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World list abbreviation: Bull. nat. Hist. Mus. Lond. (Zool.)

ISSN 0968-0470

The Natural History Museum Zoology Series

Cromwell Road Vol. 68, No. 2, pp. 51-163

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Editorial: Garth Underwood — Dedication

This issue, the last of the Zoology series of the Bulletin of the Natural

History Museum, is dedicated to Dr Garth Underwood. Garth has had

along association with the Natural History Museum. In 1964, he was

appointed Principal Research Fellow to work on snake systematics, a

project which culminated in the modestly titled “A contribution to the

classification of snakes” (Underwood, 1967). This book had a major

impact on snake classification, pioneering the use of soft anatomy as

a source of systematic characters. Its importance may be readily

appreciated from the many references made to itin many of the papers

in this special issue of the Bulletin (see especially Kochva in the

introduction to his paper on burrowing asps, Atractaspis). In a more

informal sense, Garth’s association with the Natural History Museum

started much earlier than 1964; a visit to the Museum in the late 1930's

apparently gave him useful information for answering his Higher

School Certificate papers in Zoology! Like many zoologists, an

interest in natural history was something that was ingrained, and it

seems that Garth always was seeking explanations for biological

phenomena. His father, Leon Underwood, an eminent British sculp-

tor and painter, dedicated a book called Animalia, subtitled Fibs

about Beasts to Garth, showing him as a baby, thoughtfully looking at

a frog. The book offers poetic or fanciful explanations about the

animals within its pages, rather than scientific ones. The dedication

reads: “To Garth, For whom cleaving facts asunder fall, And fancy

sheds a healing light on all”. Garth, if not then, certainly now seeks

more objective, scientific interpretations in the biological sciences,

particularly of snake relationships.

Even a brief dedication such as this would be seriously deficient

if it did not mention the contribution Garth has made to herpetology,

not just in terms of his published work but through his encourage-

ment and supervision of the studies of others. “A contribution to the

classification of snakes” was a starting point; Garth has always

sought new characters to shed new light on snake relationships,

devised new ways of looking at data, and has never been afraid to

revisit previous work to improve upon and revise earlier results. He

has passed on these ideas to others; within the Museum alone he has

supervised no less than 6 PhD’s, most relating to snakes, but also

encompassing frog and insect systematics. He has also run under-

graduate and postgraduate courses in taxonomy, through times when

systematics was less appreciated than formerly or even today.

Many people owe Garth a considerable debt of gratitude for his

help, guidance and support. He has been an inspiration to genera-

tions of undergraduates, postgraduates and scientific colleagues

worldwide; we hope he will be pleased with this token of our

appreciation.

Editors for this issue:

Barry Clarke and Mark Wilkinson

Sadly, Garth died on 15th October 2002 before this issue came out. He had seen or was aware of much of its contents.

Photograph showing Garth Underwood in May 1966 when he was working on his “Contribution to the classification snakes”. © The Natural History Museum

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 51-55

Hemipenial variation in the African snake

genus Crotaphopeltis Fitzinger, 1843 |

(Serpentes, Colubridae, Boiginae)

THOMAS ZIEGLER

Zoologisches Forschungsinstitut und Museum Alexander Koenig, Adenauerallee 160, D-53113 Bonn,

Germany. e-mail: dr.th.ziegler@ t-online.de

JENS BODTKER RASMUSSEN

Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen @, Denmark. e-

mail: jbrasmussen @ zmuc.ku.dk

Synopsis. Hemipenial variation within the six recognized species of the African snake genus Crotaphopeltis is described. The

hemipenial ornamentation of the widely distributed species, C. hotamboeia and C. hippocrepis, seems fairly constant whereas the

ornamentation of C. degeni and C. tornieri, species with disjunct distributions, displays relatively large intraspecific variation.

In spite of the variation, the size and ornamentation of the hemipenes serve to distinguish between sympatric and parapatric

species.

INTRODUCTION

The various species within the African snake genus, Crotaphopeltis

have been treated in a series of taxonomic papers (Rasmussen, 1985;

1993a; 1997; Rasmussen et al., 2000). Hemipenes have been exam-

ined in situ and in everted or even in partly everted condition where

possible. Recent collecting has increased the number of specimens

with everted hemipenes. This provides a welcome opportunity for

redescribing the hemipenes of the six recognized species. Further,

differences between the hemipenes of the various isolated popul-

ations of C. tornieri, of C. degeni, and of the various populations of

the widely distributed C. hotamboeia may provide an indication of

the taxonomic status of some of the populations.

MATERIAL AND METHODS

Specimens included in the present study are held in the collections of

the following museums: The Natural History Museum, London

(BMNH); California Academy of Sciences, San Francisco (CAS);

Museum of Comparative Zoology, Harvard (MCZ); Musée Royal

d’ Afrique Centrale, Tervuren (MRAC); Rijksmuseum van Naturlijke

Historie, Leiden (RMNH); National Museum of Natural History,

Washington (USNM); Zoologisches Forschungsinstitut und Mu-

seum Alexander Koenig, Bonn (ZFMK); Zoological Museum,

University of Copenhagen, Copenhagen (ZMUC).

In the following list the catalogue numbers and places of origin are

given for each specimen of the six currently recognized Crotapho-

peltis species:

Crotaphopeltis barotseensis. BOTSWANA: Okawanga Delta

(ZMUC 631232).

Crotaphopeltis braestrupi. SOMALIA: Mareri, ca. 8 km SW of

Gelib (CAS 153370, 153379).

Crotaphopeltis degeni. CAMEROON: Gueme (MRAC 73-15-

R209). ETHIOPIA: Gambela (USNM 24389). SUDAN: Assalaya,

10 mls E. of Kosti (RMNH 24411, 25018). TANZANIA: Tumba,

Lake Rukwa (ZMUC 631233): Minziro Forest (ZMUC R631598,

R631610, R631618, R631621). UGANDA: Kome Island, Victoria

Nyanza (BMNH 1984.883).

Crotaphopeltis hippocrepis. GHANA: Legon (ZFMK 63880); Legon

Hill (ZMUC R631238); Legon Road, Achimota (ZFMK 63775);

Wa, Secondary School (ZFMK 63875, 63877).

Crotaphopeltis hotamboeia. CONGO: Tchissanga (ZMUC

R631177). GHANA: Wa (ZFMK 63874). KENYA: Langata, NW

of Nairobi (ZMUC R63984). SOUTH AFRICAN REPUBLIC:

Cape Peninsula (ZMUC R63894); Tshaneni (ZMUC R63889). SU-

DAN: Talanga Forest (ZMUC R63980); Torit (ZMUC R63979).

TANZANIA: Magombero Forest (ZMUC R63921); Msolwa area,

Rubeho Mountains (ZMUC R631205—06, R631208—10); Rungwe

Mountains (ZMUC R631264, R631266, and R631268). ZAIRE: 6

km NE of Kafumba, near Kikwit (ZMUC R631072).

Crotaphopeltis tornieri. TANZANIA: East Usambara Mountains:

Amani (R631122—3); Kwamkoro (R631127). Rungwe Mountains:

Rungwe Mission ZMUC R631257. Udzungwa Mountains: Kihanga

River, Udzungwa Scarp Forest Reserve ZMUC R631269-70;

Kilanzi-Kitungulu Forest Reserve ZMUC R631244-45, R631252—

54, R631256. West Usambara Mountains: Mazumbai (ZMUC

R63963, R631129, R631135, R631137, R631140, R631142-3,

R631146—7, R631155).

Terminology follows B6hme (1988) and Ziegler & Bohme (1997).

Preparation of the hemipenes of specimens previously preserved in

alcohol was done according to the method described by Pesantes

(1994) and Ziegler & Bohme (1997).

RESULTS

Crotaphopeltis barotseensis (Fig. 1). In situ hemipenes extend to

subcaudal scute no. 7-8 (x=7.4, n=5) (Rasmussen, 1997). The only

known everted hemipenes of this species have been prepared from a

preserved specimen (ZMUC R631232). Consequently the organs

are somewhat wrinkled, hardened and not completely distended.

rm wey LUUL

Fig. 1 Crotaphopeltis barotseensis, right hemipenis in sulcal, left

hemipenis in asulcal view of ZMUC R631232.

Pedicel covered with tiny spines. Lower truncus covered with

several somewhat enlarged spines, the most conspicuous on each

side of the sulcus. Spines decrease in size towards the terminal

somewhat calyculate apex. Sulcus spermaticus unforked, leading

directly to the apex.

Crotaphopeltis braestrupi (Fig. 2). In situ hemipenes extend to

subcaudal scute no. 15—23 (x=18.4, n=61) and may be twice as long

as in sympatric C. hotamboeia (Rasmussen, 1985). This distinctive

difference is not reflected in the everted organs; however, the

hemipenes of the present specimens (CAS 153370, 153379) are not

entirely everted.

Pedicel covered with tiny spines except for a longitudinal depres-

sion on the outer asulcate surface that extends from the base of the

pedicel to the lower truncus. Lower truncus covered with two to

three slightly enlarged spines, one on either side of the sulcus and a

less conspicuous one on the asulcate surface. Spines decrease in size

towards the terminal somewhat calyculate apex. Sulcus spermaticus

unforked, leading directly to the apex.

Crotaphopeltis degeni (Fig. 3). In situ hemipenes extend to subcaudal

scute no. 7-11 (x=8.4, n=35) (Rasmussen, 1997; Rasmussen ef al.,

2000).

T. ZIEGLER AND J.B. RASMUSSEN

Fig. 2 Crotaphopeltis braestrupi, asulcal view of right hemipenis of

CAS 153379.

Fig. 3 Crotaphopeltis degeni, asulcal view of hemipenes of ZMUC

R631621.

HEMIPENIAL VARIATION IN CROTAPHOPELTIS

In the specimens from Minziro Forest, Tanzania, with freshly but

not completely everted hemipenes (ZMUC R631598, R631610,

R631618, R631621) superficial genital morphology is as follows:

Pedicel covered with tiny spines. Lower truncus somewhat con-

stricted and with two distinctly enlarged spines: one outside the

sulcus spermaticus and another on the inner truncal surface. Re-

maining spines slightly decreasing in size towards the apex. Sulcus

unforked, running directly to the apex.

In the specimen from Lake Rukwa, Tanzania (ZMUC R631233)

the right hemipenis was everted after fixation. The somewhat wrin-

kled, hardened and incompletely distended organ bears scarcely

detectable, slightly enlarged spines on the lower truncus. In this

specimen the sulcus is unforked, running directly to the apex, ending

in a terminal extension. Tip of apex calyculate.

Incontrast, in the incompletely everted hemipenes of the two speci-

mens of Crotaphopeltis degeni from Sudan (RMNH 24411, 25018)

the lower truncus bears a ring of several distinctly enlarged spines.

In the uneverted hemipenes of specimens from Ethiopia (USNM

24389), Uganda (BMNH 1984.883) and Cameroon (RGMC 73-15-

R209) clearly enlarged lower truncal spines are discernible.

Crotaphopeltis hippocrepis (Fig. 4). In situ the hemipenes extend to

subcaudal scute no. 8—12 (x= 10.1, n= 38) (Rasmussen et al., 2000).

Pedicel covered with tiny spines except for a longitudinal depres-

sion on the asulcate surface. Lower truncus with two distinctly

Fig. 4 Crotaphopeltis hippocrepis, sulcal view of left hemipenis of

ZFMK 63877.

Fig.5 Crotaphopeltis hotamboeia, asulcal view of hemipenes of ZMUC

R631177.

Fig. 6 Crotaphopeltis hotamboeia, asulcal view of hemipenes of ZMUC

R631210.

enlarged spines on either side of the sulcus (ZFMK 63875, 63877,

ZMUC R631238), each followed above by several (usually 1-3)

enlarged spines, apically decreasing in size (see also Rasmussen et

al., 2000: fig. 3). Even in the only basally everted hemipenes of

ZFMK 63775 and ZFMK 63880 these enlarged spines are easily

recognizable. The remaining spines of truncus and apex are me-

dium-sized, decreasing in size towards the apex which is calyculated

terminally. Unforked sulcus spermaticus leading directly towards

the apex, ending in a terminal extension.

Crotaphopeltis hotamboeia (Figs 5,6). In situ hemipenes extend to

subcaudal scute no. 7-14 (x=10.1, n=308).

Pedicel of the hemipenis of C. hotamboeia covered with tiny spines

except for a longitudinal depression on the asulcate surface. Lower

truncus with three distinctly enlarged spines, one on each side of the

sulcus, the third on the asulcate surface (ZFMK 63874, ZMUC

R63889, R63979-80, R631177, R631264, 631266, R631268). Even

in the only basally everted hemipenes of ZMUC R63894, R63984,

and R631072 these three enlarged spines are also easily detectable.

Distal to the three enlarged spines the hemipenis is covered with

medium-sized spines decreasing in size towards the apex. The very tip

of the apex seems to be somewhat calyculate. Unforked sulcus is

leading directly to the apex ending in a terminal extension.

Fig. 7 Crotaphopeltis tornieri, asulcal view of hemipenes of ZMUC

R631147.

Contrary to this condition the hemipenes of ZMUC R631205-6

and R631208—-10 (Msolwa area, Rubeho Mts., Tanzania) have, in

addition to the three enlarged spines, a ring consisting of variously

enlarged spines on the asulcate surface of the middle truncus. A

similar condition was found in the hemipenes of ZMUC R63921

(Magombero Forest, ca. 50 km S Mikumi, Tanzania).

Crotaphopeltis tornieri (Fig. 7). In situ hemipenes extend to

subcaudal scute no. 7—11 (x=8.4, n=27) (Rasmussen, 1993a; unpubl.).

The pedicel of the hemipenis of C. tornieri is covered with tiny

spines except for a longitudinal depression on the asulcate surface.

Lower truncus usually with some enlarged spines. Distal to the

enlarged spines, the spines become smaller towards the apex, which

is terminally calyculate. Sulcus spermaticus is not forked and leads

directly to the apex ending in a terminal extension.

In specimens from East and West Usambara Mountains the largest

spine is on the outside of the lower truncus, the second largest on the

asulcate surface. The spine ornamentation of the hemipenes of the

West Usambara population was somewhat variable, in the hemipenes

of ZMUC R63963 (Rasmussen, 1993: fig. 2) no distinctly enlarged

spine could be found on the asulcate surface.

In some specimens (ZMUC R63 1245 and R631252) from Kilanzi-

Kitungulu Forest Reserve, Udzungwa Mountains, the enlarged spine

on the outside of the lower truncus is relatively small; furthermore

an enlarged spine on the asulcate surface is scarcely detectable. In

other specimens (ZMUC R631244, R631253—4 and R631256) from

the same area, various enlarged spines are present on the lower

truncus.

In specimens from Kihanga River, Udzungwa Scarp Forest Re-

serve (ZMUC 631269-70) and from Rungwe Mission, Mount

Rungwe (ZMUC 631257), only the enlarged spine on the outside of

T. ZIEGLER AND J.B. RASMUSSEN

the lower truncus is easily seen. On the asulcate surface some

enlarged spines are present.

DISCUSSION

The hemipenial structures of Crotaphopeltis share several characters,

e.g., pedicel largely covered with tiny spines, lower truncus with

enlarged spines, spines decrease in size distally, apex calyculate,

sulcus spermaticus unforked and leading directly to the apex. Regard-

ing the simple and stout to elongate hemipenes within Crotaphopeltis,

principally the differences in ornamentation of the (lower) truncus

seem to offer a clue as to separate these taxa, in spite of the relatively

large interspecific variation displayed.

Crotaphopeltis barotseensis principally has one moderate en-

larged spine on each side of the sulcus in the hemipenes of the single

specimen examined. The species has a restricted distribution in

Central Southern Africa and is easily distinguished from sympatric

C. hotamboeia by general morphology (Rasmussen, 1985) as well

as hemipenial morphology.

Hemipenes of Crotaphopeltis braestrupi have two to three slightly

enlarged spines on the truncus, one on each side of the sulcus and an

inconspicuous one on the asulcate side. Comparing the hemipenes

of C. braestrupi with those of sympatric C. hotamboeia from Kenya

and Somalia, Rasmussen (1985) stated: ‘The ornamentation is also

very different. In C. braestrupi the hemipenis is covered with

slender spines, of which three are somewhat enlarged. In C.

hotamboeia the hemipenis is covered with stout spines of which

three basal ones are strongly enlarged (Rasmussen, 1985: fig. 9).” It

is difficult to judge the form of the variable spines (slender versus

stout), which depend on the condition and the method of preparation

of the hemipenes, but the three distinctly enlarged spines on the

lower truncus are nonetheless characteristic of the hemipenes of C.

hotamboeia across its entire distribution, i.e., Sub-Saharan Africa.

Further studies are needed to show whether a separate taxon is

justified for the specimens from Msolwa and Magombero Forest in

Tanzania which, in addition to the three enlarged spines, have a ring

consisting of some distinctly enlarged spines on the asulcate side of

the hemipenes. External morphological investigations so far do not

support such an assumption (Rasmussen, in prep.).

The hemipenes of Crotaphopeltis degeni usually bear two (speci-

mens from Tanzania) to several enlarged truncal spines (specimens

from Cameroon, Ethiopia, Sudan, Uganda). Concerning the truncal

spines of the hemipenes of Crotaphopeltis degeni from Sudan

Rasmussen (1997) stated, ‘up to six enlarged, stout spines, one each

side of the sulcus and two to four (usually three) more or less

enlarged spines on the asulcate aspect of the organ’. The lower

truncal spines of the hemipenis of a specimen from Lake Rukwa,

Tanzania appear only slightly enlarged, most probably due to ever-

sion after fixation. Rasmussen (1997) observed only two enlarged,

proximal spines in the incompletely everted hemipenes of speci-

mens from Kenya and Uganda. Crotaphopeltis degeni apparently

has a disjunct distribution like that of Causus resimus (Spawls and

Branch, 1995). Despite the intraspecific variation of this taxon it is

easily distinguished from sympatric C. hotamboeia and parapatric

C. hippocrepis by hemipenial morphology and as well as general

morphology (Rasmussen et al., 2000).

The hemipenes of Crotaphopeltis hippocrepis are characterized

by the possession of two distinctly enlarged spines, each followed

by arow of accessory spines decreasing in size apically. This unique

ornamentation of the hemipenes seems fairly constant within the

entire distribution area (West Africa) of C. hippocrepis and the

species seems to be homogeneous (Rasmussen ef al., 2000).

HEMIPENIAL VARIATION IN CROTAPHOPELTIS

In the northern part of its distribution (The Usambara Mountains)

the hemipenes of Crotaphopeltis tornieri usually have two slightly

enlarged spines, one on the outside of the truncus and one (rarely

missing) on the asulcate side. Based on external morphology,

Rasmussen (1993) found significant differences between the popul-

ations of C. tornieri from East and West Usambara Mountains. The

present results of the genital investigation do not lend support to the

recognition of different forms, nor do molecular (Gravlund, 2002) or

microdermatoglyphic (Berggreen, 1996) studies. Accordingly, the

differences found in numbers of ventral and caudal scutes between

these areas are probably due to genetic drift in small, isolated

populations.

Gravlund (2002) found significant differences between the mole-

cular composition of the northern and southern populations of C.

tornieri in the Eastern Arc. In particular, the population from the

Rungwe Mountains is very different molecularly from those of the

Udzungwa and the Usambara Mountains. The present study also

shows slight hemipenial differences between these populations. In

the hemipenes of the populations from Kihanga River (Udzungwa

Scarp Forest Reserve) and the Rungwe Mountains only the enlarged

spine on the outside of the truncus is visible. The picture, however,

becomes blurred as hemipenes of specimens from Kilanzi-Kitungulu

(Udzungwa Mountains) may have either a relatively small spine on

the outside and likewise on the asulcate side or various enlarged

spines on the truncus. Thus, the data on genital morphology indicate

that the spine ornamentation of the lower truncus in the hemipenes

of C. tornieri is variable even within single populations and with

current knowledge should not be used for defining different taxa

within the C. tornieri complex. This is in accordance with Berggreen

(1996) who found some microdermatoglyphic variation within and

between the various populations. The variation, however, was not

population specific. Crotaphopeltis tornieri (s.l.) is restricted to the

montane forest of the Eastern Arc of Tanzania and is easily distin-

guished from sympatric/parapatric C. hotamboeia from the lowland

savanna.

Thus, irrespective of the fact that intraspecific variation may

occur within the various species of Crotaphopeltis, the ornamenta-

tion of the lower truncus serves at least to distinguish between the

males of sympatric or parapatric species. The length at least of the

inverted hemipenes may also serve to distinguish between the

species and so may the unique rows of accessory spines in the

hemipenes of C. hippocrepis. Here, it is interesting to note, that the

pattern of the latter species is similar (Dowling, in litt.) to that of the

sister-genus Dipsadoboa (Rasmussen, 1979), which is also charac-

terized by similar, highly derived genital morphological features

(Rasmussen, 1993b).

ACKNOWLEDGEMENTS. For the loan and making available material for

examination we thank C. McCarthy (BMNH), R. Drewes (CAS), J. Rosado

(MCZ), D. Meirte (MRAC), M. Hoogmoed (RMNH), L. Ford (USNM), and

W. Bohme (ZFMK). We are grateful to B.T. Clarke and two anonymous

referees for commenting on the manuscript. Support for travel for the junior

author to Tervuren, Bonn, and London has been gratefully received from the

Danish National Research Council, Grant no. 56043.

REFERENCES

Berggreen, A. 1996. Microdermatoglyphics of snake scales. Unpublished Master’s

thesis, University of Copenhagen. 78p + 2 appendices.

Bohme, W. 1988. Zur Genitalmorphologie der Sauria: funktionelle und

stammesgeschichtliche Aspekte. Bonner zoologische Monographien 27: 1-176.

Graylund, P. 2002. Molecular phylogeny of Tornier’s cat snake (Crotaphopeltis

tornieri), endemic to East African mountain forests: biogeography, vicariance events

and problematic species boundaries. Journal of Zoological Systematics and Evolu-

tionary Research 40: 46-56.

Pesantes, O.S. 1994. A method for preparing the hemipenis of preserved snakes.

Journal of Herpetology 28: 93-95.

Rasmussen, J.B. 1979. An intergeneric analysis of some boigine snakes — Bogert’s

(1940) Group XIII and XIV (Boiginae, Serpentes). Videnskabelige Meddelelser fra

dansk Naturhistorisk Forening 141: 97-155.

1985. A new species of Crotaphopeltis from East Africa, with remarks on the

identity of Dipsas hippocrepis Reinhardt, 1843 (Serpentes: Boiginae). Steenstrupia

11: 113-129.

1993a. The current taxonomic status of Tornier’s cat-snake (Crotaphopeltis

tornieri). Amphibia-Reptilia 14: 395-409.

1993b. A taxonomic review of the Dipsadoboa unicolor complex, including a

phylogenetic analysis of the genus (Serpentes, Dipsadidae, Boiginae). Steenstrupia

19: 129-196.

— 1997. On two little known African water snakes (Crotaphopeltis degeni and C.

barotseensis). Amphibia-Reptilia 18: 191-206.

——,, Chirio, L., & Ineich, I. 2000. The Herald Snakes (Crotaphopeltis) of the Central

African Republic, including a systematic review of C. hippocrepis. Zoosystema 22:

585-600.

Spawls, S. & Branch, B. 1995. The dangerous snakes of Africa. Natural History:

Species Directory: Venoms and Snakebite. 192p. Blandford, London.

Ziegler, T. & Bohme, W. 1997. Genitalstrukturen und Paarungsbiologie bei squamaten

Reptilien, speziell den Platynota, mit Bemerkungen zur Systematik. Mertensiella,

Rheinbach 8: 1—207.

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Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 57-74

Issued 28 November 2002

Review of the Dispholidini, with the

description of a new genus and species from

Tanzania (Serpentes, Colubridae)

D.G. BROADLEY

Research Associate, Natural History Museum of Zimbabwe, Bulawayo, Zimbabwe

Present address: Biodiversity Foundation for Africa, P.O. Box FM 730 Famona, Bulawayo, Zimbabwe. email:

broadley @ telconet.co.zw

V. WALLACH

Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, U.S.A. email:

vwallach@ oeb.harvard.edu

SYNOPSIS. The tribe Dispholidini (Bourgeois 1968) is reviewed, paying particular attention to dentition and visceral anatomy.

A new genus and species, Xyelodontophis uluguruensis, is described from the Uluguru Mountains in Tanzania. All five genera

have enlarged rear maxillary teeth. Thrasops seems to be basal, Rhamnophis shows the development of dagger-like teeth tapering

from base to tip, then the other three genera appear to radiate, with Xyelodontophis having more derived dagger teeth broadest

in the middle, while Dispholidus and Thelotornis seem to have independently developed enlarged grooved rear fangs.

Thrasops schmidti is recognised as a relict evolutionary species. No subspecies of Rhamnophis aethiopissa or Dispholidus

typus are recognised, but the population of Dispholidus on Pemba Island probably represents an undescribed species.

INTRODUCTION

From the time of Boulenger’s catalogues (1893-96), it was custom-

ary to separate the aglyphous colubrid snakes (subfamily Colubrinae)

from the opisthoglyphs (subfamily Dipsadomorphinae or Boiginae),

see for example Loveridge (1957) and FitzSimons (1962).

Bourgeois (1968) erected a subfamily Dispholidinae, including

the aglyphous genera Thrasops Hallowell 1857 and Rhamnophis

Giinther 1862, and the opisthoglyphous genera Dispholidus

Duvernoy 1832 and Thelotornis A. Smith 1849. Subsequent authors

have often treated Rhamnophis as a synonym of Thrasops (e.g.

Hughes & Barry, 1969; Pitman, 1974; Spawls, 1978; Hughes, 1983;

Trape & Roux-Estéve, 1995; Chippaux, 1999) and many have

considered these aglyphous snakes to be members of the tribe

Philothamnini (e.g. Dowling & Duellman, 1978).

During areview of the genus Thelotornis in East Africa (Broadley,

2001), a snake from montane forest on the summit of the Uluguru

Mountains was initially assumed to represent a new species. How-

ever, examination of its rear maxillary teeth showed that they were not

the anticipated grooved fangs, but distinctive curved dagger-shaped

teeth with sharp anterior and posterior ridges, which are widest

midway along the tooth. To determine the relationships of this strange

snake to the other taxa of the Dispholidini, its skull was prepared (after

examination of the dental gland) and compared with skulls of the other

genera. This prompted a review of the genera Thrasops and

Rhamnophis, which appear to represent basal taxa of the Dispholidini.

As the ‘Dagger-tooth Vine Snake’ of the Uluguru Mountains seems to

be transitional between Rhamnophis and Thelotornis, but cannot be

accommodated in any of the existing genera of the tribe Dispholidini,

it is proposed to erect a new genus and species for it. In external

appearance and scale counts it resembles Thelotornis, but it lacks the

distinctive horizontal key-hole shaped pupil of that genus.

Itis with pleasure that we dedicate this paper to Garth Underwood,

in recognition of the major contributions that he has made to our

understanding of African snakes.

MATERIALS AND METHODS

This study is largely based on material available in the Natural

History Museum of Zimbabwe and the Museum of Comparative

Zoology, Harvard, with additional data derived from the literature.

Unfortunately the collections in the Natural History Museum were

not accessible. Loveridge’s 1944 revisions of Thrasops, Rhamnophis

and Thelotornis were based largely on scalation, supplemented by

maxillary tooth counts and coloration of head and neck in the case of

Thelotornis. We have emphasised the morphology of the rear max-

illary teeth and skull, and have also used data from the visceral

anatomy, using the Philothamnini as the outgroup for comparative

purposes. Data for good series of Philothamnus angolensis,

Hapsidophrys lineatus and H. smaragdina were available [Broadley

(1966) provisionally synonymised Gastropyxis Cope 1860 with

Hapsidophrys Fischer 1856, and this move is supported by the

visceral data]. In the species accounts we have only presented

chresonymies, full synonymies are included in the review of the East

African Thelotornis (Broadley, 2001) and investigation of the vari-

ation in the wide-ranging genus Dispholidus awaits future workers!

In the description of the visceral anatomy, the mean value for most

characters as % snout-vent length (SVL) is presented first, followed

parenthetically by the range or midpoint (MP) value. When only the

name of an organ is given, the value represents its length. Ratios of

two visceral characters are presented in fractional notation. When

only one value is given for a character, it is identical in the two

specimens or differs by less than 0.1%.

The position of the umbilicus is determined by the most anterior

ventral bearing a scar (the scar usually covers three ventrals and the

umbilicus exited through the medial scute). The umbilical scar-vent

interval is calculated by dividing the number of ventrals from the

scar to the vent by the total number of ventral scutes.

Material for which skulls or viscera were examined is listed in

appendices. Institutional abbreviations follow Leviton et al. (1985),

with the addition of:

IRSL = Instituit d’Rechereche Scientifique, Lwiro, Democratic

Republic of Congo (DRC); UNAZA = Université National du Zaire,

Kisangani, DRC; VW = Van Wallach dissection number (museum

deposition of specimen unknown).

CHARACTER ANALYSIS

1. Rear maxillary teeth. The three rear maxillary teeth of Thrasops

flavigularis (type species) and T: jacksonii are enlarged and sepa-

rated from the small anterior teeth by a diastema, they taper from

base to tip and have slight ridges anteriorly and posteriorly (Fig. 1A,

Group B dentition of Jackson & Fritts, 1995). The posterior ridge

becomes blade-like in some genera, e.g. Heterodon (Kardong, 1979),

Thamnophis (Wright, et al., 1979) and Stegonotus (Jackson & Fritts,

O95):

The same teeth in Rhamnophis aethiopissa (Fig. 1B) and R. batesi

(Fig. 1C) are curved, with sharp anterior and posterior ridges, but not

nearly as well developed as in the ‘Dagger-tooth Vine Snake’ of the

Uluguru Mountains, in which the ridges are broadest midway along

the tooth, which is leaf-shaped, narrowing at the base (Fig. 1F). In

Dispholidus and Thelotornis the three greatly enlarged rear maxil-

lary teeth are deeply grooved (Group D dentition of Jackson &

Fritts, 1995), but these genera retain a strong ridge on the anterior

face of the fangs. In Thelotornis, this ridge arises within the groove,

so that the venom canal is divided, before petering out well before

the fang tip (Fig. 1G, after Meier, 1981, fig 4). In Dispholidus on the

other hand, the ridge runs along the anterior edge of the groove (Fig.

1H, after Meier, 1981, fig 2).

With regard to number of maxillary teeth, Rhamnophis aethiopissa

(16 to 20 + 3) resembles Thrasops spp. (17 to 18 + 3), but R. batesi

(30 to 35 + 3, Fig. 1C) is divergent in this respect. The Dagger-tooth

Vine Snake has 14 + 3, thus matching Thelotornis (11 to 16 + II) in

actual tooth number. Dispholidus shows a marked reduction in

number of anterior teeth to 4 to 8 + II. Counts of maxillary tooth

sockets are much higher in the Philothamnini: 17-48 in Philothamnus

and 20-33 in Hapsidophrys.

2. Dental (Duvernoys’) gland. This gland is small in Thrasops and

Rhamnophis (Kochva, 1978), larger in Thelotornis (but smaller than

the orbit), still larger in the Dagger-tooth Vine Snake (subequal to

the orbit) and reaches its maximum development in Dispholidus

(Kochva, 1978), with a large, purely serous, slightly branched,

tubuloacinous Duvernoy’s gland, the tubule walls highly folded,

increasing the storage space within the gland (Taub, 1967), thus

constituting a reservoir (Underwood, 1997). The mechanism of

delivery of toxic dental gland secretions by low pressure systems

has been demonstrated for Boiga irregularis (Kardong & Lavin-

Murcio, 1993) and is effective regardless whether or not the teeth are

grooved (Weinstein & Kardong, 1994).

3. Skull. The Dispholidini were first recognised (as a subfamily)

by Bourgeois (1968) on the basis of their similar skull morphology

(Fig. 2). She drew attention to the forked ectopterygoid, large optic

fenestra and interorbital vacuity (also noted by Underwood, 1967).

The ectopterygoid is shallowly forked in Thrasops, Thelotornis and

the Dagger-tooth Vine Snake, but is very deeply forked in both

species of Rhamnophis and in Dispholidus. Underwood (1967)

noted the absence of a Vidian canal in the skulls of Thrasops and

Thelotornis, but Vaeth (1982) found a short, but distinct, Vidian

canal in the skulls of three Thrasops jacksonii.

4. Pupil shape. The pupil is round in Thrasops and Rhamnophis

(Fig. 3) as in the Philothamnini, but in Dispholidus and the Dagger-

D.G. BROADLEY AND V. WALLACH

tooth Vine Snake it may be more pear-shaped, due to an anterior

prolongation. Thelotornis is distinguished by its horizontal ‘key-

hole’ shaped pupil (Fig. 4B-D).

5. Visceral anatomy. The Dispholidini can be characterized by the

following visceral characteristics (Tables 2-4): umbilical scar-vent

interval 8—12% total ventrals; hyoid short with posterior tips at 7—

10% SVL, heart short,1.5—3.1% (mean 2.4%); right systemic arch

reduced to 0.20—0.40 left systemic arch diameter; liver narrow with

midpoint at 43-46% SVL; gall bladder craniad of pancreas and

spleen; testes normally unipartite but occasional specimens with bi-

or tri-partite organs (the additional segments being small sections

separated from the main body either posteriorly or anteriorly);

kidneys compact but segmented (15-45 segments); no tracheal

lung; trachea with narrow, well-separated cartilages that lack free

tips, tracheal membrane expanded to 2.0-4.0 (mean = 2.9) times the

circumferential width of the rings; weak development of the cardiac

lung to midheart level; tracheal entry into right lung subterminal,

right lung with small anterior lobe and small orifice; right lung

elongate (69-70% SVL), extending to 94-97% body length, cranial

vascular portion 0.15—0.25 lung length, usually with midventral

avascular strip, caudal saccular portion long 0.75—0.85 lung length;

faveolar parenchyma arranged in 2-3 tiers with pattern of transverse

smooth muscle ribs enclosing rows of paired faveoli; semisaccular

portion of lung short (0.10—0.20 vascular lung length) with abrupt

termination of parenchyma along a transverse border.

The hemipenes of the genera Thrasops, Dispholidus and

Thelotornis appear to be similar, being simple, capitate, with an

undivided sulcus. There are large basal spines which diminish in size

distally and are replaced by calyces on the distal cap (Bogert, 1940).

The organs of the Dagger-tooth Vine Snake show little difference,

the nude basal portion has four large hooks, the medial portion is

spinose and the apical portion is calyculate. The hemipenes of

Rhamnophis have not yet been described.

