HARVARD UNIVERSITY

Ernst Mayr Library

of the Museum of

Comparative Zoology

ASIATIC

HERPETOLOGICAL

RESEARCH

VOLUME 4

1992

Asiatic Herpetological Research

Editor

ERMI ZHAO

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

Associate Editors

J. ROBERT MACEY

Museum of Vertebrate Zoology, University of

California, Berkeley, California, USA

THEODORE J. PAPENFUSS

Museum of Vertebrate Zoology, University of

California, 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

Leo Borkin

Zoological Institute, St. Petersburg, Russia

Bun i Chen

Anhui Normal University, Wuhu, Anhui, China

Yuanchong Chen

Shanghai Institute of Biochemistry, Shanghai, China

ILLYA DAREVSKY

Zoological Institute, St. Petersburg, Russia

INDRANEIL D AS

Madras Crocodile Bank, Vadanemmeli Perur, Madras,

India

William E. Duellman

University of Kansas, Lawrence, Kansas, USA

Hajime Fukada

Sennyuji Sannaicho, Higashiyamaku, Kyoto, Japan

Meihua Huang

Zhejiang Medical University, Hangzhou, Zhejiang,

China

Asiatic Herpetological Research is published by the Asiatic Herpetological Research Society (AHRS) and the

Chinese Society 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.

Authors should consult Guidelines for Manuscript Preparation and Submission at the end of this issue.

All correspondence outside of the People's Republic of China and requests for subscription should be directed to AHR,

Museum of Vertebrate Zoology, University of California, Berkeley, California, USA 94720. All correspondence within

the People's Republic of China should be directed to Ermi Zhao, Editor, Chengdu Institute of Biology, P.O. Box 416,

Academia Sinica, Chengdu, Sichuan Province, People's Republic of China.

Subscription and membership are $20 per year ($40 for libraries). Postage outside of the USA and China, please

add $5 per issue. Make checks or money orders payable in US currency to AHRS. If you do not have access to US

currency, please notify us, and we will make other arrangements.

Asiatic Herpetological Research Volume 4 succeeds 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 Reptiles. 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: Scutiger boulengeri from Wcnquan (35° 24' N 99° 23' E), Qinghai Province, China. Photo by J. Robert Macey.

CarlGans

University of Michigan, Ann Arbor, Michigan, USA

David M. Green

McGill University, Montreal, Quebec, Canada

Robert F. Inger

Field Museum, Chicago, Illinois, USA

KUANGYANG LUE

National Taiwan Normal University, Taipei, Taiwan,

China

Robert W. Murphy

Royal Ontario Museum, Toronto, Ontario, Canada

Hidetoshi Ota

Department of Biology, University of the Ryukyus,

Nishihara, Okinawa, Japan

Anming Tan

University of California, Berkeley, California, USA

YUNXU TONG

Lanzhou University, Lanzhou, Gansu, China

Datong Yang

Kunming Institute of Zoology, Kunming, Yunnan,

China

Yuhua Yang

Sichuan University, Chengdu, Sichuan, China

February 1992

Asiatic Herpetological Research

Vol. 4, pp. \Al\

Two New Species of the Worm-like Lizard Dibamus (Sauria, Dibamidae),

with Remarks on the Distribution and Ecology of Dibamus in Vietnam

ILYA S. DAREVSKY1

^Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia

Abstract. -Within Vietnam and the southern part of China there dwell 5 species of worm-like lizards of

the genus Dibamus, two of them (D. greeri sp. nov. and D. bogadeki sp. nov.) are new to science. Some

new data on the distribution, ecology, morphology, coloration, as well as the structure of hemipenes and

the autotomy and regeneration of the tail is given for the species studied. The specific peculiarities of the

body and tail coloration in some dibamids may apparently draw the attention of birds of prey, and in

connection with this are regarded as the manifestation of attractive coloration and as Batesian mimicry.

Key words: Reptilia, Sauria, Dibamidae, Dibamus, China, Vietnam, ecology, taxonomy.

Introduction

According to the current data, the genus

of worm-like lizards Dibamus Dumeril et

Bibron, 1839 includes 9 species widely

distributed on the mainland and on a

number of big and small islands in

Southeast Asia. As to the mainland part

proper of this vast area, registered here

were only 4 species of which D. alfredi is

known mainly from the Malay Peninsula,

and the three others (D. bourreti, D.

montanus, and D. smithi) occur only within

Vietnam (Greer, 1985). Dibamus bourreti

was earlier reported from southern China

(Liu and Hu, 1962) and recently was found

in Hong Kong (Lazell and Lu, 1990).

From 1982 to 1988, while conducting

field herpetological investigations in

different regions of mainland and insular

Vietnam, the author collected some new

material which considerably expands the

former views on the distribution as well as

the morphological characters and ecology

of the genus Dibamus within that country.

The results of the treatment of the material

and the description of the new species are

given below.

Methods

All in all, 12 individuals of the genus

Dibamus were studied, mainly from

Vietnam. They were taken by the author

and his colleagues in the course of several

Vietnamese-Soviet zoological expeditions

from 1982 to 1988. Different species of

the genus from other parts of its range were

also examined for comparison.

Measurements of snout-vent length (SVL)

and tail length (TL) were made by

adpressing the animals against a plastic rule

taped horizontally to a bench top. All

drawings were made under an "Opton"

stereomicroscope with a camera lucida

attachment. X-ray photos were taken with

the Japanese apparatus "Softes". In the

description of the elements of scuttelation, I

mainly applied the terminology used by

Greer (1985).

The following acronyms were used:

ZIN- Zoological Institute, Russian

Academy of Sciences, St. Petersburg

(Leningrad); BM- British Museum Natural

History; MNHP- Museum Natural History,

Paris; IEMEM- Institute of Animal

Evolutionary Morphology and Ecology,

Moscow; MCZ- Museum of Comparative

Zoology; ZMMU- Zoological Museum,

Moscow State University; CAS- California

Academy of Sciences.

Species Accounts

Dibamus bourreti Angel

Figs. 1, 3, 4, 5, and 11.

This species was described by Angel

(1935) who had one specimen available

from Tamdao, Vinhphu Province, northern

Vol. 4, p. 2

Asiatic Herpetological Research

February 1992

FIG. 1. Head in dorsal, lateral and ventral view of

A- Dibamus bourreti (ZIN 20012); B- Dibamus

bogadeki (holotype, MCZ 172041); sutures; r-

rostral; n- nasal; 1- labial; fn- frontonasal; f- frontal;

i- interparietal; o- ocular; po- postocular; m-

mental; if- infralabial.

Vietnam. The same type specimen (MNHP

35417) was reexamined by A. Greer in his

revision of the family Dibamidae (Greer,

1985). Earlier, Liu and Hu (1962), having

three specimens at their disposal, were the

first to indicate this lizard for Kwangsi

Province (= Guangxi Province) in southern

China. Recently a specimen was found in

Hong Kong (Lazell and Lu, 1990). In

Vietnam, according to the literature, D.

bourreti is also known from Ninhbinh,

Hanamninh Province (Tran et al., 1982)

and from the reserve Kukfiong, Hasonbinh

Province (Darevsky and Sang, 1983). We

also found this lizard in Tamdao, An Lac

Shon Dong, Habac Province and on the

Vietnam inshore island Katba, Haiphong

Province (Darevsky, 1990), (Fig. 2).

The data on the morphology of all

specimens we examined are given in Table

1. These data considerably expand the

morphological characteristics of D. bourreti

described by Greer (1985). Already in his

102 IM 106 108 l

*-i Oi

ft-3 »-4 0-5 ■-(•

FIG. 2. Distribution of the known localities of

Dibamus species in Vietnam and southern China:

1- Dibamus bourreti; 2- Dibamus bogadeki; 3-

Dibamus greeri; 4- Dibamus sp.; 5- Dibamus

montanus; 6- Dibamus smithi.

first description, Angel (1935) noticed the

typical white coloration on the back part of

the tail in the specimen available. Lui and

Hu (1962) also pointed to the same

peculiarity of this species, for individuals

from Guangxi Province, China. This

distinguishes it from all other

representatives of the genus Dibamus and

the specimen reported from Hong Kong by

Lazell and Lu (1990). I noted the bright

milk white coloration on the end part of the

tail in individuals from Katba Island, but

specimens from Tamdao and Kukfiong

lacked it, possibly because their tails were

regenerated. Attention is also drawn to the

fact that the coloration of the tail and the

back part of the body in specimens from

Katba Island and Hong Kong is not

uniform. It is to be accounted for by the

February 1992

Asiatic Herpetological Research

Vol. 4, p. 3

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Vol. 4, p. 4

Asiatic Herpetological Research

February 1992

CM l 2

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FIG. 3. Two autotomic tails with regenerated tips

of Dibamus bourreti (upper, ZIN 20014a); (lower,

ZIN 20014b).

location of the pigment on every single

scale. It is concentrated more compactly in

its front part and is poorly marked at the

rear (Fig. 3). Greer (1985) mentions the

presence of four preanal pores on each side

of the anal opening in the only female he

examined (MNHP 35417). In this

connection it should be noted that these

pores were not observed in any of the 5

specimens I examined (3 males and 2

females). This character is apparently not

constant in D. bourreti.

Field Notes. — All the D. bourreti

specimens currently known were caught

under stones or wood debris on the ground

of a tropical forest at an elevation of 450-

900 m. Liu and Hu (1962) found two

specimens in China on the surface of the

ground in a hilly forest.

In discussing the milky white coloration

on the end part of the tail in D. bourreti, it

should be observed that this species can

also be characterized as having a

comparatively very long tail, its length

reaching 40% or more of the SVL in both

males and females (in other representatives

of the genus the length of the tail does not

exceed 20-25% of the SVL). The long tail

with a bright coloration at its end

contrasting sharply with the dark

unicolored body of the animal may qualify

as a good example of attractive coloration.

My observations show that in case of

danger (when the stone under which the

animal hides is lifted) a Dibamus abruptly

B

FIG. 4. X-ray photograph of the two autotomic

tails with regenerated tips of Dibamus bourreti A-

(ZIN 20014a); B- (ZIN 20014b). The arrow points

to place of the fracture between two neighboring

vertebrae.

raises its tail upwards which apparently

immediately attracts the attention of a bird

of prey, such as ground foraging birds like

jungle or pea fowls rummaging about in the

forest litter in search of food. Caught by a

bird, the fragile tail easily breaks off, and

the animal has time to hide itself under the

ground. Here it may be noted that out of

the 5 specimens examined, 4 had a

regenerate tail to some degree. This is seen

in the X-ray photo (Fig. 4).

Comment. — As Greer (1985) noted, the

scales on the regenerate tail in Dibamus

almost does not differ from the original.

But the new tail may be distinguished by

the arrangement of the scales on its end

part. While a normal tail is somewhat

sharp at the end and its point is covered

with concentric rows of scales gradually

becoming smaller, the regenerate tail ends

February 1992

Asiatic Herpetological Research

Vol. 4, p. 5

FIG. 5. Scales on the top of original (A) and

regenerated (B, C) tails of Dibamus bourreti; A-

(ZIN 20014a); B- (ZIN 20014b).

bluntly by a plane oval platform occupied

by some relatively big irregularly arranged

scales (Fig. 5). X-ray photographing

clearly shows the fracture which can occur

not only across one of the tail vertebra, as it

is in most other lizards, but on the border

between two neighboring vertebrae as well.

The new tail is longer owing to the fact that

the connective tissues spread out both in

length and width (Fig. 4). At the same

time, a peculiar tail "blade" up to 1 cm long

covered with scales is formed, acquiring

the bright white coloration described above

(Fig. 3).

Judging from the collection material

examined and the literature data, D. bourreti

is characterized by a distinct intraspecific

variability. Angel (1935) and Greer (1985)

noted the complete absence of labial sutures

in the only specimen from Tamdao (MNHP

35417) they studied. The specimen caught

by the author in Tamdao (ZIN 20011) is

also deprived of labial sutures. In all other

examined individuals from Vietnam, as

well as from Guangxi Privince, China (Liu

and Hu, 1962), this suture is well

developed. Within wider limits, D .

bourreti shows variations also in mid-body

scale rows (from 20-24). Some coloration

differences in various individuals were

discussed above. It is possible that the

lizards from the type locality (Tamdao) may

be isolated in a separate nominate

subspecies D. b. bourreti Angel. Further

study is needed to settle this question.

With respect to this it may be noted that the

isolated tracts of forest of the Tamdao

mountain ridge show marked endemics

among reptiles, as well as some other

groups of animals.

Dibamus greeri sp. nov.

Figs. 6,7,8, 11 and Plate 1.

Holotype.—Zm 20011; Kontarang,

Gilai-Contum Province, Vietnam; 850 m; I.

S. Darevsky; 21 June 1983; male.

Paratypes.—Zm 20016; Tram-Lap,

Gilai-Contum Province, Vietnam; 800 m;

A. Gorochov; 12 December 1988; female.

IEMEM 101; Buoenloy, Gilai-Contum

Province, Vietnam; 750 m; December 1981;

S. Smirnoff; female.

Diagnosis. — Differs from all other

species of dibamids in the following

combination of characters: medial rostral

and nasal sutures incomplete; one

postocular; two supralabials; frontal much

larger than frontonasal and than

infraparietal; posteromedial edge of the

infralabials bordered by one narrow and

long scale; 20 mid-body scale rows; 97-1 1 1

presacral vertebrae; 29-31 post sacral

vertebrae (number of vertebrae is less than

in all other Dibamus species).

Description of Holotype. — Medial

rostral and nasal sutures incomplete and

barely extending to anterior edge of rostral

pad; the labial suture well developed;

frontonasal wider than long; frontal very

big, approximately four times bigger than

frontonasal; interparietal divided into two,

each part bigger than adjacent nuchal scales

(in paratype intraparietal not divided); two

supralabials posterior to rostral pad; only

one narrow scale located along the

posteromedial edge of the infralabial with

bordering posteromedially by three small

scales situated between the second

postmental and second infralabial; 20

midbody scales; 54 subcaudals; 97

presacral vertebrae; 32 postsacral vertebrae;

SVL 82 mm; TL 23 mm; preanal pores

absent; hind limbs very short, 1.4 % of

SVL.

Vol. 4, p. 6

Asiatic Herpetological Research

February 1992

FIG. 6. X-ray photograph ol Dibamus greeri (holotype, ZIN 2001 1).

Comment. — Greer (1985) noted a

considerable morphological resemblance

between the species of Anelytropsis and

Dibamus and in particular he singled out the

species D. bourreti which is most close to

Anelytropsis papillosus in having a

complete rostral suture passing through the

nostril, a complete nasal suture, and in

some other features. As to D. greeri, this

species resembles A. papillosus in the

presense of one narrow and long scale

bordering on the posteromedial edge of the

infralabials (Fig. 7).

Coloration. — Living animals (Holotype)

uniformly purplish-brown above and below

with three distinct brightly blue rings, 6-9

body scale rows wide, two on the body and

one on the tail. Shortly after capture, one

of the rings on the body disappeared and

the two others remained (Plate 1). The two

other known individuals (females) had the

same coloration as the holotype in life, but

they lacked the blue rings. *

Hemipenis. — Everted hemipenes are

quite smooth conic formations tapering to

the apex with a small hollow near the tip

(Fig. 8). The length of the organ is 1.1

mm, and the width is 0.4 mm. No

accounts about hemipenes in the family

Dibamidae have been given prior to this

account (Greer, 1985).

Distribution. All three known specimens

were taken in the central part of the Gilai-

Contum Province in southern Vietnam

(Fig. 2). It can be assumed that this

t 1 observed whitish-gray rings on the body and

the tail in some preserved Dibamus novaeguineae

specimens from the Philippine Islands (CAS

26647, 26678, 27538, 140218, and others). It is

very possible that in living animals the rings were

blue as in D. greeri.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 7

1mh

B

FIG. 7. Dorsal, lateral and ventral view of the head of A- Dibamus greeri (holotype, ZIN 20011); B-

Dibamus greeri (paratype, ZIN 20016); C- Dibamus smithi (ZMMU R-6567). For abbreviations see Fig.

1.

FIG. 8. Everted hemipenes of Dibamus greeri

(holotype, ZIN 20011). A- Front view; B- Side

view.

species widely occurs within the Pleicu

Plateau occupying the central part of Gilai-

Contum Province.

Etymology. — Named for Allen E.

Greer, the author of numerous works in the

field of taxonomy of various groups of

lizards, including the fundamental study of

the family Dibamidae.

Field Notes. — The type specimen was

found in a big lump of the so-called

"suspected" soil. The lump, which pierced

through with plant roots of epiphytes, had

fallen down from a tree at a height of about

Vol. 4, p. 8

Asiatic Herpetological Research

February 1992

three meters. It was torn to pieces by the

author right after it fell to the ground. The

trunk of the tree was twisted with liana up

to three meters height and it was thickly

overgrown with moss. The animal seems

to have worked its way up under the cover

of the moss. After capture the lizard

behaved very aggressively, struggled to

break loose, and opened its mouth to bite.

The two other specimens were discovered

in the wood litter under the cover of the

forest. Specimens of two new species of

lizards, Sphenomorphus rufocaudatus and

Ophisaurus sokolovi (Darevsky and Sang,

1983) were found at the same locality.

The bright blue coloration in the form of

separate spots, stripes or ocelli is known to

occur in many species of diurnal lizards. It

is usually regarded as one of the features of

sexual coloration. But it is evident that the

blue rings in worm-like lizards which live

in the soil and are practically blind cannot

play this role. Some other explanation

must be found for it. Hence, it is of

interest to note that the bright blue rings on

the body of Dibamus greeri make the

animal outwardly resemble some tropical

motley colored earth worms of the

Megascolicidae family living in the forest

litter. If such worms are not edible or

venomous, it may be assumed that this

represents a peculiar case of Batesian

mimicry. The ground-foraging birds, such

as jungle fowl, spur fowl and pea fowl may

have been important selective agents in the

evolution of such a memetic resemblance as

was shown for some species of uropeltid

snakes (Gans, 1987). This assumption,

however, must be supported

experimentally, especially because the blue

rings are capable of appearing and

disappearing, and were found by the author

only in one male. They were absent in

females and have never been observed in

other species of the genus Dibamus.

Dibamus bogadeki sp. no v.

Figs. 1,9 and 10.

Dibamus cf. bourreti Lazell and Lu,

1990

Holotype. — MCZ 172041; Hei Ling

Chau, ca. 10 km southwest of Victoria,

Hong Kong; A. Bogadek; 1 April 1987

(Fig. 10).

Diagnosis. — Differs from all other

Dibamus in the following combination of

characters: medial rostral suture absent;

nasal sutures not complete; labial sutures

present; interparietal large; one postocular;

two supralaibals; 23 midbody scale rows.

Description of Holotype. — Nasal suture

incomplete; not present from lip to nostril

and extending from nostril to the ocular

only; the labial sutures well developed;

frontonasal wider than long; fontal

approximately 3 times bigger than

frontonasal; interparietal larger than

frontonasal; 2 supralabials posterior to

rostral pad; one postocular; two scales

bordering posterior edge of the first

infralabial, one of them wider than the

other; 23 midbody scales; 51+ subcaudals;

134 presacral vertebrae; 25 postsacral

vertebrae in incomplete tail; SVL 177 mm;

TL 40 mm; preanal pores absent; hindlimbs

well developed, 2.7 % of SVL. According

to Lazell and Lu (1990) and the description

by Dr. J. D. Lazell (pers. comm.) the living

animal was lilac or lavender-gray,

irregularly mottled lighter and darker, at

darkest, light plumbeous. Tail ash-white;

head flecked with ash-white, but not as

much as tail. As in D. bourreti, the white

coloration of the back part of the tail

apparently demonstrates a characteristic

case of attractive coloration.

Distribution. — It is known only from the

type locality. The only finding of this

species during all the research history of the

Hong Kong herpetofauna indicates that it

occurs very rarely on this island (Fig. 2).

According to J. D. Lazell (pers. comm.) the

following reptiles are known from the type

locality of Dibamus bogadeki, Hei Ling

Chau: Hemidactylus bowringi, Gekko

chinensis, Typhlops braminus, Pareas

margaritophorus, Python molurus, Ptyas

corros, Trimeresurus albolabres, Naja haja

and other snake species.

Etymology. — The species is named for

its first collector Fr. Anthony Bogadek,

February 1992

Asiatic Herpetological Research

Vol. 4, p. 9

FIG. 9. X-ray photograph of Dibamus bogadeki (holotype, MCZ 172041).

Comment. — On a number of

characteristics, coloration included, this

insular species is most close to D. bourreti,

which drew the attention of Lazell and Lu

(1990). At the same time, there is a clear-

cut difference between D. bogadeki and D.

bourreti, such as the important character of

an incomplete nasal suture. It is also

characterized by a large size of SVL 177

mm and by a markedly greater number of

presacral vertebrae (136). See also Table

1.

Dibamus montanus Smith

FlG. 10. Photograph of Dibamus bogadeki

(holotype, MCZ 172041).

biologist at the St. Louis School, Victoria,

Hong Kong, and coauthor of the book,

Hong Kong Amphibians and Reptiles

(Urban Council, 1986).

Smith (1921) described this species

having at his disposal a few specimens

from the Langbian Plateau in the present

Lamdong Province in southern Vietnam.

All the type series has been recently

reexamined by Greer (1985) who singled

out the Lectotype (BMNH 1946.8.3.2) out

of two specimens from Le Bosquet.

Vol. 4, p. 10

Asiatic Herpetological Research

February 1992

m

1mm

1mM

1mm

FIG. 11. Anal area with the male's hindlimbs of three Dibamus species: A- Dibamus smithi (ZMMU R-

6567); B- Dibamus bourreti (ZIN 20278); C- Dibamus greeri (holotype, ZIN 2001 1).

Two specimens of D. montanus were

captured by the author in April, 1987 at an

elevation of about 500 m in a tropical forest

on Condao Island (formerly Pulo

Condore)f

Dibamus smithi Greer

Figs. 7 and 11.

Smith (1921) was the first to notice the

differences between a part of the specimens

from the Langbian Plateau he had at his

disposal and the typical individuals of

Dibamus montanus. Greer (1985) studied

these specimens again and showed that they

refer to the new species Dibamus smithi he

had described. This species is known only

from the type locality (Daban, Lamdong

Province, Vietnam). I also had at my

disposal a specimen (ZMMU R-6467)

captured in April, 1985 by V. F.

Goncharov from Nhatrang, Phykhanh

+ Earlier these specimens were mentioned for

Condao under the name D. smithi (Dare v sky,

1990).

Province, Vietnam.

Comment. — Dibamus smithi, as well as

the closely related species D. montanus,

has a non-uniform body coloration. On

each of the body scales the dark pigment is

located more compactly in its front part

forming a peculiar reticulate pattern (Fig.

11, A). On the whole, both of these

species differ from the other representatives

of the genus Dibamus in having a more

slender body (see Table 1).

Dibamus sp.

I had at my disposal one headless

specimen (a female) from Buoneloy, Gilai-

Contum Province, Vietnam (IEMEM 102)

identified by Iordansky (1985) as D.

bourreti and used by him for studying the

head muscles. The absence of the head

prevents us from identifying the species of

this specimen. But it should be noted that

the 19 midbody scale rows clearly

distinguish it from its sympatric species, D.

greeri and the large number of postsacral

vertebrae (49) makes it different from all

February 1992

Asiatic Herpetological Research

Vol.4, p. 11

other species in the genus Dibamus from

Vietnam. It is of interest to note that in this

headless specimen, as was shown by

Iordansky (1985), some rudiments of

postfrontal bones are preserved. According

to Greer (1985), Anelytropsis papillosus

also have such bones, while the specimen

of D. greeri examined by Iordansky, as

well as D. novaeguineae (Rieppel, 1984)

lack them.

Key to the species of Dibamus from Vietnam and southern China.

1 (7). Mid-body scale rows 20-24.

2 (8). Medial rostral suture absent or incomplete (barely extending to anterior edge of

the rostral pad).

3 (4). Nasal suture complete and extending between the nostril and the posterior edge of

the rostral pad D. bourreti.

4(3). Nasal suture absent or incomplete (not extending to the posterior edge of the

rostral pad).

5 (6). Nasal suture reduced; medial rostral suture present D. greeri.

6 (5). Nasal suture present and extending from the nostril and ocular D. bogadeki.

7 (1). Mid-body scale rows 18-19 D. smithi.

8 (2). Medial rostral suture complete extending to the tip of the snout D. montanus.

Acknowledgments

I thank the following colleagues and

friends for giving valuable consultation, for

sending preserved collections of material

and help during field work in Vietnam: E.

R. Brygoo (Museum National d Histoire,

Paris); Carl Gans (University of Michigan,

Ann Arbor); Allen E. Greer (Australian

Museum, Sydney); Marinus S. Hoogmoed

(Naturhistorisch Museum, Leiden); A. V.

Gorochov (Zoological Institute, Academy

of Sciences, St. Petersburg); James D.

Lazell (Conservation Agency, Rhode

Island); N. N. Iordansky (Institute of

Evolutionary Morphology Ecology,

Moscow); V. N. Orlova (Zoological

Museum, Moscow University); Jose P.

Rosado (Museum of Comparative Zoology,

Cambridge); Nguyen van Sung (National

Center for Scientific Research of Vietnam,

Hanoi); S. V. Smirnov (Institute of

Evolutionary Morphology and Ecology,

Moscow); A. F. Stimson (British Museum,

Natural History); V. V. Yakushev (Institute

of Evolutionary Morphology and Ecology,

Moscow); and Jens V. Vindum (California

Academy of Sciences, San Francisco).

Literature Cited

ANGEL, F. 1935. Un lezard noveuau de la famille

des dibamides. Bulletin du Musdum National

d'Histoire Naturelle, Paris 2(7):354-356.

DAREVSKY, I. S., AND N. V. SANG. 1983. New

and little known lizards species from Vietnam.

Zoologitcheski Zhurnal 62:1827-1837. (In

Russian).

DAREVSKY, I. S. 1990. Notes on the reptiles

(Squamata) of some offshore islands along the

coast of Vietnam. Pp. 125-129. In Peters, G.

and R. Hutterer (eds.), Vertebrates in the tropics,

Bonn.

IORDANSKY, N. N. 1985. The jaw apparatus and

the problem of relationship between Dibamidae

and Pygopodidae (Reptilia, Squamata).

Zoologitcheski Zhurnal 64:835-848. (In

Russian).

LAZELL, J., AND W. LU. 1990. Four remarkable

reptiles from South China Sea islands, Hong

Kong territory. Asiatic Herpetological Research

3:64-66.

Vol. 4, p. 12

Asiatic Herpetological Research

February 1992

LIU, C, AND S. HU. 1962. A herpetological

report of Kwangsi. Acta Zoologica Sinica 14,

Suppl.:73-106. (In Chinese).

GANS, C. 1987. Automimicry and Batesian

mimicry in uropeltid snakes: pigment,

proportions, pattern, and behavior. Journal of

the Bombay Natural History Society 83,

Suppl.:153-158.

RIEPPEL, O. 1984. The cranial morphology of

the fossorial lizard genus Dibamus with a

consideration of its phylogenetic relationships.

Journal of Zoology, London 204:289-327.

SMITH, M. A. 1921. New or little known reptiles

and batrachians from southern Annam (Indo-

China). Proceedings of the Zoological Society

of London 1921:423-440.

GREER, A. E. 1985. The relationships of the

lizard genera Anelytropsis and Dibamus.

Journal of Herpetology 19:116-156.

TRAN, K., N. V. SANG, AND H. T. CUC. 1981.

Ket qua" dieu tra co b£n bo sat - 6ch nhdi mien

Bac Viet Nam. Ket Qud Dieu Tra Co Ban Bong

vat mi6n bac Viet Nam. Pp. 365-427. Ha Noi.

February 1992

Asiatic Herpetological Research

Vol.4, pp. 13-17|

A New Subspecies of the Dwarf Snake Calamaria lowi ingermarxi ssp. nov.

(Serpentes, Colubridae) from Southern Vietnam

ILYA S. DAREVSKY1 AND NIKOLAI L. ORLOV1

^Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia

Abstract. -The Indo-Malay species of the dwarf snake Calamaria lowi Boulenger was discovered for the

first time in Vietnam, where it is represented by the subspecies Calamaria lowi ingermarxi spp. nov. Some

other examples pointing to the historical links between the herpetofaunas of Vietnam and the insular

regions of Southeast Asia are given. A key to the subspecies Calamaria lowi and to other Calamaria

species from Vietnam is given.

Key words: Reptilia, Serpentes, Colubridae, Calamaria, Vietnam, biogeography, distribution, taxonomy.

B

FIG. 1 . A- Dorsal and B- lateral view of ZIN 20006, the holotype of Calamaria lowi ingermarxi.

Introduction

According to the last revision of the

genus of oriental colubrid dwarf snakes

Calamaria H. Boie, 1827, the widely

distributed species Calamaria lowi

Boulenger, 1877 forms three well distinct

subspecies. Of them, the nominative

subspecies C. I. lowi Boulenger occurs on

Kalimantan Island, Thailand, C. /.

wermuthi Marx and Inger is known from a

single specimen from the western part of

Java Island, Indonesia, and C. I. gimletti

Boulenger is distributed on the Malay

Peninsular mainland and the two adjoining

small islands of Aor and Riouw (Inger and

Marx, 1965). The northern most location

of this subspecies on the Malay Peninsula

is Kalantan where the holotype comes

from.

In 1982, during field herpetological

work in Vietnam, a specimen of C. lowi

was taken by the authors for the first time

in Indochina, more than 1000 km to the

northeast of the known mainland

distribution of the species. A detailed study

of this specimen showed that it belongs to a

subspecies new to science. Its description

is given below.

1992 by Asiatic Herpetological Research

Vol. 4, p. 14

Asiatic Herpetological Research

February 1992

2mm

FIG. 2. Dorsal and lateral view of the head of ZIN

20006, the holotype of Calamaria lowi ingermarxi.

Calamaria lowi ingermarxi spp. nov.

Figs. 1, 2, 3, and 4.

Holotype. — Zoological Institute,

Russian Academy of Sciences, St.

Petersburg (Leningrad), ZIN 20006;

Buoenloy, Gilai-Contum Province,

Vietnam; 750 m; I. S. Darevsky; 18 June

1982; male (Fig. 1).

Diagnosis. — Differs from all other

subspecies of Calamaria lowi in the

following combination of characters;

maxillary teeth modified; second and third

supralabials enter orbit; mental touching

anterior chin shields; ventrals uniformly

dark gray colored with light posterior

edges; 205 ventrals; 23 subcaudals.

Description of holotype . — Rostral wider

than high, portion visible from above more

that half length of prefrontal suture;

FIG. 3. Head: A- dorsal view; B- ventral view;

C- lateral view; ZIN 20006, the holotype of

Calamaria lowi ingermarxi.

FIG. 4. Left hemipenis of Calamaria lowi

ingermarxi. A- lateral; B- dorsal view.

prefrontal longer than frontal, touching first

two supralabials; frontal 2 times width of

supraocular, length about two thirds that of

the parietal; paraparietal surrounded by 6

shields and scales; nasal smaller than

February 1992

Asiatic Herpetological Research

Vol. 4, p. 15

100

110

120

Fv

=^

?0

10

0 l-

*i:m -

cP=^

« c=^ '*

O

*

250 0 250 500 750 km

" »- *- ■ ■

£S> '

^Crz$3 ■■p^'-0^

?0

100

110

l?0

* I

• 2

©3 #4

FIG. 5. Map of the main known localities of Calamaria lowi subspecies: 1- C. /. lowi; 2- C. I. gimletti;

3- C. 1. wermuthi (after Inger and Marx, 1965); 4- C. /. ingermarxi.

postocular; no preocular; postocular as deep

as eye; 4 supraoculars, second and third

entering orbit, fourth longest, first not

longer than third; mental triangular,

touching first pair of chin shields; both pair

of chin shields meeting in mid-line; 3 gulars

in midline between posterior chin shields

and first ventral (Figs. 2 and 3). Tail short,

not tapering, tip blunt; dorsal scales reduce

to 4 rows on tail opposite first to fifth

subcaudal anterior to terminal scute. Eight

modified maxillary teeth. Thirteen scale

rows, 205 ventrals, 23 subcaudals; SVL

296 mm; TL 22 mm; ratio of tail to total

length is 0.074.

The hemipenis is 4 mm in length, forked

on the top, calyces papilate (Fig. 4). Body

grown gray-bluish, immaculate; light spots

on each side of neck covering 4 scales;

lower halves of supralabials yellowish.

Ventrals and subcaucals uniformly dark

gray except for light borders at the extreme

posterior edge of the ventrals (Fig. 1).

Vol. 4, p. 16

Asiatic Herpetological Research

February 1992

Distribution. — Known only from the

type locality in central Vietnam (Fig. 5).

Probably occurs widely within the Pleicu

Plateau in the central part of Gilai-Contum

Province in central Vietnam.

Etymology. — This subspecies is named

for Robert F. Inger and Hymen Marx who

have made a great contribution to the study

of the herpetofauna of Southeast Asia.

Among other works, they are the authors of

an important summary on the taxonomy

and evolution of the snake genus

Calamaria.

Discussion

This specimen of Calamaria lowi from

Gilai-Contum Province in central Vietnam

was found a considerable distance from the

main distribution of this species, which is

the Malay Peninsula in Malaysia and the

islands of Kalimantan and Java, in Thailand

and Indonesia respectively. However, C.

lowi is not the only species suggesting

some historical link between the

herpetological faunas of Vietnam and the

insular regions of Southeast Asia. For

example, in central Vietnam at the type

locality of C. I. ingermarxi we collected a

specimen of the skink, Sphenomorphus

stellatus (Boulenger). This species is also

found in Thailand on Kalimantan Island

(Bacon, 1967). This region of Vietnam is

also the type locality of the glass lizard

Ophisaurus sokolovi Darevsky and Sang

(1983). This species is closely related to

Ophisaurus buetticoferi Mertens from

Kalimantan Island, Thailand. In the same

area a specimen of Calamaria

septemtrionalis was collected. This species

is widely distributed in Vietnam and also on

the Malay Peninsula.

The present day disjunction in the ranges

of these and some other species of reptiles

and amphibians are apparently of secondary

formation, as a result of the changes

occuring in the paleogeographic conditions

in this region. In particular, the sinking of

the water level during the Pleistocene,

which led to the separation of both

Kalimantan and Java from the mainland

(Beaufort, 1951).

Key to the species of Calamaria from Vietnam.

1 (6). Preocular present.

2 (3). Ventrals yellow, immaculate C. buchi Inger et Marx.

3 (2). Ventrals yellow, with dark lateral tips.

4 (5). Tail as thick as body, not tapering, end broadly rounded

C. septentrionalis Boulenger.

5 (4). Tail not as thick as body, tapered, pointed C. pavimentata Dumeril et Bibron.

6 (1). Preocular absent C. lowi Boulenger.

Key to the subspecies of Calamaria lowi.

1 (2). Mental not touching anterior chin shields C. /. gimletti Boulenger.

2(1). Mental touching anterior chin shields.

3 (4). Ventrals uniformly cream colored C. /. wermuthi Inger et Marx.

4 (3). Ventrals colored otherwise.

5 (6). Anterior ventrals cream, posterior ventrals almost uniformly dark brown; or

ventrals yellow with large, irregular brown squares C. I. lowi Boulenger.

6 (5). Ventrals all uniformly dark gray with light posterior borders

C. /. ingermarxi ssp. n.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 17

Acknowledgments

We are most grateful for the valuable

comments of Dr. Robert F. Inger (Field

Museum of Natural History, Chicago) and

to Dr. E. A. Arnold and Dr. A. E. Stimson

(British Museum of Natural History,

London) for the loan of comparative

material of Calamaria.

Literature Cited

BACON, J. P. 1967. Systematic status of three

scincid lizards (Genus Sphenomorphus) from

Borneo. Fieldiana, Zoology 51 (4):63-76.

BEAUFORT, L. F. 1951. Zoogeography of the

land and island waters. Sidgwick and Jackson,

Ltd., London. 208 pp.

DAREVSKY, I. S., AND N. V. SANG. 1983. New

and little known lizards species from Vietnam.

Zoologitcheski Zhurnal 62:1827-1837. (In

Russian).

INGER, R. F., AND H. MARX. 1965. The

systematics and evolution of the oriental

colubrid snakes of the genus Calamaria.

Fieldiana, Zoology 49:3-303.

February 1992

Asiatic Herpetological Research

Vol. 4, pp. 18-22

A New Species of the Genus Tropidophorus (Reptilia: Lacertilia)

Guangxi Zhuang Autonomous Region, China

from

Yetang Wen1

^Department of Biology, Guangxi Medical College, Nanning, Guangxi, China

Abstract. -A new species of Tropidophorus is described from Guangxi Zhuang Autonomous Region,

China. This new species (Tropidophorus guangxiensis) is characterized by having an undivided postmental,

that differs from T. sinicus which is divided. Though the postmental is undivided in T. thai, the new

species is separated from T. thai in having an undivided frontal, which is similar to T. sincus.

Key words: Reptilia, Lacertilia, Scincidae, Tropidophorus, China, Guangxi, taxonomy.

&ffij(

FIG. 1. Holotype of Tropidophorus guangxiensis,

GMC 85-032 from Darning Hill, Wuming (23° 23'

N 108° 30' E), Guangxi Zhuang Autonomous

Region, China.

Tropidophorus guangxiensis sp. nov.

Figs. 1, 2, 3, 4 and 5.

Holotype.— GMC 85-032 (Fig. 1), a

juvenile from Darning Shan (23° 23' N

FIG. 2. Lateral scutellation of the head of the

holotype (GMC 85-032).

108° 30' E), Wuming Xian (County),

Guangxi Zhuang Autonomous Region,

China, altitude 1240 m (Fig. 6). The

specimen was collected on June 15, 1985

by Zhaoxiang Yang and is deposited in

Guangxi Medical College (GMC).

Vol. 4, p. 19

Asiatic Herpetological Research

February 1992

FIG. 3. Dorsal scutellation of the head of the

holotype (GMC 85-032).

FIG. 4. Ventral scutellation of the head of the

holotype (GMC 85-032).

Paratypes.— GMC 85-029 and GMC-

85-030, two adult males collected with the

holotype.

Diagnosis. — This new species closely

resembles Tropidophorus sinicus Boettger,

but differs from the latter by the following

characters: a single postmental, head nearly

triangle, interparietal separating parietals

(Boulenger, 1887; Smith, 1935; Tian and

Jiang, 1986).

Description of holotype. — A juvenile

with a SVL of 39 mm and complete tail

length of 46 mm. See Table 1 for the other

measurements.

Head nearly triangle in dorsal aspect;

snout obtusely pointed, portion of rostral

visible from above, rostral wider than high;

upper head shields strongly striated;

frontonasal divided medially into two

FIG. 5. Ventral view of anal and base of tail

scutellation of the holotype (GMC 85-032).

February 1992

Asiatic Herpetological Research

Vol. 4, p. 20

FIG. 6. Type locality (dot) of Tropidophorus guangxiensis at Darning Shan (23° 23' N 108° 30' E),

Wuming Xian (County), Guangxi Zhuang Autonomous Region, China.

longitudinal parts, longer than wide, suture

of frontonasals longer than suture between

prefrontals; prefrontals pentagonal, in

contact with anterior and posterior loreals;

frontal narrower posteriorly, length 1.44

times width at widest point, 1.4 times

length of interparietal; frontoparietals

pentagonal, broader posteriorly, in contact

medially; interparietal slightly narrower

posteriorly, rounded behind, separating

parietal; parietal large, polygonal, border

five shields on each side; supraoculars

four, anterior two touching frontal;

superciliaries eight, anterior two largest,

first touching prefrontal; anterior loreal

nearly rectanglar, 1.2 times higher than

wide; posterior loreal 1 . 1 times higher than

broad; nasal undivided, 1.5 times wider

than high, nostril opening just behind

center; lower eyelid transparent (clouded),

separated from supralabials by two rows of

granular scales; presubocular one; preocular

small; postocular two; temporals majority,

some striated or with keels; primary

temporal large; supralabials eight, fifth

longest, sixth highest; infralabials six, first

longest; mental enlarged with labial border

much greater than rostral; postmental

undivided, pentagonal, wider than long;

three pairs of chinshields, first in broad

medial contact, posterior two separated by

pregulars; body scales parallel on side of

dorsum, dorsal scales slightly larger than

lateral scales, imbricated, scales of first two

rows following interparietal not keeled,

sharply keeled with acute to normal points

posteriorly by third row; scale rows around

middle of body 29 (9 dorsal, 7/7 lateral, 6

ventral); 46 transverse rows between

interparietal and rear edge of hindlimbs, 30

rows between forward edge of forelimbs

and rear edge of hindlinbs; ventrals slightly

Vol. 4, p. 21

Asiatic Herpetological Research

February 1992

TABLE 1. Measurements (mm) of Tropidophorus

guangxiensis sp.nov.

TABLE 2. Scutellation (Left/Right) of

Tropidophorus guangxiensis sp.nov.

* tail regenerated.

larger than dorsals, smooth, 27 transverse

rows between rear edge of forelimbs and

preanal scales; preanal scales four, central

two very large; supracaudals like dorsals,

but keels forming continuous ridges;

subcaudals strongly widened, smooth, in

single row except anterior four rings, 13

scale rows encircle tail at level of tenth

subcaudal, 58 scales in a longitudinal

series; scales of fore- and hindlimbs keeled

above and below as dorsal; finger lamellar

formula 5-9-11-15-7, toe lamellar formula

6-8-13-17-12 on each side, terminal lamella

tightly bound about claws; limbs adpressed

along flank toes in contact with fingers.

Color in preservative. — Head rusty

brown above and on side, with yellowish,

blackish cloudy spots; dorsum brown with

irregular cream transverse bands and spots

from neck to middle of body, middle of

body to base of tail pale (corneal epithelium

shed); tail-like torso, cream bands

narrower, lost on posterior three fourth;

limbs and digits marked in same manner as

body; upper and lower labials black , each

scale with white spot center, chin and throat

dark brown with longitudinal greyish white

stripes; venter yellowish white; underside

of tail white, subcaudals darken on both

sides forming longitudinal white stripes.

Habitat. — The species is restricted to

high mountains where mixed forest is

present. The specimens were collected

under fallen, rotten wood beside a

lumberman's domitory.

Variation. — The specimen, GMC 85-

029, has an azygos shield between the

frontonasals and the prefrontals; other

characters are listed in Tables 1 and 2.

Comparison. — This new species is

similar to T. sinicus with the frontal entire,

but differs from the latter in having the

postmental undivided. It is similar to T.

thai with the postmental single, but the

frontal of T. thai is divided (Smith, 1935;

Taylor, 1963; Tian and Jiang, 1986).

Literature Cited

BOULENGER, G. A. 1887. Catalogue of the

lizards in the British Museum (Natural History).

Vol. III. London. 575 pp.

SMITH, M. A. 1935. The fauna of Briush India,

including Ceylon and Burma. Reptilia and

February 1992 Asiatic Herpetological Research Vol. 4, p. 22

Amphibia. Vol. II- Sauna. Taylor and Francis, TIAN, W., AND Y. JIANG, (eds.) 1986.

London, 440 pp. Identification handbook of Chinese Amphibia

and Reptilia. Science Press, Beijing. 164 pp.

TAYLOR, E. H. 1963. The lizards of Thailand. (In Chinese).

Kansas University Science Bulletin 44:687-

1077.

