HARVARD UNIVERSITY

Ernst Mayr Library

of the Museum of

Comparative Zoology

May

°3 2®

Volume 10 • 2004

Editor

Er-Mi Zhao

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

Associate Editors

Raul E. Diaz

Museum of Vertebrate Zoology, University of

California, Berkeley, California, USA

J. Robert Macey

Joint Genome Institute, Walnut Creek, California, USA

Theodore J. Papenfuss

Museum of Vertebrate Zoology, University of

California, Berkeley, California, USA

James F. Parham

Joint Genome Institute, Walnut Creek, California, USA;

Museum of Paleontology, University of California,

Berkeley, California, USA

Editorial Board

Robert F. Inger

Field Museum, Chicago, Illinois, USA

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 Institute, St. Petersburg, Russia

Bihui Chen

Anhui Normal University, Wuhu, Anhui, China

l-Jiunn Cheng

Institute of Marine Biology, National Taiwan Ocean University,

Keelung, Taiwan, China

Ilya Darevsky

Zoological Institute, St. Petersburg, Russia

Indraneil Das

Madras Crocodile Bank, Vadanemmeli Perur, Madras, India

William E. Duellman

University of Kansas, Lawrence, Kansas, USA

Hajime Fukada

Sennyuji Sannaicho, Higashiyamaku, Kyoto, Japan

Carl Gans

University of Michigan, Ann Arbor. Michigan, USA

Xiang Ji

Hangzhou Normal College, Hangzhou, Zhejiang, China

Pi-peng Id

Yantai Normal College, Yantai, Shandong, China

Robert W. Murphy

Royal Ontario Museum, Toronto, Ontario. Canada

Goren Nilson

University of Goteborg, Goteborg. Sweden

Nikolai Orlov

Zoological Institute, St. Petersburg, Russia

Hidetoshi Ota

Department of Biology, University of the Ryukyus, Nishihara,

Okinawa, Japan

Soheila Shafii

University of Shahid Bahonar, Kerman, Iran

Hai-tao Shi

Hainan Normal University, Haikou. Hainan, China

Xiu-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, Jiangsu. China

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

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Asiatic Herpetological Research Volume 10 succeeds Volume 9 (2001), Volume 8 (published in 1999), Vol. 7 (1997), Vol.6 (1995), Vol.5 (1993),

Vol. 4 (1992), Vol. 3 (1990), and Chinese Herpetological Research Vol. 2, which was published at the Museum of Vertebrate Zoology. 1988-1989.

as the journal for the Chinese Society for the Study of Amphibians and Reptiles. Volume 2 succceeded Chinese Herpetological Research 1987.

published for the Chengdu Institute of Biology by the Chongqing Branch Scientific and Technological Literature Press, Chongqing, Sichuan.

China. Acta Herpetologica Sinica ceased publication in June, 1988.

Cover: The cover image is of Gonocephalus chamaeleontinus from Pulau Tioman, Pahang, West Malaysia. Photo by L. Lee Grismer.

2004

Asiatic Herpetological Research

Vol. 10, pp. 1-7

A New Species of Dibamuc (Squamata: Dibamidae) from West Malaysia

Raijl E. Diaz1’2’*, Ming Tzi Leong3, L. Lee Grismer1, and Norsham S. Yaakob4

MCZ

i 1 IRRAF

Department of Biology, La Sierra University, Riverside, CA 925/5-8247, USA

~ Museum of Vertebrate Zoology’, University of California, Berkeley, CA 94 720, USA

* Corresponding author E-mail: rauldiaz1 a herkeley.edu

Department of Biological Sciences, National University of Singapore, Kent Ridge,

ir. \ / CT w ?C

Singapore 119260, Republic of Singapore

4 Forest Research Institute Malaysia, Kepong, 52109 Kuala Lumpur, Malaysia

Abstract. - A new lizard of the genus Dibamus is described from Pulau Tioman and Pulau Tulai, Pahang, West

Malaysia. This species most closely resembles D. novaeguineae, D. kondaoensis, D. leucurus and D. montanus , but

differs from all congeneric species in exhibiting the following combination of characters: postoculars 1, scales bor-

dering first infralabial 4, SVL 123 mm, 25-26 midbody scale rows, frontonasal and rostral sutures complete, and the

presence of slightly posteriorly notched cycloid body scales as an adult.

Key words. - Dibamus, Dibamus tiomanensis , new species, Dibamidae, Pulau Tioman, West Malaysia.

Introduction

The genus Dibamus presently contains 18 species (see

Greer, 1985; Darevsky, 1992; Das, 1996; Honda et al.,

1997; Ineich, 1999; Honda et al., 2001; Das and Lim,

2003; Das and Yaakob, 2003), a two-fold difference

from the detailed review of the group by Greer (1985).

Species of the genus Dibamus collectively range

throughout southeast Asia, from southern China and the

Philippines through Indonesia. Dibamus alfredi was

described by Taylor (1962) from Thailand. D. alfredi

were later found on the island of Nias, off the west coast

of Sumatra (Greer, 1985) and from Danum Valley in

Sabah State, Borneo (Tan, 1993; Das and Yaakob, 2003).

A large gap was then left between Thailand and Borneo.

Lim and Lim (1999) reported D. cf. alfredi from Pulau

Tioman. Upon examination of their specimen, one from

Pulau Tioman, and another from P. Tulai, we conclude

that these specimens constitute a new species described

herein. Pulau Tioman lies between longitudes 104° 7' to

104° 15' E and latitudes 2° 44' to 2° 54' N (Bullock and

Medway, 1966). Finding another endemic population on

this island provides another reason for its conservation

as well as further studying its rich herpetofauna.

Material and Methods

Single females from both Pulau Tulai and Pulau Tioman

were collected, fixed in 10% formalin, and preserved in

70% ethanol. Both specimens were deposited in the

Zoological Reference Collection (ZRC) at the Rattles

Museum of Biodiversity Research. Sliding calipers were

used for all length measurements. Terminology used fol-

lows Greer (1985) and Honda et al. (1997). Individuals

were sexed externally under a dissecting microscope:

males were identified by having two small, flap-like

limbs (one on each side of the vent) (Dumeril and

Bibron, 1839).

Taxonomy

Dibamus tiomanensis , new species

Figs. 1, 2

Holotype. - ZRC. 2. 34 10, adult male collected at

Kampung Paya, Pulau Tioman, Pahang, West Malaysia

(Fig. 2) on 16 September 1995.

Paratypes. - Adult female (ZRC 2.5092) collected along

the trail to Bukit Bakau, Pulau Tulai, West Malaysia

(Fig. 2) collected 14 July 2001. Juvenile female

(ZRC. 2. 5260) collected along the Tekek-Juara Cross

Island Trail, Pulau Tioman, West Malaysia collected 1 1

July 2001.

Diagnosis. - Dibamus tiomanensis differs from all other

species of Dibamus in having cycloid scales which are

slightly notched posteriorly as an adult and flat cycloid

light brown dorsal scales with cream borders as a juve-

nile. It also differs from other Dibamus in having the fol-

lowing combination of characters: rostral sutures incom-

plete; nasal and labial sutures complete; scales bordering

posterior edge of first infralabial 4; postocular 1; trans-

verse scale rows just posterior to head 29, at midbody

25, proximally anterior to vent 21; subcaudals 45; snout

blunt in lateral profile (Fig. 1; Table 1); presacral verte-

brae 124; postsacral vertebrae 23 (Table 3).

Vol. 10, p. 2

Asiatic Herpetological Research

2004

Figure 1 . Photograph of Dibamus tiomanensis, new species, on forest leaf litter.

Description of holotype. - Snout-vent length 92.5 mm;

tail length 13.1 mm; midbody diameter 2.5 mm. Snout

bluntly rounded; nostril lateral; rostral pad with large

number of evenly distributed sensory papillae; rostral

sutures incomplete; nasal sutures complete from nostril

Figure 2. Lateral (A), dorsal (B), and ventral (C) view of

head of Dibamus tiomanensis , new species, (f: frontal,

fn: frontonasal, ip: interparietal, if: first infralabial, I: labial

suture, m: mental, n: nasal suture, o: ocular, po: postoc-

ular, si: supralabial)

to ocular; labial sutures complete from anterior part of

nasal suture to mouth; frontonasal six times wider than

long; frontal approximately 1.05 times wider than fron-

tonasal; interparietal bordered posteriorly by four slight-

ly smaller nuchal scales; postocular one; supralabial

one; scales bordering posteromedial edge of first infral-

abaial four; ear opening absent; eyes dimly visible

through ocular; body scales notched posteriorly; trans-

verse scale rows just posterior to head 23, at midbody

25, at just anterior to vent 23; subcaudals 50; tip of tail

blunt, not terminating in a spine; hind limb length 2.6

mm.

Description of paratypes. - The paratypes (both

females) are similar to the holotype in all aspects except

the following: transverse scale rows posterior to head

29, transverse scale rows anterior to vent 2 1 and 22, and

subcaudals 45 and 48.

Variation. - Paratype ZRC.2.5260 is the only juvenile.

It shows a possible ontogenetic change in scale mor-

phology. Juveniles have cycloid, flat, and light brown-

cream bordered scales. Adults have posteriorly notched

brown scales.

Color in life. - Adults have a brown ground color both

dorsally and ventrally, except on the snout and jaws

which are a lighter shade of brown. Juveniles have a

cream-colored snout and jaws which contrast well with

the darker spotted sensory papillae and body scales

which are light-brown bordered with cream. Manthey

and Grossman (1997:205) present a color photograph of

the holotype.

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Asiatic Herpetological Research

Vol. 10, p. 3

Table 1. Comparison of several scale characters and measurements within Dibamus. The size of the frontal is meas-

uied relative to the frontonasal and the interparietal relative to the surrounding anterior body scales. Sample sizes for

postoculars and scales on posterior edge of infralabials are given in parentheses. Entries for midbody scale rows and

subcaudal scales are as follows from top to bottom: range, mean, and sample size (modified from Greer, 1985). (*= 1

& 3 refer to 1 scale present on the left infralabial and 3 on right; **=tail regenerated; *** = text in Das and Yaakob (2003)

mentions 3 scales bordering the infralabials in diagnosis, whereas 4 scales are mentioned in description of holotype).

Vol. 10, p. 4

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2004

Table 1. Continued.

Figure 3. Map of Southeast Asia showing the distribution

of known Dibamus tiomanensis specimens. (1) Trail to

Bukit, Pulau Tulai, (2) Tekek-Juara Cross island trail on

Pulau Tioman (from Kg. Tekek to Kg. Juara)

Etymology. - This species is named after the type local-

ity for the holotype (Pulau Tioman = Tioman Island)

Distribution. - Endemic to Pulau Tioman and adjacent

Pulau Tulai (Fig. 2).

Comparisons. - Dibamus tiomanensis was listed as D.

cf. alfredi owing to its geographic proximity to D. alfre-

di , which occurs in Peninsular Malaysia and Thailand

(Manthey and Grossman, 1997; Taylor 1963). The pres-

ence of four scales bordering the first infralabial posteri-

orly differentiates the new species, Dibamus tiomanen-

sis, from D. bogadeki, D. booliati , D. bourreti , D. dehar-

vengi, D. greeri , D, ingeri, D. kondaoensis, D. mon-

tanus, D. smithi, D. somsaki, and D. vorisi. In having

one post ocular present, D. tiomanensis differs from D.

alfredi, D. celebensis, D. novaeguineae, D. seramensis,

and D. taylori. From the remaining two congeners, D.

i 1 i i

1 mm 1 mm

Figure 4. Lateral (A), dorsal (B), and ventral (C) view of

heads of Dibamus alfredi (left) and Dibamus

novaeguineae (right). Figures from Greer (1985). [f:

frontal, fn: frontonasal, ip: interparietal, if: first infralabial,

I: labial suture, m: mental, n: nasal suture, o: ocular, po:

postocular, si: supralabial]

tiomanensis differs from D. montanus Smith, 1921

(Langbian Plateau, Vietnam) in having more pre-sacral

vertebrae (124 vs. 112-114) and D. leucurus (Bleeker,

1860) (Sumatra, Borneo) in the presence of slightly pos-

teriorly notched cycloid scales as an adult.

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Asiatic Herpetological Research

Vol. 10, p. 5

Table 2. Matrix of diagnostic characters and their states for species of Dibamus (modified from Greer, 1985).

* = See Table 1 for information on this character state.

D. nicobaricum is included in this study following

Das' ( 1 996) redescription and reevaluation of the species

(in which it is inaccurately referred to as D. nicobaricus

through parts of the paper) despite Honda et al. (2001)

avoidance of it's recognition as a nominate species.

Great difficulty arises in finding specimens of

Dibamus for study due to their fossorial lifestyle. As a

result, many descriptions are based on 2-5 individuals.

An unusually large collection of D. novaeguineae from

Mt. Canlaon, Negros Island, Philippines (Greer,

1985:150) has given a unique insight to how variable

morphological characters can be within a single popula-

tion (See Table 1). Further studies are needed in study-

ing variation within this family as slight character state

variances have warranted the recognition of new species

[See Das and Lim (2003), Das and Yaakob (2003), and

this paper] which may prove to be a variant of an already

described taxon.

Vol. 10, p. 6

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2004

Table 3. Sacral vertebrae count of described species of

Dibamus.

Natural History

The holotype was found under a large stone in Kampung

Paya, Pulau Tioman. ZRC 2.5092 was found beneath

leaf litter in loose dirt adjacent to a large rock and bam-

boo stands in secondary forest along the trail to Bukit

Bakau on Pulau Tulai at 20 m elevation. ZRC.2.5260

was found beneath a decaying log one meter from the

cross-island trail in primary forest on Pulau Tioman.

Adult Dibamus tiomanensis displayed a behavior

most likely intended to ward off a predator. When

picked up or startled, the body scales flare up at an angle

almost perpendicular to the body. When viewed, the

smooth surface appears rugose, resembling the bristle-

covered epidermis of an earthworm. It is possible that a

non-palatable species of worm exists in the same area

and has served as a model for D. tiomanensis to mimic.

Darevsky (1992) mentions that D. greeri has bright blue

rings on its body, perhaps mimicking a megascolicid

worm inhabiting the same leaf litter. Such mimicking

behavior was also recently reported in D. booliati (Das

and Yaakob, 2003).

Acknowledgments

We thank Mr. Sahir bin Othman, Director of Wildlife,

Perhilitan, for permission to conduct fieldwork in the

Seribuat Archipelago and Peter Ng, Chang Man Tang

and Kelvin Kok Peng Lim for the loan of specimens. We

also thank Allen Greer and Ted Papenfuss for reviewing

the manuscript. We especially thank Indraneil Das for

his significant contribution to the manuscript and for

providing sacral counts. We would also like to thank all

the students of Tropical Field Biology 487e from La

Sierra University who provided field assistance, and

Karen Klitz for her help with Fig. 2.

Literature Cited

Bullock, J. A. and L. Medway. 1966. Observations on

the Fauna of Pulau Tioman and Pulau Tulai:

General Introduction. Bulletin of the National

Museum, Republic of Singapore. No. 34, March

1966.

Darevsky, I. S. 1992. Two new species of worm-like

lizard Dibamus (Sauria: Dibamidae) with remarks

on the distribution and ecology of Dibamus in

Vietnam. Asiatic Herpetological Research 4:1-12

Das, I. 1996. The validity of Dibamus nicobaricum

(Fitzinger in Steindaehner, 1867) (Squamata:

Sauria: Dibamidae). Russian Journal of

Herpetology3(2): 157-162

Das, I. and K. K. P. Lim. 2003. Two new species of

Dibamus (Squamata: Dibamidae) from Borneo.

Raffles Bulletin of Zoology 51(1): 137-141 .

Das, I. and N. Yaakob. 2003. A new species of Dibamus

(Squamata: Dibamidae) from Peninsular Malaysia.

Raffles Bulletin of Zoology 51(1): 143- 147

Greer, A. E. 1985. The relationships of the lizard gen-

era Anelytropsis and Dibamus. Journal of

Herpetology 19:116-156.

Honda, M. and J. Nabhitabhata, H. Ota., T. Hikida.

1997. A new species of Dibamus (Squamata:

Dibamidae) from Thailand. Raffles Bulletin of

Zoology 45(2):275-279

Honda, M., H. Ota, T. Hikida, and I. S. Darevsky 2001.

A new species of the worm-like lizard, Dibamus

Dumeril & Bibron 1839 (Squamata Dibamidae),

from Vietnam. Tropical Zoology 14:119-125.

Ineich, I. 1999. Une nouvelle espece de Dibamus

(Reptilia: Squamata: Dibamidae) du Vietnam.

Bulletin de la Societe zoologique de France 124

(3):279-286

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Vol. 10, p. 7

Lim, K. P and L. J. Lim. 1999. The terrestrial herpeto-

fauna of Pulau Tioman, Peninsular Malaysia.

Raffles Bulletin of Zoology 6:131-155.

Manthey, U. and W. Grossmann. 1997. Amphibien &

Reptilien Siidostasiens. NTV Verlag, Munster, 512

pp.

Taylor, E. H. 1962. New oriental reptiles. University of

Kansas Science Bulletin 44( 14):687- 1 077

Taylor, E. H. 1963. The lizards of Thailand. University

of Kansas Science Bulletin 44:687-1077.

2004

Asiatic Herpetological Research

Vol. 10, pp. 8-

A New Species of Leptolalax (Anura: Megophryidae) from

Pulau Tioman, West Malaysia

L. Lee Grismer, Jesse L. Grismer, and Timothy M. Youmans

Department of Biology, La Sierra University, Riverside, CA 92515-8247

Abstract. - A new species of Leptolalax is described from a cave at the top of Gunung Kajang, Pulau Tioman, Pahang,

West Malaysia. It differs from all other Malaysian species of Leptolalax in several aspects of coloration and in hav-

ing smooth as opposed to rough or pebbled skin on the dorsum.

Key words. - Leptolalax , Anura, Tioman, Malaysia.

Introduction

There are at least eight species of Leptolalax found

throughout West Malaysia and Borneo (Berry, 1975;

Inger et al., 1995; Inger et al., 1997; Matsui, 1997) but

only one of these, L. gracilis, is known from both

regions. In an unpublished document, Day (1990)

reported Leptobrachium sp. from Pulau Tioman,

Pahang, West Malaysia based on five larvae collected in

the Tengkuk Air Cave (Gua) at 1000 m elevation on

Gunung Kajang. Lim and Lim (1999) referred these lar-

vae to Leptolalax gracilis based on three additional lar-

vae they collected at a lower elevation (ca. 400 m) on

Gunung Kajang. More recently, Grismer et al. (2004)

reported two adults from Gua Tengkuk Air.

Examination of those adults indicates that they belong to

the genus Leptolalax not Leptobrachium (but they are

not L. gracilis). We therefore, refer these specimens and

the larvae of Lim and Lim (1999) to the new species

described herein.

Materials and Methods

The following measurements were made with sliding

calipers to the nearest 0. 1 mm: adults; snout-vent length

(SVL), tibial length (TL), head width (HW), head length

(HL), and diameter of tympanum (TYM). Tadpoles

(Table 1); interorbital distance (IOD), intemarial dis-

tance (IND), tail length (TL), and tail height (TH).

Tadpoles were preserved in 10% formalin and trans-

ferred to 70% ethanol. Due to shrinking and wrinkling,

head-body width (HBW), head-body height (HBH), and

tail height (TH) are likely to be underestimated.

Observations on external morphology were made with

the use of a dissecting microscope. Specimens were

compared to material listed in Appendix I and descrip-

tions in Berry (1975), Inger (1985), Inger et al. (1997),

Inger et al. (1995), Inger and Stuebing (1997), Malkmus

(1992), and Matsui (1997).

Leptolalax kajangensis , new species

(Figs. 1-2)

Holotype. - ZRC 1.7714; adult male, 34.0 mm SVL;

found inside Gua Tengkuk Air, Gunung Kajang, Pulau

Tioman, Pahang, West Malaysia at 1000 m in elevation.

Collected by Jesse L. Grismer and Timothy M. Youmans

on 21 July, 2001.

Paratype. - ZRC 1.7715; adult male, 35.0 mm SVL.

Same data as holotype.

Diagnosis. - Leptolalax kajangensis differs from all

other Malaysian species of Leptolalax in lacking distinct

dark crossbands on the limbs and having a generally

dark, unicolor to weekly patterned dorsum. It differs fur-

ther from L. arayai, L. dringi, L. gracilis, L. hamidi, and

L. maurus, in having smooth, as opposed to rough, warty

skin. It differs further from L. dringi, L. gracilis, and L.

heteropus in lacking dark spots on the ventrum. It dif-

fers further from L. gracilis and L. hamidi in lacking a

dark inguinal blotch and from L. gracilis in lacking a

distinctly bicolored forelimb and dark markings on the

ventral surface of the foreleg.

Description of holotype. - Habitus moderately slender,

head longer than wide; snout rounded in dorsal profile,

weakly projecting beyond lower jaw; nostrils raised,

directed dorsolaterally, and situated on canthi, near tip of

snout; canthi rounded; lores slightly oblique; eye large,

diameter slightly longer than length of snout; intemarial

distance less than interorbital distance; interorbital width

slightly greater than length of snout; tympanum visible,

less than one-half diameter of eye, separated from eye

by width of tympanum; vomerine teeth absent; tongue

notched, without papillae.

Forelimbs slender; fingers slender, unwebbed, tips

rounded; first finger equal in length to second; no subar-

ticular tubercles or elongate comified pads visible

beneath fingers; large inner palmar tubercle present and

Vol. 10, p.9

Asiatic Herpetological Research

2004

Figure 1. Photograph of Leptolalax kajangensis , new

species, on forest leaf litter.

much smaller outer palmar tubercle at base of fourth

digit.

Hindlimbs relatively short; heels overlap when

limbs flexed; tibiotarsal articulation of adpressed limb

reaches tip of snout; tips of toes rounded; third and fifth

toe equal in length; slight webbing between first and

second and second and third toes only; oval inner

metatarsal tubercle present; subarticular tubercles

absent.

Skin on back smooth to faintly pebbled; flanks

faintly pebbled; limbs smooth to faintly pebbled; promi-

nant supratympanic fold extending from eyelid to shoul-

der; ventral surfaces smooth.

Coloration. - In life and ethanol, dorsal surfaces almost

black with no visible pattern except for minute, faint,

light-colored spots; limbs slightly lighter with faint dark

mottling; faint dark mottling on flanks blending to gray-

ish dusty ventral surfaces punctated by minute gray

spots. Supratympanic fold darker than dorsum. Iris

metallic gold in life.

Measurements of holotype. - SVL 34.0 mm; TL 14.2

mm; HW 18.5 mm; HL 10.0 mm; TYM 1.6 mm.

Variation. - The paratype closely approximates the

holotype in all aspects of coloration and morphology. It

differs in the following measurements: SVL 35.0 mm;

TL 14.6 mm; HW 19.4 mm; HL 9.4 mm TYM 1.8 mm.

Etymology. - This species is named after the type local-

ity of Gunung Kajang, Pulau Tioman, West Malaysia

Tadpoles. - Table 1 lists measurements, growth stages,

and tooth row formulae of tadpoles. Based on specimens

(ZRC 1.3339-41); stages 30, 36, and 37 (Gosner, 1960)

from a small stream at 333 m below Gua Tengkuk Air on

G. Kajang and specimens (0051-54 uncatalogued spec-

imens in the British Museum reported by Day, 1990)

stage 30 (Gosner, 1960) from Gua Tengkuk Air. Head

and body relatively large and round; nostrils dorsally

located, closer to tip of snout than eye; eyes dorsolater-

al, not visible from below; spiracle sinistral, nearer to

eye than vent; vent dextral, opening at margin of ventral

fin; dorsal fin slightly deeper than ventral fin, not

extending onto head-body; fins not deeper than caudal

musculature; oral apparatus not emarginate; mouth sub-

terminal; bordered by a single row of conical papillae;

large submarginal papillae without denticles; jaw

sheaths black, robust, strongly arched, and finely serrat-

ed; upper jaw lacking medial notch; denticles small;

rows A1 and P5 markedly shorter than adjacent rows.

Tadpoles (ZRC. 1 .3339-41) from stream dusky brown

above with faint darker mottling; venter cream colored,

nearly immaculate; faint dark stippling on caudal fins,

edges clear and immaculate; lateral line hash marks dis-

tinct. Tadpoles from Gua Tengkuk Air (uncatalogued

BM specimens) lack pigment and are white to transpar-

ent in life.

Comparisons with other species. - Leptolalax kajan-

gensis differs from all other Malaysian species of

Leptolalax on the basis of skin surface texture and col-

oration. Leptolalax arayai , L. dringi , L. gracilis , L.

hamaidi , L. m auras , and L. pe/odvtoides all have coarse-

ly textured skin ranging from distinctive corrugations in

Table 1. Selected measurements (mm), growth stage (GS), and labial tooth row formulae (LTRF) of Leptolalax

kajangensis. Abbreviations follow Materials and Methods. * = Specimen damaged.

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Asiatic Herpetological Research

Vol. 10, p. 10

Figure 2. Tadploe of Leptolalax kajangensis at type local-

ity.

L. dringi to isolated tubercles of varying sizes in L. gra-

cilis (Inger and Stuebing, 1997; Inger et al. 1997;

Matsui, 1997). Leptolalax kajangensis resembles L. pic-

tus and L. pelodytoides in having smooth to weakly peb-

bled skin on the dorsum (Inger et al. 1995) but differs

from L. pictus in lacking small tubercles on its sides

(Malkmus, 1992). Leptolalax kajangensis falls within

the size range (SVL 34.0-35.0 mm) of L. dringi (SVL

30.0-38.8 mm), L. gracilis (SVL 31.0-48.0 mm), L. het-

eropus (SVL 33.0-35.0 mm), L. pelodytoides (SVL 30.0-

42.0 mm), and L. pictus (SVL 3 1 .0-47.0 mm) but is larg-

er than L. arayai (SVL 29.9) and L. mams (SVL 26.0-

32.0). Leptolalax kajangensis differs most notably from

other species in coloration. Its generally unicolor black

dorsal pattern contrasts sharply with the various mottled

body patterns of L. dringi , L. hamidi, L. heteropus , L

pelodytoides , and L. pictus. It does resemble L. maurus

to some extent in that L. maurus has a black unicolored

dorsum but differs in that the latter also has lighter col-

ored limbs with darker crossbars and light colored spots

on the flanks, patterns which are absent in L. kajangen-

sis. Leptolalax gracilis also has a generally dark dorsal

coloration with varying degress of dark mottling but is

distinctive in having a light colored brachium. The sin-

gle specimen of L. arayi has a light ground color with

darker crossbands on the limbs.

Natural history. - Both specimens of Leptolalax kajan-

gensis were found in a cave (Gua Tengkuk Air) near the

summit of Gunung Kajang at approximately 1000 m in

elevation. This subterranean, obliquely oriented cavern

is formed from the overhang of large boulders piled on

top of one another. It contains a small pond (3 m x 4 in)

drained by a small subterranean stream (1-3 m in width

by 2-4 cm in depth) running for 3-4 m along the cave

floor. Both specimens of L. kajangensis were observed

in the afternoon sitting on top of large rocks adjacent to

the stream approximately 10 m from the entrance to the

cave and approximately 10 m below the outside ground

level. It was from the subterranean pond that Day (1990)

collected "large tadpoles" he referred to as

Leptobrachium sp. We observed additional tadpoles and

assume these to be larvae of Leptolalax kajangensis

based on the fact that the type material were collected

from the same stream and adults were observed calling

from the edge of the pond.

Three additional larvae examined here

(ZRC. 1.3339-41) were collected from a lower stream on

Gunung Kajang at approximately 400 m on 26 June

1996 (Lim and Lim, 1999). We tentatively assign these

to Leptolalax kajangensis because they match the larvae

from Tengkuk Air in morphology (Table 1). However,

the Tengkuk Air specimens lack pigment and are white

to transparent in life (Fig. 2). ZRC. 1 .3339-41 are coun-

tershaded with dark pigment above and have minute

dark flecks on a light venter. This indicates that either L.

kajangensis is not confined to only the upper most ele-

vations of Gunung Kajang or that there may be an addi-

tional species of Leptolalax found lower down on the

mountain.

Biogeography. - Pulau Tioman had a land positive con-

nection with Peninsular Malaysia as late as the

Pleistocene (Voris, 2000). The presence of amphibian

species on Pulau Tioman such as Leptolalax kajangen-

sis, Megophrys nasuta , Rana hosii , R. picturata and oth-

ers that require streams with moderate to strong currents

for reproduction suggests these species are unlikely can-

didates for long distance dispersal over flat, low-lying

landscape (Inger and Voris, 2001). Pulau Tioman was

part of a large granitic arc of mountains extending from

what is currently peninsular Malaysia through the

Kepulauan Anambas and Natunas across the Greater

Sunda Shelf which provided a dispersal corridor for

montane species (Inger and Voris, 2001) across the flat,

low-lying exposed Sunda Shelf. Thus, the presence of

stream-breeding species requiring moderate to fast flow-

ing water on Pulau Tioman is most likely a result of vic-

ariance.

Acknowledgments

We thank Mr. Sahir bin Othman, Director of Wildlife,

PERHILITAN, for permission to conduct field work in

the Seribuat Archipelago. We thank Peter Ng and

Kelvin Lim of Raffles Museum of Biodiversity

Research (ZRC) and Harold Voris and Alan Resetar of

the Field Museum of Natural History (FMNH) for

allowing us to examine specimens in their care. For

comments on the manuscript we are grateful to R. F.

Inger and for field assistance we thank Geoff Powells.

Vol. 10, p. 11

Asiatic Herpetological Research

2004

Literature Cited

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

Malaysia. Tropical Press, Kuala Lumpur.

Day, M. 1990. Zoological research. In: Day, M. and T.

Mowbray (eds.). University of Bristol Tioman

Archipelago Expedition, Peninsular Malaysia,

1988, Final Report. Unpublished Report pp. 25-43.

Gosner, K. L. 1960. A simplified table for staging anu-

ran embryos and larvae with notes on identification.

Herpetologica 16:183-190.

Grismer, J. L., L. L. Grismer, I. Das, N. S. Yaakob, L. B.

Liat, L. T. Ming, T. M. Youmans, R. A. Sosa, and H.

Kaiser. 2004. Species diversity and checklist of the

herpetofauna of Pulau Tioman, peninsular Malaysia

with a preliminary overview of habitat utilization.

Asiatic Hereptological Reserch 10:247-279.

Inger, R. F. 1985. Tadpoles of the forested regions of

Borneo. Fieldiana Zoololgy. New Series No.26:l-

89.

Inger, R. F., M. Lakim, A. Biun, and P. Yambun, 1997.

A new species of Leptolalax (Anura:Megophryidae)

from Borneo. Asiatic Herpetological Reserach 7:48-

50.

Inger, R. F. and R. B. Stuebing, 1997. A Field Guide to

Frogs of Borneo. Natural History Publications,

Kota Kinabalau.

Inger, R. F., R. B. Stuebing, and F. L. Tan. 1995. New

species and new records of anurans from Borneo.

Raffles Bulletin of Zoology 43 : 1 1 5- 1 3 1 .

Inger, R. F. and H. K. Voris. 2001. The biogeographical

relations of the frogs and snakes of Sundaland.

Journal of Biogeography 28:863-891.

Lim, K. K. P. and L. J. Lim. 1999. The terrestrial her-

petofauna of Pulau Tioman, Peninsular Malaysia.

Raffles Bulletin of Zoology. Supplement 6:131-

155.

Malkmus, R. 1992. Leptolalax pictus, sp. nov. (Anura:

Pelobatidae) vom Mount Kinabalu/Nord-Borneo.

Sauria, Berlin 14:3-6.

Mastsui, M. 1997. Call characteristics of Malaysian

Leptolalax with a description of two new species

(Anura: Pelodatidae). Copeia 1997:158-165.

Voris, H. K. 2000. Maps of Pleistocene sea levels in

Southeast Asia: shorelines, river systems, time dur-

ations. Journal of Biogeography 27:1153-1167.

2004

Asiatic Herpetological Research

Vol. 10, pp. 12-16]

A New Species of Kukri Snake, Oligodon (Colubridae),

from Pulau Tioman, West Malaysia.

Tzi Ming Leong1 and L. Lee Grismer2

* Department of Biological Sciences, National University of Singapore, Singapore 119260

- Department of Biology, La Sierra University, Riverside, California 92515-8247, USA

Abstract. - A unique species of Oligodon is described from the type locality of Pulau Tioman, West Malaysia. In

terms of scalation, it is most comparable with the Bornean O. subcarinatus, but does not exhibit any feeble keeling

of scales. In addition, its body color and patterns are unique in having a red dorsum, pink ventral surface, and indis-

tinct pale bars on the nape and body.

Key words. - Oligodon , kukri snake, Pulau Tioman, West Malaysia.

Introduction

The kukri snakes belonging to the genus Oligodon Boie,

1827 are so named because of the presence of unique

posterior maxillary teeth, shaped like Ghurka kukri

knives. In addition, members belonging to this genus are

small to medium-sized ground dwelling species charac-

terised by having a large slightly upturned rostral shield,

short head, round pupil, and a cylindrical body with

smooth scales (Tweedie, 1983; Cox et al., 1998). Many

species possess a distinct dark chevron mark on the nape

and a stripe across the anterior part of the head and down

over/through the eye. Although Oligodon is well repre-

sented in South and Southeast Asia, there are only three

species on Peninsular Malaysia, namely O. octolineatus

Schneider, O. purpurascens Schlegel, and O. signatus

Gunther (Tweedie, 1983). In Borneo, eight species have

been recorded [O. annulifer Boulenger, O. cinereus

Gunther, O. everetti Boulenger, O. octolineatus

Schneider, O. purpurascens Schlegel, O. signatus

Gunther, O. subcarinatus Gunther, and O. vertebralis

Gunther]. However, the occurrences of true O. annulifer

and O. cinereus on Borneo remain to be verified

(Stuebing and Inger, 1999).

On Pulau Tioman, ca. 40 km from the southeast

coast of the peninsula, one species ( O . purpurascens)

has been reliably recorded thus far (Grismer et al., 2004;

Hendrickson, 1966). The presence of O. octolineatus on

the island, though possible, remains to be verified (Lim

and Lim, 1999). Day (1990: 38) reported the presence of

a distinct, new form of Oligodon from the cross-island

(Tekek-Juara) trail, but did not provide any diagnostic

characters. It was merely mentioned that this form

resembled O. signatus , but had differences in terms of

head scalation and dorsal colouration. We collected a

specimen from the same locality on 16 July, 2001 that is

different from all other nominal species of Malaysia and

is herein named and described as new.

Materials and Methods

Prior to preservation in 10% formaldehyde, the speci-

men was photographed and liver tissue sampled. Total

length, tail length, and snout-vent length were obtained

using a measuring tape (to nearest 1 mm). Additional

measurements taken, using vernier callipers (to nearest

0.1 mm), include eye diameter (ED); head length (HL),

taken from the union of the posteromedial comers of the

parietals to the tip of the snout; head depth (HD), taken

from the dorsal surface of the head to the ventral surface

of the jaw immediately posterior to the eye; and snout

length (SL), taken from the anterior margin of the eye to

the tip of the snout. The scale counts included upper

labials, number of upper labials in contact with eye,

lower labials, preoculars, postoculars, ventrals, subcau-

dals, and midbody scales. Comparative material was

examined from the Zoological Reference Collection

(ZRC) [Raffles Museum of Biodiversity Research

(RMBR), National University of Singapore], the

Department of Wildlife and National Parks, Peninsular

Malaysia (DWNP) herpetological collection, the Bishop

Museum, Hawaii (BPBM), and Museum fur

Naturkunde, Humboldt-Universitat, Berlin, Germany

(ZMB).

Oligodon booliati, sp. nov.

Holotype: ZRC.2.5153, adult female, collected on the

night of 16 July, 2001, at 2130 hrs by T. M. Leong and

K. M. Crane, while it was crawling on a concrete stair-

case in primary forest along the Tekek-Juara trail, ca.

150 m ash, Pulau Tioman (Pahang, Peninsular

Malaysia). Deposited at the Zoological Reference

Collection (ZRC).

Paratypes: (1) BPBM 13933, subadult male, collected

on 17 April 1962 by J. R. Hendrickson, at Ulu Lalang,

Asiatic Herpetological Research

2004

Vol. 10 p. 13

Figure 1. Dorsal view of Oligodon booliati holotype, ZRC.2.5153 (live coloration).

ca. 700 m asl and (2) ZMB 64446, adult female, collect-

ed in May 2001 by W. Grossmann and C. Scafer on the

top of the Tekek-Juara Trail at 300 in asl.

Diagnosis. - 6-7 upper labials, 2nd and 3 rd or 3rd and

4th touching eye, 7 lower labials, 17 mid-body scales,

143-153 ventrals, 54-60 subcaudals. Loreals present.

Head scales without distinct patterns. No distinct stripe

running through eye. In life, body deep maroon red dor-

sally and along flanks, salmon pink on the ventrals and

subcaudals. Ventrals without dark spots. Indistinct dark

brown transverse bars (19-22) on body, starting from

nape and fading increasingly towards tail. Thin, dark

brown stripes on anterior sides of 5th and 6th upper labi-

als, immediately posterior to eye.

Description of Holotype. - Adult female, total length:

510 mm, tail: 121 mm, snout-vent: 389 mm, ED: 2.2

mm, HL: 10.8 mm, HD: 6.9 mm, SL: 5.0 mm; head stout

(HD/HL 0.64), slightly broader than neck; snout moder-

ate, oblique in dorsal profile, oval in lateral profile; eye

20% of head length, pupil round; rostral shield large, tri-

angular, visible from above, width (3.5 mm) greater than

height (3.0 mm), concave below; rostral in direct contact

with first upper labials, nasals and internasals; trapezoid

prefrontals posterior to intemasals, curving at canthus

rostrals to meet triangular postnasals; single, almost tri-

angular frontal, slightly longer (4.8 mm) than wide (4.2

mm), posterior point terminating 1.2 mm beyond poste-

rior margin of eye; frontal flanked by prominent

supraoculars, length of supraocular (3.0 mm) 1 .4 of ED;

7 upper labials, increasing in size to 6th, 3rd and 4th in

contact with eye; a small (0.5 x 0.5 mm) loreal scale

present on left, but absent on right, allowing contact

between right prefrontal and 2nd upper labial; one preoc-

ular and one postocular present on both sides; 7 lower

labials, first pair elongated transversely, confining men-

tal to meet medially, 4th pair largest; anterior chinsh ields

longer than (almost double) posterior chinshields; 17

scale rows at neck and midbody, but 15 at one head

length anterior to vent; 143 ventrals, lateral margins vis-

ible from the sides; 59 subcaudals, all divided; anal

shield single. Colour in life deep maroon red on dorsum

and flanks (Fig. 1). Ventrals salmon pink, the colour

becoming increasingly intense towards the tail tip (Fig.

2), without any melanistic pigmentation. Head scales

without markings dorsally. Distinguishable grey-brown

pigmentation visible in other head scales: dorsal portion

of 4th upper labial (point of contact with eye), anterior

margins of 5th and 6th upper labials, anterior margins of

1st to 4th lower labials, in between anterior chinshields

towards the anterior, within mental, and lower surface of

rostral. Crossbars on body faint. 21 crossbars from nape

towards tail tip. Upon preservation, and storage in alco-

2004

Asiatic Herpetological Research

Vol. 10, p. 14

Table 1 Measurements, scale counts, and number of crossbars among Oligodon booliati sp. nov. type materials (holo-

type and two paratypes). L/R = Left/Right sides.

Figure 2. Ventral view of Oligodon booliati holotype,

ZRC.2.5153 (live colouration).

hoi, the colours gradually faded to a lighter shade. A lat-

eral view of the head is illustrated in Fig. 3.

Description of paratypes. - Rostral shield large, visible

from above. BPBM 13933 has 7 upper labials with the

3rd and 4th touching eye. ZMB 64446 has 6 upper labials

with the 2nd and 3rd touching the eye. Loreal scale (0.5

x 0.5 mm) present on both sides in BPBM 13933 and

fused to the postnasal on both sides in ZMB 64446 (1.0

x 1.0 mm). One preocular and one postocular. Seven

lower labials, 17 midbody scales, 146 ventrals, 60 sub-

caudals in BPMB 13933 and 153 ventrals and 54 sub-

caudals in ZMB 64446. First pair of infralabials separat-

ed medially by the mental in ZMB 64446. Total length

(BPBM 13933): 348 mm; tail: 88 mm; snout-vent: 260

i i

Figure 3. Lateral view of head (left side) of Oligodon boo-

liati holotype, ZRC.2.5153. Scale bar = 5mm.

mm. Total length (ZMB 64446): 373 mm; tail: 82 mm;

snout-vent: 291 mm. Anal shield single, subcaudals

paired. Colour in preservative faded to a cream colour.

No distinctly striking markings on head, faint crossbars

on body (22 in BPBM 13933, 19 in ZMB 64446).

Measurements and scale counts of type materials are

summarised in Table 1 .

Etymology. - This new species is named in honor of

Lim Boo Liat, of the Department of Wildlife and

National Parks (Peninsular Malaysia), whose contribu-

tions to our better understanding of Malaysia's natural

history dates back to the 1950's. Flis publications include

the description of a new snake ( Macrocalamus tweediei

Li in, 1963) and the popular reference book Poisonous

Snakes of Peninsular Malaysia (Lim, 1982).

Vol. 10 p. 15

Asiatic Herpetological Research

2004

Table 2. Comparisons between the Oligodon species (arranged alphabetically) of Peninsular Malaysia and Borneo,

including Oligodon booliati sp. nov. (measurements and scalations after Manthey & Grossmann, 1997). Lo = Loreal,

UL - Upper Labials, MB = Midbody, V = Ventrals, SC = Subcaudals.

Discussion

The number of upper labials (6-7) in Oligodon booliati

may be used to distinguish it from O. purpurascens (8)

and O. taeniatus (8), although O. annulifer and O.

cinerens may occasionally possess eight upper labials.

O. booliati shares the same number of midbody scales

(17) as O. octolineatus, O. signatus, and O. subcarina-

tus (instead of 15 in O. annulifer , O. everetti and O. ver-

tebral is) but may be distinguished from O. octolineatus

by the absence of any longitudinal stripes along the

body, from O. signatus by the presence of loreal scales,

and from O. subcarinatus by the lack of feeble keels on

its scales. This new species is assumed to be endemic to

Pulau Tioman. Comparisons of measurements and scala-

tion between O. booliati and the other species of

Oligodon in Peninsular Malaysia and Borneo are sum-

marised in Table 2.

Comparative Material Examined

Oligodon bitorquatus. - ZRC.2.3875, Bandung, West

Java; ZRC.2.3876, Gunong Hedjo, Cheribon, West Java;

ZRC.2.3957, Pengalengan, Java.

Oligodon octolineatus. - ZRC.2.2295, 2399, 2559,

3161, 3850, 3853-3855, 3859-3860, 3865, 5058,

Singapore; 3861, 3863-3864, Johor Bahru, Johor,

Peninsular Malaysia; 3862, 3867, Selangor, Peninsular

Malaysia.

Oligodon purpurascens. - ZRC.2.3869, Sumatra,

Indonesia; ZRC.2.3877-3879, Singapore; ZRC.2.3880-

3881, Pulau Gallang, Riau, Sumatra, Indonesia;

ZRC.2.3882, 3884, 3885, 3887, Johor, Peninsular

Malaysia; ZRC.2.3883, Forest Research Institute

Malaysia, Kepong, Selangor, Peninsular Malaysia;

ZRC.2.3886, 3888, Fraser's Hill, Pahang, Peninsular

Malaysia; Bishop Mus. 14211, Pulau Tioman.

Oligodon signatus. - DWNP.R.0005, Forest Research

Institute Malaysia, Kepong, Selangor, Peninsular

Malaysia; ZRC.2.4159, Bukit Asahan, Malacca,

Peninsular Malaysia; ZRC.2.3203, 3388, 3400, 3871-

3873, 3958, 4842, Singapore.

Oligodon taeniatus. - ZRC.2.4161, Bangkok, Thailand.

Acknowledgments

We are grateful to Sahir bin Othman (Perhilitan -

Department of Wildlife and National Parks, Peninsular

Malaysia), for permission to conduct research in the

Seribuat Archipelago; Lim Boo Liat (DWNP), Norsham

Yaakob (Forest Research Institute Malaysia), Karen M.

Crane (La Sierra University) for their enthusiastic and

active participation in the field; Karla H. Kishinami

(BPBM) and Wolfgang Grossmann (ZMB) for the loan

of specimens; Peter K. L. Ng and Kelvin K. P. Lim

(RMBR) for granting access to literature and specimens;

Robert B. Stuebing for examining the holotype and

reviewing the manuscript with encouraging rigour;

Robert F. Inger (FMNH) for critical and useful com-

ments which greatly improved the manuscript.

Literature Cited

Boie, F. 1827. Bemerkungen uber Merrem's Versuch

eines Systems der Amphibien, I. Lieferung:

Ophidier. - Isis van Oken, Jena, 20:508-566.

Cox, M. J., P. P. Van Dijk, J. Nabhitabhata and K.

Thirakhupt. 1998. A photographic guide to snakes

and other reptiles of Peninsular Malaysia,

Singapore and Thailand. New Holland. 144 pp.

2004

Asiatic Herpetological Research

Vol. 10, p. 16

Day, M. 1990. Zoological Research. In: Day, M. and T.

Mowbray (eds.). University of Bristol Tioman

Archipelago Expedition, Peninsular Malaysia,

1988, Final Report. Unpublished Report pp. 25-43.

Hendrickson, J. R., 1966. Observations on the fauna of

Pulau Tioman and Pulau Tulai. 5. The reptiles.

Bulletin of Natural History 34:53-71.

Grismer, J. L., L. L. Grismer, I. Das, N. S. Yaakob, L. B.

Liat, T. M. Leong, T. M. Youmans, and H. Kaiser.

2004. Species diversity and checklist of the herpeto

fauna of Pulau Tioman, Peninsular Malaysia, with a

preliminary overview of habitat utilization. Asiatic

Herpetological Research 10:247-279.

Lim, B. L. 1963. Macrocalamus tweediei, a new species

of Reed Snake from Malaya. Bulletin of the Nat.

Mus., Singapore 32:99-102, 1 Fig.

Lim, B. L. 1982. Poisonous snakes of Peninsular Malay-

sia. Second Edition, Malayan Nature Society in

association with Institute for Medical research,

Kuala Lumpur, 73 pp.

Lim, K. K. P. and L. J. Lim, 1999. The terrestrial her-

petofauna of Pulau Tioman. Peninsular Malaysia.

Raffles Bulletin of Zoology. Supplement No. 6:131-

155.

Manthey, U. and W. Grossmann. 1997. Amphibien und

Reptilien Siidostasiens. Natur und Tier-Verlag,

Matthias Schmidt, Munster. 511 pp.

Stuebing, R. B. and R. F. Inger, 1999. A field guide to the

snakes of Borneo. Natural History Publications

(Borneo), Kota Kinabalu, v + 254 pp.

Tweedie, M. W. F., 1983. The snakes of Malaya. 3rd

Edition. Singapore (National Printers Pte. Ltd.) 167

pp.

2004

Asiatic Herpetological Research

Vol. 10, pp. 17-21

A New Philautus (Amphibia: Rhacophoridae) from Northern Laos

Bryan L. Stuart1-’3’* and Harold F. Heatwole4

1 Field Museum oj Natural History, Department of Zoology, Division of Amphibians & Reptiles,

MOOS. Lake Shore Drive, Chicago, Illinois, USA 60605-2496;

•ji;

Corresponding author: E-mail: bstuart@fieldmuseum.org

-University of Illinois at Chicago, Department of Biological Sciences, 845 W. Taylor,

Chicago, Illinois, USA 60607-7060

^Wildlife Conservation Society, P.O. Box 6712, Vientiane, Laos

4 North Carolina State University, Department of Zoology, P.O. Box 7617, Raleigh,

North Carolina, USA 27695-7617; E-mail: harold heatwole@ncsu.edu

Abstract. - A new Philautus is described from Phou Dendin National Biodiversity Conservation Area in northern

Laos. Philautus petilus sp. nov. is most remarkable by having a very slender, elongate habitus. Other distinguishing

characteristics include having a tympanum diameter 80% of the eye diameter, white asperities on the dorsum, and

distinctive coloration consisting of a soft yellow-beige dorsolateral surface with broken black stripes posteriorly, a

lavender wash on dorsal surface of limbs, upper lip, and sides, a black stripe below edge of canthus extending from

snout tip to flanks near level of mid-body, and a black spot equal in diameter to the tympanum located just anterior

to the inguinal region.

Key words. - Laos, new species, Philautus , Rhacophoridae.

Introduction

Bourret (1942) remains the major work on the amphib-

ians of Laos, supplemented only recently by descrip-

tions of new species (Inger and Kottelat 1998; Stuart and

Papenfuss 2002). Consequently, the amphibian fauna of

Laos is imperfectly known.

From 6-26 October 1999, we conducted a herpeto-

faunal survey of Phou Dendin National Biodiversity

Conservation Area in eastern Phongsaly Province,

northern Laos, near to the tri-border area of Laos,

Vietnam, and China (Figure 1 A). The area surveyed was

mostly covered in hilly evergreen forest, sometimes

mixed with stands of natural bamboo, with small, rocky

streams flowing down hillsides into the larger, swift

Nam Ou and Nam Khang Rivers, at elevations from

600-1000 m. During the course of that work we found a

single, adult female specimen of an enigmatic, rha-

cophorid treefrog, which we describe here as a new

species of Philautus.

Materials and Methods

The single specimen found was caught in the field by

hand, preserved in 10% buffered formalin, and later

transferred to 70% ethanol. A tissue sample was taken by

preserving pieces of liver in 95% ethanol betoie the

specimen was fixed in formalin. The specimen was

deposited at the Field Museum of Natural History

(FMNH).

Measurements largely follow those of Bain et al.

(2003) and were made with dial calipers to the nearest

0.1 mm. Abbreviations used are: SVL = snout-vent

length; HDL = head length from tip of snout to the com-

misure of the jaws; HDW = head width at the commisure

of the jaws; SNT = snout length from tip of snout to the

anterior comer of the eye; EYE = eye diameter; IOD =

interorbital distance; TMP = horizontal diameter of tym-

panum; TEY = tympanum-eye distance from anterior

edge of tympanum to posterior comer of the eye; FPL =

length of finger 111 disk from the base of the pad to its

tip; FPW = width of finger 111 disc at the widest part of

the pad; TPL = length of toe IV disk; TPW = width of

toe IV disk. Measurement ratios are reported as percent-

ages (%) rounded to the nearest integer.

Philautus petilus. new species

(Figure IB)

Material examined. -Holotype: FMNH 257902, adult

female, collected by the authors on 23 October 1999 in

Phou Dendin National Biodiversity Conservation Area,

Phongsaly District, Phongsaly Province, Laos,

22°05,44,'N 102°08'10,,E, at 600 m elevation.

Diagnosis. - An elongate, slender Philautus having a

head width only 27% of SVL: tympanum diameter 80%

Vol. 10, p. 18

Asiatic Herpetological Research

2004

CHINA

VIETNAM

MYANMAR

LAOS

THAILAND

CAMBODIA

Figure 1 A-C. A. Map showing the type locality (black dot) of Philautus petilus sp. nov. in Phongsaly Province, north-

ern Laos. B. The adult female holotype (FMNH 257902) of Philautus petilus sp. nov., anesthetized prior to preserva-

tion. Photograph by Bryan L. Stuart. C. The hand of the adult female holotype (FMNH 257902) of Philautus petilus

sp. nov. in preservation. Photograph by Nikolai L. Orlov.

of eye diameter; white asperities on head, eyelids, back,

dorsal surface of tibia and forelimbs, and anterior half of

sides; no fringes, row of enlarged tubercles, or accesso-

ry flaps of skin on outer margins of limbs; black stripe

below edge of canthus extending from tip of snout to

flanks near level of mid-body; black spot slightly anteri-

or to inguinal region, equal in diameter to the tympa-

num.

Description of Holotype. - Habitus elongate, slender;

head width 27% of SVL; head slightly longer than wide;

snout obtusely pointed in dorsal view, projecting beyond

lower jaw, round in profile, not depressed; nostril later-

al, near tip of snout; canthus rounded but distinct, con-

stricted behind nostrils; lores slightly concave, oblique;

eye diameter less than snout length, interorbital distance

wider than upper eyelid; tympanum visible, not

depressed relative to skin of temporal region, tympanic

rim slightly elevated relative to tympanum, tympanum

diameter 80% of eye diameter; weak supratympanic fold

from eye to shoulder; vomerine teeth very small, in

oblique rows closer to choanae than to each other;

tongue deeply notched posteriorly.

Tips of all four fingers expanded, about two times

the width of phalanges, with circummarginal grooves,

width of finger I disc 60% the width of finger 111 disc,

width of finger III disc 71% the diameter of tympanum;

relative finger lengths I < II < IV < III; webbing absent;

fingers III and IV with large middle subarticular tuber-

cle and smaller palmar tubercle at base; fingers I and II

with large palmar tubercle at base.

Tips of toes expanded, width of toe IV disc slightly

smaller than width of finger III disc; toe V longer than

toe III; toe I webbing to midway between subarticular

tubercle and disc, continuing only as narrow fringe to

disc; toes II, III, and IV webbing to distal subarticular

tubercle, continuing only as narrow fringe to disc; toe V

webbing to midway between distal subarticular tubercle

and base of disc, continuing only as narrow fringe to

base of disc; inner metatarsal tubercle elongated, outer

metatarsal tubercle very small, almost inconspicuous.

Skin on dorsal and ventral surfaces smooth, except

for distinct, white asperities on head, eyelids, back, dor-

sal surface of tibia and forelimbs, and anterior half of

sides; no fringes, row of enlarged tubercles, or accesso-

ry flaps of skin on outer margins of limbs.

Left ovary with fewer than 25, developing, creamy-

white ova (color in preservative).

In life, top of head and back light brown with dark

brown reticulations and scattered black spotting; dorso-

lateral surface of head and body soft yellow-beige, with

short, broken black stripe on dorsolateral surface from

level of midbody extending toward groin; lavender wash

on dorsal surface of limbs, upper lip, and sides; black

stripe below edge of canthus extending from tip of snout

to anterior border of eye, and from posterior border of

eye along supratympanic fold to flanks near level of

mid-body; black spot slightly anterior to inguinal region.

2004

Asiatic Herpetological Research

Vol. 10, p. 19

equal in diameter to the tympanum; black ‘M’-shaped

marking over anus; black spot on tarsus closer to articu-

lation than foot, narrow black crossbars on hindlimbs,

some black flecking on forelimbs; venter creamy-white,

dark spotting on chin and throat, pigmentation on under-

side of hands, feet, and tibiotarsus. In preservative, yel-

low-beige and lavender coloration lost.

Measurements (mm) of holotype. - SVL 33.8; HDL

9.9; HDW 9.2; SNT 4.1; EYE 3.0; IOD 2.3; TMP 2.4;

TEY 1.5; FPL 1.5; FPW 1.7; TPL 1.3; TPW 1.4.

Comparisons. - The generic assignments of small, rha-

cophorid (or rhacophorine) treefrogs are uncertain and

debated (Bossuyt & Dubois 2001; Wilkinson et al.

2002). Therefore, we compare P petilus with all other

species of small to medium-sized rhacophorid (or rha-

cophorine) treefrogs having reduced finger webbing that

are reported from the vicinity of northern Laos, regard-

less of what genus they are currently referred to. These

include Chirixalus doriae Boulenger, C. hansenae

(Cochran), C. laevis (Smith), C. nongkhorensis

(Cochran), C. palpebralis (Smith), C. vittatus

(Boulenger), Philantus abditus Inger, Orlov, &

Darevsky, P. albopunctatus Liu & Hu, P banaensis

Bourret, P. carinensis (Boulenger), P. gracilipes

Bourret, P. gryllus Smith, P. jinxiuensis Hu, P. longchua-

nensis Yang & Li, P. maosonensis Bourret, P. menglaen-

sis Kou, P. ocellatus Liu and Hu, P. odontotarsus Ye and

Fei, P. parvulus (Boulenger), P. rhododiscus Liu and Hu,

Rhacophorus appendiculatus (Gunther), R. baliogaster

Inger, Orlov & Darevsky, R. bisacculus Taylor, R. verru-

cosus Boulenger, Theloderma asperum (Boulenger), and

T. stellatum Taylor (Bourret 1942; Taylor 1962; Inger et

al. 1999; Fei 1999; Orlov et al. 2002).

Philautus petilus differs from all species of

Chirixalus Boulenger by lacking the two outer fingers

appearing to be opposable to the two inner ones (present

in Chirixalus). Philautus petilus further differs from C.

doriae and C. nongkhorensis by lacking outer finger

webbing (outer fingers 1/3 webbed in doriae and

nongkhorensis), from C. hansenae, C. laevis and C. vit-

tatus by lacking light-colored dorsolateral stripes (pres-

ent in hansenae, laevis and vittatus), and from C. palpe-

bralis by lacking a yellow streak from below eye to

shoulder (present in palpebralis). Philautus petilus dif-

fers from P. abditus by having a visible tympanum (hid-

den in abditus) and lacking large black spots on the legs

(present in abditus). Philautus petilus differs from P

albopunctatus by having dorsal asperities (absent in

albopunctatus) and lacking white blotches on the snout,

dorsum and above anus (present in albopunctatus).

Philautus petilus differs from P. carinensis by having

the snout longer than the eye diameter (snout shorter

than eye diameter in carinensis) and by having a slender

habitus (stocky habitus in carinensis). Philautus petilus

differs from P gracilipes by having a head width 27% of

SVL (head width 45% of SVL in gracilipes), having the

width of finger III disc 71% the diameter of tympanum

(width of finger III disc equal to the diameter of tympa-

num in gracilipes), and lacking mostly green coloration

with dark-brown eyelids (present in gracilipes).

Philautus petilus differs from P. jinxiuensis by lacking a

large interorbital dark blotch extending posteriorly into

two broad, dark dorsolateral stripes (present in jinxiuen-

sis). Philautus petilus differs from P. longchuanensis by

having a tympanum diameter larger than width of finger

III disc (tympanum diameter smaller than width of fin-

ger III disc in longchuanensis). Philautus petilus differs

from P. maosonensis by having the head slightly longer

than wide (head wider than long in maosonensis ), by

having the snout projecting beyond the lower jaw (snout

not projecting beyond lower jaw in maosonensis), by

having the tympanum diameter 80% of eye diameter

(tympanum diameter approximately 2/3 eye diameter in

maosonensis), and by lacking a thin band between the

eyelids, a large dark marking on the back, and a dark

spot behind the axilla (present in maosonensis).

Philautus petilus differs from P. menglaensis by having

smooth skin with asperities on the dorsum (warty skin

on dorsum in menglaensis) and by having a tympanum

diameter larger than the width of finger III disc (tympa-

num diameter smaller than or equal to width of finger III

disc in menglaensis). Philautus petilus differs from P.

ocellatus by lacking a round black blotch on the occiput

(present in ocellatus). Philautus petilus differs from P

parvulus by having the snout longer than the eye diam-

eter (snout shorter than eye diameter in parvulus), hav-

ing a visible tympanum (hidden in pamulus), and having

the nostril close to the tip of snout (nostril midway

between eye and tip of snout in parvulus). Philautus

petilus differs from P. rhododiscus by lacking dark

brown coloration with black spots, grayish-white ventral

marbling, and reddish-orange finger and toe discs (pres-

ent in rhododiscus). Philautus petilus differs from P.

banaensis, P. gryllus , P odontotarsus, R. appendicula-

tus, R. bisacculus, and R. verrucosus by lacking dermal

fringes or tubercles on the limbs (present in banaensis,

gryllus, odontotarsus, appendiculatus , bisacculus, and

verrucosus). Philautus petilus differs from all species of

Theloderma Tschudi by having smooth skin with dorsal

asperities (skin rugose in Theloderma).

Etymology. - The species name petilus (L.) means slen-

der, referring to the distinct habitus of the holotype.

Ecology. - The holotype was collected at 2215 h on a

bamboo leaf 1 m above the ground in hilly evergreen

Vol. 10, p. 20

Asiatic Herpetological Research

2004

torest mixed with bamboo, approximately 200 m from

the bank of the Nam Ou River, at 600 m elevation.

Remarks. - The generic assignments of small, rha-

cophorid (or rhacophorine) treefrogs are uncertain,

debated, and likely to be considerably revised in the near

future (Bossuyt & Dubois 2001; Wilkinson et al. 2002).

Many species have been moved among the genera

Chirixalus Boulenger and Philautus Gistel (Frost 2002).

Philautus petilus does not have the two outer fingers

appearing to be opposable to the two inner ones (Figure

1C), which is diagnostic of the genus Chirixalus (Liem

1970). Historically, Philautus was diagnosed by the

absence of vomerine teeth (Leim 1970; Bossuyt and

Dubois 2001), but this character is known to vary7 with-

in a species, and consequently Liem (1970) included

species in the genus Philautus that sometimes have

vomerine teeth. Philautus petilus has very small vomer-

ine teeth. Bossuyt and Dubois (2001) proposed that only

species having direct aerial development (lacking a free-

swimming aquatic tadpole) be included in the genus

Philautus. The mode of reproduction in P. petilus is

unknown, but it does have a small clutch size (the left

ovary of the holotype holds fewer than 25 ova). Dring

(1987) reported total clutch sizes of only 2-26 eggs in

five species of Philautus , including the type species, P.

aurifasciatus. In the absence of a phylogeny and more

substantial reproductive data, we recognize that our

placement of petilus into the genus Philautus is tenta-

tive.

Acknowledgments

The opportunity to work in Laos was made possible by

the Wildlife Conservation Society / Division of Forest

Resource Conservation Cooperative Program. The

Ministry of Agriculture and Forestry (Vientiane, Laos)

permitted export of specimens to the Field Museum of

Natural History. Bee Thaovanseng assisted with field-

work in Laos. Financial support was provided by The

John D. and Catherine T. MacArthur Foundation (with

Harold Voris and Robert Inger), the National

Geographic Society (Grant no. 6247-98), and the

Wildlife Conservation Society. Harold Voris, Alan

Resetar, Jamie Ladonski, and Jennifer Mui facilitated

examining specimens at the Field Museum of Natural

History. Sophie Molia translated French descriptions

and Tan Fui Lian translated Chinese descriptions. Robert

Inger, Nikolai Orlov, and Jeff Wilkinson shared their

taxonomic opinions on the specimen. Nikolai Orlov

photographed the preserved specimen. Robert Inger,

Raoul Bain, and an anonymous reviewer improved the

manuscript.

Literature Cited

Bain, R. H., A. Lathrop, R. W. Murphy, N. L. Orlov, and

Ho Thu Cue. 2003. Cryptic species of a cascade

frog from Southeast Asia: taxonomic revisions and

descriptions of six new species. American Museum

Novitates 3417:1-60.

Bossuyt, F. and A. Dubois. 2001. A review of the frog

genus Philautus Gistel, 1848 (Amphibia, Anura,

Ranidae, Rhacophorinae). Zeylanica 6(1): 1-1 12.

Bourret, R. 1942. Les batraciens de l’lndochine.

Memoires de Flnstitut Oceanographique de

flndochine 6:1-547.

Dring, J. 1987. Bornean treefrogs of the genus Philautus

(Rhacophoridae). Amphibia-Reptilia 8(1987): 19-

47.

Fei, L. 1999. Atlas of Amphibians of China. Zhengzhou:

Henan Publishing House of Science and

Technology. 432 pages, [in Chinese].

Frost, D. R. 2002. Amphibian Species of the World: an

online reference. Version 2.21 (15 July 2002).

Electronic database available at

http://research.amnh.org/herpetology/amphibia/

index.html.

Inger, R. F. and M. Kottelat. 1998. A new species of

ranid frog from Laos. The Raffles Bulletin of

Zoology 46(l):29-34.

Inger, R. F., N. Orlov & I. Darevsky. 1999. Frogs of

Vietnam: a report on new collections. Fieldiana,

Zoology New Series, 92:1-46.

Liem, S. S. 1970. The morphology, systematics, and

evolution of the Old World treefrogs

(Rhacophoridae and Hyperoliidae). Fieldiana

Zoology 57:1-145.

Orlov, N. L., R. W. Murphy, N. B. Ananjeva, S. A.

Ryabov, & Ho Thu Cue. 2002. Herpetofauna of

Vietnam, a checklist. Part I. Amphibia. Russian

Journal of Herpetology 9(2):8 1-104.

Stuart, B. L. and T. J. Papenfuss. 2002. A new salaman-

der of the genus Paramesotriton (Caudata:

Salamandridae) from Laos. Journal of Herpetology

36(2): 145-148.

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Asiatic Herpetological Research

Vol. 10, p. 21

raylor, E. H. 1962. The amphibian fauna of Thailand.

University of Kansas Science Bulletin 63(8): 265-

599.

Wilkinson, J. A., R. C. Drewes, and O. L. Tatum. 2002.

A molecular phylogenetic analysis of the family

Rhacophoridae with an emphasis on the Asian and

African genera. Molecular Phylogenetics and

Evolution 24: 265-273.

2004

Asiatic Herpetological Research

Vol. 10, pp. 22-27~|

Rediscovery of the Philippine Forest Turtle, Heosemys leytensis

(Chelonia; Bataguridae), from Palawan Island, Philippines

Arvin C. Diesmos1’2’3, Genevieve V. A. Gee3, Mae L. Diesmos3’ 4, Rafe M. Brown2’3’5,

Peter J. Widmann3’6, and Judeline C. Dimalibot7

1 National Museum of the Philippines, Padre Burgos Avenue, Ermita 1000, Manila, Philippines;

Current address: Department of Biological Sciences, National University of Singapore,

Block S3 14 Science, Drive 4, Singapore 117543; E-mail: kaloula@i-manila.com. ph

- Angelo King Center for Research and Environment Management; Marine Laboratory,

Silliman University, Bantayan, Dumaguete City, Negros Oriental, Philippines 6200.

J Wildlife Conservation Society of the Philippines, Room 106 Institute of Biology, University of the Philippines,

Diliman 1101, Quezon City, Philippines; E-mail: jutisha@yahoo.com

4 Department of Biological Sciences, College of Science, University of Santo Tomas

Espaha, Manila; E-mail: msleonida@lycos.com

5 Section of Integrative Biology, University of Texas, Austin Texas, 78712;

Current address: Museum of Vertebrate Zoology, 3101 Valley Life Science Building,

University of California, Berkeley, CA 94720; Email: rafe@mail.utexas.edu

^ KATALA Foundation, Jacana Road, Bancao-Bancao, PO. Box 390, Puerto Princesa City 5300,

Palawan, Philippines; E-mail: widpeter@yahoo.com

7 Palawan Council for Sustainable Development, Sta Monica, Puerto Princesa City 5300,

Palawan, Philippines.

Abstract. - We report new observations from natural populations of the critically endangered Philippine forest turtle,

Heosemys leytensis. Previously known from two cotypes (reportedly from Leyte Island) that were destroyed during

World War II, a lone specimen in a U.S. collection, and a specimen purchased on Palawan Island in the late 1980s,

its status in the wild has been uncertain since its discovery. Our recent surveys of Palawan and nearby Dumaran

islands have documented natural populations that are under immediate threat due to over-harvesting and loss of habi-

tat. Records of captive animals and interviews with residents from these islands suggest that this species is heavily

exploited for food, pet trade, and ornamental fish pond curiosities. There is an urgent need to establish a conservation

program to study and protect remaining natural populations.

Heosemys leytensis, Asian freshwater turtles, turtle trade, Philippine forest turtle, Palawan Island,

Key words. -

Philippines.

Introduction

Taylor (1920) described the Philippine forest turtle,

Heosemys leytensis, on the basis of two specimens that

were collected by Gregorio Lopez. These specimens

were reportedly collected from a swamp at the

Municipality of Cabalian, southern Leyte Province,

Leyte Island, Philippines (Fig. 1). The cotypes (a male

and a female) were eventually deposited in the

Philippine Bureau of Science (Taylor, 1944) but were

destroyed during the World War II firebombing of

Manila (Brown and Alcala, 1978; Buskirk, 1989).

Between Taylor’s (1920) description and the late

1980s, no additional specimens or information became

available for this species, although its status as a valid

species has never been challenged (e.g., Pritchard, 1979;

Ernst and Barbour, 1989; Iverson, 1992). In 1988,

Timmerman and Auth reported on a specimen purchased

from a local resident of the Municipality of Taytay,

northern Palawan Island (Fig. 1). Buskirk (1989)

described a neotype for the species (CAS 60930) based

on a single specimen also reportedly from Cabalian,

Leyte.

Since these reports, numerous herpetologists,

including us, have searched for H. leytensis at Cabalian,

Leyte (Fig. 1) without success. The apparent rarity of the

species formed the basis of its listing under CITES

Appendix II and by IUCN as a Critically Endangered

species (Hilton-Taylor, 2000). Chelonian biologists

questioned whether the species was really rare or just

unstudied, extinct or extirpated, and whether the speci-

men reported by Timmerman and Auth (1988) was from

Vol. 10, p. 23

Asiatic Herpetological Research

2004

Figure 1 . - Map of Palawan Island group in relation to the

Philippines (inset) and Leyte Island. The type locality

(Taylor, 1920) of H. leytensis is indicated with a star;

recent trade or captive animal locations include (1)

Brooke’s Point, (2) Rizal, (3) Aborlan, and (4) Puerto

Princesa and known natural populations include (5)

Taytay, and (6) Dumaran Island.

a natural population on Palawan or the result of interis-

land trade (Ernst and Barbour, 1989; Iverson, 1992; Das,

1995; Gaulke, 1995). The question remained whether H.

leytensis occurred on Leyte Island or whether the origi-

nal type locality data were in error.

In late 2001, as part of a comprehensive status

assessment of Palawan’s endemic amphibians and rep-

tiles, we began a survey of forested sites throughout the

island. We soon became aware of three nonmarine tur-

tle species present in some local wet markets and in the

possession of local wildlife traders. Two species Cuora

amboinensis and Cyclemys dental a , are common on

Palawan (Taylor, 1920; Alcala, 1986; Gaulke and Fritz,

1998; Widmann, 1998; ACD and RMB, pers. obs.). A

third species, frequent in the wildlife and food trade, was

identified as Taylor’s (1920) Heosemys leytensis.

New observations. - The live specimens we examined

match published descriptions of H. leytensis (Taylor,

1920; Buskirk, 1989; Ernst and Barbour, 1989): cara-

pace unkeeled except for posterior vertebrals; vertebrals

broader than long; anterior marginals projecting beyond

cervicals, rendering anterior rim from slightly to strong-

ly serrated; plastron much smaller than carapace, nar-

Figure 2. - Live H. leytensis from natural population on

Dumaran Island, northern Palawan: (A) An individual of

undetermined sex in a small stream on Dumaran Island;

(B) close up of the head.

rowing anteriorly and posteriorly; angular notch

between gulars deep and distinct; notch between gulars

and humerals present, less distinct; anal notch deep and

circular; three to four enlarged transverse scales present

on anterior side of each foreleg; coloration rusty brown

with darker margins on anterior scutes; narrow7 white to

pale yellow line crosses head just behind auricular open-

ings, medially divided in some specimens (Figs. 2-5). A

full technical redescription of the morphology of H.

leytensis will be published elsewhere (Diesmos et al..

unpublished data).

We located captive animals for sale in markets at

the Municipalities of Brookes Point, Aborlan, Rizal.

Puerto Princesa City, and Taytay (Fig. 1). The animals

were for sale as pets, ornamental fish pond curiosities,

and for food. Additionally, H. leytensis individuals were

found in public restaurants in the capital city' of Puerto

Princesa (Fig. 4b). In many areas, residents expressed

the belief that the keeping of pet H. leytensis specimens

brings the owner good luck.

We found natural populations in the vicinity' of Lake

Manguao, Municipality of Taytay, Palawan Island and

on Dumaran Island (Fig. 2). Exact localities are not

given to protect these populations. Several individuals

of each natural population were observed in slow-mov-

2004

Asiatic Herpeto/ogical Research

Vol. 10, p. 24

Figure 3. - (A) Dorsal view of carapace and (B) ventral

view of plastron of a subadult H. leytensis of underter-

mined sex (captive pet, reportedly wild-caught locally)

from Dumaran Island, N. Palawan.

ing streams, quiet side pools, and nearby disturbed

gallery forests (Fig. 4a), at most a few meters from the

water’s edge. Residents in these localities reported to us

that turtles are always located in the general vicinity of

water, but that they can be found many meters away

from water as well. Residents also report that H. leyten-

sis burrows in stream banks and retreats under large

nearby limestone boulders in the dry season when

streambeds run dry.

Interviews with Tagbanwa tribe members in the

Municipality of Taytay suggest that in some areas this

species is fairly common. Reports of natural popula-

tions in the southern localities of Rizal and Brookes

Point will need to be confirmed. In these areas inter-

viewed persons claimed that H. leytensis was present in

nearby forests but we were unable to locate wild animals

ourselves.

Discussion

Our recent field observations confirm that H. leytensis

occurs naturally on Palawan and at least on one of its

northern satellite islands. Despite numerous surveys of

suitable habitat at Cabalian, Leyte conducted by E.

Figure 4. - (A) Preferred stream habitat of H. leytensis

from Dumaran Island, northern Palawan; (B) Heosemys

leytensis , Cuora amboinensis , and Cyclemys dentata

specimens alive in captivity in restaurant of Puerto

Princesa City, Palawan Island.

Taylor, A. Alcala, and ourselves, no additional specimens

of H. leytensis have been collected there. Interviews

with residents in the vicinity of Cabalian, have failed to

find verbal accounts of fresh-water turtles that fit the

description of H. leytensis. We suspect that the species

does not and never has naturally occurred on Leyte. We

prefer the use of the common name “Philippine forest

turtle” given that we have only observed animals in rem-

nant old-growth forests and our sense is that this species

is forest dependent.

It is possible that Taylor or Lopez mislabeled or oth-

erwise confused locality information assigned to the

original co-types on Leyte and the third specimen at

CAS (Buskirk, 1989). Taylor (1920) also reported

Cyclemys dentata from Cabalian, Leyte (see also

Iverson, 1992). This species has not since been reported

from Leyte and is otherwise restricted in the Philippines

to Palawan and the Sulu archipelago (Fig. 1; Taylor.

1920; Gaulke, 1995; Gaulke and Fritz, 1998). The fact

that another conspicuous Palawan turtle species was

reported at the same time and from the same site on

Leyte (Taylor, 1920) suggests that a group of specimens

from Palawan were mixed into collections from Leyte or

Vol. 10, p. 25

Asiatic Herpetological Research

2004

Figure 5. - A live Heosemys leytensis from the Municipality of Taytay, northern Palawan Island, Philippines.

Watercolors by Mr. Rene Aquino.

were mislabeled. Based on information from the CAS

herpetological registry, it is clear that G. Lopez also col-

lected on Coron and Busuanga (Fig. 1) which would

appear to be a likely source of the presumably erroneous

“Leyte” specimens of C. dentata and H. leytensis. Thus,

we suspect that a locality error is the basis of the specif-

ic epithet and the long-held belief that H. leytensis natu-

rally inhabits the island of Leyte. Whether H. leytensis

has ever been introduced outside of Palawan or the

country, remains to be documented.

Finally, given the geological history and the

Pleistocene formation of isolated paleoislands in the

Philippines (Heaney, 1985; Hall, 1996, 1998) it is not

surprising that H. leytensis may be restricted to Palawan

and satellite islands. Based on available information

from other groups of Philippine endemics, it is some-

what rare for a species to be shared between both the

Palawan (Palawan + Busuanga + Coron + Culion +

Dumaran) and the Mindanao (Mindanao+BohoI+Leyte+

Samar) Pleistocene Aggregate Island Complexes

(PAlCs). That is, based on previously-elucidated pat-

terns of biogeography (Brown and Alcala, 1970; Brown

and Diesmos, 2001; Brown and Guttman, 2002; Evans

et al., 2003), we would expect to find Philippine

endemics with restricted distributions on the Palawan

PAIC or the Mindanao PAIC, but not necessarily both.

There are some exceptions to these apparent trends, but

they appear to be rare and limited to non-endemic wide-

spread species that are also shared with the islands of the

Sunda Shelf (Borneo, Java, Sumatra, etc.), or wide-

spread Philippine endemics that are also found through-

out the rest of the archipelago (Inger, 1954; Alcala and

Brown, 1998; Brown and Alcala, 1970, 1978. 1980)

Recommendations. - We recommend that an immediate

exhaustive survey of the Palawan PAIC (including

Balabac, Coron, Busuanga, Culion, and Dumaran) be

undertaken to determine the status of natural H. leyten-

sis populations. Basic knowledge of the species' distri-

bution. habitat requirements, and natural population size

will be a necessary requirement for designing effective

conservation strategies. To combat illegal hobbyist, con-

sumptive, and/or medicinal trade, wildlife managers will

need to have reasonable estimates of numbers of animals

2004

Asiatic Herpeto/ogical Research

Vol. 10, p. 26

Table 1 . - Standard measurements of H. leytensis speci-

mens from captivity (Nos. 1-20) and a natural population

(Nos. 21-24; Dumaran Isl ). Carapace Length and Width

are straight-line distances; Carapace Width measured at

widest point; Tail Length measured from posterior edge

of cloaca to tip of tail. Sex undetermined; all measure-

ments are in mm.

being illegally harvested. Legislative protection of the

species will need to be adjusted to recognize its current

known distribution on Palawan and not Leyte. We

expect that a specific conservation strategy will be nec-

essary to protect this species from unchecked exploita-

tion. The fact that the entirety of Palawan is officially

designated a national protected area provides some

assurance, but we suspect additional measures will need

to be undertaken to protect this species while promoting

its study. The legal “Protected Area” status of Palawan

Island clearly is not deterring local exploitation of this

species. Local education programs and public awareness

campaigns targeting both the general public and local

environmental authorities may be the key to insuring

that H. leytensis does not become another casualty of the

“Asian turtle crisis” (van Dijk et al., 2000). Many basic

questions regarding the distribution, demography, ecolo-

gy, reproductive biology, and phylogenetic affinities of

H. leytensis remain to be answered.

Acknowledgments

This publication is a contribution of HerpWatch

Palawan 2001, a project funded by the BP Conservation

Programme (Silver Award No. 1554). ACD, MLD,

GVAG, and JCD wish to thank their former institutions

for supporting this work: De La Salle University-

Dasmarinas, Haribon Foundation, and Palawan State

University. The Protected Areas and Wildlife Bureau of

the Philippine Department of Environment and Natural

Resources and the Palawan Council for Sustainable

Development facilitated research permits. We especially

thank Althea Lota, Anson Tagtag, Marlynn Mendoza,

Carlo Custodio, Mundita Lim, Wilfrido Pollisco, Linda

Bacosa, Joselito Alisuag, Adelwisa Sandalo, and Rene

Villegas. Indira Widmann, Siegfred Diaz, Deborah

Villafuerte, Rolito Dumalag (Philippine Cockatoo

Conservation Project), and Sabine Schoppe (State

Polytechnic College of Palawan) extended much appre-

ciated assistance and shared relevant information. We

thank C. R. Infante for help during initial field survey

work on Palawan and I. Das and M. Gaulke for provid-

ing some critical reference material. We thank James

Parham (University of California, Berkeley) and Bryan

Stuart (Field Museum, Chicago) for providing refer-

ences and for applying just the right amount of pressure

to help us finish this report, and we thank Greg Pauly,

Jen Weghorst, George Zug, and Bryan Stuart for critical

reviews of earlier drafts of the manuscript. Special

thanks are due to Rene Aquino (National Museum of the

Philippines) for use of his painting of H. leytensis in life.

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2004

Asiatic Herpetological Research

Vol. 10, pp. 28-37

Molecular Systematics of Old World Stripe-Necked

Turtles (Testudines: Mauremys)

Chris R. Feldman1’* and James F. Parham2’3

1 Department of Biology, Utah State University, Logan, UT, 84322-5305, USA,

* Corresponding Author E-mail: elgaria@biology.usu.edu.

"Evolutionary Genomics Department, Joint Genome Institute, 2800 Mitchell Drive,

Walnut Creek, CA, 94598, USA.

University of California Museum of Paleontology, University of California, Berkeley, CA, 94720-3140, USA,

E-mail: parham@socrates. berkeley. edu

Abstract. - Nine extant species of Mauremys (including Ocadia and Chinemys) represent a geographically widespread

yet morphologically and ecologically conservative group of batagurid turtles. Here we examine the evolutionary rela-

tionships of Mauremys using 1539 base pairs of mitochondrial DNA encoding portions of COI, ND4, and three adja-

cent tRNA genes. These data contain 246 parsimony informative characters that we use to erect hypotheses of rela-

tionships for Mauremys. Both maximum parsimony and Bayesian methods suggest that Mauremys japonica, M.

sinensis , M. nigricans , and M. reevesii form a well-supported monophyletic clade, as do M. mutica and M. annamen-

sis. Furthermore, our analyses show that M. mutica is paraphyletic with respect to M. annamensis. The western taxa

M. leprosa, M. caspica, and M. rivulata remain problematic and do not form a monophyletic group sister to the Asian

taxa. Nevertheless, an east-west biogeographic hypothesis cannot be discounted with our molecular genetic data.

Key words. - Turtles, Bataguridae, Mauremys, molecular phylogenetics, mitochondrial DNA

Introduction

The Old World turtle genus Mauremys is represented by

morphologically and ecologically conservative species

that are diagnosed by a rigid plastron and a striped head

and neck. These semi-aquatic, batagurid (= geoemydid,

see Joyce et al., in press) turtles occupy lotic and lentic

environments in both forested and arid habitats through-

out Asia and the Mediterranean.

The genus contains some of the most commercially

important freshwater turtles in Asia. For example, M.

mutica is one of the most commonly reared and highly

traded chelonians in Asia (Lau and Shi, 2000). Other

Mauremys species have been at the center of a conserva-

tion and systematics controversy. In fact, two newly

described Mauremys may be polyphyletic hybrids

(Parham et al., 2001; Wink et al., 2001; Spinks et al.,

2004).

Given the mounting conservation interest in the tur-

tle fauna of Asia (van Dijk et al., 2000), understanding

the extant diversity and phylogenetic relationships

among the Bataguridae are areas of active research (Wu

et al., 1999; Honda et al., 2002b; Barth et al., 2004;

Spinks et al., 2004). The genus Mauremys has received

particular attention because of this recent conservation

crisis and taxonomic confusion. The first examination of

evolutionary relationships within Mauremys was a mor-

phological treatment of the genus based on shell and

scute measurements (Iverson and McCord, 1994).

Consistent with the disjunct distribution of Mauremys,

Iverson and McCord (1994) suggested that East Asian

taxa form a monophyletic group, sister to a

Mediterranean and Middle Eastern clade. A subsequent

study used 12S and 16S ribosomal genes to resolve the

phylogenetic relationships among species of Mauremys

(Honda et al., 2002a). In contrast to the east-west

hypothesis of Iverson and McCord (1994), Honda et al.

(2002a) suggested that the deepest phylogenetic splits

within Mauremys occur between Asian taxa. The ribo-

somal mtDNA data also cast doubt on the monophyly of

traditional Mauremys by including the east Asian

species, Chinemys reevesii, as the sister taxon to M.

japonica. Two recent studies examined more extensive

sequence data, predominantly cyt b mtDNA, as well as

a more comprehensive sampling of batagurids (Barth et

al., 2004; Spinks et al., 2004). Both studies firmly estab-

lished the placement of Mauremys within the

Bataguridae and show that the Chinemys and Ocadia are

phylogenetically nested within Mauremys (Barth et al.,

2004; Spinks et al., 2004). Barth et al. (2004) offer two

possible solutions to reconcile the paraphyly of

Mauremys: 1) split the species of Mauremys into four

genera; 2) lump Chinemys and Ocadia into an expanded

Mauremys. While Barth et al. (2004) refrain from a tax-

onomic decision, Spinks et al. (2004) adopt an expand-

ed Mauremys. We also endorse an inclusive Mauremys

Vol. 10, p. 29

Asiatic Herpetological Research

2004

because we consider expanding genera to well-support-

ed clades of species functionally preferable to proliferat-

ing monotypic genera based on subjective, typological

ideas of uniqueness (Feldman and Parham, 2002;

Parham and Feldman, 2002; Spinks et al., 2004).

Our objective here is to provide an independent esti-

mate of Mauremys phylogeny using different molecular

markers from other recent systematic investigations and

separate museum voucher specimens (Barth et al., 2004;

Spinks et al., 2004). We hope that our data help resolve

areas of uncertainty in the emerging consensus on

Mauremys systematics. In addition, our study will add to

the growing body of information on the evolutionary

history and diversity of Asia’s threatened batagurid

fauna (Wu et al., 1999; Honda et al., 2002b; Barth et al.,

2004; Spinks et al., 2004).

Materials and methods

Taxon sampling and laboratory protocols. - We

obtained liver tissue from 17 museum specimens repre-

senting nine currently recognized species of Mauremys

and three species of Cuora (Appendix 1). The nine

species of Mauremys used in our study include: M.

annamensis, M. caspica, M. japonica, M. leprosa, M.

mutica, M. nigricans , M. reevesii, M. rivulata, and M.

sinensis. We do not consider “M iversoni ”, “M

pritchardF, “O. glyphistoma ” or “0. philippenF to be

valid taxa because specimens matching these species (all

described from the pet trade) are likely hybrids (Parham

et al., 2001; Wink et al., 2001; Spinks et al., 2004). In

addition, we also excluded “M megalocephald’\ which

is probably a diet-induced variant of M. reevesii (Iverson

et al., 1989; Barth et al., 2002). However, we do include

a “M iversonF-Uke hybrid specimen described in

Parham and Shi (2001) because mtDNA from this

hybrid specimen is demonstrably Mauremys (Parham et

al., 2001). All vouchers correspond to well-documented

reference material and original species descriptions.

We isolated genomic DNA from tissue samples by

standard proteinase K digestion and phenol/chloroform

purification (Maniatis et al., 1982). We amplified 700 bp

of mtDNA encoding a section of COI via PCR (Saiki et

al., 1988) using primers HCO-2193 and LCO-1490

(Folmer et al., 1994). We amplified an additional 900 bp

region of mtDNA encoding a portion of ND4 and flank-

ing tRNA histidine (tRNAhis), serine (tRNAser), and part

of leucine (tRNAIeu) using primers ND4 and Leu

(Arevalo et al., 1994). We used the following thermal

cycle parameters for 50pl amplification reactions: 35

cycles of lmin denature at 94°C, lmin anneal at 45°C

(COI) or 52°C (ND4), and 2min extension at 72°C. We

purified PCR products using the Wizard Prep Mini

Column Purification Kit (Promega, Inc.) and used puri-

fied template in lOpl dideoxy chain-termination reac-

tions (Sanger et al., 1 977) using ABI Big Dye chemistry

(Applied Biosystems, Inc.) and the primers listed above.

Following an isopropanol/ethanol precipitation, we ran

cycle-sequenced products on a 4.8% Page Plus

(Ameresco) acrylamide gel using an ABI 377 automated

sequencer (Applied Biosystems, Inc.). We sequenced all

samples in both directions.

Sequence analyses. - We aligned DNA sequences with

the program Sequencher™ 4.1 (Gene Codes Corp.), and

translated protein coding nucleotide sequences into

amino acid sequences using MacClade 4.0 (Maddison

and Maddison, 2000). We identified tRNA genes by

manually reconstructing their secondary structures using

the criteria of Kumazawa and Nishida (1993). We

deposited all mitochondrial DNA sequences in GenBank

(Appendix 1).

We performed a partition homogeneity test (PH),

similar to the incongruence length differences test (ILD;

Farris et al., 1994), to determine whether the ND4 and

COI data could be combined. We used PAUP* 4.0b 10

(Swofford, 2002) to generate a null distribution of length

differences using 1000 same-sized, randomly generated

partitions from the original data with replacement.

To evaluate base substitution saturation at first, sec-

ond, and third codon positions, we plotted the uncorrect-

ed percent sequence divergence of transitions and trans-

versions versus the corrected maximum likelihood esti-

mates of divergence for each codon position.

Phylogenetic analyses. - We used maximum parsimony

(MP; Farris, 1983) and maximum likelihood-based

Bayesian (Larget and Simon, 1999) phylogenetic meth-

ods to infer evolutionary relationships among batagurid

species. We conducted MP analyses in PAUP* and

Bayesian analyses with MrBayes 3.0b4 (Huelsenbeck

and Ronquist, 2001). We polarized the phylogeny via

outgroup comparison (Maddison et al., 1984) using the

Asian box turtles Cuora mouhotii, Cuora picturata , and

Cuora trifasciata. Other molecular phylogenetic studies

suggest these turtles are appropriate outgroup taxa (Wu

et al., 1999; Honda et al., 2002b; Barth et al., 2004;

Spinks et al., 2004).

We executed MP analyses with the branch-and-

bound search algorithm (Hendy and Penny, 1982) using

equally weighted, unordered characters. To assess nodal

support, we used the bootstrap resampling method (BP;

Felsenstein, 1985) employing 1000 pseudoreplicates of

branch-and-bound searches in PAUP*. Additionally, we

calculated branch support (DI; Bremer, 1994) for all

nodes using the program Tree Rot 2c (Sorenson, 1999).

We performed Bayesian analyses to estimate branch

lengths and search for additional tree topologies. To

2004

Asiatic Herpetological Research

Vol. 10, p. 30

determine the most appropriate model of DNA substitu-

tion tor reconstructing Mauremys relationships under

the Bayesian method, we executed hierarchical likeli-

hood ratio tests (LRT; Felsenstein, 1993; Goldman,

1993; Yang, 1996) in the program Modeltest 3.06

(Posada and Crandall, 1998). Because MrBayes 3.0b4

can perform singular phylogenetic analyses using differ-

ent models of evolution, we performed two separate

LRTs on the two mtDNA regions. The model of

nucleotide substitution that best fit the COI data was the

HKY model (Hasegawa et al., 1985) in conjunction with

r (Yang, 1994a; 1994b), and I (Gu et al., 1995), while

the slightly less complex HKY + T model of DNA evo-

lution best fit the ND4 data. We then performed

Bayesian tree searches, allowing separate parameter

estimates under the two models of DNA substitution for

the COI and ND4 data partitions. We did not specify a

topology or nucleotide substitution model parameters a

priori. We ran Bayesian analyses for 3 x 10^ genera-

tions using the Metropolis-coupled Markov chain Monte

Carlo (MCMCMC) algorithm with four heated Markov

chains per generation, sampling trees every 100 genera-

tions. To determine when the Markov chains had con-

verged on stable likelihood values, we plotted the -lnl

scores against the number of generations (Huelsenbeck

and Ronquist, 2001). We then computed a 50 % major-

ity rule consensus tree after excluding those trees sam-

pled prior to the stable equilibrium. Nodal support is

given by the frequency of the recovered clade, which

corresponds to the posterior probability of that clade

under the given models of sequence evolution (PP;

Rannala and Yang, 1996; Huelsenbeck and Ronquist,

2001). Lastly, we performed three Bayesian runs to be

sure that independent analyses converged on similar log-

likelihood scores (Leache and Reeder, 2002).

Results

Genetic variation. - Sequences from the protein coding

regions appear functional and there are no gene

rearrangements in the data (Kumazawa and Nishida,

1995; Kumazawa et al., 1996; Macey and Verma, 1997;

Macey et al., 1997). However, ND4 in the batagurids

studied here appears truncated relative to that of emydid

turtles, which have three additional residues:

Phenylalanine, Tyrosine, and Cysteine (Feldman and

Parham, 2002). Instead, these batagurids possess a stop

codon, followed by a 12 bp stretch of highly polymor-

phic DNA between ND4 and tRNAhis. Additionally,

tRNAser has a short D-stem, instead of a D-arm replace-

ment loop like that of most metazoan taxa (Kumazawa

and Nishida, 1993). This unusual tRNA condition is also

seen in emydid turtles (Feldman and Parham, 2002).

The PH test shows that length difference between

the sum of the COI and ND4 trees and the combined

COI and ND4 trees is not significantly different from the

randomly generated test statistic ( P = 0.93). Therefore,

we combined the aligned DNA sequences for subse-

quent phylogenetic analyses.

Of the 1539 aligned nucleotides, 369 are variable

and 246 are parsimony informative. Among ingroup

taxa, 289 sites are variable and 205 parsimony informa-

tive. Of the 369 variable characters, 60 occur at 1st

codon positions, 15 at 2nd positions, 261 at 3rd positions,

and 33 in tRNAs. The scatter diagrams are linear and

show no evidence of multiple hit problems for transi-

tions or transversions (data not shown).

Phylogenetic relationships. - The branch-and-bound

equally weighted MP analysis produces a single most

parsimonious tree (L = 661; Cl = 0.626; RI = 0.683) that

is consistent with the model-based Bayesian analyses

(Fig. 1). All three Bayesian analyses converge on the

same topology and nearly identical mean log-likelihood

values, parameter estimates, and nodal support. Thus we

simply present results from the final search. The parti-

tioned HKY + T+ I and HKY + TBayesian analysis (3 x

10^ generations) attains stable log-likelihood values

within the first 15,000 generations, but we were conser-

vative and discarded the first 20,000 generations.

Because we sampled trees every 100 generations, we

discarded the first 200 trees and retained 29,800

Bayesian trees, which we used to generate a 50% major-

ity rule tree, and for which consensus values represent a

group’s posterior probability (Huelsenbeck and

Ronquist, 2001). The summary topology of the nearly

30,000 Bayesian trees (mean -lnl = 5205.5110, G2 =

24.5038; mean ti/tv (COI) = 10.8360; G2 = 10.6335;

mean a(COI) =0.5479, a2 = 0.8874; mean Pinvar (COI)

= 0.4163, O2 = 0.0291; mean ti/tv (ND4) = 12.3499; G2

= 9.0505; mean a(ND4) =0.2431, G2 = 0.0009) differs

from the MP tree in the placement of only one taxon

(Fig. 1).

In both analyses, species of Cuora unambiguously

group to the exclusion of Mauremys , (BP = 100%; DI =

19; PP = 100%). Mauremys japonica is a member of a

clade containing M. nigricans, M. reevesii and M. sinen-

sis (BP = 100%; DI = 13; PP = 100%), yet relationships

among these taxa are not well resolved, as indicated by

the low nodal support and conflict between MP and

Bayesian reconstructions. The MP tree places M. sinen-

sis sister to a group linking M. japonica , M. nigricans,

and M. reevesii (DI = 1), wherein M. nigricans and M.

reevesii form an additional clade (BP = 86%; DI = 5).

Alternatively, the Bayesian tree connects M. japonica to

M. sinensis (PP = 59%), sister to the M. nigricans the M.

reevesii clade (PP = 99%). The M. japonica , M. nigri-

cans, M. reevesii, and M. sinensis clade is sister to a

Mauremys leprosa (Morocco) I Mauremys leprosa (Morocco)

Vol. 10, p. 31

Asiatic Herpetological Research

2004

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Table 1. Pairwise comparisons of mtDNA sequences among Mauremys and related taxa. Note: values above the diagonal indicate uncorrected pairwise differences (/o) while

those below the diagonal denote HKY +F+ I sequence divergences (%).

2004

Asiatic Herpetological Research

Vol. 10, p. 32

poorly supported M. mutica, M. armamensis, “M iver-

sonf\ M. leprosa, and M. caspica assemblage (DI = 2;

PP = 61%). Within this large group, M. mutica , M. anna-

mensis and “M iversonf form a strongly supported

clade (BP = 99; DI = 15; PP = 100%). In fact, inclusion

of both M. armamensis and “M iversoni ’ render M.

mutica paraphyletic; two M. mutica (ROM 25613,

25614) are more closely related to M. annamensis and

“M iverson F than they are to a Chinese M. mutica

(MVZ 230476) (BP = 100%; DI = 36; PP = 100%).

Within this “ mutica complex”, M. annamensis and “M

iversonr are weakly allied (BP = 60%; DI = 1 ; PP = 86).

This entire Umutica complex” is then sister to a weakly

supported M. leprosa and M. caspica clade (DI = 1).

Finally, both MP and Bayesian analyses suggest that M

rivulata is sister to a monophyletic clade containing the

rest of Mauremys, but this phylogenetic arrangement

receives almost no statistical support (DI = 2; PP =

60%).

Phylogenetic relationships. - Both MP and Bayesian

phylogenetic methods show that M. japonica is a mem-

ber of a clade containing M. nigricans, M. reevesii, and

M. sinensis, exclusive of other Mauremys. The M.

japonica, M. nigricans, M. reevesii, and M. sinensis

clade is joined to a poorly supported M. mutica, M.

annamensis, M. leprosa, and M. caspica assemblage.

