of motivations is absent or

it is possible to realize through the behavioral pattern

several motivations simultaneously (e.g. the search for

food and a sexual partner in the course of search

behavior). The physical state of the animal and its

external circumstances do not pose obstacles to the

fulfillment of the corresponding type of activity

(Ovsyanikov and Badridze, 1989).

The "confident gait" was often observed in course

of encounters between monitors (see section "Exam-

ples of behavior of monitors...", exs 1. 7; fig 14a).

This gait probably testifies to the self-confidence and

calm of the animal. His contactant evidently inter-

prets it as a threat of attack or the possibility of such

threat. In all directly observed instances the approach

by "confident gait" provoked an unambiguous

response. The approached animal manifests anxiety

(see exs 7, 9 and Fig. 14, 16) or displays a peaceable-

ness/submission (ex 1 ). The latter instances are rare.

Attack. When a monitor attacks a large prey he either

immediately rushes on it, abruptly starting a sprint, or

sneaks up to it before rushing from a distance of 3-5

m away. The sneaking up monitor walks with a rapid

step, creeping along the ground, often uses shrubs and

relief of the land as a cover. The act of lowering him-

self to the ground is also characteristic of the monitor

that is avoiding danger (Fig. 3b). When sneaking up

and when rushing the monitor holds his head and tail

horizontally. During an ordinary hunt all observed

actions were directly connected with prey-catching.

Any special displays were absent. In general, posture

of body of a monitor in assault is the same as in "con-

fident gait".

Attacks on conspecifics were observed only in two

situations: a) when a female protects her nest burrow

(Tsellarius and Men'shikov 1995); b) when an animal

with a lower social status rudely breaks the "rules of

etiquette", suddenly appearing, for example, at a dis-

tance closer than individual distance (ex 4 and Fig.

12). In such circumstances the emotional state of the

attacking monitor may be characterized as anger or

rage. Any signals which are expressed through spe-

cialized postures and movements during an attack

1997

Asiatic Herpetological Research

Vol. 7. p. I I I

were not recorded. In 1992 we observed how a large

monitor, considerably larger than the proprietress of

the burrow, returned repeatedly over the course of a

few days to the nesting burrow of the female that we

had named Biteress and attempted to dig up the bur-

row in her absence (Tsellarius and Men'shikov 1995).

The female, having found the arrival at work, drew

close to him with quick dashes from shrub to shrub,

slightly lowering herself to the ground, and lunged at

him from a distance of 2-5 meters away. Biteress's

behavior was, down to the most minute details, simi-

lar to the behavior of a monitor stealing up to his prey.

In all observed instances attacked animal immediately

resorted to flight.

The "threatening gait". The lizard moves in the

direction of an adversary at a slow pace. His tail may

not touch the ground but may, on certain occasions,

leave distinct imprints on both sides of his trail (giv-

ing the impression that the lizard is whipping his tail

enroute). When walking the monitor "drags his feet",

leaving distinct tracks in the sand from the dragging

of his ringers and claws. We can say nothing more

definite about this pose because it has been noted only

in encounters whose course has been reestablished

from tracks. The track of "threatening gait", however,

is very distinct from all other tracks. The female

leaves such a trail when she moves away from her

nesting burrow in the direction of an approaching con-

specific. Such trails have also been noted a few times

on the part of the female who directed it at a male that

is pursuing her. The "threatening gait" was recorded

in encounters between males when individual distance

was abruptly broken (ex 4. Fig. 12). In such a situa-

tion the threat was always displayed by animal with

higher "social standing"1. In every instance, the ani-

mal to which the threat was addressed sharply

changed the direction of his movement and in the

majority of cases moved away from the site of events,

sometimes taking flight. The lizards did not engage in

direct contact.

"Threatening gait" and attack were recorded in

very similar circumstances, sometimes "threatening

gait" was followed by an attack. The state of the ani-

mal in "threatening gait" may be interpreted as anger

When speaking of the social status of an individual, we had

in mind the "frequency of dominance". In other words, the

more the monitors of a given settlement occupy a subordi-

nate position in relation to a given individual, the higher his

status. As one would expect, the social status of males

turned out to be rather closely linked to size, the duration of

residence in a given settlement, and age.

rather closely linked to size, the duration of residence

in a given settlement, and age.

"Sitting dog" posture. Monitor "sits down", lifting

forepart of torso and head and looking around (Fig.

6). Very often animal assumes this pose when at great

distance away is some disturbing object (observer, for

example). "Sitting dog" posture probably is a classic

orientation response. This reaction is formed with

presence of weak fear (Hinde, 1970).

A monitor often raises his head during contact

with subordinate individual when the latter assumes

submission posture (exs.l, 3, 5 and Fig. 9). Therefore

it may be possible that the "sitting dog" posture (Fig.

6) or very similar pose also has a trace of dominance

in it. "Sitting dog" posture was observed in course of

conflict between males, when both contactants mani-

fested an unwillingness to yield (ex 9).

"Stooping"". The lizard slightly lowers his head,

simultaneously inflating his throat and pressing his

tail to the sand (Fig. 15a). This takes place during the

encounter of an animal with an unknown object in a

familiar area (e.g. a backpack, a shirt hung on a bush),

in the event of a careless movement of the observer in

hiding when the monitor lizard is not able to precisely

identify the character and source of the movement, or

during a direct encounter with another monitor that is

unknown or whose intentions the animal is not in a

position to determine, i.e. during an encounter with an

irritant that attests not to an obvious danger but to the