HARVARD UNIVERSITY

Ernst Mayr Library

of the Museum of

Comparative Zoology

I

Volume 8 • 1999

Editor

Ermi Zhao

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

Associate Editors

Kellar Autumn

Lewis & Clark College, Portland, Oregon. USA

J. Robert Macev

Department of Biology. Washington University. St. Louis.

Missouri, 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

Aaron Bauer

Villanova University, Villanova, Pennsylvania. USA

Christopher Bell

University of Texas. Austin, Texas. USA

Leo Borkin

Zoological Inslilule. St. Petersburg. Russia

Bihui Chen

Anhui Normal University, Wuhu. Anhui. China

I i Cheng

Inslilule oi Marine Biology. National Taiwan Ocean University,

Keeking. Taiwan. China

Ilya Darevsky

Zoological Institute, St. Petersburg, Russia

Indraneil Das

Madras Crocodile Bank. Vadanemmeli Peiur. Madras. India

William E. Duellman

University of Kansas. Lawrence, Kansas. USA

Hajime Fukada

Sennyuji Sannaicho, Higashiyamaku, Kyoto. Japan

Carl Cans

University of Michigan. Ann Arbor. Michigan. USA

Robert F. Inger

Field Museum. Chicago, Illinois, USA

Xiang Ji

Hang/hou Normal College. Hangzhou. Zhejiang, China

Pi-peng Li

Yantai Normal College, Yanlai. Shandong. China

Ronald Marlou

I niversitj oi Nevada, Las Vegas. Nevada, I S \

Robert W. Murphy

Royal Ontario Museum. Toronto, Ontario. Canada

(.nun Nilson

University of Goteborg, Goteborg, Sweden

Nikolai Orlov

Zoological Institute, Si Petersburg, Russia

Hidetoshi Ota

Department oi Biology, University of the Ryukyus. Nishihara.

Okinawa, Japan

James F. Parham

University of California, Berkeley. California. USA

Soheila Shafii

University ol Shahid Bahonar, Kerman, Iran

Hai-tao Shi

Hainan Normal University, Haikou, Hainan. China

\iu-ling Wang

Xinjiang Normal University, Urumqi, Xinjiang. China

Yue-zhao Wang

Chengdu Institute of Biology. Academia Sinica, Chengdu.

Sichuan. China

Yehudah Werner

Hebrew University, Jerusalem. Israel

Ken-tang Zhao

Suzhou Railway Teacher's College. Suzhou. Jiungsu China

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

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

editors encourage authors from all countries to submit articles concerning hut not limited to Asian herpetology. All correspon-

dence outside of China and requests for subscription should be sent to AHR. Museum of Vertebrate Zoology. University of

California. Berkeley. California, USA 94720. or by email to asiaherp@uclink.berkeley.edu. All correspondence within Chi-

na should be sent to Ermi Zhao. Editor, Chengdu Institute of Biology, P.O. Box 416. Chengdu, Sichuan Province. China. Au-

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Asiatic Herpetological Research Volume 8 succeeds Volume 7 published in 1997. Vol. 6 published in 1995. Vol. 5 published

in 1993, Vol. 4 published in 1992. Vol. 3 published in 1990 and Chinese Herpetological Research Vol. 2. which was pub-

lished 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 1 987. 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: Cuora galbinifrons. Diaoluoshan, 18 km N. of Nanxi. Hainan Province, China. Photo by James F. Parham.

1999

Asiatic Herpetological Research

Vol. 8, pp. 1-6

The Activity and Thermal Biology of the Fossorial Reptile, Diplometopon

zarudnyi (Amphisbaenia: Trogonophiidae) in Central Saudi Arabia

AWADH M. AL-JOHANY

Department of Zoology, College of Science, King Saud University, P.O.Box 2455, Riyadh II 45 1, Saudi Arabia.

Abstract .- The nocturnal activity of the fossorial amphisbaenid Diplometopon zarudnyi was studied in the field

and its thermal selection and tolerance were determined in the laboratory. During the study period (summer) the

animals commenced activity at 20.00 hrs (ground temperature 30-32°C) and finish their foraging between 3.00 to

4.00 hrs (ground temperature 28-26°C) before the break of dawn. The mean activity temperature determined in

the field was 31.5°C, which was usually 0.5 to 1°C higher than the ground temperature. The mean selected body

temperatures in a gradient during day and night were 26.4°C (range 15-38°C) and 26.3°C (range 14-38°C)

respectively. The Critical Thermal Maximum was 47.6°C and the Critical Thermal Minimum was 7°C. D.

zarudnyi tolerates a wide range of temperatures while maintaining its mean body temperature within a narrow

range. The role of Selected Body Temperature is discussed in relation to metabolism.

Key words.- Amphisbaenia, Trogonophiidae, fossorial reptile, Diplometopon zarudnyi, Saudi Arabia, Central

Arabia, activity, thermal preference, thermal tolerance.

Introduction

The amphishaenian family Trogonophiidae is repre-

sented in central Arabia by the single species Diplom-

etopon zarudnyi ( Al-Sadoon, 1988). The range of this

species extends to northern Arabia and the coastal

Arabian Gulf (Arnold, 1986). D. zarudnyi is an oscil-

lating digger, commonly found burrowing in low sand

dunes in open terrain and in sub-surface soils of date

palm farms. This amphisbaenian is a nocturnal for-

ager, sometimes occupying ant and termite tunnels.

In this study the nocturnal activity of D. zarudnyi

was studied in the field, and its thermal selection and

temperature tolerance were determined in the labora-

tory. A comparison of results of this study has been

made with the results of other species from different

geographical habitats.

Material and Methods

Several field trips were made during the summer sea-

son (July- August.) to habitats of D. zarudnyi located

around Riyadh city (Thummama and Dilam). Noctur-

nal activity of the animals was observed during the

activity period. Rechargeable fluorescent lanterns

were employed to illuminate the area being studied.

When tracks appeared on the sand surface, they were

followed up to the location of the animal, which was

either dug out of its subsurface position by hand or

using a small hand shovel. Soil temperature (Ts), air

temperature (Ta) and cloacal body temperature (Tb)

were taken within 15 seconds of capture by a quick

reading cloacal thermometer (Millar and Weber Co.,

Figure 2. Setup used to measure the selected body

temperature: (1) Telethermometer, (2) Thermal gradi-

ent, (3) Thermostat heater, (4) Cooling coil in water

bath, (5) Refrigerant machine, (6) 10 cm thick sand

layer, (7) 100 W heating bulb, (8) Thermistor probe.

U.S. A). Air and ground temperature were also moni-

tored every hour from dusk to dawn.

Thirty D. zarudnyi (adult animals of both sexes)

were used in the laboratory study (mean mass = 7.63

g, SD ± 2.54; mean SVL=182 mm, SD ± 13.4; mean

VTL=14 mm, SD ± 2.0). They were collected from

various locations around Riyadh city. They were

maintained for short periods in Plexiglass boxes filled

with 10 cm of clean sand. The sand was sprinkled

periodically with water. Mealworms and water were

available ad lib. The laboratory temperature was 23 ±

1.5°C.

The Selected Body Temperature (SBT) of ten

amphisbaenians was determined in a metal thermal

Vol. 8, p.

Asiatic Herpetological Research

1999

Figure 2. Method employed to tie the thermistor; the

probe (1) inserted inside the animal's cloaca and

looped to be held on the tail (2) with bands of adhesive

tape.

gradient which measured 200 x 25 x 40 cm (Fig.l).

Sand was spread evenly to a depth of 10 cm on the

base of the gradient. A temperature gradient from 10-

50°C was achieved by fitting a thermostatic hot plate

below one end and by placing an insulated ice con-

tainer constantly frozen by an immersion refrigerant

coil on the other end. The surface sand at the cool end

was sprinkled with water intermittently to prevent

desiccation. The gradient was illuminated by two 100

watt bulbs suspended 80 cm from the surface of the

sand controlled by an electronic timer to maintain the

photoperiod. The animals were left in the gradient for

one day prior to the start of the experiment for accli-

mation.

The cloacal body temperature (Tb) was monitored

with high sensitivity probes (Model 511; Yellow

Springs Inc.). The probes were connected to a multi-

channel YSI Telethermometer, and an Omniscribe

Houston Instruments continuous chart recorder. The

flexible tip of the pre-calibrated probe was inserted for

1 cm into the cloaca and held in place with 3-4 mm

bands of adhesive tape (Fig. 2). The probes remained

in place even when the animal burrowed below the

sand. Twenty four hour continuous recording of Tb

was obtained for three days on each animal and one

measurement for each hour was recorded.

These instruments were also used to measure the

Critical Thermal Maximum (CTMax) and the Critical

Thermal Minimum (CTMin). CTMax is the arith-

metic mean of the collective thermal points at which

locomotor activity becomes disorganized and the ani-

mal loses its ability to escape from conditions that

will promptly lead to its death. CTMin is the low tem-

perature that produces cold narcosis and prevents

locomotion (Pough and Gans, 1982). A sheet metal

box (25 X 20 cm) filled with a layer of sand and kept

above a thermostat heater was employed to measure

CTMax. For CTMin, a Plexiglass box (25 X 15 cm)

with a layer of sand held inside a larger insulated box

surrounded by ice cubes was employed. Twenty dif-

ferent animals ( 10 for each category) were used. Each

animal was gradually heated or cooled inside the

experimental chambers ( 1 °C increase or decrease per

minute). The probe remained inserted in the cloaca

and the body temperature was monitored continu-

ously while the test chamber sand was gradually

heated or cooled.

To determine the CTMax and CTMin, the amphis-

baenian was observed until the animal lost its righting

response when it was turned on its back. During the

CTMin experiments, after initial cooling (9.5°C), the

animal lost its ability to right itself but, after its belly

was touched by a fine paint brush, the animal exhib-

ited a wave of convulsions down the body. Further

cooling led to total loss of all responses, and the tem-

perature at which this occurred was designated as the

CTMin. All but one experimental animal survived

after returning to room temperature. After 10 days, the

animals which were used for CTMax experiments

were used to measure CTMin. The CTMin of these

animals was compared to that of the first group.

Statistical analysis was performed using GLM

procedure of Minitab package (version 8.2). Two-way

analysis of variance (ANOVA) with interaction

(unbalanced) was used for data analysis (P=<0.05).

Results

The nocturnal activity of the animals is clearly defined

during summer nights. Emergence for foraging activ-

ity begins at 22.00 hrs when the air temperature is 30-

32 °C and the ground temperature is 32-34°C. The

foraging activity subsides between 03.00 to 04.00 hrs

when the air temperature is 28-26°C and the ground

temperature is 27-25°C. After this the animals move

deeper into the sand surface (presumably to their bur-

rows or refuges) and no kind of activity is observed

during the daylight hours.

The animals were active between adjacently

located shrubby small sand dunes. Most of these sand

dunes hosted colonies of ant and termite mounds.

Movement is typically a combination of sub-surface

and surface locomotion. Undisturbed movement of

the animal over the surface of the sand was observed

only two instances. On the rest of the occasions the

animals were tracked by their impressions in the sand.

The animals move just below the surface of the sand

for two or three meters by piercing and wiggling by

strong head and body movement (probably in search

of termites). After that they come out on the surface

and effortlessly glide on the sand surface for several

meters by fast subsequent spring action. This was

done by making an VS' shape of the body and flicking

forward. Consequently this kind of activity leaves a

distinct pattern of tracks on the sand surface which

1999

Asiatic Herpetological Research

Vol. 8. p. 3

35 0-i

32.5

30.0

E

i

E

a

m 27.5

250

r= 0.6648

P=0.0132

n=13

27

— i —

28

29

30

31

32

33

34

35.0

O

32.5

300

■- 27.5-

25.04

r=06588

P=0.0143

n=13

B

27

28

29

31

33

34

Body Temperature 'C

Figure 3. A. Relationship between body temperature

(Tb) and soil temperature (Ts). B. Relationship

between body temperature (Tb) and air temperature

(Ta). (The regression line, significance value and sam-

ple size are as indicated).

can be easily differentiated between the tracks of

other animals of the habitat.

The mean field body temperature for the active

animals captured was 31.5°C (range 29.5 - 32.5°C;

n=13). Regression analysis showed a significant dif-

ference between the T\, - Ta and T^, - Ts (P<0.05; Fig.

3). The mean selected temperatures in the gradient

during the day and night were 26.4°C (SD ± 5.2) and

26.3 °C (SD ± 5.7) respectively; the temperatures

selected during day ranged between 15 and 38°C and

between 14 and 38°C during the night (Fig.4). About

ninety percent of D. zarudnyi selected temperatures

between 23 and 36°C during the day and between 21

and 36 C during the night. Temperature selected did

not differ significantly between day and night

(F=0. 14, P=0.705). However, individuals differed sig-

nificantly in temperatures selected (F=l 27.37,

P=0.001 ). Also, there was a highly significant interac-

tion between individuals and the time of day (F=7.72,

P=0.001 ). The average hourly temperature pattern of

D. zarudnyi showed a gradual increase of body tem-

perature (in the gradient) and reached its highest level

just before the end of the dark period (Fig. 5), and a

s

I

0

M

%-

C

16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38

Temperature "C

Figure 4. Representation of body temperature selec-

tion (%) by Diplometopon zarudnyi in the thermal gra-

dient during day and night periods.

gradual decrease of body temperature to its lowest

value by the end of the light period.

During the CTMax trials, animals below the soil

surface emerged when the sand temperature reached

40°C. The CTMax was 47.6°C. During the CTMin

trials, the animals lost the righting reflex at 9.4°C

(SD±1) and CTMin was 7°C (SD±0.6). The second

group of animals used in measuring CTMin lost the

righting reflex at 11.3°C (SD±1.1) and CTMin was

reached at 9.5°C (SD±0.5).

Discussion

D. zarudnyi come out of their refuges at night when

the air temperature and the soil surface temperature

are favorable. By employing two kinds of locomotion

the task of foraging is accomplished. They expend

vigorous efforts on their foraging activity, since they

have to accomplish it in a short duration: multiple

tracks crossing each other were observed for a single

animal in a wide area, giving a false impression of

many animals being active. This lead to many dead

ends while following the leads of the tracks.

Previous reports (gradient studies) assumed that

the body temperatures of amphisbaenians are equal to

soil temperatures, since readings were obtained from

the soil surrounding the animals. For a more accurate

evaluation, here, we recorded body temperatures

direct and continuously in the thermal gradient.

The selected mean temperature in the gradient

(26°C) measured in this study explains the Metabolic

rate-Temperature curve (M-T curve) reported for D.

zarudnyi; in which both the adults (mean wt.6.34 g)

and sub-adults (mean wt.3.15 g) showed stable Ot

consumption rates between 25-30°C (Al-Sadoon,

1986).

Vol. 8, p. 4

Asiatic Herpetological Research

1999

28.0

27.5

27.0

a

I 26.5

26.0

255

25.0

24 5

24.0

O

Q.

E

«

n=10

_i — i — i — 1_

18 h

24 h

6h

12h

18 h

Time

Figure 5. Mean selected body temperature pattern of Diplometopon zarudnyi in the thermal gradient during 24

hours. Numbers at each point indicate the SEM.

The body temperature for active D. zarudnyi are

higher in the field than in the laboratory because the

animals were deprived of food during the experiment,

and also may be the result of confinement to a limited

space in the gradient. Van Berkum (1980) demon-

strated that the SBT is lower in lizards with decreased

food consumption. It is recommended to measure

metabolism during the post absorptive state of diges-

tion, so as to minimize any contribution of specific

dynamic action (Eckert and Randall, 1983).

As D. zarudnyi is fossorial, the low mean selected

temperature (26°C) could extend activity and stabilize

body metabolism in the sub-surface habitat. The

present results supplement the previous published

reports of lower temperature selection in amphisbae-

nians. Avery (1982) noted that many fossorial snakes,

amphisbaenians, sea snakes, fresh water and marine

turtles, appear not to thermoregulate and that many

select low temperatures. Evidence of thermoregula-

tion in Amphisbaena mertensi was reported by Abe

(1984); mean field body temperature and preferred

temperature in the gradient was 21.1°C and 21.4°C

respectively. Also, Martin et. al. (1990) reported

marked field thermoregulation in Blanus cinereus and

it selected low field body temperatures. Gatten and

McClung ( 1981 ) reported the low mean body temper-

ature for Trogonophis weigmanni in a range of 21.7°C

to 23.4°C. A field study of Bipes biporus demon-

strated that this worm lizard can thermoregulate if

necessary, by vertical and horizontal changes in sub-

strate positioning (Papenfuss, 1982). More recently,

Diaz-Paniagua et al., (1995) during a field study of

seasonal and diel activity of Blanus cinereus, reported

an activity range of ground temperatures between

13.4 -27.8°C which is low and as well clearly indi-

cates thermoregulation.

The low temperature selection of D. zarudnyi is

also in line with the observations made on other bur-

rowing species of reptiles. Bury and Bolgooyen

(1976) determined the thermal preferendum of the

legless burrowing lizard Anniella pulchra to be 24-

25°C. Clark ( 1968) reported five subterranean species

of small snakes to select lower temperatures than sur-

face dwelling species. Burrowing snakes of the family

Uropeltidae also appear to select a low body tempera-

tures between 18°C and 20°C (Gans,1973). Low

selected body temperatures were also reported for

Anguis fragilis (Gregory, 1980).

A previous study showed that D. zarudnyi had no

endogenous circadian rhythm and no periodicity in

alternating light and darkness although it was more

active at high temperatures (Cloudsley-Thompson,

1979). The finding in the present study wherein

Diplometopon showed no significant difference

between day and night time temperature selection is

consistent with the lack of an endogenous circadian

rhythm in temperatures selected in day and night.

However, in the present results there is a highly sig-

nificant difference among individuals. This is proba-

bly due to individual differences in body weight,

health status, age and sex of the animals tested.

In the gradient D. zarudnyi elevated its body tem-

perature slightly in the second half of the night, a time

when they were seen to forage actively in the field. In

contrast, T. wiegmanni tested in a thermal gradient

showed elevated temperatures in the afternoon and

early evening (Gatten and McClung, 1981). Foraging

activity at dawn and in early morning also is reported

1999

Asiatic Herpetological Research

Vol. 8, p. 5

for Agamodon anguliceps from Somalia; the animals

were located in the top 2-3 inches of the soil at dawn,

appearing to have moved upwards during the night.

As temperatures rose, most animals disappeared from

the top 6-12 inches of the ground (Gans and Pandit.

1965).

The CTMax value for Diplometopon is similar to

that of certain terrestrial lizards of Central Arabia, but

the CTMin was higher than that reported for most

other sympatric lizards (Al-Johany, 1986). The rela-

tively high CTMin might be related to the subterra-

nean temperatures encountered by Diplometopon

which seldom fall below freezing, unlike the surface

temperatures which may drop below 0 °C. The 2.5 °C

increase in the CTMin for animals that had experi-

enced the CTMax might be attributed to a short-time

heat-hardening effect (see Maness and Hutchison,

1980).

Prior to this study there was no data available on

the held thermal ecology of D. zarudnyi. By the com-

bined result of the field and laboratory study it is now

confirmed that the animal is a thigmotherm but not in

its strict sense. Since it was observed that the animal

manages (probably by metabolic activity) to keep its

body temperature a degree or half higher than the

ground temperature.

Acknowledgments

I am thankful to Dr.Carl Gans, Department of Biol-

ogy, University of Michigan, for helpful comments

and to Dr.Roger Avery, University of Bristol, for

meticulous reading of the manuscript. Thanks are also

due to Mr. Mohammed Yousuf for help in field work,

technical assistance in the laboratory and typing of the

manuscript.

Literature Cited

Abe, A. S. 1984. Experimental and field record of pre-

ferred temperature in the neotropical amphisbaenid

Amphisbaena mertensi Stauch (Reptilia, Amphis-

baenidae). Comparative Biochemistry and Physiology

77A: 251-253.

Al-Johany, A. M. H. 1986. Ecology and reproductive

biology of Acanthodactylus schmiditi in Central Ara-

bia. Ph.D.Thesis. University of Southampton. U.K.

pp.

Al-Sadoon, M. K. 1986. Influence of a broad tempera-

ture range on the oxygen consumption rates of three

desert lizard species. Comparative Biochemistry and

Physiology 84A: 339-344.

Al-Sadoon. M. K. 1988. Survey of the reptilian fauna

of the Kingdom of Saudi Arabia II. The lizard and

amphisbaenian fauna of Riyadh province. Bulletin

ofMaryland Herpetological Society 24: 58-76.

Arnold, E. N. 1986. A key and annonated check list to

the lizards and Amphisbaenians of Arabia. Fauna of

Saudi Arabia. 8: 385-432.

Avery, R. A. 1982. Field studies of body temperature

and thermoregulation. Pp 93-166. In: C.Gans and

F.H.Pough (eds), Biology of the Reptilia Vol 12, Aca-

demic Press, London.

Bury, R. B. and T.G. Bolgooyen. 1976. Temperature

selectivity in the legless lizard, Anniella pulchra.

Copeia 1976: 152-155.

Clark, D. R. Jr. 1968. Experiments into selection of

soil type, soil moisture level and temperature by five

species of small snakes. Transactions of Kansas Acad-

emy of Sciences 70: 490-496.

Cloudsley -Thompson, J.L. 1979. Water loss and loco-

motory activity in Agarna persica and Diplometopon

zarudnyi from Kuwait. Journal of Arid Environments

2: 273-277.

Diaz-Paniagua, C, M.C. Blazquez, C. Keller, A.C.

Andreu.G. Olmedo and J. A. Mateo. 1995. Observa-

tions on seasonal and dial surface activity of the

amphisbaenian Blanus cinereus in south-western

Spain. Herpetological Journal Vol.5: 217-220.

Eckert, R., and D. Randall. 1983. Animal Physiology,

Mechanisms and Adaptations, 2nd Edition, W.H.

Freeman & Co., New York.

Gans, C. 1973. Uropeltid snakes - survivors in a

changing world. Endeavor. 32: 60-65.

Gans, C. and H.M. Pandit. 1965. Notes on a herpeto-

logical collection from Somali republic V. The

amphisbaenian genus Agamodon Peters. Ann. in 8

Zool., R.G. Mus. Afr. Cent. 134: 71-86.

Gatten, R. E. Jr. and R.M. McClung. 1981. Thermal

selection by an amphisbaenian Trogonophis wieg-

manni. Journal of Thermal Biology 6: 49-51.

Gregory, P. T. 1980. Physical factor selectivity in the

fossorial lizard Anguis fragilis. Journal of Herpetol-

ogy 14: 95-99.

Maness, J.D. and V.H. Hutchison. 1980. Acute adjust-

ment of thermal tolerance in vertebrate ectotherms

following exposure to critical thermal maxima. Jour-

nal of Thermal Biology 5: 225-233.

Martin. J., P. Lopez and A. Salvador. 1990. Field body

temperatures of the amphisbaenid lizard Blanus

cinereus. Amphibia-Reptilia 1 1 : 87-96.

Vol. 8, p. 6 Asiatic Herpetological Research 1999

Papenfuss, T.J. 1982. The ecology and systematics of

the amphisbaenian genus Bipes. Occational Paper,

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moregulation. Vol. 1. Academic Press, New York.

van Berkum, F.H. 1980. The significance of preferred

body temperature of lizards. American Zoologist 20:

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1999

Asiatic Herpetological Research

Vol. 8, pp. 7-12

Description of a New Species of Pseudorabdion (Serpentes: Colubridae) from

Panay Island, Philippines with a Revised Key to the Genus

Rafe M. Brown1'2, Alan E. Leviton3, and Rogelio V. Sison4

Section of Integrative Biology and Texas Memorial Museum, University of Texas, Austin, Texas, 78712

(rafe@mail.utexas.edu); "Geier Collections and Research Center, Museum of Natural History and Science,

Cincinnati Museum Center. 1720 Gilbert Avenue, Cincinnati, OH 45202-1401: •Department of Herpetology,

California Academy of Sciences, San Francisco, CA 941 18 (leviton® sfsu.edu); 4 Zoology Department, Natiotud

Museum of the Philippines, Executive House, P. Burgos Street, Manila, Philippines (nmuseum@webciuest.com).

Abstract.- We describe a new species of snake in the colubrid genus Pseudorabdion from the western coastal

mountain range of Panay island, Philippines. The new species appears to be related to the members of the P.

mcnamarae species group (P. mcnamarae and P. taylori from the Philippines, P. albonuchalis, and P.

saravacensis from Borneo, and P. sarasinorum from Sulawesi) but differs from each of these species by

characters of scalation and color pattern. The new species is one of several other recently-discovered vertebrates

from Panay island. Together, these discoveries suggest that diversity and endemism patterns of the Negros-Panay

Pleistocene aggregate island platform (Negros, Panay, Cebu and Masbate islands) are more complex and

interesting than previously thought.

Introduction

While engaged in a biological reconnaissance survey

of the western coastal mountain range of Panay Island

(Fig. 1 ), the senior author collected two specimens of

what appeared at the time to be Pseudorabdion

mcnamarae, a species already well know from Negros

Island. On closer examination it was discovered that

the Panay specimens differed in significant details

from the Negros population while sharing features

with P. taylori, known from Mindanao, and with P.

albonuchalis, a species earlier known only from the

type specimen (but see Inger and Leviton, 1966),

which can no longer be located, and said to have come

from Sarawak, Borneo. The observed differences

among these related species leads us to believe that

the Panay specimens represent a previously unrecog-

nized, taxonomically distinct population of Pseudo-

rabdion allied to the section of the genus

Pseudorabdion whose members possess an elongate

loreal (lori-ocular) that borders the orbit anteriorly.

Pseudorabdion

cies (Figs. 2-3)

talonuran new spe-

Holotype: PNM 2712 (Field no. PNM/CMNH 671),

adult male, collected on western foothills of Mt.

Madja-as ( 1 1°23' N, 122°09' E; elev. 1500 m), Baran-

gay Allojipan, Municipality of Culasi, Antique Prov-

ince, Panay Island, Philippines, 28 May 1992 by Rafe

Brown and Roger Sison.

Paratype: CMNH 5076 (Field no. PNM/CMNH

670), young male, other data as for holotype except it

was collected at 1410 m.

Etymology: The specific epithet is chosen from the

Antique Province dialect Caray-a, and is derived from

the words, "talon" (forest) and "uran" (rain), in refer-

ence to the high elevation rain forest habitat where the

new species was collected on Mt. Madja-as.

Diagnosis: Elongate loreal (=Iori-ocular) present,

extending from the posterior border of the nasal to the

orbit of the eye; ventrals (M) 139-146; subcaudals

(M) 36-39; total of ventrals plus subcaudals (M) 175-

185; scales of dorsum each edged with a mottling of

brown pigment, the posterior and central portions of

each scale pale, lacking a dense infusion of dark pig-

ment, the lateral and latero-ventral scales with larger

pale areas than those on the dorsum; no distinct

nuchal collar but pattern of pale centers and dark rims

characterizes nuchal scales and head shields, which

are somewhat mottled dark and light.

Pseudorabdion talonuran belongs to the section of the

genus Pseudorabdion characterized by the presence

of a loreal (lori- ocular) shield. From the allied Philip-

pine P. mcnamarae, it differs in lacking a pale nuchal

color in adults and in having more than 30 subcaudals

in both males and females; from P. taylori it differs in

having the centers and apical tips of the dorsal scales

nearly pigmentless whereas in P. taylori the centers

are pale brown, and in having the hemipenes minutely

This paper represents contribution number 23 to the results of the National Museum of the Philippines/

Cincinnati Museum of Natural History Philippine Biodiversity Inventors- (PNM/CMNH PB1)

Vol. 8, p. 8

Asiatic Herpetological Research

1999

spinose (in P. taylori the apical tips are calyculate).

Among the non-Philippine species having a lori-ocu-

lar, P. talonuran differs from P. sarasinorum in having

the anterior chin shields in contact with the mental,

from P. albonuchalis in having fewer subcaudals (36-

39 vs. 43) and the frontal not border the eye, and from

P. saravacensis in having a greater number of subcau-

dals (36-39 vs. fewer than 30) and fewer maxillary

teeth (8 vs. 14). From the remaining species in the

genus, it differs in having an elongate loreal (lori-ocu-

lar) shield that borders the eye.

Description of holotype: (Adult male) Rostral as

high as wide, portion visible from above slightly

greater than length of internasal suture; internasals

small, greatest length about one-half greatest length of

prefrontals, in contact with rostral, nasal, loreal and

prefrontal: common suture between prefrontals about

four-fifths length of frontal: prefrontal bordering eye

between loreal and supraocular, also in contact with

internasals; left prefrontal in contact with both inter-

nasals (because internasal suture offset from midline):

frontal two-thirds length of parietals, subtriangular,

three-fourths as wide as long, in contact with prefron-

tals, supraocular and parietals, but not bordering eye;

supraocular distinct, not fused to ocular brill; maxi-

mum length of parietals slightly greater than distance

to tip of snout; nasal quadrangular, undivided, resting

on first and in contact with second supralabials, nostril

pierced in anterior lower quadrant; loreal elongate,

resting on second and third supralabials. about twice

as long as its distance to tip of snout, bordering eye;

preocular absent (or more likely fused to form an

elongate loreal [lori-ocular]); postocular, subquadran-

gular, about one half size of supraocular, in contact

with fourth and fifth supralabials, not as high as eye,

its lower border extending below level of eye and

inserting between two supralabials; eye small, its

diameter equal to its distance from mouth, pupil

round; five supralabials and one large postsupralabial,

supralabials three and four border eye, fifth largest

and broadly in contact with parietals, followed by

third, second, fourth, and first in descending order of

-12

-11°

40 km

Borneo '

^'■"121° 124°

] 0-150

] 150-400

400-800

800-1200

1200-1600

>1600

Fig. 1 . Map of Panay Island, showing its position in the Philippines (inset), major cities (darkened circles), provinces

(dashed lines; names underlined) and elevational topography (see key). The type locality (Mt. Madja-as) of Pseu-

dorabdion talonuran is indicated with a star.

1999

Asiatic Herpetological Research

Vol. 8, p. 9

Fig. 2. Dorsal (A) and lateral (B) views of head of holo-

type of Pseudorabdion talonuran.

size; one large "posterior temporal" between postla-

bial and parietal; mental in contact with elongate ante-

rior chin shields; infralabials five, first three in contact

with anterior chin shields, third and fourth bordering

posterior chin shields; posterior chin shields about

three-fourths length of anterior pair, separated from

one another in the midline for two-thirds their length

by insertion of a gular scale, and about same size as

bordering gular scales; maxillary teeth eight.

Scales smooth, without apical pits, in 15 longitu-

dinal rows, not reducing posteriorly before vent; ven-

trals 146 mm; subcaudals 39 mm, paired; anal

undivided.

Hemipenes extend in situ to 8th subcaudal plate,

forked at the level of the 6th plate; apical ends with

minute spines.

Total length 265 mm; tail 46 mm; head length (tip

of snout to angle of jaws) 1 1.25 mm, (tip of snout to

posterior edge of parietals) 9.1 mm; diameter of eye

0.8 mm.

Color pattern (in alcohol): Dorsal scales each with

irregular dark borders; apical end and centers pale,

nearly pigmentless, pigmentless areas larger and more

distinct laterally; ventrals unpigmented except for lat-

eral edges; no nuchal collar.

Paratype: The paratype, a young male, differs from

the holotype in the following particulars: ventrals 139;

subcaudals 36; snout-vent length, 265 mm; tail length

47 mm; apical ends of hemipenes do not appear to be

spinose (but the everted organ is poorly preserved and

difficult to examine).

Ecological notes: The forest habitat of the new spe-

cies on Mt. Madja-as (Fig. 4) has been classified by

Whitmore (1984) as the transition zone between

mixed dipterocarp (submontane) and mossy (upper

montane) forests. The forest consists of two strata, a

canopy of 10 m and subcanopy of 3-4 m with emer-

gent trees as high as 18 m; an herb and shrub layer

vegetation was also present. The forest near the col-

lection site was mossy and contained high densities of

epiphytic ferns and orchids. The topography was

qualitatively characterized as steep, with numerous

sheer rocky valleys and forest-covered ridges (see

Ferner, et al., 1997 for more details.) Both holotype

and paratype were found beneath logs.

Remarks: The section of the genus Pseudorabdion

characterized by the presence of an elongate loreal

(lori-ocular) that borders the orbit, termed here the

"mcnamarae" section, includes three species in the

Philippines, P. mcnamarae, P. taylori, and P. talonu-

ran, and three non-Philippine species, P. albonuchalis

and P. saravacensis from Sarawak, and P. sarasi-

norwn from Gunung (Volcano) Soudara, Sulawesi.

Five species (P. longiceps, P. ater, P. oxycephalum,

P. eiselti, and P. montcmum) lack the loreal (lori-ocu-

lar); the prefrontals are in contact with the second and

third upper labials. Of the forms lacking a distinct

Fig. 3. Dorsal view of holotype (PNM 2712) of Pseudorabdion talonuran.

Vol. 8, p. 10

Asiatic Herpetological Research

1999

Fig. 4.Cloud forest habitat of Pseudorabdion talonuran at the type locality: Mt. Madja-as, Antique Province, Panay

Island, Philippines.

loreal (or if a small scale is present in the loreal posi- that its high elevation montane regions warrant more

tion, a rare occurrence among this group, it is neither intensive biodiversity survey efforts in the near future.

elongate nor does it border the orbit), P. oxycephalum,

P. ater, and P montanum are confined to the Philip- Key tO the Species of Pseudorabdion

pines, f! me/ft is known only from the type locality at

Padang, Sumatra, and P. longipes has been collected (Modified from Inger and Leviton, 1966)

at many localities on the islands of Borneo, Sulawesi, ia Lori-ocular (loreal) shield absent (if present, does

Nias, and Sumatra, from Singapore and elsewhere not border orbit); prefrontal in contact with upper

north along the Malay Peninsula, from the Riau labials 2

(Riou) Archipelago, and as far north as Ban Gnara and ^ Lori.ocular shidd presem very distincti elongate,

Patani, in southern Thailand. borders orbit; preftontal not in contact WIth upper

The presence of this new, endemic species of labials 7

snake in the coastal mountains of western Panay ^ Preocular present; supraocular present; internasal

island further bolsters our suspicion that the level ot ^ fa ^^ ^ upper labia,s; maxillary teeth , , .

endemism on Panay is greater than previously p longipes

thought. By virtue of the fact that Panay was intermit-

tently connected to Negros and Cebu at various points 2b. Preocular absent; supraocular present or absent;

during the Pleistocene (Heaney, 1986), biogeogra- internasals almost always in contact with upper labial^

phers have justifiably expected that these islands to

possess a high percentage of faunal elements in com- 3a. Supraocular absent; frontal borders orbit; nasal

mon (Leviton. 1963; Brown and Alcala, 1970). Never- divided; maxillary teeth 10 or more 4

theless, recent discoveries of other vertebrates 3^ Supraocular present; frontal does not border orbit;

endemic to Panay (Gonzales and Kennedy, 1990, nasa] undivided; maxillary teeth 10 or less 5

1996; Brown et al.. 1997; Ferner et al., 1997) suggest ^ Postocular absent; masmsay teeth 10 P. ater

1999

Asiatic Herpetological Research

Vol. 8, p. 1 1

4b. Poslocular present; maxillary teeth 22-25

P. collaris

5a. Postocular not fused to supraocular: ventrals 130;

suhcaudals 12 P. eiselti

5b. Postocular and supraocular fused; ventrals greater

than 140; suhcaudals greater than 15 6

6a. Each scale of outer row with dark centers and pale

borders; ventrals uniformly dark brown except for

extreme posterior outer edges which are pale; ocular

shield usually fused to combined supra- and postocu-

lars; suhcaudals (M) 22-24, (F) 16- 17

P. oxycephalum

6b. Each scale of outer row with pale centers: ventrals

whitish with dark brown more or less confined to a

broad median band; ocular shield not fused to com-

bined supra- and postoculars; suhcaudals (M) 28; (F)

21-24 P. montanum

7a. Anterior chin shields not in contact with mental:

nasal shield divided P. sarasinorum

7b. Anterior chin shields in contact with mental; nasal

shield not divided 8

8a. Maxillary teeth greater than 15 9

8b. Maxillary teeth fewer than 10 10

9a. Ventrals greater than 125; suhcaudals greater than

40 P. albonuchalis

9b. Ventrals fewer than 120; suhcaudals fewer than 30

P. saravacensis

10a. Pale nuchal collar usually present; suhcaudals

1 7-30; distal portion of hemipenes minutely spinose

P. menamarae

10b. Pale nuchal collar absent in adults; suhcaudals

greater than 30 11

I la. Dorsal scales uniform pale brown, each scale

thinly edged with pigmentless border; distal portion

of hemipenes calyculate P. taylori

1 lb. Dorsal scales with pale, nearly pigmentless cen-

ters and apical tips, anterior borders of each scale with

brown mottling, larger areas of latero-ventral scales

devoid of dark pigment; hemipenes minutely spinose

P. talonuran

Acknowledgments

We thank The Protected Areas and Wildlife Bureau

(PAWB) of the Philippines Department of the Envi-

ronment and Natural Resources (DENR) for facilitat-

ing collecting and export permits necessary for the

field work that contributed to this study. For logistical

assistance in the Philippines, we thank Corazon Cati-

bog-Sinha (DENR), A. Alcala (Silliman University),

P. Gonzales (PNM), R. Kennedy (CMNH) and the

provincial DENR authorities of Antique Province.

For the loans of specimens, we thank the follow-

ing individuals and their respective institutions

(museum acronyms, with the exception of CMNH.

follow Leviton et al., 1985): J. Vindum and R. Drewes

(CAS), R. Kennedy and J. Ferner (CMNH), and P.

Gonzales (PNM). Financial support for RMB's travel

to CAS was provided by the C. Stearns Fellowship of

the California Academy of Sciences. We thank J. Bar-

celona (PNM) for assistance with the Caray-a deriva-

tion of the new species name.

Support for RMB's field work was provided by the

Society for the Study of Amphibians and Reptiles, the

Roschman Student Enrichment fund of the College of

Arts and Sciences, and the Zoology and Botany

Departments of Miami University (Oxford, Ohio).

The PNM/CMNH PBI was supported by a grant (to R.

Kennedy and P. Gonzales) from the John D and

Catherine T. MacArthur Foundation and by the bene-

factors of Cincinnati Museum of Natural History.

We thank D. Cannatella and A. Diesmos for com-

ments on earlier drafts of this manuscript.

Literature Cited

Brown, W. C. and A. C. Alcala. 1970. The zoogeogra-

phy of the Philippine Islands, a fringing archipelago.

Proc. California Acad. Sci. 38:105-130.

Brown, W. C, R. M. Brown, and A. C. Alcala. 1997.

Species of the hazelae group of Platymantis

(Amphibia: Ranidae) from the Philippines, with

descriptions of two new species. Proc. California

Acad. Sci. 49:405-421, Figs. 1-4.

Ferner, J. W., R. M. Brown, and A. E. Greer. 1997. A

new genus and species of moist closed canopy forest

skinks from the Philippines. Jour. Herpetol. 31:187-

192, Figs. 1-3.

Gonzales, PC. and R.S. Kennedy. 1990. A new spe-

cies of Stachyris babbler ( Aves: Timaliidae). from the

island of Panay, Philippines. Wilson Bull. 102: 367-

379.

Gonzales, PC. and R.S. Kennedy. 1996. A new spe-

cies of Crateromys (Rodentia: Muridae) from Panay,

Philippines. J. Mamm. 77:25-40.

Heaney, L. R. 1986. Biogeography of small mammals

in SE Asia: estimates of rates of colonization, extinc-

tion and speciation. Biol. Jour. Linnaen Soc, London

28:127-165, Figs. 1-8.

Inger, R. F, and A. E. Leviton. 1961. A new colubrid

snake of the genus Pseudorabdion from Sumatra.

Fieldiana: Zoology 44:45-47, Fig. 1.

Vol. 8, p. 12

Asiatic Herpetological Research

1999

Inger, R. F., and A. E. Leviton. 1966. The taxonomic

status of Bornean snakes of the genus Pseudorabdion

Jan and of the nominal genus Idiopholis Mocquard.

Proc. California Acad. Sci., 34:307-314, Figs. 1-3.

Leviton, A. E., and W. C. Brown. 1959. A review of

the genus Pseudorabdion with remarks on the status

of the genera Agrophis and Typhlogeophis (Serpentes:

Colubridae). Proc. California Acad. Sci., 29:475-508,

Figs. 1-10.

Leviton, A. E. 1963. Remarks on the zoogeography of

Philippine terrestrial snakes. Proc. California Acad.

Sci. 31:369-416, Fig. 1.

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

Dawson. 1985. Standards in herpetology and ichthy-

ology: Part I. Standard symbolic code for institutional

resource collections in herpetology and ichthyology.

Copeia 1985: 802-832.

Appendix 1. Specimens Examined

In addition to specimens listed in earlier publications

by Leviton and Brown ( 1959) and by Inger and Levi-

ton (1961 and 1966), the following new materials

have been examined:

Pseudorabdion mcnamarae: Philippine Islands:

Negros Island: Negros Occidental Prov.: CAS 185577

- Panakiyo, 22 km E Isabela, 16 April 1960 by Q. and

L. Alcala. Negros Oriental Prov.: CAS 186052 - Cuer-

nos de Negros. 3600-3800 ft., 24 December 1959 by

Q. Alcala and R. Empeso.

P. talonuran: See Holotype and Paratype sections for

this species.

P. albonuchalis: Malaysia: Sarawak (Fourth Divi-

sion): CAS 101500 - Niah, Tangap, 6 December 1960

by T. Harrison.

P. oxyeephalum Philippine Islands: Panay Island:

Aklan Prov.: CAS 137643 - Nabas, Laserna Barrio, 12

May 1973 by L. Alcala. Negros Island: Negros Occi-

dental Prov.: CAS 185453-185457 - Hinoba-an Town,

barrios Alim and Asia, 9-10 June 1967 by L. Alcala

and party: Barrio Asia, 30 May-3 June 1967 by A.

Alcala, L. Pelingon and F Pelingon. Negros Oriental

Prov.: CAS 1 10974 - Camp Lookout. Valencia, 14

June 1967 by L. and F. Pelingon: 24-25 km NW of

Bondo [about 10 km N of Siaton], 27-31 December

1958 by A. Alcala and party.

1999

Asiatic Herpetological Research

Vol. 8, pp. 13-17

Anguis melanostictus Schneider, 1801, a Valid Species of Barkudia

(Sauria: Scincidae) from Southeastern India

INDRANEIL DAS

Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300, Kota

Samarahan, Sarawak, East Malaysia

Abstract.- Anguis melanostictus Schneider, 180I, based on a watercolor in Russell (1796), from the Coromandel

coast of India, is shown to be a species of Barkudia, nonconspecific with B. insularis Annandale, 1917, and is

revived. B. melanosticta, is compared with the holotype and other specimens of B. insularis from Orissa State,

and shown to be larger (SVL 161.0-164.9 mm, vs. 107.0-143.0 mm), in addition to differing in the following

characteristics: palatal teeth present (vs. absent); anterior lobe of tongue distinctly narrowed (vs. not

differentiated); and lobules around ear opening absent (vs. present). A neotype of Barkudia melanosticta

(Schneider, 1801) is designated, based on an adult female from Visakhapatnam, Andhra Pradesh State,

southeastern India (ZSI 20627).

Key words.- Sauria, Scincidae, Anguis melanostictus,

designation, Andhra Pradesh, southeastern India

Barkudia insularis, Barkudia melanosticta, neotype

Introduction

Patrick Russell (1726-1805), perhaps the lirst Western

herpetologist in India, a medical doctor by training,

was posted as naturalist by the British East India

Company at Vizagapatam (at present Visakhapatnam,

Andhra Pradesh, southeastern India). Russell is best

known for a two volume folio of watercolors of

snakes, published in 1796 and 1801-1802 (finished

between 1807-1810; see Adler, 1989; Zhao and Adler,

1993), that concentrated on the fauna of the region.

Russell's books are unique in that he used local ver-

naculars of the species illustrated, but not their scien-

tific or English names, and several leading

herpetologists of the time have named new species on

the basis of the watercolors in Russell. Accounts of

the life of Patrick Russell can be found in Adler

(1989) and Smith ( 1931). The only reptile that is not a

snake described and illustrated in Russell (1796: 48;

PI. XLII), a blind worm snake (Typhlops j-like reptile,

was named Anguis melanostictus by Schneider, 1801.

Russell referred to the species only by the local ver-

nacular name, Rondoo talooloo pam (an obvious cor-

ruption of 'renda talu pam', Telugu for two-headed

snake), and referred the species to the genus Anguis.

Subsequent workers (e.g., Gray, 1845; Giinther, 1864)

have assigned the species provisionally to the genus

Anguis, the latter author crediting the name, in error,

to Merrem (1820). The species is unlisted in the next

several major works on the herpetology of the region,

including Boulenger ( 1 890) and Smith (1935).

Because the description was substantial, including

details of scalations, coloration and scale counts, it is

clear that the species illustrated by Russell and named

as Anguis melanostictus by Schneider ( 1 801 ) is a spe-

cies of Barkudia, known to be endemic to the east

coast of peninsular India (see Smith, 1935). Diagnos-

tic features described by Russell (1796) matches only

this genus amongst all other southern Asian species of

scincids: ventrals 151; head and neck subequal; the

forehead covered with "laminae of unusual shapes"

(fide Giinther, 1864); teeth small, numerous: eyes lat-

eral, small: nostrils small: trunk cylindric, of the small

thickness throughout the body; body scales imbricate;

each with a black dot, and eight to 10 parallel dotted

lines forming a line that runs from the head to the end

of the tail; length 10.5 inches: tail round, smooth, its

tip blunt: tail length 4.5 inches; color reddish-brown;

ventrals and subcaudals glossy white.

The genus Barkudia and its type species, B. insu-

laris, was established on a single specimen of a leg-

less scincid from Barkuda Island, Chilka Lake (19°

46'N; 85° 20'E), Ganjam District, Orissa State, East-

ern India, by Annandale (1917). Smith (1935) pro-

vided a redescription of the species, expanding the

original description based on a reexamination of the

holotype at the Zoological Survey of India (ZSI). No

further species of the genus has been described and

Greer (1970), in his analysis of the phylogenetic rela-

tionships of scincid lizards, included the genus in the

subfamily Scincinae. Although subsequent specimens

have been found at the type locality (Annandale,

Vol. 8, p. 14

Asiatic Herpetological Research

1999

Figure 1 . The neotype of Barkudia melanosticta (ZSI 20627). Bar = 20 mm.

1921; also ZSI 22540, collected from the type locality

on 5 July, 1961), and from adjacent Nandan Kanan

Biological Park (20° 13'N; 85° 50'E), Cuttack Dis-

trict, Orissa State (Biswas and Acharjyo, 1980), little

is known of its biology (see Murthy, 1990a; 1990b).

Ganapati and Nayar (1952) reported Barkudia insu-

laris from Waltair (17° 44'N; 83° 23'E; close to Visa-

khapatnam: 17° 42'N; 83° 18'E), Andhra Pradesh

State, Southeastern India, at a distance of circa 300

km to the southwest of the type locality of B. insu-

laris, and Ganapati and Rajyalakshmi (1955:279)

noted that the type of the species was reported lost.

Several subsequent publications (e.g., Murthy, 1990a;

Pillai and Murthy, 1982: Sanyal, 1993; Sanyal et at..

1993; Subba Rao, 1996) uncritically accepted the

Waltair locality and listed the Andhra Pradesh locality

for the species, although both Tikader and Sharma

(1992) and Welch et al. (1990) omit this southern

record. The recent rediscovery of the holotype of B.

insularis by Das and Dattagupta (1997), permits an

examination of this and additional material and a

comparison with material from Waltair reveal that the

Andhra Pradesh material is not conspecific with B.

insularis. This paper redescribes the Southeast Indian

material and designates a neotype.