Within this grouping, M. mutica and M. annamensis

form a solid clade, congruent with shell and scute data

(Iverson and McCord, 1994), other molecular data

(Barth et al., 2004; Spinks et al., 2004) but not 12S and

16S mtDNA data (Honda et ah, 2002a). Our analyses

further suggest that M. mutica is paraphyletic. Two M.

mutica (ROM 25613, 25614) purchased in Vietnam are

more closely related to M. annamensis than they are to

topotypic M. mutica (MVZ 230476) from China. We

tested the paraphyly of M. mutica by constraining the

MP searches to recover only those trees that produce a

monophyletic M. mutica. The shortest two trees generat-

ed by the constraint search are 697 steps long (Cl =

0.594; RI = 0.636), 36 steps longer than the uncon-

strained MP tree. The two-tailed Wilcoxon signed-ranks

test (Templeton, 1983) fails to support (P < 0.0001) the

monophyly of M. mutica. The mutica complex is linked

to a tenuous M. leprosa and M. caspica group. Lastly,

both MP and Bayesian phylogenetic analyses tentatively

place M. rivulata sister to a monophyletic clade contain-

ing the remaining ingroup taxa.

Genetic Variation. - Our samples of M. leprosa from

Spain and Morocco, and M. caspica from Iran and

Bahrain, show no intraspecific haplotype diversity

Discussion

Vol. 10, p. 33

Asiatic Herpetological Research

2004

(Table 1), yet exhibit sizeable morphological variation

(Busack and Ernst, 1980). This discrepancy between

intraspecific mtDNA diversity and geographic variation

seems to be common among turtles (e.g., Lenk et al.,

1999; Starkey et ah, 2003) and may be related to exten-

sive phenotypic plasticity or the slow rate of molecular

evolution in turtles (Avise et ah, 1992; Lamb et ah,

1994).

In contrast, most interspecific mtDNA variation

appears extensive, with uncorrected sequence diver-

gences higher than 8% between a number of ingroup

taxa (Table 1). Additionally, the mitochondrial sequence

divergences between M. rivulata and M. caspica (Table

1), formerly considered conspecifics (Fritz and Wischuf,

1997), are equivalent to or greater than the genetic dis-

tances observed between other congeneric emydid and

batagurid turtles (e.g., Feldman and Parham, 2002;

Starkey et ah, 2003; Stuart and Parham, 2004). Hence,

these mtDNA data, together with the differing shell mor-

phologies, distinct color patterns, and unique habitat

preferences of M. rivulata and M. caspica (Busack and

Ernst, 1980), support the recent elevation of M. rivulata

as a distinct evolutionary lineage independent of M.

caspica (Fritz and Wischuf, 1997).

Mauremys annamensis, a robust batagurid endemic

to central Vietnam, is characterized by extensive axillary

buttresses, a massive bridge, a slightly tricarinate and

high-domed shell, a vividly striped head and neck, and

reverse sexual size-dimorphism (McDowell, 1964;

Iverson and McCord, 1994). The taxon is so distinctive

it was once placed into its own genus, Annamemys

Bourret 1939. McDowell (1964) originally demonstrat-

ed that M annamensis and M. mutica share a number of

derived features and Iverson and McCord (1994) subse-

quently confirmed a close kinship between these taxa

with shell measurements. Hence, the close relationship

revealed by our mitochondrial genes is not novel. What

is surprising, however, is that M. annamensis differs

from Vietnamese M. mutica and our “M iverson?'- like

hybrid by only two transitions. Furthermore, this clade

shows a roughly 6% uncorrected sequence divergence

from topotypic M. mutica from Zoushan Island,

Zheijung Province, eastern China. In contrast, distantly

collected samples of M. leprosa and M. caspica show no

such intraspecific mtDNA variation (Table 1). These

data question our ideas of species limits within

Mauremys. Is M. annamensis a distinct species? Does

M. mutica represent multiple species?

Several potential hypotheses might account for

these unexpected results. M annamensis may simply

represent a recent species, derived from M. mutica , or

even a geographical variant of M. mutica. The dramatic

morphological differences exhibited by M. annamensis

could reflect intense selection and rapid phenotypic evo-

lution while the minute mitochondrial divergences and

paraphyly represent the nature of speciation and unsort-

ed polymorphism. Alternatively, there may be historical

or ongoing introgression between M. annamensis and

Vietnamese M. mutica , perhaps facilitated by selection.

Two additional hypotheses involve the possibility

of hybridization. While our specimen of M. annamensis

conforms to the species description, it was acquired

from a Chinese turtle farm (Appendix 1) where M. anna-

mensis and M. mutica are reared together in large num-

bers (J.F. Parham, pers. obs.). Hence, our M. annamen-

sis could be a captive hybrid between M. annamensis

and M. mutica , though we find no morphological char-

acters supporting this notion. Ideally, we would examine

the morphology and compare the sequences of a wild-

caught M. annamensis to our sample, but to our knowl-

edge, no tissued, field-collected vouchers of M. anna-

mensis exist in collections; all modern museum speci-

mens of M. annamensis have been obtained from either

animal markets or the pet trade.

Another possibility is that the Vietnamese M. muti-

ca could be hybrid offspring of female M. annamensis

and male M. mutica, accounting for the scant mtDNA

differences between Vietnamese M. mutica and M.

annamensis and the sizeable divergences between these

samples and topotypic M. mutica. Although the

“Vietnamese M. mutica ” are phenotypically similar to

typical M. mutica, their darker coloration is evocative of

M. annamensis. Both Barth et al. (2004) and Spinks et

al. (2004) found substantial mitochondrial variation

between M. mutica and M. annamensis, but we do not

know the provenance or morphology of their samples.

The hybridization of batagurid turtles has lead to

other cases of taxonomic confusion (Parham and Shi,

2001; Parham et al., 2001; Shi and Parham, 2001; Wink

et al., 2001; Spinks et al., 2004) and cannot be discount-

ed here. Unfortunately, our small sample size prohibits

us from effectively evaluating these hypotheses. Clearly

a more detailed genetic study is needed to unravel this

problem. With our present knowledge, any change in

conservation policies for M. annamensis, one of the

world’s most poorly known turtles, would be premature.

Biogeography. - The distribution of Mauremys is char-

acterized by a major break between the Zagros

Mountains of western Iran (easternmost M. caspica ) and

the Annamite Mountains of central Vietnam (range of M.

annamensis). This disjunction includes the entire Indian

subcontinent (home to a diverse, endemic batagurid

fauna), and the inhospitable Tibetan plateau. We suggest

that the collision of India into Asia may be the vicariant

event responsible for the current distribution of

Mauremys, as proposed for anguine lizards (Macey et

al., 1999). Molecular data are ambiguous on this point.

2004

Asiatic Herpetological Research

Vol. 10, p. 34

Given that neither eastern nor western species assem-

blages appear monophyletic (though a Wilcoxon signed

ranks test topology test cannot discount this hypothesis

[P = 0.35]), the current divergences between the living

species may have occurred before the development of

the Indo-Tibetan gap. The collision and subsequent

uplift of the Tibetan plateau took place in multiple stages

between 50 and 10 MYBP (Shackleton and Chang,

1988; Dewey et al., 1989; Windley, 1988). Hervet

(2004) attributed some Paleogene (>50 MYBP)

European fossils to the stem of Mauremys , but did not

investigate their relations to east Asian Mauremys. In

addition to employing additional molecular markers to

vouchered museum specimens, the integration of all

extant Mauremys into analyses of morphological charac-

ters and fossil taxa will be necessary to unravel the his-

torical biogeography of this clade of turtles.

Acknowledgments

We thank T. J. Papenfuss, C. Cicero, and D. B. Wake

(MVZ), and R. W. Murphy (ROM) for kindly contribut-

ing specimens and tissues essential to this project. We

are grateful to M. E. Pffender and P. G. Wolf for gener-

ously providing laboratory space, and D. G. Mulcahy

and W. B. Simison for much needed lab assistance. We

appreciate helpful discussions about phylogenetic meth-

ods from E. M. O’Neill, A. D. Leache, and F. T.

Burbrink, and useful comments on this manuscript from

M. D. Matocq, J. R. Mendelson III, E. D. Brodie Jr., H.

B. Shaffer, and two anonymous reviewers. We also

thank P. Q. Spinks and U. Fritz for sharing unpublished

data. Finally, we thank K. Padian and T. J. Papenfuss for

funding, space, advice, and encouragement. This is

University of California Museum of Paleontology

Contribution #1826 and LBNL #54656. This research

was performed under the auspices of the U.S.

Department of Energy, Office of Biological and

Environmental Research.

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Appendix 1.

Specimens used and GenBank Accession numbers for

DNA sequence data. Acronyms are: MVZ = Museum of

Vertebrate Zoology, Berkeley, California; ROM = Royal

Ontario Museum, Toronto, Ontario; AF or AY =

GenBank (http://www.ncbi.nlm.gov).

Mauremys annamensis - Purchased in turtle farm in

Hainan Province, China, no real locality data; MVZ

238937; AY337338, AY337346. Mauremys caspica -

Field collected on Bahrain Island, Bahrain; MVZ

230971; AY337339, AY337347. Mauremys caspica -

Field collected in West Azarbaijan Province, Iran; MVZ

234281; AY337340, AY337348. “ Mauremys iversoni ” -

Purchased in turtle farm in Hainan Province, China, no

real locality data; MVZ 230475; AF348275, AF34281.

Mauremys japonica - Pet trade specimen, no locality

data; MVZ 234647; AY337341, AY337349. Mauremys

leprosa - Field collected in Tetouan Province, Morocco;

MVZ 178059; AY337342, AY337350. Mauremys lep-

rosa - Field collected in Cadiz Province, Spain; MVZ

231989; AY337343, AY337351. Mauremys mutica -

Field collected in Zoushan Island, Zhejiang Province,

China; MVZ 230476; AF348262, AF348278. Mauremys

mutica - Purchased from a turtle trader in Yen Bai

Province, Vietnam; ROM 25613; AF348260,

AF348279. Mauremys mutica - Purchased from a turtle

trader in Yen Bai Province, Vietnam; ROM 25614;

AF348261, AF348280. Mauremys rivulata - Field-col-

lected in Bursa Province, Turkey; MVZ 230212;

AY337344, AY337352. Mauremys ( =Ocadia ) sinensis -

Field-collected in Hainan Province, China; MVZ

230479; AY337345, AY337353. Mauremys nigricans -

Pet trade specimen, no locality data, MVZ 130463;

AF348264, AF348289. Mauremys reevesii - Pet trade

specimen, no locality data, MVZ 230533; AF348263,

AF348288. Cuora picturata - Purchased from a turtle

trader in Dong Nai Province, Vietnam, ROM 37067;

AF348265, AF348292. Cuora trifasciata - Pet trade

specimen, no locality, MVZ 230636; AF348270,

AF348297. Cuora mouhotii - Purchased from a turtle

trader in Bac Thai Province, ROM 35003; AF348273,

AF348286.

2004

Asiatic Herpetological Research

Vol. 10, pp. 38-52

A Preliminary Report on Southeast Asia’s Oldest Cenozoic Turtle Fauna

from the Late Middle Eocene Pondaung Formation, Myanmar.

J. Howard Hutchison1, Patricia A. Holroyd1, and Russell L. Ciochon2

1 Museum of Paleontology, 1101 Valley Life Sciences Building, University of California,

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

J

- Departments of Anthropology and Pediatric Dentistry, University of Iowa, Iowa City, Iowa, 52242, U.S.A.

Abstract. - Late middle Eocene fossils from the Pondaung Lormation of central Myanmar document Southeast Asia’s

oldest Cenozoic turtle fauna. Although the material is fragmentary, seven distinct turtle taxa are recognized. These

include a podocnemid pleurodire, anosteirine and carettochelyine carettochelyids, two or more trionychine triony-

chids, and a testudinid. Of these, only the carettochelyine carettochelyid is complete enough to recognize as a new

taxon, Burmemys magnifica, gen. et sp. nov. The Pondaung turtle fauna is one of the best known of its age from

Southeast Asia but comparisons with the limited literature of the Eocene faunas from China, Mongolia, and the Indian

subcontinent indicate it is probably biogeographically unique. Among the recognized genera, only Anosteira is known

from other Eocene Asian localities, and the presence of pleurodires is unusual.

Key words. - Reptilia, Testudines, Carettochelyidae, Burmemys , Myanmar, Pondaung Lormation, Paleontology,

Eocene.

Introduction

The origins of Southeast Asia’s herpetofauna are poorly

understood, as there are few fossils that document the

origin of the major groups inhabiting the region. The

oldest known herpetofauna from this region is from the

Pondaung Lormation, a late middle Eocene (approx. 37

Ma) set of rocks exposed in the Chindwin-Irrawaddy

Basin of Myanmar (formerly Burma). The Pondaung

fauna is best known for its mammalian fauna (e.g.,

Colbert, 1938; Tsubamoto et al., 2000), and little atten-

tion has been devoted to the remainder of the fauna. In

prior reports, Buffetaut (1978) noted the presence of

both unidentified crocodilians and dyrosaurids; Sahni

(1984) and Rage (1987) noted unidentified Lacertilia.

These reports were based primarily on a rather limited

collection made by Bamum Brown in 1922 and housed

in the American Museum of Natural History, New York.

Savage and Russell (1983) and Broin (1987) list

“Pelomedusid/Emydidae”, “Carettochelyoidea”, and tri-

onychids from the Pondaung. Outside the Pondaung

region, the only other report of turtles from Southeast

Asia is Ducrocq et ah’s (1992) mention of two types of

?Emydidae from the late Eocene site of Krabi, Thailand.

Here we present a preliminary description of the turtles

based on a more thorough study of these collections, and

additional collections in the University of California

Museum of Paleontology, Berkeley, California.

Localities and age. - fossils occur in a number of local-

ities occurring in the upper 100+ meters of the otherwise

marine Pondaung formation. The majority of the speci-

mens discussed here come from localities to the west

and northwest of Mogaung village, Myaing Township,

central Myanmar (fig. 1), that have been collected inter-

mittently over the past 80 years. As a consequence, most

specimens have limited, descriptive locality data that

provides locations based on distances from known vil-

lages. Recent fieldwork has provided detailed, GPS

based mapping of the most productive outcrops and per-

mit us to place most of the historic localities in a more

accurate and stratigraphically detailed framework.

Those localities we can place with confidence are shown

in figure 1. Localities whose positions are approximate

are shown with dashed lines. Concordances for locali-

ties that have been published under more than one name

or number are provided in the caption of figure 1 and

are based on Colbert (1938), maps on file at the

American Museum of Natural History, field notes of J.

Wyatt Durham and Donald E. Savage on file at the

University of California Museum of Paleontology, data

contained in Tsubamoto et al. (2000, 2002) and Gunnell

et al. (2002), and field observations by PAH and RLC.

fossils occur in place and as erosional lag coming

out of reddish to purplish mudstones (Pig. 2 A-C).

fossil wood is also commonly found (Pig. 2D), attesting

to the presence of the ancient forest. Soe et al. (2002)

interpreted sediments including these localities as swale-

fills and/or paleosols deposited in an ancient floodplain;

stratigraphic sections for these localities are contained in

Gunnell et al. (2002). Based on comparisons of tempo-

ral distribution and faunal resemblance data of the

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28° N

24 “N

20° N

ia°N

Figure 1. Locality Map of Pondaung Formation localities. V78090=Thandaung kyitchaung and possibly AMNH locali-

ties A14-16, 18-19; V83106, 3.5 mi SW of Mogaung = AMNH A31; V83111 "1 .25 mi NW Paukkaung" probably equals

Pk2; V83116 probably equals Yarshe kyitchaung. V96001-V96002 = AMNH A22 and Lema kyitchaung; V98019

"Thidon or near Bahin", possibly equal to Pkl or Pk2.

Pondaung mammalian fauna with other Asian and North

American mammal faunas, as well as additional con-

straining evidence from marine invertebrates, Holroyd

and Ciochon (1994) concluded that the Pondaung fauna

is best considered latest middle Eocene in age and

broadly contemporaneous with Asian faunas assigned to

the Sharamurunian Land Mammal Age, a finding con-

firmed by recent fission-track dates that provide a date

of 37.2 +/- 1.2 Ma (Tsubamoto et al., 2002).

Abbreviations. - AMNH, American Museum of Natural

History, New York, New York, U.S.A.; UCMP.

University of California Museum of Paleontology,

Berkeley, California, U.S.A.

Systematic Paleontology

Testudines Batsch, 1788

Pleurodira Cope, 1865

Pelomedusoides Cope, 1868

Podocnemididae Cope, 1868

?Podocneniididae unident.

Referred Material. - UCMP locality V83108; UCMP

153798, right peripheral 3. UCMP locality V 83 113;

UCMP 147052, partial left hypo-xiphiplastron. UCMP

locality V96002: UCMP 142245, left incomplete epi-

p I astro n.

MAP 1

MAP 2

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Figure 2. Fossil localities of the Pondaung Formation. A. UCMP locality V96001, Lema kyitchaung; B. UCMP locali-

ty V96002, Lema kyitchaung; C-D. UCMP locality V96007, near Mogaung, showing the common occurrence as float

of both turtle bone (C) and petrified wood (D) on the surface.

Description. - The epiplastron (UCMP 142245, Fig.

3A) lacks the posterolateral part but is otherwise well

preserved. The scale covered surfaces are very finely

textured with delicate but well-defined sulci. Faint

growth corrugations are present on the gular scale

(extragular of Hutchison and Bramble, 1981). There is a

prominent anteriorly-projecting gular spur, and the epi-

plastron margin is distinctly concave between the mid-

line and the gular spur. There is an intergular scale (gular

of Hutchison and Bramble, 1981) spanning the midline

that projects anteriorly into the anterior embayment. The

scales overlap extensively onto the dorsal surface with

little exposure of the visceral surface. The intergular

expands slightly posteriorly on the ventral surface and

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Figure 3. A-C. Podocnemidae? indet. A. UCMP 142245, incomplete left epiplastron, dorsal, medial suture and ven-

tral views. B. 153798, right peripheral 3, external and visceral views. C.UCMP 147052, hypo-xiphiplastron fragment,

dorsal view, spot indicates center of bump. D-E. Testudinidae. D. UCMP 142226, partial right epiplastron, cross-sec-

tion (as indicated) and dorsal views. E. UCMP 149166, partial right xiphiplastron, dorsal view. Scale bars equal 1 cm.

extends onto the entoplastron. Dorsally the intergular

extends slightly more than one-half the length of the

inter-epiplastral suture and is parallel-sided. On the ven-

tral surface, the gular is triangular with the lateral mar-

gins converging to a point at the entoplastron margin.

The hypo-xiphiplastron fragment, UCMP 147052

(Fig. 3C), is broken on all the edges except the free mar-

gin. It exhibits a narrow overlap of the femoral and anal

scales onto the dorsal surface (less than one-fifth the

transverse length as preserved). The swelling at the

anterolateral comer indicates an ascendant hypoplastral

buttress. The sutures are fused. A short expanse of the

femoral-anal scale sulcus is preserved at the extreme

posterior end. Medial to the scale margins on the dorsal

side is a large elliptical swelling that has a smooth sur-

face and may have been divided by the hypo-xiphiplas-

tron suture.

The peripheral 3 (UCMP 153798, Fig. 3B) lacks the

dorsal margin. The body of the peripheral is robust and

without a change in plane between the pleural and mar-

ginal surfaces. The surface is smooth and unsculptured.

The sulci are shallow but well defined. The free margin

is acutely angled. On the visceral side, the marginal

scales rise up from only about one-third of the peripher-

al depth. There is no indication of an axillary scale. The

finely dentate suture for the hyoplastron buttress rises

anteriorly and may have overlapped peripheral 2-3

suture. There is a gap in the hyoplastral suture near the

posterior margin, for passage of the musk duct. The

length between the anterior and posterior sutures along

the free margin of the peripheral is 37.9 mm.

Discussion. - The dorsal scale overlap, truncated anteri-

or margin, undivided intergular, and relatively thick epi-

plastra resemble selected extant or fossil

Pelomedusoides (Bothremydiae, Podocnemididae, and

Pelomedusidae). The prominent epiplastral spurs resem-

ble those of the pelomedusid Kenyemys Wood, 1983,

from the Pliocene of Kenya. Flowever, the Pondaung

form differs in the greater excavation of the gular

embayment, intergular extending onto the entoplastron,

and restriction of the gular scales to the epiplastra (i.e.,

not reaching the midline). The scale arrangement is sim-

ilar to that of the podocnemidid Neochelys Bergounioux,

1954 (Broin, 1977; Jimenez et al., 1994) from the

Eocene of Europe. Neochelys may also possess a rela-

tively prominent gular spur (Broin, 1977, fig. 59), but

differs in the less extensive dorsal overlap of the scales

and lesser development of an epiplastral embayment.

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Figure 4. Anosteira sp., A. UCMP 131736, right hypoplastron, ventral view. B. UCMP 131737, lateral fragment of left

hypoplastron, ventral view. C. UCMP 147030, left peripheral 6, external, posterior, visceral, and anterior views. Scale

bars equals 1 cm.

The presence of a prominent musk duct on the

peripheral 3, absence of an axillary scale, and strong

indication of a hyoplastral buttress rising onto the first

costal is consistent with Neochelys- like pleurodires. The

hypoplastron fragment may be referable to the same

taxon, but the area of the pelvic sutures is broken off.

The general similarity to at least some Neochelys

favors a placement of the Pondaung Formation speci-

mens in the Podocnemididae.

Cryptodira Cope, 1868

Testudinidae Gray, 1825

Testudinidae undet.

Referred Material. - UCMP locality V6204: UCMP

149166, right xiphiplastron fragment. UCMP locality

V96009: UCMP 142226, partial right epiplatron.

Description. - The epiplastron (UCMP 142226, Fig.

3D) lacks the gular region. The remaining part of the

free margin is greatly thickened along the anterior edge

of the dorsal scale covered portion. The posterior rim of

this thickened gular area overhangs the visceral surface.

The ventral surface is longitudinally convex. The

sutures are moderately thick and dentate.

The anterolateral part of a right xiphiplastron

(UCMP 149166, Fig. 3E) is referred to the Testudinidae

on the basis of the strong overlap of the femoral scale

dorsally, its inflated appearance, and fairly porous sur-

face texture.

Discussion. - The morphology of the epiplastron is typ-

ical of testudinids and a few batagurids. The rather

porous bone, inflation of the gular area, and general

nature of the sutures and surface texture agrees best with

that of a testudinid. The overhang of the posterior gular

rim is derived in testudinids and absent or poorly devel-

oped in such tortoises as Hadrianus Cope, 1872,

Stylemys Leidy, 1851, Sharemys Gilmore, 1931,

Kansuchelys Yeh, 1963, and Ergilemys Ckhikvadze,

1972. The epiplastron thus resembles more derived tor-

toises such as Testudo Linnaeus, 1858.

Testudinoidea Fitzinger, 1826, indet.

Referred material. - UCMP locality V96019: UCMP

147051, posterior part of left hypoplastron. UCMP

locality V78090: UCMP 170495, partial neural. UCMP

locality V98109: UCMP 170522, shell fragments.

Description. - The hypoplastron is represented by a

fragment (UCMP 147052) that preserves the portion

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Figure 5. Burmemys magnifica gen. et sp. n. A. UCMP 61212, adult left hypoplastron (type), ventral view. B. UCMP

131745. juvenile left hypoplastron, ventral view. C. UCMP 154993, posterior part of juvenile left epiplastron, ventral

view. D. UCMP 131747, anterior part of juvenile left xiphiplastron, dorsal and ventral view. E. UCMP 157444, juvenile

left costal 2, external view. F. UCMP 147022, neural, external view. G. UCMP 157442, suprapygal, external view. Scale

bars equals 1 cm.

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Figure 6. Burmemys magnifies gen. et sp. n. A. AMNH 14196, left peripheral 1, anterior suture, external and visceral

views. B. UCMP 147021, left peripheral 1, external, posterior suture and visceral views. C. UCMP 147027, left periph-

eral 2, external and visceral views. D. UCMP 147002, left peripheral 3, external, visceral and posterior suture views.

E. UCMP 61211, left peripheral 4, external and visceral views. F. UCMP 147001, left peripheral 4 fragment, visceral

and posterior suture views (arrow points to flat hyoplastral suture). G. UCMP 131756, juvenile left peripheral 5, suture

view. H. UCMP 61218, left peripheral 6, external, posterior suture, visceral and anterior suture views. I. UCMP 142223,

right peripheral 7, external, anterior suture, visceral, posterior suture views. J. UCMP 157445, juvenile left peripheral

7 external, visceral, and anterior suture views. K. UCMP 142244, right peripheral 8, external, anterior suture, viscer-

al and posterior views. L. AMNH 1911, left peripheral 10 and pygal, external view. Scale bars equal 1 cm.

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posterior to the buttress. The free margin is slightlv con-

vex. The femoral scale distinctly but narrowly overlaps

the dorsal side. The margin dorsal margin of the scale is

marked by a shallow sulcus and the bone continues to

thicken medially before thing nearer the midline. A par-

tial neural (UCMP 170495) has a distinct carina with a

rounded top.

Discussion. - The referred fragmentary specimens do

not appear to belong to other known taxa in the fauna

and agree in general morphology with testudinoids,

probably testudinids or batagurids. The neural resembles

those of carinate batagurids.

Carettochelyidae Boulenger, 1887

Anosteirinae Lydekker, 1889

Anosteira Leidy, 1 87 1

Anosteira sp.

Referred material. - UCMP locality UCMP V78090:

UCMP 131752, peripheral 9 or 10; UCMP 131754,

hypoplastron fragment; UCMP 131755, posterior frag-

ment of nuchal; UCMP 147115, neural. UCMP locality

V83106: UCMP 131736, medial right hypoplastron

fragment; UCMP 131737, lateral hypoplastron frag-

ment; UCMP 131741, peripheral 7; UCMP 131742,

peripheral 8; UCMP 131744, costal fragments; UCMP

131746, anterior fragment of a right peripheral 6. UCMP

locality V96001: UCMP 147005, hypoplastron frag-

ment; UCMP 147011, left peripheral 7. UCMP locality

V96002: UCMP 147030, left peripheral 6. UCMP local-

ity V96008: UCMP 147024, right peripheral 2. UCMP

locality V96009: UCMP 142225, peripheral 9 or 10.

Description: The hyoplastron resembles those seen in

typical Anosteira and Pseudanosteira Clark, 1932, and

lacks the truncated anteromedial articulation of the new

genus described below. This specimen differs from

Allaeochelys Noulet, 1867, in having a narrower poste-

rior lobe and narrower bridge area.

The peripherals are referred to Anosteira on the

basis of their small size and well-formed sutures. Most

also show the presence of weekly-defined sulci on the

external surface. All the peripherals have sharp margin-

al carina, and the surface is finely pustulate. The gom-

photic pits for reception of the plastron on peripheral 6

(UCMP 147030, Fig. 4C) lie within a longitudinal

trough that traverses the peripheral. The latter is 12.6

mm along the free margin carina and 12.5 mm from the

carina to the costal suture. A partial peripheral 6 (UCMP

131746) has the trough on the plastral suture filled with

8-9 vertically elongated pits and a shaip lateral carina.

The two gomphotic pits on peripheral 7 also occur with-

in a trough, but on peripheral 7 the trough is only

approximately two-thirds the length of the bone. The

peripheral 7 (UCMP 147011) is 12.0 mm along the cari-

na. The specimen tentatively identified as peripheral 9 or

10 (UCMP 131752) is deeper than long (16 mm along

the margin, 18 mm in depth).

The posterior nuchal fragment has the typical caret-

tochelyid nuchal pedicle. A faint transverse sulcus is

present, and another faint longitudinal sulcus near the

midline is visible.

A small neural (UCMP 147115) is also referred to

Anosteira on the basis of the small size and patterned

surface, narrow length to width ratio, and low and broad

central carina.

Discussion. - Anosteira is known from both Asia (5

species) and North America (1 species) in the Eocene.

The closely related genus Pseudanosteira is limited to

North America and distinguishable from Anosteira only

by details of the top of the carapace. No elements in the

Pondaung collection resemble Pseudanosteira. The

presence of sulci on the peripherals, nuchal, and costal

fragments indicates it should be assigned to Anosteira.

The Pondaung specimen is most parsimoniously

referred to Anosteira in the absence of any evidence that

Pseudanosteira occurs anywhere in Asia. Previous

records of Anosteira are confined to China and

Mongolia.

Carettochelyinae Boulenger, 1887

Burmemys magnified gen. et sp. nov.

Holotype. - UCMP 61212, adult left hypoplastron (Fig.

5 A) from UCMP Locality V6204 (near Myaing), found

by J. Wyatt Durham, late Professor of Paleontology at

the University of California, Berkeley.

Paratypes. - AMNH locality “1 mile northeast of Gyat,

Magwe Province”: AMNH 1911, pygal, peripheral 10

fragment, and costal fragment. AMNH locality “1 mile

north of Koniwa”: AMNH 1919, left first peripheral;

AMNH 1928, distal half of right first peripheral; AMNH

14196, partial left peripheral 1; AMNH 14197, plastron

fragment. UCMP locality V6204: UCMP 61211, left

peripheral 4; UCMP 61218, left peripheral 6. UCMP

locality V78090: UCMP 131750, juvenile lateral

hypoplastron fragment, UCMP 131751, juvenile periph-

eral fragment; UCMP 131753 juvenile xiphiplastron

fragment; UCMP 154994, proximal costal fragment.

UCMP locality V83106: UCMP 13 1738, juvenile right

hypoplastron; UCMP 131739, juvenile hypoplastron

fragment; UCMP 131745, juvenile left hypoplastron.

UCMP locality V 83 111: UCMP 128406, right peripher-

al 2. UCMP locality V83 1 1 6: UCMP 1 3 1 748, hypoplas-

tron fragment. UCMP locality V83143: UCMP 131747,

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anterior part of left xiphiplastron. UCMP locality

V96001: UCMP 147001, left peripheral 4 fragment;

UCMP 147002, partial left peripheral 3; UCMP 147003,

anterior peripheral fragment; UCMP 147009, neural;

UCMP 147010, peripheral fragment; UCMP 147012,

juvenile medial hypoplastron fragment. UCMP locality

V96002: UCMP 142244, right peripheral 8; UCMP

154984, anterior peripheral fragment. UCMP locality

V96008: UCMP 147021, left first peripheral; UCMP

147023, posterior peripheral fragment; UCMP 147027,

left peripheral 2; UCMP 147028, partial right peripheral

1; UCMP 147029 distal fragment of a costal. UCMP

locality V96009: UCMP 142223, right peripheral 7.

UCMP locality V99498: UCMP 157443, neural; UCMP

157446, shell fragments.

Referred material. - UCMP locality V96001: UCMP

147004, plastron fragment. UCMP locality V83106:

UCMP 131740, hyoplastron fragment. UCMP locality

V78090: UCMP 131756, juvenile left peripheral 5;

UCMP 154993, posterior fragment of left epiplastron.

UCMP locality V99498: UCMP 157442, suprapygal;

UCMP 157444, left costal 2; UCMP 157445, left periph-

eral 7.

Diagnosis. - Burmemys is distinguished from other

carettochelyines by the combination of asymmetrical

articulation of the hyo-hypoplastra, narrow hypoplastral

bridge, and large size (estimated carapace length greater

than 1000 mm).

Description. - The holotype hypoplastron (UCMP

61212, Fig. 5 A) is massive. The anterior suture of the

left hypoplastron consists of two sutures. The suture

with the left hyoplastron is sinusoidal, curving antero-

medially, and joins a distinct, straight and anteromedial-

ly-facing suture, presumably for articulation with the

right hyoplastron. The ventral sculpture consists of a

pattern of irregular, closely-spaced tubercles that radiate

from a focal point lateral to the middle of the medial

moiety. Laterally, the tubercles coalesce into ridges radi-

ating laterally. The sutures are finely dentate and thick

(13 mm). The lateral margin and posterior half of the

medial part is broken away in the type, but these are pre-

served in the juvenile specimen (UCMP 131745, Fig.

5B). The width of the medial part of the hypoplastron

measured from the apex of the inguinal notch to the

plastral midline is only one-half or less of the maximum

hypoplastral width. The inguinal notch is open and not

confined as in Carettochelys Ramsey, 1887. The anteri-

or-posterior width of the bridge area is one-half or less

the width of the xiphiplastral lobe of the hypoplastron.

The referred juvenile specimens exhibit the same sutur-

al shapes as the adult (type) but the inguinal notches are

shallower, sculpture less organized, and lateral extent of

the lateral arm of the bridges are shorter.

The posterior part of a juvenile epiplastron (UCMP

154993, Fig. 5C) is referred to Burmemys on the basis of

the convex curvature of the lateral margin that indicates

a short and rounded anterior lobe, and an obtuse angle

between the entoplastral and hyoplastral sutures indicat-

ing a short and broad entoplastron.

Two xiphiplastra (UCMP 131747, Fig. 5D; UCMP

131753) are referred to Burmemys on the basis of rela-

tively larger size, converging (non-parallel) medial and

lateral margins of the anterior moiety, and thinning

rather than thickening toward the midline suture. Both

specimens are small (proximal width of UCMP 131747

is 20 mm) and thus considered as juveniles.

The juvenile left costal (UCMP 157444, Fig. 5E) is

nearly uniformly thin, parallel sided, and sculptured

with a subdued and random pattern of low pustules and

short ridges. The distal margin forms about a 45 degree

angle to the sides. There are no sulci. The parallel sides

and high angle of the distal margin indicate a second

costal.

The distal end of an adult costal (UCMP 147029) is

subtlety sculptured with longitudinal irregular ridges.

The distal suture is weakly dentate but patent except

above the rib. The rib ends protrudes prominently.

Although damaged, the distal width is about 70 mm.

A large neural (UCMP 147009, Figs. 5F) is relative-

ly narrow, lacks a midline carina, and has subtle sculp-

ture of very shallow dimples. It has a midline length of

51 mm, maximum width of 32 mm, and maximum

thickness of the lateral side of 15.4 mm.

The suprapygal (UCMP 157442, Fig. 5G) is trian-

gular with a distinct medial carina. The surface sculpture

consists of irregular vermiform ridges that radiate from

the central area of the posterior margin. It is longer than

wide (32.2 mm long, 31.5 mm wide).

At least nine peripheral positions are represented.

The sculpture is variable consisting of distinct tubercles

at one extreme to anastomosing pits and ridges at the

other. The free margins of adult specimens are rounded

but may be acute in juveniles. There are no indications

of scale sulci.

The first peripheral exhibits distinct sutures with the

first costal, nuchal and second peripheral. The free mar-

gin perimeter is asymmetrically curved. The largest

specimens (AMNH 1919, Fig. 6A; UCMP 147021, Fig.

6B) have perimeter lengths of 114 and 119 mm, maxi-

mum depths of 90 and 81 mm, maximum thicknesses at

the posterior suture of 33 and 27 mm, and maximum

thicknesses at anterior suture of 28 and 25 mm respec-

tively.

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The two second peripherals differ in size. UCMP

147026 (Fig. 6C) is massive with a free margin length of

82 mm, maximum depth of 67 mm, and maximum thick-

ness of the anterior suture of 20 mm. Comparable meas-

urements of UCMP 128406 are 45, 40, and 11 mm

respectively. The second peripheral is roughly rectangu-

lar in external view.

The only specimen referred to the third peripheral

(UCMP 147002, Fig. 6D) is lacking the anteroventral

and posterodorsal corners. The anterior part of the dor-

sal suture is a semi-scarf joint — probably for the rib end

of the first costal. The peripheral thickens noticeably

towards the posterior suture and reaches a thickness of

32 mm at the suture.

The fourth peripheral (UCMP 61211, Fig. 6E) is

damaged anteriorly and dorsally and locally abraded. Its

length along the lateral carina is 75 mm. The free mar-

gin curves posteromedially on the posterior moiety to

form a plastral articulation. The plastral articular surface

is relatively flat but deep (up to 16 mm) and without pits

for the hyoplastral buttress or normal dentations, thus

indicating a weakly ligamental and kinetic joint. The lat-

eral carina is broadly rounded. The peripheral 4 frag-

ment (UCMP 147001, Fig. 6F) also shows this rather flat

and deep (19 mm) hyoplastral suture.

A small peripheral, probably a left peripheral 5

(UCMP 131756, Fig. 6G) is considered a juvenile of this

species. The plastral arm is very short with a longitudi-

nal trough enclosing a series of gomphotic pits. The lat-

eral carina is slightly rounded and broadly upturned. The

length of the lateral carina is 22 mm and has a posterior

thickness of about 9 mm.

A relatively complete left peripheral 6 (UCMP

61218, Fig. 6H) has a damaged plastral margin and lacks

the dorsal suture. The plastral and costal arms converge

posteriorly. The plastral articulation is broken anteriorly

but posteriorly has a longitudinal trough indicating inter-

digitation with the hypoplastron. The lateral carina is

rounded and slightly upturned. The length along the lat-

eral carina is 82 mm.

A peripheral 7 (UCMP 142223, Fig. 61) of an adult

measures 99 mm along the marginal carina, 100 mm

from the carina to costal margin, posterior thickness of

29 mm and an anterior thickness of more than 45 mm.

The hypoplastral suture is damaged but trough-like,

extends about half-way along the medial side, and

appears to have housed one or two recessed pits. The

isolated peripheral 7 (UCMP 157445, Fig. 6J), a pre-

sumed juvenile, closely resembles Carettochelys with

the hypoplastral buttress rising up the central part of the

medial side. The free margin is sharp and broadly

upturned. The length of the free margin is about 34 mm.

The adult peripheral 8 (UCMP 142244, Fig. 6K) is

massive and slightly shorter than deep (97 mm along the

lateral carina and 105 mm from the carina to costal

suture). An anteriorly-deepening trough divides the

medial surface into dorsal and ventral arms anteriorly.

The pygal (AMNH 1911, Fig. 6L) is distinctly

trapezoidal with a short anterior side and a low but sharp

medial crest. The sculpture consists of widely spaced

irregular tubercles that fade out near the medial crest and

free margin. An associated posterior peripheral 10 frag-

ment has a sculpture of irregular ridges and tubercles

that radial from a central focus.

Discussion. - The absence of scales and large size place

Burmemys in the Carettochelyinae. Of the three Eocene

genera of Carettochelyinae, Burmemys differs from all

in the presence of two distinct anterior articular sutures

on one of the hypoplastra. This most likely represents an

asymmetrical articulation with the hyoplastra, with one

of the hyoplastra extending well across the midline to

form an angled articulation with the opposite hypoplas-

tron. Even where the hyo-and hypoplastra are not mirror

images with one of the hypoplastra contacting the oppo-

site hyoplastron (e.g., Anosteira in Hay, 1908, Fig. 353),

the midline suture remains straight as in other Paleogene

carettochelyids and the plastral midline suture usually

exhibits some limited kinesis. This asymmetry is not

unusual in turtles, but within carettochelyids was known

only to a lesser degree in some Carettochelys. The

hypoplastron in extant Carettochelys insculpta Ramsey,

1887 may cross the midline to form a short angled suture

with the opposite hyoplastron (AMNH 84212, and

Rooij, 1915, fig. 123a). This occurs on the left hyoplas-

tra on both of these.

Burmemys resembles anosteirines and differs from

extant Carettochelys, Hemichelys Lydekker, 1887, (pi.

XII, fig. 2) from the Eocene of the Punjab, and

Chorlakkichelys Broin, 1987 (pi. 1, fig. 2) from the

Eocene of Pakistan in the relatively broad inguinal

notch. Burmemys additionally differs from

Chorlakkichelys and Carettochelys in having a distinct-

ly narrow bridge area. The general proportions of the

hypoplastron resemble those of Allaeochelys from the

Eocene of Europe (Broin, 1977, PI. XVI, Fig. 3). The

suprapygal differs from Allaeochelys, Carettochelys,

Hemichelys and probably Chorlakkichelys in being

longer than wide.

Burmemys is also the largest carettochelyid

described to date. Based on scaling up of the elements

in comparison to other carettochelyids, we can estimate

that the shell length of Burmemys exceeded 1000 mm.

This estimate suggests that Burmemys is among the

largest turtles known, but is smaller than estimates Head

et al. (1999) provided for Eocene trionychids from

Pakistan, which may have reached more than 2000 mm

in length, and is smaller than the giant Bridgerian triony-

chid from Wyoming (Gaffney, 1979).

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2004

Figure 7. Trionychinae. A. UCMP 61213, right hypoplastron, ventral view. B. UCMP 1537993, fragment of right

hypoplastron, ventral view. C. UCMP 147022, neural, external view. D. UCMP 170520, costal fragment, external view.

Scale bars equals 1 cm.

Trionychidae Gray, 1825

Trionychinae Gray, 1825

Trionychinae genus indet.

Trionychinae, large form

Referred material. - UCMP locality V6204: UCMP

61213, right hypoplastron. UCMP locality V78090:

UCMP 170497, costal fragments. UCMP locality

V83116: UCMP 153799, fragment of right hypoplas-

tron. UCMP locality V83143: UCMP 173809, plastron

fragment. UCMP locality V96001: UCMP 147020,

costal fragment. UCMP locality V96002: UCMP

154983, costal proximal fragment. UCMP locality

V96008: UCMP 147022, neural. UCMP locality

V96009: UCMP 142222, plastron fragment.

Description. - The hypoplastron (UCMP 61213, Fig.

7A) lacks the projecting spines (present in UCMP

153799, Fig. 7B) but is otherwise relatively complete.

The calloused area has well defined edges and covers

most of the ventral surface, except for the long offset

shelf on the medial edge. The calloused area is sculp-

tured with distinct pits and ridges, while the shelf is

amorphously roughened. The buttress is composed of

two protruding spikes. The posteromost of these is bro-

ken off at the base, but the larger anterior one is divided

into three fluted points at its tip.

The isolated neural (UCMP 147022, Fig. 7C), prob-

ably 6 or 7, is hexagonal and narrows distinctly posteri-

orly. The dorsal surface is weakly sculptured, lack sulci,

and is flat anteriorly but is formed into a central carina

posteriorly. The neural is 46 mm long and 50 mm wide.

Discussion. - The large size of the hypoplastron and

general conformation indicates a trionychine and gener-

ally resembles Pelochelys Gray 1864, Chitra Gray 1 844,

and Pelodiscus Fitzinger 1835 in these features, but dif-

fers in having a wide, unsculptured medial shelf.

Additional material would be needed to refine identifi-

cation.

Trionychinae, small form

Referred material. - UCMP locality V6204: UCMP

61210 plastron fragment. UCMP locality V83106:

UCMP 147116, two costal fragments.

Description. - Two distal costal fragments exhibit a

well-defined sculpture of pits and ridges with indica-

tions of longitudinal welts. The pattern extends to the

free margin with only a slight sculpture-free zone at the

free margin, suggesting an adult turtle of relatively small

2004

Asiatic Herpetological Research

Vol. 10, p. 49

size in comparison with the preceding taxon. The sculp-

ture resembles that of a trionychine rather than a

cyclanorbine such as Lissemys Smith, 1931.

Trionychinae, ornate form

Referred material. - UCMP locality V98109: UCMP

170520, two costal fragments.

Description. - The costal fragments (UCMP 170520,

Fig. 7D) exhibit a striking sculpture of large, elongate

tubercles rising above a surface composed of a general-

ly organized pattern of longitudinal rows of shallow pits

and low rides. The longitudinal axes of the raised tuber-

cles vary from anterior-posterior to medial-lateral and

are large (11-15 mm) relative to the overall size of the

larger costal fragment (maximum preserved width of 32

mm). Carapace sculpturing varies between individuals

and also ontogenetically, but the peculiar sculpture

shows some resemblance to that seen in some extant

Aspideretes Hay, 1904.

Discussion

In addition to the turtles, a variety of other lower verte-

brates are present in the Pondaung Formation including

a carcharhinid shark, Galeocerdo Muller and Henle

1837 (UCMP 142238), a clariid catfish (UCMP

128411), at least four species of agamid lizards (UCMP

128410, 130290, 142227, 142232), paleophid and colu-

broid snakes (see Head et al, in prep.), and a minimum

of two crocodilians, including a pristichampsine croco-

dylian (UCMP 147127) and a dyrosaurid (Buffetaut,

1978).

Unfortunately, reports on Asian lower vertebrates of

comparable age (Sharamurunian Asian Land Mammal

Age or late middle Eocene) are few. Thus, the limited lit-

erature, combined with the fragmentary nature of the

Pondaung fossils themselves, make detailed compar-

isons with other faunas difficult. Nonetheless, compar-

isons with known Sharamurunian lower vertebrate fau-

nas reveal only a few similarities between the Pondaung

and any other locality. Pleurodires are previously unde-

scribed from Asia, although Broin (1987) notes the pres-

ence of “Pelomedusidae and / or Emydidae” from the

middle Eocene of Pakistan and Oligocene of India. An

adocid was described by Gilmore (1931) from the late

middle Eocene of Mongolia, but none were identified in

the Pondaung assemblage. The carettochelyid genus,

Anosteira , has been reported from age-equivalents in

Manchuria (Zangerl, 1947) and Guangdong, China (Sun

Ailing et al., 1992) and from slightly younger sediments

in Shandong and Guangdong provinces (Yeh, 1963).

The only other carettochelyines described from Asia are

Chorlakkichelys and Hemichelys from the early middle

Eocene of Pakistan (Lydekker, 1887; Broin, 1987), and

Burmemys is the most easterly and southerly Eocene

record of the subfamily. Trionychids, as elsewhere, are

an important part of the fauna, but our material is not

sufficiently diagnostic to make any meaningful biogeo-

graphic comparisons. Testudinids are widely reported in

Chinese and Mongolian Eocene faunas (Gilmore, 1931;

Ye, 1963), but all of these appear to be more generalized

forms similar to Hadrianus or Kansuchelys. The

Pondaung form appears to be more like the modern

Testudo, and thus distinct from contemporaneous

Chinese and Mongolian taxa.

Among other reptiles, the only other agamid lizard

known in the Asian Sharamurunian is Tinosaurus yuan-

quensis from the Heti Formation (Li, 1991), but it is a

diminutive form that bears no resemblance to the

Pondaung agamids. Crocodilians are known elsewhere,

but not in detail. In overall diversity, the Pondaung

fauna shares more general resemblances to the better-

known Irdinmanhan faunas, especially that of the

Kuldana Formation of Pakistan (Broin, 1987).

Based on the fragmentary evidence available to

date, several observations can be made regarding the

Pondaung lower vertebrate fauna. Faunal endemicity is

supported by the number of unique taxa, and the compo-

sition of the turtle fauna is unusual with trionychoids

(especially carettochelyids) dominating. Faunal compo-

sition and the large size of these turtles are consistent

with an interpretation of these sites as representing a

warm, tropical floodplain environment, deposited fairly

near shore. The aquatic habits of most of the lower ver-

tebrates suggest that during late middle Eocene time the

Pondaung region was a well-drained floodplain environ-

ment, a finding consistent with previous geological

interpretations (e.g., Bender, 1983, Soe et al., 2002).

Acknowledgments

We are grateful to Donald E. Savage, Ba Maw, and

Thaw Tint for reinitiating fieldwork in the Pondaung

region in the late 1970’s, and Brig. -Gen Than Tun and

Major Bo Bo from the Office of Strategic Studies,

Ministry of Defense for arranging our visits to

Myanmar. Tin Thein, Aye Ko Aung, Aung Naing Soe,

and other members of the Pondaung Fossil Expedition

team are thanked for their assistance during our stays

and their help while in the field. Eugene Gaffney,

Charlotte Hotton, and Mark Norell kindly provided

access to and assistance in use of the AMNH collections

and associated records. Walter Joyce reviewed the man-

uscript and provided constructive criticisms. Funding

for fieldwork in Myanmar has been provided by the

Smithsonian Foreign Currency Program (from Public

Vol. 10, p. 50

Asiatic Herpetological Research

2004

Law 480 funds), the L.S.B. Leakey Foundation, the

University of California Museum of Paleontology, the

University of North Carolina at Charlotte Foundation,

the University of Iowa Center for Pacific and Asian

Studies, the Office of the Vice President for Research

and the Human Evolution Research Fund of the

University of Iowa Foundation. This is UCMP contribu-

tion no. 1836.

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A Review of the Comparative Morphology of Extant Testudinoid Turtles

(Reptilia: Testudines)

Walter G. Joyce1 and Christopher J. Bell2

1 Department of Geology and Geophysics, Yale University, New Haven, CT 06511

E-mail: walter.joyce@yale.edu

Department of Geological Sciences, The University of Texas at Austin, Austin, TX 78712

E-mail: cjbell@mail. utexas. edu

Abstract. - With an expansive geographic distribution, an excellent fossil record, and over 140 recognized extant

species, testudinoid turtles constitute one of the most diverse and widespread clades of turtles. The current under-

standing of the distribution of morphological characters among testudinoid turtles is poor. Improved knowledge will

help to facilitate accurate identification of fossil remains, and to provide a reliable morphological data set for phylo-

genetic analyses. We provide a critical review of skeletal and scute characters commonly utilized in previous system-

atic analyses of Testudinoidea. Description and illustration of character states, discussion of their distribution within

Testudinoidea, and polarity determinations for 93 characters are provided. Our preliminary results indicate that onto-

genetic changes in skeletal structure are an important source of variation within Testudinoidea. Sexual variation, onto-

genetic variation, and intra- and inter-population variation are inadequately documented for most testudinoid taxa.

Furthermore, data matrices of morphologic characters in the existing literature must be carefully reconsidered.

Previously published morphologic data provide reasonably strong support for the monophyly of 'Testudinidae.' Strong

morphologic support for a monophyletic 'Emydidae' is lacking, and 'batagurid' monophyly has not been rigorously

tested in the literature. Because a new research cycle centered on testudinoid phylogeny is now under way, it is essen-

tial to critically re-examine the underlying assumptions and working hypotheses that have governed this field of study

over the last 20 years.

Key words. - Testudines, Testudinoidea, Testudinidae, Emydidae, Bataguridae, Geoemydidae, morphology, systemat-

ics.

Introduction

Pond turtles and land tortoises (collectively,

Testudinoidea) form one of the largest and most wide-

spread clades of living turtles, with more than 140 extant

species and an almost worldwide distribution. The dis-

covery and description of many new fossil testudinoids

in the last half century, combined with the emergence

and ascendancy of molecular techniques in systematics,

provide new opportunities to explore the evolutionary

history of the group in unprecedented detail.

Concomitant with the appearance of these new data sets

and analytical techniques comes an increasing apprecia-

tion for conservation efforts to preserve these turtle lin-

eages and help to secure their future in the face of

increasing human predation and habitat encroachment.

This is true especially for the Asian representatives of

this clade (e.g., van Dijk et al., 2000) but also is relevant

at a more generalized and inclusive level (e.g., Rhodin,

2000).

Our recent attempts to diagnose fossil testudinoids

reliably and to place them within a phylogenetic context

led to the recognition that a critical re-evaluation of mor-

phological data and purported synapomorphies for the

subclades of testudinoid turtles is desirable. A more

thorough understanding of morphological data sets will

provide not only a means by which molecular trees may

be independently assessed, but also will form an essen-

tial foundation for diagnosing and interpreting fossil

specimens. This in turn will facilitate the integration of

fossil taxa into future systematic analyses, and will

enhance our understanding of the paleobiogeography

and divergence times of extant lineages.

The recent flurry of published works appears to rep-

resent the beginning of a new research cycle ( sensu

Kluge, 1991) in testudinoid systematics. We suggest that

an important part of this cycle will be a critical re-exam-

ination of the working hypotheses that have governed

testudinoid systematics since the publication of

McDowell’s (1964) seminal work on the group. A key

component of this will be the assessment of fundamen-

tal, often unstated, assumptions that underlie current

hypotheses of relationship. Our contribution to this

research cycle is the first critical reappraisal of morpho-

logical characters applied to testudinoid systematics

since the work of Hirayama (1985). The emerging

improvement in our understanding of testudinoid rela-

tionships based on molecular sequence data will certain-

Vol. 10, p. 54

Asiatic Herpetological Research

2004

ly result in numerous new questions (e.g., regarding

paleobiogeography, the timing of sequence and evolu-

tionary divergences, and the evolution of morphological

adaptations) that will demand a clearer understanding of

testudinoid morphology.

The purpose of this paper is to present a preliminary

revision and discussion of the morphological characters

previously utilized in investigations of testudinoid sys-

tematics. Our goal here is not to produce a phylogenetic

hypothesis (indeed, we deliberately eschew such a pro-

duction), but rather to evaluate the morphological data

that have been, and will be, used to generate such

hypotheses. To enhance our discussion and facilitate

improved communication about testudinoid morpholo-

gy, we provide illustrations of all characters states we

discuss.

Abbreviations. - Institution and collection abbrevia-

tions: CAS, California Academy of Sciences, San

Francisco, California; CM, Carnegie Museum of Natural

History, Pittsburgh, Pennsylvania; FMNH, Field

Museum of Natural History, Chicago, Illinois; IVPP,

Institute of Vertebrate Paleontology and

Paleoanthropology, Beijing, China; KU, The University

of Kansas Natural History Museum, Lawrence, Kansas;

LMNH, Louisiana Museum of Natural History, Baton

Rouge, Louisiana; MCZ, Museum of Comparative

Zoology, Harvard University, Cambridge,

Massachusetts; TNHC, Texas Natural History

Collections, Texas Memorial Museum, Austin, Texas;

TUMNH, Tulane University Museum of Natural

History, New Orleans, Louisiana; YPM, Yale Peabody

Museum, New Haven, Connecticut.

Abbreviations used in figures: AB, abdominal

scute; af, articular facet; an, angular; bo, basioccipital;

CE, cervical scute; co, costal bone; ent, entoplastron;

epi, epipterygoid; fdm, foramen dentofaciale majus; fr,

frontal; fpp, foramen palatinum posterius; HU, humeral

scute; hyo, hyoplastron; hypo, hypoplastron; ju, jugal;

MA, marginal scute; mx, maxilla; ne, neural bone; pa,

parietal; pal, palatine; PEC, pectoral scute; pf, pre-

frontal; PL, pleural scute; pm, premaxilla; po, postor-

bital; pt, pterygoid; qj, quadratojugal; qu, quadrate; VE,

vertebral scute; vf, vomerine foramen; vo, vomer.

Material and Methods

We examined 309 testudinoid specimens representing

93 species, but focused our efforts on 46 representative

species. The list of specimens examined is provided in

Appendix 1. Turtle shell nomenclature follows Zangerl

(1969) and cranial nomenclature follows Gaffney

(1972). Of the 46 focal species, most were recognized as

valid species by Ernst and Barbour (1989), with the

exception of texana, which they placed within ‘ concin -

na .’ Generic allocations for testudinoid species varied

widely over the last 50 years and are subject to differing

opinions today, particularly because the monophyly of

many testudinoid genera remains untested. We conse-

quently suppress the use of generic names wherever pos-

sible and use species epithets only. This procedure also

has the advantage of precisely associating observations

with species only instead of higher taxonomic cate-

gories. Most extant turtles have distinct species names,

but among those turtles discussed in this review the

species epithets insculpta, nelsoni , oculifera , ornata,

and platynota each appear twice ( insculpta under

Glyptemys and Carettochelys; nelsoni under Pseudemys

and Terrapene\ oculifera under Graptemys and

Psammobates\ ornata under Pseudemys and Terrapene;

platynota under Geochelone and Notochelys ). For clari-

ty in these instances, we indicate our usage with a sin-

gle-letter generic abbreviation. A complete list of all cur-

rently recognized testudinoid species and all outgroup

species used herein is provided in Appendix 2 together

with a list of their various generic assignments used in

the last 50 years.

Our use of the classic higher categories is always

restricted to their phylogentic crown. ‘Emydinae’ (sensu

McDowell, 1964) are also referred to as ‘Emydidae,’

‘emydids,’ or North American pond turtles;

‘Batagurinae’ (sensu McDowell, 1964) as ‘Bataguridae,’

‘batagurids’ or Asian pond turtles; and ‘Testudinidae’

(sensu McDowell, 1964) as ‘testudinids’ or (land) tor-

toises. We make no a priori assumptions of monophyly

for any of these categories, and retain single quotations

around these names throughout the text to emphasize

our uncertainty.

We attempted to examine most significant morpho-

logical characters commonly utilized in systematic stud-

ies of testudinoids, but the majority of our observations

concern the skeletal system and scute characters. Almost

all characters were derived from the literature. Major

sources for each category were: ‘Batagurinae’

(Hirayama, 1985; McCord et al., 1995; Yasukawa et ah,

2001); ‘Testudinidae’ (Crumly, 1982, 1985, 1994); and

‘Emydinae’ (Gaffney and Meylan, 1988; Burke et ah,

1996). Additional characters were also found in

Mlynarski (1976), Shaffer et ah (1997), and other

sources cited in the character discussions. With few

exceptions, morphological features were examined on

specimens themselves; evaluations based on previously

published literature are indicated where applicable.

Sexual dimorphism, ontogenetically influenced poly-

morphisms, and geographic variation in morphology are

not well explored in testudinoid turtles. These areas are

in need of much more research. A full exploration of

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Asiatic Herpetological Research

Vol. 10, p. 55

such variation is beyond the scope of this work, but we

aie able to make some preliminary observations regard-

ing morphological change through ontogeny in some

anatomical systems.

Polarizing characters with the help of outgroups

proved to be a difficult task, mostly because all relevant

extant sister taxa are highly specialized after more than

65 million years of independent evolution. Furthermore,

hypotheses of the systematic relationships of the major

groups of cryptodires reveal a highly unstable picture

(e.g., Bickham, 1981; Gaffney, 1975, 1985; Gaffney et

al., 1991; Shaffer et al., 1997) making it impossible to

make any a priori decisions regarding the succession of

outgroups. We consequently assessed polarity for most

characters by examining select outgroup taxa and the

ingroup taxa. Where polarity is not clear from outgroup

comparison, we sometimes relied upon ingroup com-

monality. To allow full transparency, we discuss every

polarity decision at the end of each character descrip-

tion.

Outgroup taxa include the cryptodires caretta ,

odoratus, serpentina , and spinifera, and the pleurodires

gibba , siebenrocki, subglobosa, and subrufa. For a num-

ber of characters, especially of the shell, neither ingroup

nor outgroup analysis of extant taxa proved useful. In

these instances, polarity was based on literature descrip-

tions of the “lindholmemydid” taxa Gravemys,

Lindholmemys , and Mongolemys . These Cretaceous,

Asian, fossil taxa are not well described in the literature,

but sufficient material and description exists to use these

taxa to help polarize character states (e.g., Khosatzky

and Mlynarski, 1971; Sukhanov, 2000; Danilov and

Sukhanov, 2001). The group may not be monophyletic,

but putative members currently are hypothesized to sit

along the phylogentic stem of Testudinoidea (Danilov

and Sukhanov, 2001). We purposefully did not use the

fossil taxon ‘ Echmatemys’ as an outgroup taxon

(Hirayama, 1985), because its phylogenetic position out-

side of Testudinoidea or even ‘Batagurinae’ is not suffi-

ciently demonstrated.

All figures were produced using digital photogra-

phy and processed using Adobe Photoshop. Images were

digitally enhanced using the burn and burnish tools and

the unsharp mask filter option.

Taxonomic and Systematic Background. - Despite the

increased attention directed towards testudinoids by sci-

entists, hobbyists, and nonprofessional enthusiasts in the

last thirty-five years, our collective conceptualization of

the higher-level (beyond the specific and generic) sys-

tematics within this clade remained virtually unchanged

since the work of McDowell (1964). The various tax-

onomies in current use owe their existence in large part

to historical contexts that are not well appieciated by

many authors. A brief summary is given here.

During the second half of the 19th century, a num-

ber of attempts were made to work out higher-level tes-

tudinoid relationships and to apply taxonomic conven-

tions that were designed (to a greater or lesser extent) to

communicate conceptualizations of these relationships.

In his synopsis on the turtles of North America, Agassiz

(1857) united all pond turtles into the Emydoidae and

subdivided this group into a three monotypic subfami-

lies (Deirochelyoidae for reticularia, Evemydoidae for

blandingii, Cistudinina for T. ornata and Carolina ) fol-

lowed by the subfamilies Clemmydoidae (for G. insculp-

ta, guttata, marmorata, and muhlenbergii ) and

Nectemydoidae (for those species currently placed in the

genera Pseudemys, Trachemys, Graptemys , Malaclemys

and Chrysemys). Most land tortoises were placed in

Testudinidae by Theobald (1868); he also included all

‘leaf turtles and tortoises’ (e.g., amboinensis, emys, den-

tata, grandis, tricarinata ) in Geoemydidae, and an

eclectic group of aquatic turtles, including mega-

cephalum, serpentina, kinostemids, and all remaining

testudinoids, in Emydidae. Subsequently, all land tor-

toises (including emys and impressa) were united in the

Testudinidae by Gray (1870). Those species currently

placed in Pseudemys and Trachemys were assigned by

Gray (1870) to the Pseudemydae; the Asian taxa baska,

borneoensis, thurjii, kachuga, and ocellata were

assigned to the Bataguridae, and all hinged pond turtles,

‘true terrapins,’ and ‘snail-eating pond turtles’ to the

Holarctic families Cistudinidae, Emydidae, and

Malaclemmydae, respectively.

Despite these early attempts, most subsequent

authors (e.g., Boulenger, 1889; Siebenrock, 1909;

Lindholm, 1929; Smith, 1931; Bourret, 1941) ignored

(or were unaware of) these works and simply divided all

testudinoid turtles into two speciose subgroups: tortois-

es (Testudinidae or Testudininae) and pond turtles

(Emydidae or Emydinae). This situation remained static

for nearly 100 years until the comprehensive and influ-

ential work of McDowell (1964). He not only divided all

known pond turtles into several species complexes

(‘ Hardella,' ‘ Batagur ,’ ‘ Orlitia ,’ ‘ Geoemyda ,’

‘ Chrysemys ,’ ‘ Deirochelys,' and ‘ Emys ’ complexes), but

also concluded that pond turtles can be divided clearly

into two subgroups, the predominantly North American

‘Emydinae’ and the Asian and central American

‘Batagurinae.’ Furthermore, McDowell (1964) reasoned

that tortoises are not the sister group of pond turtles, but

rather were likely derived from a ‘batagurine’ ancestor.

These conclusions were later corroborated by the first,

and to date only, comprehensive morphological cladistic

analysis of ‘batagurine’ systematics (Hirayama, 1985).

The influence of McDowell’s (1964) work is best

understood when considering its continuous impact on

Vol. 10, p. 56

Asiatic Herpetological Research

2004

subsequently proposed phylogenies. Despite differences

of opinion regarding generic- and species-level system-

atic arrangements, virtually all major synthetic works in

the last thirty years followed McDowell’s (1964) subdi-

vision of pond turtles into the ‘Batagurinae’ and

‘Emydinae' (e.g., Mlynarski, 1976; Pritchard, 1979;

Ernst and Barbour, 1989), even though 'Batagurinae’

may best be regarded as a paraphyletic taxon

(McDowell, 1964; Hirayama, 1985). The fundamental

division proposed by McDowell is also reflected in more

recent studies centered on using various molecular tech-

niques to elucidate phylogeny, the majority of which

dealt with treatments of in-group relationships within

one or the other of McDowell’s groups (Sites et al.,

1984; Bickham et al., 1996; Carr and Bickham, 1986;

Wu et al., 1999; McCord et al., 2000; Feldman and

Parham, 2002; Honda et al., 2002; Iverson et al., 2002;

Stephens and Wiens, 2003).

Admittedly, the list of autapomorphic characters

compiled by Crumly (1985) for the ‘Testudininae’ com-

pellingly corroborates the hypothesis of tortoise mono-

phyly. However, most characters that currently unite

‘Emydinae’ or ‘Batagurinae + Testudininae’ seem to

support these groupings weakly, because the derived

states typically are not found within all species of the

ingroup and commonly also are observed in species of

the alleged sister group (e.g., Hirayama, 1985; Gaffney

and Meylan, 1988). In addition, several of the characters

that purportedly distinguish ‘Batagurinae +

Testudininae’ from the ‘Emydinae’ probably should be

considered primitive for the entire group (Gaffney and

Meylan, 1988). Even if some characters do successfully

unite a group, monophyly is not established until the

involved characters are demonstrated to be derived with-

in Testudinoidea. Furthermore, the simple demonstra-

tion of monophyly for a given group does not automati-

cally imply that it must be the sister to the remaining

taxa. For instance, ‘Emydinae’ may be monophyletic,

but monophyly does not necessarily demand that

‘Emydinae’ be regarded as the sister to ‘Batagurinae +

Testudininae.’ It is at least plausible that ‘Emydinae’ is

situated within ‘Batagurinae,’ a possibility that is not

adequately explored and tested in the literature.

Similarly, most of the groupings considered by

Gray (1855, 1870) and Agassiz (1857) were not dis-

cussed in recent literature, even though they might be

valid. For instance, given the considerable list of mor-

phological similarities that are shared by hinged turtles

of the New and Old World (e.g., development of a plas-

tral hinge, reduction of posterior neural elements, fusion

of the femoral trochanter, great reduction of the tempo-

ral arch) perhaps Gray (1870) was truly visionary in

uniting these turtles as the ‘Cistudinidae.’ Only a global

cladistic analysis with no a priori assumption regarding

internal relationships can evaluate these alternatives and

produce testable results. It is toward this end that we

offer our critical reappraisal of morphological characters

in testudinoids.

Results and Discussion

Cranium

(1) Shape of the fissura ethmoidalis; 0 = narrow or

closed, keyhole-shaped, Fig. 1; l = very wide, Fig. 2

(modified from Crumly, 1982, 13; Hirayama, 1985, 1;

McCord et al., 1995, 5).

The general configuration of the fissura in ‘emy-

dids’ and ‘batagurids’ is keyhole-shaped (McDowell,

1964). Different proportions and widths are apparent

(especially in the ventral part of the fissura), and were

scored by Hirayama (1985) and Crumly (1982) as dis-

crete character states. Our survey of many taxa reveals

morphological intermediates, and the expression of var-

ious states appears to have an ontogenetic component in

which younger individuals exhibit a relatively larger fis-

sura, which corresponds to a less-ossified nasal cavity.

However, a rather significant morphological gap can be

observed between tortoises and pond turtles. For the

purpose of this review, we lumped Hirayama’s (1985)

states into our state 0, and Crumly ’s (1982) into our state

1. The scoring presented by Hirayama (1985) and

McCord et al. (1995) permitted phylogenetic resolution

within ‘batagurids’, and that of Crumly (1982) within

tortoises. Our revised scoring permits support only for

the hypothesis of a monophyletic ‘Testudinidae.’

Polarity: Pleurodires lack a defined fissura eth-

moidalis. A keyhole-shaped fissura ethmoidalis is pres-

ent in spinifera, odoratus, caretta, serpentina , and

Mongolemys, and this condition is considered primitive

for testudinoids.

(2) Medial inflection of the inferior descending process-

es of the frontal; 0 = absent, or very small, Fig. 3; 1 =

present, well-developed, medial contact present or

almost present, Fig. 4 (modified from Hirayama, 1985,

2).

In most turtles, a gutter (the sulcus olfactorius) is

formed along the ventral surface of the ffontals. This

gutter transmits the olfactory nerve. The lateral rims of

the sulcus sometimes form processes that descend ven-

tromedially to surround the nerve from below

(McDowell, 1964). According to Hirayama (1985) these

processes are well-developed, or are in contact medially,

in ocellata and hamiltonii. We confirm the presence of

well-developed processes in these taxa and add petersi,

N. platynota, and all sampled tortoises to the list. We

recommend that this character not be subdivided into

additional character states, because the descending

processes of the ffontals grow larger through ontogeny.

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Asiatic Herpetological Research

Vol. 10, p. 57

Polarity: A medial inflection is absent in all out-

groups and the vast majority of the ingroup. We consid-

er its presence to be derived.

(j) Frontal contribution to the orbital rim; 0 — present,

no prefrontal/postorbital contact on dorsal surface, Fig.

5; 1 = absent, frontal excluded from orbital rim by pre-

frontal/postorbital contact, Fig. 6 (modified from

Crumly, 1982, 17; Hirayama, 1985, 3; Shaffer et al.,

1997, 97; Yasukawa et al, 2001, 1).

Three states for this character were scored by

Hirayama (1985) and Yasukawa et al. (2001): frontal

contribution always or usually present, frontal some-

times excluded from orbital rim, and frontal always

excluded from orbital rim. Our sample size for many

taxa does not permit a reliable assessment of intraspecif-

ic variation in this character, and thus our initial scores

differed for some taxa from those of Hirayama (1985).

We add peter si and N. platynota to the list of taxa in

which the frontal appears always to be excluded. For

those taxa that sometimes exclude the frontals, we con-

firm this polymorphic condition in crassicollis, and add

agassizii and annulata. Our sample was too small to

confirm the reported polymorphic condition in

amboinensis , and pulcherrima by Hirayama (1985) and

Yasukawa et al. (2001), but we scored these taxa as

polymorphic based on their observations. We also fol-

lowed Crumly (1982) by coding pardalis as polymor-

phic, even though we were not able to observe this in our

sample. Our coding differs from that of Shaffer et al.

(1997) for Heosemys and reeves ii. In their analysis, they

used spinosa (in which the frontal contributes to the

orbital rim), but we used grandis (in which it does not).

In both specimens of reevesii available to us, the frontal

clearly does not participate in the orbital margin. Given

the contrary statement by Shaffer et al. (1997), reevesii

may be polymorphic for this character.

Polarity: The frontal participates in the orbital rim

in pleurodires and spinifera , it is excluded in odoratus

and caretta, and it is polymorphic in serpentina. No pat-

tern is apparent within the ingroup. Given that the

frontal clearly contributes to the orbital rim in

Mongolemys, we consider its absence to be derived.

(4) Contact between jugal and pterygoid; 0 = present,

medial process of jugal well-developed and touching the

pterygoid, Fig. 7; 1 = absent, medial process reduced,

Fig. 8 (modified from Hirayama, 1985, 11, 12; McCord

et al., 1995, 3; Burke et al, 1996, 23; Yasukawa et al,

2001, 4, 5).

The jugal of most testudinoid turtles is expanded at

its ventral end to form a medial process that contacts the

pterygoid medially (McDowell, 1964). Presence or

absence of the medial process, and presence or absence

of a medial contact with the pterygoid were treated as

two characters by Hirayama (1985) and Yasukawa et al.

(2001). The scoring for the two characters appears to be

redundant and we followed the recommendation of

Gaffney and Meylan (1988) by combining them.

We confirm the loss of a medial contact between the

jugal and the pterygoid in galbinifrons, flavomarginata,

and mouhotii (Hirayama, 1985; Yasukawa et al., 2001),

but we found this condition to be polymorphic in speng-

leri (also reported by McCord et al., 1995), and in triju-

ga. Our observations are concordant with those of Burke

et al. (1996).

Polarity: A contact between the jugal and pterygoid

in present in spinifera , odoratus, and serpentina , but is

absent (although the two bones closely approach one

another) in caretta. We conclude that the contact

between the two bones is the primitive condition for tes-

tudinoids and that their separation is derived, a conclu-

sion also reached by Hirayama (1985). Our polarity

determination is opposite that used by McCord et al.

(1995), who mistakenly claimed to have derived their

polarity assessment from Hirayama (1985).

(5) Contact between jugal and palatine; 0 = absent, Fig.

9; 1 = present, Fig. 10 (Gaffney and Meylan, 1988,

F5.4).

The presence of a contact between the medial

process of the jugal and the palatine was used previous-

ly in support of a monophyletic Deirochelyinae

(Gaffney and Meylan, 1988). We confirm the formerly

observed distribution of this character within ‘emydids’

with the exception of reticularia, which does not exhib-

it a contact. A contact is present in numerous

‘batagurids,’ such as borneoensis, reevesii, and hamil-

tonii, but was absent in all examined members of

‘Testudinidae.’

Polarity: A contact between the jugal and the pala-

tine is present in caretta, odoratus, and pleurodires, but

is absent in spinifera and serpentina. A contact is absent

in Mongolemys. We consequently consider its presence

to be derived.

(6) Contact of the epipterygoid with the jugal; 0 = clear-

ly absent, Fig. 11; 1 = present, or almost present,

epipterygoid forms a long lateral process that approach-

es the jugal, Fig. 12 (Gaffney and Meylan, 1988, F8.1;

Shaffer et al., 1997, 106).

According to Gaffney and Meylan (1988) the

epipterygoid and the medial process of the jugal

approach one another or are in contact in reticularia and

the various species they included in Pseudemys and

Trachemys. They also noted a contact between these two

elements in species they classified in Graptemys, but the

condition in those taxa was interpreted to be a result of

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Asiatic Herpetological Research

2004

the medial expansion of the jugal and not a lateral

expansion of the epipterygoid, and consequently was

regarded as non-homologous (Gaffney and Meylan,

1988). We confirm the contact or near contact of these

two elements in reticularia, decor ata, scripta, alaba-

mensis, P. nelsoni, rubriventris, texana , flavimaculata,

geographica , kohnii, nigrinoda , G. ocidifera, ouachiten-

sis, and versa , and also report it in picta and terrapin.

Contact was clearly absent in the specimens of harbour i,

ernsti, and gibbonsi we examined. We made no assess-

ments of homology, but accept any contact between

these two elements as the derived state (as was done by

Shaffer et al., 1997). Among ‘batagurids,’ we also found

a close approach in reevesii.

Polarity: A contact, or near contact, between the

epipterygoid and the jugal is absent in all outgroups and

the vast majority of the ingroup. We consider its pres-

ence to be derived.

(7) Contact of the inferior process of the parietal with

the medial process of the jugal; 0 = absent, Fig. 13; 1 =

present, Fig. 14 (Hirayama, 1985, 13).

Our coding differs significantly from that of

Hirayama (1985). In reevesii , N. platynota, and bealei

we found no contact between the parietal and jugal,

although these were the only three taxa in which

Hirayama (1985: table 2) scored it to be present.

However, we found a pronounced contact between these

two elements in subtrijuga, a species scored by

Hirayama (1985: table 2) as lacking such a contact, but

shown on his tree (Hirayama, 1985: fig. 2) as a unique

‘batagurid’ feature convergent with some ‘emydids.’

Among ‘emydids,’ a well-developed contact occurs in

barbouri and other broad-headed species currently clas-

sified in Graptemys.

Polarity: There is no contact between the inferior

process of the parietal and the medial process of the

jugal in all outgroups and the vast majority of the

ingroup. A contact is considered to be the derived condi-

tion.

(8) Contact of the inferior process of the parietal with

the maxilla; 0 = absent, Fig. 13; 1 = present, Fig. 14

( Hirayama , 1985, 14).

Our coding differs from that of Hirayama (1985).

According to his character matrix (table 2) a contact

should be present between the inferior process of the

parietal and the maxilla in reevesii and mouhotii, but his

cladogram (fig. 2) indicated that the presence of a con-

tact should be regarded as a uniquely derived autapo-

morphy of subtrijuga. We found no contact in reevesii or

mouhotii. Of the testudinoid species we examined, sub-

trijuga is the only one that shows this feature.

Polarity: There is no contact between the inferior

process of the parietal and the maxilla in all outgroups.

Its presence is considered to be derived.

(9) Extent of quadratojugal; 0 = quadratojugal well

developed, firmly attached to jugal, Fig. 15; 1 = quadra-

tojugal present, contact lost with jugal, Fig. 16; 2 =

quadratojugal so heavily reduced that it appears to be

absent in many skeletal specimens, Figs. 17, 18 (modi-

fied from Hirayama, 1985, 16; Shaffer et al., 1997, 47;

Burke et al., 1996, 21; McCord et al., 1995, 6; Yasukawa

et al., 2001, 7, 8).

Variation in the structure of the temporal region of

turtles was discussed in detail by Zdansky (1924) and

comments specific to testudinoids were provided by

Zangerl (1948) and McDowell (1964). We originally

scored the reduction of the quadratojugal as three differ-

ent characters: loss of contact with the jugal, loss of con-

tact with the squamosal, and the apparent loss of the

quadratojugal. All five logically possible combinations

were observed, but in most testudinoid turtles the tem-

poral arch is so slender that the contact between the

quadratojugal and squamosal is commonly reduced to a

sliver that would have to be scored as ‘just barely pres-

ent’ or ‘just barely absent.’ We therefore abandoned our

efforts to evaluate the contact between the quadratojugal

and squamosal. Our observations generally agree with

those of McDowell (1964), Hirayama (1985), Burke et

al., (1996), McCord et al. (1995), and Yasukawa et al.

(2001).

We purposefully avoid addressing the apparent lack

of a quadratojugal in many species as an absence,

because previous work by Zdansky (1924) showed that

the quadratojugal of some ‘batagurids’ is so poorly ossi-

fied and connected to the surrounding elements that it

tends to be lost in skeletal specimens (Figs. 17, 18). An

example of this problem can be found among the many

conflicting statements made regarding the presence of

this element in N. platynota (e.g., Smith, 1931; Bourret,

1941; McDowell, 1964; Ernst and Barbour, 1989).

Polarity: The quadratojugal is present and firmly

attached to the jugal in all outgroups, with the exception

of chelids. Its reduction is considered to be derived.

(10) Contribution of jugal to the rim of upper temporal

emargination (Hirayama, 1985, 15); 0 = absent, Figs.

19, 20; 1 = present, Fig. 21.

Participation of the jugal in the rim of the upper

temporal emargination was reported previously in

hamiltonii and ocellata (Hirayama, 1985). We confirm

its presence in both species, but in one of the hamiltonii

specimens we examined (MCZ 120333) the jugal forms

a significant part of the rim only on one side of the skull;

on the other side, which appears abnormal and likely

represents a teratology, it does not. In all other species

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Vol. 10, p. 59

available to us, the jugal does not participate in the rim.

In subtrijuga, the jugal is excluded from the upper tem-

poral emargination by narrow extensions of the postor-

bital and quadratojugal (Fig. 20).

Polarity: The jugal participates in the upper tempo-

ral rim ot spinifera , but it is excluded in odoratus, caret-

ta , serpentina , Mongolemys , and most pleurodires. We

consider the participation of the jugal in the rim of the

upper temporal emargination to be the derived condition

within testudinoids.

(11) Contact between the quadratojugal and the articu-

lar facet of the quadrate; 0 = absent, Fig. 22; l = pres-

ent, quadratojugal sends a process ventrally along the

rim of the cavum tympani and touches the lateral edge

of the articular facet, Fig. 23 (modified from Hirayama,

1985, 17).

The original character definition (Hirayama, 1985,

character 1 7) is inappropriate, because the jugal does not

contact the articular surface of the quadrate in any turtle

except for madagascariensis and dumerilianus (Gaffney

and Meylan, 1988). However, because Hirayama indi-

cated in his tree that the only ‘batagurid’ taxon to exhib-

it this character is subtrijuga , we assume that he was

referring to a contact between the quadratojugal and the

articular facet of the quadrate, a characteristic of subtri-

juga only among testudinoids. A contact between the

two elements was reported previously for reevesii in the

character matrix published by Hirayama (1985), but we

conclude that this must be a publishing error, because it

stands in conflict with his tree. In the specimens of

reevesii available to us, there is no contact. It is possible

that the scoring for subtrijuga and reevesii were flipped,

at least in part, in the Hirayama (1985) matrix (in which

the taxa were listed next to one another).

Polarity: A contact between the quadratojugal and

the articular surface of the quadrate is absent in

spinifera , but present in odoratus , caretta, and serpenti-

na, and consequently could be considered primitive.

However, based on ingroup commonality and the

absence of a contact in Mongolemys , we consider a con-

tact to be derived for Testudinoidea.

(12) Contact between quadratojugal and maxilla; 0 =

absent, Fig. 22; 1 = present, Figs. 23, 24 (Hirayama,

1985, 18).

According to Hirayama (1985), among ‘batagurids’

a contact between the quadratojugal and maxilla is only

present in subtrijuga and reevesii. We did not find a

contact in our specimens of reevesii , but confirm its

presence in subtrijuga.

Gaffney and Meylan (1988) listed a contact

between the quadratojugal and maxilla as a synapomor-

phy for Platystemina {megacephalum + ‘ Chelydropsis'}

and as an independently evolved synapomorphy for

Kinostemidae, whereas Shaffer et al. (1997) noted a

contact to be present in Kinostemidae, C. insculpta, and

megacephalum. Our observations confirm the presence

of a contact in all of these extant groups. Among testudi-

noids, subtrijuga is unique in having an extensive con-

tact in lateral view (Fig. 23). In several ‘emydids,’ a con-

tact is present on the inside of the temporal arch ( bar -

bouri, and nigrinoda; polymorphic in geographica , G.

oculifera, and texana; Fig. 24). For now, we scored all

taxa as present, regardless of whether the contact is vis-

ible in lateral view, medial view, or both. In several other

‘emydid’ taxa, the bones closely approach one another,

but do not actually meet, on the inside of the temporal

arch ( alabamensis , ernsti, flavimaculata, gibbonsi,

kohnii, P. nelsoni ).

Polarity: A contact is present between the quadrato-

jugal and maxilla in odoratus, but absent in spinifera,

caretta, serpentina, and Mongolemys. We consider the

presence of a contact to be derived for Testudinoids.

(13) Medial contact of the maxillae along the anterior

margin of the jaw; 0 = absent, Figs. 25, 26; 1 = present,

Fig. 27 (modified from Hirayama, 1985, 20; McCord et

al., 1995, 2; Yasukawa et al., 2001, 10).

In most testudinoids, the anteromedial ends of the

maxillae are separated medially by the premaxillae

along the anterior margin of the jaw (Fig. 25). Hirayama

(1985) noted that the maxillae have a medial contact in

some ‘batagurids,’ which was confirmed by McCord et

al. (1995) and Yasukawa et al. (2001) for spengleri and

several other species that they included in the genus

Geoemyda. We found a broad medial contact of the max-

illae in spengleri and annulata (Fig. 27). In some

species, the maxillae approach one another along the

ventral rim of the nasal opening (e.g., amboinensis,

mouhotii, pulcherrima, crassicollis ), but a well-devel-

oped contact is never present (Fig. 26).

Polarity: The maxillae do not meet medially along

the anterior margin of the jaw in odoratus, caretta , ser-

pentina, and Mongolemys. A medial contact is present in

spinifera but only along the ventral border of the exter-

nal nares. We consider a medial contact along the ante-

rior margin of the jaw to be the derived condition with-

in Testudinoidea.

(14) Size of the foramen orbito-nasale; 0 = small, less

than 1/6 of orbit length, Figs. 28, 29; 1 = large, more

than 1/6 of orbit length, Fig. 30 (modified from

Hirayama, 1985, 33; Gaffney and Meylan, 1988, F9.3,

FI 0.2, G10.3, HI 1.1, HI 6.3; Crumly, 1982, 25; Crumly,

1994, 12).

We were cautious when first approaching this char-

acter due to the inconsistent usage and definition of

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Asiatic Herpetological Research

2004

small and ‘large’ by various authors. However, after

assessing the size ot this foramen based on its size rela-

tive to the length of the orbit, we were surprised to see

that we were able to reproduce Hirayama’s (1985) scor-

ing for the ‘batagurids’ without too many difficulties. In

contrast, our initial observations of tortoises were in

stark contrast to those of Crumly (1982, 1985, 1994) and

Gaffney and Meylan (1988). This may be due to the thin

nature of the palatine of many tortoises, and the relative

ease with which that part of the palate can be damaged

during skeletal preparation and handling. Furthermore,

the foramen becomes progressively more closed with

increased ontogenetic age (Crumly, 1982). We encoun-

tered similar problems in attempting to score reticularia

and blandingii. Because we deem this character to be

potentially useful for helping to resolve phylogeny with-

in ‘batagurids’ and ‘emydids,’ we decided to score all

testudinoids with delicate palatines (i.e., all tortoises,

reticularia , and blandingii ) as ‘unknown.’ We acknowl-

edge that our redefinition of the character is still subjec-

tive and somewhat problematic, but using this definition

we were able to unambiguously score all the ingroup

taxa we examined.

Polarity: The foramen orbito-nasale is large in ser-

pentina, odoratus, and spinifera, but small in caretta.

We consider presence of a large foramen orbito-nasale to

be the derived condition within testudinoids, because the

foramen is small in Mongolemys.

(15) Contact between maxilla and vomer; 0 = present,

Fig. 31; 1 = absent, vomer separated from the maxilla

by the premaxilla, Fig. 32 (Hirayama, 1985, 31; Crumly,

1982, 21; Yasukawa et al., 2001, 14).

We generally agree with previous scorings for this

character (Hirayama, 1985, Crumly, 1982, Yasukawa et

al., 2001). We confirm the absence of a contact in

amboinensis and pulcherrima, but our scoring differs

slightly for those taxa that Hirayama (1985) coded as

‘intermediate apomorphic,’ a character state that we

interpret as polymorphism. Of those taxa that Hirayama

(1985) and Yasukawa et al. (2001) scored as intermedi-

ate (flavomarginata, caspica, annulata ), our sample size

is too small to confirm whether both character states are

present. We consequently follow these authors by scor-

ing those taxa as polymorphic.

Polarity: A contact between the maxilla and vomer

is present in all outgroups. The loss of this contact is

derived for testudinoids.

(16) Size of the foramen palatinum poster ius; 0 = large,

Fig. 33; 1 = small, Fig. 34 (modified from Hirayama,

1985, 22; Gaffney and Meylan, 1988, F2.2, F6.1;

McCord et al., 1995, 4; Yasukawa et al., 2001, 12).

Our characters 16 and 17 were published originally

by Hirayama (1985) as one character that combined two

morphological features: the size of the foramen palat-

inum posterius (f.p.p.) and participation of the pterygoid

in the margin of the f.p.p. Although four possible com-

binations of these features are logically possible, only

two were originally included (participation present,

f.p.p. large; participation absent, f.p.p. small). Gaffney

and Meylan (1988) also used this character within ‘emy-

dids,’ but their character applied only to the exclusion of

the pterygoid from the f.p.p. We decided to subdivide

Hirayama’s (1985) character into one character that

describes the size of the f.p.p. and a second that address-

es the position of the pterygoid relative to the f.p.p.

We found no difficulty in identifying the f.p.p. as

‘large’ or ‘small,’ (Figs. 33 and 34, respectively), and no

ambiguous condition was encountered. Because our

character definition only includes two character states,

our scorings do not reflect those of other workers with a

more limited target group (e.g., McCord et al., 1995). In

juveniles the f.p.p. tends to be larger, but during later

ontogenetic stages the f.p.p. is slowly reduced in size.

Polarity: The f.p.p. is small in odoratus, spinifera,

and most pleurodires; it is absent in caretta, but is large

in serpentina and Mongolemys. We consider a small

f.p.p. to be the derived state.

(17) Position of the pterygoid relative to foramen palat-

inum posterius (f.p.p.); 0 = pterygoid situated posterior

to the f.p.p., Fig. 33; 1 = pterygoid situated posterior to

the f.p.p., but sends a process anterior and lateral to the

f.p.p., Fig. 34.

Our survey of testudinoids indicated that reliable

assessment of participation of the pterygoid in the f.p.p.

may be difficult because many species show an ontoge-

netic change in configuration of this part of the palate. In

juveniles, the f.p.p. typically includes the pterygoid in its

posterior margin. During later ontogenetic stages the

pterygoid is excluded. In spite of this, it appears that the

relative position of the pterygoid tends to stay constant

during ontogeny.

Polarity: The anterior end of the pterygoid is situat-

ed posterior to the f.p.p. in odoratus, serpentina, most

pleurodires, and Mongolemys, but is situated lateral to

the f.p.p. in spinifera. We consider a posterior position to

be primitive for Testudinoidea.

(18) Epipterygoid participation in the trigeminal fora-

men; 0 = absent, Fig. 35; 1 = present, epipterygoid

clearly separates the parietal and pterygoid in lateral

view, Fig. 36.

The anteroventral rim of the trigeminal foramen of

most testudinoid turtles is formed by the parietal and

pterygoid. The epipterygoid commonly comes close to

the foramen, but does not form part of it. In spengleri

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Vol. 10, p. 61

and mouhotii , the epipterygoid consistently participates

in the margin of the trigeminal foramen thus separating

the parietal and pterygoid, at least in lateral view.

Polarity: The epipterygoid forms part of the

anteroventral rim of the trigeminal foramen in the

majority of outgroups, with the exception of pleurodires

that lack a definitive ossified epipterygoid (Gaffney,

1979). The condition is unclear for Mongolemys.

However, within the ingroup we found this character

only in the seemingly rather specialized turtles spengleri

and mouhotii. We consequently consider its presence to

be secondarily derived.

(19) Vomerine foramen ; 0 = absent, Fig. 37; 1 = pres-

ent, Fig. 38 (Gaffney and Meylan, 1988, H4.1; Crumly,

1994, 15).

The vomerine foramen (= anteromedial vomerine

aperture of Crumly, 1982 and 1994 [in part]) is a small

opening that pierces the vomer along the midline just

posterior to the foramen praepalatinum (Bramble, 1971).

The presence of a vomerine foramen was noted in agas-

sizii and berlandieri by Bramble (1971), and was used

by Gaffney and Meylan (1988) to unite various species

currently placed in Gopherus as a clade. Its irregular

presence in elegans, elongata, chilensis, and radiata

was reported by Crumly (1982). Specimens in our sam-

ple enable us to confirm its presence in agassizii,

berlandieri , and chilensis.

Polarity: The vomerine foramen occurs in only a

few ‘testudinids’ and it is absent in all outgroups. Its

presence is considered derived for Testudinoidea.

(20) Development of the foramen praepalatinum as a

canal (canalis praepalatinum) that is concealed by a

bony secondary palate in ventral view; 0 = absent, Fig.

39; 1 = present, Fig. 40 (modified from Hirayama, 1985,

24).

In most testudinoids, the foramen praepalatinum is

a small opening that connects the nasal cavity with the

roof of the oral cavity (Fig. 39). However, in a number

of taxa with extensively developed secondary palates,

the anterior nasal artery passes through an elongated

canal that is concealed in ventral view by the bony sec-

ondary palate (e.g., baska , tentoria , petersi: ; Fig. 40). We

refer to this structure as the canalis praepalatinum. Our

scorings are fully consistent with those of Hirayama

(1985).

Polarity: The foramen praepalatinum is absent in

spinifera (Gaffney, 1979) and caretta (Nick, 1912), and

is developed as a true foramen that is exposed in ventral

view in odoratus, serpentina , and Mongolemys. The

development of a canalis praepalatinum is considered

the derived condition within Testudinoidea.

(21) Contact between pterygoid and basioccipital; 0 =

present, Fig. 41; 1 = absent, Fig. 42 (modified from

Gaffney and Meylan, 1988, FI. I, F10.3, H18.3; Crumly,

1994; Shaffer et al., 1997, 103).

Two of the most often-cited characters that purport-

edly help to distinguish the ‘Emydidae’ from the

‘Bataguridae’ are the batagurine process and the contact

between the pterygoid and the basioccipital (McDowell,

1964). Both traits are commonly combined as one char-

acter (e.g., Gaffney and Meylan, 1988) and even seem to

have been confused with one another (e.g., Mlynarski,

1976; Shaffer et al., 1997). The batagurine process is a

poorly-defined feature that, in McDowell’s original

usage (1964) appears to consist of a lateral process of

the basioccipital that floors the recessus scalae tympani.

Many testudinoid species (including non-‘batagurines’)

have a laterally-projecting process of the basioccipital; it

may or may not floor the recessus scalae tympani, but it

is often obscured from view in articulated specimens.

When disarticulated material is examined, a broader dis-

tribution of this feature (assuming it is interpreted as we

have done above) across testudinoids is revealed.

Within Testudinoidea, the pterygoid commonly

sends a process posteriorly and contacts the basioccipi-

tal just lateral to the basisphenoid. This character

appears to be absent in most ‘emydids,’ but is present in

terrapin and those species that are currently attributed to

Graptemys (Gaffney and Meylan, 1988). We noticed a

strong ontogenetic component to this character within

‘emydids.’ The pterygoid is commonly rather short dur-

ing younger ontogenetic stages, but finally reaches the

basioccipital in later stages. For instance, among our

specimens of terrapin, orbicularis , and texana, the

pterygoid does not contact the basioccipital in younger

individuals, but a clear contact is present in adults. We

score such species as polymorphic, but note that ontoge-

netically influenced polymorphisms are not well

explored in turtles.

Among ‘batagurids,’ we noted a similar pattern.

Contrary to general belief we were not able to observe a

contact between the pterygoid and the basioccipital in all

taxa traditionally classified in this group (e.g., trijuga ,

pulcherrima, sinensis). As with the ‘emydids,’ there

seems to be an ontogenetic effect in which younger

specimens tend not to have a contact. Where recognized,

we scored these species as polymorphic.

We found much conflicting data regarding the dis-

tribution of this character among tortoises (Crumly,

1982, 1985, 1994; Gaffney and Meylan, 1988). Among

the specimens we examined, we note the complete

absence of a contact only in graeca\ polymorphisms

were observed in polyphemus and horsfieldi. Again, an

ontogenetic component is apparent.

Polarity; A contact between the pterygoid and

Vol. 10, p. 62

Asiatic Herpetological Research

2004

basioccipital is present in all outgroups. Its absence is

considered to be derived.

(22) Contact of the pterygoid with the articular facet of

the quadrate ; 0 = absent, Fig. 43; 1 = present, Fig. 44

(Hirayama, 1985, 38).

According to the data matrix published by

Hirayama (1985) he only observed this contact in

reeves ii, however, in his tree (fig. 2) the contact is

mapped as an autapomorphy of subtrijuga. We confirm

the presence of a contact between the posterior process

of the pterygoid and the articular surface of the quadrate

in subtrijuga. It is the only taxon we examined that dis-

plays the derived condition.

Polarity: A contact between the pterygoid and the

articular surface of the quadrate is absent in all out-

groups and the vast majority of the ingroup. We consid-

er its presence to be derived.

(23) Closure and depth of the incisura columella auris;

0 = absent, incisura is open, Fig. 44; 1 = present,

incisura closed, Fig. 45 (Crumly, 1985; Gaffney and

Meylan, 1988, HI. 3).

The incisura columella auris is a notch that is

formed by the quadrate and that holds the stapes and

eustachian tube (Gaffney, 1972). In a number of turtles,

the incisura closes to fully surround the stapedial shaft

(Gaffney and Meylan, 1988). Within testudinoids, the

incisura evidently is closed in most tortoises (Crumly,

1985). We are able to confirm the presence of such a

closed incisura in all ‘testudinids’ we examined with the

exception of one specimen of kleinmanni (CAS

228431), the smallest of the species now classified in

Testudo. In a number of ‘batagurids’ and ‘emydids’ the

incisura commonly is very narrow and even appears to

be closed, however, a closer look under the microscope

combined with a probing needle reveals that this appar-

ent closure is produced by dry tissues that remain in this

area in many articulated skulls. The only ‘batagurid’ for

which we sometimes found a closed incisura is N.

platynota; in that species the quadrate does not fuse

together forming a solid ring behind the incisura, but this

is also the case for many tortoises (e.g., some belliana,

emys, some homeana, some kleinmanni). In some cases,

the polymorphism we noted (e.g., in belliana and home-

ana) appears to be a result of ontogenetic age, with older

individuals displaying a greater degree of fusion at the

posterior part of the incisura.

Polarity: The polarity of this character is somewhat

ambiguous, because the incisura columella auris is

closed in serpentina and spinifera , but open in caretta

and odoratus. We conclude that its presence is derived

within testudinoids because it is absent in Mongolemys.

Mandible

(24) Angular contribution to the sulcus cartilaginis

Meckelii; 0 = present, the angular contributes to the sul-

cus and is as long or longer than the prearticular, Fig.

47; 1 = absent, the angular is shorter than the preartic-

ular, Fig. 48 (modified from Gaffney and Meylan, 1988,

FI. 4).

A broad contact of the angular with Meckel’s carti-

lage was used by McDowell (1964) to characterize the

‘Emydinae’ and later used by Gaffney and Meylan

(1988) as a synapomorphy to unite the same grouping.

As it was originally worded, this character is difficult to

observe in its literal sense for most museum specimens,

because the Meckel’s cartilage usually is not present in

modern and fossil skeletal specimens. We suggest that

the spirit of McDowell’s (1964) character can be evalu-

ated by examining the participation of the angular in the

sulcus cartilaginis Meckelii. We confirm that a small to

broad angular contribution is present in all ‘emydids’

with the exception of rubriventris. In most ‘batagurids,’

the angular is a short bone that does not participate in the

sulcus and barely spans half the distance the prearticular

does. However, a small but clear contribution to the sul-

cus is present in an eclectic group comprised of baska ,

dentata, thurjii , punctularia, and some grandis. We were

not able to carefully evaluate potential polymorphisms

in these taxa.

Polarity: An angular contribution to the sulcus car-

tilaginis Meckelii is present in all cryptodiran outgroup

taxa. We consider is absence to be derived.

(25) Contact between surangular and dentary; 0 =sim-

ple contact, Fig. 49; 1 = strongly interdigitated suture,

Fig. 50 (Crumly, 1982, 12; Crumly, 1985; Gaffney and

Meylan, 1988, H6.1).

In most testudinoids, the surangular and dentary

meet along the lateral side of the mandible in a simple,

overlapping contact. According to Crumly (1982, 1985),

this contact is stabilized through a finger-like process of

the surangular that interdigitates with the dentary in all

tortoises except emys , impressa, and those species he

classified in Gopherus. We confirm the absence of this

character in agassizii, berlandieri, emys, impressa, and

polyphemus, but also did not observe it in areolatus.

Polarity: An interdigitated contact between the

surangular and dentary is absent in all outgroups and the

majority of the ingroup. We consider its presence to be

derived.