6. Dorsal head coloration. The development of complex head

patterns may aid in species recognition. All four species of Thrasops

have the head uniform olive when subadult, eventually becoming

uniform black. Rhamnophis batesii has a uniform brown or black

head, while that of R. aethiopissa is green, with the shields margined

with black. A somewhat similar black vermiculation on a yellow or

green ground is found in males of some populations of Dispholidus

typus, but many have no colour pattern. The Dagger-tooth Vine

Snake has dark margins to the head shields and yellow labials. The

four species of Thelotornis can be distinguished by the colour

pattern of the head (Broadley, 2001). The top of the head is uniform

green in T. kirtlandii (Fig. 4B), T. usambaricus and some T.

mossambicanus, but blue-green with black and pink speckling in T-

capensis (Fig. 4D). The temporals are uniform green in T. kirtlandii

(Fig. 4B) and T. usambaricus, brown with black speckling in 7:

mossambicanus (Fig. 4C), and pink margined with black in T.

capensis (Fig. 4D). The supralabials are uniform or with faint green

or grey stippling in T. kirtlandii, but the other taxa have black spots,

usually including a speckled black triangle on the sixth labial.

7. Throat pattern. All members of the Dispholidini (and some

members of the Philothamnini) can inflate the throat in a threat

display, reaching its maximum development in Dispholidus.

Chippaux (1999, Pl. 17) illustrates this phenomenon in Thrasops

flavigularis, where the black dorsum contrasts with the pale throat,

but in T. jacksonii the throat often becomes entirely black.

Rhamnophis has the dark green dorsal scales bordered with black,

the throat is yellowish in R. batesii and green in R. aethiopissa.

Dispholidus comes in a wide range of colour patterns, but usually

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES 3/8)

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Smm

Fig. 1 Dentition: Left — maxillae of: A. Thrasops flavigularis; B. Rhamnophis aethiopissa; C. Rhamnophis batesii; D. Thelotornis kirtlandii; E.

Dispholidus typus. Right — teeth of: F. Xyelodontophis uluguruensis; G. Dispholidus typus; H. Thelotornis kirtlandii. (A, C, D, E after Chippaux, 1999; B

after Bourgeois, 1968; F, G, H after Meir, 1981).

20)

D.G. BROADLEY AND V. WALLACH

Fig. 2 Skulls of: A. Xyelodontophis uluguruensis; B. Thelotornis mossambicanus; C. Rhamnophis batesit; D. Dispholidus typus.

has a black spot on the side of the neck (Broadley, 1983, fig. 144), in

this species the inflation may extend half way down the body. The

inflated throat of Thelotornis is grey-white with distinctive black

markings — crossbars in 7: kirtlandii, chevrons in T. usambaricus,

one or two elongate blotches in 7. mossambicanus and two larger

dorsally extensive blotches in T: capensis.

&. Temporals and occipitals. \n Thrasops there are almost invari-

ably 1 + 1 temporals and there are no enlarged occipital shields. In

Rhamnophis there is a single large temporal: R. batesii has four large

occipitals, while R. aethiopissa has two very large ones. In

Dispholidus, Thelotornis and the Dagger-tooth Vine Snake there are

usually 1 + 2 temporals and three occipitals (or two separated by a

smaller interoccipital). The Philothamnini tend to have more numer-

ous temporals (1 + 1 up to 2 + 2 + 2) and no enlarged occipitals.

9. Supralabials (Table 1). Thrasops usually has 8 supralabials, the

fourth and fifth entering the orbit. Rhamnophis batesii has 7 or 8, 4

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES

Note

Fig. 3 Head shields of: A. Thrasops flavigularis; B. Thrasops occidentalis, with midbody scalation to the right, compared with midbody scalation of T.

flavigularis on the far right (after Parker, 1940); C. Thrasops jacksonii; D. Rhamnophis aethiopissa; E. Rhamnophis batesii.

D.G. BROADLEY AND V. WALLACH

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Fig. 4 Head shields of: A. Xyelodontophis uluguruensis (holotype); B. Thelotornis kirtlandii, C. Thelotornis mossambicanus; D. Thelotornis capensis; E.

Dispholidus typus.

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES 63

Table 1 Dispholidini compared with Philothamnini: variation in midbody scale rows, ventrals, subcaudals and supralabials (rare variations in

parentheses).

Taxon midbody rows

Philothamnus spp.* (13) 15

Hapsidophrys spp.** 15

Thrasops flavigularis 13 (15)

Thrasops occidentalis 15 — 19 (21)

Thrasops jacksonii (17) 19 (21)

Thrasops schmidti (16) 17 (19)

Rhamnophis aethiopissa 15 — 17 (19)

Rhamnophis batesii 13

Xyelodontophis uluguruensis 19

Thelotornis kirtlandii 19

Thelotornis usambaricus 19

Thelotornis mossambicanus (17) 19 (23)

Thelotornis capensis 19

Dispholidus typus (17) 19 (21)

ventrals subcaudals supralabials [in orbit]

135-213 60-175 8/9 [4 to 6]

150-176 90-172 8/9 [4 to 6]

195-215 128-146 8 (9) [4,5 (5,6)]

175-187 119-140 8 (7) [4,5 (5,6)]

187-211 130-155 8 (9) [4,5 (5,6)]

168-184 121-149 8 [4,5]

154-179 117-159 6 — 9 [3,4; 4,5; 5,6]

163-179 91-114 7-8 [4,5; 5,6]

168-169 ? 8 [4,5]

162-189 139-161 8 (7, 9) [4,5 (5,6)]

156-169 151-175 8 (9) [4,5 (3,4,5)]

149-166 127-158 8 [4,5]

144-177 128-165 8 [4,5]

164-201 104-142+ * 7 (3,4)

*Data from Hughes (1985). **Data from Chippaux (1999). “168 in D. ‘pemba’ (MCZ 45587).

& 5 or5 & 6 entering orbit. The widespread R. aethiopissa is more

variable, 6 to 9 labials, often with 3 & 4 entering orbit in southern

and eastern populations. Thelotornis and the Dagger-tooth Vine

Snake usually have 8 (4 & 5) and Dispholidus 7 (3 & 4).

10. Dorsal scales (Table 1). In Thrasops the dorsals are smooth in

juveniles, the median rows keeled in adults, number of rows at

midbody varies from 13-15 in 7: flavigularis (which has the dorsals

twice as long as the ventrals) to 17—21 (usually 19) in 7. jacksonii. In

Rhamnophis the dorsals are smooth, with the vertebral row enlarged,

13 rows in R. batesii and 15-19 rows in R. aethiopissa. The dorsals

are feebly keeled and usually in 19 rows in Thelotornis and the

Dagger-tooth Vine Snake, while Dispholidus usually has 19 rows of

strongly keeled scales. In the Philothamnini there are usually 15

scale rows, which are usually smooth in Philothamnus, but keeled in

Hapsidophrys.

11. Ventral counts (Table 1). The highest counts are found in

Thrasops flavigularis and the lowest in Thelotornis capensis.

12. Subcaudal counts (Table 1). The lowest counts are found in

Rhamnophis batesii and some populations of Dispholidus typus,

while the highest are found in the two forest species of Thelotornis.

SYSTEMATIC ACCOUNT

Thrasops flavigularis (Hallowell)

Yellow-throated Bold-eyed Tree Snake

Dendrophis flavigularis Hallowell, 1852, Proc. Acad. nat. Sci.

Philadelphia: 205. Type locality: ‘Liberia’, later corrected to

Gabon.

Hapsidophrys niger Giinther, 1872, Ann. Mag. nat. Hist. (4) 9: 25.

Type locality: Gaboon.

Thrasops pustulatus Buchholz & Peters, 1875, Monatsh. Akad.

Wiss. Berlin: 199. Type locality: Mungo, Cameroon.

Thrasops flavigularis Bocage, 1895: 97; Bogert, 1940: 58; Loveridge,

1944: 132; Trape & Roux-Estéve, 1995: 40; Chippaux, 1999: 95.

Thrasops flavigularis flavigularis Stucki-Stirn, 1979: 319.

Thrasops flavigularis stirnensis Stucki-Stirn, 1979: 632.

DIAGNOsIS. Dorsal scales in 13-15 rows at midbody, the dorsals

much longer than the ventrals; ventrals 191-214; subcaudals 128—

146; usually 2 labials in contact with the lowest postocular; no

enlarged occipitals.

DESCRIPTION. Supralabials 8 (rarely 9), fourth & fifth (rarely fifth

& sixth) entering orbit; infralabials 9-12, the first 3-5 in contact

with anterior sublinguals; preoculars | or 2; postoculars 3 (rarely 2),

usually 2 labials in contact with the lowest; temporals | + 1; no

occipitals. Dorsals in 17-15-13, 17-13-11, 15-13-13, 15-13-11 or

13-13-11 rows, feebly keeled in adults; ventrals 191-214; cloacal

divided; subcaudals 128-146 pairs.

COLORATION IN LIFE. Subadults olive to dark brown above, head

uniform, body mottled with black and yellow, the black being on the

interstitial skin and bases of the scales, the yellow in the centres of

the scales, the yellow spots very pronounced on the tail. Chin and

throat yellow, rest of venter chequered black and yellow. Adults

usually uniform black above, venter blackish, but throat usually

yellow or brownish white.

SIzeE. Largest d (IFAN 687 — Sibiti, Congo-Brazzaville) 1514 +

586 = 2100 mm (Villiers, 1966); largest 2 (AMNH 50573 — Metet,

Cameroon) 1235 + 505 = 1740 mm (Bogert, 1940). Stucki-Stirn

(1979) gives the maximum length as 240 cm.

HABITAT. Lowland forest.

DISTRIBUTION. Southwestern Nigeria, Bioko Island, Cameroon,

Gabon, Congo-Brazzaville, extreme eastern Democratic Republic

of Congo and northwestern Angola (Fig. 5).

Thrasops occidentalis Parker

Western Bold-eyed Tree Snake

Thrasops occidentalis Parker, 1940, Ann. Mag. nat. Hist. (11) 5:

273, fig. 1 & 2a. Type locality: Axim, Gold Coast [= Ghana];

Loveridge, 1944: 131; Cansdale, 1961: 31, Pl. vi, fig. 11 & 12;

Hughes & Barry, 1969: 1018; Chippaux, 1999: 100.

DIAGNOSIS. Dorsal scales in 15—21 rows at midbody, the vertebral

row widened; ventrals 175-187; subcaudals 119-140; 3 labials in

contact with lowest postocular.

DESCRIPTION. Supralabials 8 (rarely 7 or 9), the fourth & fifth

(rarely fifth & sixth) entering orbit; infralabials 8—10, the first 4—6 in

contact with anterior sublinguals; preocular 1; postoculars 3, 3

labials in contact with the lowest; temporals 1 + 1; no occipitals.

Dorsals in 15—21 rows at midbody, the median rows keeled in adults,

smooth in juveniles; ventrals 175-187; cloacal divided; subcaudals

119-140 pairs.

COLORATION IN LIFE. Juveniles with head and neck olive, body

chequered in black and yellow above and below. Adults black

above, chin and throat pale yellow, rest of venter dark olive.

SIZE. Largest d (BMNH 66.1.28.6 — Sierra Leone, paratype) 670

+ 495 = 1165 mm; largest 2 (BMNH 1911.6.30.2 — Axim, Ghana,

holotype) 682 + 403 = 1085 mm. Cansdale (1961) states that this

species can exceed 210 cm.

HABITAT. Lowland forest.

DISTRIBUTION. Guinea east to southwestern Nigeria (Fig. 5).

Thrasops jacksonii Giinther

Jackson’s Bold-eyed Tree Snake

Thrasops Jacksonii Giinther, 1895, Ann. Mag. nat. Hist. (6) 15: 528.

Type locality: Kavirondo, Kenya.

Rhamnophis jacksonii Boulenger, 1896: 632.

Thrasops Rothschildi Mocquard, 1905, Bull. Mus. natn. Hist. nat.

11: 287. Type locality: ‘Afrique orientale anglaise’.

Thrasops jacksonii jacksonii Loveridge, 1936: 249, 1944: 134 &

1957: 264; Bogert, 1940: 58; Witte, 1953: 200; Laurent, 1956:

187, 354 & 1960: 46; Roux-Estéve, 1965: 66, fig. 17; Villiers,

1966: 1739; Bourgeois, 1968: 124, 278, fig. 51; Pitman, 1974: 99,

Pl. G, fig. 4; Spawls, 1978: 5; Broadley, 1991: 532; Hinkel, 1992:

319, Pl. 306; Trape & Roux-Estéve, 1995: 40.

DIAGNOSIS. Dorsal scales in 19 (very rarely 17 or 21) rows at

midbody; ventrals 187-214; cloacal divided; subcaudals 129-155;

usually two labials in contact with lowest postocular.

VARIATION. Supralabials 8 (rarely 9, very rarely 7), fourth and

fifth (rarely fifth and sixth) entering orbit; infralabials 9-13, the first

4—6 in contact with anterior sublinguals; preoculars 1—2 (rarely 3);

postoculars 3 (very rarely 2 or 4), usually 2 labials in contact with

lowest; temporals 1 + 1 (very rarely 1 + 2); no occipitals. Dorsals

keeled in 19 (very rarely 17 or 21) rows at midbody; ventrals 181—

214; cloacal divided; subcaudals 129-155 pairs.

COLORATION IN LIFE. Subadults dark olive above, mottled with

black and buff posteriorly, greenish yellow below, becoming cheq-

uered black and yellow posteriorly. Adults uniform black above and

below, or with the throat yellow or greyish. Iris of eye black.

SIZE. Largest 6 (AMNH 12288) 1320 + 580 = 1900 mm, largest 2

(AMNH 12290) 1550 + 610 = 2160 mm, both from the Ituri Forest,

Orientale Province, D.R.C. (Schmidt, 1923). Pitman (1974) puts the

maximum length at about 2300 mm.

HABITAT. Rain forest and gallery forests from about 200 m in the

lower Congo region to 2400 m on Mount Elgon (Pitman, 1974).

DISTRIBUTION. From the lower Congo, east through the Congo

basin to southern Central African Republic, southern Sudan, Uganda,

western Kenya and northwestern Zambia (Broadley, 1991) (Fig. 5).

Thrasops schmidti Loveridge

Schmidt’s Bold-eyed Tree Snake

Thrasops jacksonii schmidti Loveridge, 1936, Proc. biol. Soc. Wash-

ington 49: 63. Type locality: Meru Forest, Mount Kenya, Kenya;

1944: 137 & 1957: 264; Spawls, 1978: 5.

DIAGNOSIS. Dorsal scales in 17 rows; ventrals 168—184; subcaudals

121-149; two labials in contact with lowest postocular.

DESCRIPTION. Supralabials 8, the fourth and fifth entering the

orbit; infralabials 10-12, the first 4 or 5 in contact with anterior

sublinguals; preocular 1; postoculars 3, the lowest in contact with 2

D.G. BROADLEY AND V. WALLACH

labials; temporals | + 1; no occipitals. Dorsals in 17 (rarely 19) rows

at midbody, faintly keeled; ventrals 172-184; cloacal divided;

subcaudals 121-147 pairs.

COLORATION IN LIFE. Subadult olive brown above, greyish white

below, subcaudals grey. Adults uniform black.

Size. Largest ¢ (MCZ 9276 — Meru Forest, Kenya, holotype) 700

+ 365 = 1065 mm; largest? (NMK 1222 — Embu Forest, Kenya)

1200 + 455 = 1655 mm; largest unsexed (formerly NMK — Muthaiga,

Nairobi, Kenya, paratype) 1671 +584 =2255 mm (Loveridge, 1923,

1936).

HABITAT. Montane forest.

DISTRIBUTION. Forests of the Kenya highlands from Mount Kenya

south to Nairobi (Fig. 5).

REMARKS. JT. schmidti is readily diagnosable on ventral counts

and is separated from the population of 7: jacksonii in the Kakamega

Forest by 300 km, including the dry rift valley, so it is considered to

represent an independently evolving taxon.

Rhamnophis aethiopissa Ginther

Splendid Dagger-tooth Tree Snake

Rhamnophis aethiopissa Ginther, 1862, Ann. Mag. nat. Hist. (3) 9:

129, Pl. x. Type locality: West Africa; Roux-Estéve, 1965: 65, fig.

16; Chippaux, 1999: 97.

Thrasops splendens Andersson, 1901, Bihang Till K. Svenska Vet.-

Akad. Handl. 27(5): 11, Pl. 1, fig. 8. Type localities: Bibundi &

Mapanja, Cameroon.

Rhamnophis ituriensis Schmidt, 1923, Bull. Amer. Mus. nat. Hist.

49: 81, fig. 4. Type locality: Niapu, Belgian Congo [= D.R.C.];

Witte, 1941: 202.

Rhamnophis aethiopissa elgonensis Loveridge, 1929, Bull. U. S.

natn,. Mus. 151: 24. Type locality: Yala (= Lukosa) River at the

foot of Mount Elgon, Kenya; 1944: 129.

Rhamnophis aethiopissa aethiopissa Loveridge, 1944: 126; Perret,

1961: 136; Villiers, 1966: 1739; Stucki-Stirn, 1979: 335, figs.

Rhamnophis aethiopissa ituriensis Loveridge, 1944: 128; Laurent,

1956: 189, 355; 1960: 47 & 1964: 108; Bourgeois, 1968: 109, fig.

43-46; Broadley, 1991: 532.

Thrasops aethiopissa elgonensis Loveridge, 1957: 264; Pitman,

1974: 101, Pl. T, fig. 3; Spawls, 1978: 5.

Thrasops aethiopissa aethiopissa Hughes & Barry, 1969: 1018;

Trape & Roux-Estéve, 1995: 40.

Thrasops (Rhamnophis) aethiopissa Hinkel, 1992: 144, Pl. 130.

DIAGNOSIS. Dorsal scales in 15-17 (rarely 19) rows at midbody,

the vertebral row enlarged; ventrals 154-179; cloacal divided;

subcaudals 117—159; two or three labials in contact with the lowest

postocular; two large occipitals.

DESCRIPTION. Supralabials 6—9, the 3 & 4,4" & 5" or 5" & 6"

entering orbit; infralabials 7-11, the first 3—6 in contact with the

anterior sublinguals; preocular | (very rarely 2); postoculars 2—3

(very rarely 4); a single temporal; two large occipitals (one longitu-

dinally divided and the other semidivided in NMZB-UM 2548).

Dorsals smooth, or vertebral and paravertebral rows keeled (Perret,

1961) in 15-17 (very rarely 13 or 19) rows at midbody (usually 17

rows in West Africa, Cameroon, Gabon and Central African Repub-

lic, 15 rows elsewhere); ventrals 154-179; cloacal divided;

subcaudals 117-159 pairs, the lowest counts in Uganda and western

Kenya.

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES 65

THRASOPS

FLAVIGULARIS

OCCIDENTALIS

JACKSONII

SCHMIDT!

FLAVIGULARIS & JACKSONII

200 oO 200 400 800 = 800

RHAMNOPHIS

AETHIOPISSA

BATESII

AETHIOPISSA & BATESII

XYELEDONTOPHIS ULUGURUENSIS

200 ° 200 400 666cO (8c

1000' 1700 1400 1600 1800 2000 KILOMETRES

1000 1700 1400 1600 1800 2000 KHOMETAES

Fig.5 Distributions of the genera Thrasops (upper), Rhamnophis and Xyelodontophis (lower).

COLORATION IN LIFE. Above, head olive-brown, uniform or poste-

rior shields black-edged; body green with scales tipped or bordered

with black; tail black with a green stripe on each scale row. Chin and

throat yellow-green, rest of venter pale green, a dark median line on

the subcaudals.

SIZE. Largest d (MRAC 12257 — Kiroziret Forest, Kivu, D.R.C.)

948 + 509 = 1457 mm (Laurent, 1956); largest 2 (NHRM 1979 —

Bibindi, Cameroon, syntype of T. splendens) 950 + 520 = 1470 mm

(Andersson, 1901).

HABITAT. Rain forest and gallery forest from sea level up to 2000

metres.

DISTRIBUTION. Guinea east to the Democratic Republic of the

Congo, Rwanda, Uganda and western Kenya, south to northern

Angola and northwestern Zambia (Broadley, 1991) (Fig. 5)..

REMARKS. Roux-Esteve (1965) placed R. a. ituriensis in the syn-

onymy of the typical form and R. a. elgonensis hardly warrants

subspecific recognition. Both subspecies were based on variable

characters: the number of midbody scale rows, subcaudals and

supralabials, and there are no major breaks in the distribution of the

species.

Rhamnophis batesii (Boulenger)

Spotted Dagger-tooth Tree Snake

Thrasops batesii Boulenger, 1908, Ann. Mag. nat. Hist. (8) 2: 93.

Type localities: Akok and Efulen, Cameroon; Trape & Roux-

Esteve, 1995: 40; Chippaux, 1999: 99.

Rhamnophis batesii Schmidt, 1923: 83, fig. 5; Loveridge, 1944:

125; Laurent, 1956: 355, Pl. xx, fig. 1; Perret, 1961: 136; Villiers,

1966: 1739; Stucki-Stirn, 1979: 339.

DIAGNOSIS. Dorsal scales in 13 rows at midbody, vertebral row

enlarged; ventrals 163—179; cloacal entire; subcaudals 92-119; two

labials in contact with lowest postocular.

DESCRIPTION. Supralabials 7 (rarely 6 or 8), the fourth & fifth

(rarely third & fourth or fifth & sixth) entering orbit; infralabials 8 or

9, the first 4—6 in contact with anterior sublinguals; preocular 1

(rarely 2); postoculars 3 (rarely 2 or 4), 2 labials in contact with the

lowest; a single temporal; 4 occipitals (3 in MRAC 19070 due to

fusion of right hand pair; the median pair transversely divided in

NMZB 13206). Dorsals smooth in 13-13-11 or 13-13-9 rows, verte-

bral row enlarged; ventrals 163-179; cloacal entire; subcaudals

92-123 pairs.

COLORATION IN LIFE. Dorsum pale violet-brown, many scales

black at the base and along lower edge, giving a plaited effect to the

supracaudals. Chin and throat cream, rest of venter pale green, with

black labial sutures and numerous black spots or blotches on the

venter.

SIZE. Largest d (MCZ 38393 — Batouri District, Cameroon) 827 +

390 = 1217 mm; largest 2 (BMNH —) 1450 + 350 = 1800 mm.

HABITAT. Rain forest between 400 and 1000 metres.

DISTRIBUTION. Cameroon, Gabon and Congo-Brazzaville, east

through the Congo basin to the Orientale and Kivu Provinces of the

DD EREEH (ise)!

Xyelodontophis gen. nov.

DIAGNOSIS. A member of the tribe Dispholidini, differing from

the other genera in the development of strongly curved rear maxil-

lary teeth, which have sharp flanges anteriorly and posteriorly and

narrow at the base, hence the name Xyelodontophis = Dagger-tooth

Snake. Both species of Rhamnophis also have ‘dagger-shaped’ rear

maxillary teeth, but they are less well developed and the teeth taper

from base to tip, while Thelotornis and Dispholidus have large

deeply grooved rear fangs. The new genus agrees with Thrasops and

Thelotornis in having a shallowly forked ectopterygoid bone, whereas

Rhamnophis and Dispholidus have a deeply forked ectopterygoid.

In general form and scalation the new snake agrees with Thelotornis,

but it lacks the distinctive horizontal pupil of that genus.

D.G. BROADLEY AND V. WALLACH

Xyelodontophis uluguruensis sp. nov.

Dagger-tooth Vine Snake

HOLOTYPE. NMZB 7443 (Figs lf, 2a, & 4a) an adult female from

Lupanga Peak, Uluguru Mountains, Tanzania (06° 52' S: 37° 43' E),

collected by Jon Lovett in November, 1983 (KMH 2636). Named

for the Uluguru Mountains, to which it is probably endemic.

PARATYPE. ZMB 48153, an adult male from Bondwa Peak, Uluguru

Mountains (06° 54'S: 37° 40' E) at 1650 m, collected by D. Emmrich

(DE 413) in November, 1989.

DIAGNOsIs. As for Xyelodontophis gen. nov.

DESCRIPTION (paratype variations in parentheses). Rostral feebly

recurved onto upper surface of snout; very large nostril in a single

nasal; loreals 2; preocular 1; postoculars 3; temporals | + 3; a pair of

large occipitals behind the temporals, separated by elongate interpa-

rietal; supralabials 8, the fourth and fifth entering the orbit; infralabials

9, the first four or five in contact with the anterior sublinguals.

Dorsals elongate, narrow, in 21-19-13 rows, moderately to feebly

keeled, with single large apical pits; ventrals angular, but not keeled,

168 (169); cloacal longitudinally divided; subcaudals 132+ (18+),

tail truncated. The paratype male has an umbilical scar on ventrals

147-149.

COLORATION IN PRESERVATIVE. Top of head brown, shields nar-

rowly margined with black, labials, chin and throat immaculate.

Body grey-brown, bases of scales (and interstitial skin anteriorly)

black; venter uniform pale grey apart from some irregular brown

margins to the free edges of the ventrals. The paratype male has the

head and nape bronze, supralabials immaculate yellow, rest of

dorsum black speckled with green and brown in life (Emmrich, pers.

comm.); chin and throat yellow, rest of venter rapidly darkening to

black with a few light markings.

VISCERAL ANATOMY (Tables 2-4). Umbilical scar-vent interval

11.6% VS (10.7-12.5%); peritoneum black; hyoid posterior tip

7.8% (7.6-8.1%); heart short 2.3% (2.0-2.6%), midpoint 25.2%

(24.9-25.5%), junction of systemic arches ventrolateral and 0.71%

(0.69-0.74%) heart length posterior to heart, right arch 0.33 diameter

of left at junction; heart-liver gap 5.7% (5.5—5.9%), heart-liver

interval 35.8% (34.3-37.2%); liver long 27.8% (26.4—29.2%) and

narrow, midpoint 46.0% (45.7-46.2%), nearly contacting the gall

bladder (liver-gall bladder gap 0.1% [0-—0.2%]); liver-gall bladder

interval 29.3% (28.3-30.4%), liver-kidney gap 28.0% (27.6-28.4%),

liver-kidney interval 65.5%, liver length/right lung length ratio

0.40; gall bladder 1.4% (1.2—1.6%), midpoint 60.7% (59.9-61.5%),

located anterior to the subequal pancreas 1.7% (1.5-1.9%) with

small spleen (0.7%) attached cranially; gall bladder-gonad gap

10.7% (9.7-11.8%), gall bladder-gonad interval 23.0% (22.8-

23.2%); gonads light yellow in color, right testis 4.8% (MP =

74.4%), left testis 4.1% (MP = 79.9%), total testis midpoint 77.4%;

right ovary 5.3% (MP = 74.9%) with 6 small ova and 7 follicles, left

ovary 4.9% (MP = 81.6%) with 5 small ova and 8 follicles, total

ovary midpoint 78.0%, total gonad midpoint 77.7%; gonad-kidney

gap 4.8% (4.4-5.3%); adrenal glands orange, very narrow and

elongate, adjacent to posterior end of gonads, right adrenal 2.3%

(2.2-2.5%), midpoint 75.4% (74.8-76.1%), left adrenal 2.6% (2.5—

2.7%), midpoint 81.6% (81.2—82.1%), total adrenal midpoint 78.5%

(78.4-78.6%); gall bladder-kidney gap 26.4% (26.3-26.5%), gall

bladder-kidney interval 37.5% (36.3-38.8%); kidneys dark brown,

segmented but compact with deep creases, right kidney 9.2% (8.0—

10.4%) with 20 segments, midpoint 92.4%, right kidney length/liver

length ratio 0.34; left kidney 7.0% (6.1—7.9%) with 21 segments,

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES 67

Table 2 Adult Dispholidini compared with Philothamnini: visceral characters as % snout-vent length

GS 1 U-V Hy HLG HLT L_ LMP LGBG LGBI GBMP GBGG GBKG TGMP GKI TA TAMP TMP RL PY LL

Pxeeeeaon 6. 7.3 29:0) 18:8 42:8 3:5 24.2 56.6 11.7 PE, To 23) 137 76:9) 95.5) 4

Five-O 4G) 910) 2910! 17.3) 45:6 1013’ — 293 65.3 10.1 20.2 US e221 14.6 76.1 98.1 1.4

omeeOm moss 14 8:8) 29'3° . 17.7 146.6, 5:6 ~ 29:5 66.2 17.0 22.1 S32 2010) 1:2 847 I510 784° 97.9 “0:8

SRO 7. 68-0. 29.2. 142 456 6.2 22:6 60.0 11.3 23.9 ie ORAS 17.9 WM5toy 68:4 Sia) 226

Miso 7.2 8 26 15.5 445. 77 20.0 52.6 9.8 23.4 TOM 26.3555.3)) ALO) SAG 1691S 196429

NOtmeeasas 6.7 99 260 140 43:9 7.5 23.0 592 8.8 25.1 76.1 28:2. 52:6" 47/5:8 9 145 P7ES S7iGr S38

sme 2 L057" 9.35 °26:97 14:8 44.8 9:0 2510 6l7 Ts 20.8 76.0 27.22 46 77.0 148 686 964 3.9

RA 12 74 102 74 27.1 174 440 53 244 58.8 12S Dik T2033. OG TAS GD 3a Oo Se alE2

Bee On 91958767 30:0! 20M 45.0 7A 284 62.8 13.4 23.6 79:6 204 29 804 143 714 977 14

Diemer 19:0) 7.3 29:0 19:0 44:1 7.2 27:5 61.7 7A 18.8 TiO Soe 2.9) 69H 42) 71055 96325

Dele On soe. 6:0) 30:2 21.7 429 S35 28.5 59:9 12.1 PAKS) (2a eco! 4.9 Sie) S-0OF le) eIOOr les

Gms 98:2 7.1) -31.9 22:3 442 7.8 31.8 64.0 8.2 18.6 ASG 23:4 30 TOOT SiG! ~ 70F S96 as

lomo 7.1 7.2 32.2 228 473 64 31:0 (66:5 10.5 21.6 C2 20:2 2-2 838:8% 15:2) (67:27 95-7" Well

WV oes «67.2 (69 636.306«—626.9 «845.7 45 33.3 64.6 9.3 193 S05 298 2s 86, SAN 72's) S969 IES

UR 72 "65° 340 255 449 60 332 64.5 10.5 20.8 805" 2058 “US sls 13:47) 7s 9610" 0

AUR no 7:8 5.7 35:8 27.8 46.0 01 293 60.7 10.7 26.4 Viel 25IA AIS T1855 11323 1686, 93:4. 1:4

(GS = genus/species: PA = Philothamnus angolensis, HL = Hapsidophrys lineatus, HS = Hapsidophrys smaragdinus, TF = Thrasops flavigularis, TJ = Thrasops jacksonii, TO

= Thrasops occidentalis, TS = Thrasops schmidti, RA = Rhamnophis aethiopissa, RB = Rhamnophis batesii; DT = Dispholidus typus, DP = Dispholidus ‘pemba’, TC =

Thelotornis capensis, TK = Thelotornis kirtlandii, TM = Thelotornis mossambicanus, TU = Thelotornis usambaricus, XU = Xyelodontophis uluguruensis; n = sample size, UV

= umbilical scar to vent as % total ventrals, Hy = hyoid posterior tip, HLG = heart-liver gap, HLI = heart-liver interval, L = liver length, LMP = liver midpoint, LGBG = liver-

gall bladder gap, LGBI = liver-gall bladder interval, GBMP = gall bladder midpoint, GBGG = gall bladder-gonad gap, GBKG = gall bladder-kidney gap, TGMP = total gonad

midpint, GKI = gonad-kidney interval, TA = total adrenal length, TAMP = total adrenal midpoint, TMP = trachea midpoint, RL = right lung length, PT = right lung posterior

tip, LL = left lung length).

Table 3. Adult Dispholidini compared with Philothamnini: visceral characters as ratios

GS R/LSA K/L RK/L LK/RK KOL NTR AL/LL RB/LL LB SS/DV V/S LL/RL LW/LL

PA 0.39 0.39 0.37 0.83 0.76 72 0.54 1.00 2.83 0.19 0.18 0.02 0.42

HL 0.36 0.68 0.67 0.83 0.80 75 - 0.41 0.53 0.14 0.17 0.02 0.30

HS 0.39 0.49 0.47 0.85 0.77 101 - 0.23 0.56 0.13 0.16 0.01 0.42

te 0.33 0.88 0.66 0.83 0.38 90 0.31 0.13 0.60 0.09 0.25 0.04 0.21

TJ 0.41 0.70 0.57 0.75 0.40 92 0.36 0.21 0.67 0.10 0.23 0.04 0.22

TO 0.37 0.86 0.71 0.75 0.45 120 0.24 0.10 0 0.11 0.24 0.08 0.13

TS 0.20 0.93 0.82 0.78 0.50 89 0.13 0.11 0.50 0.10 0.26 0.06 0.29

RA 0.29 0.48 0.50 0.69 0.48 76 0.87 0,24 1.45 0.10 0.16 0.02 0.26

RB 0.22 0.48 0.46 0.81 0.76 We) 1.00 0.19 1.67 0.13 0.15 0.02 0.35

DT 0.24 0.65 0.54 0.78 0.36 72 0.76 0.80 1.29 0.17 0.20 0.03 0.29

DP 0.25 0.41 0.33 0.74 0.40 oF 0.90 0.21 4.00 0.21 0.15 0.02 0.30

AKG 0.32 0.59 0.50 0.68 0.52 71 0.57 0.21 1.00 0.13 0.15 0.02 0,28

TK 0.26 0.37 0.37 0.74 0.55 75 0.54 0.19 Peal 0.14 0.15 0.01 0.25

TM 0.31 0.45 0.41 0.72 0.57 76 0.68 0.20 2.19 0.16 0.14 0.02 0.24

TU 0.38 0.43 0.39 0.79 0.63 71 0.79 0.17 3.00 0.14 0.12 0.01 0.39

XU 0.33 0.35 0.34 0.76 0.67 si?) 0.83 0.42 1.00 0.39 0.13 0.02 0.20

(genus/species acronyms as for Table 2, R/LSA = right systemic arch diameter/left systemic arch diameter, K/L = total kidney length/liver length, RK/L = right kidney length/

liver length, RA/RK = right adrenal length/right kidney length, LK/RK = left kidney length/right kidney length, KOL = kidney overlap/total kidney length, NTR = estimated

number of tracheal rings/10% SVL, AL/LL = anterior lobe length/left lung length, RB/LL = right bronchus length/left lung length, LB = mean number of cartilages in left

bronchus (including bronchial ring), SS/DV = semisaccular lung/dense vascular lung, V/S = vascular lung/saccular lung, LL/RL = left lung length/right lung length, LW/LL =

left lung width/left lung length).

midpoint 94.0%, left kidney length/liver length ratio 0.26; left

kidney/right kidney 0.76, kidney overlap 0.67; kidney-vent interval

12.2% (11.6-12.8%), kidney-vent gap 2.5% (2.1-2.9%).