Material and Methods

The following measurements were taken with dial

vernier caliper (to the nearest 0.1 mm): snout- vent

length (SVL; from tip of snout to vent), tail length

(TL; from vent to tip of unregenerated tail), tail width

(TW; measured at base of tail); head length (HL: dis-

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

width (HW; measured at angle of jaws), head depth

(HD; maximum height of head, from occiput to

throat), body width (BW; greatest width of body), eye

diameter (ED; greatest diameter of orbit), eye to nos-

tril distance (E-N; distance between anteriormost

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

distance between anteriormost point of eyes and tip of

snout), eye to ear distance (EE: distance from anterior

edge of ear opening to posterior corner of eyes), inter-

narial distance (IN; distance between nares), and

interorbital distance (IO; between orbits).

Comparative material of Barkudia insularis exam-

ined includes: ZSI 18075 (holotype of Barkudia insu-

laris Annandale. 1917), Barkuda Island, Chilka Lake,

Orissa, Eastern India; ZSI 22540: Barkuda Island,

Chilka Lake, Orissa, Eastern India); ZSI 24086.1 and

24086.2 (Nandan Kanan Biological Park, Cuttack

District, Orissa, Eastern India).

Systematic account

Barkudia melanosticta (Schneider, 1801) nov.

comb. (Figs. 1-2)

Neotype. ZSI 20627 (adult female), Visakhapatnam

(17° 42'N: 83° 18'E), Andhra Pradesh State, South-

eastern India, 47.8 m above mean sea level, collected

by P. N. Ganapati, 17 August 1954. The type locality

is indicated in Fig. 3.

Other material. ZSI 25135 (adult female), collected

by M. V. Subba Rao, 1984.

Diagnosis. A member of the genus Barkudia Annan-

dale, 1917, B. melanosticta (Schneider, 1810), can be

distinguished from B. insularis Annandale, 1917, as

follows: larger size (SVL 161.0-164.9 mm, vs. 107.0-

143.0 mm): palatal teeth present (vs. absent); anterior

lobe of tongue distinctly narrowed (vs. not differenti-

ated from the posterior lobe of tongue); and lobules

around ear opening absent (vs. present).

Description of neotype. Adult female. Snout-vent

length 164.9 mm; head elongated (HL/SVL ratio

0.05), narrow (HW/SVL ratio 0.04), depressed (HD/

HL ratio 0.61), indistinct from neck; snout long (E-S/

HW ratio 0.74), longer than the eye diameter (ED/E-S

ratio 0.33). projecting beyond mandible: parietal eye

absent; supraoculars three, supraoculars II and III

largest; supraciliaries present; scales on snout and

forehead smooth; rostral emarginate laterally, contact-

ing supranasals posteriorly; rostral large, lacking ros-

tral groove, wider than deep (rostral width = 3.0 mm;

rostral depth = 1.7 mm; width/depth ratio 1.76), con-

1999

Asiatic Herpetological Research

Vol. 8, p. 15

Figure 2. Head of the neotype of Barkudia melanos-

ticta (ZSI 20627) in dorsal (top left), ventral (top right)

and lateral (bottom) views. Bars = 5 mm. 20627). Bar

= 20 mm.

tacted posteriorly by two nasals and two semicircular

supranasals that are narrowly in contact. Posteroven-

trally, rostral in contact with supralabial I. Nares slit-

like, situated within nasals, oriented laterally, nasals

in narrow contact with supralabial I. Supranasals con-

tact supralabial I laterally and frontonasal posteriorly:

frontonasal trapezoid, wider than long, contacting

supranasals anteriorly and frontal posteriorly: frontal

deeper than frontonasal, constricted laterally, where it

contacts supraocular I; at its posterior end, frontonasal

contacts a V-shaped interparietal, which is wider than

frontal, a single pair of parietals contacts interparietal:

a single preocular between loreal and orbit. Eye

reduced (ED/HL ratio 0.18), orbit situated dorsolater-

al^; four supralabials (supralabial III in suborbital

position), supralabial IV largest: supralabial followed

by a single small scale; infralabials 4; upper eyelids

undeveloped; lower eyelids scaly; two postoculars: a

single anterior and two posterior temporals; ear open-

ing minute, slitlike, measuring 0.05 mm; situated lat-

erally at approximately the level of jaws; lobules

Figure 3. Map of India (marker = 800 km), showing

(enlarged on right; marker = 400 km) eastern and

southeastern India, and the distribution of the two spe-

cies of Barkudia. Reference: Spots, B. insularis (both

in Orissa State); triangle, B. melanosticta (in Andhra

Pradesh State). See text for details.

around ear opening absent; eye-to-ear distance less

than eye-to-nostril distance (E-E/E-N ratio 1.19).

Inner rim of upper jaw smooth. Mental large, semicir-

cular, wider than deep, single trapezoidal postmental,

larger than mental, its width 0.29 per cent head width.

Postmental contacts infralabial I, but fails to contact

infralabial II, bounded posteriorly by a pair of

smooth, rounded, juxtaposed chin scales that are sepa-

rated by a single scale. Tongue narrowly elongate, dis-

tinctly narrowed distally, with a median cleft and

scattered papillae on the dorsal surface. Palate with

teeth arranged in a regular series; maxillary and

manibular teeth oriented towards the posterior, regu-

larly arranged.

Body slender, elongate (SVL/BW ratio 0.04). Scales

smooth, scale size subequal dorsal ly as well as ven-

trally. Anals three, smooth; preanal not enlarged, over-

lapped by the last ventral; two scales border anal

laterally, exceeding its posterior level, over vent.

Limbs absent. Tail short, tail length 67.5 mm, much

shorter than snout- vent length (TL/SVL ratio 0.41 ),

tail base slightly swollen and bluntly rounded at tip.

Ventral surface of tail with smooth, undifferentiated

subcaudals; scales on the postanal region and at the

proximal part of the tail base smooth.

Coloration, (in alcohol) Dorsally yellowish-brown,

turning chestnut brown towards the posterior half of

tail; the tail tip (last 5 mm of tail) dark brown dorsally

and ventrally, except for a pale yellow spot on the

Vol. 8, p. 16

Asiatic Herpetological Research

1999

ventrum. Ventrum of body uniformly yellow-cream.

In life, these lizards are typically "glossy brown with

a black spot in the middle of each scale" (Ganapati

and Rajyalakshmi, 1955).

Measurements . (neotype, followed by ZSI 25135

[an adult female]; in mm) SVL 164.9 (161.0); TL

67.5- original unregenerated (32.2- partially regener-

ated); TW 4.7 (5.1); HL 8.7 (6.7); HW 6.6 (6.2); HD

5.3 (4.9): BW 6.8 (6.3); ED 1.6 (1.2); E-N 3.2 (3.1);

E-S 4.9 (4.1); E-E 3.8 (3.3); 10 4.7 (5.0); and IN 3.3

(3.5).

Scutellation. (neotype, followed by ZSI 25135 in

parentheses).- Ventrals (between postmental and prea-

nal) 145 (143); subcaudals 78 (36+): supralabials 4

(4) (III in suborbital position in both types); infralabi-

als 4 (4); and midbody scale rows 20 (20).

Variation. The non-type differs from the neotype in

the following details: anal divided, lateral scales do

not exceed level of anal; which bear fine keels and

first scale following postmental contacts infralabial I.

In the original description, the subcaudal count given

(120) is significantly larger than that shown by the

neotype- 78 (tail-tip regenerated in the non-type), but

it is likely that adult males (of which no specimens

have been examined) have longer tails and therefore,

larger subcaudal counts. For instance, in a single male

Barkudia insularis (ZSI 18075) examined, the sub-

caudal count was 108, as opposed to 82 in the only

female (ZSI 24086) with an original tail.

Natural history. Several authors have provided infor-

mation on the natural history of Barkudia melanos-

ticta, including Ganapati and Nayar ( 1952), Ganapati

and Rajyalakshmi (1955), Subba Rao (1996) and

Subba Rao and Nageswara Rao ( 1998). The local pro-

tection given to the new species has precluded the col-

lection of additional specimens.

Comparisons

The species being revived from obscurity is clearly a

member of the genus Barkudia Annandale, 1917, due

to the following features: fore and hind limbs absent,

upper eyelids undeveloped, lower eyelids scaly, eyes

vestigial, ear opening slitlike; nares situated in nasal,

and body elongated. These features, in combination,

separate members of the genus Barkudia from two

other genera (both monotypic) of limbless scincids to

which it is apparently closely related, including Sep-

sophis Beddome, 1870, containing Sepsophis puncta-

tus Beddome, 1870, from the Eastern Ghats of

Southeastern India and Chalcidoseps Boulenger,

1887, containing Chalcidoseps thwaitesii (Gunther.

1872), from the Knuckles Range of Central Sri Lanka

(see Smith, 1935, for diagnoses).

Barkudia melanosticta (Schneider, 1801) differs

from B. insularis Annandale, 1917, in the following

features: palatine teeth present (vs. absent); anterior

lobe of tongue narrowed (vs. not differentiated): and

lobules around ear opening absent (vs. present). The

two specimens known are larger (SVL 161.0 and

164.9 mm) than the four (see Materials and Methods)

examples of B. insularis (SVL 107.0- 143.0 mm)

examined.

Barkudia melanosticta is known only from the

Andhra University Campus at Visakhapatnam (north-

eastern Andhra Pradesh State, southeastern India),

and is thus separated from the two known localities of

B. insularis by a distance of circa 300 km to the

southwest. Most of Russell's collections were pre-

sumably made in and around Visakhapatnam, ca. 5

km southeast of Waltair, the only known locality of B.

melanosticta.

Acknowledgments

For permission and facilities to examine comparative

material at the ZSI, I thank J. R. Alfred and Shyamal

Kumar Chanda. Basudeb Dattagupta, Nemai Charan

Gayen and Sujay Raha rendered curatorial assistance.

M. V Subba Rao supplied the second example. Kraig

Adler, Sushil Dutta, Allen Greer, Van Wallach and

Romulus Whitaker offered comments on the manu-

script.

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1999

Asiatic Herpetological Research

Vol. 8, pp. 18-24

The Dates of Publication of Amphibian and Reptile Names by Blanford and

Stoliczka in the Journal and Proceedings of the Asiatic Society of Bengal

INDRANEIL DAS

Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.

Present address: Institute of Biodiversity and Environmental Consen'ation, Universiti Malaysia Sarawak, 94300

Kota Samaralian, Sarawak, Malaysia, email: idas@maillwst.unimas.my

Abstract.- The dates of publications of the Proceedings and the Journal of the Asiatic Society of Bengal are

discussed. Several names of amphibians and reptiles were proposed, along with brief descriptions, by W. T.

Blanford and F. Stoliczka in the monthly Proceedings before their intended formal description in the Journal, in

some cases, a year before. These earlier publications constitute formal descriptions according to the Code of

Zoological Nomenclature. A listing of two genera (one amphibian and one reptile) and 24 species (three

amphibians and 21 reptiles) is appended; the type localities include Turkmenistan, Pakistan, India, Myanmar and

Malaysia.

Key words.- Amphibians, reptiles, dates of publication. Proceedings and Journal of the Asiatic Society of Bengal.

Founded in 1784 by the Orientalist, Sir William Jones

(1746-1794; see Cannon, 1960, for a biographic

sketch), the Asiatic Society of Bengal, with its head-

quarters in Calcutta, has played, according to a report

in Nature at the turn of the century, "...a leading part

in the exploration of the natural history, philology,

antiquities, and other branches of scientific inquiry

connected with the East" (Anonymous, 1907).

Although Jones himself was opposed to the collection

of zoological specimens (Bose, 1885), examples of

both plants and animals did start to arrive from vari-

ous parts of the British Indian Empire, and occasion-

ally from outside. Coupled with the expeditions

organized or participated in subsequently by the staff

of the Museum of the Society, the Asiatic Society of

Bengal came to acquire one of the most important

zoological reference collections in the world, which,

after the passing of the Museum Act in 1 866, came to

the Indian Museum (Fermor, 1936) and is at present

maintained by the Zoological Survey of India (Sewell,

1932; Das et al., 1998).

The periodicals of this two century old institution

included the Journal and the Proceedings, which

gradually replaced several leading oriental journals of

the period, including the Asiatick Researches and the

Calcutta Journal of Natural History. Because of

delays in publishing the Journal (started in March

1832, the old series continuing until 1904, see

Chaudhuri, 1956), the Society started the Proceedings

in January 1865 (which were issued monthly till

December 1904). The Proceedings was out "as soon

as possible, after every monthly meeting", according

to the information on the cover page, as opposed to

and separate from the more widely circulated Journal,

which was published only once in two to three months

(Mitra, 1885). As mentioned on an untitled page of

the first issue, the separation of the Journal (which

was issued in a "new series" between 1905 and 1934,

when the Proceedings was reunited with the Journal)

from the Proceedings was "In accordance with the

announcement of the Council in the Annual Report

read at the Annual General Meeting held on the 1 1th

January, 1865" (Blanford and Heeley, 1865). Each

fascicle of the Proceedings comprised 10-30 pages,

and contained reports of the progress of the Society,

including financial statements, additions of books to

the library and coins to the Society's numismatic col-

lection, exhibition notices, correspondence from its

members and lists (and losses) of members, and also,

"short notes, which were not deemed fit for introduc-

tion into the Journal" (Mitra, 1885).

Because the Society's Proceedings was less well

known than the Journal and the ambiguity of descrip-

tions in abstracts versus in "full papers", the dates of

some of the descriptions of several genera and species

of amphibians and reptiles from Asia have been

assigned incorrectly in subsequent works (e.g., Smith,

1935; 1943) to the description published in the Jour-

nal, when, in fact, they were validly published earlier,

in some cases, a year before, in the Proceedings.

Some of the leading naturalists of the day read papers

on faunistics, including the descriptions of new taxa,

in the monthly meetings of the Society, which were

reported as "abstracts" in the Proceedings. These

1999

Asiatic Herpeiological Research

Vol. 8, p. 19

abstracts propose both new names and provide

descriptions and diagnoses, thereby constituting a

valid description according to the Code of Zoological

Nomenclature. Since the aforementioned fascicles

were generally issued monthly, and distributed to

members through subscription, publication was rapid,

leading to several names being available before their

more complete description. In some of the cases, the

titles of the papers published in the Journal and Pro-

ceedings were identical, in others, there were minor

differences, such as the use of the more formal 'Rep-

tilia' in Blanford (1879a) instead of 'reptiles' in Blan-

ford (1879b). Regrettably, the type localities of some

taxa are different in the two publications, the Journal

tending to have a more precise type locality. In one

instance. (Blanford, 1878a), the type locality ("Foot

of Nawlabu hill, west of Tavoy") is different from that

which appeared in the purported formal description

(Blanford, 1878b: "Foot of Nawlabu Hill, east of

Tavoy..."). If illustrations depicting the new taxon

being described for the first time were provided, these

appeared in the Journal. The months and, where avail-

able, dates of issue of each fascicle making available

new zoological names are annotated with the refer-

ences in Table 1. Only names published in the Pro-

ceedings that are at present attributed to the intended

formal description in the Journal have been listed.

Names dealt with in this communication have

been proposed either by William Blanford (1832-

1905) of the Geological Survey of India, or Ferdinand

Stoliczka (1838-1874), Secretary of the Natural His-

tory Department of the Asiatic Society of Bengal. Two

genera (one amphibian and one reptile) and 24 species

(three amphibians and 21 reptiles) were described as

new by the aforementioned workers in the Proceed-

ings before their intended formal publication in the

Journal. Of these, one genus (an amphibian) and 16

species (three amphibians and 13 reptiles) are at

present considered valid (see Table 1 ). The geographi-

cal coverage of the type localities includes Turkmeni-

stan (five), Pakistan (five), India (five), Myanmar

(six), and Malaysia (five).

Acknowledgements

Supported by a Fulbright Fellowship. Research on the

manuscript was conducted at the Widener and Ernst

Mayr Libraries of Harvard University. I thank Kraig

Adler, Roy McDiarmid, Hobart Smith and Van

Wallach for comments on the manuscript.

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1999

Asiatic Herpetological Research

Vol. 8, p. 21

Wall, F. 1923. A hand-list of the snakes of the Indian

Empire. Part II. Journal of the Bombay Natural His-

tory Society 29: 598-632.

Wall, F. 1924. A hand-list of the snakes of the Indian

Empire. Part III. Journal of the Bombay Natural His-

tory Society 29: 864-878.

Zhao, E.-M. and K. Adler. 1993. Herpetology of

China. Society for the Study of Amphibians and Rep-

tiles, Contributions to Herpetology, No. 10. SSAR,

Oxford, Ohio. 522 pp, 48 pi.

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1999

Asiatic Herpetological Research

Vol. 8, pp. 25-28

Size and Shape Description of Oviductal Eggs of Draco obscurus formosus

(Squamata: Agamidae)

C.H. Diong1 and S.Y.T. Soon2

Division of Biology, School of Science, Nanyang Technological University, N1E, 469 Bukit Timah Road,

Singapore 259756; -Interactive Math Exploration Center, 02-16, Waterloo Center, Singapore 180261.

Abstract.-Owidactai eggs were obtained by an abdominal dissection from a gravid Draco obscurus formosus

which was captured near the northern limits of this species distribution during the Malaysian Heritage and

Scientific Expedition to Belum, Temengor Forest Reserve, Ulu Perak, Peninsular Malaysia in 1993 and 1994.

Egg size, shape, the species-specific egg bicone coefficient , clutch mass, and clutch volume are described. This

is the first report that describes the egg and clutch characters of this species.

Key words,

coefficent.

Reptilia, Squamata, Agamidae, Draco obscurus formosus. Peninsular Malaysia, egg shape, bicone

Introduction

Size and shape characteristics of eggs, as well as the

ecological implications of egg parameters, have been

extensively studied in birds (e.g.. Preston, 1968, 1969.

1974: Paganelli et al., 1974; Hoyt, 1979; Smart, 1991)

but rare in reptiles (Iverson & Ewert, 1991; Maritz

and Douglas. 1994). One reason for this neglect lies in

the fact that most squamate reptiles lay soft, flexible-

Figure 1 . A. The adult female Draco obscurus formosus

(ZRC.2.3693) from Sungei Halong, Temengor Rain For-

est, Ulu Perak, Peninsular Malaysia. SVL = 87 mm. B.

A clutch of four fully-shelled oviductal eggs of Draco

obscurus formosus. Note the pinched projections at

both ends of each egg.

shelled eggs. Length and width dimensions of such

eggs change as they absorb or lose water through the

soft parchment shell to produce changes in their size,

shape, volume, and surface area. Consequently, soft-

shelled eggs have to be measured in their oviducts or

soon after they are oviposited. This is in contrast to

rigid-shelled eggs of crocodilians, geckos, birds, and

some chelonians which can be measured at any time

after being laid.

Iverson and Ewert ( 1991 ) applied Preston's (1968)

formulation to describe reptile eggs firstly. This for-

mulation was developed to describe the shape of avian

eggs and assumed that an egg was axis-symmetric and

the revolved egg outline on the x-axis gives its volume

of revolution. Recently, Maritz and Douglas (1994)

Vol. 8,

p.2t

Asiatic Hei-petological Research

1999

y value

b

Figure 2. The coordinates and linear dimensions used to describe the shape of Draco obscurus formosus eggs;

the outline of the egg shape, excluding the pinched ends, is generated by Mathematica software program. See

text for details.

employed the Preston formulation to demonstrate the

shape of reptile eggs from two linear measurements,

egg length L, maximum width W, and the bicone coef-

ficient c2. The bicone coefficient is a species-specific

parameter which measures bluntness at both ends of

an egg: c2 is negative for eggs with pointed ends, pos-

itive for eggs with blunt ends, and zero when the

shape is a perfect ellipse.

During the Malaysian Heritage and Science Expedi-

tion to the Belum Temengor Forest Reserves in 1993

and 1994, a gravid female of Draco o. formosus, a

subspecies endemic to southern Peninsular Thailand

and Peninsular Malaysia (Boulenger, 1903, 1908;

Musters, 1983) was collected (Diong et al. 1995).

This presented an opportunity to collect oviductal

eggs for size and shape quantization for this subspe-

cies.

Material and Methods

Material examined

One gravid female (Fig. la) was collected on 9 Dec

1994 from a trunk of a large tree along Sungei [river]

Halong, about 2 km upstream of Camp Halong (5°

24 X 101° 18Ti), Temengor Rain Forest Reserve, Ulu

Perak, Malaysia, during the Belum Scientific Expedi-

tion (Diong et. al. 1995). Specimen was measured and

dissected the day after collection. Head and body

shape, as well as mass of body and egg were mea-

sured to the nearest 0.01 mm and 0.01 g by digital cal-

ipers (Mitutoyo) and electronic balance (Ohaus),

respectively. Voucher specimen was deposited in the

Zoological Reference Collection, School of Biologi-

cal Sciences, National University of Singapore.

Quantization of egg shape

Length (L) and maximum width (W) of each egg were

measured to obtain elongation (E = LAV), bicone

coefficient (c2) and volume (V) using the method

described by Maritz and Douglas ( 1994). The outline

1999

Asiatic Herpetological Research

Vol. 8. p. 27

of the egg was described parametrieally using the Pre-

ston formulation, as follows :

cos(8).

- (£)-.e<

0° < 0 < 360°

1 + c2cos 0),

Mathematica (1993) software programme was

used to generate the shape described by the paramet-

ric equations. A 35 mm slide of the clutch of eggs was

projected on to a white cardboard mounted on a wall

and three lines parallel to the y axis (c.a. 2/3 W) were

drawn to the outline of each egg (Fig. 2) to obtain

measurements of 1, w, L, and W from the projected

image; this procedure was repeated for the other half

of the egg so that the bicone for each egg was an aver-

age of six estimations. The bicone coefficient was

determined with the formula, c-, = -I . - 1 ) ,

where r = — , a = ~( 7 I ~ ' • anc' was surjse-

quently used to estimate egg volume, V (in cm ), as

follows: V = ^L^(l+|c2 + !4 Clutch vol-

ume was defined as the sum of individual egg volume

in the clutch.

Results

Size of female lizard

Body mass 10.02 g, snout-vent length (SVL) 87 mm;

tail length (TL) 167 mm; head length (HL) 16.78 mm;

jaw length (JL) 16.86 mm, head width (HW) 10.59

mm; hind leg length (HLL) 270 mm; hind foot length

(HFL) 170 mm; fore leg length (FLL) 270 mm; fore

foot length (FFL) 9 mm.

Clutch size, egg size, and shape quantization

of eggs

The clutch consisting of 4 oviductal eggs; 2 eggs in

each oviduct; 2 yolked ova and 4 whitish ova in right

ovary, 2 yolked ova and 5 whitish ova in left ovary;

yolked ova, 5.07 - 5.15 mm in diameter, white unde-

veloped ova 1.50 - 1.72 mm in cross diameter. Eggs

turgid, shelled with chalky-white parchment-like

membrane. Egg shape ellipsoidal, ends blunt, but each

with pinched cap at ends (Fig. lb, 2). Pinched ends

solid, thick, firm, flat and in same plane, less than half

a semi-circle; outline of lip-like pinched structure

asymmetric. Mean ± SD of L excluding pinched ends

for 4 eggs 11.83 ± 0.53 mm (range: 10.94 - 12.30

mm); L including pinched ends 13.00 ± 0.26 mm

(range: 12.14- 13.40 mm); W 8.71 ± 0.20 mm (range:

8.40 - 8.91 mm); elongation L/W 1.36 ± 0.08 (range:

1.23 -1.41); mean egg bicone coefficient c2 -0.021 ±

0.008 (range: -0.032 to - 0.010); egg volume 0.487 ±

0.022 cm3 (range: 0.460 - 0.510); egg mass 0.497 ±

0.022 g (range: 0.470 - 0.520 g); density 1.0205 ±

0.0009 (range: 1.0 196 - 1.0217). Total clutch volume

1.86 cm ; total clutch mass 1.99 g; relative clutch

mass [clutch mass divided by female (clutch plus

body) mass] in percent, 19.86; relative clutch mass

[clutch mass divided by female (body only, exclusive

of clutch) mass) in percent, 24.78

Discussion

The present specimen has TL/SVL ratio equaled to

1.92 which is a middle size compared to Musters'

(1983) report of 1.89 - 1.99 for females of this spe-

cies. Musters (1983) while reporting a mean SVL of

82 ± 7mm for four females of this lizard and a mean

clutch size of 3.7 for three females of Draco obscurus

formosus, made no reference to egg shape of this liz-

ard. Hendrickson (1966) recorded a mean clutch size

of 2 in D. melanopogon (n = 14) and a mean clutch

size of 4 in D. volans (n = 20). This suggests that

clutch sizes in D. o. formosus and D. volans may be

similar, being larger than that in D. melanopogan.

Among these gliding agamid lizards, clutch size is

probably constrained by body size and clutch mass as

a larger clutch mass is likely to reduce the horizontal

displacement covered during gliding. In the present

study, the total clutch mass accounted for almost 20

percent of female body mass.

The three Draco species, D. obscurus formosus,

D. melanopogan, and D. volans, all have contrasting

egg shapes. Causility of variation of egg shape in the

genus are unknown. The eggs are distinctly pointed at

both ends in D. melanopogan but are ellipsoidal,

blunt, and smoothly rounded at both ends in D. volans

(Hendrickson, 1966). Eggs of D. obscurus formosus is

a nearly perfect ellipsoid as indicated by the species-

specific bicone coefficient, c2 -0.021, which is very

close to Ci = 0, the value for a perfect ellipse. Addi-

tionally, the eggs are much rounder, as indicated by its

elongation factor of 1.36 which is smaller in eggs of

D. volans (E = 1.6) and D. melanopogon (E = 2.06),

as calculated from Hendrickson's (1966) L and W

measurements of the eggs. The most unusual structure

of D. o. formosus eggs is the flat projections pinched

outwards from both ends. The significance of the cres-

Vol. 8, p. 28

Asiatic Herpetological Research

1999

cent-shaped pinched ends is unknown, but they may

function as reserves of parchment shell materials to

allow the stretching and expansion of the egg during

development.

Acknowledgments

The first author thanks the Malaysian Nature Society

for permission to participate in the Belum Scientific

Expedition; to L. S. Tay for field assistance, and to T.

Hikida for identifying the specimen. This study was

partially supported by the Nanyang Technological

University, Singapore research grant RP10/92 to the

first author.

Literature Cited

Boulenger, G. A. 1903. Report on the batrachians and

reptiles. Fasciculi Malayenses Zoology, 1:130-176,

figs. 1 -3, pis. 5-10.

Boulenger, G. A. 1908. Report on the Gunong Tahan

expedition, May - Sept 1905. Ill Fishes, batrachians

and reptiles. Journal of the Federated Malay State

Museum, Singapore, 3: 61-69.

Diong, C. H., B. H. Kiew, and B. L. Lim. 1995. An

annotated checklist of the lizard fauna in the Temen-

gor Forest Reserve. Hulu Perak, Malaysia. Malayan

Nature Journal (Belum Expedition, Temengor 1993-

1994), 48(3&4): 353-356

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tin of Raffles Museum, Singapore 34:53-71.

Hoyt, D. F. 1979. Practical methods of estimating vol-

ume and fresh weight of bird eggs. AUK 96: 73-77.

Iverson, J. B. and M. A. Ewert. 1991. Physical charac-

teristics of reptile eggs and a comparison with avian

eggs. Pp. 87-100. In D.C. Deeming and M.W.J. Fer-

guson (eds). Egg incubation: its effects on embryonic

development in birds and reptiles. Cambridge Univer-

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Maritz, M. F. and R. M. Douglas 1994. Shape quanti-

zation and the estimation of volume and surface area

of reptile eggs. Journal of Herpetology 28(3): 281-

291.

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2.2, Wolfram Research, Champaign, Illinois, U.S.A.

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avian egg: surface area, volume, and density. CON-

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bridge, U.K.

1999

Asiatic Herpetological Research

Vol. 8, pp. 29-37

Diel Activity of Ranodon sibiricus (Amphibia: Hynobiidae) in Relationship to

Environment and Threats

Dag Dolmen1, Rudolf A. Kubykin2 and Jo V. Arnekleiv1

Norwegian University of Science and Technology, The Museum; N-7004 Trondheim, Norway. National

Academy of Science, Inst, of Zoology; Almaty 480032, Kazakhstan.

Abstract. -¥vt\d studies on the diel activity of Ranodon sibiricus were carried out in Dzhungaria, southeastern

Kazakhstan, in August 1994 and June 1995. Counts showed that adults and juveniles were strongly nocturnal,

which was also confirmed with the help of IR light/photocell equipment, whereas larvae were active both night

and day. The daily activity period of adults and juveniles started near the 5-lux limit and peaked around 23-01

hrs. Its length followed that of the night and was accordingly shorter in June than in August. When the activity of

aquatic adults and juveniles started in the early night, about 5% came out of the water and walked on land

alongside the brook. Most ranodons, however, were relatively stationary sit-and-wait predators in the water. The

nocturnal activity of/?, sibiricus protects it against dehydration (terrestrial animals), strong UV radiation and

diurnal predators. The most important task of the nocturnally and diurnally active larvae is to grow as fast as

possible to survive the first, hazardous hibernation. The difference in diel activity between adults/juveniles and

larvae reduces intraspecific competition and cannibalism within the population. Because of their secretive life,

metamorphosed stages of R. sibiricus are not easily accessible to predators or Man. Hence, the most important

threat is probably the large herds of cattle grazing in the area. Since adults and juveniles are well hidden by day,

when the cattle wade the brooks, they are fairly safe, but cattle may pose a great threat to ranodon eggs and

larvae.

Key words. -Ranodon sibiricus. Kazakhstan, diel activity, rare species, environmental adaptation, threats.

Introduction

A threatened, secretive species

The salamander Ranodon sibiricus Kessler, 1866 is

distributed in the Dzhungarian mountains of south-

eastern Kazakhstan and the extreme west of Xinjiang

province in China. Its range is very small and has

undergone many man-made changes during the past.

The species is therefore threatened and is on the red

list of the former Soviet Union/Kazakhstan (Bannikov

et al. 1978; Zhao and Adler 1993). Its habitat is cold,

clear mountain brooks. Because of their quite secre-

tive way of life, individuals are not always easy to find

even where they may be locally abundant. Although

Shnitnikov (1913) found it easily, Brushko and Nar-

baeva ( 1988) emphasized the difficulties of finding R.

sibiricus in the mountain rivers. Its secretive life is

also reflected in its nocturnal activity, an aspect briefly

touched upon by several authors (Shnitnikov 1913:

Paraskiv 1953; Kubykin 1986: Narbaeva and Brushko

1986; Wang 1990).

As part of a wider ecological study of Ranodon

sibiricus in Dzhungaria, we investigated its activity,

partly in 1993, but more thoroughly in 1994 and 1995,

to learn the details of its diel activity rhythm and pos-

sible adaptations to the environment. Several other

questions were also of interest. For instance, do the

larvae behave differently from the metamorphosed

animals to reduce intraspecific competition and canni-

balism (as in Triturus; see Dolmen 1988)? Does the

nocturnality of the species really make it almost safe

from terrestrial predators and Man? To what extent

can R. sibiricus avoid the heavy impact of some 150

cows which graze along and trample in the brooks

when crossing the study area twice a day in summer

(Kubykin et al. 1995; Dolmen et al. 1997)?

A preliminary report on these studies was pre-

sented by Dolmen et al. (1995). Hereafter. Ranodon

sibiricus is mostly referred to as ranodon.

Principles of measuring activity

In principle, there are at least three ways of mea-

suring the activity of an animal: 1 ) with an actograph

or other technical device such as light beam/photocell

equipment, 2) by interval trapping of active animals,

and 3) by counting active animals. All three methods

have been successfully used for Triturus species

(Salamandridae) in Europe (e.g. Himstedt 1971; Dol-

men 1983a,b; Griffiths 1985).

Vol. 8, p. 30

Asiatic Herpetological Research

1999

Preliminary studies

In June 1993. the trapping technique was tried out for

ranodons in a small brook in the Borokhudzir valley

in Dzhungaria. On 15 June, 10 simple funnel traps (1

L "Cola traps") and two more complicated traps with

eight entrances each (constructed by Arne Haug) were

placed in a 15 m long stretch of a small brooklet

(Brook 3) in which six ranodons and 50 double

clutches of eggs had been registered two days earlier.

Alternate traps had their entrances pointing down-

stream and upstream. The traps were checked/emptied

every third hour throughout a day and night, but no

ranodons were caught. The water temperature varied

between 3.8 °C and 7.6 °C. On 17 June, a similar set-

up was tried on a 15 m stretch of another, somewhat

larger brook (Brook 1) where, in addition to the ran-

odons living there naturally, 38 additional ones were

released. A few were caught during the next day and

night, but never more than two each time.

However, a study of a third brook (Brook 5) at

night revealed that many ranodons were going onto

land and wandering on the dew-wet banks beside the

brook. On a 500 m stretch at 23.00-24.00 hrs. (stan-

dard time), four men with torches counted 14 ran-

odons that were active on wet land and 1 1 hidden

under stones alongside the brook. Although aquatic

individuals were also active, the main movements up

and down the brook seemed to be taking place on

land, not in the water. The trapping technique in water

was accordingly unsuitable for measuring the activity

of ranodons.

For 1994 and 1995. it was therefore decided to use

the counting method for measuring the activity of ran-

odons, and for comparison, data from the use of light

beam/photocell equipment could serve as a control.

Description of the area

The study area, on the southern slopes of the River

Borokhudzir catchment in Dzhungaria at an altitude

of approximately 2200 m, consists of grazing for cat-

tle, bog, and juniper-covered hillsides. Two small trib-

utary brooks to the River Borokhudzir (Brook 1 and

Brook 5), approximately 200-300 m apart, were cho-

sen for the study. Both were spring-fed, about 2-50

cm deep and 30-80 cm wide, and had gravelly or

stony bottoms. In a few places, turf almost overgrew

and covered the water. Boulders, where terrestrial ran-

odons hid, could also be found on land alongside the

brooks. The velocity of the water at different sites

along the two brooks varied from 0.0-0.2 and 0.0- 1 .0

m/s, respectively. Measurements were made in August

1994 when the flow was low.

The weather in both periods was mostly clear. The

air temperatures in August 1994 and June 1995 varied

between 5.7 °C and 17.1 °C, and 3.5 °C and 21.0 °C,

respectively. The air humidity in August 1994 varied

from less than 50 to 100% RH, with maximum

humidity at night. The water temperature at the site

investigated in Brook 1 varied in August 1994

between 5.5 °C in the early morning and 19.3 °C in

the afternoon, and in June 1995 between 5.0 °C and

20.0 °C. In Brook 5, the water temperature varied

between 6.2 °C and 14.8 °C in August 1994 and 4.8

°C and 15.6 °C in June 1995. A more detailed descrip-

tion of the area is given by Dolmen et al. (1997).

Material and Methods

Field investigations

The study took place in August 1994 and June 1995.

Two persons equipped with good torches examined a

total of 90 m and 190 m, respectively, along the two

brooks (Brook 1 and Brook 5) every second hour for

three days and nights. The walking speed was approx-

imately 8 m/min. Deep pools and shallow slowly-

flowing water were especially well examined, and

also the nearest 2-3 m on land alongside the brooks.

No stones were turned, however, and no ranodons

were disturbed, except possibly by the torchlight. The

two brooks had been divided into sections of 5 or 10

m, respectively, for statistical use. and the number of

ranodons in each section were counted separately. The

numbers in different main developmental stages were

also kept apart: 0+ (young larvae, less than one year

old), 1+ (old larvae and metamorphosed individuals

from the previous year), larger juveniles, and adults.

Aquarium investigations

In December 1994, additional investigations of the

activity of two ranodon individuals, an adult and a

large juvenile, were carried out in Almaty. An experi-

mental aquarium was made of transparent plexiglass

shaped like a circular channel. The outer diameter was

36.5 cm, the inner diameter 15 cm and the height 10

cm. The aquarium was filled half full of water brought

from Dzhungaria and some large stones acted as shel-

ter for the animals and to enable them to climb up into

the air. The aquarium was equipped with an infra-red

light beam/photocell system (Visolux LS 4-GaAs).

The beam was set to a diameter of about 2 mm and

focused near the bottom of the aquarium, where the

ranodons usually walk around. Interruptions of the

beam were recorded by an electric counter (Visolux

LU GaAs), which was read every second hour

throughout eight days and nights. Food was not pro-

1999

Asiatic Herpetological Research

Vol. 8, p. 31

vided during the experiment. The aquarium was

placed inside a building, close to a north-facing win-

dow. The light regime was therefore natural, i.e.

approximately like outside. The temperature was con-

stant and slightly lower than the usual room tempera-

ture.

The same equipment, connected to a 12V car bat-

tery, was used for an adult and a large juvenile in

D/hungaria in June 1995. The aquarium was pro-

tected from disturbance and strong sunshine by being

placed halfway under a car and partly covered with a

blanket. The water was replenished (in daytime) once

during the experiment, which ran for barely three days

and nights. On the second evening, the onset of activ-

ity was studied in more detail at 5-minute intervals for

two hours.

Environmental factors

Light intensities between 0 and 10 lux normally act as

Zeitgeber for activity in plants and animals (cf. Dol-

men 1983b). The 5-lux value is therefore often used in

activity studies as a limit between day and night. In

our study it was determined subjectively, evening and

morning. The 5-lux value in Dzhungaria occurs

roughly 10-15 minutes before (or after) the 0.1-0.5

lux values, which corresponds well with the light

intensity required for reading a newspaper, for

instance. This was confirmed with a Hartmann and

Braun ECLX 4 luxmeter.

The times for reading the Visolux counter were set

approximately symmetrically around the darkest time

of night (ca. 24.00-00.30). All hours mentioned here-

after refer to standard time, not summer time. An

important difference in the understanding of diagrams

based on the two methods used for measuring activity

here is that a) the counting method measures the

activity at the time of counting, whereas b) the IR

beam/photocell method measures the activity during

the two hours preceding the time when the counter is

read.

Statistics

Wilcoxon's matched-pairs signed-ranks test (two-

tailed) was used to test any significance levels in the

activity measured in the field, the number of ranodons

within the different brook sections being counted for

an hour and comparison being made with the situation

two hours later.

The same test was used for the aquarium study,

but it was based on the ranodon counts for all the days

within a certain time interval combined, and these

were compared with the corresponding counts in the

next time interval.

The chi-square test was used to find out whether

or not the activity patterns had a significant diurnal

(06-18 hrs.) or nocturnal (18-06 hrs.) predominance,

and the chi-square test with two variables withoul

expected values was used to test any differences in

activity pattern between, for example, adults and lar-

Results

The field activity studies

The activity of Ranodon sibiricus was definitely noc-

turnal, but with some modifications with respect to the

developmental stage and the month of the year. The

animals in all stages were amazingly clever at hiding

during parts of the day and night. Several were seen at

night on a gravelly bottom along stretches of the

brook which we had searched very thoroughly in day-

time without finding any.

In August 1994, the diel activity showed basically

the same patterns in both brooks, although the peak

apparently varied slightly from day to day between 21

and 01 hrs. (Fig. 1).

Adults and juveniles had similar patterns, and seen

together the rise in activity level from 19 to 21 hrs.

was always statistically significant (P<0.002: Wil-

coxon's signed-ranks test, see Fig. 1 ). Likewise, the

decrease in activity from 03 to 05 hrs. was always sig-

nificant in Brook 5, where most animals were regis-

tered (P<0.002). The variation in the time of peak

activity from day to day was usually not significant.

In Brook 1, the larvae showed a similar rise in

activity from 19 to 21 hrs. When 0+ and 1+ larvae are

counted together, the increase is significant (P<0.002

or P<0.02) on two of three dates. The activity of 0+

larvae in Brook 5 was not as well defined as in Brook

1, being much more diurnal. In contrast to adults and

juveniles, and also to the larvae of the other brook,

which were all mainly nocturnal (P«0.001; chi-

square test), the larvae of Brook 5 showed a much

higher degree of diurnality (nocturnality tested:

0.20<P<0.30). Indeed, traces of diurnal activity can

also be seen in the 0+ larvae of Brook 1 .

The period of activity of this species fitted very

well with the light and dark periods, i.e. activity was

connected with the part of the 24-hour period when

the light intensity was below 5 lux. This was approxi-

mately 20.00-05.30 hrs. at that time of year. Except

for young larvae, any activity outside that period was

negligible.

A pattern similar to that of August 1994 was

revealed in June 1995. The period of darkness (<5

Vol. 8, p. 32

Asiatic Herpetological Research

1999

Hrs.

09 11 13 15 17 19 21 23 01 03 05 07 09 j9 11 13 15 17 19 21 23 01 03 05 07 09

45-

40-

3S -

Hrs

09 11

13 15 17 19 21 23 01 03 05 07 09 09 11 13 15 17 19 21 23 01 03 05 07 09

25

11 13 15 17 19 21 23 01 03 05 07 09 09 1 1 13 15 17 19 21 23 01 03 05 07 09

Figure 1 . Diel activity of Ranodon sibiricus, based on

counts in Brooks 1 and 5 in August 1994. Levels of sta-

tistical significance: * P<0.05 or P<0.02; ** P<0.01 or

P<0.002.

lux) in June was shorter than in August, i.e. about

21.00-04.30 hrs., and the activity peaks of adults and

large juveniles were narrower, at 23 (21) or 01 hrs.

(Fig. 2).

The youngest stage (1 + ) showed activity peaks

varying from 21 to 03 hrs. and also some diurnal

activity. At least three times, larvae (one each time)

were even registered directly exposed to sunshine, at

1 1, 13 and 17 hrs. Nevertheless, on the whole, the lar-

vae definitely had a nocturnal pattern.

The activity period of the species again fitted very

well with the (shorter) dark period. The rise in activity

from 19 to 21 hrs. was always significant (P<0.002 or

0.02) in Brook 5, both for adults/juveniles and 1+ lar-

vae, as was the decline from 03 to 05 hrs (P<0.002,

0.01, 0.02 or 0.05), and usually even 01-03 hrs. for

adults and juveniles in both brooks (P<0.002, 0.02 or

0.05). The day-to-day variation in peak activity seen

at midnight was not significant.

The aquarium studies

In the aquarium investigations in December 1994, the

ranodons also showed a definite nocturnal activity,

with peak activity at 20-22, 22-00 and/or 00-02 hrs. A

cumulative curve for the whole period of investigation

5

10-

15

20-

I 11 13 15 17 19 21 23 01 03 05 07 09 09 11 13 15 17 19 21 23 01 03 05 07 09

Figure 2. Diel activity of Ranodon sibiricus in Brooks 1

and 5 in June 1995. For explanation, see Fig. 1.

had a main peak at 02 hrs. (i.e. peak activity at 00-02

hrs.) and a minor peak at 22 hrs. (i.e. 20-22 hrs.). with

little or no activity during the light hours. The rise in

activity from 16-18 to 18-20 hrs. and from 22-00 to

00-02 hrs. was significant (P<0.05), as was the

decrease from 00-02 to 04-06 hrs. (two time intervals

seen together) (Fig. 3).

The activity period of the animals at this time of

year was clearly longer than the activity measured in

summer, as was the period of darkness (<5 lux),

which lasted from approximately 17.30 to 08.00 hrs.

The aquarium study in June 1995 confirmed the

results of the field investigations, although there were

minor deviations, probably for methodological rea-

sons. Activity was negligible until 21 hrs. when a rise

in activity occurred resulting in a peak at 21-23, 23-01

or 01-03 hrs. (Fig. 4).

In the more detailed aquarium investigations on 20

June, the activity started about 15 minutes before the

5-lux limit was reached in the open. However, since

the aquarium was partially covered (see Methods), the

1999

Asiatic Herpetological Research

Vol. 8, p. 33

Hrs.

12 14 16 1!

20 22 00 02 04 06 08 10 12

Hrs.

13 15 17 19 21 23 01 03 05 07 09 11 13

No.

Figure 3.Diel activity of two Ranodon sibiricus speci-

mens kept in an aquarium under natural lighting condi-

tions for eight days and nights in December 1994,

based on the IR light/photocell method. Level of statis-

tical significance: * P<0.05.

light intensity there was a bit lower and the activity

probably started at a light value very close to 5 lux. It

increased gradually over the next hour (Fig. 5).

Observations of aquatic and terrestrial ran-

odons

By far the majority of active ranodons were found

in the water, not on land. The frequencies of finds

made on land relative to the total number of ranodon

counts were only 6.1% (N=425) and 3.6% (N=279)

for August 1994 and June 1995, respectively. The

number of ranodons counted on land alongside the

brooks was thus relatively low, but sometimes

increased when the number counted in the water

increased. Animals walking on the moist grassy

ground beside the brooks had a wet skin and were

considered not to be really terrestrial, but aquatic ani-

mals which had only left the water temporarily for

some reason.

Not all ranodons were active to the same degree at

the same time, not even near midnight. In June 1993,

when we counted ranodons on land at 23.00-24.00

hrs., i.e. when the activity was at its highest, 14 were

seen walking along the bank, but another 1 1 really ter-

restrial specimens (with a dry skin) were still passive

and very sluggish, hiding under stones.

Discussion

The activity pattern

Ranodon sibiricus proved to be highly nocturnal, with

very little, if any, activity during the day. An exception

was the young larvae (0+) in August, in part also the

one-year old larvae (1 + ) in June, which showed a cer-

tain amount of diurnal as well as nocturnal activity.

The 5-min. reading in the aquarium study showed in

detail that the ranodons gradually started their activity

near the 5-lux limit in the evening. When that limit

150-1

100

50

0

350

300-

250-

200-

150-

100

50-

0

20O

150

100-

50

0

19-20 June 1995

20-21 June

21-22 June

— i 1 l — i 1 1 1 1 1 —

13 15 17 19 21 23 01 03 05 07 09 11 13

Figure 4. Diel activity of two Ranodon sibiricus speci-

mens kept in an aquarium under natural lighting condi-

tions for nearly three days and nights in June 1995,

based on the IR light/photocell method.

was again reached in the morning, the activity had

decreased to approximately zero. This means that

even though the species is clearly nocturnal, it uses all

the time it can get for activity, i.e. mainly hunting.

Most earlier authors have noted the extreme noc-

turnal habits of the ranodons and the more diurnal

habits of the larvae (Shnitnikov 1913; Kubykin 1986;

Narbaeva and Brushko 1986). Metamorphosed speci-

mens, both in water and on land, hide under stones

during the day, but come out at night and often move

upstream or downstream for some distance. Wang

(1990) stated that in western Xinjiang, China, ran-

odons also hides among plants and under stones dur-

ing the day and is active between 24 and 06 hrs. The

Xinjiang province, like the rest of China, follows

Beijing time, which is three hours earlier than sun

time in western Xinjiang. The true activity time of

ranodons in western Xinjiang should therefore be

around 21-03 hrs., i.e. similar to that found in our

investigations in eastern Kazakhstan.

Vol. 8, p. 34

Asiatic Herpetological Research

1999

19

20

21

22

24

01

No.

5 mm.

10-

5-

0

20 June

19

Figure 5. Details of the onset of activity of two Ranodon

sibiricus specimens kept in an aquarium under natural

lighting conditions on 20 June 1995, based on the IR

light/photocell method. Activity values are shown as

counts per 5 minutes (dots) and per 2 hours (trian-

gles). The activity started near the 5-lux limit of light

intensity (see text for further explanation).