(26) Height of the processus coronoideus; 0 = as high as

dentary, Fig. 51; 1 = rising significantly above the den-

tary, Fig. 52 (modified from Hirayama, 1985, 45).

The coronoid of most turtles is a small bone that

produces a minor knobby projection that rises only little

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Asiatic Herpetological Research

Vol. 10, p. 63

above the adjacent dentary, if at all. According to

McDowell (1964) and Hirayama (1985) the coronoid is

larger and rises moderately above the dentary in

borneensis and crassicollis, and in reeves ii and subtriju-

ga the coronoid is very large and produces a robust

process that sits high above the dentary. We confirm

these observations, however, we were also able to

observe moderately developed coronoid processes in

kachuga and tentoria. Among ‘emydids,’ we also

observed moderately developed coronoids in barbouri,

ernsti, jlavimaculata, geographica , gibbonsi, kohnii ,

and terrapin. Unlike Hirayama (1985), we only utilize

one derived character state, because it is difficult to

objectively measure and discretize the relative height of

the coronoid among turtles.

Polarity: The coronoids of caretta, serpentina , and

odoratus are small and do not rise above the dentary, but

the coronoid of spinifera is well developed and forms a

moderate process. The lower jaw is not described for

Mongolemys. We consider well-developed coronoids to

be derived within testudinoids.

(27) Foramen dentofaciale majus; 0 = small, Fig. 53; 1

= large and situated within a large lateral fossa, Fig. 54

(Hirayama, 1985, 47).

The foramen dentofaciale majus of most testudi-

noids is a small opening that is situated on the lateral

side of the mandible, just ventral and slightly anterior to

the coronoid. The foramen dentofaciale majus is greatly

enlarged in thurjii and ocellata and is situated at the

anterior end of an expanded lateral fossa (Hirayama.

1985). We confirm the enlargement in those taxa, and

further note its presence in petersi.

Polarity: The foramen dentofaciale majus is small in

all outgroups and the vast majority of the ingroup. Its

presence is considered to be derived.

Triturating Surfaces

(28) Participation of palatine in the triturating surface

of the upper jaw; 0 = absent, Fig. 55; 1 = present, Figs.

56, 57 (Hirayama, 1985, 26; Gaffney and Meylan, 1988,

F2. 1).

In some testudinoids, the palatine has a ventrolater-

al maxillary process that participates in the triturating

surface of the upper jaw. The degree of participation

varies among taxa, and within some species. A clear and

extensive participation is present in barbouri , ernsti ,

geographica , gibbonsi , petersi , rubriventris, script a,

terrapin, texana , and versa. It is weakly developed in

hamiltonii, ocellata, G. oculifera, ouachitensis, reevesii,

subtrijuga, and some individuals of baska.

Participation was used by Gaffney and Meylan

(1988) to unite Terrapene spp., blandingii , guttata, G.

insculpta, marmorata, muhlenbergii, and orbicularis as

a clade within the ‘Emydidae.’ In our observations, how-

ever, this participation also is absent among other ‘ emy-

dids ’ such as jlavimaculata, kohnii, nigrinoda, picta, and

reticularia (we were not able to evaluate adequately the

potential for polymorphism in these taxa). In addition, it

appears that the absence of a palatine participation rep-

resents the plesiomorphic state for testudinoids, thus

eliminating its value for diagnosing monophyletic

groups.

Polarity: The palatine does not participate in the trit-

urating surface of spinifera, but does so in odoratus,

caretta, and serpentina. The palatine does not participate

in the triturating surface of Mongolemys and only occurs

in Testudinoids with highly derived secondary palates.

We consequently consider the participation of the pala-

tine in the triturating surface to be derived within tes-

tudinoids.

(29) Participation of the vomer in the triturating surface

of the upper jaw; 0 = absent, Figs. 56, 57, 58; 1 - pres-

ent, Fig. 59 (Hiray>ama, 1985, 25).

The triturating surface is the grinding surface of the

jaw. In most turtles, it is formed on the upper jaw pre-

dominantly by the maxilla and premaxilla. However, in

turtles with extensive secondary palates the vomer may

also participate. In texana, the vomer may have a ventral

projection that barely separates the maxillae in the mid-

line, but it does not participate in the triturating surface

proper because it sits in a dorsal concavity within the

palate (Fig. 56). Our scorings differ from those of

Hirayama (1985) for mouhotii (which Hirayama scored

as “intermediate apomorphic” and we score as absent

because it does not have a secondary palate) and subtri-

juga (in our specimens the vomer does not descend to

the palatal surface, but this species may be polymor-

phic). This character is polymorphic in barbouri.

Polarity: Because the vomer does not participate in

the triturating surface of odoratus, spinifera, caretta,

serpentina, and Mongolemys, its participation is consid-

ered to be the derived condition for Testudinoidea.

(30) Presence and number of lingual ridges of the tritu-

rating surfaces of the upper and lower jaws; 0 = no lin-

gual ridges present, Fig. 60; 1 = one lingual ridge pres-

ent, Figs. 61-62; 2 = two lingual ridges present (modi-

fied from Hirayama, 1985, 29, 44; Gaffney and Mey4 an,

1988, F7.2, F9.1)

Most turtles lack lingual ridges on their triturating

surfaces (Fig. 60), but one or two such ridges are devel-

oped in a number of testudinoids (Figs. 61-62). These

ridges run parallel to the labial surface of the maxilla

and dentary, and typically do not meet their counterpart

on the midline. They are not necessarily a continuous

structure (Fig. 61), and may be divided into several com-

Vol. 10, p. 64

Asiatic Herpetological Research

2004

ponents. In some cases, an extensive ridge-like structure

can create the appearance of an additional ridge at the

extreme lingual margin of the maxilla bordering the

internal nares; however, we consider these to be the

thickened rim ot the internal nares rather than an addi-

tional ridge. Among ‘batagurids’ and ‘emydids,’ one lin-

gual ridge is present in alabamensis , borneoensis , deco-

rata, kachuga , P. nelsoni, ocellata, petersi, rnbriventris,

scripta, sinensis, tentoria, texana, and thnrjii. Two lin-

gual ridges are developed in baska. We found lingual

ridges in all tortoises we examined except erosa, bel-

liana , and homeana.

Hirayama (1985) originally scored this character as

two separate characters, one for the mandible and one

for the maxilla. In our observations, the triturating sur-

face of the lower jaw closely mimics that of the upper

jaw, creating an occlusal surface that closely reproduces

the function of cusps in mammalian cheek teeth. Both

characters were scored in parallel in Hirayama’s matrix,

and we see no reason to consider them independent.

Polarity: All outgroups lack lingual ridges on the

triturating surfaces. We consequently consider their

presence to be derived.

(31) Well- dev el oped serrations on labial or lingual

ridges of the triturating surfaces of the upper and lower

jaws; 0 = absent, Fig. 60; 1 = present, Fig. 61 (modified

from Hirayama, 1985, 21, 27, 41, 43, 46; Gaffney and

Meylan, 1988, F9.2; Yasukawa et al., 2001, 11).

Well-developed serrations on the lingual and labial

ridges of the upper and lower jaws are developed in sev-

eral ‘batagurids’ and ‘emydids’. A number of tortoises

and other ‘batagurids’ (e.g., carbonaria, pardalis, sulca-

ta, annulata, and areolata) exhibit serrations on their

ramphothecae, but unlike the bony, tooth-like serrations

of borneoensis, thurjii, petersi, or texana, these crenula-

tions are weakly developed, leaving very little or no

trace of serrations on the underlying bone. In compari-

son to those taxa with well-developed serrations, it very

difficult to establish a consistent scoring system for taxa

with fine crenulations, because many specimens will not

exhibit any serrations, probably due to wear of the ram-

phothecae. Unlike Hirayama (1985) and Yasukawa et al.

(2001) we scored all taxa with such weak serrations as

absent.

Unfortunately, even in those taxa with well-devel-

oped serrations, the serrations are not always evenly

developed on all ridges. We consequently combined all

of Hirayama’s (1985) characters relating to serrations

into one character. Because serrations commonly occur

on all available ridges, this treatment will also help to

avoid unconsciously weighting the presence of serra-

tions with up to five characters. In those taxa that have

them, the ridges themselves often have very different

morphologies; this character needs to be critically

reevaluated with adequate sample sizes for the relevant

taxa.

Polarity: All of our outgroup taxa and the majority

of the ingroup taxa lack strong serrations. We interpret

their presence to be derived.

(32) Median ridge or sulcus of the triturating surface of

the upper jaw; 0 = both structures absent, Fig. 60; l =

median ridge present, Fig. 62; 2 = median sulcus pres-

ent, Fig. 63 (modified from Hirayama, 1985, 30;

Crumly, 1985, 1994, 4; Gaffney and Meylan, 1988,

H3.1).

In a number of testudinoid turtles with partially

developed secondary palates and lingual ridges, addi-

tional structures are formed along the midline of the

upper jaw that typically correspond to reciprocal struc-

tures of the lower jaw. The upper jaw of petersi is char-

acterized by a narrow sulcus (Fig. 63) and the mandible

exhibits a low median ridge. On the other hand, in

baska, borneoensis, thurjii, kachuga, agassizii,

berlandieri, and polyphemus, a ridge runs along the mid-

line (Fig. 62), which typically corresponds to a sulcus in

the lower jaw. An incipient ridge also was reported in

emys (Crumly, 1994), but we were not able to confirm

this on the specimen available to us.

Polarity: A median ridge is absent in all outgroups

and the vast majority of the ingroup. Its presence is con-

sidered to be derived.

(33) Posterior extension of the lower triturating surface

behind the symphysis of the dentary; 0 = absent, Fig.

64; 1 = present, Fig. 65 (Hirayama, 1985, 42; Gaffney

and Meylan, 1988, G5.2).

In several ‘batagurids,’ the triturating surface of the

dentary forms a shelf along the midline that extends so

far posteriorly that the symphysis cannot be seen when

the mandible is observed in dorsal view (McDowell,

1964). Our scorings fully agree with those of Hirayama

(1985) for the ‘Bataguridae,’ but we disagree with

Gaffney and Meylan (1988) who asserted that this char-

acter also occurs in some ‘Emydidae.’ Admittedly, sev-

eral species currently placed in the genera Graptemys,

Pseudemys, and Trachemys have greatly expanded tritu-

rating surfaces of the dentary, but in all of the specimens

available to us, the symphysis is always visible in dorsal

view.

Polarity: An extended triturating surface of the den-

tary does not occur in any outgroup taxon. We consider

its presence to be derived.

Carapace

(34) Carapace strongly tricarinate in adult; 0 = absent,

Figs. 66, 67; 1 = present, Fig. 68 (modified from

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Asiatic Herpetological Research

Vol. 10, p. 65

Hirayama, 1985, F; McCord et al., 1995, 10; Yasukawa

et al., 2001, 24).

Three distinct carapacial ridges are present in the

adults of reevesii, hamiltonii, spengleri , subtrijuga, tri-

juga, and mouhotii. We cannot replicate Hirayama’s

(1985) placement of this character as an autapomorphy

in hamiltonii. In our observations, the carinae in hamil-

tonii are not better developed than in some other taxa. In

fact, they are more weakly developed than those in

mouhotii (Fig. 68). Because keels are present in the

young and subadults of such taxa as crassicollis (Fig.

67), mutica, and sinensis, but disappear with age, and

because we were not able to observe the juveniles of

most species, we restricted this character to those

species that exhibit well-developed tricarinae as adults.

Three keels were reported to be present in the adults of

dentata (McCord et al., 1995), but we cannot confirm

this (tricarinae are not present on our younger speci-

mens).

Polarity: Tricarinae are absent in our outgroup

species ( caretta , odoratus, serpentina , spinifera, gibba,

siebenrocki, subglobosa, and subrufa), but do appear

occasionally in some of their close relatives, such as

scorpioides, temminckii, and fimbriatus. We consider the

presence of tricarinae to be derived within

Testudinoidea.

(35) Significant serration of the posterior peripherals; 0

= absent, Fig. 66; 1 = present, Fig. 68 (modified from

Hirayama, 1985, D; McCord et al., 1995, 11; Yasukawa

et al., 2001, 23).

We generally agree with previous observations

reported for this character (Hirayama, 1985). However,

because the carapace rim is at least slightly serrated in

almost all turtles, we rephrase the character definition to

include only significantly serrated posterior peripherals

as found, for example, in crassicollis, dentata, grandis,

mouhotii, N. platynota, and spengleri. Among the ‘emy-

dids’ and ‘testudinids,’ the peripherals of barbouri,

erosa, fiavimaculata, geographica, homeana, kohnii,

nigrinoda, oculifer, G. oculifera, pseudogeographica,

and versa also are serrated. It is important to note that

our scores are based on the peripheral bones; the amount

of carapacial serration greatly depends on the presence

or absence of the marginal scutes in the specimens used,

because the scutes greatly accentuate the amount of ser-

ration, if present. We find no conflict with the codings of

McCord et al. (1995) and Yasukawa et al. (2001).

Polarity: Serrated posterior peripherals are present

in caretta, but absent in odoratus, serpentina , and most

pleurodires. However, due to ingroup commonality and

its absence in taxa placed within “Lindholmemydidae”

we conclude that its presence is derived.

(36) Carapace of adult tectiform in cross-section with a

strong posterior projection on the third vertebral scute;

0 = absent, Fig. 69; 1 = present, Fig. 70 (Hirayama,

1985, N).

According to Hirayama (1985), this character only

occurs in tecta and tentoria. For our sample, we were

able to confirm its presence in tecta and tentoria and

also observed it in barbouri ( barbouri and other species

now classified in Graptemys may be sexually dimorphic

for this character). The descriptive term ‘tectiform’ is

somewhat problematic, because any turtle shell can be

considered ‘roofed’ (Fig. 69). We regard a carapace as

tectiform if its sides are more-or-less flat and meet along

the midline at a rather sharp angle (Fig. 70). Many tes-

tudinoids, and notably those ‘emydids’ currently classi-

fied within Graptemys, have a somewhat tectiform cara-

pace as juveniles, but that morphology typically is lost in

the adults.

Polarity: Because all outgroups and the majority of

the ingroup do not have a tectiform carapace, we consid-

er its presence to be derived.

(37) Shape and orientation of the second neural; 0 =

second neural hexagonal, short sides positioned anteri-

orly, Fig. 71; 1 = second neural hexagonal, short sides

positioned posteriorly, Fig. 72; 2 = second neural

octagonal, Fig. 73 (modified from Hirayama, 1985, G;

Yasukawa et al., 2001, 25).

(38) Shape and orientation of the third neural; 0 = third

neural hexagonal, short sides positioned anteriorly, Fig.

71; 1 = third neural hexagonal, short sides positioned

posteriorly, Fig. 72; 2 = third neural square, Fig. 74; 3

= third neural octagonal, Fig. 75 (modified from

Hirayama, 1985, G; Yasukawa et al, 2001, 25).

Originally, Hirayama (1985) only discussed the ori-

entation of the neurals in general, which is fully suffi-

cient for his ‘batagurid’ ingroup, because almost all indi-

viduals exhibit his two suggested character states.

However, in most tortoises the second and/or third neu-

rals are not hexagonal, but rather are square or octago-

nal, making it impossible to assign them to one of

Hirayama’s (1985) character states. We consequently

split Hirayama’s original character into two characters,

restricted their application to the second and third neu-

ral, and added additional character states.

Our observations generally agree with those of

Hirayama (1985) and Yasukawa et al. (2001) for

‘batagurids,’ with the exception of annandalei in which

we found the short side of the second and third neurals

to be positioned anteriorly, and not posteriorly as was

indicated by Hirayama (1985).

Polarity: The short side of the second and third neu-

ral bones faces posteriorly in odoratus and spinifera but

Vol. 10, p. 66

Asiatic Herpetological Research

2004

anteriorly in caretta. The shape of the second and third

neurals is extremely variable in serpentina. However, in

Lindholmemys and Mongolemys the short side of the

second and third neurals is positioned anteriorly. We

consider that condition to be primitive for

Testudinoidea.

(39) Medial contact of the seventh and/or eighth costal

bones; 0 = absent, Fig. 76; 1 = present, Fig. 77

(Hirayama, 1985, V; Yasukawa et al., 2001, 26).

In some testudinoid turtles, the posterior costal

bones meet along the midline due to the reduction of the

posterior neural elements. The original character defini-

tion provided by Hirayama (1985) and Yasukawa et al.

(2001) was worded to indicate a contact between the

seventh and eighth costal bones among some

’batagurids.’ We are unable to reproduce their results if

the character definition is taken literally. For example, in

all our specimens of amboinensis and galbinifrons, the

eighth costals meet on the midline, but the seventh

costals do not. However, if the character definition is

modified to include any contact of the seventh or eighth

costals, our results are concordant with those of

Hirayama (1985) and Yasukawa et al. (2001). In addition

to the Asian box turtles, we report a medial contact of

the posterior costals in baska, Carolina, coahuila, T. nel-

soni, T. ornata and rnbida.

Polarity: A medial contact of the seventh and/or

eighth costals is absent in serpentina, but present in

spinifera, caretta, many kinostemids, and many pleu-

rodires. Although a composite reconstruction of a puta-

tive “lindholmemydid” from the Early Cretaceous of

Japan was illustrated with the seventh costals in contact

at the midline (Hirayama et al., 2000, fig. 11), such a

contact is absent in other specimens of Lindholmemys

and Mongolemys. Its presence within testudinoids is pre-

dominantly in the highly derived box turtles, and we

conclude that its presence is derived for Testudinoidea.

(40) Cervical scute; 0 = present, Fig. 78; 1 = absent,

Fig. 79 (modified from Crumly, 1985, 1994, 34; Gaffney

and Meylan, 1988, H5.2, FI 10.1; Shaffer et al., 1997,

41).

The presence and shape of the cervical scute is used

commonly to determine phylogenetic relationships

within tortoises. According to Crumly (1985) the cervi-

cal scute is very narrow or absent in all tortoises except

agassizii, berlandieri, emys, flavomarginatus, impressa,

and polyphemus. We generally agree with these observa-

tions, but when this character is applied to all testudi-

noids intraspecific variation is so great that the character

becomes essentially useless. We consequently limit our

scoring to the mere presence or absence of the cervical

scute. We confirm the observations of Gaffney and

Meylan (1988) that this scute is absent in carbonaria,

chilensis, elegans, nigra, par dalis, and sulcata and addi-

tionally code homeana and erosa as polymorphic.

Polarity: The cervical scute is present in all cryp-

todiran outgroups that have scutes on their carapace. We

consider its absence to be derived.

(41) Number of vertebral scutes; 0 = five, Fig. 80; 1 =

six or more, Fig. 81 (Hirayama, 1985, P).

We confirm Hirayama’s (1985) observation that

there are at least six vertebral scutes in N. platynota.

Additional scutes occasionally occur in other species,

but are best considered abnormalities; they typically

lack the symmetrical associations with adjacent pleural

scutes seen in N. platynota.

Polarity: All testudinoids, except for N. platynota,

have five vertebral scutes. We consider the presence of

six scutes to be derived.

(42) Position of the anterior sulcus of the fourth verte-

bral scute; 0 = sulcus lies on the fifth neural, Fig. 82; 1

= sulcus lies on fourth neural, or on the suture between

the fourth and fifth neural, Fig. 83; 2 = sulcus lies on the

sixth neural, or on the suture between the fifth and sixth

neural, Fig. 84 (modified from Hirayama, 1985, L+M).

(43) Position of the posterior sulcus of the fourth verte-

bral scute; 0 = sulcus lies on the eighth neural, or on the

homologue of the eighth neural, if the seventh is reduced

(e.g., in most tortoises), Fig. 85; 1 = sulcus lies on the

seventh neural, or on the suture between the seventh and

eight neural, Fig. 86; 2= eighth neural absent, sulcus

overlies costals that meet at the midline, Fig. 87 (modi-

fied from Hirayama, 1985, L+M).

The size of the fourth vertebral scute was addressed

with two characters by Hirayama (1985) but the total

range of morphological variability in testudinoids is not

encompassed by his character definitions. In most tes-

tudinoids, the fourth vertebral scute covers the posterior

half of the fifth neural bone, the sixth and seventh neu-

rals, and the anterior half of the eighth neural. A number

of variations are known, and simply counting the num-

ber of neural bones covered by this scute results in prob-

lems by creating a false perception of homology. For

instance, a fourth scute that partially overlies the fourth

and seventh neurals and fully covers the fifth and sixth,

can strictly be said also to cover four neurals, but the ele-

ments involved are only partially homologous with the

common condition. We attempt to resolve these issues

by establishing two new characters that preserve what

we think was Hirayama’s (1985) original intent, but that

permit a more accurate representation of the association

between the fourth vertebral scute and the underlying

neural bones.

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Asiatic Herpetological Research

Vol. 10, p. 67

Some problems that are associated with scoring this

character include the prevalence of scute abnormalities

among testudinoids (e.g., Coker, 1905, 1910; Newman,

1906; Zangerl and Johnson, 1957). Specimens exhibit-

ing such abnormalities were scored as unknown. The

notable exception to this is N. platynota, in which a

sixth, or even a seventh, vertebral scute is always pres-

ent.

Polarity: Determining the polarity through outgroup

relationship is somewhat difficult, because almost every

outgroup exhibits a different condition, especially for

the posterior sulcus. Based on ingroup commonality, and

the presence of our zero state in both Lindholmemys and

Mongolemys, we consider the sulci of the fourth verte-

bral scute to be primitively situated on the fifth and

eighth neural bones.

(44) Posterior margin of first vertebral scute significant-

ly narrower than its anterior margin; 0 = absent, Fig.

88; 1 = present, Fig. 89 (modified from Hir ay ama, 1985,

C).

When originally proposed, this character was

applied to a posterior constriction of all vertebral scutes

(Hirayama, 1985). If strictly applied, this character is

absent in all taxa, because the fifth vertebral scute never

is constricted along its posterior edge relative to the

anterior edge. If each scute is viewed by itself, it

becomes apparent that especially the fourth vertebral

scute tends to be narrowed posteriorly, as can be

observed in all species now classified in the genera

Graptemys, Heosemys, Trachemys, and Testudo among

others. According to Hirayama (1985), posterior narrow-

ing is limited to crassicollis and borneensis and unites

them as a synapomorphy. We were able to replicate this

distribution only if the character definition was restrict-

ed to the first vertebral scute, in which the posterior mar-

gin is significantly narrower than its anterior margin in

those two species only. In making this change, however,

this character becomes at least partly redundant with

characters 45 and 47.

Polarity: Outgroup analysis reveals that posterior

narrowing of the first vertebral scute is present only in

odoratus\ it is absent in Lindholmemys and

Mongolemys. We regard the presence of a posterior nar-

rowing of the first vertebral scute to be derived.

(45) Anterior half of the first vertebral scute much nar-

rower than posterior half especially in adults; 0

absent, Fig. 90; 1 = present, Fig. 91 (modified from

Hirayama, 1985, R).

We confirm the clear presence of an anteriorly nar-

rowed first vertebral scute in dentata and spinosa as

reported by Hirayama (1985), and note that grandis is

polymorphic. Because the anterior sulcus of the first ver-

tebral scute commonly is restricted to the nuchal bone in

several other taxa, but the scute shows no anterior nar-

rowing, we limit the original character definition to the

shape of the first vertebral scute only. This peculiar mor-

phology seems to be the result of growth that is limited

to the anterior edge and the posterior half of the lateral

edge of the first vertebral scute. As a consequence, this

character is not apparent in juveniles, but becomes

increasingly accentuated in adults.

Polarity: Anterior narrowing of the first vertebral

scute is absent in all outgroups and within the large

majority of the ingroup. We consider its presence to be

derived.

(46) Significant contact of the tenth marginal scute with

the fifth vertebral scute; 0 = absent, Fig. 92; 1 = pres-

ent, Fig. 93 (modified from Hirayama, 1985, K).

Contact of the tenth marginal scute with the fifth

vertebral scute was reported previously only in baska,

smithii, tecta, and tentoria (Hirayama, 1985). We are

able to confirm the presence of a very well developed

contact in all but smithii (not seen), and we add spinosa

to the list of species in which this contact may occur (it

is polymorphic for spinosa ; contact is present in CAS

228368, but absent in the smaller CAS 228459, so onto-

genetic differences may explain the polymorphism). We

also note slight contacts in some specimens of other

species (e.g., agassizii, borneoensis, carbonaria, home-

ana, orbicularis, pardalis, and polyphemus ), but by

rewording Hirayama’s (1985) original character to

include only significant contact, we are able to retain

what we believe was his original intent.

Polarity: Due to the absence of contact in all out-

groups in which it is applicable and the predominance

within the ingroup, we consider its presence to be

derived.

(47) Contact of the second marginal scute with the first

vertebral scute; 0 = absent, Fig. 94; 1 = present, Fig. 95

(Hirayama, 1985, O; see also Tinkle, 1962, table 1,

‘Seam A ’).

According to Hirayama (1985), the first vertebral

scute usually (>90%) contacts the second marginal scute

in japonica, leprosa, and caspica. He also noted that the

scutes are sometimes in contact in N. platynota and

bealei. For our sample, we are able to confirm this con-

tact as a polymorphism for bealei , caspica , japonica ,

and leprosa , but the contact is clearly absent in all our

specimens of N. platynota. We also note that these scutes

are sometimes in contact in picta, amboinensis, orbicu-

laris, and terrapin. Together with all of the above, these

taxa were scored as polymorphic. The only taxa to

exhibit a consistently well-developed contact are reticu-

laria and blandingii.

Vol. 10, p. 68

Asiatic Herpetological Research

2004

Polarity: A clear contact between the second mar-

ginal scute and the first vertebral scute does not exist in

caretta or serpentina , but both morphologies occur in

kinostemids and pleurodires. The scutes are not in con-

tact in Lindholmemys and Gravemys , but they are in con-

tact in Mongolemys. The polarity for this character is

ambiguous.

(48) Contact of the sixth marginal scute with the third

pleural scute; 0 = absent, Fig. 96; 1 = present, Fig. 97

(modified from Hirayama, 1985, B; see also Tinkle,

1962, table 3, ‘Seam C’).

The contact between the sixth marginal and third

pleural scutes is easily enough rendered as a simple

"presence or absence’ character, but this hides the range

of possible morphological variation. The degree of con-

tact can range from extensive to a condition where the

two scutes just barely contact at their comers. Several

taxa exhibit a condition where these scutes either barely

touch or do not touch one another at their comers, but

whenever several specimens were available to us, they

typically turned out to be polymorphic. For this reason

Gaffney and Meylan (1988) called this character ‘dubi-

ous.’ We scored such borderline cases as polymorphic,

even if not enough specimens were available to corrob-

orate this.

We confirm Hirayama’s (1985) observations

regarding the absence of a contact between these scutes

in baska, ocellata, tecta, tentoria, and thurjii, and we

add petersi and spinosa to that list. Taxa that we score as

polymorphic include annandalei, borneensis, borneoen-

sis, caspica, crassicollis, grandis, hamiltonii, japonica,

punctularia , reevesii, sinensis, subtrijuga, and trijuga.

Whereas all ‘emydids’ lack a contact, tortoises exhibit

both character states.

The presence of a contact between the sixth margin-

al scute and the third pleural scute was considered by

Hirayama (1985) to unite crown group ‘batagurids’ and

‘testudinids’ as a synapomorphy. Given the patchy dis-

tribution of this character, and widespread polymor-

phism, it seems to be of little use.

Polarity: A contact between the sixth marginal scute

and the third pleural scute is absent in most outgroups.

The exception is caretta ; this is not surprising because

caretta has five instead of four pleural scutes. We con-

sider the presence of a contact to be derived.

(49) Twelfth marginal scute; 0 = two present, their com-

mon sulcus only partially subdivides the pygal bone,

Fig. 98; 1 = two present, but their common sulcus fully

subdivides the pygal bone, Fig. 98; 2 = both twelfth

marginal scutes fused along the midline, Fig. 99 (modi-

fied from Mlynarski, 1976; Crumly, 1985, 1994, 35;

Gaffney and Meylan, 1988, H2.1).

According to McDowell (1964, p. 240 and table 1

number 4) members of the ‘Emydinae’ can be distin-

guished from the ‘Batagurinae’ based on an incomplete

subdivision of the pygal bone by the median sulcus of

the posterior-most marginals. We found exceptions with

picta, N. platynota, pulcherrima, reevesii, ret icul aria,

and spengleri, which do not always clearly exhibit the

pattern that would be predicted by McDowell’s (1964)

statement, but we note that the expression of this charac-

ter will depend significantly on the shape of the pygal

bone. In all tortoises except emys and impressa, the

twelfth marginal scutes are fused to from a single supra-

caudal scute that covers the posterior part of the cara-

pace (Crumly, 1985). For this condition, we created a

third character state.

Polarity: The twelfth marginal scutes are fully sep-

arated in all outgroups that have them, and their com-

mon sulcus fully subdivides the pygal bone. The pygal

bone in “lindholmemydids” is polymorphic, with the 0

state found in Lindholmemys and Mongolemys, and the

1 state in Gravemys. Either state 0 or state 1 is primitive

for Testudinoidea; the midline fusion of the twelfth mar-

ginals is a derived feature for ‘Testudinidae’.

Bridge

(50) Sutured contact between plastron and carapace; 0

= present, plastron and carapace are tightly connected

by an osseous bridge, Fig. 100; 1 = absent, plastron is

attached to carapace by connective tissue, Fig. 101

(modified from Hirayama, 1985, Q; Shaffer et al., 1997,

58; Yasukawa et al. 2001, 21a).

(51) Presence and development of anterior buttresses; 0

= anterior buttresses absent, Fig. 102; 1 = anterior but-

tresses present but small, and not in contact with the first

costal bones, Fig. 103; 2 = anterior buttresses long and

thin and just barely in contact with the costal bones, if at

all, Fig. 104; 3 = anterior buttresses well developed and

in clear contact with the first costal bones, Fig. 105; 4 =

anterior buttresses very large and in direct contact with

the first dorsal rib, Fig. 106 (modified from Hirayama,

1985, Q; Gaffney and Meylan, 1988, A 14.2; Yasukawa

et al, 2001, 28).

(52) Presence and development of posterior buttresses;

0 = posterior buttresses absent, Fig. 107; 1 = posterior

buttresses present but small, and not in contact with the

costal bones, Fig. 108; 2 = posterior buttresses long and

thin and just barely in contact with the costal bones, if at

all, Fig. 109; 3 = posterior buttresses well developed

and in clear contact with costal bones V and VI, Fig.

110; 4 = posterior buttresses well developed but onlv in

clear contact with costal bone V, Fig. Ill (modified from

Hirayama, 1985, Q; Gaffney and Meylan, 1988, A 14.2,

Shaffer et al, 1997, 55; Yasukawa et al, 2001, 29).

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Vol. 10, p. 69

(5j) Medially-directed pivoting process for plastral

hinge developed on fifth peripheral bone; 0 = absent,

Fig. 112; 1 = present, Fig. 113.

(54) Complete or almost complete overlap of hyoplas-

tron/hypoplastron suture by the pectoral/ abdominal sul-

cus; 0 = absent, Fig. 114; 1 = present, Fig. 115 (modi-

fied Gaffney and Meylan, 1988, F3.2; Burke et al., 1996,

16; McCord et al., 1995, 13; Yasukawa et al., 2001,

21b).

In most testudinoid turtles, the plastron is attached

to the carapace via a fully ossified bridge and variably

developed plastral buttresses. In species with a kinetic

plastron, the bridge is typically absent and the plastron is

attached to the carapace via connective tissues (e.g.,

amboinensis, blandingii , Carolina , dentata, galbinifrons,

mouhotii , orbicularis , T. ornata). The original configu-

ration of this character tied the presence of plastral kine-

sis to the reduction of the buttresses (Hirayama, 1985).

However, within testudinoid turtles the morphology of

the buttresses varies significantly and independently

from plastral kinesis. We consequently split this charac-

ter into three discrete characters concerned with the

morphology of the bridge and the buttresses.

We also developed two new characters that pertain

to the morphology of the bridge region: the presence of

medially-directed processes on the fifth peripherals that

act as pivots for the plastral bones during shell closure

(Bramble, 1974) and a revised plastral kinesis character

(Gaffney and Meylan, 1988; McCord et al., 1995) that

considers plastral-kinesis to be well developed only in

those taxa in which the pectoral/abdominal sulcus fully

overlaps the hyoplastron/hypoplastron suture, allowing

optimal movement between the two plastral lobes. Most

taxa with plastral kinesis also have well-developed piv-

oting processes on the fifth peripherals, but notable

exceptions are orbicularis and N. platynota. In

blandingii , the process is modified into an anteroposte-

riorly-elongated, flattened process that extends along

most or all of the length of the fifth peripheral (Fig. 113).

In some specimens of blandingii , a similar structure is

developed on the sixth peripheral as well.

Polarity: Reconstructing the basal condition for

these characters within testudinoids is difficult, because

all living cryptodiran outgroups do not have plastral but-

tresses and commonly lack osseous bridges. However,

the bridge of Gravemys, Mongolemys, and

Lindholmemys is osseous, shows no signs of kinesis, and

(at least in Lindholmemys) the anterior and posterior but-

tresses are well developed and touch the costal bones.

We consider that morphology to be primitive for

Testudinoids.

(55) Contact between inguinal and femoral scutes; 0 =

absent, Fig. 116; 1 = present, Fig. 117 (Crumly, 1985,

1994, 42; Gaffney and Meylan, 1988, H3.3, HI 5.2).

Within tortoises the complete or frequent absence of

a contact between the inguinal scute and the femoral

scute was used previously to hypothesize the monophy-

ly of several smaller clades, for example {graeca + her-

manni + horsfieldi + kleinmanni + marginata + tornieri }

(Crumly, 1985) and {agassizii + berlandieri + flavomar-

ginatus + polyphemus } (Gaffney and Meylan 1988). We

confirm the absence of a contact in representatives of the

first group, but not in the second. Among the second

group (traditionally classified together in Gopherus) the

contact is strongly reduced, but still is present. Among

‘batagurids’ and ‘emydids,’ a contact is absent in all taxa

with the noteworthy exception of hamiltonii.

Polarity: Determining the polarity for this character

is somewhat difficult because all living outgroups have

an arrangement of plastral scutes that is rather different

from testudinoids. However, based on ingroup common-

ality and the absence of a contact in the

“Lindholmemydidae,” we conclude that the presence of

a contact between the inguinal and femoral scutes

should be considered derived for Testudinoidea.

(56) Presence of musk glands; 0 = inguinal and axillary

gland present; 1 = axillary gland present only; 2 = musk

glands absent (modified from Crumly, 1985).

(57) Presence of anterior musk duct foramina; 0 = musk

glands and their foramina present, Fig. 118; 1 = musk

glands present, but foramina not developed; 2 = musk

glands and foramina absent (modified from Hirayama,

1985, A; Gaffney and Meylan, 1988, FI. 2, F5.3; Burke

et al., 1996, 20).

(58) Presence of posterior musk duct foramina; 0 =

musk glands and their foramina present, Fig. 119 ; 1 =

musk glands present, but foramina not developed; 2 =

musk glands and foramina absent (modified from

Hirayama, 1985, A; Gaffney and Meylan, 1988, FI. 2,

F5.3; Burke et al., 1996, 20).

According to Hirayama (1985), the presence of

musk duct foramina characterizes the paraphyletic

assemblage ‘Batagurinae’ (sensu Hirayama, 1985, not

Gaffney and Meylan, 1988). We believe the difference

of opinion between Hirayama (1985) and Gaffney and

Meylan (1988) regarding this character is based on fail-

ure to make clear the distinction between the presence of

musk glands and the presence of musk duct foramina.

Musk glands are developed in almost all extant turtles

(Waagen, 1972), and we consequently agree with

Gaffney and Meylan (1988) that their presence should

be considered primitive for all cryptodiran turtles.

Vol. 10, p. 70

Asiatic Herpetological Research

2004

However, even though most turtles have musk glands,

true musk duct foramina are developed only in some

pleurodires (e.g., Chelodina, Emydura), some ‘emy-

dids,’ and all “batagurids,’ making a monophyletic

Testudinoidea (sensu Hirayama, 1985) possible. Distinct

musk duct grooves are present on the anterior peripher-

als of Kinostemidae, and tiny foramina are sometimes

associated with these (Hutchison, 1991).

Because the presence of musk glands does not nec-

essarily result in the development of musk duct forami-

na, we decided to score these two characters separately.

We relied on an unpublished thesis on the musk glands

of turtles (Waagen, 1972) to determine the presence of

musk glands for most taxa. In scoring taxa not investi-

gated by Waagen (1972) we only recorded presence of

musk glands if musk duct foramina provided positive

evidence for their presence (e.g., baska, bealei, borneen-

sis, galbinifrons , kachuga, mouhotii , petersi, pulcherri-

ma, spengleri, and tentoria). Many tortoises, conse-

quently, had to be scored as unknown, because they

were not analyzed by Waagen (1972) and do not exhibit

musk duct foramina (e.g., elongata, homeana, horsfiel-

di, and pardalis ).

Our scoring of the musk duct foramina is derived

from a combination of osteological observation and data

provided by Waagen (1972). Taxa not reported to pos-

sess musk glands (Waagen, 1972) were checked for

musk duct foramina, but none were found. For those

species that Waagen reported as having musk glands, we

sought musk duct foramina on osteological specimens.

Several taxa with musk glands, but only lightly ossified

bridges, do not exhibit musk duct foramina (e.g.,

blandingii, dentata , flavomarginata, orbicularis , and

pulcherrima) or show an asymmetry with foramina only

visible anteriorly (e.g., N. platynota). In taxa that pos-

sess them, the musk duct foramina are sometimes con-

tained entirely within the peripherals (e.g., N. platyno-

ta), and sometimes between the peripheral and the plas-

tral buttress (e.g., reevesii).

Polarity: Given the presence of musk glands in all

extant outgroups (Waagen, 1972), their absence should

be considered derived. Musk duct foramina are not

described for “lindholmemydids” but J. H. Hutchison

specifically searched for them in Mongolemys speci-

mens housed at IVPP and found no trace of them.

Because musk duct foramina are developed in the vast

majority of the ingroup, we consider their absence to be

derived for testudinoids.

Plastron

(59) Extensive overhanging lip of the epiplastra; 0 =

absent, Fig. 120; 1 = present, Fig. 121 (Gaffney and

Meylan 1988, H5.1, 9.2).

In most testudinoid turtles, the epiplastra are rather

flat with a slight increase in thickness along the anterior

margin. In contrast, many tortoises have strongly thick-

ened epiplastral margins that sometimes form an over-

hanging lip along the interior rim of the plastron.

According to Gaffney and Meylan (1988) the presence

of such an overhang of the epiplastra unites all tortoises

except those classified in the genera Manouria (Fig.

120) and Gopherus, with a reversal occurring in giant

insular forms. We confirm this general pattern, but we

note the absence of an overhang in tornieri. A interior

overhang is absent also in all extant ‘emydids’ and

‘batagurids,’ but a small overhang is present in extinct

Ptychogaster and Echmatemys (Mlynarski, 1976, figs.

78, 8 1), taxa generally considered to belong to either the

‘Emydidae’ or ‘Batagurinae.’

Polarity: An overhanging lip on the epiplastra is

absent in all outgroups and the majority of the ingroup.

We consider its presence to be derived.

(60) Intersection of the entoplastron by the humeropec-

toral sulcus; 0 = absent, Fig. 122; 1 = present, Fig. 123

(Hirayama, 1985, X; Crumly, 1985; Gaffney and

Meylan, 1988, F5.1; McCord et al., 1995, 15).

This character was used to help resolve relation-

ships within ‘batagurids’ by Hirayama (1985) but we

were unable to replicate his results in our analysis. We

agree with Crumly (1985) that the sulcus crosses the

entoplastron in at least one species classified in the

genus Indotestudo (i.e., elongata ), but the sulcus is at the

entoplastron/hyoplastron suture in our specimen of

forsteni. The condition in species now commonly classi-

fied in Testudo varies widely (e.g., the suture crosses the

entoplastron in graeca and horsfieldi, but does not in

hermanni or kleinmanni). We also agree with Gaffney

and Meylan (1988) on their distribution of this character

among the ‘Emydidae,’ however, our scoring for picta,

orbicularis, and blandingii is polymorphic, because the

sulcus generally runs along the suture between the ento-

plastron and the hypoplastra, but may barely fall on

either side.

Polarity: The polarity is ambiguous if only extant

taxa are considered. The plastron of most outgroups is

too different from that of testudinoids to be of any use

for polarizing this character. For instance, the plastron of

spinifera lacks scutes, and that of serpentina, odoratus,

and caretta is too heavily modified to enable a meaning-

ful comparison. Both character states are commonly

found in ‘batagurids,’ ‘emydids,’ and testudinids, mak-

ing an ingroup analysis futile. The humeropectoral sul-

cus is distinctly posterior to the epiplastron in Gravemys

and Mongolemys, so we consider an intersection of this

suture with the entoplastron to be derived.

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(61) Anal notch of the plastron; 0 = present, Fig. 124; 1

= greatly reduced, Fig 125; 2 = absent, Fig. 126 (mod-

ified from Hirayama, 1985, W; Yasukawa et al, 2001,

22).

The plastron of most testudinoid turtles has a signif-

icant anal notch. The absence of such an anal notch for

amboinensis, galbinifrons, and flavomarginata was

reported by Hirayama (1985) and we confirm those

observations. An anal notch also is absent in belliana,

Carolina , coahuila , erosa , homeana, T. nelsoni , and T.

ornata. To accommodate the presence of a reduced anal

notch we modify Hirayama’s (1985) character by creat-

ing a third character state. A reduced anal notch is found

in blandingii, orbicularis, N. platynota, and reticularia.

In at least one species (mouhotii), a distinct anal notch is

present in larger individuals, but small specimens have a

reduced notch (scored as polymorphic in our matrix);

this suggests that development of an anal notch may be

subject to ontogenetic variation in at least some testudi-

noids.

Polarity: In caretta and serpentina an anal notch is

not present, however, their plastra are narrow and

tapered posteriorly. The fleshy plastron of spinifera is

smooth along its posterior margin, but this cannot be

observed in osteological preparations. A notch is weak-

ly developed in at least some Lindholmemys, but is

absent in Mongolemys. A notch is present in kinostem-

ids, pleurodires, most of the ingroup, and in Gravemys.

We conclude that its absence should be considered

derived for our ingroup.

(62) Anal scutes fused; 0 = absent, Fig. 127; 1 = pres-

ent, Fig. 127 (Hirayama, 1985, Z).

The anal scutes of adult galbinifrons, and flavomar-

ginata are at least slightly fused, especially along their

posterior medial border. We fully agree with Hirayama’s

(1985) treatment for this character. Anal scute fusion can

be identified easily in macerated specimens (Fig. 127),

because the anal scutes will not separate from one anoth-

er, as will all other scutes.

Polarity: Anal scute fusion is absent in the vast

majority of turtles, and is considered to be the primitive

condition.

(63) Plastral scutes with vibrant, radiating color pat-

tern; 0 = absent, Fig. 128; 1 = present, Fig. 129

(Hirayama, 1985, S; McCord et al, 1995, 16 Yasukawa

et al, 2001, 32).

Vibrant, radiating color patterns of the plastral

scutes of dentata, grandis, and spinosa were noted by

Hirayama (1985) and McCord et al. (1995). We add

tcheponensis to this list, as well as the testudinids geo-

metricus and P. oculifera. In our specimens, the pattern

of dentata and tcheponensis is not as vibrant as in gran-

dis and spinosa.

Polarity: Vibrant, radiated color patterns are miss-

ing in all outgroups and the majority of the ingroup.

Their presence is derived.

Postcranium and Soft Tissue

(64) Development of a suprascapula; 0 = absent; 1 =

present, Fig. 130 (Gaffney and Meylan, 1988, F3.1;

Burke et al, 1996, 11).

(65) Development of an episcapula; 0 = absent; 1 =

present, Fig. 130 (Gaffney and Meylan, 1988, F4.1;

Burke et al, 1996, 11).

The presence of both a suprascapula and an epis-

capula apparently is limited to blandingii and the species

currently classified in Terrapene. A suprascapula is also

present in orbicularis. Both structures are involved in

the locking mechanism of the anterior plastral lobe dur-

ing shell closure (Bramble, 1974). These structures are

difficult to verify in most osteological preparations,

because they may dissociate from the scapula and be dif-

ficult to recognize, and because they may ossify only in

older individuals. The specimen we dissected to illus-

trate these features (TNHC 62532, a T. ornata with cara-

pace length of 103 mm) has a completely cartilaginous

episcapula, and a predominantly cartilaginous supras-

capula (Fig. 130). It is therefore much easier to confirm

their presence than verify their absence. We followed

Bramble’s (1974) account of these structures and scored

our matrix accordingly, as probably did Gaffney and

Meylan (1988) and Burke et al. (1996).

Polarity: Suprascapulae and episcapulae are absent

in all outgroups and the majority of the ingroup. Their

presence is considered to be derived.

(66) Shape of coracoid blade; 0 = long and narrow, Fig.

131; 1 = short and very wide, Fig. 131 (Crumly, 1985,

1994; Gaffney and Meylan, 1988, HI. 7).

The coracoid blade of all ‘emydids’ and

‘batagurids’ is an elongate bone with a narrow, short

shaft and a long, wedge-shaped coracoid blade that is

about two times wider than the base. In tortoises, this

bone is still wedge-shaped, but relatively much shorter

and with a blade that is considerably wider, typically

four times the width of the base (Crumly, 1985, 1994;

Gaffney and Meylan, 1988). We agree with previously

published observations.

Polarity: The coracoid blade of caretta, serpentina,

and odoratus is long and narrow and that of spinifera is

long, but not wedge-shaped. We consider a long and nar-

row coracoid blade to be primitive for Testudinoidea.

(67) Number of manual claws; 0 = five, Fig. 132; 1 =

four, Fig. 133 (modified from Hirayama, 1985, J).

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Asiatic Herpetological Research

2004

Most testudinoid turtles have five manual claws

with the exception of baska and horsfieldi, both of

which have only four. We did not verify this character

independently for all species, due to an overall lack of

articulated skeletons and our limited access to pickled

specimens. However, because the number of claws of

the forelimbs is an easily determinable, discrete number

that is regularly noted and described in the literature, we

scored all remaining taxa from the comprehensive infor-

mation provided by Ernst and Barbour (1989).

Polarity: Five manual claws are present in serpenti-

na, odoratns, and almost all pleurodires (excluding

species currently classified in Chelodina and

Hydromedusa ); three are present in spinifera, and two in

caretta. The condition in “lindholmemydids” is

unknown. Based on ingroup commonality, we consider

five claws to be primitive for the ingroup.

(68) Number of phalanges of manus and pes; 0 = digi-

tal formula of2-3-3-3-3 or 2-3-3-3-2, Fig. 132; 1 = dig-

ital formula with less than 2-3-3-3-2, Fig. 133 (Crumly,

1985; Gaffney and Meylan, 1988, Hl.l).

The digital formula of most testudinoid turtles is 2-

S-3-3-3 or 2-3-3-3-2. Among tortoises, the manus and

pes are greatly shortened and the digital formula is typi-

cally reduced to 2-2-2-2-2 or less (Auffenberg,

1974:135-136; Crumly, 1985). Due to the dissociated

nature of most of the material we viewed, we were not

able to verify the digital formulae of most of the turtle

taxa we included. However, when articulated hands and

feet were present, we never found anything to contradict

the statements made above. We scored all tortoises

based on information provided by Auffenberg (1974)

and Crumly (1985).

Polarity: All outgroups and the majority of the

ingroup do not have a reduced digital formula. We con-

sequently consider the reduced formula to be derived.

(69) Webbing between digits; 0 = present, well devel-

oped, Fig. 134; 1 = absent, or at least strongly reduced,

Fig. 135 (Hirayama, 1985, b).

Due to their semi-aquatic nature, most testudinoids

have well-developed webbing between the digits of their

hands and feet. In more terrestrial species, however, the

webbing often is reduced. Unfortunately, there seems to

be a gradient in the development of webbing, from

extremely well developed (e.g., baska, reticularia) to

moderately developed (e.g., dentata, guttata) to virtual-

ly non-existent (e.g., spengleri ). We nevertheless were

able to reproduce Hirayama’s (1985) distribution for the

‘batagurids’ with the exception of grandis and spinosa,

which have reduced webbing (grandis is the only ‘bor-

derline’ taxon we found, but its webbing is reduced rel-

ative to those taxa we scored as having well-developed

webbing). Among ‘emydids,’ we note that the webbing

is heavily reduced in Carolina, T. nelsoni, and T. ornata.

All tortoises lack webbing.

Polarity: All outgroups and the majority of ingroup

taxa have webbed hands and feet. We consider the

absence of webbing to be derived.

(70) Sexual size dimorphism; 0 = absent; 1 = present,

female much larger than male (Gaffney and Meylan,

1988, F5.2; Burke et al., 1996, 37).

In almost every species of turtle, there is some

expression of sexual size dimorphism (Berry and Shine,

1980; Gibbons and Lovich, 1990). The difference in size

between the sexes can be expressed as a ratio and typi-

cally shows considerable variation depending on the

population (Gibbons and Lovich, 1990). We initially

tried to score this character with three character states, as

done by Burke et al. (1996), differentiating between

species with larger males, larger females, and equally

sized sexes, but we abandoned that, because exact data

are missing for most ‘batagurid’ taxa. We consequently

only score taxa as being sexually dimorphic if females

are at least 1 .4 times larger than the males. Our scores

are derived from Gibbons and Lovich (1990) and Ernst

and Barbour (1989).

Polarity: Sexual size dimorphism is prevalent in

most outgroups. In spinifera the female is much larger,

in odoratus and serpentina the male tends to be slightly

smaller, in caretta the sexes are of similar size. The out-

group polarity is thus ambiguous, but in the majority of

the ingroup pronounced sexual dimorphism is absent.

Problematic Characters

We encountered difficulties in evaluating a number of

previously used characters, and we provide some sum-

mary statements for those in this section. Most of these

characters were not pursued thoroughly in our study

because we were not able to understand the original

descriptions, were unable recover discrete character

states, or because at an early point in our investigation of

the character we detected significant variation in expres-

sion of character states within taxa. In the latter case

greater sample sizes or new methodological techniques

(e.g., Wiens, 1995; Smith and Gutberlet, 2001) will be

required to tease out a phylogenetic signal.

(A) Frontal contribution to the supratemporal rim

(Hirayama, 1985, 4).

The anterior extent of the upper temporal emargina-

tion is difficult to define in many taxa, and is impossible

to determine in those with a fully emarginated temporal

region (e.g., T. ornata ). The result is a high degree of

ambiguity and a general lack of discrete character states.

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(B) Contact between postorbital and quadrate

(Hirayama, 1985, 10).

In the vast majority of ingroup taxa, there is no con-

tact between the postorbital and the quadrate. Such a

contact was observed only in japonica and punctularia

by Hirayama (1985). In specimens of japonica available

to us, we were not able to confirm this contact. CAS

228348 is a skeleton from a diseased specimen of punc-

tularia. On the right side of the skull there is a possible

(but only slight) contact. It is possible that the contact is

actually between the postorbital and the quadratojugal

(Fig. 136). We also found a minimal contact in one spec-

imen of annulata. Given these diverging observations

and the minute contact that is present in our material, we

regard (for now) any contact within the ingroup as an

abnormality.

(C) Absence of the “ posterior process of the postor-

bital” (Hirayama, 1985, 8).

We cannot determine unambiguously what

Hirayama (1985) meant by this character. In our assess-

ment of testudinoids, both a posterolateral and a postero-

medial process of the postorbital can occur. In

Hirayama’s (1985) analysis, only grandis and spinosa

lack a “posterior process of the postorbital.” These

species are also the only ‘batagurid’ taxa to fully lack a

temporal arch. We suspect that this character may some-

how be referring to a lack of a bony temporal arch.

(D) Processus inferior parietalis ‘‘medially approximat-

ing each other, cranial cavity ant eroventr ally narrow-

ing” (Hirayama, 1985, 5; McCord et al., 1995, 7;

Yasukawa et al, 2001, 2).

We acknowledge the validity of this character as

was originally worded by McDowell (1964). However,

we find it difficult to determine how strongly the con-

striction of the brain case must be before it can be con-

sidered present. We were unable to develop unambigu-

ous discrete character states for this feature.

(E) Subdivision of the foramen nervi trigemini (Crumly,

1982; Hirayama, 1985, 6).

This character was used originally by Crumly

(1982) to infer phylogenetic relationships within

‘Testudinidae’. For his ingroup, Crumly (1982)

observed a great amount of polymorphism, with no sin-

gle species either completely lacking or always exhibit-

ing a subdivision of the foramen. He also noted asym-

metry for this character between the left and right side of

some individuals. We confirm the common presence of

a subdivided trigeminal foramen in representatives of

‘Testudinidae,’ and the occasional presence in individu-

als of ‘Emydidae’ and ‘Bataguridae’ (e.g., areolata, den-

tata, flavimaculata, N. platynota , and rubida). A signifi-

cant amount of variation can be observed in two speci-

mens of borneensis available to us, that exhibit left/right

asymmetry and the full spectrum from a fully intact (Fig.

137), to partially subdivided (Fig. 138), to fully subdi-

vided (Fig. 139) trigeminal foramen. Given that most

taxa are represented by three or fewer skulls in our

study, it is apparent that we are not able to fully docu-

ment the amount of variation exhibited by testudinoids.

(F) Contact between postorbital and squamosal

(Hirayama, 1985, 9).

Gaffney et al. (1991) noted that absence of this con-

tact is associated with the upper temporal emargination

and considered it informative at the level of their analy-

sis. Within our ingroup, all turtles have substantial upper

temporal emarginations, resulting in the contact being

just barely present, or just barely absent, or polymorphic

(e.g., picta, petersi , texana, crassicollis). See comments

above under character 9.

(G) Median premaxillary notch (Hirayama, 1985, 19;

Yasukawa et al., 2001, 9)

(H) Large cusps near the suture of the premaxillae and

maxillae (Hirayama, 1985, 28).

Initially, we were faced with the problem of defin-

ing these two characters independently from one anoth-

er, because the presence of two tightly spaced, opposing

cusp-like structures along any margin will automatically

result in the development of a median notch. An addi-

tional problem relating to these characters is the ques-

tion of whether these features should be observed on the

ramphotheca or the maxilla.

Large, tooth-like cusps are clearly present in a num-

ber of taxa (e.g., thurjii ) but so is the full spectrum of

smaller cusps, making it impossible to clearly define

discrete character states. Furthermore, if all species were

evaluated for medial notches that existed even if the

cusps were removed, all taxa in our sample would show

a medial notch. We were unable to develop a consistent

method for scoring this character for all testudinoid

species.

(I) ‘‘Antero-medial portion of the upper triturating sur-

face formed by premaxillae and maxillae” (Hirayama,

1985, 23; Yasukawa et al., 2001, 13).

We are neither able to replicate the full meaning of

this character nor formulate truly discrete character

states. A connection with the development of the second-

ary palate is evident, but the morphology of this region

seems to be sufficiently covered by a number of other

characters.

Vol. 10, p. 74

Asiatic Herpetological Research

2004

(J) Participation of the vomer in the foramen praepalat-

innm (Crumly, 1982, 10; Hirayama, 1985, 32; Yasukawa

et al., 2001, 15).

Within testudinoid turtles, the foramen praepalat-

inum perforates the nasal cavity at the border between

the premaxilla and the vomer. When the foramen is posi-

tioned slightly more anteriorly, it is fully surrounded by

the premaxilla, when it is minutely farther posterior it is

surrounded by the vomer. Considering the impact of

such minute changes, it is not surprising that our scoring

for this character generally seems to be in conflict with

that of Hirayama (1985) and Crumly (1982). This char-

acter appears to be subject to great intraspecific varia-

tion.

(K) Foramen palatinum posterius enclosed within the

brain cavity (Hirayama, 1985, 34).

According to Hirayama (1985), in reevesii (only)

the foramen palatinum posterius is enclosed within the

region of the brain cavity due to a flared descending

process of the parietal. We cannot confirm this observa-

tion for any testudinoid turtles (including three speci-

mens of reevesii).

(L) Participating bones in the processus trochlearis

oticum (Hirayama 1985, 37; Gaffney and Mey l an, 1988,

Gaffney et al. 1991, 6; McCord et al., 1995, 8; Shaffer et

al., 1997, 74, 258 Yasukawa et al., 2001, 18).

The relative participation of the prootic, parietal,

and quadrate to the processus trochlearis oticum was

used previously by a number of authors to infer phylo-

genetic relationships within turtles. Our observations

confirm the great variety of morphologies that can be

observed in this region. However, the amount of

intraspecific variation is considerable and the full spec-

trum of possible morphologies seems to be filled, mak-

ing it difficult to discern discrete character states. Future

research in the area may result in more clearly defined

discrete character states.

(M) Length of the crista supraoccipitalis (Hirayama,

1985, 40).

A long crista supraoccipitalis was observed by

Hirayama (1985) for borneensis. The character states he

used are defined by relative length of the crista supraoc-

cipitalis to the “condylo-basal length.” Unfortunately,

we could not replicate this because it is not clear exact-

ly how the length of the crista was measured.

Furthermore, a true morphological gap seems to be

missing between the admittedly very long crista of

borneensis and other ‘batagurids’ with an elongated

crista. This character is problematic, because it is poor-

ly defined and lacks discrete character states.

(N) Bony sutures and sulci lost in old adults (Hirayama,

1985, I).

According to Hirayama (1985), loss of sutures and

sulci occurs in baska, borneoensis, and borneensis only.

We are able to confirm this, but we do not have individ-

uals of all other species that are sufficiently old enough

to positively confirm that they also do not exhibit this

feature at old age. In subsequent treatments, loss of

sutures and loss of sulci should be treated as separate

characters.

(O) Ossification of cornu branchiale II (Hirayama,

1985, 48; Yasukawa et al., 2001, 20).

This character was used previously to unite tortois-

es with a number of ‘batagurid’ taxa (Hirayama, 1985).

The hyoid apparatus of turtles is often disarticulated in

skeletal preparations, making is difficult to positively

confirm if an ossified cornu branchiale is present or

absent. However, for those taxa for which we were able

to observe the hyoid apparatus, we were not able to con-

firm Hirayama’s (1985) observation of a reduced cornu

branchiale II in some ‘batagurids’ (e.g., galbinifrons,

spengleri). Instead, these taxa exhibit a cornu branchiale

II that is not significantly different from most other

‘batagurids.’

(P) Double articulation between the fifth and sixth cer-

vical vertebrae (Hirayama, 1985; Gaffney and Mey lan,

1988, FI. 5).

Most articular surfaces of the cervical column are

rather homogenous within all testudinoid turtles

(Williams, 1950). A double articulation between the fifth

and sixth cervical previously was considered to be a

unique character that unites the ‘Emydinae’ (McDowell,

1964). This character also was used by Hirayama (1985)

and with reservations by Gaffney and Meylan (1988).

Our observations generally confirm the presence of a

more or less clear double articulation in most ‘emydids,’

however, this features is also present in a number of

‘batagurids’ confirming that this character is highly vari-

able within the ingroup (Williams, 1950; Gaffney and

Meylan, 1988). Unfortunately, discrete character states

are lacking; we were able to observe the full morpholog-

ical spectrum from a clear singular articulation to a clear

double articulation.

(Q) Scapular prong with lateral concavity (Hirayama,

1985, E).

Hirayama (1985) reported this character as an

autapomorphy for subtrijuga only. However, we cannot

identify this morphology in any of our specimens of sub-

trijuga.

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(R) Large facet of the ilium for the testoscapularis and

testoiliacus (Hirayama, 1985, T; Yasukawa et al., 2001,

34)

(S) Extensive development of both testoscapularis and

testoiliacus (Hirayama, 1985, U).

An extensive development of the testoscapularis

and testoiliacus muscles together with an associated

large scar on the ilium was reported by Bramble (1974)

for Asian and North American box turtles. Whereas we

have no reason to doubt his assessment of the develop-

ment of these muscles for box turtles, we were not able

to score this character for most of the remaining taxa.

The shape of the ilium was explored and illustrated for

some ‘emydids’ and ‘batagurids’ by Yasukawa et al.

(2001:122-123).

(T) Ossification of the epipubis (Gaffney and Meylan,

1988, F5.5).

The identification (and confirmation of presence or

absence) of an ossified epipubis (Fig. 141) is somewhat

difficult for most species, because it seems to ossify

rather late in ontogeny, and can fall off during prepara-

tion. Our tentative observations confirm the presence of

an ossified epipubis in numerous adult ‘emydids’ and

‘batagurids,’ typically terrestrial forms (e.g., T. ornata,

G. insculpta , N. platynota, yuwonoi). An improved sam-

ple of adult specimens of all taxa, however, is necessary

to reveal the true distribution of this character.

(U) Diploid Number of Chromosomes (Hirayama, 1985,

0; Shaffer et al., 1997, 43).

The diploid number of chromosomes was used by

Carr and Bickham (1986) to hypothesize a sister group

relationship between the ‘Emydinae’ and subtrijuga, fol-

lowed by borneensis and crassicollis and finally the rest

of the ‘Batagurinae.’ Whereas most ‘batagurids’ alleged-

ly have 52 chromosomes, subtrijuga, borneensis, crassi-

collis, and ‘emydids’ are supposed to have 50 chromo-

somes. We view these results with caution, because a

brief review of the relevant literature reveals great dif-

ferences in chromosomal counts for a variety of taxa.

For instance, according to the work of Killebrew (1977)

and Bickham (1981), amboinensis has 52 chromosomes,

however, Gorman (1973) reported only 50. Similar con-

flicts can also be found for dentata (Bickham, 1981;

DeSmet, 1978; Gorman, 1973; Stock, 1972), subtrijuga

(Bickham, 1981; Killebrew, 1977), trijuga (DeSmet,

1978; Carr and Bickham, 1986), sinensis (Bickham,

1981; Killebrew, 1977; Stock, 1972), crassicollis

(Killebrew, 1977; Stock, 1972; Bickham and Baker,

1976), and some of the species currently placed in

Graptemys (Killebrew, 1977; McKown 1972),

Trachemys (DeSmet, 1978; Killebrew, 1977; Stock,

1972) and Mauremys (Killebrew, 1977; Stock, 1972).

This conflict in primary data is probably best understood

when considering the nature of testudinoid chromo-

somes: whereas 14 pairs of chromosomes have a consid-

erable size, all of the remaining ones are extremely

small. Given these circumstances, it seems reasonable to

hypothesize that one pair of chromosomes may be

unrecognized during analysis.

(V) Plica media spade-shaped (Gaffney and Meylan,

1988, F7.1).

The penile soft anatomy of turtles was comprehen-

sively reviewed by Zug (1966) and one of his characters,

the shape of the plica media, was used by Gaffney and

Meylan (1988) to unify species placed in Chrysemys,

Deirochelys, Trachemys, and Pseudemys as a mono-

phyletic group. In his detailed description of the plica

media, Zug (1966) referred to the shape of this structure

as being “spade-shaped” in those taxa, but made similar

claims for other taxa too. Furthermore, based on the

illustrations that were provided by Zug (1966) for other

taxa, the plica media of species placed in Graptemys,

Malaclemys, Rhinoclemmys, and Platysternon appear

“spade-shaped” also, even though Zug (1966) did not

explicitly use those descriptive words. This anatomical

system should be carefully reevaluated for all testudi-

noids, with special attention given to definition of dis-

crete characters.

(W) Ossifications within the fenestra postotica.

In some taxa, portions of the fenestra postotica are

closed or obscured by ossifications (noted, but without

exemplars, by Gaffney, 1972). In our largest specimen

of grandis (CAS 228443) a short, spike-like ossified

process extends posterodorsally from the dorsal edge of

the quadrate process of the pterygoid, and crosses the

fenestra postotica. It is situated ventral to the stapes (col-

umella auris), medial to the incisura columella auris, and

lateral to the fenestra ovalis (Fig. 141). In some speci-

mens, the dorsal tip of a similar structure approaches or

meets a posterodorsally-inclined process that extends

from the dorsal surface of the pterygoid, near the suture

with the prootic. In our largest specimen of N. platynota

(CAS 228342) the two processes meet to enclose the

stapedial shaft in a ring of bone situated at approximate-

ly the midpoint between the fenestra ovalis and the

medial opening of the incisura columella auris. Our

other, smaller, specimen of N. platynota shows no devel-

opment of these processes. It seems likely that there is

an ontogenetic component in the expression of this fea-

ture. It does not appear to have any systematic signifi-

cance, but in any case it is not widespread within

Testudinoidea.

Vol. 10, p. 76

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Conclusions

Our observations can be used to draw some tenta-

tive conclusions regarding the current level of under-

standing about morphological variation within testudi-

noid turtles. In addition, we provide some cautionary

statements about the quality of morphological data now

in use for assessing systematic relationships among

these turtles. It is clear from a perusal of the relevant lit-

erature, and from our data, that there is reasonably

strong morphological support for a monophyletic

‘Testudinidae.’ Support for monophyly of ‘emydines’

and ‘batagurines’ is not as impressive. The paraphyly of

‘Batagurinae’ (with respect to ‘Testudinidae’) was

explicitly proposed by Hirayama (1985) and has been

generally accepted since that time, although some

strides have been made towards resolving relationships

among some ‘batagurine’ taxa. The monophyly of

‘Emydinae’ seems to have been implicitly assumed by

many workers, but remains to be established in the con-

text of a rigorous phylogenetic analysis of all relevant

taxa. The interpretation of several morphological fea-

tures shared between some ‘emydines’ and some

‘batagurines’ as either convergence or synapomorphy

remains an important and interesting challenge. For

example, there are intriguing morphological similarities

between subtrijuga and some species classified in the

genus Graptemys (e.g., contact of the jugal and descend-

ing process of the parietal; contact of the quadratojugal

with the articular facet of the quadrate; contact between

the quadratojugal and the maxilla; ventral process of the

pterygoid approaching the articular surface of the

quadrate). These similarities may be due to functional

convergence as a result of a molluscivorous diet, but

they raise questions about the propriety of utilizing sub-

trijuga as an outgroup for systematic studies of ‘emy-

dines’ (e.g., Burke et al., 1996). Additional similarities

are reported for chromosome numbers in subtrijuga and

‘emydines’ (see ‘Problematic Character’ U, above).

A seriously deficient understanding of morphologi-

cal variation is one of the greatest inadequacies of cur-

rent perspectives on morphological data in turtles gener-

ally, and testudinoids specifically. Few published studies

have been conducted to evaluate the range and causes of

sexual, ontogenetic, intra- and inter-population variation

in morphological characters within testudinoids. Our

preliminary considerations of ontogenetic variation,

combined with reports of sexual variation (e.g., Berry

and Shine 1980; Gibbons and Lovich, 1990; Stephens,

1998) and new studies exploring the complex interac-

tions of morphological evolution with behavioral char-

acteristics and environmental conditions in turtles (e.g.,

Lindeman, 2000; Herrel et al., 2002; Joyce and Gauthier,

2003; Claude et al., 2003) emphasize the importance of

pursuing these questions further. Our decision not to

produce a phylogenetic hypothesis in this paper was

based primarily on two considerations. The first is the

relatively small sample size we used for many taxa in

this study (although it is comparable to sample sizes

from other, previously published, studies), and the fact

that several taxa are not represented in our work. The

second consideration is our sense that the current under-

standing of morphological variation in testudinoid tur-

tles is insufficiently mature to permit reliable phyloge-

netic hypotheses based solely on morphological data.

The most expedient way to address the need for greater

documentation of variation within testudinoid species is

to utilize existing museum collections to the greatest

extent possible, and secondarily to develop responsible

collecting programs that are designed with this need in

mind.

Our results also indicate that morphological data

matrices currently in the literature should not be taken at

face value. We had particular difficulties replicating

some of the scoring in the Hirayama (1985) matrix. That

seminal analysis (completed prior to the widespread use

of computer-assisted analytical methods in systematics)

laid the foundation for nearly all subsequent work on

‘batagurine’ morphology (including our own), and its

importance in shaping our current conceptualization of

‘batagurine’ phylogeny cannot be overstated. The work

of pathfinders in all fields of inquiry is often subjected

to the greatest scrutiny by the next generation of

researchers. Our statements and contradictory observa-

tions in this paper in no way denigrate Hirayama’s work;

instead, we view our efforts as minor attempts to correct

the few inconsistencies in his analysis, and to contribute

our observations to the body of knowledge that he began

to synthesize 20 years ago.

The accurate interpretation and understanding of

the morphological descriptions of previous authors were

among the great challenges we faced when we began our

studies of testudinoid skeletal morphology. Much of our

confusion could have been averted if adequate illustra-

tions accompanied all published character descriptions,

but such documentation often is an expensive undertak-

ing. Our photographs of character states discussed in

this paper are intended to facilitate communication

among turtle enthusiasts, and to provide a baseline for

future comparisons and discussions about testudinoid

morphology. We hope that adequate illustration of all

newly proposed characters will become standard prac-

tice among turtle systematists. It seems likely that our

interpretations of characters will differ in some respects

from those of our colleagues, and we anticipate that our

decisions regarding ‘problematic characters’ (discussed

above), and our choices with respect to ‘lumping’ or

‘splitting’ previously published character states, will

generate much spirited discussion in the years ahead.

2004

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Vol. 10, p. 77

Figure 1. Character 1(0): CAS 228437, texana, Figure 2. Character 1(1): CAS 228404, belliana,

anterior view. anterior view.

Figure 3. Character 2(0): CAS 228458, texana , Figure 4. Character 2(1): CAS 228404, belliana ,

left lateral view. left lateral view.

Figure 5. Character 3(0): CAS 228444, mouhotii ,

left ventrolateral view of orbit.

Figure 6. Character 3(1): CAS 228443, grandis,

left ventrolateral view of orbit.

HM

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Figure 7. Character 4(0): CAS 228443, grandis ,

right anterolateral view of orbit.

Figure 8. Character 4(1): CAS 228420, mouhotii,

right anterolateral view of orbit.

Figure 9. Character 5(0): CAS 228444, mouhotii,

left anterolateral view of orbit.

Figure 10. Character 5(1): CAS 228438, texana ,

left anterolateral view of orbit.

Figure 11. Character 6(0): CAS 228443, grandis,

right posterolateral view.

Figure 12. Character 6(1): CAS 228439, texana,

right posterolateral view, postorbital removed.

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Figure 13. Character 7(0) and 8(0): CAS 228438, Figure 14. Character 7(1) and 8(1): CAS 228445,

texana, left anterolateral view of orbit. subtrijuga, left anterolateral view of orbit.

Figure 15. Character 9(0): CAS 228447,

orbicularis, left lateral view.

Figure 16. Character 9(1): CAS 228444,

mouhotii, left lateral view.

Figure 17. Character 9(2): YPM 14074,

galbinifrons, left lateral view.

Figure 18. Character 9(2): YPM 14080,

galbinifrons, left lateral view.

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Figure 19. Character 10(0): CAS 228444,

mouhotii, left lateral view.

Figure 20. Character 10(0): CAS 228446,

subtrijuga, left lateral view.

Figure 21. Character 10(1): YPM 10339,

hamiltonii, left lateral view of orbit.

Figure 22. Character 11(0) and 12(0):

CAS 228447, orbicularis, left lateral view.

Figure 23. Character 11(1) and 12(1):

CAS 228446, subtrijuga, left lateral view.

Figure 24. Character 12(1): CAS 228438,

texana, right posteroventral view of lower

temporal fossa.

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Figure 25. Character 13(0): CAS 228361,

reevesii, anterior view.

Figure 26. Character 13(0): CAS 228419,

amboinensis , anterior view.

Figure 27. Character 13(1): CAS 228371,

spengleri , anterior view.

Figure 29. Character 14(0): CAS 228443,

grandis , left posterolateral view of orbit.

Figure 28. Character 14(0): CAS 228444,

mouhotii, left posterolateral view of orbit.

Figure 30. Character 14(1): CAS 228438,

texana , left posterolateral view of orbit.

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Figure 31. Character 15(0): CAS 228342,

N. platynota , ventral view of palate.

Figure 32. Character 15(1): CAS 228419,

amboinensis, ventral view of palate.

Figure 33. Character 16(0) and 17(0): ' Figure 34. Character 16(1) and 17(1):

CAS 228447, orbicularis , ventral view of palate. CAS 228420, mouhotii, ventral view of palate.

Figure 35. Character 18(0): CAS 228443, Figure 36. Character 18(1): CAS 228444,

grandis, right lateral view of trigeminal foramen. mouhotii, right dorsolateral view of trigeminal

foramen.

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Figure 37. Character 19(0): CAS 228447,

orbicularis, ventral view of palate.

Figure 38. Character 19(1): TMM 2813,

berlandieri, ventral view of palate.

Figure 39. Character 20(0): CAS 228335,

crassicollis, ventral view of palate.

Figure 40. Character 20(1): FMNH 259430,

tentoria, posteroventral view of palate.

Figure 41. Character 21(0): CAS 228443,

grandis, ventral view of brain case.

Figure 42. Character 21(1): CAS 228338,

reticularia, ventral view of brain case.

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Figure 43. Character 22(0): CAS 228443,

grandis , ventromedial view of right basicranium.

Figure 45. Character 23(0): CAS 228437,

texana , right lateral view of quadrate.

Figure 44. Character 22(1): CAS 228445,

subtrijuga , ventromedial view of right

basicranium.

Figure 46. Character 23(1): CAS 228342,

N. platynota, right lateral view of quadrate.

Figure 47. Character 24(0): CAS 228447,

orbicularis , right lateral view of mandible.

Figure 48. Character 24(1): CAS 228335,

crassicollis , right lateral view of mandible.

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Figure 49. Character 25(0): CAS 228447,

orbicularis, left lateral view of mandible.

Figure 50. Character 25(1): CAS 228411,

carbonaria, left lateral view of mandible.

V

Figure 51. Character 26(0): CAS 228404,

belliana , left lateral view of mandible.

Figure 52. Character 26(1): CAS 228361,

reevesii, left lateral view of mandible.

Figure 53. Character 27(0): CAS 228361,

reevesii, left posterolateral view of mandible.

Figure 54. Character 27(1): YPM 10861, thurjii,

left posterolateral view of mandible.

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Figure 55. Character 28(0): CAS 228342,

N. platynota, ventral view of palate.

Figure 56. Character 28(1) and 29(0):

CAS 228437, texana , ventral view of palate.

Figure 57. Character 28(1) and 29(0):

CAS 228445, subtrijuga , ventral view of palate.

Figure 58. Character 29(0): CAS 228419,

amboinensis , ventral view of palate.

Figure 59. Character 29(1 ): CAS 228361 ,

reevesii , ventral view of palate.

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Figure 60. Character 30(0), 31(0), and 32(0):

CAS 228447, orbicularis , oblique ventral view of

palate.

Figure 62. Character 30(1) and 32(1):

TMM 2813, berlandieri, ventral view of palate.

Figure 61. Character 30(1) and 31(1):

CAS 228437, texana , oblique ventral view of

palate.

Figure 63. Character 32(2): CM 124246, petersi,

ventral view of palate.

Figure 64. Character 33(0): CAS 228443,

grandis, dorsal view of mandible.

Figure 65. Character 33(1): CAS 228361,

reevesii, dorsal view of mandible.

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Figure 66. Character 34(0) and 35(0):

CAS 228448, blandingii, dorsal view of

carapace.

Figure 67. Character 34: CAS 228451,

crassicollis , dorsal view of juvenile carapace

showing tricarinae.

Figure 68. Character 34(1) and 35(1):

CAS 228444, mouhotii, dorsal view of carapace.

Figure 69. Character 36(0): CAS 228376, Figure 70. Character 36(1): CM 259430, tentoria

galbinifrons, posterior view of shell. anterior view of shell.

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Figure 7 1 . Character 37(0) and 38(0):

CAS 228346, blandingii, dorsal view of

carapace.

Figure 72. Character 37(1) and 38(1):

CAS 228343, spengleri, dorsal view of carapace.

Figure 73. Character 37(2): CAS 228408,

elongata, dorsal view of carapace.

Figure 74. Character 38(2): CAS 228399,

horsfieldi , dorsal view of carapace.

Figure 75. Character 38(3): CAS 228445,

subtrijuga, dorsal view of neurals II - IV.

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Figure 76. Character 39(0): CAS 228399, Figure 77. Character 39(1): CAS 228375,

horsfieldi, posterodorsal view of carapace. Carolina, posterodorsal view of carapace.

Figure 78. Character 40(0): CAS 228371,

spengleri, dorsal view of carapace.

Figure 79. Character 40(1): CAS 228430,

carbonaria, anterodorsal view of carapace.

Figure 80. Character 41(0): CAS 228368,

spinosa, dorsal view of carapace.

Figure 81. Character 41(1): CAS 228450,

N. platynota, dorsal view of carapace.

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Figure 82. Character 42(0): CAS 228338, Figure 83. Character 42(1): FMNH 259430,

reticularia , posterodorsal view of carapace. tentoria, posterodorsal view of carapace.

Figure 84. Character 42(2): CAS 228344, emys, Figure 85. Character 43(0): CAS 228413,

posterodorsal view of carapace. insculpta, posterodorsal view of carapace.

Figure 86. Character 43(1): YPM 14678,

platynota, posterodorsal view of carapace.

Figure 87. Character 43(2): CAS 228345,

amboinensis, posterodorsal view of carapace.

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Figure 88. Character 44(0): CAS 228368,

spinosa , dorsal view of carapace.

Figure 89. Character 44(1): CAS 228335,

crassicollis , dorsal view of carapace.

Figure 90. Character 45(0): CAS 228430,

carbonaria , anterodorsal view of carapace.

Figure 92. Character 46(0): YPM 11653,

spengleri, posterodorsal view of carapace.

Figure 91. Character 45(1): CAS 228341,

grandis, dorsal view of first vertebral scute,

anterior to top.

Figure 93. Character 46(1): CAS 228368,

spinosa , posterodorsal view of carapace.

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Figure 94. Character 47(0): CAS 228371,

spengleri, dorsal view of carapace.

Figure 95. Character 47(1): YPM 10382,

blandingii , dorsal view of carapace.

Figure 96. Character 48(0): CAS 228450, Figure 97. Character 48(1): CAS 228430,

N. platynota, left dorsolateral view of carapace. carbonaria, left dorsolateral view of carapace.

Figure 98. Character 49(0): CAS 228458, texana

(left); 49(1): CAS 228341, grandis (right); dorsal

view of pygals.

Figure 99. Character 49(2): CAS 228449,

pardalis , posterior view of carapace.

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Figure 100. Character 50(0): CAS 228399,

horsfieldi, lateral view of carapace.

Figure 101. Character 50(1): CAS 228375,

Carolina , lateral view of carapace.

Figure 102. Character 51(0): CAS 228342,

platynota, ventral view of anterior plastral lobe.

Figure 104. Character 51(2): CAS 228408,

elongata, internal view of shell from posterior.

Figure 103. Character 51(1): CAS 228419,

amboinensis, ventral view of anterior plastral

lobe.

Figure 105. Character 51(3): CAS 228406,

insculpta , internal view of shell from posterior.

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Figure 106. Character 51(4): YPM 14073, thurjii, Figure 107. Character 52(0): YPM 691, Carolina ,

left ventral view of first thoracic rib. ventral view of posterior plastral lobe.

Figure 108. Character 52(1): CAS 228434,

blandingii, ventral view of posterior plastral

lobe.

Figure 110. Character 52(3): CAS 228361,

reevesii, medial view of partial right shell.

Figure 109. Character 52(2): CAS 228349,

pardalis, medial view of partial right shell.

Figure 111. Character 52(4): CAS 228341,

grandis , medial view of partial right shell.

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Figure 112. Character 53(0): CAS 228447,

orbicularis, ventral view of carapace.

Figure 114. Character 54(0): CAS 228399,

horsfieldi, ventral view of shell.

Figure 113. Character 53(1): CAS 228345,

amboinensis (left); CAS 228373, blandingii

(right); ventral view of carapaces.

Figure 115. Character 54(1): CAS 228345,

amboinensis, ventral view of shell.

Figure 117. Character 55(1): YPM 12653, erosa,

right posterolateral view of carapace.

Figure 116. Character 55(0): CAS 228403,

tornieri, right posterolateral view of carapace.

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Figure 120. Character 59(0): CAS 228416,

impressa , dorsal view of epiplastra.

Figure 121. Character 59(1): CAS 228397,

carbonaria , dorsal view of epiplastra.

Figure 118. Character 57(0): CAS 228335,

crassicollis , anterior view of shell.

Figure 119. Character 58(0): CAS 228335,

crassicollis, posterior view of shell.

Figure 122. Character 60(0): CAS 228437,

texana, ventral view of anterior plastral lobe.

Figure 123. Character 60(1): CAS 228345,

amboinensis, ventral view of anterior plastral

lobe.

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Figure 124. Character 61(0): CAS 228437,

texana , ventral view of posterior plastral lobe.

Figure 126. Character 61(2): CAS 228376,

galbinifrons , ventral view of posterior plastral

lobe.

Figure 128. Character 63(0): CAS 228450,

platynota, ventral view of plastron.

Figure 125. Character 61(1): YPM 14678,

N. platynota, ventral view of posterior plastral

lobe.

Figure 127. Character 62(0): CAS 228345,

amboinensis (left); 62(1): CAS 228376,

galbinifrons (right); ventral view of anal scutes.

Figure 129. Character 63(1): CAS 228368,

spinosa, ventral view of plastron.

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Figure 130. Character 64(1) and 65(1):

TNHC 62532, ornata, lateral view of right

scapulacoracoid.

Figure 132. Character 67(0) and 68(0):

YPM 14677, blandingii, top view of lower arm

and manus.

Figure 134. Character 69(0): YPM 2983,

terrapin, top view of lower arm and manus.

Figure 131. Character 66(0): CAS 228345,

amboinensis (left); 66(1): CAS 228397,

carbonaria (right); coracoids.

Figure 133. Character 67(1) and 68(1):

YPM 16450, horsfieldi, top view of lower arm

and manus.

Figure 135. Character 69(1): YPM 14445,

spengleri, top view of lower arm and manus.

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Figure 136. CAS 228348, punctularia, right

lateral view.

Figure 137. FMNH 224107, borneoensis, left

anterolateral view of trigeminal foramen.

Figure 138. FMNH 224107, borneoensis, right

anterolateral view of trigeminal foramen.

Figure 139. FMNH 224122, borneoensis , right

anterolateral view of trigeminal foramen.

Figure 140. CAS 228378, Carolina, dorsal view Figure 141. CAS 228443, grandis,

of pelvis. posteroventral view of otic region.

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As practicing vertebrate paleontologists, we also

hope that our efforts here will stimulate additional inves-

tigation and publication of the extensive fossil record of

testudinoid turtles. Morphology is, of course, of para-

mount importance for the interpretation of fossils. Our

visits to many museums in the last several years

revealed an abundance of unpublished testudinoid fossil

material. Although a phylogenetic analysis was not a

goal of this research, we adopt the convenient and now

familiar means of summarizing morphological data by

providing a character matrix that summarizes some of

our observations. Although character data can be used to

assist paleontologists in diagnosing fossil testudinoid

specimens, we also encourage paleontologists to utilize

our study as a starting point for basic morphologic

descriptions. Description of differential diagnostic char-

acters generally is an adequate minimum for the erection

of a new taxon. However, such a diagnosis is, in itself,

not particularly helpful to systematists trying to score a

matrix and place a fossil into a broader phylogenetic

context. Descriptions of new fossil specimens (and taxa)

will be most useful if they include discussions of char-

acter state data for all preserved anatomical regions.

This current summary of morphological characters that

traditionally are used in systematic treatments of testudi-

noids can be used as a preliminary guide to the anatom-

ical regions and features that would be most useful when

included as part of a description of new fossil material.

Acknowledgements

We are greatly indebted to a number of institutions

and their staff for providing generous access to skeletal

and wet specimens: Jens Vindum (CAS), Stephen

Rogers and John Wiens (CM), Alan Resetar and

Maureen Kearney (FMNH), John Simmons and Linda

Trueb (KU), Jim McGuire (LMNH), Jose Rosado

(MCZ), Travis LaDuc and David Cannatella (TMM),

Harold Dundee (TUMNH), and Gregory Caldwell-

Watkins and Jacques Gauthier (YPM). We extend our

thanks to Rick Van Dyke for the gift of specimens to

support this research. Gabe Bever, Julien Claude, Jason

Downs, Jacques Gauthier, Jason Head, Pat Holroyd,

Howard Hutchison, Lyndon K. Murray, Jim Parham, and

Krister Smith (in alphabetical order) provided useful

comments and criticisms regarding this project. All

images containing YPM specimens were reproduced

with courtesy of the Peabody Museum of Natural

History, Yale University, New Haven, CT. Special

thanks go to Ted Papenfuss and Jim Parham for provid-

ing us with the unique opportunity to publish the results

of this study, and to Julien Claude and Howard

Hutchison for their detailed and insightful reviews. The

Brett Stems Award for Chelonian Research (CAS), the

Visiting Scholar Fund (FMNH), and Yale University

Graduate Fellowships provided funding to WGJ.

Additional financial support was provided by the

Geology Foundation of The University of Texas at

Austin.

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Appendix 1

List of specimens used.

agassizii, CAS 33867, FMNH 216746, FMNH 250843;

alabamensis , CM 95968, CM 95991; amboinensis, CAS

153872, CAS 228345, CAS 228369, CAS 228412, CAS

228419, FMNH 224009; annandalei , FMNH 258876,

FMNH 258879, FMNH Moll3036; annulata, CAS

SUR7425, CM 87903, YPM 15410; arachnoides, MCZ

54050; areolatus , MCZ 42214; areolata , CM 47957,

CM 87904; barbouri, CAS SUR12063, TUMNH 15400,

TUMNH 15428, TUMNH 15429, TUMNH 16899;

basket, FMNH 224095, FMNH 224097, FMNH 224213,

FMNH 224124, FMNH 224226; bealei, CM 118554,

FMNH 255270, FMNH 226542; belliana, CAS 228394,

CAS 228404; berlandieri , TNHC 2813; blandingii,

CAS 12837, CAS 228346, CAS 228373, CAS 228434,

CAS 228448, YPM 14677, YPM 10382; borneensis ,

FMNH 224001, FMNH 224003, FMNH 224004,

FMNH 224005, FMHH 224140; borneoensis, FMNH

224107, FMNH 224122, FMNH 224129, FMNH

251499, MCZ 42198; carbonaria , CAS 228397, CAS

228411, CAS 228427, CAS 228430; caretta, CAS 8383,

FMNH 31021; Carolina , CAS 228375, CAS 228378;

caspica, CAS 141118, CM 118517, FMNH 19714,

FMNH 74505, FMNH 98764; chilensis, CM 112252;

coahuila, KU 46929, KU 92623, MCZ 120335; crassi-

collis, CAS 228335, CAS 228451, FMNH 11091, MCZ

7821, MCZ 134451; decor ata, CM 118590; dentata,

CAS 134332, KU 47170, MCZ 29567, CAS 228333,

CAS 228362, CAS 228414; elegans, CAS 228396; elon-

gata , CAS 228408, FMNH 183740, FMNH 257382;

emys, CAS 228344, FMNH 63749, FMNH 224034; ern-

sti, TUMNH 13460, TUMNH 13462, TUMNH 16899;

erosa, YPM 12653; flavimaculata , TUMNH 15375,

TUMNH 15404, TUMNH 15747, TUMNH 15787;

flavomarginata, CAS 18040, CAS 228356, CAS

228357, CAS 228359, FMNH 21651 5\flavomarginatus,

MCZ 1 64926 \forsteni, CAS 228433; galbinifrons, CAS

228358, CAS 228360, CAS 228367, CAS 228376, YPM

14074, YPM 14080; geographica , CAS 12809,

TUMNH 15391, TUMNH 15392, TUMNH 15410,

TUMNH 15430; geometricus, MCZ 32184; gibba, CAS

228392; graeca, CAS 217732, CAS 228435, LMNH

54855, LMNH 54861; grandis , CAS 228341, CAS

228443, FMNH 224038, YPM 15431; guttata , CAS

8696, CAS 228372, CAS 228386, FMNH 211573;

hamiltonii , MCZ 120333, YPM 10399; hermanni, CAS

228400, CAS 228401, CAS 228402; homeana , CAS

228409, CAS 228423, CAS 228428, CAS 228429, CAS

228455, FMNH 19794; horsfieldi , CAS 120707, CAS

228398, CAS 228399, CAS 228421, CAS 228425, YPM

16450; impressa, CAS 228416; G. insculpta, CAS

228406, CAS 228407, CAS 228413; japonica, YPM

15482, YPM 15486; kachuga, FMNH 224128, FMNH

224152; kleinmanni, CAS 228422, CAS 228426, CAS

228431; kohnii, TUMNH 10237, TUMNH 12121,

TUMNH 14544, TUMNH 15678; leprosa, CM 137031;

marmorata, CAS no number, CAS 188533, CAS

220052, FMNH 22076; mouhotii, CAS 228365, CAS

228374, CAS 228420, CAS 228444; muhlenbergii,

LMNH 55352, MCZ 52248; mutica, LMNH 54883; P.

nelsoni, CM 67311; nigra, CAS 8125, CAS 8289;

nigrinoda , TUMNH 15147, TUMNH 15317, TUMNH

15408, TUMNH 15750; ocellata, CAS 228336; G.

oculifera, TUMNH 26, TUMNH 3359, TUMNH 7548,

TUMNH 12402, TUMNH 16928; P. oculifera , CAS

165598, CAS 220645, CAS 220646; odoratus, YPM

13622, CAS 228351, CAS 228352, CAS 228353; orbic-

ularis, CAS 173223, CAS 228347, CAS 228415, CAS

228447, LMNH 10347, YPM 15479; T. ornata, CAS

228381, CAS 228382, CAS 228383, CAS 228384,

TNHC 62532; ouachitensis, CM 61656, CM 84696;

pardalis, CAS 148630, CAS 228349, CAS 228410,

CAS 228418, CAS 228432, CAS 228449; petersi, CAS

8608, CM 124246, CM 124247; picta, CAS 13889, CAS

228379, CAS 228380, CAS 228385; N. platynota, CAS

228342, CAS 228450, CM 118586, FMNH 224216,

YPM 14678; polyphemus, CAS 14090, LMNH 43344,

LMNH 43354, LMNH 59320; pulcherrima, CAS

11754, CAS 228355, CAS 228366, CAS 228377; pul-

chra, LMNH 48092; punctularia, YPM 465, CAS

228348; reevesii, CAS 31437, CAS 228361, CAS

228364; reticularia, CAS 228338, CAS 228388, LMNH

14565, LMNH 14569, LMNH 49145, LMNH 54856,

LMNH 78580; rubida, CM 87907, CM 87908;

rubriventris, CM 34409, CM 45188; scripta, CAS

SUR8642, CAS 228436, CAS 228442, LMNH 15684;

serpentina, CAS 228452, YPM 6369, CAS 228457;

siebenrocki, CAS 228393; signatus, CAS 228405, MCZ

42217, MCZ 42218; sinensis, CAS 18031, CAS

228339; spengleri, CAS 21008, CAS 228331, CAS

228332, CAS 228343, CAS 228371, YPM 11653, YPM

14445; spinifera, CAS 65705, CAS 228350, CAS

228354, YPM 656; spinosa, CAS 228368. CAS 228459;

subglobosa, CAS 228334; subtrijuga, CAS 16996, CAS

228445, CAS 228446, CAS 228453, CAS 228454; sub-

rufa, CAS 228389, CAS 228390, CAS 228391; tchepo-

nensis, CAS 228363, CAS 228370; tecta, CM 89923;

tentoria, FMNH Moll3026, FMNH Moll3028, FMNH

Moll3032, FMNH 259430; tentorius, MCZ 41944,

MCZ 46604; terrapin, CAS 43640, CAS 228340, CAS

228387, YPM 2983; texana , CAS 30965, CAS 228437,

CAS 228438, CAS 228439, CAS 228440, CAS 228441,

CAS 228456, CAS 228458; thurjii, FMNH 224135,

FMNH 224153, MCZ 62523, MCZ 62524, YPM 14072,

YPM 14073, YPM 14074; tornieri, CAS 139704, CAS

228395, CAS 228403, CAS 228417, CAS 228424; tri-

Vol. 10, p. 106

Asiatic Herpetological Research

2004

Aldabrachelys, Dipsochelys,

Geochelone, Megalochelys

Geochelone

Geochelone, Indotestudo

Chrysemys , Pseudemys, Trachemys

Geochelone, Manouria

Graptemys

Kinixys

Homopus

Graptemys, Malaclemys

Cistoclemmys, Cuora, Geoemyda

Gopherus

Chrysemys, Pseudemys

Geochelone, Indotestudo, Manouria

Callopsis, Geoemyda, Rhinoclemmys

Chrysemys, Pseudemys, Trachemys

Cistoclemmys, Cuora

Graptemys, Malaclemys

Psammobates

Graptemys

Testudo

Geoemyda, Heosemys

Clemmys

Geoclemys

Testudo

Kinixys

Agrionemys, Testudo

Geochelone, Manouria

Calemys, Clemmys, Glyptemys

Clemmys, Mauremys

Kachuga

Pseudotestudo, Testudo

Graptemys

Clemmys, Mauremys

Geoemyda, Heosemys

Kinixys

Testudo

Clemmys, Emys

Geoemyda, Rhinoclemmys

Cuora, Cyclemys, Geoemyda, Pyxidea

Calemys, Clemmys, Glyptemys

Clemmys, Mauremys

Callopsis, Geoemyda, Rhinoclemmys

Kinixys

Chrysemys, Pseudemys, Trachemys

Chrysemys, Pseudemys

Terrapene

Chelonoidis, Geochelone

Chinemys

Graptemys, Malaclemys

Morenia

Graptemys, Malaclemys

Psammobates

Cyclemys

2004

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Vol. 10, p. 108

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Vol. 10, p. 109

10110

2004

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Vol. 10, pp. 110-113

Trade Data and Some Comments On the Distribution of

Mauremys annamensis (Siebenrock, 1903)

Minh Le1’*, Thang Hoang2, and Due Le3

1 American Museum of Natural History, Department of Herpetology,

Central Park West at 79th Street New York, NY 10024

-19th Le Thanh Tong St., Hanoi, Vietnam

3 WWF Indochina Programme, 53-Tran Phu St., Ba Dinh, Hanoi, Vietnam; IPO Box 151, Hanoi, Vietnam

* E-mail: minhl@amnh.org

Abstract. - This trade survey of Annam Pond Turtle reveals that this species is likely to have larger distribution than

previously thought. The records in the trade in Quy Nhon and Ho Chi Minh City suggest its range could extend much

further south. In addition, given the one way south-north trade route, the absence of Mauremys mutica in the trade

south of Hai Van Pass and the reported absence of M. annamensis in the trade north of the Pass support the hypoth-

esis that the Pass is the natural barrier for the two species ranges. This hypothesis combined with the long existence

of the Pass might indicate that the speciation between the two species happened when their ancestors dispersed across

the Pass, and were subsequently isolated, by the means of rafting or walking through narrow land strip emerged dur-

ing the low sea level period. In terms of conservation, M. annamensis has become much rarer even in the trade, sug-

gesting immediate conservation measures to protect it.

Key words. - Mauremys annamensis, Bataguridae, Hai Van Pass, Truong Son Range, distribution, biogeography.

Distribution of Mauremys annamensis. - The Annam

Pond Turtle, Mauremys annamensis, was first described

by Siebenrock in 1903 based on a specimen collected

from Phuc Son or Phuoc Son (15° 33' 00" N; 108° 04'

00" E) (southwest of Tourane, now known as the city of

Da Nang) in Central Vietnam. Another specimen was

collected by Bourret from Fai Fo (Hoi An), an ancient

city about 50 km from Da Nang (Bourret, 1941). Since

then, it seems that little effort has been made to record

the distribution of this species in the wild. Iverson

(1992) and Iverson et al. (1999) cite only the above

records from Bourret for their maps of global turtle dis-

tribution.

According to Bourret (1941), this species was very

abundant in the marshes and slow-moving water bodies

in the lowland areas of the cities of Hoi An and Da

Nang. Both Hoi An and Da Nang, however, are now

very populated cities surrounded by rice paddies, which

are unlikely to be suitable habitats for this species. This

is because the intensive use of chemicals, such as herbi-

cides and pesticides, in rice paddies through out Vietnam

makes it difficult for turtles to survive in this environ-

ment.

To better understand its distribution, we did a 6-day

trade survey in the August of 1996. The survey covered

three cities, namely Quy Nhon (13° 46’ 00” N; 109° 14’

00” E), Da Nang, and Hue (16° 28' 00" N; 107° 36’ 00"

E), and their surrounding areas. We interviewed turtle

dealers at the collecting points, where turtles were

bought from collectors and awaited to be shifted to

China. We used the book Turtles of the World (Ernst and

Barbour, 1989) for identification key. In addition, since

the initial purpose of the survey is to determine the trade

status of M. annamensis, we identified, but did not

record the availability of other turtle species in the col-

lecting points.