Trachea 25.1% (25.0—25.2%) with an estimated 149 rings (144—

154) or 58.9 (58.6-59.2) per 10% SVL, trachea midpoint 13.8%

(13.7-13.9%), tracheal rings narrow and well-separated from their

neighbours, lacking free tips, tracheal membrane expanded to 3.5

times the tracheal ring circumference; tracheal lung lacking, only

slight development of a cardiac lung (0.7%) anterior to the right

lung; tracheal entry into right lung subterminal; right bronchus 0.3%

with 3 cartilages; anterior lobe of right lung very short 1.0% (0.9-

1.2%), its connecting orifice of moderate diameter; right lung 68.6%

(66.0—71.2%), right lung midpoint 60.1% (59.1-61.2%), vascular

portion of right lung 8.0% (7.2-8.7%) with three tiers of faveoli

distributed dorsoventrally around inner lung circumference; vascular

lung lacking midventral avascular strip; faveolar pattern consists of

transverse ribs enclosing transverse rows of paired diamond-shaped

faveoli; vascular lung with semisaccular or sparse/dense vascular

portion ratio 0.39 (0.35-0.42); saccular (avascular) lung 59.6%

(58.0-61.3%), vascular lung/saccular lung ratio 0.13 (0.12-0.14),

posterior tip of lung 93.9% (91.7-96.2%).

Left lung complex consists of an orifice at 26.3% (26.2—26.5%),

a bronchus 0.1% with two rings in female (bronchus absent in male),

and a vestigial lung 1.4% (1.1—1.6%). The left lung, with a left lung/

right lung ratio of 0.02, supports a reticulated network of trabeculae

and has a width/length ratio of 0.20 (0.15—0.25).

Xyelodontophis, while resembling Thelotornis in external mor-

phology, is distinct from the latter genus in a number of internal

characters: heart-liver gap, heart-liver interval, liver length, gall

bladder midpoint, gall bladder-kidney gap, total gonad midpoint,

D.G. BROADLEY AND V. WALLACH

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REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES 69

gonad-kidney interval, total adrenal length and midpoint, adrenal/

kidney length ratio, total kidney/liver length ratio, number of tra-

cheal rings, right bronchus/left lung ratio, semisaccular/dense

vascular lung ratio, right lung posterior tip, left bronchus cartilages,

and left lung width/length ratio. Xyelodontophis is also unique in

differing from the rest of the Dispholidini in the means of the

following characters: heart-liver interval, liver length, liver mid-

point, liver-gall bladder gap, total gonad length, liver-kidney interval,

gall bladder-kidney gap, total gonad length, right kidney and total

kidney/liver length ratios, number of tracheal rings, semisaccular/

dense vascular lung ratio, lack of ventral avascular strip in vascular

lung, liver/right lung length ratio, and posterior tip of right lung.

In contrast to other Dispholidini, Xyelodontophis is most similar

to Thelotornis in hyoid length, liver-gall bladder interval, and

trachea midpoint; it is most similar to Rhamnophis and Thelotornis

in total kidney midpoint, kidney-vent interval, and left lung length;

it is most similar to Dispholidus, Rhamnophis and Thelotornis in

total gonad midpoint; and it is most similar to Dispholidus in total

adrenal length and adrenal/kidney length ratios.

HEMIPENIS. In the paratype male the single organs extend to the

seventh subcaudal, the sulcus spermaticus is simple (on the left

organ the sulcus lies on the medial side, on the right organ it lies on

the lateral surface). In situ, the basal portion (2 subcaudals) is nude

with four large hooks, the medial portion (2 sc) is spinose and the

apical portion (2 sc) is calyculate. The sulcus is bordered by two

basal hooks 5 mm long and the two largest hooks (7 mm) are on the

asulcate side. The calyces on the apex are smooth and form a

network (with 1-2 mm cavities) very similar to the faveoli of the

snake lung. The proximal 24 calyces are spinose with several tiny

spinules on each calyx. The spines completely surround the organ

and are arranged in 7-8 rows, increasing in size from distal (4 rows,

1 mm long) through medial (3 rows, 2 mm) to proximal (1 row, 3

mm); there are 7 large spines on the right organ and 8 on the left. The

everted organ would probably show some resemblance to that of

Thelotornis kirtlandii (Doucet, 1963: Fig. 40).

SIZE. Length 740 + 407+ mm (snout-vent 830 mm, tail truncated

near base).

DiET. The holotype contained a recently swallowed leaf chame-

leon, Rhampholeon uluguruensis, an endemic species recently

described from Bondwa Peak (Tilbury & Emmrich, 1996).

HABITAT. Montane evergreen forest. The habitat is described by

Tilbury & Emmrich (1996).

DISTRIBUTION.

Ss)

Probably endemic to the Uluguru Mountains (Fig.

Thelotornis kirtlandii (Hallowell) Forest Vine Snake

Leptophis Kirtlandii Hallowell, 1844, Proc. Acad. nat. Sci. Phila-

delphia: 62. Type locality: Liberia, type ANSP 5271.

Oxybelis Lecomtei Duméril & Bibron, 1854, Erpét. Gen., 7: 821.

Type locality: Gabon.

Tragophis rufulus Duméril & Bibron, 1854, Erpét. Gen., 7: 827.

Type locality: Senegal.

Oxybelis violacea Fischer, 1856, Abhand. Nat. Ver. Hamburg, 3:91,

Pl. ii, fig. 7. Type locality: Edina, Grand Bassa County, Liberia.

Dryiophis Kirtlandii Bocage, 1895: 119 (part).

Thelotornis kirtlandii Schmidt, 1923: 112, Pl. xiv; Bogert, 1940: 69;

Witte, 1953: 247, fig. 82; Laurent, 1964: 116.

Thelotornis kirtlandii kirtlandii Loveridge, 1944: 149 (part).

DIAGNOsIS. Top of head, including temporal region, uniform green;

neck with black crossbands; supralabials immaculate or with fine

green or grey stipple; rostral and nasals strongly recurved onto top of

snout; infralabials 7-11 (mode 9); ventrals 162-189; subcaudals

132-172.

DESCRIPTION. Rostral and anterior nasals recurved onto top of

snout; a single loreal (in eastern populations); preocular 1; postoculars

3 (2 in two specimens from Digba through fusions with supraocular

or fifth labial) ; temporals 1+2 (very rarely 1+1 or 2+2); supralabials

8 (rarely 9 or 10), the fourth and fifth (rarely fifth and sixth) entering

the orbit: infralabials 7 to 11, the first 4 or 5 (very rarely 3) in contact

with the anterior sublinguals. Dorsal scales feebly keeled in 19-19-

13 rows (17 rows at midbody in four specimens from Kivu: Laurent,

1956, 1960); ventrals 164-179 in dd, 164-189 in 2°: cloacal divided;

subcaudals 135-157 in dd, 138-165 in22.

COLORATION. Top of head uniform green, supralabials white,

often with fine green or grey stipple; body mottled grey, green and

brown, with black crossbars anteriorly (ZMUC R631282 lacks

black markings on the neck), lighter below. The specimen illustrated

by Hinkel (1992: fig. 129) appears to be uniform dark brown on top

of the head, with heavy brown infuscation on the labials. This could

be a captive specimen that has been exposed to strong sunlight, such

a change has been observed in a captive Thelotornis at Watamu on

the Kenya coast (S. Spawls, pers comm.).

Size. Largest d (AMNH 12279 — Niangara, D.R.C.) 850 + 480 =

1330 mm, largest 2(ZMUC R631282 — Massisiswi, Udzungwa Mts,

Tanzania) 1050 + 660 = 1710 mm.

HABITAT. Lowland forest in west and central Africa, relict popul-

ations in montane forests in Tanzania.

DISTRIBUTION. Islands of the Bijagos Archipelago, Guinea Bissau,

east through forested areas of west Africa and the Congo basin to

Uganda and southern Sudan, south to northern Angola, northwest-

ern Zambia (Broadley, 1991) and south-central Tanzania (Rasmussen,

1997) (Fig. 6).

Thelotornis usambaricus Broadley Usambara Vine Snake

Thelotornis kirtlandii (not Hallowell) Stejneger, 1893: 733.

Thelotornis kirtlandii kirtlandii (not Hallowell) Loveridge, 1944:

149 (part).

Thelotornis capensis mossambicanus (not Bocage) Broadley, 1979:

126 (part); Rasmussen, 1997: 138 (part).

Thelotornis usambaricus Broadley, 2001, Afr. J. Herpetol. 50 (2):

58. Type locality: Amani Nature Reserve, (Kwamkoro/

Kwemsambia Forest Reserve), East Usambara Mountains, Tan-

zania. Holotype: NMZB 16182

DIAGNOSIS. Top of head, including temporal region, uniform green;

neck with black chevrons; supralabials with scattered black spots,

usually including a triangle on the sixth labial; rostral and nasals not,

or only feebly, recurved onto top of snout; infralabials 9-13 (mode

11); ventrals 145-169; subcaudals 143-175.

DESCRIPTION. Rostral just visible from above; nasal entire; loreals

1 or 2; preocular 1; postoculars 3; temporals 1 + 2 (very rarely 1 + 3);

occipitals 2, separated by a small interoccipital; supralabials 8 (very

rarely 9), the fourth and fifth or third, fourth and fifth entering the

orbit; infralabials 9 to 13, the first 4 or 5 in contact with the anterior

sublinguals. Dorsal scales very feebly keeled, in 19-19-13 or 19-19-

11 rows; ventrals 156-166 in dd, 145-169 in 2, cloacal divided;

paired subcaudals 146-175 in dd, 143-169 in2?.

COLORATION. ‘Top of head, including temporals, uniform green in

life, supralabials, chin and throat white or pale orange, with a few

black spots and usually a speckled black triangle extending back

from the eye through the lower postocular and sixth labial to the lip,

a few black spots on posterior sublinguals and gulars; dorsum

mottled brown, green and pale grey, three or four vague black

chevrons on neck (more distinct in subadults); venter mottled pale

brown and green.

SIZE. Largest 6 (BMNH 1974.547) 640 + 454 = 1094 mm;

largest (ZMUC R631310) 790 + 490 = 1280 mm, both from Amani.

HABITAT. Coastal forest.

DISTRIBUTION. The Usambara Mountains, with apparently relict

populations on the lower slopes of other isolated mountains in the

Eastern Arc chain and on the Kenya coast (Fig. 6).

Thelotornis mossambicanus (Bocage) Eastern Vine Snake

Oxybelis Lecomtei (not Duméril & Bibron) Peters, 1854: 623 (part).

Thelotornis Kirtlandii (not Hallowell) Peters, 1882: 131 (part), PI.

xix, fig. 2

Dryiophis Kirtlandii var. mossambicana Bocage, 1895, Herp. An-

gola & Congo: 119. Type locality: Manica, Mozambique.

Lectotype MBL 1843 (destroyed).

Thelotornis kirtlandti capensis (not A. Smith) Mertens, 1937: 14.

Thelotornis capensis (not A. Smith) Bogert, 1940: 70 (part), fig. 11.

Thelotornis capensis capensis (not A. Smith) Laurent, 1956: 230 &

378.

Thelotornis capensis mossambicanus Broadley, 1979: 129.

Thelotornis mossambicanus Broadley, 2001: 60.

DIAGNOSIS. Top of head green to pale brown, uniform or speckled

with black; temporals brown speckled with black; neck with black

lateral blotch; supralabials with scattered black spots, including a

triangle on the sixth labial; rostral and nasals not, or only feebly,

recurved onto top of snout; infralabials 9-13 (mode 11); ventrals

144-172; subcaudals 123-167.

DESCRIPTION. Rostral and nasals barely visible from above; loreals

usually 2 (rarely 1, very rarely 0 or 3); preocular 1; postoculars 3

(rarely 2 or 4); temporals 1 + 2 (very rarely 1 + 1, 1 + 3 or 2 + 2);

supralabials 8 (rarely 9, very rarely 6 or 7), the fourth and fifth

(rarely fifth and sixth, very rarely third and fourth, or third, or fifth

only) entering orbit; infralabials 9-13, mode 11, the first 4 or 5 in

contact with the anterior sublinguals; dorsal scales usually in 19-19-

11 or 19-19-13 rows, very rarely 17, 21 or 23 rows at midbody (23

recorded by Rasmussen, 1997); ventrals 144-168 in dd, 145-172

in 22; cloacal divided; subcaudals 131-167 in dd, 123-153 in2?.

COLORATION. Crown of head uniform green or with a black

speckled Y-shaped marking, or brownish, entirely speckled with

black (the two extremes may occur within a population, as on Mafia

Island); temporal region always brown, speckled with black;

supralabials white spotted with black, including a triangle on sixth

labial, chin and throat speckled with black; dorsum ash grey with

diagonal rows of whitish blotches and flecks of brown and pink or

orange, neck with one or two elongate black blotches; venter

greyish, streaked with brown.

SIZE. Largest d(MHNG 1376.34 —Newala, Tanzania) 910+ 525+

(tail truncated); largest 2 (NMZB-UM 4157 — Mutare, Zimbabwe)

895 +510 = 1405 mm, but MCZ 18476 from Zengeragusu, Tanza-

nia, has a snout-vent length of 920 mm (tail truncated).

HABITAT. Savanna and coastal forest.

DISTRIBUTION. Southern Somalia south to central Mozambique at

D.G. BROADLEY AND V. WALLACH

about 22°30' S, west to the shores of Lake Tanganyika, Malawi and

eastern Zimbabwe (Fig. 6).

Thelotornis capensis capensis A. Smith

Southeastern Savanna Vine Snake

Thelotornis capensis A. Smith, 1849, Ill. Zool. S. Africa, Rept. App.:

19. Type locality: ‘Kaffirland and the country towards Port

Natal’, i.e. Durban (type lost).

Thelotornis kirtlandii capensis Loveridge, 1944: 154 (part).

Thelotornis capensis capensis Broadley, 1979: 126.

DIAGNOsIS. Top of head blue-green with pink and black speckling

forming a ‘Y’ or ‘T’ marking, or speckling covering entire top of

head; temporals pink margined with black; neck with black lateral

blotches; supralabials with scattered black spots, including a trian-

gle on the sixth labial; rostral and nasals not, or only feebly, recurved

onto top of snout; infralabials 9-13 (mode 11); ventrals 144-164:

subcaudals 127-155.

DESCRIPTION. Rostral and nasals barely visible from above; loreals

usually 2 (rarely 1, very rarely 0 or 3); preocular 1; postoculars 3

(rarely 2 or 4); temporals 1 + 2 (very rarely 1 + 1 or 1 + 3);

supralabials 8 (very rarely 7 or 9), the fourth and fifth (very rarely

third & fourth, fifth & sixth or third, fourth and fifth) entering orbit;

infralabials 9-13, mode 11, the first 4 or 5 (very rarely 3 or 6) in

contact with anterior sublinguals; dorsal scales usually in 19-19-13

rows , rarely in 17 rows at midbody (15 rows only in TMP 45554):

ventrals 144-160 in dd, 148-162 in 2°: cloacal divided; subcaudals

133-155 in dd, 127-147 in2?

SIZE. Largest 6 (NMZB 6389 — Gwanda, Zimbabwe) 830 + 506 =

1336 mm; largest 2?(TMP 5615 — Hectorspruit, Mpumalanga, South

Africa) 911 + 455 = 1366 mm.

HABITAT. Savanna.

DISTRIBUTION. Southwestern Zimbabwe and southeastern Bot-

swana, south through the northern provinces of South Africa and

Swaziland to southern Mozambique and KwaZulu-Natal (Fig. 6).

Thelotornis capensis oatesii (Ginther)

Oates’ Savanna Vine Snake

Oxybelis Lecomtei (not Duméril & Bibron) Peters, 1854: 623 (part,

Tete).

Dryiophis oatesii Ginther, 1881, In Oates’ Matabeleland and the

Victoria Falls, App. : 330, Col. Pl. D. Type locality: Matabeleland

(= western Zimbabwe), type BMNH 1946.1.9.76.

Thelotornis Kirtlandii (not Hallowell) Peters, 1882: 131 (part).

Thelotornis kirtlandii capensis Loveridge, 1944: 154 (part).

Thelotornis capensis (not A. Smith) Witte, 1953: 249, fig. 82.

Thelotornis kirtlandii oatesii Loveridge, 1953: 277.

Thelotornis capensis oatesii Laurent, 1956: 231, fig. 35

DIAGNOSIS. Top of head blue-green with pink and black speckling

forming a ‘Y’ or “T’ marking; temporals pink margined with black;

neck with black lateral blotches; supralabials with scattered black

spots, including a triangle on the sixth labial; rostral and nasals not,

or only feebly, recurved onto top of snout; infralabials 9-13 (mode

11); ventrals 150-177; subcaudals 126-168.

DESCRIPTION. Rostral and nasals barely visible from above; loreals

usually 2 (rarely 1, very rarely 0); preocular 1; postoculars 3 (rarely

2, very rarely | or 4); temporals 1 + 2 (very rarely 1 + 3 or 1 + 1);

supralabials 8 (rarely 7, very rarely 9), the fourth and fifth (very

rarely third & fourth, fifth & sixth, third, fourth & fifth, or third, or

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES

12° 1

42° 48°

Fe eis

@ ss kirtlandii

18° O _usambaricus

® = mossambicanus

| Vs capensis

24°

| kirtlandii & mossambicanus

kirtlandii & capensis

usambaricus & mossambicanus

eas

mossambicanus & capensis

rien

o 12° 18°

2 30°

x ;

36° 42° 4g° 54° 60°

2 9 200 400 = 600, 8D 1000: 1700 1400 1800 1 KILOMETRES

| 24° 18° 12° 6° o

Fig. 6 Distribution of the genus Thelotornis.

fourth only) entering orbit; infralabials 9-13, mode 11, the first 4 or

5 (rarely 3) in contact with anterior sublinguals; dorsal scales

usually in 19-19-11 or 19-19-13 rows, very rarely 17 rows at

midbody; ventrals 150-177 in 6d, 153-177 in 22; cloacal divided;

subcaudals 132-173 in 6d, 126-168 in 9.

SIZE. Largest d (NMZB 3828 — Mtorashanga, Zimbabwe) 1062 +

620 = 1682 mm; largest 2(NMZB 3600 — Lake Kariba, Zimbabwe)

975 + 560 = 1535 mm, but NMZB-UM 1061 from Shurugwe,

Zimbabwe, has a snout-vent length of 1050 mm (tail truncated).

HABITAT. Savanna.

DISTRIBUTION. Southern Angola and northern Namibia, west

through northern Botswana, Zambia and southeast Katanga (D.R.C.)

to Zimbabwe, western Mozambique and Malawi (Fig. 6).

Dispholidus typus (A. Smith)

Bucephalus typus A. Smith, 1828, South African Commercial Ad-

vertiser 3 (144): 2, col. 4. Type locality: Eastern districts of South

Africa; 1829, Zool. Journ., 4: 441 (B. typicus).

Bucephalus Jardineti A. Smith, 1828, South African Commercial

Advertiser 3 (144): 2, col. 4. Type locality: Cape Town, South

Africa; 1829, Zool. Journ., 4: 422.

Bucephalus gutturalis A. Smith, 1828, South African Commercial

Advertiser 3 (144): 2, col. 4. Type locality: Forests of the eastern

districts of South Africa; 1829, Zool. Journ., 4: 442.

Bucephalus Bellii A. Smith, 1828, South African Commercial Ad-

vertiser 3 (144): 2, col. 4. Type locality: Eastern districts of South

Africa; 1829, Zool. Journ., 4: 442.

Dispholidus Lalandti Duvernoy, 1832, Ann. Sci. Nat. (Paris) 26:

150. Type locality: Cape of Good Hope.

Dendrophis colubrina Schlegel, 1837, Essai Phys. Serp. 2: 238, Pl.

ix, fig. 14-16. Type locality: Rondesbosch, [Western] Cape Prov-

ince, South Africa.

Bucephalus viridis A. Smith, 1838, Illus. Zool. S. Africa, Rept.: Pl.

iii. Type locality: Old Latakoo [Northern Cape Province], South

Africa.

Bucephalus capensis A. Smith, 1841, Illus. Zool. S. Africa, Rept.: Pl.

x-xill. Type locality: Cape Province, South Africa; Bocage,

1895: 121.

Dendrophis pseudodipsas Bianconi, 1848, Nuovi Ann. Sci.Nat. (2)

10: 108, Pl. iv, fig. 2 & 1850. Spec. Zool. Mosamb. 40, PI. iv, fig.

2. Type locality: [Inhambane] Mozambique. Holotype: Bologna

100296.

Thrasops jacksonii mossambicus Mertens, 1937, Abhand.

senckenberg. naturf. Ges., No. 435: 13. Type locality: Cheringoma

Farm, Inhaminga, Mozambique. Holotype SMF 22246.

Dispholidus typus kivuensis Laurent, 1955, Revue Zool. Bot. Afr. 51:

127. Type locality: Uvira, Kivu. Congo Belge [=D.R.C.]. Holotype

MRAC 17505.

Dispholidus typus punctatus Laurent, 1955, Revue Zool. Bot. Afr.

51: 129. Type locality: Dundo, Angola. Holotype MRAC 17395.

Dispholidus typus occidentalis Perret, 1961, Bull. Soc. neuchateloise

Sci. nat. 84: 138. Type locality: Cameroon, no type designated.

Boomslang

DIAGNOSIS. Dorsal scales strongly keeled in 19 (rarely 17 or 21)

rows at midbody; ventrals 164—201; anal divided; subcaudals 94—

142.

DESCRIPTION. Supralabials 7 (rarely 8 or 6), the third and fourth

(rarely 5'" & 6") entering orbit; lower labials 8-13, the first 3-6 in

contact with anterior sublinguals; preocular 1; postoculars 3 (very

rarely 2 or 4), the lower in contact with two labials; temporals 1 + 2

(very rarely 1 +1, 1 + 3,2 + 1, 2 + 2 or 2 +3); three enlarged

D.G. BROADLEY AND V. WALLACH

occipitals, the middle one subtriangular. Dorsals strongly keeled in

19 (rarely 17 or 21) rows; ventrals 164-201; cloacal divided;

subcaudals 94—142 pairs.

COLORATION IN LIFE. Juveniles are speckled dark grey-brown

above, with paired blue spots on some adjacent scales that become

visible when the skin is stretched, the lower scale rows are grey and

the venter is white, heavily stippled with dark red-brown. The head

is brown above, the labials and chin white, sometimes with some

black spots, and the throat is bright yellow. The iris of the eye is

bright green. The juvenile coloration is gradually lost as the snake

approaches one metre in length and there is great variation in adult

colour pattern.

Males are usually green, with or without black-edged scales,

females usually olive or brown above, paler below. This sexual

dimorphism in colour pattern does not always apply, for example

green females are not uncommon in Mozambique and KwaZulu-

Natal, while in southwestern Zimbabwe some males are olive-brown

above and duck-egg blue below. In East Africa a uniform black

phase may occur in either sex. In the Eastern Cape Province (the

‘type locality’) males are usually black above, each scale and head

shield with a green or yellow spot, venter yellow-green, each ventral

bordered with black, but in the southwestern Cape the dorsum is

uniform black and the venter yellow. In the western form described

as D. t. punctatus Laurent, the males are black above, each scale or

head shield with an orange spot, ventrals violet edged with black.

Females are usually red-brown above, paler below.

SIZE. Largest ¢ (NMZB 3947 — Mutoko, Zimbabwe) 1290 + 530

= 1820 mm; largest 2 (NMZB 3820 — Makote, Newala, Tanzania)

1447 + 475 = 1922 mm (tail tip truncated). C.J.P. lonides recorded a

brown male from Tanzania that measured 2134 mm (Pitman, 1974).

HABITAT. Savanna.

DISTRIBUTION. Senegal east to the Horn of Africa, south to the

southwestern Cape, excluding areas of rain forest, grassland and

desert.

REMARKS. The data for the solitary specimen examined from

Pemba Island, Tanzania (MCZ 45587), confirm the long held opin-

ion of Barry Hughes that this population is taxonomically distinct:

he will describe it when he has access to more material. The

subspecies described by Laurent (1955) were based on male colora-

tion and subcaudal counts, but there is clinal variation in both

characters. The species needs to be reviewed, using material from

throughout its extensive range.

Key to the genera and species of Dispholidini

la. Nasal divided; rear maxillary teeth not grooved ...............-:..:0+ 2

1b. Nasal entire; enlarged grooved fangs on posterior maxilla ......... 8

2a. Head elongate with two loreals in tandem; temporals 1+2; maxillary

teeth 17, the last three enlarged and dagger-shaped ...................4.

Tagua desSter situedoves/dsbsvbeien sesassbsseeee ouverts Xyelodontophis uluguruensis

2b. Head short with single loreal; temporals 1+1 or one only; maxillary

teeth 20-38, the last three enlarged ................:.:sscssssssseseessnseeseess 3

3a. Vertebral scale row enlarged; a single temporal; 2 or 4 enlarged

OGCCIPItALS =. we. foes enciseeseee cies eeseescupi ase snes izeses cones Soest eae eee 4

3b. Vertebral scale row not enlarged; 1+1 temporals; no enlarged

OCCUPA Siawh. 5. Le scedk Aa ceste csc caecnds Kontabhensstetistehshueneaee tees tee 5

4a. Cloacal shield entire; midbody scale rows 13; occipitals 4...........

Eason ne saeaae dedi encsvocestnuseuun te Sittaee seeohcee te teen eeneete cet Rhamnophis batesii

REVIEW OF DISPHOLIDINI WITH NEW TANZANIAN GENUS AND SPECIES 73

4b. Cloacal shield divided; midbody scale rows 15-19; occipitals 2

Boeet aasvaietnasiarecs Ceetangeead emtcernsac es vanes cctckccaes Rhamnophis aethiopissa

Sa. Dorsal scales twice as long as lower row of laterals and ventrals;

midbody scale rows 13 (rarely 15) .............. Thrasops flavigularis

5b. Dorsal scales subequal in length to the ventrals; midbody scale rows

UNRATED ID) Seeest eee senaq sect avo astica < Way acaba nsevansdectcvarasmunedescesetes as 6

6a. Three supralabials in contact with lower postocular ................00++

cot oS SOREEE ty SCE AES EP Pr CP CEP mereE REE PEE PEE Co eR Thrasops occidentalis

6b. Two supralabials in contact with lower postocular ................00+. 7

Ta.

7b. Midbody scale rows usually 17; ventrals 168-184 ........ cee

MMM ee NOG core dnrenedvacent svcnsereaqcevnsente Thrasops schmidti

8a. Head elongate; pupil horizontal, keyhole shaped; eight supralabials,

OMA CMTE CMCCLUNS OLD Ib. .......cecrerervscsnenceeuervospenncntsnnseatchivaces 9

8b. Head short; pupil round or pear-shaped; seven supralabials, third

BMA MOTE NtELUAPIOLDIE <.-2-.cecctscesencnucecsscracesueane Dispholidus typus

9a. Top of head, including temporal region, uniform green; black

crossbands or chevrons on neck; habitat forest ...........::ccce 10

Ob. Top of head uniform green or black speckled, temporal region

always brown, speckled with black, or pink, shields margined with

black; neck with black lateral blotches; habitat usually savanna

I Es Sara Lonn sachs p hs Spestc ani ndsch ies adunsndvoteennessaaezape (hl

10a. Rostral and nasals strongly recurved onto top of snout; infralabials

7-11, mode 9; supralabials immaculate or with fine green or grey

SUNT aparece ceepave. ven Wastlts soeisvlawc ces eanadiods avenue seustieaseavees T. kirtlandii

10b. Rostral and nasals not, or only slightly, recurved onto top of snout;

infralabials, 9-13, mode 11; supralabials with scattered black spots,

usually including a triangle on the sixth labial ...... T. usambaricus

Ila. Top of head bright green to pale brown, uniform or speckled

with black; temporals brown speckled with black ...........0....0+-

PREM e ei aehece cae ceiesrcreccuccstenetesstevesstegaetersssevnrs T. mossambicanus

11b. Top of head blue-green with pink and black speckling forming a *Y°

or “T’ marking, or speckling covering entire top of head; temporals

Penkemmansined With DLACK .cscc.c.acceveccvaenseuessandbencesesavens T. capensis

ACKNOWLEDGEMENTS. We are indebted to K.M. Howell (UDSM) for

donating the snake that becomes the holotype of Xyelodontophis uluguruensis.

VW wishes to particularly thank the following curators that permitted

dissection of material in their care: K.-S. Chifundera (IRSL), G. Lenglet

(IRSNB), J. Hanken and J.P. Rosado (MCZ) and R. Giinther (ZMB). DGB is

grateful to D. Rotich (NMK) for the loan of Thrasops schmidti material and

I. Ineich (MNHN), A. Resetar (FMNH), R. Giinther (ZMB) and G. Lenglet

(IRSNB) for printouts of their Dispholidini holdings.

REFERENCES

Bocage, J. V. Barboza du 1895. Herpétologie d’Angola et du Congo. xx + 203 pp.

Lisbonne: Imprimerie Nationale

Bogert, C. M. 1940. Herpetological results of the Vernay Angola Ezpedition, with

notes on African reptiles in other collections. Part I. Snakes, including an arrange-

ment of African Colubridae. Bulletin of the American Museum of Natural History 77:

1-107.

Boulenger, G. A. 1896. Catalogue of the snakes in the British Museum (Natural

History). 3: xiv + 727 pp.

Bourgeois, M. 1968. Contribution 4 la morphologie comparée du crane des ophidiens

del’ Afrique Centrale. Publications de I’ Université Officielle du Congo a Lubumbashi

18: 1-293.

Broadley, D. G. 1966. A review of the Natal green snake, Philothamnus natalensis (A.

Smith), with a description of a new subspecies. Annals of the Natal Museum 18 (2):

417-423.

1979. Problems presented by geographical variation in the African vine snakes of

the genus Thelotornis. South African Journal of Zoology 14: 125-131.

1983. FitzSimons’ Snakes of southern Africa. 387 pp. Parklands: Jonathan Ball &

Ad. Donker.

1991. The herpetofauna of northern Mwinilunga District, northwestern Zambia.

Arnoldia Zimbabwe 9 (37): 519-538.

2001. A review of the genus Thelotornis A. Smith in eastern Africa, with the

description of a new species from the Usambara Mountains (Serpentes: Colubridae:

Dispholidini). African Journal of Herpetology 50 (2): 53-70.

Cansdale, G. S. 1961. West African Snakes. London: Longmans. 74 pp.

Chippaux, J.-P. 1999. Les serpents d'Afrique occidentale et centrale. Paris: Editions

de I’ IRD (Collection Faune et Flore tropicales 35). 278 pp.

Doucet, J. 1963. Les serpents de la République de Cote dIvoire. Acta Tropica 20: 201—

340.

Dowling, H. G. & Duellman, W. E. 1978. Systematic Herpetology: a synopsis of

families and higher categories. 118 + vii pp. New York: HISS Publications.

FitzSimons, V. F. M. 1962. The snakes of southern Africa. 423 pp. Cape Town/

Johannesburg: Purnell.

Hinkel, H. 1982. Herpetofauna. /n: Fischer, E. & Hinkel, H. La Nature et l’Environment

du Rwanda. Mainz: Ministerium des Innern und fiir Sport, Rheinland-Pfalz. 452 pp.

Hughes, B. 1983. African snake faunas. Bonner Zoologische Beitrdge 34: 311-356.

— 1985. Progress on a taxonomic revision of the African Green Tree Snakes

(Philothamnus spp.). Proceedings of the International Symposium on African

Vertebates, Bonn, 1985: 511— 530.

Hughes, B. & Barry, D. H. 1969. The snakes of Ghana: a checklist and key. Bulletin

de I’ Institut Fondamental de l'Afrique noire, sér. A, 31: 1004-1041.

Jackson, K. & Fritts, T. H. 1995. Evidence from tooth surface morphology for a

posterior maxillary origin of the proteroglyph fang. Amphibia-Reptilia 16: 273-288.

Kardong, K. V. 1979. ‘Protovipers’ and the evolution of snake fangs. Evolution 33:

433-443.

Kardong, K. V. & Lavin-Murcio, P. A. 1993. Venom delivery of snakes as high-

pressure and low-pressure systems. Copeia 1993: 650-664.

Kochva, E. 1978. Oral glands of the Reptilia. Jn Gans, C. & Gans, K.A. (eds) Biology

of the Reptilia 8. New York: Academic Press. Pp. 43-94.

Laurent, R. F. 1955. Diagnoses préliminaires de quelques Serpents venimeux. Revue

Zoologique et Botanique Africaine 51: 127-139.

1956. Contribution a |’Herpetologie de la Region des Grands Lacs de |’ Afrique

Centrale. Annales du Musée Royal du Congo Belge, Sér. 8vo, 48: 1-390.

1960. Notes complémentaires sur les Chéloniens et les Ophidiens du Congo

oriental. Annales du Musée Royal du Congo Belge, Sér. 8vo, 84: 1-86.

Leviton, A. E., Gibbs, R. H., Jr., Heal, E. & Dawson, C. E. 1985. Standards in

herpetology and ichthyology: Part I. Standard symbolic codes for institutional

resource collections in herpetology and ichthyology. Copeia 1985: 802-832.

Loveridge, A. 1923. Notes on East African snakes collected 1918-23. Proceedings of

the Zoological Society of London: 87\-897.

1936. New tree snakes of the genera Thrasops and Dendraspis from Kenya

Colony. Proceedings of the Biological Society of Washington 49: 63-66.

1944. Further revisions of African snake genera. Bulletin of the Museum of

Comparative Zoology 95: 121-247.

— 1953. Zoological results of a fifth expedition to East Africa. III Reptiles from

Nyasaland and Tete. Bulletin of the Museum of Comparative Zoology 110: 143-322.

1957. Check list of the reptiles and amphibians of East Africa (Uganda; Kenya;

Tanganyika; Zanzibar). Bulletin of the Museum of Comparative Zoology 117: 151—

362, i-Xxiv.

Meier, J. 1981. The fangs of Dispholidus typus Smith and Thelotornis kirtlandii Smith

(Serpentes: Colubridae), Revue Suisse Zoologique 88: 897-902.

Mertens, R. 1937. Reptilien und Amphibien aus dem siidlichen Inner-Afrika.

Abhandlungen der Senckengergischen Naturforschenden Gesellschaft 435: 1-23.

Peters, W. C. H. 1854. Diagnosen neuer Batrachier, welche zusammen mit der

friiher (24. Juli und 17. August) gegebenen Ubersicht der Schlangen und Eide-

schen mitgetheilt werden. Bericht tiber die zur Bekanntmachung geeigneten

Verhandlungen der kéniglich-preussischen Akademie der Wissenschaften zu

Berlin: 614-628.

1882. Naturwissenschaftliche Reise nach Mossambique auf Befehl seiner Majestat

des Konigs Freidrich Wilhelm IV. In der Jahren 1842 bis 1848 ausgefiihrt von

Wilhelm C. H. Peters. Zoologie ///, Amphibien. 191 pp. Berlin: G. Reimer

Perret, J.-L. 1961. Etudes herpétologiques Africaines III. Bulletin de la Société

neuchateloise des Sciences naturelles 84: 133-138.

Pitman, C. R.. 1974. A guide to the snakes of Uganda. (Revised Edition) 290 pp.

Codicote: Wheldon & Wesley.

Rasmussen, J. B. 1997. Tanzanian records for vine snakes of the genus Thelotornis,

with special reference to the Udzungwa Mountains. African Journal of Herpetology

46: 137-142.

Roux-Estéve, R. 1965. Les Serpents de la région de La Maboké — Boukoko. Cahiers de

la Maboké 3: 51-92.