We had no opportunity to investigate newly-

hatched larvae. In 1995, in the most favourable brook

(Brook 1), the first larvae hatched during the second

half of June. According to Paraskiv (1953), newly-

hatched larvae remain in calm, shallow water well

illuminated by the sun, where they hide among stones

on the bottom. However, they often come out and lie

on the stones, and are active by day, not avoiding the

sunshine (cf. Kubykin 1986). We found that at least

part of this diurnal activity lasted throughout the sum-

mer - although the main activity was nocturnal in

August - and even to some extent in the next year

(June). A well-defined phase shift from diurnal to noc-

turnal activity, as described, for example, for Triturus

cristatus larvae (see Dolmen 1983a,b), probably does

not take place. Paraskiv (1953) mentions that older

larvae, at the time of their metamorphosis when their

gills are becoming resorbed and they are going onto

land, avoid the sunshine and keep to shady places.

Water phase and land life

The metamorphosed ranodons stay in water or on

land, or alternate more or less regularly between these

two media. In daytime, but also sometimes at night,

we found terrestrial individuals in damp hollows

under stones and the like within a few metres of the

water. We made no attempt to specifically measure the

activity of such animals. The activity of ranodons in

the brooks increased at night, however, and some also

went up on to land. We are therefore dealing with two

categories of ranodons on land: true terrestrial ani-

mals, which have a dry skin and which stay on land

for a day or more, and aquatic ranodons, which have a

wet skin and which only temporarily come out of the

water (Dolmen et al. 1997).

Shnitnikov (1913) and Paraskiv (1953) also noted

that juvenile and adult ranodons leave the water or

their terrestrial hiding places at twilight and in dark-

ness, and are then active and are found on the banks of

brooks, where they often move long distances (cf.

Kubykin 1986; Narbaeva and Brushko 1986).

However, as these authors pointed out. not all ran-

odons leave the water at night, at least not at the same

time. The majority, in fact, stay in the water and may

only occasionally come up. We found that when the

weather had been dry for many days (August 1994

and June 1995), relatively fewer ranodons were found

on land, walking around at night or hiding under

stones, than when the weather was wet (June 1993).

Environmental adaptations

The nocturnal/crepuscular activity pattern in amphibi-

ans is probably ultimately an adaptation to the night

and day temperature and air humidity cycles. The vul-

nerability of the animals to dry conditions makes it

necessary for them to hide during the driest and hot-

test hours, and even when, like the ranodons, they stay

in water, this pattern is maintained. Most urodeles are

thus primarily nocturnal, although their activity pat-

tern may vary ontogenetically (e.g. Noble 1954;

McDiarmid 1994). The activity is proximately con-

trolled by the light/dark cycle. Different temperature

regimes, even a rise in temperature of as much as 10-

15 °C, seemed to have little, if any, influence on the

activity pattern of Ranodon sibiricus. Relative humid-

ity, or at least the moisture on the ground, could be

important for whether or not amphibians will walk on

land, however. All records of ranodons walking on

land were made when the air humidity was above

80% RH, always between 21.00 and 03.00 hrs.

Another factor which could represent a threat to

Ranodon sibiricus, living at high elevations (ca. 1700-

2700 m), is the strong UV radiation. Except for a very

few larvae of the youngest stages (0+ in August and

1+ in June), no animals were seen voluntarily expos-

ing themselves directly to the sun. For cold-stenother-

mic animals like R. sibiricus, it is probably even more

important to be noctumally active than it is for most

other amphibians. High temperatures, i.e. more than

22 °C, are reported to be lethal, at least to ranodon lar-

vae (Brushko and Narbaeva 1988). Temperatures were

as low as 6.0-11.5 °C in the air and 4.8-1 1.0 °C in the

water during the peak aquatic and land-walking activ-

ity of ranodons at night. Maximum air temperatures

during the day were 17.1-21 °C, and water tempera-

1999

Asiatic Herpetological Research

Vol. 8, p. 35

Hrs. 11 13 15 17 19 21 23 01 03 05 07 09 09 11 13 15 17 19 21 23 01 03 05 07 09

%

40 H

30

20 H

10

0

10

20

30

40

50

_i i _i i i_

Brook 1

— ad., |uv. N=166

— 0+ larvae N=168

-- 1+ larvae N=28

15-18 Aug. 1994

ad., juv. N=425

0+ larvae N=151

Brook 1

ad., juv. N=75

1+ larvae N=52

18-21 June 1995

Brook 5

ad., juv. N=279

1+ larvae N=409

Figure 6. Relative degree of activity (%) of Ranodon sibiricus adults/juveniles and larvae in Brooks 1 and 5 (cf. Figs.

1-2). Young larvae (0+, and in part 1+) exhibit a markedly greater degree of diurnality than older life stages.

tures reached 19.3-20.0 °C. A few larvae were

counted during the warmest periods, too.

We made no specific study of the possible influ-

ence of moonlight on the activity of ranodons. How-

ever, when we compared our data on activity with

notes on the weather, etc, we found no trend of, for

instance, decreasing activity when the half moon (at

the most) was sometimes shining. The light regime

under such circumstances was also always well below

the 5-lux limit.

Ranodon sibiricus is clearly more nocturnal than,

for instance, the Triturus species studied by Dolmen

( 1983a,b). It can also be seen that the activity period

of R. sibiricus in June was shorter than in August,

which is in conformity with the length of the night. A

similar phenomenon was shown for the more crepus-

cular Triturus vulgaris and T. cristatus in Norway

(Dolmen 1983a,b). Moreover, although normally two-

peaked, in northern latitudes at midsummer the crep-

uscular peaks of the Triturus species fused, and the

activity curve thus revealed only one, long midnight

peak when real nights (<5 lux) disappeared. Espe-

cially T. vulgaris, being the more crepuscular species,

takes advantage of these long periods of twilight in

northern latitudes in that its hunting day thereby

becomes longer and its growth better.

The activity period of the strictly nocturnal Ran-

odon sibiricus, however, becomes shorter at midsum-

mer. It is advantageous for an animal to have the

opportunity to seek food for as many hours as possi-

ble; the ranodons in fact spends the whole night. Its

activity is limited, however, by the varying light

regime through the season, i.e. the period per day and

night when light intensity is below 5 lux, which again

is relatively short at midsummer. The need for protec-

tion against climatic factors, as described above, and

possibly from (diurnal) predators thus seems to be

greater than the need for extra growth in metamor-

phosed ranodons.

However, a marked difference could be seen in the

diel activity of metamorphosed ranodons and larvae,

especially 0+ larvae aged 1-2 months (Fig. 6). The

youngest stages seem to be more or less active both

day and night. Still younger larvae than those we have

studied are possibly even more diurnally active (cf.

Paraskiv 1953). A probable explanation of the pro-

longed activity of the larvae, compared to older

stages, is their need to eat and grow as much as possi-

ble during the short frost-free season in the moun-

tains. Being large may perhaps increase their chances

of surviving their first, most hazardous, winter. Grow-

ing is therefore probably their most important task. A

larger size also makes their migration up or down the

brook to hibernation sites in late autumn easier and

protects them from predatory fish (see below).

By staying during the summer in the lower,

warmer part of small brooks, in shallow water, and

alternating between shade and sunshine (Paraskiv

1953: Dolmen et al. 1997), the metabolism of the lar-

vae is raised and kept at a near optimal level. There

are, however, certain limits for a cold-stenothermic

animal like Ranodon sibiricus. Small larvae are sensi-

tive to warm weather, and 22 °C is said to be lethal

(Brushko and Narbaeva 1988).

Such a difference in diel activity and microhabitat

between adult urodeles and their larvae is not uncom-

Vol. 8, p. 36

Asiatic Herpetological Research

1999

mon (McDiarmid 1994). Dolmen (1983a,b; 1988)

interpreted it as a means to reduce intraspecific com-

petition between different developmental stages and

as protection against cannibalism, which may be com-

mon in salamanders and which is also known to occur

in Ranodon sibiricus (Kubykin 1986: Wang 1990:

Kuzmin 1991a). In species whose adults and larvae

live sympatrically, a behavioural mechanism which

favours the avoidance of cannibalism could presum-

ably be of adaptive value.

Hunting strategy

During our preliminary studies in June 1993, the

method we used for trapping ranodons in water failed

and we concluded that most translocations of Ran-

odon sibiricus, at least at that particular time of year,

probably took place on land. However, only a small

proportion of our many records of active ranodons in

1994 and 1995 were made on land. We therefore con-

clude that most of their activity, like hunting (not

longer translocations), is nevertheless aquatic. Hence,

ranodons are probably largely sit-and-wait hunters, as

maintained by Paraskiv ( 1953), too; they do not move

about much in the water. This contrasts with the Euro-

pean Triturus species (see Dolmen 1983a,b), which

live in the stagnant water of ponds and small lakes.

For a running-water species like R. sibiricus, it may

be more economic to sit and wait for drifting prey

than to spend energy looking for them.

Our preliminary results on food items showed that

Ranodon sibiricus is an opportunist when it comes to

choice of prey, and thus supports the results of stom-

ach analyses made by Kuzmin (1991b). There was

also a tendency for ranodon stomachs to be at their

fullest after midnight. Based on the undigested stom-

ach contents of a few specimens caught in daytime,

Shnitnikov (1913) suggested that the ranodons feeds

by day. However, apparently no ranodons caught by

him at night were examined.

Diel activity and predators

During the day, metamorphosed ranodons cleverly

hide under boulders and in earth cavities in the brook

bed and are often difficult to catch. Because of their

strict nocturnality and their ability to hide in daytime,

night searches with good torches are the best way of

looking for ranodons in a brook. Searches in daytime

may be strenuous, and often negative if the population

density is not large. At night, however, the animals are

easy to see in small and medium-sized brooks.

It can be expected that the activity cycles of a

predator and its prey will coincide. Wild boars Sus

scrofa and grey herons

Ardea cinerea are said to be natural predators of

ranodons (Brushko and Narbaeva 1988), likewise

black storks Ciconia nigra (Shnitnikov 1913). We

think that some of the many species of birds of prey

which occur in great numbers in the mountains (e.g.

buzzards Buteo spp.) will also occasionally take ran-

odons if they had the opportunity. However, of these

terrestrial predators, only the wild boar is nocturnal.

Adults and large juvenile ranodons therefore seem to

have few, if any, really important predators. However,

two kinds of fish (Diptychus maculatus and D.

dybowskii (Cypriniformes)) are present in the River

Borokhudzir, at least in the main river. Fish, which are

usually nocturnal or crepuscular, may therefore be

potential predators of ranodon larvae. However, since

these fish are absent, or extremely rare, in the small,

spring-fed brooks in which the ranodons breeds, they

are hardly a threat to the ranodons there.

The influence of cattle

The negative influence of cattle on Ranodon sibiricus

has been mentioned by several authors (Kubykin

1986; Narbaeva and Brushko 1986; Brushko and Nar-

baeva 1988; Wang 1990; Dolmen et al. 1997). Dam-

age is mechanical when the cattle trample in the

brooks, crushing ranodons and destroying eggs. Their

excrements may also pose a threat to eggs and small

larvae.

In 1993, up to about 150 cows, watched by shep-

herds on horseback, twice daily crossed the brooks of

the study area. There were also flocks of horses, sheep

and goats. Corresponding numbers of domestic ani-

mals were seen in 1994 and 1995. Most crossing of

brooks took place in daylight at about 8 hrs. and 20

hrs., and at that time the adult and juvenile ranodons

were still relatively safe in their hiding places. Never-

theless, we twice found dead ranodons which had

been crushed under the feet of cows. On other occa-

sions, we came across mechanically damaged eggs,

presumably the victims of wading cattle. Larvae, too,

may suffer from cattle. However, we believe that the

damage to metamorphosed ranodons is not really

large (cf. Kubykin 1986).

Conclusions

Ranodon sibiricus is a nocturnal species in the juve-

nile and adult stages, whereas the activity of young

larvae is more evenly distributed through the day and

night. The difference in diel activity between larvae

and metamorphosed stages probably reduces intraspe-

cific competition and cannibalism. In daytime, the

ranodons hide cleverly in the brook bed or on land.

This secretive life makes them difficult to find, both

1999

Asiatic Herpetological Research

Vol. 8. p. 37

for diurnal predators and people. At night, however,

the ranodons are easy to see. Their nocturnality also

makes adult and juvenile ranodons less vulnerable to

mechanical damage from grazing cattle, but eggs and

larvae may easily be harmed.

Acknowledgments

Marina V. Basargina was our excellent interpreter and

good helper during all three field trips. Richard Binns

has kindly improved the language of the manuscript.

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ian and reptilian feeding ecology in the USSR. Herpe-

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odon sibiricus. Alytes 9:135-143.

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razmeshenie i razmernyy sostav populyatsii semirech-

enskogo lyagushkozuba v istokakh reki Borokhudzir

(Population number, local distribution and size com-

position of the Semirechensk salamander in the

sources of the Borokhudzir River). Pp. 181-186. In

E.V. Gvozdev (ed.), Redkie Zhivotnye Kazakhstana.

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kozub) (The Semirechensk salamander (lyagushko-

zub)). Izvestiya Akademii Nauk Kazakhskoy SSR,

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Shnitnikov, V.N. 1913. Neskol'ko dannykh o Semire-

chenskom tritone (Ranidens sibiricus Kessl.) (Some

data about the Siberian salamander (Ranidens sibiri-

cus Kessl.)). Ezhegodnik Zoologicheskogo muzeya

Akademii Nauk SSSR 18(53):1 18-122 (St. Peters-

burg).

Wang, Xiu-ling 1990. [Six unpublished abstracts on

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Oxford, Ohio.

1999

Asiatic Heij>etological Research

Vol. 8, pp. 38-42

The Hemipenes of Chinese Species of Deinagkistrodon and Gloydius

(Serpentes: Crotaiinae)

Peng Guo1, Fu-ji Zhang, and Yue-ying Chen

Chengdu Institute of Biology: the Chinese Academy of Sciences, Chengdu 610041, China

Abstract.- The hemipenes of eight species of two genera, Gloydius and Deinagkistrodon are described in detail

and illustrated. The results indicate that ( 1 ) the structures of hemipenes of Gloydius markedly different from that

of Deinagkistrodon, (2) more similarities are present among species of Gloydius. At the end of the paper, the

taxonomic relationships among species revealed by hemipenial structures are discussed.

Key words.- Serpentes, Crotaiinae, Deinagkistrodon, Gloydius, Hemipenes.

'Present address: Sichuan Yibin Teachers College. Yibin, Sichuan 644007. China.

Introduction

Since Cope has firstly implied the characters of reptil-

ian hemipenes to the classification in 1893, their

important value in the classification and phylogeny

was realized by more and more researchers around

world (Pope, 1935; Smith, 1943: Dowling et al., 1960;

Zhang et al., 1984; Zhang, 1986; Branch, 1988; Mao,

1989; Gloyd et al., 1990; Malnate, 1990). Although

some of hemipenes of Chinese Deinagkistrodon and

Gloydius were described (Pope, 1935; Smith, 1943;

Mao, 1989; Gloyd et al., 1990; Malnate, 1990) previ-

ously, the authors didn't illustrate them except Gloy-

dius brevicaudus and Deinagkistrodon acutus.

Prior to this paper, a comparative anatomy on

skull of these two genera was done (in press.), we

confirm that there are eight valid species of Deinagki-

strodon and Gloydius in China. At the present work,

the feathers of the hemipenes of these eight species

will be described in detail, and the taxonomic rela-

tionships indicated by their structures will also be dis-

cussed, they will provide additional and further data

for the classification and systematic of these species.

Material and Methods

The materials used in this study are based up forma-

lin-preserved adult specimens; all of them are depos-

ited in Chengdu Institute of Biology, the Chinese

Academy of Sciences. The number and locality of

examined and figured specimens are listed in Table 1 .

In this paper, the descriptive terminology gener-

ally followed literature (Dowling et al., 1960; Zhang

et al., 1984: Branch, 1986). In a majority of cases, the

fully everted hemipenes were illustrated. In a few

cases, the partly everted hemipenes were everted arti-

ficially. The drawings were done under the binocular-

dissecting microscope.

Results

Gloydius ussuriensis (Emelianov). The divided

hemipenis (Fig.l) extends to eighth subcaudal plate

and is forked opposite the third. While the Russia

(Kebrovka, Primorskiy Kray) specimens described by

Gloyd et al. (1990) and Malnate (1990) extend to the

eleventh subcaudal and are forked for eight subcau-

dals. It is spinous proximally, calyculate distally. The

transition from spines to calyces is inconspicuous.

The calyculate area is about equal to that of spinous

one. The calyculate edges are spinous. Over sixty

spines, they reduce in size distally and away from sul-

cus. Base of organ, proximal to the large spinous, is

beset with very minute spines. Centripetal sulcus dis-

tinct, forking near the crotch which is about the sec-

ond subcaudal, it ends at the tips of the organ. The lips

of sulcus are spinous and calyculate in the respective

areas of ornamentation.

The M. retractor penis magnus ends in the twenty-

third to twenty-fifth subcaudal, it is forked at the level

of the eleventh subcaudal before its insertion the dor-

sal organ. The dorsal lobe is one subcaudal longer

than the ventral lobe (in situ).

G. brevicaudus (Stejneger). The hemipenes (Fig. 2)

of the specimens from Anhui and Zhejiang extend to

the fifth to eighth subcaudal plate and are forked at the

level of the third to fourth subcaudal. Base of the

organ nude. The proximally half of the organ is

spinous and the other half calyculate. The calyculate

ridges bears tiny spines. Gloyd et al. (1990) also

described the hemipenes from Anhui, they were sure

that the lips of top calyces were smooth. The demar-

1999

Asiatic Herpetological Research

Vol. 8, p. 39

Table 1 . Material used in this study.

cation between the two areas is inconspicuous. In the

spinous area, there are about twenty-eight to thirty

spines, they become larger away from the sulcus. Sul-

cus prominent, it is forked at the second subcaudal

and ends at the tips of the organ. The lips of the sulcus

are spinous in the spinous area and calyculate in the

calyculate area. The M. retractor penis magnus origi-

nates at the level of the twenty-firth to twenty-fourth

subcaudal, and is forked for the length of two to four

subcaudals before its insertion the organ dorsal.

In this paper, three specimens from Liaoning,

which are dominated brevicaudus by Gloyd (1972),

were also examined, they are different from the form-

ers slightly. The calyce is restrict to the tips of the lob,

its extent is about fourth of the spinous one. The M.

retractor penis magnus, which is about ten to fourteen

in length, is shorter than the former one. it is forked

for the length of two subcaudals. The hemipenes of

two specimens examined extend to the seventh or

eighth subcaudal, and are forked at the level of the

fourth subcaudal, but the other one is much longer, it

extends to the twelfth subcaudal and is forked at the

level of the seventh subcaudal. Our observation is

consistent with Gloyd et al. (1990) and Malnate

(1990).

G. intermedius (Strauch). The hemipenis (Fig. 3) is

seven to eleven subcaudals in length, forked for the

length of four to five subcaudals. It is spinous proxi-

mally half, and the distally half of the organ is calycu-

late. The line of changing from spines to calyces is

inconspicuous. The calyces small adjacent to the sul-

cus but larger away from it, their lips bearing tiny

spines. About sixty spines are present in the spinous

area, they reduce in size distally and near the sulcus.

One or two strongly enlarged spines adjacent to the

sulcus at the crotch level. Small spines are found in

the base of the organ. The sulcus is forked at the level

of the second to the fourth subcaudal, it continues to

the tips of the lobes. The sulcus prominent, its lips are

spinous or calyculate in the respective area of orna-

gantation. M. retractor penis magnus originates at the

level of the twenty-seventh to twenty-ninth subcaudal,

it is forked for the length of two to four subcaudals

before its insertion at the organ tips.

G. saxatilis (Emelianov). The hemipenis (Fig. 4) of

this species extends to the ninth to the eleventh sub-

caudal plate, forked at the level of the third or forth

subcaudal. It is spinous proximally and calyculate dis-

tally. The spinous and calyculate areas are about equal

in length, the demarcation between two areas is incon-

spicuous. There are about sixty to seventy spines near

the crotch, including six much larger spines, four of

them appearing on the surface near the crotch, while

the other two are on the opposite side. The spines

reduce in size distally on the organ lobes. The margins

of the calyces are spinous. The base of the organ is

covered with tiny spines. While Gloyd et al. (1990)

previously described the specimens collected from

Korea (near Seoul), the organ base nude, the lips of

the distal cups are smooth. The sulcus is bifurcated at

the level of the second subcaudal and extends to the

tips of the organ, their lips are prominent, bearing a

few spines in the spinous area and calyces in the caly-

culate area. The M. retractor penis magnus originates

at the level of the twenty-fourth to twenty-fifth sub-

caudal, and is forked for the length of two to three

subcaudals before its insertion at the organ tips.

G. shedaoensis (Zhao). In this species, the hemipenis

(Fig. 5) is eight to ten subcaudals in length, and

forked for five to six subcaudals. The base of the

Vol. 8, p. 40

Asiatic Herpetological Research

1999

ttgl

Figure 1 . The right everted hemipenis of G. ussuriensis

(CIB785185, Panshi, Jilin)

Figure 2. The right everted hemipenis of G. brevicaudus

(CIB 726108, Taiping, Anhui)

Figure 3. The right everted hemipenis of G. interme-

dius (CIB 8010015, Xingyuan, Xinjiang)

Figure 4. The right everted hemipenis of G. saxatilis

(CIB 79I0090, R. Zhuang, Liaoning)

organ is covered with tiny spines. Spinouse proxi-

mally, calyculate distally. The margins of calyces are

tiny spines. The extent of calyces is about half of

spines. Line of changing from spine to calyces is

inconspicuous. There are ninety to one hundred spines

in the spinous area, and six especially larger spines in

each lobe. The sulcus prominent, forked at the level of

the third subcaudal, and extends to the tips of the

organ rami. Sulcus lips are spinous or calyculate in

the respective areas of ornamentation. The M. retrac-

tor penis magnus originates at the level of the twenty-

fourth to twenty-seventh subcaudal and is bifid for the

length of two to three subcaudals before its insertion

at the organ tips.

G. strauchii (Bedriaga). The hemipenis (Fig. 6)

examined extends to the seventh to eleventh subcau-

dal and is forked for four to five subcaudals. It is

spinous proximally half, and the distally half is caly-

culate. The line of changing from spines to calyces is

inconspicuous. The calyces are small adjacent to the

sulcus but larger away from it, their lips bearing tiny

spines. About sixty spines are present in the spinous

area, they reduced in size distally and near the sulcus.

One or two strongly enlarged spines are adjacent to

the sulcus at the crotch level. Small spines are present

in the base of the organ. The sulcus forks at the level

of the second to fifth subcaudal, and continues to the

tips of the lobes. The lips of the sulcus prominent,

they are spinous or calyculate in the respective areas

of ornamentation. M. retractor penis magnus origi-

1999

Asiatic Herpetological Research

Vol. 8, p. 41

nates al the level of the twenty-seventh to twenty-

Figure 5. The right everted hemipenis of G. shedaoensis

(CIB 79110006, Shedao, Liaonong)

Figure 6. The right everted hemipenis of G. strauchii

(CIB 755127, Hongyuan, Sichuan)

ninth subcaudal, and is forked for the length of two to

Figure 7. The right everted hemipenis of G qinlingensis

(840050, Qinling, Shaanxi)

four subcaudals before its insertion at the organ tips.

G. qinlingensis (Song). The hemipenis (Fig. 7)

extends to the eleventh subcaudal plate in length and

is forked at the level of the fifth subcaudal. Minute

spines are present in the base of the organ. It is

spinous proximally, calyculate distally, the spinous

area is about twice to third times as the calyculate

one. The line of demarcation between two areas is

inconspicuous. The calyculate edges are spinous,

there are approximately thirty to forty spines in the

spinous region. The sulcus bifurcates the fourth to

fifth subcaudal, terminates at the tips of the organ.

Sulcus is distinct, bearing spines in spinous area and

Figure 8. The right everted hemipenis of D. acutus (CIB

6416190, Fujian)

calyces in the calyculate one. The length of M. rec-

tractor penis niagnus extending is 14 subcaudals and

it is forked for the length of two subcaudals before its

insertion at the organ tips.

Deinagkistrodon acutus (Gunther). The hemipenis

(Fig. 8) extends to the eleventh to thirteenth subcaudal

and is forked opposite the fourth subcaudal, base of

organ nude. The proximally half of the organ is spi-

nouse, the distally half calyculate, the demarcation

between these two areas is distinct. The calyces with

smooth margins reduce in size distally and near the

sulcus. The spines are about sixth to seventy, they are

larger on the lateral surface of each lobe than those

Vol. 8, p. 42

Asiatic Herpetological Research

1999

near the sulcus. The sulcus forks at the level of the

fourth subcaudal, it extends to the tips of the each

lobe. The lips of sulcus prominent, they bearing caly-

ces in the calyculate region and smooth in the spinous

area. M. retractor penis magnus originates at the level

of the twenty-sixth subcaudal and is bifid for the

length of two to four subcaudals before its insertion at

the tips of the organ.

Discussion

The hemipenes are deeply forked in eight Chinese

species of pitvipers, the shape of the everted hemipe-

nes are "Y". It is spinous proximal ly and calyculate

distally. The centripetal sulcus is consistently bifur-

cated on the basal part of the organ in all of the spe-

cies examined, and it extends to the tips of the lobes.

These similarities reveal the taxonomic relationships

between genus Gloydius and Deinagkistrodon. The

deeply forking of the hemipenis and the bifurcation of

the sulcus in the basal region of the organ are exactly

like those of the other pitvipers (Pope, 1935; Smith,

1943).

D. acutus can be characterized by presence of the

fowling hemipenial structures: (1) the margins of the

calyces are smooth: (2) transition from spines to caly-

ces is abrupt and conspicuous: (3) the sulcus lips are

smooth in the spinous area: (4) the base of the organ is

naked. These conditions further confirmed the validity

of the independent generic status of Deinagkistrodon.

The seven species of Gloydius exhibit rather con-

servative and stable hemipenial structures, the inter-

specific variation is only limited to: ( 1 ) the length of

the hemipenes and the depth of their forking: (2) the

extent of the calyculate area on the lobes; (3) the

length of the retractor muscle and the depth of their

forking; (4) the manner of insertion of the retractor

muscle onto the organ; (5) the number of enlarge

spines. The results above indicated that the differenti-

ation of the hemipenial structures in Gloydius is little.

Acknowledgments

This project was supported by the Special Fund for

Classification & Fauna, the Chinese Academy of Sci-

ences (950633), and by Chengdu Diao Science Fund,

the Chinese Academy of Sciences.

The authors express their grateful appreciation to

Prof. E. M. Zhao, Chengdu Institute of Biology, the

Chinese Academy of Sciences, for providing literature

and reviewing the manuscript. We also thank the fol-

lowing people for presenting with studying speci-

mens: Prof. M. H. Huang. Zhejiang Medical

University: Prof. M. T Song, Shaanxi Institute of

Zoology; Prof. Y. H. Zhou, Xinjiang Normal Univer-

sity; Prof. K. C. Huang, Dalian Museum of Natural

History.

Literature Cited

Branch, W. R. 1986. Hemipenial morphology of Afri-

can snakes: a taxonomic review, part I: Scolecophidia

and Boidae. Journal of Herpetology 20(3): 285-299.

Dowling, H. G. and J. M. Savage. 1960. A guide to the

snake hemipenis: a survey of basic structure and sys-

tematic characters. Zoologica 45: 2, 17-28.

Gloyd, H. K. and R. Conant. 1990. Snakes of Agkistr-

odon Complex: A Monographic Review. Oxford

(Ohio), USA. 614pp.

Malnate, E. V. 1990. A review and comparison of

hemipenial structure in the genus Agkistrodon (sensu

lato). pp. 583-588. //;: H. K. Gloyd and R. Conant

(eds.), Snakes of Agkistrodon Complex: A Mono-

graphic Review. Oxford (Ohio), USA.

Mao, S. H., FY. Yin, and Y W. Guo. 1984. The hemi-

penes of common Taiwanese venomous snakes. Her-

petologica 40(4): 406-410.

Pope, C. H. 1935. The Reptiles of China, Natural His-

tory of Central Asia, X. American Museum Natural

History, New York. 604pp.

Smith, M. A. 1943. The fauna of British India, Ceylon

and Burma, including the whole of the Indo-Chinese

sub-region. Reptilia and Amphibia, vol. III-Serpentes.

Taylor and Francis, London. 583pp.

Zhang, F J.. S. Q. Hu. and E. M. Zhao. 1984. [Com-

parative studies and phylogenetic discussions on

hemipenial morphology of the Chinese Colubrinae

(Colubridae)]. Acta Herpetologica Sinica, new series

3(3): 23-44. (in Chinese).

Zhang, F J. 1986. [Comparative studies on hemipe-

nial morphology of the Chinese Opisthoglyph genera

(Reptilia: Colubridae)]. Acta Herpetologica Sinica,

new series 5(4): 166-170. (in Chinese).

Zhao, E. M. and K Adler. 1993. Herpetology of

China. Oxford (Ohio), USA. 522pp.

1999 Asiatic Herpetological Research Vol. 8, pp. 43^47

Catalogue of Type Specimens of Reptiles in the Herpetological Collections of

Chengdu Institute of Biology, the Chinese Academy of Sciences

Peng Guo1, Fu-ji Zhang, and Yue-ying Chen

Chengdu Institute of Biology, The Chinese Academy of Sciences, Chengdu, Sichuan 610041, China

Abstract.- There are nearly 15,000 specimens and 300 species of Chinese reptiles that are preserved in the

herpetological collections of Chengdu Institute of Biology (CIB), the Chinese Academy of Sciences, these

species are over 70% of the known species in China. Most of these specimens were collected by the scientific

research personnel in the herpetology department of CIB in sixty years. In these specimens there are about 400

type series specimens (28 species or subspecies) which were selected by the scientific research personnel in the

herpetology department of CIB when they described the new taxon. In order to reflect the achievements in

scientific research on Chinese reptiles in CIB and provide the facility to scientific research and academic

exchange, it is helpful to list all of the type specimens in the collections.

Key words.- Reptiles, type specimens, Chengdu Institute of Biology, China.

'Sichuan Yibin Teachers Colleae. Yibin, Sichuan 644(X)7, China.

LACERTILIA

AGAMIDAE:

Calotes medogensis Zhao and Li, 1984

Acta Herpetol. Sin., Chengdu, [new ser.], 3(4): 77.

Holotype: CIB 8370177, Male;Yarang, Medog Co., Xizang Autonomous Region; 910 m; Coll. S. Q. Li, 7.

23, 1983.

Japalura szechwanensis Hu and Zhao, 1966

Acta Zootaxon. Sin., Peking, 3(2): 158.

Holotype: CIB 613047, Male: Baishui He, Peng Co., Sichuan Prov.; 2000 m; Coll. C. C. Liu; 5. 9, 1961.

Allotype: CIB 6130460, Female; the same locality and time as holotype.

Paratype: CIB 625131, Male; Mt. Erlang, Tianquan Co., Sichuan Prov.; 1400 m; 8, 1962.

Laudakia papenfussi Zhao, 1998

Zoological Research, Kunming, 19(5): 401.

Holotype: CIB 775001, Male: Mayang River Valley between Mayang Village and Diya Village, Zanda Co.,

Xizang Autonomous Region; 3300 m; Coll. R. Z. Zhang; 7. 1, 1976.

Laudakia wui Zhao, 1998

Acta Zootaxon. Sin., Beijing, 23(4): 440.

Holotype: CIB 7315012, Male; Yi'ong, Bomi Co., Xizang Autonomous Region: 2350 m: Coll. Y. M. Jiang;

6. 11, 1973.

Allotype: CIB 7315014, Female; the same locality and date as the holotype.

Paratypes: CIB Nos. 731501 1, 7315013, Females. CIB Nos. 7315008-10, Juveniles; the same locality and

date as the holotype; CIB Nos. 73115037-38, Juveniles; between Tangmai and Yi'ong, Bomi Co.,

Vol. 8, p. 44 Asiatic Herpetological Research 1999

Xizang Autonomous Region; 2150 m; Coll. X. E. Wu; 7. 5, 1973.

Phrynocephalus vlangalii hongyuanensis Zhao, Jiang, and Huang , 1980

Acta Zool. Sinica, Beijing, 26(2): 178.

Holotype: CDS 785795, Male: Coll. E. M. Zhao: 7. 25, 1978.

Allotype: CIB 785825, Female; Coll. Y. M. Jiang; 8. 2, 1978.

Paratypes: CIB Nos. 7551 1 1-12, 7551 14-15, 785793-94, 785796-824, 785826-27. 7 Males and 27 Females;

Coll. Y. Gao; 8, 1978.

Hongyuan Co., Sichuan Prov.: 3500 m.

=Phrynocephalus hongyuanensis Zhao, Jiang, and Huang , 1980

Ref: Y Z. Wang and Y M. Jiang, (1992), in: Y. M. Jiang (ed.). Coll. Papers Herpetol., Chengdu: 111.

Phrynocephalus zetangensis Wang, Zeng, and Wu, 1996

Zoological Research, Kunming, 17(1): 27.

Holotype: CIB 0156, Male.

Allotype: CIB 0157, Female.

Paratypes: CIB 0151, Male: CIB Nos. 0154, 0158, Female; CIB 0155, Juvenile.

Zetang, Xizang Autonomous Region; 3950 m; Coll. Z. L. Fang and Z. J. Liu: 7. 5, 1993.

GEKKONIDAE:

Tenuidactylus medogensis Zhao and Li, 1987

Acta Herpetol. Sin., Chengdu, [new ser.], 6(1 ): 48.

Holotype: CIB 8380188, Female.

Paratype: CIB 8380187, Juvenile ( Male ?).

Kabu, Medog Co., Xizang Autonomous Region; 1250 m; Coll. S. Q. Li; 1983.

=Cyrtodactylus medogensis (Zhao and Li, 1987)

Ref: Zhao, E. M. and K. Adler, (1993), Herpetology of China, Oxford (Ohio), p: 179.

SCINCIDAE:

Eumeces liui Hikida and Zhao, 1989

Copeia, Gainesville, ( 1 ): 111.

Allotype: CIB 645026. Male; Wuchang, Hubei Prov.: 3. 31, 1965.

Scincella huanrenensis Zhao and Huang, 1982

Acta Herpetol. Sin., Chengdu, [new ser.], 1(1 ): 3.

Paratypes: CIB Nos. R810012, R810014, R810015-18, R810040-41; Huanren Co., Liaoning Prov.; 700 m;

Coll. K. C. Huang; 5. 8, 1981.

Leiolopisma tsinlingensis Hu and Zhao, 1966

Acta Zool. Sin., Peking, 1 8( 1 ): 82.

Holotype: CIB 627050, Male; 1800 m; Coll. G. F Wu and E. M. Zhao; 6. 13, 1962.

Allotype: CIB 627039, Female: 1820 m: 6. 10, 1962.

Paratypes: Cib Nos. 627025-27, 627029, 627051-53, Males, CIB Nos. 627020-24, 627034-36, 627040-

627049, 627069, Females, OB Nos. 627028, 627030-32, 627054-62, 627070, Juveniles.

Mt. Tsinling [= Qinling], Chouchih [= Zhouzhi Co.], Shaanxi Prov..

=Scincella tsinlingensis (Hu and Zhao, 1966)

Ref: Y Z. Wang and E. M. Zhao, (1986), Acta Herpetol. Sin., Chengdu, [new ser.], 5(4): 276.

1999 Asiatic Herpetological Research Vol. 8, p. 45

SERPENTES

XENOPELTIDAE:

Xenopeltis hainanensis Hu and Zhao, 1972

Key Chin. Snakes [= Mater. Herpetol. Res., 1 1, Chengdu: 36.

Holotype: Cib 64III6016, Male; Dali, Mt. Diaoluo, Hainan Prov.; 200 m: 5. 15, 1964.

Allotype: CIB 64III6650, Female; Yacha Matou, Baisa Co., Hainan Prov.; 217 m; 9. 4, 1964.

=Xenopeltis hainanensis hainanensis Hu and Zhao, 1972

Ref: E. M. Zhao, (1995), Sichuan Jour. Zool., Chengdu, 14(3): 107.

COLUBRIDAE:

Achalinus meiguensis Hu and Zhao, 1966

Acta Zootaxon. Sin., Peking, 3(2): 162.

Holotype: CIB 639101, Female; Liang He Kou, Meigu Co., Sichuan Prov.; 2520 m; Coll. X. Y Tang; 5. 22,

1963.

Paratypes: CIB Kang076, Female: Tu Ba Kou, Baoxing Co., Sichuan Prov.; CIB Nos. 561836-37, 570080,

Female, CIB Nos. 562154, 562174, 600030, Male; Mt. Omei, Sichuan Prov..

Natrix optata Hu and Zhao, 1966

Acta Zootaxon. Sin., Peking, 3(2): 160.

Holotype: CIB Chuan3624, Male: Liangfeng Gang, Mt. Omei, Sichuan Prov.: 700 m; Coll. C. C Liu; 8. 9,

1940.

Paratypes: CIB Nos. 561760, 562168, 562221, 570072, 600039, 645201, Males, Cib Nos. R001, 561764,

562167, 562231, Females, 2 Juveniles; Mt. Omei, Sichuan Prov.; 1956-1960.

=Amphiesma optata (Hu and Zhao, 1966)

Ref: E. M. Zhao and Y M. Jiang, ( 1986), Acta Herpetol. Sin., Chengdu, [new ser.], 5(3): 239.

Dinodon rosozonatum Hu and Zhao,1972

Key Chin. Snakes [= Mater. Herpetol. Res., 1 ], Chengdu: 36.

Holotype: CIB 64III6089, Male; Dali, Mt. Diaoluo, Hainan Prov.; 200 m; 5. 21, 1964.

Allotype: CIB 64III5246, Female; Mt. Wuzhi, Hainan Prov.; 540 m: 5. 1 1, 1964.

Paratypes: 3 Males and 5 Females; Mt. Diaoluo, Mt. Wuzhi and Haikou, Hainan Prov.; 80-580 m; 1964-

1972.

Macropisthodon rudis multiprefrontalis Zhao and Jiang , 1981

Acta Herpetol. Sin., Chengdu, [old ser.], 5(7): 55.

Holotype: Cib 6515143, Male; Xichang, Sichuan Prov.; 2650 m; Coll. C. C. Liu; 6. 8, 1965.

Allotype: CIB 6515142, Female; Xichang, Sichuan Prov.: Xichang, Sichuan Prov.; 2650 m: Coll. G. F. Wu:

6. 8, 1965.

Paratypes: CIB Nos. 6515001, 65II5148, Males, CIB Nos. 6515034, 65U5012, Females, CIB 580960, Juve-

nile; Huili Co., Zhaojue Co., Yuexi Co., and Ganluo Co., Sichuan Prov.; 2000-2630 m; Coll. D. Y

Yang; 8, 1958 and 5-6, 1965.

Oligodon mulizonatum Zhao and Jiang, 1981

Acta Herpetol. Sin., Chengdu, [old ser.], 5(7): 54.

Holotype: CIB 80II0289, Male.

Allotype: CIB 80II0290, Male, CIB Nos. 80II0274, 80II0291, Juveniles.

Luding Co., Sichuan Prov.; 1400 m; 8. 17, 1980.

Opisthotropis guangxiensis Zhao, Jiang, and Huang, 1978

Vol. 8, p. 46 Asiatic Herpetological Research 1999

Mater. Herpetol. Res., Chengdu, 4: 21.

Holotype: CIB 602488, Male; Mt. Yao [ = Dayao Shan ], Guangxi Prov.; 6. 19, 1960.

Allotype: CIB 601588, Female; Mt. Yao [ = Dayao Shan ]. Guangxi Prov.; 4. 28, 1960.

Paratype: CIB 603583, Female; Longsheng Co., Guangxi Prov.; 7. 2, 1960.

Plagiopholis unipostocularis Zhao, Jiang, and Huang, 1978

Mater. Herpetol. Res. Chengdu, 4: 21.

Holotype: CIB 505121, Female; Yunnan Prov..

Rhabdophis adleri Zhao, 1997

Asiat. Herpetol. Res., Berkeley, 7: 166

Holotype: CIB 64III5917, Male; Dali Village in Mt. Diaoluo. Lingshui Co., Hainan Prov.; 225 m: 6. 10.

1964.

Allotype: CIB 64HI5228, Female; Mt. Wuzhi, Qiongzhong Co.. Hainan Prov.; 500 m: 5. 10, 1964.

Paratypes: CIB Nos. 64IU51 12, 51 14-15, Females; 4. 24-25, 1964; CIB 64III5883, male, CIB 64III5441,

Juvenile, 6. 1-9, 1964; Mt. Diaoluo, Lingshui Co., Hainan Prov.; 82-217 m; CIB 64III6612, Juvenile;

Mt. Yinggeling, Baisha Co., Hainan Prov.; 670 m; 8. 25, 1964.

Rhabdophis nuchalis pentasupralabralis Jiang and Zhao, 1983

Acta Herpetol. Sin., Chengdu, [new ser.], 2(1 ): 60.

Holotype: CIB 80110040, Male; 2750 m; Coll. E. M. Zhao; 7. 26, 1980.

Allotype: CIB 80II0056, Female: 2750 m; Coll. Y M. Jiang; 7. 26, 1980.

Paratypes: 95 Males, 48 Females, and 65 Juveniles; 2750-2850 m; 7. 24-28, 1980.

Jiulong Co.. Sichuan Prov..

=Rhabdophis pentasupralabralis Jiang and Zhao, 1983

Ref: E. M Zhao, (1995), Jour. Suzhou Rail. Teach. Coll. (Nat. Sci.), Suzhou (Jiangsu), 12(2): 38.

Sibynophis chinensis miyiensis Zhao and Kou, 1987

Chin. Herpetol. Res., Chengdu, No. 1: 4.

Holotype: CIB 105027, Male; Miyi Co., Sichuan Prov.: 880 m: Coll. S. H. Kang: 6, 1986.

Allotype: CIB 105025, Female; Miyi Co., Sichuan Prov.; 880 m; Coll. S. H. Kang; 6, 1986.

Paratypes: CIB Nos. 105026, 105028, 105030-31, Males; CIB 105029. Female; Lugu Lake, Sichuan- Yun-

nan border; 2600 m; Coll. Z. T. Kou; 1985.

VIPERIDAE:

Trimeresurus mangshanensis Zhao, 1990

Sichuan Jour. Zool., Chengdu, 9( 1 ): 11.

Holotype: CIB ZS8901, Female.

Paratype: CIB ZS8902, Female.

Pingkeng, Mt. Mang, Yizhang Co., Hunan Prov.; 700-900 m; Coll. G. H. Chen and Y L Tao; 9, 1989.

=Ermia mangshanensis (Zhao, 1990)

Ref: Zhang, F. J., ( 1993), in: Zhao. E. M. et al. (eds.), Proceedings of the First Asian Herpetological Meet-

ing, Beijing, p: 56.

Agkistrodon shedaoensis Zhao, 1979

Acta Herpetol. Sin., Chengdu, [old ser.], 1( 1 ): 4.

Holotype: CIB 7910005, Male; Shedao, Liaoning Prov.; 5. 19, 1979.

=Gloydius shedaoensis (Zhao, 1979)

Ref: A. R. Hoge et al. , ( 1978/79), Poisonous Snakes of the World. Part I. Check list of the Pit Vipers Viper-

oidae, Viperidae, Crotalinae. Mem. Inst. Butantan, Sao Paulo, 42/43. p: 194.

Trimeresurus monticola zayuensis Jiang, 1977

1999 Asiatic Herpetological Research Vol. 8, p. 47

Acta Zool. Sin., Beijing, 23( 1 ): 67.

Holotype: CIB 7315024, Male; 1800 m; 7. 22, 1973.

Allotype: CIB 7315025, Female: 2070 m: 7. 30. 1973.

Paratype: CIB 73II5349, Male; 1965.

Zayu Co., Xizang Autonomous Region.

=Ovophis zayuensis (Jiang, 1977)

Ref: E. M. Zhao. (1995). Jour. Suzhou Rai. Teach. Coll. (Nat. Sci.), Suzhou (Jiangsu), 12(2): 37.

Ovophis monticola zhaokentangi Zhao, 1995

Sichuan Jour. Zool., Chengdu. 14(3): 109.

Paratype: CIB 740003, Male; Pianma, Lushui Co., Yunan Prov.; 1980 m; 3. 17, 1974.

Tritneresurus medoensis Zhao, 1977

Acta Zool. Sin., Peking, 23( 1 ): 66.

Holotype: CIB 73II5208, Male; 1200 m; Coll. E. M. Zhao and Y. Gao.

Allotype: CIB 73II5209, Male; 1400 m; Coll. E. M. Zhao and X. E. Wu.

Near A-nie Bridge, Medog Co., Xizang Autonomous Region; 8. 3, 1973.

Tritneresurus stejnegeri ehenbihuii Zhao, 1995

Sichuan Jour. Zool., Chengdu, 14(3): 1 10.

Holotype: CIB 64III5599. Male: Mt. Diaoluo, Lingshui Co., Hainan Prov.; 250 m: 6. 6, 1966.

Allotype: CIB 64III5945, Female; Mt. Diaoluo, Lingshui Co., Hainan Prov.; 250 m: 6. 11, 1966.

Paratypes: CIB Nos. 64ID.5906, 64III5944, 641115978-79, 64IB6013, 641116043-44, 64III6069, 64III6101,

64III6104, 64III6107, Males; 64III5600, 64III5735, 64HI6014, Females; Mt. Diaoluo, Lingshui Co..

Hainan Prov.; 225-290 m; 6. 6-15, 1964. CIB Nos. 64IH5110, 64III5181, 641115261-62, Males; Mt.

Wuzhi, Qiongzhong Co. Hainan Prov.; 500 m: 4. 23-5. 12, 1964.

Tritneresurus xiangchengensis Zhao, Jiang, and Huang, 1978

Mater. Herpetol. Res., Chengdu, 4: 21.

Holotype: CIB 725050, Male; 3100 m; 10. 7, 1972.

Allotype: CIB 725049, Female; 3200 m.; 10.10, 1972.

Paratypes: CIB 725048, Male; CIB Nos. 725051-57, 5 Females and 2 Juveniles; Xiangcheng Co., Sichuan

Prov.: 3000-3200 m; 10. 1-28, 1972.

Acknowledgments

We wish to express our deep gratitude to Prof. Er-Mi Zhao for reviewing the manuscript and offering suggestion.

This project is supported by the Special Fund for Biology Collections, the Chinese Academy of Sciences, and by

Chengdu Diao Sciences Fund, the Chinese Academy of Sciences.

1999

Asiatic Herpetological Research

Vol. 8. pp. 48-52

Correlations of Reproductive Parameters of Two Tropical Frogs from Malaysia

Ibrahim H. Jaafar1, Ahmad Ismail2, and Abd-rahman Kurais2

Biological Sciences Program, School Of Distance Education, Universiti Sains Malaysia, 11800, Minden,

Penang, Malaysia. "Department of Biology, Faculty of Science and Environmental Studies, Universiti Putra

Malaysia, 43360. UPM, Selangor, Malaysia.

Abstract.- A study on the relationships of reproductive parameters such as fecundity, egg size, clutch weight and

body size of two frogs, Rana cancrivora (Gravenhorst) and R. limnocharis (Boie), from Malaysia was carried

out in February 1992. The results showed that all the parameters quantified were greater in R. cancrivora than in

R. limnocharis. No correlation was found between the spawned clutch size and egg size for both species.

However, correlation analyses of unspawned clutch showed that there exist positive relationships between female

size and clutch size, female size and clutch weight, female size and egg weight, clutch size and clutch weight,

and clutch weight and egg weight in R. cancrivora. For R. limnocharis positive correlations were found between

clutch size and clutch weight, and clutch weight and egg weight for the unspawned complement. The advantages,

non-advantages, correlation and non-correlations of these parameters with respect to their reproductive strategies

and success of these frogs are discussed and compared with the current information from the literature.