We observed that this species was still common in

the trade in Quy Nhon and Da Nang. In Quy Nhon and

its outskirt, we visited three collecting points. In the first

one, we identified 2 adult M. annamensis. In the other

two collecting points, we found 3 and 4 juveniles,

respectively. In Da Nang and its surrounding areas, we

visited four sites with three to four specimens in each

sites. They were all young and juvenile turtles. From the

interviews with local people in Quy Nhon and Da Nang,

it was apparent that this species could well survive in the

human-modified environment, such as lakes and fish-

ponds, if there were no collecting activities by local peo-

ple. Local trade dealers and collectors, encountered in

collecting points in Quy Nhon and Da Nang, suggested

that this species still existed in the water bodies in the

nearby region. Le and Trinh (2001) also indicated that

the species could occur in Tra My, Tien Phuoc, and

probably Hiep Due Districts, Quang Nam Province.

The occurrence of M. annamensis in Quy Nhon is

very interesting since this species had been believed to

have very restricted distribution. More remarkably, Le

and Broad (1995) reported that M. annamensis even

extended far south to Ca Mau, Minh Hai Province inhab-

iting Melaleuca forests (around 9° 29' 00" N; 105° 20'

Vol. 10, p. Ill

Asiatic Herpeto/ogical Research

2004

Map scale: 1:15,000,000

Figure 1. Topographic map of Vietnam.

00" E;) situated at the southern tip of Vietnam. It is pos-

sible that Le and Broad misidentified this species in their

survey (Jenkins, 1995). However, Peter Paul van Dijk,

Le Trong Dat, and Douglas Hendrie on May 30, 2000

found this species in Ben Chuong Duong Street shops in

Ho Chi Minh City (Hendrie, 2000a). This evidence com-

bined with the one-way trafficking of turtles (from south

to north) (Le and Broad, 1995) indicates that M. anna-

mensis may have much wider distribution than previous-

ly thought.

This hypothesis is also supported by Le and Trinh

(2001). Their interviews with local dealers, in May

2001, in Quang Nam Province revealed that one dealer

in Thang Binh District bought this species from the ship-

ments transported from the south. Le and Trinh (2001)

also suggested that A/, annamensis is naturally distrib-

uted in Tra My, Tien Phuoc, and probably Hiep Due

Districts, Quang Nam Province. These authors also indi-

cated an interesting fact that turtle hunters only sell their

animals to the local dealers. This manner of trade

demonstrates that the local trade data can be informative

in determining the limit of the natural ranges of some

species.

It is noted that we did not encounter any M. mutica

in the areas in Quy Nhon and Da Nang. Le and Trinh

(2001) also did not find any M. mutica in their trade

investigation, which covered seven districts and one

town in Quang Nam Province, and the city of Da Nang.

According the pattern of turtle trade in Vietnam plotted

by Le and Broad (1995), turtles have been collected

from the south and transported to the north. They are

finally destined in the border between and Vietnam and

China, where they are traded in an enormous volume.

The one-way south north trafficking leads to the conclu-

sion that M. mutica does not occur in Da Nang, located

in the southern side of Hai Van Pass, or southern areas

of the city.

In the survey, we found no evidence for M. anna-

mensis distributed in the northern side of the Hai Van

Pass. Interviews with turtle dealers from two collecting

points in the city of Hue (north of Hai Van Pass)

revealed that this species was only transported to the city'

from the south and there was no record of this species in

the surrounding areas. It is also interesting that the deal-

ers called this species Rua Dep Nam (Beautiful Southern

Turtle) as compared to Rua Dep Bac (Beautiful Northern

Turtle), here referred to Mauremys mutica. According to

them, M. mutica came only from areas north of Hai Van

Pass. In the house of a trader in Hue, we observed about

20 M. mutica from 1 to 2 kg, but no M. annmensis. In the

other site, we did not find any M. mutica or M anna-

mensis.

Given the fact that Hue and Da Nang is only 100 km

apart, it is very likely that Hai Van Pass (at around 16°N)

forms the natural boundary of these two species since

the Pass stands in between two cities. Records from pre-

vious studies also support this hypothesis (Iverson.

1992; Nguyen and Ho, 1996). Thus, the mountain range,

which cuts through the country, is most certainly the

northern boundary of M. annamensis' range and south-

ern boundary of M. mutica's range. Because they are the

lowland inhabitants, the Pass (1712m above sea level at

the summit) seems to be a significant barrier.

Some studies have suggested that the Pass is the

border between two zoological regions. Northern

Central Vietnam (Northern Truong Son) and Central

Vietnam (Central Truong Son) for such groups as rodent,

bird, fish, and lizard (Bobrov, 1993; Dao, 1978. Cao,

1989). In addition, Fooden (1996) showed in Figli that

the distribution two closely related gibbon taxa,

Hylobates gabriellae siki and H. gabriellae gabriellae ,

has been separated by the Pass. Even though primate is

more likely to possess higher dispersal ability, the barri-

er seems significant enough to block their expansion. In

2004

Asiatic Herpeto/ogical Research

Vol. 10, p. M2

fact, the Truong Son Mountain Range in general has

established dispersal barriers for Cuora galbinifrons

species complex (Stuart and Parham, 2004).

Hai Van Pass is a part of Truong Son Mountain

Range (Annamite Mountains), which runs throughout

most of the country’s length. The Pass meets the South

China Sea and effectively divides the country into two

different sections. It is formed by aluminous granite, and

probably emerged about 250 Mya in the early Triassic

(Lepvrier et al., 1997). If the Pass is actually the natu-

ral boundary of these two species’ ranges, it can be

hypothesized that the speciation between M annamensis

and M mutica was occurred when their ancestors dis-

persed across the Hai Van Pass and then were subse-

quently isolated. Since these turtles are good swimmers,

one possible scenario is that they rafted on the sea to get

to the other side of the Pass. Another possibility is that

they traveled south through a narrow land belt exposed

during the low sea level period. According to Prentice

and Denton (1988), before from 6 Mya to 0.9 Mya the

sea level fluctuated at an average of 70m below the pres-

ent sea level. At this level, a few kilometers of the con-

tinental shelf could be opened to the east of the Pass

(Voris, 2000) and well served as a travel route for these

turtles. However, these hypotheses are very preliminary

and, therefore, should be carefully tested in a much more

comprehensive study in the future.

Trend in the trade of M. annamensis. - In recent years,

turtles in the Southeast Asian region, especially in

Vietnam, have been critically threatened by the trade

with China. The trade has been driven by the Chinese

long tradition of using turtles as food and medicines.

Many species might go extinct in very near future unless

urgent protection measures are implemented (van Dijk,

2000; Hendrie, 2000). In Vietnam, species such as

Cuora trifasciata , believed to be able to cure cancer, is

at considerable risk due to its significant economic value

(about 1 000 USD per individual or even more (Lovich et

al ., 2000; Le and Trinh, 2001)). For M. annamensis , in

addition to the general demand from China, there are

also interests in keeping them as pets in countries such

as the U.S. The United States Fish and Wildlife Service

indicated that from 1996 to 1999 small numbers were

imported to the U.S. from Vietnam (Consideration of

Proposals for Amendment of Appendices I and II).

Weissgold (2002) even maintained that the imports

increased during 1999-2001. Due to the risk posed by

the trade and habitat destruction, this species has been

listed in the Appendix II and in the critically endangered

category by CITES and IUCN, respectively.

It is clear that the number of M. annamensis has

declined dramatically in recent years. The market value

of this species, approximately $5 to $7 per kg (Le and

Broad, 1995; Le and Trinh, 2001; and this survey), can

generate substantial interests among poor local people.

In our survey in 1996, this species was still pretty com-

mon in the trade. My personal observation in Dong

Xuan market, Hanoi, in 1998 also confirmed the com-

monness of this species. More recently, Hendrie (2000b)

reported that the occurrence of this species in turtle con-

fiscated shipments is less frequent compared to the pre-

vious years. Le and Trinh (2001) reported that this

species was very rare in the trade compared to other

species — only second to Golden Turtle ( Cuora trifasci-

ata). In fact, they only encountered only one juvenile in

the whole period of the survey. Thus, this species should

be given the highest priority in conservation programs in

the near future.

Acknowledgments

We would like to thank Drs. Ross Kiester and James

Juvik for their support of the field trip. Bryan Stuart

encouraged and convinced ML that the information in

this paper is important. Comments from two anonymous

reviewers and Jim Parham help improve the paper. ML

is supported by a NASA grant (No. NAG5-8543) to the

Center for Biodiversityand Conservation at the

American Museum of Natural History and a Columbia

University/CERC Faculty Fellowship.

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toises in Asia, Running, Yunnan Province, China.

2004

Asiatic Herpetological Research

Vol. 10, pp. 1 14-1 1 9 1

Neotype of Testudo terrestris Forsskal, 1775 (Testudines, Testudinidae)

Jarmo PeralA1 and Roger Bour2

^ Department of Biological and Environmental Sciences, PO Box 65 (Biocenter 3, Viikinkaari 1),

FIN-00014 University of Helsinki, Finland; E-mail: jarmo.perala@helsinki.fi

^ Laboratoire des Reptiles et Amphibiens, Museum national d’Histoire naturelle,

25 rue Cuvier, 75005 Paris, France; E-mail: bour@mnhn.fr

Abstract. - We discuss and clarify the nomenclatural status of Testudo terrestris Forsskal, 1775. Testudo terrestris, a

taxon based on a syntype series, was until now a valid name for tortoises from parts of Egypt, Arabia and the Levant,

according to the International Code of Zoological Nomenclature. On the contrary, all type locality restrictions from

the 20th century regarding the name Testudo terrestris Forsskal, done without the fixation of a name-bearing specimen

(lectotype or neotype), are invalid. Because the name is valid, and because the syntypes, listed but not identified in

the original description, are untraceable, and to permanently fix the name and its type locality, we designate a neotype

for Testudo terrestris Forsskal based on a specimen from Aleppo, Syria.

Key words. - Taxonomy, Testudines, Testudinidae, Testudo terrestris Forsskal, 1775, nomenclatural validity, neotype.

Forsskal and Mediterranean tortoises. - During his

fatal travel (1761-1763) in the eastern Mediterranean

countries, the Finn Petter Forsskal (1732-1763) encoun-

tered tortoises, briefly described by the name Testudo

terrestris in his diary, which was published as a posthu-

mous work by Carsten Niebuhr (1733-1815), a German

traveller and surveyor, in 1775 [= Forsskal, 1775].

Strauch (1862: 69) remarks in a footnote that Forsskal

(1775) discusses a tortoise, Testudo terrestris, which

occurs in Aleppo and Lebanon, without describing it,

and Anderson (1896: 68) writes that “it is useless

attempting to identify this animal” “from Loheia, north

of Hodeida,” with reference to Forsskal (1775).

Forsskal ’s itinerary took him through the following

localities: Malta, Smyrna (Izmir), Constantinople, Alex-

andria, Rosetta, Cairo, Suez, Jedda, ending up in Yarim,

Arabia Felix (Yemen), where Forsskal died of malaria in

1763. Tortoises were reported from A1 Lufyayyah

(Yemen), Cairo (Egypt), Lebanon, Lattakia (A1 Ladhiq

-Tyah) and Aleppo (both in Syria) (Fig. 1). Forsskal

(1775) indicated that the chelonians are called “Zol-

hafae” by the Arabs (Forsskal, 1775); as for their distri-

bution, he specified: “Kahirae non frequens vivit,

Aleppo autem & ad Libanon copiosor,” translated by

Daudin (1801: 225) as: “It is rare in Cairo, but can be

found rather abundantly near Aleppo and towards

Mount Lebanon”. At best, Forsskal himself was thus

able to see tortoises in situ in northern Egypt (Nile Delta

and Suez area) only, that is those which are actually

called either Testudo kleinmanni Lortet, 1883 (the Egyp-

tian tortoise) or the vicariant T. werneri Perala, 2001.

This interpretation is in accordance with the vernacular

name of the Egyptian tortoise, Anderson (1898: 30;

“Sohlafa” pronounced “Zihlifa”) and Flower (1933:

742; “Educated people in Egypt employ the word ‘Zal-

heefah’”). Niebuhr’s subsequent route back home took

him via Basra, Baghdad, Mosul, Diyarbakir, Aleppo,

Lebanon and Palestine (Hansen, 1962; Niebuhr, 1772,

1973). Niebuhr, the only surviving member on the expe-

dition to Arabia Felix, continued to Bombay (Mumbai),

India, from where he shipped the natural history notes

(Niebuhr, 1772: xix) and specimens (Niebuhr, 1973:

120) collected by Forsskal via London to Copenhagen.

A considerable amount of material in the Forsskal col-

lection in Copenhagen was destroyed in bombings by

the British in 1807 (Nielsen, 1993). The type of T. ter-

restris is said to be "apparently lost" (Webb in Iverson,

1992). The name is not fixed to a single name-bearing

specimen.

Nomenclatural validity of Testudo terrestris. - Testudo

terrestris Forsskal, 1775, one of the oldest species group

names in the genus Testudo Linnaeus, 1758 sensu lato

(in the sense of Lapparent de Broin, 2001; Perala

2002a), is nomenclaturally valid, according to the

present International Code of Zoological Nomenclature

(ICZN, 1999): it was published before 1931 and thus

does not need to have a full diagnosis by which it can be

identified. Only “a description or a definition” per se is

needed (ICZN, 1999: Article 12). In this respect the

remark by Forsskal (1775) pertaining to the tortoises’

length (“...foot-long...”), as well as that made of the

shapes of plastra of both sexes, is enough, even if these

characters were incorrect. Moreover, although the name

Vol.10, p. 1 15

Asiatic Herpeto/ogical Research

2004

Figure 1. Map of geographical localities mentioned in

Forsskal's (1775) description, which together constituted

the type locality of Testudo terrestris Forsskal until the

present work.

is accompanied by the remark “Obs.” (Forsskal, 1775:

12), it is also listed under the headings “Descripta” (p.

viii) as well as “Nominata” (p. ix) alongside with valid

names such as Testudo triunguis Forsskal, 1775, that is,

current Trionyx triunguis. The book contains a multitude

of other descriptions of valid taxa which cannot be

rejected based on the arguments (see below) about the

use of the Latin language, a contemporary standard,

alone. Based on Niebuhr’s subsequent route back home,

Gasperetti et al. (1993) suggested that it may actually be

Niebuhr who is responsible for the name T. terrestris

Forsskal. As Niebuhr’s role is not explicit in the original

publication, the authorship of the name remains with

Forsskal (ICZN, 1 999: Art. 50.1.1 ).

Testudo terrestris overlooked, rejected, then revali-

dated. - After its publication, and during about 180

years, the nominal species Testudo terrestris Forsskal,

1775, although nomenclaturally valid, was nevertheless

overlooked by most authors (except Strauch, 1 862 and

Anderson, 1896), some of them (Gray, 1831; Dumeril

and Bibron, 1835) only mentioning Testudo zolkafa and

Testudo zohalfa , respectively, based on Forsskal’s

(1775) vernacular Zolhafae, and which nornina nuda

appear in the above works as synonyms of Testudo

graeca Linnaeus, 1758 and Testudo mauritanica

Dumeril and Bibron, 1835, respectively. On the other

hand, at least one scientist worked to revive the nominal

species. A brief history of the case is presented by Bour

in David (1994: 86). The name Testudo terrestris

Forsskal was resurrected, and therefore revalidated, by

Wermuth (1956: 402), who improperly (without speci-

men fixation) designated “Arabia” as type locality.

Simultaneously, Wermuth considered to ask the Interna-

tional Commission on Zoological Nomenclature to

invalidate the nominal species Testudo terrestris

Forsskal; unfortunately, his attitude changed radically

(1958: 149-153) and he used this name to designate the

Near Eastern population of Testudo (as Testudo graeca

terrestris Forsskal), restricting the type locality to

“Libanon-Gebirge, Israel” [sic], and mistakenly extend-

ing its range to Libya. It must be outlined that there is a

gap in the range of Testudo graeca ( sensu lato) complex

tortoises between Israel and Libya, the latter containing

the range of the recently described species Testudo

cyrenaica Pieh & Perala, 2002. Wermuth had at his dis-

posal one Libyan specimen (SMF 36127; paratype of T.

cyrenaica ), from Dernah, which he thought to be identi-

cal with Middle-Eastern tortoises (Pieh & Perala, 2002).

Wermuth’s validation was disapproved by Buskirk (in

Ernst et al., 2000; unpublished manuscript from the

early 1990s; and pers. comm, to both authors); H igh-

field (in Ernst et al., 2000; and: http: //www.tor-

toisetrust.org/articles/newfloweri.html); J. F. Parham

(pers. comm.); and Perala (1996); among others. Their

opposition is based on several arguments such as: a

description is lacking with reference to the remark

“Obs.” in Forsskal (1775); the species cannot be identi-

fied from the “description”; there is no type specimen: a

“false” type locality; the name “ Testudo terrestris ” is

just Latin for a terrestrial chelonian, used without inten-

tion to describe a new species.

Need of a neotype. - Rather to resurrect Testudo terres-

tris Forsskal (Wermuth, 1956). it would have been pref-

erable: (1) either to suppress this imprecise name (and

which is a more recent homonym of the nominal species

Testudo terrestris Fermin, 1 765, for which Wermuth had

to successfully request the invalidation by the Interna-

tional Commission on Zoological Nomenclature; ICZN,

1963: Opinion 660); (2) either to use it to name Testudo

kleinmanni , a name revalidated only in the 1950s by

Mertens & Wermuth (1955), and independently by Lov-

eridge & Williams (1957). It could still be possible to

ask the ICZN to officially suppress the name Testudo

2004

Figure 2. Neotype of Testudo terrestris Forsskal, 1775, specimen n° NMW 18674: 2, sub-adult female. Upper left: lat-

eral view (right side); Upper right: dorsal view; Lower left: ventral view. Lower right: living specimen of Testudo terres-

tris, adult female, from Aleppo (topotype); CL = 185 mm, Ml = 143 mm, HE = 99 mm.

terrestris Forsskal, 1775. However, we reject this option

because: (1) the name is presently widely used (in all

recent check-lists, with more than fifty references),

although with vagueness about the identity of the con-

cerned population; (2) there is no valid name to desig-

nate the species of Testudo living in the Middle-East,

more precisely in the area of the upper Euphrates -

Tigris drainage; (3) the name Testudo terrestris

Forsskal, 1775 became available by the very ruling of

the International Commission on Zoological Nomencla-

ture (ICZN, 1963), and it is unlikely that the Commis-

sion would reverse its opinion. Accepting the

nomenclature proposed by Wemuith, one of us (RB)

proposed to emend the type locality of Testudo terrestris

Forsskal to the vicinity of Aleppo (= Halab), Syria

(Bour, 1989: 14), in the interest of clarifying the status

of this taxon and as a first step towards the description

of a neotype. However, such restriction of the type

locality, as well as the earlier restrictions proposed by

Wermuth (1956, 1958), are invalid according to the

Code (ICZN, 1999; Art. 76.3), because these actions

were not done in connection with the selection of a lec-

totype or neotype. Therefore we here propose the formal

description of a neotype of Testudo terrestris Forsskal,

1775. All the animals listed (although not identified;

therefore untraceable) by Forsskal (from Al-Luljayyah,

Cairo, Lebanon, Lattakia and Aleppo) actually represent

syntypes, according to the Code (ICZN, 1999; Art.

72. 1 . 1 ), and thus the type locality of T terrestris encom-

passes the region containing all those localities (ICZN,

1999; Art. 73.2.3). A neotype could legitimately be

selected from any of those per se. Besides sea turtles,

only Centrochelys sulcata (Miller, 1779), a land tortoise

(possibly introduced), and Pelomedusa subrufa

(Lacepede, 1788), a fresh-water turtle, are known to

occur in Yemen (Obst & Wranik, 1987; Gasperetti et al.,

1993; Al Safadi, 1997); therefore no Testudo sp. could

have been observed in Al-Luljayyah by the Forsskal -

Niebuhr expedition. Following the earlier choice, made

in accordance with the available data, and also with the

current taxonomical practice (e.g., Perala, 2002b). in

order to preserve the stability of the nomenclature, and

Vol.10, p. 117

Asiatic Herpetological Research

2004

to objectively delimit Testudo terrestris Forsskal from

all other species in the Testudo graeca ( sd .) complex,

we choose a specimen collected in Aleppo (and which

locality has by chance a historical background in tor-

toise literature: cf. Siebenrock, 1913).

The neotype of Testudo terrestris. - To fix the name and

type locality, we hereby designate a specimen from the

Vienna Natural History Museum No. NMW 18674:2,

collected in Aleppo by Viktor Pietschmann in March

1910, as the neotype of Testudo terrestris Forsskal,

1775, according to Articles 75 and 76 (ICZN, 1999).

The neotype is a subadult female with a straight-line

carapace length (CL) of 136.8 millimeters. Note: all

morphometric characters are according to the standards

published in Perala (2001). As a result of our neotype

designation (ICZN, 1999; Art. 76.3), the type locality of

Testudo terrestris Forsskal, 1775 is restricted to Aleppo

(Alep, Halab; 36°12’ N, 37°09’ E), Syria (Syrian Arab

Republic). (For the range of T. terrestris , see Perala,

2002b.)

Description. - Sub-adult female. Most scutes marked

with about a dozen of conspicuous growth ridges and

grooves; areolae of the carapace feebly bumped, neatly

displaced caudally, and also dorsally on the costals.

Longitudinal profile high, regularly domed, highest at

third vertebral, slightly behind the middle of the shell

(Fig. 2, top left). The outline of the shell short, squarish,

anterior and posterior free borders only very feebly cut

out. Vertebrals wide in dorsal view, the fourth the small-

est; the first one with almost straight lateral borders,

moderately wider anteriorly than posteriorly (Fig. 2, top

right). Cervical (= nuchal) four-sided, very wide; supra-

caudal distally as wide as vertebrals, regularly convex in

its middle; all common sutures of marginals nearly sub

equal (= height of lateral ones, and length of anterior

and posterior ones); only marginals 9-11 are slightly

flaring. Gulars well prominent but short and narrow,

their common suture very short; a pair of rather large

axillaries on each side; pectorals with a very short com-

mon (medial) suture, included about four times in the

medial suture of humerals; inguinals small, separated in

a larger distal part and a very small proximal part con-

tacting femorals; rear lobe of plastron hardly mobile,

short, anals both long and wide, with parallel anterior

and posterior borders: their particular shape at first sight

resembles the usual shape observed in males (Fig. 2,

bottom left). Head covered above with two large and

roughly pentagonal scutes, the frontal and the prefron-

tal, symmetrical about their common suture. Five nails

at each hand, the inner one smaller but well developed;

four at each foot. Anterior side of the fore-arm covered

between the elbow and the wrist by about fifteen large

scutes, the four largest being triangular, neatly distinct

from the background of the scaly skin; outer border of

this area covered by a row of six triangular, overlapping

scutes. Tail relatively long and regularly tapering, also

giving a rather masculine appearance, ending with

slightly enlarged but discrete flat scutes; a small isolated

spur on each thigh.

General color greenish yellow, often lighter close to

the sutures, with large darker, grayish areas apparently

deep in the scutes. Blackish marks reduced on the cara-

pace, limited to incomplete and irregular narrow lines

along the anterior sutures of the scutes (marginals, cos-

tals), also on the lateral borders of vertebrals; areolae or

areolar areas slightly and irregularly flecked with black,

on costals 1-3 and on vertebrals 1-3. Dark patches wider

on the plastron, issued from the areolae, roughly extend-

ing along the rear third of each scute (from pectorals to

anals), restricted to a narrow band on the humerals; lim-

its of the patches are inconspicuous, with a gradual

shading, delimiting few lighter or darker radiating lines.

Soft parts mostly yellowish, in places with a brownish

tinge, with well contrasting blackish flecks on the homy

beak (upper and lower, forming a ‘moustache’), on pre-

frontal, on the large triangular scutes of the fore-arms,

and on the heels; all nails are also heavily pigmented,

from dark brown to black.

Additional morphometric data derived from the

neotype are presented in the following (all measure-

ments in mm): maximum plastron length (PL) = 122.7,

midline plastron length (PL-m) = 1 1 1.8, maximum mid-

body width (MI) = 100.2, maximum width of shell at

posterior marginals (MA) - 104.4, maximum gular

scute length (GU-1) = 15.3, maximum gular scute width

(GU-w) = 27.3, gular scute height (GU-h) = 13.2, maxi-

mum shell height (HE) = 70.0, maximum width of ante-

rior shell opening (ASO-w) = 69.9, maximum height of

anterior shell opening (ASO-h) = 21.9, left minimum

bridge length (BR) = 59.9, maximum humeral scute

width (HUM-w) = 63.7, maximum pectoral scute width

(PEC-w) = 86.6, maximum abdominal scute width

(ABD-w) = 89.9, maximum femoral scute width (FEM-

w) = 64.1, maximum anal scute width (AN-w) = 51.9,

maximum nuchal scute length (NU-1) = 1 1.4, maximum

nuchal scute width (NU-w) = 10.0, intergular length

(GU-m) = 13.4, interhumeral length (HUM-m) = 22.8,

interpectoral length (PEC-m) = 7.7, interabdominal

length (ABD-m) = 42.1, interfemoral length (FEM-m) =

10.8, interanal length (AN-m) = 18.7, maximum width

of first vertebral scute (Vl-w) = 35.2, maximum width

of second vertebral scute (V2-w) = 36.4, maximum

width of third vertebral scute (V3-w) = 41.0, maximum

width of fourth vertebral scute (V4-w) = 33.8, maxi-

mum width of fifth vertebral scute (V5-w) = 41.3, maxi-

mum length of first vertebral scute (V 1 -1) = 26.9,

2004

maximum length of second vertebral scute (V2-1) =

28.0, maximum length of third vertebral scute (V3-1) =

25.6, maximum length of fourth vertebral scute (V4-1) =

23.3, maximum length of fifth vertebral scute (V5-1) =

3 1 .8, first costal length (C 1) = 43.0, second costal length

(C2) = 28.7, third costal length (C3) = 28.1, fourth cos-

tal length (C4) = 22.9, maximum dorsal width of supra-

caudal (SUP-d) = 23.4, maximum ventral width of

supracaudal (SUP-v) = 40.4, maximum median length

of supracaudal (SUP-1) = 21.7, maximum head width

(HEAD) = 21.6, minimum distance between right eye

and tympanum (EYE-TY) = 6.9, minimum distance

between right eye and nostril (EYE-NO) = 6.5.

Figure 2 (lower right) depicts a living female (topo-

type) Testudo terrestris Forsskal from the type locality,

Aleppo, Syria.

Acknowledgments

We warmly thank James Buskirk (Oakland, CA) and

James Parham (University of California, Berkeley) for

personal communications, as well as two anonymous

reviewers for comments, which had a positive impact on

the manuscript, Richard Gemel, Heinz Grillitsch and

Franz Tiedemann (all from the Naturhistorisches

Museum, Vienna) for the loan of specimens, the Aca-

demic Kippis Society (AKS) for spiritual guidance, and

Annemarie Ohler (Museum national d’Histoire

naturelle, Paris) for logistical help.

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2004 Asiatic Herpetological Research . Vol. 10, PP- 120-125

An Ocadia sinensis x Cyclemys shanensis hybrid

(Testudines: Geoemydidae)

Maik Schilde1, Dana Barth2 and Uwe Fritz3

1 Opalstr. 31, D-043 19 Leipzig, Germany; E-mail: maik.schilde@ufz.de

-University of Leipzig, Institute of Zoology, Molecular Evolution & Animal Systematics,

Talstr. 33, D-04103 Leipzig, Germany; E-mail: dbarth@rz.uni-leipzig.de

3 Zoological Museum (Museum fur Tierkunde), Natural History State Collections Dresden, A. B. Meyer Building,

Konigsbriicker Landstr. 159, D-0 11 09 Dresden, Germany; E-mail: uwe.fritz@snsd.smwk.sachsen.de

Abstract. - A captive bred Ocadia sinensis x Cyclemys shanensis hybrid is described. Its hybrid status was confirmed

by a comparison of a 1036 bp fragment of the mitochondrial cytochrome b gene with the putative mother (C. shanen-

sis) and genomic ISSR fingerprinting. This is the first report of an intergeneric hybrid between very distantly related

geoemydid turtles. All previous geoemydid intergeneric hybrids have been crossings within or between two sister

clades containing the currently accepted genera ( Chinemys , Mauremys, Ocadia ) and ( Cuora , Pyxidea).

Key words. - Cyclemys, Ocadia, testudines, intergeneric hybrid.

Introduction

Recently several new cases of intergeneric chelonian

hybrids became known to science (reviewed in Galgon

and Fritz, 2002). Most of them belong to the Southeast

Asian family Geoemydidae, long known under its junior

synonym Bataguridae. However, current research on the

molecular phylogeny of geoemydids has shown that

some species traditionally attributed to different genera

are more closely related than previously thought (Wu et

al., 1999; McCord et ah, 2000; Honda et ah, 2002a, b;

Barth et ah, in press; Stuart and Parham, in press), sug-

gesting that they should be better lumped in the same

genus. Thus, some of the hybrids may be in fact not

intergeneric. In this paper we report a captive bred

hybrid between two distantly related Southeast Asian

geoemydids, representing an undoubtedly intergeneric

cross.

According to the cited studies, there are several

major clades among geoemydids. One clade contains the

currently recognized genera Chinemys, Mauremys,

Ocadia, Cuora, and Pyxidea (McCord et ah, 2000;

Honda et ah, 2002a, b; Barth et ah, in press), and anoth-

er one, being the sister clade, Cyclemys, Sacalia,

Heosemys, Hieremys, Notochelys, and Leucocephalon

(McCord et ah, 2000; Honda et ah, 2002b).

The turtle described herein is the result of a

hybridization of an Ocadia sinensis male and a

Cyclemys shanensis female, representatives of two of

the major clades of the Geoemydidae. This hybrid

demonstrates that very distantly related geoemydids are

capable of hybridizing successfully. It underlines the

possibility that some recently described Southeast Asian

chelonians ( Ocadia glyphistoma, O. philippeni ), which

are only known from few pet trade specimens, might

also be hybrids.

The specimen. - The turtle described below hatched in

the live collection of M. Schilde from an egg of a

Cyclemys shanensis, laid August 13, 2002. The second

egg of the same clutch did not develop. The mother was

a long term captive, and kept with a Cyclemys shanensis

male and two Ocadia sinensis males. The elongated

eggs measured 56.5 x 20.0 mm. One quickly developed

a white band as typical for fertile eggs. It was incubated

constantly at 28°C on Vermiculite. On October 26, 2002

a healthy turtle with a straight line shell length of 33 mm

hatched (Figs. 1-4). Its color pattern resembled Ocadia

sinensis but the general form was more similar to

Cyclemys (roofed, distinctly tricarinate shell, serrated

posterior marginal scutes), suggesting that it might be a

hybrid. We decided to use two molecular methods to test

this hypothesis.

Materials and Methods

We sequenced a 1036 bp portion of the mitochondrial

cytochrome b gene (cyt b) of the captive bred turtle for

comparison with the putative mother. Because mito-

chondrial DNA is inherited in the maternal line, the

sequence of the putative hybrid should be identical with

the mother ( Cyclemys shanensis ). Species identification

of the Cyclemys was done by morphological means and

comparison with the mitochondrial cyt b sequences of

Guicking et al. (2002); the Ocadia sinensis males were

determined morphologically.

Blood samples were obtained by coccygeal vein

puncture. Samples were stored as described in Haskell

Vol. 10, p. 121

Asiatic Herpetological Research

2004

Figure 1 .

Figure 2.

Figure 3.

Figure 4.

Fig. 1-4. The captive bred Ocadia sinensis x Cyclemys shanensis hybrid, September 2003 (11 months old). The roofed,

distinctly tricarinate shell and the serrated posterior marginals resemble Cyclemys spp. The neck and facial stripes as

well as the plastral pattern are similar to O. sinensis. The plastral pattern was more contrasting as a hatchling and has

faded during growth. Photos: F. Hohler.

and Pokras (1994) and Arctander (1988). Additional

blood samples and photographs (dorsal and ventral

aspects) of the captive bred turtle (MTD T1262), the

Cyclemys shanensis female (MTD T816), and the two

Ocadia sinensis males (MTD T8 1 7-8 1 8) are in the tissue

collection of the Zoological Museum Dresden. DNA

extraction was carried out using the QIAamp Blood

Mini Kit (Qiagen). Primers mt-A (Lenk and Wink, 1997)

and HI 5909 (Lenk et al., 1999) were used to amplify a

DNA fragment containing 1036 bp of cyt b. PCR and

sequencing conditions were as described in Barth et al.

(in press). Sequencing reactions were performed on an

ABI 3100 Genetic Analyzer. Alignment was carried out

with CLUSTAL X, v. 1.8 (Thompson et ah, 1997) with

default parameters. To demonstrate the considerable

genetic difference between Cyclemys and Ocadia com-

pared to other hybridizing geoemydids, Mega 2.1

(Kumar et ah, 2001) was used for estimation of genetic

distances. Cyt b sequence data for calculating genetic

distances are from Barth et ah (in press) and Guicking et

ah (2002).

To exclude the possibility of a gynogenetic or

parthenogenetic origin of the specimen and to identify

the putative father, we conducted genomic fingerprint-

ing with Inter Simple Sequence Repeats (1SSR) for the

captive bred specimen, the Cyclemys female and both

Ocadia males. ISSR PCR produces species-specific

genomic fingerprints (Gupta et ah, 1994; Zietkiewics et

ah, 1994; Wink et ah, 1998. 2001; Nagy et ah, 2003)

useful in detecting turtle hybrids (Wink et ah, 2001).

Hybrid specimens share about 50% of their ISSR PCR

products with the respective paternal and maternal

species (Wolfe et ah, 1998: Wink et ah, 2001; Storch et

ah, 2001 ). ISSR PCR is a simple and cheap method, and

the results are easily reproducible (Bornet and

Branchard, 2001). Gynogenesis or pseudogamy, the

development of unfertilized eggs by activation through

sperm of another species, as well as parthenogenesis is

not known in turtles. However, if the captive bred spec-

imen should be of such origin, the ISSR profiles should

be identical with its biological mother.

The primer 5 -GACAGACAGACAGACA-3' was

used to generate ISSR fingerprints for the captive bred

specimen, the putative mother ( Cyclemys shanensis ),

and both Ocadia sinensis males. Each reaction mix con-

tained 100 ng of genomic DNA, 20 pmol primer, 1 U

2004

Asiatic Herpetological Research

Vol. 10, p. 122

Table 1. ISSR fingerprints of the Ocadia sinensis x Cyclemys shanensis hybrid and parental species (bioogica

mother and father plus the second 0. sinensis male kept with the mother). Only polymorphic and diagnostic

products shown.

MTD T = Museum fur Tierkunde Dresden Tissue Collection; + = PCR product present, - = PCR product lacking.

Taq-polymerase (SIGMA), 2.5 pi lOx PCR buffer

(SIGMA) and 2.5 pi of 200 pM dNTPs in a total volume

of 25 pi. Amplification conditions were 4 min initial

denaturation (94°C), followed by 31 cycles of 1 min at

94°C, 1 min at 54°C, and 2 min at 72°C, final extension

of 7 min (72°C). PCR reactions were performed on an

Eppendorf thermocycler.

15 pi of each PCR reaction was separated on 2%

agarose gels (25 cm), stained in ethidium bromide solu-

tion (0.5 pg/ml) and visualized under UV light. The 100

bp DNA ladder Plus (MBI Fermentas) was used as a size

standard. PCR was repeated under identical conditions

to test reproducibility of results. DNA fragments were

scored manually. Band sharing coefficients were calcu-

lated according to Storch et al. (2001).

Results and Discussion

As expected, the cyt b sequence of the captive bred tur-

tle and the putative mother ( Cyclemys shanensis ; EMBL

acc. no. AJ604513) proved to be identical. ISSR finger-

printing produced highly variable profiles which were

species-specific and permitted individual identification

of both Ocadia sinensis males (Table 1). The captive

bred turtle shared 6 of its 13 bands with the mother

(band sharing coefficient 0.5) and 7 bands with one of

the O. sinensis males (band sharing coefficient 0.52).

Because the captive bred turtle and this O. sinensis male

exclusively share some fragments, we identified this tur-

tle as the biological father. Thus, both methods con-

firmed the hybrid origin of the captive bred turtle.

Except for an unconfirmed, anecdotal newspaper

record of natural hybrids between Cuora flavomargina-

ta and Geoemyda japonica in Japan (Anonymous,

1995), all previous geoemydid intergeneric hybrids have

been crossings within or between two sister clades con-

taining the currently accepted genera ( Chinemys ,

Mauremys, Ocadia) and {Cuora, Pyxidea ); Chinemys

reevesii x Cuora amboinensis kamaroma (Galgon and

Fritz, 2002), Chinemys reevesii x Mauremys japonica

(Yasukawa et al., 1992), Chinemys reevesii x Mauremys

mutica (= "Mauremys pritchardi" , Wink et al., 2001),

Cuora amboinensis kamaroma x Mauremys annamensis

(Fritz and Mendau, 2002), Cuora bourreti x Pyxidea

mouhotii (= "Cuora serrata ", Parham et al., 200 1 ; Stuart

and Parham, in press), Cuora galbinifrons x Pyxidea

mouhotii (= "Cuora serrata ", Parham et al., 2001; Stuart

and Parham, in press), and Cuora trifasciata x

Mauremys mutica (= " Mauremys iversoni", Parham et

al., 2001 ; Wink et al., 200 1 ). Cyclemys belongs to anoth-

er major clade, comprising the genera Cyclemys ,

Sacalia , Heosemys, Hieremys , Notochelys , and

Leucocephalon (McCord et al., 2000). Cyclemys is sep-

arated by a considerable genetic distance from Ocadia

(Table 2), surpassing the genetic distances of the other

hybridizing geoemydids.

Superficially our hybrid Ocadia sinensis x

Cyclemys shanensis resembles O. sinensis due to its

striped head and neck and the spotted plastral pattern.

This leads to the speculation that the morphologically

similar Ocadia philippeni McCord and Iverson, 1992

and O. glyphistoma McCord and Iverson, 1994 might be

also intergeneric hybrids, as earlier suggested by van

Dijk (2000), Fau and Shi (2000), Parham and Shi

(2001), and Galgon and Fritz (2002). Both species were

described on the basis of only a few pet trade turtles

(McCord and Iverson, 1992, 1994), and until now no

Vol. 10, p. 123

Asiatic Herpetological Research

2004

Table 2. Pairwise genetic distances (cyt b) between

hybridizing geoemydid species.

Cyt b

Geomydid species pairwise

distances

Chinemys reevesii - Cuora amboinensis 0.104

Chinemys reevesii - Mauremys japonica 0.050

Chinemys reevesii - Mauremys m utica 0.070

Cuora amboinensis - Mauremys annamensis 0.098

Cuora galbinifrons - Pyxidea mouhotii 0.059

Cuora trifasciata - Mauremys mutica 0.104

Ocadia sinensis - Cyclemys shanensis 0.118

additional specimens became known to science. For

some individuals of three other pet trade taxa a hybrid

status has been unambiguously demonstrated: Two tur-

tles identified as Mauremys pritchardi McCord, 1997

proved to be hybrids of Chinemys reevesii and

Mauremys mutica (Wink et al., 2001). Three Mauremys

iversoni Pritchard and McCord, 1991 originated from

crossing Cuora trifasciata and Mauremys mutica

(Parham et al., 2001; Wink et al., 2001), and several

Cuora serrata Iverson and McCord, 1992, have been

demonstrated to be hybrids between Cuora galbinifrons

and Pyxidea mouhotii and of Cuora bourreti and

Pyxidea mouhotii (Parham et al., 2001; Stuart and

Parham, in press).

Until now it is unknown whether all specimens of

these taxa are of hybrid origin, and if so, whether the

crosses occurred in the wild, in captivity, or whether one

or the other form might represent a natural, stable hybrid

taxon (Parham et al., 2001; Wink et al., 2001). Many

Southeast Asian chelonians are facing extinction due to

overexploitation (van Dijk et al., 2000). Therefore,

many conservation efforts are established around the

globe, including CITES listing and captive breeding

programs for several species. A correct taxonomy is the

prerequisite for any conservation measure. Hence, it is

crucial to determine whether the mentioned taxa repre-

sent real evolutionary entities and deserve high priority

in conservation, this includes also natural hybrid taxa

(Allendorf et al., 2001), or whether they are only inci-

dentally occurring hybrids, without any conservation

relevance.

Acknowledgments

Special thanks go to Michael Wink and Daniela

Guicking, Heidelberg, for sharing unpublished geoemy-

did sequences with us and to Thomas U. Berendonk,

Leipzig, for technical advice. James R. Buskirk,

Oakland, provided the newspaper report on Cuora flavo-

marginata x Geoemyda japonica hybrids.

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2004

Asiatic Herpetological Research

Vol. 10, pp. 126-128

New Data on the Trade and Captive Breeding of

Turtles in Guangxi Province, South China

Haitao Shi1, Zhiyong Fan2, Feng Yin3, and Zhigang Yuan4

' Department of Biology, Hainan Normal University, Haikou , 571158, Hainan Province, P. R. China.

E-mail:haitao-shi@263.net; Fax: 0898-65890520; Tel: 0898-66752479; 65883521.

-Fauna Division, The Endangered Species Import and Export Management Office of China (CNMA)

#18 Hepingli Dongjie, Beijing 100714, P. R. China.

J Department of Science and Education, China Wildlife Conservation Association, #18 Hepingli Dongjie,

Beijing 100714, P. R. China.

^Department of Biology, Guangxi Medicine University, 530021, Nanning, PR. China.

Abstract. - New data on the captive breeding and trade of turtles in Guangxi Province, China, are presented. These

data are from four turtle farms and three markets surveyed in May 2002. The scale of captive breeding in Guangxi

is larger than previously known. At the same time, the number of wild turtles in the markets may be decreasing.

Issues concerning the licensing of turtle farms and the effectiveness of enforcement are discussed.

Key words. - China, Guangxi, turtles, trade, farming.

Introduction

The People’s Republic of China is Asia’s most signif-

icant importer of tortoises and freshwater turtles and

more comprehensive studies on its wildlife trade are

urgently needed (Li and Li, 1997; van Dijk, et al., 2000).

There is a long history of wildlife consumption in

Guangxi, and traditional Chinese medicine is as popular

as in neighboring Guangdong Province. Li and Li( 1 997)

reported that there are at least 91 species of animals

involved in the wildlife trade in Guangxi, mostly turtles

and snakes. The sheer volume of the wildlife trade on

the border between China and Vietnam is astonishing,

and may be unprecedented in the history of internation-

al wildlife trade. Guangxi is one of the main corridor for

the import and export of wildlife from land and sea into

mainland China. Although China has recently increased

its level of protection for imported and exported turtles

(Meng et al., 2002), the effectiveness of these new meas-

ures is not well demonstrated. We report data on four

turtle farms and three markets surveyed in late May

2002.

Turtle farms

Shifu turtle farm (Shifu Town, Nanping City). - The

turtle farm was founded in 1996, its area is 65 ha. At it’s

height it included -70,000 turtles: -60,000 Trachemys

sripta elegans, -7,000 Pelodiscus sinensis , and -600

Ocadia sinensis. However during a very heavy flood on

July 5, 2001 in the area, almost all the turtles escaped or

drowned. The farm is rebuilding, but now includes only

-700 Mauremys mutica, -200 Palea steindachneri and

-50 Cuora trifaciata.

Quanming wildlife farm (Located at Quanming

Town, Daxin County). - The farm began to raise turtles

in 1996. It has -80 Mauremys mutica and 47 Chelydra

serpentina. Their 36 female Chelydra lay 30-35 eggs

three times every year. So they get more than 3000 eggs

every year. They are expanding to include Macroclemys

temminckii. Besides turtles, the wildlife farm also breed

successfully 1800 Tokay Geckos ( Gekko gecko ) and for

several decades has also bred the Masked Palm Civet

(Paguma larvata ).

Qingzhou turtle farm 1 (Qingzhou City). - This farm

has been raising turtles since 1981, but was not very suc-

cessful until 1997. In 2001, the farm had -1000

Mauremys mutica and -300 Cuora trifaciata. In the past

they also bred Trachemys scripta elegans , but switched

to Cuora trifaciata and Mauremys mutica due to the

higher price for the two species. The owner of this farm

claims that there are dozens more farms in Qingzhou

that were founded based stock from his farm. The phe-

nomena of Mauremys mutica mixed with Cuora trifaci-

ta was found here, mirroring the conditions of a farm in

Tunchang, Hainan Province (Shi & Parham, 2001). It

was impossible for us to visit the farm without the local

officials of Forestry Department forcing the farmer to

accept us. The owner prefers to remain secret in order to

avoid theft, taxes, and people wanting to borrow money.

Vol. 10, p. 127

Asiatic Herpetological Research

2004

Qingzhou turtle farm 2 (Qingzhou city). - This farm

was founded in 1986. It encompasses 4 hectares, and

includes —7,000 Mauremys mutica , —6,000 Trachemys

scripte elegans , -2700 Pelodicus sinensis, -800 Cuora

trifaciata, 200 Cuora flavomarginata and 3 Pelochelys

bibroni. Approximately, 30,000 hatchlings are bred

every year. Unlike the owner of the previously reported

farm, the owner of this farm, Wusong Ma, is friendly,

generous, and open to visitors. Many famous people

have visited his turtle farm, including a former Chinese

national vice-premier, the Governor of Guangxi, and the

Minister of Agriculture Department. Unfortunately, all

this attention may have led to a large theft of Mauremys

mutica in April of 2001. According to the owner of the

farm, the value of these turtles was 50,000 USD. Despite

this, Mr. Ma remains non-secretive and has even set up

at least 20 additional farms.

Remarks on turtle farms. - The senior author (HS)

looked over the licenses for captive breeding of turtles at

the Forestry Department of Guangxi Province. More

than 600 farms (of various sizes, including small breed-

ing operations) were licensed in Guangxi Province. Zou

Yi, an official in the Guangxi Forestry Despartment,

informed us that another governmental department

(Agriculture Department) issues even more licenses for

turtle farming, but we do not have these numbers.

Moreover, most breeding operations are illegal and not

licensed. Consequently, determining the actual number

of commercial, often secretive, turtle breeders will

require intensive survey and investigation.

Turtle Markets

Nanning Road Trade Market in Nanning City. - Five

stalls with 14 species and 194 turtles were found in this

market. The species included 58 Pelodiscus sinensis, 24

Pyxidea mouhotii, 21 Platysternon megacephalum, 17

Mauremys mutica, 15 Trachmys script a elegans, 1 3

Cyclemys dent at a, 13 Palea steindachneri, 12 Sac alia

quadriocellata, 8 Indotestudo elongata, 4 Cuora

amboinensis, 4 Ocadia sinensis, 2 Heosemys grandis, 1

Hieremys annandalei, andl Orlitia borneensis.

Dongfeng Market in Qingzhou City. - Three stalls

with 9 species and 64 were found in Dongfeng Market

in Qingzhou. The species included 19 Trachmys scripta

elegans, 1 8 Indotestudo elongata, 9 Manouria impressa,

5 Malayemys subtrijuga, 4 Cuora amboinensis, 4

Pyxidea mouhotii, 2 Geoemyda spengleri, 2 Heosemys

grandis, and 1 Cuora galbinifrons.

Danqing Wholesale Market in Nanning City. - 5 stalls

with 4 species and 42 turtles were found in this market.

Sixty (71%) of the turtles were Platysternon mega-

cephalum. Platysternon was sold at every stall. I was

told that they came from turtle farms, but they refused to

tell where these turtle farms were.

Remarks on turtles. - According to Lu Qi, the vice

director of the Wildlife Management Section of the

Guangxi Forestry Department, the past three years have

seen a sharp decrease in the numbers of turtles in the

markets and he attributes this to increased enforcement.

This increased enforcement coincides with an ever-

growing commercial effort to breed these turtles. For

example, Manying Huang (professor of biology at

Guangxi Medicine University) states that there are over

3000 families that raise Cuora trifasciata in Nanning

City. However, the increased level of enforcement has

led to many captive-bred turtles also being confiscated.

If indiscriminant confiscations continue it could depress

the development of captive breeding of turtles in China.

Acknowledgments

We would like to thank Manying Huang, professor at

Guangxi Medicine University, Qi Lu, Zou Yi and others,

officials in Forestry Deaprtment of Guangxi Province,

for their assistance with the survey. This work was fund-

ed by National Natural Science Foundation of China

(No. 30260019), Foundation for University Key Teacher

by the Ministry of Education and Wildlife Conservation

Association of China. James Parham helped to correct

the English and provided helpful comments.

Literature Cited

Li, Y. and D. Li. 1997. The investigation on wildlife

trade across Guangxi borders between China and

Vietnam. Conserving China’s Biodiversity. Reports

of the Biodiversity Working group, China Council

for International Cooperation on Environment and

Development: 118-127.

Meng, X., Z. Zhou and B. L. Stuart. 2002. Recent

actions by the People’s Republic of China to better

control international trade of turtles. Turtle and

Tortoise Newsletter 5:15-16.

Shi, H. and J. F. Parham. 2001. Preliminary

Observations of a large turtle farm in Hainan

Province, People’s Republic of China. Turtle and

Tortoise Newsletter, issue 3: 4-6.

2004

Asiatic Herpetological Research

Vol. 10, p. 128

van Dijk, P. P., B. L. Stuart and A. G. J. Rhodin (Eds.).

2000. Asian Turtle Trade: Proceedings of a

Workshop on Conservation and Trade of Freshwater

Turtles and Tortoises in Asia. Chelonian Research

Monographs 2:1-164.

2004

Asiatic Herpetological Research

Vol. 10, pp. 129-150

Recent Records of Turtles and Tortoises from

Laos, Cambodia, and Vietnam

Bryan L. Stuart1’2’3’4’* and Steven G. Platt4’5

1 Field Museum of Natural History, Department of Zoology, Division of Amphibians & Reptiles,

1400 S. Lake Shore Drive, Chicago, Illinois 60605 USA. E-mail: bstuart@fieldmuseum.org

* Corresponding author and address

z University of Illinois at Chicago, Department of Biological Sciences (M/C 066),

845 W. Taylor, Chicago, Illinois 60607 USA

3 Wildlife Conservation Society, P.O Box 6712, Vientiane, Lao PDR

4 Wildlife Conservation Society, P.O. Box 1620, Phnom Penh, Cambodia

5 Present address: Department of Math and Science, Oglala Lakota College,

P.O. Box 490, Kyle, South Dakota 57752-0490 USA

Abstract. - The chelonian fauna of Laos, Cambodia, and Vietnam remains poorly known and is currently threatened

by widespread and intensive exploitation for food and traditional Chinese medicine. The distributions of many species

are uncertain owing to a paucity of records. Because turtles are so extensively traded in the region, most records now

come from animals in trade. We emphasize that authors must be explicit about how their records were obtained to

allow other workers the ability to critically evaluate the accuracy of the distribution record. We here present detailed

information on recent (1993-2002), vouchered records of 19 species of freshwater turtles, tortoises, and marine tur-

tles collected in the field or obtained from hunters, abandoned hunting camps, villages, or markets in Laos, Cambodia,

and Vietnam.

Key words. - Testudines, turtles, tortoises, Laos, Cambodia, Vietnam, distribution.

Introduction

Although mainland Southeast Asia has long been

regarded as a hotspot of chelonian diversity (van Dijk et

al., 2000), the turtle and tortoise fauna of Laos,

Cambodia, and Vietnam (formerly known as French

Indochina) remains poorly known. Biological investiga-

tion was limited prior to World War II, and since then

decades of civil unrest, political instability, and military

conflict have largely prevented fieldwork. Consequently

few museum records exist (summarized by Iverson,

1992) and with the exceptions of Smith (1931) and

Bourret (1941), little information is available on the

occurrence and distribution of chelonians in former

French Indochina. A recent photographic identification

guide to the region (Stuart et al., 2001) and country

reviews of Laos (Stuart and Timmins, 2000), Cambodia

(Touch et al., 2000), and Vietnam (Flendrie, 2000) sum-

marized information on chelonian distributions, but pro-

vided few details concerning new records on which

these accounts are based.

Exploitation of chelonians for food and medicinal

markets is widespread in Laos, Cambodia and Vietnam

(Jenkins, 1995; Le Dien Due and Broad, 1995, Lehr,

1997; Timmins and Khounboline, 1999; van Dijk et al.,

2000; Ziegler, 2002; Holloway 2003). Hunters in rural

villages capture turtles and tortoises for local consump-

tion or to sell to traders who periodically visit villages to

purchase wildlife. Although turtles and tortoises are

locally consumed and domestically traded in Laos,

Cambodia, and Vietnam, most are exported to markets

in southern China (Stuart et al., 2000; van Dijk et al.,

2000). Chelonians from Laos and Cambodia are usually

transported to Vietnam, where they join with

Vietnamese turtles on northward routes to China (Stuart

et al., 2000). Because Laos and Cambodia are source

rather than destination or transfer countries, specimens

obtained from markets in Laos or Cambodia usually

originated from that country. However, trade specimens

in Vietnam may have originated from Vietnam, Laos,

Cambodia, or beyond. The volume of this trade is

believed to pose a serious threat to the continued viabil-

ity of wild chelonian populations throughout Southeast

Asia (van Dijk et al., 2000).

Because turtles and tortoises are extensively and

visibly traded in Southeast Asia, most recent distribution

records are based on animals observed in trade rather

than collected from the wild. The geographic origin of

many trade specimens can be difficult if not impossible

to determine, especially those obtained in urban mar-

kets. Uncritical acceptance of these records by workers

has led to inaccurate characterization of species distribu-

tions, with serious biological, conservation, legal, and

regulatory implications. Additional confusion has result-

Vol. 10, p. 130

Asiatic Herpetological Research

2004

ed from the realization that some species of Asian turtles

described during the last two decades were based on

type specimens obtained from Hong Kong animal deal-

ers who provided inaccurate or fabricated locality data,

leaving the geographic origin of many in doubt (Dalton,

2003; Parham et al., 2001). Distribution records that

explicitly state how the turtles were obtained are there-

fore clearly important, given the historical paucity of

information, uncertainties in recent literature, and the

serious conservation threats faced by these taxa.

We here report recent distribution records of chelo-

nians from Laos, Cambodia, and Vietnam that can be

verified with voucher specimens or photographs. These

records were obtained by (1) us during herpetological

surveys conducted from February 1998 through May

2001, (2) other workers in the region between 1993 and

June 2002, and provided to us, or (3) other workers who

deposited specimens at the Field Museum of Natural

History, Chicago, USA since 1993. For each record we

note whether the specimen was collected in the field,

found in abandoned hunting camps, obtained from

hunters or residents in rural villages, or purchased from

markets.

It should be emphasized that our collecting activi-

ties had little if any detrimental impact on populations of

wild chelonians. The number of collected specimens on

which we report is insignificant when compared to the

millions of chelonians annually consumed by the

wildlife markets of southern China (Lau et al., 2000).

Furthermore, the majority of specimens we and others

collected in the field were shells of animals consumed

by rural villagers. Chelonian shells are commonplace

and easily obtained in villages; shells are retained by

hunters as trophies, sold or kept for medicinal purposes,

and used as food containers for domestic animals and

rice scoops. Our collecting activities certainly provided

no stimulus for the additional harvesting of wild chelo-

nians. Finally, we believe that further scientific collect-

ing is warranted in the region, as most species remain

under-represented in museum collections, and taxonom-

ic study can affect conservation priorities (Parham and

Shi, 2001; Stuart and Thorbjamarson, 2003).

Methods and Conventions

Measurements were taken to the nearest 0.1 cm with 80

cm sliding calipers. We use the following abbreviations:

CL = maximum straight carapace length, including

spines or projections (i.e. not necessarily the mid-line);

CW = maximum carapace width, including spines or

projections; PL = maximum plastron length, including

spines or projections; BD = maximum depth of complete

specimen (head and neck extended in trionychid speci-

mens). Measurements were not reported if shell damage

precluded accurate measurement.

Records are presented under each species account in

the following format where applicable: Field Museum of

Natural History (FMNH) or figure number, type of

record, measurements (defined above), locality includ-

ing coordinates if available, approximate elevation and

brief habitat description if field-collected, circumstances

of origin if not field-collected by collector or photogra-

pher, date specimen was collected or photographed, and

name of collector or photographer. In the case of records

obtained from hunters or villages, the name of collector

refers to the person who preserved the specimen or pro-

vided the record to us rather than to the name of the per-

son who actually captured it from the wild. In the same

cases, the date of collection refers to the date the collec-

tor (as previously defined) obtained the specimen or

took the photograph rather than to the date it was

removed from the wild.

GPS coordinates are presented only if the original

collector provided them, and in the same format as orig-

inally provided. Coordinates that we generated for the

purposes of mapping the records are not presented.

Marine turtle records are not mapped.

Species Accounts

Platysternidae

Platysternon megacep/ialum Gray, 1831

[Map 1]

Laos. - Fig. 1, photograph only, Huaphahn Province,

Vieng Tong District, Ban Sa Kok Village, 20° IF N

103° 12' E, captured by resident of Ban Sa Kok, 29 April

1998, B. L. Stuart. FMNH 258749, complete specimen,

CL = 9.3, CW = 7.3, PL = 6.9, BD = 2.6, Bolikhamxay

Province, Khamkeut District, Nape border area, stream

in wet evergreen forest, 19 March 1997, D. Davenport.

Fig. 2 (and Fig. 4 in Stuart and Timmins, 2000), photo-

graph only, Khammouan Province, Nakai District,

Nakai-Nam Theun National Biodiversity Conservation

Area, Ban Xiangthong Village, 17° 54' 05" N 105° 23'

50" E, one of eleven individuals in the possession of a

Vietnamese trader leaving Ban Xiangthong, 17

November 1998, B. L. Stuart. Fig. 3, photograph only,

Xe Kong Province, Dakchung District, Ban Daklan

Village, 15° 21.61' N 107° 01.70' E, captured by resi-

dents of Ban Daklan, D. Showier, December 1997.

Vietnam. - FMNH 252164, complete specimen, CL =

1 5.5, C W — 1 1 .6, PL =12.7, BD = 5.2, Gia-Lai Province,

Ankhe District, Buon Loi Village, 20 km northwest of

Kannack town, Annamite Mountains, 14° 20' N 108° 36'

E, 700-750 m, found in burrow under overhanging

stream bank, 31 March 1995, I. Darevsky and N& L.

Orlov.

2004

Asiatic Herpetological Research

Vol. 10, p. 131

Remarks. - Ziegler (2002) reported the species in local

trade in Ha Tinh Province, Vietnam.

Geoemydidae

Batagur baska (Gray, 1831 “1830-35”)

[Map 2]

Cambodia. - Platt et al. (2003) reviewed the status of B.

baska in Cambodia and reported on a breeding popula-

tion in the Sre Ambel River System of Koh Kong

Province.

Cuora amboinensis (Daudin, 1 802)

[Map 3]

Cambodia. - Fig. 4, photograph only, Battambang

Province, Ek Phnom District, Koh Chivang Commune,

Prek Toal Village on Tonle Sap Lake, 13° 14' 28" N 103°

39' 32" E, captured by residents of Prek Toal, 27 August

1999, B. L. Stuart, J. Smith, and K. Davey. FMNH

259411, broken carapace and plastron, Kandal Province,

Trayo Village, 11° 19’ 02" N 105°09’ 47" E, obtained

from hunter in Trayo, 05 July 2000, S. G. Platt. Fig. 5,

photograph only, two living turtles, CL = 19.3 and PL =

17.5, CL = 20.6 and PL = 18.9, Kampong Thom

Province, Sary Village, 12° 48.48' N 104° 44.19’ E, col-

lected by Sary residents in Tonle Sap, 21 June 2000, S.

G. Platt, Heng Sovannara, and Long Kheng. Fig. 6, pho-

tograph only, CL = 20.4 cm, PL = 18.5, Koh Kong

Province, Sre Ambel Town, in house of wildlife trader,

1 1 ° 07.30’ N; 1 03° 44.73’ E, 27 August 2000, S. G. Platt,

B. L. Stuart, and Vuthy Monyrath. Fig. 7, photograph

only, CL = 11.6, PL = 11.0, Koh Kong Province, Koh

Kong Town near municipal airport, 11° 37.11’ N; 103°

00.98’ E, crossing road in open grassland bordered by

Melaleuca and Rhizophora swamp, 07 February 2001,

S. G. Platt, Heng Sovannara, and Long Kheng.

Laos. - FMNH 255262, complete specimen, CL = 16.7,

CW = 11.7, PL = 15.2, BD = 7.5, Champasak Province,

Mounlapamok District, Dong Khanthung Proposed

National Biodiversity Conservation Area, Ban Khiem

Village, 14° 14’ N 105° 20’ E, captured by residents of

Ban Khiem for food, 24 July 1998, B. L. Stuart.

Vietnam. - Fig. 8, photograph only, Kien Giang

Province, An Minh District, photographed in a reptile

trade shop, 09° 45’ 04" N 104° 59’ 35" E, 31 October

2000, B. L. Stuart.

Cuora galbinifrons Bourret, 1939

[Map 4]

Laos. - FMNH 256544, complete specimen, CL = 16.6,

C W = 12.2, PL = 1 6.2, BD = 8.0, Khammouan Province,

Nakai District, Nakai-Nam Theun National Biodiversity

Conservation Area, 17° 50’ N 105° 35’ E, 900 m, wet

evergreen forest, found under brush in leaf litter on hill-

side 500 m from nearest stream, 13 December 1998, B.

L. Stuart. FMNH 255273, carapace only, CL = 18.1,

CW = 12.9, Khammouan Province, Yommalat District,

Khammouan Limestone (= Phou Hin Poun) National

Biodiversity Conservation Area, Ban That Mouang Khai

Village, 17° 32’ N 105° 04’ E, consumed by residents of

Ban That Mouang Khai, 01 April 1998, B. L. Stuart.

Vietnam. - FMNH 255694, complete specimen, CL =

19.2, CW = 13.0, PL = 18.0, BD = 8.5, Nghe An

Province, Tuong Duong District, Pu Mat Nature

Reserve, 19° 03’ N 104° 37’ E, 600 m, wet evergreen hill

forest, in leaf litter along Khe Mat Stream, 14 September

1998, B. L. Stuart. FMNH 255695, complete specimen,

repatriated to Vietnam before measurements could be

taken, collecting information same as FMNH 255694.

Remarks. - The subspecies C. galbinifrons galbinifrons

Bourret, 1939 is treated here as a full species following

the recommendation of Stuart and Parham (2004).

Ziegler (2002) reported the species in local trade in Ha

Tinh Province, Vietnam, and Fritz et al. (2002) reported

hybrids of C. galbinifrons and C. bourreti in local trade

in Ha Tinh and Quang Binh Provinces, Vietnam.

Cuora mouhotii (Gray, 1862)

[Map 5]

Laos. - FMNH 258880, carapace only, CL = 16.1, CW

= 11.0, Khammouan Province, Boualapha District, Hin

Nam No National Biodiversity Conservation Area, Ban

Tasang Village, eaten by residents of Ban Tasang, 30

December 1995, R. J. Timmins. FMNH 258881 , cara-

pace only, CL= 17.3, CW = 13.0, collecting information

same as FMNH 258880. FMNH 258887, plastron only,

PL = 16.8, Bolikhamxay Province, Nam Kading

National Biodiversity Conservation Area, eaten by vil-

lagers living in Nam Kading, 01 May 1995, R. J.

Timmins.

Remarks. - The species mouhotii was previously placed

in the monotypic genus Pyxidea Gray, 1863, but we allo-

cate it to the genus Cuora following Honda et al. (2002)

and Stuart and Parham (2004). Ziegler (2002) reported

the species in local trade in Ha Tinh Province, Vietnam.

Cyclemys atripons Iverson and McCord, 1997

[Map 6]

Cambodia. - FMNH 259050, complete specimen, CL =

21.4, CW = 16.2, PL = 20.7, BD = 8.4, Mondolkiri

Province, Pichrada District, Phnom Nam Lyr Wildlife

Vol. 10, p. 132

Asiatic Herpetological Research

2004

Sanctuary, near 12° 32' 16" N 107° 32' 00" E, 600-700

m, evergreen gallery forest, found on sand bank at base

of large boulder 1.5 m from swift, shallow stream, 21

June 2000, B. L. Stuart. FMNH 259051, complete spec-

imen, CL = 22.7, CW = 17.0, PL = 21.2, BD = 8.0, Koh

Kong Province, Sre Ambel District, Sre Ambel Town,

11° 07' 20" N 103° 44' 45" E, obtained from turtle trad-

er who reported specimen came from Sophat Village,

downstream from Sre Ambel Town, 27 August 2000, B.

L. Stuart and S. G. Platt. FMNH 259052, complete spec-

imen, CL = 18.0, CW = 15.0, PL =16.7, BD = 6.2, col-

lecting information same as FMNH 259051. FMNH

259412, carapace and incomplete plastron, CL = 19.3,

CW = 15.2, Koh Kong Province, Sre Ambel District,

BoeungTradok Pong Village, 11° 31' 10" N 103° 46' 55"

E, obtained from hunter in Boeung Tradok Pong, 24

August 2000, B. L. Stuart and S. G. Platt. FMNH

259414, plastron only, PL = 16.5, collecting information

same as FMNH 259412. FMNH 259415, plastron only,

PL = 16.2, collecting information same as FMNH

259412. FMNH 259416, plastron only, PL = 14.9, Koh

Kong Province, Sre Ambel District, Chaouethail Pious

Village on Sre Ambel River, 11° 18' 03' N, 103° 44'

56”E, obtained from hunter in Chaouethail Pious, 21

August 2000, B. L. Stuart and S. G. Platt. FMNH

259417, plastron only, PL = 19.2, collecting information

same as FMNH 259416. FMNH 259422, plastron only,

PL = 20.2, Koh Kong Province, Sre Ambel District,

Chay Reap Village, west bank of Sre Ambel River, 11°

29' 10" N 103° 47' 00" E, <10 m, obtained from hunter

in Chay Reap, 23 August 2000, B. L. Stuart and S. G.

Platt. Fig. 9, photograph only, two living animals, CL =

13.7 cm and PL = 13.0 cm, CL = 20.8 cm and PL = 19.6

cm, Koh Kong Province, Kaoh Pao River, 11° 44.46' N;

103° 04.80' E, surrounding hills covered in dense ever-

green forest with some mangrove along shoreline,

obtained from fishermen, taken in crab traps set in river,

10 May 2001, S. G. Platt, Heng Sovannara, and Long

Kheng.

Remarks. - Fritz and Ziegler ( 1 999) reviewed records of

Cyclemys from the region. Species boundaries within

the genus Cyclemys remain uncertain (Fritz and Ziegler,

1999; Guicking et ah, 2002). The specimens we

assigned to C. atripons have plastra that are largely yel-

low with densely pigmented bridges; complete speci-

mens exhibit nearly immaculate chins. These character-

istics are typical of both C. atripons and C. pulchristri-

ata Fritz, Gaulke & Lehr, 1997, two species that were

described almost concurrently in 1997. Cyclemys

atripons and C. pulchristriata have been considered the

same taxon (Iverson in Guicking et ah, 2002). However,

Fritz et ah (2001) concluded that C. atripons has more

ventral neck stripes (7-8 light and 7-9 dark stripes when

counted from one mouth comer to the other) than C. pul-

christriata (5-7 light and 5-7 dark stripes). FMNH

259050 has 8 dark and 7 light ventral neck stripes,

FMNH 259051 has 10 dark and 9 light ventral neck

stripes, but in FMNH 259052 the ventral side of the neck

is nearly immaculate like the chin and completely lacks

striping. These few samples demonstrate that ventral

neck stripes are more variable than stated by Fritz et ah

(2001). In a phylogenetic analysis of a 982 bp fragment

of the mitochondrial cytochrome b gene, Guicking et ah

(2002) recovered two clades in the atripons-pulchristri-

ata complex that differed by up to 4.5% sequence diver-

gence. Samples referred to atripons and pulchristriata

appeared in both clades, but the authors assigned these

names according to whether the sample originated from

Cambodia {atripons) or Vietnam {pulchristriata ), rather

than based on their morphology. The findings of

Guicking et ah (2002) suggest that more than one

species of Cyclemys with mostly yellow plastra, densely

pigmented bridges, and immaculate chins could exist,

but it remains unclear whether the two clades corre-

spond to what have been described as atripons and pul-

christriata. We assign the name C. atripons rather than

C. pulchristriata to our samples because the type locali-

ty of C. atripons is geographically closer to most of our

samples than to that of C. pulchristriata. Clearly, further

studies into the morphological and genetic variation in

Cyclemys are warranted, particularly with samples of

certain provenance.

Cyclemys tcheponensis (Bourret, 1939)

[Map 7]

Laos. - Fig. 10 (and Fig. 7d in Stuart et ah, 2001), pho-

tograph only, Bolikhamxay Province, Thaphabat

District, Phou Khao Khouay National Biodiversity

Conservation Area, near That Xay Waterfall, 1 8° 27' N

103° 10' E, 300 m, dry evergreen forest mixed with bam-

boo, sleeping on bottom of 4 x 4 m pool in forested

stream, 26 June 1998, B. L. Stuart. FMNH 258870,

complete specimen, CL = 9.7, CW = 8.0, PL = 8.7, BD

= 3.6, Bolikhamxay Province, Khamkeut District, pur-

chased in Lac Xao Market, 14 December 1996, D.

Davenport. FMNH 258871, complete specimen, CL =

9.0, CW = 8.1, PL = 8.3, BD = 3.6, collecting informa-

tion same as FMNH 258870. FMNH 258875, complete

specimen, CL = 20.6, CW = 15.2, PL = 20.3, BD = 8.5,

Khammouan Province, Nakai District, Houay Moey

Stream (tributary of Nam Pheo River), Ban Na Meo

Village, dry evergreen forest, 07 March 1997, D.

Davenport and J. Chamberlain. FMNH 255263, com-

plete specimen, CL= 17.1, CW = 13.6, PL= 16.1, BD =

6.5, Khammouan Province, Nakai District, Khammouan

Limestone (= Phou Hin Poun) National Biodiversity

2004

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Vol. 10, p. 133

Conservation Area, 17° 53' N 104° 52' E, 570 m, dry

evergreen lorest mixed with deciduous trees and pine,

caught on streambank by hunter using dog, 26 March

1998, B. L. Stuart and T. Chan-ard.

Remarks. - Species boundaries within the genus

Cycle my s remain uncertain (Fritz and Ziegler, 1999;

Guicking et al., 2002). The specimens we assigned to C.

tcheponensis have dark radiating patterns of the plastra,

pigmented chins, head and neck stripes, and dorsal spot-

ting on the crown of the head, as illustrated by Fritz and

Ziegler (1999) and Fritz et al. (1997). Fritz and Ziegler

(1999) reviewed records of Cyclemys from the region,

and Ziegler (2002) reported the species in local trade in

Ha Tinh Province, Vietnam.

Cyclemys sp.

[Map 8]

Cambodia. - FMNH 259418, carapace only, CL = 19.5,

CW = 14.7, Kampong Speu Province, Koh Kong

Samling Logging Concession, 11° 24' 15" N 103° 49'

47" E, 200 m, recovered from hunter’s camp, mixed

deciduous forest and grassland, 15 February 2000, J.

Walston. FMNH 259419, carapace only, CL = 22.1, CW

= 16.1, collecting information same as FMNH 259418.

FMNH 259420, carapace only, CL = 19.1, CW = 15.9,

collecting information same as FMNH 259418. FMNH

259421, plastron only, PL = 21.2, collecting information

same as FMNH 259418. FMNH 259423, plastron only,

PL = 21.0, Koh Kong Province, Sre Ambel District,

Chay Reap Village, west bank of Prek Sre Ambel River,

11° 29' 10" N 103° 47' 00" E, <10 m, obtained from

hunter in Chay Reap, 23 August 2000, B. L. Stuart and

S. G. Platt.

Laos. - FMNH 258893, carapace only, CL = 21.8, CW

= 16.6, Champasak Province, Pakxong District, Ban

Latsasin Village, near Xe Nam Noy River, 800 m, eaten

by residents of Ban Latsasin Village, 02 April 1995, T.

D. Evans.

Remarks. - The condition of these shell fragments pre-

cludes identifying them to species. They are not neces-

sarily a species different from atripons or tcheponensis.

Heosemys grand is (Gray, 1860)

[Map 9]

Cambodia. - FMNH 259409, carapace only, CL = 30.5,

CW = 22.6, Phnom Penh, Oreussay Market, purchased

in market, 17 May 1999, S. G. Platt. FMNH 259405,

plastron only, PL = 26.5, Koh Kong Province, Sre

Ambel District, Boeung Tradok Pong Village, 11° 31'

10' N 103° 46' 55" E, obtained from hunter in Boeung

Tradok Pong, 24 August 2000, B. L. Stuart and S. G.

Platt. FMNH 259406, plastron only, PL = 20.8, Koh

Kong Province, Sre Ambel District, Chaouethail Pious

Village on Sre Ambel River, 11° 18' 03" N 103° 44' 56"

E, obtained from hunter in Chaouethail Pious, 21 August

2000, B. L. Stuart and S. G. Platt. Fig. 11, photograph

only, CL = 3 1 .8, PL = 28.6, Koh Kong Province, Thmor

Andart Village along Stoeng Metoek River, 11° 49.23'

N, 102° 53.62' E, captured by residents of Thmor

Andart, 10 May 2001, S. G. Platt, Heng Sovannara, and

Long Kheng. FMNH 259407, plastron only, PL = 19.4,

collecting information same as FMNH 259406.

Laos. - FMNH 255271, carapace only, CL = 23.6, CW

= 18.3, Khammouan Province, Thakhek District,

Khammouan Limestone (= Phou Hin Poun) National

Biodiversity Conservation Area, Ban Na Village, 1 7° 33'

N, 104° 52' E, eaten by residents of Ban Na, 02 April

1998, B. L. Stuart. FMNH 258885, plastron only, PL =

27.0, Khammouan Province, Khammouan Limestone (=

Phou Hin Poun) National Biodiversity Conservation

Area, Ban Namphick Village, eaten by residents of Ban

Namphick, 22 May 1994, R. J. Timmins. FMNH

258894, carapace only, CL = 36.3, CW = 24.7, collect-

ing information same as FMNH 258885. FMNH

258889, plastron only, PL = 13.9, Laos, Khammouan

Province, Khammouan Limestone (= Phou Hin Poun)

National Biodiversity Conservation Area, Ban

Chocksavang Village, eaten by residents of Ban

Chocksavang, 22 May 1994, R. J. Timmins. FMNH

258882, carapace only, CL = 23.2, CW = 19.1,

Savannakhet Province, Thaphangthong District, Xe

Bang Nouan National Biodiversity Conservation Area.

Ban Houay Meun Village, eaten by residents of Ban

Houay, 20 June 1994, R. J. Timmins. FMNH 258883.

carapace (broken) and plastron only, PL = 36.6. collect-

ing information same as FMNH 258882 except collect-

ed 19 June 1994. FMNH 258877, carapace only, CL =

34.1, CW = 24.2, Salavan Province, Toumlan District.

Xe Bang Nouan National Biodiversity Conservation

Area, Ban Nalan Village, eaten by residents of Ban

Nalan, 15 June 1994, R. .1. Timmins. FMNH 258878.

intact shell only, CL = 36.8. CW = 25.8, PL = 35.3, BD

= 14.7, Salavan Province, Xe Bang Nouan National

Biodiversity Conservation Area, Ban Konglur Village,

eaten by residents of Ban Konglur, 10 June 1994, R. J.

Timmins. FMNH 258891, carapace only, CL = 17.3,

CW = 15.1, Salavan Province, Xe Bang Nouan National

Biodiversity Conservation Area, Ban Nasompeng

Village, eaten by residents of Ban Nasompeng, 09 June

1994, R. J. Timmins. FMNH 258890, carapace (broken)

only, CL = 19.4, Champasak Province, Pathoumphon

District, Xe Pian National Biodiversity Conservation

Area, Xe Pian River upstream from Ban Phonsaat

Village, 100 m, discarded in camp along Xe Pian River

2004

Figures 1-15. See text for locality details and circumstances of the record. 1. Platysternon megacephalum Huaphahn

Province, Laos (photo B. L. Stuart); 2. Platysternon megacephalum Khammouan Province, Laos (photo B. L. Stuart)

3. Platysternon megacephalum Xe Kong Province, Laos (photo D. Showier); 4. Cuora amboinensis Battambang

Province, Cambodia (photo B. L. Stuart); 5. Cuora amboinensis Kampong Thom Province, Cambodia (photo S G

Platt); 6. Cuora amboinensis Koh Kong Province, Cambodia (photo S. G. Platt); 7. Cuora amboinensis Koh Konq

Province, Cambodia (photo S. G. Platt). 8. Cuora amboinensis Kien Giang Province, Vietnam (photo B L Stuart)' 9

Cyclemys atripons Koh Kong Province, Cambodia (photo S. G. Platt); 10. Cyclemys tcheponensis Bolikhamxav

Province, Laos (photo B. L. Stuart); 11. Heosemys grandis Koh Kong Province, Cambodia (photo S G Platt) 12

Hieremys annandalii Battambang Province, Cambodia (photo B. L. Stuart); 13. Hieremys annandalii Siem Reap

Province, Cambodia (photo S. G. Platt); 14. Hieremys annandalii Kampong Thom Province, Cambodia (photo S G

Platt); 15. Malayemys subtrijuga Battambang Province, Cambodia (photo B. L. Stuart).

2004

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Vol. 10, p. 135

Figures 16-27. See text for locality details and circumstances of the record. 16. Malayemys subtrijuga Kampong Thom

Province, Cambodia (photo S. G. Platt); 17. Malayemys subtrijuga Kandal Province, Cambodia (photo S. G. Platt); 18.

Malayemys subtrijuga Vientiane, Laos (photo W. G. Robichaud). 19. Manouria impressa Koh Kong Province,

Cambodia (photo S. G. Platt). 20. Manouria impressa Ratanakiri Province, Cambodia (photo Suon Phalla/TRAFFIC).

21. Manouria impressa Xe Kong Province, Laos (photo B. L. Stuart). 22. Chelonia mydas Kampong Speu Province,

Cambodia (photo B. L. Stuart). 23. Eretmochelys imbricata Sihanoukville Province, Cambodia (photo S. G. Platt). 24.

Dermochelys coriacea Gulf of Thailand, near Sihanoukville, Cambodia (photo Vanna Nhem). 25. Amyda cartilaginea

Koh Kong Province, Cambodia (photo S. G. Platt). 26. Amyda cartilaginea Khammouan Province, Laos (photo B. L.

Stuart). 27. Pelochelys cantorii Kratie Province, Cambodia (photo D. Gambade).

after being eaten by hunters. May 1995, T. D. Evans.

FMNH 255266, complete specimen, CL = 7.5, CW

6.4, PL = 6.2, BD = 2.5, Champasak Province,

Mounlapamok District, Dong Khanthung Proposed

National Biodiversity Conservation Area, 14° 07' N 105°

29' E, 60 m, grassland with dry dipterocaip and ever-

green forest along Xe Lepou River, found in mud at bot-

tom of flooded marsh, water depth about 15 cm, 1 1 July

1998, B. L. Stuart. FMNH 255272, carapace only, CL =

28.6, CW = 22.2, Champasak Province, Mounlapamok

District, Dong Khanthung Proposed National

Biodiversity Conservation Area, Ban Thahin Village, on

Xe Lepou River, 14° 08' N 105° 35' E. 60 m, eaten by

residents of Ban Thahin, 17 July 1998. B. L. Stuart.

Vol. 10, p.

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20 N

15 N

10 N

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m

Maps 1-17 of records given in the text: shaded circles represent records collected in the field; half-shaded circles rep-

resent records obtained from hunters, abandoned hunting camps, or villages; unshaded circles represent records pur-

chased from markets.

Hieremys annandalii (Boulenger, 1903)

[Map 10]

Cambodia. - FMNH 259408, carapace only, CL = 32.3,

CW = 24.8, Phnom Penh, Oreussay Market, purchased

in market, 17 May 1999, S. G. Platt. FMNH 258876,

carapace and plastron, CL = 40.3, CW = 26.9, PL = 35.5,

Battambang Province, Ek Phnom District, Koh Chivang

Commune, Prek Toal Village on Tonle Sap Lake, 13° 14'

28" N 103° 39' 32" E, <10 m, eaten by residents of Prek

Toal who captured it from nearby flooded forest, 27

August 1999, B. L. Stuart, J. Smith, K. Davey. Fig. 12,

photograph only, same collecting information as FMNH

258876 except not yet eaten. FMNH 259398, carapace

only, CL = 37.4, CW = 26.7, Siem Reap Province, Siem

Reap District, Choeng Khneas Port on Tonle Sap Lake,

found in fisherman’s house, 28 June 2000, B. L. Stuart

and S. G. Platt. Fig. 13, photograph only, two living ani-

mals, CL = 42. 1 and PL = 34.7, CL = 33.4 and PL = 28.2,

Siem Reap Province, Siem Reap District, Choeng

Khneas Village, 13° 15.18' N; 103° 49.37' E, collected

by residents of Choeng Khneas from Tonle Sap, 4

October 2000, S. G. Platt, Heng Sovannara, Long

Kheng, and Vuthy Monyrath. Fig. 14, photograph only,

CL = 37.2, PL = 28.4, Kampong Thom Province,

Kampong Thom Town, 12° 42.69' N; 104° 53.31' E,

photographed in market, 21 June 2000, S. G. Platt, Heng

Sovannara, and Long Kheng.

Laos. - FMNH 258879, carapace and plastron only, CL

= 33.3, CW = 23.0, PL = 31.3, Attapu Province,

Sanamsai District, Xe Pian River Basin, Ban Chanto

Village, 100-150 m, eaten by residents of Ban Chanto,

21 April 1995, T. D. Evans. FMNH 259399, carapace

only, CL — 29.7, CW — 22.0, Attapu Province, Sanamxai

2004

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Vol. 10, p. 145

District, Ban Mai Village, 14° 42' 30" E 106° 29' 50" E,

obtained trom hunter in Ban Mai, 18 September 2000,

B. L. Stuart and S. G. Platt.

Vietnam. - FMNH 259074, complete specimen, CL =

12.4, CW = 10.8, PL = 11.5, BD = 5.6, Kien Giang

Province, An Minh District, Dong Hoa Town, 09° 45'

25" N 105u 00' 03" E, <10m, purchased from a reptile

trade shop, 10 November 2000, B. L. Stuart.

Malayemys suhtrijuga (Schlegel and Muller, 1844)

[Map 11]

Cambodia. - FMNH 259404, carapace only, CL= 19.2,

CW = 14.1, Phnom Penh, purchased in market, 07 July

2000, S. G. Platt. FMNH 259403, carapace only, CL =

21.5, CW = 16.9, Siem Reap Province, Siem Reap

District, Siem Reap Town, purchased from turtle restau-

rant, 11 December 1999, S. G. Platt. Fig. 15, photograph

only, Battambang Province, Ek Phnom District, Koh

Chivang Commune, Prek Toal Village on Tonle Sap

Lake, 13° 14' 28" N 103° 39' 32" E, captured by resi-

dents of Prek Toal, 27 August 1999, B. L. Stuart, J.

Smith, K. Davey. FMNH 259402, plastron only, PL =

17.8, collecting information same as FMNH 259403.

FMNH 259401, carapace (broken) and plastron, CL =

23.2, PL = 20.0, Kampong Thom Province, Kampong

Thom Town, obtained from restaurant, 22 June 2000, S.

G. Platt. Fig. 16, photograph only, CL = 21.3, PL = 17.5,

Kampong Thom Province, Sary Village, 12° 48.48' N

104° 44.19' E, collected by residents of Sary in Tonle

Sap, 21 June 2000, S. G. Platt, Heng Sovannara, and

Long Kheng. Fig. 17, photograph only, CL = 19.8, PL =

16.6, Kandal Province, Bassac Marshes, Prasat Village,

11° 17.72' N, 105° 08.61' E, captured by residents of

Prasat, 5 July 2000, S. G. Platt, Heng Sovannara, and

Long Kheng. FMNH 259400, plastron only, PL = 12.6,

Koh Kong Province, Sre Ambel District, Chay Reap

Village, west bank of Sre Ambel River, 11° 29' 10" N

103° 47' 00" E, <10 m, obtained from hunter in Chay

Reap, 23° August 2000, B. L. Stuart and S. G. Platt.

Laos. - Fig. 18, photograph only, Vientiane

Municipality, Vientiane, crossing road near culvert, May

1999, W. G. Robichaud. FMNH 258868, complete spec-

imen, CL = 8.4, CW = 6.9, PL = 7.3, BD = 3.6, Vientiane

Municipality, Vientiane, purchased in That Luang Fresh

Food Market, 27 February 2000, B. L. Stuart. FMNH

255269, carapace only, CL = 15.9, CW = 12.9,

Khammouan Province, Yommalat District, Khammouan

Limestone (= Phou Hin Poun) National Biodiversity

Conservation Area, Ban Vieng Village, 17° 20' N, 104°

57' E, eaten by residents of Ban Vieng, 30 March 1998,

B. L. Stuart. FMNH 258888, plastron only, PL = 12.8,

Khammouan Province, Khammouan Limestone (= Phou

Hin Poun) National Biodiversity Conservation Area,

Ban Chocksavang Village, eaten by residents of Ban

Chocksavang, 22 May 1994, R. J. Timmins. FMNH

259653 plastron (broken) only, collecting information

same as FMNH 258888. FMNH 259654, plastron only,

PL = 12.5, collecting information same as FMNH

258888. FMNH 255268, intact shell, CL = 10.9, CW =

8.8, PL = 9.2, BD = 4.8, Champasak Province,

Mounlapamok District, Dong Khanthung Proposed

National Biodiversity Conservation Area, Ban Thahin

Village, on Xe Lepou River, 14° 08' N 105° 35' E, 60 m,

eaten by residents of Ban Thahin, 17 July 1998, B. L.

Stuart. FMNH 255267, complete specimen, CL = 10.9,

CW = 8.4, PL = 9.3, BD = 4.7, Champasak Province,

Mounlapamok District, Dong Khanthung Proposed

National Biodiversity Conservation Area, Ban Tap Seng

Village, 14° 15' N 105° 41' E, mixed deciduous forest,

captured by resident of Ban Tap Seng for food, 25 July

1998, B. L. Stuart.

Vietnam. - FMNH 259075, complete specimen, CL =

5.3, CW = 4.3, PL = 4.4, BD = 2.7, Kien Giang

Province, Vinh Thuang District, U Minh Thuong Nature

Reserve, 09° 32' 40" N 105° 05' 11" E, <10m, flooded

grassland and agricultural fields, caught in fishing net

set in canal, 02 November 2000, B. L. Stuart. FMNH

259394, complete specimen, CL = 4.8, CW = 3.8, PL =

3.9, BD = 2.4, Kien Giang Province, An Minh District,

U Minh Thuong Nature Reserve, 09° 37' 29" N 105° 07'

59" E, <10m, flooded grassland and agricultural fields,

taken in fishing net, 16 November 2000, B. L. Stuart.

Sacalia quadriocellata (Siebenrock, 1903)

[Map 12]

Laos. - FMNH 255270, carapace only, CL = 13.8, CW

= 10.6, Huaphahn Province, Vieng Tong District, Nam

Et National Biodiversity Conservation Area, Nam Peun

River, 20° 17’ N 103° 25' E, 985 m, found in hunter’s

camp, 01 April 1998, P. Davidson. FMNH 256542,

complete specimen, CL = 14.2, CW = 10.3, PL =12.5,

BD = 4.5, Khammouan Province, Nakai District, Nakai-

Nam Theun National Biodiversity Conservation Area,

Annamite Mountains, 17° 50' N 105° 35' E, 600 m, wet

evergreen forest along Houay Dreng Stream, found 1 m

deep in pool with sandy substrate, 01 December 1999,

B. L. Stuart. FMNH 256543, complete specimen, CL =

7.2, CW = 6.7, PL = 5.9, BD = 2.8, Khammouan

Province, Nakai District, Nakai-Nam Theun National

Biodiversity Conservation Area, Annamite Mountains,

17° 56' N 105° 31' E, 600 m, Houay Maka-Noi Stream

near Ban Maka Village, collected by resident of Ban

Maka, 15 November 1999, B. L. Stuart.

Remarks. - Ziegler (2002) field-collected and reported

the species in local trade in Ha Tinh Province, Vietnam.

Vol. 10, p. 146

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Siebenrockiella crass icollis (Gray, 1831)

[Map 13]

Cambodia. - FMNH 259054, complete specimen, CL =

14.3, CW = 10.5, PL = 11.7, BD = 5.8, KhampongThom

Province, Khampong Thom Town, 12° 42' N 104° 53' E,

purchased from turtle trader in Khampong Thom Town,

21 June 2000, S. G. Platt. FMNH 259053, whole speci-

men, CL = 15.9, CW - 12.0, PL =13.7, BD = 6.8, Koh

Kong Province, Sre Ambel District, Chay Reap Village,

west bank of Sre Ambel River, 11° 29' 10" N 103° 47'

00" E, <10 m, captured by residents of Chay Reap, 24

August 2000, B. L. Stuart and S. G. Platt. FMNH

259396, intact shell, CL = 16.4, CW = 12.1, PL = 13.7,

BD = 6.6, Koh Kong Province, Sre Ambel District, Chay

Reap Village, west bank of Sre Ambel River, 1 1° 29' 10"

N, 103° 47' 00" E, <10 m, obtained from hunter in Chay

Reap, 24 August 2000, B. L. Stuart and S. G. Platt.

FMNH 259397, plastron only, PL = 16.1, Koh Kong

Province, Sre Ambel District, Kohriem Village on Sre

Ambel River, obtained from hunter in Kohriem, 27

August 2000, B. L. Stuart and S. G. Platt. FMNH

259055, complete specimen, CL = 16.2, CW = 11.5, PL

= 12.8, BD = 5.9, Koh Kong Province, Sre Ambel

District, Prek Kroch River (tributary of Sre Ambel

River), 11° 06' 20" N, 103° 39’ 35" E, <10 m, flooded

paddy at edge of mangrove and Melaleuca forest, cap-

tured by fisherman in bamboo fish trap set at that loca-

tion, 27 August 2000, B. L. Stuart and S. G. Platt.

Remarks. - FMNH 259053 has a pale streak extending

from the ear to the lower jaw, but the heads of FMNH

259054-55 are entirely dark, with no pale markings.

Testudinidae

Indotestudo elongata { Blyth, 1853)

[Map 14]

Cambodia: FMNH 262316, carapace only, CL = 14.7,

CW = 10.0, Mondolkiri Province, Keo S’Marr District,

Samling Logging Concession, 200 m, mixed deciduous

forest and grassland, found in hunter’s camp, 13 May

2000, J. Walston. FMNH 262315, plastron only, PL =

19.8, Koh Kong Province, Sre Ambel District, Chay

Reap Village, west bank of Sre Ambel River, 1 1° 29' 10"

N, 103° 47' 00" E, <10 m, obtained from hunter in Chay

Reap, 23 August 2000, B. L. Stuart and S. G. Platt.

TC001 (held in the Field Museum of Natural History,

Division of Amphibians & Reptiles), blood sample only,

collecting information same as FMNH 262315, obtained

from hunter in Chay Reap and released after taking

blood sample, 23 August 2000, B. L. Stuart and S. G.

Platt. FMNH 262312, plastron only, PL = 18.2, collect-

ing information same as FMNH 262315. FMNH

262307, carapace only, CL = 25.6, CW = 15.1, collect-

ing information same as FMNH 262315. FMNH

262297, carapace only, CL = 24.7, CW = 14.6, Koh

Kong Province, Sre Ambel District, Boeung Tradok

Pong Village, 11° 31' 10" N, 103° 46' 55" E, obtained

from hunter in Boeung Tradok Pong, 24 August 2000, B.

L. Stuart and S. G. Platt. FMNH 262313, plastron only,

PL = 19.4, collecting information same as FMNH

262297. FMNH 262314, plastron only, PL = 18.2, col-

lecting information same as FMNH 262297. FMNH

262302, carapace and plastron, CL = 19.5, CW = 13.0,

PL = 16.5, Koh Kong Province, Sre Ambel District,

Kohriem Village on Sre Ambel River, obtained from

hunter in Kohriem, 27 August 2000, B. L. Stuart and S.

G. Platt. FMNH 262311, plastron only, PL =15.4, Koh

Kong Province, Sre Ambel District, Chaouethail Pious

Village on Sre Ambel River, 11° 18' 03" N, 103° 44' 56"

E, obtained from hunter in Chaouethail Pious, 21 August

2000, B. L. Stuart and S. G. Platt. FMNH 262310, plas-

tron only, PL = 14.8, collecting information same as

FMNH 262311.

Laos. - FMNH 262294, carapace only, CL = 22.8, CW

= 14.0, Khammouan Province, Boualapha District, Hin

Nam No National Biodiversity Conservation Area, Ban

Tasang Village, eaten by residents of Ban Tasang, 30

December 1995, R. J. Timmins. FMNH 259056, com-

plete specimen, CL = 17.0, CW = 10.9, PL = 14.8, BD =

7.4, Khammouan Province, Nakai District, Khammouan

Limestone (= Phou Hin Poun) National Biodiversity

Conservation Area, Ban Na Bon Village, limestone karst

with dry evergreen/mixed deciduous forest, 17° 54' N

104° 51' E, captured by residents of Ban Na Bon for

food, 22 March 1998, B. L. Stuart and T. Chan-ard.

FMNH 262304, carapace only, CL = 17.9, CW = 12.4,

Khammouan Province, Thakhek District, Khammouan

Limestone (= Phou Hin Poun) National Biodiversity

Conservation Area, Ban Na Village, 17° 33' N, 104° 52'

E, eaten by residents of Ban Na, 02 April 1998, B. L.

Stuart. FMNH 262299, carapace only, CL = 24.2, CW =

15.4, Khammouan Province, Khammouan Limestone (=

Phou Hin Poun) National Biodiversity Conservation

Area, Ban Namphick Village, eaten by residents of Ban

Namphick, 22 May 1994, R. J. Timmins. FMNH

262295, carapace only, CL = 25.2, CW = 15.1, collect-

ing information same as FMNH 262299. FMNH

262296, carapace only, CL = 26.9, CW = 16.7, Salavan

Province, Xe Bang Nouan National Biodiversity

Conservation Area, Ban Konglur Village, eaten by resi-

dents of Ban Konglur, 10 June 1994, R. J. Timmins.

FMNH 262301, carapace only, CL = 29.0, CW = 18.1.

Attapu Province, Xe Nam Noy River, Ban Mun Houa

Muang Village, 300 m, eaten by residents of Ban Mun

Houa Muang, April 1995, D. Showier. FMNH 262303.

2004

Asiatic Herpetological Research

Vol. 10, p. 147

Figure 28. See text for locality details and circumstances

of the record. Pelochelys cantorii Champasak Province,

Laos (photo I. G. Baird).

carapace only, CL = 23.3, CW = 14.4, Attapu Province,

Sanamsai District, Xe Kong River, near Ban Sompoy

Village and Cambodian border, 90 m, discarded cara-

pace found in camp after being eaten by hunters, May

1995, T. D. Evans. FMNH 262298, carapace only, CL =

22.3, CW = 14.3, Champasak Province, Pathoumphon

District, Xe Pian National Biodiversity Conservation

Area, Xe Pian River upstream from Ban Phonsaat

Village, 100 m, discarded carapace found in camp along

Xe Pian River after being eaten by hunters. May 1995,

T. D. Evans. FMNH 262308, carapace only, CL = 17.7,

CW = 11.4, Champasak Province, Mounlapamok

District, Dong Khanthung Proposed National

Biodiversity Conservation Area, found in hunter’s camp

near Nong Sathevada Wetland, 14° 13' N 105° 36' E, 100

m, 04 March 1998, C. Francis. FMNH 262306, carapace

only, CL = 18.9, CW = 12.0, Champasak Province,

Mounlapamok District, Dong Khanthung Proposed

National Biodiversity Conservation Area, Ban Baw

Village, 14° 14'N, 105° 27' E, eaten by residents of Ban

Baw, 18 July 1998, B. L. Stuart. FMNH 262305, cara-

pace only, CL = 26.6, CW = 15.9, Champasak Province,

Mounlapamok District, Dong Khanthung Proposed

National Biodiversity Conservation Area, Ban Khiem

Village, 14° 14' N, 105° 20' E, eaten by residents of Ban

Khiem, 24 July 1998, B. L. Stuart. FMNH 262300,

carapace only, CL = 24.9, CW = 14.7, Champasak

Province, Mounlapamok District, Dong Khanthung

Proposed National Biodiversity Conservation Area, Ban

Kadian Village, 14° 26' N, 105° 42' E, eaten by residents

of Ban Kadian, 29 July 1998, B. L. Stuart.

Remarks. - Ziegler (2002) reported the species in local

trade in Ha Tinh Province, Vietnam.

Man our id impress a (Gunther, 1882)

[Map 15]

Cambodia. - Fig. 19, photograph only of two intact

shells, CL = 26.6 and PL = 23.8, CL = 22.8 and PL =

19.9, Koh Kong Province, Thmor Andart Village, along

Stoeng Metoek River, 1 1° 49.23' N, 102° 53.62' E, col-

lected by residents of Thmor Andart, 1 0 May 200 1 , S. G.

Platt, Heng Sovannara, and Long Kheng. Fig. 20, pho-

tograph only, Ratanakiri Province, Oyadao District,

found in house of Vietnamese wildlife trader on

Cambodian side of Oyadao border checkpoint, Suon

Phalla/TRAFFIC, 16 June 2002.