Schmidt, K. P. 1923. Contributions to the herpetology of the Belgian Congo based on

the collection of the American Museum Congo Expedition, 1909-1915. Bulletin of

the American Museum of Natural History 49: 1-146.

Spawls, S. 1978. A checklist of the snakes of Kenya. Journal of the East Africa Natural

History Society & National Museum 31 (167): 1-18.

Stucki-Stirn, M. C. 1979. Snake Report 721. A comparative study of the herpetological

fauna of the former West Cameroon. 650 pp. Teuffenal: Herpeto-Verlag.

Taub, A. M. 1967. Comparative histological studies on Duvernoy’s gland of colubrid

snakes. Bulletin of the American Museum of Natural History 138: 1-50.

Tilbury, C. R. & Emmrich, D. 1996. A new dwarf forest chameleon (Squamata:

Rhampholeon Ginther 1874) from Tanzania, East Africa with notes on its infrageneric

and zoogeographic relationships. Tropical Zoology 9: 61-71.

Trape, J. F. & Roux-Estéve, R. 1995. Les serpents du Congo: liste commentée et clé

de détermination. Journal of African Zoology 109: 31-50.

Underwood, G. 1967. A Contribution to the Classification of Snakes. British Museum

(Natural History) Publication No. 653. Trustees of the British Museum (Natural

History), London. 179pp.

1997. An overview of venomous snake evolution. /n Thorpe, R.S., Wiister, W. &

Malhotra, A. (eds) Venomous snakes: ecology, evolution and snakebite (Symposia of

the Zoological Society of London, No. 70) Pp. 1—13.

Vaeth, R. H. 1982. Variations in the vidian canal system in Thrasops jacksonii

(Serpentes, Colubridae). Journal of the Herpetological Association of Africa. 28:

10-13.

Villiers, A. 1966. Contribution a la faune du Congo (Brazzaville). Mission A. Villiers

et A. Descarpentries. XLII. Reptiles Ophidiens. Bulletin de I’ Institut Francais de

l'Afrique noire, Sér. A, 28: 1720-1760.

Weinstein, S. A. & Kardong, K. V. 1994. Properties of Duvernoy’s secretions from

opisthoglyphous and aglyphous colubrid snakes. Toxicon 32: 1161-1185.

Witte, G.-F. de 1953. Reptiles. Exploration du Parc National de |’'Upemba, Mission

G.-F, de Witte, 6: 1-322.

Wright, D.L., Kardong, K.V. & Bentley, D.L. 1979. The functional anatomy of the

teeth of the Western Terrestrial Garter Snake, Thamnophis elegans. Herpetologica

35: 223-233.

Appendix 1. Material for which skulls were prepared:

Dispholidus typus (NMZB-UM 3058; NMZB 922, 1350, 1658,

3322, 10870, 13378); Rhamnophis aethiopissa (NMZB_ 10793,

16726); Rhamnophis batesti (NMZB 13206); Xyelodontophis

uluguruensis (NMZB 7443 — holotype); Thelotornis capensis

(NMZB-UM 88, 16199, 17922); Thelotornis kirtlandii (NMZB

32185); Thelotornis mossambicanus (NMZB-UM 3058; NMZB

11390); Thelotornis usambaricus (NMZB 15629); Thrasops

flavigularis (NMZB 16725); Thrasops jacksonii (NMZB 10717).

D.G. BROADLEY AND V. WALLACH

Appendix 2. Material examined internally:

Dispholidus typus (BMNH 1979.205; FMNH 58379; IRSL 2 un-

numbered; IRSNB 1328la—b, MCZ 18223, 32475, 32478, 53458,

53730-31, 55250, 55255, 67927), Dispholidus ‘pemba’ (MCZ

45587), Hapsidophrys lineatus (BMNH 1979.165—-67; IRSL 15

unnumbered; SDSU unnumbered; UNAZA 4 unnumbered; VW

1010), Hapsidophrys smaragdinus (BMNH 1979.157-59; FMNH

179036; IRSL 14 unnumbered; MZUSP 8159; PEM 3363, 3403;

UNAZA 4 unnumbered; VW 907, 1012, 1026, 1068, 1099),

Philothamnus angolensis (IRSL 23 unnumbered; MZUSP 8174-75,

8177; NMV D55548; PEM 3382-83; SDSNH 6386566; UF 52485,

80395-99, 80671; UNAZA 4 unnumbered; VW 1086, 1197, 1211,

1254, 1429-30, 1451, 1745, 1986-87, 1990, 2226; ZRC 2.3427),

Philothamnus bequaertii (MCZ 47846), Philothamnus carinatus

(UNAZA 2 unnumbered), Philothamnus dorsalis (UNAZA 2 un-

numbered), Philothamnus heterodermus (UNAZA 1 unnumbered),

Philothamnus heterolepidotus (LSUMZ 40781), Philothamnus

hoplogaster (BYU 30895), Philothamnus macrops (MCZ 23244),

Philothamnus nitidus (UNAZA 1 unnumbered), Philothamnus

occidentalis (VW 6360), Philothamnus punctatus (MCZ 52666),

Xyelodontophis uluguruensis (NMZB 7443; ZMB 48153),

Rhamnophis aethiopissa IRSL 6 unnumbered; MCZ 13607, 258900,

38392, 48343, 178494; SDSNH 63873; SDSU unnumbered),

Rhamnophis batesii IRSNB 2813; MCZ 13604, 38393), Thelotornis

capensis (FMNH 191163; MCZ 41963, 44581, 69036; ZMB 23526),

Thelotornis kirtlandii (FMNH 205972, 214828; IRSL 1 unnum-

bered; IRSNB 5370, 5371la—b, 6451, 6454; MCZ 22523, 49687,

49734, 51835; SDSU unnumbered; ZMB 21627), Thelotornis

mossambicanus (FMNH 248040; MCZ 51628, 56922: ZMB 16783,

28001), Thelotornis usambaricus (MCZ 23349; ZMB 16786, 21130),

Thrasops flavigularis (MCZ 8776-77; MHNG 967.20, 1520.68,

1520.75, 1520.78), Thrasops jacksonii (BMNH 1979.190-91; UF

52476; MCZ 25954: MZUSP 8178-79: UNAZA 5 unnumbered;

VW 1077, 1083, 1230, 1232, 1965, 2350), Thrasops occidentalis

(MCZ 55232; UG C34P12), Thrasops schmidti (MNHN 1940.197,

1974.1; NRM 2297b).

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 75-81

-fRAE= roe

Issued 28 November 2002

On the African leopard whip snake,

Psammophis leopardinus Bocage, 1887

(Serpentes, Colubridae), with the description

of a new species from Zambia

BARRY HUGHES

57 Snaresbrook Road, London EI] IPQ, England.

E. WADE

Middlesex University, Cat Hill, Barnet, Hertfordshire, EN4 SHT, England.

SYNOPSIS. An examination of scalation and dentition of specimens in Brussels (IRSN), Tervuren (MRAC) — mostly Bredo

collection, and London (BMNH) from Angola, Congo-Kinshasa and Zambia suggests the existence of a species which is neither

P. sibilans leopardinus of which the type is from Namibia, nor P. ‘sibilans’ [mossambicus] of Congo-Kinshasa and Zambia, but

a new species previously unnamed.

INTRODUCTION

Bocage (1887:206) described from Catumbela, Angola a Psam-

mophis (MBL 1798, now destroyed) with a striking reticular pattern

on the neck and anterior part of the body as a variety of Psammophis

sibilans, a taxonomic treatment later followed by Broadley (1977).

More recently Brandstatter (1995, 1996: Fig. 4) has recognised P.

sibilans as occurring no further south than the northern part of

Tanzania and has treated Bocage’s variety as P. brevirostris

leopardinus, following an earlier practice by Broadley (1971). Hehas

followed Broadley (op. cit.) in assigning to this subspecies Zambian

specimens showing the same reticular pattern on the neck. However,

such a pattern occurs sporadically elsewhere, as in West African

specimens of P. sibilans (BMNH 1930.6.5.8 from Mogonori, Ghana;

1956.1.5.87 from Ikoyi, Lagos, Nigeria; CM 24636 from Accra;

MNHN 1985.442-3 from Ghana; ZMH R04466 from Gana Gana or

Segbana, Niger Delta, Nigeria: these have neck bars sometimes

interconnected as in /eopardinus. Dependence on pattern for identifi-

cation in a genus whose species are notorious for their variability is

unconvincing. In an attempt to find other, more reliable criteria by

which to distinguish species of Psammophis, total tooth counts were

undertaken and revealed significant differences between specimens

of ‘/eopardinus’ from Angola and those from Zambia. Secondly, the

Zambian specimens are often of a colour pattern rarely met with

elsewhere during the study of several thousand specimens from all

parts of Africa and the Middle East. Thirdly, the ventral and subcaudal

counts of the Zambian specimens are lower than those from neigh-

bouring localities in Zambia and Congo-Kinshasa. Fourthly, a SEM

micrograph of adorsal scale ofaspecimen from Ikelenge (Brandstatter,

1995: Fig. 39) differs considerably from those of species assigned to

the P. sibilans complex. For these reasons, it is thought necessary to

coin a new name for the Zambian specimens.

SYSTEMATICS

Psammophis zambiensis sp. nov. Zambian Whip Snake

Psammophis sibilans, not Linnaeus 1758, Pitman, 1934: 297 (part,

Chimikombe specimens only).

Dromophis lineatus, not Dumeril & Bibron, Laurent 1956:247

Kundelungu male & female.

Psammophis ? sibilans Broadley & Pitman 1960: 445

Psammophis brevirostris leopardinus Broadley 1971:88;

Brandstatter, 1995: 53, Fig. 39 and 1996: 48 (Zambian specimens

only); Haagner et al. 2000: 16.

Psammophis sibilans leopardinus (Zambian specimens) Broadley

1977:18

Psammophis brevirostris leopardinus Brandstatter 1996:48 (Zam-

bian specimens only)

HOLOTYPE. BMNH1959.1.1.81 supposedly from ‘Abercorn’ (now

Mbala) area of Zambia, part of the H.J. Bredo collection, sent on

from Brussels, but likely to be from Mweru-Wantipa — see discussion

(Figs 1-3).

PARATYPES. IRSN 2561,2565-6 of same origin, BMNH

1932.9.9.132—3 from Chimikombe at 4500 ft. (= Chimilombe,

Solwezi District); NMZB 10635-6, 10736, 10757 from Ikelenge

(Broadley 1991:529); IRSN 2562 from Mambwe; IRSN 2567 and

PEM 1438/12 from Mporokoso District (probably Mweru-Wantipa);

IRSN 2563 from Mweru-Wantipa, and IRSN 2564 from an unknown

source in Zambia; MRAC 18622-—3 SERAM, Kundelungu Plateau

1750 m, Congo-Kinshasa (Laurent 1956:247 as Dromophis lineatus).

All specimens, except two (BMNH 1932.9.9.132-3) are female;

Haagner et al (2000) have listed two more males as *P. brevirostris

leopardinus’.

DIAGNOSIS. Often distinguished by a combination of the reticular

body pattern of /Jeopardinus but lacking the higher tooth counts of

the latter (Table 1.). A detailed description of colouration, based on

5 specimens, is given by Broadley & Pitman (1960:445) but can be

summed up by saying that they are greenish rather than the usual

khaki-brown and the scales heavily edged in black. Unlike associ-

ated specimens of P.’sibilans’ the vertebral ‘chain’ is more like a

stripe, the lighter marking on each vertebral scale being more of a

line than a spot; and behind the eyes the head is crossed by three

transverse light bars — a common feature in many Psammophis spp.

but these are narrow, as in P.angolensis or Dromophis lineatus.

Smaller specimens (e.g. Fig. 2-3) are more distinctly marked with

greater contrast around the body. As Haagner et al (2000) have

76 B. HUGHES AND E. WADE

Fig. 1 Head of P. zambiensis (adult holotype, BMNH 1959.1.1.81) seen in (a) dorsal, (b) lateral and (c) ventral views.

Table 1 Dentitions — left/right sides.

species museum no. max.pre-2F post.dentary palatine pterygoid ;

leopardinus 1937.12.3.166 5/5 23/24 11/9 23/18 ;

(Namibia) i

zambiensis 1959.1.1.81 4/3 17/14 9/8 17/14

zambiensis 10636 -/3 14/13 8/9 13/12

zambiensis 10736 4/4 15/14 8/9 16/15 :

zambiensis 10521 3/3 15/15 8/8 16/16 ;

zambiensis 10522 3/3 13/- 9/8 15/14

zambiensis 10523

zambiensis 18622 3/3 16/16 7/8 14/15 .

zambiensis 18623 4/4 17/15 8/9 17/18

zambiensis 1932.9.9.132 3/3 17/19 9/9 17/16 :

zambiensis 1932.9.9.133 3/3 20/20 8/8 19/18

zambiensis 1953.1.2.15 3/3 17/18 8/8 18/18 .

sibilans 1953.1.2.14 3/3 19/18 8/8 16/15?

A NEW PSAMMOPHIS FROM ZAMBIA

Fig. 2 Head of juvenile paratype P zambiensis (IRSN 10523) seen in (a) dorsal, (b) lateral, and (c) ventral views.

noticed, the reticular neck pattern is not always present and these

specimens are distinguished from ‘sibilans’ by their lower ventral

counts and usually by lower subcaudal counts (Table 2).

Brandstatter (1995: Fig. 39) has provided aSEM micrograph of a

dorsal scale from a P. zambiensis paratype NMZB 10636, and the

micro-ornamentation resembles that of Dromophis lineatus (his Fig.

83) more than any species of the P. sibilans complex.

HABITAT. Unfortunately, no field notes are available for this species,

but the fact that many specimens appear to have originated from the

Mweru-Wantipa suggests that it requires a marshy habitat like

Dromophis lineatus, with which it is sympatric in this area (Broadley

& Pitman, 1959). In the Ikelenge area there there are many suitable

dambos and one local specimen had eaten an Eumecia anchietae, a

large skink that frequents such places (Broadley, 1991). The

Sanolumba snake had eaten a ranid frog (Haagner ef al., 2000).

OTHER SPECIES AND SOURCES OF DATA

Psammophis leopardinus {only those with numbers seen by BH,

those without numbers DGB data or from publications].

ANGOLA -— Bella Vista MCZ; Caconda MBL x 8; Capelongo

AMNH x 6 ; Catengue SMF x 2; Catumbela MBL lectotype,

destroyed; Iona TM; Luanda USNM; Lobito Bay AMNH R50612-—

3, R50617-8, and x5; Oncocua, 37 km NE on way to Otchinzau TM;

NAMIBIA — Swakop-Tal, Namib Desert BMNH 1937.12.3.166.

Psammophis ‘sibilans’, currently treated as P. mossambicus.

CONGO-KINSHASA — Kambore MRAC 2017; Kansenia MRAC

7002, 7639; Kapanza MRAC 9649-50; Kapiri MRAC 7027, 7056—

78 B. HUGHES AND E. WADE

Fig. 3 Stretches of the body of Pzambiensis between ventral scales 50 and 57 seen in dorsal and ventral views. (a, b) Adult holotype (BMNH

1959.1.1.81); (c,d) juvenile paratype (IRSN 10523).

A NEW PSAMMOPHIS FROM ZAMBIA

Table 2 Scale counts (sample size)

species M ventrals F ventrals M subc. F subce.

‘leopardinus’ 151-71 (9) 151-74 (20) 79-104(4) 80-105 (10)

‘leop.’ refined 151-65 (8) 151-67 (16) 79-104(4) 80-105 (8)

zambiensis 148-61 (5) 149-65 (17) 80-90 (3) 75-86 (9)

‘sibilans’ 167-77 (32) 167-77(19) 89-103 (26) ?81—100(12)

N.B. The P. ‘leopardinus’ data is for Angolan specimens and from Broadley (pers.

com.): I suspect that specimens of another species are included and P. ‘/eop. refined’

has the data of that species removed. The P. ‘sibilans’ (currently treated as P.

mossambicus) data is from Zambian specimens so called by Broadley (1971:88)

although he has since referred them to P. phillipsi (Broadley 1983) and later P.

mossambicus (Broadley, in prep.), and from Haagner et al (2000) who treat their

specimens as P. mossambicus. The P. zambiensis data incorporates that of P.

‘brevirostris leopardinus’ from Haagner et al. (2000).

Fig. 4 Brandstiitter’s (1996, fig. at p. 48) map of the occurrence of

Psammophis brevirostris leopardinus.

9, 7061; Kapolowe MRAC 9970;Kasai MRAC 968; Kasenyi IRSN

6861; Lofoi MRAC 598; Lubumbashi [as Elizabethville] IRSN

6310; MRAC 7661, 8378-9, 9397-8; Lukafu MRAC 7187, 71199-

201, 7217; Luluaborg St Joseph MRAC 2627-9; Luebo MRAC

2996; Lukonzolwa MRAC 2165; Lusambo MRAC 16378, 16381;

Merode MRAC 3113; Moero Lake Region MRAC 15323; Musosa

IRSN 4780-1; Niambi to Baudouinville MRAC; Pweto MRAC 252,

260, 1980, 1999, 2027; Sandoa MRAC 7935, 7941, 7967-9, 8271-

2, 9854; Tembwe MRAC 4186, 4216, 4237-8;

MALAWI-Chitipa (as Fort Hill) BMNH 97.6.9.135—6; Chiromo

BMNH 1959.1.3.37; Chiromo, 20 km N of Mangochi (as Fort

Johnston); Fort Johnston BMNH 1926.5.8.49; Kasungu AMNH;

Kondowe (=Livingstonia Mission) to Karonga BMNH 97.6.9.132—

4; Nkhotakhota (as Kota Kota) BMNH 96. 12.12.19; Mkanga BMNH

1959.1.3.38; Mlanje River AMNH; x 2; Mtimbuka AMNH x 4;

Mulanje Mt. AMNH; Nchisi AMNH x 2; Nkahta Bay to Ruarwe

BMNH 97.6.9.131 (Boulenger 1897:801); Zomba BMNH

93.10.26.57, 94.2.13.12 (Giinther 1894:618, Boulenger

1896:164,1,m), 1933.4.5.2; Zomba Mt BMNH 1948.1.2.28.

NAMIBIA — Old Sangwali (Broadley 1983; Barts & Haacke

1997).

TANZANIA — Ipiama ZMB 16984; Kingani, nr Dunda ZMB

172777, 17338; Zimba ZMB 23476;

ZAMBIA — IRSN 8834,b—c, 10520, Broadley & Pitman 1960;

ZFMK 18904; Barotseland MNHN 1921.533; Buleya IRSN 8802

(Bulaya of Broadley & Pitman 1960); Chipangali UM; Chisi Lake

(Broadley & Pitman 1960); Chunga, Kafue N.P. UM; Dumdumwensi

UM 20841; Fort Manning BMNH 1962.497; Ikelenge x 2 (Broadley

1991 as Pphillipsii); Kabinda BMNH 1932.9.9.130; Kabwe (as

Broken Hill) BMNH 1932.5.3.95-100, 1932.9.9.134—8, 1936.3.6.34,

1959.1.1.96; Kalabo FMNH, UM; Kaputa IRSN 8805,a, Broadley

& Pitman 1960); Kasama IRSN 8832, Broadley & Pitman 1960;

Lachisi IRSN 8830; Lealui MNHN 20.104, 21;533; Lusaka, 100 km

SW of ZFMK 18904; Makupa IRSN 8835,a,b; Mambwe IRSN

8804, 8828-9, Broadley & Pitman 1960; Maskie’s, Namwala Dis-

trict BMNH 1932.5.3.95-8. 1932.5.3.101; Mbala (as Abercorn,

Broadley & Pitman 1960) BMNH 1959.1.1.81, 1959.1.1.96; IRSN

8798a—-e — 803,a, 8799a—b, 8800-1, 8806-27, 8836-8, 8839

(Broadley & Pitman 1960 as Psammophis subtaeniatus sudanensis):

Mkanda UM; Mporosoko IRSN 8803a—b (Mporokoso of Broadley

& Pitman 1960); Msoro UM (Wilson 1965); Mukupa (Broadley &

Pitman 1960); Muswema IRSN 8833, Broadley & Pitman 1960;

Mweru—Wantipa IRSN 8831, Broadley & Pitman 1960;

Namantombwa Hill, Mumbwa UNZA; Nchelenge, Luangwa Valley

BMNH 1932.12.13.231; Ngoma, Kafue N.P. UM; Nsangu BMNH

1932.9.9.131; Sayiri UM (Wilson 1965); Serenje BMNH

1953.1.2.13-6 ; Yacobi Village, Luangwa Valley LACM;

ZIMBABWE -— Bari, Chikwakwa UM; Bulawayo UM x 3; Elim

Mission, Inyanga UM; Harare (as Salisbury) NMK; Harare (as

Salisbury), Borrowdale Brook UM x 2; Inkomo UM; Mabalauta

UM; Mazoe (Broadley 1959) BMNH 1902.2.12.96-7; Mondoro

UM; Odzi UM x 2; Rugare, Inyanga UM; Umsweswe Bridge,

Gatooma UM; Umtali UM x 3 (Broadley 1959) BMNH 1954.1.3.23—

4; Vumba Mt UM x 2; Wankie N.P., main camp UM x 2.

Psammophis zambiensis (other, non-type specimens)

ZAMBIA — Ikelenge NMZB 10636, and x 2; PEM x 7; Mbala (as

Abercorn, Broadley & Pitman 1960) IRSN 10521—2; Mbala area (as

‘Abercorn’ but see Discussion); BMNH 1959.1.1.81; Mporosoko

(Broadley & Pitman 1960 as Mporokoso) IRSN 10523; PEM x 2

(Haagner et al 200); Sakeji School PEM x 6 (Haagner et al., 2000).

DISCUSSION

The many names by which Zambian P.’sibilans’ has been known

(see above under synonymy) is an indication of the uncertainly

which attends identification of specimens of this species complex.

The very distinctive colouration of some specimens of P. zambiensis

attracts attention but it is not reliable in separating this species from

other(s) with which it may be sympatric. A letter from Desmond

Vesey-FitzGerald to Donald G. Broadley (Broadley, pers. comm.),

dated 29 Sept. 1959, suggests that the source of ‘Abercorn’ speci-

mens is to be doubted: ‘I would guess that all these snakes may have

come from Mweru-Wantipa in Mporokoso District, where Bredo

would have been collecting in the 1943/44 period.’ Vesey-FitzGerald

(1958) collected long series of P. sibilans [= P. mossambicus] in

B. HUGHES AND E. WADE

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Fig.5 Map of area of sympatry between P.‘sibilans’ (O, literature ref. which may include zambiensis; @ specimen seen by BH or DGB and P.zambiensis

A specimens seen). Many records taken from Broadley (1983:146, map 36 of P. ‘phillipsii’, others from an as yet unpublished, revised map (DGB in

prep.) which we have been privileged to see. Localities listed by country and quarter degree square (without ‘se’ prefix); sources indicated when locality

is a map plot without name. For locality data see Appendix 1.

Abercorn [= Mbala] District, but none had either the characteristic

pattern or low ventral counts of P. zambiensis. However, he did

record one snake from Chinsali (10.32 C1) with only 160 ventrals

and 90 subcaudals, which may have been a P. zambiensis, but it was

apparently not preserved. Only by collecting data on a large number

of specimens can the limits of variability become known and

consistent differences in meristic data become apparent.

P. zambiensis and P. ‘sibilans’ appear to be sympatric at Mbala

(Abercorn) (Fig. 3, se08.31C4) but all of the P. zambiensis speci-

mens so attributed are likely from Mweru-Wantipa (see above), so

that true sympatry may occur only at Mporokoso (se09.30), Ikelenge

(sel1.24a2) Serenje (se13.3061) and near Mchinji (13.32d4). The

co-occurrence over such a large distance — more than 600 km from

Ikelenge to Mweru Wantipa without more instances of sympatry

suggests the occupation of different habitats.

P. zambiensis seems to be distinct from P. leopardinus to the south

and P.‘sibilans’ (or ‘phillipsi’) to the north; the true identity of the

latter can become clearer only after analysis of specimens from the

whole of the Congo Basin and West Africa.

ACKNOWLEDGEMENTS. We are indebted to Donald Broadley for his usual

generosity with his data and advice and for the loan of specimens; to curators

Charles Myers and Richard Zweifel (AMNH), Georges Lenglet (IRSN,

Brussels), Danny Meirte (MRAC, Tervuren), Rainer Giinther (ZMB), and

Colin McCarthy (BMNH) for similar loans and providing one or both of us

with working space and answering our many queries.

REFERENCES

Barts, M & W.D. Haacke. 1997. Zur Reptilienfauna der Tsodilo-Berge und

Angrenzender Gebiete im NW-Botswana. Teil 2: Sauria: 2 Serpentes. Sauria 19:15—

Dil

Bocage, J.V.B. du. 1887. Mélanges erpétologiques. IV. Reptiles du dernier voyage de

MM. Capello et Ivens a travers |’Afrique. Jornal de Sciencias Mathematicas,

Physicas e naturaes. Lisboa. 10: 201-208.

A NEW PSAMMOPHIS FROM ZAMBIA

Boulenger, G.A. 1896. Catalogue of the snakes in the British Museum (Natural

History). 3, 727 p.

1897. A list of the reptiles and amphibians collected in Northern Nyasaland by

Mr.Alex Whyte, F.Z.S. and presented to the British Museum by Sir Henry H.

Johnston, K.C.B., with descriptions of new species. Proceedings of the Zoological

Society of London [1897]: 800-803.

1910. A revised list of the South African reptiles and batrachians, with synoptic

tables, special reference to the specimens in the South African Museum and descrip-

tions of new species. Annals of the South African Museum. 5: 455-538.

Brandstatter, Frank. 1995. Eine Revision der Gattung Psammophis mit

Beriicksichtigung der Schwesterngattungen innerhalf der Tribus Psammophiini

(Colubridae; Lycodontinae). Dissertation zur Erlangung des Grades des Doktors der

Naturwissenschaften der Mathematisch-Naturwissenschaftlichen Fakultét der

Universitat des Saarlandes. Saarbriicken. 480 pp.

— 1996. Die Sandrennattern. Die Neue Brehm-Biichkerei 636.. Westarp

Wissenschaften, Magdeburg. 142 pp.

Broadley, D.G. 1959. The herpetology of Southern Rhodesia Part 1. Snakes. Bulletin

of the Museum of Comparative Zoology 120: 1-100.

1971. The reptiles and amphibians of Zambia. Puku (6): 1-143.

—1977. A review of the Genus Psammophis in southern Africa (Serpentes:

Colubridae). Arnoldia Rhodesia 8(12): 1-29.

—— 1983, 1990. FitzSimons’ snakes of southern Africa. 387 p. Jonathan Ball & Ad.

Donker, Parklands, South Africa.

1991. The herpetofauna of northern Mwinilunga District, Northwestern Zambia.

Arnoldia Zimbabwe 9 (37): 519-538.

In prep. A review of the species of Psammophis south of latitude 12 S degrees

(Serpentes: Psammophiinae).

—— & Pitman, C.R.S. 1959. On a collection of snakes taken in Northern Rhodesia by

Monsieur H.J. Bredo. Occasional Papers of the National Museums of Southern

Rhodesia (24B): 437-451.

Gunther, A. 1894. Second report on the reptiles, batrachians, and fishes transmitted by

Mr. H.H. Johnston, C.B., from British Central Africa. Proceedings of the Zoological

Society of London {1893}: 616-628.

Haagner, G.V., Branch, W.R. & Haagner, A.J.F. 2000. Notes on a collection of

reptiles from Zambia and adjacent areas of the Democratic Republic of the Congo.

Annals of the Eastern Cape Museums 1: \-25.

Johnsen, P. 1962. Notes on African snakes, mainly from Northern Rhodesia and

Liberia. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening I Kobenhavn

124:115-130.

Laurent, R.F. 1956. Contribution a |’herpétologie de la région des Grands Lacs de

l’ Afrique centrale. Annales du Musée royal du Congo Belge (sér. 8) 48: 1-390.

Norton, C.C. & Peirce, M.A. 1985. Caryospora species from Zambian snakes. African

Journal of Ecology 23: 59-62.

Peirce, M.A. 1984. Some parasites of reptiles from Zambia and Indian Ocean islands

with a description of Haemogregarina zambiensis sp. nov. from Dispholidus typus

(Colubridae). Journal of Natural History 18:211-217.

Pickersgill, M. & C.A. Watson. 1998. Report on the reptiles observed on a field trip

to Eastern Africa, October 1996—August 1997. Herptile 23:145-149.

Pitman, C.R.S. 1934. A check list of Reptilia and Amphibia occurring and believed to

occur in Northern Rhodesia. In: A report on a faunal survey of Northern Rhodesia.

pp. 292-312. Government Printer, Livingstone.

Sweeney, R.C.H. 1961. Snakes of Nyasaland. Zomba: Nyasaland Society. 200 pp.

Swynnerton, G.H. 1957. Notes on the fauna. Reptiles. Annual Report of the Game

Preservation Department of Tanganyika Territory (1955-6): 28-29.

Vesey-FitzGerald, D.F. 1958. The snakes of Northern Rhodesia and the Tanganyika

borderlands. Proceeding and Transactions of the Rhodesia Scientific Association.

46: 17-102.

Wilson, V.J. 1965. The snakes of the Eastern Province of Zambia. Puku 3: 149-170.

Appendix 1

ANGOLA - 17.19d3 DGB in prep. BOTSWANA - 18.21b4 DGB

in prep.; cl DGB in prep. CONGO-KINSHASA - 06.23a4 Merode;

06.24c3 Kapanza; 06.29c4 Tembwe; 07.28a3 Kiambi; 07.29 Niambi

to Baudouinville; 07.29b2 Baudouinville; 08.25c3 Kamina; 08.26a2

Kikondja. 08.26c2 Nyonga; 08.28b4 Pweto; 08.28d3 Lukonzolwa;,

09.22d3 Sandoa; 09.28b2 Moero Lake region; 10.22a4 Dilolo;

10.26a3 Kansenia; Kapiri; 10.26d3 Kambove; 10.27 Katanga;

10.27a2 Lofoi; 10.27d1 Lukafu; 10.27d2 SERAM, Kundelungu;

10.28b3 Kasenga; 11.26b2 Kapolowe; 11.27¢c2 Lubumbashi [as

Elizabethville] 11.24b1 Sanolumba ; MALAWI — 09.33c2 Chitipa

(as Fort Hill); 09.33d1 Misuku Hills; 09.33d4 Karonga (Pickersgill

& Watson 1998); 10.34a3 Nyungwe; 10.34cl Kondowe (=

Livingstonia Mission); 10.34c3 Nchenachena; 11.33b2 Rumpi;

11.34a3 Nkhata Bay to Ruarwe; 12.34c4 Nkhotakhota (as Kota

Kota); 13.32a2 Kasungu; 13.34a3 Nchisi Mt.; 14.34a4 Dedza;

14.35a3 Mtimbuka; a4 Mangochi (as Fort Johnston); 15.35a4

Zomba; b3 Mchenga; c3 Limbe (Sweeney 1961:147); d3 Mlanje

Mt.; 16.34b2 Likabula R., Mt Mlanje; 16.35a3 Broadley (1983, as

P.phillipsii); b1 Broadley (1983 as P.phillipsii); ¢1 Chiromo

(Broadley 1983 as Pphillipsii); Makanga. MOZAMBIQUE -

16.31b1 DGB in prep; 17.35d3 Broadley (1983); 18.33a3 Broadley

(1983); 18.34a4 Broadley (1983); 18.35b4 Broadley (1983); NA-

MIBIA - 17.24c1 DGB in prep.; c2 DGB in prep.; e4 DGB in prep.;

d4 DGB in prep.; 17.25c3 DGB in prep.; 18.23b3 Old Sangwali;

TANZANIA - 07.31d4 Zimba; 08.31b2 Milepa; 08.35b4 Uzungwa

(as Udzungwa Mts); 09.33d2 Ipiama. ZAMBIA — 08.29c4 Mukupa

Katandula; 08.29d3 Lake Chisi, Mweru-Wantipa; 08.29d4 Kaputa;

08.31¢4 Mbala (as Abercorn); 09.28b2 Molo; 09.29c3 Kawambwa;

09.30a3 Mporokoso; 09.31b2 Mambwe; 10.30c3 Luwingu District;

10.31a2 Kasama; 10.31b1 Nchelenge; 11.24a2 Ikelenge; Sakeji

School; 11.31¢c4 Mpika; Nsangu R.; 12.26b3 Chimilombe (as

Chimikombe); 12.27b4 Chingola (Haagner ef al., 2000); dl

Lufwanyama Farm (Haagner et al., 2000); d2 Musenga (Haagner et

al., 2000); 12.28¢3 Kitwe (Haagner et al., 2000); d3 Ndola (Johnsen,

1962): 12.28c1 24 km W of Mufulira (Johnsen, 1962); 12.30a2

Kabinda, Lukulu R.; 12.32¢1 Yakobe (as Yacobi), Luangwa Valley;

12.33a3 Lundaz (Wilson, 1965)i; 12.34c4 Kota Kola; 13.24c1

Kabompo.; 13.25b4 Kasempa; 13.28a2 8km W. of Luanshya.;

13.30a2 DGB in prep.; a3 Katete (Wilson, 1965); bl Serenje — P.

zambiensis sympatric with P. ‘sibilans’; 13.31d2 Msoro; b3 Nsangu

River, W of Lavushi River; 13.32a3 Chikowa (Wilson, 1965); bl

Chipangali (Wilson, 1965); b3 DGB in prep.; e2 Kalichero (Wilson,

1965); e4 Sayiri (Wilson, 1965); d1 Chipata (Wilson 1965, as Fort

Jameson); d2 Mkanda; d4 near Mchinji (as Fort Manning); 13.33a2

Kasanga; 14.22d3 Kalabo; 14.27¢c3 Mumbwa; 14.28a4 Kabwe (as

Broken Hill);14.30d1 Kacholola; 15.22b1 Buleya; b4Ndau School;

15.23a1 Lealui; 15.25d4 Ngoma, Kafue N.P.; 15.26a1 Chunga,

Kafue N.P.; e2 Maskies; Fort Manning (Wilson, 1965); 15.27d3

100 km SW of Lusaka; d4 Mazabuka.; 15.28a4 Lusaka; b3 50 km

E. of Lusaka; e2 Balmoral, (Peirce, 1984; Norton & Peirce, 1985)

Chilanga; 15.29c2 DGB in prep.; d2 DGB in prep.; 16.23d1 Kachola

(Wilson 1965, as Kacholola); 16.25c3 Machile Forest Station.; ¢4

Mulanga; d4 Katanda; 16.26c1 Dumdumwensi; ¢4 Kasusu; 16.27¢3

Nansi Farm; d4 Chezia confluence, Kariba Lake; 17.24a3 Katima

Mulilo; a4 Wenela base, Caprivi; 17.26a2 Kalomo; c4 DGB in

prep.; d4 Ihaha; 17.27b1 Kariba lake, Lulongwe confluence;

18.21b4 Broadley (1983); cl Broadley (1983); 18.23b3 Old

Sangwali; ZIMBABWE -— 16.28c4 Lake Kariba, Bumi confluence;

dil Kariba lake, Sanyati basin; 16.29d3 DGB in prep; 16.30b4

Mzarambanitam; ¢3 Salator Farm, Mkanguru; 16.31d3 Mt Darwin

(Broadley, 1959); 17.28c3 Sengwa R.; 17.30a1 DGB in prep.; a3

Sinoia (Broadley, 1959); bl Msitkwe R., Mutorashanga; cl

Selukwe; c2 Broadley (1983); e3 Kutama (Broadley, 1959);c4

Broadley (1983); dl Inkomo, d2 Mazoe (Boulenger 1910;

(Broadley, 1959); Mt Hampden (Broadley, 1959); d3 Norton

(Broadley, 1959); d4 Hunyani (Broadley, 1959); 17.31a3 Broadley

(1983); cl Harare (as Salisbury, Broadley 1959); Borrowdale Brook;

c2 Bari, Chikwakwa; ¢3 Harare (as Salisbury, Boulenger 1910); e4

Melfort (Broadley, 1983); 17.32a3 5 km W of Mutolo Broadley

(1983); d2 Elim Mission, Inyanga; d3 Maristvale, Nyanga (Broadley

1983); d4 Nyamaropa, Nyanga (Broadley, 1983); 18.26c4 Broadley

(1983); d2 Broadley (1983); 18.27c2 Broadley (1983); 18.32b4

Broadley (1983).