February 1992

Asiatic Herpetological Research

Vol. 4, pp. 23-361

A Preliminary Report on the Reptile Fauna of the Kingdom of Bhutan with

the Description of a New Species of Scincid Lizard (Reptilia: Scincidae)

Aaron m. Bauer1 and Rainer Gunther2

^Department of Biology, Villanova University, Villanova, Pennsylvania, USA, 19085

2Museumfiir Naturkunde der Humboldt Universitat zu Berlin, Invalidenstrasse 43, Berlin, Germany

Abstract. -The herpetofauna of the Kingdom of Bhutan has been poorly studied and few collections of

Bhutanese reptiles have been made. Reptiles collected by the 1972 expedition of the Naturhistorisches

Museum Basel (Switzerland) are presented as a basis for a preliminary species list for this eastern

Himalayan country. Specimens representing seven families and 18 species were examined. Included is a

new species of scincid lizard of the genus Mabuya. An additional five species have been reported from

Bhutan and numerous other taxa are known from adjacent regions of Sikkim and Assam. Most of the fauna

is pan-oriental in derivation and is widespread to the east, west and south. A number of species, however,

are primarily Indo-Chinese in their affinities and extend only as far west as eastern Nepal. Collections from

eastern Bhutan and from elevations over 1500 m are particularly small and additional field work will be

required to provide a complete picture of the reptiles of the country.

Key words: Reptilia, Sauria, Scincidae, Mabuya, Bhutan, Himalayas, biogeography, zoogeography.

Introduction

Acharji and Kripilani (1951) reported

that the herpetofauna of the western

Himalayas was poorly researched in

comparison with that of the eastern portion

of the range. Since the time of their

publication this condition may be said to

have reversed, with several major and

many minor expeditions reporting on the

herpetofauna of the Kingdom of Nepal,

particularly the region from Annapurna to

the west (Cox, 1985; Dubois, 1974a,

1974b; Leviton et al., 1962; Mrsic, 1980;

Nanhoe and Ouboter, 1987; Sura, 1987,

1989; Swan and Leviton, 1958). In the

eastern Himalayas, numerous workers have

reported on the reptiles of Sikkim and West

Bengal (e.g., Annandale 1912; Gunther,

1864; Inglis et al., 1920) reviewed the

herpetofauna of the Abor district (= central

Arunchal Pradesh), some 225 km east of

Bhutan. Nonetheless, no comprehensive

works on the region have been compiled.

The Kingdom of Bhutan has long

remained a gap in the knowledge of eastern

Himalayan zoology, especially that of the

herpetofauna (Annandale, 1912; Ouboter

1986; Swan and Leviton, 1962). Bhutan

occupies approximately 47000 km2 in the

eastern Himalayas (Fig. 1). To the north it

is bordered by Tibet (Xizang Zizhiqu), to

the east by Arunchal Pradesh, to the south

by Assam, and to the west by Sikkim and

the Darjeeling district of West Bengal.

Government policy severely limiting

foreign travel and research in the Kingdom

has, until quite recently, left Bhutan as a

zoological terra incognita in south central

Asia. Fortunately, a great deal of Bhutan

lies within national parks, sanctuaries or

reserves (Hawkins, 1986) so that there may

yet be opportunities to study its fauna in a

relatively undisturbed state.

To date only four papers have been

published on the herpetofauna of Bhutan.

Bustard (1979, 1980a, 1980b) published a

conservation document and two short notes

on the status of the gavial (Gavialis

gangeticus) in Bhutan. Biswas (1975)

reported on a small collection of reptiles

from Bhutan and described a new taxon,

Calotes bhutanensis. We here report on a

much more extensive collection of reptiles

and amphibians from Bhutan collected by

the Zoologische Expedition des

Naturhistorischen Museums Basel

(NMBA) in 1972. This material is

supplemented by additional information

from literature sources.

Vol. 4, p. 24

Asiatic Herpetological Research

February 1992

FIG. 1. Map of the eastern Himalayas and adjacent regions showing the position of Bhutan. Closed

circles indicate the capitol cities of each country.

Methods

Specimens were collected in the

Kingdom of Bhutan in April-May 1972 by

the Zoologische Expedition des

Naturhistorischen Museums Basel

(NMBA), primarily by Drs. O. Stemmler

and M. Wurmli. Specimens were

examined while on loan at the Museum fiir

Naturkunde, Berlin. Other material

referred to is from the collections of the

Academy of Natural Sciences of

Philadelphia (ANSP), the U.S. National

Museum (USNM) and the Zoological

Survey of India (ZSI). Live weights for

some specimens were obtained from the

field notes of the collectors. The following

abbreviations are used throughout this

paper: LW = live weight, SC = subcaudal

scales, SVL = snout-vent length, TL = tail

length, V = ventral scales. Measurements

were taken only from representative

specimens of each taxon and samples

generally reflect typical individuals from

each series.

All of the localities represented by the

NMBA expedition are in southwestern

Bhutan. Literature records from other

collections also include several localities in

the central and eastern regions of the

country. Localities of the NMBA

expedition have already been characterized

in the literature (Baroni-Urbani et al.,

1973). To avoid repetition only the

latitudes, longitudes, and elevations of

those localities at which reptiles

werecollected are provided below, along

February 1992

Asiatic Herpetological Research

Vol. 4, p. 25

28°N

92°E

100 km

FIG. 2. Map of the Kingdom of Bhutan showing the localities referred to in the text. See Methods for

names, elevations and coordinates of numbered localities.

with the same information for literature and

other specimen localities. Latitudes and

longitudes are approximate as no adequate

gazetteer exists for Bhutan and several

localities not appearing on any available

maps could only be bracketed between

known places by reference to collectors

field notes. The following numbered

localities are marked on Figure 2:

1. Samchi (400 m),

26° 54' N 89° 14' E.

2. Phuntsholing (200-400 m),

26°51'N 89°26'E.

3. Khala and Balu Jhura (200 m),

26°50'N 89°26'E.

4. 14 km N of Phuntsholing,

(850-950 m), 26° 53' N 89° 27' E.

5. 87 km N of Phuntsholing (1700 m),

27°05'N, 89°35'E.

6. Chimakothi (2200 m),

27° 10' N 89°34'E.

7. 110 km N of Phuntsholing (2000 m),

27° 12' N 89°34'E.

8. 125 km N of Phuntsholing (2100 m),

27° 15' N 89°35'E.

9. Paro (2300 m),

27°26'N 89°25'E.

10. Thimphu (2300-2500 m),

27°29'N 89°3 7'E.

11. Wangdi Phodrang (1400 m),

27°29'N 89°54'E.

12. Tamji (2450 m),

27° 40' N 89°54'E.

Vol. 4, p. 26

Asiatic Herpetological Research

February 1992

13. Batase (1500 m),

27° 00' N 90° 37' E.

14. Panjurmane (1525 m),

27° 10' N 90° 43' E.

15. Manas River,

26°50'N 90°59'E.

16. Rongtong (2042 m),

27° 16' N 91° 32' E.

17. Samdrup Jhongkhar (300 m),

26°52'N 91°28'E.

Species Recorded from the

Kingdom of Bhutan

Reptilia

Crocodylia

Family Gavialidae

Gavialis gangeticus (Gmelin, 1789)

Ross (1989) included Bhutan in his list

of the recent distribution of the gharial.

Bustard (1979, 1980a, 1980b) reported that

this species had recently been extirpated

from its primary habitat in the Kingdom of

Bhutan, the Manas River. The last

specimens were seen in the 1960's.

Bustard (1980a, 1980b) and Groombridge

(1987) have suggested reintroducing the

species into suitable habitat. At present a

small population survives in the Indian

portion of the Manas River (Whitaker,

1987).

Sauria

Family Agamidae

Calotes bhutanensis Biswas, 1975

Biswas (1975) described this endemic

species on the basis of a single specimen

(ZSI 22480) from Panjurmane (listed as

Janjurmane by Biswas). Although he

provided mensural characters to distinguish

C. bhutanensis from the very similar C .

versicolor, the validity of this taxon must

remain in doubt. The values provided by

Biswas (1975) suggest that the single

specimen falls within the range of variation

displayed by C. versicolor. Moody (1980)

in his systematic revision of the Agamidae

was apparently unaware of this description

and did not recognize the species either as

distinct or as a junior synonym. Until such

time as C. bhutanensis is reevaluated in the

context of the genus Calotes as a whole we

tentatively recognize it a taxon

distinguishable from C. versicolor on the

basis of the minor scalation and color

features delineated by its describer.

Calotes versicolor (Daudin, 1 802)

(17 specimens examined): Phuntsholing

NMBA 22582-92, ZMB 48784-85; Balu

Jhura NMBA 22593; Wangdi Phodrang

NMBA 22594-6.

LW adult males 27.0-36.4 g (x = 31.68

g, n = 4), LW females and juveniles 5.8-

21.1 g (x = 9.96 g, n = 8).

In addition to the specimens examined,

Biswas (1975) reported a specimen from

Samdrup Jhongkhar, Bhutan. Calotes

versicolor is widespread throughout the

Oriental region, including all of the

southern slopes of the Himalayas. Smith

(1935) and Cox (1985) recorded the

species as common up to 1980 m in the

Himalayas. It is widespread in most of

Nepal and in adjacent regions of Sikkim

and the Darjeeling District (Acharji, 1961;

Acharji and Kripilani, 1951; Leviton et al.,

1956; Mrsic, 1980; Nanhoe and Ouboter,

1987; Rendahl, 1937; Sura, 1987, 1989;

Swan and Leviton, 1962). Barbour (1912)

recorded this species from the Tista Valley

near the Bhutanese frontier of Sikkim.

Japalura variegata Gray, 1853

(2 specimens examined): 87 km N of

Phuntsholing NMBA 22597-8. Biswas

(1980) obtained a specimen from Batase,

Bhutan. Giinther (1865) recorded this

taxon from Sikkim, and Hora (1926) and

Smith (1935) reported that this species was

common throughout the eastern Himalayas

at elevations of 330-2970 m. Annandale

(1906) initially reported J. yunnanensis

February 1992

Asiatic Herpetological Research

Vol. 4, p. 27

FIG. 3. Holotype of Mabuya quadratolobus Baur anf Giinther (NMBA 10275). Note general coloration

pattern.

from Buksa (=Buxa), near the

Bengalese/Bhutan frontier, but later

described the same specimen as J.

bengalensis, now regarded as a synonym

of J. variegata.

Family Gekkonidae

Hemidactylus brookii Gray, 1845

(1 specimen examined): Samchi NMBA

22599.

Swan and Leviton (1962) did not record

this species among the fauna of Nepal, but

it has since been reported as locally

common at lower altitudes (Mrsic, 1980;

Nanhoe and Ouboter, 1987). Mitchell and

Zug (1988) found it to be the most

abundant gecko at their locality in the Terai

of Nepal as did Cox (1985) at his central

Nepalese sites.

Hemidactylus frenatus

Dumeril and Bibron, 1836

(39 specimens examined): Samchi

NMBA 22600-7; Phuntsholing NMBA

22608-34; ZMB 48786-89.

LW 1.0-6+.2 g (x = 3.16 g, n = 32),

LW males (x = 3.43 g, n = 13), LW

females (x = 2.97 g, n = 19).

Leviton et al. (1956) and Swan and

Leviton (1962) recorded this species from

Dharan (ca. 330 m) in Eastern Nepal and

Cox (1985) found it common in Tharu, in

central Nepal. Annandale (1912) regarded

the species as common at low altitude

throughout the eastern Himalayas.

Platyurus platyurus (Schneider, 1797)

(5 specimens examined): Phuntsholing

NMBA 22635; Wangdi Phodrang NMBA

22636-7; no precise locality NMBA 22638-

9.

LW 2.5-5.2 g (x = 3.63 g, n = 3).

Annandale (1912), Cox (1985), Leviton

et al. (1956), Mrsic (1980), and Swan and

Leviton (1962) recorded this species from

central and eastern Nepal at elevations up to

1500 m and Smith (1935) and Taylor

(1962) recorded it from Sikkim. The

species is also known from southeastern

Tibet (Kraig Adler, pers. comm.).

Family Scincidae

Mabuya quadratilobus

Bauer and Giinther, n. sp.

Figs. 3 and 4.

Holotype.— NMBA 22681, lowest

terrace on the right bank of river valley

west of Samchi, Bhutan (26°54'N,

89°14'E), elevation 450 m. Collected by

M. Wiirmli and C. Baroni-Urbani, 12 May

1972.

Paratypes. — (11 specimens): NMBA

22682-87, ZMB 48769, 48775-78 all from

Samchi, Bhutan. Collected 8 May 1972 by

Vol. 4, p. 28

Asiatic Herpetological Research

February 1992

B.

Fig. 4. A) Lateral and B) dorsal views of the head

of Mabuya quadratolobus (NMBA 10275). Note

the ear lobules, enlarged fifth supralabial and

carinate dorsal scales.

O. Stemmler (NMBA 22682, 22688) and

11 May 1972 by O. Stemmler and M.

Wiirmli (NMBA 22683-87, ZMB 10281-

84).

Diagnosis. — Mabuya quadratilobus is

distinguished from all other Asian members

of the genus by the following combination

of characters: lower eyelid with transparent

disk; three large, squared lobules at anterior

margin of ear; seven supralabials with fifth

approximately 2.5 x length of first; dorsal

scales tricarinate.

Description of holotype. — A juvenile,

36.0 mm SVL, LW 1.3 g. TL (incomplete)

25.8 mm (TL of intact paratype NMBA

48777 = 130% SVL). Axilla-groin length

14.2 mm. Hindlimb length 13.8 mm.

Scalation (Fig. 4). — Frontonasal broader

than long; prefrontals large, in broad

contact; frontoparietals large, paired;

distinct interparietal; parietals each bordered

posteriorly by a single nuchal (unilaterally

fragmented in holotype); nostril entirely

within nasal; small supranasals present, in

narrow contact dorsally; two loreals,

anterior larger than posterior; lower eyelid

with central transparent disk (diameter

approximately 50% of eye); four

supraoculars, decreasing in size in the order

2>3>4>1; six supracilliaries; seven

supralabials, fifth and sixth under eye; sixth

supralabial separated from orbit by series of

small suboculars; fifth supralabial 2.5 x

length of anteriormost supralabials; seven

or eight infralabials, roughly equal in size;

first and second infralabials contact

postmental; two enlarged pairs of chin

shields, first pair in narrow contact.

Ears moderately large; tympanum

sunken; anterior margin of ear with three

flattened, distinctly squarish lobules;

remainder of scales on anterior margin of

ear slightly raised.

Dorsal scales tricarinate, with lateral

carinations more well developed than

medial; medial ridge limited to posterior

scale edge on many lateral and posterior

scales; carinated scales continue on to

proximal region of tail; dorsal scales

approximately equal in size, decreasing

slightly on flanks; 35 scale rows around

mid-body.

Limbs pentadactyl; scales on dorsal

surface of limbs weakly tricarinate; palmar

scales spinose; 14 unkeeled lamellae under

fourth toe.

Color (in preservative). — Dorsum olive

brown with series of dark brown marks on

distal edges of scales, forming irregular

spots on nape and broken transverse bands

at every second scale row on body. Light

dorsolateral stripe, one and one half scale

rows wide, from level of ear to tail. Dark

brown stripe beneath light stripe, extending

February 1992

Asiatic Herpetological Research

Vol. 4, p. 29

from anterior corner of eye on to tail,

passing beneath eye as a narrow dark line,

disrupted and diffuse through ear, flecked

with blue-white scales ventrally and fading

towards flanks. Venter white. Dorsal

surfaces of limbs brown, scales edged with

dark brown, forming a diffuse, irregular

reticulate pattern.

Variation. — The paratypes resemble the

holotype in all major features. All

specimens appear to be juveniles and

possess yolk scars. Some specimens show

minor fragmentation of some head scales.

LW 0.5-1.3 g (x = 0.85 g, n = 11); SVL

28.9-36.0 mm (x = 32.1 mm, n = 8).

Etymology. — The name derives from the

Latin lobus (lobe) and quadratus (square)

and is in reference to the striking ear

lobules characteristic of this species.

Unfortunately the phylogeny of the

lygosomine skinks in general, and Mabuya

in particular, is not well resolved. Greer

(1974, 1979) regarded Mabuya as ancestral

to other skink lineages and suggested that

the south-east Asian species of the genus

exhibited the greatest number of

plesiomorphic features. If this is true, then

this group must also be paraphyletic. The

only comprehensive treatment of Mabuya

as a whole has been that of Horton (1973),

who provided a key to the species and an

overview of the evolution and

biogeography of the numerous species

groups by geographic region. More than

20 Asian Mabuya were recognized by

Horton (1973), but no unified picture of

relationships among these taxa was

presented. In most existing keys to the

herpetofauna of the greater Indian region

(e.g., Smith, 1935) the new species falls

out most closely with Mabuya dissimilis, a

species from the western Himalayan

region. Comparison with the types (ANSP

9537-8) and other specimens of the latter

taxon, however, reveal major differences

and the two taxa are clearly distinct, if

closely related at all. With the material at

hand we are unable to offer any meaningful

suggestion as to the close relationship of

Mabuya quadratilobus .

Scincella sikkimensis (Blyth, 1853)

(45 specimens examined): Phuntsholing

NMBA 22640; 87 km N of Phuntsholing

NMBA 22641; Chimakothi NMBA 22642-

51, ZMB 48779-83; 110 km N of

Phuntsholing NMBA 22652-60; 125 km N

of Phuntsholing NMBA 22661; Paro

NMBA 22662-67; Thimphu NMBA

22668-76; Tamji USNM 166443; no

specific locality NMBA 22667-80.

LW 0.6-3.5g (x = 1.62g, n = 35), SVL

(larger specimens only) 45.8-55.8 mm (x =

49.48 mm, n = 6), TL 144-148% SVL (n =

3).

Ouboter (1986) reported a maximum

SVL of 55.7 mm and an average of 39.1

mm. Although only larger individuals of

the Bhutanese sample were measured, it

appears that populations from the

northeastern extent of the range may be

slightly larger than average. Specimens

examined in detail revealed at least three

different head scale patterns, reflecting

fusions and fragmentation of the standard

pattern reported by Ouboter (1986). For

example, NMBA 22668 possessed a

fragmented frontonasal, NMBA 22663 had

both prefrontals fused to the frontal, and

NMBA 22662 had unilateral prefrontal-

frontal fusion.

Hora (1927) recorded the species from

Sikkim and other neighboring areas of

India, and Cox (1985), Mrsic (1980), Sura

(1987), and Swan and Leviton (1962)

reported specimens from central Nepal.

Gruber (1981) and Ouboter (1986)

highlighted the confusion surrounding the

identity of the Himalayan species of

Scincella in general, but demonstrated that

S. sikkimensis is the characteristic species

of eastern Himalayas. As defined by

Ouboter (1986) it appears to be limited

chiefly to mesic oak forest regions on the

southern flanks of the range. Nanhoe and

Ouboter (1987) characterized this species as

a common inhabitant of forest clearings or

edges, generally below 3000 m throughout

the Himalayan region to the east of Jaljala

Pass in central Nepal. Ouboter (1986)

Vol. 4, p. 30

Asiatic Herpetological Research

February 1992

stated that the species was not known from

localities below 1200 m. However, Mrsic

(1980) recorded specimens below 1000 m

in Nepal and the Bhutanese localities

reported here, especially Phuntsholing,

clearly indicate that the species may occupy

the entire elevational range of the tropical-

subtropical belt of the foothills. The

presence of such low altitude specimens

give some credence to occurrence of

Scincella sikkimensis at Parasnath Hill,

south of the Gangetic Plain in Bihar, the

type locality of Mocoa sacra, a junior

synonym of S. sikkimensis.

Sphenomorphus indicus (Gray, 1853)

(5 specimens examined): 87 km N of

Phuntsholing NMBA 22689-92, ZMB

48768.

LW 9.4-26.5g (5c = 17.58, n = 5),

Maximum SVL 104.7 mm (NMBA 22689,

a large female containing embryos), TL

128-130% SVL (n = 2)

Hora (1927) reported this species from

"the eastern Himalayas below Darjeeling"

and Smith (1935) and Taylor (1962)

mentioned material from Sikkim. Although

literature records in the region are few, the

species is widespread in the eastern

Himalayas (Annandale, 1912; Rendahl,

1937).

Sphenomorphus maculatus

(Blyth, 1853)

(4 specimens examined): Samchi

NMBA 22693; Phuntsholing NMBA

22694. In addition the Basel Expedition

collected two specimens, NMBA 22695-6,

from 23 km N of Siliguri (ca. 150 m) in the

Jaipalguri District of India.

LW 3.0-4.0 g (x = 3.5 g, n = 2), SVL

45.0-58.8 mm (x = 50.6 mm, n = 4), TL

144-200% SVL, n = 4).

Nanhoe and Ouboter (1987) concluded

that this Indo-Chinese species was limited

in its distribution to low altitude riverine

forests. The Bhutanese localities reported

here support this. Smith (1935) mentioned

specimens from Sikkim.

Family Varanidae

Varanus bengalensis (Daudin, 1802)

(3 specimens examined): Phuntsholing

NMBA 22697-8, 22740. Specimens were

also sighted at Samchi.

This species is common throughout

much of the eastern Himalayas as well as

Assam (Annandale, 1912). Cox (1985)

reported a specimen from central Nepal at

Patan.

Serpentes

Family Typhlopidae

Ramphotyphlops braminus

(Daudin, 1803)

(24 specimens examined): Samchi

NMBA 22699-713; Phuntsholing NMBA

22714-17, ZMB 48770-74, 48774.

LW 0.3-1.0 g (x = 0.72 g, n = 21).

Largest specimen ZNB 48771, SVL 146.0

mm, TL 2.0 mm. All specimens have 20

scale rows around mid-body and show the

head scale suture pattern typical of this

species.

This widespread and easily transported

snake has also been recorded from Nepal

(Kramer, 1977; Mrsic, 1980; Nanhoe and

Ouboter, 1987) and Sikkim (Rendahl,

1937).

Family Pythonidae

Python molurus (Linnaeus, 1758)

Although we know of no Bhutanese

specimens in collections, the statement of

Harris et al. (1964) that "pythons" were

common inhabitants of the Duars Plains of

Bhutan, must surely refer to this species. It

has been recorded from comparable habitats

February 1992

Asiatic Herpetological Research

Vol. 4, p. 31

in Nepal (Kramer, 1977).

Family Colubridae

Amphiesma platyceps (Blyth, 1854)

(1 specimen examined): Wangdi

Phodrang NMBA 22741 (475 + 184 mm,

186 V, 98 SC).

This species has previously been

recorded from Sikkim, Assam and Nepal

(Kramer, 1977; Mrsic, 1980; Nanhoe and

Ouboter, 1987; Smith, 1943; Swan and

Leviton, 1962) and is widely distributed in

the Himalayas.

Amphiesma stolata (Linnaeus 1758)

Biswas (1975) collected a single

specimen from Samdrup Jhongkhar in

eastern Bhutan. This is a widely

distributed pan-oriental species that appears

to thrive in disturbed areas (Nanhoe and

Ouboter, 1987).

Boiga ochracea ochracea

(Gunther, 1868)

(2 specimens examined): Phuntsholing

NMBA 22730, juvenile (280.5 + 73.8 mm,

4 g, 234 V, 108 SC); NMBA 22731, adult

male, badly damaged (925 + 284 mm, 241

V, 118 SC).

This species is common in the eastern

Himalayas and is known from the Buksa

Duars along the southern boundary of

Bhutan (Smith, 1937).

Pseudoxenodon macrops (Blyth, 1854)

(2 specimens examined): 125 km N of

Phuntsholing NMBA 22738, male, head

and neck severely damaged (975 + 227

mm, 164 V, 63 SC); Wangdi Phodrang

NMBA 22739 (710 + 183 mm, 169 V, 67

SC).

Nanhoe and Ouboter (1987) regarded

this species as an Indo-Chinese form,

extending through the eastern Himalayas as

far west as Jaljala Pass in west central

Nepal.

Trachischium guentheri Boulenger, 1890

(4 specimens examined): 87 km N

Phuntsholing NMBA 22732-35. Largest

specimen (NMBA 22735), 226.3 + 38.6

mm.

Kramer (1977) and Swan and Leviton

(1962) reported this species from Nepal,

and Smith (1943) from Sikkim and

Darjeeling.

Xenochrophis piscator

(Schneider, 1799)

(12 specimens examined): Phuntsholing

NMBA 22718-29. The specimens are all

neonates (typical individuals 140.5 + 64.8

mm) and were collected along with 16 egg

shells. Smith (1943) reported clutch sizes

of 8-87 in this species. Nanhoe and

Ouboter (1987) reported this species as

common at low altitudes in association with

water and Annandale (1912) reported its

presence at elevations as high as 1450 m in

the western Himalayas. The species range

extends throughout the Oriental region.

Kramer (1977) and Swan and Leviton

(1962) reported Nepalese localities.

Zaocys nigromarginatus (Blyth, 1854)

(1 specimen examined): 87 km N

Phuntsholing NMBA-Field Number

10258, total length 1980 mm, badly

damaged.

This large snake is an eastern form,

ranging from Yunnan to the eastern

Himilayas (Smith, 1943). It is known

from elevations of up to 2500 m.

Family Elapidae

Bungarus niger Wall, 1908

(1 specimen examined): Phuntsholing

NMBA 22736 (667 + 120 mm, 221 V, 56

SC).

Although this taxon has long been

known from the eastern Himalayas and

Assam (Smith, 1943), it has not been

recorded from eastern Nepal by any of the

Vol. 4, p. 32

Asiatic Herpetological Research

February 1992

recent reviewers of the fauna of that region.

Ophiophagus hannah (Cantor, 1 836)

Biswas (1975) reported a juvenile

specimen from Rongtong in the Manas

Valley. This species has recently been

recorded from as far west as eastern Nepal

(Nanhoe and Ouboter, 1987).

Species Likely to Occur in Bhutan

In addition to the 23 species listed

above, it is certain that a great many more

reptile species are yet to be found in

Bhutan, both in the more well-known, but

richer lowlands, and the less-well collected

higher elevations. No turtles have been

reported from Bhutan, but several species

are likely to occur. Among the batagurine

emydids the range of Kachuga tecta

brackets Bhutan, with records from Sikkim

in the west (Moll, 1987) and the Dihang

River in the east (Annandale, 1912).

Kachuga drongoka has been collected in the

Brahmaputra River in the Kamrup District

of Assam (Moll, 1986) and was illustrated

in a distribution map as occurring in Bhutan

by Tikader and Sharma (1985). Cuora

amboinensis , Melanochelys tricarinata, M.

trijuga, Kachuga smithii, K. tentoria and

K. sylhetensis have been reported from the

Manas Tiger Reserve in Assam (Das, 1988)

and Hardella thutjii, Indotestudo elongata

and Lissemys punctata also approach the

borders of Bhutan. The freshwater turtles

are known either from the Tista to the west

or the Brahmaputra to the south (Das,

1985; Iverson, 1986; Smith, 1933; Tikader

and Sharma, 1985) and might be expected

to occur at lower elevations in the Torsa,

Wong Chu, Sankosh, and Manas drainages

of southwestern and south central Bhutan.

It is highly probable that additional lizard

species may also be found in Bhutan. The

gekkonid Hemidactylus flaviviridis occurs

in Nepal (Cox, 1985; Sura, 1987, 1989)

but apparently does not reach the eastern

Himalayas. Hemidactylus garnotii, on the

other hand, extends only as far west as

central Nepal (Cox, 1985; Nanhoe and

Ouboter, 1987; Sura, 1989), where it has

only recently become established. The

latter species almost certainly occurs at

lower elevations in Bhutan. Hemidactylus

bowringii was recorded by Barbour (1912)

from the Tista Valley near the Bhutanese

frontier with Sikkim, but no more recent

remarks on this species in the area in

question have appeared in the literature.

Among agamids, Japalura tricarinata occurs

in eastern Nepal, Sikkim, and the

Darjeeling area, it may be expected to occur

in the southwestern corner of Bhutan,

although the Basel expedition found no

specimens despite their intense collecting

effort in and around Phuntsholing.

Japalura andersoniana was described from

the Dafla Hills, near the eastern border of

Bhutan and is another potentially

indigenous agamid. Annandale (1906)

suggested that Ptyctolaemus gularis might

be found in the Buksa Duars along the

southern frontier of Bhutan. There are a

great many snake taxa that might be

expected to occur in Bhutan. Over 40

species have been recorded from Nepal

(Kramer, 1977). In the family Typhlopidae

at least Ramphotyphlops jerdoni and R.

oligolepis and possibly R. diardi extend to

the border regions of Bhutan. The colubrid

fauna of adjacent Sikkim and Assam is

exceptionally rich (Smith, 1943). Welch

(1988) listed Ahaetulla p. prasina, Boiga

gokool, Boiga multifasciata and

Rhabdophis himalayana as well as Boiga o.

ochracea as taxa occurring in Bhutan.

However, these records were purportedly

derived from Smith (1943), who, in fact,

listed no material from Bhutan. Welch's

(1988) apparent criterion for inclusion in

the Bhutanese fauna was Smith's (1943)

mention of the "eastern Himalayas" in his

distributional comments. In addition, at

least four species of Oligodon occur in

Sikkim or the Jaipalguri District of India

and may also be found in Bhutan.

Additional specimens and species almost

certainly exist in museum collections, but

have never been reported in the literature.

It is also likely that the cobra, Naja naja

kaouthia, occurs in Bhutan. Smith

(1943:434) presented a distribution map

showing most of Bhutan within the range

of the subspecies. The nominate

subspecies is illustrated as just reaching the

southwest corner of the country. The true

February 1992

Asiatic Herpetological Research

Vol. 4, p. 33

status of these forms relative to one another

remains unclear. They occur in sympatry

in a number of areas and are probably

specifically distinct (Wiister and Thorpe,

1989). To date, however, there have been

no specimens to confirm the presence of

either form in Bhutan, although there are

records from Nepal (Acharji, 1961;

Kramer, 1977).

Discussion

Himalayan zoogeography has been

reviewed extensively by previous authors

(e.g., Annandale, 1912; Blanford, 1901;

Dubois, 1981; Hora, 1948; Nanhoe and

Ouboter, 1987; Smith, 1933; Swan and

Leviton, 1962). All have used

approximately the same divisions in

identifying the affinities of the faunal

elements of the region. Bhutan lies

primarily within the Eastern Himalayan

province of the Indo-Chinese subregion of

the classically-defined Oriental region. The

herpetology of the eastern Himalayas in

general is known from a number of faunal

reports from eastern Nepal (e.g., Leviton et

al., 1956) and northeastern Bengal

(Annandale, 1912), as well as from

descriptions of new species, especially

amphibians (see Dubois, 1974a). Swan

and Leviton (1962) recorded 85 snake and

lizard species from Sikkim and the adjacent

Darjeeling area of India. As yet material is

insufficient to compare the similarity and

richness of the Bhutanese fauna with these

figures. Bhutan is characterized by north-

south flowing rivers that ultimately drain

into the Brahmaputra and thence to the Bay

of Bengal. To the north the higher peaks of

the Himalayas form a barrier to reptile

movement. Mountain ridges also form

partial barriers to the west and east. Only

to the south is there low altitude access to

Bhutan. The mountains further subdivide

the country into a series of valleys between

which communication is likely only in the

subtropical south. As a consequence, the

majority of the species recorded are pan-

oriental in their distribution or, like

Platyurus platyurus, Sphenomorphus

maculatus, and Pseudoxenodon macrops,

are primarily Indo-Chinese species that

extend only as far west as eastern or central

Nepal. Eastern Himalayan endemics

include Trachischium guentheri and

Scincella sikkimensis. The distribution of

the two putatively endemic forms described

from Bhutan, Calotes bhutanensis and

Mabuya quadratilobus n. sp., remains

poorly known, but it is probable that at

least the latter may be found in adjacent

Sikkim or Assam. None of the taxa

reported here reflect Tibetan or

Mediterranean influences as reported for the

Nepalese reptile fauna by Swan and

Leviton (1962) and Nanhoe and Ouboter

(1987). At least in part, this is a reflection

of the limitation of previous collecting

efforts to the valleys and lower elevations

of Bhutan. This same factor precludes a

meaningful elevational analysis of

herpetofaunal distribution at this time. In

Bhutan, as elsewhere in the Himalayas,

there appears to be a strong correlation

between zonation of vegetation and that of

amphibians and reptiles (Dubois, 1974a,

1974b, 1981; Nanhoe and Ouboter, 1987).

The elevational profiles provided by

Baroni-Urbani et al. (1973) characterized

the native vegetation of the lower elevations

of Bhutan as: moist sal forest (200-800

m), evergreen montaine forest (700-1600

m), evergreen deciduous forest (1600-2800

m), and Rhododendron - conifer forest

(2800-3500 m). Dubois (1974b) regarded

elevations below 1000 m in neighboring

Nepal as tropical, those to 2000 m as

subtropical and those to 3000 m as

temperate, with higher elevations subalpine

or alpine in their climate and floral

characteristics. Although each of the

vegetation types is represented by at least

one collecting site, all are within the tropical

or subtropical zones, biasing the fauna

sampled against Tibetan or Mediterranean

taxa which would be expected to occur at

higher, more temperate elevations (Swan et

al., 1962). On the basis of the known

fauna of other areas of the Eastern

Himalayas only a fraction of the expected

species have as yet been recorded. Further,

phylogenies have not been proposed for the

majority of the known taxa, precluding the

application of cladistic biogeographic

methods (Humphries and Parenti, 1986) in

the analysis of pattern. It would thus be

premature to speculate about long-term

Vol. 4, p. 34

Asiatic Herpetological Research

February 1992

historical biogeographical patterns of the

Bhutanese reptile fauna and a more detailed

analysis is defered to a later date.

Acknowledgments

We are grateful to the participants of the

Naturhistorisches Museum Basel

expedition and to the authorities of the

museum, in particular Dr. Eugen Kramer,

for permission to identify and publish a

report of their collections. The staff of the

United States National Museum provided

useful comments and access to literature.

In particular Dr. Bruce Beehler provided

assistance in the location of Bhutanese

collecting sites and Addison Wynn

confirmed the identification of the

typhlopids. Prov.-Doz. Dr. Wolfgang

Bohme (Museum Koenig, Bonn) also made

significant contributions to the manuscript.

The holotype of Mabuya quadratilobus was

photographed at the University of Calgary

through the efforts of Dr. Tony Russell.

The senior author thanks the authorities of

the Museum fur Naturkunde der Humboldt

Universitat zu Berlin for extending the

invitation that led to this collaborative

project.

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February 1992

Asiatic Herpetological Research

Vol. 4, pp. 3-mT|

First Records of the Pipe Snake (Cylindrophis) in China

Kraig Adler1, Ermi Zhao2 and Ilya S. Darevsky3

^Cornell University, Neurobiology and Behavior, Seeley G. MuddHall, Ithaca, New York 14853, USA

2Chengdu Institute of Biology, P.O. Box 416, Chengdu, Sichuan, China

^Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia

Abstract. -Cylindrophis ruffus (Laurenti, 1768), the red-tail pipe snake, previously known from Burma

through Indochina and the East Indies, is reported from three localities in southern China (Hainan, Hong

Kong, and Xiamen). These are the first Chinese records for this snake family (Aniliidae or Uropeltidae,

according to different classifications). Justification is given for spelling the specific epithet ruffus and not

rufus.

Key words: Reptilia, Serpentes, snakes, Aniliidae, Uropeltidae, Cylindrophis, China, Indochina.

Introduction

The genus Cylindrophis is comprised of

eight species of snakes distributed in Sri

Lanka and from Burma through Indochina

and the East Indies. Until now, there were

no records for China. Historically, this

genus has been placed in the primitive

family Aniliidae (e.g., Goin et al., 1978;

Rieppel, 1979; Underwood, 1967), which

also includes Anomochilus of western

Malaysia and Sumatra, and Anilius of

South America; Loxocemus of Mexico and

Central America is sometimes also included

in this family. McDowell (1975, 1987),

however, separated the two Asian genera

from the Aniliidae, and placed them in the

subfamily Cylindropheinae of the family

Uropeltidae, which includes the shield-

tailed snakes (subfamily Uropeltinae), a

group of seven genera of burrowing snakes

restricted to Sri Lanka and peninsular India.

Chinese Records

We wish to report the first specimens of

this genus (and family) from China. All

appear to be referrable to the most widely

distributed species in the genus,

Cylindrophis ruffus (Laurenti, 1768),

which ranges from Burma to Vietnam,

south through peninsular Malaysia and

Indonesia (Fig. 1). The published records

nearest to China are for Bhamo, Burma

(Boulenger, 1888) and Myitkyina, Burma

(Wall, 1926), both of which localities are

about 50 km from the western border of

China's Yunnan Province. The species is

also known from northern Thailand:

Chiang Mai in the northwest and Sakon

Nakhon in the northeast (Cox, pers.

comm.). Deuve (1970) reported C. ruffus

from several localities in western Laos as

far north as Vientiane. Bourret (1935)

described four specimens in the collection

of the University of Hanoi, but none of

these has precise locality data; there are no

recent records from northern Vietnam (Tran

etal., 1981).

Our new records are from three widely-

separated localities in southern China (see

Fig. 1), as follows:

Fujian Province: Xiamen (Amoy

Island); Department of Biology, Xiamen

University, two unnumbered specimens,

collected at Xiamen by a farmer who dug

them out of the soil, date unknown but

prior to 1969.

Hainan Province: Hainan, no further

locality data; Zoological Institute, St.

Petersburg (Leningrad), (ZIN 7509),

collected in 1888 by Alfred Otto Herz.

Hong Kong: No further locality data;

Museum of Comparative Zoology (MCZ),

Harvard University, (MCZ 5489), collected

by a "Capt. Muller," and received in

exchange with Peabody Museum, Salem,

in 1886.

1992 by Asiatic Herpetological Research

Vol. 4, p. 38

Asiatic Herpetological Research

February 1992

';

u" .UojjP

JJegF0

Pal»waU

fpfraitzs"

B.d*l>'"c S'r /flm^'^

i

FIG. 1. Distribution of Cylindrophis ruffus in Indochina and southern China. The range extends through

Indonesia (including Sumatra, Java, and Borneo) as far east as the Celebes and nearby Batjan and Sangihe

islands. The new localities in China are Hainan, Hong Kong, and Xiamen (arrows). There are no known

authentic records from northern Vietnam. The dashed line indicates the northernmost limit of the South

China Biogeographic Region. (Base map adapted from New York Times Atlas of the World, 1985).

All of these localities are in that part of

China designated, on biogeographic

grounds, as the "South China Region"

(China Natural Geography Editorial Board,

1979), an area in southern China that

extends from western Yunnan eastward to

Fujian Province and includes Hainan and

Taiwan (Fig. 1). These records are all the

more surprising since this part of China has

been collected by herpetologists for many

decades. Clifford H. Pope and Malcolm A.

Smith failed to find Cylindrophis during

their extensive field work in Hainan in the

1920s, and Rudolf Mell, who resided in

Canton (=Guangzhou) from 1908 to 1921

and made comprehensive collections from

southern China, never found it. It is

unreported in Fujian by Ting and Zheng

(1974) in their survey of the snakes of that

province and also from Hong Kong

(Karsen et al., 1986; Romer, 1979). It is

possible, of course, that our specimens

from Hainan and Hong Kong, being old

records and without precise locality data,

merely were shipped from these places and

the specimens actually originated

elsewhere, but the newer records from

Fujian, even further north along the

Chinese coast and more distant from the

main range of the species, are undoubtedly

authentic.

On geographic grounds, the Chinese

specimens are referrable to the nominate

subspecies, C. r. ruffus. For the record,

we provide some meristic data for the

February 1992

Asiatic Herpetological Research

Vol. 4, p. 39

TABLE 1 . Meristic data for the Hainan Island and

Hong Kong Calamaria.

Hainan and Hong Kong specimens (Table

1); unfortunately, we have been unable to

reexamine the Fujian specimens to obtain

comparable data.

Further descriptive details are given

elsewhere (Zhao and Adler, 1989; Zhao

and Darevsky, 1990).

Natural History

Insofar as is known, all species of pipe

snakes, as they are commonly called, are

live bearing, inoffensive, and secretive in

nature, often being collected beneath fallen

vegetation or dug up by farmers from their

subterranean burrows. In Thailand, C.

ruffus is locally common and has been

collected in rice fields (it takes readily to

water) and in gardens near houses, where it

easily burrows in soft earth (Smith, 1943).

Schmidt (1928) reported a specimen found

in a salt water lagoon.

This is a distinctive snake, both

morphologically and behaviorally, and

should be easily recognized by collectors.

Members of the genus Cylindrophis are

heavy-bodied snakes, with no neck

constriction and a very short tail (Fig. 2A).

They reach a total length of nearly one

meter. The body of C. ruffus is banded

and boldly so on the venter. Males have

pelvic vestiges with tiny hind limbs

terminating in a claw-like spur on each side

of the vent. According to literature reports,

these snakes make little attempt to escape

FIG. 2. Cylindrophis ruffus. A: Hong Kong

specimen (MCZ 5489); note absence of neck

constriction and the very short tail (arrow marks

location of vent). B-C: Adult specimens, probably

from Thailand, in defensive posture. When

threatened, the head typically is hidden beneath the

body (B) or in debris (C) and the posterior end of

the body and tail are flattened, held over the body,

and sometimes aimed at the intruder, as shown in

B.

Vol. 4, p. 40

Asiatic Herpetological Research

February 1992

when exposed, but flatten the entire body

and curl the posterior end of the body and

the tail over the body, thus exposing the

bright red bands on their ventral surface

(Fig. 2B-C). Persons collecting in

southern China, including Taiwan, should

make a special effort to look for this snake.

Correct Spelling of ruffus

Laurenti (1768, p. 71) originally named

this taxon Anguis ruffa (two fs). His

original description is brief: "CXXXVIII.

Anguis ruffa. DIAGN. Corpore aequali,

ruffo, lineis transversalibus albis

interruptis; abdomine vario. Habitat

Surinami; hospitatur in Museo

Gronoviano,,y or in translation, "[Species]

138. Anguis ruffa. Diagnosis. Body

uniform, red, broken white transverse

bands; abdomen various. Lives in

Surinam; housed in Gronovius's

Museum." The description apparently is

based on Anguis species number 6 in

Gronovius (1756, p. 54), where fuller

details are given. Gmelin (1789)

apparently was the first to cite Laurenti's

new species, which he called Anguis rufus

(one f). Wagler (1828) associated this

species with his new genus Cylindrophis,

although he called his new species C.

resplendens, now regarded as a synonym

of ruffus. There can be little question that

Laurenti intended the spelling with two fs

and not as emended by Gmelin. Laurenti

used the two-f spelling twice in his

description (in both printings of the book;

for details of these editions, see Adler,

1989, pp. 12-13) and this spelling was not

corrected on his errata page. In classical

Latin, rufus is invariably spelled with a

single /, which probably led to Gmelin's

emendation. However, in late Latin

inscriptions and manuscripts, doubling of

consonants was often used to preserve the

length of the preceding vowel, here a long

u, for purposes of pronunciation

(Grandgent, 1907); thus, the alternate

spelling ruffus is a perfectly acceptable

form. Laurenti, in fact, routinely doubled

consonants before and after vowels in the

names of species throughout his book. The

International Code (1985, article 32) states

that an author's original spelling must be

preserved unless it contravenes provisions

of Articles 27-31 {ruffus does not) or there

is evidence in the original publication of an

inadvertent error (there is none). Thus,

"Anguis ruffa" is the correct original

spelling in the sense of the Code. The

Code makes no explicit statement about

doubling of consonants, but in passim there

are several instances of such names used as

examples in that book.

Acknowledgments

We thank Pere Alberch and Jose Rosado

(Museum of Comparative Zoology,

Harvard University) for loaning us the

Hong Kong specimen and some

comparative material. The USA National

Academy of Sciences has supported

Adler's and Zhao's research on the Chinese

herpetofauna, through its Committee on

Scientific Communication with the People's

Republic of China. Peter K. Knoefel and

Frederick M. Ahl provided advice

concerning classical Latin and Merel J. Cox

helped to delineate the range of C. ruffus in

Thailand. David M. Dennis kindly

supplied the photographs of living pipe

snakes.