Laos. - FMNH 262321, carapace only, CL = 23.7, CW

= 17.3, Phongsaly Province, Phongsaly District, Phou

Dendin National Biodiversity Conservation Area, Ban

Sopkang Village, 22° 05'51"N, 102° 15' 02" E, eaten by

residents of Ban Sopkang, 17 October 1999, B. L. Stuart

and H. F. Heatwole. FMNH 262317, carapace only, CL

= 27.7, CW = 19.9, collecting information same as

FMNH 262321. FMNH 262324, carapace only, CL =

28.6, CW = 20.2, Huaphahn Province, Vieng Tong

District, Phou Louey National Biodiversity

Conservation Area, Ban Sa Kok Village, 20° 11" N, 103°

12" E, eaten by residents of Ban Sa Kok, 30 April 1998.

B. L. Stuart. FMNH 262319, carapace only, CL = 27.0.

CW = 19.9, collecting information same as FMNH

262324. FMNH 262323, carapace and plastron, CL =

20.8, CW= 16.3, PL= 19.4, collecting information same

as FMNH 26234. FMNH 262318, carapace only, CL =

25.0, CW = 19.2, Huaphahn Province, Vieng Tong

District, Phou Louey National Biodiversity

Conservation Area, Ban Phone Xong Village, eaten by

residents of Ban Phone Xong, 04 May 1998. D. Showier.

FMNH 262322, plastron only, PL = 21.1, Khammouan

Province, Hin Nam No National Biodiversity

Conservation Area, Ban Katok Village, eaten by resi-

dents of Ban Katok, 12 January 1996, R. J. Timmins.

Fig. 21, photograph only, Xe Kong Province, Kaleum

District, Ban Talouy-Ngai Village. 15° 59' 50" N, 106°

57' 22" E, captured by residents of Ban Talouy-Ngai, 27

June 1999, B. L. Stuart. FMNH 262320. carapace only,

CL = 27.6, CW = 20.6, Attapu Province, Xe Nam Noy

River, Ban Taot Village, 800 m, eaten by residents of

Ban Taot, April 1995, D. Showier.

Remarks. - Lehr and Holloway (2000) obtained a single

carapace of M. impressa from a hunter in Ratanakiri

Province, Cambodia, who claimed to have captured the

turtle in mountains north of Siem Pang, Stung Trens

Province.

Vol. 10, p. 148

Asiatic Herpeto/ogical Research

2004

Cheloniidae

Clielonia my das (Linnaeus, 1758)

Cambodia. - Fig. 22, photograph only, Kampong Speu

Province, Phnom Srouch District, Srei Khlong Market,

07 June 2000, B. L. Stuart.

Eretmoclielys imbricata (Linnaeus, 1766)

Cambodia. - Fig. 23, photograph only, Sihanoukville

Province, Mitta Pheap District, Koh Rong Island, Bagnu

Village, obtained from fisherman in Bagnu, 01 January

2000, F. Goes.

Dermochelyidae

Dermochelys coriacea (Vandelli, 1761)

Cambodia. - Fig. 24, photograph only. Stuart et al.

(2002) discussed in detail this record from offshore of

the southern point of Koh Sra Mauch Island in the Gulf

of Thailand, near Sihanoukville.

Trionychidae

Amy da cartilaginea (Boddaert, 1770)

[Map 16]

Cambodia. - Fig. 25, photograph only, CL = 7.4, Koh

Kong Province, Koh Kong Knong Village, 11° 25.97' N;

103° 09.77' E, captured locally by villager in Stoeng

Kep River, II May 2001, S. G. Platt, Heng Sovannara,

and Long Kheng.

Laos. - FMNH 258869, complete specimen, CL = 7.4,

CW = 6.8, PL = 2.1, BD = 5.7, Vientiane Municipality,

Vientiane, purchased in That Luang Fresh Food Market,

27 February 2000, B. L. Stuart. FMNH 258874, com-

plete specimen, CL = 29.5, CW = 26.0, PL = 20.6, BD =

9.5, Bolikhamxay Province, Northern Extension

Proposed National Biodiversity Conservation Area, Ban

Chom-Tong Village, near Nam Mouan River, captured

by hunters in Nam Mouan River, 18 March 1995, R. J.

Timmins. Fig. 26, photograph only, Khammouan

Province, Nakai District, Nakai-Nam Theun National

Biodiversity Conservation Area, Ban Kao-Oy Village,

17° 43' 39" N 105° 20' 05" E, captured by resident of

Ban Kao-Oy, 03 November 1998, B. L. Stuart. FMNH

255264, complete specimen, CL = 1 8.2, C W = 1 6.4, PL

= 13.8, BD = 4.5, Khammouan Province, Thakhek

District, Khammouan Limestone (= Phou Hin Poun)

National Biodiversity Conservation Area, 17° 33' N,

104° 52' E, obtained from villager who captured it while

fishing, 01 April 1998, B. L. Stuart. FMNH 255265,

complete specimen, CL - 1 8.7, CW 16.7, PL 15.2,

BD = 4.9, Khammouan Province, Nakai District,

Khammouan Limestone (= Phou Hin Poun) National

Biodiversity Conservation Area, 17° 54' N, 104° 51' E,

obtained from villager who caught it in the Nam Thon

River, 28 March 1998, B. L. Stuart.

Vietnam. - FMNH 252163, whole specimen, CL= 12.5,

CW = 10.7, PL = 10.4, BD = 3.8, Gia-Lai Province,

Ankhe District, Buon Loi Village, 20 km northwest of

Kannack Town, Annamite Mountains, 14L 20' N, 108°

36' E, 700-750 m, Daklest River in the village, 07 May

1995, I. Darevsky and N. L. Orlov.

Remarks. - Farkas and Ziegler (2002) reviewed records

of A. cartilaginea from Vietnam, Laos, and Cambodia.

Peloclielys cantor ii Gray, 1 864

[Map 17]

Cambodia. - Fig. 27, photograph only, Kratie Province,

Kratie District, Kratie Town, purchased from fisherman

in a Kratie market and released in the Mekong River

after being photographed, September 2000, D.

Gambade.

Laos. - Fig. 28, photograph only, Champasak Province,

Khong District, Ban Hang Khone Village, captured by

residents of Ban Hang Khone in the Mekong River, I. G.

Baird.

Acknowledgments

We thank Ian Baird, James Chamberlain, Ilya Darevsky,

David Davenport, Peter Davidson, Thomas Evans,

Charles Francis, Heng Sovannara, Long Kheng, Denis

Gambade, Troy Hansel, Frederic Goes, Nikolai Orlov,

William Robichaud, Sergei Ryabov, Shi Haitao, David

Showier, Suon Phalla/TRAFFIC, and Robert Timmins

for providing us their specimens or photographs. We

thank An Dara, Bui Huu Manh, Tanya Chan-ard,

Benjamin Hayes, Harold Heatwole, Heng Sovannara,

Khamkoun Khounboline, Long Kheng, Nguyen Van

Cuong, Augustus McCrae, William Robichaud, Philip

Round, Suon Phalla, Bee Thaovanseng, and Vuthy

Monyrath for assistance with collecting specimens in the

field. The opportunity for BLS to work in Laos was

made possible by the Wildlife Conservation Society /

Division of Forest Resource Conservation Cooperative

Program, and in Vietnam by Fauna & Flora

International, CARE International in Vietnam, and the

staff of Pu Mat and U Minh Thuong Nature Reserves

The opportunity for BLS and SGP to work in Cambodia

was made possible by the Wildlife Conservation Society

/Ministry of Agriculture, Forestry and Fisheries/

2004

Asiatic Herpetological Research

Vol. 10, p. 149

Ministry ot Environment Collaborative Program.

Financial support was provided by the National

Geographic Society (Grant no. 6247-98 with Harold

Heatwole), the Wildlife Conservation Society, and The

John D. and Catherine T. MacArthur Foundation. Harold

Voris, Alan Resetar, and Jamie Fadonski facilitated

examining specimens at the Field Museum of Natural

History. Sean Bober constructed the maps. Two anony-

mous reviewers improved the manuscript.

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2004

Asiatic Herpetological Research

Vol. 10, pp. 151-160

Studies on Pakistan Lizards: Cyrtopodion stoliczkai (Steindachner, 1867)

(Gekkonidae: Gekkoninae)

Kurt Auffenberg1’*, Kenneth L. Krysko2, and Walter Auffenberg1

1 Florida Museum of Natural History, Powell Hall,

P. O. Box 112710, University of Florida, Gainesville, FL 32611 USA

* E-mail: kauffe@flmnh.ufl.edu

2 Florida Museum of Natural History, Division of Herpetology,

P. O. Box 117800, University of Florida, Gainesville, FL 32611 USA

V 1928-2004 )

Abstract. - Cyrtopodion stoliczkai (Steindachner, 1867) is diagnosed based on the examination of 44 morphological

characters in a series of 25 specimens collected near Skardu, Federally Administered Northern Areas (FANA),

Pakistan. Observations on geographic distribution, habitat, and reproduction are provided. The questionable taxo-

nomic status of Gymnodactylus yarkandensis Anderson, 1872 is discussed. Alsophylax {Altiphylax) boehmei

Szczerbak, 1991 is regarded as a junior synonym of C. stoliczkai.

Key words. - Cyrtopodion stoliczkai , Cyrtopodion yarkandensis, Alsophylax (Altiphylax) boehmei, gecko, lizard, tax-

onomy, Pakistan.

Introduction

The diverse gecko fauna of Pakistan is poorly under-

stood. Particularly problematic are the angular-toed or

thin-toed geckos variously assigned to Cyrtodactylus,

Cyrtopodion, and Tenuidactylus. Much of the taxonom-

ic confusion stems from a general dearth of adequate

material. Large series of specimens from which to iden-

tify variation in important taxonomic characters are

lacking in most cases. Examination of specimens col-

lected during surveys by Walter Auffenberg and the

Zoological Survey Department of Pakistan in the 1980s-

1990s provide insights to many questions regarding

some of these poorly defined taxa. One such species,

Cyrtopodion stoliczkai (Steindachner, 1867), is dis-

cussed below. Future contributions will examine addi-

tional species.

Materials and Methods

ITerpetological collections were made in the vicinity of

Skardu, Federally Administered Northern Areas

(FANA), Pakistan in late August 1991. A series (n = 25)

of Cyrtopodion stoliczkai comprised of all size classes

ranging from newborns to adults was collected from

under slabs of caliche broken off the edge of a dry creek

bed near the Skardu Airport, ca. 10 km west of Skardu.

These specimens were subsequently deposited in the

Florida Museum of Natural History, University of

Florida (UF 81327 - 81351).

This entire series was examined for 44 morpholog-

ical characters (Tables 1 and 2). Although most of these

counts and measurements are standard, clarification on

certain characters are provided. Only original (not

regenerated) tails were measured. The left side is given

first for scale counts taken on both sides of the speci-

men. Character 6 was obtained by counting the scales

surrounding five randomly selected enlarged dorsal

tubercles. Character 12 lists color bands in the following

order: occipital region, nape, body (from forelimbs to

sacrum), and original tail. Character 13 lists the left side

only for the number of scales between the eye and ear.

The numbers of longitudinal rows of enlarged dorsal

tubercles (Character 14) and transverse rows of ventral

scales (Character 15) were taken at mid-body.

Source acronyms follow Leviton et al. (1985):

BMNH (British Museum of Natural History, London);

MCZ (Museum of Comparative Zoology, Harvard

University); NMW (Naturhistorisches Museum. Wien);

UF (Florida Museum of Natural History, University of

Florida); ZFMK (Zoologischen Forschungsinstitutes

und Museums Alexander Koenig, Bonn); ZSI (Indian

Museum, Zoological Survey of India, Calcutta); ZSMH

(Zoologische Staatssammlung Miinchen).

Results

Table 2 illustrates the variation of 44 morphological

characters examined in 25 Cyrtopodion stoliczkai from

Skardu. We found that these characters overlap with

those available for Alsophylax (Altiphylax) boehmei

Szczerbak, 1991. Therefore, we believe that A. boehmei

should be considered a junior synonym of C. stoliczkai

(see Discussion).

Vol. 10, p. 152

Asiatic Herpetological Research

2004

Figure 1. Cyrtopodion stoliczkai (Steindachner, 1867) -

dorsal and ventral views of adult (UF 81349) and

subadult specimen (UF 81334) similar in size to holo-

type of Alsophylax ( Altiphylax ) boehmei (Szczerbak,

1991); both specimens collected near Skardu Airport,

ca. 10 km. west of Skardu, FANA, Pakistan.

Cyrtopodion stoliczkai (Steindachner, 1 867)

[Fig. 1; Tables 1,2]

Diagnosis. - Medium-sized geckos (snout-vent length

[SVL] of largest adult = 46.5 mm), tail slightly longer

than body (longest tail = 53.4 mm), SVL/tail length,

mean = 0.854, Standard Deviation [SD] = 0.0455 (n =

11); limbs moderate, hind limb extends to axilla, fore-

limb to near nostril; body and head somewhat dorso-

ventrally compressed. Head moderate (head

length/SVL, mean = 0.267, SD = 0.0267, head

width/head length, mean = 0.696, SD = 0.0370, head

height/head width, mean = 0.593, SD = 0.0546), snout

equal to or slightly longer than distance between eye and

ear. Eye large (eye diameter/eye - nostril, mean = 0.704,

SD = 0.0665); ear rounded to ovate, small, ear diame-

ter/eye diameter, mean = 0.148, SD = 0.0463. Nostril

bordered by rostral, first supralabial, and normally 3

postnasals, occasionally fused to form 2 postnasals or

split into 4 scales, medial postnasal smaller than others,

1 - 2 medial scales between postnasals (lacking in one

specimen), when 2 present, one is often much larger than

the other. Dorsal head scales generally homogeneous in

size and shape, slightly larger on snout; 17-20 interor-

bital scales; loreals often with small projections on pos-

terior half of eye; rostral partially cleft; 9-11 supralabi-

als (12 on right side of one specimen), 7-9 inffalabials.

Mental triangular, longer than broad. 3 pairs of post-

mentals (rarely 2), decreasing in size posteriorly, first

pair in contact, with a broad suture; second pair rarely

disproportionate in size; third pair often variable in size,

may be substantially enlarged on one side, often separat-

ed from inffalabials by a series of small scales. Dorsum

of body and limbs with small roundish, beaded to flat

scales intermixed with larger, roundish tubercles; tuber-

cles surrounded by rosettes of 7 - 9 small scales, 2-3

times larger than granular scales, smooth, flat to round-

ed, sometimes indistinctly keeled, slightly conical later-

ally; arranged in 8 - 10 (rarely 12) longitudinal rows, lat-

eral rows indistinct. Lateral fold indistinct, often absent.

Venter with roundish, slightly imbricate scales, 25-31

across middle of belly; 113 - 135 from postmentals to

cloaca. Preanal and femoral pores absent. Femoral

spines absent. Cloacal spines present, 1 - 2 per side.

Digits moderate, subdigital lamellae well-developed,

nearly as broad as digit, 1 6 - 20 on fourth finger, 10-12

on first toe, 19-27 on fourth toe. Tail dorso-ventrally

compressed on anterior two-thirds, round on posterior

one-third; anterior half with dorsal medial groove; ante-

rior half distinctly segmented, swollen and lobed lateral-

ly in adults, less so in subadults and juveniles, tapering

to point; 5 whorls on anterior one-third on tail; each seg-

ment on anterior half with one enlarged dorso-lateral

tubercle and 2 - 3 enlarged, bluntly conical lateral tuber-

cles per side, medial tubercles largest; tubercles reduced

in size and number (2) distally, indistinct or absent on

posterior one-third; 6 - 7 rows of scales per whorl, ter-

minal row not enlarged, squared-off posteriorly, not

acuminate or keeled; 2 series of small subcaudals,

cycloid, not greatly enlarged transversely, only about

twice as large as adjacent scales, separated by medial

groove on anterior half to two-thirds of tail; regenerated

tail without segments and lobes, uniformly covered in

small flattened scales.

Dorsal ground color light to medium gray with 7 -

10 irregular transverse darker gray bands, with even

darker posterior margins; 1 on occipital area, 1 on nape,

and 5 - 8 on body; 10 - 15 on tail; limbs with short gray-

ish bands; grayish-brown band from nostril through eye;

top of head irregularly mottled; labials with dark speck-

les; venter whitish.

2004

Asiatic Herpetological Research

Vol. 10, p. 153

Table 1. Morphological Characters examined for

Cyrtopodion stoliczkai from Pakistan. See text for character

descriptions.

1. Number of post-nasals

2. Number of medial scales between post-nasals

3. Number of supralabials

4. Number of infralabials

5. Number of interorbitals

6. Number of scales surrounding dorsal tubercle (ran-

domly counted 5 tubercles)

7. Number of scales between postmentals and cloaca

8. Number subdigital lamellae on fourth toe

9. Number of pairs of postmentals

10. Number of whorls on anterior one-third of tail

11. Number of large, lateral tubercles on each tail whorl

12. Number of color bands on head, nape, body, and tail

13. Number of scales between eye and ear (left side only)

14. Number of longitudinal rows of tubercles

15. Number of transverse rows of ventral scales at mid-

body

16. Number of subdigital lamellae on first toe

17. Presence (+) and number of cloacal spines

18. Number of scale rows per tail whorl (max. 8 whorls

counted)

19. Number of subdigital lamallae on fourth finger

20. First pair of postmentals in contact (+) or not in con-

tact (-)

21. Scales on top of head homogeneous in size (+) or not

homogeneous in size (-)

22. Dorsal tubercles present (+) or absent (-)

23. Mental triangular (+) or not triangular (-)

24. Tail whorls distinct (+) or indistinct (-)

25. Preanal pores present (+) or absent (-)

26. Color pattern of dorsum banded (+) or not banded (-)

27. Color band from nostril through eye to nape present

(+) or absent (-)

28. Femoral spines present (+) or absent (-)

29. Femoral pores present (+) or absent (-)

30. Enlarged tubercles on limbs present (+) or absent (-)

31. Roundish dorsal tubercles present (+) or absent (-)

32. Dorsal tubercle sculpture rounded (+) or not rounded

(-)

33. Medial subcaudals in series (+) or not in series (-)

34. Distal scale row of tail whorl enlarged (+) or not

enlarged (-)

35. Tail dorsoventrally compressed (+) or not compressed

(-)

36. Snout-vent length (SVL)

37. Tail length

38. Head length

39. Head width

40. Head height

41. Nostril-eye distance

42. Eye-ear distance

43. Eye diameter

44. Ear diameter

Distribution. - Cyrtopodion stoliczkai has been record-

ed from various localities (see references cited herein)

in the upper Indus River valley ranging from Leh,

Kashmir to Skardu, Pakistan, a distance of almost 300

km by air (Fig. 2). This species was collected in the

Kargil vicinity in Kashmir along one of the many tribu-

taries of the upper Indus River and may occur in other

associated river valleys as well. The Shyok River, a

large tributary draining areas to the north of the Indus

River, remains virtually unexplored. The Indus River

enters a series of gorges west of Skardu, which may

impede dispersal in that direction.

Habitat. - Cyrtopodion stoliczkai occurs in the Pamir-

Karakorum Highlands region of northern Pakistan and

adjacent Kashmir at elevations from 2300 to 3700 m.

Vegetation is sparse in this region, being generally con-

fined to human occupation sites, seeps, streams, and

forested valleys. The intervening barren landscape is

characterized by stark and steep mountainsides, rock

and boulder fields, and large areas of clay, caliche, and

sand. This species has not been collected from human

habitations. Some individuals from the large series col-

lected by Stoliczka during the Second Yarkand

Expedition were found under stones (Blanford, 1878).

Gruber (1981) collected most of his series in rocky

habitats, although one specimen was found in a small

hole in a willow tree. Our series was collected from

small cracks and fissures between slabs of caliche (see

above).

Reproduction. - In the vicinity of Skardu, hatching

occurs in mid to late August. In addition to several new-

borns, three full-term eggs (UF 81352) were collected in

a cavity between slabs of caliche on 29 August 1991.

Although collected together, it is unknown if these rep-

resent a single clutch or communal oviposition site. Egg

measurements range from 9.7 - 11.1 mm in length and

7.6 - 8.5 mm in width.

Discussion

The assignment of the species epithet " stoliczkai " to the

genus Cyrtopodion Fitzinger, 1843 is arbitrary. The

generic assignments of the angular-toed geckos of

South and Central Asia have undergone a great deal of

revision over the last few decades (see Anderson, 1999

for a synopsis of the nomenclature history). In this

paper we follow the simplified arrangement presented

by Anderson (1999) on Iranian species of this group, as

we assign all Pakistan species of angular-toed geckos to

the genus Cyrtopodion. We also find it prudent, consid-

ering the current taxonomic confusion, not to allocate

subgenera. Cyrtopodion stoliczkai is presently not

Vol. 10, p. 154

Asiatic Herpetological Research

2004

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2004

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Vol. 10, p. 155

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Vol. 10, p. 156

Asiatic Herpetological Research

2004

assigned to a subgenus, but is regarded as a member of

the "Tibeto-Himalayan" group. Our somewhat cursory

examination of other members of this group, including

C. baturensis (Khan, 1992), C. chitralensis (Smith,

1935) (synonymized with C. walli (Ingoldby, 1922) by

Khan, [1992]), and C. mintoni (Golubev and Szczerbak,

1981), clearly shows that this group is highly artificial.

Khan and Rosier (1999) did not consider

Cyrtopodion stoliczkai as a member of the Pakistan

gecko fauna, confining it to the upper Indus River valley

in Kashmir. However, the morphological characters of

our series from Skardu closely match those of Szczerbak

and Golubev (1986, 1996) and Khan and Rosier (1999).

Therefore, C. stoliczkai does indeed occur in Pakistan.

Cyrtopodion stoliczkai (Steindachner, 1867) was

described from a single specimen collected by

Ferdinand Stoliczka in 1865 near Karoo, north of Dras,

in northern Kashmir (Blanford, 1878). Some previous

authors have cited Steindachner (1869) as the original

description, but this actually refers to a reprint of the ear-

lier work (K. Adler, pers. comm.). This single specimen

was subsequently transferred to the Naturhistorisches

Museum, Wien (Vienna, Austria), where Steindachner

designated it as the holotype (NMW 16756) in honor of

its collector. The holotype is well-illustrated by

Szczerbak and Golubev (1986, 1996:Fig. 92). During

the Second Yarkand Expedition (1873 - 1874), Stoliczka

collected an additional 46 specimens from the type

locality and a few localities eastward to Leh in the Indus

River valley of central Ladakh, Kashmir. These speci-

mens were subsequently deposited in the Indian

Museum, Calcutta (Blanford, 1878). Annandale (1913)

enumerated only 31 specimens in the Indian Museum

collections in his treatment of Indian Gymnodactylus.

Zugmayer (1909) and Brongersma (1935) reported this

species from Lamayuru and Leh, respectively, both

localities being in central Ladakh. Gruber (1981) col-

lected 14 specimens from a few localities in the same

general area as Stoliczka in 1865, which were deposited

in the ZSM. Khan and Rosier (1999) presented a

detailed redescription of C. stoliczkai based on this last

series, but were unable to examine the holotype and the

series in the Indian Museum. Khan and Rosier (1999)

erroneously referred to a specimen of C. stoliczkai in the

2004

Asiatic Herpetological Research

Vol. 10, p. 157

Museum of Comparative Zoology (MCZ 7132) as both

a syntype and paratype. This specimen cannot be consid-

ered either, as Steindachner mentioned only one speci-

men in the original description, and Constable (1949:84)

did not provide any type designation for this MCZ spec-

imen. This specimen was received by the MCZ via

exchange with the Indian Museum, Calcutta, in June

1908 (Constable, 1949:61; J. Rosado, pers. comm.).

Stoliczka is given as the collector (Constable, 1949:61).

Stoliczka died in 1874 during the Second Yarkand

Expedition's return to India, indicating that his large

series from Ladakh in the Indian Museum was collected

in 1873 during the outbound portion of the expedition.

We must assume that the MCZ specimen originates from

this large series, however, it is possible that Stoliczka

made additional collections in Ladakh between 1865

and 1873. Nevertheless, it is clear that Steindachner

(1867) examined only one specimen at the time C.

stoliczkai was described and the MCZ specimen cannot

be a type. Additionally, Khan and Rosier (1999) referred

to MCZ 7132 as a topotype. This may or may not be cor-

rect, as Stoliczka's journal from the Second Yarkand

Expedition indicated that only some of his specimens

were collected at the type locality (Blanford, 1878) and

others were collected elsewhere. However, since the

only locality information available for the MCZ speci-

men is "Ladakh", it cannot be ascertained that it is actu-

ally one of the specimens collected at the type locality.

Gymnodactylus walli Ingoldby, 1922 and G. yarkan-

densis Anderson, 1872 were regarded as synonyms of

Cyrtopodion stoliczkai by Smith (1935), a view fol-

lowed by virtually all subsequent authors. Minton

(1966) referred to a single specimen from Udigram,

Swat District, Northwest Frontier Province, Pakistan as

C. stoliczkai , which was later found to be a distinct

species (Mertens, 1969:26; Khan, 1980:14; described as

Gymnodactylus mintoni by Golubev and Szczerbak in

1981). Khan (1992) produced a compelling argument to

consider Cyrtopodion walli distinct from C. stoliczkai

based on an examination of the type specimens in the

British Musuem. We are unable to resolve the synonymy

of C. yarkandensis (Anderson, 1872). Blanford (1878)

relegated C. yarkandensis to the synonymy of C.

stoliczkai (Steindachner, 1 867), and subsequent authors

followed this view (Annandale, 1913; Boulenger, 1890;

Kluge, 1991, 1993, 2001; Mertens, 1969; Minton, 1966;

Smith, 1935; Szczerbak and Golubev, 1986, 1996;

Wermuth, 1965; Zhao and Adler, 1993). Khan (1994)

resurrected C. yarkandensis based on an examination of

a single specimen housed in the British Museum

(BMNH 72.3.22.4). A comparison of color transparen-

cies taken during a study of the same specimen by W.

Auffenberg in the early 1990s, along with our series

from Skardu, indicate that this specimen is probably best

assigned to C. stoliczkai. However, important morpho-

logical characters cannot be ascertained from the trans-

parencies or Khan's (1994) description. Szczerbak and

Golubev (1986, 1996) also assigned this specimen to C.

stoliczkai. Whether C. yarkandensis is a distinct taxon

or a synonym of C. stoliczkai can be determined only

with a thorough examination of the types housed in the

Indian Museum, Calcutta. We provide the following

notes on C. yarkandensis at this point merely for a his-

torical perspective.

Anderson (1872) mentioned two specimens in his

description of Cyrtodactylus yarkandensis. These were

supposedly collected in Yarkand (= Shache, Xinjiang,

China; Zhao and Adler, 1993) during the First Yarkand

Expedition in 1870 (Blanford, 1878). This locality was

doubted by Blanford (1878:12-13), maintaining that the

types of C. yarkandensis were identical to the C.

stoliczkai specimens collected by Stoliczka during the

Second Yarkand Expedition in Ladakh, some of which

were taken from the type locality of C. stoliczkai.

Blanford (1878:13) stated "The specimens described by

Dr. Anderson as Cyrtodactylus yarkandensis were

brought, with others, by a collector, who accompanied

Dr. Henderson on the mission which was sent to

Yarkand in 1870; this mission traversed precisely the

same route through Kashmir and Leh as the second in

1 873 - 74, and I do not think there can be any reasonable

doubt that the real locality whence Cyrtodactylus

yarkandensis was obtained must have been Ladak, and

not Yarkand." Annandale (1913:316) incorrectly attrib-

uted the collection of the types of C. yarkandensis to

Stoliczka during the Second Yarkand Expedition. That

mission embarked in 1873, about one year after

Anderson's (1872) description of C. yarkandensis. Khan

(1994) referred to this specimen (BMNH 72.3.22.4;

"Yarkhand") as a syntype. The specimen catalogue at the

British Museum indicates that this specimen was

"Presented by [the] Indian Museum Calcutta through Dr.

Anderson" and cataloged on March 22, 1872 (C.

McCarthy, pers. comm.), the same year the species was

described. Anderson (1872:381) mentioned only two

specimens in the original description and Annandale

(1913:316) referred to two specimens (ZSI 3792 - 93) as

types of C. yarkandensis (as a synonym of

Gymnodactylus stoliczkai Steindachner) in the Indian

Museum, Calcutta. It can be assumed that these were the

specimens on which Anderson based his description,

thus the status of the British Museum specimen remains

nebulous.

Alsophylax ( Altiphylax ) boehmei Szczerbak, 1991

was described from two specimens collected by G.

Osella from Skardu, Pakistan in July 1976. Although we

did not examine the holotype, we have no doubt that the

description of this species is based on subadult

Vol. 10, p. 158

Asiatic Herpetological Research

2004

Cyrtopodion stoliczkai. This relationship was originally

suggested by Golubev (in Szczerbak and Golubev,

1996:200, footnote). Morphological characters for A.

boehmei provided by Szczerbak (1991) fall within the

range of variation in those we recorded for C. stoliczkai

(Table 1). The holotype (ZFMK 38773, see Fig. 3 in

Szczerbak, 1991) matches the subadults in our complete

growth series collected in Skardu in 1991 (Table 2). The

whorls of the anterior third of the tail of C. stoliczkai do

not become swollen and lobed until maturity, but

Szczerbak (1991) lacked a sufficient series of specimens

to make this determination.

Golubev (in Szczerbak and Golubev, 1996:200,

footnote) also suggested that Tenuidactylus baturensis

Khan and Baig, 1992 may also be conspecific with

Cyrtopodion stoliczkai. Our examination of one speci-

men collected near the type locality of T. baturensis indi-

cates that although it is similar in overall morphology,

this species appears to be distinct.

Khan (200 1 ) divided the Tibeto - Himalayan group

of Cyrtopodion into three subgroups: Stoliczkai sub-

group = C. baturensis (Khan and Baig, 1992), C.

stoliczkai (Steindachner, 1867), and C. yarkandensis

(Anderson, 1872); Tibetinus subgroup = C. battalensis

(Khan, 1993), C. dattanensis (Khan, 1980), C.

himalayanus (Duda and Sahi, 1978), C. mintoni

(Golubev and Szczerbak, 1981), and C. tibetinus

(Boulenger, 1905); and the Walli subgroup - C. walli

(Ingoldby, 1922) (including C. chitralensis [Smith,

1935] as a synonym) and C. kirmanense (Nikolsky,

1900). Our preliminary examination of most of these

taxa reveals that Khan's system has merit concerning

overall morphological and ecological data. Further

investigations into the Pakistan gecko fauna and that of

adjacent areas will undoubtedly lead to further discover-

ies of new species and more clearly define those already

described.

Acknowledgments

We would like to thank the Division of International

Conservation, United States Fish and Wildlife Service

(Washington, D. C.), Deutscher Akademischer

Austauschdienst, Bonn, Germany, and the Office of

Sponsored Research, University of Florida for the fund-

ing support awarded to W. Auffenberg that made possi-

ble the fieldwork and museum visits by him. We also

thank Kraig Adler (CU), Steve Anderson (University of

the Pacific), M. S. Khan (Secane, Pennsylvania), Arnold

Kluge (UMMZ), Colin McCarthy (BMNH), and Jose

Rosado (MCZ) for pertinent literature, insight, and the

examination of specimens under their care. We also rec-

ognize Max Nickerson and Wayne King (Florida

Museum of Natural History) for their encouragement

and support. Tammy Johnson prepared Fig. 2. We thank

the dedicated staff of the Zoological Survey Department

of Pakistan, particularly Mohammad Farooq Ahmed,

former Director, Hafizur Rehman, Shamim Fakhri, and

Aleem Khan, for their support and assistance throughout

the fieldwork portion of this project.

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other reptiles. Proceedings of the Zoological

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Anderson, S. C. 1999. The Lizards of Iran. Society for

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Annandale, N. 1913. The Indian geckos of the genus

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Blanford, W. T. 1878. Scientific results of the Second

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Boulenger, G. A. 1890. The Fauna of British India,

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Duda, P. L. and D. N. Sahi. 1978. Cyrtodactylus

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2004

Asiatic Herpetological Research

Vol.10, pp. 161-163

Antimicrobial Activity in the Skin Secretion of Bufo viridis (Laurenti, 1768)

Ba§aran Dulger1’*, Ismail Hakki Ugurta§2, and Murat Sevinc2

Canakkale Onsekiz Mart University, Faculty of Science & Arts, Department of Biology, C an akkal e-Turkey

2

Uludag University, Faculty of Science & Arts, Department of Biology, Bursa-Turkey

*

Correspondence author, E-mail: dbasaran@comu.edu.tr; Fax number: +90.286.2 180533

Abstract. - In this study, antimicrobial activity of various extracts prepared from Bufo viridis skin secretion were

tested against the microorganisms by disk diffusion method. Escherichia coli ATTC 10536, Listeria monocytogenes

ATCC 19117, Klebsiella pneumoniae UC57, Salmonella typhi ATCC 19430, Staphylococcus aureus ATCC 6538P,

Mycobacterium smegmatis CCM 2067, Rhodotorula rubra and Saccharomyces cerevisae ATCC 9763 were used.

According to our results, the extracts prepared from Bufo viridis skin secretion have high antimicrobial activity

against the tested microorganisms.

Keywords. - Bufo viridis, Amphibia, antimicrobial activity, skin secretion.

Introduction

Amphibians have skin glands producing mucous and

poison. Amphibians have been studied and have

attracted special attention from a toxicological point of

view. Various substances with antimicrobial activity

have been isolated from skin secretions of amphibian

species (Dapson, 1970; Croce et al., 1973; Dapson et al.,

1973; Preusser et al., 1975; Cevikbas, 1978). Several

toxins in amphibian poisons have been used as experi-

mental tools and contributed to significant progress in

physiology. Some toxins (Batrachotoxins) specifically

block the inactivation of the voltage regulated Na+ chan-

nels in nerve and muscle cells, which causes a massive

inflow of Na+. The cells become irreversibly depolar-

ized, which, among other things, produces heart arrhyth-

mia and respiratory failure and finally cardiac

insufficiency. In humans, some amphibian toxins (Bufo-

tenin) produce symptoms similar to those of LSD (Lutz,

1971; Edstrom, 1992). In previous studies, some skin

secretions showed remarkable cytotoxic activity against

eukaryotic cells (Kolbe et al., 1993; Sanna et al. 1993).

The aim of the this study is to test the antimicrobial

activity of Bufo viridis skin secretions against Gram-

positive, Gram-negative bacteria and yeast cultures for

future possible use in providing pharmacological tools

for the study of new drugs and aid in benefitting human

health.

Materials and Methods

Specimens of Bufo viridis were collected from different

regions in Bursa, Turkey in March 1998. Collected frogs

were brought to the laboratory and kept in an aquarium.

Before experimentation, the frogs were washed first

with tap water and then with distilled water. They were

placed for 3-5 minutes in a glass jar containing a piece

of cotton soaked with ether to stimulate skin secretions.

The secretion accumulated on the skin was obtained by

scraping the body of the animals with a spatula. The

foamy secretion thus obtained was placed in a tube, left

in an 80°C water bath for 30 min and centrifuged at

5,500 rev/min for 30 min. After centrifugation, the pre-

cipitate was used in the experiments. Before using in the

experiments, the precipitate was diluted with distilled

water 0.1 M HC1, 0.1 M NH4OH, and 1 M phosphate

buffers (pH: 4 and pH: 7).

In this study, Escherichia coli ATTC 10536, Liste-

ria monocytogenes ATCC 19117, Klebsiella pneumo-

niae UC57, Salmonella typhi ATCC 19430,

Staphylococcus aureus ATCC 653 8P, Mycobacterium

smegmatis CCM 2067 bacteria cultures and Rhodot-

orula rubra and Saccharomyces cerevisae ATCC 9763

yeast cultures were used.

In vitro antimicrobial activity studies were carried

out by the Agar-Disc Diffusion Method. Mueller Hinton

Agar (Oxoid) was preferred as the most suitable

medium for antimicrobial activity studies. Each extract

was implemented into a sterile disc in varying concen-

trations starting from 20 pi. Each disc was 6 mm in

diameter.

Bacteria and yeast cultures were suspended in 4-5

ml Brain Heart Infusion Broth (Oxoid) and Malt Extract

Broth (Difco). Bacteria were incubated in 37°C for 2-5

hours. Yeast cultures were incubated in 30°C for 5-7

hours. A visible turbidity was obtained at the end of this

time. The turbidity of bacterial suspension was adjusted

Vol.10, p. 162

Asiatic Herpetological Research

2004

Table 1. Antimicrobial activity of various extracts of Bufo viridis skin secretions on microorganisms.

(+) : Inhibition zone less than 1 mm surrounding the 6 mm paper disk.

+ : Inhibition less than

++ : Inhibition comparable to

+++: Inhibition more than 10 pg penicillin or sulconazole / disk; Inhibition zones of references : 12-16 mm diameter.

according to Macfarland Standard Tube [0,5] with phys-

iologic serum and inoculation performed. Prepared bac-

terial suspension was mixed with a sterile applicator and

excess fluid of applicator was removed by rotating the

applicator to one side of the tube. We streaked the entire

Mueller Hinton Agar surface in three different direc-

tions by rotating the plate 60° angles after each streak-

ing. Yeast cultures were inoculated into Muller Hinton

Agar (102 cfu/ml). All petri dishes after inoculation were

allowed to dry for 15-20 min at room temperature (bac-

teria at 35°C and yeast at 30°C). Inhibition zone diame-

ters were measured after 24-48 hours (Collins et al.

1987, NCCLS 1993). In addition, continued only sol-

vent was used as negative control disc and antibiotic

penicillin and sulcanozole discs were used as references.

Experiments were repeated three times and results were

expressed as average values.

Results and Discussion

Antimicrobial activity effects of five different extracts,

which were prepared by using distilled water, 0.1 N

HC1, 0.1 N NH4OH, 1 M phosphate buffers (pH: 4 and

pH: 7), were obtained from the skin secretions of Bufo

viridis against bacteria and yeast cultures, results are

given in Table 1.

According to our findings, all the extracts of skin

secretion against the yeast cultures exhibit higher anti-

microbial activity than that of a compared antibiotic.

The 0.1 M HC1 extract shows more effect than that of

the other extracts against bacteria. 1 M phosphate buffer

(pH: 4 and 7) extracts exhibited minor effects against

Escherichia coli. However, phosphate buffer (pH: 4 and

7) extracts exhibited strong effects against the other bac-

teria. It can be said that the active substance obtained

from Bufo viridis skin secretion dissolves easily in the

0.1 M HC1 and has high antimicrobial activity as a con-

sequence. It has been reported that sensitivity of the

microorganisms to the chemotherapeutic agents

changes from strain to strain (Cetin et al., 1989). Our

results are in agreement with the other authors’ results.

Inhibition zone diameters around the control disc

were measured as 0-1 mm. In this study, antimicrobial

effects of the prepared extracts on the tested microor-

ganisms were determined by using different solvents.

Croce et al. (1973) investigated antimicrobial activ-

ity of skin secretions from Bombina variegata pachy-

pus. They homogenized skin secretion with phosphate

buffers (pH: 4 and 7) 1 M HC1, 1 M NH4OH and dis-

tilled water. These homogenates show high antimicro-

bial activity against Staphylococcus aureus but they do

not show any antimicrobial effect against Aspergillus

niger, Trichophyton mentagrophytes ATCC 8757 and

Candida albicans.

Cevikbas (1978) examined antibacterial activity in

the skin secretions of Rana ridibunda. The author

reported that skin secretion of Rana ridibunda shows

antibacterial activity at different levels. However, in our

2004

Asiatic Herpetological Research

Vol.10, p. 163

piesent study, skin secretions of Bufo viridis against the

yeast cultures shows more antimicrobial activity than

that of the bacterial cultures. Our findings parallel those

reported in the above studies. In Amphibia, antimicro-

bial activity of skin secretions differ at both the generic

and specific levels.

Although the antimicrobial activity of skin secre-

tions from Bufo viridis , Bufo vulgaris , Salamandra mac-

ulosa and Salamandra atra were determined (Pavan,

1962; Pavan and Nascimbene, 1948), antimicrobial

activity ot skin secretion from Bufo marinus, Triturus,

and Xenopus were not observed (Preusser et al., 1975;

Kolbe et al., 1993; Ozeti and Yilmaz, 1994). Antiyeast

activity observed in our study was not observed in

Croce’s et al. study (1973). Our results show that skin

secretion components from Bufo viridis may be different

from Bombina variegata pachymus.

Acknowledgments

The authors are grateful to Aegean University, Science

Faculty, Department of Biology, and Basic and Indus-

trial Microbiology for supplying the strain of microor-

ganism used in the study.

References

Cetin, T. E. and N. Gurler. 1989. Bakterilerin Antibiyo-

tiklere Duyarlilik Deneyinin Yapilmasi. Kukem

12:2-5.

Cevikbas, A. 1978. Antibacterial activity in the skin

secretion of the frog Rana ridibunda. Toxicon

16(2): 195-197.

Collins, C. M., P. M. Lyne, and J. M. Grange. 1989.

Microbiological Methods, Six Edition. Butter-

worths & Co. Ltd., London. 410 pp.

Croce, R., N. Giglioli, and L. Bolognani. 1973. Antimi-

crobial activity in the skin secretions of Bombina

variegata pachymus. Toxicon 1 1 :99-100.

Edstrom, A. 1992. Venomous and Poisonous Animals.

Kriger Publishing Company. Malabar, Florida.

USA. 226 pp.

Kolbe, FI. V. L, A. Fluber, P. Cordier, U. B. Rasmussen,

B. Bouchon, M. Jaqunod, R. Vlasak, E. Delot, and

G. Kreil. 1993. Xenoxins: A Family Of Peptides

From Dorsal Gland Secretion Of Xenopus laevis

Related To Snake- Venom Cytotoxins And Neuro-

toxins. Journal of Biological Chemistry

268(22): 16458-16464.

Lutz, B. 1971. Venomous Animals and Their Venom.

Academic Press, London. 423-427 pp.

NCCLS. 1993. Performance Standards for Antimicro-

bial Disk susceptibility Tests. Approved Standard

NCCLS publication M2- A5, Villanova, PA, USA.

Ozeti, N. and F Yilmaz. 1994. [Amphibians of Turkey].

Aegean University Press, Izmir. 151 pp.

Pavan, M., 1962. Die Antibiotica tierischer Herkunft.

Zeitschrift Fur Hygiene und Infektionskrankheiten

34:136-138.

Pavan, M., and A. Nascimbene. 1948. Studi sugli antibi-

otici di origine animale. Bolletino Societa Medico-

chirurgica, Pavia 1-2:229.

Preusser, H. J., G. Habermehl, M. Sablofski, and H. D.

Schmall. 1975. Antimicrobial activity of alkoloid

from amphibian venoms and effects on the ultras-

tucture of yeast cells. Toxicon 12: 285.

Sanna, A. P., A. Bamabei, and G. Delfino. 1993. The

Cutaneous Venom of Bombina orientals : Cytotoxic

Effects on the human HL 60 Cell Line and A Com-

parison with Bombina variegata. Journal of Natural

Toxins 2(2): 16 1-173.

Analysis of the Stomach Contents of the Lycian Salamander

Mertensiella luschani (Steindachner, 1891)

(Urodela: Salamandridae), Collected from Southwest Turkey

Serdar Du§en, Mehmet Oz, and M. Rizvan Tunc

Akdeniz University, Faculty of Arts and Sciences, Department of Biology,

07058, Antalya, Turkey

Abstract. - In this paper, the stomach contents of 116 specimens (39 males, 47 females, and 30 juveniles) from the

Southwest Turkey Mertensiella luschani populations are analyzed. A total of 342 prey items were identified and their

frequency of occurence and percent of diet were tabulated. The majority of the diet consisted of Insecta (50.58%),

and within Insecta, Coleoptera (65.32%) was the major order represented. In addition to insects, M. luschani feeds on

Gastropoda (19.59%), Arachnida (16.08%), Myriapoda (8.57%), Clitelliata (3.50%) and Crustacea (1.75%).

Key words. - Mertensiella luschani , stomach contents, prey, southwest Turkey.

Baran and Atatiir, 1980, M. 1. billae Franzen and Kle-

wen, 1987, and M. 1. flavimembris Mutz and Steinfartz,

1995. Mertensiella luschani is not dependent on water,

it inhabits humid soils and crevices under the Pinus bru-

tia forests, Mediterranean maquis, and open rocky

areas. Its vertical distribution ranges between 15-1300

m.

Various studies have been done on M. luschani in

terms of its taxonomy (Franzen et all, 2001), ecology

(Klewen, 1991; Steinfartz and Mutz, 1998), and repro-

ductive biology (Ozeti, 1973; Ozeti, 1980). The aim of

Figure 1. Collecting localities of Mertensiella luschani in Southwest Turkey. 1-Kocagol, 2-Dodurga, 3- Letoon, 4-Nadar

lar, 5-Finike, 6-Buyukgaltlcak, 7-Hurma, 8-Fersin

Introduction

Nine subspecies of the Lycian Salamander, Mertensiella

luschani, are distibuted along the coast of Southwestern

Turkey and on some islands (e.g., Kastellorizon, Meis,

Kekova, and Karpathos) (Baran and Atatiir, 1997; Ba^-

oglu et al., 1994; Veith et ah, 2001). These are M. 1. lus-

chani Steindachner, 1891, M. 1. helverseni Pieper, 1963,

M. 1. atifi Ba?oglu, 1967, M. l.fazilae Ba^oglu and Atat-

ur, 1974, M. l.finikensis Ba^oglu and Atatiir, 1975, M. 1.

antalyana Ba^oglu and Baran, 1976, M. 1. basoglui

Vol.10, p. 165

Asiatic Herpetological Research

2004

Table 1. Composition of the stomach contents of Mertensiella luschani (39 males, 47 females, 30 juve-

niles) collected from the Southwest Turkey. N: The numbers of every prey found in all stomachs, n: The

number of stomachs every prey type was found in.

2004

Vol.10, p. 166

Hvmenoptera 1 7 . 92%

Dermaptera 4.62%

Heteroptera 4.05%

.Lepidoptera 2.89%

■ Collembola 2.31 %

- Diptera 1.73%

Others 1.16%

- Coleoptera 65.32%

Figure 2. Distribution of the insect groups in numerical

percentages.

the present preliminary investigation on seven M. lus-

chani subspecies (except M /. flavimembris and M. I

helverseni ) from eight localities in Southwest Turkey is

an analysis of stomach contents.

Materials and Methods

Specimens for this study were collected from the eight

localities in Southwest Turkey during the known activ-

ity period of M. luschani (December-February, 1999). A

total 116 (39 males, 47 females, and 30 juveniles) M

luschani specimens were collected by hand under

stones. Collection sites are shown in Figure 1.

Once collected, the salamanders were taken to the

laboratory to undergo stomach-flushing. A thin pipe

wash bottle is inserted in salamander’s esophagus and

stomach. Gentle pressure on the wash bottle forces dis-

tilled water in to the stomach and forces the food out

throught mouth (modified from Gittins, 1987). The prey

items obtained from each specimen were labeled and

stored in 10 cc. bottles containing 70% ethanol. Dried

pieces from both undigested and partially digested prey

were placed on microscope slides and held in place with

cellophane tape (Du§en and Oz, 2001). These pieces

consisted of whole body, wings, thorax with abdomen,

head, and mouth parts. Through this approach, identifi-

cation to the lowest taxonomic categories was

attempted, samples were examined using a stereomicro-

scope with 10-25x magnification. Prey items were iden-

tified and grouped utilizing methods described

elsewhere (Demirsoy, 1998a,b; Grzimek, 1979a,b,

Lodos, 1986; Riehm, 1984)

Results

We did not observe any significant differences in the

stomach contents of seven subspecies males, females

and juveniles; they were thus evaluated together. Of the

116 specimens (39 males, 47 females, and 30 juveniles),

only two females had empty stomachs. Small unrecog-

nizable insect remains (parts of heads and larvae, anten-

nae, wings, etc.) of the stomach contents are not

included to the numerical analysis. Other non-food

materials such as small pebbles, sand grains, plant parti-

cles, and pieces of feather, possibly ingested during prey

capture were not included either.

A total of 342 prey items were counted from the

investigated stomach contents (Fig. 2); Insecta 173

(50.58%), Gastropoda 67 (19.59%), Arachnida 55

(16.08%), Myriapoda29 (8.57%), Clitelliata 12 (3.50%)

and Crustacea 6 (1.75%). Table 1 presents the stomach

contents with respect to prey groups (their taxonomic

grouping, number of prey items, and percentages of

preyers).

Insects were identified to the ordinal level. The total

number of prey and their percentages are as follow:

coleopters 113 (65.32%), hymenopterans 31 (17.92%),

dermapterans 8 (4.62%), heteropterans 7 (4.05%), lepi-

dopterans 5 (2.89%), dipterans (1.73%), collembolan 4

(2.31%), homopterans 1 (0.57%), and isopterans 1

(0.57%) (Fig. 2). The same insect orders can be ranked

from the viewpoint of the number of prey eaten; their

percentages are as follows: coleopterans 51 (43.96%),

co

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Figure 3. Distribution of the insect groups regarding prey eaters.

Vol.10, p. 167

Asiatic Herpetological Research

2004

hymenopterans 19 (16.37%), dermapterans 8 (6.89%),

heteropterans 6 (5.17%), lepidopterans 5 (4.31%), col-

lembolans 3 (2.58%), dipterans 3 (2.58%), homopterans

1 (0.86%), and isopterans 1 (%0.86) (Fig. 3).

When the prey groups are evaluated by their absolute

values and relative percentages within the food,

coleopterans 51 (43.96%), have the priority. Other con-

sumed invertebrates as follows: Pulmonata 36

(31.03%), Aranae 27 (23.27%), Pseudoscorpion ida 15

(12.93%), Diplopoda 15 (12.93), Clitelliata 9 (7.75%),

Chilopoda 9 (7.75%), and Isopoda 6 (5.17%).

Discussion

This study was conducted to learn more about the feed-

ing preferences of M. luschani collected from southwest

Turkey. The results showed that M luschani feeds

heavily on coleopters and gastropods.

The chance of a food item being taken depends on the

abundance and ease of capture of the different food cate-

gories. Coleopters, although fairly fast moving are

abundant in the foraging area. Gastropods and arachnids

although easier to catch are slightly less abundant.

The results suggest that M. luschani is an opportunist

predator on diverse forms. This situation is related to the

type of habitat they live in and abundance of prey spe-

cies in the vicinity.

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M. R. Tun?. 2001. A revision of population designa-

tion and geographic distribution of the lycian sala-

mander Mertensiella luschani (Steindachner, 1891).

Zoology in the Middle East 22:67-82.

2004

Asiatic Herpetological Research

Vol. 10, pp. 168-175

First Description of Egg Sacs and Early Larval Development in

Hynobiid Salamanders (Urodela, Hynobiidae, Batrachuperus )

from North-Eastern Iran

Mehregan Ebrahimi1, Hagi Gholi Kami2, Matthias Stock3

1 Department of Biology, Faculty of Sciences, University of Shiraz, P.O.Box:? 1 454-1460,

Shiraz, Iran; E-mail: emehrgan@yahoo.com

2 Department of Biology, Faculty of Sciences, University of Agricultural Sciences and Natural Resources,

P.O.Box:491 65-386, Gorgan, Iran; E-mail: hgkami2000@yahoo.com

3 Museum of Vertebrate Zoology, University of California, Berkeley, Department of Integrative Biology,

3101 Valley Life Sciences Building #3 160, Berkeley, CA 94720-3160, USA; E-mail: matthias@berkeley.edu

Abstract. - Here we present the first life history data from a natural habitat on the clutch and from the laboratory on

the early embryonic development of an Iranian hynobiid salamander (the Eastern nominal taxon, Batrachuperus gor-

ganensis). We compare these observations with those of other hynobiid species. The egg sac of B. gorganensis var-

ied from 80 to 182 mm (mean 132.5), and in width from 16 to 22.5 mm (mean 18.9). Single sacs, the largest known

for the genus, contained 31-52 eggs (mean 37.4) in four rows per cross section. Egg sac data are more similar to those

of Ranodon sibiricus (and B. musters i) than to Eastern Batrachuperus ( longdongensis , tibetanus, pinchonii,

karlschmidti, yenyuanensis ), which have strings of single eggs. As is typical of all Batrachuperus, eggs of B. gorga-

nensis are non-pigmented. Embryonic B. gorganensis larvae may exhibit rudimentary balancers, possibly like those

of Ranodon sibiricus, but further investigation is necessary. Detailed morphometric measurements of the larvae of B.

gorganensis and color photographs of some developmental stages are presented.

Key words. - Hynobiidae, Batrachuperus, Batrachuperus gorganensis, Batrachuperus persicus, Batrachuperus

mustersi, Ranodon sibiricus, Iran, egg sacs, embryonic development, larvae, balancer, taxonomy, morphometries.

Introduction

The southwestern-most representatives of the salaman-

der family Hynobiidae occur within the narrow, East-

West oriented Hyrcanian Corridor (= Hyrcania) of

Northern Iran. The corridor is a “unique relict biogeo-

graphic area,” which is “well defined as the south-west-

ern and southern shores of the Caspian Sea ...” and is

“one of the most clearly defined and delineated

provinces in the Irano-Turanian region44 (Fet, 1994). The

Persian mountain salamander, Batrachuperus persicus

Eiselt and Steiner, 1970, was based on larvae collected

from the western part of Hyrcania (NW-Iran, mountains

near Asalem, Gilan province; Eiselt and Steiner, 1970).

Subsequently, specimens that metamorphosed in captiv-

ity were described and several additional localities were

reported (see Schmidtler and Schmidtler, 1971; Steiner,

1973).

The second nominal taxon, Batrachuperus gorga-

nensis (Clergue-Gazeau and Thorn, 1979), was

described from a single adult male type discovered in a

cave from the eastern edge of the Hyrcanian Corridor

(Clergue-Gazeau and Farcy, 1978). Baloutch and Kami

(1995), Kami and Vakilpoure (1996) as well as Kami

(1999, 2004) published additional data on the biology

and distribution of Iranian hynobiid salamanders, all

assigned to B. persicus. Stock (1999) provided a flow-

cytometric DNA measurement (34.77 pg, but based on

GC-biased DAPI-staining, see also Litvinchuk et al.,

2004) and a Giemsa-stained karyotype (2n = 62) of

topotypic B. gorganensis (i.e. the eastern taxon). Stock

also described external larval changes during the devel-

opment from 40 mm until metamorphosis (100 mm),

and reviewed previous papers (see also map with geo-

graphic coordinates of all previously published localities

- Stock, 1999: Fig. 1). After examination of topotypic

subadults and larvae of both taxa as well as morphome-

tric comparisons with B. mustersi, B. pinchonii, and

Ranodon sibiricus, Stock considered a clinal variation of

characters between the western {B. persicus ) and the

eastern nominal taxon (B. gorganensis ) possible (see

also Thom and Raffaelli, 2001: 122). However, molecu-

lar and cytogenetic data as well as a continuous exami-

nation of the morphological variation throughout the

Hyrcanian corridor are lacking.

Both nominal Iranian taxa (cf. Anderson, 1985;

Brame, 1985: 567; Duellman and Trueb, 1986: 497;

Thom and Raffaelli, 2001) are considered two out of

currently nine species of the genus Batrachuperus

(Frost, 2002). Risch (1984) regarded gorganensis to

belong to a separate genus (. Paradactylodon; see Reilly,

1987). While the molecular phylogeny of eastern

Vol. 10, p. 169

Asiatic Hcrpetological Research

2004

Figure 1. Locality: a. Sketch map of northern Iran with its

forested regions and the study area, the educational for-

est of Shastkola; b. Shastkola forest with districts I and II

and streams. The left arrow marks the Shastkola river; c.

District II of Shastkola forest shown in (b) with its 31 land

parcels, the spring of Manzoulak is situated in parcel 14.

Batrachuperus has been examined (Fu et al., 2001),

molecular comparisons of their relationships with

Western Batrachuperus and Ranodon as well as between

the latter taxa are not yet available. However, unpub-

lished results (Macey et al. in prep., with phylogram pre-

sented in Larson et al., 2003: 44, Fig. 2.4) provide evi-

dence that Iranian Batrachuperus may be more closely

related to Ranodon (Kazakhstan, China) and B. muster-

si (Afghanistan) than to the Eastern Batrachuperus

species (Tibet, China). Ranodon sibiricus has five toes

on the hind limbs while B. mustersi, and B. persicus/B.

gorganensis have only four. However, the intraspecific

variation found by Reilly (1983) in B. mustersi , which

sometimes has five instead of four toes, demonstrates

how ambiguous this character can be.

In general, there is still a lack of biological data on

the Iranian taxa, e.g., their egg sacs and early larvae

have never been examined. Only remains of egg cases of

B. persicus were found by Steiner (1973) in late July in

the Central Elburz range and the reports on larvae start

from a minimum size of 22.7 mm (Central Iran; Steiner,

1973) and “about 30 mm” (NW-Iran, Schmidtler and

Schmidtler, 1970). Here we present the first data on the

clutch of the Eastern Hyrcanian hynobiid taxon (B. gor-

ganensis) from a natural habitat. We add some data on

its development in the laboratory and compare these

observations with the features known from other hyno-

biid species.

Results and Discussion

Spawning site. - All clutches (Table 1) were found in

Cheshme-ye (= spring of) Manzoulak (36°42' N, 54 2 1

E), which flows into an artificial pond (3.20 x 2.15 x

1.25 m). Its bottom is covered with a thick layer ( ca . 15

cm) of tree leaves. Some crabs ( Potamon sp.) and lar-

vae of Odonata, Trichoptera, Coleoptera,

Ephemeroptera were observed. Manzoulak spring is one

of the important water resources of the Shastkola educa-

tional forest (3716 ha), which is situated 13 km South-

West of Gorgan city between 36° 41 36° 45' N and 54c

20' - 54° 24' E, on the northern slopes of the Elburz

mountains (Fig. 1). These mountains reach elevations

ranging from 240 m, above the Caspian Sea in the North

to 2168 m (Gholle-ye-leila Kouh). Shastkola forest is

divided into two organizational units, districts I (1698.6

ha) and II (2017.4 ha). The spring is situated in II [Fig.

lc, land parcel 14 (75 ha), 650 m to 830 m]. Outcrops

consist mainly of a sequence of sandstones and schist in

the lower part and Triassic sand stones in the upper

parts. Shastkola forest has a Caspian climate, and the

nearest climate station is Gorgan (155 m a.s.l.).

However, local climate at the breeding site differs con-

siderably from that at the foothills and we currently have

no detailed climatic data on the site. Water temperature

during collection was below 10°C. The forest tree and

shrub species include Fagus orientalis , Carpinus betu-

lus, Parrotia persica, Ruscus hyrcana , and Ilex aquifo-

lia (for further information: Azadfar, 1994: Azadfar and

Darghahi, 2002), which adds to the accumulating evi-

dence that the Iranian hynobiid taxa inhabit humid

regions mainly overgrown with the plant assemblage

Fagetum hyrcanum in lower elevations in the West of

their range: Parrotio-Carpinetum: in eastern parts of the

Elburz N-slope: Carpinetum orientalis , Quercus

macr anther a\ see also ref. in Stock. 1999).

Description of clutches, eggs and larvae. - About 70

clutches and four adult salamanders were discovered

when leaves were removed from the pond by G. Yolmeh

on January, 28, 2002, but only two of the clutches and

one adult specimen (total length: 21 1 mm) were sent to

the Museum of Zoology of Gorgan University (ZMGU).

In the following year on February. 8. 2003, one complete

and two incomplete clutches were collected in the same

pond by M. Ebrahimi and G. Soltanpour. We presume

that spawning, at least at this site, happened between the

second half of January and the first days of February.

2004

Asiatic Herpetological Research

Vol. 10, p. 170

Figure 2 (A-J). A. Natural habitat of Batrachuperus gorganensis. Stream near Manzoulak spring, photograph taken:

March, 10, 2003. B Clutch, preserved, collection date: March, 10, 2003, photograph taken: April, 6, 2003. C. Clutch,

collection date: March, 10, 2003, photograph taken: April, 4, 2003. D. The same clutch as in C, collection date: March,

10, 2003, photograph taken: April, 4, 2003. E. Fixed embryo, 7 days before hatching, photograph taken: October, 9,

2003. F Fixed larva, 4 days after hatching, photograph taken: October, 9, 2003. G. Living larva, 18 days after hatch-

ing, photograph taken: April, 6, 2003. H. Living larva, 18 days after hatching, photograph taken: April, 6, 2003. I. Living

larva, 24 days after hatching, photograph taken: April, 6, 2003. J. Fixed larva, 34 days after hatching, photograph

taken: October, 9, 2003.

However, in general, the breeding season in both Iranian

nominal taxa might last as long as in some other

Hynobiids (e.g. in Ranodon sibiricus from the end of

April until the beginning of August - Kuzmin, 1995:

111; from May to beginning of August in B. karlschmidti

- Liu, 1950: 91).

During collection, some egg sacs broke. Originally,

the clutches were attached by their stalks to a stone at the

corner of the pond; no egg sacs were observed on its

walls. As is usual in Batrachuperus , each clutch consist-

ed of two asymmetrical, colorless, cylindrical gelatinous

sacs that were connected by gelatinous filaments form-

ing an attaching stalk and had free filaments at their

nonanchored conical ends. As in Ranodon sibiricus (see

Kuzmin, 2001: 40), egg sac data varied between and

within clutches (see Fig. 2 B-D; Table 1). Each cylindri-

cal gelatinous sac contained four rows of eggs per cross

section and each egg was surrounded by a spherical

gelatinous envelope. As is known from Ranodon sibiri-

cus (see Kuzmin and Thiesmeier, 2001: 42 and ref.

therein), these four egg rows produce a tetrahedral shape

immediately after clutch deposition. However, as the

result of an ingress of water, sacs later strongly increase

in size. We believe that all discovered clutches had

already finished this first swelling, which usually gradu-

ally continues throughout the embryonic development

leading to a considerable enlargement of the sacs until

hatching. Tables 2 and 3 show comparisons of egg sac

length and width of eight hynobiid species. Data on

length and width should be evaluated with some reser-

vations, because the number of specimens examined or

time after clutch deposition is imperfectly known.

However, egg sacs of B. gorganensis probably are larg-

er than those of any of the close relatives of the taxon

(with the possible exception ot B. longdongensis ) and

appear to contain among the highest number of eggs per

Vol. 10, p. 171

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2004

Table 1 . Overview of described clutches of Batrachuperus gorganensis.

sac (Table 4). In addition, R. sibiricus and B. gorganen-

sis share the common feature of four rows of eggs per

cross section in an egg sac, while all Eastern taxa ( B .

longdongensis, B. tibetanus, B. pinchonii, B.

karlschmidti, B. yenyuanensis ) seem to have only a sin-

gle row of eggs in an egg case (judging from photo-

graphs and Zhao and Hu, 1988: 32). This feature

remains obscure in B. mnstersi, since neither Reilly’s

(1983) description nor Nawabi’s (1965) photograph

resolve the question satisfactorily, but more than a single

row appears to be present. Egg number may be a taxo-

nomic character but might not affect fecundity since

some species seem to deposit more than one clutch per

breeding period (Liu, 1950; Reilly, 1983).

The diameter of the initially yellowish (as in all

Batrachuperus and R. sibiricus) eggs varied from 4.10

to 5.00 mm (mean 4.56; n = 10) when the clutch was

found. The early eggs had a white animal pole whereas

the vegetal pole was pigmented gray. Unfortunately,

early eggs were not photographed. The separation of

eggs in a row was less than the diameter of an egg. Egg

number varied from 7 to 1 1 per row (2 egg sacs exam-

ined) and from 31 to 52 in each sac (see Table 1). The

eggs have substantial amounts of yolk, as also is typical

of stream-breeding R. sibiricus (Kuzmin and

Thiesmeier, 2001).

Three complete clutches and one incomplete clutch

were kept in a refrigerator at 5-7°C (for conditions see

Stock, 1999). The first larvae to hatch were found on

March, 19, 2003, and the latest specimens to hatch were

observed on March, 25, 2003 (i.e. 40 to 46 days after

discovery, respectively). Some larvae at different devel-

opmental stages were fixed in 4% formalin and 70%

alcohol and measurements were taken from all speci-

mens (summarized in Table 5). We report some larval

developmental traits and link them by inserting the

approximate stage (see inserted number in [...]) of nor-

mal development for Ranodon sibiricus drawn by

Kuzmin and Thiesmeier (2001: 46, after the description

ofLebedkina, 1964).

Hatching larvae [stage 1] exhibited limb buds (Fig.

2F). Although no balancers were observed in hatched

larvae (Fig. 2F), we believe that a rudimentary structure

observed in an embryo fixed 7 days before hatching

(Fig. 2E) could be a balancer. These enigmatic,

ephemeral larval organs, found in three of the ten fami-

lies of salamanders (Crawford and Wake, 1998), are

present in many species of Hynobiidae (Crawford and

Wake, 1998: 115). In the presumed close relative of the

Iranian hynobiids, B. mustersi (see introduction), dis-

tinct balancers are well documented (Nawabi, 1965, see

also Reilly, 1983). Although such a well developed

Table 2. Egg sac length of eight* hynobiid species, comparison of available data on Batrachuperus mustersi from

Nawabi (1965), Reilly (1983), and Sparreboom (1979); on R. sibiricus (from Brushko and Narbaeva 1988, cited from

Kuzmin and Thiesmeier 2001); B. gorganensis (our data); B. longdongensis, B. tibetanus, B. yenyuanensis from Fei

and Ye (2001), B. pinchonii and B. karlschmidti horn Liu (1950) and Fei and Ye (2001); in R. sibihcus numbers in paren-

theses show rare values in late stages of embryonic development (* some authors synonymized B. karlschmidti with

B. tibetanus, but see Fu et al. 2001 and Frost 2002).

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Vol. 10, p. 172

Table 3. Egg sac width of eight hynobiid species, comparison of available data; same sources as in table 2, the only

available value for R. sibiricus is from an egg sac of 72-75 mm length.

organ is absent in Ranodon sibiricus (cf. Crawford and

Wake, 1998: 115), the presence of rudimentary bal-

ancers in the species appears possible. Regel (1968: 17,

see “pb” in her Fig. 7, transl. from Russian) wrote on R.

sibiricus larvae in developmental stage 3 (15-17 mm):

“On the lateral surface of the distal end of the palatino-

quadratum cartilage an excrescence develops, which is a

rudimentary proc. balancer (Rusconi’s hook)”. Although

balancers are not cartilaginous structures, Kuzmin and

Thiesmeier (2001: 43) quote this as an indication of

rudimentary balancers in Ranodon. Based on these

observations, we believe that at least rudimentary bal-

ancers will be found in B. gorganensis (and B. persi-

cusl), and we recommend further comparative investi-

gation with histological methods. Secondary loss of well

developed balancers may be an adaptation of the

“limnophilous mountain brook type” of larvae in B. gor-

ganensis / B. persicus (discussed in Stock, 1999: 237).

According to available data, balancers may be absent in

all species of Batrachuperus from China and Tibet

(Table 4).

In larvae eight days after hatching (d.a.h.) [stage 2-

3], the head had differentiated and forelimbs had a

shovel-like form, but only hind limb buds were visible.

The yolk sac regressed and was very small in larvae 14

d.a.h. (April, 2nd, 2003). In larvae 16-18 d.a.h. [stage 6-

7] (Fig. 2G-H), the yolk sac had disappeared, dark spots

became visible at the back, and the tail fin developed,

although development of the digits was incomplete

(April, 4, 2003). In larvae 24 d.a.h. [stage 8-9] (Fig. 21),

digits were well developed in forelimbs, but the toes of

hind limbs were still incomplete (April, 12, 2003). In

larvae 34 d.a.h. [stage 12] (Fig. 2J) the forelimbs were

completely developed, digits were clearly distinguish-

able, and tips of all digits and toes exhibited brown

homy claws. The ventral surface had a milky color, the

upper part of the tail and the tail fin showed dark spots,

and the eyes appeared completely developed. Through

time, the dark spots became more abundant at the tip of

tail, and the mouth. Darkly pigmented dots appeared on

part of the head and trunk, the flanks, the upper parts of

the tail, and the upper tail fin. At this stage, larvae were

fed with nauplius larvae of Artemia. In larvae 46 d.a.h.,

the belly remained spotless, but the flanks, dorsal body

parts and upper parts of the tail showed dark spots.

Larvae 62 d.a.h. exhibited brownish spots on the body

and dark spots became rarer (larger larvae had golden

dots on the gills and on parts of the body). The anterior

part of the upper tail fin extended to the occiput.

In addition to the clutches described above, more

than 20 large larvae with a total length of almost 10 cm

were collected in the leaves of the breeding pond, but

only one adult specimen was found. The pond was

searched completely, but no larvae smaller than about 10

cm were found. Therefore, we conclude that all these

large larvae apparently stemmed from the preceding

year. The growth rate data of the larvae hatched from the

clutches in our laboratory fit well with the later develop-

mental stages reported by various previous authors from

natural habitats (summarized in Stock, 1999: Tab. 3).

Table 4. Number of eggs per sac, number of egg rows per cross section and presence of a balancer of eight hynobi-

id species, comparison of available data; same sources as in table 2, except for B. lorigdongensis in which the char-

acter was inferred from the ovary of voucher MVZ 208610.

Vol. 10, p. 173

Asiatic Herpetological Research

2004

dis-

tance

min. max snout number

eye dist. hind distance hight to ant. of rec-

total head body body tail head diame- eye to foreleg leg between dorsal point ognized mass

2004

Asiatic Herpetological Research

Vo). 10, p. 174

Table 5 (previous page). Morphometric data on early larvae of Batrachuperus gorganensis.

d.a.h. = days after hatching; SD = standard deviation; Min = minimum; Max = maximum;

N = number of larvae measured (the value in parentheses shows from how many clutches the measured larvae orig

inated)

According to these studies, larvae from the first season

may reach a total length of 30 to 62 mm (persicus,

between June and August) and 41 to 50 mm {gorganen-

sis, mid of June), respectively, and must overwinter

before they form “large larvae”, which can enter meta-

morphosis in the following year.

Conclusions and Future Research

Our initial studies support the relationship of the three

taxa Ranodon sibiricus, Batrachuperus mustersi and the

Iranian hynobiid(s), i.e. B. persicus and B. gorganensis.

These taxa have apparently more features in common

than with the Batrachuperus taxa East of Tibet. In addi-

tion to the essential need for molecular data, it would be

valuable and interesting to study egg deposition in the

natural habitats in more detail and to collect data

throughout the range of the Iranian hynobiid salaman-

ders, especially from the central and western portions.

During proof reading, one of us (HGK) provided infor-

mation that MMTT 452, 453, and 454 are eggs of B. per-

sicus, found near the road from Asalem to Khalkhal, col-

lected May, 20, 1975, by M. Thireau, R. Khazaie and R.

G. Tuck.

Acknowledgments

M. E. and H. G .K. wish to thank G. Yolmeh for provid-

ing material and initial information on the spawning

pond, as well as G. Soltanpour for help during the field

work. M. S. thanks David Wake for references and

advice, Tate Tunstall for translation from Chinese, S. L.

Kuzmin for data on R. sibiricus, G. Wogan and J.

Vindum for references, Robert Hijmans for cartographic

support, J. Robert Macey and Theodore Papenfuss for

permission to include unpublished information about

relationships of Hynobiidae, Joao Alexandrino for talk-

ing about natural history, James Parham for (im-)

patience with the final version of the manuscript, and

Robert Bingham for checking the English.

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Reilly, S.M. 1983. The biology of the high altitude sala-

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Reilly, S.M. 1987. Paradactylodon : a junior synonym

for Batrachuperus. Amphibia-Reptilia 8:283-284.

Schmidtler, J.F., and J.J. Schmidtler. 1971. Eine

Salamander-Novitat aus Persien. Batrachuperus

persicus. Aquarien-Magazin 11:443-445.

Sparreboom, M. 1979. [Eggs of Batrachuperus muster-

si ]. Lacerta 37(5):83-88 (In Dutch).

Steiner, H.M. 1973. Beitrage zur Kenntnis von

Verbreitung, Okologie und Binomie von

Batrachuperus persicus (Caudata, Hynobiidae).

Salamandra (Frankfurt/M.) 9(1): 1-6.

Stock, M. 1999. On the biology and the taxonomic sta-

tus of Batrachuperus gorganensis Clergue-Gazeau

et Thorn, 1979 based on topotypic specimens

(Amphibia: Caudata: Hynobiidae). Zoologische

Abhandlungen des Staatlichen Museums fur

Tierkunde Dresden 50(1 4):2 17-241.

Thom R., and J. Raffaelli. 2001. Les Salamandres de

FAncien Monde. Boubee, France, 449 pp. [partly

revised version of the original publication 1968].

Zhao, Er-mi, and Qixiong Hu. 1988. Studies on Chinese

tailed amphibians. Pp. 1-43. In Er-Mi Zhao (ed.)

Studies on Chinese salamanders. Contributions to

Herpetology, no. 4. Society for the Study of

Amphibians and Reptiles, Oxford, Ohio.

Histochemical Characterization of the Lingual Salivary Glands of the

House Gecko, Ptyodactylus hasselquistii (Squamata: Gekkonidae)

Bashir M. Jarrar and Noory T. Taib

Zoology Department, College of Science, King Sand University, P.O.Box 2455, Riyadh 11451 Saudi Arabia.

Abstract. - Histochemical investigations of the lingual salivary glands of the house gecko, Ptyodactylus hasselquistii

have been conducted. The glands are comprised of mucous and mucoserous cells. Mucous cells secrete or elaborate

neutral mucosubstances, neuraminidase sensitive carboxylated mucins, hyaluronidase resistant sulfomucins, but are

devoid of proteins. The mucoserous cells secrete and elaborate neutral mucosubstances and glycoproteins but are

devoid of sialomucins and sulfomucins. The results are discussed in the context of the feeding habits and phylogeny

of reptiles.

Key words. - Histochemistry, lingual, salivary glands, house gecko, Ptyodactylus hasselquistii, Gekkonidae.

Introduction

Histochemical studies on the lingual salivary glands of

vertebrates have mainly been concerned with mammals,

whereas little attention has been paid to the lingual sali-

vary glands of non-mammalian vertebrates. Most stud-

ies on the lingual salivary glands of reptiles have

focused with morphological and histological aspects

while few histochemical studies have been carried on

these glands (Raynaud, 1961; Gabe and Saint-Girons,

1969; Lopes et al., 1982; Taib and Jarrar, 1985a; 1985b;

1985c; 1986; Taib, 1986, Asgah et al., 1990).

Nevertheles, the literature on the lingual secretions of

lizards is rather scanty and their consitituents have yet

to be determined.

The present study is a detailed histochemical char-

acterization of the lingual salivary glands of the house

gecko, Ptyodactylus hasselquistii.

Materials and Methods

Twenty adults of each male and female house gecko

Ptyodactylus hasselquistii were trapped from different

houses in Riyadh city, Saudi Arabia. They were killed by

etherization and the whole tongue was removed from

each animal and quickly immersed for 24 hrs in one of

the following fixatives: neutral buffered formalin,

Bouin's fluid and Gendre's fluid. They were then thor-

oughly washed in running water, processed for serial

sectioning at 4-5 pm thickness and the sections were

stained with haematoxylin-eosin or with Mallory

trichrome for histological examination, whereas the sec-

retary cells of the glands were characterized by the cri-

terion of Gabe and Saint-Girons (1969). Other sections

were used for the following histochemical reactions:

Neutral mucosubstances. - Periodic acid-Schiff (PAS)

technique (Gurr, 1962), PAS after diastase digestion

(McManus and Mowry, 1964), PAS after alpha-amylase

digestion (Luna, 1968), PAS after acetylation blockade

(McManus and Cason, 1950), PAS after acetylation-

saponification (Oxello et al., 1 958), PAS after phenylhy-

drazine treatment (Spicer et al., 1967) and PAS after

treatment with chloroform and methanol.

Acid mucosubstances. - Alcian blue (AB) at pH 2.5,

1.0, and 0.4 (Mowry, 1956; Luna, 1968).

Distinction between acidic and neurtal mucosub-

stances. - AB (pH 2.5)-PAS (Mowry and Winkler, 1956)

and AB (pH 1.0)-PAS (Spicer et al., 1967).

Distinction between sulfomucins and sialomucins. -

Aldehyde fuchsion (AF) and AF-AB, pH 2.5 (Spicer and

Meyer, 1960); weak (25°C, 16 hr), mild (37°C, 4hr) and

strong (60°C h hr) methylation-saponification- AB (PH

2.5) (Spicer, et al., 1967); toluidine blue (TB) buffered at

pH 1.7 and 3.4 (Landsmeer, 1951), critical electrolyte

concentration (CEC) technique for extinction of

alcianophilia at pH 5.6 in the presence of gradual con-

centation of Mg2+ (Scott and Dorling, 1965).

Enzyme digestion tests. - Diastase-PAS technique

(McManus and Mowry, 1964); neuraminidase

(Sialidase, Vibrio chlolerae, type V)-AB (pH 2.5)

(Spicer and Warren, 1960); hyaluronidase (testicular)-

AB (pH 2.5) (Spicer et al., 1967). Ribonuclease diges-

tion (Love and Rabotli 1963); neuraminidase-TB (pH

3.7), hyaluronidase-TB (pH 2.0) were employed. In

each case control sections were incubated for the same

length of time at the same temperature in buffer solu-

tions without the enzyme.

Vol. 10, p. 177

Asiatic Hcrpetological Research

2004

Figure 1. Lingual glands of P hasselquistii after staining

with haematoxylin-eosin. Note that the mucous cells of

the lingual glands are located in the papillar space of the

papillae. x950.

Figure 2. Lingual glands of P. hasselquistii after staining

with PAS. The reactivity of the glands confirms the pres-

ence of the neutral mucosubstances. x950.

Figure 3. Lingual glands of P hasselquistii after staining

with AB (2.5), confirming the presence of sialomucins

and sulfomucins. x950.

Figure 4. Lingual glands of P. hasselquistii after staining

with AB (I.O)-PAS. The bluish purple color indicates the

presence of neutral and sulfated mucosubstances simul-

taneously. x950.

Figure 5. Lingual glands of P. hasselquistii after staining

with CEC at 0.3M Mg++, confirming that the mucosub-

stances produced by the glands contain carboxyl and

sulfated groups. x950.

7- •

Figure 6. Lingual glands of P. hasselquistii after staining

with MBPB, indicating the protein contents of the glands

secretion. x700.

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Asiatic Herpetological Research

Vo). 10, p. 178

Proteins. - Mercuric bromophenol blue method (Mazia

et al., 1953); ninhydrin-Schiff (Yasuma and Itchikawa,

1953), mercuric-bromophenol blue (MBPB) and PAS

after trypsin digestion (Pearse, 1972).

Photographs. - Photographs were taken with a 35mm

Zeiss Ikon camera on Kodacolor NR 100 film.

Results

The lingual salivary glands of the house gecko,

Ptyodactylus hasselquistii occupy the papi liar invagina-

tion of the posterior two-thirds of the dorsal surface

together with the lateral sides of the tongue. The anteri-

or part of the tongue is devoid of any glandular structure

and covered by keratinized squamous epithelium. These

glands are made of mucous cells located in the inner

papillar space of the filiform papillae (Fig. 1) together

with simple tubular structures made of mucoserous cells

seen at the most posterior part of the dorsum. The

mucous cells have an alveolar cytoplasm and flattened,

basally located nuclei with clear apical ends resting on a

delicate basement membrane.

As summarized in Table 1, the mucous cells of the

lingual glands of P. hasselquistii exhibited strong PAS

reactivity (Fig. 2) which was neither labile to alpha-

amylase nor to saliva digestion but completely lost by

phenylhydrazane treatment. Flowever, this reactivity

was completely blocked by acetylation and was partly

restored by deacetylation-PAS sequential techniques.

They showed marked alcianophilia at both pH 2.5 (Fig.

3) and 1 .0 but to lesser extent at pH 0.4. They also react-

ed with both PAS and AB and stained bluish purple with

AB (2.5)- PAS and AB (1.0) PAS (Fig. 4). These glands

also reacted with AF as well as with AF-AB (2.5) and

AF-AB ( 1 .0). The alcianophilia of the glands was part-

ly lost at pH 2.5 with acid hydrolysis and weak methy-

lation and there after restored by saponificiation tech-

niques. They demonstrated alcianophilia with the CEC

techniques at 0.1M, 0.2M, and to some extent at 0.3M

Mg2+ (Fig. 5) and showed metachromasia at pH 3.4 and

1.7 but reacted negatively to all protein detection tests.

The mucoserous cells of the glands showed PAS

reaction, exhibited no alcianophilia at pH 2.5 and 1.0

and were orthochromatic at pH 3.4 and 1.7 but reacted

positively to all protein detection tests (Fig. 6). No sex-

ual dimorphism was observed in the lingual secretion of

the species under study.

Discussion

The lingual salivary glands present great diversity in

morphology amongst the various groups of reptiles.

These glands are entirely absent from Varan idae.

Amphisbaenia, Ophidia and some species of Cheloma

such as Chelonia mydas (Kochva, 1978). On the other

hand, these glands are simple consisting of three differ-

ent types of goblet cells in most species of Testudinidae

(Nalvade and Varute, 1976; Taib and Jarrar, 1984).

Some lizard possess mainly goblet cells together with

simple tubular glandular structures in their tongues

(Nalvade and Varute, 1976; Shevliuk, 1976; Taib and

Jarrar 1985 b; 1985c and 1986), while others have more

developed lingual salivary glands as seen in some

Agamidae, Iguanidae, Gekkonidae, Anguidae and

Chamaleonidae (Gabe and Saint-Girons, 1969; Kochva,

1978; Asgah et al., 1990). On the bases of the results of

the present study and in view of the criterion of Gab and

Saint-Girons (1969), the lingual salivary glands of

Ptyodactylus hasselquistii are made ot unicellular

mucous goblet cells lining the dorsal epithelium of the

tongue with mucoserous simple tubular glandular appa-

ratus at the base of the tongue. The structure of the lin-

gual salivary glands of P. hasselquistii is different from

those of Tupinambis teguixin , Agama blandfordi,

Uromastyx microlepis, Acanthodactylus schmidti and

Scincus mitranus , which have only mucous cells in their

lingual glands (Lopes et al, 1974; Taib and Jarrar,

1985b; 1985c; 1986; Taib, 1986). According to Gabe

and Saint-Girons (1969), the lingual glands are mucous

in Gekkonidae, mucoserous on Sphenodontidae,

Anguidae and Pygopodidae, but seromucous in

Chamaleonidae and serous in some speices of Iguanidae

and Agamidae. The grading from non-glandular tongues

through unicellular with or without simple tubular glan-

dular structure to only simple tubular and to then tubu-

lo-alveolar ones may reflect developmental stages

towards the definitive lingual glands of higher verte-

brates (Shevliuk, 1976; Kochva, 1978).

A tentative interpretation of the types of mucosub-

stances in the lingual glands of P. hasselquistii can be

made from the results of the different histochemical

reactions used in the present investigation and from the

classification of mucosubstances proposed by Mowry

and Winkler, 1956; Spicer and Meyer, 1960; Scott and

Dorlling, 1965; Pearse, 1972). Neutral mucosubstances

are PAS positive, diastase resistant, as well as unstain-

able by cationic dyes. Acetylation produces derivatives

of primary and secondary amines which prevent 1, 2

glycol groups, from reacting with PAS indicating the

presence of neutral mucosubstances or sialic acid, sepa-

rately or simultaneously. Alcian blue is generally con-

sideied as being specific for identifying acid mucosub-

stances where alcianophilia at pH 2.5 and 1 .0 is specific

tor sialomucins and sulformucins respectively (Mowrv

and Winkler, 1956). In the combined aldehyde fuchsin-

alcian blue sequential techniques, sulfomucins stain pur-

ple blue and sialomucins blue (Spicer and Meyer. 1960)

Vol. 10, p. 179

Asiatic Herpetological Research

2004

Table 1. The histochemical reactions in the lingual salivary glands of Ptyodactylus hasselquistii.

Reactions: - negative; ± weak; +, moderately positive; ++, intensely positive; Cb, complete blockade; M,

mild; Pb, partial blockade; Nb, no blockade; S, strong; TB, toluidine blue; W, weak.

Colors: B, blue; Bp, bluish purple; P, pink.

Glands: MC, mucous cells; MSC, mucoserous cells.

Sialomucins can be identified by alcianophilia at pH 2.5

which is partially lost following acid hydrolysis and

completely removed after neuraminidase digestion, but

neuroaminidase did not affect the staining of sulfated

mucosubstances. A loss of alcianophilia after

hyaluronidase digestion is due to the removal of

hyaluronic acid and chondroitin sulfates. Methylation

blocks subsequential stainig of simple mucosubstances

by esterification of carboxyl groups and complex sulfat-

ed mucosubstances desulphation. Subsequent treatment

with potassium hydroxide (saponification) after methy-

lation will restore the staining of carboxyl groups (Drury

et al., 1967). The mucosubstances that are stained at

0. 1 M MgCl2 in the CEC reaction, but not at 0.2M MgCl2

are believed to contain carboxyl group and no sulfate

groups. Sulfated mucosubstances, on the other hand,

stain strongly and selectively at 0.2M Mg2" but lose

their alcianophilia at different levels with increasing

MgCl2 concentration (Spicer and Lillie, 1960). The lin-

gual glands of the species under study resisted trypsin

digestion and the action of (chloroform-methanol)

which excludes the possibility of lipids and proteins.

Accordingly, the lingual salivary glands of of the house

gecko, Ptyodactylus hasselquistii contain neutral muco-

substances, sialadase labile carboxylated mucosub-

stances and hyaluronidase resistant sulfomucins and gly-

coproteins.

The lingual secretions of P. hasselquistii are differ-

ent from those of some lizards such as Tupinambis

teguixin and Agama blandfordii which contain neutral

2004

Asiatic Herpetological Research

Vol. 10, p. 180

mucosbstances and sialomucins but no sulfomucius

(Lopes et al., 1974; Taib and Jarrar, 1985c). They also

differ from the secretions of the lingual glands of

Uromastyx microlepis, Acanthodactylus schmiditi,

Scincus mitranus and Stenodactylus slevini which con-

tain neutral mucosubstances, sialomucins and sulfor-

mucins but no glycoprotein (Taib and Jarrar, 1985b,

1986; Taib, 1986; Asgah et al., 1990). Neutral mucosub-

stances have been demonstrated in the secretions of all

studied reptiles that possess salivary glands while phylo-

genetically, the absence of sulfomucins in the lingual

glands would favour the concept that sialomucins secre-

tive cells are more primitive than sulfated mucosub-

stances secretive ones. In addition, the heterogenous his-

tochemical recactivity of the lingual glands might have

appeared in the evolutionary lines of reptiles to meet the

different changes in the feeding habits of various

species. Neutral mucins were present in the lingual

glands of almost all studied reptile species while sialo-

mucins together with neutral mucosubastances were

identified in the lingual glands of all insectivorous rep-

tiles so far studied (Nalvade and Varute, 1972; Taib and

Jarrar, 1985c, 1986; Taib, 1986). The lingual glands of

all insectivorous and carnivorous reptiles studied thusfar

exhibited sulfomucins. More work is needed to elucidate

whether the lingual secretion diversity of reptiles imply

phylogenetic relationships or different feeding habits.

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2004

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Vol. 10, pp. 182-190

The Biology of the Persian Mountain Salamander, Batrachuperus persicus

(Amphibia, Caudata, Hynobiidae) in Golestan Province, Iran

Haji Gholi Kami

Department of Biology, Faculty of Sciences, University of Agricultural Sciences

and Natural Resources, P O. Box 49165, Gorgan, Iran.

Abstract. - The Persian Mountain Salamander, Batrachuperus persicus, is a hynobiid endemic to Iran and is distrib-

uted in specific localities of Hyrcanian forests in four northern provinces of Iran. The biology of this salamander was

studied at four localities in Golestan Province of Iran, especially in Shirabad Cave, between 1996 and 1999.

Information is presented about the cave and other localities. This salamander has four fingers and toes. The larval

stages of the salamander are found at all times of year and probably don't transform during the first year. The head

form of small larvae is wider posteriorly while the head form of large larvae, juveniles and adult specimens is more

or less rectangular. Juveniles have more yellow spots than adults. Juvenile and adult specimens are found inside and

outside of water in the cave but in other localities they can be found in burrows around springs and are not active dur-

ing the day. They feed on larval and adult forms of insects and other arthropods. Adults also feed on small specimens

of bats ( Myotis blythyii) inside of the cave. Some large specimens are cannibalistic and feed on larvae and juveniles

of B. persicus in natural habitats and in the laboratory. This species does not hibernate inside the cave and is active

all times of the year. The total length of the longest specimen was 268.5 mm.

Key words. - Amphibia, Hynobiidae, Batrachuperus persicus, Iran.

Introduction

The Persian Mountain Salamander, Batrachuperus per-

sicus Eiselt and Steiner 1970, was described based on

five salamander larvae collected near Asalem in the

Talesh Mountains in Gilan Province of Iran (Eiselt and

Steiner, 1970) (See editorial note and Ebrahimi et al.,

2004). Subsequently J. J and J. F Schmidtler collected

some larvae in Weyser, southeast of Chalus, in

Mazandaran Province, Iran, in 1970. These transformed

in captivity and a brief description of juvenile specimens

was presented (Schmidtler and Schmidtler, 1971).

Primary information was presented on adult specimens

in Ardabil Province of Iran (Baloutch and Kami, 1995).

New distribution records were published some years ago

(Kami and Vakilpoure, 1996). Adult specimens of this

species were described for the first time together with

their habitats in Gilan and Ardabil provinces of Iran

(Kami, 1999).

The biology of this salamander has been studied in

the laboratory and in natural habitats especially in

Shirabad Cave of Khanbebain. Students of Gorgan

University and I have visited Shirabad Cave twelve

times between 1996 and 1999. Detailed information on

the other localities is sparse and these localities must be

studied more in the future.

Study areas. - Batrachuperus persicus is distributed in

the four northern provinces of Iran (Fig. 1). Figure 2

shows new localities of Batrachuperus persicus in

Golestan Province. Most of the research was done at

locality 1 (Shirabad Cave), other localities were visited

only one time. Climatic information for five cities of

Golestan Province is summarized in Table 1 .

Locality 1. Shirabad Cave- Shirabad Cave (36° 57' N,

55° 03' E) is situated 70 km East of Gorgan, southeast of

Khanbebain and Shirabad Village at about 420 m above

sea level (Fig. 3, 4). The cave and waterfalls were desig-

nated as a National Park by the Department of

Vol. 10, p. 183

Asiatic Herpetological Research

2004

Tab 1. Summary of climatic information (15 years) in five cities of Golestan province of Iran.

Figure 2. Localities of of Batrachuperus persicus in Golestan Province, Iran: 1- Shirabad Cave, 2 - Vantakhteh; 3- Near

Shirabad Cave; 4- Spring of Khouklou; 5- Barankouh (36° 45' N, 54° 25' E), about 10 km south west of Gorgan, almost

1100 m elevation; 6- Spring of Khonakou, situated south southwest of Gorgan, Jahannama Protected Area, Valley of

Sorkhcheshmeh, below elevations of Pir-e-zan (elevations of Pahlavan Ghaleh), 1800 m elevation; 7- elevations of

Yakhkesh (36° 42' N, 54° 23' E) about 15 km south of Gorgan, 2300 m elevation; 8- Water falls of Shirabad; 9- Valley

of Loushan, inside of valley, (36° 42' N, 54° 41' E) about 30 km southeast of Gorgan; 10- Region of Aram-e-

Sorkhcheshmeh opposite side of Siah Marzkouh, Village of Aliabad. Circles are cities: 1- Gorgan; 2- Aliabad; 3-

Ramian; 4- Azadshahr; 5- Gonbad-e-kavous; 6- Minoudasht; 7- Kalaleh.

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Vol. 10, p. 184

Table 2. Dates of study, air and water temperature of four

localities in Golestan province of Iran.

37°00

Environment of Gorgan and Gonbad-e-Kavous in 1998.

There are seven waterfalls below the cave. The entrance

of the cave is about 15 m high and is at least 3-4 m high

in other parts of the cave. It is almost 240 m long and is

completely dark. Water emerges from the mouth of the

cave and flows to the river and waterfalls at all times of

the year.

No plant species live inside the cave, but there is

Lycopodium sp on the floor of cave from the entrance to

about 10 m inside of it on large flat stones. Some plant

species that were identified outside the entrance of the

cave on 28 February 1997 and 17 April 1997 are:

Pteridum aquilinum, Adianthum capillus-veneris,

Athyrium flix-mas, Phyllitis scolopendrium, Funaria sp,

Celtis australis, Evonymus latifolia, Convulvulus

(=Calistegia) sepium, Hedera pastochowii, Lamium

album, Carex pendula, Rubus hyrcana, Ficus carica,

Danae recemosa, Acer insigne, Parrotia persica,

Carpinus betulus Cyclamen elegans, Marcantia sp.

The water temperature of cave is 10-13°C (Mean

1 1 .6°C) and is constant from the entrance to end of cave.

Air temperature of cave varied between 1 2.5-2 1°C over

six visits. The inside of the cave is a little warmer than

the entrance of the cave (Table 2).

Locality 2. Vantakliteli. - The Spring of Vantakhteh (36°

40' N, 54° 25' E ) is about 1 8 km south of Gorgan City

and 5 km southwest of Ziarat Village at about 1200-1300

55°00'

+

55°05'

+

37°00'

kouh-e-NargesI

0 331 m

Daland water resource

To Khanebain

\

\__ Shirabad village

Figure 3. That National park that includes the cave and

waterfalls of Shirabad (1650 Hectares).

m elevation. Salamanders were observed in this locality

in 1979 and later in Yakhkesh (2300 m elevation) on 25

November, 1999. There are two springs in this locality

that are formed from soil and limestone and situated to

east. Water flows from springs to the Souteh River.

The sides of the river were frozen and snowy. The

springs are 3-4 m above the river. Water temperature of

one spring was 6.5 and other 7°C. Air temperature was

6°C at 13:30 and 2°C at 15:30. Snow was melted in east

side of the springs. Some plant species found around the

springs are as follows: Rosa albicans, Berberis vulgaris,

Juniperus communis, Carpinus orientalis, Juncus

effusus, Circium nekarmanicum, St achy s bizantica. Five

salamanders, all metamorphosed, were found inside of

burrows near the springs.

Locality 3. Near Shirabad Cave. - Locality 3 is a small

pond (about 2m x 2m) in southwest of Shirabad Village

and 20 m above Shirabad Cave. Water depth was almost

50 cm. Around this shady pond were stones, lichens and

trees {Danae racemosa, Quercus sp). A Grass Snake

(Natrix natrix), Marsh Frogs (Rana ridibunda), crabs

{Potamon sp.; and larvae of Batrachuperus persicus

with total length of 3-4 cm were observed. No adult or

metamorphosed salamanders were seen. Air temperature

was 20-23. 5°C and water temperature was 19°C at 1000

on 10 July 1997. Some larvae such as Gerridae

(Heteroptera), Chironomidae (Diptera), Ephemeroptera,

and Amphipoda (Gamaridae), earthworms

(Lumbricidae), and Gastropoda were collected inside

and around the pond under decaying logs.

Vol. 10, p. 185

Asiatic Herpetological Research

2004

Table. 3. Measurments of living Batrachuperus persicus inside of Shirabad cave of Golestan province of Iran. All spec-

imens were released after measuring. All measurements are in mm.

2004

Asiatic Herpetological Research

Vol. 10, p. 186

Locality 4. Spring of Khouklou. - The Spring of

Khouklou (36° 44' N, 54° 53' E) is situated almost 23 km

south of Aliabad at about 1500 m elevation. This spring

is 200 m west of Chenarbin and along side of the

Khouklou River and situated to north beneath a large

rock. This locality was studied on 26 May 1999. Six

specimens were seen and three of them were collected.

All specimens had external gills.

Materials and Methods

Shirabad Cave was studied 12 times and the other local-

ities only one time between 1996 and 1999. Air and

water temperature of the cave and two other localities

measured on some dates. Important plant species of

localities were identified. Measurements (total, head,

trunk, and tail lengths) were done on living specimens of

salamanders inside the cave. Some specimens (larval

and transformed) collected and brought to aquaria at the

zoology laboratory of Gorgan University and kept with

ice. Some specimens (30) were fixed in alcohol or for-

malin. Almost all fixed transformed salamanders were

dissected and stomach contents and sexes were noted.

Morphometric and meristic characters of specimens

were taken. The behavior of salamanders was studied

inside the cave and in the laboratory. On each visit the

total number of salamanders was counted from the

entrance to the end of the cave.

Preserved specimens of Batrachuperus persicus

studied for this research are as follows: ZMGU 67, 273,

Shirabad Cave collected by H. Naghghash and M.

Rahmani in 1994; ZMGU 246, 281, 282, 283, 284, near

Shirabad Cave collected by H. Kami, A. Maghsoudlou,

M. Rahmani, M. Azma on 10 July 1997; One specimen

without number collected in Shirabad Cave by A.