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 83-90

xX xX RW ie ae Ses

-7D

Morphological variation and the definition of

species in the snake genus Tropidophis

(Serpentes, Tropidophiidae)

S. BLAIR HEDGES

Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park,

Pennsylvania 16802, USA. e-mail sbh1 @psu.edu

)

Issued 28 November 2002

SYNOPSIS. Historically, the definition of species in the Neotropical snake genus Tropidophis has been difficult because of

intraspecific variation in scalation and a paucity of specimens of most taxa. There were 13 species recognized at the time of the

last review in 1960, but additional species have since been discovered and a taxonomic review and update is needed. Data on

morphological variation are presented here and used to clarify the status of the described taxa. Because many taxa are allopatric

with their closest relatives, it is necessary to make decisions as to their status as species or subspecies. As a gauge of species status

in the genus, character divergence in ten pairs of closely related sympatric species was examined. Typically, such species are

differentiated by two non-overlapping colour pattern differences, often in combination with a diagnostic (non-overlapping) or

overlapping difference in scalation. Using this criterion, seven taxa previously considered as subspecies are here elevated to

species status, whereas seven other taxa are retained as subspecies, although in some cases they are allocated to different species.

As aresult, the genus Tropidophis is considered here to comprise 29 species, 26 of which are West Indian and 15 of those are

restricted to Cuba.

INTRODUCTION

Tropidophis are typically small, stout-bodied snakes of the family

Tropidophiidae that occur in South America and the West Indies.

This family is amember of the primitive snake Infraorder Henophidia

(Underwood, 1967). As recognized here, there are 29 valid species

of Tropidophis and all but three occur in the West Indies, where Cuba

(15 species) is the centre of diversity (Table 1). They are nocturnal

and feed mostly on sleeping lizards (especially Anolis), but also on

frogs (especially Eleutherodactylus); other nocturnal snakes may

impinge on Tropidophis ecologically. All are viviparous and most

are terrestrial, although several Cuban species are arboreal and

gracile in habitus. They exhibit a diversity of colour patterns that

include spots (mostly), bands (saddles), and stripes. They have the

unusual ability of being able to change their colouration, physiologi-

cally (Hedges, Hass & Maugel, 1989). Typically they are paler when

active (at night) and dark while inactive. Species distributions tend

to be greatly restricted, with species endemic to single islands or

island banks, and often to small areas on an island. However, species

density can be high, and as many as six species are sympatric in

some areas of Cuba.

Historically, the taxonomy of Tropidophis has been difficult to

study because of small numbers of specimens and a paucity of

diagnostic characters. For example, two of the earliest described

species, 7; maculatus and T: pardalis, have been confused repeat-

edly. Boulenger (1893) and Stull (1928) commented on the confusion

of these species by Cope (1868), whereas Schwartz and Marsh

(1960) later commented on their confusion by Stull! Most of these

early problems in Tropidophis taxonomy stemmed from the use of

characters later found to be unreliable, such as the keeling of scales

or hemipene morphology. It was not until Schwartz and Marsh

(1960) assembled a large number of specimens and collected exten-

sive data on proportions, scalation and pattern that the systematics of

this genus became reasonably well known. Although it was a large

study, it was not comprehensive because it omitted species related to

T. melanurus and those placed by Schwartz (1957) in the semicinctis

group. However, their success was in recognizing the utility of

colouration and pattern characters, and that species diagnosis in this

genus often requires consideration of multiple characters, some of

which may not be individually diagnostic.

This is not a comprehensive revision of the genus but rather a

taxonomic update, motivated by the many changes that have occurred

since that last major review (Schwartz & Marsh, 1960) and the need

to summarize what is known of morphological variation in the

genus. Another motivation is to address a recurring problem in the

systematics of this group: determining the species status of allopatric

populations and taxa. In the process, taxa previously considered as

subspecies are here elevated to species status, some are assigned to

different species, and others are left unchanged.

MATERIALS AND METHODS

The data presented herein are almost entirely from the literature, or

were used in published studies (but not necessarily published in the

form here). Most derive from the raw data sheets of the late Albert

Schwartz, used primarily in several publications (Schwartz, 1975;

Schwartz & Garrido, 1975; Schwartz & Henderson, 1991; Schwartz

& Marsh, 1960; Schwartz & Thomas, 1960; Thomas, 1963).

Schwartz’s Cuban specimens are in the American Museum of

Natural History and his other material is almost entirely in the

collection of the Museum of Natural History, University of Kansas.

In addition to those data, I have included data from specimens I and

colleagues have collected during the last two decades of field work,

and which, for the most part, formed the basis of several published

studies: (Hedges, Estrada & Diaz, 1999; Hedges & Garrido, 1992;

Hedges & Garrido, 1999; Hedges & Garrido, 2002; Hedges, Garrido

& Diaz, 2001). This material is in the National Museum of Natural

History (Smithsonian) and in Cuban collections (National Museum

of Natural History, Havana; Institute of Ecology and Systematics,

Table 1 Species, species groups, and distributions of snakes of the genus

Tropidophis.

Distribution

Species Species Group

T. battersbyi Laurent taczanowskyi South America

T. bucculentus Cope melanurus Navassa Island

T. canus Cope melanurus Bahamas

T. caymanensis Battersby melanurus Grand Cayman

T. celiae Hedges, Estrada, and Diaz melanurus Cuba

T. curtus Garman melanurus Bahamas

T. feicki Schwartz maculatus Cuba

T: fuscus Hedges and Garrido pardalis Cuba

T. galacelidus Schwartz and Garrido pardalis Cuba

T. greenwayi Barbour and Shreve haetianus Turks and Caicos

T. haetianus Cope haetianus Hispaniola

T. hardyi Schwartz and Garrido pardalis Cuba

T. hendersoni Hedges and Garrido pardalis Cuba

T. jamaicensis Stull jamaicensis Jamaica

T. maculatus Bibron maculatus Cuba

T. melanurus Schlegel melanurus Cuba

T. morenoi Hedges, Garrido, and Diaz maculatus Cuba

T. nigriventris Bailey pardalis Cuba

T. pardalis Gundlach pardalis Cuba

T. parkeri Grant melanurus Little Cayman

T. paucisquamis Miiller taczanowskyi South America

T. pilsbryi Bailey pardalis Cuba

T. schwartzi Thomas melanurus Cayman Brac

T. semicinctus Gundlach and Peters maculatus Cuba

T: spiritus Hedges and Garrido pardalis Cuba

T. stejnegeri Grant jamaicensis Jamaica

T. stullae Grant jamaicensis Jamaica

T. taczanowskyi Steindachner taczanowskyi South America

T. wrighti Stull pardalis Cuba

Havana). In nearly all cases, museum numbers and localities of

those specimens are listed in the publications and therefore are not

repeated here.

In some cases, summary data presented in the tables of Schwartz

and Marsh (1960) do not agree with those in the raw data sheets or

with data mentioned in the text of Schwartz and Marsh, presumably

because of typographical errors in their tables. Some of the data

presented later in Schwartz and Henderson (1991), such as the

ventral range of 7: canus and caudal range of T. maculatus, appear to

be derived from those typographical errors. Although these errors

are minor, the summary data presented in this paper were taken

directly from Schwartz’s raw data sheets, to avoid any confusion,

and supplemented with additional data. Also, some characters were

not scored by Schwartz in some species (e.g., parietal contact in T.

feicki, T; melanurus, T. semicinctus, etc) or at all (e.g., ratios of eye

length to head width and head width to neck width, and aspects of

colour pattern). In those cases, specimens at hand were examined to

fill in the gaps. Ihave examined preserved material of most taxa, and

have observed and collected 12 of the species: T. canus, T. feicki, T.

fuscus, T. greenwayi, T. haetianus, T. maculatus, T. melanurus, T.

pardalis, T. pilsbryi, T. stejnegeri, T. stullae, and T. wright.

Because this is not a comprehensive revision, there was no

attempt to survey all collections for holdings of Tropidophis or to

examine all available material. It is anticipated that such an under-

taking will be attempted in the future.

RESULTS AND DISCUSSION

The conclusion of this taxonomic update is the recognition of 29

species of Tropidophis (Table 1). This is an increase of about six

species over the number recognised earlier this year (Hedges &

S.B. HEDGES

Garrido, 2002). The difference involves the elevation of some taxa

previously considered as subspecies. Below, I discuss the utility of

different characters used, my reasoning in determining species

boundaries, and the taxonomic issues involved in each geographic

area. The phylogeny and biogeography of species in this genus,

using DNA sequence data, is discussed elsewhere (S. B. Hedges, S.

C. Duncan, A. K. Pepperney, in preparation). The species group

status (Table 1) is based on that work, but otherwise the focus of this

current assessment is the definition of species boundaries, not

phylogenetic relationships.

Characters

Variation in 20 characters among the 29 species of Tropidophis is

shown in Tables 2-4. They are grouped into those involving propor-

tions (Table 2), scalation (Table 3), and pattern and coloration (Table

4). In general, sexual dimorphism in Tropidophis is not pronounced

and therefore data from both sexes can be combined, with the

exception of body size, which shows slight differences. Characters

that I have found to be of limited value have been eliminated. These

include four that are commonly scored in snake systematics: upper

and lower labials and the pre- and postoculars. All four are variable

within species and in almost all cases, not diagnostic. Upper labials

are usually 9-10 and lower labials usually 9-12 in all species. In T.

melanurus and some related species, labial counts tend to be higher,

although even in those cases there is often overlap. There is usually

one preocular and 2-3 postoculars in Tropidophis, although some

species occasionally have two preoculars and as many as 4

postoculars; however, variation in ocular scales does not appear to

be of taxonomic utility. Examples of exceptions, as noted by Schwartz

and Marsh (1960), are 7: pardalis (usually 2 postoculars) and T.

maculatus (usually 3 postoculars), although such differences are

rarely diagnostic. Stull (1928) considered the forking of the hemipenis

(bifurcate versus quadrifurcate) to be a diagnostic character but

Schwartz and Marsh (1960) could not identify any species or

specimens with a quadrifurcate condition. Also, such a character

would not be very useful in this group because of limited material

and scarcity of specimens with properly everted hemipenes.

Schwartz scored several other characters in Tropidophis, but I

have also found them to be of limited value in diagnosing taxa. In the

case of relative tail length (Schwartz & Marsh, 1960), it is useful in

distinguishing 7: canus from T. curtus (see below) but otherwise is

difficult to score because of tail damage in some specimens, and

overlapping of ratios. The colour of the tail tip (pale versus dark) was

useful in distinguishing Cayman Islands Tropidophis from T.

melanurus (Thomas, 1963), and other trends are noticeable, but

differences between juveniles and adults, and intraspecific variabil-

ity, make it a less useful character.

Now considering the 20 tabulated characters, maximum snout-

vent length (SVL) is useful because some species differ greatly in

body size, and most individuals encountered are adults. Two ratios

(Table 2) that I have found to be of utility are eye length/head width

(i.e., relative size of the eye) and head width/neck width (..e.,

distinctiveness of the head). Both ratios are larger in the arboreal

species T. feicki, T; semicinctus, and T: wrighti, and in another

gracile Cuban species (7. fuscus) that is possibly arboreal (Hedges &

Garrido, 1992). Unfortunately, both show variation within species

and sample sizes still are small.

Despite the intraspecific variability in the scale characters (Table

3), some are useful when considered simultaneously with other

characters. Ventral and midbody scale row counts are perhaps the

most useful whereas caudal counts and posterior scale row counts

are the least useful. Contact of the two parietal scales can be

iii ee eee

SNAKE OF THE GENUS TROPIDOPHIS

Table 2 Variation in proportions of snakes of the genus Tropidophis.

Max. SVL (mm) Eye diameter/

Species males females head width

T. battersbyi na’ na na

T. bucculentus 360 596 0.19-0.24 (2)

T. canus 363 338 na

T. caymanensis 470 438 0.26 (1)

T. celiae na 344 0.28 (1)

T. curtus 357 354 0.25 (1)

T. feicki 411 448 0.28-0.32 (4)

T. fuscus 287 304 .30-.33 (2)

T. galacelidus 187 405 0.28 (1)

T. greenwayi 313 301 0.23 (1)

T. haetianus 534 Si 0.22-0.25 (8)

T. hardyi 303 334 0.26-0.31 (2)

T. hendersoni 302 315 0.28 (1)

T. jamaicensis 338 306 0.20-0.21 (3)

T. maculatus SPAL 347 0).23-0.32 (5)

T. melanurus 770 957 0.21-0.26 (8)

T. morenoi na 295 0.24—-0.27 (2)

T. nigriventris 184 227 na

T. pardalis 264 287 0.24-0.27 (4)

T. parkeri 422 512 0.24 (1)

T. paucisquamis 101 283 0.24—0.28 (3)

T. pilsbryi 295 260 .24—.25 (2)

T. schwartzi 385 321 na

T. semicinctus 383 408 0.30-0.34 (2)

T. spiritus 320 372 0.24-0.37 (4)

T. stejnegeri 395 529 0.22-0.28 (3)

T. stullae 260 248 0.23-0.25 (3)

T. taczanowskyi 305* 243 0.27-0.30 (2)

T. wrighti 330 323 0.32-0.34 (7)

Head width/

neck width Sample size! References?

na 1 1

1.50-1.55 (2) 4 2-5

na 20 2,6

1.59 (1) 13 2-3,7

ils l((@) 1 8

1.35 (1) 93 2-3, 6

1.76—2.24 (4) 29 2-3,9

1.83-1.99 (2) 8 10-11

1.45 (1) 6 2-3, 6, 12

1.35 (1) 16 2-3, 6

1.28-1.52 (8) 158 2-3, 6, 13

1.30-1.49 (2) 8 2-3, 6, 12

1.45 (1) 1 14

1.47-1.54 (3) 23 2-3,6

1.30-1.92 (5) 25 2-3,6

1.28-1.77 (8) 100 2-3, 15

1.39-1.52 (2) 2 16

na 4 A (oy, 72

1.26-1.63 (4) 161 2-3, 6

1.95 (1) 21 2-3,7

1.53-1.71 (3) 3 2-3

1.59-1.62 (2) 8 2-3, 6, 10

na 17 2-3, 7

1.70-1.88 (2) 26 2-3,9

1.35 (1) 4 17

1.39-1.48 (3) 23 2-3, 6

1.78-1.86 (3) 4 2-3, 6

1.46-1.51 (2) 3 3, 10, 18

1.77-2.24 (7) 17 2-3,9

‘number of specimens used for most measurements and counts, unless otherwise indicated in parentheses.

*primary sources of the data reported in this and other tables: | (Laurent, 1949), 2 (Albert Schwartz, unpublished data), 3 (S. B. Hedges, unpublished data), 4 (Thomas, 1966), 5

(Bailey, 1937), 6 (Schwartz & Marsh, 1960), 7 (Thomas, 1963), 8 (Hedges er al., 1999), 9 (Schwartz, 1957), 10 (Hedges & Garrido, 1992), 11 (Ansel Fong, unpublished data),

12 (Schwartz & Garrido, 1975), 13 (Schwartz, 1975), 14 (Hedges & Garrido, 2002), 15 (Schwartz & Thomas, 1960), 16 (Hedges er a/., 2001), 17 (Hedges & Garrido, 1999), 18

(Stull, 1928).

‘data not available

4sex not determined

diagnostic in some comparisons (Hedges & Garrido, 2002), but

problems arise in how different people score the character (e.g.,

when an interparietal is present and scales barely touch). As already

noted, the keeling of the dorsal scales is often variable within

species. Many species have weakly keeled scales that are noticeable

only above the vent region and are difficult to score consistently, and

depend sometimes on condition of preservation. However, some

species consistently have smooth scales and others (e.g., T.

melanurus) have distinctly keeled scales.

Colour and pattern variation (Table 4) has been important in

Tropidophis taxonomy, in part because the snakes are frequently

spotted and this provides yet additional characters to count. In fact,

- Schwartz and Marsh (1960) considered coloration and pattern to be

the most reliable characters, in combination with scalation, for

‘separating and combining’ taxa. Except for T: feicki, which has

crossbands, most species have 2—12 rows of body spots. I have used

the Schwartz and Marsh (1960) methods of scoring body spots and

spot rows. Spot rows include those on the dorsum and venter, all

around the body (both sides) whereas body spots are counted along

one row of spots (usually just to one side of middorsal region) from

behind the head to just above the vent. Typically, the largest and

most distinctive spots are those near the middorsal region. This

reaches an extreme in species of the melanurus group where some

individuals have only those two spot rows present, resulting in

widely varying row counts (e.g., 2-10). Occipital spots sometimes

fused to form a white neckband, are diagnostic of several species

(e.g., T. celiae, T. galacelidus, T. pilsbryi, T. stejnegeri) and are

common in others (e.g., ZT. pardalis).

The dorsal ground colour of most species is a shade of brown or

grey, and often variable within species. I once collected two speci-

mens of T. pilsbryi in the same rock pile in Cuba, and was initially

misled into thinking they were different species because one was

brown and the other grey. On the other hand, 7: stullae is consist-

ently pale tan and differs from the other two Jamaican species, which

are darker. Also, two boldly spotted species that occur sympatrically

in western Cuba can be distinguished by, among other things, their

dorsal ground colour: greyish pink in T. feicki and yellow to orange

in 7. semicinctus. Although most species are spotted, those in the

melanurus group often have narrow lateral stripes as well as a

middorsal stripe. The absence of middorsal spot contact occurs in

two related species, 7: maculatus and T. semicinctus, and the two

Bahaman species 7. canus and T: curtus are united by the presence

of an anteriolateral (face and neck) stripe. Ventral pattern is diagnos-

tic for T. nigriventris (almost completely dark) and in several species

that lack a ventral pattern, but otherwise most have different degrees

of spotting and flecking.

Species boundaries

Most taxonomists discern the presence of sympatric species by

covariation of multiple characters from individuals of a single

locality, indicating lack of gene flow between the species. For

example, in a series of dark and pale snakes found together, two

species would be indicated if all of the dark snakes also had small

S.B. HEDGES

Table 3 Variation in scalation of snakes of the genus Tropidophis. (Numbers and character states in brackets represent rare or infrequent occurrences; Y =

yes, N = no; other notation as in Table 2.

Species Ventrals Caudals Anterior

T. battersbyi 200 41 21

T. bucculentus 183-186 28-32 24-25

T. canus 170-183 29-35 21[20,22,23]

T. caymanensis 183-200 33-38 23-27

T. celiae 203 30 25

T. curtus 146-173 22-37 19-27

T. feicki 217-235 34-41 23-25[19,21]

T. fuscus 160-185 30-36 21-24

T. galacelidus 177-186 29-35 25-27

T. greenwayi 155-165 26-30 23-25

T. haetianus 170-194 27-39 23-27

T. hardyi 153-172 31-48 20-24

T. hendersoni 190 33 23

T. jamaicensis 167-181 28-36 23-27

T. maculatus 189-208 28-40 22-25

T. melanurus 188-217 31-44 24-27[19]

T. morenoi 198-199 42-44 23

T. nigriventris 144-150 25-26 23-25

T. pardalis 140-157 23-34 PAL23

[19,22,24,25]

T. parkeri 199-212 3341 25(23,24]

T. paucisquamis 170-178 37-40 21

T. pilsbryi 160-169 26-31 22-25

T. schwartzi 191-205 31-39 25)

T. semicinctus 201-223 33-41 21,23[22,24,25]

T. spiritus 183-200 35-39 21-23

T. stejnegeri 181-190 30-38 25-27[23]

T. stullae 166-170 31-34 25

T. taczanowskyi 149-160 25-27 23-25

T. wrighti 192-215 36-45 21-23

heads and fewer spots than the pale snakes (thus, body colour would

be covarying with head size and spot number). In the case of

allopatric populations, it is typically assumed that character differ-

ences similar to or greater than observed between sympatric species

indicate that the two forms are different species. Thus, the ‘yard-

stick’ used for assessing allopatric populations is character divergence

between closely related, sympatric species. This is the principle that

I use here in assessing species status within Tropidophis. It is a

practical species concept but is based on the observation that species

are reproductively isolated from each other, as noted by Darwin

(1859) and later articulated by Mayr (1942) as the biological species

concept.

The reason that a particular degree of differentiation is necessary,

rather than a minimal diagnostic difference, concerns the ‘reality’ of

species in evolution. Almost all species are fragmented (structured)

to some degree, and many populations can be diagnosed by one or a

few nucleotide differences or minor morphological differences.

However, through time, such populations frequently combine and

separate again as part of the reticulate nature of gene flow and

evolution within species. It is only those populations that have

differentiated sufficiently, genetically and/or morphologically, and

presumably reflecting a length of time, that evolve reproductive

isolation from other populations. Thus, to assign species status to

diagnosable, but ephemeral, populations during one slice of time is

arbitrary from an evolutionary standpoint. Although Frost and Hillis

(1990) recommended abandoning the use of quantitative criteria

(molecular and morphological) for discerning species status of

allopatric populations, they did not propose anything to replace that

procedure and thus few have heeded their recommendation.

Dorsal scale rows

Parietal Keeled

Midbody Posterior contact dorsals

23 7 N N

25-27 17-19 N Y

23[22] 16-21 N/Y Y[N]

23[25] 17[19] N N/Y

| 19 Y¢ N

23-25 17-22 N[Y] Y[N]

23-25 17-19 N/Y N

23 15-19 N Y.

25-27 19-20 N Y

25-27 17-19 WC N

25-27[23,29] 17-19[21] Y[N] N

23-25 18-20 N/Y N/Y

25 19 N NE

25-29 15-23 N/Y N

25[23] 17-21 N/Y N/Y

27-29 17-21 N ¥

[24,25,26,30] [16,22,23,24]

23 17 N N

23-25 18-22 N N

23,29 17-21[16] N/Y N[Y]

[21,22,24]

27(25,26] 17[18,19] N Ne

21 17 NY N

23-25 17-21 N N/Y

25[26] 17[15] N Ne

25[21-24] 17-20 N/Y N

23 iN5/ N N

25,27[26] 17-19 N/Y Y

25 16-19 N N

23 19-21 ny! YG

21-23 17[16,18,19] N N

Sympatric species of Tropidophis occur only in Cuba. In western

Cuba, the following six species have been found in the general

region of Canasi, Habana Province: T. celiae, T. feicki, T. maculatus,

T. melanurus, T. pardalis, and T. semicinctis. In central Cuba, the

following six species have been found in the vicinity of the Trinidad

mountains: T: galacelidus, T. hardyi, T. melanurus, T. pardalis, T.

semicinctis, and T. spiritus. In eastern Cuba, the following four

species are known from the region of Baracoa, Guantanamo Prov-

ince: T: fuscus, T. melanurus, T. pilsbryi, and T. wrighti. To identify

the level of character divergence associated with species differentia-

tion in Tropidophis, 1 now focus on four clusters of sympatric

species, each of which are members of the same species group: (1)

feicki/maculatus/semicinctis,(2) celiae/melanurus, (3) pardalis/

galacelidus/hardyi, and (4) fuscus/wrighti/pilsbryi.

In cluster (1), 7. maculatus and T. semicinctis are closest relatives

according to DNA sequence evidence (S. B. Hedges, S. C. Duncan,

A. K. Pepperney, in preparation) and are distinguished primarily by

colour pattern: the number of body spots (no overlap) and number of

spot rows (no overlap). All scale counts in those two species overlap,

although T- semicinctis tends to have a higher number of ventrals. In

the case of T. feicki and T. maculatus, there are non-overlapping

differences in ventral counts, body spots, and spot rows. Consider-

ing 7. feicki and T. semicinctis, the ground colour and spot rows are

non-overlapping, and the ventral counts are different but overlap

slightly.

In cluster (2), T. celiae and T. melanurus, which are close relatives

according to DNA sequence evidence, completely overlap in all

scale counts, although parietal contact might be considered diagnos-

tic if there were more than one specimen of T. celiae. Otherwise,

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about the only characters that distinguish these two species are body

size and aspects of coloration (e.g., neckband in T- celiae and higher

number of body spots). In case the reader is wondering, the presence

of enlarged ova in the small holotype of T: celiae, and details of the

pattern, indicate it is not a juvenile 7: melanurus (Hedges et al.,

IGS).

In cluster (3), there are no molecular data available for 7:

galacelidus and T. hardyi to confirm their species group association

with T. pardalis. However the association is supported by the fact

that there are no diagnostic (non-overlapping) scale or pattern

characters that distinguish 7. hardyi and T. pardalis. This problem

was noted in the original description (Schwartz & Garrido, 1975).

However, 7: hardyi has a higher number of ventrals, even though

overlapping with 7: pardalis, and it is a larger species with a

distinctly smaller head. The latter character caused Schwartz and

Garrido to associate (as a subspecies) 7: hardyi with the small-

headed T. nigriventris. The third sympatric species of this trio, T-

galacelidus, can be distinguished from the other two species by its

higher number of ventrals, dorsal spots, and spot rows (all non-

overlapping).

In the case of cluster (4), DNA sequence evidence place all three

together as close relatives. Tropidophis fuscus and T: pilsbryi have

no completely diagnostic scale differences, although the combina-

tion of ventral scale counts and midbody scale rows will distinguish

the species. Also, T. fuscus has a more gracile body shape. The third

species, 7: wrighti, is diagnosed from the other species by its higher

ventral counts, and fewer dorsal spots and spot rows (all non-

overlapping).

To summarize, of the ten combinations of closely related, sympatric

species, nearly all were distinguished by at least two non-overlap-

ping differences in colour pattern, or (less frequently) body

proportions. In addition, there was usually one other difference

(either non-overlapping or overlapping) in scalation. More distantly

related species of Tropidophis often have two (or more) non-over-

lapping differences in scalation, in addition to any other differences.

This suggests a temporal sequence in character differentiation, with

colour pattern and body proportion differences accruing first, fol-

lowed by scalation differences. Ideally, one would like to use

molecular data as well for assessing differentiation, although tissue

samples still are not yet available for many taxa. Using this morpho-

logical criterion for assessing species status in. Tropidophis, 1 will

now review the current status of the taxa in this genus.

Hispaniola

Only one species (7: haetianus), with three subspecies, occurs on

Hispaniola: T: h. haetianus (most of island), T: h. hemerus (distal

portion of the Tiburon Peninsula in Haiti) and T. h. tiburonensis

(extreme eastern portion of the Dominican Republic). Although

Schwartz and Marsh (1960) and Schwartz (1975) have considered

the Jamaican taxa to be subspecies of T: haetianus, genetic evidence

has shown that they are more closely related to the Cuban species

(Hass, Maxson & Hedges, 2001) and thus are removed from 7:

haetianus (see below). Also, the Cuban specimens of 7: haetianus

discussed by Schwartz and Marsh (1975) and Schwartz and Garrido

(1975) have been removed from that species and assigned to a new

species, 7: hendersoni (Hedges & Garrido, 2002). Because the

subspecies of Hispaniolan 7: haetianus are parapatric and apparently

intergrade (Schwartz, 1975), and because their character differentia-

tion is less than that of sympatric species, I suggest retaining their

current taxonomic status as subspecies. It is possible that genetic

studies in the future may further clarify their status. Thus, T.

haetianus is confined to Hispaniola and contains three subspecies.

S.B. HEDGES

Navassa Island

Four specimens of 7: bucculentus are known from this small island

between Hispaniola and Jamaica, but apparently no snakes have

been seen in over 100 years and thus the species is considered extinct

(Powell, 1999). Since it was described by Cope (1868), there has

been considerable confusion as to its species status and relationship

with other species. Most who have examined the type series, includ-

ing me, have noted a resemblance to 7: melanurus (Thomas, 1966),

although Stull (1928) instead considered it a subspecies of T. pardalis.

There is no overlap in ventral counts between T. bucculentus and T.

melanurus, and almost no overlap in caudal counts. Although there

appear to be pattern differences between the two species, the single

specimen in the Academy of Natural Sciences (Philadelphia) differs

from the other three specimens (National Museum of Natural His-

tory, Smithsonian) in terms of ventral pigmentation (Bailey, 1937).

Based on the diagnostic scalation differences alone, I would con-

sider T: bucculentus as a valid species. The unusual geographic

location of a species with apparent Cuban affinities, on Navassa

Island, is remarkable. With the exception of the anole (Anolis

longiceps), other species on Navassa have affinities with nearby

Hispaniola (Powell, 1999; Thomas, 1966), which is logical based on

the westerly direction of ocean currents. However, the eastern tip of

Cuba is further east than Navassa, and ocean currents flow southerly

through the Windward Passage separating Cuba and Haiti. Dispersal

on those currents is thus possible and is the most likely explanation

for the origin of 7: bucculentus (and A. longiceps) on Navassa and

possibly the gecko Sphaerodactylus notatus on the Morant Cays

southeast of Jamaica. The locally changing direction of water

currents during a hurricane may also have aided in the dispersal of

these taxa.

Cuba

With 15 described species, Cuba is the hot spot of species diversity

in the genus. Recently, two subspecies described by Schwartz and

Garrido (1975) were elevated to species status and a new species

was described from eastern Cuba (Hedges & Garrido, 2002).

Character differences among many of the Cuban species have been

discussed above (see ‘Species Boundaries’), and I consider all 15

species to be valid. Also, I am aware of material that likely repre-

sents additional, undescribed species. Undoubtedly, more species

will be discovered.

Two remaining taxa are considered subspecies of 7: melanurus: T.

m. dysodes and T. m. eriksoni (Schwartz & Thomas, 1960). The

former is known from three female specimens from near La Coloma,

Pinar del Rio Province, and the latter is restricted to Isla de Juventud.

These taxa differ from 7. m. melanurus primarily in size of the dorsal

spots and in having bolder, darker colouration, with 7: m. dysodes

having the darkest pigmentation of the three subspecies. The ventral

counts of 7: m. eriksoni are low for the species, but there is

considerable overlap with the other two taxa. Considering that there

are no diagnostic differences in body proportion or scalation, and the

colouration differences, although real, are not as trenchant as those

distinguishing sympatric, closely related species (e.g., TZ: maculatus

and T. semicinctis), | am inclined to leave their status as subspecies

unchanged until additional data warrant a reconsideration.

Jamaica

The three Jamaican taxa, originally described as full species, are

closer to Cuban taxa than to T: haetianus based on immunological

data (Hass et al., 2001) and DNA sequence data (S. B. Hedges, S.C.

Duncan, A. K. Pepperney, in preparation). However, they form a

SNAKE OF THE GENUS TROPIDOPHIS

single genetic and morphological group (jamaicensis group), and

are distinguished morphologically from the Cuban species at the

species level, although they are closest to species of the pardalis

group. The question then remains as to whether they should be

treated as a single species (T: jamaicensis) or three separate species:

T. jamaicensis, T. stejnegeri, and T. stullae. However, using the

morphological criterion for species status, I recommend the latter.

Each of these three taxa can be diagnosed based on scalation, body

proportions, and colour pattern, and they are as different from each

other as sympatric species in Cuba. In body size, T: stejnegeri (529

mm SVL) is considerably larger than T. stullae (260 mm SVL), with

T. jamaicensis (338 mm SVL) being intermediate in size. Ventral

counts of T. stejnegeri do not overlap with those of 7: stullae, and

counts of T. jamaicensis are nearly completely non-overlapping

with the other two taxa. Tropidophis stejnegeri has keeled scales and

occipital spots whereas the other two taxa are smooth scaled and

lack occipital spots. Additionally, dorsal ground colours differ,

being yellowish-grey (T. stejnegeri), chocolate brown (T.

Jamaicensis) and pale tan (7: stullae). A middorsal stripe is present

in T. stejnegeri and T. stullae but absent in T: jamaicensis. The head

of T: stejnegeri is pointed but that of 7: stullae is distinctly squared-

shaped.

The Bahamas Bank

Six taxa are currently recognized from the Bahamas Bank:

Tropidophis canus androsi Stull (Andros Island), 7: c. barbouri

Bailey (central Bahamas, from Eleuthera to Ragged Island), T. c.

canus Cope (Great Inagua), 7: c. curtus Garman (New Providence,

Bimini Islands, and Cay Sal Bank), T. g. greenwayi Barbour and

Shreve (Ambergris Cay), and 7. g. lanthanus Schwartz (Caicos

Islands). Schwartz and Marsh (1960) considered all except the last

two to be subspecies of a single species (7: canus) and that arrange-

ment has since been followed. However, it is worth reviewing

morphological variation in 7: canus in the context of our current

understanding of species definitions in the genus. Recent evidence

from DNA sequences has shown that 7: greenwayi is most closely

related to T: haetianus (Hispaniola) and unrelated to the complex

currently considered under 7: canus.

Among the four subspecies of 7: canus, T. c. canus stands out both

morphologically and geographically. It is isolated in the south, being

separated from the northern taxa by islands apparently lacking

Tropidophis: Crooked, Acklins, Mayaguana, and Little Inagua. It

has a higher number of ventrals (170-183). One specimen (1%) of

the northern group has 173 ventrals; all others have fewer than 168

ventrals. Anterior and midbody scale rows in T. c. canus typically

are 21-23 whereas they are typically 23-25 in the northern taxa,

although there is some overlap. The tails of 7: c. canus are distinctly

shorter, averaging 11% (9.4—12.1), compared with 13% (11.0-15.2)

in the northern taxa. Rows of body spots number 6-8 in T: c. canus

whereas they are typically 10 or more in the northern taxa; overlap

consists of nine specimens (10%) of northern taxa with eight rows

and two (2%) with nine rows, and one (5%) T. c. canus with nine

rows. This degree of difference is the same or greater than that seen

between sympatric species of Tropidophis in Cuba, and therefore the

northern taxa should be removed from 7: canus.

The status of the three northern Bahaman taxa is problematic at

this time. Clearly there is geographic variation among these forms.