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I February 199T

Asiatic Herpetological Research

Vol.4, pp. 42-54 1

A New Species of Grass Snake, Natrix megalocephala, from the Caucasus

(Ophidia: Colubridae)f

NIKOLAI L. ORLOV1 AND BORIS S. TUNIYEV2

^Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia

2Causasian State Biosphere Reserve, Sochi, Russia

Abstract. -A new species of Grass Snake, Natrix megalocephala, is described from the Caucasus

Mountains, of Azerbaijan, Georgia, and Russia. It differs from Natrix natrix in having a very thick

massive body, a large broad head, and enlarged frontal and temporal scales. Natrix megalocephala is found

in habitats with Colchida refugia vegetation.

Key words: Reptilia, Serpentes, Colubridae, Natrix, Azerbaijan, Caucasus, Georgia, Russia, USSR,

biogeography, distribution, taxonomy.

Introduction

In studying museum specimens of the

genus Natrix Laurenti and working with

Colchida snakes in the wild, we came to the

conclusion that three species of grass

snakes inhabit the Caucasus. This is based

on a morphological analysis of specimens

in collections. The possible genesis of the

species and the formation of their present-

day habitats is discussed.

Methods

We examined 15 specimens of Natrix

natrix persa Pallas, 15 specimens of N.

natrix scutata Pallas, and 19 specimens of

Natrix from the western Caucasus which

were thought to be a new species. The

following characters were used: 1- snout

vent length in mm (L); 2- tail length in mm.

(L. cd.); 3- number of scales around the

middle of the body (Sq.); 4- number of

ventrals (Ventr.); 5- number of subcaudals

(S. cd.); 6- number of upper labials (Lab.);

7- number of lower labials (Sublab.); 8-

length and width of the frontal; 9- length

and width of the parietals; 10- length,

height, and width of the head.

A comparative description of skulls in

+ This publication combines material previously

published in Russian by Orlov and Tuniyev

(1986a) with additional information.

Natrix n. scutata and the new species was

done. For a number of characters we

calculated mean numbers (x), error of mean

(m), and standard deviation (a) using

statistics from Lakin (1968).

Results

An analysis of the data show that the

grass snake which occurs within the

western Caucasus (known as the Colchida)

refugia may be regarded as a separate

species. This species, due to a very big

head, was given the name Natrix

megalocephala (Orlov and Tuniyev,

1986a). The common English name is the

Colchida Grass Snake.

Nomenclature Remarks

A number of synonyms were proposed

for the Caucasus Grass Snake. However,

after a detailed study, we came to the

conclusion that none of the proposed

synonyms fits the form described.

Nordmann (1840) mentioned two forms

for the Caucasus: Tropidonotus natrix var.

colchica and Tropidonotus natrix var.

nigra. The description and the drawing of

the first form agrees with Natrix natrix

persa (Pallas). That of the second form

agrees with Natrix natrix scutata (Pallas).

Derjugin (1899) regarded the form

Tropidonotus natrix var. nigra as a color

variation of T. natrix. Radde (1899) also

February 1992

Asiatic Herpetological Research

Vol. 4, p. 43

FIG. 1 . Various views of the head of the holotype

(ZIN 11846) of Natrix megalocephala from

Pitsunda, Abkhazia, Georgia.

'

FIG. 3. Ventral view of the holotype (ZIN

11846) of Natrix megalocephala from Pitsunda,

Abkhazia, Georgia.

FIG. 2. The head of the holotype (ZIN 1 1846) of

Natrix megalocephala from Pitsunda, Abkhazia,

Georgia.

FIG. 4. Dorsal view of the holotype (ZIN 1 1846)

of Natrix megalocephala from Pitsunda, Abkhazia,

Georgia.

Vol. 4, p. 44

Asiatic Herpetological Research

February 1992

mentioned that the form. T. natrix var.

scutata Pallas, which had black coloration,

occured in Likani in the vicinity of

Borjomi. Dinnik (1902) observed

Tropidonotus natrix var. ater Eichwald,

which actually are melanistic specimens of

N. natrix. Nikolsky (1913, 1916) gives

three forms of Tropidonotus natrix with

regard to the Caucasus: a typical form,

Tropidonotus natrix natrix; T. n. var.

scutatus Pallas; T. n. var. ater Eichwald.

The latter corresponded to melanistic

specimens of Natrix natrix.

The synonym "ater" cannot be used as

the name for the new species because

Eichwald (1831) employed it with regard to

melanistic individuals of the valid species

N. n. scutata (Pallas) from the suburbs of

Astrakhan, Russia. Terentyev and

Chernov (1949) and Milyanovsky (1957)

suggested that N. n. persa and N. n. natrix

occured in the Caucasus. The

overwhelming majority of authors have

named two forms for the Caucasus: Natrix

n. scutata (Pallas) and N. n. persa (Pallas),

(see, Bischoff and Engelmann, 1976;

Mertens and Wermuth, 1960).

The three forms, N. n. natrix, N. n.

persa and N. n. scutata which inhabit the

USSR territory are given in the field guide

of the herpetofauna of the USSR regarding

the Caucasus (Bannikov et al., 1977).

To date there is no definite conception

about the distribution and interaction of

Natrix natrix subspecies, particularly in the

western portion of its range. Presently

from 3 to 9 subspecies are recognized

(Thorpe, 1975). In his recent work Thorpe

(1980) suggested two initial centers of

Natrix speciation for the mainland: western

European and eastern European centers.

Natrix megalocephala

Orlov and Tuniyev, 1986

Holotype. — ZIN 1 1846, an adult female

from Pitsunda, Abkhazia, Georgia, western

Caucasus. The specimen was collected in

1909 by K. Satunin (Figs. 1, 2, 3 and 4).

Description of holotypes. — SVL 960

mm, tail length 240 mm. Head is covered

by large regular scales. Upper labials 8 on

the right and 7 on the left. Lower labials

are 1 1 on the right and 9 on the left. One

preocular and 3 postoculars on both sides.

The nasal touches 2 upper labials. Parietals

are large, 17 mm in length and 6 mm in

width. Large anterior chin shields are set in

two rows. Between posterior chin shields

are 3 rows of small scales 1+1+2. Two

rows of greatly enlarged irregular scales

follow temporals and parietals. The width

of the anterior chin shields are greater than

there height. The width of internasals

equals their length. The length of

prefrontals is greater than their width.

Nineteen scales surround the mid-body.

On the level of the 6th ventral scale from

the head and the 6th ventral from the tail

there are 19 and 17 scale rows respectively.

There are 172 ventrals. Two rows of

subcaudals, 68 scales each. The anal plate

is divided. The first row of lateral scales

bordering the ventrals has a smooth

surface. The scales of the second row are

barely keeled. The remainder are distinctly

keeled. Lateral and dorsal coloration is

bright black. The first half of ventrum is

spotted with alternating black and white

spots. Towards the tail white coloration

vanishes. White spots become smaller.

Subcaudals are black. Unspotted head is

black from above and white from below.

White coloration extends onto the lower

portion of upper labials. Black stripes go

along the edge of lower labials.

Description of paratypes. — ZIN 9039,

18794, 21535, 11243, 18794, 11247,

11862, 9594, 18211, 16653, 5273 (Fig. 5

and Table 1).

Diagnosis. — This snake differs from the

various subspecies of the closely related

species Natrix natrix Laurenti in having 1) a

very thick massive body; 2) a remarkable

big broad head; 3) enlarged frontal and

temporal scales.

Unlike the subspecies of N. natrix, in N.

megalocephala sutures between closely

adjacent head shields are not that well

defined. In N. natrix scales which cover

the head from above (prefrontal, frontal,

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Asiatic Herpetological Research

Vol. 4, p. 45

TABLE 1. Morphological characters of Natrix megalocephala.

preocular and pareitals) form a smooth

surface. In N. megalocephala head scales

are reliefed. The hatchlings of N .

megalocephala have two light blotches on

the head. This character, which is present

in a number of Natrix species, is an

ancestral feature (Fig. 6). While maturing,

the light blotches vanish and the snakes

acquire strong black coloration. All adult

specimens of N. megalocephala are pure

black dorsally, having no light blotches.

Comparative Description of Skulls in

Natrix megalocephala and Natrix natrix

scutata. — The skull of iV. megalocephala is

relatively higher and broader than that of N.

n. scutata (Fig. 7). There is a sharp grade

going from the frontal to the nasal.

Whereas in N. n. scutata the two bones lie

in one plane. In N. megalocephala the

parietal is slightly concave, whereas in TV.

n. scutata it is slightly protuberant laterally.

In N. megalocephala the scaled bone

ncreases towards the ocular hole, whereas

n N. n. scutata it is rectangular. The

quadrate is very broad at the junction with

he squamosum bone. The articular bone is

less concave than in N. n. scutata at the

unction with the pterygoid. In TV .

megalocephala the articular bone is

concaved inward to the skull. In TV. n.

scutata, however, dental and articular bones

form an exteriorly smoothly concaved arc.

On the lower surface of the basisphenoid

there is a well expressed longitudinal crest.

In N. n. scutata it is feebly expressed. On

the transversum of the basioccipital there is

a hollow which is absent in N. n. scutata.

Geographic Distribution. — The species'

range covers the western Transcaucasus. It

occurs from the suburbs of Tuapse,

Krasnodarsky Territory, Russia in the west

to the Chorokh River of Georgia and

Turkey in the southwest. From Tuapse,

the border of the distribution goes over the

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FIG. 5. Various views of the head of Natrix

megalocephala from Lagodekhi, Georgia.

Great Caucasus Ridge and then streatches

along thefoothills up to the area where the

Urushten and Malaya Laba rivers merge in

Krasnodarsky Territory, Russia.

Isolated populations are found along the

southern slope of the western Caucasus in

the vacinity of Lagodekhi, Georgia and

Vartashen, Azerbaijan. Isolated

populations are also found on the eastern

slope of Adjaro-Imeretinsky Ridge, in the

vicinity of Borjomi, Georgia (Fig. 8).

The species habitat is associated with the

Colchida or western Transcaucasian

botanico-geographical province

(Kuznetsov, 1891, 1909). Distributions of

isolated populations of Natrix

megalocephala coincide with vegetation

refugia of the Colchida type in Belo-

Labinsky district, in the canyon of mid-

flow of the Kura River and a number of

refugia on the southern slopes of the

Eastern Caucasus.

FIG. 6. Juvenile specimen

megalocephala (ZIN 19967).

of Natrix

Biotopic and Elevational Distribution. —

In western Transcaucasia Natrix

megalocephala ranges from the Black Sea

slope of the Great Caucasus Ridge up to the

subalpine belt. On the northern slope and

in the eastern refugia this species occurs in

the mountains up to 1000 m (Table 2). The

biotypes of N. megalocephala are

represented by forests of the Colchida type:

evergreen secondary trees, Fag us

orientalis, Quercus iberica, Taxus baccata,

Buxus colchica, Laurocerasus officinalis,

Fagetum nudum, Castanetum colchicum,

Alnetum strutiopteridosum, Fageto-Abieta

athirio-mixtogerbosa. More seldom

Quercetum azaleosum. This snake also

occurs in transformed areas such as forest

edge meadows, tea plantations, and

secondary hornbeam woods. Natrix

megalocephala is a mesophyllic species, but

unlike Natrix natrix and Natrix tesselata, it

is well adapted to swift montane rivers. In

case of danger, this species can hide in

swift waters.

Abundance. — It is a common but not

numerous species. It never forms such

dense populations as are found in N. natrix

and N. tesselata. The highest density is

observed in mixed Alder and Willow

forests along river beds, where up to three

specimens per kilometer walked may be

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FIG. 7. Skulls oi Natrix natrix scutaia (a, b) and Natrix megalocephala (c, d).

encountered.

Seasonal and Daily Activity. — On the

Black Sea coast of the Caucasus near

Sochi, N. megalocephala comes out of

hibernation in March and remains active

until November or early December. At

elevations of 600 to 1600 m the activity

period is shorter. For instance, in a gorge

of the Achipse River, we have observed

active snakes from the end of April to the

end of September. In the spring and fall N.

megalocepliala is active in the afternoon. In

these seasons snakes may be encountered

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FIG. 8. Distribution of Natrix megalocephala. Russia, Krasnodarsky Territory: 1- mouth of the

Urushten River; 2- Kisha Cordon, Caucasian Reserve; 3- Stanitsa (a small settlememt in the country side)

of Khamyshki; 4- Tuapse; 5- Lazorevskoye; 6- Sergei-Pole; 7- Sochi; 8- Malaya Khosta River; 9- Yew-box

Grove; 10- Achipse River. Georgia: 11- Lake Ritza; 12- Sukhumi; 13- Batumi; 14- setdement of Kheba;

15- setdement of Likani; 16- Borjomi; 17- Lagodekhi. Azerbaijan: 18- setdement of Vartashen. T- Type

locality, Pitsunda, Abkhazia, Georgia, a- Isotherm of the coldest month, above -3°C. b- Amount of

precipitation not less than 800 mm (after Gerasimov, 1966).

basking up to 1000 m away from a water

source during the warmest hours. In the

summer along the Black Sea coast N.

megalocephala is active in the morning,

during the late afternoon, and at night. For

instance, in the Yew-box Grove of the

Caucasus Preserve in the Labirintovaya

Wash, Sochi, Krasnodarsky Territory,

Russia, we observed N. megalocephala

hunting for Pelodytes caucasicus in July

from 2100 until 2330 hours. Summer

activity at mid-elevations has a daily two

peaked pattern: from 0900 until 1130

hours, and from 1630 until 1800 hours. It

is interesting to note that in the summer N.

natrix and N. tesselata are active strictly

during the day along the Black Sea coast of

the Caucasus.

Breeding. — A female N. megalocephala,

collected in the canyon of the Achipse River

on 11 August 1985, laid 13 eggs. Table 3

gives comparative data on size of the eggs

and hatchlings of N. megalocephala, N.

natrix, and N. tessalata. These data show

that N. megalocephala lays much bigger

eggs and its hatchlings are bigger in size

compared to the other representatives of the

genus. A female, which was collected in

the Yew-box Grove of the Caucasus

Preserve in the Labirintovaya Wash, Sochi,

Krasnodarsky Territory, Russia during

June 1990, laid a clutch of 11 eggs in

captivity on 20 August, 1990. The eggs

were incubated at 26-29° C and hatched on

29 September, 1990.

Diet. — Natrix megalocephala feeds

mainly on amphibians. Adults prey

actively on adult Bufo verrucosissimus. In

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TABLE 2. Habitat descriptions of Natrix megalocephala populations.

TABLE 3. Size of eggs and hatchlings of Natrix natrix, Natrix tesselata and Natrix megalocephala.

Note: 1- according to data of Bannikov et al. (1977); 2- according to data of Scherbak and Scherban (1980).

June, 1982 we collected a specimen in a

canyon of the Achipse River. It was 850

mm in length and contained a toad 120 mm

in length. In the Achipse Station within the

Caucasus Preserve this species was

observed to prey on Triturus vittatus, and

in the Yew-box Grove, on Pelodytes

caucasicus. Hatchlings feed mostly on

tadpoles and small specimens of P .

caucasicus and Rana macrocnemis. We

have observed juvenile N. megalocephala

preying on these amphibians in water

puddles of meadows and former river beds

of swift rivers in the vicinity of Sergei-Pole

(Serge Field), Krasnaya Polyana (Red

Meadow), Guzeripl, Yew-box Grove,

Achipse River Valley and a number of other

spots in the western Caucasus.

Shedding . — We observed snakes

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TABLE 4. A comparison of morphology and pholidosis in Natrix natrix scutata, N. natrix persa, and N.

megalocephala.

shedding skin on the southern slope of the

Great Caucasus Ridge at an elevation of

850 m from late June to early July.

Discussion

Natrix megalocephala differs from other

Natrix species in external morphology,

skull composition, size of eggs and

hatchlings. There are also ecological

differences. These differences suggest an

ancient separation of Natrix megalocephala

(Tables 1 and 4). In the east and southeast

N. megalocephala is sympatric with A'.

natrix persa. Sympatry has been observed

near Borjomi and Batumi, Georgia. In the

west and northwest portion of its

distribution, in the suburbs of Tuapse,

Goryachy Kluch (Hot Springs),

Khamychki and the Urushten River bed, of

Krasnodarsky Territory, Russia N.

megalocephala lives sympatrically and often

symbiotopically with Natrix natrix scutata.

In the collections of the Zoological Institute

St. Petersburg (Leningrad) there are

specimens (see ZIN 18744 and ZIN 1 1284)

collected from near Chornaly (suburbs of

Batumi, Georgia) and from Stanifsa (a

small settlement in the country side) of

Khamyshky, Krasnodarsky Territory,

Russia. Both Natrix species lived

sympatrically (Fig. 9).

Within the town of Pitsunda, Abkazia,

Georgia there is an isolated population of

Natrix natrix scutata. Apparantly, it is a

relict of the holocene xerathermal epoch.

Natrix megalocephala may also be

encountered at this spot (Fig. 10). Radde

(1899) thought that melanistic Natrix from

the Borjomi Canyon, Georgia were

Tropidonotus natrix var. scutatus Pallas.

He wrote: "It is interesting that this variety

occurs in Likani where it lives together with

T. natrix L, typ". Nikolsky (1913, 1916)

also wrote about sympatric occurance of N.

natrix typ., N. natrix scutatus and Natrix

natrix ater on the southern side of the Great

Caucasus Ridge. In the areas where N.

megalocephala lives sympatrically with

February 1992

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Vol. 4, p. 51

'map

*r

FIG. 9. The heads of Natrix megalocephala (a, b, c) and Natrix natrix scutata (d, e, f) from sympatric

populations at Stanitsa of Khamyshki, Krasnodarsky Territory, Ruissia.

other subspecies of Natrix natrix we did not

find hybrid characters in morphology

(Intergrading features). In all areas where

N. megalocephala comes into contact with

N. natrix and N. tessalata it has a distinct

morphological isolation (Table 4). Despite

evident phylogenetic relationship between

N. megalocephala and N. natrix it is

probable that these species diverged from

some ancient ancestral form not on the

territory of the Caucasus Isthmus, but

rather beyond it, when the Caucasus had

been an island. Supposedly, not less than

three faunogenetic centers contributed to the

invasion of Natrix species to the Caucasus

Isthmus in the Miocene: Asia Minor,

Kirkand-Elbursk, and South Europe

(Vereshchagin, 1958). Apparantly the time

of invasion and distribution differed. The FlG 10 The heads of Natrix al hala (a>

fact is supported by the entire location of b) and Na(rix na[rix SCMMa (c> d) from tnc

habitats and interaction of such forms as N. pop^^ in the vacinity of Pitsunda, Abkhazia,

natrix persa, and N. natrix scutata which Georgia, the type locality for Natrix

form intergrading populations in the megalocephala.

Vol. 4, p. 52

Asiatic Herpetological Research

February 1992

Caucasus, and N. megalocephala, which in

each overlapping area is distinctly separated

from N. natrix and N. tesselata.

It is evident that an ancestral form of N.

megalocephala came from Asia Minor in the

Miocene at the time the island of Caucasus

joined Asia Minor (Vereshchagin, 1958).

The Pleiocene was the time of apparent

general invasion of N. megalocephala to

forested subtropic areas of the Great

Caucasus and the western portion of the

Small Caucasus. At that time, this territory

was covered with moisture loving

vegetation similar to the type that presently

exists in the Colchida refugia (Kharadze

1974; Kholyavko et al., 1978). Vipera

kaznakowi Nikolsky invaded the Caucasus

in a similar way. Its present habitat

coincides with the range of N .

megalocephala (Orlov and Tuniyev, 1986b,

1990). Abundant food items like various

Anura (Chkhikvadze, 1984) also

contributed to the broad distribution of this

species under the favorable conditions of

damp subtropics. It is evident that at the

end of the Pleistocene, N. natrix persa

colonized the Talysh Mountains, presently

the Azerbaijan-Iran border. This species is

to a great extent associated with a

xerothermal regime. This is suggested by

the present range of the form which covers

semideserts and the dry steppes of eastern

Transcaucasus, Dagestan, and northern

Iran. During Pleistocene glaciation, which

covered high elevations of the Great and

Small Caucasus (Gvozdetsky 1954, 1958;

Markov et al., 1965), the habitat of N.

megalocephala had apparantly split into: 1)

the Colchida portion where subtropical

vegetation was preserved even in the most

severe periods of glaciation (Adamyants,

1971; Vereshchagin, 1958) and 2) other

smaller spots lying between the Belaya

Laba (White Laba) and Malaya Laba (Small

Laba) rivers, in Borjomi Canyon and in the

area of Lagodekhi-Zakataly, all in Georgia.

In the Pleistocene N. natrix scutata

invaded the Precaucasus. Previously it was

probably ousted by glaciers from the

European Plain to the lower areas of the

Don and Volga rivers. The Manychsky

Strait, which occasionally used to connect

the basins of the Black and Caspian seas

(Kvasov, 1975) would not have been able

to be a barrier for such water-loving forms

as N. natrix scutata to invade the

Precaucasus. Alternation of regressions

and transgressions of these seas (Kvasov,

1975; Vereshchagin, 1958) might provide a

wave shaped invasion for N. natrix scutata

to the Caucasus. During interglacier and

particularly the postglacier Holocene

period, a shift of all vegetation belts in the

Caucasus occured (Vereshchagin, 1958).

This contributed to the isolation of N .

natrix scutata and probably N. natrix natrix.

In the Holocene, formation of habitats

occupied by Natrix species and subspecies

had apparently been finished. The habitats

acquired contours similar to those presently

existing. Arid areas of eastern

Transcaucasia did not allow N .

megalocephala to restore the eastern portion

of its former distribution.

Analysis of the recent range of N.

megalocephala shows that the species does

not exceed the limits where the January

isotherm is -3 C° and precipitation is not

less than 800 mm yearly (Gerasimov,

1960). This along with the preference of

Colchida subtropical vegetation in general

support the fact that this warm and water

dwelling species is ancient. Bartenev and

Reznikova (1935) observed a higher degree

of melanism in representatives of the

Colchida fauna, some snakes included. In

this area melanistic specimens of Coluber

najadum (Maim in and Orlov, 1977) and

Vipera kaznakowi are found. Black color

is also prevalent in the coloration of N.

megalocephala from the Colchida.

It is interesting to note that apart from

melanism both V. kaznakowi and N .

megalocephala from the Colchida are

characterized by: 1) a big head, 2) a

massive body, and 3) a very small

population density compared to their

closely related species.

Acknowledgments

We would like to express our sincere

gratitude to Ilya S. Darevsky who aided us

a lot in preparing this paper and to

February 1992

Asiatic Herpetological Research

Vol. 4, p. 53

Rostislav A. Danov and Dmitrey G.

Akimov who provided the drawings. Lena

Bortuleva translated the manuscript into

English.

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endemic groups in the Big Caucasus].

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House, Leningrad 12:70-76. (In Russian).

KHOLYAVKO, V. S., D. A. GLOBA-

MTKHAILENKO, ANDE. S. KHOLYAVKO 1978.

[The tree atlas of the Caucasus]. Forest Industry

Publishing, Moscow. 215 pp. (In Russian).

KVASOV, D. D. 1975. Late Quaternary History of

big lakes and inner seas of Eastern Europe.

Science Publishing, Leningrad. 278 pp. (In

Russian).

KUZNETSOV, N. I. 1891. [Elements of the

Mediterranean area in Western Transcaucasia].

Notes of the Russian Geographic Society, St.

Petersberg 23(3): 1-190. (In Russian).

KUZNETSOV, N. I. 1909. Principles of dividing of

the Caucasus in botanic -geographical provinces.

In Papers of Russian Geographic Society. St.

Petersburg, ser. 8, vol. 24, n. 3, 1-174 pp. (In

Russian).

LAKIN, G. G. 1968. Biometry. High School

Publishing. Moscow. 284 pp. (In Russian).

MAIMIN, M. Y., AND N. L. ORLOV. 1971. On

three cases of melanism in Squamates. P. 27

In Problems of Herpetology. Abstracts of 5th

Soviet All-Union Conference. Science

Publishing. Leningrad. (In Russian).

MARKOV, K. K., G. I. LAZUKOV, AND V. A.

NIKOLA YEV. 1965. [The Caucasus]. Pp. 306-

321. In Quaternary Period (Glacier

anthropogenic period), vol. 1, Territory of the

USSR, part 2. Area of Ancient Glaciation of

High Mountains of the USSR South, chapter 2,

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February 1992

Moscow University Press, Moscow. (In

Russian).

MERTENS R., AND H. WERMUTH. 1960. Die

Amphibien und Reptilien Europas. Dritte

Liste, nach dem Stand vom 1 Januar 1960,

Frankfurt a. Main. 264 pp.

MTLYANOVSKY, Y. S. 1957. [On the snake fauna

of Abkhazia]. Works of the State Museum of

Abkhazia, Sukhumi, Tbilisi 2:199-203. (In

Russian).

NIKOLSKY, A. M. 1913. [Reptiles and

amphibians of the Caucasus]. The Caucasus

Museum Press, Tiflis, Georgia. 272 pp. (In

Russian).

NIKOLSKY, A. M. 1916. [Reptiles. The fauna of

Russia and adjacent countries, II, Ophidia].

Academic Press, Petrograd. 350 pp. (In

Russian).

NORDMANN, A. 1840. Cataloque raisonne des

mammiliferes de la faune Pontigue. In Voyage

dans la Russie Meridionale et la Crimee, par la

Hungrie, la Valachie et la Moldavie, execute en

1837, Paris, vol. 3. 350 pp.

ORLOV, N. L., AND B. S. TUNIYEV. 1986a. [A

new species of the grass snake Natrix

megalocephala sp. nov from the Caucasus].

Proceedings of the Zoological Institute,

Leningrad 158:116-139. (In Russian).

ORLOV, N. L., AND B. S. TUNIYEV. 1986b.

[Present ranges, possible ways of their

formation and phylogeny of the three species of

vipers from the Eurosiberic group (V .

kaznakowi complex) in the Caucasus].

Proceedings of the Zoological Institute, USSR

Academy of Sciences, Leningrad 157:104-135.

(In Russian).

ORLOV, N. L., AND B. S. TUNIYEV. 1990. Three

species in the Vipera kaznakowi complex

(Eurosiberian Group) in the Caucasus: their

present distribution, possible genesis, and

phylogeny. Asiatic Herpetological Research

3:1-36.

PALLAS, P. S. 1814. Zoogeographic rosso-

asiatica, sistens omnium animalium extenso

imperio rossico et adjacentibus maribus

observatorum recensionem. t. 3. Petropoli.

Acad. Scient. 428 pp.

RADDE, G. J. 1899. Museum Caucasicum. Die

Sammlungen des Kaukasischen Museums, Vol.

I, Zoology. Tiflis. 520 pp.

SCHERBAK, N. N., AND M. SCHERBAN. 1980.

[Amphibians and reptiles of the Ukranian Karpat

Mountains]. Naukova Dumka Publishing

House, Kiev, Ukraine. 253 pp. (In Russian).

TERENTYEV, P. V., AND S. A. CHERNOV. 1949.

[Guide to reptiles and amphibians]. Soviet

Sciences Publishing, Moscow. 315 pp. (In

Russian)

THORPE, R. S. 1975. Biometric analysis of

incipient speciaton in the ringed snake, Natrix

natrix (L.). Experientia 31:180-182.

THORPE, R. S. 1980. Microevolution and

taxonomy of European reptiles with particular

reference to the grass snake Natrix natrix and the

wall lizards Podarcis sicula and P. melisellensis.

Biological Journal of the Linnean Society.

London 14 (2):2 15-233.

VERESCHAGIN, N. K. 1958. [Genesis of the

terrain fauna of the Caucasus Isthmus]. Pp.

506-514. In Fauna of the USSR, Vol. 5.

Montane Areas of the European Part of the

USSR, Academic Press, Moscow. (In

Russian).

February 1992

Asiatic Herpetological Research

Vol. 4, pp. 55-56|

Cyrtodactylus madarensis Sharma (1980), a junior synonym of Eublepharis

macularius Blyth (1854)

INDRANEILDAS1

1 Animal Ecology Research Group, Department of Zoology, University of Oxford, South Parks Road, Oxford

0X1 3PS, England

Key words: Reptilia, Sauna, Gekkonidae, Cyrtodactylus madarensis, Eublepharis macularius, systematics.

Cyrtodactylus madarensis was described

by Sharma (1980) based on a single

juvenile male from near Madar (alt. 263 m),

approximately 5 km north-west of Ajmer

City, Rajasthan, in north-western India.

No diagnosis of the new species was

provided and the author compared his new

find, for reasons uncited, only with the

gekkonid, Cyrtodactylus stoliczkai, which

is restricted to the extreme northern parts of

India (Kashmir and Ladakh) and north-

western Pakistan (North-West Frontier

Province) and adjacent China (Welch et al.,

1990).

Examination of the photographs and a

close scrutiny of the type description of

Cyrtodactylus madarensis revealed that the

generic assignment of this taxon has been

erroneous. The plate (No. IV: A)

accompanying the paper clearly shows

thick upper eyelids that are pale in color,

which have been considered diagnostic of

another gekkonid genus, Eublepharis (see

Smith, 1935; Minton, 1966; Daniel, 1983).

In general, the color pattern of the dorsum

of the type is strikingly similar to Daniel's

(op cit.) Eublepharis macularius (Blyth,

1854) juvenile (Plate 16, top).

Other generic characters of Eublepharis

that were present in the type of

Cyrtodactylus madarensis include the

presence of lamellae under the digits; a

segmented, cylindrical tail; dorsum of body

with small granular scales intermixed with

large subtrihedral tubercles; and imbricate

ventral scales. Specific characters of

Eublepharis macularius noted in

Cyrtodactylus madarensis include a large

head with a distinct, narrow neck; pointed

snout; prominent tubercles on the dorsum;

nine upper labials; ten lower labials; hind

limbs reaching axilla; tail cylindrical,

segmented, tapering to a point and tail

length (36 mm) shorter than snout-vent

length (50 mm). The description of

coloration of dorsum agrees with that of

Eublepharis macularius provided by Smith

(1935) for juveniles (dark brown with

bands and a white nuchal loop), and as

previously noted, the type of C. madarensis

is virtually identical in coloration to the

juvenile of E. macularius illustrated in

Daniel (1983). Adults off. macularius are

dark brown or reddish brown above, with

the bands breaking up into spots.

Underwood (1954) revived the genus

Cyrtodactylus Gray (1827), whose

members are widespread from the shores of

the Mediterranean eastwards through the

Indian subcontinent, to Australia and the

islands of the south-west Pacific. The

subsequent splitting up of the genus by

Szczerbak and Golubev (1986) has been

criticised by Bauer (1987), but none of the

members of this taxonomically complex

group of padless geckos possess thick

movable eyelids. Eyelids among

gekkonids, in fact, are restricted to the

eublepharines.

Males of Eublepharis macularius possess

9-18 preanal pores (Smith, 1935), which

were not present in the type of

Cyrtodactylus madarensis, according to the

type description. However, the type was a

juvenile male (snout-vent length 50 mm).

Eublepharis macularius is known to reach

about 250 mm in total body length, the 300

mm length supposedly attained by the

species according to Theobald (in Smith,

1935) may refer to a third species of Asian

Vol. 4, p. 56

Asiatic Herpetological Research

February 1992

eublepharid, Eublepharis angramainyu (G.

Benyr, pers. comm.).

Bhati (1989) synonymised Eublepharis

macularius (Blyth, 1854) with E .

hardwickii Gray (1827) after claiming to

have examined a large series from

Rajasthan. However, no evidence of this

opinion was presented in the

communication. In fact, another recent

worker, Grismer (1988) has show both

species of Indian eublepharids to be valid

and that the ranges of the two species of

Indian eublepharine geckos are separated

by the plains of north-central India.

Eublepharis macularius enters India in the

north-west, with an apparently isolated

population in northern Maharashtra State in

western India, whereas E. hardwickii is

restricted to north-eastern peninsular India

and probably Bangladesh. The locality of

Sharma's Cyrtodactylus madarensis

therefore falls within the known range of

the first named species.

Thus, I consider Cyrtodactylus

madarensis a junior synonym of

Eublepharis macularius, a gekkonid lizard

found in north-western India, Pakistan, and

Afghanistan.

In the description of his new species,

Sharma claimed that the skin of his

specimen exhibited luminescence. No

explanation for this observation could be

given in the present note, except that the

pale bands on the dorsal aspect of the body

of Eublepharis macularius juveniles appear

extremely conspicuous against the dark

brown background, a color pattern that may

be aposematic.

Literature Cited

BAUER, A. M. 1987. The gekkonid fauna of the

USSR and adjacent countries (Book Review).

Copeia 1987(2):525-527.

BHATI, D. P. S. 1989. A critical evaluation of

the species of Eublepharis Gray 1827 (Reptilia:

Sauria). Proceedings of the First World

Congress of Herpetology. University of Kent at

Canterbury, 11-19 September: 28 (Abstract).

BLYTH, E. 1954. Proceedings of the Society.

Report of the Curator, Zoological Department.

Journal of the Asiatic Society of Bengal 23:737-

740.

DANIEL, J.C. 1983. The book of Indian reptiles.

Bombay Natural History Society, Bombay. 141

pp.

GRISMER, L. L. 1988. Phylogeny, taxonomy,

classification, and biogeography of eublepharine

geckos. Pp. 369-469. In R. Estes and G.

Pregill (eds.), Phylogenetic relationships of the

lizard families. Essays commemorating Charles

L. Camp. Stanford University Press, Stanford.

MINTON, S. A., JR. 1966. A contribution to the

herpetology of West Pakistan. Bulletin of the

American Museum of Natural History

134(2):27-184.

SHARMA, R. C. 1980. Discovery of a luminous

geckonid lizard from India. Bulletin of the

Zoological Survey of India 3(1&2):111-112,

lpl.

SMITH, M. A. 1935. The fauna of British India,

including Ceylon and Burma. Reptilia and

Amphibia. Vol. 2. Sauria. Taylor and

Francis, London. 440 pp.

SZCZERBAK, N. N. AND M. L. GOLUBEV. 1986.

[The gekkonid fauna of the USSR and adjacent

countries]. Nauka Dumka Publishing House,

Kiev. 232 pp. (In Russian).

UNDERWOOD, G. 1954. On the classification and

evolution of geckos. Proceedings of the

Zoological Society of London 124(3):469-492.

WELCH, K. R. G., P. S. COOKE, AND A. S.

WRIGHT. 1990. Lizards of the Orient: A

checklist. Robert E. Krieger Publishing

Company, Malabar, Florida. 162 pp.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 57|

The Type Locality of Agkistrodon halys caraganus

ROGER CONANT1

^Department of Biology, University of New Mexico; mailing address 6900 Las Animas NE, Albuquerque,

New Mexico 87110, USA

Key words: Reptilia, Serpentes, Viperidae, Agkistrodon halys caraganus , Kazakhstan, type locality.

Wolfgang Bohme (1991) called attention

to an error in the designation of the type

locality for Agkistrodon halys caraganus

(Eichwald). Inasmuch as Bohme's

correction appears in German in the midst

of his long, detailed review of the

Agkistrodon complex by Gloyd and Conant

(1990), and thus may be overlooked, it

seems advisable to summarize the facts

briefly in English. Eichwald (1831), in

describing caraganus, wrote "Hab. in ora

orientali caspii maris Tjuk-karaganensi ..."

In 1969, when Dr. Gloyd transferred his

major attention from the North American

members of the genus to those of the Old

World, he searched diligently but failed to

find any locality on any map of Asia

available to him that matched the one given

by Eichwald (fide Kathryn J. Gloyd, who

assisted him with his bibliographical

work). He eventually interpreted the

locality as Karaganda, north of Lake

Balkhash, because of its similar spelling

and its location within the range of the

taxon as implied from the list given by

Paraskiv (1956). The type locality for

caraganus was thus stated and mapped in

Gloyd and Conant (1990) as Karaganda. It

is unfortunate, during my own lengthy and

much later study on caraganus, that I did

not compare Eichwald's original statement

with more recently published maps. In the

(London) Times Atlas of the World, on

plate 46, Mys Tjub Karagan (Cape Karagan

Hill) appears at the tip of the Mangyshlak

Peninsula on the eastern side of the Caspian

Sea. This is certainly the equivalent of

Eichwald's "Tjuk-karaganensi," as Bohme

pointed out. The type locality for

Agkistrodon halys caraganus is on the

eastern edge of the Caspian Sea in

Kazakhstan and not at the city of

Karaganda.

Literature Cited

BOHME, W. 1991. Review of Gloyd, H. K. and

R. Conant (1990): Snakes of the Agkistrodon

complex. A monographic review. Salamandra

27:126-128.

EICHWALD, E. 1831. Zoologia specialis quam

expositis animalibus turn vivis, turn fossilibus

potissimum Rossiae in universum, et Poloniae

in specie . . . Vilnae, Typis Josephi Zawadzki

3:170.

GLOYD, H. K., AND R. CONANT. 1990. Snakes

of the Agkistrodon complex: A monographic

review. Society for the Study of Amphibians

and Reptiles, Contributions to Herpetology 6.

vi, 614 pp.

PARASKIV, K. P. 1956. [Reptiles of

Kazakhstan]. Academy of Sciences of

Kazakhstan, Alma-Ata. 288 pp. (In Russian).

I February 1992

Asiatic Herpetological Research

Vol. 4, pp. 58-61

Evaluation of Snake Venoms among Agkistrodon Species in China1

Yuancong Chen1, Dawei Zhang2, Kexian Jiang2 and zho-nghui Wang2

^Shanghai Institute of Biochemistry, Shanghai, China

2Shanghai Institute of Biological Products, Shanghai, China

Abstract. -Venom toxicity and enzymatic activities were examined in six species of Chinese

Agkistrodon and Deinagkistrodon acutus. The venom toxicity of A. inlermedius is the strongest, ten

times that of Deinagkistrodon acutus. The venoms of A. blomhoffii brevicaudus, A. blomhoffii

ussuriensis, and A. shedaoensis are the next strongest. Agkistrodon saxatilis venom had a similar toxicity

as A. strauchii venom and they are more similar to Deinagkistrodon acutus in toxicity.

Key words: Reptilia, Serpentes, Viperidae, Agkistrodon, Deinagkistrodon, China, venom, toxicity.

Introduction

Agkistrodon snakes are widespread and

abundant in China. According to Zhao et

al. (1981) and Chen et al. (1984) they

should be classified as: (1) Agkistrodon

blomhoffii brevicaudus Stejneger, (2) A. b.

ussuriensis Emelianov, (3) A. intermedius

(Strauch), (4) A. saxatilis Emelianov, (5)

A. shedaoensis Zhao, (6) A. strauchii

Bedriaga (Plate 1), (7) A. monticola

Werner, and (8) Deinagkistrodon acutus

(Gloyd, 1979). The later was formerly

regarded as Agkistrodon acutus.

The components and properties of

venoms from these species are strikingly

different from each other (Zhao et al.,

1981). From the standpoint of venoms the

general designation of Chinese Agkistrodon

as only one species, A. halys Pallas,

should not be accepted. Recently in China,

Agkistrodon venoms have been used to

make medicines to cure thrombotic disease

and cancers. SVATE (Snake Venom Anti-

thrombotic Enzymes) was first prepared

from the venom of A. shedaoensis from

Snake Island in Dalian, and was effective in

curing thrombosis. Since there was a

shortage of A. shedaoensis venom, the

venom of A. b. brevicaudus from Zhejiang

in eastern China was also used. However

the product of A. shedaoensis seemed

+ This publication was previously published in

Chinese by Chen et al. (1990).

better than that from A. b. brevicaudus.

Later, two products, one named Qin Suan

Mei using the venom of A. b. ussuriensis,

and the other named Defibrinogenase using

the venom of D. acutus also appeared in

clinical application, but their efficiency and

side reactions differed from each other.

787 Snake Venom Capsules, made by

Shanghai Xin-Le District Hospital using the

crude venom of A. b. brevicaudus for

treatment of cancers has a magically

inhibitory effect on the growth of malignant

tumour cells. These observations aroused

our interest to understand the differences of

Agkistrodon venom properties. In this

paper we determined the toxicity (LD50),

and enzymatic activities of arginine

esterase, proteolytic and fibrinolytic

enzymes to evaluate the quality of selected

pit-viper venoms.

Methods

Snake Venoms

Agkistrodon b. brevicaudus were

purchased from the Shanghai Experimental

Animal Supply Station. Agkistrodon b.

ussuriensis, A. shedaoensis, and A.

strauchii were kindly provided by

Professor Ermi Zhao of the Chengdu

Institute of Biology. Agkistrodon

intermedius was kindly provided by Mr.

Jinbao Yu from Xinjiang Institute of

Chemistry. Deinagkistrodon acutus were

purchased from Jindezeng Snake Institute,

Jiangxi.

1992 by Asiatic Herpetological Research

February 1992

Asiatic Herpetological Research

Vol. 4, p. 59

Chemical Reagents

BAEE (N-benzoyl arginine ethyl ester

hydrochloride), are products of th

Dongfeng Factory of Biochemical

Reagents. Human fibrinogen and thrombin

are products of the Shanghai Institute of

Biological Products and casein is a product

of the Factory of Chemical Reagents,

Shanghai. All other chemical reagents are

analytical grade.

Toxicity (LD50)

Toxicity (LD50) was assayed (Litchfield

and Wilcoxon, 1949). We dissolved 3-5

mg of snake venom in physiological saline,

and then diluted the venom solution to 1-5

concentrations. Swiss mice of 18-20

grams of body weight, were divided into

five groups, with six individuals each.

Mice were injected intra-abdominally with

0.4 ml of venom solution. After injection

observations were made within 48 hours.

The death rate (LD50) was then calculated.

Enzymatic Activities

1. Arginine esterase (United States

Pharmacopea, 1980). — BAEE solution

(0.8 mm moles) was prepared by

dissolving BAEE in 0.05 M pH 8.0 tris-

HC1 buffer solution. Three ml of BAEE

solution was inserted into a cuvette and 0.1

ml of snake venom solution was added.

Spectrophotometric measurements were

made at 253 nm and 25°C. The unit of

activity is calculated according to the

formula, U/mg =Ai - A2/O.OO3 x TWAT.

The last value is at the linear part of the

curve, where A2 is the initial value, T is the

time tested, and W is the weight of venom

in miligrams.

2. Proteolytic enzyme (Rick, 1963). —

One gram of casein was dissolved in 100

ml of 0.05 M Tris-HCl pH 7.8 buffer in a

boiling water bath and the undissolved

materials were filtered. We transfered 2 ml

of filtrate to a test tube and incubated it in a

37° C water bath. Then two ml of venom

solution (2 mg / ml) was added. After 15

minutes we added 15 ml of 15%

trichloroacetic acid and mixed it

thoroughly, filtering after 30 min. The

filtrate was measured at 280 nm. We

calculated the tyrosine released from the

standard curve of tyrosine. The unit of

activity is denoted by jig of Tyr/15 x mg of

venom.

3. Fibrinolytic enzyme (Deogny et al.,

1975). — We dissolved 0.5 grams of human

fibrinogen in 10 ml of pH 7.75 barbiturate

buffer and transfered 5 ml of the solution

into each of two petri dishes (8 cm

diameter). We subsequently added 1 ml of

thrombin (about 4 units) and mixed it

thoroughly. Then we immediately added 5

ml of 2% agar solution (below 60°C) and

mixed it again to get a uniform plate. Wells

were punched in the plate into which was

put 10 \i\ of venom solution; incubated at

37°C for 18 hours. One unit of activity is

equal to 1 mm2 of lysis on the plate. The

activity is denoted by units = mm2/mg of

venom.

Results

The venom toxicity of A. intermedins is

the strongest, ten times that of

Deinagkistrodon acutus (Table 1). The

venoms of A. b. brevicaudus and A. b.

ussuriensis are the next strongest.

Neurotoxins were isolated from these

venoms. A presynaptic neurotoxin,

Agkistrodotoxin, has been purified from

the venom of A. b. brevicaudus (Chen et

al., 1981) and its amino acid sequence also

has been determined (Kondo, 1989).

Three presynaptic neurotoxins were

purified from the venom of A. intermedius.