Maghsoudlou on 8 May 1998; ZMGU 267, Shirabad

Cave, collected by A. Maghsoudlou on 21 May; ZMGU

266, 268, 269, 270, 272, 285, 286, 427, 428, 429, col-

lected by H. Kami, M. Fatemi, N. Okhli, N.

Moghaddam, J. Ghasemi, M. Mahmoudi, R. Zakeri, on

19 May 1998; ZMGU 275, 430, Shirabad Cave, proba-

bly collected by H. Kami, S. Afzali, R. Ghaemi on 28

February 1997; ZMGU 276, Jahannama Protected Area,

south of Gorgan and Ziarat Spring of Khonakou, collect-

ed by N. Torbatinejad on 10 June 1997; ZMGU: 277,

278, Vantakhteh, collected by H. Kami, S. Afzali, M.

Firouznia, H. Rezaee, Y. Shakoumahalli, Y. Nariman, on

25 November 1996; ZMGU 279, 280 without correct

information (probably Vantakhteh or Shirabad); ZMGU

333, 335, Shirabad Cave, collected by M. Goli, S. Afzali

and eight other students of Gorgan University on 27

April 1999; ZMGU 343, Spring of Khouklou, collected

by H. Absalan, S. Hosseini, on 26 May 1999.

Vol. 10, p. 187

Asiatic Herpetological Research

2004

o

Is-

CN

Z>

o

N

Cl)

o

c

>

o

X2

0

T3

<

E

in

h"

=)

o

N

c

03

O — -

0-g

O 03

o I'

Q-S

0 Jl>

00

0

O

o

c

E

0

oo

o _0

CO =3

0

03

^ TO

<q o

? 0

0 ■-

Q_ II

O c

■Sl

03 O

-fc 0

0 *“

QQ j-'

o ^

Is

O 0

=3

"o ■g

ro >

o

CO 0

0 *7.

m ^

2 5

0 o

<-> 0

O C

To c6

>- 0

0 <-

c II

e™

0 c

g ro

i- 0

0 2

E c

o 0

f!

o 0

*> ^

in -o

<d.9>

_ i_

-Q T3

lE 0

Table 6. Summary of information on the feeding of B. per-

sicus in Golestan province of Iran. ZMGU 75 is from

Ardabil province.

Results

Measurements of specimens from the localities are pre-

sented in Table 3. Morphometric and ineristic characters

of preserved salamanders are summarized in Table 4 and

Table 5. The maximum total length of this species

expected 15-20 cm (Schmidtler and Schmidtler 1971).

The total length of the longest specimen was 268.5 mm.

Description of larvae. - In small larvae (Total length less

than 80-100 mm), the head is large, depressed, more or

less triangular with rounded end anteriorly, wider poste-

riorly, with small eyes and poorly developed eyelids;

black horny margin present in lower jaw; gills large;

vomerine tooth-bundle arc-shaped, situated anterolater-

ally, and extending in front of the choanae, short, in the

middle hardly discernibly separated from one another.

Trunk with 11-14 costal grooves, vertebral groove often

present, forelimbs are longer than hind limbs, tips of fin-

2004

Asiatic Herpetological Research

Vol. 10, p. 188

Figure 4. A- One of seven waterfalls of Shirabad Cave (Golestand Province, Iran). Batrachuperus persicus are found

in the water near the edges of the pond (Photo by R. Ghaemi 2/28/97); B- The entrance of Shirabad Cave (Photo by

R. Ghaemi 2/28/97); C- Myotis blythyi, an abundant bat species of Shirabad Cave and one of the food items of

Batrachuperus persicus ; D- Larval specimen of Batrachuperus persicus from Shirabad Cave collected 2/28/97 (Photo

by A. Sanee 3/11/1997); E- Juvenile specimen of Batrachuperus persicus about 10 days after metamorphosis.

Collected from Shirabad Cave 2/28/97 (Photo by A. Sanaee 4/8/97).

gers with black homy pads, their arrangements are

3>2>4>or<l; arrangement of toes are often 3>2>4>1;

adpressed limbs not overlapping; tail highly compressed

from laterally, upper caudal fin very distinct, reaching to

occiput in some specimens, lower caudal fin reaching to

posterior of cloaca, cloacal aperture is oval or elliptical.

In larger larvae the head is more or less rectangular,

adpressed limbs overlapping, upper and lower caudal

fins not clearly distinct. The 12 larvae specimens exam-

ined (fixed or living) in this study (see Tables 3, 4) have

a tail length which is smaller (Table 4) or longer (Table

3) than the head plus body length.

Description of juveniles. - Head more or less elliptical,

decreasing toward the rear, adpressed limbs overlap-

ping, upper and lower caudal fins are not distinct, tail

more or less rounded especially at base of it. Four juve-

nile specimens examined in this study (see Tables 3, 4),

have a tail length which is often smaller than the head

plus body length.

Description of adults. - Head form is more or less rec-

tangular, or wider anteriorly. Eyelids well developed and

movable, width of eyelid is less than distance of inter-

eyelids (interoculars), distance of external nostrils are

longer than distance of nostril to anterior of eye, nostrils

are semi-circle; vomerine tooth-bundle is different from

that of larvae, inner portion of it is longer than outer one.

Trunk with 11-14 costal grooves, adpressed limbs over-

lapping. Tail compressed laterally in some specimens

and with thin upper and lower caudal fins, and in some

specimens more or less rounded especially at base.

Cloacal aperture is longitudinal and in some specimens

cross-shaped, and longitudinal protuberance is present

inside of cloaca in others. The 16 adult specimens exam-

ined in this study (see Tables 3, 5) have a tail length

which is longer than head plus body length except two

specimens (ZMGU 273, 335) which have tail lengths

smaller than head plus body length.

Coloration - Small larvae (Total length 40 mm) are in

general light yellow without any distinct spots; dark

eyes very distinct in small larvae, larger larvae have

irregular dark gray spots, ventral portion of larvae light

and without spots; dorsum of ZMGU 285 is dark gray;

Iris yellowish, pupil dark, bases of all limbs yellow^e!-

low color of forelimbs not reaching to knee but in

hindlimbs reaching to knee. Yellow spots of larvae are

Vol. 10, p. 189

Asiatic Herpetological Research

2004

more than in adults. Juveniles are darker than larvae.

Yellow spots are less in adult, and ZMGU 269 is deep

violet and have only one yellow spot beside of vertebral

groove. Yellow spots of adults are often in vertebral

groove.

Feeding. - Batrachuperus persicus feeds on larvae and

adult forms of some orders of insects and probably other

arthropods. They also feed on bats ( Myotis blythyi) in

Shirabad Cave (Fig. 4). Some specimens are cannibalis-

tic and feed on smaller specimens of B. persicus espe-

cially in captivity. Algae, that may be eaten with other

insects, was found in one larva. Stomach is white with a

thin wall. Total length of digestive system of ZMGU 267

was 337 mm from anterior of stomach to posterior of

cloaca. Contents of stomachs of some dissected B. per-

sicus are shown in Table 6.

Behavior. - Small larvae and adult large salamanders are

usually almost motionless inside of cave. They have no

reaction to light. Adults escape to water. Adults swim

more slowly than larvae under water. Adults are active in

Shirabad Cave in all times of year but in other localities

are not active during the daytime.

Parasites. - Many nematodes and mastigophorans were

found inside the cloaca of one salamander from locality

2. Some nematodes moved freely and some were inside

of a cyst.

Metamorphosis. - Larvae are found at all times of the

year in Shirabad Cave and probably don’t transform dur-

ing the first year. A newly transformed juvenile was

found on February 25 1997. Larvae transform rapidly in

captivity probably as a result of starvation and higher

temperature.

Habitat. - Batrachuperus persicus was studied in four

localities and observed in some other localities in

Golestan Province of Iran. Larvae were found inside of

small shady ponds. Juveniles and adults were found

inside and outside of water in Shirabad Cave but in other

localities live in borrows about 20 cm long. Some spec-

imens found above stones, and some in grooves of

stones near water in Shirabad Cave. One specimen was

1 meter away of water and moved 0.5 meter on the stone

which was in an almost vertical position.

Measurements. - Measurements are summarized in

Tables 3, 4, and 5. Total length of the smallest larvae was

36.2 mm and of the longest one was 105 mm. Juveniles

are smaller than the largest larvae. Total length of the

longest adult was 268.5 mm.

Distribution. - Batrachuperus persicus collected or

observed by students of Gorgan University, staffs of

Department of Environment of Gorgan and Gonbad-e-

Kavous, and by me in many localities in Golestan

Province of Iran. These localities are listed on figure 2.

Discussion

These salamanders are active at all times of year in

Shirabad Cave, but in other localities found in borrows

of near of springs during daytimes and are probably

active at night. Larval salamanders have morphological

adaptations that correlate with the environments that the

larvae inhabit (Noble 1927 in Petranka 1988). One

dichotomy is that between species that typically breed in

running versus standing water habitats. In this division

larvae of Batrachuperus persicus are “stream-type” lar-

vae. A third group of aquatic larvae (“mountain brook”

larvae) was recognized by Valentine and Dennis (1964)

that is perhaps better viewed as an extreme form of the

stream-type morphology (Petranka, 1998). It is better

recognized larvae of B. persicus to this type of larvae.

Feeding on bats by adults of B. persicus may be unique

in the world of salamanders.

Acknowledgments

I am much indebted to N. Okhli for various assistance in

the field and in laboratory and typing the manuscript. I

would like to thank the students of Gorgan University

(M. Sabbaghpour, R. Ramezani, S. Afzali, S.Ashrafi, R.

Zakeri, M. Azma, M. Rahmani, H. Naghghash, G.

Daryanabard, H. Zohouri, A. Sanaee, A. Maghsoudlou,

M. Mahmoudi, J. Ghasemi, M. Goli) for their coopera-

tion during field work in Golestan Province and for tak-

ing the photographs. Thanks to staffs of Department of

Environment of Gorgan and Gonbad-e-Kavous especial-

ly R. Ghaemi, M. Firoznia Y. Shahkoumahalli and H.

Abslan for their cooperations. I am grateful 1 to N.

Abbasy and M. Fatemi, N. Moghaddam for identifica-

tion of plants and A. Abdoli for identification of water

insects. I am also thankful to T. Papenfuss, Museum of

Vertebrate Zoology, University of California, Berkeley,

for all his recommendations, encouragements, and read-

ing the manuscript before publication.

Editor’s Note

The name Batrachuperus persicus Eiselt and Steiner,

1970. Ann. Naturhist. Mus. Wien, 74:77 (Holotype:

NHMW 19435:4 [larval specimen], type locality:

Talysch Mountains near Assalem, Gilan Province, Iran,

small creek about 800 m) has priority over

2004

Asiatic Herpetological Research

Vol. 10, p. 190

Batrachuperus gorganensis Clerque-Gazeau and Thom,

1979. Bull. Soc. Hist. Nat. Toulouse 114:455 (Holotype:

MNHMP 1978-1982, type locality: At the edge of a cav-

ernous stream on a clay bank 200 m inside the entrance

of a cave, situated between the village of Gorgan and

Ali-Abad, Elborz Mountain Range of north-central Iran,

near the southeast shore of the Caspian Sea and with an

elevation of 400 m above sea level). The type localities

of the two nominal taxa lie at the extreme western and

eastern ends respectively of the known Iranian range of

Batrachuperus. Most recent authors have considered the

two specimens conspecific and a small number of popu-

lations distributed between the two type localities have

been discovered. However, the taxonomic status of B.

gorganensis as well as that of intermediate populations

remains unsettled. Unsettled; see also discussion of the

problem in Ebrahimi et al. (2004). Indeed, Risch (1984,

Alytes, Paris 3:44) made B. gorganensis the type of his

monotypic genus, Paradactylodon. SCA

Literature Cited

Baloutch, M and H. G. Kami. 1995. Amphibians of Iran.

Tehran University Publication, Tehran. 177 pp.

(In Farsi).

Clergue-Gazeau, M. and R. Thom. 1979. Une nouvelle

espece de salamander du genere Batrachuperus in

provence de l’lran septentrional (Amphibia,

Caudata, Hynobiidae). Bulletin Societe d’Histoire

Naturellell4 (3/4):455-460, Toulouse.

Ebrahimi, M., H. G. Kami, and M. Stock. 2004. First

description of egg sacs and early larval develop-

ment in Hynobiid Salamanders (Urodela,

Hynobiidae, Batrachuperus) from north-eastern

Iran. Asiatic Herpetological Research 10:168-175.

Eiselt, J. and H. M. Steiner. 1970. Erstfund eines hyno-

biiden Molches in Iran. Annalen des

Naturhistorischen Museum Wien 74:77-90.

Kami, H. G. and E. Vakilpoure. 1996. Geographic distri-

bution of Batrachuperus persicus. Herpetological

Review 27 (3): 147.

Kami, H. G. 1999. Additional specimens of the Persian

Mountain Salamander, Batrachuperus persicus

from Iran (Amphibia: Hynobiidae). Zoology in the

Middle East 19:37-42.

Petranka, J. W. 1998. Salamanders of the United States

and Canada. Smithsonian Institution Press,

Washington and London. 587 pp.

Schmidtler, J. J. and J. F. Schmidtler. 1971. Eine

Salamander- Novitat aus Persien, Batrachuperus

persicus. Aquarien Magazin 5(1 1). 443-445,

Stuttgart.

Steiner, H. M. 1973. Beitrage zur Kenntnis der

Verbreitung, Okologie und Bionomie von

Batrachuperus persicus. Salamandra 9:1-6.

Valentine, B. D. and D. M. Dennis. 1964. A comparison

of the gill-arch system and fins of three genera of

larval salamanders, Rhyacotriton, Gryinophilus,

and Ambystom a. Copeia 1964:196-201.

| 2004

Asiatic Herpetological Research

Vol. 10, pp. 191-201

Annotated Checklist of Amphibians and Reptiles of Pakistan

Muhammad Sharif Khan

Apt H A 17, 151-S. Bishop Ave., Secane, PA 19018, USA

E-mail: typhlops99@hotmail.com

Abstract. - From recent herpetological collections several new amphibian and reptilian taxa have been added to the

herpetofauna of Pakistan. Thus raising the number of species from Minton's 144 and Mertens' 178 to 225.

Key words. - Checklist, Pakistan, herpetofauna.

Introduction

Following is the checklist of amphibian and reptile

species that, so far, have been recorded and described in

the major works on the herpetology of the subcontinent

from the areas now included in Pakistan (Gunther, 1864;

Murray, 1884, 1886, 1892; Boulenger, 1890, 1896;

Smith, 1931, 1935, 1943). Recently described and

recorded species from Pakistan are also included in it

(Anderson and Leviton, 1966, 1967, 1969; Anderson

and Minton, 1963; Cherlin, 1981, 1983; Szczerbak,

1991; Golubev and Szczerbak, 1981; Ingoldby, 1922;

Mertens 1969a,b, 1970, 1971, 1972, 1974; Baig, 1988,

1989, 1998, 1999; Baig and Bohme, 1996; Baig and

Gvozdik, 1998; Dubois and Khan, 1979; Minton, 1966;

Minton and Anderson, J. 1965; Minton et al., 1970;

Khan, A. Q. and Khan, M.S. 1996; Khan, 1972, 1974,

1980, 1984a, b, 1988, 1989, 1991, 1992, 1993a, b, 1994,

1997a, b,c, 1998, 1999a, b, 2000, 2001a, b, 2003a, b; Khan

and Baig, 1992; Khan and Khan, R.Z., 1997; Khan and

Tasnim, 1989, 1990; Khan and Rosier, 1999; Rastegar-

Pouyani, 1999.

Frogs and Toads

Bufo stomaticus Liitkin, 1 862

Bufo surdus Boulenger, 1891

Bufo viridis zugmayeri Eiselt and Schmidtler, 1973

Family: Microhylidae

Microhyla Tschudi, 1828

Microhyla ornata (Dumeril and Bibron, 1841)

Uperodon Dumeril and Bibron, 1841

Uperodon systoma (Schneider, 1799)

Family: Ranidae

Euphlyctis Fitzinger, 1843

Euphlyctis cyanophlyctis cyanophlyctis (Schneider,

1799)

Euphlyctis cyanophlyctis microspinulata Khan,

1997

Euphlyctis cyanophlyctis seistanica (Nikolsky, 1900)

Family: Bufonidae

Bufo Laurenti, 1768

Bufo himalayanus Gunther, 1 864

Bufo latastii Boulenger, 1882

Bufo melanostictus hazarensis Khan, 200 1

Bufo olivaceus Blanford, 1874

Bufo pseudoraddei pseudoraddei Mertens, 1971

Bufo pseudoraddei baturae Stock, Schmid,

Steinlein, and Grosse, 1999

Bufo siacheninsis Khan, 1997

Hoplobatrachus Peters, 1 863

Hoplobatrachus tigerinus (Daudin, 1802)

Fejervarya Bolkay, 1915

Fejervarya limnocharis (Boie, 1834)

Fejervarya syhadrensis ( Annandale, 1919)

Nanorana Gunther, 1836

Nanorana pleskei (Gunther, 1896)

Vol. 10, p. 192

Asiatic Herpetological Research

2004

Paa Dubois, 1975

Paa barmoachensis (Khan and Tasnim, 1989)

Paa hazarensis Dubois and Khan, 1979

Paa sternosignata (Murray, 1885)

Paa vicina (Stoliczka, 1872)

Sphaerotheca Dumeril and Bibron, 1841.

Sphaerotheca breviceps (Schneider, 1799)

Turtles and Tortoises

Family: Cheloniidae

Caretta Rafiuesque, 1814

Caretta caretta (Linnaeus, 1758)

Chelonia Brongniart, 1800

Chelonia my das (Linnaeus, 1758)

Eretmochelys Fitzinger, 1843

Eretmochelys imbricata (Linnaeus, 1766)

Lepidoc/ielys Fitzinger, 1843

Lepidochelys olivacea (Eschscholtz, 1824)

Family: Dermochelyidae

Dermochelys Blainville, 1816

Dermochelys coriacea (Vandelli, 1761)

Family: Emydidae

Geoclemys (Gray, 1821)

Geoclemys hamiltonii (Gray, 1821)

Har della Gray, 1870

Hardella thurjii Gray, 1 870

Kachuga Gray, 1856

Kachuga smithii (Gray, 1 863)

Kachuga tecta (Gray, 1831)

Family: Testudinidae

Agrionemys Khozatsky and Mlynarsky, 1966

Agrionemys horsfieldii (Gray, 1844)

Geochelone Fitzinger, 1835

Geochelone elegans (SchopfF, 1792)

Family: Trionychidae

Aspideretes Hay, 1835

Aspideretes gangeticus (Cuvier, 1 825)

Aspideretes hurum (Gray, 1831)

Chitra Gray, 1 844

Chitra indica (Gray, 1831)

Lissemys Smith, 1 93 1

Lissemys punctata andersoni Webb, 1980

Crocodiles and Gavials

Family: Crocodylidae

Crocodylus Laurenti, 1768

Crocodylus palustris Lesson, 1831

Family: Gavialidae

Gavialis Oppel, 1811

Gavialis gangeticus (Gmelin, 1789)

Lizards

Family: Agamidae

Brachysaura Blyth, 1856

Brachysaura minor (Hardwicke and Gray, 1827)

Cables Cuvier, 1817

Calotes versicolor versicolor (Daudin, 1 802)

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Calotes versicolor farooqi Auffenberg and Rehman,

1995

Japalura Gray, 1853

Japalura kumaonensis (Annandale, 1907)

Laudakia Gray, 1845

Laudakia agrorensis (Stoliczka, 1872)

Laudakia badakhshana (Anderson and Leviton, 1969)

Laudakia caucasia (Eichwald, 1831)

Laudakia fusca (Blanford, 1876)

Laudakia himalayana (Steindachner, 1869)

Laudakia lirata (Blanford, 1874)

Laudakia melanura nasiri Baig, 1999

Laudakia melanura melanura Blyth, 1854

Laudakia microlepis (Blanford, 1874)

Laudakia nupta (de Filippi, 1843)

Laudakia nuristanica (Anderson and Leviton, 1969)

Laudakia pakistanica (Baig, 1989)

Laudakia pakistanica auffenbergi Baig and Bohme,

1996

Laudakia pakistanica khani Baig and Bohme, 1996

Laudakia tuberculata (Hardwicke and Gray, 1827)

Phrynocephalus Kaup, 1 825

Phrynocephalus clarkorum (Anderson and Leviton,

1967)

Phrynocephalus euptilopus Alcock and Finn, 1896

Phrynocephalus luteoguttatus Boulenger, 1887

Phrynocephalus maculatus Anderson, 1 872

Phrynocephalus ornatus Boulenger, 1 887

Phrynocephalus scutellatus Olivier, 1807

Trapelus Cuvier, 1816

Trapelus agilis Olivier, 1804

Trapelus agilis agilis (Olivier, 1804)

Trapelus agilis pakistanensis Rastegar-Pouyani, 1999

Trapelus megalonyx Gunther, 1 864

Trapelus rubrigular is Blanford, 1876

Trapelus ruderatus baluchianus (Smith, 1935)

Family: Chameleonidae

Chamaeleo Laurenti, 1768

Chamaeleo zeylanicus Laurenti, 1768

Family: Eublepharidae

Eublepliaris Gray, 1 827

Eublepharis macularius (Blyth, 1854)

Family: Gekkonidae

Agamura Blanford, 1 874

Agamura persica (Dumeril, 1856)

Altigekko M.S. Khan, 2003

Altigekko baturensis (Khan and Baig, 1992)

Altigekko boehmei (Szczerbak, 1991)

Altigekko stoliczkai (Steindachner, 1 869)

Bunopus Blanford, 1874

Bunopus tuberculatus Blanford, 1874

Crossobamon Boettger, 1888

Crossobamon lumsdeni (Boulenger, 1887)

Crossobamon maynardi (Smith, 1933)

Crossobamon orientalis (Blanford, 1876)

Cyrtopodion Fitzinger, 1843

Cyrtopodion agamuroides (Nikolsky, 1900)

Cyrtopodion kachhense kachhense (Stoliczka, 1872)

Cyrtopodion kachhense ingoldbyi Khan, 1997

Cyrtopodion kohsulaimanai (Khan, 199 Id)

Cyrtopodion montiumsalsorum { Annandale, 1913)

Cyrtopodion potoharensis Khan, 2001

Vol. 10, p. 194

Asiatic Herpetological Research

2004

Cyrtopodion scabrum (Heyden, 1 827)

Cyrtopodion watsoni (Murray, 1 892)

Hemidactylus Oken, 1817

Hemidactylus brookii Gray, 1845

Hemidactylus flaviviridis RUppell, 1835

Hemidactylus frenatus Schlegel, 1836

Hemidactylus leschenaultii Dumeril and Bibron, 1836

Hemidactylus persicus J. Anderson, 1872

Hemidactylus triedrus (Daudin, 1802)

Hemidactylus turcicus (Linnaeus, 1758)

Indogekko M.S. Khan, 2003

Indogekko fortmunroi (Khan, 1993)

Indogekko indusoani (Khan, 1980)

Indogekko rhodocaudus (Baig, 1998)

Indogekko rohtasfortai (Khan and Tasnim, 1990)

Mediodactylus Szczerbak and Golubev, 1977

Indogekko walli (Ingoldby, 1 922)

Ptyodactylus Goldfuss, 1820

Ptyodactylus homolepis Blanford, 1876

Rhinogecko de Witte, 1973

Rhinogecko femoralis (Smith, 1933)

Rhinogecko misonnei de Witte, 1973

Siwaligekko M. S. Khan, 2003

Siwaligekko battalensis (Khan, 1993)

Siwaligekko dattanensis (Khan, 1980)

Siwaligekko mintoni (Golubev and Szczerbak, 1981)

Teratolepis Gunther, 1 870

Teratolepis fasciata { Blyth, 1853)

Teratoscincus Strauch, 1863

Teratoscincus microlepis Nikolsky, 1899

Teratoscincus scincus (Schlegel, 1858)

Teratoscincus scincus keyserlingi Strauch, 1 863

Tropiocolotes Peters, 1880

Tropiocolotes depressus Minton and J. A. Anderson,

1965

Tropiocolotes persicus persicus (Nikolsky, 1903)

Tropiocolotes persicus euphorbiacola Minton, S.

Anderson, and J. A. Anderson, 1970

Family: Lacertidae

Acanthodactylus Wiegmann, 1834

Acanthodactylus blanfordii Boulenger, 1918

Acanthodactylus cantoris Gunther, 1 864

Acanthodactylus micropholis Blanford, 1874

Eremias Wiegmann, 1 834

Eremias acutirostris (Boulenger, 1887)

Eremias aporosceles (Alcock and Finn, 1896)

Eremias fasciata Blanford, 1874

Eremias persica Blanford, 1874

Eremias scripta (Strauch, 1867)

Mesalina G ray, 1838

Mesalina brevirostris Blanford, 1874

Mesalina watsonana (Stoliczka, 1872)

Ophisops Menetries, 1832

Ophisops elegans Menetries, 1832

Ophisops jerdonii Blyth, 1853

Family: Scincidae

Ablepharus Fitzinger, 1823

Ablepharus gray anus (Stoliczka, 1872)

Ablepharus pannonicus (Fitzinger, 1823)

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Asiatic Herpetological Research

Vol. 10, p. 195

Chalcides Laurenti, 1768

Chalcides ocellatus (Forskal, 1775)

Eurylepis Blyth, 1854

Eurylepis taeniolatus taeniolatus (Blyth, 1854)

Lygosoma Hardwick and Gray, 1827

Lygosoma punctata (Linnaeus, 1766)

Mabuya Fitzinger, 1826

Mabuya dissimilis (Hallowed, 1860)

Mabuya macular i a (Blyth, 1853)

Novoeumeces Griffith, Ngo, and Murphy, 2000

Novoeumeces blythianus (J. Anderson, 1871)

Novoeumeces indothalensis (M.S. Khan and M.R.Z.

Khan, 1997)

Novoeumeces schneider ii zarudnyi (Nikolsky, 1900)

Ophiomorus Dumeril and Bibron, 1839

Ophiomorus blanfordi Boulenger, 1887

Ophiomorus brevipes (Blanford, 1874)

Ophiomorus raithmai S. Anderson and Leviton, 1966

Ophiomorus tridactylus (Blyth, 1853)

Scincella Mittleman, 1950

Scincella himalayana (Gunther, 1 864)

Scincella ladacensis (Gunther, 1864)

Family: Uromastycidae

Uromastyx Merrem, 1 820

Uromastyx asmussi (Strauch, 1 863)

Uromastyx hardwickii Gray, 1 827

Family: Varanidae

Varanus Merrem, 1820

Varanus bengalensis (Daudin, 1 802)

Varanus flavescens (Hardwicke and Gray, 1 827)

Varanus griseus (Daudin, 1803)

Varanus griseus caspius (Eichwald, 1831)

Varanus griseus koniecznyi Mertens, 1954

Ophidia: Snakes

Family: Leptotyphlopidae

Leptotyphlops Fitzinger, 1843

Leptotyphlops blanfordii (Boulenger, 1890)

Leptotyphlops macrorhynchus (Jan, 1 862)

Family: Typhlopidae

Ramphotyphlops Fitzinger, 1843

Ramphotyphlops braminus (Daudin, 1803)

Typhlops Oppel, 1811

Typhlops ahsanai M.S. Khan, 1999

Typhlops diardii Schlegel, 1839

Typhlops diardii platyventris M.S. Khan, 1998

Typhlops ductuliformes M.S. Khan, 1999

Typhlops madgemintonai madgemintonai M.S. Khan,

1999

Typhlops madgemintonai shermanai M.S. Khan, 1999

Family: Boidae

Eryx Daudin, 1803

Eryx conicus (Schneider, 1801)

Eryx johnii (Russell, 1801)

Eryx tataricus speciosus Zarevsky, 1915

Python Daudin, 1803

Python molurus (Linnaeus, 1758)

Family: Colubridae

Amphiesma Dumeril, Bibron and Dumeril, 1854

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Vol. 10, p. 197

Telescopus Wagner, 1830

Telescopus rhinopoma (Blanford, 1874)

Xenochrophis Gunther, 1864

Xenochrophis cerasogaster cerasogaster (Cantor, 1839)

Xenochrophis piscator piscator ( Schneider, 1799)

Xenochrophis sanctijohannis (Boulenger, 1 890)

Family: Elapidae

Bungarus Daudin, 1803

Bungarus caerulens caeruleus (Schneider, 1801)

Bungarus sindanus razai M. S. Khan, 1985

Bungarus sindanus sindanus Boulenger, 1847

Naja Laurenti, 1768

Najanaja (Linnaeus, 1758)

Naja oxiana (Eichwald, 1831)

Family: Hydrophiidae

Astrotia Fisher, 1856

Astrotia stokesii (Gray, 1 846)

Enhydrina Gray, 1849

Enhydrina schistosa (Daudin, 1803)

Hydrophis Latreille, 1802

Hydrophis caerulescens (Shaw, 1 802)

Hydrophis cyanocinctus Daudin, 1 803

Hydrophis fasciatus (Schneider, 1799)

Hydrophis lapemoides (Gray, 1 849)

Hydrophis mamillaris (Daudin, 1 803)

Hydrophis ornatus (Gray, 1 842)

Hydrophis spiralis (Shaw, 1 802)

Lapemis Gray, 1835

Lapemis curtus (Shaw, 1 802)

Microcephalophis Lesson, 1834

Microcephalophis cantoris (Gunther, 1 864)

Microcephalophis gracilis (Shaw, 1802)

Pelamis Daudin, 1803

Pelamis platurus (Linnaeus, 1766)

Pr aes cut at a Wall, 1921

Praescutata viperina (Ph. Schmidt, 1852)

Family: Viperidae

Daboia Gray, 1842

Daboia russelii russelii (Shaw and Nodder, 1797)

Echis Merrem, 1 820

Echis carinatus (Schneider, 1 820)

Echis carinatus astolae Mertens, 1969

Echis carinatus multisquamatus Cherlin, 1981

Echis carinatus sochureki Stemmier, 1964

Eristicophis Alcock and Finn, 1896

Eristicophis macmahonii Alcock and Finn, 1897

Macrovipera Reuss, 1 927

Macroviper a lebetina obtusa (Dwigubsky, 1832

Pseudocerastes Boulenger, 1 896

Pseudocerastes bicornis Wall, 1913

Pseudocerastes persicus (Dumeril, Bibron, and

Dumeril, 1854)

Family: Crotalidae

Gloydius Hoge and Romano-Hoge, 1981

Gloydius himalayanus (Gunther, 1864)

Vol. 10, p. 198

Asiatic Herpetological Research

2004

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Vol.10, pp. 202-207

A Morphological and Taxonomic Study on Lacerta parva Boulenger, 1887

(Sauria: Lacertidae) from West Taurus, Turkey

Y. KUMLUTA^1’*, S. H. Durmu^1, Y. Kaska2 , M. Oz3 AND M. R. TUNg3

' Dokuz Eyliil Universitesi, Buca Egitim Fakiiltesi, Biyoloji A.B.D. Buca- / zmir, Turkey.

2 Pamukkale Universitesi, Fen-Edebiyat Fakiiltesi, Biyoloji Boliimu Denizli-Turkey.

J A kdeniz Universitesi, Fen-Edebiyat Fakiiltesi, Biyoloji Boliimii Antalya-Turkey.

jjj

To whom correspondence should be addressed E-mail: yusuf.kumlutas@deu.edu.tr

Abstract. - The morphometric measurements of taxonomically important characters, coloration, and pholidosis fea-

tures of 74 Lacerta parva specimens collected from West Taurus, Turkey were investigated. Statistical analyses were

done and these results were compared with those from relevant literature. Some of the characters were found to be

different on the specimens from different localities. New localities from southwest Turkey were also discovered dur-

ing this study.

Key words. - Lacerta parva, West Taurus, Turkey.

Introduction

Lacerta parva was first identified as a new species

based on a female specimen collected from Kayseri,

Turkey (Boulenger, 1887). In later studies, the distribu-

tion of this species was extended to include all of Anato-

lia and the Caucasian region (Werner, 1902; Nesterow,

1912; Nikolsky, 1915; Bird, 1936; Bodenheimer, 1944;

Mertens, 1952; Ba§oglu and Baran, 1977; Baran et al.,

1992; Baran and Atatiir, 1998). The distribution of this

species was extended to Europe by giving the locality

from Tekirdag, Turkey (Venchi-Bologna, 1996).

Peters (1962) compared the variations and similari-

ties between Caucasian and Anatolian populations by

examining the 131 and 74 specimens, respectively.

Atagiin (1984) also did a comparative study on the 208

specimens collected from six different sub-populations

(Fethiye, Denizli, Konya, Ankara, Kayseri, Erzurum)

from Anatolia. Recently, Mtilayim et al. (2001) studied

46 specimens collected from Golka§i Village, Bey^ehir-

Konya and found much more similarities between

Konya and Fethiye populations as previously mentioned

by Atagiin (1984).

This work investigates the distribution of this spe-

cies in the west of Turkey and also provides morpho-

metrical comparison of these specimens with previously

collected specimens and relevant literature. We try to

resolve the taxonomical situation of the sub-populations

of Lacerta parva in Anatolia.

Material and Methods

Most of the specimens were obtained from Taurus,

southwest of Anatolia. A sum of 22 male, 38 female and

14 juvenile specimens were collected. These specimens,

collected during the years of 1995-1997, were kept at

ZDEU (Zoology Department of Ege University). The

locations where the samples were collected are given in

Figure 1. The list of material is given below as the

Departmental Identification Code, sex, number of speci-

mens, locality, date, initials, and surname of the collec-

tors respectively.

List of Material

1) 140 / 1995, 1 male, Bey§ehir, 19.09.1995, Leg. M.

Oz.

2) 238 / 1996 1-9 males, 10-22 females, Bozhoyiik

Ovacik-Elmali, 18.06.1996, Leg. Y. Kumluta§ , R.

Tun9, S. H. Durmu§ .

3) 239 / 1996, 1-5, 6-13, 14-27 Juv., gayryakas -

Gazipa^a, 23.08.1996, Leg. Y. Kumluta§, M. Oz, R.

Tun?.

4) 163 / 1997, 1-7, 8-24 , Beyobasi, 25.06.1997, Leg. Y.

Kumluta§, M. Oz, R. Tun?.

Coloration of living specimens was determined by

eye, slides were taken, and then the specimens fixed

with the traditional processes and kept in 70% alcohol.

The morphometric measurements were done with a dig-

ital calliper with an accuracy of 0.02 mm. The body

Measurements taken and their descriptions and indexes

of the characters are as follows. Pileus Width (PW):

Vol.10, p. 203

Asiatic Herpetological Research

2004

Figure 1. The distribution of Lacerta parva in Turkey.

Collection localities in this study. Refer to the materials list for details.

Collection localities from literature (Peters, 1962; Atagiin, 1984; Ba§oglu-Baran, 1977;

Baran et al. , 1992; Venchi-Bologna, 1996; and Miilayim et al. , 2001).

The widest distance between the parietal plates. Pileus

Length (PL): The distance from the posterior point of

parietal plates to the tip of rostrum. Head and Body

Length (HBL): The distance between the front tip of

rostrum and front edge of anus. Body Length (BL): The

total length of body from tip of rostrum to the end of

tail. Tail Length (TL): The length of tail from anus to

the tip of tail. Forelimb Length (FL): The length of

forelimb from the body connection to the tip of longest

finger. Hind-limb Length(HL): The length of hind

limb from the body connection to the tip of fourth fin-

ger. Pileus Index (PI)=PW/PLxl00, Tail Index

(TI)=TL/BLxl00 and Forelimb Index (FI)=FL/

BLxlOO were also calculated. The ANOVA statistical

test were used in comparison of the measurements and

the ratios (Minitab, 1991). The values of “Coefficient of

difference (CD)” were used in comparison of some

characteristics among the population (Mayr, 1969).

Results

Pholidosis and Morphometric Measurements

2004

Table 1 : The results of descriptive statistics on some of the characteristics of L. parva specimens (These measurem

are given as miiimeter).

Rostrale were connected to the nostril and the numbers

of postnasal plate were occasionally two (96%), only

one (3%) in two specimens and one specimen had one

on the left and two on the right. The number of occipital

plates were also commonly one (97%) but divided into

two in two (3%) specimens. The numbers of supercili-

ary plates was five in 44 specimens (59.4%), six in 23

specimens (31.1%), four in four specimens (5.4%),

seven in two specimens (2.7%) and nine in one speci-

men (1.4%). The numbers of supralabial plates, in front

of the subocular plate, was usually four (74.3%); three

in two specimens (2.7%); four (one small and three big)

in three specimens (4.05%); five in two specimens as

two small and three big ones; four big and one small in

six (8.1%) other specimens; six (four big and two small)

in two specimens, seven (four big and three small) in

two specimens. The distal end of the collaria was jagged

in shape and the numbers varied between five and eight

with a mean of 6.7. The results from statistical analyses

of the above mentioned measurements are presented in

Table 1; comparative results with other literature are

presented in Table 2. There were no statistical differ-

ences (F-test, P>0.05) between the specimens collected

from different locations in this study.

Although the T-test does not show any statistical

differences (P>0.05) between males and females, males

have relatively higher values than females. For example,

the mean length of the pileus was 11.15 (Min.= 9.64 -

Max =16.60) in males and 9.99 (8.72 - 11.50) in

females. The coefficient of differences (CD) was 0.59.

The width of the pileus was 5.53 (4.74 - 6.23) in males

and 5.14 (4.38 - 6.90) in females and the CD was 0.44.

Vol.10, p. 205

Asiatic Herpetological Research

2004

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The tail was longer in males (76.59) than females

(70.62) and the CD of this measurements was 0.28.

Color and Pattern. - Dorsal coloration is more ground,

grayish-brown in the Elmali population and lighter

brown in the other three populations studied. A slim

dark line was present from posterior of occipital scute

towards the posterior. This line does not stretch to the

base of forelimbs in juveniles. There were few dark

spots on the vertebrals of some specimens (11%). Dark

blotches extending dorso ventral ly from vertebal line

formed bands, particularly on Beyobasi specimens. The

supra-temporal line was usually continuous until the

middle part of body; broken lines continued posteriorly

to the base of the tail or sometimes until the tip of tail in

some specimens. Small spots are present, their central

parts are greenish-blue and surrounding areas are dark

starting at the base of the forelimb and usually continu-

ing posteriorly. The subocular line is dirty white in color

and continues to the hindlimbs. Dark spots were present

under this line in some specimens.

Ventral scales are yellow in males, especially dur-

ing the breeding season (which change to white later in

the season), and lighter in females. However, the color

under the hind limb was sometimes yellowish; the other

parts were pinkish-white for females. Dark stains on

ventralia were absent on the samples, except for the last

ventral plate.

Ecological Observations. - The three specimen collec-

tion localities were new localities for L. parva , except

for the Bey§ehir population. These habitats were nearly

2000 m in altitude (i.e., Bozhoyiik-Ovacik 1800 m.,

(fayiryakasi-Gazipa§a 1850 m.,

Beyobasi 1900 m.). The 22 specimens, from

Bozhoyiik-Ovacik population, were caught between

bushes and small vegetation. The weather was a bit

cloudy and the temperature was approximately 24°C.

Laudakia stellio and Ablepharus kitaibelii species were

also observed in the same habitat. The specimens from

Cayiryakasi and Beyobasi were caught while active or

under stones at the temperature around 29°C. The col-

lection habitats of the specimens were covered mainly

small bushy vegetation not big trees. Lacerta danfordi ,

Mabuya vittata, Cyrtopodion kotschyi and Natrix natrix

species were also observed in the same area.

Evaluation and Discussion

There were no statistical differences between the differ-

ent populations in this study, but tail length, pileus

length, fore-limb and hind-limb lengths, and the number

of femoral openings were higher in males than females.

Vol.10, p. 206

The head and body length and the number of lateral

plate lines were higher in females than males. Atagiin

(1984) reported that only one plate is present behind the

postnasal plate in 26% of the specimens from the Erzu-

rum population, but not present in the remaining five

populations in his work. We did not record any such

character from our specimens. Atagiin (1984) also

reported that the division of the occipital plate was also

different in the Erzurum population by having a higher

number of divisions. This population was also studied

by Peters (1962), but he did not mention such differ-

ences. Only a small percent (3%) of our specimens

showed a division in the occipital plate.

Peters (1962), in his study comparing L. parva pop-

ulations between Caucasia and Anatolia, found that the

mean number of dorsalia were different (males = 35.97;

females = 34.76) in Caucasian population than Anato-

lian population (males= 38.52; females= 37.53). Our

values from West Taurus (males= 37.68; females=

36.42) were very similar to Peters (1962) values from

Anatolia. This value, along with other parameters, are

presented in Table 2. As it can be seen from this table,

the results of this work are very close to the results of

the Bey§ehir population reported by Mulayim et al.

(2001).

Peters (1962) also reported the mean number of

lamellae under the fourth finger to be very similar

between the Caucasian (males= 21.6; females= 21.2)

and Anatolian (males= 22.6; females= 22.1) specimens.

Our results for this character were slightly lower than

Peters’ results but very close to the results of Mulayim

et al. (2001) (Table 2). The number of femoral openings

reported by Peters (1962) were slightly higher (males=

17.56; females= 16.46) for Caucasian than for Anatolian

(males= 17; females= 15.91) specimens. The number of

femoral openings in this study were found to be very

close to the most eastern Anatolian population of Erzu-

rum (Table 2). The HBL, the mean numbers of supra-

cilliar plate, lateral plates in ventralia were very similar

with the results of Mulayim et al. (2001), but the mean

number of median gularia in this study was very close to

the Fethiye population reported by Atagiin (1984).

There were no remarkable differences in color and pat-

tern reported by others (Peters, 1962; Atagiin, 1984;

Baran et al., 1992; Miilayim et al., 2001) and our

results.

As it can be seen from our present and other previ-

ous studies, phenotypic variation among the reptile pop-

ulations from Turkey have been quantified extensively

using morphological characters. Comparison of mor-

phometric measurements may yield a new subspecies,

but the different populations of L. parva from Turkey

may vary even genetically. Unfortunately, genetic diver-

sity at the intra-specific level is not available for any

species in Turkey. Sequencing DNA, in particular

mtDNA, may help to solve the taxonomic problems

present in the herpetofauna of Turkey, as it was done for

other amphibian species (i.e. Garcia-Paris et al., 1998)

and for sea turtles (i.e., Bowen et al., 1994; Kaska,

2000).

Acknowledgments

This work is some part of the project [Project No:

TBAG-1475 (196T021)] supported by TUBITAK (The

Scientific and Technical Research Council of Turkey).

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Baran, i. and M. K. Atatiir. 1998. Turkiye Herpeto faunas

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Boulenger, G. A. 1887. Catalogue of The Lizards In The

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Anelytropidae, Dibamidae, Chamaeleontidae),

London, 1-575.

Bowen, B. W., N. Kamezaki, C. L. Limpus, G. H.

Hughes, A. B. Meylan and J. C. Avise. 1994. Glo-

bal phylogeography of the loggerhead turtle

{Caretta caretta ) as indicated by mitochondrial

DNA haplotypes. Evolution 48:1820-1828.

Garcia-Paris, M., M. Alcobendos, and P. Alberch. 1998.

Influence of the Guadalquvir river basin on mito-

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chondrial DNA evolution of Salamandra salaman-

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24:191-197.

Mayr, E. 1969. Principles of Systematics Zoology. Mac-

Graw Hill Book Co., Inc. New York, 428 pp.

Mertens, R. 1952. Amphibien und Reptilien aus der

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Minitab Reference Manual PC Version. 1991. Release

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inde Morfolojik Bir £ali§ma. Anadolu University

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2:345-349.

Nesterow, P. W. 1912. K gerpetologii judo-sapadnowo

sakawkasja I pogranitschnoj tschasti Maloi Asii

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skaukasiens und der Agrenzenden Teile von Klein-

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Nikolsky, A. M. 1915. Fauna Rossii i Sopredelnych

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Boulenger) und ihre Verwandtschafts-beziehungen

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schaften Mathematische - Naturwisssenschaften.

Abt. I, 111:1057-1121.

2004

Asiatic Herpetological Research

Vol. 10, pp. 208-214

Genetic Variation Among Agamid Lizards of the Trapelus agilis

Complex in the Caspian-Aral Basin

J. Robert Macey1’2’* and Natalia B. Ananjeva3

1 Department of Evolutionary Genomics, Joint Genome Institute, Lawrence Berkeley

National Laboratory, 2800 Mitchell Drive, Walnut Creek, CA 94598-1631, USA

2 Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA

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

*To whom correspondence should be addressed: E-mail: jrmacey@lbl.gov

Abstract. - Allozyme variation is examined in eight populations of Trapelus from the Caspian-Aral Basin of the for-

mer USSR. Thirty one loci (15 variable) exhibit remarkably low levels of genetic variation with only a Nei's genet-

ic distance of 0.1 17 across 2500 km. An isolated population on the European side of the Caspian Sea is found to phe-

netically cluster inside the Asian populations examined, suggesting that it should not be considered taxonomically dis-

tinct.

Key words. - Reptilia, Squamata, Agamidae, Trapelus , Central Asia, biogeography, allozyme electrophoresis.

Introduction

The Trapelus agilis complex is distributed on the Iranian

Plateau and adjacent regions of southwestern Asia, as

well as in the Caspian-Aral Basin to the north in the inte-

rior of Asia. Two separate populations of the Trapelus

agilis complex are separated by the Caspian Sea in the

Caspian-Aral Basin (including regions draining to Lake

Balkhash) of the former USSR. One population on the

eastern side of the Caspian Sea ranges from western

China, Kazakhstan, and Kirgizistan in the north, to

Turkmenistan (Fig. 1), Uzbekistan, and Tadjikstan in the

south. This Central Asian population is continuous with

Iranian, Afghan, and other southwest Asian populations

referred to Trapelus agilis. On the western side of the

Caspian Sea in Europe a small population occurs in

Chechenia and Dagestan, Russia. The two populations

occurring in the Caspian-Aral Basin are placed either in

a separate species, T. sanguinolentus, or subspecies, T.

agilis sanguinolentus. Taxonomic controversy also

exists as to the status of the isolated European popula-

tion of Trapelus. Some authors consider the European

population to be a distinct subspecies of T. sanguinolen-

tus ( T. s. sanguinolentus ) with the Central Asian popula-

tions being referred to T. s. aralensis (Ananjeva and

Tsaruk, 1987). Others consider the European and Asian

populations in the Caspian-Aral Basin to be a single

taxon, either T. sanguinolentus (Bannikov et al., 1977)

or T. agilis sanguinolentus (Wermuth, 1967). The focus

of this study is on the relative position of the European

and Asian populations in the Caspian-Aral Basin. The

Caspian-Aral Basin populations are always grouped

together either as a species or as one or two distinct sub-

species relative to the southwest Asian populations

referred to as T. agilis.

Trapelus is an old genus of Agamid lizards with an

Afro-Arabian origin (Macey et al., 2000b). Sequence

divergence between Trapelus species in Africa ( Trapelus

savignii ), Arabia (T. persicus ), the Iranian Plateau ( T.

agilis ), and the Caspian-Aral Basin ( Trapelus sanguino-

lentus population 6 of this study), which form a clade, is

10.7-13.9% for the mitochondrial DNA segment span-

ning from nadl to coxl (Macey et al., 2000b). Applying

the rate of 1.3% change per million years for pairwise

comparisons as calculated for this segment of mitochon-

drial DNA in agamid lizards of the genus Laudakia

(Macey et al., 1998), divergence times among these

species of Trapelus are estimated to be 8.3 to 10.7 mil-

lion years before present (MYBP). These data suggest

that the genus has been in Asia since the Miocene.

Allozyme data are used to distinguish hypotheses of

early divergence of the European and Asian trans-

Caspian populations into discrete entities, verses colo-

nization of the European side of the Caspian Sea by

western Asian populations. High mountains in the

Caucasus and Elburz ranges prevent colonization of the

European population from the south, where a continuous

land connection does exist to Trapelus populations in

Iran. The Caspian-Aral Basin corresponds to much of

the Paratethys Sea, which during the Miocene almost

completely dried up 5-6 MYBP and then returned briefly

in the Pliocene, 3.0-3.5 MYBP (Steininger and Rogl,

1984). Divergence following the early period (5-6

MYBP) when much of the Caspian-Aral Basin was

Vol. 10, p. 209

Asiatic Herpetological Research

2004

Figure 1. A Trapelus from Repetek Desert Reserve Station, Repetek (38° 34' N, 63° 11' E), Chardjou Region,

Turkmenistan. The photo was taken in May, 1989. This is a representative of population 5 of this study.

available for colonization, should halt gene flow in the

late Miocene or Pliocene and two discrete populations

are expected to be detected, one in Europe and one in

Asia. Alternatively, a more recent colonization from a

founder event, when the Caspian Sea level fluctuated in

the Pleistocene, should have a much later restriction in

gene flow and therefore the European population may be

expected to be nested within the Asian population.

Material and Methods

Laboratory Protocols. - Tissues were taken in the field,

immediately frozen in liquid nitrogen, and later trans-

ferred to an ultracold freezer and maintained at -80° C.

For analysis of allozymic variation, liver and muscle tis-

sues were homogenized separately. Horizontal starch-

gel electrophoresis was employed to differentiate varia-

tion in 3 1 presumptive loci. The 3 1 loci and eight buffer

conditions utilized to resolve them are displayed in table

1. Allozymes were stained using standard methods

(Harris and Hopkinson, 1976; Murphy et al., 1990;

Richardson et al., 1986; Selander et al., 1971).

Carboxylic ester hydrolase (Dimeric Esterase) was

resolved using 4-methylumbelliferyl acetate as the sub-

strate, Alcohol dehydrogenase (ADH) was resolved

using 7h7ra-2-Hexen-l-ol as the substrate, an unidenti-

fied peptidase (PEP-1) was resolved using L-leucyl-L-

alanine as the substrate, and Peptidase D (PEP-D) and an

unidentified peptidase (PEP-2) with the use of L-pheny-

lalanyl-L-proline as the substrate. The isozymes, and

loci if more than one, were labeled according to their

migration from anode to cathode.

Specimen Information. - Museum numbers and locali-

ties for voucher specimens are presented below.

Acronyms are CAS for California Academy of Sciences,

San Francisco and MVZ for Museum of Vertebrate

Zoology, University of California at Berkeley. Russia:

(population 1) Tersko-Kumskaya nizmennast (the low-

land between Terek and Kuma Rivers), 15 km WNW

(airline) of Voskresenskaya, which is approx. 25 km

NNW of Gudermes (43° 21' N 46° 06' E),

Schelkovskaya District, Chechen-lngush Autonomous

Republic (CAS 182952, 183032-183038). Kazakhstan;

(population 2) Almaty (43° 15' N 76° 57' E), Almaty

Region (MVZ 216014-216016, CAS 183047-183051).

Uzbekistan: (population 3) sand dunes on the west side

of the Surkhan Darya (River), on the Kumkurgan (37°

48' N, 67° 37' E) to Denau (38° 16' N, 67° 54’ E) Rd.,

Surkhan Darjinskaya Region (CAS 183004-183006).

2004

Asiatic Herpetological Research

Vol. 10, p. 210

Table 1. The 31 protein loci scored and the electrophoretic conditions within which they were resolved.

^Tissue abbreviations are: L = liver; M = skeletal muscle.

^Electrophoretic conditions: (1) Lithium-borate/Tris-citrate pH 8.2, 250 v for 6 h (Selander et al., 1971); (2) Amine-cit-

rate (Morpholine) pH 6.0, 250 v for 6 h (Clayton and Tretiak, 1972); (3) Tris-citrate/borate pH 8.7, 250 v for 5 h

(Selander et al., 1971); (4) Histidine-citrate pH 7.8, 150 V for 8 hours (Harris and Hopkinson, 1976); (5) Phosphate-cit-

rate pH 7.0, 120 v for 7 h (Selander et al., 1971); (6) Tris-citrate II pH 8.0, 130 v for 8 h (Selander et al., 1971); (7) Tris-

HCL pH 8.5, 250 v for 4 1/2 h (Selander et al., 1971); (8) Tris-maleate-EDTA pH 7.4, 100 v for 10 h (Selander et al.,

1971).

CEST-D = Dimeric Esterase

Turkmenistan: (population 4) SW bank of the Amur

Darya (River), approx. 2 km NE of Nephtezavodsk

which is 30 km WNW of Deynau (39° 15' N, 63° 1 T E),

Chardjou Region (CAS 179552-179559); (population 5)

1 km north of Repetek Desert Reserve Station, Repetek

(38° 34’ N, 63° 1 1 ' E), Chardjou Region (CAS 1 79 1 99-

179203, 179416-179420), and Repetek Desert Reserve

Station, Repetek (38° 34' N, 63° 11' E), Chardjou

Region (CAS 179331); (population 6) 55 km north of

Ashgabat (37° 57' N, 58° 23' E) on the Ashgabat -

Bakhardok (38° 46' N, 58° 30' E) Rd. then 21 km WNW

on dirt Rd., Ashgabat Region (CAS 179758-179767);

(population 7) Ashgabat (37° 57' N, 58° 23' E),

Ashgabat Region (MVZ 216087-216092); (population

8) near Iolotan’ [YolotanJ (37° 18' N, 62° 21' E), Mary

Region (MVZ 216013).

Data Analysis, - Nei’s (1978) unbiased genetic distance

and Rogers (1972) genetic similarity were calculated

using BIOSYS-I (Swofford and Selander, 1981).

Phenetic clustering was constructed using the neighbor-

joining algorithm (Saitou and Nei, 1987), which does

not require rate uniformity, using PAUP* 4.0 (Swofford,

1999) and Nei’s (1978) unbiased genetic distance.

Results

Variable Loci. - Fifteen of the 31 loci screened show

variation among the sampled populations (Table 2). Up

to five different allelic states are recognized per loci

among populations with no more than four allelic states

being present within a population.

Genetic Distances. - Allozymic variation among sam-

pled populations of Trapelus is surprisingly low (Table

3). The two geographically most distant samples, the

European side of the Caspian-Aral Basin (West Caspian)

and Kazakhstan (Almaty), have a Nei’s (1978) unbiased

genetic distance of only 0.117 across 2500 km. The

highest Nei’s (1978) unbiased genetic distances recov-

Vol. 10, p.211

Asiatic Herpetological Research

2004

p*®c^romorPh frequencies for the 15 polymorphic loci from eight populations of Trapelus sampled. Localities

are West Caspian (WCA), Almaty (ALM), Uzbekistan (UZB), Nephtezavodsk (NEP), Repetek (REP), 70 km NW

Ashgabat (NWA), Ashgabat (ASH), lolotan' (IOL). See text for complete localities of all populations used.

Table 3. Matrix of genetic distance and identity coefficients from the eight populations of Trapelus sampled. Nei's unbi-

ased genetic distance (Nei, 1978) is above the diagonal, Rogers genetic similarity (Rogers, 1972) is below the diago-

nal and sample sizes are on the diagonal. See text for specimen deposition and complete localities of all populations

used.

2004

Asiatic Herpetological Research

Vol. 10, p. 212

Genetic Distances among USSR Populations of Trapelus agilis Complex

Figure 2. Map of the Caspian-Aral Basin and southwest Asia showing the distribution of the Trapelus agilis complex.

Dots depict populations sampled. Lines connect populations in major areas, West Caspian, Kazakhstan, Uzbekistan

and Turkmenistan. Nei's unbiased genetic distance (Nei 1978) is plotted between areas. The Turkmen populations are

averaged. The western most sample on the west side of the Caspian Sea is population 1 (table 3). The eastern most

sample is Almaty in Kazakhstan (population 2). To the southwest of this sample is the Uzbekistan population (popula-

tion 3). Four of the Turkmen samples are connected by lines. The most northeastern is population 4 from

Nephtezavodsk and the most southeastern is population 5 from Repetek. The most northwestern is population 6 from

70 km NW Ashgabat and the most southwestern is population 7 from Ashgabat. Population 8 from lolotan' is not includ-

ed in the average of Turkmen populations because of the low sample size of one and it is distributed between dodu-

lations 5 and 7. H H

ered are 0.088-0.145 (note that the highest value is with

a sample size of one) between the northwestern popula-

tion in Kazakhstan (Almaty) and all other populations

sampled in the Caspian-Aral Basin. The European pop-

ulation on the western side of the Caspian Sea is separat-

ed from all other populations except the Kazakhstan

(Almaty) population by Nei’s (1978) unbiased genetic

distances of 0.026-0.066. The population in Uzbekistan

is distinct from those in Turkmenistan by Nei’s (1978)

unbiased genetic distances of 0.019-0.048.

Mapping these genetic distances on geography

reveals a pattern of isolation by distance in which all dis-

tances appear relatively additive (Fig. 2). Clustering of

these data in a neighbor-joining phenogram and rooting

the tree on the longest path places the Kazakhstan

(Almaty) population and Uzbekistan sample in a basal

Vol. 10, p. 213

Asiatic Herpetological Research

2004

West Caspian (1)

*— 70 km NW Ashgabat (6)

•“ Ashgabat (7)

lolotan’ (8)

Nephtezavodsk (4)

— Repetek (5)

Uzbekistan (3)

Airaa-Aty (2)

0.01 changes

Figure 3. Neighbor-joining phenogram rooted on the

longest path. Note that the European population on the

western side of the Caspian Sea is nested inside the

Asian populations sampled and appears as the sister

population to its nearest Asian population (70 km NW

Ashgabat). Population numbers corresponding to figure

1, and tables 2 and 3 are given adjacent to locality

names.

position. The European (West Caspian) population

appears nested within the Turkmen populations and as

the sister population to its nearest Asian population (70

km NW Ashgabat), (Fig. 3). This pattern is consistent

with the observed genetic distances.

Discussion

The Age of Trapelus in the Caspian-Aral Basin. - The

European population of Trapelus is found to cluster phe-

netically within the Asian populations with little genetic

differentiation, suggesting that these taxa do not repre-

sent distinct forms. The low genetic diversity in

Trapelus of the Caspian-Aral Basin probably indicates a

recent dispersion of Trapelus throughout the Caspian-

Aral Basin. Nei’s (1978) unbiased genetic distances do

not exceed 0.117 (with the exception of Kazakhstan to

lolotan’ Turkmenistan with a sample size of one). A very

approximate estimate of divergence time and genetic

distance is 14 million years for a Nei’s D of 1.0 (Maxson

and Maxson, 1979). Given this rate these data suggest a

divergence of Trapelus populations in the Caspian-Aral

Basin at around 1.6 MYBP. This result suggests that

Trapelus did not diverge in the Caspian-Aral Basin until

the Pleistocene, well after the last drying of the

Paratethys Sea 3.5 MYBP (Steininger and Rogl, 1984).

Comparison to Other Taxa. - One additional genus of

lizard has been sampled from the Caspian-Aral Basin for

allozyme variation. The northern populations of the

gekkonid genus Mediodactylus from Almaty and the

Junggar Depression of China show a minimum of two

fixed differences when compared to a southern popula-

tion in the Kara Kum Desert (Macey et ah, 2000a). This

divergence is greater than those observed among

Trapelus where no fixed differences are detected

between Almaty (population 2) and the Kara Kum

Desert (populations 4-8). Because the Caspian-Aral

Basin has had periods of inundation followed by drying

over the last 6 million years, and the surrounding moun-

tains of the Pamir-Tien Shan are older providing a land

refuge (10 million years old; Abdrakhmatov et al.,

1996), taxa in the Caspian-Aral Basin may show differ-

ent levels of divergence.

Taxonomic Recommendations. - Because Trapelus

sanguinolentus in the Caspian-Aral Basin is distin-

guished from Trapelus agilis of the Iranian Plateau by

10.9% sequence divergence for the mitochondrial DNA

segment spanning from nadl to coxl (Macey et al.,

2000b), we consider them separate species. No more

than a single fixed difference is observed between pop-

ulations of Trapelus in the Caspian-Aral Basin.

Therefore, we interpret these populations to be a single

taxon, T. sanguinolentus. Further work comparing pop-

ulations in Southwest Asia is needed in order to deter-

mine the specific status of these populations.

Acknowledgments

This work is LBNL-54654 and was performed under the

auspices of the U.S. Department of Energy, Office of

Biological and Environmental Research, under contract

No. DE-AC03-76SF00098 with the University of

California, Lawrence Berkeley National Laboratory.

This work was also supported by grants from the

National Geographic Society (4110-89 and 4872-93 to

Theodore J. Papenfuss and J.R.M.), Russian Foundation

of Basic Research (N 02-04-48720 to N.B.A.), Scientist

School (NS 1647.2003.4 to N.B.A.), the California

Academy of Sciences and the Museum of Vertebrate

Zoology. We thank Tatjana N. Duysebayeva for tissue

specimens. Nikolai Orlov, Theodore J. Papenfuss,

Sakhat M. Shammakov, and Boris S. Tuniyev aided with

field work. Kraig Adler and Allan Larson provided valu-

able comments on an earlier draft of the manuscript. The

first author thanks David B. Wake and Margaret F. Smith

2004

Asiatic Herpetological Research

Vol. 10, p. 214

for the opportunity to collect allozymic data at the

Museum of Vertebrate Zoology.

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M. W. Hamburger, T. A. Herring, K. B. Kalabaev, V.

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46. (In Russian).

Bannikov, A. G., I. S. Darevsky, V. G. Ishchenko, A. K.

Rustamov, and N. N. Shcherbak. 1977. [Guide to

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Clayton, J. W., and D. N. Tretiak. 1972. Amine-citrate

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Harris, H., and D. A. Hopkinson. 1976 et seq. Handbook

of Enzyme Electrophoresis in Human Genetics,

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Papenfuss. 2000a. Phylogenetic relationships

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2004

Asiatic Herpetological Research

Vol.10, pp. 215-216

The Feeding Biology of Rana macrocnemis Boulenger, 1885

(Anura: Ranidae), Collected in llludag, Bursa, Turkey

iSMAlL H. UGurta^, Hikmet S. Yildirimhan, and Mehmet Kalkan

Uludag University’ Science-Art Faculty ; Department of Biology’ Bursa-Turkey

Abstract. - In this study gut contents of 64 mature specimens (34 male, 30 female) from Rana macrocnemis popula-

tion collected from Uludag(Bursa) are analyzed. The results indicate that the majority (68.05%) of the food items is

composed of insects.

Key words. - Rana macrocnemis , feeding, stomach content.

Introduction

Rana macrocnemis is a very common species in the

northern and eastern Caucasus and has dispersed into

Western and Northern Anatolia in Turkey. Also known

as a “mountain frog”, its altitudinal distribution ranges

from 1,000 to 2,300 m. It generally lives in open areas

or in small brooks in or near the woods. It is also seen in

areas w ith muddy bottoms or close to water. Many stud-

ies have been conducted to find out the feeding biology

of amphibia (Bohme 1975; Boulenger, 1897; Schreiber,

1912; Beschkov, 1970; Lamb, 1984; Yilmaz, 1984;

Sampetro, 1986; Gittins, 1987; AtatUr, 1993; Ugurtas

1995), but no detailed study exists on the feeding biol-

ogy of Rana macrocnemis. The aim of this study is to

establish various animal groups that are taken as prey by

this species.

Materials and Methods

The specimens of Rana macrocnemis used in this study

were collected in three localities between June and July

1997 (Fig. 1). These localities are:

Kirazlyayla (1 6 males, 30 females)

Hotels Area (10 males)

(^obankaya (8 females)

The specimens were found between the hours 730

and 1930 hours in daylight, but were observed to appear

more often between 1030 and 1500 hours. We used

Parker (1982), Lodos (1983, 1986), and Caglar and

Demirsoy (1992, 1999) to identify prey items.

Results

We did not observe any significant discrepancies in the

stomach contents of males and females. Thus, they were

evaluated together. Of the 64 specimens collected dur-

Figure 1 . Localities where Rana macrocnemis speci-

mens were collected.

ing the feeding period, two had empty stomachs.

Among stomach contents which were investigated, 626

prey items were counted. Of these prey items, 426

(68.05%) belonged to Insecta, 36 (5.75%) to Arach-

nida, 44 (7.02%) to Gastropoda, 4 (0.63%) to Myri-

apoda, 112 (17.89%) to lsopoda and 2 (0.31%) to

Acarina groups. Two (0.31%) juveniles of Rana mac-

rocnemis were also found as stomach content.

The number of prey items found in stomachs and

their taxonomy are listed below. It was found that the

majority of food taken by Rana macrocnemis was com-

posed of insects (68.05%). 144 (36.15%) were

Coleoptera, 82 (19.24%) Plecoptera, 94 (22.06%)

Diptera, 40 (9.38%) Hymenoptera. 36 (8.45%) Odonata,

6 ( 1 .40%) Orthoptera, 6 ( 1 .40%) Lepidoptera, 4 (0.93%)

Homoptera and four (0.93%) in Hemiptera (Fig. 2). As a

result of this study on the stomach contents, we con-

□ Cole op be ra (36 15 %)

■ Plecoptera (1 9 24 %)

□ Diptera (22 06 %)

□ Hymenoptera (9 38 %)

■ Odonata (8 4 5 %)

□ Orthcptera (1 40 %)

□ Lep ideptera (140%)

■ Homoptera (0 93 %)

M Hemiptera (0 93 %)

Figure 2. The precentages of insect groups taken as

prey.

elude that Rana macrocnemis is an opportunity feeder

that utilizes any prey in its environment that it has the

ability to consume.

Acknowledgments

Demirsoy, A. 1999. Ya amin 7'emel Kurallar, Omurgas-

zlar -Bocekler Di§inda, Cilt II, Kisim I, Meteksan

A. Ankara, S, 724-939.

Gittins, S. P. 1987. The Diet of the Common Toad ( Bufo

bufo) Around A Pong in Mid-Wales. Amphibia-

Reptilia 8: 13-17.

Lamp, T. 1984. The Influence of Sex and Breeding Con-

dition on Microhabitat Selection and Diet in the Pig

Frog Rana gryllio. 1 he American Midland Natural-

ist 1 1 1(2):31 1-318.

Lodos, N. 1983. Tiirkiye Entomolojisi (Genel Uygula-

mal ve Faunistik), Cilt I Ege Universitesi Matbaas

Ziraat Fak. Yayinlari 282:134-336

Lodos, N. 1986. Tiirkiye Entomolojisi (Genel Uygula-

mal ve Faunistik), Cilt II Ege Universitesi Matbaas

Ziraat Fak. Yaynlar 429:57-498

This work was supported by grants from Uludag Uni-

versity Scientific Research Fund (2001/60)

Literature Cited

Atatiir, M. K. 1993. A Preliminary Study on the Feeding

Biology of Rana ridibunda (Anura, Ranidae) popu-

lation from Bey^ehir Lake. Turkish Journal of Zool-

ogy 17(2): 127- 131.

Beschkov, V. 1970. Biologie und Verbreitung des

Griechischen Froschers {Rana graeca BLGR.) (In

Bulgarian) Academie Bulgare des Sciences. Bulle-

tin de L'institut de Zoologie et Musee. Tome 31:5-

17.

Boulenger, G. A. 1897. The Tailless Batrachians of

Europe. Part. I. Addlard and Son. Hanover Square,

London

Bohme, W. 1975. Zum Vorkommen von Pelobates syri-

aens Boettger, 1889 Griechland. Senck. Biol.

56:199-202.

£aglar, M. 1974. Omurgasiz Hayvanlar, Anatomi-

Sistematik. II. Kisim. U. Yayinilar, Fen Fak, Sayi

123, Fen Fakultesi Basimevi, Istanbul, S, 157-206.

Demirsoy, A. 1992. Yaamn Temel Kurallari,

Omurgasizlar - Entomoloji. Cilt II, Kisim II,

Meteksan A. Ankara, S, 338-814.

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Book Company.

Sampedro, M. A., and L. Montanez. 1986. Food of

Rana catesbeiana in Two Different Areas of Cuba.

P. 413-416. In Z. Rocek (ed.). Studies in Herpetol-

ogy. Charles University, Prague.

Schreiber E. 1913. Herpetologia Europea. Gustav Fis-

cher, Jena.

Ugurta§, . H., and M. Oz . 1995. Bursa ve Sakarya li

Pelobates syriacus (Anura, Pelobatidae)

Populasyonlarmin Beslenme Biyolojisi Uzerine Bir

On Cali§ma. Turkish Journal of Zoology 19:273-

275.

Yilmazj. 1984. Trakya Kuyruksuz Kurbagalari Uzerine

Morfolojik ve Taksonomik Bir Ara§tirma. Do§a Biy

oloji, S. A2, 8(2): 244-264.

[2004

Asiatic Herpetological Research

Vol. 10, pp. 217-223

Morphological Observations on the Erythrocyte and Erythrocyte

Size of Some Gecko Species, Turkey

Murat Sevinc*, Ismail Hakki UGurta§, Hikmet Sami Yildirimhan

Uludag University, Science and Art Faculty, Department of Biology, Bursa, Turkey

* To whom correspondence should be addressed; E-mail: smurat@uludag.edu.tr

Abstract. - In this study, erythrocyte size and morphology of the four gecko species [Asaccus elisae, Hemidactylus

turcicus, Cyrtopodion scaber and C. heterocercus mardinensis (Gekkonidae)] from Turkey were examined. Forty-two

specimens were used in this study, of which twelve were A. elisae, eight were H. turcicus , twelve were C. scaber, and

ten were C. h. mardinensis. Erythrocyte morphology of these examined species was described using Wright’s tech-

nique. The sizes of erythrocytes and their nuclei were measured using an ocular micrometer at a magnification of

1600x. The results of this study were compared with previous works on the other reptile species. The longest erythro-

cytes were found in H. turcicus and the shortest in A. elisae. In terms of the studied species, the nucleus and erythro-

cyte sizes were found to be correlated (Gekkonidae: r = 0.39; P < 0.001).

Key words. - Gekkota, Turkey, erythrocyte.

Introduction

Initial studies on the blood of reptiles described the

structures, often comparing them with those of the other

vertebrates. Literature on the haematology of reptilian

blood are based on a few studies where most were con-

cerned with especially European species (Saint Girons,

1970).

Various authors have focused on the different circu-

lating blood cell types of different reptiles (Taylor and

Kaplan, 1961; Heady and Rogers, 1963; Hartman and

Lessler, 1964; Szarski and Czopek, 1966; Duguy, 1970;

Saint Girons, 1970; Mateo et al., 1984; Canfield and

Shea, 1988; Cannon et al., 1996; Alleman et al., 1999;

Sevin? et al., 2000; Atatiir et al., 2001; Sevinc and Ugu-

rta§, 2001; Ugurta§ et al., 2003). Some authors have

studied seasonal (Hutton, 1960; Cline and Waldman,

1962; Haggag et al., 1966) or sexual (Altland and

Thompson, 1958) variations in the number of blood

cells of different reptile species. In addition, researchers

have studied the number of blood cells of different rep-

tiles (Baker and Kline, 1932; Charipper and Davis,

1932; Altland and Thompson, 1958; Hutton, 1961;

Hutchinson and Szarski, 1965; Engbretson and

Hutchinson, 1976; Mateo et al., 1984). Furthermore,

authors have also studied haemoglobin and hematocrit

content of blood and hematopoiesis of different reptiles

(Altland and Thompson, 1958; Hutton, 1961; Goin and

Jackson, 1965; Engbretson and Hutchinson, 1976;

Newlin and Ballinger, 1976; Mateo etal., 1984; Alleman

et al., 1999).

In Turkey, hematological studies have generally

been conducted on humans and some economically

important animals. However, there are few hematologi-

cal studies of the reptiles living in this country (Sevin?

et al., 2000; Atatiir et al., 2001; Sevin? and Ugurta§,

2001; Ugurta§et al., 2003).

In the current study, our aim was to describe and

measure erythrocytes of Asaccus elisae (Werner, 1895),

Hemidactylus turcicus (Linnaeus, 1758), Cyrtopodion

scaber (Heyden, 1827) and C. heterocercus mardinensis

(Mertens, 1924) which live in Turkey. This study is the

first of its kind on Turkish species.

Materials and Methods

In this study, twelve (6 males, 6 females) individuals of

Asaccus elisae, eight (4 males, 4 females) of

Hemidactylus turcicus, twelve (8 males, 4 females) of

Cyrtopodion scaber and ten (4 males, 6 females) of C.

heterocercus mardinensis (Gekkonidae) were examined.

Twenty-two specimens examined were male and twenty

were female.

The study was performed on 01-05 June 2000. H.

turcicus species were collected from Hatay (36° 34' N,

36° 09' E) and the other specimens were from §anliurfa

(36° 53' N, 39° 02' E) (Fig. 1; Table 1). Blood was

obtained by cutting the tail (Duguy, 1974). Immediately

after blood was obtained in heparinized capillary tubes,

blood smears were prepared. Three or five blood smears

were prepared per individual. The smears were air-dried

and stained with Wright’s stain (Hartman and Lessler,

1964). Twelve drops of Wright’s stain were dropped on

the slides and allowed to remain on the slide one and

half minutes before rinsing with phosphate buffer (pH

6.5). The slides were allowed to stand for ten minutes at

room temperature, were washed with distilled water,

and allowed to dry.

Vol. 10, p. 218

Asiatic Herpetological Research

2004

On each slide, fifty mature erythrocytes and their

nuclei were measured by means of an ocular micrometer

at a magnification of 1600x. In this way fifty erythrocyte

sizes were calculated. Erythrocyte and nucleus measure-

ments of examined species are given in tables 2-5.

Erythrocyte and nucleus sizes were, respectively, calcu-

lated according to the formulas [(EL x EW x pi) / 4] and

[(NL x NW x pi) / 4]; where EL is the erythrocyte length,

EW is the erythrocyte width, NL is the nucleus length

and NW is the nucleus width.

Results

Erythrocytes, or red blood cells, of geckos are nucleat-

ed, oval cells. Their nuclei are also oval and centrally

located, like those of the other reptiles. The cytoplasm of

mature erythrocytes appeared both light, dark pink, and

homogeneous under Wright’s stain. Nuclei of mature

erythrocytes are chromophilic (Figs. 2-5).

Because there were no significant differences

between the erythrocyte sizes of female and male geck-

os, data from the females and males of individual

species were combined.

The longest erythrocytes were found in Hemi-

dactylus turcicus. The mean length of mature erythro-

cyte of H. turcicus was 16.98 mm (± 1.26 standard devi-

ations, with a range of 14.64-19.52 mm) (Table 2; Fig.

6) and also erythrocyte size and length/width ratios of H.

turcicus are given in table 2.

The shortest erythrocytes were found in Asaccus

elisae. The mean length of mature erythrocytes of A.

elisae was 14.96 mm (± 0.79 standard deviations, with a

range of 13.42-17.08 mm) (Table 3; Fig. 6). Erythrocyte

size and length/width ratios of A. elisae are given in

table 3.

The widest erythrocytes were found in Cyrtopodion

scaber. The mean width of mature erythrocytes of C.

scaber was 10.26 mm (± 0.78 standard deviations, with

a range of 8.54-12.20 mm) (Table 4; Fig. 7). Erythrocyte

size and length/width ratios of C. scaber are given in

table 4.

The narrowest erythrocytes were found in

Cyrtopodion heterocercus mardinensis. The mean width

of mature erythrocyte of C. h. mardinensis was 9. 1 8 mm

(± 0.70 standard deviations, with a range of 6.71-10.98

mm) (Table 5; Fig. 7) and also erythrocyte size and

length/width ratios of C. h. mardinensis are given in

table 5.

The longest nuclei were found in Cyrtopodion

scaber. The mean length of mature nuclei of C. scaber

Table 1. Materials list. NM: number of males; NF: number of females; CD: collection date; CL: collection locality. All

specimens are from the Zoology Museum in Uludag UniversityScience and Art Faculty, Department of Biology.

2004

Asiatic Herpetological Research

Vol. 10, p. 219

Figure 2. Erythrocyte and nucleus sizes of Hemidactylus

turcicus.

Figure 4. Erythrocyte and nucleus sizes of Cyrtopodion

scaber.

was 6.81 mm (± 0.60 standard deviations, with a range

of 5.49-8.54 mm) (Table 4; Fig. 6). Nucleus size and

length/width ratios of C. scaber are given in table 4.

The shortest nuclei were found in Asaccus elisae.

The mean length of mature nuclei of A. elisae was 6.06

mm (± 0.58 standard deviations, with a range of 4.88-

7.32 mm) (Table 3; Fig. 6). Nucleus size and

length/width ratios of A. elisae are given in table 3.

The widest nuclei were found in Cyrtopodion hete-

rocercus mardinensis. The mean width of mature nuclei

of C. h. mardinensis was 3.78 mm (± 0.44 standard devi-

ations, with a range of 3.05-4.88 mm) (Table 5; Fig. 7).

Nucleus size and length/width ratios of C. h. mardinen-

sis are given in table 5.

The narrowest nuclei were found in Hemidactylus

turcicus. The mean width of mature nuclei of H. turcicus

was 3.53 mm (± 0.42 standard deviations, with a range

of 3.05-4.27 mm) (Table 2; Fig. 7). Nucleus size and

length/width ratios of H. turcicus are given in table 2.

Discussion

Investigations carried out by various authors (Hartman

Figure 3. Erythrocyte and nucleus sizes of Asaccus

elisae.

Figure 5. Erythrocyte and nucleus of Cyrtopodion hetero-

cercus mardinensis.

and Lessler, 1964; Szarski and Czopek, 1966; Saint

Girons, 1970; Seving et al., 2000; Seving and Ugurta§,

2001; Atatiir et al, 2001; Ugurta§et al, 2003) reported

that the sizes of erythrocytes vary in members of the

four orders of reptiles.

Within the class Reptilia, the largest erythrocytes

are seen in Sphenodon punctatus , turtles, and crocodil-

ians (Hartman and Lessler, 1964; Saint Girons, 1970;

Alleman et al., 1984).

Cryptodiran turtles have the largest erythrocytes

from all previously studied reptiles (Saint Girons, 1970).

The shortest erythrocytes are found in the Lacertidae

family (Hartman and Lessler, 1964; Saint Girons, 1970;

Seving et al., 2000; Seving and Ugurta§, 2001).

Saint Girons (1970) reported erythrocytes and

nuclei measurements of some gecko species. In

Coleonyx variegatus, erythrocyte length is 18.9 pm and

width is 9.6 pm; nucleus length is 7.3 pm and width is

3.7 pm. In Gehyra variegata, erythrocyte length is 17.2

pm and width is 1 1.5 pm; nucleus length is 6.3 pm and

width is 3.8 pm. In Heteronota binoei, erythrocyte

length is 21.4 pm and width is 10.7 pm; nucleus length

is 8.1 pm and width is 3.4 pm.

Vol. 10, p. 220

Asiatic Herpetological Research

2004

Table 2. Erythrocyte dimensions of Hemidactylus turcicus with standard deviations. EL: erythrocyte length, EW. ery

throcyte width; ES: erythrocyte size; NL: nucleus length; NW: nucleus width; NS: nucleus size.

Table 3. Erythrocyte dimensions of Asaccus elisae with standard deviations. EL: erythrocyte length; EW: erythrocyte

width; ES: erythrocyte size; NL: nucleus length; NW: nucleus width; NS: nucleus size.

Table 4. Erythrocyte dimensions of Cyrtopodion scaber with standard deviations. EL: erythrocyte length; EW: ery-

throcyte width; ES: erythrocyte size; NL: nucleus length; NW: nucleus width; NS: nucleus size.

Table 5. Erythrocyte dimensions of Cyrtopodion heterocercus mardinensis with standard deviations. EL: erythrocyte

length; EW: erythrocyte width; ES: erythrocyte size; NL: nucleus length; NW: nucleus width; NS: nucleus size.

2004

Asiatic Herpetological Research

Vol. 10, p. 221

12

Asaccus elisae Hemidactylus Cyrtopodion C. heterocercus

turcicus scaber mardinensis

Dl Erythrocyte

@ Nucleus

Examined species

Figure 6. Erythrocyte and nucleus lengths of examined specimens.

Cannon et al. (1996) reported the leukocyte mor-

phology and size of the roughtail gecko Cyrtopodion

scabrnm. However, they did not report any information

on the erythrocyte of this species.

In reptiles, the numbers of erythrocytes are smaller

than in mammals or birds. Lizards have more erythro-

cytes than snakes, and turtles have the fewest. Since

lizards have the smallest erythrocytes of all reptiles, and

turtles the largest, there may be an inverse correlation

between the number of erythrocytes and their size; this

hypothesis was advanced by Ryerson (1949) (Duguy,

1970).

In this study, the longest erythrocytes were found in

H. turcicus, the shortest in A. elisae, the largest in C.

scaber and the narrowest in C. heterocercus mardinen-

sis. The longest nuclei were found in C. scaber, the

shortest A. elisae , the largest in C. heterocercus mardi-

nensis and the narrowest in H. turcicus (Tables 2-5; Figs.

6,7).

In the present study, erythrocyte morphology and

the results of erythrocytes and nuclei sizes (Tables 2-5;

Figs. 6,7) are agreement with the other results carried

out by (Saint Girons, 1970).

Acknowledgments

The authors would like to thank to MSc. student

Abdulmiittalip Akkaya for helping during studies.

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2004

Asiatic Herpetological Research

Vol. 10, pp. 224-229

Distribution and Conservation Status of Neurergus microspilotus

(Caudata: Salamandridae) in Western Iran

Mozafar Sharifi* and Somayeh Assadian

Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran.

E-mail: sharifimozafar@hotmail. com

Abstract. - Field and laboratory observations of the Yellow Spotted Newt, Neurergus microspilotus (Nestrov, 1917),

in western Iran have yielded preliminary data on conservation biology and distribution of this species. New distribu-

tional ranges have been determined for Neurergus microspilotus in its Iranian range in the mid-Zagros Mountains. In

streams occupied by Neurergus microspilotus, dissolved oxygen, temperature, discharge, N03, and P04 were meas-

ured. Land use practices, adjacent riparian habitats and channel substrate were also determined. Four new stream

habitats were identified. On the basis of interviews with local inhabitants, three other streams were identified as like-

ly habitat for Neurergus microspilotus. Measurements of relative abundance of N. microsphilotus indicate that this

animal is likely to occur in higher numbers in cold and first order streams located at high altitudes in the western edge

of the Iranian plateau on the mid-Zagros Range. The limiting factor for the yellow spotted newts in western Iran

appears to be human disturbance. In the last four years, one of the five known streams with N. microspilotus, in the

area of Ghorighala, has virtually lost its entire population due to pollution by a tourist facility and local sewage efflu-

ence.

Key words. - Neurergus microspilotus , salamander, first order stream, distribution, conservation.

Introduction

Available information on the conservation biology of the

western Iranian salamanders is scarce. Investigations

made in the 1970s (Schmidtler and Schmidtler, 1975)

indicated that three of four species of salamanders

belonging to the genus Neurergus {N. crocatus, N.

microspilotus and N. kaiseri ) occur in Iran. There is no

recent information on distribution and abundance of

these species for assessment of conservation. However,

a world-wide concern over declines in amphibian popu-

lations (Wake, 1991; Gardner, 2001) is equally pertinent

in remote areas of western Iran. Amphibians are sensi-

tive to land-use alteration (Wilkins and Peterson, 2000)

and there is widespread concern that environmental pol-

lution and land deterioration are responsible for their

decline (Richardson, et al 2000). Several factors are

known to have contributed to the declines, including

habitat destruction (Sala et al, 2000), fragmentation of

habitat (Sjogren, 1991, Marsh and Trenham, 2000), and

alteration of species composition of communities

through the introduction of exotic predators and

pathogens (Beebee, 1977). In addition, acidification and

other chemical pollution, alteration of climate (Pounds

and Crump, 1994), disease and road kill (Carey, 1993,

2000) are candidates for the amphibian decline.

Relatively few caudate species occur in Iran. These

include seven species of the genera Triturus,

Batrachuperus, Neurergus, and Salamandra (Balutch

and Kami, 1995). Newts of the genus Neurergus have a

relatively wide geographic distribution, ranging from

western Iran (Zagros Mountains) and extending into Iraq

and southern Turkey (Balutch and Kami, 1995). There is

no sufficient information regarding the geographic dis-

tribution of the three species of newts that occur in west-

ern Iran. Previous investigations indicate that the pri-

mary distribution range of Neurergus microspilotus is in

the mid-Zagros range at the border of Iran and Iraq

(Nesterov, 1917; Schmidtler and Schmidtler, 1975). This

information also indicates that Neurergus kaiseri and

Neurergus crocatus are expected to occur in southern

and northern parts of the Zagros Range, respectively.

Recent investigations on N. microspilotus confirms that

this newt occurs in highland streams in the mid-Zagros

region (Assadian and Sharifi, 2002; Rastegar Pouyani

and Assadian, 2002).

The aims of the present study are to determine the

geographic distribution and conservation biology of

Neurergus microspilotus. To improve conservation

efforts related to this species, information is needed on

physico-chemical characters of the habitat. For this rea-

son, we measured some variables in the aquatic environ-

ment and adjacent terrestrial habitats.

Vol. 10, p. 225

Asiatic Herpetological Research

2004

Figure 1. Geographic distribution of Neurergus microspilotus in streams of the mid-Zagros Range in western Iran.

Those streams with the species have been shown by (1). Those streams that expected to have the animal are shown

by (2).

Study Areas

The Iranian basin is a large triangular depression flanked

by Elbourz Mountains in the north and the Zagros

Mountains in the west. The Zagros Mountains extend

diagonally from eastern Turkey to the north of the

Persian Gulf and Pakistan border. This range is part of a

greater geographic unit arising from the east of the

Anatolian Plateau of Turkey and expanding southward

to include Iran, Afghanistan, Pakistan and further east to

the western edge of the Tibetan Plateau. The Zagros

Mountains act as barriers to the incoming air parcels

from the west and receive precipitation according to

their height and longitude. In general, the northern and

western portions of the range receive considerably more

rainfall than those in the south and east. The average

annual precipitation in the northern Zagros ranges from

400 to 800 mm. per year. Most of the central and south-

ern Zagros receive between 300 and 500 mm

(Ghobadian, 1990).

The western Zagros Range meets the northern

Mesopotamian Plain, a low land with a hot and dry cli-

mate. In some parts of the Zagros Range, where this

meeting takes place over a relatively short distance a

steep environmental gradient is encountered where high

altitude and cold climate from the Iranian Plateau dif-

fuse into the low altitude and warm Mesopotamian Plain

in just few kilometers. The weather condition in the

western edge of the Iranian Plateau in the mid-Zagros

Range is characterized by a pronounced seasonal varia-

tion including a long freezing period in winter and a

mild summer. Although the average annual precipitation

in this area is around 500 mm, most of this comes as

snow. As a result, many seasonal and permanent streams

at the western side of the Zagros Range are nourished by

heavy snow accumulated on the high mountains. In the

lowlands of the northern Mesopotamian Plain, which in

some parts lie only 20 or 30 km from cold uplands, sum-

mers are hot and dry and winters are free of frost.

Precipitation in this area approaches 400 mm per annum,

rarely appearing as snow. Information obtained from

Ravansar Synoptic Station (20 km from Kavat Stream in

the highlands) and Sarepolezahab on the northern

Mesopotamian Plain (40 km away from Kavat Stream)

summarizes the annual climatological data for these two

contrasting environments.

Materials and Methods

Streams, ponds, and springs were searched for adults

and larvae of Neurergus microspilotus in the mid-Zagros

Range in Kermanshah and Kurdistan provinces in west-

ern Iran in the spring and summer 2001 and 2002. In

streams where the salamander was found, channel sub-

strate, channel width, adjacent riparian plant community

type, and land use practice were determined. Where pos-

sible, relative abundance of N. microspilotus was deter-

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Vol. 10, p. 226

Table 1. Altitude at head stream, approximate length of the streams and amount of discharge (I/s) in streams where

Neurergus microspilotus was sighted.

* Based on measurement made by department of water resource.

** - Discharge measured in field by determining the velocity of water and the extent of cross-section.

mined and expressed as individuals per every ten paces.

In small streams where there was no routine hydrologi-

cal measurement of water discharge, the water discharge

was estimated by measuring velocity of water and extent

of cross-section width of the channel. In Kavat Stream,

where highest relative abundance of N. microspilotus

was found, visual estimates were made of percent chan-

nel substrate composition (Wilkins and Peterson, 2000)

by bedrock, boulder (>256mm diameter), cobble (64-

256 mm diameter), gravel (16-64 mm diameter), pebble

(2-16 mm diameter), fine sediment and coarse woody

debris. In these streams several water characteristics

were measured. These include dissolved oxygen

(Winkler method), temperature (glass thermometer),

electrical conductivity (conductivity meter), N03 and

P04 (spectrophotometer).

Results

The geographic distribution of Neurergus microspilotus

in its Iranian range is shown in Figured. These are

Kavat Stream (34° 53' N, 46° 31' E), Dorisan Stream

(35° 21 ' N, 46° 24' E), Ghorighaleh Stream (34° 54' N,

46° 30' E), Najar Stream (35° 06' N, 46° 19' E), and

Paveh Rood Stream (35° 06' N, 46° 17' E). Apart from

streams in which the newt has already been observed,

there are three other streams where, on the basis of inter-

views with local inhabitants, the presence of this animal

is likely. These streams are upstream of Marakhil River

(35° 02’ N, 46° 1 V E), Shamshir Stream (34° 59’ N, 46°

25’ E) and Hajij Stream (35° 08’ N, 46° 19’ E). Altitude,

approximate length of the streams in which N. microspi-

lotus is expected to occur, geographic position, and

water discharge are shown in Table 1 .

Physico-chemical characteristics in streams with N.

microspilotus are shown in Table 1. Water analysis has

been carried out in upper and lower reaches of

Ghorighala Stream in order to demonstrate the human

impact on the water quality.

Occurrence of the yellow spotted newt in different

aquatic microhabitats has been evaluated using the

Wilkins and Peterson (2000) classification of channel

substrate including bedrock, boulder, cobble, gravel,

pebble and fine sand sediment. The yellow spotted newt

occupies an assortment of aquatic microhabitats during

the breeding season. Visual determination of substrate

texture in Kavat Stream indicated that this newt tended

to occupy substrates that are gravel or pebble (60%).

Figure 3 demonstrate the frequency distribution of sub-

strate classes used by this newt.

Table 2. Physico-chemical characteristics of water where Neurergus microspilotus was found.

Vol. 10, p. 227

Asiatic Herpetological Research

2004

50

35

25

15

5

-5

Sarpolzahab Climograph

Figure 2. Climographs representing the pattern of precip-

itation and temperature in Ravansar at the western edge

of the Iranian Plateau and Sarepolezahab in the northern

Mesopotamian Plain. Data are 20 years mean monthly

temperature and rainfall collected at the synoptic stations

in these two cities.

Discussion

The presence of Neurergus microspilotus in Ghorighaleh

Stream has also been reported in previous studies

(Nesterov, 1917; Schmidtler and Schmidtler, 1975).

Assadian and Sharifi (2002) and Rastegar Pouyani and

Assadian (2002) have reported Neurergus microspilo-

tus in this stream. Papenfuss and Sharifi also collected

several salamanders from this stream in Spring 2000.

No information is available regarding the occurrence of

Neurergus microspilotus in other streams, therefore, the

other four streams are new records for N. microspilotus

in its Iranian range.

All Neurergus streams reported in this study with

originated from the western edge of the Iranian Plateau

(Figure 2) and join to the Dez-Karkheh watershed sys-

tem in the northern Mesopotamian Plain and finally

enter into the Persian Gulf. All these stream are first

order streams located at relatively high altitude (1100-

1600 m) and join to the main rivers in the lowland (300-

600 m) of the catchments (Table 1).

Neurergus microspilotus is a medium size salaman-

40

Bedrock Boulder Cobble Gravel Pebble Sand

Figure 3. Percent occurrence of Neurergus microspilo-

tus in various substrate size group in Kavat Stream

(n=42).

der with a slender body. Adults reach a length (snout to

vent) of 60-70 mm (mean=65.6, sd=4.63, n=20). Adults

are black dorsally and laterally, with greenish yellow

blotches. The spots are distributed on the salamander’s

body without an obvious pattern. Neurergus microspilo-

tus characteristically possess broad heads with blunt,

rounded snout. N. microspilotus is also structured for

swimming using their laterally compressed tails for

propulsion and steering during swimming.

The prevailing climatic conditions are distinctly

different between and within streams. Since these

streams are located at the western edge of the Iranian

Plateau, the climatic conditions may vary considerably

at the upper reaches compared with lower reaches of the

same streams. At the same time it appears that streams

closer to the Mesopotamian Plain are experiencing cli-

matic conditions that are different with those that are

located at the western edge of the Iranian Plateau.

Because of the steep environmental gradient the streams

occupied by Neurergus microspilotus can be convenient-

ly divided into two groups. Those located in the high

altitude and cold weather regions on the western Iranian

Plateau (Kavat, Ghorighaleh, Dorisan and Shamshir

streams) and those in the north and north eastern part of

the range which because of lower elevation experience

warmer climate (Marakhil River, Dareh Najar and

Darian streams). In Dareh Najar Stream where very few

Neurergus microspilotus were located, and also in

Marakhil and Darian streams where the animal is report-

edly seen, it is possible that the animal drifted by the

action of water currents. It is also possible that the lower

relative abundance in N. microspilotus in Dareh Najar

and possibly in the other two streams is due to the lower

altitude and the vicinity to the northern Mesopotamian

Plain.

Terrestrial habitats occupied by N. microspilotus

include diverse community types including oak-pista-

chio open woodlands dominated by Quersus branti and

Pistachio spp. This woodland grows on various soil

2004

Asiatic Herpetological Research

Vol. 10, p. 228

types, including deep sandy loam soils at the bottom of

valleys or gravelly soils on the slopes of steep valleys.

In warmer parts of its range, riparian vegetation may

also contain willow ( Salix spp.) or shrubs such as

Cerrasns and Amygdale (Amygdalus spp.). In colder

parts of the range the riparian vegetation may be charac-

terized by more hydrophobic plants such as sedges

0 Carex spp.) and sphagnum moss (, Sphagnum spp.).

Neurergus microspilotus moves from its wintering

site to the breeding streams as soon as the spring melt

occurs, from late January through early March. Within

its range, in high altitude-cold weather regions, egg-lay-

ing was observed in early May. However, it appears

that the reproductive pattern of N. microspilotus is not

tightly synchronized because unhatched eggs have been

observed as late as mid-June. No breeding activity, eggs,

or juveniles of N. microspilotus have been observed in

the low altitude warm climate part of the range. Eggs of

N. microspilotus are laid singly or in small clumps on

vegetation or on rocks. The number of oocytes in a

female dissected in laboratory was 108. Laboratory

observations of larval growth and development indicate

that larvae complete the metamorphosis in the first year.

In early autumn they still possess their gills. Larvae with

large heads, well developed dorsal fins, and bushy gills

have the ability to react suddenly with a whole body

reaction to external stimulus.

Although no information is available regarding

wintering activity of Neurergus microspilotus in its

Iranian range, the appearance of the animal in early

spring and disappearance in summer implies that this

newt requires both upland and wetland habitat that con-

tain suitable aquatic environment during the breeding

season and subterranean burrows appropriate for winter-

ing. These normally include an aquatic environment for

breeding and a terrestrial habitat where juveniles and

adults spend most of their time.

Habitat loss through divergence of streams for irri-

gation of cultivated lands is probably the single most

important factor that threatens Neurergus microspilotus

in its Iranian range. Traditionally, due to the lack of land

in steep valleys in the mid-Zagros Range, extensive

attempts have been made to construct a complex of rein-

forced terraces of land, which is cultivated for walnut

and other orchard trees. Water is diverted from its natu-

ral channel to irrigate these lands. Although no harm is

directed toward N. microspilotus in these orchards, the

impact of land use alteration especially in dry periods

causes many of these creatures to be deprived of a

healthy aquatic environment.

Although human settlement in the mid-Zagros area

is characteristically less developed compared with other

localities in western Iran, Neurergus microspilotus is

experiencing an environmental impact similar to that

found in more urbanized areas in the country. For exam-

ple, Ghorighaleh Stream originates from a cave that has

been developed by a reclamation project for visitors.

Since the construction of this unit the stream is suffering

from gross pollution caused by thousands of visitors.

Changes in water characteristics in the upper and lower

reaches of the stream are shown in Table 2. Although in

2000 and 2001 numerous Yellow Spotted Newts were

reported (Assadian and Sharifi, 2002; Rastegar Pouyani

and Assadian, 2002) no newts were seen in 2002. The

absence of Neurergus microspilotus is presumably due

to the human impacts resulting from an ecotourism cen-

ter developed in 1999 at the Ghorighaleh Cave where

the source of the stream is located. Massive solid waste

disposed by thousands of visitors together with raw

sewage released to the stream by residents of

Ghorighaleh Village can be observed in the upper reach-

es of this stream although only changes in dissolved

oxygen are evident in physico-chemical characteristics

measured in this study.

Conclusions

Although Neurergus microspilotus has been virtually

extirpated from one of five known breeding streams in

its Iranian range, it does not appear to be in immediate

danger of extinction because one is likely to find this

newt occur in other streams in the area. However, the sit-

uation for N. microspilotus is not promising as the major

threatening factors such as habitat destruction and water

pollution are operating. Robust populations occur in at

least in one of its habitats (Kavat Stream). However, the

lack of information essential to estimate population size

and population trends makes it difficult to assess conser-

vation status of this salamander. Future work should

examine the long-term effects of anthropomorphic

impacts associated with land use alteration and pollu-

tion.