For example, androsi tends to have a higher number of ventral scales

than the other two taxa, although there is considerable overlap with

barbouri and some with curtus. Within one taxon (curtus), snakes

from Bimini are distinctly larger than those from New Providence.

Both Bailey (1937) and Schwartz and Marsh (1960) noted very little

difference, overall, between barbouri and androsi. When consider-

ing the ‘species boundary’ characters noted above, there is insufficient

justification at present to recognize these taxa as distinct species.

Additional specimens and genetic analyses will be necessary to

better resolve geographic variation in northern Bahaman Tropidophis.

Until then, I suggest here that androsi and barbouri be recognized as

subspecies of T. curtus: T: curtus androsi (new combination) and 7:

curtus barbouri (new combination).

Tropidophis greenwayi lanthanus is a subspecies found in the

Caicos Islands and is distinguished by coloration difference from the

nominate subspecies on nearby Ambergris Cay (Schwartz, 1963).

However, the difference concerns ‘interspace stippling’ and not

actual numbers of spots or spot rows. There are no diagnostic scale

count differences, and the presence of two postoculars in the two

known specimens of 7: g. greenwayi is not remarkable because half

of the specimens of 7: g. lanthanus also have two postoculars, at

least on one side of the head. More material of 7: g. greenwayi 1s

needed, in addition to genetic analyses, before the species status of

T. g. lanthanus can be accurately assessed. I suggest that the latter

taxon continue to be recognized as a subspecies.

Thus, Tropidophis of the Bahamas Bank are placed here in three

species: 7: greenwayi (Turks and Caicos), 7: canus (Great Inagua),

and 7. curtus (northern and central Bahamas). The question as to

whether some Bahaman species also occur in Cuba has been raised

in the past, primarily because of two old specimens (Schwartz &

Marsh, 1960). The first is the type of 7: curtus, purportedly from

‘Cuba’ (Garman, 1887). However, morphologically it agrees with

snakes from New Providence, Bahamas, and the specimen number

(MCZ 6114) is close to other numbers in that collection from New

Providence. Also, the origin of the specimen was investigated and

found to be ‘without definite history’ (Stull, 1928). Thus, I agree

with Stull in considering this specimen to be from New Providence.

The other specimen is AMNH 2946 from ‘Nuevitas, Cuba’ (no other

information). As noted by Schwartz and Marsh (1960) it agrees in

morphology with snakes here considered as T: curtus. Although they

considered the provenance of the specimen to be correct, partly

because of the confusion surrounding the holotype, I raise the

question here that it also may be an error. The specimen number is

close to several 7. curtus from Andros Island (AMNH 2925-2927)

apparently cataloged at about the same time and its scale counts fall

within the range of counts of snakes from that island. Thus I consider

the range of 7: curtus to be restricted to the Bahamas.

The Cayman Islands

Currently there are three subspecies of 7: caymanensis recognized

from the Cayman Islands (Thomas, 1963) and they differ in scale

row counts, ventral counts, and colour pattern. Each is endemic to a

single island, and there is no evidence of intergradation. At the time

they were last reviewed (Thomas, 1963), a more conservative

definition of species boundaries in the genus prevailed. Although no

new material has been examined here, the level of differences seen

among these taxa would suggest that they are distinct species.

Tropidophis caymanensis (Grand Cayman) 1s distinguished from 7:

parkeri (Little Cayman) by its lower anterior and midbody scale

rows (23-25 versus 25—27), lower number of ventrals (183-200

versus 199-212), and a larger, darker cephalic pattern. Tropidophis

caymanensis is distinguished from T: schwartzi (Cayman Brac) by

its larger body size (maximum SVL = 470 mm versus 385 mm),

lower anterior scale rows (23 versus 25), lower, albeit overlapping,

number of ventrals (183-200, x = 192, versus 191—205, x = 198),

fewer tail spots (4-8, mode = 6 versus 5—9, mode = 8) and a larger,

darker, cephalic pattern. Tropidophis parkeri is distinguished from

T. schwartzi by its higher midbody scale rows (27 versus 25), higher

number of ventrals (199-212, x= 203 versus 191—205, x= 198), and

a larger, darker cephalic spot (Thomas, 1963).

South America

Although Stull (1928) and Schwartz and Marsh (1960) attempted to

relate one or more of the South American taxa to West Indian species

groups, I do not envision a close relationship. For example, the

keeling of the dorsal scales in 7: taczanowskyi is greater than I have

seen in any West Indian taxon. In the case of T. paucisquamus, the

low number (21) of midbody scale rows and a distinctive pattern of

middorsal stripe and blotches is not like any West Indian species, as

noted by Schwartz and Marsh (1960). The only known specimen of

T. battersbyi has been described only as having six rows of spots,

including two rows on the venter (Laurent, 1949; Pérez-Santos &

Moreno, 1991). The fact that the venters of 7? paucisquamus and T.

taczanowskyi have both been described as consisting of black and

yellow spots and bands (Stull, 1928) is noteworthy; such a pattern

and colouration is not known in West Indian taxa. This might also

suggest a relationship at least between these two species. Molecular

phylogenetic evidence (S. B. Hedges, S.C. Duncan, A. K. Pepperney,

in preparation) places T: paucisquamus outside of the West Indian

clade, reinforcing the morphological distinction. Examination of

additional specimens, and genetic data from T. battersbyi and T:

taczanowskyi, are needed to clarify the relationships of these South

American species. Until then, available evidence supports the place-

ment of the South American species in a separate species group

(taczanowskyi group).

ACKNOWLEDGEMENTS. I thank R. Henderson for providing access to the

raw scale count data and notes of A. Schwartz; L. Diaz, A. R. Estrada, A.

Fong, O. H. Garrido, and L. Moreno, for data on specimens in their posses-

sion; R. Thomas for assistance in the field; the staffs of the National Museum

of Natural History (Smithsonian), Museum of Comparative Zoology

(Harvard), and Natural History Museum (London), for loan of material or

access to the collections. This work was supported by grants from the U.S.

National Science Foundation.

REFERENCES

Bailey, J.R. 1937. A review of some recent Tropidophis material. Proceedings of the

New England Zoological Club 16: 41-52.

Boulenger, G.A. 1893. Catalogue of snakes in the British Museum (Natural History).

Vol. 1. Longmans and Company, London.

S.B. HEDGES

Cope, E.D. 1868. An examination of the Reptilia and Batrachia obtained by the Orton

Expedition to Ecuador and the upper Amazon, with notes on other species. Proceed-

ings of the Academy of Natural Sciences, Philadelphia 20: 96-140.

Darwin, C. 1859. The Origin of Species. John Murray, London.

Frost, D.R. & Hillis, D.M. 1990. Species in concept and practice. Herpetologica 46:

87-104.

Garman, S. 1887. On West Indian reptiles in the Museum of Comparative Zoology,

Cambridge, Massachusetts. Proceedings of the American Philosophical Society 24:

278-286.

Hass, C.A., Maxson, L.R. & Hedges, S.B. 2001. Relationships and divergence times

of West Indian amphibians and reptiles: insights from albumin immunology. In:

Woods CA and Sergile FE, eds. Biogeography of the West Indies: patterns and

perspectives. Boca Raton, Florida: CRC Press. 157-174.

Hedges, S.B., Estrada, A.R. & Diaz, L.M. 1999. A new snake (Tropidophis) from

western Cuba. Copeia 1999: 376-381.

& Garrido, O.H. 1992. A new species of Tropidophis from Cuba (Serpentes,

Tropidophiidae). Copeia 1992: 820-825.

& . 1999. A new snake of the genus Tropidophis (Tropidophiidae) from

central Cuba. Journal of Herpetology 33: 436-441.

& . 2002. A new snake of the genus Tropidophis (Tropidophiidae) from

Eastern Cuba. Journal of Herpetology 36: 157-161.

, —— & Diaz, L.M. 2001. A new banded snake of the genus Tropidophis

(Tropidophiidae) from North-Central Cuba. Journal of Herpetology 35: 615-617.

. Hass, C.A. & Maugel TK. 1989. Physiological colour change in snakes. Journal

of Herpetology 23: 450-455

Laurent, R. 1949. Note sur quelques reptiles appartenant a la collection de ‘Institut

Royal des Sciences Naturelles de Belgique. III. Formes americaines. Bulletin Institut

Royal des Sciences Naturelles Belgique, Bruxelles 25: 1-20.

Mayr, E. 1942. Systematics and the origin of species. Columbia University Press, New

York.

Pérez-Santos, C. & Moreno AG. 1991. Serpientes de Ecuador. Museo Regionale di

Scienze Naturali, Torino, Italy.

Powell, R. 1999. Herpetology of Navassa Island, West Indies. Caribbean Journal of

Science 35: 1-13.

Schwartz A. 1957. A new species of boa (genus Tropidophis) from Western Cuba.

American Museum Novitates (1839): 1-8.

. 1963. A new subspecies of Tropidophis greenwayi from the Caicos Bank.

Breviora, Museum of Comparative Zoology (194): \-6.

. 1975. Variation in the Antillean boid snake Tropidophis haetianus Cope. Journal

of Herpetology 9: 303-311.

& Garrido, O.H. 1975. A reconsideration of some Cuban Tropidophis (Serpentes,

Boidae). Proceedings of the Biological Society of Washington 88: 77-90.

& Henderson, R.W. 1991. Amphibians and reptiles of the West Indies. University

of Florida Press, Gainesville.

& Marsh, R.J. 1960. A review of the pardalis-maculatus complex of the boid

genus Tropidophis. Bulletin of the Museum of Comparative Zoology 123: 49-89.

& Thomas, R. 1960. Four new snakes (Tropidophis, Dromicus, Alsophis) from

the Isla de Pinos and Cuba. Herpetologica 16: 73-90.

Stull, O.G. 1928. A revision of the genus Tropidophis. Occasional Papers of the

Museum of Zoology, University of Michigan: 149.

Thomas, R. 1963. Cayman Islands Tropidophis (Reptilia, Serpentes). Breviora, Mu-

seum of Comparative Zoology: \-8.

. 1966. A reassessment of the herpetofauna of Navassa Island. Journal of the Ohio

Herpetological Society 5: 73-89.

Underwood, G. 1967. A Contribution to the Classification of Snakes. British Museum

(Natural History) Publication No. 653. Trustees of the British Museum (Natural

History), London. 179pp.

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 91-99

Atractaspis (Serpentes, Atractaspididae) the

burrowing asp; a multidisciplinary minireview

E. KOCHVA

Department of Zoology, Tel Aviv University, Ramat Aviv, 69978 Tel Aviv, Israel

CONTENTS

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SyNopSIS. The family Atractaspididae is a highly modified derivative of a lineage that apparently arose early in the history of

‘colubroid’ snakes, and its taxonomy and relationship with other ophidian groups is still uncertain. Snakes of the genus

Atractaspis have a characteristic venom apparatus, including the structure and function of the striking unit and of the venom

glands. The composition of their venom is also unique in containing several low-molecular weight components, the sarafotoxins,

Issued 28 November 2002

which affect the cardiovascular system and are similar to the mammalian endothelins.

Dedication

This paper is dedicated to Dr. Garth Underwood on the occasion of

the 35" anniversary of his classic ‘Contribution to the Classification

of Snakes’ (1967), about which one may say:

This is a small book by a great man!

And also —(T 1) 1” 12) (7277077 JI OVID (7777710 JXID

A little that contains a lot (Theodor & Albeck, 1996)

HISTORY

There are not many snake species that posed problems from the very

beginning of their discovery; one of the most prominent ones is

certainly that which we now call the genus Atractaspis of the family

Atractaspididae (Fig. 1).

The first two specimens of Atractaspis were described by Reinhardt

in 1843 as Elaps irregularis, a species that he considered to be

extremely abnormal because of the presence of only a few, very

small teeth. On the basis of squamation, Underwood inferred that at

least one of the specimens was A. dahomeyensis. The genus

Atractaspis was established by Smith in 1848 for the South African

species bibroni and since then it was variously considered as a

separate family, as a subfamily of the family Viperidae, and finally

as a genus within the Viperinae.

Already Haas (1931), on the basis of the pattern of the head

musculature, was unhappy with the inclusion of Atractaspis in the

Viperidae, but it was not until 1961 that Monique Bourgeois,

studying at the Université Officielle du Congo 4a Lubumbashi, came

out with a challenging question: Atractaspis — a misfit among the

Viperidae? This short note was followed by a detailed study suggest-

ing the establishment of a separate subfamily for a group of

opisthoglyphous colubrids together with Atractaspis (Bourgeois,

1968).

Underwood (1967) lists a long series of skeletal and other ana-

tomical characters in which Atractaspis differs from the Viperidae

and states: ‘Atractaspis differs so widely from the other vipers that

I have no doubts about reviving a separate family group taxon to

receive it’ (p. 103). This he did after a detailed analysis that resulted

in the resurrection of the subfamily Atractaspidinae (Gunther, 1858);

and, finally, the establishment of a separate family, Atractaspididae,

for the approximately 15 species of Atractaspis together with some

African colubrid genera (Underwood & Kochva, 1993).

TAXONOMY

Recently several suggestions concerning the taxonomy and relation-

ship of the Atractaspis species have been raised, mainly dealing with

the question of which additional genera should be included in the

family Atractaspididae and with which, if any, larger clades they

should be grouped (Gravlund, 2001). Underwood himself (personal

communication) is now reconsidering the composition of the family

Atractaspididae in order to decide which genera, in addition to

Atractaspis, should be included in it. However, no one is now

questioning the separate status of the genus Atractaspis, and its

apparent distinction from the other venomous snake families is

widely, though not unanimously, agreed upon. Atractaspis thus

certainly deserves the rank of a family of its own; this may also

include some rear-fanged snakes that are apparently harmless as far

as humans are concerned.

Fig. 1 Atractaspis engaddensis in a combined defensive/offensive

position. Note the arched neck and the beginning of the coiled body

with exposed tip of the tail.

DISTRIBUTION

The distribution of the Atractaspis species 1s unique (Fig. 2), starting

from the Cape of South Africa, through the entire breadth of central

Africa and along the Rift Valley to Arabia, Sinai, Jordan and Israel,

reaching its northernmost border at Mount Gilboa (Al-Oran & Amr,

1995; Kochva, 1998).

It is in Israel that the last species of Atractaspis was found and

described. It was first recorded by Aharoni in 1945 as Atractaspis

aterrimaand later described as anew species, Atractaspis engaddensis,

by Haas in 1950. A. engaddensis is very similar to the Arabian A.

microlepidota andersoni (Gasperetti, 1988), but a decision on the

exact status of the two will have to await further information on the

distribution of Atractaspis forms in the Arabian Peninsula as well as

on the toxicity and composition of their venoms (see also Al-Sadoon

et al., 1991; Al-Sadoon & Abdo, 1991; Schatti & Gasperetti, 1994).

i microlepidota group

[5 bibroni group

overlapping area

* KINSHASA

JOHANNESBURG

E. KOCHVA

BEHAVIOUR

Species of the genus Atractaspis are desert-dwelling, fossorial

snakes, whose behaviour and natural history are not well known.

The Israeli species, A. engaddensis, is mostly found in the Negev

desert and Dead Sea area, but it also extends to the Judean desert and

along the Jordan Valley up to Mount Gilboa (Fig. 2).

A. engaddensis feeds mainly on skinks, but also on lizards and

geckoes that are caught at night above or below ground, beneath

stones or other objects. In captivity, it also accepts baby mice and

rats. A. microlepidota feeds on other snakes such Typhlops and

Leptotyphlops, amphibians and small mammals, mostly rodents

(Scortecci, 1939; Greene, 1997). In a four-year field study carried

out by Akani et al. (2001) in south-eastern Nigeria, it was found that

A. irregularis fed mainly on rodents, while A. aterrima and A.

corpulenta ate lizards, skinks and snakes.

The swallowing behaviour of Atractaspis may be influenced by

its nearly vestigial teeth. As described for A. bibroni, it is character-

ised by a rather inefficient transport mechanism in which the snake

forces its head over the prey with lateral rotations around a vertical

axis, rather than with the ‘pterygoid walk’ used by other snakes.

This can be considered to be an adaptation towards feeding in

natrow spaces and explained by the lack of connection between the

pterygoid and palatine bones that are separated by a wide gap

bridged by a ligament (Deufel & Cundall, 2000; MS; see also

Underwood and Kochva, 1993).

A. engaddensis lays 2-3 elongated eggs during the months of

September—November and hatching occurs after about 3 months

(Fig. 3).

An interesting behavioural feature of this snake is its threat

posture during which it presses its head to the ground while arching

its neck (Fig. 1). This may turn either into a strike or into what

appears to be a defensive display mechanism (Greene, 1979; 1997;

Golani & Kochva, 1993). The snake forms a tight coil with the head

hidden underneath the body and the wriggling tail is exposed above

LUBUMBASHI

Fig. 2 Distribution map of Atractaspis species with the southern African bibroni group and the northern microlepidota group reaching the region of

Mount Gilboa (after Underwood & Kochva, 1993; Joger, 1997).

atte I

ATRACTASPIS — MINI REVIEW

Fig.3 Hatching of Atractaspis engaddensis.

Fig. 4 Defense mimicry posture by Atractaspis engaddensis, with hidden

head and exposed tail.

Fig.5 Tail poking by Atractaspis engaddensis.

the coil so as to mimic the head (Fig. 4). The tail ends in a sharp tip

that the otherwise immobile snake uses for poking when grasped at

the posterior end of the body (Fig. 5). This behaviour may be

mistaken for a genuine strike with the fang and deter any potential

predator. Should that not suffice, there is always the hidden head that

can be produced quickly from underneath the body coils and inflict

a real, painful and dangerous strike.

VENOM APPARATUS

The venom apparatus of Atractaspis has not been dealt with in great

detail beyond the general statement that the maxillary/fang unit is

similar to that of vipers. This similarity is, however, superficial as

the articulation between the prefrontal and maxilla in Atractaspis is

in the form of a ball and socket articulation, which is more restricted

in its movements, but apparently stronger (Pasqual, 1962). This

condition may be important for the peculiar striking of these snakes,

which is performed with one fang at a time while the mouth remains

almost entirely closed (Fig. 6). Striking in this manner may be

considered as a special adaptation for fossorial snakes that feed in

narrow burrows underground.

The venom fangs are relatively long and canaliculate and possess

a blade-like ridge near the orifice of the fang (Kochva & Meier,

1986), which may increase the wound and cause additional tissue

damage during the strike, thus facilitating the spread of venom.

Analyses of films taken during a strike through plastic sheathings

show first the establishment of a firm contact of the head with the

substrate, followed by the erection of the fang and piercing of the

substrate by arching, lateral bending and downward rotation of the

head (Fig. 6). Ejection of the venom is performed while the fang

moves backward, further cutting through the surface (Golani &

Kochva, 1988).

The venom glands have a distinctive structure with secretion

tubules arranged concentrically around the main lumen (Fig. 7).

Unlike the viperids and elapids, there are no differentiated mucous

accessory glands, but mucous cells are found in each of the secretion

tubules close to the central lumen (Kochva et al., 1967). As in the

other families of venomous snakes, there are species (the

microlepidota group, Underwood & Kochva, 1993) with elongated

venom glands that reach far beyond the corner of the mouth (Kochva,

1959). The compressor muscle accompanies the gland along its

entire length and probably squeezes it during the strike so as to

increase the pressure in the central lumen and push the venom

through the venom duct, fang canal and into the wound. The species

with short glands (the bibroni group) have a short, but thicker

compressor.

In a 756 mm long A. engaddensis the right gland reached the 30"

ventral and was 70 mm long, while in A. microlepidota it may reach

one third of the body length — more than 300 mm in a specimen of

900 mm (Scortecci, 1939). The left gland is usually longer than the

right gland in both species and it is sometimes twisted along its

longitudinal axis (Fig. 8).

VENOM

The venom of Atractaspis remained unknown for a long time,

probably because not many serious bites were reported until now

and it was thus ignored by toxinologists. In addition, the venom is

very difficult to obtain not only because of the relative paucity of

specimens collected, but also because of the difficulty in extracting

Fig. 6 Striking sequence by Atractaspis engaddensis; sequence from film

(see text).

it from the glands. Atractaspis, with its spade-shaped head, cannot

be milked the way other venomous snakes are; a special method had

to be devised as shown in Figure 9.

Even today the biochemistry and pharmacology of the venom are

known for only a few species, with almost all the information

available originating from research with the venom of A. engaddensis.

The toxicity of the venom varies among the species tested, the

most potent venom being that of A. engaddensis, exceeding by 40

times or more that of some other species (Table 1). It contains a set

E. KOCHVA

Fig. 7 Venom gland of Atractaspis engaddensis, cross section: M =

compressor muscle, L = lumen of venom gland, T = secretion tubules.

of enzymes not unlike those of other venomous snakes, a quite

powerful hemorrhagin and a group of low-molecular weight toxins,

the sarafotoxins, named after the Hebrew name of A. engaddensis —

Saraf. When the venom was first fractionated by molecular sieving

on a Sephadex G-5S0 column, 7 protein peaks were obtained. The

first two contained high-molecular weight proteins with a

hemorrhagic factor and the enzyme L-amino acid oxidase; the third

peak showed phospholipase A, activity and peaks 5 and 6 contained

very low molecular weight peptides, which made up 40% of the

venom proteins and were highly toxic in 1.v.-injected mice (Kochva

et al., 1982). These fractions were further purified resulting in

several toxins characterised as sarafotoxins (SRTX), which showed

Table 1 Toxicity of Atractaspis venoms, sarafotoxins, and mammalian

endothelins in mice, LD,, (ng/g b.w.)

A. bibroni 500.

A. dahomeyensis 2000

A. microlepidota >2000

A. micropholis >3000

A. engaddensis 75

Sarafotoxin-a 10

Sarafotoxin-b 10

Sarafotoxin-c 300

Sarafotoxin-d/e >2000

Endothelin- | 15

Endothelin-3 30

ATRACTASPIS — MINI REVIEW

Fig. 8 Elongated venom glands of Atractaspis engaddensis: V = venom gland.

Fig.9 Venom extraction from Atractaspis engaddensis using a piece of

tubing for safety and a parafilm-covered lid for the collection of venom.

a high degree of structural homology amongst themselves and with

a group of active peptides that were isolated from mammalian

endothelium, the endothelins (Fig. 10). The sarafotoxins and

endothelins are also similar in their pharmacological activity and are

1 5 10

Cys-Ser-Cys-Lys-Asp-Met-Thr-Asp-Lys-Glu-Cys-Leu-Asn-Phe-Cys-His-Gln-Asp-Val-Ile-Trp

Cys * Cys * * * Ser * * * Cys * *

Cys * Cys * * * * * * * Cys * Tyr

Cys * Cys * * * Ser * * * Cys * Tyr

Cys * Cys-Ala * * * * * * Cys * Tyr

Cys-Thr-Cys-Asn * * * * Glu * Cys * *

Cys-Thr-Cys * * * * * * * Cys * Tyr

Cys * Cys-Asn * Ile-Asn * * * Cys Met Tyr

Cys * Cys-Ser-Ser-Leu-Met * * * Cys-Val-Tyr

Cys * Cys-Ser-Ser-Trp-Leu * * * Cys-Val-Tyr

Cys * Cys-Asn-Ser-Trp-Leu * * * Cys-Val-Tyr

Cys-Thr-Cys-Phe-Thr-Tyr-Lys * * *

Cys-Ala-Thr-Phe-Leu * * *

Cys * Cys-Val-Tyr

1 5

Fig. 10

contractor.

Cys-Val-Tyr-Tyr-Cys *

composed of 21 amino acid residues, with two disulphide bridges

between Cys 1-15 and 3-11 (Yanagisawa et al., 1988; Takasaki et

al., 1988; Wollberg et al., 1990; Kochva et al., 1993). Another

member of the sarafotoxin/endothelin family, bibrotoxin, was iso-

lated from the venom of A. bibroni. It differs from SRTX-b in only

one amino acid substitution and induces vasoconstriction in rat aorta

(Becker et al., 1993). The venom of A. m. microlepidota contains a

series of peptides with a somewhat higher molecular weight that are

composed of 24 amino acids (Ducancel et al., 1999) and are

apparently less toxic than SRTX-a or b.

The sarafotoxins and endothelins are now synthesised by pharma-

ceutical companies and are widely used in both basic and applied

research, both clinical and industrial, in the field of cardiology and

in blood pressure studies (Ducancel et al., 1999; Yaakov et al.,

2000).

The various sarafotoxins (and endothelins) differ in their activity

and toxicity, the most potent ones being SRTX-a and SRTX-b

(Table 1), which exert a strong influence on the cardiovascular

system (Wollberg er al., 1988). SRTX-b shows three, apparently

separate, effects on the heart: 1) positive inotropicity, which is

manifested by an increased contractility in isolated hearts and heart

muscles and in in vivo injected mice with sublethal doses of the

15 20

SRTX-a

Ce ee SRTX-al

Cys * * * * * * SRTX-b

Cys * * * * * * SRTX-b1

Cys * * * * * * BIrX

Cys * * & % * * SRTX-c

Cys * * Gly-Ile * * SRTX-d/e

Cys * * * ‘%*%* %* * Asp-Glu-Pro A. microlepidota

Cys * Leu * Tle * * ET-1

Cys * Leu * Tle * * ET-2

Cys * Leu * Tle * * vIc

Leu * Ile * * ET-3

Cys * Leu * Tle * x ET-trout (1999)

15 20

Amino acid sequences of sarafotoxins and endothelins: BTX = bibrotoxin, ET = endothelin, SRTX = sarafotoxin, VIC = vasoactive intestinal

1.0 sec.

bef ae

Fig. 11 ECG recording after Atractaspis engaddensis envenomation. M

= mouse: v = venom injection; b — f: 120 — 600 seconds after venom

injection. H = human: upper trace — at admission to the hospital; lower

trace — 24 hours after the bite (see text).

toxin; 2) direct effect of the toxin on the cardiac conducting system;

and 3) cardiac ischemia, which is caused by constriction of the

coronary blood vessels. The latter two cause severe A—V block,

which may lead to cardiac arrest. The cardiotoxic effects are mani-

fested by marked changes in the ECG, in both human victims and in

mice injected with either SRTX-b or whole venom (Fig. 11). These

changes include an increase in amplitude of the R- and T-waves, a

prolongation of the P—R interval, ‘dropped beats’ and complete A—

V block and cardiac arrest. In addition, SRTX-b causes contraction

E. KOCHVA

of other blood vessels and may be considered as one of the most

potent vasoconstrictors.

In human patients too, cardiotoxic symptoms and a rise in blood

pressure were observed, but were considered as secondary develop-

ments of some kind of neurotoxic effects. However, neither

presynaptic nor postsynaptic neurotoxicity was observed in labora-

tory tests with nerve-muscle preparations using whole A. engaddensis

venom (Weiser ef al., 1984); SRTX does show specific binding to

different isolated regions of brain preparations, with the highest

binding capacity found in the cerebellum, choroid plexus and hip-

pocampus (Ambar ef al., 1988), but its function there is not known.

In human bites by A. engaddensis and A. irregularis, some of

which were extremely severe, changes in the ECG were observed

(Fig. 11), including S—T elevation or depression, flattening of the T-

waves and prolonged P_R intervals pointing to myocardial ischemia

and atrioventricular conduction abnormalities (Chajek et al., 1974;

Warrell, 1995; Kurnik, et al., 1999). The transient atrioventricular

block that developed in a 17-year old boy bitten on his left foot was

considered to be a secondary complication of the bite (Alkan and

Sukenik, 1974), rather than a direct influence of the toxins on the

heart.

The other systemic symptoms, which may develop within min-

utes, include fever, nausea, general weakness, sweating, pallor,

fluctuations in the level of consciousness and arise in blood pressure

(Doucet & Lepesme, 1953; Chajek et al., 1974; Kurnik et al., 1999).

Most bites were on the fingers and the local effects were demon-

strated mainly by gross oedema of the hand that extended up to the

forearm and shoulder (A. irregularis — Doucet and Lepesme, 1953;

A. corpulenta — Gunders et al., 1960; A. microlepidota — Warrell et

al., 1976) and by blistering and serous vesicles that appeared at the

site of the bite and underwent hemorrhagic transformation (Fig. 12;

Kurnik ef al., 1999). In some previously reported cases (Chajek er

al., 1974; Chajek & Gunders, 1977), local necrosis developed that

required surgical intervention including amputation. In two cases,

one by A. bibroni, the other by A. engaddensis, the bitten finger

partially or fully recovered within a month, but tenderness of the

bitten site remained for a long time (Stewart, 1965; Kurnik ef al.,

1999).

Although the bites by several species of Atractaspis, such as A.

dahomeyensis, A. aterrima, A. corpulenta and A. bibroni were mild

(Warrell et al., 1976; Tilbury & Branch, 1989), A. engaddensis, A.

irregularis and perhaps other species should be regarded as dangerous

Fig. 12 Bitten index finger showing hemorrhagic transformation of

serous vesicles.

ATRACTASPIS — MINI REVIEW

Fig. 13 Ridges on the teeth of Pachyrhachis problematicus (arrow).

mainly because of their influence on the cardiovascular system,

which may lead to death. Only a very small number of lethal cases

has been recorded until now, perhaps a total of five, three by A.

microlepidota (one adult man and two girls aged 4 and 6), one by A.

irregularis, an adult man, and one unknown (Corkill et al., 1959;

Warrell et al., 1976). Despite the fact that A. engaddensis has one of

the most potent venoms known, all patients bitten by this species

finally recovered, one probably due to ‘the immediate and energetic

treatment he received’ (Chajek ef al., 1974). Most recently (July,

2002) a forty-six-year-old man was bitten on the inner aspect of the

right thumb while trying to catch an Afractaspis engaddensis near

his home in the Judean Desert, some 15 km north west of Jericho. He

was taken to the hospital where he arrived after about 40 minutes in

serious condition. Resuscitation failed and he was pronounced dead

after about 45 minutes (Nadir & Stalnikowicz, personal communi-

cation). This is the first death by an Atractaspis engaddensis bite in

Israel. Another recent case, from Saudi Arabia, involved a two-year-

old-girl who died within one hour after being bitten on the foot by

what was identified as A. microlepidota engaddensis. The region

where the bite occurred, at Diriyah near Riyadh, Saudi Arabia, is a

ATRACTASPIDIDAE

SARAFOTOXINS HEMORRHAGINS HEMORRHAGINS

ANCESTRAL

PROTEASE

ANCESTRAL

ENDOTHELIN

VIPERIDAE

PHOSPHOLIPASE

A,-CONTAINING TOXINS

(VIPEROTOXINS, PRESYNAPTIC

NEUROTOXINS)

new distribution record for engaddensis (Al-Sadoon & Abdo, 1991;

see also Al-Sadoon et al., 1991; Gasperetti, 19881; Joger, 1997;

Schatti & Gasperetti, 1994).

It should be pointed out that the toxicity of the venom of certain

species, such as A. microlepidota, may vary according to distri-

bution, causing death in certain cases (see above) or containing less

potent toxins in others (above and Table 1).

As with other venoms, snakes and some mammals are also

resistant to Atractaspis engaddensis venom, including the local

mongoose (Herpestes ichneumon, Bdolah et al., 1997). At least in

one instance, it was found that a mongoose (Paracynictis selousi)

fed on a specimen of A. bibroni (Greene, 1997).

There is no antiserum available against any of the Atractaspis

species.

EVOLUTION

The discussion of snake origin and evolution has been recently

revived by a new and renewed examination and analysis of the

fossils discovered by Haas (1979; 1980a; 1980b) at an Upper

Cretaceous site north of Jerusalem. While the debate on the eco-

logical origin (marine or terrestrial) and the relationships of these

specimens (mosasauroid or macrostomatan) is still going on (Lee

& Caldwell, 1998; Greene & Cundall, 2000; Tchernov et al.,

2000), Rieppel & Zaher (2001) have recently concluded that

*Pachyrhachis 1s neither a basal snake, nor a link between snakes

and mosasauroids, but shows macrostomatan affinities instead’.

Pachyrhachis possesses ridges or cutting edges on its teeth

(Rieppel & Kearney, 2001; Fig. 13) and the teeth of another fossil,

Haasiophis, have still to be further investigated in detail. Should

furrows or any other suggestive structures be found, they could be

taken as plausible signs for the existence of some kind of glands

that might have secreted active substances, even before the

appearance of caenophidian snakes.

ELAPIDAE

PRESYNAPTIC NEUROTOXINS

POSTSYNAPTIC NEUROTOXINS

CARDIOTOXINS, CYTOTOXINS

ANCESTRAL PHOSPHOLIPASE

Fig. 14 Schematic representation of the possible origin of some major snake venom toxins from enzymatic precursors (partly after Strydom, 1979).

It has been suggested that a system that produced active sub-

stances with the means of introducing them into the prey probably

lay at the foundation of the major radiations of higher snakes

(Underwood & Kochva, 1993). This system underwent further

evolution in the Atractaspididae (mainly Atractaspis), Viperidae,

Elapidae and several lineages of ‘Colubridae’.

Some of the active substances were probably enzymatic in nature

and related to enzymes secreted by evolutionarily ‘older’ glands,

such as the pancreas. Indeed, phospholipases found in the venom of

Elapidae, for instance, show sequence homology with the enzymes

secreted by the mammalian pancreas. Some of the ancestral en-

zymes developed into toxins, such as hemorrhagins and neurotoxins,

with or without loss of enzymatic activity (Fig. 14; Strydom, 1979;

Kochva, 1987).

Hemorrhagins are found in two families (Viperidae and

Atractaspididae); presynaptic neurotoxins in two (Elapidae and

Viperidae); and two families each possess a specific and unique

group of toxins — postsynaptic neurotoxins in elapids and sarafotoxins

in Atractaspis.

The hemorrhagin found in the venom of Atractaspis is neutral-

ised by antibodies against Vipera palaestinae venom (Ovadia,

1987) and may thus be related to viperid hemorrhagins, originat-

ing from some kind or kinds of protease. The presynaptic and

postsynaptic neurotoxins, as well as the cytotoxins and

cardiotoxins, apparently originate from phospholipase-like mol-

ecules. The enzyme phospholipase A, may be part of the

presynaptic neurotoxins and its enzymatic activity may still be

essential for its toxicity. The postsynaptic neurotoxins, the

cytotoxins and the cardiotoxins apparently underwent major

changes including loss of enzymatic activity, chain shortening

and gain of neurotoxicity (Strydom, 1979).

The sarafotoxins are structurally very similar to the endothelins,

which are evolutionarily highly conserved, and are found in all

vertebrates, as well as in some invertebrate groups. It should be

emphasised, however, that the genes of the mammalian endo-

thelins were found on three separate chromosomes, whereas the

sarafotoxin genes seem to be located on the same chromosome.

The organisation of the SRTX genes of both A. engaddensis and

A. m. microlepidota and their precursors are also different from

those of the endothelins and may have evolved separately

(Ducancel et al., 1993; 1999).

There is, of course, a great deal of information still missing, but

the evolution of the sarafotoxins and of some of the other snake

venom toxins and their use in feeding and defense may best be

defined as exaptations; these are features that once had different

functions but are now used in a new role that enhances the fitness of

their bearers (Gould & Vrba, 1982).