Their LD50 are 38, 49 and 49 ^ig/kg of

mice respectively, higher than that of

Agkistrodotoxin which has a LD50 of 55

Hg/kg (Zhang and Hsu, 1985a). A fraction

from column chromatography of the venom

of A. b. ussuriensis has been confirmed to

be neurotoxic (Zhang and Hsu, 1985b).

The venoms of A. shedaoensis and D.

acutus are non-neurotoxic. Therefore the

potency of toxicity appears to be related to

the neurotoxin content.

Vol. 4, p. 60

Asiatic Herpetological Research

February 1992

TABLE 1 . Comparison of toxicity and enzymatic activities of Agkistrodon and Deinagkistrodon venoms.

Discussion

There are many components in the

venom of Agkistrodon which react with the

blood circulation causing bleeding, such as;

hemorrhagin, arginine esterase, proteolytic

and fibrinolytic enzymes. Three

hemorrhagins had been purified from the

venom of D. acutus (Xu et al., 1981),

which have proteolytic activity, reacting

with the blood vessel wall causing the

leakage of red cells. Arginine esterase

containing three enzymes: thrombin-like,

kallikrein and plasminogen activator, which

cause the failure of coagulation of the

blood, depression of blood pressure and

activation of fibrinolytic system.

Enzymatic activity data shows no sharp

differences in the venom of A. shedaoensis

compared to other venoms studied. The

fibrinolytic activities are very close to each

other due to the inaccuracy of the diffusion

method. We should point out that the

quality of snake venoms are deeply affected

by the conditions of milking venom, such

as; seasons, temperature and lyophylizing

equipment.

biochemical properties of presynaptic

neurotoxin from the snake venom of

Agkistrodon halys Pallas]. Acta Biochimica et

Biophysica Sinica 13:205-211. (In Chinese).

CHEN, Y., X. WU.AND E. ZHAO. 1984.

[Classification of Agkistrodon species in

China]. Toxicon 22:53-61.

CHEN, Y., D. ZHANG, K. JIANG, AND Z. WANG.

1990. [Evaluation of snake venom of Chinese

species of the genus Agkistrodon}. Pp. 312-

314. In E. Zhao (ed.) From water onto land.

China Forestry Press, Beijing. (In Chinese).

DEOGNY, L., A. WEIDENB ACH, AND W .

HAMPTON. 1975. Improved fibrin plate

method for fibrinolytic activity measurements;

Use of bentonite precipitation and agar

solidification. Clinica Chimica Acta 60:85-89.

GLOYD, H. K. 1979. A new generic name for the

hundred - pace viper. Proceedings of Biological

Society of Washington 91:963-964.

KONDO, K., J. ZHANG, K. HSU, AND H.

KAGAMIYAMA. 1989. Amino acid sequence of

presynaptic neurotoxin, Agkistrodotoxin, from

the venom of Agkistrodon halys Pallas. Journal

of Biochemistry (Japan) 105:196-203.

Acknowledgments

The authors are grateful to Professor

Ermi Zhao and Mr. Jinbao Yu for

providing valuable snake venoms.

Literature Cited

LITCHFIELD, J., AND F. WILCOXON. 1949. A

simplified method of evaluating dose effect

experiments. Journal of Pharmacology and

Experimental Therapeutics 96:99-1 13.

RICK, W. 1963. Methods of enzymatic analysis.

H. U. Bergmeyer (ed.) Academic Press, New

York. 800 pp.

CHEN, Y., X. WU, J. ZHANG, M. JIANG, AND K.

HSU. 1981. [Further purification and

UNITED STATES PHARMACOPEA, 21 REVISION.

1981. United States Pharmacopeal Convention.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 61

835 pp.

XU, X., C. WANG, J. LIU, AND Z. LU. 1981.

Purification and characterization of hemorrhagic

components from Agkistrodon aculus (hundred

pace snake venom). Toxicon 19:633-644.

ZHANG, J., AND K. HSU. 1985a. [A comparison

of neurotoxin components in the venoms of

Chinese Agkistrodon species]. Acta

Herpetologica Sinica 4:287-290. (In Chinese).

ZHANG, J., AND K. HSU. 1985b. [Presynaptic

toxins from Agkistrodon intermedius venom].

Acta Herpetologica Sinica 4:291-295. (In

Chinese).

ZHAO, E., G. WU, X. WU, Y. CHEN, M. JIANG,

J. ZHANG, AND K. HSU. 1981. [A comparison

of snake venom electrophoretogram of

Agkistrodon species of China and their value in

snake taxonomy]. Acta Zoologica Sinica

27:211-217. (In Chinese).

I February 1992"

Asiatic Herpetological Research

Vol. 4, pp. 62-67]

Female Reproductive Cycle and Embryonic Development of the Chinese

Mamushi (Agkistrodon blomhoffii brevicaudusY

MEHUA HUANG1, YUMIN CAO1, FENGXUE ZHU1 AND YUNFANG QU1

lZhejiang Medical University, Hangzhou, China

Abstract. -Agkistrodon blomhoffii brevicaudus is a species of snake with seasonal reproduction. The

female annual reproductive cycle is as follows: vitellogenesis begins in late March or early April;

ovulation is in middle June and parturition is in middle or late August, or in early September. The

gestation period lasts for about 65-75 days. By ovoviviparity, the Chinese Mamushi produces one clutch

per year. In each clutch, there are 5 to 20 juveniles with a length of 154 to 203 mm and a weight of 2.0 to

5.3 g. The size of fat bodies is inversely proportional to that of the vitellogenesis. The fat bodies were

larger in March and before hibernation (about November ) than in the other months. The process of

embryonic development is described by the external morphological investigation on 73 1 embryos from 82

females.

Key words: Reptilia, Serpentes, Agkistrodon blomhoffi brevicaudus, Chinese Mamushi, reproduction,

embryonic development

Introduction

The Chinese Mamuashi (Agkistrodon

blomhoffii brevicaudus) is distributed

mainly over southern Liaoning, Hebei,

Jiangsu, Anhui, Zhejiang, Jiangxi,

northern Fujian, Taiwan, Hubei, Shaanxi

(southern part of the Qinling Mountains),

southeastern Gansu, Sichuan and Guizhou

provinces in China. It is also scattered over

the Korean peninsula. It is a species of

poisonous snake with a high medical value,

so it attracts many scientists' attention.

This paper reports the female reproductive

cycle, embryonic development and

reproduction of" the Chinese Mamushi. It is

hoped that this paper will serve as a

reference material for research in

reproductive biology and the artificial

breeding of snakes.

Methods

Mature female Chinese Mamushi (A.

blomhoffii brevicaudus), 447-680 mm

(mean 530 mm) in length and 31-120 g

(mean 67 g) in weight, were collected from

+ This publication combines material previously

published in Chinese by Huang et al. (1990) with

additional discussion.

Tiantai County, Zhejiang Province, and

were bred in our snake garden. From

March 1984 to December 1986, 178

females (about 5 females per month) were

investigated. Each snake was measured in

total length (SVL+TL) and total weight.

The number and the size of follicles or

embryos, as well as the weight of the

ovaries and fat bodies, were examined by

dissection. The pH value, whether sperms

were stored up or not and the sperms'

activity in the oviducts were determined

too. All the above were done in order to

understand seasonal variation of sex

glands, ovulation and mating. From 1984

to 1987 in the gestation season (June, July

and August) 82 mature female snakes were

operated on and 731 embryos were

obtained. The conditions of embryonic

development were based on the studying of

the external morphology of the embryos

removed from the gravid females at regular

intervals throughout the gestation period.

Another 10 gravid females were bred apart

to observe their rate of reproduction.

Results

The Female Reproductive Cycle

I. The seasonal variation of ovary weight.

The ovary weight is expressed by

(Ci 1 QQ9 hv Avtntir* //^rn^M/^oir/j/ ftfwnrrh

February 1992

Asiatic Herpetological Research

Vol. 4, p. 63

5.00.

ff

4.50-1

4.00 -j

3.50 -j

3.00 -j

2.50-=

2.00-

1.50

1.00

0.50 A

0.00

Coefficient of Ovary

Coefficient of Fat

,.— .,... |--« -| ■-- - ,-■ ■ ■, |-« | ■-■■■ | r

Jan. Feb. Mar. April May June July Aug. Sept. Oct. Nov. Dec

FIG. 1 . Seasonal variation of ovary and fat body weight in Agkistrodon blomhoffd brevicaudus.

multiplying the coefficient of ovary (the

ratio of wet weight of a pair of ovaries to

that of total body weight of each individual)

times 100 to take the form of a percentage.

Figure 1 shows the seasonal variation. The

eggs of the ovary were transferred to the

oviduct in mid June. The coefficient of

ovary reached the lowest point in July and

then increased gradually. From late March

to April in the next year, with vitellogenesis

occuring, the coefficient of ovary rose

obviously. It reached its top value in May

or June.

//. The seasonal variation of fat bodies.

The weight of fat bodies is expressed by

multiplying the coefficient of fat (the ratio

of the wet weight of fat body to that of the

total body weight of each individual) times

100 to take the form of a percentage.

Figure 2 shows its seasonal variation with

two peaks in March and November. There

was an inverse correlation between

vitellogenesis and fat body size. Fat bodies

enlarged in spring, reduced in September

(after parturition), and then increased

gradually until November (before

hibernation).

///. The seasonal variation of follicle types.

Developing ovarian follicles were divided

into three classes by their size and location.

Previtellogenic follicles were designated as

class 1, vitellogenic ovarian follicles as

class 2, and oviductal eggs as class 3. The

Chinese Mamushi (A. blomhoffii

brevicaudus) is a species with annual snake

reproduction. All the mature females have

class 1 follicles with a diameter of 0.5 to

10.0 mm, with a transparent or white color

and round or oval shape. In April class 1

follicles were at their maximum in number.

On the average, there were 25 class 1

follicles per female. The larger the size of

the female, the larger the number of class 1

follicles it had. The largest female was 680

mm in length and 120 g in weight, and had

69 previtellogenic follicles. In

spring, vitellogenesis began and follicles

grew rapidly. Some of the class 1 follicles

Vol. 4, p. 64

Asiatic Herpetological Research

February 1992

35.

m

O

30-

25-

o

ID

20-

§ 15-

S 10-

g

O

H

5-

0-

D Previtellogenic Follicles

-0 — Vitellogenic Follicles

-A — Oviductal Eggs

■ □

a — h-

■S B— -H B H

1 1 1 1 1 1 1 1 1 1 1

Jan. Feb. Mar. April May June July Aug. Sept. Oct. Nov. Dec.

FIG. 2. Seasonal variation of follicle and egg size in Agkistrodon blomhoffii brevicaudus.

were transformed into class 2 follicles with

yellow color, oval shape, and long

diameters between 11.0-25.0 mm. They

only existed from April to June. When

follicles reached the largest value in about

middle June, ovulation occured. The date

of the earliest ovulation took place on June

16. Class 3 eggs were present in the

oviducts from middle June to late August.

The maximum diameter of an egg was 28.0

mm. The pH in the oviducts was 7.26+0.6

Embryonic Development

The development of the external

morphology is described as follows. In

middle June ovulation occurred, and eggs

transferred to the oviducts. Fertilization

and development took place. A small oval

blastodisk divided on the large ellipsoidal

yolk mass to form the blastula. Then

gastrulation proceeded to form a blastopore

marking the posterior end of the embryonic

shield (Huang et al., 1989, stages 1-3). In

late June the neural plate raised and folded.

The blastopore was still visible. Then the

neural groove appeared and expanded at the

cephalic end. The amniotic fold was

sharply raised anteriorly toward the head

and covered more than half the embryo.

After that the posterior amniotic fold was

beginning to cover the tail bud. The neural

tube was formed by the fusion of the neural

folds. The amnion was closed. The

allantois bulged slightly and was not

inflated. The first rudiments of the heart

and optic vesicles were formed (Huang et

al., 1989, stages 4-9). In early July the

allantois began to inflate. The heart took a

"U" shape and began to beat. The caudal

part of the embryo began to coil. Lans

placodes invaginated. The mandibular

segment and the auditory pits were visible.

Branchial clefts were formed with the

appearance of the nasal pits. The eye was

lightly pigmented. Furthermore, the heart

was shaped like an "S". Then both the

ventricle and auricle were distinguishable.

The cloacal mound was visible and the

rudiment of the hemipenes appeared. The

February 1992

Asiatic Herpetological Research

Vol. 4, p. 65

TABLE 1 . Reproductive data on 10 adult female Agkistrodon blomhoffi brevicaudus.

1- Nine still bom. 2- One still born.

trunk coiled 4.5 circles (Huang et al.,

1989, stages 10-11). By middle July the

hemipenes became vesicle-like projections.

The upper and lower jaws were visible and

the trunk loosened into four circles (Huang

et al., 1989, stage 12). In late July the

hemipenes were blunt fork-like projections.

The tongue was visible. The mid-line of

the ventral body was enclosed except in a

small circular area. Scales appeared on the

trunk but not on the head. The trunk

loosened further and coiled only 3-3.5

circles (Huang et al., 1989, stage 13).

During early August scales on the trunk

appeared to be keeled and their pigment

pattern was well developed. Scales and

pigmentation on the head were visible but

the pattern was not well developed. The

whole mid-line of the ventral body was

enclosed. The hemipenes were still

everted. The trunk coiled 2-2.5 circles

(Huang et al., 1989, stages 14-15 ). In

middle August the pigment pattern fully

developed. The hemipenes were inverted

in all the male specimens. Just prior to

parturition, the embryo showed all the

morphological characteristics of its own

family. (Huang et al., 1989, stage 16).

Reproduction

The gestation period lasted for about 65-

75 days and parturition occurred in middle

to late August or September. Table 1

shows the state of the reproduction of 10

gravid females. Ten gravid females

produced 10 litters which included 97

juveniles. The mean number per litter was

about 10. Among 10 litters of new babies,

about 99% had survived except one litter

which had 9 stillbirths. All the live babies

were 154 to 203 mm in length and 2.0 to

5.3 g in weight.

Discussion

I. According to Saint Girons (1982), the

reproductive cycle of male snakes has four

major types: 1) aestival (summer) or

postnuptial type; 2) mixed type; 3)

prenuptial type; and 4) continuous

reproductive activity type. The

reproductive cycle of the Chinese Mamushi

(A. blomhoffii brevicaudus) belongs to the

Vol. 4, p. 66

Asiatic Herpetological Research

February 1992

first type (Lin et al., in press), which is

found only in temperate and subtropical

regions. Spermatogenesis begins in spring

after hibernation and spermiogenesis begins

in summer. The spermatozoa are stored

throughout the winter in the epididymis and

vas deferens of the male or in the oviducts

of the female. According to Saint Girons

(1966), the reproductive cycle of female

snakes has annual types A-F-G and

biennial types B-C-D. By our observation

the Chinese Mamushi {A. blomhoffii

brevicaudus) is thought to be the annual

type F. Its mating season is spring (April

or May) and ovulation occurs regularly in

middle June, while spermatogenesis is the

aestival type. Sperm are stored in winter in

the vas deferens of the male or in the female

oviducts if there is fall mating. Sperm of

the Chinese Mamushi (A. blomhoffii

brevicaudus) may be stored in the oviducts

and kept available for about three years (Hu

et al., 1966). This characteristic is of great

benefit to the survivialship of the Chinese

Mamushi 04. blomhoffii brevicaudus).

II. Several investigators have found an

inverse correlation between reproduction

(vitelogenesis) and fat body size in snakes

(Seigel and Ford, 1987). In snakes with

annual reproduction (e.g. Opheodrys

aestivus), fat bodies enlarge in spring,

reach a low point in early to middle summer

(egg-laying) and then increase gradually

until hiberntion. In species with biennial or

triennial reproduction, e.g. Vipera berus

and Crotalus viridis, fat body reserves are

lowest at the time of parturition (Macartney

and Gregory, 1988; Seigel and Ford,

1987). Seasonal variation of fat bodies of

the Chinese Mamushi 04. blomhoffii

brevicaudus) is similar to the above

observation. There are two peaks in March

(spring) and November (hibernation). The

low point is in September (at the time of

parturition).

III. The sexual maturity of the Chinese

Mamushi (A. blomhoffii brevicaudus) is

attained in 2-3 years. Jin et al. (1983)

mentioned that vitellogenesis began in the

second spring after birth (20 months old),

350-484 mm long and 20-60 g in weight.

In the Lined Snake (Tropidoclonion

lineatum) from St. Louis, Missouri, USA,

the same result was obtained by Krohmer

and Aldridge (1985). All die females in our

experiment were mature with a length of

more than 447 mm and a weight of over 3 1

g each. There was a positive correlation

between the number of yolking follicles or

embryos and female length. The average

number of embryos from 82 females was

ten. Seventy one percent of the females

400-500 mm long contained less than ten

embryos, while 75% of the females 500-

600 mm long contained more than ten

embryos.

IV. The Chinese Mamushi is

ovoviviparous, which is evolved from

oviparity. It is said to be an adaptation to

variable environments where stochastic

events jeopardize egg survivorship. But

Seigel and Ford (1987) thought it also had

some disadvantages, including lower clutch

frequency, more mortality risks to the

parent, less intake of food and higher

metabolic cost of the parent. The clutch

mass of ovoviviparous snakes is smaller

than that of oviparous snakes. The

physiological costs of reproduction (heart

rate and oxygen consumption) significantly

increased during pregnancy in

ovoviviparous snakes. We found that

pregnant snakes cease feeding during the

last period of gestation, so they were thin

and weak after parturition. If they did not

gain enough food in time, they would be

dead during hibernation or by the next

spring. However we think that

ovoviviparity is more favorable in

protecting the filial generation because the

survival rate is much higher in the Chinese

Mamushi (A. blomhoffii brevicaudus). In

our experiment the survival rate reached 90-

99%.

Acknowledgments

This study was supported by a grant

from the National Natural Science

Foundation of China and the Education

Commission of Zhejiang Province, China.

We are very grateful to Mr. Fumine Dong

for breeding the snakes and to Miss Fan

Yang and Mr. Jinxiang Yuan for

commenting on and typing the manuscript.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 67

Literature Cited

HU, B., M. HUANG, S. HE, S. ZOU, Z. XIE,

ANDB. CAI. 1966. [A preliminary report on

some ecological observations of Agkistrodon

halys and Naja naja atra]. Acta Zoologica

Sinica 18(2):187-194. (In Chinese).

HUANG, M., Y. CAO, F. ZHU, AND Y. QU.

1989. Stages in the normal development of

the Chinese Mamushi (Agkistrodon

blommhoffii brevicaudus). Pp. 34-40. In M.

Matsui, T. Hikida and R. C. Goris (eds.),

Current Herpetology in East Asia. The

Herpetological Society of Japan, Kyoto.

HUANG, M., Y. CAO, F. ZHU, AND Y. QU.

1990. Female reproductive cycle and

embryonic development of Chinese Mamushi

(Agkistrodon blomhoffii brevicaudus). Pp.

173-177. In E. Zhao (ed.) From water onto

land. China Forestry Press, Beijing. (In

Chinese).

JIN, Y., AND H. GU. 1983. [Elementary report

on ecological observations of juvenile

Chinese Mamushi]. Journal of Zhejiang

Traditional Chinese Medical College 5:57-61.

(In Chinese).

KROHMER, R. W., AND R. D. ALDRIDGE.

1985. Female reproductive cycle of the Lined

Snake (Tropidoclonion line alum) .

Herpetologica 41(l):39-44.

LIN, X., M. HUANG, Y. YANG, AND F. DONG.

(IN PRESS). [The elementary study on the

male reproductive cycle of Chinese Mamushi

(Agkistrodon blomhoffii brevicaudus)].

Journal of Zoology, (n Chinese).

MACARTNEY, J. M., AND P. T. GREGORY.

1988. Reproductive biology of female

rattlesnakes (Crotalus viridis) in British

Columbia. Copeia 1988(l):47-56.

SAINT GIRONS, H. 1966. Le cycle sexuel des

serpentes Renimeux. Memorie Institute

Butantan Symposium International 33:105-

114.

SAINT GIRONS, H. 1982. Reproductive cycle of

the male snakes and their relationships with

climates and female reproductive cycles.

Herpetologica 38(1):5-16.

SEIGEL, R. A., AND N. B. FORD. 1987.

Reproductive ecology. Pp. 210-243. In R.

A. Seigel, J. T. Collins and S. S. Novak

(eds.). Snake Ecology and Evolutionary

Biology, Chapter 8. Macmillan Publishing

Co., New York.

I February 1992~

Asiatic Herpetological Research

Vol. 4, pp. 68-75

Investigations on Ranid Larvae in Southern Sakhalin Island, Russia

HANS-JOACHIM HERRMANN1 AND KLAUS KABISCH2

^Museum of Natural History Castle Bertholdsburg, PF 44, 0 - 6056 Schleusingen, Germany

institute for Conservation of Nature and Environmental Protection, University of Leipzig, Augustusplatz 2,

0 - 7010 Leipzig, Germany

Abstract. -Using a special chemical technique, four breeding sites of two brown frog species, Rana

amurensis and Rana chensinensis, were investigated on Sakhalin Island, Russia. They were living together

with other amphibian species under very different conditions. A puddle with Rana chensinensis larvae was

found adjacent to the Pacific coast with a salinity of 1.2%. The description of the mouth part morphology

was completed by SCAN-investigations on the micromorphology of larval teeth, horny jaws and the warty

epithelium.

Key words: Amphibia, Anura, Ranidae, Rana amurensis, Rana chensinensis, tadpoles, breeding sites, water

chemistry, salinity, micromorphology, Russia, Sakhalin Island.

Introduction

In July and August of 1989 the authors

visited the southern part of the Russian

Far East island, Sakhalin. We found in

many places the only two ranid frog

species inhabiting the island, Rana

amurensis and Rana chensinensis. In

most habitats they coexisted with the

other amphibian species of Sakhalin

Island, Salamandrella keyserlingii, Bufo

gargarizans and Hyla japonica. The

latter was only found near Kostromskoe.

In other papers (Hermann and Kabisch,

1990, 1991; Kabisch et al., 1990) the

authors report on the herpetofauna of

Sakhalin Island. The present paper is

concerned with the life and environmental

conditions of ranid frog larvae. Some

micromorphological data for the species

diagnosis are presented.

Methods

Tadpoles of Rana amurensis and Rana

chensinensis were observed in many

breeding sites on the island. Some of

them were caught and fixed in 70%

ethanol. According to a technique of W.

Pietsch (Dresden) one liter samples of

water from four breeding sites were

obtained from: (1) brook in the city park

of Jushno-Sachalinsk (Fig. 1), (2) pools

near Pjatyretske with Lysichiton

camtschatcense as the main botanical

element, (3) pond near Kostromskoe with

Alisma orientate as the dominant water

plant, (4) puddle at the Pacific coast on

the Krilon Peninsula (Fig. 2). The water

samples were analyzed in the laboratory

of W. Pietsch. The fixed larvae (24

specimens of each species, representing

stages of the beginning of hind leg

formation) were also prepared for

investigation of their micromorphology

(for technique see Herrmann, 1989). The

preparations were investigated with a

scanning electron microscope TESLA B

300 in the Technical College of Ilmenau

(Thuringia).

Results

/ . Characterization of the Breeding Sites

The water analysis data of the four

investigated breeding sites are shown in

table 1. From this information it can be

concluded that the chemical nature of the

water bodies is very different. In the first

one, in a brook in the city park of

Jushno-Sachalinks, we found larvae of

Rana chensinensis in addition to those of

Bufo gargarizans. Rana chensinensis

prefers running water as breeding sites on

Sakhalin Island. The water can be

characterized as follows: slightly acidic,

oligotrophic, poor in humic material,

(C) 199? hv A vi/7/ir H prnptnlnoirnl Rpvp/irrh

February 1992

Asiatic Herpetological Research

Vol. 4, p. 69

FIG. 1 . Tadpoles of Rana chensinensis in a brook in the city park of Jushno-Sachalinsk.

nutrient poor, poor in electrolytes, rich in

iron, and of a low total hardness. The

only vegetation at the brook consisted of

some grasses and rushes.

The second water body was a breeding

pool of Rana amurensis. It is one of four

permanent pools near the Naitsa River in

the Pjatyretske River system. The four

pools (area about 550 m2) are slightly

acidic, very poor in humic material,

nutrient poor and of a low total hardness.

In the third breeding site all amphibian

species living on the island were found:

Salamandrella keyserlingii, Rana

amurensis, Rana chensinensis, Hyla

japonica and Bufo gargarizans. Typical

species of the very rich vegetation of this

small pond (area about 80 m2) were

Alisma orientate, Juncus bufonius,

Epilobium palustre, Oenanthe

decumbens, Phleum pratense, and

Equlsetum palustre. The water was

slightly acidic, oligomesohumic, rich in

phosphates and carbonates, but of a low

total hardness.

The fourth habitat was a very small

puddle (area 1.5 m2) at the Pacific coast.

Vol. 4, p. 70

Asiatic Herpetological Research

February 1992

i •

FIG. 2. Puddle with Rana chensinensis larvae adjacent to the Pacific coast on the Krilon Peninsula.

Splashing salt water contacted this puddle

during the time of high tide. It was a

breeding site of Rana chensinensis. The

vegetation consisted of Lemna and

Juncus only. We found many pieces of

old wood in the water. The water can be

characterized as follows: slightly

alkaline, poor in humic material, nutrient

poor, rich in electrolytes and of a medium

total hardness. A typical feature of this

breeding site is the NaCl content of

1.2%. Because of the high content of

salt, the puddle can be classified as a B-

mesohalobien water representing the

upper limit of brackish water. The 24

larvae represented an earlier stage of

development compared to tadpoles of the

same species living in other breeding

places at the same time.

2. Micromorphology Investigations

The schematic drawings of the larval

mouth of Rana amurensis and Rana

chensinensis show clear differences in

their morphology (Fig. 3). With the

SCAN, the small conical teeth on the

upper and on the lower horny jaw could

be visualized in both species. In the

literature (Bannikov et al., 1977) only

February 1992

Asiatic Herpetological Research

Vol. 4, p. 71

teeth on the lower jaw were shown for

Rana amurensis. We found 69-73 in the

upper jaw of Rana chensinensis and 51-

55 in Rana amurensis. On the lower jaw

52-54 were counted in Rana chensinensis

and 46-49 in Rana amurensis (Fig. 4-6).

The labial teeth were identical in all rows

in both species. Fan-like tips, 6-13 on

each tooth, could be seen (Fig. 7). The

warty epithelium around the mouth field

of the larvae consisted of a fleshy skin.

At the margin of this structure, labial teeth

have been found (Fig. 8). The epithelium

of the larvae was composed of hexaedric

or octaedric plate cells.

Discussion

Some papers on the effects of low pH

and other chemical variables on

amphibian larvae were published by

Freda (1986) and Freda and Dunson

(1985a, 1985b, 1986). A lot of data on

acid tolerance in amphibians are

summarized in the paper of Gebhardt et

al. (1987). The lowest pH tolerated by a

brown frog, as described for Rana

sylvatica, was 3.0. Other conditions

were observed by Freda and Dunson

(1984) in experiments with Rana

catesbeiana, Rana clamitans and Rana

pipiens in the laboratory. An increasing

of the external calcium concentration

extended the survival time in acid water

by slowing the loss of sodium. So it is

possible to survive in salt water under

special conditions. There was a

regulatory principle for the magnitude of

larvae populations in breeding sites with

such special conditions obtained by

Kovaltsyk (1981). The main factors

were acidity and the contents of cat ions

in the water. Another role was played by

the temperature of the water in connection

with the photo period (Dupre and

Petranka, 1985; Floyd, 1985).

The long days in spring and summer,

as typical of Sakhalin Island, enable the

amphibian larvae to develop under

extreme conditions. These are

characterized by extreme temperature

differences, reaching minimum and

FIG. 3. Schematic drawings of the larval

mouth parts of Rana amurensis (a) and Rana

chensinensis (b).

maximum values in very short intervals,

limiting the survival of larvae. The

opportunity to survive in salt water was

described for urodeles by Jones and

Hillman (1978), (Batrachoseps), and

Romspert and McClanahan (1981),

{Ambystoma tigrinum). In the papers of

Power (1937), Andren and Nilson

(1979), Herrmann (1982), Dunson

(1977), and Guix and Lopes (1989) some

anuran species are listed as breeding and

developing in brackish waters. Fljaks

(1985) recorded some brackish breeding

sites (1.5-9%) of Bufo gargarizans and

Rana amurensis on the island of

Sakhalin. Fljaks (1985, 1986) also

reported on the mortality of the tadpoles

of Rana amurensis and Rana

chensinensis on this island. He

observed the highest mortality in the first

stages of larval development: 18-73% in

Vol. 4, p. 72

Asiatic Herpetological Research

February 1992

FIG. 4. Mouth parts of the tadpole of Rana

chensinensis (x 120).

FIG. 7. Labial teeth of the tadpole of Rana

chensinensis (x 2500).

FIG. 5. Teeth of the upper jaw of the tadpole of

Rana chensinensis (x 1500).

FIG. 6. Teeth of the upper jaw of the tadpole of

Rana amurensis (x 300).

FIG. 8. Warty epithelium of the tadpole of

Rana amurensis (x 500).

Rana amurensis and 15-66% in Rana

chensinensis. In a puddle with 9%

salinity the Rana amurensis larvae had a

mortality rate of 99.8%. An increased

mortality was also found in acidic water.

The slow development of ranid tadpoles

in puddles at the ocean coast was also

observed by Kopein (1973) in southern

Sakhalin Island.

Micromorphological data on larvae of

Rana amurensis and Rana chensinensis

were found to be absent in the literature.

Besides the macromorphology, form and

topography of nostrils, spiracle, vent

tube, lateral-line pores and buccal papillae

according to Johnston and Altig (1986),

the jaw sheaths and labial teeth can also

February 1992

Asiatic Herpetological Research

Vol. 4, p. 73

TABLE 1 . Chemical/physical data of the breeding sites.

criterion

brook in Jushno-

Sachalinks (1)

pool near

PjatyTetske (2)

pond near puddle at the Pacific

Kostroms-koe (3) coast (4)

PH

6.8

6.6

6.9

7.2

pV (KMn04

mgr1)

total hard-

ness (°dH)

carbonate

hardness (°KH)

nitrate

(mgl1)

sulfate

(mgl"1)

ammonium

(mgl"1)

iron

(mgl"1)

calcium

(mgl"1)

nitrite

(mgl1)

chloride

(mgl"1)

magnesium

(mgl"1)

CO2

(mgl"1)

Si02

(mgl1)

phosphate

(mgl"1)

lime

(mgl"1)

O2

(mgl"1)

residue of evapora-

tion (mg l"1)

residue of combus-

tion (mg l'1)

33.8

2.3

2.1

3.2

0.9

0.12

1.52

11.4

0.01

7.6

3.1

24.0

14.1

0.1

38.3

9.6

94.0

50.0

22.9

1.6

48.0

4.0

28.2

18.4

0.08

8.4

0.01

9.5

1.8

18.0

3.2

0.2

32.0

10.4

94.0

49.0

0.56

21.2

0.03

34.8

4.3

33.0

27.4

1.8

87.2

12.2

230.0

104.0

0.02

26.2

0.02

76.5

7.8

22.0

28.0

0.2

11.6

11.2

864.0

376.0

Vol. 4, p. 74

Asiatic Herpetological Research

February 1992

be used for identification of anuran

tadpoles. Wassersug (1980) and Viertel

(1982) favored micromorphology for

taxonomic classification. The present

data support the necessity to add

micromorphological data for species

diagnosis in anuran larvae.

Acknowledgments

For their excellent scientific assistance

we have to thank Dr. K. Pfeifer,

Technical College of Ilmenau, and Dr. sc.

W. Pietsch, Dresden. Furthermore we

are very grateful to Doz. Dr. sc. K.

Brauer, Paul Flechsig Institute for Brain

Research, University of Leipzig, for

critical reading of the manuscript.

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stinkpaddans Bufo calamita utbredning och

ekologi pa den svenska vastkusten. Fauna

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BANNIKOV, A. G., I. S. DAREVESKY, V. G.

ISCHENKO, A. K. RUSTAMOV, A.ND N. N.

SCHERBAK. 1977. [Field guide of the

USSR amphibians and reptiles].

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DUNSON, W. A. 1977. Tolerance to high

termperature and salinity of tadpoles of the

Philippine frog, Rana cancrivora. Copeia

1977: 375-378.

DUPRE, R. K., AND J. W. PETRANKA. 1985.

Ontogeny of temperature selection in larval

amphibians. Copeia 1985:462-467.

FLJAKS, N. L. 1985. Vyzhivaemost amfibij na

rannych etapach rasvitija na ostrove Sachalin.

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FLJAKS, N. L. 1986. Vlijanie pH sredy na

vyzhivaemost i razvite beschvostngch amfibia

Sachalina. In Sistematika i ekologija amfibij

i reptilij. Leningrad.

FLOYD, R. B. 1985. Effects of photoperiod and

starvation on the temperature tolerance of

larvae of the giant toad, Bufo marinus.

Copeia 1985:625-631.

FREDA, J. 1986. The influence of acid pond

water on amphibians: a review. Water, Air

and Soil Pollution 30:439-450.

FREDA, J., AND W. A. DUNSON. 1984.

Sodium balance of amphibian larvae exposed

to low environmental pH. Physiological

Zoology 57:435-443.

FREDA, J., AND W. A. DUNSON. 1985. Field

and laboratory studies on ion balance and

growth rates of ranid tadpoles chronically

exposed to low pH. Copeia 1985:415-423.

FREDA, J., AND W. A. DUNSON. 1985. The

influence of external cation concentration on

the hatching of amphibian embryos in water

of low pH. Canadian Journal of Zoology

63:2649-2659.

FREDA, J., AND W. A. DUNSON. 1986. Effects

of low pH and other chemical variables on the

local distribution of amphibians. Copeia

1986:454-466.

GEBHARDT, H., K. KREIMES, AND M .

LINNENBACH. 1987. Untersuchungenzur

Beeintrachtigung der Ei- und Larvalstadien

von Amphibien in sauren Gew3ssern. Natur

und Landchaft 62:20-23.

GUIX, J. C, AND R. M. LOPES. 1989.

Occurence of Hyla geographica Spix and

Bufo crucifer Wied tadpoles in brackish water

environmemts in the Jureia Region (S3o

Paulo, SE Brasil). Amphibia-Reptilia

10:185-189.

HERRMANN, H. J. 1982. Amphibien,

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Exkursionsfuhrer durch die Umgebung von

GreifsNald (II). Wissenschaftliche Beitrage

der Emst-Moritz-Arndt-Universitat.

HERRMANN, H. J. 1989. Die

mikromorphologische Differenzierung di- und

tetraploider gTiiner Kroten des Bufo viridis-

Komplexes. VerOffent Naturhistorischen

Museums Schloss Bertholdshung

Schleusingen 4:15-21.

HERRMANN, H. J., AND K. KABISCH. 1990.

Die Herpetofauna der Insel Sachalin.

Herpetofauna 12:6-10.

HERRMANN, H. J., AND K. KABISCH. 1991.

Biological investigations oiBufo gargarizans

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Cantor 1842 in Southern Sakhalin. (In

press).

JOHNSTON, G. F., AND R. ALTIG. 1986.

Identification characteristics of anuran

tadpoles. Herpetological Review 17:36-37.

tsisllennosti populjazii. Voprosy

gerpetologii, Leningrad 5:66-67.

POWER, J. H. 1937. Tadpoles in the transition

zone between fresh and sea water. Cape

Naturalist 1:127-128.

JONES, R. M., AND S. S. HILLMAN. 1978.

Salinity adaptation in the salamander

Batrachoseps. Journal of Experimental

Biology 76:1-10.

ROMSPERT, A. P., AND L. L. MCCLANNAHAN.

1981. Osmoregulation of the terrestrial

salamander, Ambystoma tigrinum, in

hypersaline media. Copeia 1981:400-45.

KABISCH, K., H. J. HERMANN, AND G.

MATJUSHKOV. 1990. Beobachtungen an

Amphibien und Reptilien Sachalins.

Aquarien Terrarien 37:235-248.

KOPEIN, E. I. 1973. 0 razmnozhenii amfibij na

juge Sachalina. Voproby gerpetologii,

Leningrad 3:100-102.

KOVALTSYK

energitseskogo

mechanizmack

L. A. 1981. 0 roli

litsinok zemnovodnych v

podderzhanija optimalnoj

VIERTEL, B. 1982. The oral cavities of Central

European anuran larvae (Amphibia).

Morphology, ontogenesis and generic

diagnosis. Amphibia-Reptilia 4:327-360.

WASSERSUG, R. J. 1980. Internal oral features

of larvae from eight anuran families:

functional, systematic, evolutionary and

ecological considerations. Miscellaneous

Publications of the Museum of Natural

History of the University of Kansas 68: 1-146.

I February 1992~

Asiatic Herpetological Research

Vol. 4, pp. 76-98

Historical Biogeography of the Phrynocephalus Species of the USSR

NATALIA B.ANANJEVA1 AND BORIS S.TUNIYEV2

^Zoological Institute, Academy of Sciences, St. Petersburg, Russia

^Caucasian State Biosphere Reserve, Sochi, Russia

Abstract. -There are 22 species and subspecies of Phrynocephalus in the USSR. Some species inhabit

sandy deserts, while others occur in hard soil and gravel deserts. Speciation and present day distributions are

a result of geologic events such as mountain building causing the isolation of valleys and basins and

changes in the direction of river courses.

Key words: Reptilia, Sauria, Agamidae, Phrynocephalus, Armenia, Azerbaijan, Kazakhstan, Kirgizistan,

Russia, Tadjikistan, Turkmenistan, Uzbekistan, USSR, biogeography, distribution, evolution.

Introduction

The reconstruction of the genesis of

Phrynocephalus species can not be based

on the paleontological evidence since data

in this field are extremely poor. The only

fossil locality is from the Pliocene of

Turkey (Zerova and Chkhikvadze, 1984).

However, a comparison of recent

arealographic patterns of species studied

with known ideas about the historical

geography and paleogeography of the

region where the species occur may be used

as one method of research. The data about

climate and the genesis of landscapes and

vegetation are of great importance.

According to recent ideas, 22 species

and subspecies of the genus

Phrynocephalus live in the USSR

(Bannikov et al., 1977; Borkin and

Darevsky, 1987). We use here the last list

and do not try to reflect more recent and

often opposing ideas about Phrynocephalus

taxonomy (Golubev, 1989a, 1989b;

Mezhzherin and Golubev, 1989; Semenov,

1987; Semenov and Dunayev, 1989;

Semenov and Shenbrot, 1982, 1990;

Shenbrot and Semenov, 1987), and about

the status of some populations, subspecies,

and species. This paper does not consider

problematic nomenclature problems that

need special research. We try here to

understand the present complicated

distribution of Phrynocephalus in the

USSR. This includes their disjunct

populations. We also try to explain the

possible ways of the development and

formation of the distributions of different

forms independendy from the disagreement

on the opinion about their taxonomic status.

We discuss here the information about the

ranges of these lizards and although the

status of some of them may be problematic,

this does not so strongly influence our

speculations about historical biogeography.

Most Phrynocephalus species inhabit

Middle Asia and Kazakhstan territories.

Only a few species penetrate to the eastern

part of the northern Caucasus and eastern

Transcaucasia. Phrynocephalus versicolor

kulagini extends to the southern regions of

Tuva Autotomous Republic, Russia (Fig.

1).

Discussion

As is well known, it is impossible to

understand the history of the fauna without

knowing the history of the flora and

climatic and geological evolution. The

history of the flora in the Caspian region is

known from the Upper Cretaceous-

Paleogene (Korovin, 1961) when the

Tethys transgression flooded most of

Middle Asia and central Kazakhstan. In

this region a continental regime was

retained only in the Tien Shan area and in

the eastern part of the Kazakh hummock

topography (Gvozdezky and Mikhailov,

1987), (Fig. 1). At that time the Central

Asian land already had an arid regime

(Agakhanyanz, 1981). The middle of the

Gobi was probably real desert surrounded

by steppe landscapes (Serebrovsky, 1936).

February 1992

Asiatic Herpetological Research

Vol. 4, p. 77

FIG. 1 . Sea basin and land (hatched) in Middle Asia and Kazakhstan in Upper Eocene - beginning of the

Oligocene. 1- the Lower Cretaceous records of plants in Er-Olian-Duz Depression (Serebrovsky, 1936); 2-

Eocene - Oligocene records of reptiles and amphibians in Zaissan Depression (Bakradze and Chkhikvadze,

1988).

A warm tropical and subtropical climate,

humid, but from time to time with seasonal

aridity and probably with seasonal falls of

temperature, was dominant on the

continental parts of Middle Asia

(Gvozdezky and Mikhailov, 1987).

It may have promoted the growth of

such species as Taxodium distichum,

Populus balsamifera, Juglans acuminata,

Fagus antiposii, Liquidambar europaeum,

Diospiros sp., Gingko biloba, and

Liriodendron tulipifera. The analogous

flora was distributed throughout all of the

Siberian territory (Serebrovsky 1936).

Luxuriant thermophilous flora of Middle

Asia was accompanied by a highly rich and

diverse fauna of the Late Cretaceous such

as salamanders and frogs from the families

Scapherpetontidae, Batrachosauroidae,

Prosirenidae and Pelobaudae (Bakradze and

Chlihikvadze, 1988). Lizards of the

families Parasaniwidae, Teiidae, Anguidae,

Agamidae, Saniwidae, Gekkonidae, and

Varanidae were also present (Nesov,

1981a, 1981b).

From data about the Cretaceous flora in

southern Middle Asia, we hypothesize the

presence of a more dry and hot climate

Vol. 4, p. 78

Asiatic Herpetological Research

February 1992

(Korovin, 1961).

The Lower Tertiary findings in the Er-

Oilan-Duz Depression in Badkhyz contains

Dryrandra schrenkii, Celastrophyllum

turcmenicus and other typical xerophilous

plants which also indicates adaptation of

these plants to the survival during the hot

and dry periods during the vegetation

period (Serebrovsky, 1936), (Fig. 1).

From the Eocene fossils of the family

Agamidae were found in some localities in

Kazakhstan including the Zaissan Basin

(Bakradze and Chkhicvadze, 1988).

In the Oligocene the sea retreated and the

formation of a continental landscape began.

However, the development of relief took

place in different ways. In the Kara-Kum

and Kyzil-Kum deserts and the Ustyurt

Plateau, anticlinal and synclinal structures

were formed in the Neogene. In spite of

their platformal type of structure, they are

sufficiently sharp with an angle of

declination of more than 10°. The Turgai

Plateau and western Betpak-Dala were

slightly touched by the most recent

orogenetic movements on these small

territories. This not only resulted in the

formation of different geomorphological

structures which will be discussed below,

but also in the difference of the amplitude

of the raising and sinking of whole

territorial divisions. These differences in

the amplitude of movements have resulted

in the isolation and formation of the specific

relief in each of the plains in Middle Asia

(Voskresensky, 1968).

In the middle Oligocene there was a

sharp change in the composition of the

herpetofauna of the Zaisan Depression.

The early Oligocene giant salamanders

(Zaissanurus), giant snakes (Boidae),

Glyptosaurinae, etc. were replaced by

amphibians of the families Pelobabidae,

Ranidae, and Bufonidae and by boids of

the genus Bransateryx (Bakradze and

Chkhikvadze, 1988).

The formation of two centers of

speciation of the genus Phrynocephalus

probably began on the boundary of the

Paleogene-Neogene time in arid regions of

Central Asia and in the southern part of

Middle Asia (Fig. 2). Until middle or late

Pliocene the herpetofauna of Central Asia

and Turan represented, more or less, a

single unit (Chkhikvadze et al., 1983). The

independent formation of Central Asian and

Middle Asian centers of different fauna

began readily after their separation by

mountain structures of Alpic orogenesis

(Ananjeva, 1986; Chernov, 1959; Geptner,

1938; Peters, 1984).