Acknowledgments

The authors wish to express their gratitude to Professor

D. B. Wake for his great help in reviewing the manu-

script. This study was supported by Razi University

grant.

Literature Cited

Assadian, S. and Z. Sharifi. 2002. Distribution and con-

servation status of Neurergus microspilotus in west

em Iran. 1st Iranian conference on Animal Science

and Biodiversity.

Vol. 10, p. 229

Asiatic Herpetological Research

2004

Beebee, T. J. C. 1977. Enviromental change as a cause

ot Natterjack Toad (Bufo calamita) declines in

Britain. Biological Conservation 11:87-102.

Baloutch, M. and H. G. Kami. 1995. Amphibians of

Iran. Tehran University Publications. [In Farsi]

Carey, C. 1993. Hypotheses concerning the causes of the

disappearance of boreal toads from the mountains

of Colorado. Conservation Biology 7:355-362.

Carey, C. 2000. Infectious disease and worldwide

declines of amphibian populations, with comments

on emerging diseases in coral reef organisms and in

humans. Enviromental Health Perspectives,

1 08(Suppl): 143-150.

Gardner, T. 2001. Declining amphibian populations: a

global phenomenon in conservation biology.

Animal biodiversity and conservation 24.2:25-44.

Ghobadian, A. 1990. Natural features of the Iranian

Plateau. Kerman University Publication Centre.

Kerman, Iran.

Marsh, D. M. and P. C. Trenham. 2000. Metapopulation

dynamics and amphibian conservation.

Conservation Biology 15:40-49.

Nesterov, P. V. 1917. Tri novych chvostatych amfibii is

kurdistana. Annuaire du Musee Zoologique de

L’Academie des Sciences, Petrograd 21:1-30.

Pounds, J. A. and M. L. Crump. 1994. Amphibian

declines and climate disturbance: the case the

Golden Toad and the Harlequin Frog. Conservation

Biology 8:72-85.

Rastegar Pouyani, N. and S. Assadian. 2002. Sexual

dimorphism in Neurergus microspilotus

(Caudata:Salamandridae). 1st Iranian conference of

Animal Science and Biodiversity.

Sala, O. E., F. S. I. Chapin, J. J. Armesto, E. Berlow, J.

Bloomfield, R. Dirzo, E. Huber-Sanwald, L. F.

Huenneke, R. B. Jackson, A. Kinzig, R. Leemans,

M. Lodge, H. A. Mooney, M. Oesterheld, N. L.

Pofif, M. T. Sykes, B. H. Walker, M. Walker, and D.

H. Wall. 2000. Global biodiversity scenarios for the

year 2100. Science 287: 1770-1774.

Sjogren, P. 1991. Extinction and isolation gradients in

metapopulations: the case of the pool frog {Rana

lessonae). Biological Journal of the Linnean

Society 42:135-147.

Schmidtler, J. J. and J. F. Schmidtler. 1975.

Untersuchujngen an westpersischen Bergbach-

molchen der Gattung Neurergus Caudata,

Salamandridae). Salamandra 11:84-98.

Wake, D. B. 1991. Declining amphibian populations.

Science 253:860

2004

Asiatic Herpetological Research

Vol.IO, pp. 230-234

An Investigation on the Blood Cells of the Leopard Gecko,

Eublepharis angramainyu (Reptilia: Sauria: Eublepharidae)

Murat Tosunoglu1, Dinner Ayaz2, Cemal Varol Tok1, and Ba^aran Dulger1

1 Qanakkale Onsekiz Mart University, Faculty of Science-Literature, Department of Biology, Terzioglu Campus,

Qanakkale, Turkey

2Ege University, Faculty of Science, Department of Biology, 35100 Bornova, Izmir , Turkey

Abstract. - In this study, blood cell counts and sizes in three adult Eublepharis angramainyu specimens (one male,

two female) collected from SE Anatolia (Sanlurfa - Birecik). The number of erythrocytes in 1 mm3 ranged between

870,000 and 950,000 (average 910,000). The mean total length of erythrocytes was calculated as 20.35 pm, the width

as 10.59, the size as 169.68 pm2; the mean nucleus length as 7.50 pm, the width as 4.15 and the size as 24.47 pm2.

Small lymphocytes had a mean diameter of 9.78 pm, big lymphocytes 13.71 pm, monocytes 15.37 pm, neutrophiles

16.56 pm, eosinophiles 17.59 pm, and basophiles 12.87 pm. The mean length of thrombocytes was measured at 8.82

pm, and the width at 5.93 pm.

Key words. - Eublepharis angramainyu , Sauria, blood cell count, blood smears, erythrocytes, leucocytes, thromb-

ocytes.

Introduction

Eublepharis angramainyu Anderson and Leviton, 1966,

also known as the “leopard gecko”, was first found

between Masjid Soleyman and Batsvand in the Khuzes-

dan province of Iran. The species was reported to range

in the western foothills of the Zagros Mountains and

Mesopotamia in Iraq and Iran, and NE Syria with a ver-

tical distribution of 300 to 1000 meters (Anderson and

Leviton, 1966; Leviton et al., 1992; Disi and Bohme,

1996; Anderson, 1999). Studies conducted in recent

years (Go9men et al., 2002) established that the species

also inhabited SE Anatolia (Sanliurfa-Birecik).

Although there are a number of studies on the distribu-

tion, morphology and ecology of the species (Anderson

and Leviton, 1966; Leviton et al., 1992; Disi and

Bohme, 1996; Anderson, 1999; Go9men et al., 2002), a

literature review has not revealed any detailed haemato-

logical studies.

Most studies on the haematology of different spe-

cies are related to blood cell counts (Alder and Huber,

1923; Hutchison and Szarski, 1965; Duguy, 1970;

Arikan, 1989) and blood cell sizes (Szarski and Czopek,

1966; Hartman and Lessler, 1964; Atatiir et al., 1998,

1999). The number haematological studies related to

amphibian and reptile species living in Anatolia has

been increasing in recent years (Arkan, 1989; Atatiir et

al., 1998, 1999, 2001; Sevin9 et al., 2000). In this study,

the number and sizes of blood cells of Eublepharis

angramainyu were determined and photographs of their

blood cells presented.

Materials and Methods

Three adult specimens (one male, two female) examined

in this study were collected near £i9ekalan Village

between 2200-2400 hours at an altitude of 400 m during

the species breeding season (01 July, 2002). Blood sam-

ples were taken within the first three days after the spec-

imens were collected live in the wild and brought to the

laboratory.

Blood cell counts were carried out by means of

Neubauer hemocytometer. Hayem solution was used to

dilute the erythrocytes. Wright- Stained blood smears

were made use of in the measurement (erythrocytes, leu-

cocytes and thrombocytes) and computation of blood

cells. The necessary blood samples were obtained by

cardiac (ventriculus) puncture, via heparinized hemat-

ocrit capillaries. Blood cell measurements were taken by

means of a MOB-l-15x ocular micrometer. On each

blood smear, measurements related to 40 randomly cho-

sen erythrocytes (total erythrocyte length, total erythro-

cyte width, nucleus length and nucleus width) were

made, and the nucleus size was calculated) according to

the formula EL.EW./4 and the nucleus size according to

the formula NL.NW./4 (Duguy, 1970; Atatiir et&al.,

2001). Moreover, micrometric measurements were

made on leucoytes and thrombocytes. Photographs of

Vol.10, p. 231

Asiatic Herpetological Research

2004

Figure 1 : The blood cells of Eublepharis angramainyu. A-

erythrocytes, B- small lymphocyte, C- large lymphocyte,

D- monocyte, E- neutrophil, F- eosinophil, G- basophil,

H- a cluster of thrombocytes.

blood cells were taken using a Carl Zeiss Jena micro-

scope at 40x magnification.

Results

Male and female specimens were assessed together as

there were no significant differences between them with

respect to the number and size of blood cells. As in other

lizrds, the erythrocytes belonging to Eublepharis angra-

mainyu are also ellipsoidal cells with nuclei. The nuclei

are also ellipsoidal, somewhat regular and centrally

located (Figure 1A). The mean total length of the eryth-

rocytes (L) was calculated as 20.35 pm the width (W) as

10.59 pm, the size (S) as 169.68 pm2; the mean nucleus

length (NL) as 7.50 pm, the width (NW) as 4.15 pm,

and the size (NL) as 24.47 pm2. The number of erythro-

cytes in 1 mm3 of blood ranged between 870,000 and

950,000 (average 910,000) (Table 1).

Lymphocytes have a spherical shape. Both small

and large lymphocytes were examined in the blood

smears prepared (Figure IB, C). Large lymphocytes

were 13.71 pm in diameter and had a large cytoplasmic

zone and a centrally-located, large, round nucleus. The

cytoplasm is stained pale blue and the nucleus purplish

blue using the Wright Stain. No granule formation was

observed in the cytoplasm. Small lymphocytes had a

mean diameter of 9.78 pm (Table 1). The large nucleus

covers the majority of the cell’s area; the cytoplasm is in

the shape of a thin ring. Lymphocytes are the most com-

monly seen leucocytes in the preparates.

Although resembling the large lymphocytes in size,

monocytes are easily distinguished from the shape of

the nucleus (Figure ID). They have a mean diameter of

15.37 pm Granule formation was observed in the cyto-

plasm (Table 1). The nucleus is not oval, but depressed

on one side and occupies at least half of the cell. The

cytoplasm is stained light purple and the nucleus dark

blue. They are the second most common leucocytes

after lymphocytes and neutrophiles.

Neutrophiles are spherical cells with a mean diame-

ter of 16.56 pm (Table 1). Using the Wright Stain, the

cytoplasm is stained light blue and the nucleus dark

blue. There are very fine granules in the cytoplasm (Fig-

ure IE). The nucleus is a structure with lobes and seg-

ments. They are the most common leucocytes second to

lymphocytes.

Eosinophiles have a diameter of 1 7.59 pm (Table 1 ).

The cytoplasm is stained light blue and the nucleus dark

blue. Large, round, bright red granules within the cyto-

plasm strike eye as the most distinctive characteristic of

these cells (Figure IF). The nucleus was seen to have

two lobes. These cells take the fourth place in the prepa-

ration of smears after lymphocytes, monocytes and neu-

trophiles.

Basophiles are oval-shaped with a mean diameter

of 12.87 pm (Figure 1G and Table 1). When stained by

means of the Wright Stain, dark bluish purple granules

within the light blue cytoplasm are in a position marking

the dark blue nucleus. These cells are rarely seen in the

preparates.

Thrombocytes are spindle-shaped cells with a mean

length of 8.82 pm, a width of 5.93 pm (Figure 1H and

Table 1). In the Wright-Stained preparates, dark stained

cells with large oval nuclei and small irregular cytopla-

sic zones form groups of two or more.

2004

0, p. 232

Table 1: The established counts, measurements and sizes concerning the blood cells of Eublepharis angr

amainyu (in m and m2). N: Number of specimens; n: Number of measurements/computings in each speci

men; Ext: extreme values; SD and SE: standard deviations and the standard errors of the means,

respectively.

Table 2: The number of erythrocytes in 1 mm3 of blood in different lizard species.

Vol.10, p. 233

Asiatic Herpetological Research

2004

Table 3: Sizes of erythrocytes and nuclei in different lizard species according to various researchers (EL/

EW: Erythrocyte Length/Erythrocyte Width Ratio, ES: Erythrocyte Size (pm2), NL/NW: Nucleus Length/

Nucleus Width Ratio, NS: Nucleus Size (pin2), N/C: Nuclear surface/Cell surface ratio).

Discussion Literature Cited

As stated in the ‘Results’ section, E. angramainyu spec-

imens were collected during the mating season and did

not display sexual dimorphism with respect to the num-

ber of erythrocytes and sizes. It has been found that

there are significant differences among lizard families

with respect to the number and size of erythrocytes, and

the members of Gekkonidae have the highest number of

erythrocytes among lizards (Alder and Huber, 1923;

Hutchison and Szarski, 1965; Duguy, 1970). Values

belonging to the number of blood cells determined in

diffeent lizard species (Table 2), by various researchers

were compared with those we obtained for E. angra-

mainyu in the present study, and it was established that

the number of erythrocytes in 1 mm3 of blood was very

close to that of Hemidactylus turcicus (Gekkonidae)

species, but different from that of other lizard species.

Values we obtained in E. angramainyu with respect

to the sizes of erythrocytes and nuclei were compared

with those determined for some lizard species (Table 3),

and it was found that values concerning the sizes of

erythrocytes and nuclei were very close to those of spe-

cies belonging to Gekkonidae family. When compared

with the other lizard species, E. angramainyu can be

said to have the largest erythrocytes with respect to the

sizes of erythrocytes and nuclei.

Alder, A. and E. Huber. 1923. Untersuchungen iiber

Blutzellen und Zellbildung bei Amphibien und

Reptilien. Folia Haematologica 29: 1-22.

Anderson, S. C. and A. E. Leviton. 1966. A new species

of Eublepharis from Southwestern Iran (Reptilia:

Gekkonidae). Occasional Papers of the California

Academy of Science 53:1-5.

Anderson, S. C. 1999. The Lizards of Iran (Contribu-

tions to Herpetology Vol. 15). Society for the Study

of Amphibians and Reptiles, Missouri, USA. 422

pp.

Arikan, H. 1989. Anadolu'daki Rana ridibunda (Anura:

Ranidae) populasyonlarinin kan hticrelerinin sayisi

bakirmndan incelenmesi. Turkish Zoology 13:54-

59.

Atatiir, M. K., H. Arikan, and A. Mermer. 1998. Eryth-

rocyte sizes of some Urodeles from Turkey. Turkish

Journal of Zoology 22:89-91.

Atatiir, M. K., H. Arikan, andi. E. Qevik. 1999. Erythro-

cyte sizes of some Anurans from Turkey. Turkish

Journal of Zoology 23:111-114.

Atatiir, M. K., H. Arkan, i. E. £evik, and A Mermer.

2001. Erythrocyte measurements of some Scincids

from Turkey. Turkish Journal of Zoology 25:149-

152.

2004

Vo) JO, p. 234

Disi, A. M., and W. Bohme. 1996. Zoogeography of the

amphibians and reptiles of Syria, with additional

new records. Herpetozoa 9(l/2):63-70.

Duguy, R. 1970. Numbers of blood cells and their varia-

tion. Pp. 93-109. In C. Gans and F. H. Pough (eds.),

Biology of Reptilia, Volume 3. Academic Press,

London and New York.

Go9men, B., M. Tosunoglu, and D. Ayaz. 2002. First

Record of the Leopard Gecko, Eublepharis angra-

mainyn (Reptilia: Sauria: Eublepharidae) from

Anatolia. Herpetological Journal 12(2):79-80.

Hartman, F. A. and M. A. Lessler. 1964. Erythrocyte

measurements in Fisches, Amphibia and Reptiles.

Biological Bulletin 126:83-88.

Hutchison, H. V. and H. Szarski. 1965. Number of

erythrocytes in some Amphibians and Reptiles.

Copeia 3:373-375.

Leviton, A. E., S. C. Anderson, K. Adler, and S. A.

Minton. 1992. Handbook to Middle East Amphibi-

ans and Reptiles. In Contributions to Herpetology,

Vol. 8., Society for the Study of Amphibians and

Reptiles. Missouri, USA.

Sevin9, M., i. H. Ugurta§, and H. S. Yildirimhan. 2000.

Erythrocyte measurements in Lacerta rudis (Rep-

tilia, Lacertidae). Turkish Journal of Zoology

24:207-209.

Szarski, H. and G. Czopek. 1966. Erythrocyte diameter

in some amphibians and reptiles. Bulletin of the

Polish Academy of Sciences Biological Sciences

14(6):433-437.

2004

Asiatic Herpetological Research

Vol. 10, pp. 235

A Record of Boiga ochracea walli (Stoliczka, 1870) from Bangladesh

M. Farid Ahsan* and Shayla Parvin

Department of Zoology, University of Chittagong, Chittagong 4331, Bangladesh.

5jc

Corresponding author E-mail: mfahsan@ctgu.edu

Abstract. - Two specimens of Boiga ochracea specimens from Bangladesh are referred to Boiga ochracea walli.

The locality data for these specimens are lost, but they are probably form the University of Chittagong campus.

These are the first records of this subspecies for Bengladesh.

Key words. - Boiga ochracea , Bangladesh.

While identifying snake species preserved in the

Departmental Museum of Zoology, Chittagong

University (CU), two specimens of Boiga ochracea

walli (Stoliczka, 1870) were found. One was collected

in 1975, but the localities where they were found are

unknown. Both specimens were probably collected form

the University of Chittagong campus. The occurrence of

Boiga ochracea in Bangladesh was first reported by

Khan (1982) based on a specimen collected from

Chittagong Hill Tracts. Khan (1982) did not identify the

specimen to subspecies. Smith (1943) reported the sub-

species range as Burma (now Myanmar) south of Lat.

25°; Tenasserim; the Andaman and Nicobar Islands.

Both localities of Boiga ochracea walli from Chittagong

(this report) and B. ochracea from Chittagong Hill

Tracts (Khan 1982) are close to Myanmar and south of

the latitude mentioned by Smith (1943). This report

extends the subspecies range up to Bangladesh and it

may occur in other parts of the country like Greater

Sylhet, Cox's Bazar, and the districts of Chittagong Hill

Tracts (i.e., Rangamati, Khagracheri and Bandarbans) as

they have similar habitats.

The CU specimens have the following characters

(although the natural colour may have changed due to

the effects of preservation): faded greyish above, verte-

bral series of scales paler than others, ventral side of

body whitish. Smith (1943) described the subspecies as

"greyish, reddish or yellowish brown above (coral red in

life), some of the scales finely edged with black and

forming more or less distinct transverse lines or bars,

best marked in the young; the vertebral series of scales

sometimes lighter than the others; paler below; lips and

chin whitish".

The CU specimens have eight supra labials, 4th, 5th

and 6th below the eyes; one pre and two post-oculars

present. Smith (1943) stated that there is normally one

pre-ocular, not reaching the upper surface of the head;

anterior genials about as long as the posterior, latter in

contact with one another or separated by small scales;

vertebrals strongly enlarged. The measurements of the

CU specimens are compared below with those reported

by Smith (1943).

Literature Cited

Khan, M. A. R. 1982. Wildlife of Bangladesh - a check-

list. Dhaka University Press, Dhaka. 173 pp.

Smith, M. A. 1943. The fauna of British India, including

Ceylon and Burma. Reptilia and Amphibia, Vol. 3

Serpentes. Taylor and Francis Ltd., London. 583 pp.

Table 1. - The table shows that the Smith's (1943) specimens and the present ones are similar.

or (1943)

2+3

2004

Asiatic Herpetological Research

Vol. 10, pp. 236-240

Some Aspects of Breeding Biology of the Bengal Lizard

(Varanus bengalensis) in Bangladesh

M. Farid Ahsan1 and M. Abu Saeed2

^ Department of Zoology, University of Chittagong, Chittagong 4331, Bangladesh; E-mail: mfahsan(fctgu.edu

-AGROCARE, Golden Plaza (1st Floor), 58 Shaheed Taj uddin Ahmed Sharani, Mohakhali, Dhaka 1212,

Bangladesh

Abstract. - Some aspects of breeding biology of the Bengal, or Gray, Monitor Lizard ( Varanus bengalensis ) were

studied in the farm area of Azra Produces Impex (a private enterprise) at Bhaluka, Mymensingh from 1995 to 1997.

The feeding success, caring, egg-laying, clutch-size, incubation of neonate care were observed. The eggs were laid

between August and October with a mean clutch-size of 21.1 (range 10-32, n=25). The mean incubation period was

192.7 days (range 189-216 days, n=678) with a hatching success of 3.3% which was very low due to many reasons.

Some problems regarding farming of the species are discussed.

Key words. - Varanus bengalensis , Bengal lizard, breeding, farming, Bangladesh.

Introduction

The Bengal, or Gray, Monitor Lizard ( Varanus ben-

galensis) is one of the three varanid species found in

Bangladesh. It is most widely distributed throughout the

country, including many islands, in both forested and

non-forested open wooded areas. It is economically

important for its valuable skin and its role in the ecosys-

tem, especially in controlling some pests. In

Bangladesh, some tribes like the Shawtal, Kulee, Kukis,

etc., also eat its meat.

The few research works that have been done on

varanids in Bangladesh mainly deal with their distribu-

tion. However, Whitaker and Hikida (1981) and Akond

et al. (1982) briefly worked on the ecology and stomach

contents of varanids. There is no published report on the

captive breeding of varanids of Bangladesh. Azra

Produces Impex, a private enterprise, started a project in

Bangladesh on the farming of V bengalensis. As advisor

(MFA) and consultant (MAS) we looked into the bio-

logical aspects of the project. This paper deals with the

preliminary observations on feeding, caring, egg-laying,

clutch-size, incubation of eggs, and caring of hatchlings.

Some problems regarding farming of the species have

also been discussed.

Study Area and Study Animals

The Varanus breeding farm of Azra Produces Impex is

situated at Habirbari of Bhaluka Thana (Mymensign

District, Bangladesh, 24° 21' N and 90° 21' E). It is 71

km north of Dhaka City and located adjacent to the

Dhaka-Mymensign Highway. The farm was inaugurated

in June, 1995 within a concrete boundary wall (about 3

Figure 1. Adult Varanus bengalensis eating supplied

food.

m high including wire rope) enclosure with an entrance

(gate) on the western side along the said Highway. The

total area of the farm is 37.74 acres (16.77 ha). There are

50 ponds inside the farm and a lake excavated around

the periphery of the farm. One open wire-net enclosure

(37 m x 61 m x 1 m) with a concrete base (of 25.4 cm)

has also been made inside the farm area for some of the

lizards (about 200 individuals).

A total of 2, 112 Bengal lizards (685 [32.4%] males

and 1427 [67.6%] females) were released inside the

farm area. These lizards were captured by professional

hunters from wild stock (with the permission of the con-

cerned authority, Ministry of Environment and Forests,

Government of the People's Republic of Bangladesh) of

Greater Mymensign and Tangail districts between 4

June and 9 September, 1995. Before releasing, each

lizard was physically checked and sex recorded. Injured

and immature lizards were rejected.

Vol. 10, p. 237

Asiatic Herpetological Research

2004

Figure 2. Eggs of Varanus bengalensis in a natural nest (left) and being prepared for artificial incubation (right).

Methods

Food. Cleaned pieces of stomach (omasum part only) of

bovines, collected from different slaughter houses of

Dhaka city, were supplied to the lizards as food. Food

was supplied only inside the wire-net enclosure in trays

(25.4 cm x 25.4 cm x 5 cm, made up of tin sheet). In

other parts of the farm, food was thrown near the roost-

ing places (close to bushes) of the lizards. Usually foods

were supplied to the lizards every alternate day (except

for Sunday) - half of the farm area was covered in one

day and the rest half in the next day. About 100-150 such

stomachs were offered to the lizards on every feeding

day (Fig. 1).

Eggs. Eggs (Fig. 2, Table 1) were collected from holes

in the soil (dug obliquely) and holes of termite mounds

(either natural or made by lizards) and placed inside arti-

ficial holes made in the incubation cages. Special pre-

cautions were taken during handling of eggs to avoid

shaking or turing upside down, so that, embryos do not

get loose or shift from the original position.

Incubation. An incubation area was selected inside the

farm where two cages were built (Fig. 3), each one hav-

ing a small entrance. Cage-I was closed cart-shaped

(12.5 m x 4.6 m x 2.6 m), made of wire-net (mesh size

5 mm x 5 mm) with a concrete base and supported by

rods. Inside the cage three artificial incubation beds

were built - western (1240 cm x 1 16 cm x 55 cm), mid-

dle (1240 cm x 110 cm x 48 cm) and eastern bed (1240

cm x 95 cm x 32 cm). Spaces between western and mid-

dle beds were 53 cm, and between middle and eastern

were 43 cm. In each bed, two storied oblique holes were

excavated - the western bed had holes only in the east-

ern side, the eastern only in the western side, and the

middle bed had holes on both sides. Sandy, granular, and

dry soils were placed on the floor of each hole and dry

sands on the hole mouth. The roof of each hole was

made by moist sandy loam. The top of each bed was

covered with grasses. Each hole (length 30 cm and

diameter 10 cm) was marked by numbered stick plate.

Altogether there were 190 holes in cage-I and 30 eggs

were placed in each hole. When all holes of cage-I were

filled with eggs (totalling 5,700), the second cage (cage-

II) was built in the eastern periphery of the cage-I. Cage-

II was closed rectangular-shaped (12.5 m x 7.9 m x 2.5

m) formed of wire-net (mesh size 5 mm x 5 mm) and

supported by rods and poles. Here, only pits were dug,

and 30 eggs were placed in each pit. There were 500

such pits (containing 14,499 eggs in total) in this cage

and each one was marked with numbered stick plate.

These pits were filled with loose soils in such a way that

a 5-7 cm thick soil layer was on the eggs. The pits were

covered with broad (palm) leaves during hot days to

retain moisture in the soil. When topsoil of cage-II was

too dry, water was added. Later on, some grasses grew

naturally.

Hatching and Hatchability. After two months of incu-

bation, several nests were excavated weekly to check for

hatching and 2-5 eggs were opened to see the develop-

ment of embryos (Fig. 4). Those hatched (Fig. 5) were

immediately transferred into baby nursery. When suffi-

cient number of hatchlings were obtained in cage-I, all

the remaining eggs which seemed to be still alive were

transferred into 7 big trays (0.5 m x 2.5 m x 0.25 m) in

the nursery, these trays were kept separate from the

hatched lizards by a wall of 1 m within the nursery. The

earlier mentioned precautions were taken during this

transfer. Eggs were placed half-buried in the tray soil

with the usual cover. Each tray was checked twice a day

(morning and late afternoon) and the number of hatch-

lings was recorded. Then hatchlings were released

immediately in the nursery after careful noting of their

measurements (Table 2).

2004

Asiatic Herpetological Research

Vol. 10, p. 238

Figure 3. Incubation cages for Varanus bengalensis. Cage I (left), Cage II (right). See text for description.

Table 1. Varanus bengalensis egg sizes (n=24).

Baby Nursery. The concrete floor of the nursery (9.5 m

x 3.6 m x 3 m) was covered with sandy loam soil. Tin

sheets (40 cm high) were fitted against the nursery walls

to prevent the escape of the baby lizards. Lumps of ter-

mite mounds containing termites (adults, mostly eggs

and larvae) were placed in the periphery of the nursery

as food for the hatchlings. Other foods offered to the

babies were crushed boiled poultry eggs, minced beef

and minced clean stomach of bovine. Two artificial

small water reservoirs (25.4 cm x 25.4 cm x 5 cm) were

made in the nursery.

All non-hatched eggs were piled and randomly 100

eggs from incubation cage-I and 150 from incubation

cage-II were opened to determine the percentage of

undeveloped eggs and dead embryos (Fig. 4).

Observations, Results, and

Discussion

Food. Besides the supplied food, lizards were also seen

to eat arthropods especially beetles and grubs from cow-

dung, and small fish (mainly Tilapia , which were

Table 2. Size of hatchling Varanus bengalensis (n=39).

* Total length (snout to tail tip), body length (snout

to anus), and tail length (anus to tail tip).

released in the lake for propagation).

Caring. Sick lizards were provided with food closer to

them. Medical treatment was not given.

Eggs. Eggs were white, oval, with soft leathery skin and

contained a large yolk supply. The farm staff collected a

total of 20,499 eggs from the holes of termite mounds

during 11 September to 30 October, 1995. Although the

first clutch of eggs (18) were found on 10 August, 1995

inside a termite mound on the embankment of a pond

inside the farm, this was not recorded by the farm staff

(so it is excluded from the total count). The average col-

lection of eggs was 512.67 + 134.49 (range 160-1210,

n=38 days) per day.

Whitaker and Hikida (1981) and Akond et al.

(1982) stated that the egg-laying period of Bengal lizard

in Bangladesh is November and December. Daniel

(1983), however, reported that eggs were collected from

mid April to October in India. In Sri Lanka, the peak

breeding period of Bengal lizard is January to April, but

eggs also occur during June to December in ground logs

or termite mounds (Deraniyagala, 1958). In the present

study the egg-laying period was much earlier than that

recorded by Whitaker and Hikida (1981) and Akond et

al. (1982).

The mean size of egg was 5.71 cm in length, 2.92

cm in width and 26.93 gm in weight (Table 1). From

India, Daniel (1983) reported that the average egg size

of gray lizard was 4.9 x 3.8 cm (range 4.7 x 3.6 to 5.5 x

4.4 cm, n=50) and weighed 1 1.4 gm (range 8.3-14.3 gm,

n=25). The size of eggs in this study (Table 1) is close to

that reported by Daniel (1983), but the weight data are

very different.

Clutch size, dutch size varies according to the size and

age of the females, larger and older females lay more

eggs than younger and smaller ones. The average clutch

size was 21.1 + 7.4 (range 10-32, n=25). The clutch

size of Bengal lizard was 8-32 (Whitaker and Hikida,

Vol. 10, p. 239

Asiatic Herpetological Research

2004

Table 3. Minimum and maximum air temperatures and soil temperature (°C) during study period.

1981; Akond et al., 1982) and 20-30 (Khan, 1987) in

Bangladesh, while 8-30 in India (Daniel, 1983). The

range of present observation is close to the mentioned

works except for Khan (1987).

Incubation period. On average, the incubation period

of egg was 192.72 + 4.59 days (range 189-216 days,

n=678 eggs). The first lizard hatched on 18 March and

the last on 4 June, 1996. Most of the lizards hatched late

at night or early in the morning; some also hatched dur-

ing the day.

Previously recorded incubation periods for the

Bengal Monitor Lizards of Bangladesh were 7-8 months

(i.e., 210-240 days) (Whitaker and Hikida, 1981); 6-8

months (i.e. 180-240 days) (Akond et al., 1982) and 7-8

months (i.e. 210-240 days) (Khan, 1987). Daniel (1983)

mentioned that the incubation period of Bengal lizard in

India was 8-9 months (i.e. 240-270 days). The present

incubation period is closer to that recorded by Whitaker

and Hikida (1981) and Akond et al. (1982), but smaller

than that reported by Daniel (1983). The egg-hatching

month has been mentioned as July (Whitaker and

Hikida, 1981) and June-July (Akond et al., 1982) while

in the present observation it spreads over mid March to

early June.

The variation in the incubation period of the present

work and those of the above mentioned works could be

due to the effect of some ecological factors like temper-

ature, moisture, rainfall, etc. We recorded air tempera-

ture in the farm and soil temperature of nest of the incu-

bation cage-I (and later baby nursery) which give an

indication of these conditions (Table 3).

Hatchlings and hatching success. The average total

length and weight of the hatchlings were 19.72 cm and

13.61 gm, respectively (Table 2). Out of 20,499 eggs,

only 678 babies hatched. The hatching success, in this

case, was 3.3%. (All the hatched eggs [678] were from

cage-I only and the hatching success was 11.9%, but the

eggs from cage-II resulted the poor hatching success i.e.,

3.3%). After hatching out, a baby lizard did not eat for

the next 2-3 days due to a continued absorbance of its

yolk reserve. Neonate lizards ate termite eggs and larvae

from the supplied lumps of termite mounds inside the

Figure 4. Varanus bengalensis in two stages of development: embryo (left), newly hatched (right).

2004

Asiatic Herpetological Research

Vol. 10, p. 240

Figure 5. Varan us bengalensis neonates.

nursery and crushed boiled poultry eggs from the feed-

ing trays. They showed less interest to eat minced beef

and minced bovine stomach. Babies also drank water

and preferred to roost in cold, damp areas inside grasses

or water hyacinths, which were kept in a few places

inside the nursery.

The poor hatching success of eggs in this study was

most probably due to: (1) soil in the incubation cage-II

became compact due to rain and killed embryos; (2)

mis-handling of eggs by the staff during egg transplan-

tation; (3) unregulated temperature and moisture in the

incubation cages. Of these reasons, the first one was

most important because only 12 eggs hatched from the

incubation cage-II (where 14,799 eggs were transplant-

ed) and dead embryos or babies were found in 70% of

the eggs (n=140). On the other hand, we were not sure

whether all the unhatched eggs were fertilized or not.

The additional reason for this huge damage of eggs was

the negligence of the Managing Director of the project

to implement our suggestions in constructing incubation

cage-II.

Problems regarding farming

The following problems were faced during the study

period:

1 . The set up of the project is not well designed and

scientific.

2. Lack of electricity.

3. Instructions/suggestions given (jointly by the

advisor and consultant) to the Managing Director

(MD) of the project were not properly followed.

4. Research facilities provided by the farm are poor.

Recommendations

1. Lizards should be caged rather than distributing

them throughout the farm. A few small cages should

be built for research.

2. Needs devoted staff.

3. Needs electricity.

4. Incubation cages should be constructed like cage-I.

5. Needs incubation chamber, or at least a place(s)

where temperature and moisture fluctuaions are not

drastic.

6. Needs separate “nursery” cages for neonates and

juveniles.

7. Above all, instructions and suggestions proposed

jointly by the advisor and consultant should be con-

sidered in all activities.

Acknowledgments

Dr. M. A. G. Khan, Department of Zoology, University

of Chittagong has kindly reviewed this manuscript. The

proprietor and farm staff of Azra Produces Impex helped

us in various ways. We thank them all.

Literature Cited

Akond, A. W., F. Ahsan, and M. Rahman. 1982. Monitor

lizards of Bangladesh. Proceedings of the Second

National Conference on Forestry held in 21-26

January 1982:540-545.

Daniel, J. C. 1983. The book of Indian reptiles. Bombay

Natural History Society, Bombay. 141 pp.

Deraniyagala, P. E. P. 1958. Reproduction in the moni-

tor lizard, Varanus bengalensis (Daudin). Spolia

Zeylanica. 28:161-166.

Khan, M. A. R. 1987. Bangladesh er banayaprani, part I

(Wildlife of Bangladesh, vol. I). Bangla Academy

Press, Dhaka. 175 pp. (In Bengali).

Whitaker, R. and T. Hikida, 1981. Report of project for

mation mission to Bangladesh (monitor lizards).

FAO, Rome.

2004

Asiatic Herpetological Research

Vol. 10, pp. 241-244

A New Locality for the Rare Bornean Skink, Lamprolepis vyneri

(Shelford, 1905) (Sauria: Scincidae)

Indraneil Das

Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak,

94300, Kota Samar ahan, Sarawak, Malaysia; E-mail: idas@ibec.unimas.my

Abstract. - A specimen of the Bornean arboreal skink, Lamprolepis vyneri (Shelford, 1905), hitherto known from the

holotype from Gunung Balingan, Sibu Division, Sarawak, and a second possible specimen from the upper reaches of

Sungei Mahakam, Kalimantan, is reported from Bukit Balian, near the Kayan settlement of Kelep, at Sungei Asap, at

the base of Gunung Dulit, Kapit Division, Sarawak. The species is illustrated for the first time.

Key words. - Lamprolepis vyneri , redescription, Scincidae, Sarawak, Borneo.

Introduction

The genus Lamprolepis Fitzinger, 1843, which was

revived from the synonymy of Dasia Gray (1829), by

Greer (1970) contains four nominal species of arboreal

skinks. Two of these are endemic to Borneo (L. nieuwen-

huisii and L. vyneri ), a third ( L . leucosticta ) to Java

(Manthey and Grossmann, 1997:263) and the fourth {L.

smaragdina ) is widespread in the Philippines, Sulawesi,

Lesser Sundas, the Republic of Belau, the Carolines,

New Guinea, the Solomons and Santa Cruz Islands

(Brown and Alcala, 1980:76-79; Greer, 1970). The first

two species are arguably the least well known of all

Bornean lizards. L. nieuwenhuisii (Lidth de Jeude, 1905)

was described from "Long Bloe" (= Long Blu or Bloeoe,

00° 43' N; 114° 25' E), on the upper reaches of Sungei

Mahakam, Kalimantan Tengah Province, Indonesia;

RMNH 4455, holotype). It has subsequently been col-

lected from isolated localities in northern Borneo,

including Nanga Tekalit Camp on Sungei Mengiong,

Kapit Division (reported as Dasia vyneri by Lloyd et al.,

1968, based on FMNH 138542; 147562); and Pangkalan

Lobang at Niah National Park, Miri Division (FMNH

131528), both in Sarawak State; and Kiau, Gunung

Kinabalu National Park, Ranau District (MCZ 43494;

BMNH 1929.12.22.96 and ZRC 2.1595); and

Mahunbayon, Gunung Kinabalu National Park, Ranau

District (MCZ 43495), both in Sabah State, East

Malaysia.

Lamprolepis vyneri (Shelford, 1905) is more poorly

known. Named for Charles Vyner Brooke (1874-1963),

the Rajah Muda of Sarawak at the time of description of

the species, and subsequently, the Third Rajah of

Sarawak between 1917-1946, it is only known from the

holotype, BMNH 1946.8.15.56 (ex-BMNH

1909.8.18.2), from "Mount Balineau, Muka district,

Sarawak" (= Gunung Balingan, 01° 25' N; 1110 28' E,

Sibu Division, East Malaysia), according to the original

description. However, in the records of the Sarawak

Museum (Anon., 1903), the type locality is given as

"Mt. Balingean" (in Muka District, Sibu Division,

Sarawak). Lidth de Jeude (1905) questionably assigned

to this species a specimen from the upper reaches of

Sungei Mahakam (00° 30' S; 117° 15' E), Kalimantan

Timur Province, which apparently differed from

Shelford's (1905) species in some trivial details of squa-

mation and body proportions. The location of this spec-

imen is unknown, but was examined by De Rooij

(1915), who allocated it to the present species. This

species has never been illustrated.

A second specimen (ZRC 2.5513; Figs. 1-2) of

Lamprolepis vyneri is reported here from Bukit Belian

(03° 08' 34.4" N; 113° 55' 45.5" E), near the Kayan set-

tlement of Kelep, at Sungei Asap, situated at the base of

Gunung Dulit, Kapit District, Sarawak. It was collected

dead on 6 November 2001 from a logging road.

Material and Methods

The specimen was photographed upon collection, fixed

in neutral buffered formalin and subsequently trans-

ferred to 70% ethanol, within a week of collection. The

following measurements were taken with Mitutoyo™

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

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

vent to end of unregenerated tail; tip missing), tail width

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

tance between posterior edge of last supralabial and

snout-tip), head width (HW; measured at angle of jaws),

head depth (HD; maximum height of head, from occiput

to throat), ear length (EL; greater ear length); eye diam-

eter (ED; greatest diameter of orbit), eye to nostril dis-

tance (E-N; distance between anteriormost point of eyes

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

Vol. 10, p. 242

Asiatic Herpetological Research

2004

Figure 1. The Sungei Asap specimen of Lamprolepis vyneri (ZRC 2.5513), showing (left) general view of body and

(right) close-up of head and forebody.

between anteriormost point of eyes and tip of snout), eye

to ear distance (E-E; distance from anterior edge of ear

opening to posterior comer of eyes), intemarial distance

(IN; distance between nares), interorbital distance (10;

shortest distance between orbits), tibia length (TBL;

straight length of tibia, from knee to sole), in addition to

measurements of digits, taken on the left limbs, from the

base to tip. Scale counts and external observations of

morphology were made using an Olympus SZX9 dis-

secting microscope. Institutional abbreviations follow

Leviton et al. (1985), except ZRC is retained for USDZ,

following conventional usage.

Description of Lamprolepis vyneri from Bukit Belian,

Sungei Asap (ZRC 2.5513). - Habitus relatively slen-

der, snout- vent length 55.2 mm; head elongate (HL/SVL

ratio 0.20), narrow (HW/HL ratio 0.65), moderately

depressed (HD/HL ratio 0.11), slightly distinct from

neck; snout long (E-S/HW ratio 0.72), longer than the

eye diameter (ED/E-S ratio 0.75), projecting slightly

beyond mandible; interparietal distinct; parietal eye

absent; supraoculars four; second and third largest;

supraciliaries 8/8; first supraciliary contacts frontal;

scales on snout and forehead smooth; rostral contact

frontonasal posteriorly; rostral small, wider than deep

(rostral width = 2.0 mm; rostral depth = 1.2 mm;

width/depth ratio 1.67), contacted posteriorly by nasal

and frontonasal; posteroventrally, rostral in contact with

first supralabial; nares slit-like, situated on upper level

of nasal, oriented laterally; nasal in broad contact with

first supralabial; supranasals moderate in size, separat-

ed; frontonasal trapezoid, wider than long, contacting

frontal and prefrontals posteriorly; frontal longer than

frontonasal, not constricted laterally; frontoparietals in

contact with each other and with three supraoculars, and

posteriorly, with interparietal and parietals; a single pair

of parietals contacts interparietal; parietals separated

behind by an azygous scale; loreals two, anteriormost

longer than deep; a small dorsal presubocular, and a

wider ventral one; eye large (ED/HL ratio 0.35); post-

suboculars two; supralabials seven, with supralabials 4-

6 in suborbital position; supralabials three, fifth and

sixth larger than the others; infralabials six; lower eyelid

scaly; a single preocular between loreal and orbit; pos-

toculars two; pretemporals two; two anterior and two

posterior temporals; ear opening narrow, measuring 1.9

mm; situated laterally at a level slightly higher than

jaws; a few lobules around ear opening present; tympa-

num deeply sunk; eye-to-ear distance less than eye-to-

nostril distance (E-E/E-N ratio 1 .26); a pair of enlarged

nuchals, partially separated by a single cycloid scale;

mental large, semicircular, wider than deep; postmental

single, trapezoidal, larger than mental, its width 1.8 mm

or 25.4 per cent head width; postmental contacts first

infralabial only, bounded posteriorly by a pair of

smooth, squarish, juxtaposed chin shields that are in

contact; three pairs of enlarged chin shields, the first in

contact with each other, the second separated by a single

scale, the third separated by three scales; tongue narrow-

ly elongate, narrowed distally, with a median cleft and

scattered papillae on the dorsal surface; maxillary and

mandibular teeth small, undifferentiated.

Body slender, elongate (SVL/BW ratio 6.81); dor-

sum and venter with smooth scales, with faint striae,

scale size subequal dorsally as well as ventrally; anals

six, smooth; outer overlapping inner; preanals three, not

greatly enlarged, overlapped by last ventral, third pre-

anal exceeding its posterior level, over vent; flank scales

reduced in size.

Limbs well developed, pentadactyle; adpressed

limbs meeting at level of heels; lamellae under finger IV

numbering 18; lamellae under toe IV numbering 20; rel-

ative length of fingers (measurements in mm, in paren-

theses): 4 (4.5) > 3 (4.4) > 2 (3.5) > 5 (2.7) > 1 (2.0); rel-

ative length of toes: (measurements in mm, in parenthe-

ses): 4 (7.8) > 3 (5.6) > 5 (5.5) > 2 (4.7) > 1 (3.0).

Tail long, preserved tail length over 40.5 mm (tip

missing), longer than snout-vent length; tail base slight-

ly swollen; ventral surface of tail with smooth; subcau-

dals very wide; scales on the postanal region and at the

proximal part of the tail base smooth.

Coloration. - Forehead olive-yellow, edged with black;

dark smudges on forehead scales; scales on dorsum of

2004

Asiatic Herpetological Research

Vol. 10, p. 243

Figure 2. Head of Lamprolepis vyneri (ZRC 2.5513) in

dorsal (left) and ventral (right) views. Scale bars = 10

mm.

body bright yellow, edged with black, appearing as four

dark longitudinal lines that extend along the body to

slightly beyond the base of tail; yellow dorsolateral

stripe, 2-3 scale wide, runs from behind level of the axil-

la, across the inguinal region, continuing along the side

of the tail; venter, including the gular, pectoral and

abdominal regions, undersurface of tail and of limbs yel-

lowish-green, unpattemed; scales on flanks black-edged,

reddish-orange, with scattered yellow scales; the same

coloration is found on the upper surfaces of the fore and

hind limbs; tail alternately banded yellowish-brown,

each band one scale wide, and pale yellow; tongue and

inner lining of mouth yellowish-pink; inner lining of

body cavity yellowish-pink in preservative.

Measurements (in mm). - BW 8. 1 ; ED 3.8; E-E 4.8; EL

1.2; E-N 3.8; E-S 5.1; IN 1.7; IO 4.5; HD 5.8; HL 10.9;

HW 7.1; SVL 55.2; TBL 7.7; and TL 40.5 - original

unregenerated, tip missing; TW 5.3.

Scutellation. - Ventrals (between postmental and pre-

anal) 49; midbody scale rows 22; subcaudal count

unknown (tail-tip missing); supralabials seven (fourth,

fifth and sixth in suborbital position) and infralabials

six.

Variation. - The Sungei Asap specimen differs from the

holotype in the following particulars: SVL 55.2 vs 52.0

mm; supraoculars on left side four (vs five in the holo-

Figure 3. Map of Borneo showing the known localities

for Lamprolepis vyneri. 1 = Gunung Balingan, Sibu

Division (type locality); 2 = Bukit Balian, near Sungei

Asap, Kapit Division.

type, as shown on the apparently anomalous right side of

the head of the Bukit Belian specimen). The bright red

and yellow coloration of the flanks of the Bukit Belian

specimen turned to dark brown after three months of

storage in preservative. Shelford (1905), who presum-

ably examined a preserved specimen, reported the flanks

as being olive-gray, van Lidth de Jeude's (1905) speci-

men was 63 mm in SVL, and showed five black stripes,

but only three entering the sacral region and tail-base.

This poorly-preserved specimen was described as "putty

grey", with several cephalic scales edged with black.

Notes on Natural History. - The specimen being

reported here was found freshly dead on a logging track

at the base of Bukit Belian (03° 08' 34.4" N; 113° 55'

45.5" E), near Kelep, Sungei Asap, a Kay an resettlement

colony in Kapit (Seventh) Division, central Sarawak. It

may have fallen off a log that was being transported,

because the members of the genus are highly arboreal,

and the present specimen was otherwise physically

intact, except for the missing tail-tip, and not run over.

The area lies within a lowland dipterocarp forest with

strands of the Bornean ironwood tree, Eusideroxylon

zwageri (Iban name: Belian, which gives the hill its

name) at 186 m elevation. Perhaps coincidentally, the

holotype was taken at a similar-sounding locality,

Gunung Balingan, for which no general habitat descrip-

tion is available. One is therefore tempted to speculate

Vol. 10, p. 244

Asiatic Herpetological Research

2004

that both localities derive their names for their strands of

the Bornean ironwood, a dipterocarp much in demand

from the timber industry for its durability, and hence

threatened by logging. The new locality, at the base of

Gunung Dulit, is ca. 190 km east of the type locality,

across the Lumut Range (Fig. 3).

Acknowledgments

I thank the Institute of Biodiversity and Environmental

Conservation, Universiti Malaysia Sarawak, for sup-

porting my research on the herpetofauna of Borneo, and

Esther Bala for field assistance. For loans of the holo-

types of Lamprolepis vyneri and L. nieuwenhuisii, I am

grateful to C. J. McCarthy, BMNH, and M. S.

Hoogmoed, RMNH, respectively. I would like to thank

R. F. Inger, A. Resetar and H. K. Voris, FMNH; J. E.

Cadle, J. Rosado and the late E. E. Williams, MCZ, and

K. K. P. Lim, P. K. L. Ng and C. M. Yang, ZRC, for per-

mitting me to examine comparative material under their

care and Allen Greer and an anonymous reviewer for

comments on a draft manuscript. Finally, thanks are due

to Gary Geller, Jet Propulsion Laboratory, National

Aeronautics and Space Administration, for generating

Fig. 3.

Literature Cited

Anonymous. 1903. Museum. The Sarawak Gazette

33:236.

Brown, W. C., and A. C. Alcala. 1980. Philippine lizards

of the family Scincidae. Silliman University.

Natural Science Monograph Series 2. Silliman

University Press, Dumaguete. 264 pp.

De Rooij, N. 1915. The reptiles of the Indo- Australian

Archipelago. Vol. I. Lacertilia, Chelonia,

Emydosauria. E. J. Brill, Leiden. 384 pp.

Greer, A. E. 1970. The relationships of the skinks

referred to the genus Dasia. Breviora (348): 1-30.

Leviton, A. E., S. C. Anderson, R. H. Gibbs, E. Heal,

and C. E. Dawson. 1985. Standards in herpetology

and ichthyology. Part I. Standard symbolic codes

for institutional resource collections in herpetology

and ichthyology. Copeia 1985(3):802-832.

Lloyd, M., R. F. Inger, and F. W. King. 1968. On the

diversity of reptile and amphibian species in a

Bornean rain forest. American Naturalist

1 02(928):497-5 1 5.

van Lidth de Jeude, T. W. V. 1905. Zoological results

of the Dutch scientific expedition to central Borneo.

The reptiles. Part I. Lizards. Notes from Leyden

Museum 25(16): 187-202.

Manthey, U., and W. Grossmann. 1997. Amphibien and

Reptilien Siidostasiens. Natur und Tier Verlag,

Munster. 512 pp.

Shelford, R. 1905. A new lizard and a new frog from

Borneo. Annals & Magazine of Natural Histoiy,

Series 7, 15:208-210.

Asiatic Herpetological Research Vol. 10, pp. 245-246 [

Leptobrachium smithi Matsui, Nabitabhata, and Panha, 1999 (Anura:

Megophryidae), an Addition to the Fauna of Myanmar (Burma)

Indraneil Das1 and Sh yamal Kumar Chanda2

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

Kota Samar ahan, Sarawak, Malaysia; E-mail: idas@ibec.unimas.my

“ Amphibia Section, Zoological Survey of India, Fire-Proof Spirit Building,

27, J. L. Nehru Road, Kolkata 700 019, India

Abstract. - Three specimens of Leptobrachium from the collections of the Zoological Survey of India are identified

as Leptobrachium smithi. These specimens were collected

of Leptobrachium smithi for Myanmar.

Key words. - Anura, Leptobrachium , Myanmar, Burma.

Leptobrachium smithi Matsui et al. (1999) was

described from peninsular Thailand, based on popula-

tions that were formerly referred to L. hasseltii Tschudi,

1838 (see Frost, 1985). This species was recently report-

ed from Chandubi in the Mayeng Hill Reserve Forest

and Garbhanga Reserve Forest, Kamrup District, Assam

State, north-eastern India by Sengupta et al. (2001). We

here report specimens from Myanmar in the collection

of the Zoological Survey of India (ZSI) that are allocat-

ed to L. smithi.

Three specimens of Leptobrachium smithii were

examined: ZSI 10439-40, from "Ahsoon" (unlocated), in

Tenasserim, Myanmar, altitude "2,000 feet", collected

by the Swedish journalist, novelist, poet and ship cap-

tain, Gustaf Arthur Ossian Limborg (1849-1908) in

1 877. Limborg's expedition to what was then Burma was

sponsored by Lord Tweeddale (Kjellgren, 1983) and his

collections are distributed in Sweden and the US). Also

examined was ZSI 11841, from Lampi Island, Mergui,

collected by John Anderson, in 1882 (referred to by

Anderson, 1889, as from "Sullivan Island", an older

name for Lampi, 10° 50' N; 98° 15' E).

The material from Myanmar match the description

of original description of Leptobrachium smithi , in addi-

tion to additional specimens examined from Assam State

(see Sengupta et al., 2001), in showing the following

characteristics: moderate body size (snout-vent length

22.4-43.4 mm; head width 6.6-18.1 mm; n = 3); small

inner metatarsal tubercle; dorsum smooth; and absence

of rows of dermal ridges on dorsal surface of limbs. All

specimens referred to here are discolored, hence other

characters used in separating L. smithi from L. hasseltii ,

such as absence of white spots on sides of body and on

thigh; absence of dark spots on ventrum; and absence of

dark markings on dorsum, that differentiates the north-

Limborg in 1877. These are the first confirmed records

em L. smithi from the southern L. hasseltii , are indis-

cemable.

The known distribution of Leptobrachium smithi is

thus north-eastern India, Myanmar (first country record

on the basis of ZSI specimens reported here) and

Thailand. Matsui et al. (1999) suspected the occurrence

of the species in southern Myanmar, based of the larval

description of L. hassseltii by Annandale (1917:153-

157, as Megalophrys hasseltii ), from the Dawna Hills of

the Tenasserim. We have examined these specimens

(ZSI 16735-43) that carry the following locality "Misty

Hollow, w side of Dawna Hills, L. Burma". Surprisingly,

Annandale, neither in his 1917 monograph, nor in any

other works, have referred to the specimens from Burma

mentioned earlier, although all of these were available to

him (see Sclater, 1892).

Acknowledgments

We thank J. R. B. Alfred, Director, Zoological Survey of

India, Kolkata and Colin J. McCarthy, The Natural

History Museum, London, for permission and facilities

at their respective institutions. Saibal Sengupta, Arya

Vidyapeeth College, made comparative material avail-

able to us, and Erik Ahlander, Swedish Museum of

Natural History, Stockholm, provided details on the life

of Ossian Limborg.

Literature Cited

Anderson, J. 1 889. Report on the mammals, reptiles, and

batrachians, chiefly from the Mergui Archipelago,

collected for the Trustees of the Indian Museum.

Journal of the Linnean Society (Zoology) 21:331-

350.

Vol. 10, pp. 246

2004

Annandale, N. 1917. Zoological results of a tour in the

Far East. Batrachia. Memoirs of the Asiatic

Society of Bengal 6:119-155; PI. V-VI.

Frost, D. R. (Ed). 1985. Amphibian species of the world.

A taxonomic and geographical reference. Allen

Press, Inc., and Association of Systematics

Collections, Lawrence, (iv) + v + 732 pp.

Kjellgren, L. 1983. En prastson som alskade havets vag.

Om kaptenen och litterataren Ossian Limborg.

Sumlen (Svenskt Visarkiv) 1983:57-74.

Matsui, M., J. Nabhitabhata, and S. Panha. 1999. On

Leptobrachium from Thailand with a description of

a new species (Anura: Pelobatidae). Japanese

Journal of Herpetology 18(1 ): 1 9-29.

Sclater, W. L. 1892. List of the Batrachia in the Indian

Museum. Indian Museum, Calcutta,

viii + 43 pp.

Sengupta, S., N. K. Choudhury, and I. Das. 2001.

Leptobrachium smithi Matsui, Nabhitabhata and

Panha, 1999 (Anura: Megophryidae), a new record

for India. Journal of the Bombay Natural History

Society 98(2):289-291.

Asiatic Herpetological Research Vol. 10, pp. 247-279

Species Diversity and Checklist of the Herpetofauna of Pulau Tioman,

Peninsular Malaysia, With a Preliminary Overview of Habitat Utilization

Jesse L. Grismer1, L. Lee Grismer1, Indraneie Das2, Norsham S. Yaakob3,

Lim Boo Liat4, Tzi Ming Leong5, Timothy M. Youmans1, and Hinrich Kaiser1

* Department of Biolog)’, La Sierra University, Riverside, CA 925 1 5-8247, USA

-Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak,

94300 Kota Samarahan, Sarawak, Malaysia

' Forest Research Institute Malaysia, Kepong, 52109 Kuala Lumpur, Malaysia

4 Taman Negara (PERHILITAN), Km 10 Jalan Cheras, 50664 Kuala Lumpur, Malaysia

3 Department of Biological Sciences, National University of Singapore, Singapore 119260

Abstract. - The environmental diversity of Pulau Tioman, a 48 km2 island off the eastern coast of Peninsular Malaysia,

supports a remarkably diverse herpetofauna (97 species) with 22 frogs, one caecilian, one non-marine turtle, 34

lizards, and 39 snakes. The majority of this herpetofauna (74%) occurs in lowland dipterocarp forests. Fifteen new

island records and eight newly described, or as yet undescribed, species are reported, bringing the number of endem-

ic species to at least 11.

Key words. - Pulau Tioman, Malaysia, herpetofauna, habitat diversity, checklist.

Introduction

Pulau Tioman (Tioman Island) is centrally located on the

Sunda Shelf 38 km off the southeast coast of Peninsular

Malaysia in the South China Sea (Fig. 1). Despite its

small size of approximately 48 km2, it supports a diverse

array of habitats. The island's coastline and low-lying

periphery is dominated by mangrove and coastal vegeta-

tive communities whereas inland areas support lowland

dipterocarp forest on the alluvial foothills and hill dipte-

rocarp forest at upper elevations (Latiff et al. 1999).

Topographically, Pulau Tioman is characterized by steep

mountainous terrain reaching 1,035 m in elevation.

Exposed granitic outcroppings consisting of large boul-

ders define much of the island's rugged interior and its

slopes are cut by several fast-flowing, boulder-strewn

streams. As discussed below, this environmental diver-

sity contributes to the island's remarkable herpetological

diversity with 23 amphibians, one non-marine turtle, 33

lizards, and 39 snakes now confirmed as present on the

island (Table 1). This is in contrast to the relative depau-

perate herpetofauna of the surrounding islands of Tulai

(Grismer et al., 2001b), Aur (Escobar et al., 2002a;

Grismer et al., 2001a), Dayang (Wood et al., 2003),

Pemanggil (Youmans et al., 2002), Sembilan and

Seribuat (Wood et al. in prep), Sibil and Besar (Wood et

al., 2004a,b) and Tinggi (Escobar et al., 2002b).

Prior to Elendrickson (1966a,b), no herpetofaunal

survey had been undertaken on Pulau Tioman and only

Figure 1. Location of Pulau Tioman, West Malaysia, in

the South China Sea.

limited accounts on particular taxa existed (i.e.,

Boulenger, 1912; Smith, 1930; de Haas, 1949).

However, despite the thoroughness of Hendrickson

(1966a,b) and subsequent efforts by Day (1990), Lim

and Lim (1999), Hien et al. (2001), and Grismer et al.

(2002a), the herpetofauna of this small island still

Vol. 10, p. 248

Asiatic Herpetological Research

2004

Mangrove swamps (0 m)

Coastal vegetation (0-80 m)

Lowland dipterocarp forest (80-300 m)

Hill dipterocarp forest (300-950 m)

Ridge forest (950-1,035 m)

Distribution of vegetation zones on Pulau

Tioman. Modified from Latiff et al. (1999).

remains incompletely known. This is evidenced by the

13 new island records since Grismer et al. (2002a) and

Hien et al. (2001) and eight newly described and unde-

scribed species reported herein. Additionally, there has

been no attempt to establish the distribution or habitat

use of each species on Pulau Tioman. Therefore, the

intent of this paper is to report the results of the latest

herpetofaunal surveys which not only list new additions

to the island but new island localities of species known

to be present. The latter will serve as the basis for a pre-

liminary categorization of habitat use for each species

based on its presence in different vegetation zones.

Figure 3. Mangrove swamp at Kampung Paya.

Vegetation Zones

Vegetation zones generally serve to highlight broad cat-

egorical differences between habitats across sizable geo-

graphic areas. On Pulau Tioman, as elsewhere, these

categorical differences lack well-defined geographic

boundaries (Ashton, 1995) and with the exception of

mangrove communities, each zone transitions smoothly

and continuously into another along an altitudinal tran-

sect. We use five different vegetation zones (Fig. 2),

modified after Latiff et al. (1999), to characterize habi-

tat differences on Pulau Tioman.

Mangroves (0 m; Fig. 3). - Mangrove swamps are dis-

junctly distributed along the island's coastline.

Characteristic plant species include Rhizophora apicula-

ta, Bruguiear gymnorhiza, Excoecaria agallocha , and

Avicennia alba , which in some localities are unusually

tall with large girth, attesting to the old age of the grove.

Coastal vegetation (0-80 m; Fig. 4). - Coastal vegeta-

tion forms a relatively narrow zone between the man-

grove swamps (when present) and the lower reaches of

the lowland dipterocarp forest. It is characterized by

2004

Asiatic Herpetological Research

Vol. 10, p. 249

Fig. 6. Hill dipterocarp forest on Gunung Kajang. Fig. 7. Ridge forest at summit of Gunung Kajang.

2004

Figure 8. Collecting localities on Pulau Tioman. G. = Gunung (mountain); Kg. = Kampung (village); S. - Sungai

(river); Tk. = Telok (bay); U. = Ulu (headwater).

palms, such as Pandcmus dubius, and moderately-sized

trees such as Scaevola taccada , Calophyllum inophyl-

lum, and Vitex trifolia. Dipterocarp trees are noticeably

absent.

Lowland dipterocarp forest (80-300 m; Fig. 5). -

Lowland dipterocarp forest occurs on the alluvial slopes

between coastal vegetation and hill dipterocarp forest

and is usually dominated by large non-dipterocarp trees

such as Arenga pinnata , Caryota mitis, and Nenga

macrocarpa. A few large dipterocarp species such as

Anisoptera curtisii and N eobalanocarpus heimii exist as

emergents.

Hill dipterocarp forest (300-950 m; Fig. 6). - This

zone is situated immediately above and adjacent to the

lowland dipterocarp forest with which it is continuous.

The transition from lowland dipterocarp forest to hill

dipterocarp forest at approximately 300 m is essentially

imperceptible and many plant species common to the

lowland dipterocarp forest occur at lower elevations in

the hill dipterocarp forest, a pattern paralleled by some

species of amphibians and reptiles. To illustrate this we

use the term low hill dipterocarp forest (300-500 m) and

high hill dipterocarp forest (500-950 m). Hill diptero-

carp forest is dominated throughout by large species of

Shorea and Dipterocarpus.

Ridge forest (hill top summits between 950-1035 m;

Fig. 7). - Ridge forest occurs on summits where mosses,

ferns, lichens, and bryophytes predominate. Due to

increased exposure to sun and wind, trees are relatively

short. At this altitude, species such as Garcinia penan-

giana , Licuala tiomanensis , and Scleria sumatrensis

dominate and presumably have adapted to live in the

damp wind-blown environment typical of ridge forests.

Materials and Methods

Our data were collected from various localities (Fig. 8)

on five trips; 12-24 March and 7-16 July, 2001 and 19-

27 March, 13-21 July, and 6-19 August, 2002 unless

indicated otherwise. Individuals sighted but not collect-

ed or photographed are listed but considered to be

unconfirmed records. Collecting was done during the

day by hand and blowpipes and at night by torch light.

During July 2001 and 2002, three pitfall trap arrays with

three 1 5-m drift fence sections at each array were sta-

tioned in lowland dipterocarp forest at 142 m and 241 m

along the Tekek-Juara trail. A third array was estab-

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lished on the beach near boulders in coastal vegetation 1

km south of Kampung Tekek. Collecting site elevations

were estimated with the aid of a hand-held global posi-

tioning satellite unit. Distribution data for species not

addressed in the accounts below but listed in Table 1

were taken from Lim and Lim (1999).

Representatives of all species collected were pho-

tographed, tissued for liver, preserved, and deposited in

the Department of Wildlife (PERHILITAN; JAM cat.

nos.), Kulala Lumpur, Malaysia; Forest Research

Institute of Malaysia (FRIM), Kulala Lumpur, Malaysia;

the Zoological Reference Collection (ZRC) of the

Raffles Museum of Biodiversity Research at the

National University of Singapore; and the La Sierra

University Herpetological Collection (LSUHC),

Riverside, California, USA. Material from

Hendrickson's (1966a,b) collection deposited in the

Bishop Museum (BPBM), Honolulu, Hawai’i and Day's

(1990) collection (uncatalogued in the British Museum

of Natural History, London) was also examined. All tis-

sues have been deposited at La Sierra University.

Photographs are catalogued in the La Sierra University

Photographic Collection (LSUPC) in the herpetology

laboratory of L. Lee Grismer. The taxonomy of ranid

genera follows Inger and Voris (2001).

Annotated Checklist

Amphibia

Order: Anura

Family: Megophryidae

Leptolalax kajangensis Grismer, Grismer, and

Youmans, 2004

(Fig. 9)

Localities. - Larvae collected from 400 m on

Gunung Kajang were reported by Lim and Lim (1999).

Day (1990) reported larvae from a pool at Gua Tengkuk

Air at 845 m. On 19 March 2001, we collected two

adults (ZRC 1.7714-15) from Gua Tengkuk Air sitting

on boulders approximately 2 m from the water 10 m

below the surface of the cave floor. On 23 March, 2001,

a specimen (LSUHC 4431) was collected from a cave at

the summit of Gunung Kajang at 1035 m. On 10 August,

2002 and adult female (LSUPC-F1497) was observed at

210m elevation along the Tekek-Juara trail. This species

occurs from lowland dipterocarp to ridge forests. This

species was originally known only from tadpoles and

was reported as Leptobrachium sp. (Day, 1990) and

Leptolalax gracilis (Lim and Lim, 1999). Examination

of the adults indicated they belonged to the new species

Leptolalax kajangensis (Grismer et al., 2004).

2004

Asiatic Herpetological Research

Vol. 10, p. 255

Family: Bufonidae

Ansonia tiomanica Hendrickson, 1966

(Fig. 10)

Localities. - Gua Sinah at Ulu Lalang (800 m;

Hendrickson, 1966b).

New localities. - On 3 November, 2000, a specimen

(LSUPC-F439-45) was photographed sitting on the ver-

tical surface of a rock near the top of the Tekek-Juara

trail at 220 m. On 19-21 March, 2001, we observed

approximately 10 specimens in Gua Tengkuk Air at 845

m on Gunung Kajang. All were climbing on large boul-

ders both in and outside of the cave. This species ranges

from lowland dipterocarp to high hill dipterocarp forest

in association with boulders in the vicinity of water.

Bufo asper Gravenhorst, 1829

Localities. - Sungai Nipah (80-200 m; Day, 1990).

New localities. - On 21 March 2001, we observed a

specimen (LSUPC-F380-81) along the Sungai

Mentawak (ca. 195 m) along the water's edge on a

downward sloping face of a boulder. On 23 March,

2002, we observed 11 specimens during the day and

night sitting on rocks at the edge of and within the

Sungai Mentawak of which three (LSUHC 4443, 4447-

48) were collected. This species occurs in coastal vege-

tation and lowland dipterocarp forest.

Bufo melanostictus Schneider, 1799

Localities. - Kampung Tekek (Lim and Lim, 1999).

New localities. - On 7 July, 2001, we collected

specimens from Kampung Mukut (ca. 10 m) and on 9

July additional specimens (LSUHC 3754; ZRC 1.8248-

49) were collected from the beginning of the Tekek-

Juara trail (ca. 80 m) on the forest floor. On 9 July,

2001, a specimen (LSUHC 3814) was collected beneath

a board at Kampung Paya (ca. 15 m). This species

ranges from coastal vegetation to lowland dipterocarp

forest.

Bufo parvus Boulenger, 1877

Localities. - Sungai Paya; Kampung Juara; and

Sungai Keliling (Lim and Lim, 1999).

New localities. - Two specimens (JAM 1860-61)

from Kampung Tekek were collected on 6 November,

1997. Additional specimens (LSUHC 3969-71, 3976-

77, 3981; ZRC 1.8269) were collected on 11-17 July

2001 from the Tekek-Juara trail pitfall traps (142 m) and

from Telok Dungun (ca. 25 m; ZRC 1.826j) on 12 July,

2001. This species ranges from coastal vegetation to

lowland dipterocarp forest.

Family: Microhylidae

Chaperina fusca Mocquard, 1 892

Localities. - Sungai Air Besar; Teluk Penut; and

between Kampung Tekek and Kampung Lalang (Denzer

et al., 1989: 27).

New localities. - On 10 July, 2001, a specimen

(LSUHC 3833) was collected from Telok Nipah (ca. 20

m) under a flat rock at the edge of a narrow stream. At

Telok Penut, tadpoles were also collected from deep

holes in rocks located along the shore of a dried-up

stream bed on 9 July, 2001 and were observed along the

Tekek-Juara Trail in root holes, tree cavities, and pitfall

traps from 200-245 m elevation. On 7 July, 2002 adults

(LSUHC 4667-71) and tadpoles were found in water

catchments within fallen palm fronds along the Sungai

Mentawak at 195 m. This species ranges from coastal

vegetation to low hill dipterocarp forest.

Kalophrynus pleurostigma Tschudi, 1838

(Fig. 11)

Localities. - Gunung Kajang trail at 245 m in eleva-

tion (Escobar et ah, 2003).

New localities. - On 17 July, 2002, a specimen

(LSUHC 4682) was collected at 200 m elevation along

the Tekek-Juara trail. On 9 August, 2002, a specimen

(LSUHC 5024) was collected at night on Gunung

Kajang at 813 m as it was ascending the vertical surface

of a small rock. This species ranges from lowland

dipterpcarp to high hill dipterocarp forests.

Family: Ranidae

Fejervarya cancrivora Gravenhorst, 1829

Localities. - Kampung Lalang and Kampung Tekek

(Hendrickson, 1966b).

New localities. - On 12 July, 2001, a specimen was

collected at Telok Dalam (ca. 10 m) and released. The

individual was sitting approximately 1 m from the edge

of the water. When approached another specimen

jumped into the water and buried itself in leaf liter at the

bottom of the stream. This species occurs in mangroves

and coastal vegetation.

Limnonectes blythii Boulenger, 1920

Localities. - Sedagong; Sungai Air Raja at

Kampung Genting; Sungai Durian Kallang at Kampung

Paya; Sungai Besar waterfall along Tekek-Juara trail;

Sungai Pasal; Sungai Keliling; Sungai Paya; Sungai

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2004

Baharu; and Tekek-Juara trail (Lim and Lim, 1999).

New localities. - We add an additional specimen

(LSUHC 3832) from Sungai Raya (ca. 100 m) collected

on 10 July, 2001 and from the Sungai Mentawak

(LSUHC 4642; 195 m) collected on 19 July, 2002. Both

specimens were sitting near the water's edge on a large

rock at night. Additonal speciemens (LSUHC 4646-47)

were collected from a small stream at the back of Telok

Monkey (ca. 3 m) on 19 July, 2002. This species occurs

in coastal vegetation and lowland dipterocarp forest.

Limnonectes hascheanus Stoliczka, 1870

Localities. - Sungai Paya (Leong, 2000); Tekek-

Juara Trail, Ulu Lalang (Hendrickson, 1966b).

New localities. - On 1 1 July, 2001, three specimens

(LSUHC 3856, 3864, 3868) were collected from the

Sungai Besar waterfall on the Tekek-Juara trail (220 m)

while sitting near the base of the waterfall on a rocky

slope. On 13 July, 2001, a specimen of L. hascheanus

was observed but not collected at Telok Dalam. On 12

July, 2001 a specimen (LSUHC 3887) was collected

from Sungai Dungun (ca.10 m). Hendrickson (1966b)

reported two specimens of this species as "Rana

(Discodeles/Platymantis) sp." Upon examination of his

material (BPBM 14200-2001) we find them to be L.

hascheanus. This species occurs in lowland dipterocarp

forest.

Rana chalconota Schlegel, 1837-1844

Localities. - Tekek-Juara trail; Kampung Tekek;

Sungai Keliling; Sungai Mentawak; and Sedagong (Lim

and Lim, 1999).

New localities. - On 21 March, 2001, a juvenile

(LSUPC-F285) was observed sitting on a leaf approxi-

mately 0.5 m above the ground behind a house in

Kampung Juara (5 m). On 9 July 2001, three specimens

(LSUHC 3803-05; ZRC 1.8255) were collected from

Sungai Nipah (10 m). All were found inside large boul-

der caves situated within the stream. On 12 July, 2001,

three specimens (LSUHC 3886, 3909-10) were collect-

ed from Telok Dungun (15 m). This species ranges from

coastal vegetation to low hill dipterocarp forest.

Rana erythraea Schlegel, 1837-1844

Localities. - Kampung Tekek (Hendrickson,

1966b).

New localities - On 9 July, 2001, a specimen

(LSUHC 3815) was collected at sea level from

Kampung Paya from along a large pond just behind the

beach. On 21 March, 2002, one specimen was found

during the day sitting on the branch of a mangrove tree

I m above the water at Air Batang (ca. 5 m). This

species occurs in mangrove and coastal vegetation.

Rana hosii Boulenger, 1891

Localities. - Tekek-Juara trail; Kampung Paya;

Sungai Kalang; and Sungai Ayer Besar waterfall on the

Tekek-Juara trail (Lim and Lim, 1999).

New localities. - On 13 July, 2001, a specimen was

observed along Sungai Dungun, but not collected. On

II July, 2001, a specimen (LSUHC 3819) was collected

along Sungai Raya (ca. 50 m). On the evening of 19

July, 2002, three specimens (LSUHC 4625-26) were

collected along the Sungai Mentawak at 195 m in eleva-

tion while sitting on vegetation. This species occurs in

lowland dipterocarp and low hill dipterocarp forest.

Rana picturata Boulenger, 1920

(Fig. 12)

Localities. - Tributary of Sungai Mentawak (Day,

1990).

New localities. - Day (1990) reported a specimen

Rana signata from a tributary of the Sungai Mentawak

at 300 m. We have examined that specimen (uncata-

logued in the British Museum of Natural History) and

find it to be R. picturata. We report additional speci-

mens of R. picturata from the Sungai Mentawak at 1 95

m collected on 24 March, 2002 (LSUHC 4435-41) and

19 July, 2002 (LSUHC 4636-40). All were found

perched on rocks or vegetation along the water's edge

during the evening. This species is found in coastal and

lowland dipterocarp forest.

Family: Rhacophoridae

Nyctixalus pictus Peters, 1871

(Fig. 13)

Localities. - A single specimen (ZRC 1.8268) was

collected from the Tekek-Juara trail (ca. 240 m) on the

night of 16 July, 2001 (Leong and Crane, 2002). It dif-

fers from other populations of N. pictus in that its body

and limbs are yellow in coloration instead of orange or

brownish. Another specimen was heard calling on 14

July, 2001 along a small stream on the Tekek-Juara trail

(ca. 100 m) by LBL and NSY. This specimen constitutes

a new record for Pulau Tioman. This species occurs in

lowland dipterocarp forest.

Polypedates leucomystax Boie, 1 829

Localities. - Kampung Tekek and Kampung Juara

(Lim and Lim, 1999).

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New localities. - On 7 July, 2001, a specimen

(LSUHC j770) was collected on the Tekek-Juara trail

(241 m) while sitting on a leaf approximately 1 m above

the ground. On 1 1 July, 2001, a specimen was observed

in the Sungai Dungun (ca. 10 m) but not collected. This

species ranges from coastal vegetation to low hill dipte-

rocarp forest.

Theloderma horridum Boulenger, 1903

(Fig. 14)

Localities. - On the evening of 22 March, 2002, one

specimen ot Theloderma horridum was found on the

side ot a large tree (ca. 1 m in diameter) near the Tekek-

Juara trail at 245 m in elevation (Grismer et al. 2003a).

On 14 July, 2002, another specimen was found on the

Tekek-Juara trail at 140 m elevation. This species is

found in lowland dipterocarp forest.

Reptilia

Order: Squamata

Family: Agamidae

Acanthosaura armata Ftardwicke and Gray, 1827

Localities. - Tekek-Juara trail (Hendrickson,

1966b).

New localities. - On 13 July, 2001, a specimen

(LSUHC 3873) was collected in primary forest south of

Kampung Salang (ca.80 m). On 18 March, 2001 two

specimens were observed at Gua Tengkuk Air on

Gunung Kajang at 845 m. One was photographed

(LSUPC-L7070-71). The latter specimens had patterns

that were considerably darker than those of specimens

from lowland forests which appears to be a function of

substrate matching. On 17 July, 2002, two specimens

were collected at Telok Monkey (ca. 40 m). One

(LSUHC 4598) was 1 m above ground level on a small

(ca. 10 cm in diameter) tree facing head-up. The other

(LSUHC 4599) was observed sitting on a hollow log

that was lying on the forest floor. When approached, it

ran into the hollow of the log in an attempt to escape.

This species ranges from coastal vegetation to high hill

dipterocarp forest.

Aphcmiotis fusca Peters, 1 864

Localities. - Sedagong; Tekek-Juara trail; Kampung

Asah (Lim and Lim, 1999).

New localities. - On 18 March, 2001, an individual

was photographed (LSUPC-L593 1-36) and released on

Gunung Kajang at 320 m in elevation. On 12 July, 2001,

a male and female (LSUHC 3897; ZRC 2.5147) were

collected from Telok Dalam off the same tree, facing

head up approximately 1 .5 m above the ground at 20 m.

On 9 July, 200 1 , a sighting was made at Sungai Benuang

at 15 m. On 9 July, 2001, an individual (LSUHC 3818)

was collected from a tree in Kampung Mukut and anoth-

er (ZRC 2.5131) from a sapling approximately 0.5 m

above the ground at Telok Nipah at 20 m. This species

ranges from lowland dipterocarp to low hill dipterocarp

forest.

Bronchocela cristatella Kuhl, 1820

Localities. - Tekek-Juara trail near Kampung Juara;

Kampung Juara; Kampung Tekek; and Kampung Mukut

(Lim an Lim, 1 999).

New localities. - On 19 July, 2000, a specimen was

photographed (LSUPC-L762) at Kampung Air Batang at

15 m. On 13 July, 2001, a specimen was observed from

primary forest in Telok Dalam at 15 m. On 18 July,

2002, one specimen (LSUHC 4613) was observed on a

tree in coastal forest at Telok Monkey (ca. 20 m). On 1 1

August, 2002, a specimen (LSUHC 5046) was collected

from 15 m above ground level on a branch at the base of

Gunung Kajang at 291 m in elevation. This species

occurs from coastal vegetation to low hill dipterocarp

forest.

Draco fimbriatus Kuhl, 1820

(Fig. 15)

Localities. - On 8 July, 2001, a specimen (ZRC

2.5130) was collected from a large dipterocarp tree

approximately 6 m above the ground at 160 m on the

Tekek-Juara trail. On 9 July, 2001, a second specimen

(LSUHC 3823) was collected approximately 4 m above

the ground at 142 m on the same trail. On 1 7 July, 2002.

a male and female were observed 20 m above ground

level on the side of a tree in coastal vegetation at Telok

Monkey (ca. 20 m). The male (LSUHC 4601) was col-

lected. These specimens constitute new island records.

This species occurs in coastal vegetation and lowland

dipterocarp forest.

Draco haematopogon Boie, 1831

(Fig. 16)

Localities. - On 20 March. 2001, an adult male

(SVL 106 mm) and female (SVL 100 mm) were collect-

ed, photographed (LSUPC-L7072-78), and released

from near Gua Tengkuk Air on Gunung Kajang at 845

m. The male had a yellow dewlap with a black spot at

base surrounded by orange and the female had an

orangish dewlap with a yellow fringe. Both were found

on a large dipterocarp tree facing head up approximate-

Vol. 10, p. 258

Asiatic Herpetologica/ Research

2004

Fig. 9. Leptolalax kajangensis from Gua Tengkuk Air, Gunung Kajang.

Fig. 10. Ansonia tiomanica from Tekek-Juara trail.

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Fig. 1 1 . Kalophrynus pleurostigma from the Tekek-Juara trail.

Fig. 12. Rana picturata from the Sungai Mentawak.

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2004

Fig. 13. Nyctixalus pictus from the Tekek-Juara trail.

Fig. 14. Theloderma horridum from the Tekek-Juara trail.

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Vol. 10, p. 26)

Fig. 1 5. Draco fimbriatus from the Tekek-Juara trail.

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Fig. 1 8. Crytodactylus tiomanensis from the Tekek-Juara trail.

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Vol. 10, p. 263

Fig. 19. Lipinia vittigera from Salang.

Fig. 20. Sphenomorphus sp. from the summit of Gunung Kajang.

Vo!. 10, p. 264

2004

Fig. 22. Calamaria ingeri from the Tekek-Juara trail.

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Fig. 23. Chrysopelea pelias from the Tekek-Juara trail.

Fig. 24. Dendrelaphis striatus from Teluk Monkey.

Vol. 10, p. 266

2004

Fig. 25. Fordonia leucobalia from Kampung Tekek.

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Fig. 27. Gonyosoma oxycephalumUom Kampung Juara. Photo by Pauli Hien.

Fig. 28. Oligodon purpurescens from the Gunung Kajang trail.

• ■

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2004

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Fig. 29. Rhabdophis chrysargos from the Tekek-Juara trail.

Fig. 30. Sibynophis melanocephalus from Kampung Juara.

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Vol. 10, p. 269

Figure 31. Trimeresurus sp. (male) from Tekek-Juara trail.

ly 6 m above the ground. These specimens constitute a

new island record. This species occurs in high hill dipte-

rocarp forest.

Draco melanopogon Boulenger, 1887

Localities. -Tekek-Juara trail; Sedagong; Kampung

Asah; Kampung Paya; and Gunung Kajang at 800 m

(Lim an Lim, 1999).

New localities. - On 9 and 1 1 March, 2001, respec-

tively, a specimen (LSUHC 3809) was colleted from

Telok Nipah (10 m) and Sungai Nipah (LSUHC 3869) at

20 m. Day (1990) reported an unidentified species of

Draco at Telok Nipah based on his sighting of two indi-

viduals with pinkish dewlaps displaying at one another.

We observed individuals with pinkish dewlaps at Telok

Nipah and elsewhere to be female D. melanopogon. On

13 July, 2001, a specimen (LSUHC 3908) was collected

at Telok Dalam in primary forest at 20 m. On 12 July,

2001, several specimens were observed at Telok Dungun

at 10-35 m. On 13 July, 2001, a specimen (LSUHC

3903) was collected at Kampung Salang at 10-15 m.

Two specimens (LSUHC 3798. 3809) were collected

from Sungai Benuang (10 m) and one (LSUHC 3822)

from Sungai Raya on 9 July, 2001 at 40 m. One speci-

men (LSUHC 502 1 ) was collected on Gunung Kajang at

813 m on 8 August, 2002. This species ranges from

coastal vegetation to high hill dipterocarp.

Draco sum atr anus Schlegel, 1844

Localities. - Kampung Tekek; Sungai Mukut at

Kampung Mukut; and Kampung Air Batang (Lim and

Lim, 1999).

New localities. - On 9 March. 2001. a male with a

blue head was collected from Sungai Nipah at approxi-

mately 20 m. On 8 July, 200 1 , two specimens (LSUHC

3777; ZRC 2.5121) were collected from the Tekek-Juara

trail in lowland forest at 80-150 m. On 12 July, 2001 an

individual (LSUHC 3899) from Telok Dalam was found

during mid-day in the mangroves approximately 3 m

above ground. On 13 July, 2001, a specimen (LSUPC-

L3 103-04) was photographed at Telok Dungun at an ele-

vation of 15 m. On 13 July, 2001, an individual was

observed in coastal vegetation at Kampung Salang at

approximately 10 m in elevation. All lizards were found

facing head-up on trees. This species ranges from man-

grove to lowland dipterocarp forest.

Vol. 10, p. 270

2004

Gonocephalus chamaeleontinus Laurenti, 1768

Localities. - Tekek-Juara trail, Kampung Paya

along the trail to Gunung Kajang (Lim and Lim, 1999).

New localities. - On 9 July, 2001 an individual was

observed on Sungai Benuang at 15 m. On 10 July, 200 1 ,

a specimen (LSUHC 3881) was found at Telok Dungun

in primary forest at 20 m. On 13 July, 2001, a specimen

was observed from Kampung Salang in primary forest at

10 m. On 19 July, 2002, two specimens (LSUHC 4623-

24) were observed at night sleeping on vegetation ca. 5

m above ground level along the Sungai Mentawak at

195 m. On 10 August, 2002, a specimen was observed

on a small tree at Gua Tengkuk Air on Gunung Kajang

at 845 m. All were found 2-5 m above the ground on the

side of trees facing head-up. This species occurs from

lowland dipterocarp to high hill dipterocarp forest.

Gonocephalus grandis Gray, 1 845

Localities. - Sungai Asah; Sungai Nipah;

Sedagong; and Sungai Air Besar (Lim and Lim, 1999).

New localities. - On 1 1 July, 2001, a male and a

juvenile were sighted on trees along the Sungai Raya but

not collected. On 15 July, 2001, a adult male was col-

lected from a trail behind and leading out of Kampung

Tekek. On 19 July, 2002, four specimens (LSUHC

46 1 9-22) were observed on trees near the edge of Sungai

Mentawak at 195 m. Additional specimens were

observed on trees along a small stream at 291 m at the

base of Gunung Kajang. This species ranges through

lowland dipterocarp to low hill dipterocarp forests pri-

marily in association with streams.

Family Gekkonidae

Cnemaspis kendallii Gray, 1 845

Localities. - Tekek-Juara trail (Lim and Lim, 1 999).

New localities. - On 18 March, 2001, individuals

were observed at the base of Gunung Kajang and along

the Sungai Mentawak (80-200 m). Additional speci-

mens (LSUHC 3797) were collected at Sungai Benuang

(9 July, 2001; LSUHC 3797; ca. 20 m), Kampung Paya

(9 July, 200 1 ; LSUHC 38 1 1 ; ca. 15 m), Sungai Raya ( 1 1

July, 2001; LSUHC 3820; ca. 12 m), Kampung Salang

(12 July, 2001; LSUHC 3878; ca. 10 m), and Telok

Dalam (12 July, 2001; observed only). Additional spec-

imens were found at Mukut (15 July, 2002; LSUHC

4566; ca. 50 m) and Telok Monkey (18 and 29 July,

2002; ca. 35 m; LSUHC 4615 and 4666, respectively).

All were found on rocks or trees during both day and

night. This species ranges from coastal vegetation to

low hill dipterocarp forest.

Cnemaspis limi Das and Grismer, 2003

(Fig. 17)

Localities. - Tekek-Juara trail; Gunung Rokam;

Gunung Kajang at 950 m (Lim and Lim, 1999).

New localities. - On 19 March, 2001, specimens

(LSUPC-L3662-65) were photographed at Gua Tengkuk

Air on Gunung Kajang at 845 m and from the summit at

1035 m. On 10 July, 2001, three specimens (LSUHC

3888, 3902; ZRC 2.5 149) were collected in primary for-

est at Kampung Salang at 20 m. On 1 1 July, 2001, a

specimen was observed at Telok Dungun at 100 m. On

9 July, 2001, a specimen was observed at the Sungai

Raya at 25 m. On 17 and 18 July, 2002, two specimens

(LSUHC 4596, 4616) were collected off rocks at Telok

Monkey (ca. 20 m). On 19 July, 2002, one specimen

(LSUHC 4629) was collected from the Sungai

Mentawak at 195 m. The Pulau Tioman population was

originally reported as C. nigridia (Hendrickson, 1966a)

but was described as a new species (Das and Grismer,

2003) All specimens were observed on steep faces of

large boulders in shaded areas or within deep rock

crevices. This species occurs from coastal vegetation to

ridge forest.

Cosymbotus craspedotus Mocquard, 1 890

Localities. - On 9 November, 1997, a single speci-

men (JAM 1834) was collected from the palm groves in

Kampung Tekek at the base of the Tekek-Juara trail at 50

m while facing head down approximately 3 m above the

ground. This constitutes a new island record. This

species occurs in coastal vegetation.

Cosymbotus pi atyurus Schneider, 1792

Localities. - Kampung Tekek (Grismer et al.,

2002a).

New localities. - On 13 July, 2001, a juvenile (ZRC

2.5146) was collected in a restaurant on the beach at

Kampung Salang. This species occurs in coastal vege-

tation.

Cyrtodactylus quadrivirgatus Taylor, 1962

Localities. - No locality data provided (Manthey

and Grossmann, 1997:228).

New localities. - On 2 November, 2000, a specimen

was observed and photographed (LSUPC-L33 13) while

sitting on a leaf approximately 1 .5 m above the ground

along the Tekek-Juara trail at 190 m. On 19 2001 March,

a single specimen was observed at Gua Tengkuk Air on

Gunung Kajang at 845 m. One specimen (LSUHC 5622)

was collected off vegetation along the Sungai Mentawak

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at 195 m on 7 August, 2002. This species ranges from

lowland dipterocarp to high hill dipterocarp forest.

Cyrtodactylus tiomanensis Das and Lim, 2000

(Fig. 18)

Localities. - Tekek-Juara trail; Gunung Kajang at

400 m and 750 m (Lim and Lim, 1999).

New localities. - On 12 March, 2001, several spec-

imens were observed on large boulders within and

around Gua Tengkuk Air on Gunung Kajang at 845 m.

On 20-22 March, 2001, several specimens were

observed (LSUPC-L7002-09) on boulders, trees, and

leaf-litter at the forest's edge on the beach 1 km south of

Kampung Tekek. One specimen (LSUHC 4597) was

collected from Telok Monkey (ca. 20 m) on 17 July,

2002. This species ranges from coastal vegetation to

high hill dipterocarp forest.

Gehyra mutilata Wiegmann, 1834

Localities. - Kampung Tekek and Kampung Mukut

(Hendrickson, 1966a).

New localities. - On 16 March, 2001, a specimen

(LSUPC-L6080-84) was photographed during the

evening on the Tekek-Juara trail at approximately 200

m. This species occurs in lowland dipterocarp forest and

in disturbed habitat.

Gekko monarchus Dumeril and Bibron, 1836

Localities. -Sungai Keliling (Hendrickson, 1966a).

New localities. - On 22 March, 2001, specimens

(LSUPC-L7044-45) were photographed from the Tekek-

Juara trail, on boulders, trees or short vegetation from

50-100 m. On 23 March, 2001, specimens (LSUPC-

L7046-49) were photographed on rocks from the boul-

der caves on the beach 1 km south of Kampung Tekek.

This species occurs in coastal vegetation and lowland

dipterocarp forest.

Hemidactylus frenatus Dumeril and Bibron, 1836

Localities. - Kampung Tekek (Hendrickson,

1966a).

New localities. - On 9 July, 2001, two specimens

(LSUHC 3807-08) were collected at Telok Nipah at 5 m

beneath the wood of an abandoned shack. On 22 March,

2001, a specimen was collected and released at

Kampung Juara. This species occurs in coastal vegeta-

tion usually near human habitations.

Ptychozoon kuhli Stejneger, 1902

Localities. - On 16 March, 2001, a specimen

(LSUPC-L70 10-26) was photographed along the Tekek-

Juara trail approximately 3 m above the ground on a

large strangler fig at approximately 200 m. On 18 March

2001, an individual was found on the Tekek-Juara trail

facing head down on a large dipterocarp tree approxi-

mately 6 m above the ground at 250 m. On 10 July,

2001, a single specimen (LSUHC 3835) was found on

the Tekek-Juara trail on a large metal pole approximate-

ly 3 m above the ground at 142 m. On 16 July, 2001, a

specimen was sighted in a coconut palm grove in

Kampung Tekek at the base of the Tekek-Juara trail at 80

m. One specimen (LSUHC 5042) was collected from 20

m above ground level on the side of a tree along the

Sungai Mentawak at 195 m on 11 August, 2002. These

specimens confirm this species' presence on Pulau

Tioman, first reported as an unconfirmed sighting by

Grismer et al. (2002a). This species ranges from coastal

vegetation to lowland dipterocarp forest.

Family: Scincidae

Dasia olivacea Gray, 1 839

Localities. - Kampung Tekek; Kampung Paya;

Sungai Asah (Hendrickson, 1966a).

New localities. - On 16 March, 2001, a specimen

was observed on the Tekek-Juara trail at 200 m in eleva-

tion in primary forest. Another was seen on a large

dipterocarp tree approximately 2.5 m above the ground

at 80 m. On 10 July, 2001, an individual (LSUHC 3863)

was collected from Kampung Mukut at 5 m. On 12 July,

2001, a sighting of a D. olivacea was recorded at

Kampung Salang at 10 m. This species occurs from

coastal vegetation to low hill dipterocarp forest.

Emoia atrocostata Lesson, 1830

Localities. - On 11 July, 2001, an individual was

sighted at Kampung Salang at 10 m on a wooden bridge

near the coast. On the same day a specimen was collect-

ed from intertidal rocks on neighboring Pulau Tulai

(Grismer et al., 2001b). This species occurs in the man-

groves and along rocky shorelines (see Hendrickson,

1966a) but remains unconfirmed for Pulau Tioman.

Eutropis multifasciata Kuhl, 1820

Localities. - Sedagong; Sungai Pasal; Tekek-Juara

trail; and Kampung Paya (Lim and Lim, 1999).

New localities. - On 11 July, 2001, several speci-

mens were sighted at Telok Dungun and Telok Dalam

(10-35 m). On 12 July, 2001, specimens were observed

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Asiatic Herpetological Research

2004

from Kampung Salang (10 m) and from rock cracks in

the waterfall in the Sungai Raya at 80 m. One individ-

ual observed at the waterfall jumped off a rocky face

into the water approximately 2 m below to escape.

Many other specimens were observed along the Sungai

Mentawak on 19-22 July, 2002. Juveniles were found

on rocks within the stream and would jump into the

water to escape. Some would dive below the surface

and cling to the edge of rocks for several minutes. Many

others were observed along the Gunung Kajang trail

from 195-245 m in elevation. This species ranges from

coastal vegetation to low hill dipterocarp forest.

Larutia seribuatensis Grismer, Leong, and Yaakob,

2003

Localities. - On 20 August, 2002, an individual

(LSUPC-L182) was observed abroad on the forest floor

in high hill dipterocarp forest at ca. 400 m immediately

following a rain shower. This species is also known

from coastal vegetation on Pulau Tulai (Grismer et al.,

2003). This species ranges from coastal vegetation to

high hill dipterocarp forest. It is currently being

described as a new species endemic to Pulau Tulai and

Pula Tioman (Grismer et ah, 2003).

Lipinia vittigera Boulenger, 1 894

(Fig. 19)

Localities. - Unconfirmed sighting at Kampung

Asah (Lim and Lim, 1999).

New localities. - From 10-16 July, 2001, specimens

were sighted at Sungai Raya (40 m), Tekek-Juara trail

(210 m), the base of the Tekek-Juara trail (45 m; a juve-

nile with a bright orange tail), Telok Nipah (25 m), and

Telok Dungun (30 m). One specimen (ZRC 2.5 1 5 1) was

collected in primary forest at Kampung Salang at 40 m.

One specimen was cited on a tree at the base of Gunung

Kajang at 291 m on 24 March, 2002. All were observed

foraging on the sides of large trees 3-5 m above the

ground. A hatchling (LSUHC 4814) was collected in

flotsam and coral at the water's edge in Telok Monkey.

These specimens confirm this species' presence on Pulau

Tioman. This species ranges from coastal vegetation to

low hill dipterocarp forest.

Lygosoma bowringii Gunther, 1 864

Localities. - On 15 March, 2001, a specimen was

collected beneath a trash can in Kampung Tekek, pho-

tographed (LSUPC-L6058-66), and released. On 18

March, 2001, a specimen was observed at Kampung

Juara at 5 m. On 8 July, 2001, a specimen was collect-

ed from the Tekek-Juara trail at 140 m. On 9 July, 200 1 ,

a specimen was sighted in Kampung Paya at sea level.

This species ranges from coastal vegetation to lowland

dipterocarp forest.

Sphenomorphus scotophilus Boulenger, 1900

Localities. - Gunung Kajang at 845 m and the

Tekek-Juara trail (Lim and Lim, 1999).

New localities. - On 19 March, 2001, two speci-

mens (LSUPC-L3286-87) were observed and pho-

tographed from the summit of Gunung Kajang at 1035

m and at Gua Tengkuk Air at 845 m. On 9 July, 2001, a

specimen (LSUHC 3806) was collected at Sungai

Benuang at 20 m. On 9 July, 2001, a specimen (ZRC

2.5135) was collected from the rocks in the Sungai Raya

at 45 m. Several were seen on rocks along the trail south

of Salang on 13 July, 2001. Additional specimens were

collected from Telok Nipah (9 July, 2001; LSUHC

3806), Mukut (9 July, 2001; LSUHC 3821), and Telok

Monkey (17 July, 2001; LSUHC 4595 between 10 m

and 20 m). This species ranges from coastal vegetation

to ridge forest.

Sphenomorphus sp.

(Fig. 20)

New localities. - On 22 March, 2002, a specimen

(LSUHC 4429) of a new species of Sphenomorphus was

collected along the Gunung Kajang Trail at 510 m in ele-

vation. On 8 August, 2002, a hatchling of the same

species (LSUHC 5031) was collected on the summit of

Gunug Kajang at 1035 m. Many other specimens were

observed in the leaf litter of the forest floor between

300-1035 m on Gunung Kajang. This species ranges

from low hill dipterocarp to ridge forest. It is currently

being described (Grismer, in prep.).

Family: Varanidae

Varanus nebulosus Gray 1 83 1

Localities. - Sedagong; Kampung Air Batang;

Kampung Salang; and Kampung Tekek (Lim and Lim,

1999).

New localities. - On 18 March, 2001, several indi-

viduals were observed in Kampung Juara basking on

coconut palms 1-6 m above the ground. On 17 March,

2001, a juvenile and adult were observed along the

Tekek-Juara trail (100 m and 275 m). Varanus nebulo-

sus were also seen at Telok Dalam, Telok Dungun.

Kampung Paya, Kampung Mukut, and Telok Nipah (0-

80 m). This species ranges from coastal vegetation to

lowland dipterocarp forest.

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Asiatic Herpetological Research

Vol. 10, p. 273

Var anus salvator Laurenti, 1768

Localities. - Sedagong; Kampung Salang;

Kampung Asah; Kampung Tekek (Lim and Lim, 1999).