ACKNOWLEDGMENTS. I would like to thank first and foremost Garth

Underwood for everything he taught me, and not only in Herpetology, and for

a long and fruitful co-operation and warm friendship. I thank the editors of

the Bulletin for inviting me to take part in this publication and Avner Bdolah,

David Cundall, Alexandra Deufel, Dan Graur, Eyal Nadir, Olivier Rieppel,

Ruth Stalnikowicz and Garth Underwood for comments on the manuscript

and for sharing with me some of their unpublished findings. The remarks of

the referees and the help of the Editor are also highly appreciated.

I am very much indebted to my co-workers in Israel, South Africa and

Japan for their major share in the different disciplines of the Atractaspis

research and to the undergraduate and graduate students (listed in the

references) and to many more who picked up the sarafotoxin project (with or

without endothelin) and developed it into such a broad and deeply interesting

field, with still much more to be expected in the future.

E. KOCHVA

Special thanks are due to Moshe Alexandroni, Lydia Maltz, Omer

Markowitz, Naomi Paz, Amikam Shoob and Varda Wexler for help with the

illustrations and with the preparation of the manuscript.

REFERENCES

Aharoni, I. 1945. Animals hitherto unknown to or little known from Palestine. Bulletin

of the Zoological Society of Egypt, Supplement (6): 40-41.

Alkan, M.L. & Sukenik, S. 1974. Atrioventricular block in a case of snakebite

inflicted by Atractaspis engaddensis. Transactions of the Royal Society of Tropical

Medicine and Hygiene 69: 166.

Akani, G.C., Luiselli, L.M., Angelici, F.M., Corti, C. & Zuffi, M.A.L. 2001. The case

of rainforest stiletto snakes (genus Afractaspis) in southern Nigeria. Evidence of

diverging foraging strategies in grossly sympatric snakes with homogeneous body

architecture? Ethology, Ecology and Evolution 13: 89-94.

Al-Oran, R.M. & Amr, Z.S. 1995. First record of the Mole Viper, Atractaspis micro-

lepidota engaddensis, from Jordan. Zoology in the Middle East, Reptilia 11: 47-49.

Al-Sadoon, M.K. & Abdo, N.M. 1991. Fatal envenoming by the snake Atractaspis

newly recorded in the central region of Saudi Arabia. Journal of King Saud

University, Science 3: 123-131.

,Al-Farraj,S.A. & Abdo, N.M. 1991. Survey of the reptilian fauna of the Kingdom

of Saudi Arabia. III. An ecological survey of the lizard, amphisbaenian and snake

fauna of Al-Zulfi area. Bulletin of the Maryland Herpetological Society 27: \—22.

Ambar, I., Kloog, Y., Kochva, E., Wollberg, Z., Bdolah, A., Oron, U. & Sokolovsky,

M. 1988. Characterization and localization of a novel neuroreceptor for the peptide

sara-fotoxin. Biochemical and Biophysical Research Communications 157: 1104—

1110.

Bdolah, A., Kochva, E., Ovadia, M., Kinamon, S. & Wollberg, Z. 1997. Resistance

of the Egyptian mongoose to sarafotoxins. Toxicon 35: 1251-1261.

Becker, A., Dowdle, E.B., Hechler, U., Kauser, K., Donner, P. & Schleuning, W-D.

1993. Bibrotoxin, a novel member of the endothelin/sarafotoxin peptide family, from

the venom of the burrowing asp Atractaspis bibroni. Federation of European

Biochemical Societies (FEBS) 315: 100-103.

Bourgeois, M. 1961. Atractaspis — a misfit among the Viperidae? News Bulletin of the

Zoological Society of South Africa 3: 29.

1968. Contribution a la morphologie comparée du crane des ophidiens de

l'Afrique centrale, Vol. XVII. Publications de |’ Université Officielle du Congo a

Lubumbashi: |—293.

Chajek, T., Rubinger, D., Alkan, M., Melamed, R.M. & Gunders, A.E. 1974.

Anaphylactoid reaction and tissue damage following bite by Atractaspis engaddensis.

Transactions of the Royal Society of Tropical Medicine and Hygiene 68: 333-337.

& Gunders, A.E. 1977. Clinical and biochemical observations following

bites of Atractaspis engaddensis. Rofe Hamishpaha 7: 119-122.

Corkill, N.L., lonides, C.J.P. & Pitman, C.R.S. 1959. Biting and poisoning by the

mole vipers of the genus Atractaspis. Transactions of the Royal Society of Tropical

Medicine and Hygiene 53: 95-101.

Deufel, A. & Cundall, D. 2000. Feeding in stiletto snakes. American Zoologist 40:

996-997.

Feeding of Atractaspis (Serpentes: Attractaspididae): A study in conflicting

functional constraints. (MS)

Ducancel, F., Marte, V., Dupont, C., Lajeunesse, E., Wollberg, Z., Bdolah, A.,

Kochvya, E., Boulain, J.-C. & Ménez, A. 1993. Cloning and sequence analysis of

cDNA encoding precursors of sarafotoxins. Journal of Biological Chemistry 268:

3052-3056.

——,, Wery, M., Hayashi, M.A.F., Muller, B.H., Stécklin, R. & Ménez, A.

1999. Les sarafotoxines de venins de serpent. Annales de l'Institut Pasteur/Actualités

10: 183-194.

Doucet, J. & Lepesme, P. 1953. Sur un cas d’envenimation par Atractaspis, vipéridé

ouest-africain. Bulletin d’Institut francais d'Afrique noire 15: 855-859.

Gasperetti, J. 1988. Snakes of Arabia. Fauna of Saudi Arabia 9: 169-450.

Golani, I. & Kochva E. 1988. Striking and other offensive and defensive behaviour

patterns in Atractaspis engaddensis (Ophidia, Atractaspididae). Copeia 1988: 792—

oie

1993. Tail display in Atractaspis engaddensis (Atractaspididae, Serpentes).

Copeia 1993: 226-228.

Gould, S.J. & Verba, E.S. 1982. Exaptation — a missing term in the science of form.

Paleobiology 8: 4-15.

Gravlund, P. 2001. Radiation within the advanced snakes (Caenophidia) with special

emphasis on African opistoglyph colubrids, based on mitochondrial sequence data.

Biological Journal of the Linnean Society 72: 99-114.

Greene, H.W. 1979. Behavioral convergence in the defensive displays of snakes.

Experientia 35: 747-748.

1997. Snakes, the Evolution of Mystery in Nature. University of California Press,

Berkeley, Los Angeles, London, pp. 351.

ATRACTASPIS — MINI REVIEW

—— & Cundall, D. 2000. Limbless tetrapods and snakes with legs. Science (287):

1939-1941.

Gunders, A.E., Walter, H.J. & Etzel, E. 1960. Case of snake-bite by Atractaspis

corpulenta. Transactions of the Royal Society of Tropical Medicine and Hygiene 54:

279-280.

Gunther, A. 1858. Catalogue of the colubrine snakes in the collection of the British

Museum. British Museum (Natural History), London, 281 pp.

Haas, G. 1931. Uber die Morphologie der Kiefermuskulatur und die Schadelmechanik

einiger Schlangen. Zoologisches Jahrbuch, Abteilung anatomie 54: 333-416.

— 1950. A new Arractaspis (Mole Viper) from Palestine 1950: 52-S3.

— 1979. On anew snakelike reptile from the Lower Cenomanian of Ein Jabrud, near

Jerusalem. Bulletin du Muséum national d'Histoire naturelle, Section C: Sciences de

la Terre, Série 4 (1): 51-64.

1980a. Pachyrhachis problematicus Haas, snakelike reptile from the lower

Cenomanian: ventral view of the skull. Bulletin du Muséum national d'Histoire

naturelle, Section C: Sciences de la Terre, Série 4 (2): 87-104.

1980b. Remarks on a new ophiomorph reptile from the lower Cenomanian of Ein

Jabrud, Israel, pp. 177-192. In L.L. Jacobs (ed.), Aspects of Vertebrate History:

essays in honor of Edwin Harris Colbert. Museum of Northern Arizona Press,

Flagstaff, 393 pp.

Joger, U. 1997. Tiibinger Atlas des Vorderen Orients, Giftschlangen (Middle East

Venomous Snakes). Dr. Ludwig Reichert Verlag, Wiesbaden.

Kochya, E. 1959. An extended venom gland in the Israel Mole Viper, Atractaspis

engaddensis Haas 1950. Bulletin of the Research Council of Israel B8: 31-34.

1987. The origin of snakes and evolution of the venom apparatus. Toxicon 25: 65—

106.

1998. Venomous snakes of Israel: Ecology and snakebite. Proceedings of the joint

Israeli-Jordanian Conference on Venomous Animal Bites, Amman, Jordan, I July

1998. Ofer Shpilberg & Dani Cohen, Eds. Public Health Reviews 26: 209-232.

——,, Bdolah, A. & Wollberg, Z. 1993. Sarafotoxins and endothelins: evolution,

structure and function. Toxicon 31: 541-568.

— & Meier, J. 1986. The fangs of Atractaspis engaddensis Haas (Serpentes:

Atractaspididae). Revue Suisse de Zoologie 93: 749-754.

, Shayer-Wollberg, M. & Sobol, R. 1967. The special pattern of the venom gland

in Atractaspis and its bearing on the taxonomic status of the genus. Copeia 1967:

763-772.

—, Viljoen, C.C. & Botes, D.P. 1982. A new type of toxin in the venom of snakes

from the genus Afractaspis (Atractaspidinae). Toxicon 20: 581-592.

Kurnik, D., Haviv, Y. & Kochva, E. 1999. A Snake bite by the burrowing asp,

Atractaspis engaddensis. Toxicon 37: 223-227.

Lee, M.S.Y. & Caldwell, M.W. 1998. Anatomy and relationships of Pachyrhachis

problematicus, a primitive snake with hindlimbs. Philosophical Transactions of the

Royal Society, London. B 352: 1521-1552.

Ovadia, M. 1987. Isolation and characterization of a hemorrhagic factor from the venom

of the snake Atractaspis engaddensis (Atractaspididae). Toxicon 25: 621-630.

Pasqual, J.R.H. 1962. The biting mechanism of Atractaspis. The Nigerian Field 27:

137-141.

Reinhardt, I.T. 1843. Beskrivelse of nogle nye Slangearter. Kongelige danske

Videnskabernes Selskabs, Afhandlinger (10): 233 -279.

Rieppel, O. & Kearney, M. 2001. The origin of snakes: limits of a scientific debate.

Biologist (48): 110-114.

& Zaher, H. 2001. Re-building the bridge between mosasaurs and snakes. Neues

Jahrbuch fiir Geologie und Paldontologie, Abhandlungen (221): 111-132.

Schatti, B. & Gasperetti, J. 1994. A contribution to the herpetofauna of Southwest

Arabia. Fauna of Saudi Arabia 14: 348-419.

Scortecci, G. 1939. Gli Ofidi Velenosi dell’Africa Italiana. Istituto Sieroterapico

Milanese, Milan, 287pp.

Smith, A. 1848. //lustrations of the Zoology of South Africa, Reptilia. Smith, Elder &

Co., London.

Stewart, M.M. 1965. A bite by a burrowing adder, Atractaspis bibronii. The Journal

of the Herpetological Association of Rhodesia (23/24): 47-S0.

Strydom, D.J. 1979. The evolution of toxins found in snake venoms. In: Snake

Venoms, Handbook of Experimental Pharmacology, (C.Y. Lee, ed.) (52): 258-275.

Springer Verlag, Berlin, 1130 pp.

Takasaki, C., Tamiya, N., Bdolah, A., Wollberg, Z. & Kochva, E. 1988. Sarafotoxin

S6: Several isotoxins from Atractaspis (Burrowing Asps) venom that affect the

heart. Toxicon (26): 543-548.

Tchernoy, E., Rieppel, O., Zaher, H., Polcyn, M.J. & Jacobs, L.L. 2000. A fossil

snake with limbs. Science (287): 2010-2012.

Theodor, J. & Albeck, C. (eds) 1966, Midrash Bereshit Raba, (5, 7), Jerusalem.

Tilbury, C.R. & Branch, W.R. 1989. Observations on the bite of the southern

burrowing asp (Atractaspis bibronii) in Natal. South African Medical Journal (75):

327-331.

Underwood, G. 1967. A Contribution to the Classification of Snakes. British Museum

(Natural History) Publication No. 653. Trustees of the British Museum (Natural

History), London. 179pp.

— & Kochva, E. 1993. On the affinities of the burrowing asps Atractaspis (Serpentes:

Atractaspididae). Zoological Journal of the Linnean Society 107: 3-64.

Warrell, D.A. 1995. Clinical toxicology of snakebite in Africa and Middle East/

Arabian Peninsula, pp. 433-492. In: Clinical Toxicology of Animal Venoms and

Poisons (Meier J. & J. White, eds.), CRS Press, Boca Raton, Florida, 752 pp.

, Ormerod, L.D. & Davidson, N. McD. 1976. Bites by the night adder (Causus

maculatus) and burrowing vipers (genus Afractaspis) in Nigeria. The American

Journal of Tropical Medicine and Hygiene 25: 517-524.

Weiser, E., Wollberg, Z., Kochva, E. & Lee, M.S.Y. 1984. Cardiotoxic effects of the

venom of the burrowing asp, Afractaspis engaddensis (Atractaspididae, Ophidia).

Toxicon 22: 767-774.

Wollberg, Z., Bdolah, A. & Kochya, E. 1990. Cardiovascular effects of mammalian

endothelins and snake venom sarafotoxin. In: Calcium Channel Modulators in Heart

and Smooth Muscle: Basic Mechanisms and Pharmacological Aspects, pp. 283-299

(Abraham, S. & G. Amitai, eds.), VCH, Weinheim/Deerfield Beach, Florida and

Balaban, Rehovot/Philadelphia.

. Shabo-Shina, R., Intrator, N., Bdolah, A., Kochva, E., Shavit, G, Oron, Y.,

Vidne, B.A. & Gitter, S. 1988. A novel cardiotoxic polypeptide from the venom of

Atractaspis engaddensis (Burrowing Asp): Cardiac effects in mice and isolated rat

and human heart preparations. Toxicon 26: 525-534.

Yaakov, N., Bdolah, A., Wollberg, Z., Ben-Haim, S.A. & Oron, U. 2000. Recovery

from sarafotoxin-b induced cardiopathological effects in mice following low energy

laser irradiation. Basic Research in Cardiology 95: 385-389.

Yanagisawa, M., Kurihara, H., Kimura, S., Tomobo, Y., Kobayashi, M., Mitsui, Y.,

Yazaki, Y., Goto, K. & Masaki, T. 1988. A novel potent vasoconstrictor peptide

produced by vascular endothelial cells. Nature 332: 411-415.

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 101-106

Issued 28 November 2002

Origin and phylogenetic position of the Lesser

Antillean species of Bothrops (Serpentes,

Viperidae): biogeographical and medical

implications

WOLFGANG WUSTER AND ROGER S. THORPE

School of Biological Sciences, University of Wales, Bangor LL57 2UW, UK

MARIA DA GRACA SALOMAO

Laboratorio de Herpetologia, Instituto Butantan, Av. Vital Brazil 1500, O05503-900 Sao Paulo—SP, Brazil

LAURENT THOMAS

Service des Urgences, CHRU, 97200 Fort de France, Martinique (French West Indies)

GIUSEPPE PUORTO

Museu Biologico, Instituto Butantan, Av. Vital Brazil 1500, O05503-900 SGo Paulo—SP, Brazil

R. DAVID G. THEAKSTON

Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK

DAVID A. WARRELL

Centre for Tropical Medicine, University of Oxford, John Radcliffe Hospital, Headington, Oxford OX3 9DU,

SYNOPSIS. We use mitochondrial DNA sequences to infer the origin and phylogenetic position of the Lesser Antillean species

of the pitviper genus Bothrops, B. caribbaeus and B. lanceolatus. The two species form a monophyletic group, which in turn forms

the sister clade to the Bothrops asper-atrox complex. High levels of sequence divergence among the Caribbean species, and

between them and the nearest mainland relatives, suggest a relatively ancient origin of these snakes. The hypothesis that the

Lesser Antillean Bothrops are the result of a recent colonisation event from within the South American B. atrox complex is

rejected, as is the hypothesis that they were introduced to their island habitats by aboriginal humans. The high level of

morphological apomorphy displayed by B. lanceolatus suggests a stepping-stone colonisation, St. Lucia being colonised first and

then Martinique from St. Lucia. The medical implications of these findings are discussed: a recent case of envenoming from Saint

Lucia suggests that Bothrops caribbaeus causes the same thrombotic syndrome of envenoming as B. lanceolatus.

INTRODUCTION

The genus Bothrops Wagler, 1824 contains most of the pitviper

fauna of South America. The genus (including the arboreal species

sometimes assigned to Bothriopsis) contains approximately 36

species, with a wider variety of body shapes and natural history traits

than in any other New World pitviper genus. This greater diversity

has been ascribed to the fact that Bothrops was the first group of

pitvipers to reach the South American continent, thus giving ample

opportunity for adaptive radiation (Wiister et al., in press).

Two species of Bothrops occur in the Lesser Antilles: Bothrops

caribbaeus (Garman, 1887) on St. Lucia, and Bothrops lanceolatus

(Lacepéde, 1789) on Martinique. The status and origin of these

forms has been the subject of much debate. Long considered to be

conspecific with Bothrops atrox, B. lanceolatus was revalidated by

Hoge (1952), and the validity of B. lanceolatus and B. caribbaeus

confirmed by Lazell (1964). This latter interpretation has been

followed by most authors since then (e.g., Campbell & Lamar,

1989). However, Sandner Montilla (1981, 1990) regarded the Lesser

Antillean Bothrops as conspecific with each other, as well as with

mainland Bothrops asper and the northern Venezuelan populations

of the B. asper-atrox complex.

The origin of the Antillean Bothrops has been the subject of much

speculation and mythology. This includes popular tales that the

snakes were originally introduced by Carib Indians in their attempts

to gain control of the islands from resident Arawaks (Dowling,

1965), and the notion that dispersal from the South American

mainland is common and ongoing (Sandner Montilla, 1981).

The reptile fauna of the Lesser Antilles is primarily the result of

long-distance dispersal by individual species, as these islands have

not been linked to the South American mainland or any other

landmass at any time in their history (Thorpe ef al., in press;

Malhotra and Thorpe 1999). This means that some species present in

these islands represent long-standing endemic lineages (Thorpe et

al., in press; Malhotra and Thorpe 2000), whereas others appear to

be the result of relatively recent dispersal events from well-defined

source populations or taxa in South America, as is the case for the

genus Corallus (Henderson & Hedges, 1995).

Compared to morphological data, molecular markers such as

mitochondrial DNA (mtDNA) sequence data have the advantage

that they can give an estimate of phylogeny reasonably free of the

confounding effects of differing natural selection pressures on the

external phenotype. Moreover, molecular sequence data also have

the advantage that they can give at least an approximate estimate of

times of divergence between lineages, although the interpretation of

molecular clocks is subject to various analytical and empirical

problems (Hillis et al., 1996).

Several recent mtDNA-based phylogenetic analyses of the genus

Bothrops have included the Antillean species. SalomAo et al. (1997,

PLATE 1

Bothrops caribbeus © R.S. Thorpe

1999), using 580 b.p. of cytochrome b sequence, found B. caribbaeus

and B. lanceolatus to the sister species of the South American

populations of the B. atrox complex. However, the study included

only a limited sampling of South American members of the B. atrox

complex, and did not include representatives of B. asper from

Central America.

The aim of this paper is to explore in more depth the origin of the

Antillean Bothrops, and its implications for other fields, using an

expanded dataset of more sequence information from a larger number

of potentially related species.

MATERIALS AND METHODS

We obtained tissue (ventral scale clippings or tail tips) and/or blood

samples from species representing the principal clades within the

genus Bothrops (including Bothriopsis), as well as the closely

related Bothrocophias — see Wiister et al. (in press). We also

included samples of the B. asper-atrox complex from around the

coast of South and Central America, as these have been considered

to be potential founder populations from which the ancestor of

Antillean Bothrops could have arisen. For outgroup rooting, we used

sequences of Bothrops alternatus and Bothrocophias microphthal-

mus. Two regions of the mitochondrial DNA molecule were amplified

using the polymerase chain reaction (PCR): a 767 base pair (bp)

section of the gene for cytochrome b (cytb), and a 900 bp region of

the gene for NADH dehydrogenase subunit 4 (ND4). Details of

primers and laboratory protocols are given in Pook et al. (2000).

Sequences were aligned by eye against published Bothrops

sequences (Puorto et al., 2001). In order to test for the presence of

saturation of certain categories of substitution, we calculated Tamura—

Nei distances between all samples. This takes into account deviations

from equal base compositions and differences in substitution rates

among nucleotides. We then plotted unadjusted p-distances for

transitions and transversions, and for the three codon positions

separately, against Tamura—Nei distances. A decline in the rate of

accumulation of individual categories of substitution with increased

Tamura—Nei distances indicates saturation of that substitution category.

We checked all sequences for insertions, deletions or the presence

of stop codons. Any of these would have indicated that the sequences

represent nuclear insertions of the mitochondrial genes (Zhang and

Hewitt, 1996). The sequence data were assayed for the presence of

a significant phylogenetic signal by means of the g1 tree skewness

W. WUSTER ET AL.

Bothrops lanceolatus © D. Warrell

statistic (Hillis and Huelsenbeck, 1992), calculated from 100,000

trees randomly generated by PAUP* 4.0b8 (Swofford, 2001).

Sequence divergences between clades were estimated using the

program Phyltest (Kumar, 1996).

We analysed our sequence data using both maximum parsimony

(MP) and maximum likelihood (ML) as optimality criteria. Using

multiple optimality criteria should identify those parts of a

phylogenetic tree that are supported independently of the optimality

criterion used. Such nodes should inspire greater confidence than

nodes that are unstable and vary depending on method of analysis.

All analyses were carried out using the program PAUP* 4.0b8

(Swofford, 2001).

For MP analyses, we selected Bothrops alternatus and B. micro-

phthalmus as outgroups. We employed the heuristic search algorithm

of PAUP* 4.0b8, using TBR branch swapping and 100 random

addition sequence replicates. The analysis was carried out on the

unweighted data only.

The extent to which individual nodes on the tree were supported

by the data was assessed using bootstrapping and Bremer (1994)

branch support. Non-parametric bootstrap was implemented using

heuristic searching, 1000 replicates, TBR branch swapping and 10

random-addition-sequence replicates per bootstrap replicate. Bremer

branch support for individual nodes was calculated through the use

of the converse constraint option of PAUP*.

For ML analyses, we identified the most appropriate model of

sequence evolution through the use of the MODELTEST software

(Posada & Crandall, 1998). A first ML search was run, using

heuristic searching, a neighbour-joining starting tree and TBR branch

swapping, and the sequence evolution parameters identified by the

Modeltest software. These parameters were then re-estimated from

the resulting ML tree, and a further search run using these re-

estimated parameters. This was repeated until further estimates

yielded no further changes of parameter values or tree likelihood

scores. Bootstrap analysis involved 100 replicates, using NJ starting

trees and NNI branch swapping.

An important consideration of any proposed scientific hypothesis

is whether the data supporting it can reject alternative hypotheses

with statistical significance. In other words, do the data allow us to

reject the null hypothesis that differences in tree optimality between

the optimal tree and trees consistent with alternative hypotheses are

due to random chance? In the case of the Antillean Bothrops, we

tested the following alternative phylogenetic hypotheses: (1) non-

monophyly of the Antillean Bothrops, i.e., the Antillean populations

of Bothrops result from separate colonisation events; (ii) non-

ANTILLEAN BOTHROPS 103

microphthalmus

alternatus

00/39 jararaca

insularis

73/6 81/8 taeniatus

pulcher

punctatus

96/12 00/19 Jararacussu

brazili

7 lanceolatus

100/186 caribbaeus

caribbaeus

100/14 asper - Belize

100/ef atrox - Suriname

atrox - Fr. Guyana

aa 94[2\aq/5 atrox - Guyana

leucurus - D. Martins

400/13 /eucurus - Salvador

86/2"— leucurus - P. Seguro/T. Freitas

100/15 }99/6 colombiensis - S. Francisco

colombiensis - Guaibacoa

n.s./1 colombiensis - A.d.Orituco

10 65/1 atrox - Sta. |zabel

100/1 marajoensis - |. Marajo

50/1 atrox - S. Bento

61/1! marajoensis - S. C. Arari

52/3

56/2 24

microphthalmus

alternatus

100 jararaca

insularis

80 81 taeniatus

pulcher

67, 100 Jararacussu

brazili

punctatus

100 lanceolatus

100 fr caribbaeus

100 caribbaeus

asper - Belize

colombiensis - A. d. Orituco

87 atrox - Sta. Izabel

g9_|100 - marajoensis - |. Marajo

atrox - S. Bento

SS. marajoensis - S.C. Arari

10q colombiensis - S. Francisco

colombiensis - Guaibacoa

0.1 4007 atrox - Suriname

atrox - Fr. Guyana

Q7ig4— atrox - Guyana

ioof /eucurus - D. Martins

leucurus - Salvador

88™ /eucurus - P. Seguro/ T. Freitas

Fig. 1 Maximum parsimony (top) and maximum likelihood (bottom) estimates of the phylogeny of Bothrops. In the MP tree, numbers before the slash

refer to bootstrap support, numbers after the slash indicate Bremer support. In the ML tree, numbers on nodes indicate bootstrap support.

104

monophyly of the B. asper-atrox complex, 1.e., that the Antillean

populations originate from within the B. asper-atrox complex; (ii1)

non-monophyly of the South American B. atrox complex, i.e., that

the Antillean species originate from within the cis-Andean B. atrox

complex, paralleling the phylogeography of Corallus (Henderson &

Hedges, 1995); and (iv) monophyly of B. caribbaeus, B. lanceolatus,

B. asper and northern Venezuelan populations of the B. asper-atrox

complex to the exclusion of the cis-Andean B. atrox complex, as

implied by the classification of Sandner Montilla (1990). We used

Wilcoxon signed-ranks (WSR) tests (Templeton tests — Templeton,

1983) to compare the optimal MP tree and MP trees depicting

alternative hypotheses, and Shimodaira—Hasegawa (SH) tests

(Shimodaira & Hasegawa, 1999) to compare the corresponding ML

trees.

RESULTS

We aligned a total of 1401 b.p. of mtDNA sequence information

(ND4: 693 b.p.; cytb: 708 b.p.). The sequences included no indels or

stop or other nonsense codons, and contained the usual bias towards

transitions and substitutions concentrated into third codon positions

typical of mitochondrial DNA. We conclude that our sequences

represent mtDNA rather than nuclear insertions. Samples are listed

in Appendix 1. The 100,000 random trees generated a skewness

statistic of g1=—0.599403, rejecting the null hypothesis that the data

contain no significant phylogenetic signal (P < 0.01; Hillis and

Huelsenbeck, 1992).

Levels of sequence divergence among the taxa included ranged

from 0.3% to 13.65% (unadjusted p-distance). Bothrops caribbaeus

and B. lanceolatus differ from each other by 4.3%, and from the B.

asper-atrox group by an average of 5.77% and 6.15% respectively,

with an average divergence of 5.9% when the Antillean haplotypes

are treated as a single clade. Levels of sequence divergence within

the B. asper-atrox clade range from 0.3% to 5.5%

The MP analysis resulted in a single most parsimonious tree of

1030 steps (CI 0.5398; HI 0.4602; RI 0.6465). In this tree, the two

Antillean taxa formed a clade, which in turn forms the sister clade of

all samples of the Bothrops asper-atrox complex (Fig. 1).

The MODELTEST software identified the GTR+I+G model, a

submodel of the general time-reversible model (Yang et al., 1994) as

optimal for the data at hand. A ML tree was constructed using the

parameters calculated by MODELTEST, and the parameters were

recalculated from the resulting tree, and used in a further ML search,

which resulted in a tree with the likelihood score -In(L)= 6652.69 122.

Further estimates of sequence evolution parameters did not result

in any change of parameter values or tree likelihood score (Fig. 1).

The MP and ML trees differ only in branching order within the cis-

Andean B. atrox complex, and in the relative position of the B.

Jararacussu-brazili clade and B. punctatus.

The results of our tests of alternative tree topologies are shown in

W. WUSTER ETAL.

Table 1. Neither the WSR nor the SH test significantly reject the

possibility that the two Antillean species may be the result of

separate colonizations of the Lesser Antilles, although the result of

the SH test was almost significant. They do, however, significantly

reject the hypothesis that the Antillean species originate from within

the cis-Andean radiation of the B. asper-atrox complex, and also

reject Sandner Montilla’s suggestion of conspecificity between B.

lanceolatus, B. caribbaeus, B. asper and northern Venezuelan

Bothrops, to the exclusion of other South American populations of

the B. atrox group.

DISCUSSION

Our results confirm the position of the Antillean species of Bothrops

as the sister clade of the Bothrops asper-atrox complex, as suggested

by Salomao et al. (1997, 1999) and Wiister et al. (1997, 1999). The

monophyly of the Antillean taxa is supported by high bootstrap and

Bremer support values, although a tree supporting this arrangement

is not significantly longer than the optimal tree constrained not to

include this clade.

The high level of sequence divergence between the Antillean

Bothrops and their mainland relatives (5.9%) is consistent with a

lineage split dating back to the Miocene or earliest Pliocene. Wiister

et al. (in press) suggested a rate of sequence evolution for cytb and

ND4 of between 0.66 and 1.4% My in Neotropical pitvipers. This

would date the timing of the split between the Antillean Bothrops

clade and the B. asper-atrox clade at 4.2-8.9 Mya, i.e., the late

Miocene or earliest Pliocene. Similarly, the split between B.

caribbaeus and B. lanceolatus (sequence divergence: 4.3%) can be

dated to 3.1-6.5 Mya. Hedges (1996) estimated the divergence of

the B. asper-atrox complex to have taken place within the last 4 My,

and assumed dispersal to the Antilles to have taken place during that

timeframe, whereas our data suggest a slightly earlier lineage split.

In any case, it can be concluded that the two Antillean Bothrops

species represent two relatively old, independent lineages. Obviously,

in view of the errors inherent in any attempt at molecular clock

usage, these estimates should be treated as approximations rather

than exact timings.

The notion that these populations are the result of a recent

dispersal event from within South America, as is the case in West

Indian Corallus (Henderson & Hedges, 1995), is refuted by both

tree topology and statistical tree comparison tests. Equally, the

notion that the presence of these snakes in the Lesser Antilles is the

result of a primitive form of biological warfare among aboriginal

people (Dowling, 1965) will have to be abandoned, despite its

romantic appeal.

The colonisation sequence of the two species can be resolved

from morphological data, particularly scalation. In terms of dorsal

and ventral scale counts, B. caribbaeus is indistinguishable from

many populations of the B. asper-atrox complex. On the other hand,

Table 1 Differences in tree length or likelihood, statistics, and their significance, between the most parsimonious or the most likely trees, and trees

constrained to be compatible with alternative phylogenetic or biogeographical hypotheses.

d(steps)

Non-monophyly of B. caribbaeus and B. lanceolatus 7

Non-monophyly of B. asper-atrox complex 5

Non-monophyly of cis-Andean B. atrox complex 15

Monophyly of B. caribbaeus, lanceolatus, asper 18

and northern Venezuelan populations

Wilcoxon signed-ranks

Shimodaira—Hasegawa

-Z ie d(InL) Ip

1.4000 0.1615 15.05075 0.054

1.1471 — 1.5076 0.1317-0.2513 3.15866 0.181

2.4019 0.0163* 20.06423 0.018*

2.9200 — 3.0870 0.002 — 0.0035* 24.34213 0.005*

em fh 6 aati

ANTILLEAN BOTHROPS

B. lanceolatus has higher ventral and dorsal scale row counts than

practically all populations of the B. jararacussu-punctatus-atrox

clade. This suggests that the extreme scale counts found in B.

lanceolatus represent an autapomorphy compared to B. caribbaeus

and mainland Bothrops. This makes a hypothesis of dispersal from

the mainland to St. Lucia, and then a further dispersal event to

Martinique, more parsimonious than dispersal to Martinique

followed by further dispersal to St. Lucia. Since St. Lucia lies

between South America and Martinique, this scenario is also more

geographically parsimonious than the alternative. The slightly

greater length of the branch leading to B. lanceolatus is also consist-

ent with this hypothesis (De Salle & Templeton, 1988; Thorpe et al.,

1994).

An understanding of the phylogenetic position of Bothrops

caribbaeus and B. lanceolatus may also have implications for their

venom composition and the treatment of snakebite in the Caribbean.

Bothrops lanceolatus envenoming has been documented to produce

a unique syndrome different from that of other species of Bothrops.

In addition to local symptoms such as pain, swelling, bleeding at the

site of the bite, ecchymosis and necrosis, which are common to most

crotaline envenomings, the systemic bothropic syndrome observed

in Central and South America is characterised by the development of

consumption coagulopathies and spontaneous systemic bleeding,

depending on venom components which affect clotting factors as

well as haemorrhagins which damage vascular endotheliums

(Barrantes et al, 1985; Kamiguti ef a/, 1991). On the other hand,

apart from similar local signs, the severity of systemic envenoming

by Bothrops lanceolatus in Martinique was correlated with the

development of multiple cerebral infarctions and/or other major

vessel occlusion that may appear within 8 hours to 7 days after the

bite in approximately 30 to 40% of cases (Thomas er al, 1995, 1998).

Infarctions can develop in patients who present initially with signs

of moderate envenoming with normal blood clotting and low serum

levels of venom antigens. The infarction process can involve several

small vascular territories altogether, and is associated with the

development of an isolated thrombocytopenia. Bogarin et al. (1999)

demonstrated that Bothrops lanceolatus venom, obtained from 20

specimens collected at different locations in Martinique, is devoid of

thrombin-like enzymes and of in vitro coagulant and defibrinating

activities, and is not coagulant when added to human citrated

plasma, even at concentration as high as 100 g/mL. These data

suggest that thromboses observed in human B. lanceolatus enven-

oming result from a toxin-linked vasculitis process rather than from

a systemic procoagulant effect. However, the exact thrombogenic

mechanism responsible for these thromboses remains unexplained.

The monophyly of Bothrops lanceolatus and B. caribbaeus leads to

the prediction that these snakes may share venom properties, which

may in turn be of importance for the treatment of patients bitten by

these snakes. In particular, do bites by B. caribbaeus result ina similar

thrombotic syndrome as observed in B. lanceolatus? Bothrops

caribbaeus envenoming was poorly documented until now. However,

the case of a 32 year old man who was bitten in Saint Lucia and who

subsequently developed multiple cerebral infarctions in the anterior

and posterior cerebral artery territories was recently published (Nu-

meric et al, 2002). The clinical presentation of this patient was

identical to that of patients bitten by Bothrops lanceolatus. Thus,

envenomings from these two species develop a unique systemic

thrombotic syndrome, which differs fundamentally from the defibri-

nation and bleeding syndrome that characterizes all other Bothrops

asper-atrox complex envenomations. This example suggests that, at

least in some cases, an understanding of the phylogeny of medically

important snakes can help predict the syndrome of envenoming to be

expected from a hitherto undocumented species.