Key words.- Aiiura, Ranidae, Rana cancrivora, R. limnocharis, Malaysia, reproductive parameters, female size,

clutch size, egg size, clutch weight, egg weight.

Introduction

The fecundity or clutch size in amphibians is highly

variable depending on body size and reproductive

mode (Salthe, 1969: Salthe and Duellman, 1973:

Kaplan, 1980). As a general rule, large species pro-

duce more eggs than smaller ones and species that

have generalized reproductive modes have larger

clutches than those with specialised modes (Duellman

and Trueb, 1986). The fecundity and hatching success

of an amphibian population play an important role in

the propagation and future survival of the population

(Ibrahim and Ahmad, 1992). Reproductive success of

a female depends upon the number of eggs produced

and their quality, but are constrained by physiological

capacities of the female and the trophic quality of the

environment (Rafinska, 1991). The number of eggs

deposited by amphibians varies greatly from species

to species and this large disparity in fecundities is

explained by differences among amphibians in sizes

of eggs, patterns of development, sizes of females and

reproductive behaviour (Porter, 1972: Salthe and

Duellman. 1973: Kuramoto, 1978; Kaplan, 1980).

Studies on the fecundity of temperate frogs have gen-

erated considerable data on this facet of amphibian

reproduction (Collins, 1975: Kuramoto, 1978; Duell-

man and Trueb, 1986), but information on tropical

oriental species are few and far between. Berry (1964)

reported that seven anuran species in Singapore

exhibited difference in fecundities between and within

species, while four species of frogs from Malaysia

also showed differences in fecundities both between

and within species (Ibrahim and Ahmad, 1992). Inger

and Bacon (1968) found that four large ranids in

Borneo have clutch sizes in excess of a thousand eggs,

while Yorke (1983) reported that the average clutch

size for a rhacophorid in Malaysia to be 225 eggs.

Ovum size is another important aspect of anuran

reproductive biology. Large ovum size is generally

associated with large female body size and thus

directly hints of better fitness and survival value. Egg

size variability in amphibians has been interpreted as

adaptive since, where breeding habitats vary unpre-

dictably, production of a wide range of sizes may

enhance adult fitness more than does the output of a

single 'optimal' egg size (Tejedo and Reques, 1992).

The egg size of numerous temperate anurans are well

documented in the literature (e.g. Salthe, 1969; Salthe

and Duellman, 1973; Bell and Lawton, 1975; Collins,

1975; Kuramoto, 1978; Jorgensen, 1981; Duellman

and Trueb, 1986; Reading, 1986; Rafinska, 1991;

Tejedo and Reques, 1992), but again however, only a

few reports concerning this parameter are available

for tropical species (e.g. Liem, 1959; Alcala, 1962;

Inger and Bacon, 1968; Uchiyama et al., 1990).

Rana cancrivora (Gravenhorst) and R. limno-

cluiris (Boie) are two species of anura that have a

wide distribution across the oriental zoogeographical

realm (Church, 1960: Alcala, 1962; Berry 1964;

Inger, 1966; Kuramoto, 1978). In spite of this only a

1999

Asiatic Herpetological Research

Vol. 8, p. 49

handful of information have been published concern-

ing the fecundity and size of their eggs (Alcala, 1962;

Berry, 1964; Kuramoto. 1978). It is also evident from

the literature that there exist considerable variations in

the relationships of body size, egg size and fecundity

within the Amphibia (Salthc, 1969; Collins, 1975;

Kuramoto, 1978; Jorgensen, 1981; Reading, 1986;

Duellman and Trueb, 1986). This paper therefore

determines the fecundity and egg size of both R. can-

crivora and R. limnocharis and then examines the

existing relationships in the reproductive parameters

of both frogs.

The Study Site

The place chosen for the study is a rice growing

region near the small town of Tanjung Karang (3°

20'N. 101° 10'E), in the state of Selangor, elevation

about 3 m above mean sea level. It is situated about

100 km to the northwest of Kuala Lumpur, the Malay-

sian capital. Previously this area was a freshwater peat

swamp forest which was opened up and converted to

paddy fields by settlers in the 1920's. Presently due to

the improved and upgraded irrigation and drainage

system, the farmers are planting two rice crops a year.

Material and Methods

To determine the fecundity and egg size of spawned

eggs, newly deposited egg clutches of both species

were collected from recently innundated rice fields.

Breeding choruses were visited, amplecant pairs of

frogs were located and their positions marked with

wooden pegs. Male frogs usually start calling as soon

as dusk sets and individuals of both species usually

initiated mating as soon as the males begin clasping

the females. This usually occurs at around OlOOhrs or

0200 hrs. The pairs will then move into the flooded

rice paddy and egg laying will occur around 0500 hrs.

The number of eggs in each clutch were then recorded

and the eggs collected and preserved in 4% formalin

and kept in labeled, airtight plastic 40 dram bottles. In

the laboratory, 30 to 50 eggs from each clutch were

then randomly chosen and their diameters measured

under a stereo microscope with an ocular micrometer

to determine the mean size of eggs of each species.

All eggs measured were between Stages 3 and 9 of

Gosner(1960).

To investigate the relationship between female

body size and, (a) the number of unspawned eggs, (b)

weight of unspawned egg clutch and (c) the weight of

unspawned eggs, the snout-urostyle length of gravid

females with large pigmented ova in the oviducts

were measured, the unspawned egg complement were

weighed (clutch weight) and counted (clutch size or

fecundity). This is a modified method of Kuramoto

( 1978). Inger and Bacon (1968) reported that in most

Indomalayan frogs the eggs in the ovary are esscn

tially in two size classes : an enlarged or developing

set and a much smaller, white "undeveloped set' ; the

latter contributes no significant portion to the total

volume of the ovary.

Results

Forty-two spawned batches of R. cancrivora eggs and

thirty-four of R. limnocharis were collected from the

field in February 1992. These were investigated for

fecundity and size of spawned eggs. In addition thirty-

two batches of R. cancrivora eggs and thirty of R. lim-

nocharis were obtained from sacrificed gravid

females.

The results showed that the average number of

eggs laid by R. cancrivora females from Tanjung

Karang is 1077.9 (sd = ± 238.97, range 662 tol677).

That for R. limnocharis 405.5 (sd = ± 92.45, range

233 to 657). Weighted t-test for unequal variance

(Cochran and Cox, 1957) showed that the number of

eggs oviposited by R. cancrivora is significantly

greater than that laid by R. limnocharis (t = 16.751, p

<0.001,df=74).

The mean diameter of R. cancrivora eggs is 1.35

mm (sd = ±0.091, range 1.16 to 1.53) while the mean

diameter of R. limnocharis eggs is 1.15 mm (sd = ±

0.027, range 1.10 to 1.21). Again a weighted t-test for

unequal variance showed that the egg size for both

species is significantly different (t = 12.980, p <

0.001, df =74). However, no correlation was found

between the spawned clutch size and egg size for both

species.

For clutch complement of unspawned R. cancriv-

ora eggs, the average clutch size was 2904.6 (sd = ±

1600.6, range 889 - 7573), the average clutch weight

was 2.25 g (sd = ± 1.726, range 0.37 - 5.71) and the

average egg weight was 0.75 mg ( sd = ± 0.257, range

0.28 - 1.35). The same parameters for R. limnocharis

was 702.6 (sd = ± 306.49, range 312 - 1659), 0.40 g

(sd = ± 0.264, range 0.074 - 1.04) and 0.55 mg ( sd =

± 0.249, range 0.237 - 1.01) respectively. Weighted t-

tests for unequal variance on the clutch size, clutch

weight and egg weight between the two species

showed that these parameters were significantly dif-

ferent ( t = 7.634, p < 0.001, df = 60; t = 6.799, p <

0.001, df =60; and t = 3.019, p < 0.05, df = 60 respec-

tively).

Correlation analyses carried out on the reproduc-

tive parameters of unspawned eggs for each species

showed that for R. cancrivora there is a positive corre-

Vol. 8, p. 50

Asiatic Herpetological Research

1999

lation between female size and clutch size (p < 0.001,

r = 0.6333), female size and clutch weight (p< 0.001, r

= 0.6867), female size and egg weight (p < 0.05, r =

0.4073), clutch size and clutch weight (p < 0.001. r =

0.8870) and clutch weight and egg weight (p < 0.001.

r = 0.5983). There was no statiscally significant corre-

lation between clutch size and egg weight. For R. lim-

nocharis however, there exists positive correlation

between clutch size and clutch weight (p < 0.001, r =

0.7501 ) and clutch weight and egg weight (p < 0.001,

r = 0.6818) only, while no correlation was found

between female size and clutch size, female size and

clutch weight, female saize and egg weight, and

clutch size and egg weight.

Discussion

The number of eggs oviposited by breeding females

of both species were lower than that found in their

ovaries. This is not unexpected because presumably

the breeding females were depositing the complement

of eggs that were mature and retaining the unripe ones

for later oviposition ( Inger and Bacon, 1968; Telford

and Dyson, 1990). It is likely that both females of/?.

cancrivora and R. limnocharis in Tanjung Karang

may breed more than once during the breeding sea-

son. Wells (1976) concluded that one of the major

advantages of a prolonged breeding period may be the

capacity for females to breed twice or more in a single

season. Hence it is possible that as a security measure

the females only release a portion of eggs from their

ovarian complement. The incidence of multiple

clutches is not uncommon in amphibians and have

been reported in anumber of anuran species (Collins,

1975; Howard, 1978; Perril and Danial, 1983; Telford

and Dyson, 1990; Rafinska, 1991).

Alcala (1962) and Uchiyama (1990) reported that

the clutch size for R. cancrivora was probably more

than 2000 and 1800 eggs respectively. Our study

found a lower clutch size than these two. Berry (1964)

presented data on the number of ovarian eggs in Sin-

gaporean R. limnocharis. Calculations based on her

data gave the average clutch size for her samples as

576.4 eggs (range 266-1318). This is comparable to

the results of this study. However, Kuramoto (1978)

reported larger clutch size, clutch weight and egg

weight for R. limnocfiaris from Japan. This discrep-

ancy could be due to the clinal effect within the spe-

cies (Duellman and Trueb, 1986) or even

geographical differences, since the Japanese frog

would be at the northernmost edge of its distribution.

The difference in egg size between different dif-

ferent populations of amphibian species have been

attributed to adaptation of the population to their par-

ticular environment (Pettus and Angleton, 1967;

Salthe and Duellman. 1973; Jorgensen, 1981). There

exists a positive correlation between egg size and

hatchling size in frogs (Salthe and Duellman, 1973)

and a large metamorphic size is important because of

the interrelationship of body size, time of metamor-

phosis, age at first reproduction and fecundity ( Wil-

bur, 1972; Wilbur and Collins, 1973; Doty, 1978).

Thus the observed larger egg size of R. cancrivora

over R. limnocharis could probabaly be assumed to

confer reproductive advantage with respect to fecun-

dity, and could probably also be assumed to do the

same with respect to metamorphic size, post meta-

morphic growth and age at first reproduction.

The interspecific differences in the sizes of eggs in

amphibians is well documented in the literature (Inger

and Bacon, 1968; Collins, 1975; Kuramoto, 1978;

Duellman and Trueb, 1986). For example. Collins

(1975) found that there is significant difference in

average egg diameter between Hyla versicolor, R. syl-

vatica, Bufo americanus and R. catesbeiana, while for

H. crucifer and Psuedoacris triseriata there was no

significant difference. Generally this reflects the great

variety in amphibian species with respect to egg pro-

duction, reproductive modes and other demographic

parameters (Salthe and Duellman, 1973; Kuramoto,

1978; Kaplan, 1980; Duellman and Trueb, 1986) as

well as the diversity of adaptations to the different

array of environmental selection and pressure. Pheno-

typic plasticity related to female age, size, trophic

conditions and genetic factors also contribute to the

observed egg size variation in amphibians (Berven,

1982; Rafinska, 1991). Hence it is not surprising that

there exists significant difference in egg size between

R. cancrivora and R. limnocharis in this study since ,

as mentioned earlier, a number of workers have con-

cluded that within a reproductive mode, the greater

the female size, the larger will be the ovum size

(Salthe and Duellman, 1973; Kuramoto, 1978;

Kaplan, 1980).

For R. cancrivora in this study, there exist positive

correlations between female size and clutch size,

female size and clutch weight, clutch size and clutch

weight, and clutch weight and egg weight. Since body

size is an indication of body condition, the high corre-

lation between body size and clutch size is expected

(Reading, 1986). Other workers also found that there

is a positive relationship between clutch size and

female body size (Pettus and Angleton, 1967; Salthe

and Duellman, 1973; Collins, 1975; Howard, 1978;

Kuramoto, 1978; Banks and Beebee, 1986; Gibbons

and McCarthy, 1986; Reading, 1986). The positive

relationship between clutch size and clutch weight.

1999

Asiatic Herpetological Research

Vol. 8, p. 51

and clutch weight and egg weight in R. cancrivora is

also anticipated because generally speaking, the

greater the egg number, the greater will be the clutch

weight, and the greater the egg weight, the higher the

clutch weight. Kuramoto (1978) also found the same

phenomenon in some of his Japanese anurans and

similarly Reading ( 19861 found that there was a trend

as a whole in the population of British B. bufo for egg

weight, egg number and ovary weight to increase with

female size.

Collins (1975) reported that there was positive

correlation between egg diameter and female body

size in R. sylvatica, H. versicolor and B. americanus

from Michigan. Banks and Beebee (1986) found that

snout-vent lenght is correlated with egg size in B.

calamita from England and suggested that this was, in

part, an adaptation to survive in habitats with erratic

pond provisions. However, in this study no correlation

could be found between female body lenght and egg

size (as quantified by egg weight) in both R. cancriv-

ora and R. limnocharis, nor could Kuramoto (1978)

find a relationship between female body weight and

egg weight in R. limnocharis, R. tagoi, R. hrevipoda,

H.japonica and Rhacophorus schlegelii. He attributed

this event to the fact that all these species are lentic

water-breeding frogs that generally produced their

egg output, not in smaller number of large eggs but in

larger number of small eggs. Thus no obvious advan-

tage is procured in producing large eggs by large

females. Also Jorgensen ( 1981 ) reported that egg size

is not directly related to body size in R. temporaria in

Denmark, while Howard (1978) wrote that the aver-

age egg size for R. catesbeiana from Michigan is not

correlated to female size. Rafinska (1991) found no

correlation between egg size and snout-vent lenght in

European Bombina bombina, and Collins (1975) also

found no statistically significant correlation between

egg diameter and female body size in P. triseriata, H.

crucifer and R. catesbieana. Why some species exhib-

ited correlation between female size and egg size

while others do not lack complete explaination at this

point, and even Howard (1978) was convinced that the

underlying reasons for such relationships remain

unclear.

It is thus evident that variations occuring in the

relationships of reproductive parameters in various

amphibian species are results of selective forces and

environmental constraints that shape their life history

traits such that a species will optimize reproductive

energy into producing the optimum number of off-

springs to ensure future survival and continuance of

the species. And since anuran species occupy various

and diverse types of habitats and have different types

of reproductive strategies, they are thus subjected to

various differences in environmental pressures to

which they must adapt in order to survive and prosper.

This then manifests into the huge variability of

amphibian reproductive demography as what we are

witness to today.

Acknowledgments

The authors wish to express their gratitude to Univer-

siti Putra Malaysia for use of facilities, and to the

Malaysian Government for financing the project

under the Intensified Research in Priority Areas Grant.

The participation of IHJ was made possible through a

study grant from the Univcrsiti Sains Malaysia.

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1999

Asiatic Herpetological Research

Vol. 8, pp. 53-59

Utilization of Energy and Material in Eggs and Post-hatching Yolk in an

Oviparous Snake, Elaphe taeniura

XlANG Jl', PlNG-YUE SUN1, SHUI-YU FU2, AND HUA-SONG ZHANG2

Department of Biology, Hangzhou Normal College, Hangzhou 310036, Zhejiang, China; Email (XJ):

xji@puhlic.hz-zj.cn; ''Department of Chemistry, Hangzhou Normal College, Hangzhou 310036, Zhejiang, China

Abstract. -The duration of incubation of Elaphe taeniura eggs at 30±0.3°C averaged 54.9 days. During

incubation, pliable-shelled eggs of E. taeniura increased in wet mass. Dried shells of the freshly laid egg

averaged 17.6c/< of the entire egg dry mass. Freshly laid eggs had significantly heavier shells than did hatched

eggs with the same wet mass at oviposition. Dry mass conversion from egg contents of the freshly laid egg to

hatchling averaged 84.5%. During incubation, approximately 74.6% of non-polar lipids and 80.8% of energy in

egg contents of the freshly laid egg were transferred to the hatchling, with 25.4% of non-polar lipids and 19.2%

of energy used for embryogenesis. Shells from freshly laid eggs had higher levels of calcium and magnesium

than did shells from hatched eggs. Fully developed embryos could obtain almost all magnesium from the yolk

but withdraw approximately 35.6% of their total calcium requirements from the eggshell. A few days after

hatching, a decrease in post-hatching yolk mass was accompanied by an increase in carcass mass, indicating that

post-hatching yolk could be used to support early growth of hatchlings.

Key Hwd.s.-Reptilia: Squamata: Elaphe taeniura: Incubation; Egg; Post-hatching yolk; Hatchling

Introduction

As for reproductive investments in eggs and embry-

onic development, there are two patterns that seem to

be common in oviparous reptiles. One pattern is that

total energy and material stored in eggs generally

exceed the needs for producing a complete hatchling.

Hence, a portion of yolk, namely post-hatching yolk

or residual yolk, may remain unutilized at the time of

hatching. Post-hatching yolk represents a supply of

energy and material for early activities of hatchlings

(Kraemer and Bennett, 1981; Troyer, 1983, 1987;

Wilhoft, 1986; Congdon and Gibbons, 1989); how-

ever, the exact function of this portion of resources

allocated by the mother in eggs is not very clear.

There is a growing evidence showing that resources in

the post-hatching yolk can be transferred to the car-

cass (=total hatchling-yolk sac-fat bodies). The conse-

quence of this transference is that carcass increases in

mass during the first post-hatching days of hatchlings

(Ji et al., 1997a). The other pattern is that embryos

must mobilize minerals (e.g., calcium) from the egg-

shell to complete development (e.g.. Bustard et al.,

1969: Jenkins, 1975: Packard and Packard, 1984,

1989; Packard et al„ 1984a, b; Shadrix et al„ 1994; Ji

et al„ 1996, 1997a, b). As the consequence of this

mobilization, eggshell decreases in mass and ash con-

tents during incubation, particularly at the late stage

of incubation (Ji et al., 1996, 1997a, b; Zhao et al„

1997). In this paper, we present data on a colubrid

snake. Elaphe taeniura. We address the following top-

ics: ( 1 ) conversion of energy and material from egg to

hatchling during incubation, (2) sources of calcium

and magnesium during embryogenesis, and (3) post-

hatching yolk and its contribution to early growth of

newly emerged hatchlings.

Material and Methods

Elaphe taeniura is one of the most common snakes in

our study areas in the Zhoushan Islands (29° 32'-31°

04' N, 121° 30'-123° 25' E), Zhejiang, eastern China.

The distributional range of E. taeniura covers most

provinces of China (including Taiwan and Hainan),

India (Darjeeling and Assam), Indochina, and the

northern half of Malay Peninsula (Zhao and Adler,

1993). For this species, many aspects of biology spe-

cies have been previously examined, but little infor-

mation on incubation and reproduction is available

other than incidental notes (see Huang and Jin, 1990).

Four gravid E. taeniura [snout-vent length: 1 10.0-

155.0 cm; body mass (excluding the clutch): 233.4-

778.7 g] were obtained from a private collector in

Baiquan, Dinghai, the Zhoushan Islands, in mid-June

1994. The snakes were individually maintained in our

laboratory in 80 x 80 x 80 cm wire cages until ovipo-

sition (mean=16.3 days). We removed eggs from the

Vol. 8, p. 54

Asiatic Herpetological Research

1999

cages, measured and weighed them within 6 h of ovi-

position, and then randomly selected two eggs from

each of the first three clutches and one egg from the

last clutch to determine egg composition. Egg con-

tents (embryo plus yolk) of the dissected freshly laid

eggs were removed, placed in pre-weighed small

glass dishes, and weighed to the nearest 0.1 mg.

Shells from the freshly laid eggs were rinsed briefly,

weighed to the nearest o.l mg, and then were saved

for later analysis. All dissected freshly laid eggs con-

tained a small embryo, which was too small and frag-

ile to be sampled separately, and therefore was

included with yolk.

Eighteen eggs, 1/3-buried in moistened substra-

tum, were incubated in a constant temperature cham-

ber at 30±0.3°C. The incubation medium consisted of

sand to water in a ratio of 4: 1 , and water was added

periodically to keep the initial water content. We mea-

sured and weighed the incubating eggs at weekly

intervals before day 42. and daily intervals thereafter.

Four eggs failed to hatch following incubation.

Hatchlings were measured and weighed immediately

after they left the eggs. Shells from hatched eggs were

rinsed briefly, weighed to the nearest 0.1 mg, and then

were frozen for later analysis. Nine hatchlings (2-3

from each clutch; hereafter 0-day hatchling) were fro-

zen immediately after hatching. The remaining 5

hatchlings (1-2 from each clutch; hereafter 7-day

hatchling) were fasted at room temperatures (26-

38°C) for 7 days, and then frozen. The preserved

hatchlings were later thawed, dissected, and separated

into the carcass, yolk sac. and fat bodies.

All samples for determinations of non-polar lipids,

ash, calories, calcium, and magnesium were oven

dried to constant mass at 65 °C, weighed, and then

ground in a mortar and pestle. Non-polar lipids were

extracted from all samples of egg contents, carcass,

post-hatching yolk, and fat bodies for a minimum of

5.5 h using absolute ether in a Soxhlet apparatus. The

mass of non-polar lipids in each sample was calcu-

lated as the difference in sample dry mass before and

after extraction.

Ash and calories of samples of egg contents, car-

cass, post-hatching yolk, and fat bodies were deter-

mined using a GR-2800 adiabatic bomb calorimeter

(Changsha Instruments). Titrations were performed of

the residue after calorimetry to correct for nitrogenous

wastes. Samples of eggshells were burned in a muffle

furnace at 550 °C for 24 h to determine ash mass.

Samples for calcium and magnesium determina-

tions were weighed out into glass tubes and digested

completely in hot concentrated nitric acid. Digestates

were brought to volume in volumetric glassware and

stored in a refrigerator until analysis for calcium and

magnesium. Concentrations of the two elements in the

digestates were determined using a WFX-1B model

atomic absorption spectrophotometer (The 2"

Beijing Optical Instruments). To check if there were

any differences in calcium and magnesium contents

between shells from freshly laid eggs and hatched

eggs, we took equal amount of sample from each

shell, pooled separately the samples from the freshly

laid eggs and hatched eggs, and treated them as two

different samples.

All variables were tested for normality using Kolmog-

orov-Smirnov test and for homogeneity of variance

using Bartlett's test prior to further statistical analysis,

and arc-sine transformation was performed for per-

centage data. We used analyses of variance (ANOVA),

analysis of covariance (ANCOVA), regression statis-

tics, and partial correlation analysis to analyze our

data. Significance level was set at a=0.05. Prior to

testing for differences in adjusted means, the homoge-

neity of slopes was checked. Throughout this paper,

values are presented as mean±l standard error.

Results

Elaphe taeniura laid pliable-shelled eggs. Clutch size

in our sample averaged 8.8+0.9 (range=8-ll, N=4).

Freshly laid eggs averaged 26.8±0.6 g (range=20.8-

32.3, N=35) wet mass, 54.1±0.9 mm (range=45.7-

63.2, N=35) length, and 28.8±0.4 mm (range=25.0-

33.1, N=35) width. During incubation, eggs increased

in wet mass and, one day prior to hatching, weighed

110.0±3.5% (range=98.6-135.9, N=14) of egg wet

mass at oviposition. The incubation time averaged

54.9±0.2 days (range=54. 1-55.7, N=14). Newly

emerged young averaged 17.1±0.7 g (range=13.2-

21.8, N=14) wet mass, 381.4±3.5 mm (range=357.0-

405.0, N=14) SVL, and 88.5±1.9 mm (range=77.0-

103.0, N=14) tail length.

The data on components of the freshly laid eggs and

0-day hatchlings are given in Table 1. Egg contents

averaged 74.0% water by mass; egg contents averaged

92.4% organic material, 7.6% ash, 31.5% non-polar

lipid, 1 .36% calcium, and 0.39% magnesium by dry

mass (Table 1 ). Shells from the freshly laid eggs aver-

aged 17.6% of total egg dry mass, and 81.7% organic

material and 18.3% ash by shell dry mass (Table 1).

Shells from freshly laid eggs had higher levels of cal-

cium (8.21%) and magnesium (0.75%) than did shells

from hatched eggs (calcium: 6.31%; magnesium:

0.61%).

0-day hatchlings averaged 70.6% water by mass.

These hatchlings averaged 89.1% organic material.

1999

Asiatic Herpetological Research

Vol. 8, p. 55

Table 1 . Components and F values of the ANCOVA for 7 Elaphe taeniura freshly laid eggs and nine 0-day

hatchlings. Data are expressed as adjusted meam+1SE with total egg wet mass at oviposition as the covariate.

Symbols immediately after F values represent significant levels: NS P>0.05, * P<0.05, " P<0.01, and *** P<0.001.

10.8% ash. 27.8% non-polar lipids, 2.49% calcium,

and 0.48% magnesium by dry mass (Table 1 ). Shells

from hatched eggs averaged 85.1% organic material

and 14.9% ash by dry mass (Table 1 ).

0-day hatchlings contained significantly lower quanti-

ties of total dry mass, organic mass, non-polar lipids,

and energy, but significantly higher quantities of cal-

cium and ash mass than did egg contents (Table 1).

There was no significant difference in the quantity of

magnesium between egg contents and 0-day

hatchlings (Table 1 ). Shells from hatched eggs con-

tained lower quantities of total dry mass and ash mass

than did shells from the freshly laid eggs. No signifi-

cant difference in organic mass was found between

shells from the freshly laid eggs and hatched eggs

(Table 1 ).

During incubation, approximately 84.5% of dry mass,

74.6% of non-polar lipids, and 80.8% of energy in egg

contents of the freshly laid egg were transferred to the

hatchling, with 15.5% of dry mass, 25.4% of non-

polar lipids, and 19.2% of energy used for embryo-

genesis (Table 1 ). Fully developed embryos could

obtain almost all magnesium from the yolk, but

should withdraw 35.6% of their total calcium require-

ments from sources other than yolk (Table 1 ).

Egg contents (1.3610.07%, range=1.14-1.62%, N=7)

of the freshly laid egg had a higher level of calcium

than did post-hatching yolk (0.9910.10%,

range=0.64-1.45%, N=9) (ANOVA: FU4=8.38,

P<0.05). There was no significant difference in the

level of magnesium between egg contents

(0.3910.03%, range=0.32-0.45%, N=7) and post-

hatching yolk (0.4210.05%, range=0.27-0.62%, N=9)

(ANOVA: FU4=0.54, P>0.05).

Dry masses of carcass (r=0.96, Fj 7=157.76,

P<0.001) and fat bodies (r=0.88, F, 7=55.29,

Vol. 8, p. 56

Asiatic Herpetological Research

1999

Table 2. A comparison between nine 0-day and five 7-day hatchlings of Elaphe taeniura. Data are expressed as

mean±1 SE; all mass units are in grams.

0-day hatchling

7-day hatchling

Hatchling wet mass at hatching

Hatchling wet mass 7 days after hatchling

Decrease in wet mass

Hatchling dry mass

Carcass

Yolk sac

Fat bodies

% water of hatchling

18.8±0.9

5.28±0.31

3.51 ±0.20

0.66±0.05

1.11±0.09

70.6+0.5

15.7±0.3

15.0±0.2

0.70±0.22

4.00±0.06

3.18±0.05

0.09±0.01

0.7310.02

73.2±0.3

P<0.001 ) of the 0-day hatchlings were both correlated

with total hatchling dry mass. In the 7-day hatchlings,

we only found a positive correlation between carcass

dry mass and total hatchling dry mass (r~=0.88,

F, 3=22.34, P<0.05). 7-day hatchlings had signifi-

cantly heavier carcasses than did 0-day hatchlings

with the same wet mass at hatching (ANCOVA:

Fu |=16.38, P<0.01) (Table 2). There was a negative

correlation between post-hatching yolk dry mass and

carcass dry mass when holding total hatchling dry

mass and fatbody dry mass constant (r=-0.90, t=6.53,

df=10, P<0.001 ). There was no significant correlation

between post-hatching yolk dry mass and fatbody dry

mass when holding total hatchling dry mass and car-

cass dry mass constant (r=0.43, t=1.50, df=10,

P>0.05). There was no significant correlation between

carcass dry mass and fatbody dry mass when holding

total hatchling dry mass and post-hatching yolk dry

mass constant (r=-0.20, t=0.65, df=10, P>0.05). 7-day

hatchlings (23.2±0.4%, range=22.1-24.1%, N=5) had

significant lower levels of non-polar lipids than did 0-

day hatchlings (27.4±0.6%, range=25.3-29.5%, N=9)

(FU2=32.1,P<0.001).

Discussion

Similar to that reported for pliable-shelled eggs of

other reptiles (e.g.. Fitch, 1954; Fitch and Fitch, 1967;

Andrews and Sexton, 1981; Vitt and Cooper, 1986;

Vleck, 1991: Ji et al., 1996, 1997a, b), eggs of E. tae-

niura overall increased in wet mass and swelled dur-

ing incubation due to a net gain of water absorbed

from the substrate on which the eggs were incubated.

However, water uptake seemed not to be obligate for

E. taeniura eggs, because some eggs whose final mass

was less than initial mass also hatched successfully.

Small E. taeniura embryos were present in all

freshly laid eggs, but they, relative to the large egg

size, were too small to be considered as an important

part of the egg at oviposition. Therefore, the transfer-

ence of energy and material from egg to hatchling

during incubation was approximately equal to the

transference overall. This makes it possible to com-

pare our data with those for other oviparous reptiles

whose freshly laid eggs also contain small embryos

and embryonic stage is near the oviparous end in the

oviparity-viviparity continuum (Shine, 1983). Elaphe

taeniura exhibited high conversion efficiencies of

energy and material from egg to hatchling. The values

in Table 3 show that the conversion efficiencies of

energy and material recorded in E. taeniura were

higher than those reported for any other studied rep-

tiles. The values in the Table also show that the con-

version efficiencies vary considerably among species;

however, the explanations to these differences are

unknown at this time. It has been known that costs of

embryonic development vary considerably among

reptiles (Dmf el, 1970; Black et al., 1984), parental

investment in each offspring should be related to its

survivorship (Congdon ad Gibbons, 1989; Fischer et

al., 1991), and incubation environments may influ-

ence embryonic development (Gutzke and Pachard,

1987). So, further studies in a wider field covering

parental reproductive investment, embryonic metabo-

1999

Asiatic Herpetological Research

Vol. 8, p. 57

Table 3. Comparison of conversion efficiencies of dry mass, non-polar lipids, and energy between Elaphe taeniura

and other oviparous reptiles.

lism, and ecology of neonates will be very important

for our giving reliable explanations.

As in other oviparous squamates (Packard et al.,

1984a, 1985; 1988; Ji et al., 1996, 1997a, b), turtles

(Packard et al., 1984b; Packard and Packard 1986),

and the American alligator (Packard and Packard,

1989), Elapeh taeniura embryos use eggshell as a sec-

ondary source of calcium. The result that eggshells

decreased in mass and calcium content during incuba-

tion supports this interpretation. The level (35.6%) of

calcium withdrawn by E. taeniura embryos from the

eggshell was much lower than the values reported for

crocodilians and turtles (50-80%; Bustard et al., 1969;

Jenkins, 1975; Packard and Packard, 1984, 1989). In

squamates, the level was slightly lower than that

reported for Eumeces fasciatus (39%; Shadrix et al.,

1994) but higher than those reported for Eumeces

chinensis (19%; Ji et al., 1996), Coluber constrictor

(20%; Packard et al., 1984a), Elaphe carinata (31%;

Ji et al., 1997a), and Naja naja atra (14%; Ji et al.,

1997b). These differences presumably reflect the

interspecific differences in eggshell structure and allo-

cation of minerals between eggshell and yolk.

The level of calcium in E. taeniura post-hatching

yolk was significantly lower than that in egg contents

of the freshly laid egg. This suggests that E. taeniura

Vol. 8, p. 58

Asiatic Herpetological Research

1999

embryos deplete the yolk of almost of its calcium

before hatching and none of the calcium withdrawn

from the eggshell is deposited in the yolk. This pattern

of mobilization and deposition of calcium is similar to

that observed in other non-crocodilian reptiles (e.g.,

Packard et al., 1984b, 1985, 1987; Packard and Pack-

ard. 1986: Packard and Packard, 1988: Shadrix et al.,

1994).

The estimated amount of magnesium in egg con-

tents of the freshly laid egg (95.9% of total magne-

sium in the hatchling) was slightly less than that in the

hatchling. We are presently not very certain that E.

taeniura embryos use the eggshell as an additional

source of magnesium, because any slightly biased

estimation might account for the remaining 4.1% of

magnesium. However, the fact that shells from

hatched eggs were lighter in mass and lower in the

level of magnesium seemed to imply that E. taeniura

embryos should withdraw a small portion of magne-

sium from the eggshell. Since studies of embryonic

magnesium metabolism have been unfortunately

extremely limited, we cannot discuss this problem in

detail. In the American alligator (Packard and Pack-

ard, 1989) and other species of snakes that have stud-

ied by us, embryos apparently obtain all magnesium

necessary for development from the yolk.

One interesting finding In this study was that a

decrease in post-hatching yolk mass was accompa-

nied by an increase in carcass mass a few days after

hatching. This finding quantitatively confirms that

post-hatching yolk can be used to support early

growth of hatchlings. Compared with post-hatching

yolk, fat bodies were used mainly for hatchling main-

tenance. An obvious decrease in the level of non-polar

lipids in the 7-day hatchlings supports this interpreta-

tion.

Acknowledgments

The work was supported by a grant from the Natural

Science Foundation of China to XJ (NSFC-

39270124). A grant from Paos' Foundation supported

XJ to complete writing this paper in Spain.

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Vol. 8, pp. 60-68

Redescription and Generic Redesignation of the Ladakhian Gecko

Gymnodactylus stoliczkai Steindachner, 1969

Muhammad S. Khan1 and Herbert Rosler2

'12731 SW8th Ct.. Davie, Florida, 33325 USA 2F Freiligrath Str. 51, 06502 Thale/Harz, Germany

Abstract.- Gymnodactylus stoliczkai is redescribed on the basis of recently collected topotypes, and is

redesignated to the genus the Cyrtodactylus. It is found to be morphologically distinct from C. walli and C.

yarkandensis with which species it has long been synonymized. Reproduction, ecology and distribution of this

highland gecko is discussed.

Key words.- Cyrtodactylus stoliczkai, taxonomy, reproduction, ecology, zoogeography.

Introduction

In 1866 Dr. Ferdinand Stoliczka deposited a collec-

tion of animals, collected from different parts of the

Indo-Pak subcontinent, in Naturhistoristorisches

Museum Wien, Austria (NMW). The collection con-

tained a gecko from Karoo, north of Dras. Kashmir,

apparently collected during geological survey of west-

ern Himalayas, which was described by Steindachner

in 1867 as a new taxon, Gymnodactylus stoliczkai,

honoring its collector. The specimen is still available

in the museum under registry number NMW 16756

(Tiedemann et al., 1994). Ever since the description of

this taxon, it has become a habit with herpetologists

working on collections from northern Pakistan, to try

to place almost every angular-toed gecko encoun-

tered, in the synonymy of G. stoliczkai without going

into details of morphological comparisons: Smith,

1935 (Gymnodactylus walli Ingoldby, 1922): Minton,

1966 (Cyrtodactylus mintoni Golubev and Szczerbak,

1981) and Mertens, 1969 (Cyrtodactylus dattanensis

Khan, 1980), creating taxonomic chaos. Recent col-

lections from circum-Himalayan region has shown

that G. stoliczakai does not belong to the fauna of

Pakistan, moreover, all the geckos placed in its synon-

ymy are themselves valid independent taxa (Khan,

1992, 1993, 1994; Khan and Baig, 1992).

A long, detailed morphological redescription of

Gynnodactylus stoliczkai is urgently due, to make

intertaxal comparisons possible and to come out of

"stoliczkai myth". Due to lack of working material

the present project has considerably been delayed.

The type specimen (NMW 16756) and syntype in the

Museum of Comparative Zoology, Cambridge (MCZ

7132) are not allowed to be loaned for study. There-

fore the data for present study is drawn from several

sources: one of us (HR) has studied series of 14 topo-

types of this species in Zoologische Staatssammlung

Munchen (ZSM: Table 1: collected by Gruber, 1981),

while Dr. G. R. Zug (National Museum of Natural

History, Washington) has kindly taken data on topo-

type MCZ 7132 for us. Moreover, present redescrip-

tion is further supplemented with the data available in

literature (Steindachner, 1867:15: Boulenger,

1890:63; Smith, 1935:57; Constable, 1949:84; Szcz-

erbak and Golubev, 1986:205). Photographs of topo-

types (Fig. 1; ZSM 124.77) and (Fig. 2; ZSM 45.77),

and type NMW 16756 (Khan, 1994; Fig. 2) have

helped us immensely to understand morphology of

this important taxon.

Taxonomic Notes

Sprix's (1825:17) genus Gymnodactylus included all

the then known non dilated angular-digited geckos

(Boulenger, 1885:22, 1890:59; Annandale, 1913:309;

Smith, 1935:37). Until Underwood (1954) restricted

this genus to South American angular-digited geckos,

placing all south Asian geckos in the genus Cyrtodac-

tylus Gray 1827. Most of the subsequent workers on

the herpetology of Pakistan have followed Under-

wood's view point (Minton, 1966; Khan, 1980; Khan

and Mirza, 1977). However, Mertens (1969) is ortho-

dox and a bit cautious by retaining Gymnodactylus as

a genus and placing Pakistani geckos in the subgenus

Cyrtodactylus.

A recent break through towards a solution comes

from Szczerbak and Golubev (1984, 1986): the genus

Tenuidactylus is erected to include Palearctic angular-

digited geckos. It is divided in three subgenera to

accommodate the rest of the southeast Asian gekkota:

subgenus Tenuidactylus includes two Pakistani spe-

cies T. montiumsalsorum and T. kohsulaimanai, and

the group of Tibeto-Himalayan species: T. tibetanus.

1999

Asiatic Herpetological Research

Vol. 8, p. 61

Table 1 . Range of scale counts and measurements of topotype series of Tenuidactylus stoliczkai in Zoologische

Staatssammlung Munchen (ZSM) collection (data from juvenile ZSM 1 19/77 not taken into account).

Character

Range

Supralabials 9-11

Infralabials 7-9

Nasals 3-3

Internasals 1 -3

Postmentals 2-2

Loreals 10-15

Scales between eye-ear 15-20

Interorbitals 17-19

Tubercle rows across body middorsum 8- 1 2

Sale rows across midbelly 25-30

Midventrals 110-133

Lamellae under first toe 11-14

Lamellae under fourth toe 22-27

Cloacal spines 2-3

Granular scale rosette around dorsal tubercle 7-9

SVL 27-49.4 mm

TL 25-49.7 mm

Head length 8-1 1 .5 mm

Head width 5-10.7 mm

Head height 3-6.1 mm

Nostril-eye distance 2-4.4 m

Eye-ear distance 2-4.1 mm

Body length 10-23.6 mm

Eye diameter 2-2.8 mm

Ear diameter 0.4-0.9 mm

Head length/head width 0.99-1 .43 mm

SVUbody length 2.09-2.64 mm

Head length/head width 0.99-1 .43 mm

Distance nostril-eye/eye-ear 0.98-1.29 mm

Eye/ear diameter 2.33-5 mm

Vol. 8, p. 62

Asiatic Herpetological Research

1999

thS/1977-

Figure 1. Cyrtodactylus stoliczkai (ZSM 124.77), adult

female, with unregenerated tail.

T. mintoni, T. chitralensis, T. stoliczkai and T.kirman-

ensis; the genus Cyrtopodion Fitzinger, 1 843 is resur-

rected as a second subgenus to include four Pakistani

forms: agamuroides, scaber, watsoni and kachhensis.

A third subgenus Medioductylus is left floating (Gol-

ubev, pers. comm.. 1996).

Undoubtedly southeast Asian cyrtodactylid geckos

are morphologically distinct from Palearctic tenuidac-

tylids (Leviton and Anderson, 1970: Khan, 1988,

1989, 1991; Khan and Tasnim, 1990). Khan (1993)

maintains the genus Cyrtodactylus Gray, 1827, to

include Tibeto-Himalayan species group and all the

southeast Asian species (Smith, 1935). The southeast

Asian cyrtodactylids are a very heterogeneous assem-

blage of closely allied species. Their shared characters

are: smooth tubercular granular scales with scattered

round-oval smooth or slightly keeled tubercles on

head and body dorsum; more than 25 heterogeneous

interorbitals; subcylindrical and subequal body and

tail; dorsal vivid pattern; subdigital lamellae about

twice as broad as high with a pair of lateral row of

granular scales, lamellae not swollen at the digital

angles; 2-10 preanal pores in male, rare femoral

pores; small blunt caudal tubercles, subcaudals small

rarely broad. In the past there have been several

attempts to arrange them in a logical array (Annan-

dale, 1913; Smith, 1935: Khan, 1993). Considering

morpho-ecogeography of these geckos, we distin-

guish two lineages:

Circum-oceanic group: tropical, scattered along sub

continental coastal strip and oceanic islands, confined

between lat. 7-32° N, long 75-105° E; dorsal pattern

of vivid cross bars or spots, dorsal granular scales

mixed with larger rounded, smooth or slightly keeled

tubercles, tail and body cylindrical, tail often longer

/tfDACH4L

Figure 2. Cyrtodactylus stoliczkai (ZSM 45.77), adult

female, with regenerated tail.

than body: Cyrtodactylus pulchellus, interrnedius,

consobrinoides, angularis, khasiensis, rubidus, trie-

drus, nebulosus, collegalensis, dekkanensis, albofas-

ciatus and jayporensis.

Circum-Himalayan group: subtropical, highland

forms, mainly extending between lat. 34-4° N, long

75° 50-50'E, tubercular, beady, scarcely imbricate

granular dorsal scales, interspersed by 2-3 times

larger oval keeled or keelless tubercles arranged in

more or less in 12-13 longitudinal rows; body and tail

subequal and subcylindrical, subcaudals small in sev-

eral rows, inconspicuous dorsal pattern of transverse

bands, spots or reticulation.

Further distinguished in three subgroups:

stoliczkai subgroup: body and tail rather flat in cross

section, caudal tubercles flat, smooth; anterior half of

tail segmented, segments laterally lobulated in older

animals, regenerated tail flattened and abnormally

swollen, no preanal and femoral pores. Includes high-

land species: Cyrtodactylus lawderanus, C. stoliczkai,

C. yarkendensis and C. baturensis.

tibetinus subgroup: Body and tail round in cross sec-

tion, tail segments not distinct, 4-10 preanal pores,

feebly keeled caudal tubercles, regenerated tail not

flattened. Dorsal pattern of vivid cross bars, spots or

reticulation. Includes Tibeto- Himalayan low altitude

submountain geckos: Cyrtodactylus tibetinus, C.

himalayanus, C. mintoni, C. dattanensis and C. bat-

talensis.

walli subgroup: Body flatter, tail quadrangular in

cross section, distinctly segmented, caudal tubercles

large slightly keeled, median row of subcaudals trans-

versely enlarged; 4-6 preanal pores. Species included

are: Cvrtodactvlus kinnanensis and C. walli.

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Asiatic Herpetological Research

Vol. 8, p. 63

Table 2. Comparison of morphology of 1= Tenuidactylus yarkandensis (J. Anderson, 1872) with its closest conge-

ners: 2= T. stoliczkai (Steindachner, 1867), 3= T. iva///(lngoldby, 1922) and 4= T. baturensis Khan and Baig, 1992;

vl=vertical, (measurements in mm).

Redescription

Cyrtodactylus stoliczkai (Steindachner, 1867)

Gymnodactylus stoliczkai Steindachner,

1867, Reise Novara, Zool., 1:15 Rept. 1, Plate

2, Fig. 2, 2a.

Cyrtodactylus stoliczkai Underwood, 1954,

Proc. Zool. Soc. London, 124:475.

Type locality: near Karoo, north of Dras, Kashmir.

Holotype: NMW 16756 (Fig. 1), female, near Karoo,

north of Dras, 3200 m, Kashmir (34° 28' N, 75° 46'

E), donated by Stoliczka in 1866.

Paratypes: MCZ 7132, female, pholidosic counts and

measurements by Dr. Zug, (per comm., 1989) Ladak.

3100 m, Stoliczka, 1908.

Topotypes (14, examined): ZSM 45.77 (1,2, 3, 4, 5)

and 149.77 (1, 2, 3, 4, 5), 2 males, 5 females, three

juveniles. Phyang Ghompa, Ladakh, 3600 m, 5.7.77

and 19.8.77: ZSM 46.77, and 124.77, 2 females,

Hemis, Ladakh, 3700 m, 6.7.77 and 17.8.77: ZSM

119.77, juvenile, Kargiul. Ladakh, 2750 m, 12.8.77:

ZSM 121.77, female, Saspool, Ladakh, 3100 m,

16.8.77, all collected by Ulrich Gruber ( 1981 ).

Diagnosis: Body and tail moderately depressed, tail a

little longer than body, caudal segments of unregener-

ated tail deeply sected on lateral sides to anterior half

of the tail, three tubercles, and several series of small

subcaudals arranged in four transverse rows: body

dorsum with flat, mostly juxtaposed granular scales,

distinctly arranged in transverse rows, interspersed

with large flat smooth oval tubercles, about three

times larger than granular scales, more or less

arranged in 9-10 transverse rows across middorsum

and 19-20 along paravertebral line; 16-20 interorbital

tubercular scales: 27-32 scales across midabdomen,

117-150 midventrals; both preanal and femoral pores

not indicated: dorsal pattern of M-shaped transverse

Vol. 8, p. 64

Asiatic Herpetological Research

1999

dark bands with heavier posterior margin, broader

than interspaces.

Description of holotype NMW 16756, Fig. 1, (state-

ments in parenthesis are from paratype and topotypes

adding up to the original description of holotype

NMW 16756 by Steindachner, 1867:15): (habitus

depressed); rostral scale big (7-angular, broader than

deep), slightly convex at the upper edge, and forked in

the middle reaching the anterior end of the snout

(median dorsal rostral longitudinal furrow narrowly

misses anterior border of the rostral scale); nasal

opening (small, dorsolateral) bordered in front by ros-

tral plate, (ventrally by) second upper lip shield (first

supralabial. Note rostral shield is regarded as first

supralabial in original description), posteriorly by

three small nasal shields, of which upper most is the

largest (separated from that of other side by a pair of

granular scales, rostral area with heterogeneous tuber-

cular scales mostly arranged in longitudinal rows, 1 1-

12 tubercular loreal scales between posterior nasals

and anterior rim of orbit; head with heterogeneous

granular tubercular scales, 19-20 between orbits

arranged in longitudinal rows, smaller on eye bulg-

ings; a series of sharp supraciliary scales jutting out

from posterior half of the upper eyelid border fol-

lowed by a row of large tubercular round scales run-

ning along the eyelid; temporals and neck with small

tubercular granular scales: ear opening round, much

larger than largest dorsal tubercle).