New localities. - On 9 July, 2001, a sighting of a

Varanus salvator approximately 1.5 m in SVL was made

in Kampung Paya at 5 m. On 16 March a sighting of a

specimen was recorded in Telok Nipah. On 19 March,

2002, two specimens were observed along the banks of

the Sungai Mentawak at 195 m 2 km inland from the

coast. This species occurs in mangroves, coastal vege-

tation, and lowland dipterocarp forest provided there are

waterways serving as dispersal corridors.

Family: Dibamidae

Dibamus tiomanensis Diaz, Leong, Grismer and

Yaakob, 2004

Localities. - Kampung Paya (Lim and Lim, 1999);

Tekek-Juara trail at 80 m (Diaz et al. 2004).

New localities. - Lim and Lim (1999) reported this

population as D. cf. alfredi based on the only known

specimen (ZRC 2.3410). On 14 August, 2002 a speci-

men was found beneath a log at Air Batang at sea level.

This species is found from mangrove to lowland dipte-

rocarp forest.

Family: Typhlopidae

Ramphotyphlops albiceps Boulenger, 1898

(Fig. 21)

Localities. - On 8 July, 2001, a specimen (ZRC

2.5125) was collected from the Tekek-Juara trail, at 241

m in elevation. It was unearthed 0.3 m below the sur-

face of the ground in rocky soil while placing pit fall

traps. This constitutes a new island record. This species

occurs in low hill dipterocarp forest.

Ramphotyphlops braminus Daudin, 1 803

Localities. - Kampung Juara (Day, 1990).

New localities. - On 21 March, 2001, a specimen

(LSUPC-S2814) was found beneath a large piece of

wood in Kampung Tekek (ca. 10 m) and photographed.

On 9 July, 2001, an individual (ZRC 2.5134) was col-

lected at Kampung Paya at 5 m. This species occurs in

mangrove and coastal vegetation.

Family: Pythonidae

Python reticulatus Schneider, 1801

Localities. - Kampung Tekek and north of Telok

Dungun (Hendrickson, 1966a).

New localities. - On 6 August, 2001, K. P. Lim

(pers. comm.) informed LLG of a specimen measuring

approximately 5 m SVL he observed in Kampung Paya

on 17 July, 2001. Several specimens have been

observed by JLG, LLG, and TMY at Air Batang,

Berjaya, Kampung Juara, and Telok Nipah from 0-15 m.

This species ranges from mangrove to lowland diptero-

carp forest.

Family: Colubridae

Ahaetulla prasina Boie, 1 827

Localities. - Tekek-Juara trail at the Sungai Air

Besar crossing (Hendrickson, 1966a).

New localities. - On 20 March, 2001, a specimen

was observed and photographed (LSUPC-S2892-99) at

Gua Tengkuk Air at 845 m. On 13 July, 2001, an adult

specimen (LSUHC 3914) was collected in lowland for-

est at Telok Dungun. Two specimens (LSUHC 4687-88)

were collected from the Tekek waterfall trail at ca. 100

m on 18 July, 2002. This species occurs from coastal

vegetation to high hill dipterocarp forest.

Boiga drapiezii (Boie, 1 827)

Localities. - Tekek-Juara trail at 213 m in eleva-

tion. One specimen (LSUPC-S3797) was collected on

14 July 2003 2 m above the ground as it was crawling

down the side of a palm tree. This species represents a

new record for P. Tioman.

Boiga nigriceps Gunther, 1 863

Localities. - Kampung Juara at 100 m (Hien et al.

2001).

New localities. - On 26 March, 2002, an adult

(LSUHC 4494) was found on the Tekek-Juara trail at

night at ca.175 m as it was crawling across the trail. On

16 July, 2002, and juvenile (LSUHC 4591) was found at

night 2 m above the ground in a small tree at the damn

on the Tekek-Juara trail at 220 m. On 18 July, 2002, an

adult (LSUHC 4686) was found crawling through brush

on the Tekek waterfall trail at 185 m. This species

ranges from coastal vegetation to lowland dipterocarp.

Calamaria ingeri Grismer, Kaiser, and Yaakob, 2004

(Fig. 22)

Localities. - On 22 July, 2002, a specimen of

Calamaria (LSUHC 4716) was found within a trap in

the lower pitfall trap array. On 23 July, 2002, another

specimen (LSUHC 4800) was found in the same trap.

Vol. 10, p. 274

Asiatic Herpetological Research

2004

These specimens resemble C. lovii gimletti in coloration

but lack the enlarged second supralabial of all C. lovii

and have unique combinations of characters that set

them apart from all other Calamaria (Inger and Marx,

1965). This population was described as C. inger i

(Grismer et al. ,2004a). This species is found in lowland

dipterocarp forest.

Chrysopelea pelias Linnaeus, 1758

(Fig. 23)

Localities. - Kampung Juara (Day, 1990).

New localities. - On 19 March, 2001, a specimen

(LSUPC-S2793-2801) was observed and photographed

on a large dipterocarp approximately 4 m above the

ground on the Tekek-Juara trail at 195 m. We collected

this snake two hours after we had collected a Ptychzoon

kuhli from the same tree. The snake was facing head

down and rapidly tongue flicking the spot where we pre-

viously collected the P. kuhli. We suspect it may have

been scent trailing the gecko. On 1 1 July 2001, a spec-

imen (ZRC 2.5145) was collected from the Tekek-Juara

trail at 140 m crawling across a large boulder. This

species occurs in lowland dipterocarp forest.

Dendrelaphis cyanochloris Wall, 1921

Localities. - Tekek-Juara trail and Kampung Juara

(Hien et al., 2001).

New localities. - On 17 July 2001, one specimen

(LSUHC 4611) was found at night sleeping in brush

along the Tekek waterfall trail at 100 m. This species

occurs in lowland dipterocarp forest.

Dendrelaphis pictus Gmelin, 1789

Localities. - Tekek-Juara trail (Grismer et al.,

2002a).

New localities. - On 6 August 2001, K. P. Lim

(pers. com., 2001) informed LLG of an observation of

D. pictus in Kampung Juara on 21 July 2001. This

species ranges from coastal vegetation to low hill dipte-

rocarp forest.

Dendrelaphis striatus Cohn, 1906

(Fig. 24)

Localities. - Kampung Juara (Wood et al., 2003).

New localities. - On 21 July, 2001, one specimen

(LSUHC 4792) was observed sleeping 2 m above

ground level on a trail in Telok Monkey at 80 m. This

species is found in coastal and lowland dipterocarp for-

est and constitutes a new record for this island.

Dryocalamus subannulatus Dumeril, Bibron and

Dumeril, 1854

Localities. - On beach 1 km south of Kampung

Tekek (Grismer et al., 2002a).

New localities. - On 14 August, 2002, one specimen

(LSUHC 5051) was observed at night crawling through

the branches of a tree 2 m above ground level at the bot-

tom of the Tekek-Juara trail near the Mosque at 80 m.

This species is found in coastal and lowland dipterocarp

forest.

Elaphe flavolineata Schlegel, 1837

Localities. - Kampung Tekek (Wood et al. 2004)

New localities. - On xx March, 2003, one juvenile

specimen (LSUHC- S3 752) was found dead on the road

in Kampung Tekek at 10 m in elevation. This species is

found in coastal vegetation.

Elaphe taeniura Cope, 1 86 1

Localities. - 100 m behind last house at Kampung

Juara (Hien et al., 2001).

New localities. - On 19 July, 2002, one specimen

(LSUHC 4675) was observed 2 m above ground level

crawling on the top of a large boulder on a trail in Telok

Monkey at 40 m immediately following an afternoon

rainshower. This species is found in coastal and lowland

dipterocarp forest.

Enhydris plumbea Boie, 1827

Localities. - Sungai Raya (Lim and Lim, 1999).

New localities. - On 9 November, 1997, two speci-

mens (at PERHILITAN uncatalogued) were collected

from the Sungai Besar in Kampung Tekek. On 9 July,

2001, a specimen (LSUHC 3817) was collected from

beneath a log at Kampung Pay a at sea level. This

species occurs in mangroves and coastal vegetation.

Fordonia leucobalia Schlegel, 1837

(Fig. 25)

Localities. - On 15 July, 2001, a specimen

(LSUPC-S3253) was collected from the drainage canals

at Persona Island Resort in Kampung Tekek at 5 m and

is currently maintained as a living specimen at the

Raffles Museum of Biodiversity Research at the

National University of Singapore. This constitutes a

new island record. This species occurs in the man-

groves.

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Asiatic Herpetological Research

Vol. 10, p. 275

Gongylosoma mukutense Grismer, Das, Leong, 2003

(Fig. 26)

Localities. - On 10 July, 2001, a specimen (ZRC

2.5 141) was found at 20 m in coastal vegetation on the

trail that leads from Kampung Mukut to Sungai Raya.

The specimen was being eaten by a juvenile Ptyas cari-

natus. An additional specimen (LSUHC 4680) was col-

lected from 190 m in elevation along the Tekek-Juara

trail on 16 July, 2002. This species occurs in coastal veg-

etation and lowland dipterocarp forest.

Gonyosoma oxycephalum Boie, 1827

(Fig. 27)

Localities. - A sight record from Nipah was report-

ed by Day (1990).

New localities. - A specimen was found resting on

a branch 10 m above the surface of a small river in

Kampung Juara. It was collected and photographed by

Pauli Hien. A photo of that specimen is deposited at La

Sierra University (LSUPC-S3633). This specimen con-

stitutes a new island record. This species occurs in

coastal forest.

Lepturophis albofuscus Dumeril, Bibron and Dumeril,

1854

Localities. - Sungai Nipah (Day, 1990).

New localities. - Two specimens (LSUHC 4588-89)

were collected at night along the Tekek-Juara trail at 180

m and 220 m, respectively, on 16 July, 2002. An addi-

tional juvenile specimen (ZRC 2.5144) with a black and

white banding pattern was collected from the Tekek-

Juara trail at 200 m on 11 July, 2001. An additional

specimen (LSUHC 4411) was collected along the

Sungai Mentawak at 195 m on 16 July, 2002. This

species occurs in lowland dipterocarp forest.

Liopeltis tricolor Schlegel, 1837

Localities. - Top of Tekek-Juara trail at 245 m

(Hendrickson, 1966a).

New localities. - A single adult (LSUHC 5037) was

collected during the day along the Gunung Kajang trail

at 618 m while resting on a small branch 2 m above

ground level. This species ranges from lowland diptero-

carp to high hill dipterocarp forest.

Oligodon purpurascens Schlegel, 1837

(Fig. 28)

Localities. - Ulu Lalang and the Tekek-Juara trail

(Hendrickson, 1966a; Day, 1990).

New localities. - On 9 July, 2001, a shed skin

(LSUHC 3988) with a pattern matching that of Oligodon

purpurascens was found at Telok Dungun within a rot-

ting log at 15 m. On 1 1 August, 2002, an adult was

found crawling across the forest floor during the day at

320 m on the Gunung Kajang trail. The Pulau Tioman

population is unlike all others in that the snakes are

bright red-orange in dorsal color and have smooth as

opposed to irregular dorsal band margins. This popula-

tion is under further investigation. This species ranges

from lowland dipterocarp forest to high hill dipterocarp

forest.

Oligodon booliati Leong and Grismer, 2004

Localities. - Ulu Lalang (Hendrickson 1966a).

New localities. - On 16 July, 2001 a specimen (ZRC

2.5153) was collected from the Tekek-Juara trail at

approximately 150 m in elevation. It differs from all

other Oligodon by its bright red coloration and extreme-

ly faint banding pattern. Its scale counts fall within the

range of those of O. signatus (Leong and Grismer,

2004). Hendrickson (1966a) reported O. signatus at Ulu

Lalang in high hill dipterocarp forest. Upon examina-

tion of that specimen (BPBM 13933) we find that it con-

forms to the new species (ZRC 2.5153) reported above.

This species ranges from lowland dipterocarp forest to

high hill dipterocarp forest.

P areas vertebralis Boulenger, 1900

Localities. - Gua Tengkok Air at 810 m (Youmans

et al., 2003).

New localities. - On xx March, 2003 an adult spec-

imen (LSUPC S3696-4000) was observed crawling

throught he lower branches of a small tree approximate-

ly 1.5 m above the ground. This species is known only

from high hill dipterocarp forest.

Psammodynastes pulvurulentus Boie, 1827

Localities. - Summit of Gunung Kajang at 1035 m

(Day, 1990).

New localities. - On 17 July, 2002 a juvenile speci-

men (LSUHC 4684) was collected along the Tekek-

Juara trail while sleeping on a leaf at 230 m. Another

specimen was collected and photographed (LSUPC-

S3631) from Air Batang near sea level by Johan van

Rooijen. This species ranges from coastal vegetation to

ridge forest.

Vol. 10, p. 276

Asiatic Herpetological Research

2004

Ptyas carinatus Gunther, 1858

Localities. - Tekek-Juara trail (Grismer et ah,

2002a).

New localities. - On 3 November, 2000, a large

adult (LSUPC-S2774-80) was photographed on the

Tekek-Juara trail at 240 m in elevation. On 10 July

2001, a juvenile (ZRC 2.5142) was found on the trail

that leads from Kampung Mukut to the Sungai Raya at

20 m. The latter specimen was found eating a

Gongylosoma mukutense. On 20 July, 2002, an adult

was found crawling during the day on the Tekek water-

fall trail at 100 m. This species ranges from coastal veg-

etation to lowland dipterocarp forest.

Rhabdophis chrysargos Schlegel, 1837

(Fig. 29)

Localities. - Forest behing Kampung Juara

(Henrickson, 1966a).

New localities. - Hien et al. (2001) report this

species from the Sungai Mentawak at 150 m, at the

mouth of the Sungai Mentawak at sea level, and at

Tanjung Pisang Kera and Tanjung Batu Pulau at sea

level. We found a specimen (LSUHC 4791) at 80 m on

the Tekek-Juara trail near the Mosque. Hien et ah

(2001) report this population as Amphiesma sp. All

specimens we examined are within the variation report-

ed for Rhabdophis chrysargos except for coloration.

Specimens from the Pulau Tioman differ from others in

that adults are red anteriorly and juveniles are red-

orange throughout. Also, the white nuchal line is faint to

absent. This species occurs from mangroves to lowland

dipterocarp forest.

Sibynophis melanocephalus Gray, 1 834

(Fig. 30)

Localities. - On 18 July 2002, an adult (LSUHC

4683) was found crawling through the grass in

Kampung Juara (Grismer et ah, 2003). During capture,

it voluntarily broke off two sections of its tail in defense.

This specimen constitutes a new record for Pulau

Tioman. This species occurs in coastal vegetation.

Family Elapidae

Calliophis intestinalis Laurenti, 1768

Localities. - Telok Nipah and the Tekek-Juara trail

(Day, 1990).

New localities. - On 19 March, 2001, a specimen

(LSUPC-S 1038-40) was photographed on the trail to

Gunung Kajang at approximately 100 m in elevation

near the Sungai Mentawak. On 19 July, 2002, one spec-

imen (LSUHC 4617) was taken from a pitfall trap from

the upper array at 241 m. On 10 August, 2002, a speci-

men (LSUHC 5047) was collected crawling through the

leaf litter at Gua Tenguk Air at 845 m on Gunug Kajang.

This species occurs from lowland dipterocarp to high

hill dipterocarp forest.

Ophiophagus hannah Cantor, 1836

New localities. - A large adult (ca. 3.5 m) was pho-

tographed by Johan van Roojen in March, 2002 at Air

Batang at sea level (Van Rooijen and Van Rooijen,

2002). On Pulau Tioman this species is known only

from coastal vegetation but local people say it occurs

throughout the island (Hendrickson, 1966a). This

species occurs in mangrove and coastal vegetation.

Family: Viperidae

Trimeresurus sp.

(Fig. 31)

Localities. - Gunung Kajang at 400 m (Lim and

Lim, 1999); Gua Tenguk Air at 845 m (Day, 1990).

New localities. - On the evening 21 July, 2002, a

male was collected while sitting 7 m above ground level

on the end of a branch along the Tekek-Juara trail at 210

m. Lim and Lim (1999) referred to this species as

Trimeresurus cf. popeiorum. Its specific status is cur-

rently being investigated. This species ranges from low-

land to high hill dipterocarp forest.

Results and Discussion

The amphibians and reptiles of Pulau Tioman have vary-

ing patterns of distribution (Table 1). Some species (i.e.,

Cyrtodactylus tiomanensis and Psammodynastes pul-

verulentus ) range throughout many different vegetation

zones from coastal vegetation to ridge forest whereas

others, such as Philautus petersi, Draco haematopogon

and P areas vertebralis are restricted to only high eleva-

tions in high hill dipterocarp and/or ridge forest (Table

1). The majority of the species, however, are found in

lowland dipterocarp forest (Table 1). This region sup-

ports 74% of the amphibians, 76% of the lizards, and

74% of snakes, totaling 74% of the island’s species com-

position. The high species diversity in this vegetative

zone is due largely to its varied habitat and microhabitat

composition. Here, the terrain is characterized by many

large boulder outcrops and fast flowing, boulder-strewn

streams. The crevices, exfoliations, and shaded refugia

offered by the boulders, along with the additional micro-

habitats these features provide along a water course, add

2004

Asiatic Herpetological Research

Vol. 10, p. 277

greatly to the microhabitat diversity of this forest. Such

microhabitat diversity allows many species to specialize

into narrow environmental zones. In fact, species which

range throughout all the vegetative zones (i.e.,

Sphenomorphus scotophilus and Cyrtodactylus tioma-

nensis) do so because of their association with the

microhabitats offered by boulders. There are more

restricted species such as Ansonia tiomanica which

occur only in habitats with large boulders in the vicinity

of water at elevations above 220 m. Whereas others

(i.e., Rana hosii , Ichthyophis sp., Dogania subplana,

Gonocephalus grandis ) are confined to riparian habitats.

The species composition of the distribution patterns

will undoubtedly change with the acquisition of addi-

tional specimens. Many of the species reported from

Pulau Tioman are known from a limited number of indi-

viduals and thus, appear to exist in a limited range of

habitats. These species range throughout a far greater

number of habitats on peninsular Malaysia and so it is

likely they do so as well on Pulau Tioman. However,

even with the acquisition of new material the generality

of the observed trends in habitat use are not likely to

change significantly.

There are two sightings of unconfirmed species on

Pulau Tioman listed in an unpublished report by Day

(1990). Day's sightings range from specimens he actu-

ally observed to second hand reports he received from

locals, vacationers, and friends. Species he personally

observed (i.e., Chrysopelea paradise, see Lim and Lim,

1990 for discussion) are considered as potentially pres-

ent. The others, Leiolepis belliana and Elaphe por-

phyracea are not considered noteworthy herein. Day

(1990) also reported Rana doriae from a small tributary

of the Sungai Mentawak at 290 m. Examination of these

specimens (uncatalogued in the British Museum of

Natural History) show them to be Limnonectes blythii.

Hien et al. (2001) report that the Lycodon effraenis

reported by Manthey and Grossman (1997) was a juve-

nile Lepturophis albofuscus.

Acknowledgments

We thank Mr. Sahir bin Othman, Director of Wildlife,

PERHILITAN, for permission to conduct field work in

the Seribuat Archipelago and Peter Ng, Chang Man

Yang and Kelvin Kok Peng Lim (ZRC) and Carla H.

Kishinami (BPBM) for permitting us to examine mate-

rial under their care. We also thank all the Malaysain and

American students of the Tropical Field Biology classes

BIOL 487F and G of 2001 and 2002, respectively for

their help in the field. For comments on the manuscript

we thank J. McGuire and R. Brown.

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2004

Grismer, J. L., R. A. Escobar, III, and T. M.

Youmans. 2003a. Theloderma horridum.

Geographic distribution. Herpetological Review

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2003. Two new Southeast Asian skinks of the genus

Larutia and intrageneric phylogenetic relationships.

Herpetologica 59:552-564.

Grismer, J. L., C. Rasmussen, and R Wood, Jr.

2003. Sibynophis melanocephalus. Geographic dis-

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Grismer, L. L., I. Das, and T. M. Leong. 2003b. A new

species of Gongylosoma (Squamata: Colubridae)

from Pulau Tioman. Herpetologica 59:565-572.

Grismer, L. L., H. Kaiser, and N. S. Yaakob. 2004. A

new species of reed snake of the genus Calamaria

Boie, 1827 from Pulau Tioman, Pahang, West

Malaysia. Hamadryad 28:1-6.

Grismer, L. L., J. L. Grismer, and T. M. Youmans.

2004b. A new species of Leptolalax (Anura:

Megophryidae) from Pulau Tioman. Asiatic

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Grismer, L. L., J. A. McGuire, R. A. Sosa, and H. Kaiser,

2002a. Revised checklist and comments on the ter-

restrial herpetofauna of Pulau Tioman, Peninsular

Malaysia. Herpetological Review 33:26-29.

Grismer, L. L., N. S. Yaakob, L. B. Liat, T. M. Leong,

I. Das, R. A. Sosa, J. L. Grismer, K. M. Crane, R. E.

Diaz, S. V. Figueroa, C. A. Ledbetter, S. C.

Newbold, S. R. Newbold, C. P. Patel, J. Castro, R.

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evolution of the Oriental colubrid snakes of the

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H. B. Loo, and H. T. W. Tan. 1999. On the vegeta-

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of kukri snake, Oligodon (Colubridae) from Pulau

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petofauna of Pulau Tioman, Peninsular Malaysia.

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Reptilien Sudostasiens. Natur und Tier, Verlag 512

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rganzungen, berichtigungen und neue beobach tun-

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Vol. 10, p. 279

Wood, P. L., T. M. Youmans, C. Raynor, J. M. Bernard,

N. Hinojosa, T. Dyer, S. Andreiko, P. P. van Dijk, W.

Wuertz, L. S. Yeen, and N. A. Elias. 2002. First

report on the herpetofauna of Pulau Dyang, Johor,

West Malaysia. Hamadryad 27:284-285.

Wood, P. L. , N. A. Elias, and D. Morgan. 2003.

Dendreiaphis striatus. Geographic distribution.

Herpetological Review 34:264.

Wood, P. L. , T. M. Youmans, and T. R. Szutz. 2004.

Elaphe flavolineata. Geographic distribution.

Herpetological Review 34:88.

Wood, P. L., T. M. Youmans, J. L. Grismer, J. Wheatly, S.

Wright, C. Valdivia, A. Ponce, L. Escobar, S. Amin,

P. Baker, J. Bernard, S. Looper, N. Marsh, L.

Martin, N. Padilla, R. Rosser, A. Srivastava, V.

Srivastava, X. Wright, L. S. Yeen, H. Kaiser, and L.

L. Grismer. 2004a. First report of the herpetofauna

of Pulau Sibu, Johor, West Malaysia. Hamadryad, in

press.

Wood, P L., H. Kaiser, S. Looper, T. M. Youmans, J. L.

Grismer, and L. L. Grismer. 2004b. First report on

the herpetofauna of Pulau Besar, Johor, West

Malaysia. Hamadryad, in press.

Youmans, T. M., R. E. Escobar, III, J. L. Grismer, L. L.

Grismer, and R. Johnson. 2002. First report on the

herpetofauna of Pulau Pemanggil, West Malaysia.

Hamadryad 27: 148-149.

Youmans. T. M., P. L. Wood, and T. R. Szutz. 2003.

Pareas vertebraliss. Geographic distribution.

Herpetological Review 34:389.

Pareas stanleyi - A Record New to Sichuan, China

and a Key to the Chinese Species

Peng Guo1 and Ermi Zhao2

1 College of Life Sciences, Sichuan University, Chengdu, Sichuan, China 610041

-Chengdu Institute of Biology’, Chinese Academy of Sciences Chengdu, Sichuan Province, China 610041

Abstract. - A specimen of the Fujian slug-eating snake, Pareas stanleyi , was collected in Sichuan Province, China

for the first time. We provide a key to the Chinese species of Pareas.

Keywords. - Serpentes, Colubridae, Pareas , China, Sichuan.

An adult male of the Fujian slug-eating snake, Pareas

stanleyi (Boulenger, 1914) was captured from

Muchansi, Liujiang Town, Hongya County,

Southwestern Sichuan Province, China at noon on 02

June, 2003 (Fig. 1). This species was first described

based on one male specimen from N. W. Fokien

(=Fujian Province). It was successively found in

Zhejiang (Longquan), Jiangxi (Mt. Jinggangshan),

Guizhou (Leishan), and also Fujian (Chongan, Nanjing,

Pucheng, Shaowu). All the localities are situated within

108° 10' N, 119° 10' E and 26° 20' N, 28° 10' N. The geo-

graphic position of Liujiang Town is between 29° 44' N

and 103° 13' E . The discovery of Pareas stanleyi from

Liujiang Town extends its range about 5 degrees west-

ward and about 1.5 degrees northward. The distribution

pattern of Pareas stanleyi is Southern China.

SCU No. 20030049

An adult male. Head distinct from the neck, snout blunt,

body somewhat compressed. Rostral high, visible from

above of the head; intemasals shorter than prefrontals;

no preoculars; loreals large, its posterior end entering the

eye; prefrontals extending laterally to the sides of the

head, and touching the eye at its anterior upper corner;

supraoculars small; postoculars narrower and in contact

with the long narrower crescent subocular, which com-

pletely encircling the posterior and inferior border of the

eye; two anterior temporals, three posterior temporals;

upper labials seven, excluded from orbit; mental very

small; lower labials eight, anterior three or four in con-

tact with the anterior chin-shield; the latter three pairs,

no mental groove. Dorsal scales in fifteen rows through-

out, three median rows feebly keeled at the neck region,

seven median rows feebly keeled at the midbody, all but

the outer one row keeled before the vent, vertebral row

not enlarged; ventrals 153; anal entire; subcaudals in

pairs, 54/54+1. The coloration of this specimen is iden-

tical with the original description by G. A. Boulenger

(1914). The total length of the male Hongya specimen is

630.5 mm with a tail length of 110.5 mm. The tail is

about 17.5% of the total length.

Twenty species belong to the genus Pareas Wagler,

1830 (Welch, 1988). It ranges over East Asia,

Southeastern Asia, and South Asia (Bangladesh, Burma,

China, India [Assam], Indonesia, Japan, Kampuchea,

Laos, Malaysia, Sikkim, Thailand, and Vietnam). In

China, nine species are recognized (Zhao et al., 1998).

The authors of this paper believe that Pareas macularius

Theobald, 1868 is a synonym of P. margaritophorus

(Jan, 1866), P. komaii (Maki, 1931) is a synonym of P.

formosensis (VanDenburgh, 1909), and P. chinensis

(Barbour, 1912) may be a synonym of P. hamptoni

(Boulenger, 1905). Thus, there are only seven species

found in China, which may be distinguished by means of

the following key;

Key to Chinese Pareas

Figure 1. Pareas stanleyi from Sichuan Province, China.

1A Color purplish blue or purplish brown, with many

black and white dorsal scales forming many short trans-

verse bands Pareas margaritophorus

IB Color dark or light brown, many dorsal scales with

small black spots forming transverse line or

reticulation

Vol. 10, p. 281

Asiatic Herpetological Research

2004

2 A Mo prefrontal P areas carinatus

2B With prefrontal and entering the eye 3

3 A No preocular, loreal entering the eye 4

3B Preocular present, loreal not entering the eye (or only

its tip entering the eye) 6

4A Dorsal scales smooth 5

4B Dorsal scales keeled but the outer row smooth; back

of head with big black blotch P areas stanleyi

5A Vertebral enlarged; the fourth upper labial entering

the eye; ventrals more than 190; subcaudals more than

72; a black "X"-shaped mark behind the

parietals P areas monticola

5B Vertebral not enlarged; the fourth upper labial not

entering the eye; ventrals less than 190; subcaudals less

than 77 P areas boulengeri

6A The second upper labial touching or not touching the

crescent subocular, found only in Taiwan

Province P areas formosensis

6B The second upper labial not touching the crescent

subocular, found in mainland Pareas hamptoni

Literature Cited

Boulenger, G: A. 1914. Descriptions of new species of

snakes in the collection of the British Museum. The

Annals and Magazine of Natural History, London,

ser. 8, 14(84):482-485.

Pope, C. H. 1935. The Reptiles of China. American

Museum of Natural History, New York, Natural

History Central Asia, 10: lii, 1-604, 27 uncolored

plates, folding map.

Welch, K. R. G. 1988. Snakes of the Orient: A Checklist.

Robert E. Krieger, Malabar (Florida), vii, 183 pp.

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

SSAR & CSSAR, Ohio, 522 pp. 48 colored plates,

3 maps.

Zhao, E. M., M. H. Huang, and Y. Zong. 1998. Fauna

Sinica, Reptilia, Vol. 3: Serpentes. Science Press,

Beijing, 522 pp., 12 plates.

Intraspecific and Interspecific Genome Size Variation in yno n

Salamanders of Russia and Kazakhstan: Determination y

Flow Cytometry

Spartak N. Litvinchuk1’*, Leo J. Borkin2 and Jury M. Rosanov

' Institute of Cytology, Russian Academy of Sciences, Tikhoretsky pr. 4, St. Petersburg 194064, Russia,

* E-mail : slitvinchuk@yahoo.com

^Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia

Abstract. - The amount of DNA per diploid nucleus in Salamandrella keyserlingii and Onychodactylus fischeri from

Russia, as well as in Ranodon sibiricus from Kazakhstan was determined by flow cytometry. Onychodactylus fischeri

had the highest genome size, Ranodon sibiricus the lowest, and Salamandrella keyserlingii was intermediate. Obvious

geographic variation in genome size was revealed for Salamandrella keyserlingii and Ranodon sibiricus. The com-

parison of nuclear DNA content in eleven hynobiid species supported the genus Onychodactylus as a separate line-

age.

Key words. - nuclear DNA content, genome size, flow cytometry, Caudata, Hynobiidae, Onychodactylus fischeri,

Salamandrella keyserlingii, Ranodon sibiricus, Russia, Kazakhstan.

Introduction

Diploid genome size, measured in picograms (pg; 1 pg

= 10'12 g) of DNA per nucleus, varies widely in verte-

brates. Living amphibians represent the largest range of

genome size variability among terrestrial vertebrates,

with a minimum of 1.7 pg in male frogs of

Eleutherodactylus shrevei (Schmid et al., 2002) and

maximum of 241 pg in Necturus lewisi (Olmo, 1973).

Some extinct amphibians may have had maximum DNA

contents greater (approximately 300 pg) than the maxi-

mum known in living forms (Thoson and Muraszko,

1978).

Various methods are used for the measuring of

genome size in amphibians (for example, biochemical

analysis, Feulgen densitometry, static cell fluorometry,

ultraviolet microscopy, etc.). However, modem studies

are based on a comparatively new and very precise

method of flow DNA cytometry. As a rule, standard

errors of this method (peak mean ratios) are less than

0.5% (Rosanov and Vinogradov, 1998). Among approx-

imately 415 amphibian species examined, nuclear DNA

contents were studied by flow cytometry in about 143

species only (Gregory, 2001a).

Among some specific applications, DNA flow

cytometry has been used to examine ploidy levels

(Borkin et al., 1986, 1996, 2001a; Vinogradov et al.,

1990; Sharbel et al., 1997; Litvinchuk et al., 1998,

2001), to identify morphologically similar species

(Sharbel et al., 1995; MacCulloch et al., 1996;

Litvinchuk et al., 1997, 1999; Murphy et al., 1997;

Borkin et al., 2001b, 2003; Khalturin et al., 2003), and

to search for hybrid individuals (Borkin et al., 1987,

2002; Litvinchuk et al., 2003). Many authors have noted

a relationship between genome size and some biological

parameters, such as cellular and nuclear sizes, replica-

tion time, cell-cycle length, cell division rate, metabolic

rate, longevity, morphological complexity in the brain,

etc. (Van't Hoff and Sparrow, 1963; Goin et al., 1968;

Olmo and Morescalchi, 1975; Bachmann and Nishioka,

1978; Sessions and Larson, 1987; Shakhbazov and

Gapchenko, 1990; Licht and Lowcock, 1991; Nevo and

Beiles, 1991; Roth et al., 1994; Vinogradov, 1999;

Gregory, 2001b, 2001c; Griffith et al., 2003). However,

an adaptive value of genome size is most clearly shown

in its relationship with the timing of embryonic develop-

ment in amphibians (Bachmann, 1972; Oeldorf et al.,

1978; Homer and Macgregor, 1983; Pagel and Jonstone,

1992; Jockusch, 1997; Chipman et al., 2001; Gregory,

2002, 2003).

This research is focused on salamanders of the fam-

ily Hynobiidae, which consists of approximately 42

species. Among modem amphibians, hynobiids are rec-

ognized to be one of the primitive urodelans (e.g.,

Duellman and Trueb, 1986; Larson and Dimmick,

1993). Hynobiids inhabit various mountain regions of

Palaearctic Asia, where they have quite restricted

ranges. The territory of Russia and Kazakhstan are only

inhabited by three hynobiid species. Other family mem-

bers, such as the Siberian Salamander ( Salamandrella

keyserlingii ), is widely distributed from Northeastern

European Russia to the Kamchatka Peninsula. The

Ussuri Clawed Salamander {Onychodactylus fischeri)

can be found in the southern part of Russian Far East and

in the Korean Peninsula. The Semirechensk salamander

{Ranodon sibiricus) inhabits the Dzhungarsky Alatau

Vol. 10, p. 283

Asiatic Herpetological Research

2004

Figure 1. Distribution of Salamandrella keyserlingii (grayish area), Ranodon sibiricus (dark square), and

Onychodactylus fischeri (dark-grayish area), with localities studied (locality number as in Table 1). Dark circles desig-

nate the "Euro-Siberian" type of Salamandrella keyserlingii , white ones - "Primorsky" type.

Mountains in southeastern Kazakhstan and adjacent

China. The last two species are included in the Russian

and Kazakhstan Red Data Books, respectively. Ranodon

sibiricus is also included in the IUCN Red List of

Threatened Animals under the category "vulnerable"

(Borkin, 1998; Kuzmin, 1999). The goal of present

paper is to evaluate the intra- and interspecific genome

size variation in three hynobiid species of Russia and

Kazakhstan, with flow cytometry.

Peripheral blood cells of specimens of the Ribbed

Newt, Pleurodeles waltl, received from Prof. J. C.

Lacroix (Universite Paris VI, Paris, France) were used

as a reference standard. Details of the technique have

been published previously (Vinogradov et al., 1990;

Rosanov and Vinogradov, 1998; Borkin et al., 2001).

The relative genome size differences (RD) were calcu-

lated with use of formula: RD=(ml-m2)/(ml+m2) *

200%, where ml and m2 are the sample means.

Materials and methods

Results

Eighty-eight metamorphosed specimens from 13 popu-

lations of three species distributed in Russia and

Kazakhstan were used in this study of genome size vari-

ation. Blood was taken from the clipped tail tip. The

samples of Salamandrella keyserlingii and

Onychodactylus fischeri studied are kept at the collec-

tions of the Department of Herpetology, Zoological

Institute, Russian Academy of Sciences. All specimens

of Ranodon sibiricus were obtained from the Almaty

Zoo (Kazakhstan), and after preparation of blood sam-

ples, the live salamanders were sent to the Moscow Zoo.

The genome size variation in three hynobiid species var-

ied between 54.5 and 109.0 pg (Table 1). The lowest

nuclear DNA content was recorded in Ranodon sibiricus

(in average 55.4 pg), whereas the highest was in

Onychodactylus fischeri (107.7 pg). Salamandrella key-

serlingii was intermediate in size (66.4 pg).

Differences between populations were studied in

two species, represented by more than one sample. In S.

keyserlingii , ten samples were allocated to two main,

distinct groups with different genome sizes (Table 1 and

Fig. 1). The geographic distribution of these two groups

2004

Asiatic Herpetological Research

Vol. 10, p. 284

Table 1. Locality of origin ("Lat" is latitude, and "Lon" is longitude), sample size, genome size (in picograms, SD is

standard deviation) with the coefficient of variation (CV; in percents) for 13 populations of three hynobiid species.

Table 2. The genome size (GS; in picograms) of hynobiids, referred by some authors.

Species Locality GS Reference

Hynobius (Hynobius) dunni

H. (H.) nebulosus

H. (H.) tsuensis

H. (Satobius) retardatus

H. (Pseudosalamandra) naevis

Onychodactylus fischeri

O. japonicus

Paradactylodon gorganensis

P. mustersi

Ranodon sibincus

Salamandrella keyserlingii

Olmo, 1973

Mazin, 1978

Vinogradov, 1998

Present paper

Olmo, 1983

Stock, 1999

Morescalchi et al., 1979

Vinogradov, 1998

Present paper

Mazin, 1978

Morescalchi et al., 1979

Grafodatsky and Grigoriev, 1982

Vladychenskaya et al., 1988

Vinogradov, 1998

Present paper

1Flow cytometry; 2Feulgen's densitometry; ^Kinetics reassociation.

Vol. 10, p. 285

Asiatic Herpetological Research

2004

Table 3. Genome size (2C), range of egg diameters (mm), and time of embryonic ("Embr.") and larval ("Larv.") devel-

opment (days) in some hynobiids.

1 Laboratory conditions (temperature unknown); 2nature conditions; 3t = 10°; 4t = 16°.

Table 4. Genome size (2C), diploid number of chromosomes (2n) and number of uniarmed macrochromosomes (UM)

in some hynobiids.

2004

Vol. 10, p. 286

65 66 67 68

Genome Size (pg)

Figure 2. Genome size distribution in Salamandrella key-

serlingii.

of samples proved to not be chaotic and the "Euro-

Siberian" (8 samples) and "Primorsky" (2 samples)

groups were recognized. The data ranges of the groups

did not overlap, and the gap between both groups was

equal to 0.3 pg (Fig. 2). The "Primorsky" samples were

characterized by smaller genome size in comparison

with the "Euro-Siberian" ones: 64.4-65.2 pg vs. 65.5-

68.1 pg; the means were 64.8 pg vs. 66.9 pg. The differ-

ences (RD) between means were equal to 3.2%, and

were observed in five separate comparisons. Therefore,

these groups were shaped both by genome size and geo-

graphically.

The samples of R. sibiricus were taken from two

semi-isolated populations from upper parts of

Borokhudzir and Oy-Saz rivers. Both samples demon-

strated different genome sizes (Table 1). The ranges of

genome size values in these two samples slightly over-

lapped. The Oy-Saz sample was characterized by small-

er genome size in comparison with the Borokhudzir

sample: 54.5-55.1 pg vs. 55.1-56.7 pg; the means are

54.8 pg vs. 56.0 pg. The differences (RD) between

means were equal to 2.2%.

The coefficient of variation (CV) ranged between

0.3% and 0.9% in S. keyserlingii , between 0.3% and

1.0% in R. sibiricus , and was equal to 0.7% in the sam-

ple of O. fischeri (Table 1). The overall within-species

genome size variation in S. keyserlingii and R. sibiricus

were quite similar (1.5% and 1.3%, respectively).

Among the "Euro-Siberian" samples of S. keyserlingii ,

the CVs ranged between 0.3% (Nizhny Novgorod

Province) and 0.9% (Tomsk Province), whereas it was

equal to 0.4% in the "Primorsky" samples of S. keyser-

lingii.

Discussion

1) Genome size values in hynobiids: literature data

Presently, the nuclear DNA content has been determined

for eleven hynobiid species. However, among them,

only four species were examined through flow cytome-

try (Table 2). The first data collected about genome size

of nine hynobiid species was obtained by Italian

researchers with an application of Feulgen densitometry

(Olmo, 1973, 1983; Olmo and Morescalchi, 1975;

Morescalchi et al., 1979). According to these data,

genome size in hynobiids ranged from 32.96 pg in

Hynobius tsuensis to 102-106 pg in Onychodactylus

japonicus (Table 2). According to Mazin (1978), the

nuclear DNA content in two Russian species,

Onychodactylus fischeri and Salamandrella

(" Hynobius") keyserlingii, measured by Feulgen densit-

ometry, were similar to each other (45.5 and 42.5 pg,

respectively). Grafodatsky and Grigoriev (1982) esti-

mated genome size of Salamandrella keyserlingii (38

pg), perhaps, by means of Feulgen densitometry.

Vladychenskaya et al. (1988) studied kinetics of DNA

reassociation; they found that the nuclear DNA content

of Salamandrella keyserlingii was equal to 33.2 pg.

Using DNA flow cytometry, Vinogradov (1998) esti-

mated genome size values as 95.08 pg for

Onychodactylus fischeri, 45.59 pg for Ranodon sibiri-

cus, and 55.48 pg for Salamandrella keyserlingii.

Finally, Stock (1999) determined that genome size of

Batrachuperus gorganensis is 34.77 pg, using DNA

flow cytometry as well.

The literature values of genome size for

Onychodactylus fischeri, Ranodon sibiricus , and

Salamandrella keyserlingii expressed in absolute units

vary sometimes more than two-fold (ranges are 45.5-

95.1 pg, 45.6-50.7 pg, and 33.2-55.5 pg, respectively).

Therefore, the comparison of data provided by various

authors should be made cautiously. The contradictions

may be explained by an application of different tech-

niques (Feulgen densitometry, kinetics reassociation,

and flow cytometry), dyes, and laboratory conditions

(cell preparation methods, devices for measurements,

types of reference cell standards, etc.). It has been shown

that genome size measured with fluorochromes of dif-

ferent nucleotide specificity may differ markedly (e.g.,

Johnston et al., 1987; Birshtein et al., 1993; Vinogradov

and Borkin, 1993). For instance, the determination of

genome size by means of flow cytometry for cell sam-

ples of Salamandrella keyserlingii stained with

olivomycin and Hoechst (GC- and AT-specific fluo-

rochromes, respectively) provided 6.68 and 4.77 arbi-

trary units (Rana temporaria was taken as an internal

reference; Vinogradov, 1998). To exclude the influence

Vol. 10, p. 287

Asiatic Herpetological Research

2004

of AT/GC-structure, it is necessary to use ethidium bro-

mide or propidium iodide (Vinogradov and Borkin,

1993), which were used in our research.

To convert genome size from the relative units to

picograms, it is necessary to have data about genome

size of reference cells. Such data should be obtained

without using stains. Unfortunately, the data available

today, mentioned by various authors, do not correspond

to each other. For instance, Vinogradov (1998) reported

a genome size of reference standard Mas musculus to be

6.5 pg. Our estimations of genome size of some mam-

mals ( Homo sapiens , Mas mas cal as, Rattas norvegicas )

were the closest to that mentioned by Bianchi et al.

(1983). In our work, we used the genome size of males

of Mas musculus (C57B1) as a basic reference standard

with value of 6.8 pg. Other authors preferred other ref-

erence standards, which have different base-pair-speci-

ficity of some stains widely used in flow cytometry.

Vinogradov and Borkin (1993) listed the AT- and GC-

pair specific DNA contents (CAT and CGC) for many

species of amphibians. For instance, CAT/CGC was

equal to 1 .42 in Xenopas laevis (Mazin's reference stan-

dard), and 1.00 in Rana lessonae (= Rana " esculenta

Olmo's and Morescalchi's standard).

The estimations of Italian authors (Olmo, 1973,

1 983 ; Morescalchi et al., 1 979) and our genome size val-

ues for Ranodon sibiricas (50.7 and 54.5-56.7 pg,

respectively) and members of genus Onychodactylus

(102.0-106.0 and 106.7-109.0 pg, respectively) are quite

similar. However, data for Salamandrella keyserlingii

(42.3 and 64.4-68.1 pg, respectively) are in obvious dis-

cordance. The genome size of Onychodactylus fischeri ,

Ranodon sibiricas, and Salamandrella keyserlingii men-

tioned by Vinogradov (1998), was lower than our val-

ues, who used other stains and lower genome size esti-

mation of basic reference standard.

Unfortunately, some authors did not supply any

information about sample sizes and localities. However,

some differences in genome size might be influenced by

intra-population and geographic variation as well.

2) Within-species variation

Some authors discussed the levels of intraspecific varia-

tion in genome size. We recognized two kinds of such a

variation; namely, the "within-population" variation and

"between-population" (or geographical) variation.

A) Within Population Variation

Among amphibians, the greatest intrapopulational vari-

ation (CV = 7.5%, the data of Licht and Lowcock, 1991

were recalculated by us) was recorded for the Western

Red-back Salamander {Plethodon vehicalam). However,

the variation in other amphibian species was consider-

ably lower (Licht and Lowcock, 1991; MacCulloch et

al., 1996; Murphy et al., 1997; Lizana et al., 2000). The

variation within populations of three hynobiid species

(CVs were 0.3- 1.0%, mean was 0.67 ± 0.12%) was quite

similar to that in salamandrids (range is 0.1 -1.7%, mean

is 0.64 ± 0.03%, 99 populations studied), pelobatids, and

other anurans studied in our laboratory at the same con-

ditions (Litvinchuk et al., 1997, 1999, 200 1 a, b, 2003;

Rosanov and Vinogradov, 1998; Borkin et al., 2001b,

2003; our data).

Sexual dimorphism in genome size has been regis-

tered in some amphibian species (Schmid et al., 2002;

our data). Unfortunately, in the hynobiids examined by

us, sexual differences are not expressed in external char-

acters beyond the breeding time. Our study was based

mostly on juvenile and non-breeding adult animals, and,

therefore, we failed to reliably identify the sex without

anatomical dissections.

B) Geographical Variation

The significant geographical variation in genome size

was revealed for several amphibian species (Licht and

Lowcock, 1991; Murphy et al., 1997; Litvinchuk et al.,

1999, 2001b). In a few cases, differences (RD) exceed-

ed 8%. However, in the majority of species studied, such

differences were about 1% (Licht and Lowckock, 1991;

Borkin et al., 1997, 2000, 2001, 2003; Litvinchuk et al.,

1997, 1999, 2001b, 2003; our data). In Salamandrella

keyserlingii, the maximum genome size difference (RD

= 4.5%) was found between samples from the Khandyga

(Yakutia Republic) and Kedrovaya Pad' Reserve

(Primorsky Territory). The average differences (RD)

between the "Euro-Siberian" and the "Primorsky" sam-

ple groups of the species were equal to 3.2%.

3) Interspecies differences: developmental and kary-

ological correlations

Eleven species of the family Hynobiidae may be divid-

ed into two groups by their genome size. Two species of

the genus Onychodactylus form a group with the largest

genomes (104-108 pg). They also have the longest

embryonic and larval development periods (Table 3), as

well as the greatest number of chromosomes (Table 4).

Another group includes the remaining nine species

(33-67 pg). Among them, Salamandrella keyserlingii

has the largest genome size, and the seven species from

the genera Hynobius and Batrachuperus have smaller

sizes. Ranodon sibiricas has an intermediate genome

size. Such a distribution of genome sizes in the second

group does not seem to be associated with ovum diame-

ter, and, perhaps, with time of embryonic and larval

development (Table 3).

The comparison of genome size values in the sec-

ond group with karyological data evidenced no signifi-

2004

cant relations between the nuclear DNA content and

diploid chromosome numbers (Table 4). Nevertheless,

we found the positive correlation (r = 0.9998) between

genome size and uniarmed macrochromosome numbers.

4) Intergeneric relationships

Based on recent studies (Fei and Ye, 2000a; Fu et al.,

2001), approximately eight or ten genera of the hynobi-

ids could be recognized. The most speciose genus,

Hynobins, consists of about 24 species, which may be

arranged into three subgenera (Matsui et al., 1992;

Mizuno et al., 1995; Borkin, 1999), namely

Pseudosalamandra (7 species from Japan and Taiwan),

Satobius (1 species from Hokkaido Island), and

Hynobius (11 species from Japan, and, perhaps, 5

species from Korea and China). The family also includes

the genera Liua (1 species), Onychodactylus (2 species),

P achy hynobius (1 species), Protohynobius (1 species),

Pseudohynobius (2 species), Ranodon (1 species),

Salamandrella (1 species, which penetrates to eastern

Europe), and Batrachuperus (sensu lato) (about 9

species). The taxonomic position of Ranodon , Liua, and

Pseudohynobius was discussed (Fei and Ye, 2000b;

Kuzmin and Thiesmeier, 2001). Based on mitochondrial

DNA study, T. Papenfuss (Pers. comm, in Fu et al.,

2001) showed that the genus Batrachuperus is para-

phyletic, and consists of two groups with distinct geo-

graphic distributions. The Eastern (Chinese) group

belongs to Batrachuperus (sensu stricto) and consists of

about six species (Fei and Ye, 2000b; Fu et al., 2001;

Song et al., 2001). The western (Iran and Afganistan)

group includes two or three species (Stock, 1999), and

may be allocated to Paradactylodon.

Various authors suggested several configurations of

evolutionary relationships among hynobiids. For

instance, based on reproductive biology characters,

Thom (1969) proposed to recognize two families:

Ranodontidae, with the genus Ranodon only, and

Hynobiidae, with remaining genera. Using a set of mor-

phological and biological data, Zhao and Hu (1984) sep-

arated two "natural" groups among Chinese species: the

Hynobius group with predominantly terrestrial species

(Hynobius and Salamandrella ), and the Ranodon group

with predominantly aquatic inhabitants ( Ranodon ,

Onychodactylus , Batrachuperus , and Liua). Later, Zhao

and Zhang (1985) assigned the genus Pachyhynobius to

a third group. Combining morphological characters and

mitochondrial DNA data, Larson and Dimmick (1993)

found the closest relationships between the genera

Salamandrella and Hynobius , thus confirming the tradi-

tional acceptance of the similarity of these taxa.

However, the genus Onychodactylus was more closely

related to that lineage, whereas Batrachuperus (the east-

ern group) proved to be more distant. Recently, Fei and

Ye (2000a) have erected a new subfamily for the newly

discovered Protohynobius puxiongensis, whereas all

other hynobiids were allocated to another subfamily.

Genome size data are not in agreement with all

these suggestions, which did not recognize separate

position of the genus Onychodactylus. Apart from the

largest genome size, distincton of the genus was also

supported by morphological and karyological data

(Morescalchi et al., 1979; Olmo, 1983; Kohno et al.,

1991; Iizuka, Yazawa, 1994; Kuro-o et al., 2000;

Litvinchuk and Borkin, 2003).

5) Taxonomic considerations

Based on the intraspecific analysis, Bassarukin and

Borkin (1984), and Borkin (1994) outlined the peculiar-

ities of Salamandrella keyserlingii from the southern

part of the Russian Far East. Moreover, these authors

suggested that local populations would be considered as

a geographic race of the species (the species type terri-

tory is the Kultuk Village, Baikal Lake, Irkutsk

Province, Russia; restricted by Borkin, 1994). Indeed,

the "Euro-Siberian" and "Primorsky" groups of popula-

tions are different in allozymes (Litvinchuk et al.,

2001a), in some morphological characters (Ostashko,

1981; Bassarukin and Borkin, 1984; Borkin, 1994;

Litvinchuk and Borkin, 2003), in breeding sites

(Kuzmin, 1990), and in the shape of egg sacs and time

of larval development (Korotkov, 1977; Bassarukin and

Borkin, 1984; Sapozhnikov, 1990; Vorobyeva et al.,

1999). Therefore, geographic differences in genome size

revealed by us are in concert with differences in other

characters. Based on a concordance of various charac-

ters, including genome size, we would recognize a dis-

tinct status of the "Primorsky" samples, at least, of a sub-

specific rank. Formerly, Nikolsky (1906) and Dybowski

(1928) have coined the names Salamandrella keyser-

lingii var. tridactyla and Salamandrella keyserlingii var.

kalinowskiana, respectively, for animals from the

Russian Far East. Obviously, the first name has the pri-

ority. Therefore, populations from Russian Far East

(Primorsky Territory) should be named Salamandrella

keyserlingii tridactyla Nikolsky, 1906.

The range of Ranodon sibiricus is quite limited.

Nevertheless, it consists of several semi-isolated areas

(Brushko et al., 1988; Kuzmin et al., 1998; our data).

The populations from the upper parts of Borokhudzir

and Oy-Saz Rivers are separated from each other by a

mountain range. Therefore, it is not surprising that the

genome size difference (RD) between them is relatively

large (2.2%). However, geographical variation in the

species is poorly studied, and so the taxonomic value of

that difference is still unclear.

Vol. 10, p. 289

Asiatic Herpetological Research

2004

Acknowledgments

We thank A. G. Borissovsky (Izhevsk), V. G. Ishchenko

(Ekaterinburg), V. N. Kuranova (Tomsk), J. C. Lacroax

(Paris), I. V. Maslova (Spassk-Dal'ny), N. Panfilova

(Almaty), M. V. Pestov (Nizhniy Novgorod), G. P.

Sapozhnikov (Vilnus), V. T. Sedalishchev (Yakutsk), E.

I. Vorobyeva (Moscow), Y. Zhuravlyev (Almaty), and

the staff of Almaty and Moscow Zoo terraria for help us

in the field or providing animals. We also thank

Theodore Papenfuss (Berkeley) for valuable comments

and English corrections of the earlier version of the

paper. The research was funded by the INTAS (grant no

97-11909), the Russian Foundation for Basic Research

(the grant No. 02-04-49631), and the Federal State

Program "Integration" (the grant No. E-0121).

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2004

Asiatic Herpetological Research

Vol. 10, pp. 295-297

Anomalous (?) Nocturnal Feeding by the Agamid Lizard Calotes emma in

Northeastern Thailand

William H. Schaedla

Department of Biology, Arizona State University, RO. Box 871501 Tempe, Arizona 85287-1501, U.S.A.

E-mail: schaedla@asu.edu

Abstract. - I observed feeding by the Agamid lizard Calotes emma during the early part of the Thai monsoon season.

During this period, one individual took advantage of swarming termite reproductives and fed noctumally. Nocturnal

activity has not been reported for this genus. The lizard's behavior may have resulted from conditions created by arti-

ficial lighting. Alternately, it may constitute a normal response to a rich annually-available food resource.

Key words. - Calotes emma, feeding, termites, nocturnal,

Introduction

Agamid lizards belonging to the genus Calotes are

widely distributed throughout South and Southeast Asia.

They are characterized by semi-arboreal or arboreal

behavior, strongly diurnal activity patterns, and insectiv-

orous diets (Erdelen, 1988; Gunther, 1864; Subba Rao

1970, 1975; and Subba Rao and Rajabai, 1972).

Calotes emma is a typical member of the genus.

The species occurs from Assam through Yunnan in the

north, and Peninsular Thailand in the south. It prefers

moist forested habitat and is arboreal to semi-arboreal it

its habits (Gunther, 1 864). Here I report observations of

C. emma feeding at night in a manner apparently con-

trary to norms for the genus.

Methods

This study took place at the Sakaerat Environmental

Research Station. Sakaerat is a scientific and education-

al facility located in Northeastern Thailand at 14° 30.46'

N Latitude by 101° 55.92' E Longitude. The station

grounds cover approximately 80 km2.

Small and medium-sized wildlife is plentiful in the

area. As of this writing, 70 species of mammals, 50

species of birds, and 25 species of amphibians have been

recorded from Sakaerat. Reptile fauna is also abundant

-82 species are known to occur (Lawanyawatna and

Schaedla, 2000). Of the reptiles, C. emma is among the

most common because of the station's abundant forest

cover.

Seasonal (monsoonal) and perennial dipterocarp

forests comprise the bulk of Sakaerat's habitats. I

worked specifically in an area of Dry Evergreen Forest,

which is a Dipterocarp mosaic containing other floral

components. It is a four storied forest. The upper story

extends from 2 1 to 40 m in height and consists mostly of

Hopea ferrea , H. odorata, Shorea sericeiflora , and

atypical behavior.

Irvingia malayana. The middle story ranges from 15 to

20 m in height and contains Hydrocarpus ilicifolius,

Memocylon ovatum, and Walsura trichostemnon. The

lower story is between 4 and 24 m in height and is char-

acterized by Baccaurea sapida, Apodytes dimidiate, and

Olea salicifolia. Undergrowth is less than 4 m from the

ground, leafy, and composed mainly of Ardisia,

Canthium, and Clausena.

Average humidity at Sakaerat runs about 76% over

the course of the year. Average annual precipitation is

1,222 millimeters, and average annual temperature is

26°C. March is the hottest month with a maximum

recorded high of 37°C. January is the coolest with a

minimum recorded low of 8°C. Sakaerat generally

experiences a 3.5 month long rainy season that lasts

from early June through mid September. Conversely,

rainfall is rare from December through February

(Tongyai, 1980).

I made behavioral observations of Sakaerat's

Calotes emma on the evenings of 7, 10, and 12 June,

2001. These dates followed the onset of the local mon-

soon season, but were not monsoon days themselves.

Weather conditions were overcast, but there was no

heavy or sustained precipitation. Rainfall was light and

intermittent, accompanied by occasional lightning.

Ambient temperature was moderate, ranging from 27° to

30°C.

My observations took place from approximately

6:00 PM (dusk) to 9:00 PM. I watched from an area in

a semi-secluded part of the research station. My vantage

was the front porch of a bungalow near Sakaerat's sta-

tion headquarters, but offset in the forest and away from

the main complex of office, visitor's center, cafeteria,

and general housing. This area is dimly lit by two over-

head fluorescent lights attached to the sides of buildings.

These lights attract large numbers of insects, especially

during seasonal monsoon periods. In particular, termite

alates (winged reproductives) were present in high num-

Vol. 10, p. 296

Asiatic Herpetological Research

2004

bers on the evenings I observed. Large swarms of

Odontotermes sp. and Macrotermes sp. clouded the

local area and eventually dropped to the ground.

When termites fell to the ground, 1 observed a sin-

gle C. emma feeding them. The lizard was present all

three rainless nights, and seemed unperturbed by my

presence. It was there from dusk, or before, to nearly

9:00 PM on all three evenings. It was active, and its

behavior was restricted to the terrestrial environment. It

did not climb nearby trees or the sides of wooden build-

ings. All of its movements were directed; it displayed

no signs of disorientation in the relative darkness of its

surroundings. On the contrary, it focused on the termite

alates and fed vigorously on them as they landed.

On June 10, I captured the lizard to verily its iden-

tity as C. emma. It had been correctly identified and was

a mature female. Her stomach was distended from ter-

mite consumption, but she was not visibly gravid with

eggs.

In addition to the lizard, other predators feeding on

the termite alates included toads (Bufo melanostictus),

geckoes ( Cyrtodactylus spp .), and centipedes

(Scolopendr amorpha).

Discussion

Little is known about the exact feeding preferences of C.

emma. However, some indication of its diet might be

inferred from studies of a closely related arboreal

species. Subba Rao (1972) found that C. nemoricola in

India fed mostly on ants, while Sitana ponticeriana, an

unrelated ground-dwelling lizard, fed on termites. In

another study he found that C. nemoricola consumed a

wide variety of invertebrates ranging from beetles, to

gastropods, to earthworms. Analysis of gut contents

showed a predominance of ants but no termites. He also

noted a distinct absence of flying insects in the lizards'

stomachs (Subba Rao, 1975). Hence, feeding on winged

termites by C. emma may represent a departure from its

normal dietary habits.

Likewise, nocturnal feeding has not been reported

in the literature surrounding Calotes. In fact, members

of the genus are usually active only during the day

(Erdelen, 1988; Gunther, 1864; Subba Rao 1970, 1975;

and Subba Rao and Rajabai, 1972). C. emma at Sakaerat

is decidedly diurnal in its habits. At night they tend to

sleep on the ends of low-hanging tree branches.

Spotlighting does not wake them and they can be cap-

tured easily by anyone walking through the forest with a

headlamp. I have worked at Sakaerat for three years,

and, with the exception of the observations reported

herein, I have never seen them active at night.

Calotes is apparently physiologically predisposed

towards diurnal activity. Light has a positive affect on

both the pituitary and the hypothalmamo-neuro secreto-

ry systems of C. versicolor (Banerjee, 1972). However,

Kar (1987) found that day length (photoperiod) played a

less important role than ambient temperature in scale

regeneration by C. versicolor. He speculated this hap-

pens because the lizards' thyroid activity is elevated by

heat, rather than light.

Evening temperatures were warm on the nights I

made my observations. The lizard I observed may have

been able to extend her activity because of this. It is also

possible that the lack of sunlight was mitigated by the

presence of overhead florescent lights (albeit dim). My

subject may simply have been disrupted from its normal

circadian routine by the local environment. Some sup-

port for this possibility comes for another observational

study. Subba Rao et al. (1984) noted that abrupt changes

in light intensity, temperature, and relative humidity dur-

ing a total solar eclipse actually stimulated activity in C.

versicolor.

Of course, the feeding I observed may have been

part of C. emma' s normal behavioral regime. Termite

alates constitute a rich, but seasonally discrete food

source, induced by the onset of the monsoons. They are

available in great numbers at specific times of the year,

and they attract a wide variety of predators, including

retiles. It is therefore possible that C. emma takes advan-

tage of the bonanza via seasonal changes in behavior.

Whatever the case, nocturnal feeding by C. emma is

unusual and unreported. Even if not anomalous it

deserves future attention.

Literature Cited

Banerjee, S. K. 1973. Effect of light and darkness on the

hypothaamo-neurohypophyseal system of the gar-

den lizard, Calotes versicolor. Experientia

29(6):7 13-714.

Erdelen, W. 1988. Population dynamics and dispersal in

three species of Agamid lizards in Sri lanka: Calotes

calotes , C. versicolor , and C. nigrilabris. Journal of

Herpetology 22(l):42-52.

Gunther, A. C. L. 1864. The reptiles of British India.

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Kar, A. 1987. Relative importance of temperature and

photoperiod on the physiology of Indian garden

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Lawantayana K. and W. H. Schaedla. 2000. A Brief

Overview of the Sakaerat Environmental Research

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2004

Asiatic Herpetological Research

Vol. 10, p. 297

Pomprasertchai, K. and D. Disbanjong 1998. Changes in

the forest area at Sakaerat Environmental Research

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Subba Rao, M. V. 1970. Studies on the biology of two

selected lizards of Tirupati. British Journal of

Herpetology 4:151-154.

Subba Rao, M.V. and B. S. Rajabai, 1972. Ecological

aspects of the Agamid lizards Sitana ponticeriana

and Calotes nemoricola in India. Herpetologica

28:285-289.

Subba Rao, M. V., A Eswar, and K. Kameswara Rao,

1984. Effect of pre, during, and post total solar

eclipse on the activity pattern of an Agamid garden

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Environmental Biology 5(3): 197-201.

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forest resources. Thai government publication.

Karyological Studies on Amphibians in China

Yuhua Yang

Molecular Biology Labortary, Department of Bioengineering, Sichuan University, Chengdu, 610064, R.P.China

Abstract. - Since 1978, 79 species of anurans have been studied karyotypically using conventional Giemsa staining

and various banding techniques. The chromosome numbers are 2n=22-64 and the karyotypes are variable. The homo-

morphic and heteromorphic sex chromosomes of some species have been identified. The mitotic and meiotic chromo-

somes of 14 species in two families of Urodela have also been investigated. The family Hynobiidae is karyotypical-

ly more primitive than the family Salamandridae.

Key words. - Karyology, amphibian, Anura, Urodela.

Introduction

Karyological studies of amphibians in China were pio-

neeered by two scholars. In 1952, famous cytologist T.

C. Hsu, an American of Chinese origin, developed the

hypotonic technique for chromosome separation and

observation. In 1956, cytogeneticist J. H. Tjio, a Swede

of Chinese origin, reported that the number of human

chromosomes is 46, not 48. In China, karyological stud-

ies of amphibians began in 1978. Ninety-three species of

amphibians have been studied so far, about 42% of the

220 living amphibian species in China (Table 1).

Changes of chromosome numbers. - Kuramoto (1990)

summarized the chromosome numbers of 983 species of

anurans from 21 families (2n= 14-64). Chromosome

number changes occurred in 12 of 21 families with poly-

ploids in some species. In China, the chromosome num-

bers of 79 species from seven families are 22-64 and

variations of chromosome numbers were found in four

genera, three families (Table 2).

Only two species in the family Discoglossidae have

been studied: Bombina orientals and B. maxima. Tian

and Hu (1985) subdivided the genus Bombina into two

subgenera, Bombina and Glandula. Bombina ( B .) orien-

tals has 2n=28 chromosomes (Zhao, 1986), consistent

with the chromosome number of Discoglossus pictus in

Europe (Morescalchi, 1965; Schmid et al., 1987).

Bombina (G.) maxima has 2n=24 chromosomes (Jiang

et al., 1984), as reported by Okumoto (1974) and

Schmid et al. (1987).

The geography of the Hengduan Mountain Ranges

greatly influence the evolution of pelobatid frogs, pro-

viding refugia for some species as well as discontinuous

population distributions that promote allopatric specia-

tion (Yang et al., 1983; Hu et al., 1985). The pelobatids

distributed in the Hengduan Mountain region have dis-

tinct morphological differences adaptive to the unusual

geographic conditions. These species belong to two sub-

families, Megophryinae (Br achy tar sophrys and

Atympanophrys ) and Oreolalaxinae ( Scutiger ,

Vibrissaphora, Leptobrachium, and Oreolalax).

Available karyotypical information showed that species

studied have 2n=26 chromosomes, but karyotypical dif-

ferentiations are prominent in the family. The subgenus

Vibrissaphora is the most specialized, all five species

have 2n=26, consisting of six pairs of large chromo-

somes and seven pairs of small ones, NF=52 and one

stable secondary constriction is located in 6q (in the

NoRs region; Zhao et al., 1983). The karyotypes of three

species in genus Scutiger are similar to those of sub-

genus Vibrissaphora , except the secondary constriction

located in 2P not in 6q. Polymorphic chromosome num-

ber occured in Oreolalax. Two of the three specimens of

O. schmidti are 2n=28 and one is 2n=26 (Zheng andWu,

1989). A similar phenomenon was found in O. liang-

beiensis and C-banding showed that the extra pair of

small chromosomes is C-band negative and not B chro-

mosome (Li et al., 1990). Polymorphic chromosome

numbers were also found in three genera of

Megophryinae. Wu (1987) observed one male triploid in

Atympanophrys shapingensis. Tan et al. (1987) reported

the karyotypes of Brachytar sophrys carinensis. Among

12 individuals examined, seven males and one female

have 2n=26, three males have 2n=27, and the remaining

male has 2n=28. The extra chromosomes are metacen-

tric and between No. 10 and No. 11 in size. In addition,

there are four pairs of small chromosomes which are

telocentric in the2n=26 karyotype and two pairs of small

telocentric chromosomes were observed in M. omei-

montis (Wu, 1987; Zheng and Wu, 1989).

The karotypes of pelobatids reported by foreign

authors are 2n=26, NF=52 with no polymorphic chro-

mosome numbers found, except Leptolalax pelody-

toides with 2n=24 (Morescalchi, 1973; Morescalchi et

al. 1977; Schmid, 1980, 1987). It is interesting that a

special karyotype was observed in Rana phrynoides dis-

tributed in Hengduan Mountains. In this species, 2n=64

consisting of all telocentric chromosomes. Only one

homologous pair of NORs being found in interstitial

Vol. 10, p. 299

Asiatic Herpetological Research

2004

Table 1. A list of amphibian species studied karyologically.

segment of No. 20 chromosome, i.e, position of the sole

secondary constriction, and No. 32 being sat-chromo-

somes (Liu and Zan, 1984; Wu and Zhao, 1984). This

karyotype is unique for anurans.

Karyological Studies on wood frogs in China. - In

China, wood frogs include five species ( R . altaica, R.

amurensis, R. japonica, R. chaochiaoensis, and R.

chensinensis', Tian and Jiang, 1986). Rana chensinensis

had been called R. temproaria chensinensis (Pope and

Boring, 1940; Liu and Hu, 1961). Wu (1981) reported

the karyotype of R. chensinensis from Beijing, which

has 2n=24 chromosomes, including six pairs of large

chromosomes (relative length>7%) and six pairs of

small ones (relative length<6%), while R. temporaria in

Europe has 2n=26 (Guillemin, 1967), including five

pairs of large chromosomes and eight pairs of small

ones. Consequently, he suggested that R. chensinensis

should be a good species, not a subspecies of R. tempo-

raria. Wei et al. (1990) compared the C-bands and

NORs between R. chensinensis from type locality and R.

temporaria in Europe. As a result, in the former species,

centric C-bands located in Nos. 9 and 10 chromosomes

and telocentric C-bands in the terminations of a few

chromosomes, 28 interstitial C-bands, one pair of stan-

dard NORs in llq, and small additional NORs are

found. However, in the latter species, both centric and

telocentric C-bands are located in all chromosomes and

only three interstitial C-bands and 1 pair of NORs in lOq

were developed (Schmid, 1978). Evidently, this compar-

ison supports Wu’s suggestion.

Jiang et al. (1984), Luo and Li (1985) and Ma

(1987) indicated that R. chensinensis from different

localities have the same 2n=24 pattern, but the numbers

of subtelocentric chromosomes and the positions of sec-

ondaiy constrictionas are locality specific by comparing

the karyotypes of R. chensinensis from Beijing,

Qingdao, Lanzhou, Harbin, Hongyuan and Yanbei.

Consequently, it was suggested that R. chensinensis

might contain different subspecies .

The five species of wood frogs have 2n=24 or

2n=26 chromosomes and may be divided into two

groups: R. japonica , R. chaochiaoensis and R. amuren-

sis belong to 2n=26 group and R. chensinensis and R.

altaica to 2n=24 group. The karyotypic differences

between two groups are listed in Table 3.

Rana japonica from Hiroshima, Japan has 2n=26

chromosomes, Nos. 8 and 9 are subtelocentric and the

secondary constriction is located in 9q; R. amurensis

coreana from Korea has 2n=26, Nos. 10 and 13 subte-

locentric and secondary constriction in 9q; while R.

chensinensis from Hokkaido, Japan has 2n=24, No.l 1 is

subtelocentric and the secondary constriction in lOq

(Nishioka, et al., 1987). Matsui (1991) described R.

chensinensis from Hokkaido as a new species, R. pirica,

based on morphometric and electrophoretic studies.

The No. 6 chromosome of the species having 2n=24

is nearly the same in relative length as the sum of chro-

mosomes No. 11 and No. 12 or No. 13 of the species with

26 chromosomes, For instance, the average relative

length of No. 6 chromosomes of R. chensinensis and R.

altaica is 8.19, while the average relative lengths of

Nos. 11, 12 and 13 chromosomes of the other three

species are 4.52,4.31 and 3.82 respectively. In addition,

it is clear from Table 3 that there are more subtelocen-

tric chromosomes and secondary constrictions in the

species having 26 chromosomes than those in the

species having 24 chromosomes, and they are con-

cerned with small chromosomes. Accordingly, it is

speculated that all wood frog species would have a com-

mon ancestor, from which the species having 26 chro-

mosomes were derived and the species having 24 chro-

mosomes evolved via fusion of two pairs of small chro-

mosomes of the former. Then, the species possessing

2004

Vo). 10, p. 300

Table 2. A summary of chromosome numbers of 79 anuran species.

* = Polymorphic chromosome number occurs in some species.

different subtelocentric chromosomes and secondary

constriction positions were developed into two groups

through inversions and translocations. The high resolu-

tion R-bands of R. japonica were prepared and analyzed

(Heng, 1984), providing a practical technique for study-

ing karyotypic evolution of amphibians.

Sex chromosomes and sex-determining mechanisms. -

The first successful demonstration of sex-determining

mechanism was made by making use of reversal and

breeding experiments (Humphrey, 1942, 1945, 1957).

The applications of cytogenetic techniques, such as C-

banding, quinacrine mustard staining, Ag-NORs stain-

ing and in situ hybridization of nucleic acids, have been

helpful to the investigations on sex chromosomes and

sex-determining mechanisms in amphibians. So far,

eleven species with cytologically detected sex chromo-

somes, including XY and ZW systems, even an OW/OO

system of sex determination and multiple sex chromo-

somes in one genome(Schmid et al., 1992) were discov-

ered. Few sex-specific chromosome pairs in heteroga-

metic individuals are heteromorphic and most of them

are homomorphic.

The homomorphic chromosome pair No.4 in Rana

esculenta was identified as sex-specific chromosomes of

XX/XY type by BrdU replication banding technique. All

males have an extremely late-replication band in the

long arm of Y, which is lacking in the X (Schempp and

Schmid, 1981). The homomorphic chromosome pair

No. 10 in Bufo gargarizans was demonstrated to be sex

chromosomes of ZZ/ZW type. The Z chromosomes in

all males replicated synchronously, while Z and W chro-

mosomes of females revealed heteromorphic replication

bands at the late replication stage. There was a replica-

tion band on W chromosome’s long arm and Z chromo-

some lacked the band (Wen et al., 1982;Shang and

Deng, 1982). Similarly, the chromosome No. 6 pair in

Bufo raddei was identified as XX/XY sex chromosomes

(Deng and Shang, 1984) and the No. 9 chromosomes of

Rana nigromaculata as XX/XY sex chromosomes (Wu

and Zhang, 1985). The sex chromosomes of species

mentioned above are homomorphic and could only be

recognized by BrdU replication banding. So they are at

the initial stage of sex chromosome differentiation.

The Y or Z chromosomes of homomorphic sex

chromosomes in some anurans heterochromatinized so

Vol. 10, p. 301

Asiatic Herpetological Research

2004

Table 3. karyotypic comparison between wood frog groups.

highly that they could be recognized by C-banding or

other specific staining of constitutive heterochromatin,

for example, the XX/XY sex chromosomes in genus

Triturus (Schmid, et ah, 1979). Chinese scholars Wu and

Chen (unpublished data) determined the homomorphic

chromosome pair No. 9 as XX/XY sex chromosomes in

Rana margaratae using C-banding and quinacrine mus-

tard staining. There is one interstitial C-band, i.e, the

brightest fluorescense band, on both No. 9 chromosomes

in females. The interstitial C-band is located only in one

No. 9 chromosome, while one telocentric C-band in the

other No. 9 chromosome shows no fluorescense differen-

tiation.

The first-discovered highly heteromorphic ZW type

sex chromosomes occured in Pyxicephalus adspersus

(Schmid, 1980). The W chromosome is much smaller

than Z chromosome and its short arm is completely het-

erochromatic. Wu and Zhao (1984) and Wu et al. (1987)

demonstrated that Amolops mantzorum has well-differ-

entiated XY type sex chromosomes, the Y chromosome

is subtelocentric and mainly composed of euchromatin,

but has strong C-band in the middle of long arm and X

chromosome is metacentric by conventional Giemsa

staining and C-banding methods.

Karyological studied in urodeles. - Only two species

were studied by C-banding and the others by conven-

tional Giemsa staining. The karyotypic comparisons are

listed in Table 4. The family Hynobiidae has a wide geo-

graphical distribution. Twenty-six species in five genera

out of more than 34 species in eight genera have been

studied karyologically. The chromosome number vary

from 40 to 80 . Twelve species in Hynobius and one in

Salamandrella had been studied by C-banding, Ag-

NORs staining, and R-banding. The relationships in the

two genera were discussed by comparing banded kary-

otypes and Southern hybridizations. It is suggested that

the family is the most primitive living caudate

(Morescalchi, 1973; Kohno et al., 1991).The same con-

clusion is derived from morphological comparisons

(Zhao and Hu, 1984).

There are 17 species in seven genera in Hynobiidae

known from China. The family can be divided into two

groups: Hynobius group and Ranodon group. The

Ranodon group evolved by adaptation towards two dif-

ferent life-forms: aquatic and terrestrial. Liua and

Batrachuperus are aquatic and are closely related. Table

4 shows that seven species have high chromosome num-

bers: 2n=62-68. Their karyotypes are bimodal and sym-

metrical, with more microchromosomes (Yang, 1992).

Salamandrella keyserlingii has 2n=62 chromosomes,

the karyotype formula being 4M + 2SM + 10ST + 10T

+ 36 m (Wang et al., 1983) in accordance with that

reported by Morescalchi (1975), Morescalchi et al.

(1979), Grafodatsky et al. (1978), Kuro-o(1986), and

Ikebe et al. (1990). The bivalent number in cells of male

Batrachuperus pinchonii in diakinesis is 3 1 . We expect

the diploid chromosome number to be 2n=62 (Yang and

Zhao, 1984), but this species also has 2n=66 chromo-

somes (Kuro-o et al., unpublished data). There is little

detailed information on the cause of the difference.

The karyotypic differentiation of Hynobiidae is

more complex. First, variations in diploid chromosome

number occurred not only at the intergeneric level, but

also at the intrageneric level. For instance,

Salamandrella has 2n=62, Batrachuperus 2n=62-68,

both Liua and Pachyhynobius 2n=64. Secondly, the

numbers of microchromosomes vary from 36 to 46.

Finally, the morphology of microchromosomes are vari-

able. The numbers of M, SM, and ST are species-specif-

ic. Telocentric macrochromosomes were found in S', key-

serlingii, L. shihi and P. shangchengensis, but not in

Batrachuperus. The L. shihi and P. shangchengensis

studied were from the type localities (Zhao and Hu,

1983; Fei et al., 1983). Both two species have 2n=64

chromosomes, different from the known genera.

However, they are different in morphology of

macrochromosome and microchromosome number

(Table 4) . Therefore, the cytogenetic data provide evi-

dence supporting those genera and species.

There are four species in Batrachuperus.

Batrachuperus karlschmidti and B. yenyuanensis are

only found higher than 3000M in the Hengduan

Mountains, having 2n=68, no telocentric macromo-

somes and 44 and 46 microchromosomes respectively.

Batrachuperus pinchonii and B. tibetanus distributed

higher than 1600M of Hengduan Mountains and adja-

cent areas have 2n=62. Obviously, the karyotypic differ-

2004

Asiatic Herpetological Research

Vol. 10, p. 302

Table 4. Karyological comparisons of urodela in China. M-metacentric macrochromosomes, SM-submetacentric

macrochromosomes; ST-subtelocentric macrochromosomes; T-telocentric macrochromosomes, m-microchromo

somes.

entiations in Batrachuperus are in conformity with the

geographic distribution.

Salamandridae is the advanced family in Caudata

either from the viewpoint of karyotypic information or

from that of morphological characteristics (Morescalchi,

1973, 1975, 1979; Zhao and Hu, 1984; Yang,

1992). There are five genera of Salamandridae found in

China: Tylototriton, Echinotriton, Cynops,

Paramesotriton, and Pachytriton. Of the five genera,

Tylototriton is the most primitive and Pachytriton the

most advanced . The seven species studied in five gen-

era have the same chromosome number, 2n=24, without

microchromosomes. The karyotypes are unimodal and

symmetrical (Table 3). Interspecific differences were

found in Tylototriton. The karyotypic formula of T. kwe-

ichawensis is 16M+6SM+2ST, the same as that of T.

verrucosus. However, Nos. 6, 8 and 11 are submetacen-

tric and no secondary constriction was found in the for-

mer (Yang, 1990), while Nos. 6, 7 and 11 are submeta-

centric and secondary constriction were found at every

chromosomes except No. 12 in the latter (Seto et al.,

1982). Echinotriton andersoni has 2n=24 chromosomes,

14M + 8SM+ 2 ST, one more submetacentric chromo-

some pair than both T. kweichowcensis and T.verrucosus

(Seto et ah, 1982). In addition, the relative length of

chromosome No. 1 is the longest and that of No. 12 the

shortest in E. andersoni among the three species men-

tioned above. The karyotypic formulas of Pachytriton

brevipes and Cynops orientals are nearly identical and

only the differences of C-band patterns are found (Zhu

and Wei, 1981).

The predominant mode of karyotypic evolution in

Caudata is that the unimodal symmetrical karyotypes

with fewer chromosome number are derived from the

bimodal and asymmetrical karyotypes with more chro-

mosome number, via Robertsonian centric fusions and

pericentric inversions (Morescalchi, 1975).

Robertsonian centric fusions, which could occur

between telocentric macrochromosomes, between stable

microchromosomes, and between telocentric

macrochromosomes and stable microchromosomes,

cause reduction of the diploid number and the

microchromosome number and increase of the metacen-

tric chromosomes. Consequently, the karyotypes tend

toward stability. Pericentric inversions do not change the

diploid number, but could increase the number of meta-

centric chromosomes and the stability of karyotypes.

There are some differences in the evolutionary

trends of Hynobiidae and Salamandridae. The karyotyp-

ic evolution in Hynobiidae involves Robertsonian cen-

tric fusion as well as pericentric inversion. However, the

phylogeny of the family could not be established on the

available data. It is obvious that the karyotypes of

Salamandridae are more stable than those of

Hynobiidae. Morescalchi (1975) proposed that all

species studied possess similar karyotypes that differ

very little even at the intergeneric level. The differences

between the karyotypes mainly lie in the absolute size of

chromosomes and quantity of DNA. Accordingly, the

karyotypic diversity among the species has chiefly

resulted fiom pericentric inversions and reciprocal

translocations that result in differences between individ-

ual chromosomes by changing the telocentric chromo-

somes into metacentric ones or changing the metacentric

chromosomes into submetacentric, subtelocentric and

telocentric chromosomes.

Vol. 10, p. 303

Asiatic Herpetological Research

2004

Acknowledgments

I want to express my thanks to three professors: Zhao

Ermi, Chen Wenyuan and Wang Xizhong. Under their

encouragement and guidence this paper was worked

out. Sincere thanks are also extended to professor

Zheng Xuejing, who read and made some corrections

to this paper.

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The History of the Journal Asiatic Herpetological Research

Theodore J. Papenfuss

Museum of Vertebrate Zoology, University of California, Berkeley, C A 94720, USA

The origins of Asiatic Herpetological Research go back

34 years. Our present editor. Professor Ermi Zhao start-

ed a scientific periodical. Materials for Herpetological

Research, in 1972. Four issues were published, the last

in 1978 (Zhao and Adler, 1993). The text of all articles

was in Chinese only. The four issues were produced by

the Sichuan Biological Research Institute (now the

Chengdu Institute of Biology). Materials was followed

by Acta Herpetologica Sinica, which was also edited by

Zhao. There were two series between 1979 and 1987.

The “old series” consisted of six volumes published

from 1979-1982 and the “new series” from 1982-1987

(Zhao and Adler, 1993). The articles were in Chinese,

but English titles and often, English abstracts were

included.

Volume 1 of a new journal, Chinese Herpetological

Research, also edited by Zhao, was published in

Chongqing for the Chinese Society for the Study of

Amphibians and Reptiles, with Zhao continuing as edi-

tor. In 1988 Zhao visited the Museum of Vertebrate

Zoology, University of California at Berkeley as part of

his collaboration with J. Robert Macey and E The

MVZ’s single Mac Classic computer that could be used

for desktop publishing impressed him. At Zhao’s

request we agreed to transfer printing and distribution

from China to Berkeley. Macey and I also agreed to

serve as Associate Editors and to help assemble an inter-

national editorial board. We changed the name of the

journal to Asiatic Herpetological Research with volume

3 in 1990. With this volume 10, our journal will return

to the Chengdu Institute of Biology for printing and dis-

tribution. The quality of journals published in China is

now of world standard and the Internet, unknown in

1988, allows for easy electronic transfer of manuscripts,

and easy editing

Although our society is not large in membership, it

is very international. We have published articles by

authors from 29 countries. Fourteen new species of

amphibians and reptiles have been described since 1987.

We organized the First Asian Herpetology Meeting, held

in China in 1992, the Second Asian Herpetology

Meeting held in Turkmenistan in 1995, the Third Asian

Herpetology Meeting held in Kazakhstan in 1998, and a

Fourth Asian Herpetology Meeting in 1991 again in

China.

Literature Cited

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

Society for the Study of Amphibians and Reptiles. 522

pp.

* IT 4-

ACTA HEKPETOUX11CA SINICA

- k * a ♦ -r n

Materials of Acta Herpetologica Acta Herpetologica Chinese

Herpetology Sinica "old series" Sinica "new series" Hemetolooical

1972-1978 1979-1982 1982-1987 Research 1987

Vol. 10, p. 307

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2004

Asiatic Herpetological Research

Vol. 10, pp. 308-3 1 2

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Statistics must be accompanied by sample sizes, significance levels, and the names of any tests. Investigators

should pay careful attention to independence and applicability of tests, and randomness of samples. One of the

most frequent examples of nonindependence is the use of multiple, paired t-tests instead of analysis of variance

(anova). In general, multiple tests on the same data set are not valid. Descriptive statistics are in many cases more

appropriate than inferential statistics.

Standard Format

Manuscripts following standard format should include introduction, methods, results, and discussion sections.

While other formats are acceptable, the editors encourage the use of standard format. Please do not type in all

capital letters.

Introduction

The introduction typically states the significance of the topic and reviews prior research.

Material and Methods

This section should clearly state where, when, and how research was carried out. Include sample sizes. Protocols

designed by other investigators must be properly cited. Research materials and their manufacturers should be

listed. The reader must be able to replicate the methods of the author(s).

Results

This section states the results and their significance to the investigation. Figures and tables may be used to clarify,

but not to replace, results statements in the text. Statistics should be used when applicable. Large amounts of data

should be avoided, or included as an appendix at the end of the article.

Discussion

The discussion is a synthesis of the introduction and the results. No new information should be discussed unless

it was presented in the results section. New findings should be discussed in relation to prior research. The

author(s) should feel free to present several possible interpretations of the results. The editors particularly

encourage suggestions of future research in Asian herpetology.

Vol. 10, p. 310

2004

Manuscript Preparation

Overview

Please do not attempt to replicate the formatting style of AHR in your manuscript. All formatting except italics

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Section Headings

Articles will be published using three section heading styles. All heading levels must be on their own line, and

left justified. For the purposes of manuscript submission, Level 1 heading is bold, and generally reserved for

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Figure 2. Lateral view of live Psammodynastes pulverulentus holding a prey lizard (Anolis car-

olinensis ). Note buccal tissue surrounding the enlarged anterior maxillary and dentary teeth of

the snake.

Color Figures. AHR may publish color figures at the discretion of the editors. AHR is now published both on

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Twelve point type is preferred. Supply a detailed list of special characters (greek letters, male or female symbols,

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2004

Asiatic Herpetological Research

Vol. 10, p. 311

Literature Cited

Accurate and standard references are a crucial part of any article. This is especially important when dealing with

publications from many different countries. The reader must be able to precisely identify any literature cited.

References in the text must be checked for consistency with references in the literature cited section. All refer-

ences cited in the text must be in the literature cited section. The literature cited section may not contain any ref-

erences not mentioned in the text. Articles containing inaccurate or inconsistent literature citations will be

returned for correction.

References in Text. 1) References to articles by one or two authors must include both surnames in the order they

appear in the original publication. References to articles by more than two authors must include the first author's

surname, followed by “et al.” 2) The year of article follows the authors, separated only by a space. 3) References

with the same author and year are distinguished by the lower case characters “a, b, c, . . .” 4) References cited in

text are listed in alphabetical order by first author.

For example, “My results also incorporate literature records (Marx et al., 1982; Marx and Rabb, 1972;

Mertens, 1930; Pope, 1929; Wall, 1909, 1910a, 1910b, 1910c).”

References in Literature Cited. 1) References must include all authors, in the order that they appear in the orig-

inal publication; “et al.” is never used in a literature cited section. 2) The first author is listed surname first, ini-

tials) last. All other authors are listed initial(s) first, surname last. 3) References with the same author and year

are distinguished by the lower case characters, “a, b, c, . . .” 4) References cited are listed in alphabetical order by

first author. 5) Names of journals are not abbreviated. See below for examples:

Journal article

Dial, B. E. 1987. Energetics and performance during nest emergence and the hatchling frenzy in loggerhead sea

turtles ( Caretta caretta). Herpetologica 43(3):307-315.

Journal article from a journal that uses year instead of volume

Gatten, R. E. Jr. 1974. Effect of nutritional state on the preferred body temperatures of turtles. Copeia

1 974(4):9 1 2-9 17.

Journal article, title translated, article not in English

Ananjeva, N. B. 1986. [On the validity of Megalochilus mystaceus (Pallas, 1776)]. Proceedings of the Zoological

Institute, Leningrad 157:4-13. (In Russian).

Note that for Acta Herpetologica Sinica, the year must precede the volume number. This is to distinguish

between the old and new series, and between 1982-1987, Vols.1-6 (new series) and 1988 with no volume number,

numbers 1 and 2 (new series).

Cai, M., J. Zhang, and D. Lin. 1985. [Preliminary observation on the embryonic development of Hynobius chin-

ensis Guenther]. Acta Herpetologica Sinica 1985, 4(2): 177-180. (In Chinese).

Book

Pratt, A. E. 1892. To the snows of Tibet through China. Longmans, Green, and Co., London. 268 pp.

Article in book

Huey, R. B. 1982. Temperature, physiology, and the ecology of reptiles. Pp. 25-91. In C. Gans and F. H. Pough

(eds.), Biology of the Reptilia, Vol. 12, Physiological Ecology. Academic Press, New York.

Government publication

United States Environmental Data Service. 1968. Climatic Atlas of the United States. Environmental Data Ser-

vice, Washington, D. C.

Abstract of oral presentation

Arnold, S. J. 1982. Are scale counts used in snake systematics heritable? SSAR/HL Annual Meeting. Raleigh,

North Carolina. [Abstr].

Vol. 10, p. 312

Asiatic Herpetological Research

2004

Thesis or dissertation

Moody, S. 1980. Phylogenetic and historical biogeographical relationships of the genera in the Agamidae (Rep-

tilia: Lacertilia). Ph.D. Thesis. University of Michigan. 373 pp.

Anonymous, undated

Anonymous. Undated. Turpan brochure. Promotion Department of the National Tourism Administration of the

People's Republic of China, China Travel and Tourism Press, Turpan, Xinjiang Uygur Autonomous Region,

China.

Copyright

Asiatic Herpetological Research reserves the copyrights to all material published therein, except that excluded

by permission of the editors. Any material under a prior copyright submitted to Asiatic Herpetological Research

must be accompanied by the written consent of the copyright holder.

Submission of Manuscripts

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ures will be reduced to either 1 column (3.25”) or two columns (6.5”).

Manuscripts will be reviewed. The editors will attempt to choose reviewers whose research knowledge most

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Send manuscripts by postal mail to Editors, Asiatic Herpetological Research, Museum of Vertebrate Zoology,

3101 Valley Life Sciences Building, University of California, Berkeley CA 94720-3160 USA.

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sage is returned, or not acknowledged, you may want to try again or to send your manuscript by postal mail.

Kuinulta§, Y., S. H. Durma§, Y., Kaska, M. Oz, and M. R. Turn;. A Morphological and Taxonomic Study

on Lacerta parva Boulenger, 1887 (Sauria: Lacertidae) from West Taurus, Turkey 202-207

Macey, J. R. and N. B. Ananjeva. Genetic Variation Among Agamid Lizards of the Trapelus agilis

Complex in the Caspian-Aral Basin 208-214

Ugurta§, i. H., H. S. Yildirimhan, and M. Kalkan. The Feeding Biology of Ran a macrocnemis

Boulenger, 1885 (Anura: Ranidae), Collected in ULUDAg, Bursa, Turkey 215-216

Sevin^, M., \. H. Ugurta§, and H. S. Yildirimhan. Morphological Observations on the Erythrocyte

and Erythrocyte Size of Some Gecko Species, Turkey 217-223

Sharif i, M. and S. Assadian. Distribution and Conservation Status of Neurergus microspilotus

(Caudata: Salamandridae) in Western Iran 224-229

Tosunoglu, M., D. Ayaz, C. V. Tok, and B. Dulger. An Investigation on the Blood Cells of the

Leopard Gecko, Eublepharis angr.4mainyu (Reptilia: Sauria: Eublepharidae) 230-234

Ahsan, M. F. and S. Parvin. A Record of Boiga ochracea walli (Stoliczka, 1870) from Bangladesh 235

Ahsan, M. F. and M. A. Saeed. Some Aspects of Breeding Biology of the Bengal Lizard ( Varan us

BENGALENSIS) IN BANGLADESH 236-240

Das, I. ANew Locality for the Rare Bornean Skink, Lamprolepis vyneri (Shelford, 1905)

(Sauria: Scincidae) 241-244

Das, I. and S. K. Chanda. Leptobrachium smithi Matsui, Nabitabhata, and Panha, 1999 (Anura:

Megophryidae), and Addition to the Fauna of Myanmar (Burma) 245-246

Grismer, J. L., L. L. Grismer, I. Das, N. S. Yaakob, L. B. Liat, T. M. Leong, T. M. Youmans, and H. Kaiser.

Species Diversity and Checklist of the Herpetofauna of Pulau Tioman, Peninsular Malaysia,

With a Preliminary Overview of Habitat Utilization 247-279

Guo, P. and E. Zhao. Pareas stanleyi - A Record New to Sichuan, China and a Key to the

Chinese Species 280-281

Litvinchuk, S. N., L. J. Borkin, and J. M. Rosanov. Intraspecific and Interspecific Genome Size Variation

In Hynobiid Salamanders of Russia and Kazakhstan: Determination by Flow Cytometry 282-294

Schaedla, W. H. Anomalous (?) Nocturnal Feeding by the Agamid Lizard Calotes emma in

Northeastern Thailand 295-297

Yang, Y. Karyological Studies on Amphibians in China 298-305

Papenfuss, T. J. The History of the Journal Asiatic Herpetological Research 306-307

Editors. Guidelines for Manuscript Preparation and Submission 308-312

Asiatic Herpetological Research is created using QuarkXPress 6.0. Adobe Illustrator 10. Adobe Acrobat 6. and Adobe Photoshop

6 on both Macintosh OS 10 and Microsoft Windows XP operating system platforms. Body text is in Times New Roman and the

Headings in Arial. Using digital technology, we consumed less than 400 sheets of paper in the prepress production of this issue.

ISSN 1051-3825

Diaz, R. E., M. T. Leong, L. L. Grismer, and N. S. Yaakob. A New Species of Dibamus

(Squamata: Dibamidae) from West Malaysia

Grismer, L. L., j. L. Grismer, and T. M. Youmans. A New Species of Leptolalax (Anura: Megophryidae)

FROM PlILAU TlOMAN, WEST MALAYSIA I I

Leong, T. M. and L. L. Grismer. A New Species of Kukri Snake, Oligodon (Colubridae), from Pulau

Tioman, West Malaysia 12-16

Stuart, B. L. and H. Heatwole. A New Philautus (Amphibia: Rhacophoridae) from Northern Laos 17-21

Diesmos, A. C., G. V. A. Gee, M. L. Diesmos, R. M. Brown, P. J. Widmann, and J. C. Dimalibot.

Rediscovery of the Philippine Forest Turtle, Heosemys leytensis (Chelonia; Bataguridae), from

Palawan Island, Philippines 22-27

Feldman, C. R. and J. F. Parham. Molecular Systematics of Old World Stripe-Necked Turtles

(Testudines: Mauremys ) 28-37

Hutchison, J. H„ P. A. Holroyd, and R. L. Ciochon. A Preliminary Report on Southeast Asia’s Oldest

Cenozoic Turtle Fauna from the Late Middle Eocene Pondaung Formation, Myanmar 38-52

Joyce, W. G. and C. J. Bell. A Review of the Comparative Morphology of Extant Testudinoid Turtles

(Reptilies: Testudines) 53-109

Le, Minh, T. Hoang, and D. Le. Trade Data and Some Comments On the Distribution of Mauremys

ANNAMENS1S (SlEBENROCK, 1 903) 110-113

Perala, J. and R. Bour. Neotype of Testudo terrestris ForsskAl, 1775 (Testudines, Testudinidae) 114-119

Schilde, M., D. Barth, and U. Fritz. An Ocadia sinensis x Cyclemys shanensis hybrid (Testudines:

Geomydidae) 120-125

Shi, H., Z. Fan, F. Yin, and Z. Yuan. New Data on the Trade and Captive Breeding of Turtles in

Guangxi Province, South China 126-128

Stuart, B. L. and S. G. Platt. Recent Records of Turtles and Tortoises from Laos, Cambodia, and

Vietnam 129-150

Auffenberg, K., K. L. Krysko, and W. Auffenberg. Studies on Pakistan Lizards: Cyrtopodion stoliczkai

(Steindachner, 1867) (Gekkonidae: Gekkoninae) 151-160

Diilger, B., j. H. Ugurta§, and M. Sevin^ Antimicrobial Activity in the Skin Secretion of Bufo viridis

(Laurenti, 1768) 161-163

Du§en, S., M. Oz, and M. R. Tunq:. Analysis of the Stomach Contents of the Lycian Salamander

Mertensiella luschani (Steindachner, 1891) (Urodela: Salamandridae), Collected from Southwest

Turkey 164-167

Ebrahimi, M., H. G. Kami, and M. Stock. First Description of Egg Sacs and Early Larval Development

in Hynobiid Salamanders (Urodela, Hynobiidae, Batrachuperus ) from North-Eastern Iran 168-175

Jarrar, B. M„ and N. T. Taib. Histochemical Characterization of the Lingual Salivary Glands of the

House Gecko, Ptyodactylus hasselqu/stii ( Squamata: Gekkonidae) 176-181

Kami, H. G. The Biology of the Persian Mountain Salamander, Batrachuperus persicus (Amphibia,

Caudata Hynobiidae) in Golestan Province, Iran 182-190

Khan, M. S. Annotated Checklist of Amphibians and Reptiles of Pakistan 191-201

(Continued on inside back cover)

Herpetological

Research

Volume 11 • 2008

Chengdu Institute of Biology of the Chinese Academy of Sciences

Asiatic Herpetological Research Society at the Museum of Vertebrate Zoology,

University of California

MCZ ERNST MAYR LIBRARY

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