In discussing the center of origin of the

genus Phrynocephalus, Moody's (1980)

opinion should be noted. He suggested

that the most primitive Phrynocephalus

species is P. vlangalii inhabiting north-

eastern Tibet and Qinghai. The validity of

this conclusion is problematic because he

studied only two species of this genus in

his phylogenetic and biogeographic study

of agamids.

Of special interest for understanding the

origin of Phrynocephalus is the finding of a

new species, Phrynocephalus

langwalaensis (Sharma, 1970), from the

Radjastan Desert, in western India.

Whiteman (1978) suggested that

Phrynocephalus probably originated in the

early Miocene in Central Asia. On

Whiteman's map (Whiteman, 1978: his

figure 12) illustrating the hypothesized

dispersal of Phrynocephalus, he showed

this point in southern Middle Asia. The

reason of such term confusion is connected

with the absence of separating, in English,

the terms Central Asia and Middle Asia

traditionally used in German and Russian

geographical and zoological literature.

Middle Asia is the part of Asian territory

of the USSR from the Caspian Sea in the

west to the Chinese border in the east, and

also from the Aral-Irtysh drainage divide in

the north to the border of Iran and

Afghanistan in the south.

Central Asia is defined as the desert and

semidesert plains, tableland and high

plateaus which are limited to the east by the

southern part of Great Khingan and

February 1992

Asiatic Herpetological Research

Vol. 4, p. 79

FIG. 2. Sea basin and land (hatched) during the Lower - middle Miocene. Hypothesized centers of

Phrynocephalus speciation: A- Middle Asian center; B- western edge of the Central Asian center. Lower -

middle Miocene records (Bakradze and Chkhikvadze, 1988): 1- northern Aral Sea region; 2- Turgai; 3-

Zaissan Depression. The arrow shows the hypothesized direction of movement of ancestral forms of the

Phrynocephalus guttatus complex.

Taikhanshan ridge and to the south by the

longitudinal tectonic basin of the upper

Indus River and Brahmaputra (Tsangpa).

In the west and in the north the border of

Central Asia corresponds to the mountain

ridges of eastern Kazakhstan, Altai,

western and eastern Sayan, approximately

coinciding with the state border between the

USSR on the one hand, and China and

Mongolia on the other hand.

Eremias sp., Varanus, Ophisaurus,

Eryx, and Protestudo were found in the late

Miocene deposites in eastern Kazakhstan

(Bakradze and Chkhikvadze, 1988). The

ancestor of Phrynocephalus maculatus may

have already existed during the Neogene in

Middle Asia in the condition of southern

savannas and xerophytous vegetation of the

southern and southeastern Transcaspian

region. The ancestral form of P. raddei

(Fig. 3) may have already been distributed

along all the southern part of the Thetys

geosyncline from the Caspian Sea to the

Pamir. We can hypothesize this because

fossil remains of giant land tortoises and

monitors are known from the Pliocene in

Tadjikistan. Some lizards, Trapelus

Vol. 4, p. 80

Asiatic Herpetological Research

February 1992

FIG. 3. Sea basin and land during the Upper Miocene (Sarmat Sea is hatched). 1- Hypothesized

distribution of Phrynocephalus maculatus ancestor; 2- Hypothesized distribution of Phrynocephalus raddei

ancestor. The arrow shows the direction of continuing dispersal of the forms of the Phrynocephalus

guttatus complex.

sanguinolentus, Eremias sp., and Varanus

cf. griseus are known from the Pliocene in

Turkmenia (Ananjeva and Gorelov, 1981;

Bakradze and Chkhikvadze, 1988)

In the Pliocene, the genus

Phrynocephalus could have divided into

species complexes or into the genera

Phrynocepnalus and Megalochilus

(Ananjeva, 1986) on the territory of the

southern Kara-Kum Desert. Federovitch

(1946) assumes that one should look for

the origin of typical recent sandy desert

vegetation associations in the Neogene in

the Kara-Kum (Fig. 4).

The Miocene may be considered as the

time when the ancestral form of the

Phrynocehalus guttatus complex (Figs. 5

and 6) from the Central Asian center

penetrated as far as the eastern boundaries

of the Tethys (recent regions of Pamir- Alai

and Gissar-Darvaz mountains), (Fig. 2).

This territory, now occupied by mountains

and intermountain depressions, resembled

low mountain relief now present northwest

of Samarkand and Djizak (Voskresensky,

1968). The subsequent dispersion of this

group to the west was along the northern

shore of the Thetys (later the Sarmat Sea,

Fig. 3). Further spreading to the north was

February 1992

Asiatic Herpetological Research

Vol. 4, p. 81

FIG. 4. The middle Pliocene changes of Phrynocephalus. 1- Lower Pliocene distribution of

Phrynocephalus reticulatus; V- middle Pliocene populations of Phrynocephalus reticularis on emerged

land; 2- Lower Pliocene distribution of Phrynocephalus maculatus; 2'- middle Pliocene populations

separated by alpic orogenesis of the Kopeth-Dag. The arrows show the direction of dispersal of the species

of the Phrynocephalus guttatus complex. A- hypothesized place for divergence of Phrynocephalus and

Megalochilus; B- hypothesized place of origin for Phrynocephalus rossikowi.

prevented by phytogeographical conditions

since the plains of central Kazakhstan were

covered by deciduous forests of Populus

sp., Salix sp., Alnus sp., Zelkowa sp.,

Ulmus sp., Acer sp., i.e. the vegetation

was intermediate between the Turgai and

recent types. The xerophilous formations

were only beginning to develope in this

territory (Gvozdezky and Mikhailov,

1987).

During the first half of the Neogene, a

lake regime was predominate on the

elevated plains of Middle Asia such as the

Turgai tableland and western Betpak-Dala.

The southwestern branch of the P. guttatus

complex dispersion could have penetrated

this area. The process of uplifting took

place across the entire plains of Middle Asia

towards the end of Sarmatian time and to

the beginning of the Pliocene. The sea

basins disappeared and erosional division

of the region took place (Voskresensky,

1968). During this period, Phrynocephalus

reticulatus could have dispersed widely

over the entire plain area from the Caspian

Vol. 4, p. 82

Asiatic Herpetological Research

February 1992

FIG. 5. Phrynocephalus guttatus from the west side of the Caspian Sea in Chechen-Ingush, Russia.

Sea in the west to the Fergan Depression in

the east. This species apparently did not

reach beyond the limits of the dry subtropic

climatic belt. The same is observed at the

present (Fig. 4). In such context, the

opinion of Golubev (1989b) on the unity of

the origin of P. moltschanovi and P.

reticulatus from the forms penetrating here

from the north in the middle Pleistocene

seems to us doubtful.

The eastern branch of the P. guttatus

complex, i. e. Phrynocephalus versicolor

was widespread north and northeast of the

Tien Shan (Mountains), (Fig. 4). Isolation

of Phrynocephalus rossikowi (Fig. 4)

could have taken place on the dense river

sediments of the Amu Darya (River) which

flowed into the Caspian Sea at that time.

The Pliocene raising of Asia Minor and the

Iranian Plateau had apparently already led

to disjunction of the area inhabited by the

ancestor of Phrynocephalus helioscopus

and also by some species of the genus

Trapelus with similar ecological

requirements. The diverged populations of

P. helioscopus, P. helioscopus persicus (P.

persicus, Meszszerin and Golubev, 1989;

Nikolsky, 1915), could probably have

separated in the Pliocene. In the middle of

the Pliocene a sinking process occured in

the sand deserts of Middle Asia to the

slightly elevated Zaunguz Plateau.

However, on the Turgai Plateau in western

Betpak-Dala and on the Ustyrt Plateau the

raising of the Kysil-Kum and Mangyshlak

was no longer restored by the regime of

accumulation . The relief continued to

develope slowly by an erosion and

denudation process (Voskresensky, 1968).

It was in the middle of the Pliocene that the

disjunction of the continuous range of

Phrynocephalus reticulatus took place.

That led to isolation of three relict

February 1992

Asiatic Herpetological Research

Vol. 4, p. 83

**$,.

*

FIG. 6. Habitat of Phrynocephalus guttatus on the west side of the Caspian Sea in Chechen-Ingush,

Russia.

populations on the plateau islands not

covered by sea: South Ustyurt

Krasnovodsk, Kiysil-Kum and Fergana

Depression (Fig. 4).

The formation of the Phrynocephlalus

mystaceus complex (or genus

Megalochilus), (Figs. 7 and 8), and of the

parallel sand inhabiting P. interscapularis

complex, continued in the extreme southern

portion of Middle Asia under conditions of

sandy desert formation. The adaptive

radiation of Phrynocephalus in sympatry,

according to Peters (1984), could have

been accompanied by increasing differences

in the body size. This seems to have been

important in the evolution of P. mystaceus.

On quick moving sand dunes with steep

slopes, the largest specimens could

survive. They were able to dig

uncrumbling deep holes protecting them

from summer heat and low winter

temperatures. They were also able to

release themselves from the captivity of the

sand during movement of sand dunes. It

should be noted that ridges formed from the

stabilized aeolian landforms in the

Pleistocene when mountain structures,

which mainly determine the direction of the

air streams, were formed. It is assumed

that the direction of sand movement

remained the same at least to the Upper

Neogene (Voskresensky, 1968). The

plains with newly formed meso- and

microrelief created before the Quarternary

drying and cooling by wind activity were

alluvial plains with all the typical features

(Voskresensky, 1968).

P. mystaceus evolved under the

conditions of blowing sand. The

decreasing of body size of P. mystaceus

mystaceus in comparison with P.

mystaceus galli may be indirect evidence in

favour of this hypothesis. There may be

correlations between this change of body

Vol. 4, p. 84

Asiatic Herpetological Research

February 1992

FIG. 7. Phrynocephalus mystaceus from Repetek (38° 34' N 63° 11' E), Turkmenistan.

size and the inhabiting of P. mystaceus

mystaceus in the comparatively stabilized

Terek-Kuma rivers sands on the west side

of the Caspian Sea in Russia. Smaller sizes

of specimens of P. mystaceus are typical of

the populations from the Sari-Kum Sand

Dune, Dagestan, Russia. This form

developed under the conditions of a unique

isolated sand dune with a special wind

regime (Khonyakina, 1962).

The restricted distribution of P .

February 1992

Asiatic Herpetological Research

Vol. 4, p. 85

FIG. 8. Habiat of Phrynocephalus mystaceus (large sand dunes), Phrynocephalus interscapularis (sand

dune edges), Phrynocephalus raddei (hard packed soil to the left) from the Kara Kum Desert 80 km north of

Ashkabad (37° 57' N 58° 23' E), Turkmenistan.

mystaceus and relatively poor food

availability of the sand dunes could have

driven the small P. interscapularis back to

the dune valleys. This species, sharing a

common southern origin with P .

mystaceus, could not spread beyond the

limit of the subtropical climatic belt during

the next geological epoch. Its present

distribution almost completely lies in the

climatic zone of the continental southern

Turanian region with a small penetration to

the extreme southern part of the continental

north Turanian region (after Alisov, 1969).

These species occur were the temperature

during January -3°C in the north, up to 2°C

in the south and annual precipitation from

100 to 200 mm. According to Kashkarov

and Korovin (1936) P. interscapularis

inhabits Mediterranian deserts with a

winter-spring period of precipitation and

vegetation of the ephemeral type (Table 1).

The relatively restricted range of P .

interscapularis may be explained by some

ecological peculiarities. This lizard is very

small. It is not capable of digging deep into

the sand, and it also has a greater tolerance

to high temperatures. The temperature

preference of P. interscapularis may

fluctuate only 3°C, whereas in P .

mystaceus it may fluctuate 4°C and in

Eremias grammica up to 5°C (Cherlin and

Muzicnenko, 1983).

The mode of preference of temperatures

in P. mystaceus and Eremias grammica is

39°C which may be comparable with the

very high level of tolerance known for

Dipsosaurus dorsalis. However, for P.

interscapularis this index is still higher

(41.3°C). This may be considered an

outstanding example of adaptation of a

small lizard to extremely arid conditions.

In the north and northwestern deserts, P.

Vol. 4, p. 86

Asiatic Herpetological Research

February 1992

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mystaceus occurs on steep slopes of sand

dunes were as the sympatric P. guttatus

occurs in the valleys between sand dunes.

Large mountain ranges were formed in

the place of residial plains and low

mountain relief with a Paleozoic folded

structure. The peneplain was subjected to

folded deformations (Gvozdesky and

Mikhailov, 1987). In this context it is

difficult to share Golubev's (1989b)

opinion that the conditions of the early

Pleistocene were favorable for the

penetration of Phrynocephalus from Central

Asia to eastern Kazakhstan. However,

Golubev (1989b) noted that owing to active

alpic orogenetic processes in the Junggar

Alatau and the Tian Shan, the contact of the

reptiles between the Balkhash-Alakol and

the Junggar Depression became gradually

more difficult or was interrupted. This

period was probably characterized by

disjunction of continuous ranges and by the

isolation in the intermountain depressions

of the central branch of the P. guttatus

complex. Further history of the speciation

of each population seems to have resulted

in the formation, during the Pleistocene, of

more clearly isolated taxonomical forms in

different depressions: Hi- (P. alpherakii

according to Peters, 1984; Golubev,

1989b, or P. versicolor paraskivi according

to Semenov, 1987); Alakol Depression- (P.

versicolor ssp.), and Zaissan Depression-

(P. salenskyi according to Peters, 1984;

Golubev, 1989b, or P. melanurus

according to Semenov, 1987). Definitive

formation of eastern populations of the P.

reticulatus complex, which subsequently

led to the isolation of P. strauchi, may have

taken place at the same time. Its speciation

occured because of the isolation of the

Fergana Valley. Retaining of isolated

populations in intermountain depressions

was possible due to the absence of repeated

leveling of the relief in Neotectonic time.

This is supported by geological evidence

such as the composition and thickness of

sediments in the Hi and Fergana

depressions (Voskresensky, 1968).

Most of the distribution of P. mystaceus

seems to have been formed during the end

of the Neogene when these lizards could

have occupied all of Middle Asia, from the

Caspian Sea in the west to Balkhash Lake

in the east, and from the plains near the

slopes of Kopeth-Dagh and Hindu Kush in

the south up to the Naryn Sands in the

north. Its primary Aralo-Caspian

(Turanian) origin and distribution is

supported by all zoogeographers

(Anderson, 1968; Chernov, 1954;

Rustamov and Sczcerbak, 1985;

Vereshagin, 1966). The penetration to the

deserts north of the Caucasus Mountains

probably took place around the northern

Caspian Sea (Chernov, 1954; Darevsky,

1957).

In the Pleistocene, the Central Asian

elements of the flora dispersed from the

east to the north of Middle Asia and central

Kazakhstan. The other important center

which influenced the development of

Middle Asian vegetation was the eastern

Mediterranian center (Gvosdezky and

Mikhailov, 1987). All the plains of this

extensive region are classified by vegetation

type into two kinds of deserts:

Mediterranian (after Kashkarov and

Korovin, 1936), and subtropical deserts of

the northern zone (after Gvosdezky and

Mikhailov, 1987), or accordingly, the

deserts of the northern zone (after

Gvosdezky and Mikhailov, 1987). The

present boundary between the two zones

approximately corresponds to the boundary

distinguished by Alisov (1969) for the

climatic regions of continental northern

Turanian and continental southern

Turanian.

In the Pleistocene, speciation of the P.

guttatus complex occured in the northern

deserts of the Caspian and Aral Regions.

During the Upper Pleistocene, river beds of

the Amu-Darya and Syr-Darya rivers turned

to the Aral Sea (Voskresensky, 1968).

This resulted in a change from sand

massive on the southern coast of the Aral

Sea to loess and clay plains of river origin.

Under these conditions of hard soils, the

formation of the isolated southwestern

population of the P. guttatus group,

considered now as a separate species, P.

moltschanowi (Semenov and Shenbrot,

1982) took place (Fig. 9). The taxonomic

Vol. 4, p. 90

Asiatic Herpetological Research

February 1992

FIG. 9. Upper Pliocene changes of Phrynocephalus. A- middle Pliocene distribution of the species of the

Phrynocephalus guttatus complex. The disjunction of the continuous distribution of this complex occured

in the Upper Pliocene by: B- Junggar Alatau (Altai mountains); C- Saur and Tarbagatai mountain ridges.

1- Phrynocephalus melanurus; 2- Phrynocephalus versicolor ssp.; 3- Phrynocephalus versicolor paraskivi;

4- the place of speciation of the southwestern branch of the Phrynocephalus guttatus complex and

Phrynocephalus moltschanovi.

status of this species was discussed

recendy by Golubev (1989b).

It should be noted that the flow of

Middle Asian rivers to the Caspian Sea

changed to the Aral Sea, as a result of the

downwarp of the region (Voskresensky,

1968). This was of crucial importance for

the reconstruction of the ranges of most

sclerobiont Phrynocephalus species.

Probably before the Amu-Darya River

(Uzboi), changed its course P. raddei was

distributed on the clay and loess ares from

the Caspian Sea to Kukhistan. Its range

decreased considerably from the north and

from the south owing to orogenesis (Fig.

9). In the south this species remained on

the incline plain of the Kopeth Dagh and in

the loess regions in the estuaries of the

Murgab and Tedjen rivers.

After the Amu Darya changed its flow to

the Aral Sea, which coincided in time with

the maximal development of the sand

deserts, the area inhabited by P. raddei was

divided into a number of isolated

populations. These include the piedmont

plains in Kukhistan and the Kopeth Dagh,

February 1992

Asiatic Herpetological Research

Vol. 4, p. 91

FIG. 10. Pleistocene changes of Phrynocephalus. 1 to 1 '- the river course of the Amu Darya River (Kelif

Uzboi and Uzboi) flowing in to the Caspian Sea before the Lower Pliocene. The distribution of

Phrynocephalus raddei before the change of the Amu Darya River course to the Aral Sea is hatched. The

relictual populations (Upper Pliocene to present) after the change of the Amu Darya River course to the

Aral Sea are depicted by cross hatching. A- present distribution of Phrynocephalus guttatus kushakewichi;

B- the transformed distribution of Phrynocephalus rossikowi during the Upper Pleistocene from pre-

Pleistocene center of speciation (B').

remaining loess and other valley originated

forms of the mouth of the Murgab and

Tedjen rivers, and the dry bed of the

Uzboi. P. raddei boettgeri was formed in

the eastern isolated part and it is possible

that the western populations also present

combinations of different forms (now the

nominative subspecies P. raddei raddei,

(Fig. 10).

The genesis of the area inhabited by P.

rossikowi (Figs. 11 and 12) is also

correlated with the change of course of the

Amu Darya River. This area decreased in

the south and reached the southern coast of

the Aral Sea in the north (Fig. 10). Owing

to the constant change of the configuration

of the Amu Darya estuary also observed

now (Voskresensky, 1968). The northern

part of the range of P. rossikowi was also

changing repeatedly, resulting in the

isolation and long existence of this isolated

western population. It was described

recently as a distinct subspecies, P.

Vol. 4, p. 92

Asiatic Herpetological Research

February 1992

FIG. 1 1 . Phrynocephalus rossikowi (size x 2) from along the Amu Darya River, 30 km WNW of Deynau

(39° 15' N 63° 1 1' E), Turkmenistan.

rossikowi shammakovi. It is also possible

that the extreme northeastern population has

been isolated from the main distribution for

a long time and represents a distinct

taxonomical form.

After the formation of sand ridges and

the deeping of the dune valleys slowed, the

process of washing away the subtle

material from the ridges to the valleys with

the formation of the "takyr" landscapes

began in the Pleistocene (Voskresensky,

1968). Under such new conditions P.

helioscopus became widerspread in the

plains of Middle Asia.

The Pleistocene glaciation in Europe

resulted in the sharp displacement of

vegetation zones in the southern Russian

plains and vegetation belts in the Caucasus

Mountains. As a result, the distribution of

P. mystaceus in the deserts north of the

Caucasus Mountains was separated into a

number of isolated parts. Its range

increased in the piedmont regions north of

the Caucasus Mountains to the westward,

probably in the postglacial xerothermic time

of the Holocene. At this time P. mystaceus

reached the present border of Dagestan and

Stavropolsky Territory along the Terek-

Kuma rivers sands.

During the Pleistocene, P. mystaceus

and P. interscapularis dispersed into

mountainous Kukhistan along the sands

formed from the alluvial of the Amu Darya

(River). Phrynocephalus sogdianus

evolved as a result of the disjunction of the

Kukhistan enclave during the Upper

Quaternary from the continuous range of P.

interscapularis. This species was described

by Chernov (1959) as a subspecies, P.

interscapularis sogdianus. This form was

given the status of a distinct species after

February 1992

Asiatic Herpetological Research

Vol. 4, p. 93

FIG. 12. Habitat of Phrynocephalus rossikowi (size x 2) from along the Amu Darya River, 30 km WNW

of Deynau (39° 15' N 63° 1 1' E), Turkmenistan.

Sokolowsky (1975) discovered

considerable karyotypical differences

between P. sogdianus and P .

inter scapularis. With the alternations of the

Quarternary glacial and interglacial

epoches, the pluvial and xero-thermic

climatic periods were connected.

However, during the whole Quaternary

period, the climate was sharply continental.

The desert or desert steppe (in pluvial

epoches) regime was retained on the plains

of Middle Asia (Gvozdezky and Mikhailov,

1987).

During the Quaternary, the last

accumulation changing of the relief on the

plains in Middle Asia took place. This may

explain the present configuration of the

ranges of desert animals. The last

considerable accumulation (Khvalynskaya)

included the Caspian and low land Kara

Kum Desert, Muyn Kum and Sary Ishik

Otrau. Toad headed agamids completely

disappeared in the middle Quaternary

period from the Muyun Kum Desert. After

which only P. mystaceus could inhabit it.

The Khvalynskaya transgression of the

Caspian Sea defined the western part of the

range of P. raddei. The flooding of the

Sary Ishik Otrau sands near the southern

coast of Balkhash Lake resulted in the

almost total disappearence of P. guttatus

and P. mystaceus in this region. They are

retained probably only near the foot of

isolated island mountains that have risen

recendy among the sands in the eastern part

of Sary Ishik Otrau (Fig. 10).

Subsequently, dispersal from these refugia

and isolated areas could have led to the

formation of P. guttatus kuschakevitschi in

the Balkhash sands.

Thus, the history of the formation of

Phrynocephalus distributions, which is the

sclerobionts (hard soils) depressions and

Vol. 4, p. 94

Asiatic Herpetological Research

February 1992

the blooms of psammobionts, is correlated

with step wise development of the sand

deserts of the Middle Asian plains. It was

influenced by geological processes. All

this wide belt is correlated with the zone of

most recent downwarp along the peripheral

part of the mountain massives of Middle

Asia with the accumulation in them This

was followed by transformation of river

and estuary sediments under arid

conditions.

In some Phrynocephalus groups, species

secondarly inhabiting sands are known,

(Semenov, 1987). For example this pattern

is observed in the P. guttatus complex,

apart from typical sclerobiont forms.

Chernov (1948, 1959) noted that P.

guttatus inhabits different types of sandy

biotopes from P. mystaceus and P .

inter scpularis.

In connection with the problems

discussed, it is necessary to mention the

problem of Phrynocephalus origin. As was

already stated above, paleontological data

are available for Phrynocephalus only from

the Pliocene of Turkey. This is not enough

significant data about fossil

Phrynocephalus. The data of present

distribution and life history allow us to

speculate about the primary character of

habitats typical of these lizards. Golubev

(1989b) wrote, correctly in our opinion,

about the development of the most primitive

Phrynocephalus in gravel and sand-stone

(Gobi) deserts. Most herpetologists

(Chernov, 1948; Semenov, 1987; Whitman,

1978) suggest that the primary character is

sand biotypes. Thus, Chernov (1948)

assumed that Phrynocephalus originally

adapted to sand habitats and then moved to

hard soils. The same opinion is shared by

Whiteman (1978) and Semenov (1987). It

is interesting that all these herpetologists

use as the most serious argument, the

number of morphological adaptations

shared by all species of Phrynocephalus

and are typical of many other lizards

adapted to life in deserts. Whiteman

(1978), refering to Stebbins (1944), names

the following morphological characters: 1)

dorsoventral depressed body form; 2)

protruding labial border; 3) nostrils closed

by special valves; 4) special "scaled"

eyelids close the eyes; 5) tympanum absent

or hidden under the skin; 6) granular

smooth scales; 7) comparatively high speed

of locomotion, sometimes bipedal; 8)

increased finger surface, "sand ski"; 9) the

capacity to bury into the sand; 10) short

recurveable tail.

However a more detailed study of these

characters refutes the simplified

determination of their correlation with a

habitat in the sand. It is doubtful that the

dorsoventral depression of the body may be

an indicator of inhabiting sand biotopes.

This character is in the basis of the

identification key in the Agamidae family

(Boulenger, 1885), separating more

specialized tree agamids from all terrestrial,

rock and desert forms. It is well known

that such form of the body of mountain

agamids of the genus Stellio is not an

indicator of their origin in sand deserts.

Such characters as closed upper lip

covering the mouth, nostrils closed by

special valves, and special "horny scaled"

eyelids closing the eyes undoubtedly may

be considered as defensive structures.

However they can be developed in different

kinds of deserts (not only sand deserts)

with a typical windy regime.

Considering the ideas about the origin

oiPhrynocephalus and the so called

"primary substratum" one may assume that

the terms "desert" in general and sand

desert are sometimes confused. Thus,

Chernov (1948, p. 132) was absolutely

right that Phrynocephalus "originated and

developed in the conditions of rather sparse

vegetation." This, however, does not

permit these complexes of landscapes and

sand desert to be considered as equal. The

latter is only one type of desert and it is the

youngest from a geological aspect.

The character, tympanum absent or

hidden under the skin, is of special

importance. Analysis of the distribution of

this character and trends to the reduction of

the middle ear among all the agamids,

shows that it has arisen independently in

some evolutionary lines. The loss of the

February 1992

Asiatic Herpetological Research

Vol. 4, p. 95

tympanum and tympanum cavity is typical

of the Australian genus Tympanocryptis.

Such reduction may arise even in primitive

forms like Ceratophora, Cophotis and

Lyriocephalus. These convergent trends

are noted in Otocryptis, Phoxophrys,

Phrynocephalus, and Ptyctolaemus

(Moody, 1980). The enumeration of these

genera shows that side by side with the

desert lizards (but not psammophilous)

there are even forest species. Thus

Otocryptis is a terrestrial lizard which

prefers to inhabit the vicinity of rivers

shaded by vegetation in India and Sri

Lanka. With this consideration, further

examination of the new form,

Phrynocephalus laungwalaensis from the

Radjastan Desert of India may be

important.

The granular smooth scales also may be

observed not only in psammophilous

agamids but also in Leiolepis, Uromastyx,

and Physignathus (Moody, 1980).

Besides, an examination of the correlation

of Phrynocephalus morphological

characters and the type of substrate

(Galayeva, 1974) shows that

psammophilous species have granular

smooth scales. Where as lizards inhabiting

hard soil (rock debris desert or arid desert

with clay soil) usually have somewhat

enlarged, imbricate scales and small

protuberances. These data show that there

are gradations of morphological characters

among Phrynocephalus from sclerobionts

to psammobionts, and not indisputable

psammophilous morphological adaptations

of the whole genus. The possible

functional importance of small granular

scales in the capillary collection and

transport of the water in many desert lizards

should be noted (Schwenk and Greene,

1987).

The comparatively high speed of

locomotion, sometimes bipedal although

the limbs may be weak, are typical of many

agamids inhabiting open areas (Sukhanov,

1968; Cogger, 1975) and can not be

restricted to psammophilous species only.

The increased toe fringes are widely

discussed but there are no good

explanations of their function (Chernov,

1948; Fausek, 1906, 1959; Luke, 1986;

Werner, 1987). These structures are really

typical of many sand lizards, but simple

character environment correlation may be

misleading (Luke, 1986; Smith, 1935).

Toe fringes have arisen independently at

least 26 times in seven families of lizards

(Luke, 1986) and can be used for

locomotion on shifting sand, across water,

and for digging in some kinds of soil such

as sand and loess (Chernov, 1948; 1959;

Luke, 1986).

The original capability of burying into

the sand with horizontal movements of the

whole body is very well expressed in

psammophilous P. mystaceus and P.

inter scapular is. There exists an opinion

that such behavior may evolve only on

large areas of moving sand (Fausek, 1906).

But one should not excluded the

development of such interesting defensive

behavior on the loose sand from the

elements of cryptic and or sit and wait

behavior with similar patterns observed in

P. helioscopus on hard soil. This species

presses the depressed widening body to the

ground with several horizontal movements

before standing still.

In general, the idea of Geptner (1933)

seems to be fruitful for such

considerations. He thought that the animal

world of the sand deserts and that of the

deserts with hard soils are two formations

different in many aspects with their own, to

a considerable extent independent, ways of

development. The purpose of the

adaptations in the two kinds of landscapes

is considerably different.

To summarize the review of the recent

chorology of Phrynocephalus in the USSR

fauna, it should be noted that the

differences in the outlines of the

distributions in general correspond to two

main centers of origin. The species of

Central Asian origin have the northern most

distribution, inhabiting totally a moderate

climatic zone and the species of Milddle

Asian origin mainly did not go beyond the

limits of the subtropical climatic zone. The

relatively young species (Phrynocephalus

Vol. 4, p. %

Asiatic Herpetological Research

February 1992

helioscopus, and P. mystaceus) have the

widest distribution. A large portion of their

distributions were formed in the Pleistocene

in immediate connection with the

development of the sand deserts and

accompanied takyrs.

We can distinguish several types of the

present ranges of Phrynocephalus:

1. Miocene-Pleistocene range of a

northern Thetys origin (P. guttatus

guttatus).

2. Miocene-Pleistocene disjunct range of

a southern Thethys origin (P. raddei raddei,

and P. raddei boettgeri ).

3. Pliocene relict range: a) connected

with marine transgressions (P. reticularis

reticulatus, and P. reticulatus bannikowi);

b) connected with alpine orogenesis (P.

maculatus, P. melanurus, P .versicolor

parasskiwii, P. versicolor ssp., P.

helioscopus persicus, and P. strauchi).

4. The Pliocene-Pleistocene ranges: a)

wide (P. helioscopus heliscopus, and P.

mystaceus); b) subtropical (P .

inter scapularis, and P. sogdianus).

5. Pleistocene transformed area (P.

moltschanowi, P. rossikowi rossikowi, P.

rossikowi shammakowi, and P. guttatus

kuschakewichi ).

Since the process of continuing

aridization of Middle Asia is undoubted, it

may be predicted that a reduction in the

ranges of the stenotopic sclerobiont

Phryocephalus is occurring.

Literature Cited

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the USSR]. Mysl Publishing, Moscow.

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Proceedings of the Zoololical Institute, USSR

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I February 1992

Asiatic Herpetological Research

Vol.4, pp. 99-112|

On the Ecology of Przewalsky's Gecko (Teratoscincus przewalskii) in the

Transaltai Gobi, Mongolia

DIMITRI V. SEMENOV1 AND LEO J. BORKIN2

xSevertzov Institute of Evolutionary Animal Morphology and Ecology, Russian Academy of Sciences,

Moscow 117071, Russia

department ofHerpetology, Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034,

Russia

Abstract. -Przewalsky's Gecko {Teratoscincus przewalskii) is one of the least studied representatives of

the herpetofauna of Central Asia. We present the results of a study of the habitat, demography, spatial

distribution, activity, and diet of this lizard. Our observations indicate that individuals of T. przewalskii are

active foragers that feed primarily on beetles, and are strictly nocturnal. Individuals of this species do not

protect territories, but do exhibit aggressive behavior. We present a detailed analysis of home ranges over a

five year period.

Key words: Reptilia, Lacertilia, Gekkonidae, Teratoscincus przewalskii, Gobi Desert, Mongolia, ecology.

FIG. 1. An adult Teratoscincus przewalskii.

Introduction

From the time it was first described,

Przewalsky's Gecko (Teratoscincus

przewalskii Strauch, 1887) has remained

one of the least studied representatives of

the herpetofauna of Central Asia. As

distinguished from its close Central Asian

relative, the Turkestan Plate-Tailed Gecko

(T. scincus Schlegel), this species has been

very rarely studied in nature, and it was

only in 1961 that it was recorded in the

fauna of Mongolia (Figs. 1, 2 and Plate 1).

Occasional data on its biology are available

(Borkin et al., 1983a, 1983b; Munkhbayar,

1976; Obst, 1962; Semenov and Borkin,

1986; Szczerbak and Golubev, 1986;

FIG. 2. A juvenile Teratoscincus przewalskii.

Zhao, 1985).

In the summers of 1981, 1982, and

1985, observations of this species were

performed at the Ekhiyn-Gol (Ehiin-Gol)

Desert Station of the Joint Soviet-

Mongolian Complex Biological Expedition.

In addition, material on this species was

collected in other regions of the Transaltai

Gobi in the course of faunal surveys. The

Ekhiyn-Gol (Ehiin-Gol) Oasis is situated in

the subzone of extremely arid deserts

(average annual precipitation is 20-50 mm)

in the south of the Bayanhongor Aymag

(Province), (Fig. 3). Frosty winters with

air temperatures of as low as -34°C, hot

summers (air temperatures of up to 42°C

1992 by Asiatic Herpetological Research

Vol. 4, p. 100

Asiatic Herpetological Research

February 1992

- V*'

FIG. 3. The geographic position (dot) of Ekhiya-Gol Oasis, Transaltai Desert, Bayanhongor Aymag

(Province), Mongolia.

and ground surface temperatures of up to

70°C), abrupt daily temperature fluctuations

(up to 42°C), strong winds, and sand

storms are the main features of the local

climate (Figs. 4 and 5).

The most typical landscape of the

Transaltai Gobi is broken stone desert

plains or depressions surrounded by

mountains. Vegetation in the vicinity of the

Ekhiyn-Gol Oasis consists of Saxaul

(Haloxylon ammodendron) with some

Nitraria sphaerocarpa, Zygophyllum

xanthoxylon, Ephedra przewalskii,

Calligonum mongolicum, Reaumuria

soongorica, and others. On the edge of the

oasis there are two small sand sites with tall

Saxaul trees. On one of these sites a plot

was established for observation of geckos

(Fig. 6). Here Przewalsky's Gecko

coexists with a lacertid lizard, Eremias

vermiculata, a colubrid snake, Psammophis

lineolatus, and a boid snake, Eryx tataricus.

Another lizard species, the agamid

Phrynocephalus versicolor, was

occasionally recorded in peripheral parts of

the sands, near broken stone desert habitat

where this species is more common. More

detailed information on the nature of the

Transaltai Gobi and on the Ekhiyn-Gol

Desert Station is available from the book

"Deserts," edited by Sokolov and Gunin

(1986).

Methods

At night, geckos are easily discernible

due to a characteristic ruby reflection of

their eyes in the light of an electric torch.

Thus, lizards may be located from a

distance of a few dozen meters. To

characterize their spatial distribution,

individuals were marked by paint and by

toe-clipping on the first capture. On

subsequent captures, the lizards were

remarked with paint if necessary. White

numbers painted on the back of the animals

make them easily recognizable (until

molting) at night in the light of a torch

without much disturbance to them. This

double marking scheme allows an estimate

of the time interval between molts.

Marking and observation were performed

on a 100 by 100 m plot established on a

February 1992

Asiatic Herpetological Research

Vol. 4, p. 101

U

u

3

«

L.

O.

E

<u

H

14

Time (hrs)

18 20 22

FIG. 4. Daily variation in air and ground surface temperature at Ekhiya-Gol Oasis, Transaltai Desert,

Bayanhongor Aymag (Province), Mongolia, June 15, 1981, warmest day of the Summer.

sandy site with some Saxaul. Marked

stakes were placed at 10 m intervals. The

plot was inspected daily at various times

from June 26 to August 17, 1981, from

July 5 to August 13, 1982, and July 7-8,

1985. Gecko observations were recorded

in relation to the stakes. In 1981 and 1982,

a total of 83 geckos were marked, and 365

recaptures were recorded on the plot and

near its boundaries. In fact, all individuals

inhabiting the plot during this period were

marked. Occasional non-marked animals

appeared due to irregular invasions. The

data were processed according to Semenov

and Kulikova (1983) and Semenov and

Borkin (1985). For each individual, the

size of the home range, average and

maximum movement, average radius of

sightings, extent of reciprocal overlapping,

and changes in range position were

determined depending on the completeness

of the data. Body length, tail length, and

sex of captured animals were also recorded.

Along with observations on this permanent

plot, the population density of this species

in Ekhiyn-Gol was determined by a

complete removal study on August 16-23,

1981 on another plot of the same size,

located on the other sand site. The absolute

density with consideration of the marginal

effect was estimated according to Semenov

and Shenbrot (1985).

To characterize the daily and temperature

dependent activities of Przewalsky's

Gecko, the time of observation and air and

ground temperatures were recorded.

Cloacal temperatures were recorded from

45 geckos in three localities.

The stomach contents of 29 individuals

caught in the vicinity of the Ekhiyn-Gol

Oasis were studied. The weight of the

stomach and its contents and the taxonomic

identity, size, and dimensions of food items

were determined, and the parameters of diet

diversity were calculated according to

Semenov (1986).

The behavior of geckos in their natural

environment was observed in a corral 2 by

2 m, by 25 cm in height, constructed of

polyethylene film. Observations were

performed day and night with a red torch.

Vol. 4, p. 102

Asiatic Herpetological Research

February 1992

£

'i

3

X

>

0!

Relative Humidity

Barometric Pressure

-968

969

24 I ■ i ■ i ■ i ■ i ■ i ■ i ■ i ■ i ■ i ■ i

0 2 4 6 8 10 12 14 16 18 20 22 24

Time

962

FIG. 5. Daily variation in relative humidity and barometric pressure at Ekhiya-Gol Oasis, Transaltai

Desert, Bayanhongor Aymag (Province), Mongolia, June 15, 1981, warmest day of the Summer.

Results and Discussion

Habitat Preference

Unlike the stenotopic psammophilous T.

scincus (Szczerbak and Golubev, 1986),

Przewalsky's Gecko (also a predominantly

psammophilous species) regularly occurs in

other biotopes. It seems to depend on the

relative rarity and patchiness of sandy sites

in the Transaltai Gobi where broken stone

deserts prevail. The commonest habitat of

T. przewalskii in this region is

semistabilized sands overgrown with

Saxaul (Fig. 6). Stationary observations

are performed at precisely such a place.

The marking plot in 1981 was permanently

inhabited by 18 individuals. A similar

result was obtained on the other census plot

where 19 geckos were caught. With

consideration of the marginal effect, the last

figure yields an estimated density of 11.5

individuals per hectare. In 1982, 12

permanent residents were recorded on the

plot.

In gecko habitats, Tamarix sp. and

Calligonum mongolicum may be present in

addition to Saxaul on sand, and sometimes

replace it. On margins of oases, geckos

occur on small sandy hills with low shrubs

{Reaumuria soongorica, Zygophyllum

xanthoxylon, Ephedra przewalskii, and

rarely, Nitraria sphaerocarpa). It should be

noted that Przewalsky's gecko was found

in only part of all seemingly suitable sandy

biotopes (habitats) in the Transaltai Gobi.

They definitely avoid clear nonstabilized

sand without vegetation.

Sometimes geckos also settle on small

hills with fine soil covered by a dense

surface crust, or on takyr-like sites, such as

at Toli-Bulag in the vicinity of Ekhiyn-Gol

or at Dzamiin-Huren-Els [southernmost

Mongolia, Omnogovi Aymag (Province)].

At the latter site, geckos were numerous

under Tamarix sp. bushes and under

Nitraria sphaerocarpa. Thus, on August

31, 1982, in spite of rain, 22 individuals

were caught in a 1.5 hour period.

As well as on sandy biotopes, this

species may be found on broken stone

desert sites adjacent to sand, including

hammada absolutely devoid of vegetation.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 103

FIG. 6. A small sand hill with Saxaul Trees {Haloxylon ammodendron). This was a plot used for

observation of T. przewalskii, June 22, 1981.

According to our data, T. przewalskii

may live in areas up to 200 m distant from

sand. Obviously, this enables geckos to

populate isolated sandy areas scattered in

the Transaltai as islands in stony regions of

the desert. We note a particularly

interesting situation in Bayan-Gol

[Omnogovi Aymag (Province)] where in

the middle of July, geckos were found only

on slopes (sometimes steep) of stony hills,

and were completely absent from adjacent

sands (Semenov and Shenbrot, 1986b).

Demographic Parameters

In the Ekhiyn-Gol population, adults

with body lengths exceeding 70 mm are

prevalent. The maximum body length of a

mature gecko is 94 mm for males, and

96 mm for females. Body weight reaches

25 g. The minimum body length of

individuals that have overwintered once is

51 mm. After hatching, juveniles have a

minimum body length of 40 mm and a

body weight of about 2 g (Fig. 7).

On the plot in 1981, 16 males, 11

females, 22 subadults, and 15 juveniles

were marked. On the same plot in 1982,

13 males (12 marked the previous year), 8

females (6 marked the previous year), 15

subadults (7 marked the previous year),

and 3 juveniles were recorded. Of the 12

geckos caught on the plot in 1985, 6 were

marked in 1981-1982, including a male and

a female marked as adults in 1981, a female

marked as an adult in 1982, a male marked

as a subadult in 1981, and a male and a

female marked as subadults in 1982.

All subadults marked in 1981 reached

the adult size by the summer of 1982,

though some of them were provisionally

left in the subadult group. Thus, maturity

Vol. 4, p. 104

Asiatic Herpetological Research

February 1992

5 6 7 8

Body Length (cm)

10

FIG. 7. The relation between body weight and body length (snout to vent) in T. przewalskii.

is reached after two winters. The life span

of these geckos reaches 6 years in the wild.

It is to be taken into consideration that the

body length on a female caught in 1985

was the same as in 1981, while lizards

which had overwintered twice had a body

length of 78 mm. Thus, the life span may

exceed 6 years.

According to our measurements of

marked and recaptured geckos, juveniles

grow 15-18 mm in length by the beginning

of the next season. The annual growth of

immature individuals fluctuates between 4

to 18 mm. Adult males grow 0-8 mm;

adult females grow 0-4 mm. It should be

noted that errors of measurement of body

length of live lizards in the field are quite

high (2-4 mm). Thus, these geckos grow

rapidly during the first two years of life

before maturity, then their growth slows

down. The female mentioned above whose

length was 90 mm in 1981 remained the

same over 4 years, while a male marked in

1981, having a body length of 77 mm, was

84 mm long in 1982 and 92 mm in 1985.

Some of the prevalence of males among

recorded geckos is obviously related to

their larger home ranges (see below). The

approximate sex ratio in nature is close to

1:1.

Unfortunately there are no collections

made in the spring and the beginning of

summer, which is obviously the time of

reproduction and egg laying. Spring

begins in the Transaltai Gobi in March and

terminates in May, and is commonly dry.

Snow melts in the first half of April. The

summer months last from June to the

beginning of September. Commonly up to

80% of the annual precipitation (mainly

rainstorms) falls during three summer

months, mainly between the second half of

July and the middle of August. In this

region, T. przewalskii begin their

reproduction not earlier than the second half

of April, and probably later. Females

caught in various places from July to

August had no eggs (N = 21), and only

small follicles up to 3 mm in diameter were

present. In a female caught in May 27,

1982, 80 km southeast of Nomgon

settlement [the Omnogovi Aymag

(Province)], follicles reached 5 mm in

diameter. On August 26, 1982, N. L.

Orlov found two eggs about 16 mm in

diameter with developed embryos (see

Szczerbak and Golubev, 1986). Juvenile

February 1992

Asiatic Herpetological Research

Vol. 4, p. 105

TABLE. 1 . Spatial distribution in a population of T. przewalskii.