19-21 upper lip shields (10-11 supralabials, first

three of the same size; suture between first supralabial

and rostral scale almost equals former's length along

oral orifice); 13 lower labial shields (7-9 infralabials,

second narrowest while fourth the longest; 2-3 rows

of sublabials). The anterior most lower lip shield

(mental scale) is very large, triangular (about twice

deep as broad, extends deep between first pair of post-

mentals), three pairs of chin shields (first pair, largest,

narrowly in contact with each other behind posterior

tip of mental scale, second pair smaller, less than half

the size of first not in contact with each other), third

pair (smallest) almost fully separated from lower labi-

als (on right while in contact on left).

Body dorsum clearly granulated (with flat, juxta-

posed, rarely slightly imbricate granular scales,

arranged in transverse rows) with numerous, only lit-

tle bigger fully rounded tubercles (interspersed with

2-3 times large, flat, smooth, round or oval tubercles,

scattered evenly on body dorsum, more or less

arranged in longitudinal rows, separated from each

other by 3-4 granular scales, a rosette of 7-9 granules

around a tubercle; tubercles on sides slightly conical).

(Gular scales flat, juxtaposed or slightly imbricate,

mostly arranged in transverse rows interspersed with

larger scattered tubercles, becoming flatter and pen-

tagonal on chest, at abdomen flat, hexagonal, broader

than long, slightly imbricate rarely juxtaposed,

arranged in transverse rows, 30-32 scales across

midabdomen; slightly marked lateral abdominal folds,

5-6 rows of lateral abdominal scales differ little from

dorsals, however clearly marked from abdominals;

femoral and preanal pores absent (even their site not

marked by distinct scales; 142-149 midventral scales

between first pair of submental and anterior anal lip. A

pair of lateral cloacal tubercles, no postanal bulge).

(Limbs medium sized, covered with imbricate

smooth scales arranged in transverse and longitudinal

rows, without tubercles; subfemorals in 5-6 transverse

rows, as large as abdominals: median-subtibial scales

largest, imbricate, arranged in trans verse rows; gran-

ular postfemorals extend on to the sides of preanals,

with no tubercles; tips of finger-claws extend to ante-

rior of eye, when forelimbs are adpressed forward,

those of toes a little anterior of axilla; subdigital

lamellae 23-24 under fourth toe, equally broad

throughout, not enlarged under basal and angular

parts of digits).

Tail, as it appears in the specimen examined by us,

is regenerated in the anterior, somewhat longer than

the body. Lined on each (dorso- lateral) side by three

rows of large, spike shaped raised tubercles, of which

those of lower most row are the biggest and conical.

No large transverse plates under side of the tail

(regenerated?, this parenthesis is by Steindachner),

posterior half of the tail is with uniform scales (mor-

phologically tail of the holotype reminds original tail

of older specimens of Hemidactylus flaviviridis.

Doubtless the type specimen has original tail which is

normal for older animals of the species as in ZSM

124.77. The tail is moderately depressed, its stump is

less than half the width of body and the segmented

part almost equals body's width, a median dorsal and

ventral longitudinal slight furrow runs along its

length. Its anterior half is divided in 10 distinct later-

ally lobulated segments, while posterior unsegmented

half gradually narrows to sharp terminal tip; dorsolat-

eral^ caudal tubercles are given from the middle of

the segments, four on 1st to 5th segment, three on 6th

to 10th. The dorsal tubercles are small roundish about

2-3 times smaller than laterals which are elongated

conical blunt, in contact with each other, are gradually

reduced in size, until almost indistinct in posterior

half of the tail. Dorsally 6-7 transverse rows of hetero-

geneous, slightly imbricate, smooth, tubercular scales

cover anterior caudal segments while 4 transverse

1999

Asiatic Herpetological Research

Vol. 8, p. 65

rows of small imbricate subcaudals are present on

ventral side of segment. In the posterior quarter dorsal

and ventral caudal scales become indistinct from each

other, get longer, flatter, pointed at tips and are

strongly imbricate).

Color: Body dorsum light blue grey, with pink edged

transverse bands with denser wavy posterior edges,

broader than interspaces, three on nape, six on body

and 13 on tail (in preserved specimens bands are dark

and does not extend on subcaudals). (Head), labials

and tail plates with fine grey dots, limbs and digits

barred, ventrum light.

Measurements (in mm): Snout vent length 48, tail

length 52, trunk length 24, head length 1 1 .5, head

width 10, head height 7, eye diameter, not including

bony orbit 2.5: snout length 5: oculo-orbital space 5,

Variation: Table 1 presents the measurements and

pholidosic counts in ZSM series which fall within the

range of the type specimen NMW 1 6756 and paratype

MCZ 7132, differing in minor details of pholidosic

morphology: rostral scale is protrubrant in most of the

specimens, however, in some it is flat, the median ros-

tral groove in some specimens extend to middle,

while in other it narrowly misses the anterior end of

the scale: the supraciliary pointed scales vary in their

pointedness; dorsal tubercles uniformly scattered on

dorsum, 2-3 times larger than dorsal granular scales,

separated from each other by 2-4 granular scales, sur-

rounded by a rosset of 6-9 granular scales; lateral

abdominal folds strongly or poorly indicated.

Study of tail morphology of MCZ 7132 and speci-

mens in ZSM series indicates that the tail of the holo-

type NMW 16756 is undoubtedly original.

Steindachner (1867) himself was doubtful about its

being "(regenerated?)". In young specimens with

unregenerated tail, the tail is uniformly broad from

basal stump till mid-tail, where it gradually tapers to

its tip (ZSM 45.77:5, 1 19.77, 124.77, 149.77: 1, 2, 4,

5). As animals get older (NMW 16756 and ZSM

124.77), the anterior half of the original tail becomes

broader, flatter and deeply sected on sides so much so

it appears laterally lobulated at segments. From lateral

lobes caudal tubercles strongly jet out. While in

regenerated tail, MCZ 7132 and ZSM 49.77,the tail

swells up almost round at the base, with no indication

of segmentation, lobulations and tubercles, while pos-

teriorly it abruptly tapers. Moreover, instead of trans-

verse bands of original tail, the regenerated tail is

spotted with longitudinal spots, scattered all over it.

Tail in ZSM 45.77, 49.77:3, 45.77, 121.77 and ZSM

49.77 represent different stages of tail regeneration in

Tenuidactylus stoliczkai.

Dorsal pattern of bands is vividly distinct in juve-

niles (ZSM 1 19.77), but is gradually lost as the animal

grows older.

Sex: Though dissection is the sure way of sex deter-

mination of geckos, however, presence of prcanal and

femoral pores in males and their absence in females

arc almost universal sex indicators in these animals. In

the type specimen of Tenuidactylus stoliczkai NMW

16756, paratype MCZ 7132 and ZSM series the prea-

nal and femoral are absent, moreover their position is

not indicated by distinctiveness of scales in the area.

On the other hand, swollen postanal sacs are usually

distinct in male less so in female geckos (Smith, 1933,

1935: Khan and Baig, 1992). There is no indication of

postanal sacs in type nor in paratype, however, are

well indicated in two specimens in ZSM series which

are males. Constable (1949:84) designated MCZ 7132

as a male specimen, which on dissection is proven to

be an adult female with well developed vitellogen fol-

licles (Zug, personal communications, 1989).

Ecology: Ladakh lies around 3000 m, above timber-

line. It is completely dry snow desert, with sparse veg-

etation of herbs, shrubs and grasses. The area is

highly arid with sub-tropical continental highlands

cold climate. Heavily snowy winters, getting rain in

winter and spring. Maximum summer July tempera-

ture is 24.7° C, minimum 10.2°, while maximum win-

ter temperature in January is -1.4° C, dropping to

minimum -13.3°. Maximum rain fall, 15.0 mm, is

received during August, minimum, 1.0 mm during

November (Ahmad, 1951).

Gruber (1981) collected T. Stoliczkai from rocky

habitat, where this gecko prefers desert, bare, dry situ-

ations in the non-irrigated areas without or with very

sparse vegetation, apparently avoiding direct neigh-

borhood of human settlements. Other reptiles col-

lected from the area are Phrynocephalus theobaldi.

Laudakia himalayana, and Scincella ladacensis,

while Bufo latastii is the only amphibian recorded

from waters of the area.

Comparison with congeners: Absence of trihedral

tubercles, preanal and femoral pores, broader subdigi-

tal lamellae and peculiar tail morphology differentiate

Tenuidactylus stoliczkai from Palearctic group of

Pakistani tenuidactylid Cyrtopodion geckos: C

scaber (Heyden, 1827), C. watsoni (Murray, 1892), C.

kachhensis (Stoliczka, 1872), C. montiumsalsorum

(Annandale, 1913) and C. kohsulaimanai (Khan,

1991 ). While Pakistani members of Tibeto-Himalayan

group of cyrtodactylid geckos: C. mintoni (Golubev

and Szczerbak, 1981), C. dattanensis (Khan, 1980) C.

battalensis Khan, 1993 are similar to T. stoliczkai in

the morphology of subdigital lamellae, body configu-

Vol. 8, p. 66

Asiatic Herpetological Research

1999

ration, larger number of interorbitals, subabdominals,

however, they differ markedly from it because of their

plump rounded body and tail, tail morphology, dorsal

tuberculation and pattern which extends on the tail

ventrum, presence of preanal pores in male.

The tenuidactylid group of Pakistani geckos: T.

indusoani (Khan, 1988), T. rohtasfortai Khan and

Tasnim, 1990 and T. fortmunroi Khan, 1993 are dis-

tinguished from the nominated species by their differ-

ent body configuration, smaller number of

interorbitals, subabdominal pholidosic counts, dorsal

scalation and pattern, caudal morphology with keeled

large tubercles, single row of subcaudals, presence of

both preanal and femoral pores.

Following Annandale (1913:316), Smith

(1935:39) grouped T. stoliczkai with low altitude T.

lawderanus (Stoliczka, 1972), despite very obvious

differences from the former: more flattened body and

tail, few and feebly developed dorsal tubercles, incon-

spicuous dorsal pattern, single pair of nasal scales,

presence of preanal pores in male, tail morphology

(compare Fig. 18, Smith, 1935).

C. yarkandensis (J. Anderson, 1872) and C. walli

(Ingoldby 1922), have long been synonymized with

C. stoliczkai and C. chitralensis (Smith, 1935), mostly

due to their similar dorsal pattern, body configuration,

dorsal tuberculation and absence of pores (Boulenger.

1885; Blanford, 1878; Annandale, 1913; Smith, 1935;

Minton, 1966: Mertens, 1969: Szczerbak and Gol-

ubev, 1986). C. chitralensis has been found to be con-

specific with C. walli (Khan, 1992).

Cyrtodactylus stoliczkai is defined by the follow-

ing combination of characters: dorsal granular scales

smooth, round, beady, juxtaposed, interspersed with

oblong, smooth beady tubercles, arranged roughly in

longitudinal rows; normal tail in juveniles uniformly

broad from basal stump till mid-tail, where gradually

tapering to tip, as animal gets old, the anterior half of

the original tail becomes broader, flatter and deeply

sected on sides in lateral lobules at segments, regener-

ated tail much swollen and rounded; subcaudals

small, in several rows; caudal tubercles thick and

blunt.

Geographical Distribution

All evidence goes in favor of the idea that the family

Gekkonidae evolved in southeast Asia and dispersed

westward through southwestern Asia into Indo-Paki-

stan and Africa (Kluge, 1967). Ranges of several cir-

cum-Indian oceanic cyrtodactylids overlap, however

circum-himalayan highland geckos are widely distrib-

uted and the ranges of none of them are known to

overlap: the northern most extralimital, Cyrtodacty-

lus. yarkandensis, is known from lat. 38° 40'N, long

77° 50'E, along the western border of China's Xin-

jiang Province (Khan, 1994) and Cyrtodactylus stolic-

zkai is confined to Ladak, between lat. 34c-35° 45' N,

long 75° 50-76° 70'E (Annandale. 1913; Schmidt,

1922; Gruber, 1981). A highland Pakistani gecko, C.

baturensis, is reported from Gilgit Agency at lat. 36°

20'N, long 74° 50' E (Khan and Baig, 1992). The

western most Pakistani form, C. walli, occurs between

lat. 35-36° N, long 71-72° E. while the western extral-

imital Iranian gecko, C kirmanensis, is reported from

lat. 30° N, long 58° E (Szczerbak and Golubev. 1986).

Worldwide distribution of some geckos is largely

known to be due to human transportation (Darlington,

1957). The circum-oceanic coastal forms are charac-

teristically carried by sailors from coast to coast, how-

ever, some of the species penetrated deep inland.

Similarly, westward dispersal of Cyrtodactylus in the

lower Himalayas appears largely due to westward

migrations of Buddhist peoples and seasonal nomadic

high-low-high altitude migrations which played

important role in the distribution of cyrtodactylid gec-

kos of the area. Massive pagoda buildings and temples

are still the frequent haunts of these geckos. In the

valley-complex of the sub Himalayan system they

evolved into closely allied forms: C. mintoni, C. dat-

tanensis and C. battalensis. A parallel example of

human transportation of a gecko is presented by the

recent record of Palearctic geckos. Hemidactylus per-

sicus. from Rohtas Fort, Jhelum valley. Punjab, Paki-

stan (Khan and Tasnim, 1990). The fort was built from

1542 to 1550 with rock-blocks transported from

Balochistan. H. persicus is the dominant house-gecko

in Balochistan and has never been reported from Pun-

jab (Khan 1987; Khan and Ahmed, 1987). The present

disjunct population most probably descended from

few individuals so transported. Presently the few

observed individuals are in severe competition with

the common indigenous house gecko, H. flaviviridis,

which is dominant throughout the building. The few

individuals of H. persicus are still holding on in

remote recesses of the fort.

Acknowledgments

We wish to express our indebtedness to Dr. George R.

Zug of NMNH for taking pholidosic counts and mea-

surements on MCZ 7132 and to Dr. Michael Golebev.

Seattle, Washington, USA for valuable discussions on

the internet and translation of Russian texts.

1999

Asiatic Herpetological Research

Vol. 8, p. 67

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Appendix 1. Abbreviations used

BMNH= British Museum, Natural History. London:

CAS= California Academy of Sciences, California,

USA; MSK= Herp laboratory, 15/6 Darul Saddar

North, Rabwah 35460, Pakistan (author's personal

collection); NMW= Naturhistorisches Museum Wien,

Austria; SR= Institute of Zoology, Academy of Sci-

ences, Kiev-30, Ukraine; UF= Florida State Museum,

Gainesville, USA; USNM= National Museum of Nat-

ural History, Washington, D.C.

Appendix 2. Additional material exam-

ined

Cyrtodactylus battalensis BMNH 1990.2; C. collega-

lensis BMNH 82.4.14.28-29; C. fasciolatus BMNH

1913.11.1 1.2; C. nebulosus BMNH 82.4.14.32-33; C.

oldhami BMNH 1916.6.22.4; C. pulchellus BMNH

1916.3.27.1-2; C.triedrus BMNH 68.3.17.11-12; C.

dattanensis MSK 0056.78: C. yarkandensis BMNH

72.3.22.4; C. tibetinus CAS 196850, CAS 196854;

Gymnodactylus walli BMNH 1910.7.12.1; G. chi-

tralensis BMNH 1946.8.23.19: Tenuidactylus batu-

rensis BMNH 1990.3; T. longipes CAS 115944, SR

307:3267-68; T. longipes voraginosus CAS 130323;

T. montiumsalsorum BMNH 1904.11.19.1 and MSK

014.86; T. indusoani MSK 0467.86; T. mhtasfortai

USNM 284133; Gymnodactylus stoliczkai (photo-

graph) NMW 16756; Tenuidactylus fedtschenkoi SR

1078:8837-8; T. caspius SR 2546:16713-14; T. turc-

menicus SR 961:8016-17.

1999

Asiatic Herpetological Research

Vol. 8, pp. 69-74

Distribution and Natural History of the Lidless Skinks, Asymblepharus alaicus

and Ablepharus deserti (Sauria: Scincidae) in the Aksu-Djabagly Nature

Reserve (Western Tian-Shan Mountains), Kazakstan

Vladimir Kolbintzev1, Larissa Miroschnichenko2, and Tatjana Dujsebayeva2

Aksu-Djabagly Nature Resene. Tjulkubas Region. South Kazakstan District 487964. Kazakstan: Department

of Biology, Kazak State University. Al-Farabi Pr. 71, Almaty 480078. Kazakstan

Abstract.- The data of 8 years observations on two species of the Lidless Skinks, Asymblepharus alaicus and

Ablepharus deserti from the Aksu-Djabagly Nature Reserve (Western Tian-Shan Mountains) are analysed with

special attention to geographical distribution and to some aspects of the natural history of these lizards. It is noted

that in spite of altitude contiguity the two species form few sympatric zones with low population density. Both

species have prolongated seasonal activity, ranging from March- April to October-November. The appearance of

the skinks after winter hibernation, their activity and the beginning of breeding season depend on climatic

conditions, slope exposition and altitude of the site.

Key words.- Reptilia, Squamata, Scincidae, Asymblepharus alaicus, Ablepharus deserti, Kazakstan, distribution,

activity, breeding.

Introduction

The Aksu-Djabagly Reserve is one of the unique natu-

ral reserves of Kazakstan. Its flora and fauna are of a

great interest because of the presence a number of

endemic and localized species, as well as of species

adapted to extreme environmental conditions. The

Aksu-Djabagly Reserve occupies the western part of

the Talas Alatau Range in the Western Tian-Shan

Mountains between 1100-4200 m s. 1. Permanent

snow level is at about 3000 m. The climate is very

continental with an average monthly temperature of -

4.9 C tor the coldest month (January) and of +21.6 C

for the hottest month (July). Four basic altitudinal

zones are present in the Reserve (Karmisheva, 1973:

Kovschar, Ivashzhenko, 1990). These are mountain

foothill zone with a low mountain dry steppe and xer-

ofitic plant association; the steppe meadows, with

scattered tree-like Juniperus forests; subalpine zone

and alpine high mountain meadows.The relatively

small territory of the Aksu-Djabagly Reserve (7400 h)

is inhabited by many species typical for the zoogeo-

graphical provinces of the Europe, North Africa and

Middle Asia. Among reptiles (total number 10 spe-

cies) there are two species of the skinks , the Alpine

Lidless Skink (Asymblepharus alaicus) and the Desert

Lidless Skink (Ablepharus deserti). The first species

(Fig. 1) is widespreaded in the Reserve, the other is

rare species of the region .

Asymblepharus alaicus and Ablepharus deserti are

of an interest from few points. The taxonomic posi-

tion Asymblepharus alaicus and Ablepharus deserti

was cleared only recently after detailed revision by

Eremchenko and Shzherbak (Eremchenko, 1981;

Eremchenko a. Shzherbak, 1986) who separated the

genus Asymblepharus and suggested an independent

evolution for the two lineages of ablepharid lizards.

Data on morphology and biology of the Alpine and

the Desert Lidless Skinks are not numerous and scat-

tered through a number of works (Atayev, 1985; Ban-

nikov et al., 1977: Bogdanov, 1960; 1965; Bruschko,

1995; Said-Aliyev, 1979; Shammakov, 1981: Shnitni-

kov, 1929; Terentjev a. Chernov, 1949; Yakovleva,

1964). The monograph by Eremchenko and

Shzherbak (1986) deservs special attention because it

contains all known data on the morphology, distribu-

tion and biology of the ablepharid lizards of the

former USSR.

The distribution and biology of two skink species

remains poorly studied. The present paper deals

mainly with the distribution of the Alpine and the

Desert Lidless Skinks in the Aksu-Djabagly Nature

Reserve and presents data on their natural history.

Material and Methods

Field observations together with the description of

live and museum material carryed out on Asymble-

pharus alaicus and Ablepharus deserti over a period

of 8 years (1988-1996) and surved as a basis for the

present paper. We observed and collected skinks from

22 localities of the Aksu-Djabagly Nature Reserve

(Fig. 2). We identifyied the species in the field basing

on their external morphology and altitude distribution.

Vol. 8, p. 70

Asiatic Herpetological Research

1999

Figure 1 . The map of the localities of the Lidless Skink in the Aksu-Djabagly Nature Reserve (Western Tian-Shan

Mountains). Asymblepharus alaicus and Ablepharus deserti have independent enumeration: open circles repre-

sent the localities of Asymblepharus alaicus, closed circles represent the localities of Ablepharus deserti. Asym-

blepharus alaicus: 1) Chuuldak (2000 m); 2) Minzhilky Ravine (2600 m); 3) Kshy-Kaindy Pass (2200 m); 4) Kshy-

Kaindy Ravine (1850 m); 5) Ulken-Kaindy Pass (2900 m); 6) Ulken-Kaindy Ravine (2000 m); 7) Kaskabulak (2600-

3300m); 8) Aksay Pass (2900 m); 9) the Upper of the Djabagly River (3000 m); 10) Kizolgenkol Lake (2200 m); 1 1)

the upper of the Middle Karasay River (3000-3100 m); 12) Low Karasay Ravine (3000-3100 m); 13) south-western

slope of Kokseky Ravine (3100-3200 m); 14) eastern slope of the Aksay Ravine (2600 m). Ablepharus deserti: 1)

western mountain foothill of theTalas Alatau Range (1300 m); 2)Taldibulak Ravine (1100 m); 3) northern moun-

tain foothills of theTalas Alatau Range near Djabagly Village (1200m); 4) Djabaglitau Range (1300 m); 5) valley

between Aksu and Baldabrek Rivers near the Kizilblek Village (1400m); 6) eastern slope of the Baldabrek Ravine

(1600 m); 7) mountain foothills near the Ergaly Ravine (1200 m).

Additionaly we used museum material fixed in 10 %

neutralized formalin and preserved in 70 ethanol. The

confirmation of species identification was mainly

based on the peculiarities of the scalation around the

eyes (see Eremchenko a. Shzherbak, 1986).

We also described character of the skink habitats

together with plant composition and visually classi-

fied the dominant substrate of the sites. Altitudes and

slope exposition were also taken into consideration.

All colonlected and museum specimens were mea-

sured in mm according to Eremchenko and Shzherbak

( 1986); their life history stages were recorded as juve-

nile, subadult, adult. All the skinks captured for the

present study were returned to the sampling sites.

Skink populaton density inferred by counting the

numbers of lizards active on the ground surface along

a transect and by turning over stones which were ref-

uges over certain small square areas.

Results and Discussion

Distribution, habitats and density of the populations-

Figure 2 shows 22 localities of two species examined.

All the records (including museum material) were

made by the authors themselves.

In the Aksu-Djabagly Nature Reserve the Alpine

Lidless Skink mostly inhabits the subalpine and

alpine zones between 2500-3000 m where the density

of the lizards is highest, particularly just on passes

and on mountain ridges. For example, on 5 August

1988 we recorded 47 specimens of Asymblepharus

alaicus along the main ridge of the Kazanchukur

Range (3100 m) over an area of 50 x 50 m and over

turning more than 150 stones. During a sunny midday

1999

Asiatic Herpetological Research

Vol. 8, p. 71

Fig. 2. Asymblepharus alaicus.

in July 1995 we observed 16 adult specimens in an

area of 200 x 30 m in the course of half of hour on the

Ulken-Kaindy Pass (2900 m). Transect accounting on

the way down to 2400 m revealed 8 specimens over an

in area of 40 x 4 m. Using secondary ranges and lat-

eral splinters of the main ridge the skinks can come

down to a slope as low as 1500 m (extremely rare to

1200 m) where they have very low population density.

The habitats of Asymblepharus alaicus in the

Aksu-Djabagly are very variable. There are alpine

meadows scattered with stones (Fig. 3), rocky slopes

with Juniperus brush (Fig. 4) and scree slopes. There

is practically no Alpine Lidless Skink in sparse Juni-

perus forests. A combination of the slopes with differ-

ent exposition is the first important condition for

Asymblepharus habitats because of the possibility of

using them during different times of the day. The sec-

ond essential condition is in the presence of suitable

refuges represented by bushes, screes or stone rub-

bles.

Typical habitats for the Desert Lidless Skink in

the Aksu-Djabagly Reserve are dry-south exposed

slopes of no more than 2000 m in altitude (Fig. 5). As

a rule, the plant community includes Ferula plant xer-

ofitic steppe, with bushes of Rosa, Honeysucle, Coto-

neaster, Spirea scattered juniper trees (Fig. 6).

However, the density of Ablepharus deserti popula-

tion in the Reserve is not high in general. Only in rare

cases we observed the lizards near human settlements.

The Aksu and Djabagly rivers with their banks of

southern and northern exposure are the natural bound-

aries separating the habitats of the Alpine and the

Desert Lidless Skinks in the reserve. The two species

were found as sympatric in few areas only. This

occurs in the valleys of rivers flowing down a slopes

Fig. 3. Subalpic meadow at 3000 m of altitude is a typi-

cal locality of Asymblepharus alaicus in the Aksu-Dja-

bagly Reserve.

Fig. 4. The locality of Asymblepharus alaicus in the

Ulken-Kaindy Valley (2100 m).

having northern exposition. In this situation around at

1200-1500 m Asymblepharus alaicus occupies, as a

rule, the river banks and Ablepharus deserti inhabits

the slopes having an eastern and western exposition

(Fig. 7). However, both species have here very low

density .

Vol. 8. p. 72

Asiatic Herpetological Research

1999

Fig. 5. The locality of Ablepharus deserti in the mouth

of the Djabagly River (1200 m).

Daily and seasonal activity

Eremchenko and Shzherbak (1986) noted that the

appearance of the skinks after winter hibernation

depends on climatic conditions, slope exposition and

altitude . According to these authors, the earliest

appearance of Asymblepharns alaicus in northern Kir-

gizstan was registrated on 26 March 1977 in the Kir-

giz Range (1600 m). In the mountains bordering the

eastern coast of the Issik-Kul Lake (2400 m) and on

the slopes of the San-Kul-Too Range having western

exposition (2700 m) the lizards appear by late April.

Yakovleva (1964) noted an earlier activity of males in

comparison with females.

Our observations on the Alpine Lidless Skink in

the Aksu-Djabagly show that lizards appear after win-

ter hibernation in mid April and, as a rule, are active

untill late October-early November. On 29 October

1992 we observed some active adult specimens on the

northexposed slopes at 1900 m. On 1 November 1995

skinks were registrated on northern slope at 1300 m.

For southern slopes , active lizards were recorded later

. Based on data of Eremchenko and Shzherbak (1986)

the last active lizards in the Kirgiz Range (up to 3000

m) were registrated on 3 November 1974. It seems the

skinks have very prolonged seasonal activity. Accord-

ing to Veventzev (1978) who studied Asymblepharus

alaicus in the Almaty Nature Reserve (Northern Tian-

Shan Mountains) some individuals were occasionally

found active during sunny days even in January-Feb-

ruary when small areas of ground get free of snow. On

5 August 1988 at altitude 3100 m we recorded the

beginning of morning activity of the lizards about

11:00 hrs; air temperature +13C. That low tempera-

ture be enough for primary skink activity may shed

some light on the prolonged yearly activity of the liz-

ards.

The daily activity of the Alpine Skink from the

Aksu-Djabagly doesn't visibly differ from that of the

Fig. 6. View on southern slopes of the Djabaglitau

Range (1 500 m). The locality of Ablepharus deserti is

in the background , the locality of Asymblepharus ala-

icus in the foreground.

Alpine skink, described by Eremchenko and

Shzherbak ( 1986) for the Kirgiz Range. These authors

wrote that in spring (April - first half of May) skinks

were active between 11:00-12:00 hrs and 19:00-20:00

hrs. According to our data for summer period, these

lizards appear on ground surface earlier and are active

untill 20:00-21:00 hrs. In autumn their activity shifts

to the second half of the day.

As a rule, Ablepharus deserti appears after winter

hibernation earlier than Asymblepharus alaicus

because of lower altitude of its habitats and the exclu-

sively southern slope expositions. In the Aksu-Djaba-

gly the earliest record for the beginning of Ablepharus

deserti spring activity was noted on 8 March 1989 at

1300 m. Most of the population, however, emerges

from hibernation in mid March. Kaluzhina (1951)

reported that also in the Turkmenistan the Desert

Skink appears after hibernation in first half of March.

According to Yakovleva (1964), in Kirgizstan lizards

of this species come to the ground surface around mid

March Paraskiv (1956) studied the Desert Skink in

southern Kazakstan also noted the first half of March

as the time for the beginning of lizard activity.

In the Aksu-Djabagly the Desert Lidless Skink is

active untill late October-early November. The latest

record here belongs to 3 November 1988. In other

regions of southern Kazakstan the skinks have the

same activity pattern (Paraskiv, 1956). Yakovleva

(1964) for Kirgizia and Said-Aliyev (1979) for Tad-

jikistan reported late September - mid October as the

perod for winter leaving of Ablepharus deserti. The

daily activity pattern of Ablepharus deserti in the

Aksu-Djabagly Reserve doesn't differ markedly from

that of the Desert Skink previously described by other

authors from the surrounding territories. A visibly

variable daily activity of A. deserti was observed by

Bogdanov (1960) in Uzbekistan. For two months in

1999

Asiatic Herpetological Research

Vol. 8, p. 73

the year (March and September) skinks are active for

most of the day (from 10:00-1 1:00 hrs to 18:00-19:00

hrs), whereas in summer they have a two-peak day

activity. The first peak occupies the time between

09:00 and 12:00 hrs. The second peak is between

17:00 and 19:00 hrs. In February and October their

activity is maximal after the midday. A two-peak

activity is also typical for the Desert Skink from Kir-

gizia (Yakovleva. 1964).

All previous authors noted that juveniles and sub-

adults appear after winter hibernation earlier than

adult specimens and return later to their winter ref-

uges.

Breeding

As was first observed by Shnitnikov (1928), viviparity

is a typical feature of Ablepharus (=Asymblepharus )

alaicus. According to Yakovleva (1964), period of

breeding activity of Asymblepharus alaicus in Kir-

gizstan occupies May-June, although some specimens

copulate in July as well. Such data contraddict to

Eremchenko and Shzherbak' (1986) who registrated

frequent copulation lizards in Kirgizstan in late

March-early April. However, this contradiction could

be a consiquence of different climatic conditions in

different years . According to Said-Aliyev' (1979) in

the southern regions of Tadjikistan the Alpine Skink

copulates in late March-April, in the northern regions

in late May-first decade of June. A single female preg-

nant with the eggs of 8.2 x 5.1 mm; 10.2 x 5.0 mm

and 10.1 x 5.0 mm in diameter was found on 3 July

1954.

In the Aksu-Djabagly Reserve, we have found 5

gravid females on 5 August 1988 at an altitude of

3100 m. One of these delivered 3 youngs on the next

day. Some pregnant females approaching delivery we

have also observed 20 July 1995 at the Ulken-Kaindy

Pass (2900 m). On the next day the new born lizards

were met at 1900m. Based on our own data and Yak-

ovleva's (1964) notes over a two-month period of

embryonic development of Asymblepharus alaicus

we consider mid May - mid June as a period of copu-

lating activity of the Alpine Skink in the Aksu-Djaba-

gly Reserve.

As noted by previous authors , for Ablepharus

deserti the egg-laying period varies depending on the

geographical location of the population. In Kirgizstan.

this period occupies the first decade of June (Yakovl-

eva, 1964). In Uzbekistan, the Desert Skink lays its

eggs after mid May. Paraskiv (1956) recorded mid

May - early June as optimal time for egg-laying by A.

deserti in the Betpak-Dala Desert (southern Kazak-

stan) and in the northern coastal territory of the Aral

Sea.

Unfortunately, we have no data on the breeding

season or on the clutch size of Ablepharus deserti in

the Aksu-Djabagly Reserve. However, some informa-

tion on the breeding activity of the Desert Skink in

Kazakstan are present in the work by Bruschko

( 1995), who notes that the beginning of the breeding

season depends on altitude. In the Borolday Moun-

tains females with eggs at the last stage of the devel-

opment were found from mid May to the second half

of June. For Northern Aral Sea region Paraskiv (1956)

recorded the beginning of egg-laying by A. deserti in

second the half of May. As Eremchenko and

Shzherbak (1986) wrote, in Kirgizstan the clutch size

of the Desert Skink varies from 1 to 5 eggs and rarely

reachs 1 1 per female. Yakovleva ( 1964) recorded 2-8

eggs per female for the Kirgizstan populations. Said-

Aliyev (1979) has found 10 July 1959 one female

having 3 eggs in every oveduct, the sizes of which

varied from 9,1 x 3,2 mm to 11,1 x 4,1 mm in diame-

ter. Shammakov ( 1981 ) notes 3-5 eggs in the clutch of

the Desert Skink from Turkmenistan.

The lizards of both species become sexually

mature in the second year (Eremchenko a. Shzherbak,

1986; Said-Aliyev, 1979).

Enemies

According to literature data (Eremchenko a.

Shzherbak, 1986 ; Said-Aliyev, 1979: Yakovleva,

1964) and to our own observation, the Halys Pit Viper

Agkistrodon halys , the Mountain Raser Coluber

ravergieri, the Dione Snake Elaphe dione, the Steppe

Ribbon Snake Psammophis lineolatum, the Steppe

Viper Vipera ursini and the among birds the Legger

Grey Shrike Lanius cristatus, the Long-tailed Shrike

L. scliasch and the Rock Thrush Monticola saxalitis

are the main enemies of both the Alpine and the

Desert Skinks in nature. We also found skink rem-

nants in the nests of the Black-billed Magpie (Pica

pica). Kuzmina (1970) observed the Himalayan Ruby

Throad (Calliope pectoralis) feeding on the Alpine

Skink in the Almaty Nature Reserve.

Acknowledgments

We thank to Sergey Gryasev who helped us in the col-

lection of the animals. We are deeply grateful to Prof.

Ilya Darevskiy (Zoological Institute of Russian Acad-

emy of Sciences, St-Petersburg, Russia) who com-

mented on an early draft of this manuscript. Our

special gratitude to Prof. Emilio Balletto (University

of Torino, Italy) and Mrs. Bell (United Kingdom) for

Vol. 8, p. 74

Asiatic Herpetological Research

1999

their useful remarks on the manuscript and detail cor-

rection of English.

Literature Cited

Atayev, Ch. 1985. Reptiles of the Mountains of Turk-

menistan. Ilym. Ashkhabad. 344 pp. (In Russian).

Bannikov, A.G., I.S. Darevsky, V.G. Ishzhenko, A.K.

Rustamov and N.N. Shcherbak . 1977. Guide to the

Amphibians and Reptiles of the Fauna of the USSR,

Prosveshcheniye, Moscow. 415 pp. (In Russian).

Bogdanov, O. P. 1960. The Fauna of Uzbekskoy SSR.

Amphibians and Reptiles. Tashkent. 260 pp. (In Rus-

sian).

Bogdanov, O.R 1965. The Ecology of the Reptiles of

Middle Asia . Nauka, Tashkent. 258 pp. (In Russian).

Bruschko, Z.K. 1995. The lizards of the deserts of

Kazakhstan. Konzhik, Almaty. 228 pp. (In Russian).

Eremchenko, V.K. 1981. Systematics of Eurasian

lygosomid skinks of the genera Asymblepharus Yeri-

omchenko et Szczerbak, 1980 and Ablepharus (Fitz-

inger in Lichtenstein, 1823) (Sauria, Scincidae). Pp.

54-55. In Problems of Herpetology, Abstr. All-Union

Conf., Nauka, Leningrad. (In Russian).

Eremchenko, V.K. and N.N. Shzherbak . 1986. Able-

pharid lizards of the fauna of USSR and adjacent

countries. Ilym, Frunse. 172 pp. (In Russian).

Karmisheva, N.C. 1973. The flora and vegetation of

the Aksu-Djabagly Nature Reserve. Nauka, Alma-

Ata. 180 pp. (In Russian).

Kovshar, A.F and A. A. Ivashzhenko. 1990. The

Aksu-Djabagly Nature Reserve. Pp. 80-102. In

Sokolov, V.E., and E.E. Siroechkovskiy (eds.). Nature

Reserves of Middle Asia and Kazakstan. Misl, Mos-

cow. (In Russian).

Kuzmina, M.A.1970. The genus Caliope. Pp.610-618.

In Dolgushin, I. A., and M.N. Korelov (eds.). The

birds of Kazakstan. Vol. 3. Alma-Ata, Nauka. (In Rus-

sian).

Paraskiv, K. P. 1956. The Reptiles of Kazakhstan.

Academy of Sciences of Kazakhstan, Alma Ata. 228

pp. (In Russian).

Said-Aliyev, S.A. 1979. The Amphibians and Reptiles

of Tadjikistan. Donisch. Dushanbe. 147 pp. (In Rus-

sian).

Shammakov, S. 1981. The Reptiles of Turkmenistan.

Ilym, Ashgabat. 312 pp. (In Russian).

Shnitnikov, V.N. 1928. The Reptiles of Semirechye.

Society for the study of Kazakstan, Kizil-Orda. 85 pp.

(In Russian).

Terentyev, PV. and S.A. Chernov . 1949. Field guide

of the reptilians and amphibians. Sovetskaya Nauka,

Moscow. 340 pp. (In Russian).

Yakovleva, I.D. 1964. The Reptiles of Kirgisia.

Frunse. 272 pp. (In Russian).

Veventzev, V 1978. On the ecology of Asymblepharus

alaicus in the Almaty Nature Reserve. Pp. 15-21. In

The book of scientific works of the students of Kazak

Paedagogical Institute. Almaty. (In Russian).

1999

Asiatic Herpetological Research

Vol. 8, pp. 75-80

Seasonal Variations of Testicular and Epididymal Structure and Plasma Levels

of Testosterone in the Soft-shelled Turtle (Pelodiscus sinensis)

Wei-ping Mao and Zhao-xian Wang

Department of Biology, Nanjing Normal University; 122 Ninghai Road, Nanjing 210097, China.

Abstract.- For purpose to consider the annual cycle of testis in soft-shelled turtle, Pelodiscus sinensis, the testes

and epididymides were examined histologically, and the plasma levels of testosterone was measured by

radioimmunoassay (RIA) though the year. Gradual increase in testicular weight from May to August was

followed by a decrease in degrees. Spermatocytogenesis was first observed from late April to early May which

remained active to August. Spermatogonial division became to decline in September and stopped by the end of

November. The epididymal weights rose from August to November and remained heavy during hibernation with

a rapid decline of about 53.76% in the mating period of next year. From July to September, the epithelial cells of

epididymal ductus grew and increased in height especially. There were a great number of secretory granules in

the cytoplasm with active synthesis. The plasma concentration of testosterone started to rise in April, which then

fell in May and June. In July, it rose rapidly to peak levels and then declined to minimum. We suggested that it's

more important that the peripheral testosterone promotes reproductive behaviour and stimulates secretion

synthesis in epithelial cells of epididymis.

Ke\ words.- Pelodiscus sinensis, testosterone.

Introduction

Only scattered and equivocal literature can be found

concerning the reptilian gametogenetic cycle, the

endocrinological function of testis and pituitary gonad

interrelationships. The information is almost exclu-

sively derived from investigations on squamate spe-

cies (Bartholomew, 1953; Lofts, 1971; Courty, 1980).

One does find, however, a few studies on such reptiles

as turtles, for example: Chrysemys picta (Callard,

1976); Pelodiscus sinensis (Lofts and Tsui, 1977);

Chrysemys dorbigni (Silva, 1984). The authors of

those studies hold identical views that the testicular

structure and function of reptiles change in annual

cycle, and the epithelium of seminiferous tubule has

spermatogenetic ability in several months while in

other months it is in a static condition (Lofts, 1987).

The aquatic soft-shelled turtle, Pelodiscus sinen-

sis, lives in rivers, lakes and ponds. The available lit-

erature on its reproduction relates only to its gonads.

Hu Zeng-Gao (1988) reported that the testis of Pelo-

discus sinensis produced sperms in reproductive

period, which were used for copulation in same

period. Lofts and Tsui ( 1977) in Hong Kong reported

the results of their studies on the histological and his-

tochemical changes in the testis. They were of the

opinion that Pelodiscus sinensis has a postnuptial pat-

tern which the spermatozoa are produced soon after

mating period. The spermatozoa are stored in the epi-

didymal canals from October until their discharge in

the following April. Seasonal changes in size and his-

tology of the testis and the accessory sexual organs

(epididymis) are well known in a lot of reptile species

(Lofts, 1969; Courty, 1979), and correlated variations

in androgen levels are documented but still poorly

detailed.

It has been shown by metabolic conversion of pre-

cursors that testosterone is the principal androgen in

some reptiles as in mammals (Callard, 1967; Hews

and Kime, 1978; Courty, 1979). Seasonal changes in

the level of circulating testosterone have been

reported in a few species of reptiles but data tend to be

differ with different species (Bourne and Seamark.

1975; Callard, 1976; Silva, 1984). Some researchers

suggested that the spermatogenesis correlated with

the plasma testosterone levels in turtles (Kuchling.

1981; Silva, 1984). In other references we found that

the highest plasma testosterone levels did not appear

in spermatogenesis period, but in mating period (Cal-

lard, 1976). Lofts and Tsui (1977) considered that the

interstitial tissue was active in steroids synthesis dur-

ing mating period, but inactive during spermatogene-

sis period. The purpose of our study, therefore, was to

determine if the variations in the plasma testosterone

levels during the annual cycle in Pelodiscus sinensis

are correlated with histological variations of the ger-

minal epithelium and epididymal canals.

Vol. 8, p. 76

Asiatic Herpeiological Research

1999

Material and Methods

Animals and samples collection

The samples used in our experiments were provided

by Chang Zhou Breeding Center of Soft-Shelled Tur-

tle (near Nangjing in Jiangsu Province in east China).

The breeding environment was similar to their natural

living condition. Except December and January every

month we obtained blood plasma, testes and epid-

idymides that those were from six adult male soft-

shelled turtles, Pelodiscus sinensis (there body

weights were about 650-1000g) in one year. The

blood plasma samples were stored at -24° until the

testosterone analysis was performed. The tissue sam-

ples of testes and epididymides were weighted and

fixed in Bouin fluid.

Histological procedures

For the histological examination, a piece of testis and

a piece of epididymis (about 25mm" ) were fixed in

Bouin fluid for 24 hours. After discolored, the sam-

ples were embedded in paraffin, cut in 5um sections,

and then stained with haematoxylin and eosin.

Testosterone assay

We determined the plasma concentration of test-

osterone by radioimmunoassay (RIA) using a tech-

nique provided by WHO. The kits used in our

experiments were from Hua Mei Biological Engineer-

ing Co. (a Sino-US joint venture). Briefly, the hor-

mone was extracted from plasma samples (250-7501)

twice with 5 ml of anhydrous ether, with an average

recovery of 96%. The extract was dried at 40° by con-

stant temperature bath, and dissolved in 2 ml phos-

phate-buffered saline containing gelatin (GPBS). we

placed 0.5 ml of this solution in duplicate assay tubes

and incubated with radio labeled testosterone (H-T

10.000 cpm) and anti-testosterone antiserum (0.1 ml)

for 18-24 h at 4°C. After removing the unbound frac-

tion with dextran-coated chorale, the samples were

placed in scintillation fluid (TP-POPOP-toluene) and

the radioactivity (cpm) was detected on a liquid scin-

tillation counter. RIA data were analyzed with a pro-

gram utilizing a weighted logic-log regression

analysis on an IBM PC. All data are as the mean

±SEM.

Results

Weight and histology

The seasonal weight variations in testes and epid-

idymides of Pelodiscus sinensis are shown as unit

body weight in Figure 1. From March (shortly after

emergence from hibernation) to April, testicular

weights remained low (particularly in April). The

seminiferous tubules remained atrophied and sper-

matogenetically inactive. The germinal epithelium

contained Sertoli cells and spermatogonia only (Fig.

2A). In April there was a significant reduction (by

about 53.76%) in the epididymal weights as sperma-

tozoa were evacuated from the epididymal canals.

During May and June the epididymal weights

declined continuously (by about 19.65%, Fig. 1).

1

35 r

30

25

20

15

10

16

14

12

%

3

8-

s.

8

O

( month )

«

10 1

M

— "

m

6 J

Figure 1 . Seasonal variations in testis and epididymis weight in the soft-shelled turtle, Pelodiscus sinensis. Each point repre-

sents mean of six values.

1999

Asiatic Herpetological Research

Vol. 8, p. 77

Figure 2. Microscopic figures of testis in the soft-shelled turtle, Pelodiscus sinensis. A. The seminiferous tubules

contracted and contained Sertoli cells (St) and spermatogonia (Sg) in April 200. B.The germinal epithelium con-

tained dividing spermatogonia, spermatocytes and spermatids in May 200. C. Spermatozoa (S) were released

from germinal epithelium in June 132. D. The thickness of spermatogenetic epithelium increased but spermatozoa

decreased in July 132. E: Spermatozoa occluded the lumen of the seminiferous tubules in August132. F: The ger-

minal epithelium atrophied in February 200.

Spermatocytogenesis started from late April to early

May, and the spermatocyte layers increased progres-

sively in germinal epithelium. The testicular weights

began to increase in May. By the end of the month,

the germinal epithelium contained dividing sper-

matogonia, spermatocytes and a few spermatides (Fig.

2B). In June, spermatozoa were released from germi-

nal epithelium (Fig. 2C) without accompanying

apparent increase in epididymal weights. The active

spermatogonia division progressed until July. The

thickness of spermatogenetic epithelium increased

and the diameter of seminiferous tubules reached

Vol. 8, p. 78

Asiatic Herpetological Research

1999

T^mm

Figure 3. Microscopic figures of epididymis in the soft-

shelled turtle, Pelodiscus sinensis. A. There were great

amount of spermatozoa (S) in the ductus, The simple

columna was thin in March 200. B. The heights of epi-

thelial cells were at maximum, great amount of sper-

matozoa could be seen in the ductus in August 200.

maximum (Fig. 2D). By the end of August, when the

testicular weights were at their top values, a large

amount of spermatozoa gathered in the lumen of the

distended seminiferous tubules (Fig. 2E) and passed

into the epididymal canals with the epididymal

weights increasing rapidly.

In September, spermatogonia! division started to

decline with less frequent mitotic figures. The germi-

nal epithelium contained mainly spermatides and

spermatozoa. At that time, testicular weights began to

decrease. By the end of November, testis atrophied

highly. And there were only a few spermatozoa

remaining in the seminiferous tubules. During hiber-

nation, the testis remained atrophied, and the germinal

epithelium was composed of Sertoli cells as well as

spermatogonia only and was heavily lipoidal (Fig.

2F). Often, there were necrotic cells in the lumen of

the seminiferous tubules.

2500 -

2000 •

1000

500

Figure 4. Seasonal variations in plasma testosterone

concentration in soft-shelled turtle, Pelodiscus sinensis.

Each point represents mean SEM of six values

In the ductus of the epididymis, spermatozoa

could be recognized in great number in most months.

Although in March soon after emergence from hiber-

nation epididymal weights were high and their ductus

were full of numerous spermatozoa (Figs. 1, 3A).

Only in June (after mating period) were there mark-

edly less spermatozoa present in the ductus of the epi-

didymis. At this time the simple columnar epithelium

of epididymis became thin and the nuclei moved

toward the basal region of the cells. From the end of

July, we could see that the spermatozoa were trans-

ported form the testis into the ductus of epididymis,

and their epithelial cells increased their heights and

secretory granules in cytoplasm. In August, their

heights reached the maximum (Fig. 3B).

Plasma testosterone concentration

The variations of the plasma testosterone concentra-

tions are shown in Figure 4. In March and April

(spring), when the testis still remained atrophied, the

mean values of plasma testosterone concentration

started to rise from 160.87 pg/ml to 613.79 pg/ml.

After that, there was a fall in plasma testosterone con-

centrations which coincided with the progressive atro-

phy of the epididymides. The plasma content

remained relatively low in June, but rapidly increased

to the highest levels (2104.97 pg/ml) in July. It did not

drop significantly until September. After that, the

plasma values fell sharply to their baseline levels in

October. It could be seen that in an annual cycle of the

plasma testosterone concentration had two peaks. The

lower peak occurred during the spring and the higher

one was in summer. The higher peak coincided with

the maximal testicular weight and the hypertrophy of

the germinal epithelial cells as well as the full growth

of epithelial cells at the epididymal ductus.

1999

Asiatic Herpetological Research

Vol. 8, p. 79

Discussion

The present study has demonstrated that the sper-

matogenetic activity of germinal epithelium changes

with season in Pelodiscus sinensis. Resemhling that of

most turtles reported (Lofts, 1987), its spermatogene-

sis resumes relatively soon after the mating period, so

that advanced germinal stage is completed before the

onset of the colder winter months. Spermatozoa are

stored in the epididymal canals until the breeding sea-

son of next year. This result is consistent with that

reported by Lofts an Tsui (1977) in Pelodiscus sinen-

sis. We have to pointed out that spermatogenetic peak

that we observed is in July and August, which is

somewhat later than that observed by Lofts and Tsui.

We suggest that this discrepancy might be due to the

different temperatures and photoperiods at different

latitudes.

The measurement of plasma testosterone in the

male Pelodiscus sinensis indicates that an annual

increase in peripheral levels begins in spring after

emergence from hibernation period and is interrupted

from the end of May through June. In July and

August, the plasma testosterone rises to its maximum

level. This finding is identical to that in tortoise,

Testudo h. hermanni, reported by Kuchling ( 1981 ). In

fresh water turtle, Chrysemys picta, the highest levels

were in spring and the lowest were in summer, while

in autumn the testosterone levels increased signifi-

cantly (Callard, 1976). Although in Chrysemys dor-

higni there was only one peak of plasma testosterone

levels, the increase started in mating period and

reached the maximum value in autumn during the

principal period of spermatogenesis {Silva, 1984). It is

similar to that in Pelodiscus sinensis.

Lofts (1968) described lipid accumulation in the

interstitial cells of the testis in Pelodiscus sinensis

which occurred prior to regression of the cells them-

selves, this indicated the cessation of steroidogenesis.

Lofts and Tsui (1977) reported that they detected 3-

HSD (-3-hydroxy steroid deydrogenase) activity in

Pelodiscus sinensis. It showed that the interstitial cells

had a positive reaction for 3-HSD and were consider-

ably depleted of lipoidal droplets in the mating period

(March- April) and in the period of enhanced epididy-

mal weight (August-October), but in active spermato-

genesis period the interstitial cells were negative to

the tests. And they said that the seminiferous tubules

gave same histochemical feature of high testosterone

secretory activity at the onset of spermatogenesis. As

well known, the secretory activity of interstitial cells

coincides with the variations of plasma testosterone

levels, because the Leydig cells are the main origin of

the plasma testosterone. Therefore, there is a discrep-

ancy about the annual cycle of the secretory activity

of interstitial cells between the histochemical study

reported by Lofts and Tsui (1977) with the direct

determination of plasma testosterone levels in our

study. We also found that the seminiferous tubules

have the ability to secrete testosterone (unpublished

result).

In the turtle Chrysemys dorbigni and the tortoise

Testudo hermanni, the maximum value of plasma test-

osterone acts on the secondary sexual organs in

autumn, preparing them for the storage of spermato-

zoa which occurs in winter (Kuchling, 1981; Silva,

1984). This situation which can also be observed in

our study. The decline of plasma testosterone levels in

Pelodiscus sinensis in May and June is associated

with the decrease in epididymal weights and the atro-

phy of the epididymal epithelium. The epididymal

epithelial cells enlarge in July and August, when the

plasma levels are highest. They increase secretary

granules progressively. During this period, the epid-

idymal weights increase significantly accompanying

with the spermatogenesis. The spermatozoa are stored

and matured in the epididymis until the following

mating period.

In our study the seminiferous tubules are sper-

matogenetically inactive when the plasma testoster-

one increases in the mating period. However, when

plasma levels are low in May, the spermatogenesis

begins. It implied that the germinal epithelium is sen-

sitive to testosterone when environmental temperature

rises. Our conclusion is that the peripheral testoster-

one in Pelodiscus sinensis is more important to sup-

port reproductive behavior and stimulate the actions

of epididymis.

Acknowledgments

We wish to express our deep gratitude to Mr. Chang

Hue for assistance in our experiment. We are grateful

to Professor Ning-Zheng Sun and Mr. Shu-Yu Gu for

graphics technical assistance. This work was sup-

ported by a grant of Education Commission of Jingsu

Province, China.

Literature Cited

Bartholomew, G. A. (1953) The modification by tem-

perature of the photoperiodic control of gonadal

development in the lizard, Xantusia vigilis. Copeia,

1953:45-50.

Bourne. A. R., and R. F. Seamark (1975) Seasonal

changes in 1 7-hydroxysteroids in the plasma of a

Vol. 8, p. 80

Asiatic Herpetological Research

1999

male lizard (Tdiqua ntgosa). Comp. Biochem. Phys-

iol., 506:535-536.

Callard, I. P. (1967) Testicular steroid synthesis in the

snake Natrix sipedon pictiventris. J. Endocrinol.,

37: 105-106.

Callard, I. P., G. V. Callard, V. Lance, and S. Eccles

(1976) Seasonal changes in testicular structure and

function and the effects of gonadotropins in the fresh-

water turtle, Chrysemys picta. Gen. Comp. Endo-

crinol., 50:347-356.

Courty, Y., and J. P. Dufaure (1979) Levels of test-

osterone in the plasma and testis of the viviparous liz-

ard (Lacerta vivipara Jacquin) during the annual

cycle. Gen. Comp. Endocrinol. J9:336-342.

Courty, Y., and J. P. Dufaure (1980) Levels of test-

osterone, dihydrotestosterone and androstenedione in

the plasma and testis of a Lizard (Lacerta vivipara

Jacquin) during the annual cycle. Gen. Comp. Endo-

crinol., 42:325-333.

Hews, E. A., and D. E. Kime (1978) Testicular steroid

biosynthesis by the green lizard Lacerta viridis. Gen.

Comp. Endocrinol., 35:432-435.

Zeng-Gao Hu (1988) Studies on relationship between

blood sexual hormone and gonadal development in

soft-shelled turtle, Trionyx sinensis Wiegmann. J.

Anhui Normal University, 4:44-51.

Kuchling, G. R. Skolek-Winnisch, and E. Bamberg

(1981) Histochemical and biochemical investigation

on the annual cycle of testis, epididymis and plasma

testosterone of the tortoise, Testudo hermanii herma-

nii Gmelin. Gen. Comp. Endocrinol.. 44:194-201.

Licht, P. (1977) Evolution in the roles of gonadotro-

pins in the regulation of the tetrapad testis. In: Repro-

duction And Evolution. J. H. Calaby and C. H.

Tyndale-Biscoe, eds. Australian Academy of Science,

Canberra, pp. 101-110.

Lofts, B. (1968) Patterns of testicular activity. In: Per-

spectives In Endocrinology: Hormones In The Lives

Of Lower Vertebrates. E. J. W. Barrington and C. B.

Jorgensen, eds. Academic Press, New York and Lon-

don, pp. 239-404.

Lofts, B. (1969) Seasonal cycles in reptilian testes.

Gen. Comp. Endocrinol. Suppl., 2:147-155.

Lofts, B., and L. Y L. Choy (1971) Steroid synthesis

by the seminiferous tubules of the snake Naja naja.

Gen. Comp. Endocrinol., 17: 588-591.

Lofts, B., and H. W. Tsui (1977) Histological and his-

tochemical changes in the gonads and epididymides

of the male soft-shelled turtle, Trionyx sinensis. J.

Zool., Lond. /S7:57-68.

Lofts, B. (1987) Testicular function. In: Hormones

And Reproduction In Fishes, Amphibians, And Rep-

tiles. O. N. David and E. J. Richard, eds. Plemum

Press, New York and London, pp. 283-325.

Silva, A. M. R., G. S.Moraes, and G. E Wassermann

(1984) Seasonal variations of testicular morphology

and plasma levels of testosterone in the turtle Chryse-

mys dorbigni. Comp. Biochem. Physiol., 78-4:153-

157.

Yip, D. Y. and B. Lofts (1976) Adenohypophysial

cell-types in the pituitary gland of the soft-shelled tur-

tle, Trionyx sinensis. I. seasonal cycles. Cell Tiss.

Res., 770:523-537.

1999

Asiatic Herpetological Research

Vol. 8, p. 81

Food Consumption and Growth of Juvenile Chinese Soft-shelled Turtles

(Pelodiscus sinensis) in Relation to Body Weight and Water Temperature

CUIJUAN NlU, TlNGJUN ZHANG AND RUYONG SUN

Department of Biology. Beijing Normal University; Beijing 100875, China

Abstract.- Food consumption and growth of juvenile Chinese soft-shelled turtles {Pelodiscus sinensis) with

different body weight were measured in the laboratory at 22, 26, 28, 30, 32 and 35 °C. At 30 °C, the daily

maximum consumption Cmax (J/ind. • day) showed the following relationship with body weight W (g): Cmax =

47.58 W^ . The correlation between the maximum daily food consumption rate Rmax (J/g • day) of a turtle

with a standard body weight of 40 g, and temperature could be described as: logRmax = -0.01 36T2 + 0.8372T -

1 1.42. At ± 31 °C. a turtle with a standard body weight of 40 g has the biggest daily consumption rate of 447 J/g

• day. The daily growth rate GR (g/day) had a functional relationship with body weight at 30 °C: GR =

0.04 W0-8-48. For a turtle with a standard body weight of 40 g, GR showed the following relationship with water

temperature: GR = 30.138 - 3.671T + 0.147T2 " 0.002T3, and at 30 °C, turtles had the biggest daily growth rate

of 1.06 g/day. Gross conversion rate of the juvenile turtles (9-109 g) did not vary with body weight, but

temperature had a distinct effect on it.

Key words.- Reptilia, Testudines, Trionychidae, Pelodiscus, China, bioenergetics.

Introduction

The Chinese soft-shelled turtle (Pelodiscus sinensis)

is an aquatic chelonian of great commercial impor-

tance, widely distributed in China. Resource of this

species has decreased sharply in recent years. There-

fore, its aquaculture has become more and more

important. Basic information on the biology of P. sin-

ensis is very important in developing the technology

of its cultivation. Bioenergetics of this species is one

aspect that has not been well-studied yet (Niu et al.

1994). The purpose of this study was to investigate the

effects of body weight and water temperature on food

consumption and growth of juvenile soft-shelled tur-

tles.

Material and Methods

The experimental animals were juveniles with a live

weight ranging from 7 g to 1 12 g reared in the labora-

tory. The diet used in the experiment contained 50%

crude protein, 3% crude fat, 9.5% carbohydrate and

15% ash. Energy value of the diet was 14.64 KJ/g.

Rearing conditions

Each experimental animal was housed in a 4.6 1 glass

aquarium filled with clean tap water. 6-8 aquariums

were placed in a water bath with water temperature

controlled to an accuracy of ± 0.5 °C. The animals

were tested at six different temperatures (22, 26, 28,

30, 32 and 35 °C). The photoperiod was 12L:12D.

Turtles were fed to satiation twice a day at 8:00 and

16:00. Each turtle was acclimated at the test tempera-

ture for at least one week before the feeding experi-

ment started.

Experimental process

Before the start of the feeding experiment, turtles

were not offered food for 48 hours and weighted. In

the experiment, turtles were fed to satiation with a

pre-weighted amount of food. The uneaten portion

and feces were collected with a decompression con-

centrition equipment and dried with control diet at 65

°C to a constant weight. Food consumed by a turtle

was the difference between the dry weight of pre-

weighed amount of food and the uneaten portion. The

feeding regime lasted for a month followed by two

days of fasting. After the experiment, fresh weight

was measured again and some of the experimental

animals were sacrificed and dried to a constant weight

on 65 °C. Caloric value of the dried diets, feces, and

turtles were all measured with a Schimdzu CA-4P

caloric meter.

Data analysis

The daily maximum consumption, Cmax is an average

value during the whole experimental period. R^^ =

Cmax/W. W is the mean value of the initial and final

weight of the turtle. The daily growth rate in wet

Vol. 8, p. 82

Asiatic Herpelological Research 1 999

3.6

2.6-

oo

0.6

y = -0.01 36x2 + 0.8372X - 1 0.8 r2 = 0.83

• Standard value

° Measured value

20

— r~

30

— i

40

Temperature (°C)

Figure 1. Relationship between the daily maximum consumption rate. Rmax (J/g ■ day) of a turtle with a standard

body weight of 40 g (average value of all experimental animals) and water temperature.

weight, GR = (W, _ W0)/t, where W, and W0 is the

body weight at the end and the beginning of the

experiment, respectively, and t is the experimental

period. The gross conversion efficiency, CE — named

as the percent of energy used for body growth to con-

sumed energy — was calculated. All data were analy-

sed with SPSS/PC statistical software.

Results

Analysis of covariance showed that the maximum

food consumption of a turtle was greatly affected by

body weight and water temperature. Multiple regres-

sion analysis showed the following relationships

among the daily maximum consumption, Cmax (J/ind.-

day), wet body weight, W (g) and water temperature,

T (°C): logCmax = 0.73381ogW + 0.83541ogT -

0.0136T2 " 1 1.00; (r = 0.98, n = 45, P < 0.01). At 30

°C, Cmax (J/ind.- day) showed the following relation-

ship with body weight W (g): Cmax = 47.58W0-7907;

(r = 0.92, n = 30).

Figure 1 shows the relationship between the daily

maximum consumption rate, Rmax (J/g • day) of a tur-

tle with a standard body weight of 40 g (average value

of all experimental animals) and water temperature.

Their relationship could be described as: logRmax = -

0.0136T2 + 0.8372T - 1 1.42 (r = 0.83, n = 45). At ±

3 1 °C, a turtle with a standard body weight of 40 g has

the biggest daily food consumption rate of 447 J/g •

day. The daily growth rate, GR (g/day) also had a

close relationship with body weight and water tem-

perature, which could be showed as the following: GR

= 0.0165W + 0.9142T - 0.0156T2 " 13.16 (r = 0.89,

n = 45, P < 0.01).

Figure 2 shows the relationship between the daily

growth rate, GR (g/day) of a turtle with a standard

body weight of 40 g and water temperature. At 30 °C,

a turtle with a standard body weight of 40 g has the

biggest daily growth rate of 1.06 g/day. At 30 °C, GR

had a functional relationship with body weight as: GR

= 0.04W08248 (r = 0.78, n = 39). At five different

body weight groups ranging from 9-109 g, no distinct

differences were found among their gross conversion

efficiency, CE (F4,20 = 0.96, P > 0.05), but the tem-

perature had a distinct influence on CE (F5.20 = 4.21,

P < 0.01 ). At 22 °C, CE was about 59%. At 26-32 °C,

CE ranged from 21-27%. At 35 °C, CE declined to

12%.

Discussion

According to the present work, temperature has a pos-

itive effect on the daily maximum food consumption

and growth under 3 1 °C, but above 3 1 °C, the effect

becomes negative. Temperature for maximum growth

rate is slightly lower than the temperature for maxi-

mum food consumption. This phenomenon has also

been observed in similar studies of the lizards Uta

1999

Asiatic Herpetological Research

Vol. 8, p. 83

y = -0.0019x3 + 0.1469x2-3.6708x + 30.138 r' = 0.99

v2P

2

O

Temperature CC)

Figure 2. Relationship between the daily growth rate, GR (g/day) of a turtle with a standard body weight of 40 g

and water temperature.

stansburiana (Waldschmidt et al. 1986) and Takydro-

mus septentrionalis (Ji et al. 1993), and the southern

catfish (Silurus meridionalis) (Xie and Sun 1992).

This study indicates that effects of temperature on

food consumption and growth of soft-shelled turtles

resemble that of most fishes (Brett and Groves 1979)

and some lizards. More comparative studies should be

conducted for other reptile species.

The body weight has a double logarithm relation-

ship with Cmax, and the slope of the regression line is

0.79. This value is very similar to the exponent b

value 0.75 in the metabolic rate to body weight

regression line for turtles (Bennett and Dawson 1976).

This phenomenon suggests that food consumption is

related to metabolic rate of the turtle. As energy loss

through metabolism is a large component in the

energy budget, metabolism level may affect energy

intake to remain an effective budget. Studies on the

relationship of food consumption and metabolic rate

are recommended. Perhaps the maximum consump-

tion rate can be defined as an index of daily metabo-

lism level of the animals.

The gross conversion rate, CE is a reflection of the

consumed energy alloted to body growth. Our work

showed that under 109 g body weight, CE values of

the juvenile turtles were similar. Temperature has a

distinct effect on CE. The relatively high CE (59%) at

22 °C may be explained by the distinctly low meta-

bolic cost at a low temperature. From 26-32 °C, CE

was relatively similar, but declined at 35 °C. Smith et

al. (1981) found that for juvenile walleye pollock

(Theragra chalcogramma), CE was higher at colder

temperatures. Cui et al. (1995) showed that water tem-

perature had no effect on CE in the grass carp

(Ctenopharyngodon idella). Perhaps the relationship

of temperature with CE varies with different species.

In this work we present mathematical models

relating maximum food consumption and growth rate

to water temperature and body weight. The results can

be utilized for estimating daily amount of food needed

by juvenile turtles according to water temperature and

body weight in a turtle-culture farm.

Acknowledgments

We thank Mrs. Xihuang Cheng for her assistance in

the experiments. Thanks are due to Dr. Balazs Farkas

for improving the manuscript. We also thank Dr. Yibo

Cui for his valuable comments on the paper. The work

Vol. 8, p. 84

Asiatic Herpetological Research\999

was supported by the Chinese National Foundation of

Natural Science and the Foundation of State Key Lab-

oratory for Freshwater Ecology and Biotechnology of

China.

Literature Cited

Bennett, A.F. and W.R. Dawson 1976. Metabolism.

Pp. 127-223 //; C. Gans (ed.), Biology of the Rep-

tilia, Volume 5. Academic Press, London and New

York.

Brett, J.R. and T.D.D. Groves 1979. Physiological

energetics. Pp. 279-352 In W.S. Hoar et al. (eds.).

Fish Physiology, Volume 8. Academic Press, New

York.

Cui. Y, S. Chen and S. Wang 1995. Effect of tempera-

ture on the energy budget of the grass carp,

Ctenopharyngodon idellus Val. Oceanologia et Lim-

nologia Sinica 26:169-174.

Ji, X., W.H. Zhou, G.B. He and H.Q. Gu 1993. Food

intake, assimilation efficiency and growth of juvenile

lizards Takydromus septentrionalis. Comparative Bio-

chemistry and Physiology 105A:283-285.

Niu, C.J., T.J. Zhang and R.Y Sun 1994. Energy

metabolism of the soft-shelled turtle Trionyx sinensis

— Aquatic respiration, relative to body weight and

water temperature. Journal of Beijing Normal Univer-

sity 30:536-539.

Smith. R.L., A.J. Paul and J.M. Paul 1986. Effect of

food intake and temperature on growth and conver-

sion efficiency of juvenile walleye pollock (Theragra

chalcogramma): a laboratory study. Journal du Con-

seil international pour l'Exploration de la Mer

42:241-253.

Waldschmidt, S.R., S.M. Jones and W.P Porter 1986.

The effect of body temperature and feeding regime on

activity, passage time, and digestive coefficient in the

lizard Uta stansburiana. Physiological Zoology

59(3):376-383.

Xie, X.J. and R.Y. Sun 1992. Maximum ration level in

the southern catfish (Silurus meridionalis Chen) in

relation to body weight and temperature. Acta Ecolog-

ica Sinica 12(3):225-231.

1999

Asiatic Herpetological Research

Vol. 8, pp. 85-89

First Record of the Lacertid Acanthodactylus boskianus (Sauria: Lacertidae)

for Iran

Nasrullah Rastegar-Pouyani

Department of Zoology, Goteborg University. Box 463, SE 405 30 Goteborg, Sweden

Abstract.- The first record of the lacertid li/.ard Acanthodactylus boskianus for Iran is presented based on

material collected by the author in 1995 and 1996 from 2 km west of Harsin, Kermanshah province, western Iran,

on the Astragalus -covered sandy hills at about 1420 m elevation. Systematics and distribution of this lizard are

discussed and its conventional known subspecies are questioned.

Key words.- Acanthodactylus boskianus, Lacertidae, Subspecies,

province, Harsin, Systematics, Distribution.

New record. Western Iran, Kermanshah

Figurel . The distribution of Acanthodactylus boskianus in

north Africa and the Middle East.

Introduction

The lacertid genus Acanthodactylus Wiegman, 1834

consists of about 30 species, distributed from Spain

and Portugal across the Sahara desert and its periph-

ery to the Red Sea, over most of Arabia and as far

north as Cyprus and the Syrian-Turkish border; it also

extends through Iraq, southern, and eastern Iran,

southern Afghanistan. Pakistan and northwestern

India (Arnold, 1983).

Apart from the present record, four additional spe-

cies of this genus occur in Iran, mainly in southern

and eastern parts of the country (A. micropholis, A.

grandis, A. schmidti, and A. blanfordi) (Anderson,

1974; Anderson, in press; Salvador, 1982). As well,

A. opheodurus Arnold, may occur in lowland south-

western Iran (Anderson, in press). The genus is

Saharo-Sindian in its affinities and distribution and

does not penetrate to a great extent into the Iranian

Plateau and only two species go beyond the plateau as

far east as Afghanistan, Pakistan, and northwestern

India (A. cantoris and A. micropholis) (Clark, 1990;

Figure 2. The locality of Acanthodactylus boskianus spec-

imens collected by the author from Harsin, southeast

of Kermanshah Province, western Iran. (|) = Harsin,

(□) = Locality of A. boskianus specimens.

Salvador. 1982). This genus has recently been revised

by Salvador (1982) and Arnold (1983) who divide it

into 9 species groups. Among these groups is the "A.

boskianus and A. schreiberi "group defined by several

distinguishing characters (Arnold, 1983: 315).

So far, there is no record in the literature for the

occurrence of A. boskianus in Iran. In this paper, I

report this taxon for the first time inside Iranian terri-

tory based on three specimens (two adults and one

juvenile) collected from Kermanshah province, west-

ern Iran during my two long-term excursions on the

Iranian Plateau in 1995 and 1996.

Acanthodactylus boskianus (Daudin, 1802)

Lacerta boskiana Daudin, 1802, 3: 188, PI. 36, Fig.

2 (type locality: Egypt).

Bosc's fringe-toed lizard.

Vol. 8. p. 86

Asiatic Herpetological Research

1999

j&k*.

Figure 3. Acanthodactylus boskianus, top to bottom:

male, female, juvenile.

Definition: Usually 4 entire supraoculars, occasion-

ally the 1st divided; anterior border of ear pectinate;

temporal scales more or less keeled; eyelids slightly

denticulated; conspicuous gular told; 3 series of

scales around fingers; ventrals usually in 10 (and

sometimes 12) straight longitudinal rows; usually

large, keeled, imbricate dorsals (sometimes small,

slightly keeled and imbricate); granular scales on

flanks; moderate to strong fringe on 4th toe: upper

surface of tail with large, imbricate, sharply keeled

scales.

Distribution: A. boskianus is the most widespread

species of the genus and occupies a large area from

north Africa (Mauritania, Morocco, Algeria, Mali,

Niger, Tunisia, Libya, Chad, Nigeria, Sudan, Ethio-

pia, Egypt) eastward into the Middle East (Israel,

Lebanon, Jordan, Iraq, Syria, Turkey, and Arabian

peninsula) (Salvador, 1982). It is also reported for the

first time from Iran [(present paper) (Figs. 1-2)].

Collecting of A. boskianus specimens

I conducted two long-term excursions and field work

in various parts of the Iranian plateau in 1995 and

1996. On July 8, 1995, I surveyed the area around

Harsin, a small town in southeastern Kermanshah

province, western Iran to collect Trapelus ruderatus

and Laudakia nupta for ongoing research. In 2 km

west of Harsin (34° 17' N, 47° 24' E) on the sandy

hills covered by various species of Astragalus, I col-

lected a lacertid specimen incidentally. It was an adult

male of A. boskianus (GNHM Re. ex. 5142). I sur-

veyed this locality several times in 1995, but I could

not find more specimens of A. boskianus. Again, on

August 29, 1996, and during my second field trip to

Iran, I surveyed the same area and collected two other

specimens of A. boskianus, an adult female and a

juvenile (GNHM Re. ex. 5143-4) (Fig. 3). I collected

all specimens on an Astragalus -covered sandy hill.

£*:•<

Figure 4. Acanthodactylus boskianus on the top of an Astragalus bush, 2 km west of Harsin, Kermanshah Province,

western Iran.

1999

Asiatic Herpetological Research

Vol. 8. p. 87

among or under the Astragalus bushes. It seems that

they have acquired special adaptations for living

among and on the spiny bushes of Astragalus (Fig.

4).

Remarks

The three specimens which I collected 2 km west of

Harsin, Kermanshah province, western Iran, have the

general characteristics of most other A. boskianus

specimens except that the dorsal scales are relatively

small, as is the case in the Iraqi and Syrian popula-

tions. The main characteristics of these specimens are

as follows:

Maximum SVL (Snout-Vent Length) = 65.5 mm;

maximum TL (Tail Length) = 134 mm; scales across

mid-dorsal region 43-48: ventral plates in 10 longitu-

dinal rows with an extra row of smaller plates on each

side; four entire supraoculars; temporal region

slightly keeled, subocular does not reach the mouth

and is wedged between the 4th and 5th supralabial; 7

/ 7 upper and 7/7 lower labials; temporal scales fee-

bly keeled: anterior edge of tympanum feebly ser-

rated: feeble to moderate pectination of eyelids; 5/5

supraciliaries; 22-25 femoral pores; dorsal scales rela-

tively small and feebly keeled: 3 rows of scales

around fingers; 8-9 collar plates; distinct gular fold;

25-27 scales in a longitudinal row from symphysis of

chin shields to collar; 2 1-23 keeled lamellae under the

forth toe which is not exceptionally pectinate; ventral

plates in 25-30 transverse rows; 13-15 scales between

hindlegs; 25-26 scales on the 5th caudal whorl behind

the vent.

Coloration and color pattern: In the male speci-

men dorsum sandy grey with two light dorsolateral

stripes on each side enclosing a broad brown band

with light reticulations, also a weakly visible dark-

brown vertebral stripe present; base of tail with two

light lateral stripes, distal 4 / 5 of tail uniformly grey

dorsally, upper surface of limbs greyish-brown with

numerous light spots: upper surface of head olive-

brown; all of the ventral surfaces whitish.

In the female specimen dorsum is dark brown with

7 narrow, light stripes, the two dorsolateral ones on

each side being lighter and in strong contrast with the

dark-brown pattern of back, the three vertebral and

paravertebral ones duller, proximal 1/4 ventral part of

tail whitish, distal 3/4 pink or bright-red, other ventral

surfaces whitish.

In the juvenile specimen, upper surface of head is

light olive, dorsum dark-brownish-black with 6

strongly contrasting light lines, vertebral stripe whit-

ish on neck, disappears towards the posterior part of

back.

Systematic account

As pointed out before, Acanthodactylus boskianus is

the most widespread species of its genus. It occurs

throughout a wide range which is extended from north

Africa into the Middle East. It is a polytypic taxon

and very well represented in most museum collections

and shows obvious geographic variation in different

parts of its range. Traditionally, A. boskianus has

been divided into three subspecies; A. b. boskianus

(Daudin, 1802) in the Nile delta and some parts of

Sinai, A. b. euphraticus Boulenger 1919, from

Ramadieh (central Iraq), and A. b. asper (Audouin,

1829) which covers almost the whole of the species

range (Arnold, 1983; Boulenger, 1919, 1921; Salva-

dor, 1982).

Boulenger (1919, 1921) divided the populations of

A. boskianus into three varieties (subspecies):

The first subspecies, A.b. boskianus (forma typ-

ica), characterized by the lack of subocular contact

with the lip, the common division of the first supraoc-

ular, and the small and numerous dorsal scales (34-

52). The second subspecies, A. b. asper, characterized

by a subocular which does not border the lip, an undi-

vided first supraocular, and the large, relatively few

dorsal scales (23-38). And the third subspecies, which

I have examined the syntypes, A. b. euphraticus

(described based on 8 specimens collected at

Ramadieh on the Euphrates Front, central Iraq, in

1918 by Boulenger's son Capt. C. L. Boulenger), is

characterized by a subocular which is usually border-

ing the mouth (in 7 out of 8 specimens = 87.5%), 38-

43 scales across middle of body, 14-16 scales between

hind limbs, and 23-37 femoral pores on each side.

This simple tripartite division is not satisfactory,

for some of the supposedly distinctive features of A. b.

euphraticus are not consistent and there is some dif-

ferentiation within the populations assigned to A. b.

asper (Arnold, 1983).

As the separation or contact of subocular with the

lip is not a fixed character, it can not be considered of

taxonomic value. As well, scale counts which were

once thought typical for subspecies proved to be clinal

and are therefore not apt to discriminate subspecies

(Schleichetal., 1996).

On the other hand, Salvador (1982) divided vari-

ous populations of -4. boskianus into four groups;

north African populations, Egyptian populations, Ara-

bian populations, and Iraq, Syria, and Jordan popula-

tions. According to this author, the populations of

Vol. 8, p. 88

Asiatic Herpetological Research

1999

north Africa are relatively uniform, suggesting a

recent invasion to this region. There is a progressive

degree of variation towards the eastern part of the

range, in the Middle East. As the position of the sub-

ocular greatly varies in individuals throughout this

species entire area of distribution (this being espe-

cially so in Iraq), the taxonomic value of this charac-

ter is greatly reduced (Salvador, 1982). According to

Arnold ( 1983), over most of north Africa, the number

of dorsal scales in a transverse row at mid-body varies

from 26-41. I have examined specimens of A. boski-

anus from Sudan, Morocco, and Libya (see under

material examined). All of these specimens have 35-

37 scales across mid-body and, apparently, belong to

A. b. asper. As well, Arnold (1980) regards all popula-

tions of this lizard in the Arabian peninsula as A. b.

asper. In the Nile delta and north Sinai, populations

assigned to A. b. boskianus have high dorsal scale

counts (34-52). Populations with high dorsal counts

(38-48) also occur in northeast of Jordan, northern

and central Iraq, east Syria and adjoining Turkey. In

one specimen from Jordan (GNM.Re. ex. 4799)

which I have examined, there are 40-43 scales across

middle of dorsum. Arnold (1983) believes that geo-

graphic variation in A. boskianus reflects differences

in niche across its range. This species is often associ-

ated with dense vegetation and large dorsal scales

may well be protective when shrubs are rigid and

spiny. The fine-scaled populations occur in relatively

mesic areas where vegetation is less damaging than in

more arid regions. Reed and Marx ( 1959) reported A.

schreiberi, based on having numerous dorsal scales,

from Jarmu. Kirkuk Liwa. northern Iraq, in an iso-

lated area far from the nearest known localities for

this taxon in Lebanon. Salvador (1982) examined

these specimens and attributed them to A. boskianus.

Due to scarcity of material, the presence of A.

schreiberi in Iraq needs more confirmation. I have

studied three specimens of A. schreiberi

(GNM.Re.ex. 4646 [1-3]) from Cyprus. They have

51-59 small, rather granular, smooth, or weakly

keeled, scales across widest part of dorsum and 12

ventral plates across the widest part of venter. As well,

the temporal scales are smooth and the anterior edge

of tympanum is not serrated or very weakly so.

According to Khalaf (1959), both A. b. asper and A.

b. euphraticus occur in Iraq without specifying their

exact localities. Also. Leviton et al. ( 1992) regard A. b.

asper as the subspecies found in Iraq.

Based on the fore mentioned discussion, and with

respect to characteristics of specimens collected by

the author, it is evident that these specimens belong to

a form with fine and numerous dorsal scales which are

weakly keeled, intact first supraocular, and lack of

subocular contact with the mouth. These specimens

do not entirely fit into the Boulenger's tripartite key

(Boulenger, 1919, 1921 ). Since there is no more mate-

rial at hand, it may be difficult to say if they represent

the fourth form of A. boskianus or not. An adequate

intraspecific treatment of A. boskianus is beyond the

scope of this paper. Thus, I have chosen not to use a

subspecific name for my own material, pending a

thorough and knowledgeable revisionary work on this

widespread and polytypic taxon. In spite of the con-

siderable variation which occurs in A. boskianus, as

mentioned above, there is as yet no definitive evi-

dence that it consists of more than one species. It

appears that A. schreiberi has originated as an isolate

of A. boskianus (Arnold, 1983).

Material examined

Acanthodactylus boskianus (n = 3): GNHM. Re. ex.

5142-44, from Harsin (34° 17' N, 47° 24' E), Ker-

manshah province, western Iran.

Acanthodactylus boskianus euphraticus (n = 8):

BMNH 1946. 8. 4. 83-90, from Ramadieh, Iraq (33°

25'N,43° 17' E).

Acanthodactylus boskianus asper (n = 4): GNHM.

Re. ex. 3333, 3346, 4799, 4937, from Sudan,

Morocco, Libya, and Gaza respectively.

Acanthodactylus schreiberi (n = 3): GNHM. Re. ex.

4646 (1-3), from Cyprus.

Abbreviations

BMNH = British Museum (Natural History);

GNHM. Re. ex. = Gothenburg Natural History

Museum, Reptilia exotica.

Acknowledgements

I wish to thank Goran Nilson, for critically reviewing

of the manuscript as well as providing me Acantho-

dactylus boskianus and A. schreiberi specimens from

the collections of Gothenburg Natural History

Museum. I would like to thank Colin MacCarthy,

Department of Zoology, British Museum (Natural

History) for loan of syntypes of Acanthodactylus

boskianus euphraticus.

I am also grateful to S. C. Anderson, Biological

Science Department, University of the Pacific, Stock-

ton, California, for all of his recommendations,

encouragements, and sending informative literature,

especially his unpublished work concerning the Ira-

nian lacertids, as well as critically reviewing of this

paper.

1999

Asiatic Herpetological Research

Vol. 8, p. 89

Also, my special thanks go to the Razi University

Authorities (Kermanshah, Iran) and Ali Rassuli for

their unsparing helps during field work in western

Iran.

This work was partly supported by grants from the

Royal Swedish Academy of Sciences (Hiertza-Ret-

zius Fond), Anna Ahrenbergs and Wilhelm and Mar-

tina Lundgrens Foundations.

Literature Cited

Anderson, S. C. 1974. Preliminary key to the Turtles,

Lizards, and Amphisbaenians of Iran. Fieldiana: Zool.

65: 27-44.

Anderson, S. C. (In press). The lizards of Iran. Society

for the study of Amphibians and Reptiles.

Arnold, E. N. 1980. The Reptiles and Amphibians of

Dhofar, Southern Arabia. Pp. 295-307. In The Journal

of Oman Studies, Special Report No. 2.

Arnold. E. N. 1983. Osteology, genitalia and the

relationships of Acanthodactylus (Reptilia: Lac-

ertidae). Bull. Brit. Mus. Nat. Hist. Zool. Sen, Vol. 44,

No. 5.

Audouin, J. V. 1829. Explication sommaire des

planches de reptiles (supplement) publiees par Jules-

Cesar Savigny. Pp. 97-140. In Description de 1' Egypt

(second edition), Vol. 24. C. L. F. Panckoucke, Paris.

Boulcnger, G. A. 1919. On a new variety of Acantho-

dactylus boskianus Daudin, from the Euphrates. Pp.

459-460. In Ann. & Mag. Nat. Hist. Ser. 9, Vol. 3.

Boulcnger, G. A. 1 92 1 . Monograph of the Lacertidae.

Vol. 2, British Museum (Natural History), London.

Clark, R., 1990. A report on herpetological observa-

tions in Afghanistan. Brit. Herp. Soc. Bull., 33: 20-24.

Daudin, F. M. 1802. Histoire naturelle generale et par-

ticuliere des reptiles. Dufart, Paris.

Knalaf, K. T. 1959. Reptiles of Iraq, with some notes

on the Amphibians. Ar-Rabitta press, Baghdad, vii +

96 pp.

Leviton, A. E., S. C. Anderson., K. Adler., and S. A.

Minton. 1992. Handbook to Middle East Amphibians

and Reptiles. Society for the study of Amphibians and

Reptiles, vii + 252 pp.

Reed, C. A., and H. Marx. 1959. A herpetological col-

lection from northeastern Iraq. Trans. Acad. Sci. Kan-

sas 62: 91-122.

Salvador, A. 1982. A revision of the lizards of the

genus Acanthodactylus (Sauria: Lacertidae). Bonner

Zool. Monogr. No. 16.

Schleich, H. H., K. Werner, and K. Kabisch. 1996.

Amphibians and Reptiles of North Africa. Biology,

Systematics, Field Guide. Koeltz Scientific Books

Pub., pp. 378-381.

1999

Asiatic Herpetological Research

Vol. 8, pp. 90-101

Two New Subspecies of Trapelus agilis Complex (Sauria: Agamidae) From

Lowland Southwestern Iran and Southeastern Pakistan

Nasrullah Rastegar-Pouyani

Department of Zoology, Gbteborg University, Box 463, SE 405 30, Goteborg, Sweden, e-mail:

nasrallah.pouyani@zool.gu.se

Abstract.- Based on conducting long-term excursions and carrying out extensive field work in various parts of the

Iranian Plateau and studying preserved (museum) material including the syntypes of Olivier's Agama agilis, and

paralectotypes of Boulenger's Agama isolepis, two new subspecies of the wide-ranging Asian ground agamid

Trapelus agilis complex are described from the lowland southwestern Iran and southeastern Pakistan (and

adjoining northwestern India) respectively. The former of the new subspecies has conventionally been considered

as belonging to T. a. agilis, and the latter to T. a. isolepis. They are distinguishable from the other subspecies of T.

agilis complex by having several distinctive morphological characteristics. The distinctiveness of both

subspecies is confirmed according to the author's previous extensive studies on this complex using uni- and

multivariate analyses of morphological characters. Both subspecies mainly occur as geographical isolates in the

periphery of the main range of the complex, and both have mainly been separated from the central continuum (=

T. a. agilis) by eco-geographical barriers and are almost entirely restricted in distribution to the lowlands, desert

and semi-desert regions with high annual temperature. A taxonomic and biogeographic account as well as a key

to subspecies of T. agilis complex are presented.

Key words.- Trapelus agilis complex, T a. khuzistanensis, T a. pakistanensis. New subspecies, Agamidae,

Lowland southwestern Iran, Southeastern Pakistan, Systematics, Distribution, Biogeography.

Introduction

The, taxonomically, controversial ground agamid

Trapelus agilis is a wide-ranging species complex dis-

tributed from extreme southwestern Iran (ca 31° N,

47° E) to eastern Kazakhstan and western China (ca

48° N, 83° E) (Fig. 1 ), encompassing numerous local

populations (Rastegar-Pouyani, 1998). Traditionally,

this complex has been divided into three subspecies;

Trapelus agilis agilis (Olivier, 1804), T. a. sanguino-

lentus (Pallas, 1814), and T a. isolepis (Boulenger,

1885) (e.g., Anderson, 1974: Welch, 1983; Wettstein,

1951). The latter two subspecies are sometimes

regarded as full species by some authors (e.g., Anan-

jeva, 1981; Ananjeva and Tsaruk, 1987: Boulenger.

1885; Moody, 1980; Nikolsky, 1915; Zhao and Adler,

1993). On the other hand, Anderson (in press) places

all different forms of T. agilis complex under the

inclusive name "agilis" and believes that without a

firm statistical ground, it is not advisable to divide the

complex into separate taxonomic entities.

In a series of studies, using uni-and multivariate

statistics, the author analysed geographic variation in

T. agilis complex, synonymized T. a. isolepis (Bou-

lenger) with T. a. agilis (Olivier), designated a new

type locality as "terra typica designata" (central Ira-

nian Plateau, about 1 10 km southeast of Esfahan city)

Figure 1 . Geographic distribution of Trapelus agilis

complex. (□) = 7erra typica designata (central Iranian

Plateau, about 1 10 km southeast of Esfahan city)

(Fig. 1 ), and showed that T. agilis complex consists of

four distinct taxonomic entities (subspecies) and that

the traditional tri-partite division of the complex, to a

great extent, does not portray the actual phenetic pat-

terns of geographic variation (Rastegar-Pouyani, in

press, unpublished manuscript). The four distinct sub-

species identified are as follows:

T. a. agilis (Olivier, 1804) is distributed in the

central Iranian Plateau, central and southern Afghani-

stan, and southwestern Pakistan. Populations of this

1999

Asiatic Herpetalogical Research

Vol. 8, p. 91

Figure 2. Trapelus agilis khuzistanensis, holotype

(GNHM Re. ex. 5424); A- dorsal view, B- ventral view.

Note that almost all dorsal scales are distinctly small

and only slightly keeled.

form (as the central core of the complex) are morpho-

logically most similar to the syntypes of Olivier's

Agama agilis.

T.a. sanguinolentus (Pallas, 1814) is the northern

representative of the complex, distributed over a wide

area from northeastern Iran into the Central Asian

countries as far east as western China (Anderson, in

press; Rastegar-Pouyani, 1998; Zhao and Adlcr,

1993). The two other taxa, described in this paper as

new subspecies, are geographically isolated, occur-

ring in the southwestern and southeastern margins of

the main range of T. agilis, and mainly separated from

the central continuum (7^ a. agilis) by eco-geographi-

cal barriers. Both new subspecies are morphologically

different from the syntypes of Olivier's Agama agilis

based on several distinguishing characters (Table 1 ).

Since the subspecific name "isolepis" has been

synonymized with "agilis" and is no longer available

(Rastegar-Pouyani, in press), new taxonomic names

are designated for these two new subspecies.

So, the main objective of this work is to describe

and introduce these two new taxonomic entities based

on the study of distinguishing morphological charac-

ters which make them recognizable from the other

subspecies of T. agilis complex.

Material and Methods

I conducted three long-term excursions and carried

out extensive field work in various parts of the Iranian

Plateau in 1995, 1996, and 1998, collected hundreds

of specimens of Trapelus agilis and noted the pattern

of adaptation of different populations to the local con-

ditions as well as presence of eco-geographical barri-

ers which have been involved in differentiation and

subsequent evolution of all subspecies of this com-

plex. Also I studied preserved materials including the

syntypes of Agama agilis Olivier. 1804 and paralecto-

types of Agama isolepis Boulenger, 1 885, borrowed

from various museum collections around the world

(see under "Appendix I, Abbreviations, and Acknowl-

edgments").

In my previous studies, based on examination of

about 1000 specimens of T. agilis all over the range, I

employed uni-and multivariate statistical techniques

and explored the patterns of geographic variation in

morphological characters within this complex (Raste-

gar-Pouyani, in press, unpublished manuscript).

Indeed, the present paper is the continuation (and

part of the results) of my previous studies concerning

taxonomy and geographic variation in T. agilis com-

plex according to which both the lowland southwest-

ern Iranian as well as southeastern Pakistani

populations do warrant taxonomic recognition.

Subspecies accounts

Trapelus agilis khuzistanensis ssp. nov.1

(Figs. 2-6)

Khuzistan Ground Agama

Holotype and type locality: adult female, GNHM

Re. ex. 5224, collected by the author on 27 July 1996

from Iran, Khuzistan Province, 5 km northwest of

Haft-Gel on the road to Shushtar.

Paratypes: 14 specimens (ten males and four

females) have been designated as paratypes as fol-

lows: GNHM. Re. ex. 5225, same information as the

holotype: GNHM. Re. ex. 5226, collected by the

author on July 28, 1996 from Iran, Khuzistan Prov-

ince, 38 km south of Masjid-e-Suleiman, Golgir vil-

lage; CAS 86342, 86346, 86390, Iran, Khuzistan

Province, Tul-i-Bazum [31° 55' N, 49° 25' E], about

500 m elevation, collected by S. C. Anderson on 17

April and 22 May 1958; CAS 86403-6, Iran,

Khuzistan Province, along road to lake east of Haft-

Gel, about 300 m elevation, collected by S. C. Ander-

son on 23 May 1958; CAS 86418-19, Iran, Khuzistan

Province, along road between Haft-Gel and Masjid-

Suleiman, by S. C. Anderson on 23 May 1958: CAS

86556. Iran, Khuzistan Province, Haft-Gel (on golf

course) [31° 28' N, 49° 30' E], about 300 m elevation,

by S. C. Anderson on 5 October 1958; CAS 86464,

Iran, Khuzistan Province, along road south of Shush-

tar, by S. C. Anderson on 18 July 1958; FMNH

170936, Iran. Khuzistan Province, 85 km southeast of

Vol. 8. p. 92

Asiatic Herpetological Research

1999

Tablel . legend. Main morphological differences between T. a. khuzistanensis, T. a. pakistanensis, and the Olivier's

syntypes (T.a. agilis).

Ahwaz, Meshrageh, collected by D. Womochel and A

De Blase on 20 October 1968.

Diagnosis: Trapelus agilis khuzistanensis differs from

all other subspecies of T. agilis in its higher number of

scales around body (80-97); subequal and almost het-

erogeneous dorsal scalation with distinctly small dor-

sals and ventrals; a shorter head and neck:

significantly lower mean number of subdigital lamel-

lae under the fourth toe; reverse imbrication of the

posterior head and anterior neck scales; keeled or rug-

ose upper head scales; usually one, and sometimes

two rows of callose preanal scales (absent or slightly

developed in females); strongly compressed tail in

males of most populations; and an exclusive dorsal

coloration (yellowish-grey-cream with weak or with-

out reddish-brown cross bars).

Description of holotype: an adult female, preserved

in 70% ethyl alcohol in good condition; head short but

longer than broad with very convex forehead, its

length 0.26 of body length and 0.19 of tail length;

canthus rostralis more or less continued as a supracili-

ary ridge; nostril on, or, barely, above the canthus,

pierced in a flat shield and posteriorly directed; 3

internasals in a transverse row; upper head scales het-

erogeneous, keeled or rugose, imbricate and subim-

bricate; supraciliary ridge strongly developed,

composed of 9 scales on each side; 17-18 upper- and

Figure 3. T. a. khuzistanensis, holotype (GNHM Re. ex.

5424); neck and head regions with reversally-imbri-

cated scales.

17-17 lower labials; tympanum horizontally elliptical,

smaller than orbit, partly covered above by 4-5 small

spinose scales; scales of posterior part of head and

anterior part of neck distinctive in that their imbrica-

tion is reversed (i.e., towards the head) and the poste-

rior border of reversally-imbricated scales is defined

by a single large and pointed scale; gular pouch mod-

erately developed; gular region covered by small,

imbricate, slightly keeled or smooth scales; gular fold

and a fold in front of shoulder strongly developed;

body and head moderately depressed; limbs rather

slender; dorsal scales subequal to unequal, small,

imbricate, slightly keeled and mucronate; median dor-

1999

Asiatic Herpetological Research

Vol. 8, p. 93

Figure 4. T. a. khuzistanensis, one of the male

paratypes (FMNH 170936). Note the presence of a

strongly compressed tail and relatively heterogeneous

dorsal scalation.

Figure 6. Habitat and type locality of T. a. khuzistanen-

sis, 5 km northwest of Haft- Gel on the road to Shush-

tar, Khuzistan province, southwestern Iran. In the

foreground the author is attempting to capture the holo-

type from inside of its underground hole.

sals relatively larger, grading into distinctly smaller

scales of dorsolateral region which are only slightly

keeled and mucronate; 94-95 scales round middle of

body; scales of upper surface of limbs larger than

median dorsals, distinctly keeled, slightly mucronate:

lower surface of digits covered by bi-or tri carinate

lamellae, 18-19 under the fourth toe; ventral scales

almost as large as median dorsals, imbricate, very

slightly keeled or smooth, 84-85 scales in a single row

from gular fold to the anterior edge of anus; callose

preanal scales in one row, slightly developed, consist-

ing 10 scales; caudal scales larger than median dor-

sals, strongly keeled, distinctly mucronate, 34-36

around base of tail just behind vent; tail weakly com-

pressed at base, distinctly so towards the tip, its length

1 .39 of body length.