Sex/age groups, year Home range area,

of observations

m"

Average movement, Radius of recurrent Maximal

m sightings, m movement, m

T. przewalskii appear later than other lizard

species in the same region. In 1982, the

first juveniles were found in July, 1985

[July 10 in the Orgostiyn-Us Oasis of the

Gobi- Altai Aymag (Province), and July 13

in the Ekhiyn-Gol Oasis]. In 1985, the

first juvenile was caught on July 18 at the

Bayan-Gol area, south of the Omnogovi

Aymag (Province). However, in 1981, the

first juvenile in the Ekhiyn-Gol Oasis was

not found until August 4.

This leads us to believe that the period of

egg laying is shorter in T. przewalskii than

in the Middle Asian T. scincus, which

mates in April and lays between June and

July (rarely in the beginning of August)

(see Szczerbak and Golubev, 1986). It is

possible that Przewalsky's Gecko lays only

one clutch of 1-2 eggs, as related species

due. Demographic parameters characterize

Przewalsky's Gecko as having a K-

selection strategy (Pianka, 1981).

Spatial Distribution

Teratoscincus przewalskii do not

migrate. Most individuals possess clearly

delineated home ranges. Some geckos

seem to be nomadic, partly explaining the

disappearance of some individuals from the

plot, and the appearance of new geckos.

However, such translocations are rare; in

spite of regular surveys in the vicinity of

the plot, no marked geckos were found at

distances much exceeding their normal

range of movements. The maximum

recorded movement during one season is

140 m for an adult male in 1982 (it is

interesting that in 1981, the same lizard

moved 19.5 m, also the maximal movement

of the year). On the average, movements

were much lower (Table 1).

Home ranges do not differ much from

year to year. The seven geckos for which

home ranges were determined in 1981 had

nearly identical ranges in 1982 (Figs. 8 and

9). The mean distance between the

centroids of the 1981 and 1982 home

ranges was 19.4 m (range: 3-36 m). Other

geckos recorded in both years were found

either within their 1981 home ranges in

1982, or between 1 to 58 m from the

nearest point of observation in 1981. The

greatest distance between points of

observation in 1981 and 1982 is 180 m, by

a subadult male (first marked as a juvenile

after hatching in 1981). In 1985, six

geckos were found from 30 to 130 m from

the nearest point of observation in 1982.

Thus, Przewalsky's Gecko, like the agamid

lizard, Phrynocephalus versicolor, studied

by the same method, a gradual shift of

home ranges takes place (Semenov and

Borkin, 1985; Smirina and Semenov,

1985).

Individual movements of geckos did not

vary significantly among age/sex classes

between 1981 and 1982 (t = 0.27, N = 23,

P > 0.05). The size of home ranges and

Vol. 4, p. 106

Asiatic Herpetological Research

February 1992

FIG 8. The movements of an adult female T. przewalskii. Dot: records of the lizard in 1981. Triangle:

records of the lizard in 1982. Star: centroid of the 1981 records. Hexagon: centroid of the 1982 records.

Solid arrow: denotes the next closest sighting in time. Dashed line: arbitrary boundary of the 1981

individual range. Dot-dash line: arbitrary boundary of the 1982 individual range.

other parameters (the combined data for

both seasons) are higher in males than in

females (Table 1), but in no case is the

difference at a significant level (home

range: t = 0.61, N = 19, P > 0.05;

individual movements: t = 1.92, N = 32, P

> 0.05; radius of recurrent sightings: t =

0.77, N = 21, P > 0.05; maximum

movements: t = 1.51, N = 22, P > 0.05).

However, the home range area and the

radius of recurrent sightings is significandy

greater in males than in subadults (home

range: t = 2.66, N = 26, P < 0.05;

recurrent sightings: t = 3.12, N = 28, P <

0.01).

The home ranges of these geckos

overlap greatly (Fig. 7), irrespective of sex.

Obviously Przewalsky's Geckos are not

territorial. Their spatial distribution

corresponds to the scheme typical lizards

actively looking for their prey, living in

conditions of relatively poor visibility, and

widely exploiting nonvisual orientation

methods (Stamps, 1977).

Special attention should be given to the

movement of marked juveniles. Unlike

adults (see above), only 2 of 15 juveniles

marked in 1981 were recorded in the next

year (one of them was at a distance of 180

m; another had formed a home range 23 m

from the marking point). Altogether, 18

juveniles were marked, of which 14 were

not encountered during the same year, and

4 occurred twice each. It may be assumed

that in Przewalsky's Gecko, juveniles are

in the dispersal mode, similar to the

agamid, Phrynocephalus versicolor

(Semenov and Borkin, 1985). Having

hatched, juveniles do not form home

ranges, but disperse and only setde after the

first overwintering. Movements of

juveniles may exceed the maximum

February 1992

Asiatic Herpetological Research

Vol. 4, p. 107

FIG. 9. Individual ranges of the gecko, T. przewalskii in 1981. Open triangle: records of lizards captured

only once. Solid line: arbitrary boundary of individual ranges.

movements of adults (see above).

Shelter

Przewalsky's Geckos use their own

burrows and those of rodents as shelters.

Gecko burrows are, as a rule, made at the

base of bushes, with a semicircular

opening. The length of the burrow is a few

dozen centimeters.

Activity and Temperature

Przewalsky's Gecko is exclusively

nocturnal. This is its distinction from many

other "nocturnal" representatives of the

Gekkonidae, which are characterized by

mixed or crepuscular activities (Szczerbak

and Golubev, 1986). According to Obst

(1963), in the Galbyn-Gobi, in the first 10

days of September, geckos were active

between 20:00 and 24:00 hours. We

observed active individuals from 21:50 to

04:00 hours, at air temperatures of 16-29.5

°C and ground temperatures of 18-29 °C.

Strong wind and drizzling rain do not

decrease the activity of geckos noticeably.

Distinct periods of increased and decreased

activity are evident at different times not

clearly related to any weather conditions.

Such periods are not restricted to post-

sunset hours, as in some other gecko

species (Pianka and Pianka, 1976; Cooper

et al., 1985). This ecological aspect of this

species requires special study.

The cloacal temperature in 45 geckos

measured from 22:00 to 23:30 hours at

three different localities ranged from 17.5

to 28.5 °C. Figure 10 demonstrates the

relationship of cloacal temperature to air

temperature in 25 individuals of different

age and sex [in the vicinity of Ekhiyn-Gol

and Shara-Hulsny-Bulag oasis in the south

of Bayanhongor Aymag (Province)]. As a

rule, cloacal temperature is slightly lower

than air temperature by about 1°C. In only

six individuals was cloacal temperature

higher than air temperature. This may have

been the result of stress since these lizards

Vol. 4, p. 108

Asiatic Herpetological Research

February 1992

24 26

Air Temperature

30

FIG. 10. The relation between air and cloacal temperatures in T. przewalskii.

were either being pursued or handled for a

long time. During a few minutes of

handling, the cloacal temperature in a gecko

may increase by 3-4°C. Figure 1 1 shows

the temperatures of 1 1 geckos from the

vicinity of the Shara-Hulsny-Bulak Oasis.

Measurements were made on July 5, 1982,

during a strong wind. The sand

temperature was slightly higher than the air

temperature. The temperature of the back

of the lizards slightly exceeded the cloacal

temperature. In 20 individuals caught in

the Dzamiin-Huren-Els area in late summer

(August 31, 1982), the cloacal temperature

was 17.5-19.8°C, averaging 18.3°C, with

an air temperature of 18.0-1 8. 2°C. The

temperature of the sand surface was 1 8°C,

and the temperature of the ground air layer

dropped from 17.5 to 16.2°C during the

22:00-23:20 hour measurement period. It

should be noted that lizards were caught

and measurements made during a weak

rain.

On the whole, the above data are too

scanty and diverse to make any final

conclusions on the thermobiology of

Przewalsky's Gecko.

The strictly nocturnal activities of this

species seem to be controlled by a light

factor of by the combined action of light

and temperature, rather than by temperature

alone. In any case, suitable temperatures

occur not only at night, but also in the

evening and morning (Fig. 4), but geckos

were never met during the light of day.

Diet

Analysis of the stomach contents of

Przewalsky's Gecko (Table 2)

demonstrates that, like the Middle Asian T.

scincus, (Bannikov et al., 1977) this

species feeds mainly on beetles.

Specialization in feeding on beetles

manifests itself in the development of a

robust jaw apparatus. Relatively low

diversity parameters of feeding are the

consequence of this specialization (Table

3). Similar values are only known for

some populations of the agamid lizard,

Phrynocephalus versicolor feeding mainly

on ants. They are much higher in other

lizards of the Transaltai Gobi (Semenov,

1986). The largest food items are the

tenebrionid darkling beetles (18x6 mm),

and their larvae (24x4 mm) [these are so

large that only one beetle or one larva is

consumed at a time]; the smallest are ants

(1x3 mm). Sometimes geckos may devour

larger objects. A gecko consumed an adult

February 1992

Asiatic Herpetological Research

Vol. 4, p. 109

4>

U

3

«

t-

a.

E

H

"T

20 30 40 50

Time (min after 22:00)

FIG. 1 1 . Environmental and body temperatures in T. przewalskii versus time.

lizard, Phrynocephalus versicolor (about 80

mm in length, including the tail, and 10 mm

in width) placed in the same bag with it.

According to the observations of Szczerbak

and Golubev (1986), these geckos will

attack small lizards in a terrarium. The

average weight of a full stomach reaches

7.8% of body weight.

Molting

Prolonged observations of marked

lizards helps to record the frequency of

molting (Semenov and Shenbrot, 1986a).

Approximately half of the geckos observed

in 1981 and 1982 molted during the period

of observation. Only one individual (a

subadult male) made two molts during one

season: one in the middle of July and one in

the middle of August, 1981. As all molted

geckos were supplied with dorsal numbers

again, and since in the next year these

individuals were once again without

numbers, it may be stated that molting takes

place more than once a year. According to

our data, there are no special molting

periods, since molting individuals were

observed throughout our observation

period. Like other geckos, Przewalsky's

Gecko devours the shed skin layers (found

in two stomachs). According to

observations in a terrarium, molting occurs

quite rapidly over the period of several

hours (Obst, 1963).

Teratoscincus scincus molts not less than

three times during the season. According

to observations in captivity, molting takes

5-6 days (Szczerbak and Golubev, 1986).

Behavior

As was noted above, Przewalsky's

Geckos do not protect territories.

Nevertheless, in the corral, distinct

aggressive behavior was observed: an adult

darted at an approaching young gecko and

inflicted a powerful blow to its head

(perhaps having bitten it); one of them

emitted a short acoustic signal.

Przewalsky's Geckos have no permanent

"observation posts" on the home range, and

seemingly do not protect either the range or

their shelters. Such protection is known

for most of the Gekkonidae (Stamps,

1977). The aggressive behavior must be

related to the support of the individual

distance (Carpenter, 1965).

Judging by its movements,

Przewalsky's Gecko is a typical predator

that actively forages for its prey, in contrast

to most other geckos that mainly wait for

prey (Stamps, 1977). It is interesting to

Vol.4, p. 110

Asiatic Herpetological Research

February 1992

TABLE. 2. Stomach contents of T. przewalskii (N=14).

B is calculated according to Colwell and Futuyma (1971).

note that according to our observations in

the corral, geckos often touch the ground

surface with their tongue. Such

chemoreceptive behavior is common in the

Lacertidae and the Scincidae (Stamps,

1977), and is noted in some agamids

(Panov and Zykova, 1986; Semenov,

1985). In contrast to T. scincus,

Przewalsky's Geckos can swiftly and

easily climb bushes, and do it rather often

in escaping the pursuit. Geckos may climb

bushes up to the height of 80 cm. In the

corral, burrowing of a gecko was

observed. Only its forelegs participated.

Acoustic signaling is not noted in natural

conditions, but handled geckos sometimes

emit a brief squeak. Similar to the Middle

Asian T. scincus, the autotomized tail emits

a rather loud rustling, and wriggles for a

long time (up to 19 minutes). The skin of

these geckos is fragile, thus helping them to

"slip out" if taken in hand. When handled,

they desperately twist and try to bite.

The alarmed gecko rises in its

straightened legs and lifts up its short,

fleshy tail. In this posture, the gecko is

somewhat similar to a dog. Evidently for

this reason it is called in Mongolia,

"Nokhoy-Gurvel," meaning, "a dog

lizard."

Acknowledgments

We would like to express our gratitude

to our Soviet and Mongolian colleagues, H.

Munkhtogoo, N. L. Orlov, and H. Terbish

for their cooperation in field work. We

greatly appreciate G. I. Shenbrot's help in

processing the data, and V. B. Beyko's

advice on identification of food items. Kh.

Munkhbayar consulted and supplied us

with the photo of an adult gecko. T. J.

Papenfuss, J. R. Macey and K. Autumn

kindly corrected our manuscript . Our

research was funded by the USSR

Academy of Sciences.

February 1992

Asiatic Herpetological Research

Vol. 4, p. Ill

Literature Cited

BANNIKOV, A. G., I. S. DAREVSKY, V. G.

ISHCHENKO, A. K. RUSTAMOV, AND N. N.

SZCZERBAK. 1977. [Guide to the amphibians

and reptiles of the USSR fauna].

Prosveshchenie, Moscow. 414 pp. (In

Russian).

BORKIN, L. J., KH. MUNKHBAYAR, AND D. V.

SEMENOV. 1983a. [Amphibians and reptiles].

Pp. 52-56. In [Complex characteristics of

desert ecosystems of the Transaltai Gobi].

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BORKIN, L. J., KH. MUNKHBAYAR, AND D. V.

SEMENOV. 1983b. [Amphibians and reptiles

of the Transaltai Gobi]. Priroda, Moscow

10:68-75. (In Russian).

CARPENTER, C. C. 1965. Aggression and social

structure in iguanid lizards. Pp. 87-105. In W.

W. Milstead (ed.), Lizard ecology: a

symposium. University of Missouri Press,

Columbia, Missouri.

COOPER, W. E. JR., C. CAFFREY, AND L. J.

VITT. 1985. Diel activity patterns in the

banded gecko, Coleonyx variegatus. Journal of

Herpetology 19(2): 308-311.

COWELL, R. K., AND D. J. FUTUYMA. 1971. On

the measurement of niche breadth and overlap.

Ecology 52(4): 567-576.

MUNKHBAYAR, H. 1976. [Amphibians and

reptiles of the Mongolian People's Republic].

Ulaanbaatar. 167 pp. (In Mongolian).

OB ST, F. J. 1962. Eine herpetologische

Sammelreise nach der Mongolei. Aquarien-

Terrarien, GDR 9(1 1):333-342.

OBST, F. J. 1963. Amphibien und Reptilien aus

der Mongolei. Mitteilungen aus dem

Zoologischen Museum in Berlin 33(2):361-370.

PANOV, E. N., AND L .Y. ZYKOVA. 1986.

[Notes on the Agama sanguinolenta behaviour.

2. Everyday and communicative behaviour].

Zool. Zhurnal, Moscow 65(2):234-246. (In

Russian with English summary).

PIANKA, E. R. 1978 (1981). Evolutionary

ecology, 2nd edition. Harper and Row, New

York. (Refence in this article is made from the

Russian edition 1981. Mir. Moscow, 399 pp.).

PIANKA, E. R., AND H. D. PIANKA. 1976.

Comparative ecology of twelve species of

nocturnal lizards (Gekkonidae) in the western

Australian desert. Copeia 1976(1): 125-142.

SEMENOV, D. V. 1985. [The behaviour of

Phrynocephalus versicolor. Zool. Zhumal,

Moscow 64(10): 1545- 1555. (In Russian with

English summary).

SEMENOV, D. V. 1986. [Feeding of the motley

round-headed lizard, Phrynocephalus versicolor

(Reptilia, Agamidae) in southern Mongolia].

Bulletin of the Moscow Society of Naturalists,

series biology 91(6): 16-29. (In Russian with

English summary).

SEMENOV, D. V., AND L. J. BORKIN. 1985.

[Movements and individual ranges in

Phrynocephalus versicolor (Reptilia, Agamidae)

in the Transaltai Gobi, Mongolia]. Zool.

Zhurnal, Moscow 64(2):252-263. (In Russian

with English summary).

SEMENOV, D. V., AND L. J. BORKIN. 1986.

[Amphibians and reptiles]. Pp. 114-119. In

V. E. Sokolov and P. D. Gunin (eds.), [The

deserts of the Transaltai Gobi. The natural

features, ecosystems, and regionalization].

Nauka, Moscow. (In Russian).

SEMENOV, D. V., AND G. S. KULIKOVA. 1983.

[Home ranges and movements of

Phrynocephalus interscapularis (Reptilia,

Agamidae)]. Zool. Zhurnal, Moscow

62(8):1209-1220. (In Russian with English

summary).

SEMENOV, D. V., AND G. I. SHENBROT. 1985.

[An estimate of absolute density of lizard

populations taking into account the marginal

effect]. Zool. Zhurnal, Moscow 64(8): 1246-

1253. (In Russian with English summary).

SEMENOV, D. V., AND G. I. SHENBROT. 1986a.

[Data on molting in lizards of the genus

Phrynocephalus]. Ekologiya, Sverdlovsk 2:80-

82. (In Russian).

SEMENOV, D. V., AND G. I. SHENBROT. 1986b.

[Data on herpetofauna of southeastern

Mongolia]. Pp. 110-119. In E. I. Vorobyeva

(ed.), [Herpetological investigations in

Mongolian People's Republic]. Moscow. (In

Russian with German summary).

SMIRINA, E. M., AND D. V. SEMENOV. 1985.

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[New data on movements of P hrynocephalus

versicolor (Reptilia, Agamidae)]. Zool.

Zhurnal, Moscow 64(8): 1272- 1274. (In

Russian with English summary).

SOKOLOV, V. E., AND P. D. GUNDN (eds.). 1986.

[The deserts of the Transaltai Gobi. The natural

features, ecosystems, and regionalization].

Nauka, Moscow. 207 pp. (In Russian).

STAMPS, J. A. 1977. Social behavior and spacing

patterns in lizards. Pp. 265-321. In C. Gans

and D. W. Tinkle (eds.), Biology of the

Reptilia, Vol. 7, Ecology and Behaviour A.

Academic Press, New York.

SZCZERBAK, N. N., AND M. L. GOLUBEV. 1986.

[Geckos of faunas of the USSR and adjacent

countries]. Naukova Dumka, Kiev. 232 pp.

(In Russian).

ZHAO, K. 1985. [An investigation on the lizards

of Xinjiang Uygur Autonomous Region]. Acta

Herpetologica Sinica 1985-4(l):25-29. (In

Chinese with English summary).

February 1992

Asiatic Herpetological Research

Vol. 4, pp. 113-122|

Intrapopulational and Geographic Variation of Eremias przewalskii Strauch

in Mongolia

VALENTIN A F. ORLOVA1

^Zoological Museum of the Moscow Lomonosov State University, Russia

Abstract. -Body size and proportions, characters of pholidosis, coloration and pattern of Eremias

przewalskii from western, southern and eastern Mongolia were studied. Sexual dimorphism is displayed in

the relative sizes of the tail, head, legs, number of scales around 9- 10th tail ring and ventralia. Some

characters of pholidosis, as number of scales around the mid-body, number of femoral pores on the right

side of the thigh and others displayed clear geographic variability. Live specimens from western Mongolia

have blue ocelli on the body flanks. The lizards from southern Mongolia significantly differ from the

specimens from other parts of the range by a larger number of scales around the mid-body, number of

femoral pores on the right side of the thigh and other features. The intraspecific structure of E. przewalskii

is discussed.

Key words: Reptilia, Squamata, Lacertidae, Eremias przewalskii, Mongolia, geographic variation,

morphometries, pholidosis, population variation.

Introduction

Eremias przewalskii Strauch is a

common species of western and southern

Mongolia (Bannikov, 1958; Dely, 1979,

1980; Munkhbayar, 1973, 1976; Obst,

1963; Orlova, 1984, 1989; Orlova and

Semenov, 1986; Szczerbak, 1970, 1974;

Terbish, 1989). Earlier it was thought that

it only occured along the boundaries of

southeastern Mongolia (Bannikov, 1958;

Szczerbak, 1974). Now it is known to be

the most widely distributed lizard in this

region (Semenov and Shenbrot, 1986).

Outside of Mongolia this lizard is

distributed in northern China and Russia, in

the southern portion of Tuva Autonomous

Republic (Bedriaga, 1909; Flint, 1960;

Pope, 1935; Schmidt, 1927; Strauch, 1876;

Szczerbak, 1974).

All researchers who have observed E.

przewalskii in the wild have noted its

preference for soft soils. This species

inhabits sands overgrown with Nitraria sp.,

sand dunes with Haloxylon sp. and

Tamarix sp. In the Transaltai Gobi, E.

przewalskii rarely occurs in gravel areas

adjacent to sandy habitats (Borkin et al.,

1983). In Uws-Nuur hollow and on the

right bank of the river Khowd-gol it occurs

on semi-anchored sands with Caragana.

Rarely, E. przewalskii lives on saline soil,

in the dry gullys with almond-bush. In

Bayan-Drag it is found among the stones of

Cretaceous red sandstone precipices

(Borkin, 1986; our observations). As

compared to Eremias multiocellata, this

species does not extend into high

mountains, inhabiting either hollows and

foothills with elevations 760-1800 m above

sea level (Szczerbak, 1974) or in a

narrower range of elevation, 1030-1650 m

above sea level (Borkin, 1986).

Within its range, E. przewalskii is

syntopic with E. multiocellata (e.g., near

the well Buiesengijn-khuduk, 35-40 km

northeast of Ba-Tsagan, in Bayan-Dzag).

High variability of external

morphological features of E. przewalskii

has been noted repeatedly in the literature.

Such investigations were started by Strauch

in his description of three Eremias species

from China in 1876. Later (Boulenger,

1921; Nikolsky, 1915; Szczerbak, 1969,

1974) these forms (E. brachydactyla, E.

przewalskii and E. kessleri) were

synonymized with E. przewalskii.

Treatment of collections made by the

Herpetological Department of the Joint

Soviet-Mongolian Complex Biological

1992 by Asiatic Herpetological Research

Vol.4, p. 114

Asiatic Herpetological Research

February 1992

FIG. 1. Localities of the samples studied. See Methods below for a reference to the numbers.

Expedition of the Academies of Sciences of

the USSR and MPR allow us to report

more detailed information on

intrapopulational and geographic variability

of the species within the territory of

Mongolia. The results are later to be used

for comparative analysis of the variability

of E. przewalskii and E. multicellata, in

discussion of the relationships of these and

other Mongolian species.

Methods

Our material originates from western,

southern and southeastern Mongolia.

Localities of E. przewalskii are noted on

figure 1. Samples collected are combined

in to groups as follows:

1. Northern coast of Char-Us-Nuur

Lake, Somon Urdgol (=Chandman),

19.06.1986, coll. Kh. Terbish, n=30.

2 Gobi-Altai Aymag: Lake Beger-

Nuur, 20.07.1982, coll. Herpetological

Department, n=17 (N 5034).

3. Gobi-Altai Aymag: Lake Alag-Nuur,

15.07.1982, coll. Herpetological

Department, n=25 (N 5030).

4. Bayan-Chongor Aymag: 35-40 km

NE of Ba-Tsagaan, 30.07.1984, coll.

Herpetological Department, n=20 (N

5402).

5. South-Gobi Aymag: Shavgijn-Us,

southern Chovuun (=Noen), 19.08.1982.;

Sain Khuduk Well, 02.09.1982.; 6 km

East of Obot-Khural, 17.08.1982, coll.

Herpetological Department, n=54 (NN

5023,5029,5031).

6. East-Gobi Aymag: 43° 53' N 108°

05' E, 28.-30.07.1987, coll. G. I.

Schenbrot et al.; 60 km SSE of Dzuun-

Bayan, 06.1986, coll. G. I. Schenbrot,

n=21 (NN 5614, 5802).

In all specimens investigated (162

specimens in total) the snout-vent length

(L); tail length (L. cd.); foreleg and hindleg

length (Pa and Pp); head length, width and

height (Lp, Cp, Hp) were measured. The

indices: L/L. cd., Pa/L, Pp/U Lp/L, Cp/Lp

and Hp/Lp were calculated. The following

February 1992

Asiatic Herpetological Research

Vol.4, p. 115

characters of pholidosis were taken into

consideration: 1 - number of scales around

the midbody (Sq.); 2 - number of scales

along mid-line of throat (G.); 3 - number of

femoral pores on the right side of the thigh

(P. fm.); 4 - distance between the internal

sides of the rows of femoral pores; 5 -

number of transversal rows of pectoral and

ventral scales (ventrale); 6 - number of

scales around the 9- 10th tail ring (Sq. c.

cd.); 7 - number of subdigital lamellae on

the 4th toe of right hindleg; 8 - number

supralabial scales (labialia); 9 - number of

infralabial scales (infralabialia); 10 -

number of dorsal scales between parietals

and level of anus; 11 - number of

frontonasal scales.

In addition to characters mentioned

above, pattern and body coloration were

recorded, including the presence or absence

of blue spots on the body sides.

For the treatment of material standard

statistical methods were used (Lakin, 1980)

with the calculation X, mx and t-criterion

for revealing sexual dimorphism and

geographic differences.

Results

Sexual dimorphism. — Eremias

przewalskii males and females in Mongolia

differ from each other by there snout-vent

length in all samples, except those from

South-Gobi Aymag (5) and East-Gobi

Aymag (6). Males are slightly larger than

females. The maximum difference in linear

size between the sexes was in South-Gobi

Aymag sample (5) from southern

Mongolia, but statistically significant

differences were not revealed, as in all

other samples (Tables 1 and 2). The tail in

the males is longer than in the females

[except the samples from Gobi-Altai

Aymag (2) and Gobi-Altai Aymag (3)]; as

is length of the hind legs [except the sample

from East-Gobi Aymag (6)]. As to the

head proportions, there is a stable

difference in relative head length (P<0.01,

P<0.001). At the same time, other

proportions, mainly Hp/Lp, slightly

differed from each other in both sexes.

Some characters of pholidosis also

displayed sex differences, although

Szczerbak (1970, 1974) considered such

sexual dimorphism to be absent in E.

przewalskii. In all the samples we

investigated the number of scales around

the 9- 10th tail ring is larger in males than in

females (Fig. 2). In the samples from

Gobi-Altai Aymag (3), South-Gobi Aymag

(5) and East-Gobi Aymag (6) such

tendency is displayed in the number of

transversal rows of the pectoral and ventral

scales. In specimens from western

Mongolia (samples 1-4) the number of

scales around the middle of the body

differed between the sexes, but these

differences are statistically insignificant.

Coloration and pattern. — We did not

find clear differences in coloration and

pattern between males and females. The

ventral surface of the body, legs and tail is

always entirely white in both sexes. In the

western part of its range, E. przewalskii

has blue spots on the flanks which is less

bright in old females.

Thus, sexual dimorphism in E .

przewalskii is displayed in relatively long

tail, head, both pairs of legs, number of

scales around the 9- 10th tail ring and

ventrals in males as compared to females.

Geographic Variability

Body size and proportions. — The largest

(maximum length 84.5 mm) lizards inhabit

the southern and southeastern parts of the

country, and the smallest lizards in the

northern and northwestern regions.

Moreover, animals of minimum size have

been found near lake Alag-Nuur, Gobi-

Altai Aymag (3). Slender specimens with

relatively long tail and hind legs are seen in

the samples from Gobi-Altai Aymag (3)

and South-Gobi Aymag (5). Lizards from

the southeast of Mongolia [East-Gobi

Aymag (6) sample] are similar to those

from the south [South-Gobi Aymag (5)] in

the relative tail length, but they have a more

robust habitus and shorter hind legs. Thus,

within the range of E. przewalskii, its body

size, relative tail and hind leg length

increases from north to south. This

tendency is more clear in males. As to the

relative head size, index Ln/L is stable in all

samples (X=0.22 in femafes and X=0.24 in

males) except the sample from Bayan-

Chongor Aymag (4), where males and

females have lower values of the index

mentioned. Relative head width and height

do not allow us to differentiate between

lizards from different parts of the range.

Pholidosis . — The characters of

pholidosis demonstrate clear geographic

variation in some cases. As shown in table

3, lizards from southern Mongolia, are

sharply distinguished from others by a

markedly higher scale number around the

middle of the body (and wider variation

limits), femoral pores, scales around the 9-

10th tail ring, infradigital lamellae on the

fourth finger of the hind leg and, to a lesser

degree, by the number of transversal rows

of pectoral and ventral scales. The distance

between the rows of femoral pores is less

in lizards from the south and southeast

[South-Gobi Aymag (5) and East-Gobi

Aymag (6) samples] as compared with the

northern and northwestern ones. The

tendency of reduced mean values of some

characters of pholidosis is more

pronounced in the western part of the

range. These characters are: the number of

scales around the midbody (Sq.), (Fig. 3),

number of scales along mid-line of throat

(G.), number of femoral pores on the right

side of the thigh (P. fm.), (Fig. 4), ventrale

and number of scales around the 9- 10th tail

ring (Sq. c. cd.)

February 1992

Asiatic Herpetological Research

Vol. 4, p. 117

40r

35

30-

25

B

D

FIG. 2. Sexual dimorphism and geographic variation in the number of scales around 9- 10th tail ring (Sq.

c. cd.)

The characteristics of external

morphological features includes, along with

others, the number of scales along the spine

(from parietals to posterior border of hind

leg). For the lizards from the South-Gobi

Aymag (5) sample this feature shows a

similar situation as in many others, i.e.

their number is markedly higher than in

lizards from the western part of the range.

Other features, such as the number of

supra- and infralabials, are less variable.

Coloration and pattern. — The coloration

varies from sandy or grey to dark-brown

and black. The pattern may be made up

either of relatively thin lines, or of rather

wide, interwoven, waved stripes and spots.

The dorsal pattern of specimens from the

Great Lakes Hollow (Fig. 5) is formed by

sandy or light-coffee wavy lines or spots.

Between these colored areas there are 4

longitudinal rows of white ocelli or larger

eroded light spots. The legs (especially

hindlegs) are covered by a pattern of light

spots surrounded by brown. The upper tail

surface (about one third of the tail length)

has a similar pattern, caudally it is divided

into single dark spots, and the tip of the tail

is light. The upper surface of the head is

olive-grey in immature specimens without

spots, or with a few spots in the parietal

and supraocular scales. There is a dark and

light striped pattern on the side of the parital

scales which sometimes reaches the

supraorbital. In individual specimens the

entire head surface is covered by dark

spots, which are more or less apparent.

Temporalia are covered by a pattern of dark

spots or stripes alternating with light spots

or ocelli. The ventral surface of the body

Vol.4, p. 118

Asiatic Herpetological Research

February 1992

TABLE 3. Geographic variation in characters of pholidosis.

70

65

60

55

50

: a b

E3 B

B

D

B

FlG. 3. Geographic variability of scale number

around mid-body (Sq.) in Eremias przewalskii.

and tail are white. Each body flank has one

row of blue ocelli, not clearly visible in all

fixed specimens. The general pattern is

preserved in lizards from the lakes Alag-

Nuur (sample 3) and Bon-Tsagan-Nuur

18

14

E3 B

io - •-u -L-

E3

E3 -r

B X

E3

A B C D E F

FIG. 4. Geographic variability of the porae

femorales (P. fm.) in Eremias przewalskii.

(sample 4). However, those from Alag-

Nuur have black color, while those from

Bon-Tsagan-Nuur range from light to dark

brown. The blue spots are bright. In the

south [South-Gobi Aymag (5) sample]

February 1992

Asiatic Herpetological Research

Vol. 4, p. 119

lizards have the most bright and contrasting

dorsal pattern (Figs. 5, 6 and 7). It is black

and white, with the pileus pattern as bright.

The ventral surface is white, but a slightly

yellowish tint may be present. Regarding

the blue spots on the body flanks, one

could not make a definite conclusion.

Fixed specimens may have blue spots, but

these, as a rule, are positioned on the parts

not characteristic for their usual occurrence.

This could be a consequence of

preservation in alcohol. Intrapopulation

pattern polymorphism is characteristic of

sample 2 from the Beger-Nuur Lake

environs (Fig. 6), where the following

specimens occur: 1- with black wavy spots

(combined with white ones) on the body

flanks, with a brown tint in the mid-

dorsum; 2- with an unclear dorsal pattern

and three rows of white spots (surrounded

by black) on the body flanks; under these

rows is a row of blue ocelli on each side; 3-

with a pattern of thinner transversally

elongated, black, wavy stripes, connected

with each other or isolated, and with single

white ocelli. The same pattern covers also

the anterior one third of the tail, and is then

divided into single small spots of dark

color. The head in most cases is light-gray

or beige, with a pattern on the parietal and

temporal parts (mainly in specimens with a

fine pattern - type 3). These blue spots are

more or less visible in almost all the

specimens.

FIG. 5. The dorsal surface pattern in Eremias

przewalskii from the northern coast of Char-Us-

Nuur Lake, Somon Urdgol (=Chandman) sample 1.

Discussion

Analysis of Eremias przewalskii

intrapopulation size and proportions

variability in Mongolia reveal clear sexual

differences. They are expressed to

different degrees in populations studied

from the western, southern and

southeastern parts of Mongolia. These

differences do not concern, as a rule, the

absolute sizes of the body (L) but

relatively, length of the head, limbs and tail

are larger in males than in females. We

have also shown dimorphism of some

characters of pholidosis in our material,

including samples of adult specimens from

each locality. Such sexual dimorphism had

not been shown by Szczerbak (1974)

during his researches of Tuva (Russia),

FIG. 6. The dorsal surface pattern in Eremias

przewalskii: from Gobi-Altai Aymag, Lake Beger-

Nuur, sample 2.

FIG. 7. The dorsal surface pattern in Eremias

przewalskii: from South-Gobi Aymag, sample 5.

Vol. 4, p. 120

Asiatic Herpetological Research

February 1992

northwestern Mongolia, China and single

specimens of Eremias from southern

Mongolia. The number of scales around

the 9- 10th rings of the tail differs in all the

samples and the number of ventrals differs

in the samples from Gobi- Altai Aymag (3)

and East-Gobi Aymag (6). The coloration

and the pattern of adult specimens have no

significant sexual differences.

The wide range of pholidosis variability

is clearly expressed to various degrees in all

the samples from Mongolia. Dely (1979,

1980) speculated that an explanation of the

high variability may be ecological isolation

and interbreeding, connected with relatively

low population density and low fecundity

of the females. It was interesting to find 2

frontonasals in 25% of investigated lizards

from southern Mongolia (Orlova, 1989)

together with other characters (larger size,

contrasting coloration, larger number of

scales around the midbody, number of

dorsal scales between parietals and level of

anus, etc.). It is curious not only as a trait

reflecting the isolation of these populations

that the presence of 2 frontonasals is

normal for E. argus and occurs in E .

multiocellata as an exception. It may

suggest a close relationship of these

species, noted by previous authors

(Bedriaga, 1912; Szczerbak, 1974).

Szczerbak has not mentioned specimens of

E. przewalskii with 2 frontonasals in

Mongolia and did not report this in the

description of the species and nominative

subspecies, while Strauch (1876) indicated

it in the description of his new species.

Strauch's descriptions of 3 species from

China were based on the variability of

coloration and pattern of E. przewalskii.

Specimens with a "rough-spotted" pattern

consisting of black or dark-brown stripes

or spots drawn in transverse direction were

described as E. przewalskii.. Specimens

with a "netted" pattern consisting of fine,

fused, wavy, interwoven lines were

described as E. brachydactyla. The third

type of pattern was designated by

Szczerbak (1970) as "transitional",

intermediate between the first and the

second characteristics of E. kessleri.

Within Mongolia, these lizards' coloration

and pattern are also variable, but among

specimens studied we have not found

"rough-spotted" ones. In China, where the

dorsal pattern of the lizards is known to be

variable, nobody has mentioned the blue

spots on the body flanks, which are

characteristic of E. przewalskii in the

western part of Mongolia. Strauch (1876)

gave detailed descriptions of single

specimens of the new species, but not in

one case did he note blue spots. Possibly,

southern Mongolian specimens also do not

have these spots. In this connection the

specimen of E. kesslieri (ZIN 5145:

collection of Zoological Institute, Russian

Academy of Sciences, St. Petersburg) from

the lower Tarim, collected by N. M.

Przewalskii, is interesting. Bedriaga

(1912:577) wrote about this specimen:

"Das Originalstuck der E. kessleri stammt

aus Gansu; ein anderes soil von Przewalski

am unteren Tarim erbeutet worden sein (N

5145). Diese weit westlich vorgeruckte

Fundstelle und die Thatsache, dass nur ein

einziges, an den Seiten sonderbarerweise

blau geaugtes Individuum von dort

mitgebracht worden ist, hat in mir Anfangs

einige Zweifel hinsichtlich der Herkunft

desselben erweckt; dock uberzeugte ich

mich nachtraglich, das es im Jahre 1878

dem akademischen Museum ubergeben

worden ist, und dass der General vorher,

namlich in den Jahren 1876 und 1877, aus

seiner Reise nach dem Lob-nor in

Wirklichkeit am Unterlauf des Tarim-

Flusses gewesen ist."

In no samples from the enormous

Mongolian territory were such drastic

pattern differences recorded, as in

specimens from China, where lizards with

2 pattern types coexist (collections of the

Zoological Institute, Academy of Science,

St. Petersburg; T. J. Papenfuss and J. R.

Macey, pers. comm.).

At present, E. przewalskii is considered

a species with two subspecies: nominative

E. p. przewalskii (Strauch) (southern

Mongolia and northern China) and E. p.

tuvensis Szczerbak (Tuva, Russia, and

western Mongolia) (Szczerbak, 1970,

1974). Dely (1979, 1980), analyzing the

variation of external morphological

February 1992

Asiatic Herpetological Research

Vol. 4, p. 121

characters of lizards from Mongolia, noted

the population from the southern Gobi as

most clearly distinct. While the author did

not have the possibility of studying the

materials from Tuva, Russia he suggested

the existance of two subspecies of E.

przewalskii. At the same time, each of the

populations investigated by him was

referred to the nominative subspecies.

Determination of the structure of the

species as a whole will depend upon future

research on E. przewalskii from China

(with detailed analysis of intrapopulational

and geographic variability, including

biochemical analysis).

Acknowledgments

I would like to express my gratitude to

Drs. Kh. Terbish, S. L. Kuzmin, E. A.

Dunaev and M. Prutkina for their help in

collecting material and in the preparation of

this paper.

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biology of Amphibia and Reptilia in

Mongolia]. Bulletin of the Moscow

Association of nature searchers, section biologie

68(2):71-91. (In Russian).

BANNIKOV, A. G., I. S. DAREVESKY, V. G.

ISCHENKO, A. K. RUSTAMOV, AND N. N.

SCHERBAK. 1977. [Field guide of the USSR

amphibians and reptiles]. Prosveschenye

Publishing, Moscow. 414 pp. (In Russian).

BEDRIAGA, J. V. 1912. Wissenschaftliche

Resultate der von N. M. Przewalski nach

Central-Asien unternommenen Reisen. Band

111. (Zoologischer Theil). Abth. 1. Amphibien

und Reptilien. St. Petersburg. 769 pp.

BORKIN, L. J. 1986. [On the relationships of

lizards of the genus Eremias (Lacertidae) from

Gobi desert, Mongolia]. Proceedings of the

Zoological Institute, Leningrad 157:185-192.

(In Russian).

BORKIN, L. J., KH. MUNKHBAYAR, AND D. V.

SEMENOV. 1983a. [Amphibians and reptiles

of Transaltai Gobi]. Complex characteristic of

desert ecosystems of the Transaltai Gobi (on the

base of the desert research station and Great

Gobian Reserve).

Russian).

Puszczino:52-56. (In

BORKIN, L. J., KH. MUNKHBAYAR, AND D. V.

SEMENOV. 1983b. [Amphibians and reptiles

of Transaltai Gobi]. Nature (10):68-75. (In

Russian).

BOULENGER, G. A. 1887. Catalogue of the

lizards in the British Museum, Vol. 3. London.

576 pp.

BOULENGER, G. A. 1921. Monograph of the

Lacertidae, Vol. 2. London. 451 pp.

DELY, O. GY. 1979. Analyse der

morphologischen Eigentumlichtleiten drei

mongolischer Eremias-Arten. Vertebrata

Hungarica 19:3-84.

DELY, O. GY. 1980. Die variabilitat von drei

Eremias-Anen aus der Mongolei. Acta

Zoologia Scientiarum Hungaria 26:89-122.

FLINT, V. E. 1960. [Eremias kessleri - a lizard

species, new for USSR fauna]. Journal of

Zoology 39(8): 1264. (In Russian).

KUZMIN, S. L., L. J. BORKIN, KH .

MUNKHBAYAR, E. I. VOROBJEVA, AND D. V.

SEMENOV. 1988. [Amphibians and reptiles of

Mongolia. General aspects. Amphibia].

Science, Moscow. 248 pp. (In Russian).

MUNKHBAYAR, KH. 1970. [Species composition

of heteroterm animals of Mongolia].

Mongolian State Pedagogical Institute.

Scientific-Methodic Notes 1(8): 109-1 13. (In

Mongolian).

MUNKHBAYAR, KH. 1973. [Amphibians and

reptiles of Mongolia]. Ph.D. Thesis.

Tashkent. 38 pp. (In Russian).

MUNKHBAYAR, KH.

reptiles of Mongolia]

Mongolian).

1976. [Amphibians and

Ulan Bator. 167pp. (In

NIKOLSKY, A. M. 1915. [Fauna of Russia and

adjacent countries. Reptiles (Reptilia)]. Vol.1.

Petrograd. 532 pp. (In Russian).

OBST, F. J. 1963. Amphibien und Reptilien aus

der Mongolien. Mitteilungen aus dem

Zoologischen Museum in Berlin 39(2):361-370.

ORLOVA, V. F. 1984. [Amphibians and reptiles

of Mongolia]. Pp.1 17-1 19. In Natural

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conditions and resources of some regions of the

People's Republic of Mongolia. Bratislava. (In

Russian).

ORLOVA, V. F. 1989. [Distribution and

variability of the Eremias lizards of Mongolia].

Pp. 181-183. In Problems of Herpetology.

Kiev. (In Russian).

ORLOVA, V. F., AND D. V. SEMENOV. 1986.

[Distribution of amphibians and reptiles in

Mongolia]. Pp. 91-108. In Zoogeographical

regionalization of Mongolian People's

Republic. USSR Academy of Sciences,

Moscow. (In Russian).

ORLOVA, V. F., AND KH. TERBISH. 1986. [Data

on the herpetofauna of Dzungarian Gobi].

Pp.95- 110. In Herpetological researches in

Mongolian People's Republic. USSR Academy

of Sciences, Moscow. (In Russian).

POPE, C. M. 1935. The reptiles of China.

Natural History of Central Asia. Vol. 10.

American Museum of Natural History, New

York. 604 pp.

SCHMIDT, K. P. 1927. Notes on Chinese

reptiles. Bulletin of American Museum of

Natural History 6:467-551.

SEMENOV, D. V., AND G. I. SCHENBROT. 1986.

[Data on the herpetofauna of southeastern

Mongolia]. Pp. 110-119. In Herpetological

researches in Mongolian People's Republic.

USSR Academy of Sciences, Moscow. (In

Russian).

SZCZERBAK, N. N. 1969. [Eremias kesslieri or

E. przewalskUl]. Proceedings of the Zoological

Museum, Kiev 33:103. (In Ukranian).

SZCZERBAK, N. N. 1970. [New subspecies

Eremias przewalskii tuvensis ssp.n. (Sauria,

Reptilia) from the Tuva Autonomous Soviet

Republic and data on the species systematics as

a whole]. Zoological Herald 1970(5):31-36. (In

Russian).

SZCZERBAK, N. N. 1971. [Ecology of Eremias

przewalskii Str.]. Zoological Herald

1971(4):58-66. (In Russian).

SZCZERBAK, N. N. 1974. (Palearctic Eremias

lizards). Kiev. 293pp. (In Russian).

STRAUCH, A. A. 1876. [Reptilians and

amphibians). Pp. 3-55. In N. Przewalsky

Mongolia and Tangit's State. Vol. 11. St.

Petersburg. (In Russian).

TERBISH, KH. 1989. [Amphibians and reptiles of

West Mongolia]. Ph.D. Thesis. Ulaan Baator.

(In Russian).

February 1992

Asiatic Herpetological Research

Vol.4, pp. 123-131|

Feeding Ecology of the Caucasian Salamander {Mertensiella caucasica),

with Comments on Life History

Sergius L. kuzmin1

^Institute of Evolutionary Morphology and Ecology of Animals, Russian Academy of Science, Leninsky

prospekt, 33, Moscow 117071 Russia

Abstract. -The feeding and developmental ecology of the Caucasian Salamander (Mertensiella caucasica)

were studied in western Georgia. Age changes of larval feeding rate are weak. The main food of larvae

consists of gammarids and insects. Larval prey size spectrum widens and displaces to more large objects

during ontogenesis. However age, diurnal, seasonal and habitat differences in diet are weak. The majority

of preys are consumed with negative electivity. During metamorphosis feeding does not cease. A review of

literature on adult Caucasian Salamander feeding is presented. A comparison of larval development data

with skeletochronology suggests that metamorphosis takes place after the second wintering. Three to five

annual rings were counted in tubular bone diaphyses of mature specimens.

Key words: Amphibia, Caudata, Salamandridae Mertensiella caucasica; Caucasus Mountains, Georgia,

feeding, larvae, electivity.

caucasica (Waga, 1876) is a stenobiont

species which lives near rocky streams in

mountain forests of western Georgia and

adjacent areas of Turkey (Figs. 1, 2, and

Plate 1). Members of this relict genus were

widely distributed in Europe in the Pliocene

(Borja and Mlynarski, 1979). Data on

Caucasian Salamander ecology are very

poor, especially on feeding ecology. The

latter are limited to food composition and

feeding behaviour in captivity (Knoblauch,

1905; Lantz, 1911; Mertens, 1942; Obst

and Rotter, 1962; Rotter, 1958;

Wolterstorff, 1942), speculations on diet

based on invertebrate fauna in the

environment (Cyren, 1911; Hemmerling

and Obst, 1968; Lantz, 1911; Mertens,

1942), and observations and dissections of

single specimens (Basoglu and Ozeti, 1973;

Ekvtimishvili, 1940; Knoblauch, 1905;

Nikolsky, 1913; Sikmashvili, 1970

Wolterstorff etal., 1936). Quantitative data

on adult diet are presented only in papers

by Bozhansky and D.V.Semenov (1982)

and Ekvtimishvili (1948).

FIG. 1. Stream habitat of Mertensiella caucasica

in Akhaldaba Region, Georgia.

Introduction

The Caucasian Salamander, Mertensiella

Methods

From June to August, 1985 the ecology

of the Caucasian Salamander was studied in

the Akhaldaba environs, Borzhomi (41° 51'

N 43° 23' E) region, Georgia. In the same

Vol. 4, p. 124

Asiatic Herpetological Research

February 1992

FIG. 2. Mountain forest habitat of Mertensiella caucasica in Akhaldaba Region, Georgia.

months of 1986 additional material on

newly metamorphosed salamanders was

collected. Adults were measured (snout-

vent length- L., tail length- L. cd.), marked

by toe-clipping and released. Besides that,

we have captured larvae and newly

metamorphosed specimens. Animals of

these two age groups as well as adult

clipped toes were fixed immediately in 5%

neutral formaldehyde solution.

Before treatment, fixed larvae were

immersed in water for several hours. I

measured them by ocular-micrometer under

a stereoscopic microscope or (larger

specimens) by vernier calliper with a

precision of 0.1 mm. Then I dried them

with filter paper and weighed them with a

precision of 1 mg. To determine the

salamander age, numbers of annual rings in

femoral (larvae) or finger (adults) bone

sections were counted (according to

Smirina and Sofianidu, 1985). For the

sake of species' conservation I didn't make

dissections of mature salamanders. I have

obtained information on their feeding from

the literature cited above.

To study larval and newly

metamorphosed salamander feeding, entire

digestive tracts were obtained. Their

contents were studied under a microscope.

The bulk of food was dried with filter paper

and weighed with a precision of 0.1 mg.

Food objects were identified and measured

under the microscope. From their linear

dimensions, reconstructed weights were

determined (for details see Kuzmin, 1984

a, 1984b).

I have determined percentages of each

prey category by its weight and number.

Because of incertainty of prey length and

mass as measures of its size availability for

February 1992

Asiatic Herpetological Research

Vol. 4, p. 125

Caudata, ratio dmax/Lt. or. (see Kuzmin,

1985) was used, where dmax=maximum

prey diameter (width or height), Lt.

or.=width of amphibian mouth (between

hind angles of lip folds). It must be noted

that some later identical parameter was

successfully used in Onychodactylus

japonicus feeding behaviour investigations

(Kusano and Hayashi, 1985).

Feeding rate in different groups of

salamanders was compared by digestive

tract-fill indices:

1986).

Y=-

m-1000%

M-m

where m=food mass, M=total consumer

mass. Caloric content of different preys

was determined using the methods of

Cummins and Wuysheck (1971). After

this, the mean caloric content of food was

counted.

Trophic niche overlap was determined

using Morishita similarity index in the

form:

h=

2I PijPik

i (HML

where pjj=percent of i-th component in the

diet of j-th predator, pjk=percent if i-th

component in the diet of k-th predator, and

0<lx<l.

To estimate feeding electivity the

contents of larval digestive tracts were

compared with the invertebrate fauna of the

stream. Invertebrates were counted after

their total sampling from stream pools

where salamanders were collected. The

feeding electivity is estimated using Ivlev's

formula:

E=

r.-p.

r,+p,

Where rj=percent of i-th component in the

diet, pi=its percent in environmental

complex, and -l^E^+1. Observations on

the feeding behavior in captivity were also

conducted (for methods see Kuzmin,

Results

Body Size and Skeletochronology

All larvae sampled are clearly divided

into 3 groups by their L.: 15.4-19.5 mm

(106-108 mg), 23.7-27.5 mm (330-644

mg) and 29.0-35.4 mm (632-1400 mg).

These three groups morphologically differ

from each other (Fig. 3). Size groups 1

and 2 contained mainly specimens that were

born in the given year. Annual rings in

their femoral bone sections are as a rule

absent (Fig. 4). Larger larvae (size group

3) had one annual ring, commonly only

vaguely expressed. On the femoral bone

sections of two newly metamorphosed

animals (captured in June and August

1985) one annual ring is also recognized.

From 10 marked adults captured 13 June,

1985 (L.=66.7±1.6 mm; L.

cd.=171.5±4.3 mm) annual rings were

succesfully counted in 7. Each specimen

had on the average 3.57±0.30 (3-5) rings.

Diet and Feeding Baeliaviowr

Quantity of food consumed. — I n

laboratory conditions Caucasian

Salamanders lived some time on

endogenous yolk and transfer to active

feeding takes place at larval size group 1 (I.

A. Serbinova, pers. comm.). It must be

noted that all the smallest larvae found in

nature belong to group 1 . The latter already

feed upon exogenous prey with high

intensity. Yolk is not recognized in their

digestive tracts. Furthermore, digestive

tract-fill index (J) changes slightly with

age. Its values are similar in different

months and in different size groups (July:

group 1- 40.1±5.4%;2- 34.1±4.2%; 3-

41.5±15.2%. August: group 2-

41.8±7.2%; 3- 34.8±3.0%). Just after

metamorphosis J remains almost on the

same level (34.8±5.5%). There are little

differences in J values between the larvae

from medium and lower stream currents

(39.5±4.3% and 35. 4. ±7.0%

respectively). Salamander larvae are more

active at night than in the daytime. The

values of J are influenced by this (L.=16-

Vol. 4, p. 126

Asiatic Herpetological Research

February 1992

FIG. 3. Caucasiaan Salamanders of different ages.

A- larvae of three size groups (1-3); B- newly

metamorphosed specimen; C- adult specimen.

17 mm: 01 h - 53%; 12-13 h - 40%).

Mean caloric content of food of different

groups has a weak monthly variation (1.01-

1.24cal/mg).

Average number of preys per digestive

tract increases with larval size from

3.00±0.43 (group 1) to 4.88+1.43 (group

3).

Food spectrum of larvae widens in

ontogenesis. Along with widening, there is

a marked displacement of prey size

spectrum to larger and larger objects (Table

1, A, B). Maximum values of dmax/Lt.or.

reached 62.6%.

The main food of salamander larvae are

gammarids and larval insects (Table 2).

The smallest invertebrates, Ostracoda and

Hydracarina, occur in the diet of smallest

salamanders. Generally, age changes of

diet are weak (see Table 2). Food

similarity (h') by prey numbers are: for

groups 1 and 2 - 0.73; 1 and 3 - 0.82; 2

and 3-0.61. For weight proportions they

are 0.80, 0.73, and 0.52, respectively.

Likewise in summer (group 2 - June and

August: Ix' =0.97 by prey number and

0.50 by weight) and day (group 1: 12-13h

and 01 h: K'=0.82 and 0.75) larval diets

changed very slowly. Larval food

differences are slightly more appearent in

medium and lower stream currents

(1^=0.59 and 0.42).

Metamorphosed salamander food

composition changes sharply due to habitat

change (see Table 2). Terrestrial insects

become dominant. Food becomes more

and more diverse with age. Crustaceans,

arachnids and insects are the main adult

salamander's prey (see Table 2). At the

same time interpopulational differences in

their feeding are insufficient: for

Akhaldaba (Bozhansky and Semenov,

1982) and Baniskhevi (Ekvtimishvili,

1948) samples h.'=0.87 by numeric

percents. Sexual differences in diets are

absent (Bozhansky and Semenov, 1982).

Apart from food items, plant remains,

parasitic nematods (in newly

metamorphosed salamanders) soil and sand

were found in the digestive tracts of

February 1992

Asiatic Herpetological Research

Vol. 4, p. 127

different stages.

Feeding electivity. — This has been

studied in June larvae. Limoniidae are

positively elected by the larvae of group 3

(E=+0.52), whereas in the diet of younger

ones, these insects are not found.

Electivity to a close family, Chironomidae,

decreases during ontogenesis (group 1:

E=-0.13; 2: -0.42; 3: -1). The larvae of

group 3 ignored the smallest object -

Ostracoda (E=-l). This prey is consumed

almost unselectively by smaller larvae

(group 1: E=+0.03; 2: -0.05).

Gammaridae are utilized with weak

electivity (1: +0.06; 2: -0.32; 3: +0.23).

Salamanders of all three groups negatively

selected Trichoptera (1: -0.73; 2: -0.42; 3:

-0.43).

Feeding behaviour. In captivity, larvae

(L.=30-35 mm) noticed the large prey

(Gammaridae 3-10 mm long, Planaria

about 10 mm) from distances of 10-16 mm,

approached up to 2-3 mm and attacked.

Planaria orientation in the mouth takes 10-

20 seconds; larger gammarids, about 40

seconds. In natural conditions salamander

larvae exhibit diurnal foraging more

frequently than adults. Among the latter

this is observed mainly in wet and dark

places. During the winter salamander

feeding ceases. In the summer they forage

in shallow water more frequently than in

early spring and autumn (Ekvtimishvili,

1948). Under the water adults waited for

moving invertebrates (Knoblauch, 1905).

This may be an adaptation to foraging in a

lotic environment. According to

Knoblauch (1905), salamander feeding

requirements do not decrease even at 9°C.

My observations reveal the upper thermal

limit of adult foraging activity as 23-25°C

range. At these temperatures animals

respond to approaching invertebrates, but

don't make attempts to catch them.

Discussion

From spring to autumn larvae of

different size groups are found in streams

(Berg, 1910; Cyren, 1911; 1968;

Hemmerling and Obst, 1968; Koroljov,

1986; Mertens, 1942; my data). Evidently

L.

35-

30-

25-

20-

15-

x

T

0

n

FIG. 4. The number of annual rings (n) in the

sections of femoral bone diaphyses of young

Caucasian Salamanders of different body oength

(L.). A- larvae, June; B- Larvae, Augues; C- newly

metamorphosed specimens.

group 1 consists of recently hatched larvae

that have began their active feeding. Group

3 is metamorphic. Their share in larval

samples markedly decreased to August due

to entering land by metamorphs. Thus, the

lack of annual rings in the bones of most of

the specimens from groups 1 and 2

indicates their birth was mainly in the given

year. Animals larger than 27 mm and

newly metamorphosed specimens had one

annual ring, so they had survived one

wintering. The largest specimens of a

given birth year only slightly differ from

the smallest that had wintered. This could

be explained by a prolonged salamander

breeding period.

Vol. 4, p. 128

Asiatic Herpetological Research

February 1992

TABLE 1 . Prey size composition of Caucasian Salamander larvae (June, 1985).

A. Proportions dmax/Lt. or., %

dmax.mm 1 (n=13)

Larval size groups

2 (n=9)

5.5

14.7

23.9

33.1

42.3

51.5

3 (n=9)

4.5

11.9

19.4

26.9

34.3

41.8

B. Proportions by numbers of prey with different dmax' %

dmax, mm

Larval size groups

2

12.9

41.9

16.1

12.9

3.2

10.7

14.3

10.7

39.3

17.9

7.1

Thus, Caucasian Salamander larvae

completed their metamorphosis during the

next year after hatching. So the opinions of

a 3 year (Koroljov, 1986) or less than 1

year (Zhordaniya, 1975) larval period of

the Caucasian Salamander are not

confirmed.*

According to some authors (Bozhanski

t If the first wintering occurs in larvae just

before the start of their hind limb skeleton

ossification, the annual ring of this wintering will

be absent. If so, the first annual ring must reflect

the second wintering. If this is confirmed,

Tarkhnishvili and Servinove's (in Press) proposal

of a two-year larval period for M. caucasica is true.

and Semenov, 1982), Caucasian

Salamanders reach their maturity after the

second wintering. The secondary sex

character, male dorsal spine on the tail

base, appears when the total length

(L.+L.cd.) reaches about 130 mm

(Hemmerling and Obst, 1968; Obst and

Rotter, 1962). My skeletochronological

data do not allow me to make a perfect

determination of adult salamanders age,

because of the lack of data on the inner

annual ring resorbtion rate. Therefore, we

must consider their age to be not less than

the number of annual rings (after Smirina

and Sofianidu, 1985), i.e. 3-5 years.

The main changes of salamander trophic

niche during ontogenesis take place under

Vol. 4, p. 129

Asiatic Herpetological Research

February 1992

TABLE 2. Prey taxonomic spectrum of Mertensiella caucasica in ontogenesis. 1-3 - larval size groups;

juv. - newly metamorphosed specimens; by horizontal: 1-% by prey number; 2-% by prey weight. For

adults from Baniskhevi (n=67) data of Ekvumlshvili (1948); from Akhaldaba (n=21) data of Bozhansky and

Semenov(1982).

l.-larvae; i. -imago

the transfer from endogenous to exogenous

feeding and, to a smaller degree, at

metamorphosis. The rest of the time food

changes are insignificant. This weak

feeding variability is in accordance with the

results of single specimen dissections from

different parts of the species range

(Basoglu and Ozeti, 1973; Knoblauch,

1905; Nikolsky, 1913; Wolterstorff et al.,

1936).

Some authors (Hemmerling and Obst,

1968; Mertens, 1942) considered larval size

variability to be a result of their different

food provisions. But the data on larval age

presented above together with weak age

and spatial variability of digestive tract-fill

index and diet confirms the opposite. A

shortage of small invertebrates in streams,

however, could be a factor influencing the

comparatively large sizes Caucasian

Vol. 4, p. 130

Asiatic Herpe to logical Research

February 1992

Salamander larvae feed on, as compared

with larvae of limnophilous tailed

amphibians (Cyren, 1911). Narrow

trophic spectrum consisting of relatively

large invertebrates as far as low occurence

of small forms in stream samples served as

its indirect confirmation.

Positive electivity in larval feeding is

weakly expressed. Evidently, their diet

reflects mainly the available invertebrate

composition in the environment. A low

percentage of larval Trichoptera in

salamander diets may be connected with

their low electivity. Probably the latter is

due to the difficulty of swallowing this

energetically improfitable prey (sand case

mass could be of 5-6 times heavier than the

food object).

The environmental conditions of the

Caucasian Salamander are very uniform

and almost unchanged since Pleistocene

(Wolterstorff et al., 1936). Indirect

confirmation of an endemic ecological

pattern is the parasitological data. The

Caucasian Salamander is the host of four

parasitic nematod species. Three of them

are specific for this amphibian (Lomakin,

1982; Sharpilo, 1976, 1978; Timofeeva

and Sharpilo, 1979). Thus, the high

Caucasian Salamander trophic niche

stability at each step of its life history

reflects the stenobiont state of this species

in the western Transcaucasian relict

ecosystems.

Acknowledgments

D. N. Tarkhnishvili has carefully

provided for me the translation of papers in

Georgian and I. A. Serbinova with the

information on the start of larval feeding in

the laboratory. They jointly with R. V.

Tartarashvili gave me important assistance

in the field. E. M. Smirina has seen bone

sections and proposed valuable remarks.

L. N. Kuzmin gave important help in

salamander photography. For all these

persons I express my sincere gratitude.

Literature Cited

BERG, L. S. 1910. [Report on the Zoological

Museum of Imperial Academy mission to

Caucasus in 1909]. Ezhegodnik

Zoologicheskgo. Museya Imperatorskoi

Academii Nauk 15:153-170. (in Russian).

BASOGLU, M. AND N. OZETI. 1973. Tiirkiye

amphibileri. Ege Universitesi matbaasi,

Bomova-Izmir. 155pp. (in Turkish).

BORJA, SANCHIZ, F. DE, AND M. MLYNARSKI.

1979. Pliocene salamandrids (Amphibia

Caudata) from Poland. Acta zoologica cracov

24(4):175-188.,

BOZHANSKY, A. T. AND D. V. SEMENOV. 1982.

[Materials on biology of Mertensiella caucasica

(Amphibia, Urodela)]. Zoologichesky Zhurnal.

61(8): 1188-1192. (In Russian).

CUMMINS, K. W. AND J. C. WUYSHECK. 1971.

Caloric equivalents for investigations in

ecological energetics. Internazionale

Vereinigung fur theoretische und angewandte

Limnologie, Mitteilung N 18. Stuttgart. 162

pp.

CYREN, 0. 1911. Beitrage zur Kenntnis des

kaukasischen Feuersalamanders, Salamandra

caucasica (Waga), seiner Lebensweise und

Fortpflanzung. Berichte der Senckenbergischen

naturforschenden Gesellschaft in Frankfurt am

Main 42:175-189.

EKVTIMISHVILI, Z. S. 1940. [Amphibians of

Borzhom-Bakuriani district]. Trudy

biologischeskiikh stanzij Narkomprosa GSSR,

Tbilisi 1940(1):1 10-121. (in Russian).

EKVTIMISHVILI, Z. S. 1948. [Feeding of

Caucasian Salamander (Mertensiella caucasica

Waga)]. Trudy Zoologicheskogo Instituta

Academii Nauk Georgian SSR 1948(8):239-

245. (in Georgian).

HEMMERLING, J., AND F. J. OBST. 1968. Zur

Normalentwicklung von Mertensiella caucasia

(Amphibia, Salamandridae). Salamandra

1968(4):4-9.

KNOBLAUCH, A. 1905. Der kaukasische

Feuersalamander, Salamandra caucasia (Waga).

Berichte der Senckenbergischen naturforschenden

Gesellschaft in Frankfurt am Main 36:89-1 10.

KOROLJOV, A. V. 1986. Some data on the larvae

of Mertensiella caucasica. Pp. 281-283. In Z.

Rocek (ed.), Studies in Herpetology. Charles

University, Prague.

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KUSANO, T., AND F. HAYASHI. 1985. Prey

type- and size-related handling time of larval

salamanders, Onychodactylus japonicus.

Japanese Journal of Herpetology 1 l(l):20-24.

KUZMIN, S. L. 1984a. [Age changes of feeding

in Hynobius keyserlingii (Amphibia,

Hynobiidae)]. Zoologischesky Zhurnal

63(7): 1055-1060. (In Russian).

ROTTER, J. 1958. Die Reise nach

Transkaukasien. Aquarien-Terrarien

5(10):286-291.

SHARPILO, V. P. 1976. [Mertensinema iberica

gen. n., sp. n. (Nematoda, Trichostrongylidae,

Meertensinematinae subfm. n.) - parasite of

Caucasian Salamander]. Vestnik Zoologii N.

5:87-90. (In Russian).

KUZMIN, S. L. 1984b. Food of

metamorphosing larvae of the Siberian angle-

tooth. Soviet Journal of Ecology 14(3): 174-

178.

KUZMIN, S. L. 1985. Rate of food

consumption and prey size of the Siberian

newt. Soviet Journal of Ecology 15(5):265-

271.

KUZMIN, S. L. 1986. Elective feeding habits

and feeding behavior of Siberian angle-tooth

larvae. Soviet Journal of Ecology 16(5):282-

286.

LANTZ, L. 1911. Salamandra caucasia Waga.

Blatter fur Aquarien und Terrarienkunde 22:3-

5, 19-20, 34-35.

SHARPILO, V. P. 1978. [Gelminths of relic

animals. I Aplectana caucasica sp.n.

(Nematoda, Cosmocercidae) - parasites of

Caucasian Salamander]. Vestnik Zoologii N.

2:82-84. (In Russian).

SIKMASHVILI, N. M. 1970. [Investigation of

the feeding of amphibians and reptiles

collected in Meskhet-Djavakheti]. Bulletin of

Academy of Sciences of the Georgian SSR

60(3):717-719. (In Georgian).

SMIRINA, E. M, AND T. SOFIANIDU. 1985.

[On life span of the neotenic and

metamorphosed Alpine newts (Triturus

alpestris) from high mountains of Greece].

Zoologichesky Zhurnal 64(2):31 1-315. (In

Russian).

LOMAKIN, V. V. 1982. [New data on

morphology of Thominx tritonispunctali

n.comb.(Nematoda, Capillariidae) - parasite of

tailed amphibians]. Vestnik Zoologii 2:44-

48. (In Russian).

MERTENS.R. 1942. Der Kaukasus-Salamander

und sein Gefangenleben. Blatter fur

Terrarienkunde 53:9-12.

TARKHNISHVILI, D. N„ AND I. A. SERBINOVA.

Life history of Caucasian Salamander in the

local population. (In Press).

TIMOFEEVA, T. A., AND V. P. SHARPILO.

1979. [Euzetrema caucasica sp.nov.

(Monogenoidea, Polyopisthocotylidea) -

parasite of Caucasian Salamander].

Parasitologiya 13(5):516-521. (In Russian).

MERTENS, R. 1968. Bemerkungen zur

"Normalentwicklung" des Kaukasus

Salamanders. Salamandra 4:44-45.

NIKOLSKY, A. M. 1913. [Reptiles and

amphibians of Caucasus. Typus of His

Imperial Majesty's Gubernator of Caucasus].

Tiflis. 250 pp. (In Russian).

OBST, F. J., AND J. ROTTER 1962. Notizen zu

Mertensiella caucasica (Wagal876). Aquarien

und Terrarien Zeitschrift 15(3):84-86.

WOLTERSTORFF, W. 1942. Ein Import des

kaukasischen Salamanders (Mertensiella

caucasica). Blatter fur Terrarienkiinde

53:389.

WOLTERSTORFF, W., L. A. LANTZ, AND W.

HERRE. 1936. Beitrage zur Kenntnis des

Kaukasussalamanders {Mertensiella caucasica

Waga). Zoologischer Anzeiger 1 16(1/2): 1-13.

ZHORDANIYA, L. 1975. [Caucasian

Salamander]. Khimiya i Biologiya v Shkole.

N 3:63-64. (in Georgian).

I February 1992

Asiatic Herpetological Research

Vol.4, pp. 132-136|

Preliminary Research on the Function of the Eggshell in the Chinese

Alligator {Alligator sinensis)*

bihui Chen1 and baodong Liang2

'Department of Biology, Anhui Normal University, Wuhu, Anhui, China

^■Anhui Research Center of Chinese Alligator Reproduction, Xuancheng, Anhui, China

Abstract. -There is a layer of mucous material on the eggshell of freshly laid Chinese Alligator eggs.

Alligator eggshells have different functions in different periods of embryonic development. Over 95% of

the eggshell consists of calcite and calcium carbonate. The freshly laid egg is strong and rigid to withstand

the weight of the adult female alligator crawling over the closed and compacted nest. As incubation

proceeds, erosion craters and cracks appear on the surface of an eggshell. This change of the eggshell is

adapted to more efficient oxygen requirements and prevents the egg from dehydration or from too much

water flowing into the egg, as the embryo rapidly develops. The eggshell does not provide calcium to

supply embryonic developmental demands. The eggshell membrane plays an important role in the

antimicrobial defence of the egg.

Key words: Reptilia, Crocodilia, Alligatoridae, Alligator sinensis, China, eggshell function

Introduction

Ecological examination in the field and

long term artificial culture has revealed that

a series of changes appear in the Chinese

Alligator's (Alligator sinensis) eggshell as

the egg develops. These changes seem to

relate closely with the alligators' embryonic

development and climatic conditions. In

order to study this relationship, in 1976 we

made some observations and experiments

on the change of the Chinese Alligator's

eggshell in the course of incubation. In

1987 and 1988, we made some additional

experiments.

Methods

Experiments concerning the mucous

material covering freshly laid eggs

investigate its influence on egg incubation.

Four clutches laid by a field alligator were

marked as A, B, C, and D respectively.

There were 21 eggs in clutch A (with 1

broken and 1 infertile), 17 eggs in clutch B,

20 eggs in clutch C and 18 eggs in clutch D

(with 1 infertile). The eggs of clutches A

and B were laid in the same day. Eleven

+ This publication was previously published in

Chinese by Chen and Liang (1990).

eggs from clutch A were selected randomly

for the experiment, with 10 eggs for the

control. Eight eggs of clutch B were

selected randomly for the experiment, with

9 eggs for the control. The experimental

eggs of clutches A and B were put together

into group I. Control eggs were put

together into group II. The eggs were laid

one day earlier in clutch C than in clutch D.

Each half of the eggs of clutch C and D

used were put together in group III, the

other half of the eggs were used for a

control and were put together into group

IV. Each egg of group I and III was

washed slightly with gauze in 26°C distilled

water, had its mucous material cleaned and

was wiped dry. The eggs of group III and

IV were submerged in oxygenated distilled

water (27-28°C) for 8 hours. Then the four

groups were set in an environmental

chamber in the same condition and

incubated at 30-32°C.

The next experiment investigated the

influence of humidity on egg incubation.

Eighty-seven eggs, which were laid by an

artificially cultured alligator in the Anhui

Research Center of Chinese Alligator

Reproduction (ARCCAR), were selected

randomly and divided into three groups. In

group 1, humidity was maintained at 95%

from 0 to 21 days after laying, at 80-85%

February 1992

Asiatic Herpetological Research

Vol.4, p. 133

TABLE 1 . The influence of the mucous material surrounding Chinese Alligator (A. sinensis) eggshells

during incubation.

humidity from 22-40 days, and at about

90% humidity from 41 days to hatching.

In group 2, the humidity of incubation was

maintained at 95-100% humidity from the

beginning to the end. In group 3, humidity

was maintained at 85-95% and increased to

nearly 100% all day respectively on the

10th, 30th, and 40th days of incubation.

Generally, the embryonic developmental

state was examined with lamp light at 20

day intervals. After group 3 was treated

with high humidity, examinations were

increased. Except for humidity, the rest of

the incubation conditions of the three

groups were similar, and temperature was

maintained at 31-32°C. The method of

determining the calcium and magnesium

contents in the alligator's eggshell used by

Gu et al. (1987) was adopted. The

observations on morphological change of

the alligator's eggshell in the course of

incubation was primarily in ARCCAR.

Results

The influence of mucous material around

the alligator's eggshell on incubation is

shown in table 1.

The Joanen and McNease (1977)

experiment regarding the influence of

washed and unwashed eggs in Alligator

mississippiensis on egg incubation

suggested that washed eggs had no

influence on hatching rate, but their

emergent duration was extended. Our

results on Chinese Alligator eggs show that

washed eggs have an 84.2% hatching rate,

while unwashed eggs have a 94.7%

hatching rate (with the exception of infertile

eggs). Incubation periods of washed eggs

is delayed an average of 4 days and

emergent duration is delayed an average of

5.9 hours. The experiments of groups III

and IV indicated that after the eggs were

submerged in distilled water for 8 hours,

their hatching rates, hatching time and

hatchling's emergent duration are very

much influenced. Simultaneously, such

hatchlings after emergence are weaker and

grow slower.

Eggs in group III, in which mucous

material was cleaned, have far lower

hatching rates (15.8%) than unwashed eggs

(42%) in group IV. We consider that this

phenomenon probably is related to the

mucous material around the eggshell. The

mucous material possesses functions that

protect the egg from both dehydration and

too much environmental water flowing in.

This may protect the early embryo from

being effected by bad weather.

Clearly, this is of ecologically important

significance, because female alligator's lay

their eggs in an egg cavity piled with

grasses. The initial constructed nest is

loose, with free air circulation. When it is a

fine day and temperatures are higher, water

Vol. 4, p. 134

Asiatic Herpetological Research

February 1992

rapidly evaporates easily leading to

dehydration. Conversely, during

continuous cloudy and rainy days, the rain

easily permeates loose nests into the egg

cavity and influences normal egg

development. A small opaque white patch

was observed on the top surface of the

eggshell of a freshly laid Chinese Alligator

egg. As incubation progressed, the patch

expanded in width around the shell center

and in length towards the ends of the shell.

About one day after egg laying, it expands

approximately 2/5 around the shell, 3/4

around in two days, and completely around

the shell after three days. This band slowly

extends in length, completely reaching the

ends of the shell after about one month.

Ferguson (1982) has reported a similar

change for A. mississippiensis eggshells

and suggested a variety of explanations.

One of these explanations is the

development of erosion craters that

rendered the calcite opaque, altering the

optical properties of the shell. Another is a

drying out of the eggshell due to

polarization of the watery albumin towards

the ends of the egg and an increase in

porosity of the shell. We quite agree with

his explanations. Erosion craters on the

Chinese Alligator eggshell increased with

the advance of incubation and then

progressively became cracks. Some

longitudinal cracks were observed on the

eggshell around the third week of

incubation. They became progressively

more extensive in number and diagonal

cracks appeared around the fifth week.

Eventually these cracks became more and

more extensive in size, number, and

distribution up until hatching.

In chemical analysis of the Chinese

Alligator's eggshell, calcium carbonate in

calcite form reached above 95% (Gu et al.,

1987). This is similar to A .

mississippiensis eggshells (Ferguson,

1982). During examination of Chinese

Alligator nests in the field, broken eggs

were observed in nest cavities less than 1%

of the time. Apparently, the freshly laid

egg is strong and rigid to withstand the

weight of the adult female crawling over the

closed and compacted nest. In the initial

stage of incubation, due to nest material

decay, the resulting acidic effect produces

erosion craters on the eggshell surface.

The eggshell's strength decreases, but at

that time, the frequency of the female

alligator crawling over nest tops decreases,

so the eggshell isn't damaged. Moreover,

there is better air circulation to allow more

efficient oxygen requirements during rapid

embryonic development. In addition, there

is an increase of exchange between interior

and exterior water of the egg. At that time,

the average atmospheric temperature

remains at approximately 29-30°C. It is

uncertain whether water loss from the egg

should be present or not. In order to

explore the relations between incubative

humidity and eggshell change, we made

some experiments on the hatching rate of

alligator eggs versus humidity.

As shown in table 2, group 1 had the

best efficiency, and the hatching rate was

100%. Group 2 was hatched under high

humidity throughout the incubative period.

After the inter-period of incubation, there

were 9 eggs which took in water, the

eggshell swelling, and cracking. Four eggs

were particularly swollen, and the eggshells

membrane was cracked. Nine swollen

eggs were approximately 6.13±0.29 cm in

diameter, and 4.46±0.21 cm in width.

Fifteen normal eggs, from the same

incubative period, were randomly selected

and measured 6.14±0.27 cm in diameter,

and 3.48±0.12 cm in width. Both were

similar in diameter, but the width of the

former is about one centimeter larger than

the latter.

Packard et al. (1979) reported that the

water conductance of alligator eggs is five

times higher than that of birds eggs, which

is in keeping with the porous nature of the

late alligator eggshell. Our experimental

results agree with their report. The

humidity of group 3 was 85-95%

throughout the incubation period, and only

on 10th day increased to nearly 100%.

There were no unusual phenomenon to be

observed. On the 30th and 40th day there

was one and three dead embryos

respectively. The above experiments

indicate that high humidity in the inter-

February 1992

Asiatic Herpetological Research

Vol. 4, p. 135

TABLE 2. The effect of humidity on A. sinensis egg development.

Note: Ante-period- from the beginning of incubation to 21st day; Inter-period- 22nd day of incubation to

40th day; Post-period- 41st day of incubation to hatching.

TABLE 3. The calcium and magnesium contents of Chinese Alligator (A. sinensis) eggshells.

period is adverse to embryonic

development. In ARCCAR, incubative

humidity was maintained at over 95%

(hatching rate about 90%) throughout the

incubation period before 1986. In 1987

and 1988, humidity remained at about 95%

in the ante-period and was decreased to 80-

90% during the inter- and post-period. The

hatching rate was over 95%, and hatchlings

were strong. Both survival rate and growth

state were better. In addition, according to

observations in the field which happened to

be during the rainy season in the ante-

incubation period, nest humidity remained

at more than 95%. High humidity within

the nest can prevent water loss in the

embryo.

Weather in the wild changed, with clear

days and decreasing rainfall after the third

week of incubation (inter- and post-period).

Humidity within nest cavities measured in

the field averaged about 80-85%, and the

atmospheric temperature averaged 30-3 1°C.

At that time, some longitudinal cracks

appeared on the eggshells. As incubation

proceeded, the cracks became progressively

more extensive in size and number. Then

the exchange between interior and exterior

water of eggs increased as humidity within

the nest cavity decreased. But at that time,

the corneous layer within the skin of the

alligator embryo was well developed

allowing it to depend less on the

surrounding humidity. Clearly, such

incubative humidity is adapted to the

change of the eggshell. In addition, the

cracks progressively increased in size and

number to let more and more air through

during the growth and development of the

alligator embryo. Thus, these changes of

the eggshell are not only to satisfy

developmental needs, but also to adapt to

environmental climatic conditions. The

eggshell has different functions at different

periods of embryonic development.

Jenkins (1975) estimated that embryos

of Crocodylus novaeguinae obtains

between 1.7 and 2.4 times as much calcium

from the shell as from the egg contents.

Ferguson (1982) has reported the fact that

Vol.4, p. 136

Asiatic Herpetological Research

February 1992

embryos of A. mississippiensis obtains

much less calcium from the eggshell than

either birds or turtles, indicating that it

should be possible to grow normal

alligators using shell-less culture

techniques.

Gu et al. (1987) have analyzed the

calcium and magnesium contents of

Chinese Alligator eggshells (Table 3). As

shown in table 3, calcium contents in

eggshells after hatching are similar to

infertile eggs not incubated. This indicated

that the calcium content in eggshells which

underwent incubation for about two months

did not decrease. This is greatly different

from bird embryos which obtain a large

amount of calcium from eggshells. The

experiment proved that alligator eggshells

provide very little or no calcium for

embryonic developmental. Thus, the

eggshell does not store calcium. A lot of

experiments of artificial incubation made in

ARCCAR indicate that if Chinese Alligator

eggs are damaged due to various causes, so

long as the eggshell membrane is not

breached, and temperature and humidity is

well controlled, the eggs will develop

normally; their hatching rate still reached

over 80%. But if the membrane is

punctured, microbes easily invade and the

eggs rot and stink. This suggests that the

eggshell plays an important role in

antimicrobial defense of the egg.

Acknowledgments

We are grateful for the financial

assistance provided by the Chinese Science

Foundation. We also thank Dr. Theodore

J. Papenfuss and J. Robert Macey for their

kind help in correcting this paper.

Literature Cited

CHEN, B., AND B. LIANG. 1990. Preliminary

research on the function of the eggshell of

Chinese Alligator. Pp. 242-245. In E. Zhao

(ed.) From water onto land. China Forestry

Press, Beijing. (In Chinese).

FERGUSON, M. W. J. 1982. The structure and

composition of the eggshell and embryonic

membrane of Alligator mississippiensis.

Transactions of the Zoological Society of

London 36:99-152.

GU, H., Q. XU.AND G. GU . 1987.

[Determination of the calcium and magnesium

contents of eggshell of Alligator sinensis and

discussion on relevant problems]. Acta

Herpetologica Sinica 1987-6(l):23-26. (In

Chinese).

JENKINS, N. K. 1975. Chemical composition of

the eggs of the crocodile (Crocodylus

novae guineae). Comparative Biochemistry and

Physiology 51 A: 89 1-895.

JOANEN, T, AND L. MCNEASE. 1977. Artificial

incubation of alligator eggs and post hatching

culture in controlled environmental chambers.

Proceedings 8th Annual Workshop World

Mariculture Society.

PACKARD G. C, T. L. TAIGEN, M. J. PACKARD,

AND R. D. SHUMAN. 1979. Water vapor

conductance of testudinian and crocodilian eggs.

Respiratory Physiology 38:1-10.

I February 1992"

Asiatic Herpetological Research

Vol.4, pp. 137-140|

Electrocardiogram Research on the Chinese Alligator (Alligator sinensis)

HUIQING GU1, RONGWEN RUAN1 AND ZHENG DONG ZHANG2

lHangzhou Teachers College, Hangzhou, Zhejiang, China

2Anhui Research Center for Chinese Alligator Reproduction, Xuanzhou, Anhui, China

Abstract. -This paper is a report on the determination and analysis of the electrocardiogram of the

Chinese Alligator (Alligator sinensis) under conditions of different air temperatures all year round. From

the determination and analysis mentioned above, we discovered that the electrocardiogram of the Chinese

Alligator consists of a P wave, QRS waves and a T wave.

Key words: Reptilia, Crocodilia, Alligatoridae, Alligator sinensis, China, electrocardiogram.

Introduction

The Chinese Alligator (Alligator

sinensis) is a species of crocodilian

endemic to China. In 1987, we began to

collect data about the electrocardiogram of

Chinese Alligators under conditions of

different air temperatures throughout the

year at the Anhui Research Center of

Chinese Alligator Reproduction. We hope

that these data may be applied to studies on

growth, reproduction, ecology, and

physiology of Chinese Alligators. Here is

the detailed report of the results.

Methods

The Anhui Research Center for Chinese

Alligator Reproduction supplied nine 6

year-old adult female Chinese Alligators

weighing 7.3 to 14.6 kg for the

experiments. Using a XDH-3 hot-pen

electrocardiograph made in China, we

recorded I, II, and III standard limb leads

with the standard voltage of 1 mv=10 mm at

the paper passing speed of 25 mm per

second. Laying on its back with four legs

fixed to the operating table, the

unanesthetized Chinese Alligator's

electrocardiogram was determined by

having four needle-like electrodes made by

ourselves being placed at the four points

beneath the skin which are relevant to

standard limb leads after it calmed down.

Results

1). The amplitudes of Chinese

Alligators' electrocardiogram waves are

small. Electrocardiogram waves of I

standard limb lead are so low, even the

components of it can hardly be

distinguished. Therefore the data used in

this paper are all from the determination

from the II standard limb lead.

2). The electrocardiogram of a Chinese

Alligator basically consists of a P wave,

QRS waves and a T wave (Fig. 1). Both

the P wave and the R wave are positive, the

T wave is reverse, and the QS waves are

not clear.

3). The amplitude of the Q wave, which

is made up of Pr and PI is the smallest.

The time continued, which is at an average

of about 0. 1 8 seconds, is short. The time

difference between Pr and PI is about 0.09

seconds. The crests of the P wave are

round and the rate of appearance is

moderate (Table 1). Data show that the P

wave does not appear during the

hibernating period (from the last-ten-day

period of November to the last-ten-day

period of April of the next year). The rate

of appearance is the highest from May to

June.

4). QRS waves are the main waves.

The amplitude of the R wave is the greatest

and the crests of it are pointed. The time

continued, which is at on average about

0.14 seconds, is quite short. The rate of

appearance is the highest (Table 1).

5). The amplitude of the reverse T

Vol. 4, p. 138

Asiatic Herpetological Research

February 1992

B

pvi

-if-

.-{' .

Pr-pi

,-P

'<

*r

m

L_;"

1

^

33

R

A

D

FIG. 1. The electrocardiogram of the Chinese Alligator (Alligator sinensis ) under conditions of different

temperatures as determined in 1988. A. April 8, 14° C. B. June 20. 21° C. C. Oct. 3, 16° C. D. Dec. 9,

4°C.

February 1992

Asiatic Herpetological Research Vol. 4, p. 139

TABLE 1 . Changes in the electrocardiogram of the Chinese Alligator at different temperatures.

wave, which is greater than the P wave and

smaller than the R wave, is quite great.

The time continued, which is an average

ofabout 0.31 seconds, is the longest. The

rate of appearance is the lowest (Table 1).

The T wave does not appear during

hibernation. The rate of appearance is the

highest from May to June.

6). The heart rate is influenced by air

temperature. The rate becomes faster when

the temperature goes up and slower when

the temperature goes down. We calculated

the heart rate listed in table 1 from the

formula: heart rate = 60(s)/average time

between R and R (s) (Frequency/Minute).

7). We conclude that the electrical-axis

is under normal conditions by range

estimation.

Discussion

1). Though the Chinese Alligator is a

kind of elementary cold-blooded vertebrate,

its heart is divided into two atriums and two

ventricles. Heart beating is started by the

sinus venosus, so the components of the

Chinese Alligator's electrocardiogram,

which consists of a P wave, QRS waves

and a T wave, is closely related to those of

other vertebrates.

2). The P wave is distinctly divided into

Pr and PI (r"\). The fact that there is a time

difference between the beating of the left

and the right atriums leads to this situation.

It is similar to the situation that the crests of

the P wave is level and flat in determining

the electrocardiogram of Elaphe carinata,

Elaphe taeniura and Ptyas korros. So we

conclude that the two atriums of elementary

vertebrates can not systole and diastole at

the same time as in mammals, so there is

only one P wave in electrocardiograms of

mammals, while the P wave is divided into

Pr and PI in other vertebrates.

3). QRS waves are the reflection of the

succession of several parts of the ventricle

being excited one after another. From the

fact that the rate of appearance of the R

wave is the highest, we conclude that the

ventricle is active all year round. Blood

circulation was promoted by ventricle

motion in order to maintain life even during

hibernation. During that period, with the

reduction of the Chinese Alligator's

activities and a lowered metabolization, the

amplitude of the P wave and the T wave

becomes lower, so that it can not even be

measured with an electrocardiogram.

4). More often than not, the main wave

of the QRS waves and the T wave are of

the same direction, showing that the part

being excited earlier repolarized later, while

the part being excited later repolarized

earlier. But the fact that the T wave and the

QRS waves are of different directions in the

Chinese Alligator's electrocardiogram

shows the muscle structure of its ventricles

and the pressure change inside its ventricles

when congested. This may be somewhat

different from those of mammals.

5). The Chinese Alligator is cold-

blooded, so air temperature has a great

influence on its activities and its activities

Vol. 4, p. 140

Asiatic Herpetological Research

February 1992

depend largely on the external environment.

When air temperature goes up, it becomes

nimble, its heart rate quicker and its

metabolization active; when the temperature

goes down, it becomes sluggish, its heart

rate gets slower and its metabolization

drops.

Literature Cited

RUAN, R.,R. SONG, AND Z.ZHANG. 1988. [A

tentative report on the electrocardiogram study

of Chinese Alligator]. Zoological Research

9:82-83. (In Chinese).