Coloration and color pattern: upper surface of head

and limbs uniformly yellowish-grey, ground color of

dorsum yellowish-grey-cream with 5 large, broad,

light-brown cross bars from nape to sacrum, inter-

rupted by a series of light, large vertebral ocelli and

Figure 5. T. a. khuzistanensis, posterior ventral region

of a male paratype (GNHM. Re. ex. 5426) with one row

of callose preanal scales.

two paravertebral rows of smaller ones, proximal

upper caudal region with distinct dark-grey bars; ven-

tral surfaces uniformly whitish.

Measurements (mm): Total length = 206; Snout-vent

length (SVL) = 86: Tail length (TL) = 120; Head

length (HL) = 23; Head width (HW) = 19; Head depth

(HD) = 12.8; Length of forelimb = 45; Length of

hindlimb = 62.

Variation of the type series: all paratypes closely

approximate the holotype both in morphology and

meristics.

The range of the number of scales around body for the

whole series (n = 14) is 82-97 and the mean 88.5; in

all paratypes the number of subdigital lamellae under

the fourth toe varies between 16-19; dorsal scales are

subequal or heterogeneous (especially in males); there

are some differences, however, between male and

female paratypes.

- Male paratypes: all male paratypes (n = 10) are

either uniformly yellowish-grey-cream dorsally or

with a weakly developed pattern of dark cross bars; as

well, the ventral pattern is either uniformly whitish or

with distinct pattern of bluish-brown on the gular

region, chest and flanks; tail strongly compressed in

almost all males; preanal callose scales in one or two

rows, in the latter case the second row weakly devel-

oped, their number varies from 10-21; dorsal scales

more keeled and mucronate and distinctly heteroge-

neous, approaching T. persicus in this respect; ven-

trals weakly keeled, gular sac distinctly developed;

reverse imbrication of the posterior head and anterior

neck scales relatively more pronounced and the large

scale on posterior end of these reversally-imbricated

scales more distinctive and mucronate than in

females.

- Female paratypes: all female paratypes (n = 4)

resemble the holotype in almost all pertinent details;

the preanal pores are only in one row. weakly devel-

Vol. 8, p. 94

Asiatic Herpetological Research

1999

Figure 7. Geographic distribution of T. a. khuzistanen-

sis (A) and T. a. pakistanensis (B). Squares represent

the type localities.

oped, each occupying the tip of a scale, their number

varies from 8 to 11; all the dorsal scales weakly

keeled and mucronate; tail round or weakly com-

pressed; slight differences in dorsal pattern occur (in

some specimens the dorsal cross bars are more

intense).

Habitat: in lowland southwestern Iran and in the

western foothills of the Zagros Mountains, this sub-

species mainly occurs on sand dunes, alluvial soils,

open plains, low hills, and on dry stream channels

(Anderson, 1966a, in press: personal observations).

The type locality is specified by numerous low sand

dunes as well as gypseous hills imminented with an

open plain. The vegetation is sparse, mainly Artemi-

sia, Alhagi, Zygophylluni, and Euphorbia association.

The climate conditions being harsh, with hot and long

summers (about 40°- 50°C) and mild, short winters. It

seems that this lizard is active throughout the year but

Anderson first observed it in the western foothills of

the Zagros in early March, becoming numerous by

mid-April; both newly hatched and half-grown juve-

niles were observed in late October and early Novem-

ber (Anderson, 1963: 446).

The holotype and one of the paratypes were collected

about 5 km northwest of Haft-Gel on the road to

Shushtar. They were active when air temperature was

45°C and the substrate was 49.5°C. When alarmed,

unlike most of the central Plateau populations which

usually retreat into the base of dense bushes, they

retreated into the underground holes; this may be due

to vegetation scarcity. Both specimens were captured

inside their underground holes (Fig. 6). The third

specimen collected near the mouth of an old well in

the vicinity of the village of Golgir (38 km south of

Masjid-e-Suleiman) while trying to retreat into the

well.

Distribution: the main distributional range of this

subspecies is the Khuzistan Plain which is an exten-

sion of the Mesopotamian lowlands (Fig. 7). Also, it

penetrates into the western foothills of the Zagros

Mountains up to 900 m elevation. It is the western-

most representative of the wide-ranging T. agilis spe-

cies complex. The Zagros Mountains serve as an

strong barrier to its further eastward distribution, so it

has almost no contact with the central Iranian Plateau

nominal subspecies (T. a. agilis), except in the south-

eastern regions of Bushehr province, southern Iran

where the two taxa occur as parapatric (Rastegar-

Pouyani, Manuscript, a). Its occurrence in the lowland

southeastern Iraq is almost unlikely and, so far, there

is no proper record inside the Iraqi territory [except

the Olivier's original record (1804) which is strongly

doubtful]. If it occurs in southeastern lowland regions

of Iraq, then the Tigris might have served as an effec-

tive barrier to its further westward distribution.

In some areas of lowland southwestern Iran (e.g., 85

km southeast of Ahvaz) it occurs as sympatric with

Trapelus persicus (Blanford, 1881) but there is no

proper record of intergradation, if any, between the

two taxa.

Etymology: Trapelus agilis khuzistanensis is so

named as it is mainly restricted in distribution to the

lowlands of southwestern Iran, Khuzistan province.

Trapelus agilis pakistanensis ssp. nov.2

(Figs. 8-9)

Pakistan Ground Agama

Holotype and type locality: adult male, SMF 63258,

collected by M. G. Konieczny on 31 March 1957 from

Gaj-River, Kirthar Range, southeastern Pakistan.

Paratypes (7 specimens): SMF 63259, 63279, same

information as the holotype; SMF 63256, collected by

R. Mertens on 1st December 1952 from Sonda, Distr.

Thatta, southeastern Pakistan; SMF 63243-4, 63286-

7, collected by M. G. Konieczny on 26 April 1961

from Old Airport of Karachi, southeastern Pakistan.

Diagnosis: Trapelus agilis pakistanensis differs from

the other subspecies of T. agilis complex by having a

combination of distinctive characters; body and head

sometimes compressed (not depressed) in males;

males almost always with one row of callose preanals

(rarely a second undeveloped row may be present);

females without callose preanals: dorsal scales rela-

tively flat, subequal to homogeneous, distinctly keeled

throughout and mucronate, grading into small dorso-

laterals rather abruptly (especially in males), 67-83

around body; ventral scales also often distinctly

keeled in males; body and limbs often strongly slen-

der and head distinctly pointed (in adult males); tail

1999

Asiatic Herpetological Research

Vol. 8, p. 95

Figure 8. T. a. pakistanensis, holotype (SMF 63258); A-

dorsal region, B- ventral region. Note the presence of a

strongly compressed tail, and pointed and slender

body and head.

often strongly compressed in adult males, its length

more than 1.55 of body length; the mean number of

supra- and infralabials significantly lower than those

of the other subspecies; a rudimentary nuchal crest

often present.

Description of holotype: an adult male, preserved in

70% ethyl alcohol in good condition; head pointed

with a slightly convex forehead, its length 1.36 of its

width and 0.27 of body length and 0.15 of tail length;

canthus rostralis continued as a supraciliary ridge

which is rather strongly developed, composed of 7

scales on each side; nostril as a horizontal slit, slightly

above canthus rostralis, pierced in a triangle-shaped

scale, posteriorly directed; 4 internasals in a single

transverse row; upper head scales subequal. smooth,

or slightly rugose, imbricate and subimbricate; 14-14

upper- and 13-13 lower labials; tympanum horizon-

tally elliptical, smaller than orbit, partly covered

above by 6-8 spinose scales; no reversal imbrication

of scales on the posterior part of head and anterior

part of neck; a rudimentary nuchal crest composed of

6-7 spinose scales; gular sac moderately developed

and rather pointed posteriorly; gular region covered

by large and small, imbricate, and slightly keeled

scales intermixed: gular fold and a fold in front of

shoulder strongly developed; body slender and dis-

tinctly compressed laterally, a prominent vertebral

ridge throughout the dorsum; limbs distinctly slender;

dorsal scales subequal to homogeneous, rather large,

Figure 9. T. a. pakistanensis, holotype (SMF 63258);

posterior ventral region. Note the presence of only one

row of callose preanal scales and distinctly slender

hindlimbs.

imbricate, almost entire individual scale distinctly

keeled (unlike the eastern populations of T. a. agilis in

which only the proximal part of scales are keeled) and

mucronate; median dorsals larger, grading into dis-

tinctly smaller scales of dorso-lateral region which are

only slightly keeled and mucronate; 72-73 scales

round the widest part of body: ventral scales rather

distinctly keeled, imbricate, large, but slightly smaller

than median dorsals, 70-71 in a single longitudinal

row from gular fold to the anterior edge of anus;

scales of upper surface of limbs almost as large as

median dorsals, strongly keeled and mucronate; lower

surface of digits covered by bi- and tri-carinate keeled

lamellae, 24-25 under the fourth toe; preanal callose

scales only in one row, not exceptionally developed,

encompassing 8 scales; all caudal scales distinctly

keeled and larger than median dorsals, 33-35 around

base of tail, just behind the vent; tail long and strongly

compressed throughout, its length 1.81 times of body

length.

Coloration and color pattern: upper surface of head

yellowish-grey; dorsum uniformly sandy-grey with

numerous light scales scattered throughout; upper sur-

faces of limbs olive-brown; upper caudal region as

dorsum in coloration with barely distinct dark-brown

rings; gular region, chest, and flanks heavily suffused

by lavender-blue; other ventral surfaces yellowish-

white; no black patch on the shoulder fold.

Measurements (mm): Snout- vent length (SVL) =

101.6, Tail length (TL) = 184, Head length (HL) =

28.2, Head width (HW) = 20.7, Head depth (HD) =

13.5, Length of forelimb = 50, Length of hindlimb =

73.

Variation of the type series: all paratypes are similar

to the holotype both in morphology and meristics. In

all specimens nostril is almost above the canthus ros-

tralis and a rudimentary nuchal crest, more or less,

Vol. 8, p. 96

Asiatic Herpetological Research

1999

developed. The range of scale counts around body for

the whole series (n = 7) is 69-81 (mean 74.42). The

range of ventral scales from gular fold to the anterior

edge of anus (in a single longitudinal row) varies from

67-77 (mean 74.57). In all paratypes the number of

subdigital lamellae under the fourth toe varies from

22-26 (mean 23.85). The number of supra-and infra

labials varies from 13-16 (mean 14.55) and 12-16

(mean 14.25) respectively. Dorsal scales being homo-

geneous or subequal and, more or less, set off from

the small dorsolaterals.

However, there are some differences in morphology

between males and females:

- Male paratypes: all male paratypes (n =4) resemble

the holotype in almost all relevant details; the mean

SVL = 90.5 mm, TL = 155 mm; mean TL 1.71 times

as mean SVL; the preanal callose scales almost only

in one row (in the case of two, the second row rarely

developed), encompassing 10-11 scales (mean 10.4);

median dorsal scales enlarged, homogeneous, dis-

tinctly keeled throughout and mucronate, forming dis-

tinct ridges along dorsum, grading, rather abruptly,

into small dorsolaterals which are weakly keeled and

mucronate; all ventral scales, as in holotype, more or

less keeled, rather large, but smaller than median dor-

sals; tail strongly keeled in almost all specimens,

although body not as strongly compressed and

pointed as in the holotype; color pattern almost as in

holotype.

- Female paratypes: in females (n = 3), the body and

tail are normal (neither distinctly compressed nor

slender), the dorsal scales are moderately keeled and

mucronate and median dorsals are not clearly set off

from the small dorsolaterals; as well, ventrals are

slightly keeled and distinctly smaller than the median

dorsals; callose preanal scales absent; gular sac not as

well developed as in the holotype; in color pattern

some of them are rather different from the holotype in

the presence of, more or less pronounced, dark cross

bars and a series of vertebral light ocelli and in the

absence of ornamentation in the lower parts of body;

ventral surfaces being uniformly whitish.

Habitat: the habitat of this subspecies is character-

ised by flat alluvial plains as well as some high slopes.

The vegetation consists of some grass, herbs, and

stunted shrubs. Some populations occur on the low-

lands around Karachi, and the eastern part of the

range is a typical desert known as Thar Desert in east-

em Sind extending into adjacent northwestern India

(the great Indian Desert). This desert mainly consists

of sandy hills which vary from small dunes to hills

with 100-150 m elevation. In summer, dust storms are

the main feature of the area (Khan, 1980).

Distribution: Trapelus agilis pakistanensis, as the

southeasternmost subspecies of T. agilis complex, is

restricted in distribution to the lowland and semi-

desert regions of Sind province, southern Punjab, and

some regions of eastern Baluchistan (southern and

southeastern Pakistan), from around Hab River in the

west through Karachi and Thatta to the vicinity of

Hyderabad and Mirpur Khas eastward into the Indian

Desert (Fig. 7). Biswas and Sanyal (1977) recorded

this lizard inside the Indian territory (from Jaisalmir,

Kolayat, Pugal, Phalodi and some other localities in

Rajastan Desert, northwestern India); to the north, it is

distributed along the Kirthar Range up to the areas

south of Khuzdar (south-central Pakistan). Apparently

the Hab River serves as a barrier for further distribu-

tion of this taxon towards the west; however it is para-

patric with its T. a. agilis in the eastern regions of

Baluchistan province. In the east, it goes up to the

Nagaur District, Rajasthan, northwestern India.

Etymology: Trapelus agilis pakistanensis is so named

as it is restricted in distribution to the lowland and

semi-desert regions of southeastern Pakistan and adja-

cent northwestern India.

Taxonomic and biogeographic account

Detailed discussion concerning systematics and pat-

terns of geographic variation in Trapelus agilis com-

plex is presented elsewhere (Rastegar-Pouyani,

Manuscript a-b) and here is not dealt with in details.

As a brief account, however, it can be mentioned that I

classified all populations of Trapelus agilis complex

throughout the range into four distinctive taxonomic

entities (and as the most parsimonious definition=

subspecies): T. a. agilis (Olivier, 1804), T. a. san-

guinolentus (Pallas, 1814), T a. khuzistanensis

ssp.nov. 1 , and T. a. pakistanensis ssp.nov.2.

An ANOVA-based pairwise comparison showed

that in most metric and meristic characters these four

taxonomic entities are significantly different (P<0.05)

(Rastegar-Pouyani, Manuscript, a). Also employing

multivariate statistical techniques (principal compo-

nent analysis, canonical variate analysis, and cluster

analysis), to a great extent, showed the objectivity of

these four distinct groups within T agilis complex and

re -confirmed my previous taxonomic decisions (Ras-

tegar-Pouyani, Manuscript, b). Of the four subspecies

of T. agilis, the nominal form (T. a. agilis) occurs in a

wide range of habitats, shows higher degree of mor-

phological variability, occupies the central and south-

ern parts of the species range (these regions might

have served as a refugia during intervals of unfavor-

able and cold climatic conditions in the Tertiary and

Quaternary), and consists of two western and eastern

1999

Asiatic Herpetological Research

Vol. 8, p. 97

groups of populations (clines) (Rastcgar-Pouyani, in

press, unpublished manuseript). With regard to these

factors, it could be logical if we consider this form as

the central core of the complex and as the parental

population from which the other subspecies have been

derived. So, preliminarily, I propose the following

scenario for origination and subsequent evolution of

the three marginal subspecies which occur in the

periphery of the main range of the complex being

parapatric with the central continuum (=T. a. agilis):

It seems that T. a. sanguinolentus, in spite of being

distributed over a very wide area, is the most recently-

evolved group, originated from the parental popula-

tions in the southern parts of the range (apparently) in

the very Late Pliocene and Pleistocene (2-1.2 MYBP

=millions of years before present), invading towards

the northern and northeastern regions during intervals

of favorable climatic periods. The very low degree of

variability observed in this subspecies is indicative of

its recent history. Trapelus a. pakistanensis separated

from the central continuum in the southeastern parts

of the range (probably by dispersal or, less likely, due

to a vicariant event) distributed towards the east and

reached as far east as northwestern Indian desert. This

invasion might have taken place in the Pliocene (5-1.7

MYBP). In the southwestern part of the range, a dras-

tic vicariant event (the huge orogeny of the Zagros)

separated the southwesternmost populations from rest

of the complex and from the parental populations.

These isolated populations served as founders and,

with further divergence, gave rise to T. a. khusistanen-

sis. Apparently, this vicariant event has taken place in

the Late Miocene or early Pliocene (7-4.5 MYBP).

Therefore, we can say that both dispersal and vicari-

ance have been involved in radiation and subsequent

evolution of various subspecies of Trapelus agilis

complex though the role of dispersal in evolution of T.

a. sanguinolentus and T. a. pakistanensis, and vicari-

ance in evolution of T. a. khuzistanensis are more

prominent.

Trapelus agilis (Olivier, 1804) is the easternmost

representative of an essentially homogeneous and

similar group of about five species complexes which

also include T persicus (Blanford, 1881 ) in the Meso-

potamian Plain and lowland southwestern Iran, T. fla-

vimaculatus Riippell, 1835 in Saudi Arabia, T

savignii (Dumeril and Bibron, 1837) in Israel and

eastern Egypt, and T. tumevillei (Lataste, 1880) in

north Africa (north of Sahara). Although the mono-

phyly of Trapelus has been shown by Moody (1980)

with a morphological approach and by Joger (1991 )

using molecules (neither Moody nor Joger studied all

the species of Trapelus) but, so far, no comprehensive

revisionary study has been done on all species of this

genus and this is mainly because of political instabil-

ity of the region and difficulties in collecting proper

material throughout the range. Furthermore, even in a

few studies done on a limited number of Trapelus spe-

cies, the results obtained by morphological and the

other approaches (e.g., immunological) were contra-

dictory (e.g., Anderson, in press; Joger and Arano,

1987; Rastegar-Pouyani, in press, unpublished manu-

script).

Trapelus is mainly Saharo-Sindian in distribution,

often associated to the lowlands, desert, and semi-

desert regions with high annual temperature.

Key to the subspecies of Trapelus agilis com-

plex

la. Tail almost always round, two (or more) rows of

callose preanal scales 2

lb. Tail often compressed, often only one row of cal-

lose preanal scales, in the case of two, the second

undeveloped (preanals absent or weakly developed in

females) 3

2a. Body size variable; 65-91 scales around body;

dorsal scales subequal, weakly to moderately keeled,

often strongly mucronate; ventral scales smooth or

weakly keeled; usually 2, sometimes 3 (rarely 4-5)

rows of callose preanals; background coloration vari-

able; central Iranian Plateau, central and southern

Afghanistan, southwestern Pakistan. . Trapelus agilis

agilis (Olivier, 1804).

2b. Body stout; 52-73 scales around body; all dorsal,

ventral, and gular scales larger in size, homogeneous,

strongly keeled and mucronate; almost always 2

(rarely 3) rows of callose preanals; background color-

ation of males often dark sandy-grey; northeastern

Iran, northern Afghanistan, Central Asian Republics,

western coast of the Caspian Sea (Daghestan), west-

ern China. . . . Trapelus agilis sanguinolentus (Pallas,

1814).

3a. Body and limbs smaller than those of the other

subspecies and sometimes relatively slender, not com-

pressed; head and neck distinctly short; all body

scales smaller than those of the other subspecies; dor-

sal scales subequal to unequal (heterogeneous),

weakly to moderately keeled, weakly mucronate; 80-

97 scales around body; ventral scales slightly keeled;

scales of posterior part of head and anterior part of

neck reversally imbricated; upper head scales keeled

or rugose; often 14-19 upper- and lower labials; back-

ground coloration often yellowish grey-cream; low-

land southwestern Iran (0-900 m elevation)

Trapelus agilis khuzistanensis, ssp. nov. 1

Vol. 8, p. 98

Asiatic Herpetological Research

1999

3b. Body and limbs often distinctly slender, some-

times compressed in males; dorsal scales subequal to

homogeneous, distinctly keeled and mucronate, usu-

ally clearly set off from small dorsolaterals; 67-83

scales around body; ventrals distinctly keeled in adult

males; no reversal imbrication of head and neck

scales; upper head scales often smooth; 12-16 upper-

and lower labials; background coloration often sandy-

grey: southeastern Pakistan and adjoining northwest-

em India . . . Trapelus agilis pakistanensis, ssp. nov.2

Abbreviations

BMNH = British Museum (Natural History; (London,

UK), CAS = California Academy of Sciences (San

Francisco, USA), FMNH = Field Museum of Natural

History (Chicago, USA), GNHM = Goteborg Natural

History Museum (Goteborg. Sweden), MNHN =

Museum National d'Histoire Naturelle (Paris,

France), MZLS = Museo Zoologico de "La Specola"

(Firenze, Italy), NMW = Naturhistorisches Museum

Wien (Vienna, Austria). SMF = Museum und Fors-

chungsinstitut Senckenberg (Frankfurt, Germany),

SMNH = Swedish Museum of Natural History

(Stockholm, Sweden), ZFMK = Zoologisches Fors-

chungsinstitut und Museum Alexander Koenig (Bonn,

Germany); ZISP = Zoological Institute St. Petersburg

(St. Petersburg, Russia), ZMUC = Zoological

Museum University of Copenhagen (Copenhagen,

Denmark).

Acknowledgments

I would like to thank my supervisor. Dr. Goran Nil-

son, for all his help and cooperation as well as for crit-

ically reviewing this paper. I wish to thank the Razi

University authorities (Kermanshah-Iran) as well as

Eskandar Rastegar-Pouyani, Alireza Hashemi, Seyful-

lah Azadi, Masoud Abrishamian and Ali Rassuli for

their unsparing help during field work on the Iranian

Plateau. I am also grateful to Professor S. C. Ander-

son, Biological Science Department, University of the

Pacific, Stockton, California, for all his recommenda-

tions, encouragements, and for sending informative

literature, especially his unpublished Manuscript con-

cerning the Iranian agamids.

My special thanks also go to: Dr. Alan E. Leviton,

Department of Herpetology, California Academy of

Sciences; Dr. Colin McCarthy, Department of Zool-

ogy, British Museum (Natural History): Dr. Harold K.

Voris, Department of Herpetology, Field Museum of

Natural History; Dr. Jens B. Rasmussen, Zoological

Museum, University of Copenhagen: Dr. Franz Tiede-

mann, Naturhistorisches Museum Wien; Professor

Wolfgang Bohme, Zoologisches Forschungsinstitut

und Museum Alexander Koenig; Dr. Gunther Kohler,

Forschungsinstitut Senckenberg; Dr. Marta Poggesi,

Museu Zoologico de "La Specola"; Dr. Ivan Ineich,

Museum National d'Histoire Naturelle; and Dr. Olavi

Gronwall and S. O. Kullander, Swedish Museum of

Natural History, for loan of Trapelus specimens. Dr.

N. B. Ananjeva, Zoological Institute, Russian Acad-

emy of Sciences, St. Petersburg, who made it possible

for me to visit the herpetological collections of Zoo-

logical Institute and examine specimens of T. agilis.

This work was partly supported by grants from the

Royal Swedish Academy of Sciences ( Hiertza-Ret-

zius Fond), Anna Ahrenberg, and Wilhelm Martina

Foundations.

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Appendix 1. Material examined

Trapelus agilis agilis (n =541 )

MNHN 5708 (2) = 1994. 1 178 (2) (Olivier's syntypes):

Iraq, vicinity of Baghdad. GNHM. Re. ex. 5213-17: Iran,

Tehran prov. 50 km NE Qum on road to Tehran. GNHM.

Re. ex. 5218-28: Iran, Tehran prov. 75 km NE Qum on road

to Tehran. GNHM. Re. ex. 5229-34: Iran, Tehran prov. 5 km

NE Saveh on road to Tehran. GNHM. Re. ex. 5235-62: Iran,

Tehran prov. (50-60 km W Tehran) between Eshtehard -

Saveh. GNHM. Re. ex. 5263: Iran, Tehran prov. 30 km SE

Tehran on road to Garmsar. GNHM. Re. ex. 5264-66: Iran,

Central prov. 25km Khomain on road to Mahalat. GNHM.

Re. ex. 5267-81: Iran, Central prov. between Komain-Deli-

jan and Mahalat-Delijan roads. GNHM. Re. ex. 5282-86:

Iran, Esfahan prov.near Naragh, 50km W kashan on road to

Naragh. GNHM. Re. ex. 5287-89: Iran, Esfahan prov. 20

km ES Kashan on road to Natanz on the margin of Dasht-e

Kavir.GNHM. Re. ex. 5290-92: Iran, Esfahan prov. 80km N

Esfahan on road to Natanz.GNHM. Re. ex. 5293-97: Iran,

Esfahan prov. 70km E Esfahan on road to Naein, near Kuh-

payeh city. GNHM. Re. ex. 5298-99: Iran, Esfahan prov.

15km N Shahreza on road to Esfahan. GNHM. Re. ex.

5300-07: Iran, Fars prov. 50 km N Abadeh on road to Shahr-

eza. GNHM. Re. ex. 5308-16: Iran, Fars prov. 50- 75km S

Abadeh on road to Shiraz. GNHM. Re. ex. 5317-31: Iran,

Markazi province, 45 km E Arak on the road to Qum.

GNHM. Re. ex. 5332-34: Iran.Tehran prov., 65 km NE

Saveh on road to Robat-Karim. GNHM. Re. ex. 5335: Iran,

Markazi prov.. 50 km N of Delijan on road to Salafchegan.

GNHM. Re. ex. 5336-44: Iran, Esfahan prov., 45 km E of

Golpaygan. GNHM. Re. ex. 5346-50: Iran, Esfahan prov., 7

km E of Tiran on road to Najaf-Abad. GNHM. Re. ex.

5351-57: Iran, Esfahan prov., 25 km SE of Esfahan on road

to Dastjerd. GNHM. Re. ex. 5358-68: Iran, Esfahan prov.,

about 1 10 km SE of Esfahan city, on road from Malvajerd to

Ramsheh. GNHM. Re. ex. 5369-70: Iran, Esfahan prov., 20

km W of Ramsheh on road to Shahreza. GNHM. Re. ex.

5371-78: Iran, Fars prov., 50 km N of Abadeh (15 km S of

Izad-Khast) on road to Esfahan. GNHM. Re. ex. 5379-91:

Iran. Fars prov., 65 km SE of Abadeh on road to Shiraz.

GNHM. Re. ex. 5399: Iran. Kerman prov., 28 km NE of Sir-

jan on road to Kerman. GNHM. RE. ex. 5400-1: Iran, Ker-

man prov., 70 km NE of Sirjan on road to Kerman. Khaneh-

Sorkh Pass, about 2800 m elevation. GNHM. Re. ex. 5402-

13: Iran, Semnan Prov., 5o km E of Semnan, North of

Dasht-e- Kavir, Northeastern Iran. GNHM. Re. ex. 5414-23:

Iran, Khorasan Prov., 1 10 km East of Shahrud, Northeastern

Iran. CAS 142230: Iran.Tehran prov. Lar-Damavand.

CAS142189, CAS 142190, CAS 142182, CAS 142192,

CAS 142191, CAS 142187, CAS 142188, CAS 142183,

CAS 142184, CAS 142186, CAS 142185: Iran, Zanjan

prov. Ghazwin. CAS 142231: Iran.Tehran prov. Karadj.

CAS 142093, CAS 142094, CAS 142098, CAS 142097,

CAS 142100. CAS 142092, CAS 142096, CAS 142095,

CAS 142101, CAS 142099: Iran.Tehran prov. Saveh. CAS

141293: Iran, Tehran prov.24km W of Saveh On road to

Hamadan. [35 07 N, 50 08 E]. CAS 142194, CAS 142197,

CAS 142195, CAS 142199, CAS 142198, CAS 142193:

Iran. Esfahan prov. Mahalat. CAS 141019: Iran, Esfahan

prov.6km by road NW Ardestan. [32 26 N, 52 20 E]. CAS

141 109: Iran, Esfahan prov. 8km S of Kashan and 6km W of

road between Yazd -Kashan. [33 54 N, 51 30 E]. FMNH

Vol. 8,

100

Asiatic Herpetological Research

1999

170987. FMNH 170988: Iran, Gilan prov. 4,2 mi N of Tuke-

stan (Zanjan prov. Takestan?). NMW 33 166-1, Iran: Fars

prov. 9 km N of Abadeh. NMW 33167, NMW 33085-2:

Iran, Hormozgan prov. 14km E Bandar-Abbas. NMW 7276-

I, NMW 7276-2: Iran: Kerman prov.? Sabzewaran. NMW

7276-3: Iran: Kerman prov.? Rigmati. 150 km SE of Sabze-

waran. NMW 7276-4: Iran, Esfahan prov. 135 km N of

Esfahan. NMW 33159-3, NMW 33159-4, NMW 33159-5,

NMW 33165-1: Iran, Esfahan prov. Murcheh-Khurt, N of

Esfahan. NMW 33165-2, NMW 33165-3, NMW 33085-1:

Iran: Esfahan prov. 4 km SE Robai-Tork ( 165 km NW of

Esfahan). NMW 33085-3: Iran. Zanjan prov. 26 km SE

Ghazwin. NMW 33083-1, NMW 33083-2, NMW 33083-3:

Iran, Zanjan prov. 41 km SE Ghazwin. Elev: 1380 m. NMW

33164: Iran/Tehran prov. 60 km S of Tehran. NMW 33084-

3: Iran, East Azarbaijan prov. 42 km SE Mianeh. Elev: 1200

m. NMW 33166-1: Iran. Kerman prov. 15 km SE Kerman.

SMNH 3139-1, SMNH 3139-2, SMNH 3139-3, SMNH

3139-4, SMNH 3139-5, BMNH 85. 5. 27. 14, BMNH 85. 5.

27. 15. BMNH 85. 5. 27. 16. BMNH 85. 5. 27. 17, BMNH

85. 5. 27. 18, BMNH 85. 5. 27. 19: Iran: Tehran (exact

locality?). GNHM. Re.ex. 4437, GNHM. Re.ex. 3324,

GNHM. Re.ex. 4395-1: Iran, Gilan prov. 65 km SSW of

Rasht. GNHM Re.ex. 4395-2: Iran, Tehran prov. 150 km S

of Tehran. Siah-Kuh. Shah- Abbas post. GNHM Re.ex.

4396-1, GNHM. Re.ex. 4396-2: Iran, Mazandaran prov. 150

km E of Gorgan, Golestan Park. La Specola 30584, La Spe-

cola 30585: Iran/Tehran prov. 50 km S Qum? BMNH 1920.

3. 20. 1: Iran, Hamadan prov. Hamadan. Jinjan? BMNH

1936. 10. 12. 1: Iran. Kerman prov. N. Of Kerman, Sekonj.

7000 ft. BMNH 1934. 12. 16. 3. BMNH 1936. 12. 16. 4:

Iran. Sheakuh, seat (Salt?) desert.

BMNH 1912. 3. 26. 13, BMNH 1912. 3. 26. 14, BMNH

1912. 3. 26. 15, BMNH 1906. 8. 10. 25, BMNH 1900. 5. 9.

9, BMNH 1900. 5. 9. 10, BMNH 1900. 5. 9. 11, BMNH

1900.5.9. 12, BMNH 74. 11.23. 104, BMNH 74. 11.23.

105, BMNH 74. 1 1. 23. 106. BMNH 74. 1 1. 23. 107,

BMNH 74. 1 1. 23. 108, BMNH 74. 1 1. 23. 109, BMNH 74.

11.23. 110.BMNH74. 11.23. 111.BMNH74. 11.23. 112,

BMNH 74. 1 1. 23. 1 13: Iran, Sistan-Baluchestan prov.

BMNH 1951. 1.6. 50, BMNH 1951. 1. 6. 51-2. BMNH 94.

II. 13. 4, BMNH 94. 11.13. 5: Iran, Hormozgan prov.

BMNH 87. 12. 20. 1: Iran, Hormozgan prov. Kishim

(=Gheshm?) Island, Persian Gulf. BMNH 79. 8. 15. 10-15:

Iran, Fars prov. Dehbid, north of Shiraz. BMNH 1903. 3.

14. 1: Iran, Bushehrprov. Bushehr. BMNH 1933.4. 1. 20-

22: Pakistan, Waziristan, N. W. F. P. BMNH 86. 9. 21. 17.

BMNH 86. 9. 21. 18, BMNH 86. 9. 21. 23, BMNH 86. 9.

21. 24.BMNH 86. 9. 21. 25: Afghanistan: Helmand. ZMUC

R36133, ZMUC R36149-54, ZMUC R36160, ZMUC

R36204-5: Afghanistan: Seistan prov. Faisabad (south of

Afghanistan). ZMUC R36155-9, ZMUC R36145-8,

Afghanistan, Seistan prov. Baqrabad. ZMUC R36161:

Afghanistan, Seistan prov. Faisabad-Farah. ZMUC R36206:

Afghanistan, Kandahar prov. Przadah, W of Kandahar.

ZMUC R36208-9: Afghanistan, Kabul prov. near Kabul?

ZISP 7361: Afghanistan: Harat. NMW 33170-12: IRAN.

East Azarbaijan, 42 km SE Mianeh. NMW 33173-1-2:

IRAN, Zanjan prov. 26 km SE Qazwin. NMW 33170-1:

IRAN.Tehran prov. 95 km S Tehran. NMW 33148-1-10:

IRAN: Tehran prov. Zaveyeh, 80 km SW Tehran. NMW

7276-5-6: IRAN, Kerman prov. Sabzewaran. NMW 33175-

5, NMW 33170-5, NMW 33170-6. NMW 33170-7: Iran.

Esfahan prov. NMW 33172-3-4: IRAN: Kerman prov. 138

km S Rafsanjan. NMW 33172-5: IRAN: Kerman prov. 29

km SE Sirjan. NMW 33 165-4: IRAN, Kerman prov. 1 10 km

SW Kerman. NMW 33172-2, NMW 33175-6, NMW

33175-7: Iran: Yazd prov. 200km SE Yazd. NMW 33174-1-

8: IRAN, Khorasan prov. 15-25 km S Qayen. NMW 33163:

Pakistan: Nepandgur (where?). NMW 33162: Pakistan:

Delbandin. NMW 33161-1-2: Iran, Shirgesht Beiteabas.

NMW 33161-3: Iran, eastern Iran, Ozbak-Kuh. NMW

33172-6: Pakistan. Baluchestan prov. 50 km W Nushki.

NMW 33150-9: Iran W Sangbast. NMW 24763-1 -3 :Iran, N

Persian. Kuh Daschteh (Taj-abad). NMW 24767: Iraq.Bagh-

dad? (Paris Museum). CAS 120280-1: Afghanistan, 10km

NE Darweshan (Central Afg.). CAS 84642-45: Afghanistan,

35 mil. down stream from Girishk. Dasht-e-Margo area,

Chah-e-Angir, (Central Afg.). CAS 120242-4 Afghanistan,

12 km S Lashkargah (near Girishk), 2700ft. CAS 97990:

Afghanistan. 20 mil. SE Kandahar, 31 23 N, 65 53 E, 3800

ft. CAS 90762-9: Afghanistan, Sharisafa. 60 km NE Kanda-

har. 1400m. CAS 90777: Afghanistan,Tarnak river, 75 km

NE Kandahar. 1405m. CAS 120276-9: Afghanistan, 30km S

Ghazni-Qalat 7100ft. FMNH 20987-1-10: Iran.Esfahan

prov. Yazd-e-Khast .FMNH 20985-90: Iran, Esfahan prov.

FMNH 20988-1-2: Iran,Daria-Masila. FMNH 245507-10:

Pakistan.Baluchistan prov. SMF 63226-37, SMF 63262,

SMF 63285, SMF 63255: W-Pakistan, Siah-Kuh, S Delban-

din. BMNH 1951.1.6.54: Iran, Bandar-e-Lengeh. BMNH

1919.5.2.2-3: Iran, Fars prov. Abadeh. BMNH

1936.10.12.3: Iran, Fars prov.between Quatru-Chah Salz to

Neiriz road. BMNH 1966-355-57: Iran, Kerman prov. 148

km E Neiriz on Zaidabad road to Sirjan. BMNH

1951.1.2.20-22: Iran, Kerman prov. 20 mil. S of Kerman.

Jupar. BMNH 1951.1.6.45-48: Iran, Sistan prov. Khash, SE

Iran. BMNH 1940.3.1.19-24: Afghanistan, Ghazni, (E

Afgh.l.CAS 141028: Iran, Kerman prov. 17km SSE Minab

on inland road to Jask. CAS 141020: Iran, Kerman prov. 13

km E of Eastern edge of city of Kerman. CAS 141051: Iran.

Kerman prov. 19km SE Shagu on road to Minab. CAS

141027: Iran, Kerman prov. 21 km N Rudan on road to

Jiroft. CAS 141097: Iran, Sistan prov. 10km SW Hirmand,

abandoned village, SE of road from Zabol to Dust-e-

Mohammad Khan. CAS 141065: Iran, Baluchistan

prov. 1 3km southerly of Zahedan on road to Khash. CAS

102484-90: Iran: Sistan prov. 15 mi SW Zabol. CAS

102491-2: Iran, Fars prov. Ahram. CAS 141 149: Iran, Fars

prov. 5km northerly from Dalaky on road to Shiraz where

foothills begin. CAS 96270: Iran. Khorasan prov. Tayebat.

about 10 mi from Afghanistan border. NMW 33150-1-6:

Iran. Khorasan pro. 5 km N Taybad. NMW 33166-1 : Iran:

Kerman prov. 15 km SE Kerman.

Trapelus agilis sanguinolentus (n =238)

GNHM Re.ex. 4396 ( l-2):Iran: Mazandaran prov. 150 km E

of Gorgan, Golestan Park. GFN 40: Turkmenistan, Lowland

steppe. East Kopet Dagh. GNHM. Re. ex. GFN 41: Turk-

1999

Asiatic Herpetological Research

Vol. 8. p. 101

mcnistan. Murgub River, 150 km S of Marv (Mary).

GNHM. Re. ex. GFN 42-50:Turkmenistan, Sahra-Bairum-

Ali. 45km NW of Marv, Kara kum desert. CAS 185 104-9.

CAS 185134-5: Turkmenistan, Ashgabad region [38 00 N,

58 00 E], CAS 184570-6: Turkmenistan: Krasnovodsk

region [39 45 N. 54 33 EJ.

GNHM. Re. ex. GFN 35: Turkmenistan. Archenjan village.

GNHM. Re. ex. GFN 36: Turkmenistan. Krasnovodsk

region [39 45 N, 54 33 E]. GNHM. Re. ex. GFN 43 (1-2):

Turkmenistan, Kaka. GNHM Re. Ex 10622-3: Kazakhstan,

at the lake (artificial ) at Illi River, near village Bokter [43 54

N, 77 16 E]. ZISP5109, 13701-15 Kazakhstan, E. Kazakh-

stan, Illi River, near border of China. ZISP 5796: Kazakh-

stan.Tardski, Dshungaria, between Kazakhstan-China. ZISP

20298 (7745-79): Kazakhstan, near Ilisk city, Illi River. E.

Kazakhstan. ZISP 15143, 17329, 13695, 1 168: Kazakhstan,

near Ilisk city, Illi River, E. Kazakhstan. ZISP 1 1070 ( 1 - 1 2 ):

Kazakhstan: , Illi River, E. Kazakhstan.close to lake

Balkhash. ZISP 19115 (7643-84): Uzbekistan, Vicinity of

Nucus city. Caracal, near Aral sea. ZISP 19398 (7428-48):

Uzbekistan-Tajikestan, Fergan Valley. ZISP 15803 (1-15):

Tajikistan, Fergan Valley. ZISP 20097(371-87), 10715 (3-

13): Tajikestan-Afghanistan border, Termez. ZISP 13588,

13590(1-12), 13592.6914(1-10): Kazakhstan-Uzbekistan,

between Aral Lake and Caspian Sea. ZISP 19392 (1-24):

Russia (west of Caspian Sea), Daghestan. ZISP 15753: Iran.

Astarabad (= Gorgan?). CAS 183032-39: Russia, Chechen-

Ingush Autonomous Republic, the lowland between Terek-

Kuma Rivers [43 21 N, 46 06 E], CAS 120249-50: Afghan-

istan, 30-70 km E of Herat 3700-5350 ft. CAS 1 15922-3:

Afghanistan, Maimana, 35 54 N, 64 43 E. 884m. CAS

1 20280- 1 : Afghanistan, 10km NE Darweshan (Central

Afg.). CAS 120275: Afghanistan, 25 km E Khanabad

(between Mazare-Sharif-Faizabad), 2400ft. CAS 115920:

Afghanistan, northeastern Afghanistan. 64 mi by road E

Faizabad, 37 05 N, 70 40 E. CAS 1 15921 : Afghanistan,

Paghman Vicinity, 34 36 N, 68 56 E. 2440m. CAS 120251:

Afghanistan. 25km NW Pul-e-Khumri, 2400ft. (near Mazar-

sharif?). CAS 120255: Afghanistan, 20 km E Mazar-e-

Sharif. CAS 120253: Afghanistan, 10 km W Tashkurgan,

Near Mazar-Sharif? CAS 120256-8: Afghanistan, 20-50 km

E Mazar-e-Sharif. CAS 120259-61: Afghanistan, 45 km W

Mazar-e-Sharif, 1500ft. CAS 120273: Afghanistan, 50 km

W Mazar-e-Sharif. FMNH 161 197-9: Afghanistan, Maim-

ana, 35 54 N, 64 43 E 884 m. FMNH 161 133: Afghanistan,

64mil E Faizabad. 35 05 N, 70 40 E. FMNH 161 191-2:

Afghanistan, Paghman vicinity, 34 36 N, 68 56 E. 244m.

FMNH 141399: Iran, Mazandaran prov. 1 mi N of Pahlavi

Dezh.

pros.. 38 km S of Masjid-e-Sulaiman, Golgir village. CAS

86403-6, 86418-19 (paratypes), : Iran, Khuzistan prov.

along road to lake east of Haft-Kel. CAS 86464 (paratype):

Iran, Khuzistan an prov. along road south of Shushtar. CAS

86556 (paratype): Iran. Khuzistan prov. Haft-Kel (on golf

course) [31 28 N. 49 30 E]. CAS 86342, 86346, 86390

(paratypes): Iran. Khuzistan prov. Tuli-Bazum road [31 55

N. 49 25 E], FMNH 170936 (paratype): Iran, Khuzistan

prov. 53 mi SE Ahwaz , Mashrageh. CAS 86341, 86343-72,

86374-89: Iran, Khuzistan prov. Tuli-Bazum road [31 55 N.

49 25 E]. CAS 86320. 86323-28: Iran, Khuzistan prov.

Masjid-Suleiman [31 57,N, 49 16,E]. CAS 86322: Iran,

Binak. near Persian Gulf at foot of Kuh-e-Bang [29 44,N,

50 19,E]. CAS 86338-51: Iran, Khuzistan prov. along old

Masjid-Suleiman and Ahvaz road [32 N, 49 1 l.E]. CAS

86251: Iran. Khuzistan prov. Masjid-i-Suleiman [31 57 N,

49 16 E], CAS 86373: Iran. Khuzistan prov. road south of

Shushtar. CAS 102491-2: Iran, Fars prov. Ahram. CAS

86625: Iran. Khuzistan an prov. Binak. on Persian Gulf at

foot of Kuh-i-Bang, north of Ganaweh. [29 44 N, 50 19 E].

CAS 86487: Iran, Fars prov. Agha Jari. [29 48 N, 49 46 E].

FMNH 141392-3, 141395-6, 141398: Iran, Fars prov.

Ahram. ZISP 10335: Iran, Kochrud, Irak-Adschemi (exact

locality?) (Nikolsky's Type of Agama kennanensis , var.

brevicauda ). ZISP 9321: Iran. Kochrud. Irak-Adschemi

(exact locality?) (Nikolsky's Type of Agama kennanensis ).

ZISP 9889: Iran (exact locality ?).

Trapelus agilis pakistanensis (n =32)

SMF 63258 (holotype), 63259, 63279 (paratypes): Pakistan,

Gaj-River, Kirthar Range. SMF 63256 (paratype): Pakistan,

Sonda Distr.Thatta. SMF 63236: Pakistan, Old Airport of

Karachi. 63243-4 and 63286-7 (paratypes): Pakistan, Old

Airport of Karachi. SMF 63239, 63264: Pakistan, Hab River

at Goth Mauladad. SMF 63263: Pakistan, Jati, Sind. SMF

63276: Pakistan, Karangee at Karachi. SMF 63265: Paki-

stan, Karachi. SMF 63267: Pakistan. Karachi area. FMNH

224946: Pakistan, Sind Prov. Dadu dist. Ranicot. FMNH

244977: Pakistan, Sind Prov. Karachi Dist. Malir. conton-

ment. FMNH 244948: Pakistan, Sind Prov. Karachi Dist.

Malir, contonment. BMNH 1933.7.8.23: Pakistan, Salt

Range. Punjab. BMNH 74. 4. 29. 1432, 80. 1 1. 10. 25: Paki-

stan, Sind area. BMNH 98. 12. 22. 7-8: Pakistan: Kurrachee

(karachi). BMNH 1964-271: Pakistan, Mirpur Khas.

BMNH 1933.12.7.1: Pakistan, Sind area.

Trapelus agilis khuzistanensis (n =97)

GNHM. Re. ex. 5424 (holotype): Iran, 5 km NW Haft-Gel

on the road to Shushtar. GNHM. Re. ex. 5425 (paratype):

Iran, Khuzistan prov., 5 km NW of Haft-Gel on road to

Shushtar. GNHM. Re. ex.5426 (paratype) : Iran, Khuzistan

1999

Asiatic Herpetological Research

Vol. 8, pp. 102-106

Rhacophorus leucomystax in Vietnam with Acoustic Analyses of

Courtship and Territorial Calls

Tanya L. Trepanier1- 2, Amy Lathrop1'2 and Robert W. Murphy1-2-3

1 Department of Zoology, University of Toronto, 25 Harbord Street, Toronto, Ontario, Canada M5S 3G5, e-mail:

tanyat@rom.on.ca; 'Centre for Biodiversity and Consenation Biology, Royal Ontario Museum, 100 Queen's

Park, Toronto, Ontario, Canada M5S 2C6; Corresponding author: e-mail: drbob@rom.on.ca

Abstract.- Acoustic parameters of both courtship and territorial calls were analysed for two populations of

Vietnamese treefrogs, genus Rhacophorus. These treefrogs from Ba Be National Park and nearby Na Hang

Nature Reserve were identified as R. leucomystax as opposed to R. megacephalus, based on an acoustic analysis

of courtship calls. They represent the first confirmed record of this species outside of Borneo and suggest that the

species may also occur in China. The courtship call, composed of a long note of similar pulses and pitch, has a

mean dominant frequency of 1940 ± 154 Hz at Ba Be National Park and 1950 ± 70 Hz at Na Hang Nature

Reserve. The territorial call, a two to three note call, has a mean dominant frequency of 1940 ± 124 Hz at Ba Be

National Park and 2190 ± 256 at Na Hang Nature Reserve. No significant differences were found between the

call characters of these two populations of Vietnamese R. leucomystax. There was no significant association

between snout- vent length and dominant frequencies.

Key words.- Amphibia, Anura, call analysis, Rhacophoridae, Rhacophorus leucomystax, Vietnam, vocalizations.

Introduction

Until recently, the amphibian fauna of Vietnam has

been based on the works of Bourret (1942), and

accounts from neighbouring China (e.g., Yang, 1991;

Zhao and Adler, 1993: Zhao, 1995). The Chinese

occurrence of one species of treefrog, Rhacophorus

leucomystax, was recently placed into doubt by Mat-

sui et al. (1986) based on chromosomal, morphologi-

cal and acoustic evaluations. These authors reported

that R. leucomystax was restricted in distribution to

Borneo whereas a similar species, R. megacephalus.

occurred in Taiwan. They stated that mainland Chi-

nese populations of these frogs required further study,

but in the interim, mainland Chinese populations

should be referred to as R. megacephalus. Zhao and

Adler (1993) reported that R. leucomystax did not

occur in China, but rather that R. megacephalus

occurred throughout the country. Our recent field

work in northern Vietnam revealed the presence of

two apparent forms of treefrogs similar in appearance

to R. megacephalus and/or R. leucomystax. We suc-

cessfully recorded vocalizations of one form from two

allopatric populations. Herein, we report our analysis

of the acoustic parameters of both courtship and terri-

torial calls, including the dominant frequency, which

is species specific.

Amirans are capable of different types of vocaliza-

tions which serve different functions. The courtship

call, also known as the mating or breeding call, is

emitted by males and has two functions: the attraction

of conspecific females and the announcement of an

occupied territory to other males of the same or differ-

ent species. There are three types of courtship calls:

the courtship call produced by males in attempt to

attract a conspecific female, a territorial call produced

by a resident male in response to an courtship call

received above a critical threshold of intensity, and an

encounter call evoked during close range agnostic

interactions between males (Duellman and Trueb,

1994). The courtship call acts as a courtship isolating

mechanism (Duellman and Pyles, 1983). A second

type of call, the territorial call, is comprised of acous-

tic signals and is accompanied by corporal vibrations

produced by a male or an unreceptive female in

response to amplexus. Other types of calls include the

reciprocation call which is given by a receptive

female, and the distress call which is delivered in

response to an enemy or predator for defence.

Signals are found to vary between and within indi-

viduals and between geographically separated popula-

tions of a single species (Cocroft and Ryan, 1995).

Anurans use these differences in call characteristics to

identify individuals of the same or different species

and to signal intent. Frost and Platz ( 1983) proposed

that these interspecific and intraspecific differences in

fundamental call characteristics such as pulse rate,

duration of call, dominant frequency, or a combina-

1999

Asiatic Herpetological Research

Vol. 8, p. 103

tion of these parameters, permits females to reduce

the likelihood of error in mate choice. Anurans recog-

nize individuals of the same and different species by

their dominant frequencies.

Duellman and Pyles (1983) discovered that

smaller frogs tend to call at higher frequencies and

have a reduced auditory sensitivity compared with

larger frogs. They concluded that an upper limit of

approximately 5000 Hz is most common. Further-

more, the reception of acoustic signals is affected by

habitat and interference from synchronously calling

species. In rainforest habitats, which are complex

habitats, anurans were found to produce sounds at

lower frequencies because the dense vegetation atten-

uates sound waves, notably those at higher frequen-

cies. Therefore, transmission frequencies of less than

4(X)0 Hz would be most effective for anuran commu-

nication in such complex habitats. Partitioning of the

acoustic community can be affected by several factors

such as type of call produced, oviposition site, envi-

ronment and the onset of the breeding season (Duell-

man and Pyles. 1983). But within any given

community, the available acoustic environment is par-

titioned distinctly based on its particular ecological

and geographic assemblage of anurans. Although

selection may operate to maximize acoustic properties

for species recognition, acoustic interference from

factors of the physical habitat and from community

members also operates to minimize acoustic variabil-

ity. This implies that members of the same breeding

fauna have voices with common characteristics

(Duellman and Pyles, 1983).

Material and Methods

Frog calls were recorded and calling specimens col-

lected from two different localities in northern Viet-

nam. Approximately 24 frogs of the R. leucomystax

complex were recorded and collected in Ba Be

National Park (22°24'N 105°37'E) from 15 to 29 May

1995. Five R. leucomystax were recorded and col-

lected in the village of Pac Ban (22°21'N 105°23'E)

located in Na Hang Nature Reserve, from the 23 May

to 3 June, 1996. In both locations, frogs were selected

at random and a sufficient call sample was recorded

using a Realistic™ unidirectional microphone and a

Marantz™ PMD 201 portable cassette recorder. Air

temperatures were recorded in degrees Celsius at Ba

Be National Park at the time of capture, using a ther-

mometer; each specimen was collected during

evening hours from a concrete pool adjacent to the

Park's research centre. In Pac Ban, frogs were col-

lected from various locations, including in rice patties,

on trees, and in ponds. All specimens were eutha-

nised, preserved and deposited in the herpetology col-

lections of the Royal Ontario Museum, Toronto,

Canada. Calls were transferred from the cassette

recorder to a Macintosh computer using a Macrore-

corder™ digitizer. Sound Edit Pro™ version 2.0.5 for

Macintosh computer systems was used for call analy-

ses. Note duration, dominant frequency, fundamental

frequency, notes per call, pulses per note and time

between segments were measured. Descriptive analy-

ses were performed for all courtship and territorial

calls, using Excel™ 5.0 (Microsoft). Snout-vent

length (SVL) was measured for all specimens to the

nearest 0.1 mm using digital calipers.

Results

Of the 24 specimens recorded and digitized at Ba Be

National Park. 42 courtship calls were analysed from

22 individuals, and 33 territorial calls from 18 indi-

viduals. Table 1 summarizes measurements of call

parameters for all mating calls.

In most cases, the fundamental frequencies over-

lapped the dominant frequencies, rendering it impos-

sible to obtain exact measurements. However, in those

that were observed, the fundamental frequency

appeared to be approximately one half the value of the

dominant frequency (900-1000 Hz). Air temperatures

did not vary significantly, with a mean of 26.2°C for

territorial and courtship calls, thereby having little

effect on call characteristics. All courtship calls had

one note, and pulses ranged from 2 to 17 per note. In

contrast, all territorial calls were either 2 or 3 notes

per call, the most common being the former, with

variability in numbers of pulses in all three notes (Fig-

ure 1).

Of the 5 specimens recorded and digitized in Pac

Ban, 2 courtship calls were analysed from 2 individu-

als, and 21 territorial calls from 5 individuals. Call

parameters are summarized in Table 1. Fundamental

frequencies were obtained from the sonograms, where

values were noted as approximately one half the value

of the dominant frequency (800-900 Hz). All court-

ship calls had one note, and pulses ranged from 4 to

16 notes per call. In contrast, all territorial calls were

either 2 or 3 notes per call, the most common being

the former, with variability in numbers of pulses in all

three notes.

The courtship call resembled the sound of a trill,

or long sequence of pulses of similar pitch, whereas

the territorial calls were more similar to the sound of

clicks. Dominant frequencies were consistent within

all calls; mean dominant frequency in courtship calls

were 1940 Hz for the Ba Be population and 1950 Hz

Vol. 8. p. 104

Asiatic Herpetological Research

1999

Table 1 . Call measurement summary of note duration, notes/call, pulses/note and dominant frequencies for Rha-

cophorus leucomystax in Ba Be National Park and Pac Ban in Na Hang Nature Reserve.

Ba Be National Park

Courtship Territorial

Na Hang Nature Reserve

Courtship Territorial

for the Pac Ban population. For territorial calls, the

mean dominant frequency was also 1940 Hz in Ba Be

and 2190 Hz in Pac Ban. Therefore, R. leucomystax

has a species-specific dominant frequency of approxi-

mately 2000 Hz. A consistency between segments or

pulses was observed for the territorial calls. The mean

time between segments was 0.02 seconds (standard

deviation ±0.003).

Snout-vent length was measured for all specimens

and correlated with dominant frequency. Our regres-

sion analyses failed to confirm a significant associa-

tion (F= 1.948, p=0.176, r=0.08) between SVL and

dominant frequency.

Discussion

Call duration and pulse rate are temperature depen-

dent (Platz, 1989). Regression analysis of call charac-

teristics and temperatures achieve the highest

correlation, where a correction function is generated.

The correlation function is then used to correct data

for temperature differences revealing little variation.

For example, a few obvious differences were discov-

ered in the values of the call characteristics as shown

in the sonograms for the eastern and western samples

of Rana pipiens when differences in temperature

between the localities and variation within the locali-

ties were taken into account (Dunlap and Platz, 1981).

However, because temperatures were not significantly

variable, temperature values were not used to account

for variation in our data. Furthermore, our regression

analyses revealed that snout-vent length did not

account for variation in our acoustic data, as it does in

some other anuran species (Duellman and Pyles,

1983).

Because dominant frequency is characteristic of

species, we compared our data with those of Matsui et

al. (1986). The dominant frequency of Rhacophorus

leucomystax ranged from 2250-2550 Hz whereas it

ranged from 1040-1070 Hz in R. megacephalus. Fur-

ther, Matsui et al. (1986) found that R. leucomystax

had one note/call whereas in R. megacephalus it

ranged from 2-4 notes/call. Given that the mating

calls of our frogs from northern Vietnam had a domi-

nant frequency of 1.94-2.49 kHz (Table 1) and con-

sisted of a single note/call, we conclude that our

specimens are best identified as R. leucomystax pend-

ing additional morphological evaluations (in prepara-

tion). Our study sites at Ba Be National Park and Na

Hang Nature Reserve are located only 125 km south

of Yunnan Province, China. Consequently, given that

R. leucomystax ranges from at least Borneo to north-

ern Vietnam, the species likely also occurs in China

and elsewhere in Asia. Further, it seems likely that it

occurs sympatrically with R. megacephalus, at least in

Vietnam.

Disturbance to the environment may have negative

impact on anuran populations. As a result of

increased accessibility to Vietnam, tourists are begin-

ning to exploit the relatively primitive country. Such

exploitation will likely contribute to increased defor-

estation and wildlife loss. Human population growth

continues to rise in Vietnam at an alarming rate (ca.

2.3%/yr) and deforestation is increasing in quest for

construction materials and agriculture for both in-

country needs and cash-crop export, especially coffee.

Species mining is occurring for export of animals to

foreign countries, regardless of species type, number

or Vietnamese efforts to protect the species. Little-

john and Roberts (1975) remarked that the environ-

ment of north central Victoria, Australia, had been

greatly modified over the last 130 years by increased

land clearing for agriculture, timber cutting for build-

ing and mining, and by the establishment of extensive

irrigation and drainage systems. They suggested that

these alterations have influenced the position, extent,

and nature of the main zones of intergradation, which

may further increase dispersal due to global warming

1999

Asiatic Herpeiological Research

Vol. 8, p. 105

0 00

0 38

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8000

6000

5 4000

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Figure 1 . Call characteristics for Rhacophorus leucomystax as illustrated through audiospectrograms (frequency

vs. energy) and sonograms (frequency vs. time). An expanded oscillogram (above) shows finer details of the call.

Territorial calls from A) Babe (ROM 19334); B) Pac Ban (ROM 6514), and courtship calls from C) Babe (ROM

19486); and D) Pac Ban (ROM 6514).

and the concomitant northward movement of anuran

populations. The possibility for divergence in mating

call structure could then result increasing the fre-

quency of mismatching and nonviable offspring. Like

Victoria, it is not known what the future beholds for

the relatively fragile, undiscovered and endemic spe-

cies of Vietnam. Therefore, identification of species

for many areas of study, such as behavioural, ecologi-

cal and evolutionary fields, will be critical in the next

few years so that as many species as possible can be

studied, identified and conserved.

Acknowledgments

Collecting and export permits were made available

through Vietnam's Institute of Ecology and Biological

Resources (IEBR), Hanoi. This study was supported

by the Natural Sciences and Research Council

(NSERC) of Canada grant A3 148, by the generous

assistance of the ROM Sciences Fieldwork Fund, the

ROM Future Fund, the ROM Foundation, the Depart-

ment of ROM Volunteers, the Department of Zoology,

University of Toronto, Dr. M. Richardson and K.

Beckley, and S. Bain to R. W. Murphy. For assistance

with field work, we are extremely grateful to B. Nup-

ponen for her encouragement and support during the

data collection and analyses of these calls, as well as

A. Cox, L. Ensor, M. Hanson. B. Kus, J. Rhydderch

and M. Theberge. G. Hochachka and K. Little

recorded the calls and captured the frogs at Ba Be

National Park during May of 1995. Phan Van Mach,

Pham Due Tien, and Cao Kim Thu of IEBR assisted

in many ways with on-site arrangements.

None of our efforts to document Vietnam's fantas-

tic fauna would be possible without the assistance,

constant encouragement, and guidance of Prof. Dr.

Cao Van Sung, Director of IEBR. Le Thi Quang,

Chairman of the Na Hang District Peoples' Commit-

tee, graciously approved the collaborative biodiversity

survey work. Le Hong Binh, Director of Na Hang

Nature Reserve, provided much guidance and exper-

tise about the resources of the Reserve, and the Tay

Minority peoples. Our heartfelt thanks go to the Tay

Vol. 8, p. 106

Asiatic Herpetological Research

1999

Minority families of Pac Ban who not only shared

their houses, but also their lives. For this we are

grateful to Luong Thi May and Le Van Duy ("the

kitchen"). Ma Van Tung and Dinh Thi Thang ("men's

room"), and Ma Thi Nguy ("womens' house") for

putting up with a bunch of, at times rowdy, Canadi-

ans.

Cathay Pacific Airlines significantly contributed to

our efforts by providing free excess baggage during

international travels. Magnalight, Coleman, Johnson

Wax, Tilley Endurables, and Benjamin Film contrib-

uted significantly to the success of our Vietnam biodi-

versity project. This is a contribution from the Centre

for Biodiversity and Conservation Biology, ROM.

Literature Cited

Bourret, R. 1942. Les batraciens de l'lndochine.

Memoires de l'lnstitut Oceanographique de l'lndoch-

ine 6:x+517.

Cocroft, R. B., and M. J. Ryan. 1995. Patterns of

advertisement call evolution in toads and chorus

frogs. Animal Behaviour 49: 283-303.

Duellman, W. E., and R. A. Pyles. 1983. Acoustic

resource partitioning in anuran communities. Copeia

1983: 639-649.

Duellman, W. E. and L. Trueb. 1994. Biology of

Amphibians. The John Hopkins University Press. Bal-

timore, Maryland

Dunlap. D. G., and J. E. Platz. 1981. Geographic

variation of proteins and call in Rana pipiens from the

north central United States. Copeia 1981: 876-879.

Frost. J. S., and J. E. Platz. 1983. Comparative

assessment of modes of reproductive isolation among

four species of leopard frogs (Rana pipiens complex).

Evolution 37: 66-78.

Littlejohn, M. J., and J. D. Roberts. 1975. Acoustic

analy is of an intergrade zone between two call races

of the Limnodynastes tasmaniensis complex (Anura:

Leptodactylidae) in south-eastern Australia. Austra-

lian Journal of Zoology 23: 1 13-122.

Matsui, M., T. Seto. and T. Utsunomiya. 1986.

Acoustic and karyotypic evidence for specific separa-

tion of Polypedates megacephalus from P. leucomys-

tax. Journal of Herpetology 20: 483-489.

Platz, J. E. 1989. Speciation within the chorus frog

Pseudacris triseriata: Morphometric and mating call

analyses of the boreal and western subspecies.

Copeia 1989: 704-714.

Yang, D. 1991. The Amphibia-Fauna of Yunnan.

China Forestry Publishing House [In Chinese].

Zhao, E.-M. (ed.) 1995. Amphibian Zoogeographic

Division of China. Sichuan Journal of Zoology, 1995

Supplement. [In Chinese].

Zhao, E.-M. and K. K. Adler. 1993. Herpetology of

China. SSAR in cooperation with CSSAR, Contribu-

tions to Herpetology 10, 522 pp.

1999

Asiatic Herpetological Research

Vol.8, pp. 107-110

Immuno-chemical Study of TSV-PA, a Specific Plasminogen Activator from the

Venom of Trimeresurus stejnegeri

Yun Zhang1. Wen-hui Lee, Yu-liang Xiong, and Wan-yu Wang

Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, Yunnan, China

Abstract.- Rabbit antibodies were prepared against purified TSV-PA, a specific plasminogen activator from the

venom of Trimeresurus stejnegeri. They strongly cross-reacted with Crotalinae snake venoms like Trimeresurus

stejnegeri, Trimeresurus mucrosquamatus, Agkistrodon halys and Agkistrodon acutus. In contrast,

immunological cross-reactions with Elapidae snake venoms, Ophiophagus Hannah, Naja naja atra were

relatively lower and no cross-reactions with Bungarus fasciatus, Bungarus multicinctus venoms. On the other

hand, enzymatic assays only revealed the existence of plasminogen activation activity in the venom of

Trimeresurus stejnegeri. Except trypsin, anti-TSV-PA sera and antibodies did not cross-react with other serine

proteases, such as physiological urokinase-type plasminogen activator (u-PA) and tissue-type plasminogen

activator (t-PA). Anti-TSV-PA antibodies inhibited both the amidolytic activity and plasminogen activation

activity of TSV-PA, but they did not inhibit the plasminogen activation activity of u-PA and t-PA.

Key words.- Snake venoms, antibodies, serine proteases

'To whom correspondence should be addressed: Dr. Yun Zhang, Kunming Institute of Zoology, Chinese Acad-

emy of Sciences, Kunming 650223, Yunnan, China. Tel: (86-871 ) 5194279; Fax: (86-871 ) 5191823.

Introduction

TSV-PA, a specific plasminogen activator from the

venom of Trimeresurus stejnegeri, is a serine protease

which specifically cuts the Arg560- Val56 1 bond of

plasminogen and forms plasmin (Zhang et al., 1995).

Sequence analysis indicates that TSV-PA is a typical

snake venom serine protease which show great

homology with other snake venom serine proteases,

such as thrombin-like enzymes (Itoh et al., 1987;

Shieh et al., 1988), protein C activator (McMullen et

al., 1989), and factor V activator (Tokunaga et al.,

1988). Serine proteases are widely distributed in

snake venoms especially in Crotalinae snake venoms

(Stocker, 1990). TSV-PA is the first specific plasmino-

gen activator found in snake venoms. In this investiga-

tion, we reported the immuno-chemical study of TSV-

PA.

Material and Methods

Snake Venoms were from the stock of Kunming Insti-

tute of Zoology, Chinese Academy of Sciences. TSV-

PA from Trimeresurus stejnegeri venom is purified as

described previously (Zhang et al., 1995). TSV-PA

was denatured by adding (3-mecaptoethanol to 1%

final concentration and boiled at 100 °C for 5 min.

Native TSV-PA and denatured TSV-PA were emulsi-

fied with 50% Freund adjuvant and were administered

s.c. at 2 week intervals. Boosts, which were per-

formed when the serum titers were decreasing, were

achieved by injecting s.c. the same components, in the

presence of incomplete Freund adjuvant. The immu-

nization protocol was performed by the dose of

administered antigen 100 (ig per rabbit.

Microtitration plates (96 wells) were coated in

phosphate-buffered saline (PBS) by over night incu-

bation of antigen (5 (ig/ml) and saturation was carried

out with 3% BSA in PBS. Plates were washed with

PBS containing 0.1% Tween-20. The solutions to be

tested (100 |il/well), diluted in PBS containing 3%

BSA, were incubated 1 hour at 37 °C, then washed.

Peroxidase-labelled goat antibodies anti-rabbit immu-

noglobulins (Biosys, Compiegne) were added at a

1:2000 dilutions, incubated 1 hour at 37 °C and

washed. Substrate for peroxidase (O-phenylenedi-

amine dihydrochloride in 10 mM sodium phosphate,

pH 7.3, 0.01% H2G*2) were added and the absorbance

was recorded at 405 nm with a Dynatech microplate

reader.

Antibodies (IgG) were purified from the sera by

double ammonium sulfate precipitations (35% final

concentration), and then dialyzed against PBS. Inhibi-

tion of enzymatic activity was carried out by preincu-

bating for 30 min at 37 °C a fixed concentration of the

enzyme (5 Ug/ml) with variable amounts of antibodies

Vol. 8, p. 108

Asiatic Herpetological Research

1999

>

o

CD

c

E

<i>

CE

Table 1 . The titers of the antibodies against TSV-PA (a

specific plasminogen activator from the venom of Trim-

eresurus stejnegen)

Ig G concentration (mg/ml)

Figure 1. Inhibition of plasminogen activation by IgG

against native and denatured TSV-PA. Fixed concen-

trations of TSV-PA, human two chains lower-molecular

weight urokinase (u-PA) or human two chains tissue

type plasminogen activator (t-PA) were incubated with

various concentrations of antibodies against TSV-PA

for 30 min in 37 °C. Then the remaining plasminogen

activation activity was determined and expressed as

the percentage of the original values. (O) TSV-PA test,

(•) TSV-PA control, (A) TSV-PA test with anti-dena-

tured TSV-PA antibodies, (♦) u-PA test, (<3>) u-PA con-

trol, (■) t-PA test, (□) t-PA control.

and by testing the residual enzymatic activity. Plasmi-

nogen activation activity and amidolytic activity of

the enzymes were assayed as described by Zhang et

al. (1995).

Results

We immunized rabbits with purified TSV-PA, both in

its native and denatured forms. Table 1 shows that the

antiserum directed against native TSV-PA has a much

higher ELISA titer than that directed against dena-

tured TSV-PA, showing that native TSV-PA is much

more antigenic than denatured TSV-PA. On the other

hand, antiserum directed against native TSV-PA has a

much lower ELISA titer when coating the plate with

denatured TSV-PA, indicating that large parts of the

antibodies raised against native TSV-PA are against

comformational epitopes of the protein.

In the first series of experiments, we examined the

immunological cross-reactions by ELISA. The anti-

TSV-PA antibodies (from here, if not specially noted,

anti-TSV-PA serum and antibodies means those raised

against native TSV-PA) cross-reacted with TSV-PA

and Trimeresurus stejnegen venom. In the mean time,

they cross-reacted with several other Crotalinae snake

venoms in which we did not find the activity of plas-

minogen activation. From the ELISA titers, we can

see, first, the immunological cross-reaction with ven-

oms from Crotalinae snakes are much higher than

with those from Elapidae snake venoms. Second,

ELISA titers were defined as the serum diluuon or lmmunoglubin concentrauon that

produced half of the maximal response. The indicated values are the means of three

independent experiments, standard deviations being 10%. (1) means immuno-cross

reactions with anti -denatured TSV-PA antibodies.

even though we did not find plasminogen activity in

other venoms, but in these venoms such as Trimeresu-

rus mucrosquamatus, Agkistrodon halys and Agkistro-

don acutus there are serine proteases which are very

similar with TSV-PA in structure. This observation is

also coincident with the sequence comparison of

TSV-PA with other snake venom serine proteases like

thrombin-like enzymes, protein C activator and factor

V activator (Zhang et al., 1995). The sequence of

TSV-PA shows 64% homology with thrombin-like

enzyme from Trimeresurus flavoviridius.

We further analyzed the immunological cross-

reactions of anti-TSV-PA antibodies with other serine

proteases. T: strongly cross-reacted with batrox-

obin, a thrombin-like enzyme from Bothrops atrox

venom. In addition, they only slightly cross-reacted

with trypsin (Table 1). Even TSV-PA shares the same

biological activity (plasminogen activation) with

physiological activators, u-PA and t-PA, there is no

immunological cross-reactions among them. These

results is in agreement with that the venom serine pro-

teases which have been well studied like thrombin-

like enzymes belong to trypsin-kallikrein subfamily

(Itoh et al., 1987; 1988, McMullen et al., 1989).

1999

Asiatic Herpetological Research

Vol. 8, p. 1()9

1 20 40

TSV-PA VFGGDECNINEHRSLWLFN SNG--FLCGGTLINQDWWTAAHC

batroxobin VIGGDECDINEHPFLAFMYY SPR — YFCGMTLINQEWVLTAAHC

trypsin I IVGGYTCPEHSVPYQVSL NSGYHFCGGSLINDQWWSAAHC

t-PA IKGGLFADIASHPWQAAIFAKHRRSPGERFLCGGILISSCWILSAAHCFQERFP

u-PA IIGGEFTTIENQPWFAAIYRRHR-GGSVTYVCGGSLISPCWVISATHCFID-YP

60 80

TSV-PA DSNNFQLLFGVHSKKILNEDEQTRDPKEKFFCPNRKKDDEV — DKDIMLIKLDS

batroxobin NRRFMRIHLGKHAGSVANYDEWRYPKEKFICPNKKKNVIT — DKDIMLIRLDR

trypsin I YKSRIQVRLGEHNINVLEGDEQF-INAAKIIKHPNYSSWTL--NNDIMLIKLSS

t-PA P-HHLTVILG-RTYRWPGEEEQKFEVEKYIVHKEFDDDT--YDNDIALLQLKS

u-PA KKEDYIVYLG-RSRLNSNTQGEMKFEVENLILHKDYSADTLAHHNDIALLKIRS

100 120 140

TSV-PA SVSNSEH IAPLSLPSSP PSVGSVCRIMGWGKTIPTKEIYPDVPHCAN

batroxobin PVKNSEH IAPLSLPSNP PSVGSVCRIMGWGAITTSEDTYPDVPHCAN

trypsin I PVKLNAR VAPVALPSAC APAGTQCLISGWGNTLSNGVNNPDLLQCVD

t-PA DSSRCAQESSWRTVCLPPADLQLPDW-TECELSGYGKHEALSPFYSERLKEAH

u-PA KEGRCAQPSRTIQTICLPSM-YNDPQFGTSCEITGFGKENSTDYLYPEQLKMTV

160 180

TSV-PA INILDHAVCRTA-YSWRQVANTTLCAGILQGG RDTCHFDSGGPLICNG

batroxobin INLFNNTVCREA-Y--NGLPAKTLCAGVLQGG IDTCGGDSGGPLICNG

trypsin I APVLSQADCEAA-YP-GEITSSMICVGFLEGG KDSCQGDSGGPWCNG

t-PA VRLYPSSRCTSQHLLNRTVTDNMLCAGDTRSGGPQANLHDACQGDSGGPLVCLN

u-PA VKLISHRECQQPHYYGSEVTTKMLCAADPQWKT DSCQGDSGGPLVCSL

200 220 234

TSV-PA I FQGIVSWGGHPCGQPGEPGVYTKVFDYLDWIKSIIAGNKDATCPP

batroxobin Q FQGILSWGSDPCAEPRKPAFYTKVFDYLPWIQSIIAGNKTATCP

trypsin I Q LQGIVSWG-YGCALPDNPGVYTKVCNFVGWIQDTIAAN

t-PA DGRMTLVGIISWG-LGCGQKDVPGVYTKVTNYLDWIRDNMRP

u-PA QGRMTLTGIVSWG-RGCALKDKPGVYTRVSHFLPWIRSHTKEENGLAL

Figure 2. Amino acid sequence comparison of TSV-PA with batroxobin, rat trypsin, human t-PA and u-PA.

The sequence comparison was performed with a Clustal V software package in a computer. Sequences were from

the following sources: TSV-PA, Zhang et al. ( 1995); batroxobin, Itoh et al. ( 1987); rat trypsin, MacDonald et al.

( 1982); human t-PA and u-PA protease domains, Pennica et al. (1983) and Steffens et al. (1982).

In second series of experiments, we tested the

inhibitory effect of antibodies directed against TSV-

PA on the enzymatic activities of TSV-PA, u-PA, t-PA

and other proteases. Figure 1 shows the plasminogen

activation inhibition by antibodies against both native

and denatured TSV-PA. In agreement with the results

above, anti-TSV-PA antibodies did not inhibit the

plasminogen activation activity of u-PA and t-PA. On

the contrast, both anti-native-TSV-PA and anti-dena-

tured-TSV-PA antibodies inhibited plasminogen acti-

vation by TSV-PA. Further experiments expressed

that only anti-native-TSV-PA antibodies inhibited the

amidolytic activity of TSV-PA, but anti-denatured-

TSV-PA antibodies did not. Combining the results of

figure 1 and the inhibition of amidolytic activity of

TSV-PA, we could find that anti-native-TSV-PA anti-

bodies inhibited both amidolytic and plasminogen

activation activities of TSV-PA, on the other hand,

anti-denatured-TSV-PA antibodies did not inhibit

amidolytic activity of TSV-PA, but inhibited plasmi-

nogen activation by TSV-PA. These results indicate

that the inhibition of plasminogen activation by anti-

denatured-TSV-PA antibodies is not caused by the

block of catalytic centre but by the block of the sub-

strate binding site. Probably, this is caused by a piece

of peptide in the enzyme which involves in the bind-

ing of the substrate, especially for large protein sub-

strate binding, and which appears as a sequential

Vol. 8, p. 110

Asiatic Herpetological Research

1999

epitope. Both anti-native and anti-denatured TSV-PA

antibodies did not inhibit the thrombin-like activity of

Trimeresunts stejnegeri and Agkistrodon acutus ven-

oms.

Figure 2 shoes the sequence comparison among

TSV-PA, batroxobin, rat trypsin, human t-PA and u-

PA. TSV-PA shares 63% sequence identity with

batroxobin (a thrombin-like enzyme), 42% with rat

trypsin, but only 23% with human u-PA and 21% with

human t-PA. The sequence comparison results are in

agreement with the immuno-chemical studies above.

Discussion

Snake venoms contain numerous different proteases

which act on blood cascade (Stocker, 1990). Bio-

chemically, two main classes of these protease are

recognized: serine proteases and mealloproteinases.

For one group of venom serine proteases, they share a

trypsin homologous catalytic domain and the molecu-

lar weights are usually around 25 kDa-35 kDa

depending on the carbohydrate content of the enzyme.

Even the sequence similarity among them are around

65-70%, for example thrombin-like enzymes (Itoh et

al.. 1987; Shieh et al., 1988), protein C activator

(McMullen et al., 1989), factor V activator (Tokunaga

et al., 1988), kallikrein-like enzyme (Komori et al.,

1988) and newly determined plasminogen activator

(Zhang et al., 1995), this group of venom serine pro-

tease is characterized by their highly divergent sub-

strate specificity. Unlike their trypsin homologous,

they are usually highly specific. The explanation of

their highly homology primary sequence verse their

highly divergent substrate specificity (for protein sub-

strate) and the determination of their substrate binding

site is extremely significant in our understanding of

protein structure-function relationship and further the

protein reconstruction for medical purpose in future.

Acknowledgments

The study was supported in part by the national 863

plan, the Director fund of Chinese Academy of Sci-

ences, and in part by the fund of Yunnan Science and

Technology Commission C0085M.

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complete amino acid sequence. Journal of Biological

Chemistry 263: 17471-17481.

Zhang, Y, A. Wisner, Y L. Xiong and C. Bon. 1995. A

novel plasminogen activator from Trimeresurus stej-

negeri snake venom. Journal of Biological Chemistry

270: 10246-10255.

Asiatic Herpetological Resean /.

Vol. S, pp. 111-113

A New Locality for Cuora pani Song 1984 with Comments on its Known Range

James Ford Parham1 and Dong Li2

Department of Integrative Biology, University of California, Berkeley, CA 94720-3140 USA, email:

parham@socrates.berkeley.edu. 'Southwest Electric Power Design Institute, Dong Feng Road, Chengdu,

Sichuan. 610061, China

Abstract.- The discovery of Cuora pani Song 1984 in northern Sichuan Province. China lends credence to the

type locality in southern Shaanxi Province. The localities reported from southern Yunnan Province (the type

region of C. ''chriskarannarum " I require verification.

Key words.- Replilia, Chelonia, Bataguridae, Cuora pani, C. chriskarannarum, C. yunnanensis, C. zhoui, China

Sichuan. Yunnan, distribution, biogeography

Cuora pani Song. 1984 is the first of many new Chi-

nese chelonians to he described over the past fifteen

years. The original description was based on two

specimens from the Qin Ling Mountains (Pingli

County, southern Shaanxi Province). Later. C. pani

was inadvertently redescribed from southern Yunnan

Province as C. chriskarannarum by Ernst and

McCord (1987) based on pet-trade specimens. De

Bruin (1988) first suggested the synonymy of C.

chriskarannarum with C. pani. Subsequently, other

authors (e.g., Phillipen pers. comm. in Stubbs, 1989;

Pritchard, 1990; Zhao, 1990; McCord and Iverson,

1991) have either independently come to the same

conclusion or at least agree with it. McCord and Iver-

son ( 1991 ) recognize that this synonymy requires that

C. pani is reported from two areas which are sepa-

rated by nearly 1200 km (Fig. 1). Given this unlikely

distribution, they raise the possibility that one of the

localities (if not both) are erroneous, but withhold fur-

ther speculation since the distributions of all Cuora

are very poorly understood. In this paper we report a

new locality for C. pani which may shed some light

on this issue.

In April of 1994 one of us (DL) heard reports of a

turtle with a moveable plastron from people living in

northern Sichuan. Due to the scarcity of these turtles,

it took five years to acquire the first specimens. Three

individuals were purchased in Guangyuan City by DL

and were reportedly captured in the nearby tributaries

of the Jialing River (105°. 40' E, 32° 30' N; Fig. 1).

Two of the turtles are females; the largest is 180 mm

in straight-line carapace length and weighs 625

grams. The smaller female is 110 mm in carapace

length and 130g . The only male is a juvenile (Fig. 2),

98 mm in carapace length and weighing 95g. All three

turtles match descriptions of Cuora pani (Song, 1984;

McCord and Iverson, 1991). Diagnostic characters

include an olive head, olive-brown carapace, and.

most importantly, a plastron with dark pigment asso-

ciated with the seams in the form of rectangular bars.

The presence of these turtles in northern Sichuan

Province lends credence to the type locality of Cuora

pani in southern Shaanxi Province. The new locality

also closes the distributional gap between the southern

Shaanxi locality and the type region of C.

"chriskarannarum" from nearly 1200 km to about

1050 km. Nevertheless, we feel that the Sichuan local-

ity, by verifying the presence of C pani in the north-

ern tributaries of the Yangtze, casts doubt on the

validity of the C. "chriskarannarum" localities. The

latter localities become even more suspicious when

the distribution of other species of Cuora are taken

into account. For example, the type locality of Cuora

aurocapitata (Luo and Zong, 1988) is in the eastern

Yangtze drainage. Cuora aurocapitata is a close rela-

tive of C. pani, and may prove to be conspecific

(McCord and Iverson, 1991 ). The close relation of C.

pani and C. aurocapitata is reflected by their biogeo

graphical distribution since both taxa inhabit the

Yangtze River or its northern tributaries.

The type region of C. "chriskarannarum" is in tr.e

drainage of the Red River. Two divides separate these

localities from the type region of C. pani (in souths a

Yunnan the Pearl River drainage lies between the R<-d

River and the southwestern tributaries of the Yangtze !

We can not rule out a corridor between the Red River

and the Yangtze in northern Yunnan, but note that, in

addition to a mountainous divide, other species of

Cuora historically inhabited this area. Cuora zhoui

1 This specimen has been accessioned into the Chengdu

Institute of Biology herpetological collection as CIB-

9910544

Vol. 8, p. 112

Asiatic Herpetological Research

1999

Figure 1 . Map of China showing known localities of select aquatic Cuora species. A= C. aurocapitata, P= C. pani,

Y= C. yunnanensis, Z= C. zhoui. Localities were taken from original descriptions, McCord and Iverson (1991 ), and

Iverson (1992).

Zhao, 1990 (= Cuora pallidicephala McCord and

Iverson, 1991) and Cuora yunnanensis (Boulenger,

1906) are both reported from tributaries of the

Yangtze in northern Yunnan (Fig. 1). Like C.

"chriskarannarum" , the Yunnan records for C. zhoui

(the type series of C. "pallidicephala") are derived

from the pet trade (McCord and Iverson, 1991) and

are from a different province than the type description

(Zhao, 1990). Unfortunately, the type series of C.

zhoui itself was purchased from a market so the exact

provenience of this species remains uncertain. The

localities for C. yunnanensis, however, are probably

valid since they predate the increased turtle trade

associated with recent economic reforms in China.

The presence of at least one, and possibly two, conge-

ners within the reported range of C. pani is strange

since aquatic Cuora are generally allopatric.

A historic lowland connection between the south-

ern Yunnan and northern Yangtze Cuora pani locali-

ties would require even greater geographical

separation. Furthermore, this hypothetical connection

would pass through the known distribution of C. tri-

fasciata (McCord and Iverson, 1991), a close relative

of C. pani and C. aurocapitata (de Bruin, 1988; Bus-

kirk, 1989). In short, if the Yunnan Province C. pani

localities are real, the biogeographical history of these

turtles is very complex.

It is important to note that many of the localities

for Chinese turtles, including the one reported here,

are based upon market-bought or else pet trade ani-

mals. Pet trade localities, such as the southern Yunnan

Cuora pani localities, should be treated with caution.

The demand for rare species by turtle fanciers greatly

increases their value and, therefore, there is incentive

to hide the true locality as a "trade secret". Direct

cooperation with people from turtle-bearing prov-

inces, however, can help determine the distributions

of these rare turtles.

1999

Asiatic Herpetological Research

Vol. 8, p. 113

Figure 2. A) Ventral view of Cuora pani (male) from

northern Sichuan Province (photo by Ermi Zhao). B)

Lateral view of same individual (Photo by JFP).

Acknowledgments

We would like to thank Ermi Zhao for introducing the

authors and facilitating their collaboration. Yuezhao

Wang and Zhijun Liu provided critical assistance

regarding the acquisition and accession of CIB-

9910544. Ron de Bruin and Arie van der Meijden sup-

plied useful information on the synonymy of Cuora

pani and C. chriskarannarum. Karen Klitz created the

map for Fig. 1 and Ted Papenfuss gave editorial assis-

tance. We thank Jim Buskirk for his help and advice

along the way. Funding was provided by the Vice

Chancellor's Fellowship of the University of Califor-

nia and Grant # STZ-1-02 of the Chinese Academy of

Sciences.

Literature Cited

Boulenger, G. A. 1906. Descriptions of new reptiles

from Yunnan. The Annals and Magazine of Natural

History 7(17):567-568.

Buskirk, J. R. 1989. New locality records for Chinese

non-marine chelonians. Chinese Herpetological

Research 2:65-68.

de Bruin R. 1988 Twee nieuwe Cuora-soorten uit

China. Lacerta 47:4-6

Ernst C. H. and W. P. McCord. 1987. Two new turtles

from southeast Asia. Proceedings of the Biological

Society of Washington 100(3):62 4-628.

Iverson, J. B. 1992. A revised checklist with distribu-

tion maps of the turtles of the world. Green Nature

Books, Homestead, FL. 363 pp.

Luo B. and Y Zong. 1988. A new species of Cuora-

Cuora aurocapitata. Acta Herpetologica Sinica 3:13-

15. (In Chinese with English abstract)

McCord, W. P. and J. B. Iverson. 1991. A new box tur-

tle of the genus Cuora (Testudines: Emydidae) with

taxonomic notes and a key to the species. Herpetolog-

ica 47(4):407-420.

Stubbs, D. 1989. Tortoises and freshwater turtles: an

action plan for their conservation. IUCN/SSC Tortoise

and Freshwater Turtle Specialist Group, Canterbury,

England. 48 pp.

Pritchard, P. C. H. 1990. Review of: Turtles of the

World, by Carl H. Ernst and R. W. Barbour. Copeia

1990:602-607.

Song, M. T 1984. A new species of the turtle genus

Cuora (testudoformes: Testudinidae) Acta Zootaxc-

nomica Sinica 9(3):330-332. (In Chinese with English

abstract)

Zhao, E., T Zhou, and P. Ye. 1990. A new Chinese

box turtle (Testudinata: Emydidae )--Cuora zlioui. Pp.

213-216. In E. Zhao (ed.), From Water Onto Land.

Chinese Society for the Study of Amphibians and

Reptiles, Beijing. (In Chinese with English abstract)

1999 Asiatic Herpetological Rl Vol. 8, pp. 1 14-1 18

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Rastegar-Pouyani, Nasrullah. Two New Subspecies of Trapelus agilis Complex (Sauna:

Agamidae) From Lowland Southwestern Iran and Southeastern Pakistan 90

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TSV-PA, a Specific Plasminogen Activator from the Venom of Trimeresurus stejnegeri 107

Parham, James Ford, and Dong Li. A New Locality for Cuorapani Song 1984 with Comments

on its Known Range Ill

Guidelines for Manuscript Preparation and Submission 114

Colophon. Asiatic Herpetological Research is created using FrameMaker 5.5, Acrobat 4, and

Canvas 6 on Power Macintosh computers. The body text is set in Times Roman and the head-

ings in Helvetica. Using digital technology, we consumed less than 200 sheets of paper in the

prepress production of this issue.

ISSN 1051-3825

Al-Johany, Awadh M. The Activity and Thermal Biology of the Fossorial Reptile.

Diplometopon zarudnyi (Amphisbaenia: Trogonophiidae) in Central Saudi Arabia 1

Brown, Rafe M., Alan E. Leviton, and Rogelio V. Sison. Description of a New Species of

Pseudorabdion (Serpentes: Colubridae) from Panay Island, Philippines with a Revised Key to

the Genus 7

Das, Indraneil. Anguis melanostictus Schneider, 1801, a Valid Species of Barkudia

(Sauria: Scincidae) from Southeastern India 13

Das. Indraneil. The Dates of Publication of Amphibian and Reptile Names by Blanford and

Stoliczka in the Journal and Proceedings of the Asiatic Society of Bengal 18

Diong, C.H. and S.Y.T. Soon. Size and Shape Description of Oviductal Eggs of Draco

obscums formusus (Squamata: Agamidae) 25

Dolmen, Dag. Rudolf A. Kubykin and Jo V. Arnekleiv. Diel Activity of Ranodon sibiricus

(Amphibia: Hynobiidae) in Relationship to Environment and Threats 29

Guo, Peng, Fu-ji Zhang, and Yue-ying Chen. The Hemipenes of Chinese Species of

Deinagkistrodon and Gloydius (Serpentes: Crotalinae) 38

Guo. Peng. Fu-ji Zhang, and Yue-ying Chen. Catalogue of Type Specimens of Reptiles in the

Herpetological Collections of Chengdu Institute of Biology, the Chinese Academy of Sciences

43

Jaafar, Ibrahim H., Ahmad Ismail, and Abd-rahman Kurais. Correlations of Reproductive

Parameters of Two Tropical Frogs from Malaysia 48

Jil, Xiang, Ping-yue Sun, Shui-yu Fu, and Hua-Song Zhang. Utilization of Energy and

Material in Eggs and Post-hatching Yolk in an Oviparous Snake, Elaphe taeniura 53

Khan, Muhammad S. and Herbert Rosier. Redescription and Generic Redesignation of the

Ladakhian Gecko Gymnodactylus stoliczkai Steindachner, 1969 60

Kolbintzev, Vladimir. Larissa Miroschnichenko. and Tatjana Dujsebayeva. Distribution and

Natural History of the Lidless Skinks, Asymblepharus alaicus and Ablepharus deserti (Sauria:

Scincidae) in the Aksu-Djabagly Nature Reserve (Western Tian-Shan Mountains), Kazakstan

69

Mao, Wei-ping and Zhao-xian Wang. Seasonal Variations of Testicular and Epididymal

Structure and Plasma Levels of Testosterone in the Soft-shelled Turtle (Pelodiscus sinensis)

75

Niu, Cuijuan, Tingjun Zhang and Ruyong Sun. Food Consumption and Growth of Juvenile

Chinese Soft-shelled Turtles {Pelodiscus sinensis) in Relation to Body Weight and Water

Temperature 81

Rastegar-Pouyani. Nasrullah. First Record of the Lacertid Acanthodactylus boskianus (Sauria:

Lacertidae) for Iran 85

(Continued on inside of back cover)

Rastegar-Pouyani, Nasrullah. Two New Subspecies of Trapelus agilis Complex (Sauna:

Aeamidae) From Lowland Southwestern Iran and Southeastern Pakistan 90

*&*•

Tre'panier, Tanya L., Amy Lathrop, and Robert W. Murphy. Rhacophorus leucomystax in

Vietnam with Acoustic Analyses of Courtship and Territorial Calls 102

Zhang, Yun, Wen-hui Lee, Yu-liang Xiong, and Wan-yu Wang. Immuno-chemical Study of

TSV-PA, a Specific Plasminogen Activator from the Venom of Trimeresurus stejnegeri 107

Parham, James Ford, and Dong Li. A New Locality for Cuorapani Song 1984 with Comments

on its Known Range Ill

Guidelines for Manuscript Preparation and Submission 114

Colophon. Asiatic Herpetological Research is created using FrameMaker 5.5, Acrobat 4, and

Canvas 6 on Power Macintosh computers. The body text is set in Times Roman and the head-

ings in Helvetica. Using digital technology, we consumed less than 200 sheets of paper in the

prepress production of this issue.

ISSN 1051-3825

Al-Johany, Awadh M. The Activity and Thermal Biology of the Fossorial Reptile,

Diplometopon zarudnyi (Amphisbaenia: Trogonophiidae) in Central Saudi Arabia 1

Brown, Rate M, Alan E. Leviton, and Rogelio V. Sison. Description of a New Species of

Pseudorabdion (Serpentes: Colubridae) from Panay Island. Philippines with a Revised Key to

the Genus 7

Das, Indraneil. Anguis melanostictus Schneider, 1 801 , a Valid Species of Barkudia

(Sauna: Scincidae) from Southeastern India 13

Das, Indraneil. The Dates of Publication of Amphibian and Reptile Names by Blanford and

Stoliczka in the Journal and Proceedings of the Asiatic Society of Bengal 18

Diong, C.H. and S.Y.T. Soon. Size and Shape Description of Oviductal Eggs of Draco

obscurus formosus (Squamata: Agamidae) 25

Dolmen, Dag, Rudolf A. Kubykin and Jo V. Arnekleiv. Diel Activity of Ranodon sibiricus

(Amphibia: Hynobiidae) in Relationship to Environment and Threats 29

Guo, Peng, Fu-ji Zhang, and Yue-ying Chen. The Hemipenes of Chinese Species of

Deinagkistrodon and Gloydius (Serpentes: Crotalinae) 38

Guo, Peng, Fu-ji Zhang, and Yue-ying Chen. Catalogue of Type Specimens of Reptiles in the

Herpetological Collections of Chengdu Institute of Biology, the Chinese Academy of Sciences

43

Jaafar, Ibrahim H., Ahmad Ismail, and Abd-rahman Kurais. Correlations of Reproductive

Parameters of Two Tropical Frogs from Malaysia 48

Jil, Xiang, Ping-yue Sun, Shui-yu Fu, and Hua-Song /hang. Utilization of Energy and

Material in Eggs and Post-hatching Yolk in an Oviparous Snake. Elaphe taeniura 53

Khan, Muhammad S. and Herbert Rosier. Redescription and Generic Redesignation of the

Ladakhian Gecko Gymnodactylus stoliczkai Steindachner. 1969 60

Kolbintzev, Vladimir, Larissa Miroschnichenko. and Tatjana Dujsebayeva. Distribution and

Natural History of the Lidless Skinks, Asymblepharus alaicus and Ablepharus deserti (Sauna:

Scincidae) in the Aksu-Djabagly Nature Reserve (Western Tian-Shan Mountains), Kazakstan

69

Mao, Wei-ping and Zhao-xian Wang. Seasonal Variations of Testicular and Epididymal

Structure and Plasma Levels of Testosterone in the Soft-shelled Turtle (Pelodiscus sinensis)

75

Niu, Cuijuan, Tingjun Zhang and Ruyong Sun. Food Consumption and Growth of Juvenile

Chinese Soft-shelled Turtles (Pelodiscus sinensis) in Relation to Body Weight and Water

Temperature 81

Rastegar-Pouyani, Nasrullah. First Record of the Lacertid Acanthodactylus boskianus (Sauria:

Lacertidae) for Iran 85

(Continued on inside of back cover)

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