WEN, Y., AND M. REN. 1987. [The ABC of

Electrocardiogram]. Pp. 2-23. In Shanghai 1st

Medical College Physiology of the Human

Body. People's Publishing House of Medical

Sciences, 147 pp. (In Chinese).

BLACKFORD, L. M. 1956. The heart and

electrocardiogram of an Alligator. Circulation

14:1114-1116.

WILBER, C. G. 1960. Effect of temperature on

the heart in the alligator. American Journal of

Physiology 198(4):861-863.

February 1992

Asiatic Herpetological Research

Vol.4, pp. 141-145

Karyotypes of Two Rana from Xinjiang, China

Gang Wei1, ning xu1, Dejun Li1 and min wu2

lZunyi Medical College, Zunyi, Guizhou, China

2Xinjiang Normal University, Urumqi, Xinjiang, China

Abstract. -Karyotypes, C-bands, and Ag-NORs of Rana ridibunda (Hi River Valley, Xinjiang) and R.

altaica (Altai Mountains, Xinjiang, China) are reported. The specimens oiR. ridibunda from central Europe

have a karyotype with chromosome nos. 8 and 1 1 being both metacentric. They have a telomeric C-band

on almost every chromosome arm and a few interstitial C-bands on some chromosomes. The specimens

from the Hi River Valley have a karyotype with chromosome no. 8 being subtelocentric and no. 11

submetacentric, and no telomeric or interstitial C-bands. Chromosome polymorphism of the different

populations of the same species may explain this. We suggest that R. altaica and R. arvalis are in a middle

stage of chromosome evolution from a karyotype with 2n=26 to a karyotype with 2n=24 and chromosome

no. 6 being submetacentric.

Key words: Amphibia, Ranidae, Rana ridibunda, Rana altaica, China, Xinjiang, karyotype, C-band, Ag-

NORs, polymorphism, evolution.

Introduction

The karyotype, C-band and Ag-NORs of

Rana ridibunda from central Europe were

investigated by Schmid (1978) and the

karyotype and Ag-NORs of the same

species from Korgas, Bole and Urumqi in

Xinjiang Autonomous Region, China were

investigated by Wu (1990). In the present

study, the karyotype, C-bands and Ag

NORs of R. ridibunda were reexamined

and those of R. altaica are examined for the

first time.

Methods

The frogs used in this study are: R.

ridibunda Pallas, a male and a female from

the Hi River region in Xinjiang, China and

R. altaica Kastschenko, two males and two

females from the Altai Mountains (= Altay

Shan) region in Xinjiang. Both ends of the

femur, tibio-fibula, and humerus bones

were cut off, and the marrow cells were

washed out with 0.46 M KC1 for

chromosome preparation by a centrifugal

air-drying method. Testing of C-bands and

Ag-NORs were carried out following the

methods of Wei et al. (1990) and Xu et al.

(1990).

Results

Figure 1 depicts the karyotype, C-bands,

and Ag-NORs of R. ridibunda. For the

measurements of the karyotypes, see table

1.

The diploid number of R. ridibunda is

2n=26, which can be divided into two

groups. The large chromosome group

includes chromosome nos. 1-5, with a

relative length (R. L.) larger than 9%.

Chromosome nos. 1, 2, 4 and 5 are

metacentric and no. 3 is submetacentric.

The small chromosome group consists of

chromosome nos. 6-13, with R. L. less

than 7%. Numbers 6, 7 and 11 are

metacentric, nos. 9, 10, 12 and 13 are

submetacentric and no. 8 is subtelocentric.

The only secondary constrictions can be

readily observed on the long arms of no.

10.

With regard to C-bands, there is a

centromeric C-band on each chromosome

of R. ridibunda, but some of them are

weakly stained and no interstitial or

telomeric C-band can be observed. There

are a pair of standard Ag-NORs on the long

arms of no. 10, in the same position as the

Vol. 4, p. 142

Asiatic Herpetological Research

February 1992

.>-.<. in » u u

'y V»v£ , it »* «» M

J

1

Al II Vlf ii If

V

> .

+

\

(1 >l

1

FIG. 1 . The karyotype, C-band and Ag-NORs of Rana ridibunda.

*

». * 4

secondary constrictions.

Figure 2 depicts the karyotype, C-bands,

and Ag-NORs of R. altaica. The diploid

number of R. altaica is 2n=24, which are

compose of three groups. The large

chromosome group includes chromosome

nos. 1-5. All of them are metacentric. The

prominent secondary constrictions can be

readily observed on the long arms of no. 1,

where the standard NORs are located. The

middle sized chromosome group only

includes chromosome no. 6, with the R. L.

between 7-9%. It is also metacentric. The

February 1992

Asiatic Herpetological Research

Vol. 4, p. 143

TABLE. 1 . Chromosome measurements of R. ridlbunda and R. altaica.

small chromosome group includes

chromosome nos. 7-12. Numbers 7 and

10 are metacentric. Numbers 8, 9, 11 and

12 are submetacentric. No heteromorphic

chromosome is observed. In connection

with C-bands, there is a weakly stained

centromeric C-band on chromosome nos.

1, 2, 6, 8 and one homologous of nos. 3,

4. An obvious interstitial C-band can be

observed on lp. Some weakly stained

interstitial C-bands could also be seen on

2p, 3p, 4p, 4q, 6p and 7q, and a C block

on the long arm of one homologous of no.

9. It is noted that on the basis of C-band

and arm ratio pairing, one homologous of

chromosome no. 2 of the C-banding plate

is much shorter than the other. The R. L.

of the longer chromosome no. 2 is larger

than that of chromosome no. 1. We

suggest that translocation might have taken

place between the two homologous of

chromosome no.2.

Discussion

Rana ridibunda is distributed in central

Europe east of northwestern France, north

to the southern shore of the Baltic Sea,

south to northern Italy and the Balkans;

southwestern Asia, east to ca. 81°E latitude

in asiatic Russia and Xinjiang, China,

south to Afghanistan and Pakistan (Frost,

1985). The type locality ofR. ridibunda is

the Caspian Sea, Volga and Jaico (USSR).

The place where Schmid (1978) collected

specimens and the places where we

collected are the nearly opposite margins of

the distribution of R. ridibunda.

Comparing the results, we found that the

differences between them are as follows:

chromosome nos. 8 and 1 1 of Schmid's

result are both metacentric, but for Wu's

and our results, no. 8 is subtelocentric and

no. 11 is submetacentric. Schmid's result

indicates that a telomeric C-band is located

at the end of each arm of every

chromosome except the short arms of no. 6

and long arms of no. 12. An interstitial C-

band is on lq, 3p, 4p, 5q, 7q, 8p, 8q, and

1 1 q, but no telomeric or interstitial C-band

could be observed in our result. The

differences between them might be

polymorphism of chromosomes between

the different populations of the same

species.

Rana altaica is distributed in northern

Xinjiang (China) and southern Siberia

(Russia). The type locality of it is Altai,

USSR. It is a species of woodfrog,

belonging to the R. temporaria group. In

this group, R. temporaria is distributed

throughout Europe east to the Urals, R.

arvalis from the northeast of France to the

west of Siberia (124° E). R. chensinensis

is distributed from the Russian Far East to

Sakhalin and southern Kurile islands;

Hokkaido, Japan; Korea; eastern Mongolia;

northeastern and central China, south to

Vol. 4, p. 144

Asiatic Herpetological Research

February 1992

1

V

•t

t

-V K U n n

If (I II IA

T

ft*

** *& A|

,*

' .

#

|

! f

^

*

FIG. 2. The karyotype, C-band and Ag-NORs of Rana asiatica.

Sichuan and Hubei. R. dybowskii is

distributed from the Russian Far East;

Korea, Tsushima Island., Japan and R.

ornativentris on Honshu, Shikoku and

Kyushu islands, Japan.

Rana temporaria have a karyotype with

26 chromosomes, divided into a large

chromosome group (nos. 1-5, with R. L. >

9%) and a small chromosome group (nos.

6-13, with R. L. < 7%). However R .

arvalis, R.altaica, R. chensinensis, R.

dybowskii and R. ornativentris each have a

karyotype with 24 chromosomes, divided

into a large chromosome group (nos. 1-5),

a middle size chromosome group (no. 6

with R. L. 7-9%) and a small chromosome

group (nos. 7-12). Chromosome no. 6 of

R. arvalis and R. altaica is metacentric,

while that of R. dybowskii, R.

ornativentris and R. chensinensis is

submetacentric (Wei and Chen, 1990).

Considering that the distributional areas of

R. arvalis and R. altaica are between R.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 145

temporaria and the three other species, R.

chensinensis, R. dyhowskii and R .

ornativentris, it is suggested that the two

small chromosomes of the ancestor of/?.

temporaria merged into one middle sized,

metacentric chromosome which is

chromosome no. 6 of R. arvalis and R.

altaica. This metacentric chromosome

transformed into a submetacentric

chromosome by inversion between arms

and formed chromosome no. 6 of R .

chensinensis, R. ornativentris and R .

dybowskii.

Acknowledgments

The authors would like to express their

thanks to Prof. Ermi Zhao for encouraging

this research and allowing us to examine

the amphibian collection at the Chengdu

Institute of Biology. This research was

financially supported by the Guizhou

Scientific Committee.

Literature Cited

FROST, D. R. (ed.) 1985. Amphibian species of

the world. Allen Press and The Association of

Systematics Collections, Lawrence, Kansas.

832 pp.

SCHMID, M. 1978. Chromosome banding in

Amphibia. II. Constitutive heterochromatin

and nucleolus organizer regions in Ranidae,

Microhylidae and Rhacophoridae. Chromosoma

68:131-148.

WEI, G., AND F. CHEN. 1990. [On the

phylogenetic relationship and speciation of Rana

chensinensis]. Acta Zoologica Sinica 36(1):76-

81. (In Chinese).

WEI G., F. CHEN, AND N. XU. 1990. [An

invesugation for the karyotypic, C-banding and

Ag-NORs pattern on Rana chensinensis from

type locality]. Hereditas (Beijing) 12(l):24-26.

(In Chinese).

WU, M. 1990. Study on the karyotype and Ag-

NORs on Rana ridibunda Pallas. Hereditas

(Beijing) 12(5):15-16. (In Chinese).

XU, N., G. WEI, AND D. LI. 1990. An

investigation of the karyotype, C-band and Ag-

NORs pattern on Rana schmakeri. Hereditas

(Beijing) 12(3):22-24. (In Chinese).

I February 1992

Asiatic Herpetological Research

Vol. 4,

££.

146-157

Karyotypic Studies of Nine Species of Chinese Salamanderst

YUHUA YANG1

^Department of Bioengineering, Sichuan University, Chengdu 610041, China

Abstract. -Four species of hynobiid salamanders, from three genera, possess bimodal and asymmetrical

karyotypes with 2n=64 or 2n=68 chromosomes. Five species of salamandrids, from four genera, have

2n=24 and unimodal, symmetrical karyotypes with no microchromosomes or telocentric chromosomes.

Karyologically, Hynobiidae is the most primitive and the Salamandridae is the most advanced family in the

Caudata. The two families conform to different models of chromosome change.

Key words: Amphibia, Caudata, Hynobiidae, Salamandridae, China, karyotype.

TABLE 1 . Locality, date of collection, and number of individuals (male, female) for the 9 species used in

the karyotypic analyses.

Hynobiidae

Batrachuperus karlschmidti

B. yenyuanensis

Liua shihi

Pachyhynobius shangchengensis

Sichuan Prov., 1986

Mianning Co., Sichuan Prov., July 1986

Wushan Co., Sichuan Prov., Mar. 1986

Jinzhai Co., Anhui Prov., Apr. 1984

F

2

1

3

M

4

2

Salamandridae

Tylotolriton kweichowensis

T. verrucosus

Pachytriton labiatum

Paramesotriton chinensis

Cynops cyanurus yunnanensis

Weining Co., Guizhou Prov., Jun. 1986

Jingdong Co., Yunnan Prov., Aug. 1984

He Co., Guangxi Prov., Jun. 1986

Jingdong Co., Yunnan Prov., Aug. 1984

Introduction

There are 33 species of salamanders

known from China, including two

suborders, three families and 12 genera

(Zhao et al., 1988). Only a few of their

karyotypes have previously been reported

(Wang et al., 1983; Yang and Zhao, 1984;

Yang et al., 1986a, 1986b; Zhu and Wei,

1981). Karyotypic studies among the

Caudata (Kuro-o et al., 1987; Makino,

1932; Morescalchi, 1973, 1975;

Morescalchi et al., 1977; 1979; Schmid,

1979; Sessions et al., 1982; Seto et al.,

1986) have contributed evidence for the

phylogeny of salamanders. The present

paper reports the karyotypes of nine species

belonging to the families Hynobiidae and

Salamandridae, thereby providing

f This publication was previously published in

Chinese by Yang (1990).

additional cytogenetic data towards

understanding the phylogeny of Chinese

salamanders.

Methods

Preparation of Chromosomes

Animals used in this study were

collected from Sichuan, Yunnan, Guizhou,

Guangxi and Anhui Provinces, China from

May 1983 to June 1986 (Table 1). Mitotic

chromosomes were prepared using the

methods of Kezer and Sessions (1979)

with minor modifications. Animals were

intraperitoneally injected with 20 mg/ml of

colchicine solution about 40 to 60 hours

before sacrifice using a dosage of 0.01 ml/g

body weight. Liver and intestine were

removed, washed with 1% sodium citrate,

and sliced. Chromosome preparations

were made by air-dry and squash

techniques. Chromosomes were also

obtained using the methods of Princee and

1992 by Asiatic Herpetological Research

February 1992

Asiatic Herpetological Research

Vol. 4, p. 147

Boer (1983) and Wu (1982) with slight

modifications (Yang et al., 1986a).

Specimens were injected intraperitoneally

with PHA solution (5 mg/ml) at a dosage of

0.09 ml/g body weight, administered once

every 24 hours for three days. Twenty

four hours after the third PHA injection, the

specimens received a final injection of

colchicine (3 mg/ml) with a dosage of 30

|!g/g body weight about 14 hours before

they were sacrificed. The spleen was

removed, washed with 1% solution of

sodium citrate, ground, and put into a

hypotonic solution (0.4% KC1). A few

drops of the final cell suspensions were

used per slide, which was then placed in a

large Petri dish. Following hypotonic

treatment and fixation in the dish, the air-

dried slides were stained with 5% Giemsa

PBS (pH 6.8) for 30 minutes.

An intraperitoneal injection of colchicine

solution (3 mg/ml) was given using a

dosage of 30 (ig/g body weight for 14-24

hours before the specimens were sacrificed.

The testes were removed, rinsed with 1%

sodium citrate, ground, and put into 0.4%

KC1 solution for 1.0-1.5 hours at room

temperature. After centrifugation, the

supernatant was discarded and the

precipitate was fixed in a 3:1 solution of

methanol: acetic acid for three periods of 30

minutes each. Slides were prepared by the

air-dry method and stained with 5%

Giemsa PBS (pH 6.8) for 1 hour.

Karyotype Analysis

1. Mitotic chromosomes. —

Chromosomes were numbered and the

spreads which could be used for

karyotypes were photographed. The

karyotypes were prepared on the basis of

relative lengths and arm ratios measured

and calculated from the enlarged

photographs. The chromosomes in tailed

amphibians grade smoothly in size from the

largest to the smallest, so that it is

impossible to distinguish between the

largest microchromosomes and the smallest

macrochromosomes. No general criterion

of microchromosomes exists to date

(Morescalchi, 1973, 1975; Sessions et. al,

1982; Wang et al, 1983). In addition, the

morphology of the microchromosomes

varies with differences in the preparation

techniques and the mitotic chromosomes of

the cells analyzed. For the sake of

consistency, I have defined the

chromosomes less than 3.00% relative

length (in percentage of total haploid

length, including the microchromosomes)

as microchromosomes according to the fact

that the minimum value of relative lengths

of the smallest chromosomes in

Salamandridae, which is the most advanced

family without microchromosomes in

Caudata, is 3.00 (Table 2). The

abreviations of the chromosomes are as

follows: M-metacentric; SM-

submetacentric; ST-subtelocentric; T-

telocentric; and m-microchromosome.

2. Meiotic chromosomes. — Bivalents in

diakinesis were numbered and arranged.

The relative lengths of the bivalents were

calculated according to the principles of

ISCN (1978). The arm ratio was not

calculated due to the absence of C-band

information. The relative chiasma numbers

also were calculated (those having joined

ends were also considered to be in chiasma)

using the method presented by Imai and

Moriwaki (1982). For chromosomes in

metaphase II, the relative length and arm

ratio were measured and calculated. The

terminology for centromeric position

followed Levan et al. (1964).

Results

Hynobiidae

Batrachuperus. — B. karlschmidti

(2n=68) has 12 pairs of

macrochromosomes and 22 pairs of

microchromosomes, which is the highest

chromosome number among species of

Hynobiidae reported to date except for

Onychodactylus japonicus (2n=78; Table

3). Nos. 1-3 are metacentric and the rest

submetacentric among the

macrochromosomes (Fig. 1, Table 4).

This is a bimodal and asymmetrical

karyotype with a formula of 6M + 18ST +

44M.

B. yenyuanensis (2n = 68), consisting

Vol. 4, p. 148 Asiatic Herpetological Research February 1992

TABLE 2. Mitotic chromosome data for five species of Salamandridae.

a. Tk = Tylototriton kweichowensis, (present paper); b. Tv = T. verrocosus, (Seto et al.,1982); c. Ta = T.

andersoni, (Seto et al., 1982); d. Pb = Pachytriton brevipes, (Zhu and Wei, 1981); e. Co = Cynops

orientalis, (Zhu and Wei, 1981).

of 1 1 pairs of macrochromosomes and 23 + 16ST + 46m.

pairs of microchromosomes. Among the

macrochromosomes, nos. 1-2 are Liua. — L. shihi (2n = 64). The

metacentric, no. 4 is submetacentric, and karyotype consists of 1 1 pairs of

the rest are subtelocentric (Fig. 1, Table 4). macrochromosomes and 21 pairs of

The karyotype is bimodal and microchromosomes, nos. 1-3 being

asymmetrical, with a formula of 4M + 2SM metacentric, no. 7 submetacentric and the

February 1992

Asiatic Herpetological Research

Vol. 4, p. 149

TABLE 3. Chromosome data of some species in Hynobiidae.

rest telocentric among the

macrochromosomes (Fig. 1, Table 4). The

karyotype is bimodal and asymmetrical,

with a formula of 6M + 2SM + 4ST + 10T

+ 42M.

Pachyhynobius. — P. shangchengensis

(= Xenobius melanonychus), (2n = 64).

There are 12 pairs of macrochromosomes

and 20 pairs of microchromosomes.

Numbers 1 and 5 are metacentric, no. 2 is

subtelocentric, and the rest of the

macrochromosomes are telocentric (Fig. 1,

Table 4). This is a bimodal and

asymmetrical karyotype with a formula of

4M + 2ST+ 18T + 40M.

Salamandridae

Tylototriton. — T . kweichowensis

(2n=24) has 8 pairs of metacentric (nos. 1-

5, 7, 9-10), 3 pairs of submetacentric (nos.

6, 8 and 11) and 1 pair of subtelocentric

chromosomes (no. 12), without

microchromosomes (Fig. 2, Table 2). This

is a unimodal and symmetrical karyotype.

Twelve chromosomes in metaphase II and

twelve bivalents in diakinesis were seen on

the meiotic preparations (n=12). The

relative lengths of chromosomes in

metaphase II are larger than those of

chromosomes in mitotic metaphase (Tables

2 and 5). Both nos. 11 and 12

chromosomes in metaphase II are

submetacentric, the arm ratios being 1.7

and 2.6 respectively, while no. 11 is

submetacentric and no. 12 is subtelocentric

for the chromosomes in mitotic metaphase,

the arm ratios being 2.6 and 3.6

respectively. The differences might show

the different degree of chromosome

contraction during meiosis and mitosis

(Figs. 2, Tables 2 and 5). The relative

lengths and relative chiasma number of the

bivalents are larger than those of

chromosomes in mitotic and less than those

of chromosomes in metaphase II. The

relationship of chiasma numbers and

lengths of the bivalents in not a straight

line, for instance, the relative lengths of

Vol. 4, p. 150

Asiatic Herpetological Research

February 1992

HKKllMii

f 4 |* M " " ••

ft* #4 41 ** *• *• **

mm «• •* ** •• •» at ♦•

1 _

)f ^ >* H i<

li &* i<5 *• «• h*>

«• 4* ** M •• •• •»

** •• M M •« •» •• *a

•• *• •• •• mtt •• •• ••

2

*r« ii it ■ m

II II M •• •• ••

• § AA mm mm mmm» mm

«M •«■> •••» •«• •»-«

►• •«

FIG. 1. Karyotypes of four species of hynobiid salamanders. 1) Batrachuperus karlschmidti,!) B.

yenyuanensis, 3) Liua shihi, 4) Pachyhynobius shangchengensis.

nos. 1 and 12 are 12.47 and 5.41, while

their relative chiasma numbers are 7.96 and

8.47 respectively.

T. verrucosus (2n = 24). The haploid

chromosome number is 12. Accordingly,

the diploid chromosome number expected

is 24, which is consistent with those of T.

andersoni and T. verrucosus from different

localities (Ferrier and Beetschen, 1973;

Morescalchi, 1973; Seto et al, 1986). The

relative lengths of chromosomes in

metaphase II are larger than those of

bivalents in diakinesis (Tables 5 and 6).

The chromosomes in metaphase II are

metacentric except nos. 6, 8 and 12 of

submetacentric chromosomes and there are

no microchromosomes. The karyotype is

unimodal and symmetric. 2). The relative

chiasma numbers are not proportional to

relative lengths, for example, the relative

lengths are 9.36 and 5.25 respectively

(Table 6).

Pachytriton. — P. labiatum (2n = 24).

There are 12 bivalents in diakinetic cells

(n=12). Accordingly, the diploid

chromosome number should be 24 (Fig.

2), in accord with that of P. brevies (Zhu

and Wei, 1981). The relative chiasma

numbers of nos. 1-6 bivalents vary

basically with their relative lengths, while

the relative chiasma numbers of nos. 7-12

are more constant (Table 6).

Cynops. — C. cyanurus yunnanensis

(2n=24). There are 12 bivalents in

diakinetic cells and 12 chromosomes in

metaphase II cells (Fig. 2). Consequently,

the 2n should be 24. The chromosomes in

metaphase II are metacentric except no. 8

(SM), without microchromosomes (Fig.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 151

TABLE 4. Macrochromosome data for four species of Hynobiidae.

a. Ps=Pachyhynobius shangchengensis; b. Ls=Liua shihi;

c. Bk=Batrachuperus karlschmidti; d. By=B. yenyuanensis

2). This is a unimodal and symmetrical

karyotype, which is in accord with those of

other species in the same genus (Zhu and

Wei, 1981). The relative chiasma numbers

do not vary with the relative lengths, for

instance, the relative lengths of nos. 2 and

5 are 11.30 and 9.42, but their relative

chiasma numbers are 9.14 and 9.63

respectively.

Paramesotriton. — P. chinensis (2n=24).

Twelve bivalents were seen in the diakinetic

cells. The diploid number of 24 (Fig. 2) is

the same as that of P. hongkongensis

(Morescalchi, 1975). The relative lengths

and the relative chiasma numbers are

Vol. 4, p. 152

Asiatic Herpetological Research

February 1992

(tiiiiutiu ^X«w 00 f }»*

1 2 3

JU&AX* W0*» |*WI

^Knkka ?•«*•• »!«♦••

FIG. 2. Karyotypes of five species of salamandrid salamanders. 1-3) Tylototriton kweichowensis, mitotic

chromosomes (1), chromosomes in metaphase II (2), and meiotic bivalents (3). 4, 5) T. verrucosus,

chromosomes in metaphase II (4), and meiotic bivalents (5). 6) Meiotic bivalents of Pachytriton labiatum.

7, 8) Cynops cyanurus yunnanensis, chromosomes in metaphase II (7), and meiotic bivalents (8). 9)

Meiotic bivalents of Paramesotriton chinensis.

shown in table 6. The relationship of

chiasma numbers and the lengths of the

bivalents is not a straight line, for example,

the relative lengths of the nos. 2 and 12 are

11.89 and 3.55 respectively, while their

relative chiasma numbers are the same,

8.10.

Discussion

It has been suggested from karyotypic

data that Hynobiidae is the most primitive

group of salamanders, while Salamandridae

is the most advanced group in Caudata

(Morescalchi, 1973, 1975; Morescalchi et

al., 1979). The same conclusion is derived

from morphological comparisons (Zhao

and Hu, 1984). There are some differences

in the evolutionary ways of the two groups.

Karyotypic Evolution in Hynobiidae

The bimodal (with macrochromosomes

and microchromosomes) and asymmetrical

(with metacentric and telocentric

chromosomes) karyotype is considered to

be primitive (Morescalchi, 1975) in

reference to the karyotypic evolution in

Caudata. Among some species of

Hynobiidae, the diploid numbers are 40-66

and their karyotypes are bimodal and

asymmetrical except for Hynobius

retardatus [=Satobius retardatus (Adler and

Zhao, 1990)], (Table 3). The karyotypes

of the four species (in three genera) I

studied here are all bimodal and

asymmetrical, with 2n=64 or 68

chromosomes. Batrachuperus is one of 2

hynobiid genera in China that are aquatic

for their entire lives and different from

other genera morphologically. The diploid

number of B. karlschmidti and B.

yenyuanensis is 68, the second highest

number among species of Caudata studied

so far (Table 3). Onychodactylus is more

derived and allied with Ranodon and

February 1992

Asiatic Herpetological Research

Vol.4, p. 153

TABLE 5. Metaphase II chromosome data for 3 species of Salamandridae.

Batrachuperus (Zhao and Hu, 1984), in

accordance with the fact that O.fischeri has

2n>66 chromosomes (Sessions et al.,

1982) and O. japonicus has 2n=78

(Yamamoto, 1982). The diploid number of

B. musteri (Morescalchi et al., 1979), B.

pinchonii and B. tibetanus (Yang and Zhao,

1984) is all 62, distinctly different from

those of B. karlschmidti and B .

yenyuanensis. Both B. karlschmidti and

B. yenyanensis have 2n=68 chromosomes,

but differ in chromosome component and

morphology (Tables 3 and 4). The former

has one more macrochromosome pair and

one less microchromosome pair than the

latter. In addition, the latter has one pair of

subtelocentric chromosomes, while the

former has none. It is obvious that the

karyotypic evolution in Batrachuperus is

more complex.

Pachyhynobius shangchengensis, which

Vol. 4, p. 154

Asiatic Herpetological Research

February 1992

TABLE 6. Bivalent data for 5 species of Salamandridae.

a. Tv = Tylototriton verrucosus; b. Tk = T. kweichowensis; c. Pc = Paramesotriton chinensis; d. PI

Pachytroton labiatum; e. Ccy = Cynops cyanurus yunnansis.

is a genus and species of Hynobiidae

described on morphological characteristics

(Fei and Ye, 1983), has 2n=64. The

karyotype differs from those of other

species in Hynobiidae, providing the

cytogenetic evidence for establishing the

new genus and species.

Liua is a genus established by Zhao and

Hu (1983), based on morphological

characteristics. Liua shihii, which is the

only species, has 2n=64, the same as P.

shangchengensis. However, there are

some differences between them in

chromosome component and morphology.

Liua shihii has 11 pairs of

macrochromosomes, including 3 pairs of

metacentric, 1 pair of submetacentric, 2

pairs of subtelocentric, and 5 pairs of

telocentric chromosomes, while P.

shangchengensis has 12 pairs of

macrochromosomes, consisting of 2 pairs

of metacentric, 1 pair of subtelocentric and

9 pairs of telocentric chromosomes (Fig. 1

and Table 4).

The predominant mode of karyotypic

evolution in Caudata is that the unimodal

symmetrical karyotypes with low

chromosome number are derived from the

bimodal and asymmetrical karyotypes with

high chromosome number, through

Robertsonian centric fusions and pericentric

inversions (Morescalchi, 1975).

Robertsonian centric fusions, which could

occur between telocentric

macrochromosomes, between stable

microchromosomes, and between

telocentric macrochromosomes and stable

microchromosomes, reduce the diploid

number and/or the microchromosome

number and increase the metacentric

chromosomes. Consequently, the

karyotypes tend toward stability.

February 1992

Asiatic Herpetological Research

Vol. 4, p. 155

Pericentric inversions do not change the

diploid number, but could increase the

number of metacentric chromosomes and

the stability of karyotypes.

B. karlschmidti and B. yenyuanensis

possess 22 and 23 pairs of

microchromosomes respectively and lack

telocentric macrochromosomes.

Contrastingly, P. shangchengensis and L.

shihii have 21 and 20 pairs of

microchromosomes and 5 and 9 pairs of

telocentric macrochromosomes. It is

concluded that the karyotypic evolution of

the 4 species above has involved

Robertsonian centric fusion as well as

pericentric inversion. However, the

phylogeny of the 4 species could not be

established based on the present data. It is

necessary to have information from

chromosome banding and biochemistry in

order to define the structures and functions

of microchromosomes and telocentric

chromosomes.

Karyotypic Evolution in Salamandridae

The 5 salamandrid species studied here

all have 2n=24 chromosomes, lack

microchromosomes, and possess unimodal

and symmetrical karyotypes (Fig. 2, Tables

2 and 5) as consistent (Ferrier and

Beetschen, 1973; Seto et al., 1986; Zhu

and Wei, 1981). Morescalchi (1975)

suggested that all species studied possess

similar karyotypes that differ very little

even at the intergeneric level. The

differences between these karyotypes

predominantly concern the absolute size of

chromosomes and quantity of DNA.

Accordingly, the karyotypic diversity

among the species has chiefly resulted from

pericentric inversions that result in

differences between individual

chromosomes by changing the telocentric

chromosomes into metacentric ones, or

changing the metacentric chromosomes into

submetacentric, subtelocentric and

telocentric chromosomes. The difference,

which occured not only at the intergeneric

level, but also at the intrageneric level, are

as follows: 1. The data of chromosomes

in mitotic metaphase: as shown in table 2,

the no. 12 chromosomes of 3 species in

Tylototriton are all subtelocentric, while the

karyotypes of C. orientalis and P. brevipes

have no subtelocentric chromosomes, only

metacentric and submetacentric

chromosomes. In addition, the

chromosome differences in morphology

were seen among 3 species in Tylototriton,

4 pairs of submetacentric chromosomes in

T. andersoni, 3 pairs in T. kweichowensis

and 2 pairs in T. verrucosus. 2. The data

of chromosomes in meiotic metaphase II

(Table 5): C. cyanurus yunnanensis has

only 1 pair of submetacentric

chromosomes, while there are 4 pairs in

both T. verrucosus and T. kweichowensis.

Numbers 6, 7, 8, and 12 are

submetacentric chromosomes in T.

verrucosus and nos. 6, 8, 11, and 12 in T.

kweichowensis. 3. The data of bivalents

in diakinesis (Table 6): the relative lengths

of no. 1 bivalents of T. verrucosus and T.

kweichowensis are similar, 12.49 and

12.47 respectively, but 13.27, 12.62 and

11.92 in P. chinensis, P. labiatum and C

cyanurus yunnanensis individually. The

relative chiasma numbers of no. 1 bivalents

reveal the intergeneric and intrageneric

variations. It is noteworthy that the

interspecific and intraspecific variations of

individual bivalents on relative chiasma

number in 2 species of Tylototriton are

more distinctive than those in other genera

and species. The relative chiasma numbers

are apparently not directly proportional to

the relative lengths.

Tylototriton has karyotypically been

considered to be the most primitive genus

in Salamandridae, based on the fact that

there are more subtelocentric chromosomes

in mitotic metaphase, more submetacentric

chromosomes in meiotic metaphase II, and

more variations of relative chiasma

numbers in diakinesis. The same

conclusion was reached based on

morphological comparisons (Zhao and Hu,

1984). However, as shown in table 2, T.

andersoni has 2 more submetacentric

chromosomes pairs (nos. 10-11) than T.

kweichowensis and 1 more submetacentric

chromosomes pair (no. 10) than T.

verrucosus. The relative length of

chromosome no. 1 is largest and the

relative length of no. 12 is the shortest in T.

Vol. 4, p. 156

Asiatic Herpetological Research

February 1992

andersoni among the 3 species above.

These data could provide cytogenetic

evidence for reestablishing Echinototriton.

The mitotic chromosome number and

morphology of C. orientalis are the same as

those of P. brevipes, but the color, size and

distribution of C-bands are different from

each other. Consequently, the authors

proposed that the differences of

heterochromatic components and

distributions on chromosomes of different

genera could be the block of interspecific

fertilization (Zhu and Wei, 1981).

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I February 1992 Asiatic Herpetological Research Vol. 4, pp. 158-161 1

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Copeia 1974(4):9 12-917.

Journal article, title translated, article not in English.

Ananjeva, N. B. 1986. [On the validity of Megalochilus mystaceus (Pallas, 1776)]. Proceedings

of the Zoological Institute, Leningrad 157:4-13. (In Russian).

Note that for Acta Herpetologica Sinica, the year must precede the volume number. This

is to distinguish between the old and new series, and between 1982-1987, Vols. 1-6 (new

series) and 1988 with no volume number, numbers 1 and 2 (new series).

Cai, M., J. Zhang, and D. Lin. 1985. [Preliminary observation on the embryonic development of

Hynobius chinensis Guenther]. Acta Herpetologica Sinica 1985, 4(2):177-180. (In Chinese).

Book.

Pratt, A. E. 1892. To the snows of Tibet through China. Longmans, Green, and Co., London.

268 pp.

Article in book.

Huey, R. B. 1982. Temperature, physiology, and the ecology of reptiles. Pp. 25-91. In C. Gans

and F. H. Pough (eds.), Biology of the Reptilia, Vol. 12, Physiological Ecology. Academic

Press, New York.

Government publication.

United States Environmental Data Service. 1968. Climatic Atlas of the United States.

Environmental Data Service, Washington, D. C.

Abstract of oral presentation

Arnold, S. J. 1982. Are scale counts used in snake systematics heritable? SSAR/HL Annual

Meeting. Raleigh, North Carolina. [Abstr].

Thesis or dissertation.

Moody, S. 1980. Phylogenetic and historical biogeographical relationships of the genera in the

Agamidae (Reptilia: Lacertilia). Ph.D. Thesis. University of Michigan. 373 pp.

Anonymous, undated.

Anonymous. Undated. Turpan brochure. Promotion Department of the National Tourism

Administration of the People's Republic of China, China Travel and Tourism Press, Turpan,

Xinjiang Uygur Autonomous Region, China.

February 1992 Asiatic Herpetological Research Vol. 4, p. 161

Xinjiang Uygur Autonomous Region, China.

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FIG. 2. Lateral view of live Psammodynasles pulverulentus holding a prey lizard (Anolis

carolinensis ). Note buccal tissue surrounding the enlarged anterior maxillary and dentary teeth of the

snake.

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February 1992 Asiatic Herpetological Research Vol. 4, p. 162

ANNOUNCEMENTS

ll Meeting 1992. — The Asiatic Herpetological Research Society

ociety for the Study of Amphibians and Reptiles (CSSAR), the

d Reptile Specialist Group of Species Survival Committee of

on Herpetological Society (of the former USSR), and the

r the Study and Conservation of Amphibians (ISSCA), including

i-0 1 Conference on Oriental Amphibians will hold a joint meeting in

qq rom 15 July to 20 July. Members of these societies and others are

eting. A number of general topics will be covered in the fields of

on on, herpetological studies of various Asian regions, venomous

d captive reproduction. Registration information is available from

China: Dr. Huang Jie-tang, Qimen Institute of Snakebites,

o^ ;, China. Independent Republics of the Commonwealth of

S Dr. Ilya Darevsky, Zoological Institute, Russian Academy of

a, „ Russia. In the USA and all other countries: Dr. Theodore J.

■4^ ' Vertebrate Zoology, University of California, Berkeley, CA

P3

<tT ngress of Herpetology. — The Second World Congress of

£ d at the University of Adelaide, South Australia, Australia from

c i January 6, 1994. Information is now available concerning

q* fore and after the meeting. For information contact: Secretariat,

; of Herpetology, Dept. of Zoology, University of Adelaide, GPO

5 , Australia.

CD

a

to

o

<

v:

5' ;ty of the Commonwealth of Independent States. — The HSCIS

?d Herpetological Society) has opened its membership to all

V >rmation contact: Dr. Tatyana M. Sokolova, Zoological Institute,

*> lences, St. Petersburg, Russia.

o

-a

3

o

=r

n

3

ya S. Pp. 1-12. Holotype of Dibamus greeri (ZIN 20011) from

u-Contum Province, Vietnam. Chen, Yuancong, Dawei Zhang,

ghui Wang. Pp. 58-61. Agkistrodon strauchii from 3150 m, sand

of Waqen (33° 03' N 102° 37' E), Aba (Ngawa) Zangzu

, Sichuan Province, China. Photo by J. Robert Macey. Semenov,

3orkin. Pp. 99-112. Teratoscincus przewalskii from Dunhuang

I (40° 10' N 94° 50' E), Jiuquan Prefecture, Gansu Province,

Lrana. ivuzmin, ocrgms L. Pp. 123-131. Mertensiella caucasica from 10 km SSE of

Borzhomi (41° 51' N 43° 23' E), Georgia. Photo by J. Robert Macey.

February 1992 Asiatic Herpetological Research Vol. 4, p. 162

ANNOUNCEMENTS

Asian Herpetological Meeting 1992. — The Asiatic Herpetological Research Society

(AHRS), the Chinese Society for the Study of Amphibians and Reptiles (CSSAR), the

Chinese Amphibian and Reptile Specialist Group of Species Survival Committee of

I.U.C.N., the All Union Herpetological Society (of the former USSR), and the

International Society for the Study and Conservation of Amphibians (ISSCA), including

the Second International Conference on Oriental Amphibians will hold a joint meeting in

Anhui Province, China from 15 July to 20 July. Members of these societies and others are

invited to attend the meeting. A number of general topics will be covered in the fields of

biology and conservation, herpetological studies of various Asian regions, venomous

snakes and snakebite, and captive reproduction. Registration information is available from

the following: Within China: Dr. Huang Jie-tang, Qimen Institute of Snakebites,

Qimen, Anhui Province, China. Independent Republics of the Commonwealth of

Independent States: Dr. Ilya Darevsky, Zoological Institute, Russian Academy of

Sciences, St. Petersburg, Russia. In the USA and all other countries: Dr. Theodore J.

Papenfuss, Museum of Vertebrate Zoology, University of California, Berkeley, CA

94720, USA.

Second World Congress of Herpetology. — The Second World Congress of

Herpetology will be held at the University of Adelaide, South Australia, Australia from

December 29, 1993 to January 6, 1994. Information is now available concerning

registration and tours before and after the meeting. For information contact: Secretariat,

Second World Congress of Herpetology, Dept. of Zoology, University of Adelaide, GPO

Box 498, Adelaide 5001, Australia.

Herpetological Society of the Commonwealth of Independent States. — The HSCIS

(formerly the USSR Herpetological Society) has opened its membership to all

herpetologists. For information contact: Dr. Tatyana M. Sokolova, Zoological Institute,

Russian Academy of Sciences, St. Petersburg, Russia.

PLATE 1.— Darevsky, Ilya S. Pp. 1-12. Holotype of Dibamus greeri (ZIN 20011) from

850 m, Kontarang, Gilai-Contum Province, Vietnam. Chen, Yuancong, Dawei Zhang,

Kexian Jiang, and Zhonghui Wang. Pp. 58-61. Agkistrodon strauchii from 3150 m, sand

dunes, 7.0 km north of Waqen (33° 03' N 102° 37' E), Aba (Ngawa) Zangzu

Autonomous Prefecture, Sichuan Province, China. Photo by J. Robert Macey. Semenov,

Dimitri V., and Leo J. Borkin. Pp. 99-112. Teratoscincus przewalskii from Dunhuang

Sand Dunes, Dunhuang (40° 10' N 94° 50' E), Jiuquan Prefecture, Gansu Province,

China. Kuzmin, Sergius L. Pp. 123-131. Mertensiella caucasica from 10 km SSE of

Borzhomi (41° 51' N 43° 23' E), Georgia. Photo by J. Robert Macey.

siatic Herpetological Research

Plate 1

ibamus green

arevsky

Agkistrodon strauchii

Chen, Zhang, Jiang, and Wang

iratoscincus przewalskii

smenov and Borkin

Mertensiella caucasica

Kuzmin

The Asiatic Herpetological Research

Society (AHRS)

&

The Chinese Society for the Study of

Amphibians and Reptiles (CSS AR)

Invite You to the

Asian

Herpetological

Meeting

huangshan clty, anhui province, china

15 to 20 July, 1992

ISSN 1051-3825

CONTENTS

DAREVSKY, ILYA S. Two New Species of the Worm-like Lizard Dibamus (Sauna,

Dibamidae), with Remarks on the Distribution and Ecology of Dibamus in Vietnam... 1

DAREVSKY, ILYA S., AND NIKOLAI L. ORLOV. A New Subspecies of the Dwarf Snake

Calamaria lowi ingermarxi ssp. nov. (Serpentes, Colubridae) from Southern

Vietnam 13

WEN, YETANG. A New Species of the Genus Tropidophorus (Reptilia: Lacertilia) from

Guangxi Zhuang Autonomous Region, China 18

BAUER, AARON M., AND RAINER GUNTHER. A Preliminary Report on the Reptile Fauna

of the Kingdom of Bhutan with the Description of a New Species of Scincid Lizard

(Reptilia: Scincidae) 23

ADLER, KRAIG, ERMI ZHAO, AND ILYA S. DAREVSKY. First Records of the Pipe Snake

(Cylindrophis) in China 37

ORLOV, NIKOLAI L., AND BORIS S. TUNIYEV. A New Species of Grass Snake, Natrix

megalocephala, from the Caucasus (Ophidia: Colubridae) 42

DAS, INDRANEIL. Cyrtodactylus madarensis Sharma (1980), a junior synonym of

Eublepharis macularius Blyth (1854) 55

CONANT, ROGER. The Type Locality of Agkistrodon halys caraganus 57

Chen, yuancong, dawei Zhang, Kexian Jiang, and Zhonghui Wang. Evaluation

of Snake Venoms among Agkistrodon Species in China 58

Huang, meihua, yumin Cao, fengxue zhu, and yunfang Qu. Female

Reproductive Cycle and Embryonic Development of the Chinese Mamushi

(Agkistrodon blomhoffii brevicaudus) 62

HERRMANN, HANS-JOACHIM, AND KLAUS KABISCH. Investigations on Ranid Larvae in

Southern Sakhalin Island, Russia 68

ANANJEVA, NATALIA B., AND BORIS S. TUNIYEV. Historical Biogeography of the

Phrynocephalus Species of the USSR 76

SEMENOV, Dimitri V., AND LEO J. BORKIN. On the Ecology of Przewalsky's Gecko

(Teratoscincus przewalskii) in the Transaltai Gobi, Mongolia 99

ORLOVA, VALENTINA F. Intrapopulational and Geographic Variation of Eremias

przewalskii Strauch in Mongolia 113

KUZMIN, SERGIUS L. Feeding Ecology of the Caucasian Salamander (Mertensiella

caucasica), with Comments on Life History 123

CHEN, BIHUI, AND BAODONG LIANG. Preliminary Research on the Function of the

Eggshell in the Chinese Alligator (Alligator sinensis) 132

Gu, HUIQING, RONGWEN RUAN, AND ZHENGDONG ZHANG. Electrocardiogram Research

on the Chinese Alligator (Alligator sinensis) 137

WEI, GANG, NING XU, DEJUN LI, AND MIN WU. Karyotypes of Two Rana from

Xinjiang, China 141

YANG, YUHUA. Karyotypic Studies of Nine Species of Chinese Salamanders 146

Guidelines for manuscript preparation and Submission 158

announcements 162

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