105

Our results also have implications for the conservation of the

Antillean Bothrops. Our data show that both B. caribbaeus and B.

lanceolatus represent relatively old, independent evolutionary line-

ages, and not recent offshoots of widespread South American taxa.

Conservation policy on their respective islands needs to take this into

account. Although Lazell (1964) described both B. lanceolatus and

especially B. caribbaeus as common (and Dowling, 1965, reported

similar experiences for the latter), more recent workers have reported

these snakes to be harder to find (Powell & Wittenberg, 1998). These

observations indicate that B. caribbaeus and B. lanceolatus may have

suffered a decline in population numbers over the last few decades, and

that a reassessment of their conservation status should be a priority.

Finally, this paper also represents an opportunity to clarify some

confusion surrounding the nomenclature and synonymy of the

Caribbean Bothrops. As noted by Hoge & Romano Hoge (1978/79)

and subsequent authors, the St. Lucian lancehead was described

under several different names by Gray (1842). Species of Bothrops

described by Gray (1842) include B. cinereus (‘America’), B. sabinii

(‘Demerara’), and B. subscutatus (‘Demerara’). Gray (1849) also

described B. affinis (‘Demerara’ and ‘Berbice’).

The types of B. sabinii and B. subscutatus were the specimens

collected by Capt. (later Col.) Sabine discussed by Underwood

(1993), and are unquestionably assignable to B. caribbaeus

(Underwood, 1993; pers. obs.), of which the names B. subscutatus

and B. sabinii therefore represent senior synonyms. However, the

precedence of Garman’s well-established name B. caribbaeus over

Gray’s disused names was formally established by Wiister (2000).

The female type specimen of Bothrops cinereus, considered incertae

sedis by Peters & Orejas-Miranda (1970) and conspecific with B.

caribbaeus by Hoge & Romano Hoge (1978/79) and Powell &

Wittenberg (1998), has 31 scale rows at midbody and 224 ventral

scales. These counts are consistent with B. /anceolatus, but not with B.

caribbaeus; B. cinereus is thus a junior synonym of B. lanceolatus.

The syntypes of B. affinis are assignable to B. atrox, and are consistent

with Guyanan populations of that species based on both scalation (24—

27 dorsal scale rows, 189-200 ventrals) and colour pattern.

ACKNOWLEDGEMENTS. We thank A. Malhotra, N.C. Giannasi and A.

Tanasi (Office National des Forets de la Martinique) for help with sample

acquisition, and C.J. McCarthy for access to the types of Gray’s species of

Bothrops. Finally, Garth Underwood provided enlightening information on

Capt. Sabine’s specimens, as well as being an inexhaustible font of knowledge

on taxonomic matters of all kinds over many years. This study was funded by

the Wellcome Trust (Research Career Development Fellowship to WW, and

grant 057257//Z/99/Z), the EU (contracts TS3-CT91-0024 and IC18-CT96-

0032), Fundagao Banco do Brasil, Fundagao de Amparo a Pesquisa do

Estado de Sao Paulo (FAPESP) (grants 95/90 56-9, 97/2445-5 and 00/01850-

8), and the British Council (fellowship to MGS).

REFERENCES

Barrantes, A., Solis, V. & Bolanos, R. 1985. Alteraci6n en los mecanismos de la

coagulacion en el envenenamiento por Bothrops asper (terciopelo). Toxicon 23:

399-407.

Bogarin, G., Romero, M., Rojas, G., Lutsch, C., Casadamont, M., Lang, J., Otero,

R. & Gutiérrez, J.M. 1999. Neutralization, by a monospecific Bothrops lanceolatus

antivenom, of toxic activities induced by homologous and heterologous Bothrops

snake venoms. Toxicon 37; 551-557.

Bremer, K. 1994. Branch support and tree stability. Cladistics 10: 295-304.

Campbell, J.A. & Lamar, W.W. 1989. The Venomous Reptiles of Latin America.

Comstock, Ithaca & London.

106

DeSalle, R. & Templeton, A.R. 1988. Founder effects and the rate of mitochondrial

DNA evolution in Hawaiian Drosophila. Evolution 42: 1076-1084.

Dowling, H.G. 1965. The puzzle of Bothrops; or, a tangle of serpents. Animal Kingdom

68: 18-21.

Gray, J.E. 1842. Synopsis of the species of rattle-snakes, or family of Crotalidae.

Zoological Miscellany, Parts 2/3: 47-51.

. 1849. Catalogue of Specimens of Snakes in the Collection of the British Museum.

Edward Newman, London.

Hedges, S. B. 1996. The origin of West Indian Amphibians and Reptiles. pp. 95-128.

In: Powell, R. & Henderson, R.W. (eds) Contributions to West Indian Herpetology.

A tribute to Albert Schwartz. SSAR, Ithaca.

Henderson, R.W. & Hedges, S.B. 1995. Origin of West Indian populations of the

geographically widespread boa Corallus enydris inferred from mitochondrial DNA

sequences. Molecular Phylogenetics and Evolution 4: 88-92.

Hillis, D.M. & Huelsenbeck, J.P. 1992. Signal, noise and reliability in phylogenetic

analyses. Journal of Heredity 83: 189-195.

, Mable, B. K. & Moritz, C. 1996. Applications of molecular systematics: the state

of the field and a look to the future. pp. 515—543. In: Hillis, D.M., Moritz, C. & Mable,

B. K. (eds) Molecular Systematics, 2" edition. Sinauer, Sunderland, Massachusetts.

Hoge, A.R. 1952. Notas erpetolégicas. Revalidagao de Bothrops lanceolata (Lacépéde).

Memorias do Instituto Butantan 24: 231-236.

& Romano-Hoge, S.A.R.W.L. 1978/79. Poisonous snakes of the World. Part I.

Checklist of the pit vipers, Viperoidea, Viperidae, Crotalinae. Memorias do Instituto

Butantan 42/43: 179-310.

Kamiguti A.S., Cardoso J.L.C., Theakston R.D.G., Sano-Martins I.S., Hutton

R.A., Rugman E.P., Warrell D.A. & Hay, C.R.M. 1991. Coagulopathy and haem-

orrhage in human victims of Bothrops jararaca envenoming in Brazil. Toxicon 29:

961-972.

Kumar, S. 1996. PHYLTEST: A Program for Testing Phylogenetic Hypothesis.

Version 2. The Pennsylvania State University, University Park, Pennsylvania.

Lazell, J.D. 1964. The Lesser Antillean representatives of Bothrops and Constrictor.

Bulletin of the Museum of Comparative Zoology 132: 245-273.

Malhotra, A. & Thorpe, R.S. 1999. Reptiles and Amphibians of the Eastern Carib-

bean. MacMillan, London.

& . 2000. The dynamics of natural selection and vicariance in the Dominican

anole: comparison of patterns of within-island molecular and morphological diver-

gence. Evolution 54; 245-258.

Numeric, P., Moravie, V., Didier, M., Chatot-Henry, D., Cirille, S., Bucher, B. &

Thomas, L. In press. Multiple cerebral infarctions following a snakebite by Bothrops

caribbaeus. American Journal of Tropical Medicine and Hygiene.

Peters, J.A. & Orejas-Miranda, B. 1970. Catalogue of the Neotropical Squamata.

Part I. Snakes. Bulletin of the United States National Museum 297: \-347.

Pook, C. E., Wiister, W. & Thorpe, R. S. 2000. Historical biogeography of the western

rattlesnake (Serpentes: Viperidae: Crotalus viridis), inferred from mitochondrial

DNA sequence information. Molecular Phylogenetics and Evolution 15: 269-282.

Posada, D. & Crandall, K.A. 1998. Modeltest: testing the model of DNA substitution.

Bioinformatics 14: 817-818.

Powell, R. & Wittenberg, R.D. 1998. Bothrops caribbaeus (Garman) Saint Lucia

Lancehead. Catalogue of the American Amphibians and Reptiles (676): 1+.

Puorto, G., Salomao, M.G., Theakston, R.D.G., Thorpe, R.S., Warrell, D.A. &

Wiister, W. 2001. Combining mitochondrial DNA sequences and morphological

data to infer species boundaries: phylogeography of lanceheaded pitvipers in the

Brazilian Atlantic forest, and the status of Bothrops pradoi (Squamata: Serpentes:

Viperidae). Journal of Evolutionary Biology 14: 527-538.

Salomao, M.G., Wiister, W., Thorpe, R.S., Touzet, J.-M. & B.B.B.S.P. 1997. DNA

evolution of South American pitvipers of the genus Bothrops. pp. 89-98. In: Thorpe,

R.S., Wiister, W. & Malhotra, A. (eds). Venomous Snakes: Ecology, Evolution and

Snakebite. Clarendon Press, Oxford.

. 7 & B.B.B.S.P. 1999. MtDNA phylogeny of Neotropical pitvipers of

the genus Bothrops (Squamata: Serpentes: Viperidae). Kaupia 8: 127-134.

Sandner Montilla, F. 1981. Una nueva subespecie de Bothrops lanceolatus (Lacépéde,

1789) Familia Crotalidae. Memorias Cientificas de Ofidiologia 6: 1-15.

——. 1990. Bothrops lanceolatus (Lacepéde, 1789). Redescripcion amplia y bastante

de la especie. Estudio completo sobre su taxonomia y caracteristicas morfoldgicas.

Memorias Cientificas de Ofidiologia 10: 1-47.

Shimodaira, H. & Hasegawa, M. 1999. Multiple comparisons of log-likelihoods with

applications to phylogenetic inference. Molecular Biology and Evolution 16: 1114—

1116.

Swofford, D. L. 2001. PAUP* — Phylogenetic Analysis Using Parsimony (*and Other

Methods). Beta version 4.0b8. Sinauer, Sunderland, Massachusetts.

Templeton, A.R. 1983. Phylogenetic inference from restriction endonuclease cleavage

sites maps with particular reference to the evolution of humans and the apes.

Evolution 37: 221-244.

Thomas, L., Tyburn, B., Bucher, B., Pecout, F., Ketterlé, J., Rieux, D., Smadja, D.,

Garnier, D., Plumelle, Y. & Research Group on Snake Bite in Martinique. 1995.

Prevention of thromboses in human patients with Bothrops lanceolatus envenoming

in Martinique: failure of anticoagulants and efficacy of a monospecific antivenom.

American Journal of Tropical Medicine and Hygiene 52: 419-426.

W. WUSTER ETAL.

——, ——,, Ketterlé J., Biao T., Mehdaoui H., Moravie V., Rouvel C., Plumelle Y.,

Bucher B., Canonge D, Marie-Nelly C.A., Lang J. and other members of the

Research Group on Snake Bites in Martinique. 1998. Prognostic significance of

clinical grading of patients envenomed by snake Bothrops lanceolatus in Martinique.

Transactions of the Royal Society of Tropical Medicine and Hygiene 92: 542-545.

Thorpe, R. S., Malhotra, A., Stenson, A. & Reardon, J.T. in press. Adaptation and

Speciation in Lesser Antillean Anoles. In Deickmann, U., Metz, H.A.J., Doebeli, M.

& Tautz, D. (eds). Adaptive Speciation. Cambridge University Press, Cambridge.

, McGregor, D.P., Cumming, A.M. & Jordan, W.C. 1994. DNA Evolution and

colonization sequence of island lizards in relation to geological history: MtDNA

RFLP, cytochrome b, cytochrome oxidase, 12srRNA sequence and nuclear RAPD

analysis. Evolution 48: 230-240.

Underwood, G. 1993. A new snake from St. Lucia, West Indies. Bulletin of the Natural

History Museum (Zoology) 59: 1-9.

Wiister, W. 2000. Precedence of names in wide use over disused synonyms or

homonyms in accordance with Article 23.9 of the Code. Reptilia, Serpentes (1)

Trigonocephalus caribbaeus Garman, 1887. Bulletin of Zoological Nomenclature

EWB SY):

, Salomao, M.G., Quijada-Mascarenas, J.A., Thorpe, R.S. & B.B.B.S.P. in

press. Origin and evolution of the South American pitviper fauna: evidence from

mitochondrial DNA sequence analysis. In: Schuett, G.W., Héggren, M. & Greene,

H.W. (eds). Biology of the Vipers. Biological Sciences Press, Carmel, Indiana.

——, ——, Duckett, G.J., Thorpe, R.S. & B.B.B.S.P. 1999. Mitochondrial DNA

phylogeny of the Bothrops atrox species complex (Squamata: Serpentes: Viperidae).

Kaupia 8: 135-144.

; , Thorpe, R.S., Puorto, G., Furtado, M.F.D., Hoge, S.A., Theakston,

R.D.G. & Warrell, D.A. 1997. Systematics of the Bothrops atrox species complex:

insights from multivariate analysis and mitochondrial DNA sequence information.

pp. 99-113. In: Thorpe, R.S., Wiister, W. & Malhotra, A. (eds). Venomous Snakes:

Ecology, Evolution and Snakebite. Clarendon Press, Oxford.

Yang, Z., Goldman, N. & Friday, A. 1994. Comparison of models for nucleotide

substitution used in maximum-likelihood phylogenetic estimation. Molecular Biol-

ogy and Evolution 11: 316-324.

Zhang, D.-X. & Hewitt, G.M. 1996. Nuclear integrations: challenges for mitochon-

drial DNA markers. Trends in Ecology and Evolution 11: 247-251.

Appendix 1

Origin and vouchers of samples sequenced in this study. Institu-

tional Codes for vouchers: IB = Instituto Butantan, Sao Paulo,

Brazil, Herpetological Collection. FHGO = Fundacion Herpetologica

Gustavo Orcés, Quito, Ecuador. INHMT = Instituto de Higiene y

Medicina Tropical ‘L. Izquieta Pérez’, Guayaquil, Ecuador. ROM =

Royal Ontario Museum, Toronto. WW = Wolfgang Wiister collec-

tion. Collection numbers refer to preserved specimens unless

otherwise stated. Photographs and/or morphological data for many

unvouchered specimens are available from the first author.

Bothrocophias microphthalmus: ECUADOR: Zamora Chinchipe:

Cuenca del Rio Jamboe: Pumbami. FHGO 2566. Bothrops alternatus:

BRAZIL: Parana: Pinhao. IB 55314. B. asper: Belize: Mile 38, West-

ern Highway. WW 264. B. atrox: BRAZIL: Para: Santa Izabel. WW

735. Maranhao: Sao Bento: WW 723. FRENCH GUYANA: Mana.

WW 554. GUYANA: NorthWest District: Baramita. ROM 22848.

SURINAME: Coronie District: 7.5 km E. Totness. WW 537. B.

brazili. ECUADOR: Morona Santiago: Macuma. FHGO 982. B.

caribbaeus: SAINT LUCIA: Grande Anse. WW 144 WW 148. B.

colombiensis: VENEZUELA: Guarico: Altagracia de Orituco. WW

74. Falcon: San Francisco. J.L. Yrausquin, live coll. Guaibacoa. J.L.

Yrausquin, live coll. B. insularis: BRAZIL: Sao Paulo: Ilha da Quei-

mada Grande. Released after sampling. B. jararaca: BRAZIL: Parana:

Piracuara. WW 926. B. jararacussu: BRAZIL: Sao Paulo: Cananéia.

1B 55313. B. lanceolatus: MARTINIQUE. Not vouchered. B. leucurus:

BRAZIL: Bahia: Porto Seguro. IB 55480-1; Salvador. IB 55478.

Espirito Santo: Domingos Martins. IB 55557. B. marajoensis: BRA-

ZIL: Para: Ilha de Maraj6: 10 km NW Camara. WW 80. Santa Cruz do

Arari: WW 943. B. pulcher: ECUADOR: Zamora Chinchipe: Estacion

Cientifica San Francisco. FHGO live coll. 2142. B. punctatus: ECUA-

DOR: Pichincha: Pedro Vicente Maldonado. FHGO live coll. 2166. B.

taeniatus: ECUADOR: Morona Santiago: Macuma. FHGO 195.

a a ae

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 107-111

ea |

rs So,

Issued 28 November 2002

A contribution to the systematics of two

commonly confused pitvipers from the Sunda

Region: Trimeresurus hageni and T.

sumatranus

K. L. SANDERS, A. MALHOTRA AND R. S. THORPE

School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, Wales, UK.

SYNOPSIS. The systematics of two Southeast Asian green pitviper species, Trimeresurus hageni and T. sumatranus, are investi-

gated by canonical variate analysis. Preliminary results reveal two morphological forms corresponding to mainly 7. hageni in West

Malaysia, Thailand and Singapore and 7: sumatranus in Borneo. Allopatric populations of both taxa are examined from Sumatra.

Geographic variation is present in both species, which are distinguished mainly by head scalation, but also by colour and pattern.

INTRODUCTION

Trimeresurus sumatranus (Raffles, 1822) and 7: hageni (Lidth de

Jeude, 1886) are closely related species, occupying low elevations

in undisturbed forests and having largely overlapping ranges. The

systematics of these species and their precise distribution is an area

of long-standing confusion. Many workers assign both species to 7.

sumatranus by default (Tweedie, 1983; Lim, 1991; Jintakune, 1995;

David and Vogel, 1996) and the status of 7. hageni has been in

dispute since its initial description (Lidth de Jeude, 1886; Lidth de

Jeude, 1890; Boulenger, 1896; Brongersma, 1933).

T. hageni was described as a separate species from 7. sumatranus on

the basis that only one or two supralabial scales are in contact with the

subocular (compared with three in 7: sumatranus), and the dark edges

on head and body scales and dorsal cross-bands that are characteristic

of T. sumatranus are not present (Lidth de Jeude, 1886). The species’

distribution is widely debated, but specimens from south Thailand,

West Malaysia and Singapore are normally assigned to T: hageni, and

specimens from Borneo are normally assigned to 7: swmatranus

(David and Vogel, 1996; Cox et al., 1998; Stuebing and Inger, 1999),

but see Dring (1979) who placed specimens in the NHM collections

from West Malaysia, southern Thailand and Sarawak in 7: sumatranus.

Both species are thought to occur on Sumatra and surrounding islands

(Brongersma, 1933; Dring et al., 1989; Cox et al., 1998).

There have been few attempts to resolve the systematics of T.

hageni and T. sumatranus since their initial description; these have

been based on small sample sizes and a traditional character-by-

character approach (Boulenger, 1896; Brongersma, 1933). Given

the levels of geographic, ontogenetic and sexual variation usually

present in viper species (Wiister et al., 1992; Malhotra and Thorpe,

1997), the systematics of these taxa is best approached using modern

Statistical methods based on a broad range of morphological

characters. In this paper, we present preliminary results from an

ongoing investigation of the systematics and interrelationships of T.

hageni and T. sumatranus.

MATERIALS AND METHODS

We examined 78 specimens from museum collections in the United

States, Europe and Malaysia (Figure 1). A total of 93 characters

relating to scalation, colour and pattern were recorded for each

specimen. Ventral scales were counted from head to vent, with the

first ventral identified according to the method of Dowling (1951).

The positions of scale reductions along the body (recorded as the

number of the ventral or subcaudal scale opposite which it was

situated) were transformed to percentage ventral scale (% VS) or

caudal scale (%CS) position, in order to compensate for variation in

ventral and subcaudal scale number. Male and female specimens

were treated separately in all analyses to avoid bias caused by sexual

dimorphism.

Specimens were grouped by locality into operational taxonomic

units (OTUs). Two groups dominated the analysis, one was com-

prised of specimens from Thailand, West Malaysia and Singapore,

and another was comprised of specimens from Borneo (Sabah and

Sarawak). These groups were shown to be monophyletic by mole-

cular analysis (unpublished data), which revealed a clear

distinction between western specimens that lacked dorsal cross-

bands and had at most two supralabials connected to the subocular

scale, and eastern specimens that had dorsal cross-bands and had

three supralabials in contact with the subocular scale. Molecular

data was not available for specimens from Sumatra, and these

were grouped individually to avoid combining sympatric species

in one OTU.

Each OTU was checked prior to further analysis using Princi-

pal Component Analysis, which does not require that individuals

be assigned groups prior to the analysis. The integrity of the

OTUs was confirmed with the exception of one specimen from

Betong (south Thailand), which had dark banding and in the PCA

ordination was closest to the Borneo OTU. In subsequent analysis

this specimen was grouped separately from the other western

specimens. The OTUs used and their sample size for each sex is

listed in Table 1.

Variation between OTUs was tested for individual characters by

means of one-way analysis of variance (ANOVA). Only characters

showing significant between-OTU variation were used in subse-

quent analyses. These are presented in Table 2.

Canonical variate analysis (CVA) was used to investigate patterns

of geographic variation between OTUs. This method maximises the

separation between groups relative to variation within groups. It is a

standard multivariate method and has been applied successfully to

numerous models of geographic variation in reptiles (Wiister ef al.,

1992; Thorpe et al., 1994; Daltry et al., 1996).

108

MALAYSIA

SUMATRA

K.L. SANDERS ET AL.

PALAWAN

BORNEO

JAVA

Fig. 1 Geographic origin of specimens used in multivariate analysis. S = Trimeresurus sumatranus; H = Trimeresurus hageni; U = unidentified

specimens. Shading represents the known distribution of T: hageni and/or T. sumatranus.

Table 1 List of OTUs and sample size for each sex.

OTU Sample Size

Males Females

Thailand, West Malaysia, Singapore 16 15

North Sumatra 1 (Medan) 1 1

North Sumatra 2 (Medan) 0 1

Central Sumatra | (Padang) 1 1

Central Sumatra 2 (Padang) 0 1

South Sumatra 1 (Palembang) 0 1

Nias 1 10

Siberut 3 3

East Malaysia 4 18

Betong (south Thailand) 1 0)

Total 2, 5)

Museum Acronyms

BMNH The Natural History Museum, London, formerly the

British Museum (Natural History), London

FMNH Field Museum of Natural History, Chicago

IMR Institute of Medical Research, Kuala Lumpur

KSP Sabah Park Zoological Museum, Mount Kinabalu

National Park, Sabah

MCZ Museum of Comparative Zoology, Harvard

MHNG Museum d Histoire Naturelle de Geneva, Switzerland

NMBA Naturhistorisches Museum Basel, Switzerland

NMW Naturhistorisches Museum Vienna, Austria

QSMI Queen Saovabha Memorial Institute, Bangkok

PH Perhelitan, Kuala Lumpur

ZRC Raffles Museum of Biodiversity Research, National

University of Singapore, Singapore

RESULTS

The CVA of males shows clear separation along the first canonical

variate of specimens normally assigned to T. hageni from Thailand,

West Malaysia and Singapore and those normally assigned to T.

sumatranus from East Malaysia. The Siberut OTU and the single

specimens from Nias and northern Sumatra are closest to the main-

land T: hageni population. The specimens from Betong, Thailand

and central Sumatra are closest to the Borneo OTU, but are well

differentiated on CV2.

Analysis of females also shows strong differentiation between the

Thailand, West Malaysia and Singapore OTU and the Borneo OTU.

The Siberut and Nias specimens are phenotypically close to T.

hageni from Thailand, West Malaysia and Singapore. Specimens

from north and south Sumatra are also closely affiliated to this

mainland population. The specimens from central Sumatra are

closest to the Borneo population along CV1, although are clearly

differentiated on CV2.

CVA analysis can be used to identify the characters that account

for most variation between groups. In both sexes scalation characters

were more important in distinguishing between the taxa than were

characters relating to colour and pattern. The most important character

is the fifth supralabial scale, which meets the subocular scale in T.

sumatranus and in T. hageni is separated from the subocular by one

scale. Also important is the frequent presence of an internasal scale

in T. sumatranus, which is usually lacking in T: hageni. In addition,

T. sumatranus has fewer supralabial scales and fewer scales between

supraoculars than T: hageni. Our work verifies two of the original

diagnostic characters used by Lidth de Jeude (1886) who described

T. hageni as a distinct species that lacks dorsal cross-bands and has

fewer supralabial scales in contact with the subocular scale. How-

ever, we did not find dark edging on head and body scales to be a

valid diagnostic character on the basis that T: hageni specimens from

Nias have very strong dark edges on their head and body scales.

DISCUSSION

The results of this preliminary analysis reveal a major phenotypic

bog eae

TRIMERESURUS HAGENI AND T. SUMATRANUS

Table 2 Characters used for multivariate analysis of T: sumatranus & T. hageni.

Characters

SSeS Se SSS See SS

RO OUND aly SON OS SIDS. Ot cP 9| IND

No. of ventral scales

No. of subcaudal scales

%NS position of reduction from 21 to 19 body scale rows

%NS position of reduction from 19 to 17 body scale rows

%DV position of reduction from 19 to 17 body scale rows

%NVS position of reduction from 17 to 15 body scale rows

%CS position of reduction from 14 to 12 tail scale rows

%DV position of reduction from 14 to 12 tail scale rows

%CS position of reduction from 10 to 8 tail scale rows

% DV position of reduction from 10 to 8 tail scale rows

%CS position of reduction from 8 to 6 tail scale rows

%CS position of reduction from 6 to 4 tail scale rows

No. of supralabial scales

No. of sublabial scales

No. of scales bordering the supraocular scales

Minimum no. of scales separating the supraocular scales

Maximum no. of scales separating the supraocular scales

No. of internasal scales

No. of scales separating the fourth supralabial scale form the subocular scale

No. of scales separating the fifth supralabial scale form the subocular scale

21. No. of scales contacting the suboculars, excluding the preoculars and postoculars

22. Average no. of scales between the first ventral scales and the anterior genial scales

23. No. of scales between the last sublabial scales and first vental scales * *

24. Presence of stripe on dorsal scale row one * =

25. No. of scale rows involved in stripe *€ a

26. __ Presence of postocular stripe = *

27. No. of scale rows involved in postocular stripe ~ =

28. Presence of dark edging on body scales *

29. _No. of bands on body ** *

30. Mean no. of scales of three half bands on body = *

31. Mean no. of scales between three half bands on body -

32. Presence of dark edging on head scales +

* indicates significance value p=<0.05 (ANOVA).

division in both sexes. This corresponds to 7: sumatranus in Borneo,

central Sumatra and southern Thailand and 7; hageni in southern

Thailand, West Malaysia, Singapore, north Sumatra, south Sumatra,

Nias and Siberut. The species are best distinguished by head scalation,

but can also be identified by colour and pattern.

Geographic variation is also present at the intra-specific level.

The Siberut and Nias specimens show stronger differentiation in

males than in females. Their phenotypic similarity to mainland 7:

hageni is based mainly on scalation characters. Moreover, on the

basis of colour and pattern, the Nias population is quite distinct with

head and body scales strongly edged in black. Nias was last con-

nected to Sumatra in the geologically recent past (c. 18,000 years

ago), whereas Siberut has been isolated for around one million years

(Dring et al., 1989). The extent to which these populations have

diverged from the mainland population will be investigated using

molecular methods and may lead to taxonomic revisions.

Sumatran populations are represented by few specimens, but

these exhibit the same general pattern in males and females: 7:

sumatranus from central Sumatra appear to be strongly differenti-

ated from the Borneo OTU, whereas 7: hageni from north and south

Sumatra are only weakly differentiated from the mainland OTU.

This pattern will be tested when additional data becomes available.

An analysis of the phylogenetic relationships of these populations,

using mitochondrial sequence data, is also underway and should

help to clarify their status.

ACKNOWLEDGEMENTS. We thank our collaborators at the University of

Science, Malaysia, and in particular Dr. Shahrul Anuar. We also thank the

staff and curators of the following institutions for allowing us access to their

specimens: BMNH, FMNH, IMR, KNP, MCZ, MHNG, NMBA, NMW, PH,

QSMI, ZRC. This study was supported by the Natural Environment Research

Council studentship to KLS (NER/S/A2000/03695), the Leverhulme Trust

(F/174/1 and F/174/O), the Wellcome Trust (057257/Z/99/Z and 060384/Z/

00/Z), and the Darwin Initiative (162/6/65) with additional support for

fieldwork from the Linnaean Society of London, Side, Bonhote, Omer-

Cooper and Westwood Fund.

REFERENCES

Boulenger, G.A. 1896. Catalogue of the Snakes of the British Museum (Natural

History). Volume Il. Containing the conclusion of the Colubridae, Amblycephalidae

and Viperidae. London, British Museum (Natural History).

Brongersma, L.D. 1933. Herpetological notes I -IX. Zoologische Mededeelingen

Leiden 16: 1-29.

Cox, M.J., van Dijk, P.P., Nabhitabhata, J. & Thirakhupt, K. 1998. A photographic

guide to snakes and other reptiles of Peninsular Malaysia, Singapore and Thailand.

New Holland, UK.

Daltry, J.C., Wiister, W. & Thorpe, R.S. 1996. Diet and snake venom evolution.

Nature 379: 537-540.

David, P. & Vogel, J. 1996. Snakes of Sumatra. Edition Chimaira, Frankfurt.

Dowling, H. G. 1951. A proposed standard system of counting ventrals in snakes.

British Journal of Herpetology 1: 97-99.

Dring, J.C.M., McCarthy, C.J. & Whitten, A.J. 1989. The terrestrial herpetofauna of

the Mentawai islands, Indonsia. Indo-Malayan Zoology 6: 119-132.

Dring, J.C.M.1979. Amphibians and Reptiles from northern Trengganu, Malaysia,

with descriptions of two new geckos. Bulletin of the British Museum (Natural

History), Zoology. 34(5): 181-241.

Jintakune, P. & C. Lawan. 1995. Venomous Snakes of Thailand. The Thai Red Cross

Society, Science Division, Bangkok.

Lidth de Jeude, T. W. Van. 1886. Note X. On Cophias wagleri, Boie and Coluber

sumatranus, Raffles. Notes Leyden Museum 8: 43-54.

110 K.L. SANDERS ET AL.

10 Qo

co) O Borneo

A Thailand

West Malaysia

0 Singapore

O Siberut

“5 a + Nias

@ north Sumatra

-10

a } * Betong

-20 4

“25 T T T

-80 -60 -40 -20

Se)

5 pa|

O Or ++ A. Thailand ’

os West Malaysia :

¥ | O a 4+ @® Singapore

O Siberut

VEN

-5 + Nias

@ north Sumatra

10 | © © central Sumatra

@ south Sumatra

-15 | ©

1 | | ) !

-20 -15 -10 -5 0 5 10 15 20

Fig. 2 Canonical Variate Analysis of 7: hageni and T. sumatranus populations (top = males; bottom = females).

TRIMERESURUS HAGENI AND T. SUMATRANUS

— 1890. Note VIII. On a collection of snakes from Deli. Notes Leyden Museum 12:

17-27.

Lim, B. L. 1991. Poisonous Snakes of Peninsular Malaysia. The Malayan Nature

Society, Malaysia.

Malhotra, A. & Thorpe, R. S. 1997. New perspectives on the evolution of south-east

Asian pitvipers (genus Trimeresurus) from molecular studies. Symposium of the

Zoological Society of London (70): 115-128.

Raffles, T. S. 1822. Sir T. S. Raffles’s Descriptive Catalogue of a Zoological Collection

made in Sumatra. Transactions of the Linnean Society of London 3(2): 333-334.

Stuebing, R.B. & Inger, R.F. 1999. A field guide to the snakes of Borneo. Natural

History Publications, Borneo.

Thorpe, R.S., Brown, R.P., Day, M., Malhotra, A., McGregor, D.P. & Wuster, W.

1994. Testing ecological and phylogenetic hypotheses in microevolutionary studies.

Chapter 8. In: Eggleton, P. & Vane-Wright, R. (eds). Phylogenetics and ecology. The

Linnean Society of London.

Tweedie, M. W. F. 1983. The Snakes of Malaya. Singapore National Printers Ltd.,

Singapore.

Wiister, W., Thorpe, R.S. & Puorto, G. 1996. Systematics of the Bothrops atrox

complex (Reptilia: Serpentes: Viperidae) in Brazil: A multivariate analysis.

Herpetologica 52(2): 263-271.

Wiister, W., Otsuka, S., Malhotra, A. & Thorpe, R.S. 1992. Population systematics

of Russell’s viper: A multivariate study. Biological Journal of the Linnean Society

47: 97-113.

Appendix 1 Specimens used in morphological

FMNH 239952

FMNH 239950

FMNH 239958

FMNH 239957

FMNH 239947

FMNH 138688

NMBA 9179

NMBA 5108

NMBA 22401

NMW 28160.4

NMW 28160.3

NMW 28160.2

NMW 28160.1

NMW 28157.1

NMW 28156.1

NMW 23909.2

NMW 28159.4

NMW 23909.3

NMW 28159.2

NMW 23909.4

NMW 28159.1

NMW 28158.1

NMW 28158.2

BMNH 1936.9.12.3

BMNH 1884.1.8.47

Tenom, Sabah

Kota Mardu, Sabah

Kapit District, Sarawak

Nias, Indonesia

Palembang, Sumatra

Pangna, Thailand

Nias, Indonesia

Medan, Sumatra

Padang, Sumatra

Kedah, W. Malaysia

Betong, Thailand

Nias, Indonesia

—

—_—

analysis BMNH 1884.1.8.46 Nias, Indonesia

BMNH 1884.12.31.13 Nias, Indonesia

BMNH 1884.12.31.14 Nias, Indonesia

MUSEUM/FIELD REF ~— LOCALITY SEX BMNH 1977.1237 Siberut, Indonesia

: BMNH 1979.267 Siberut, Indonesia

oan 11190 Eee ene a BMNH 1979.268 Siberut, Indonesia

MHNG 2072.87 2 : ; BMNH 1978.1879 G.Mulu, Sarawak

UE a ee BMNH 1880.9.10.7 Singapore

ae Ak os ca here aoe : BMNH 1936.9.12.5 Kuala Tekv, W. Malaysia

ee ais5 es £ap BMNH 1967.2290 G.Benom, W. Malaysia

SESE TES WEE = KSP 04361 Kota Mardu, Sabah

: - oe Nias hy : KSP 04362 Bukit Tawau, Sabah

as nee ose aa a 2 IMR 103649 Bukit Lakai, W. Malaysia

PH 10.79 aA ae ‘Ww cee on F IMR 104270 Simpang, W. Malaysia

PH no.134 Ulu Garmiak Ww ee aaa F IMR 104271 Ulu Gombak, W. Malaysia

Be riisare7 ; pia aed IMR 105684 Ulu Gombak, W. Malaysia

anda Baik, W. Malaysia F IMR 95995 Sinmpanios Wr Malan cit

FMNH 183788 Ulu Gombak, W. Malaysia M Os ae ae

j ZRC 2.2938 Siberut, Indonesia

FMNH 143948 Selangor, W. Malaysia M f :

Shree ZRC 2.2937 Siberut, Indonesia

FMNH 138690 Kapit District, Sarawak F : =

eae ZRC 2.2936 Siberut, Indonesia

FMNH 138689 Kapit District, Sarawak F KLS 01129 Pompe Sabah

FMNH 148829 Kapit District, Sarawak F Seanho ae aa

FMNH 148830 Kapit District, Sarawak F Se ie ae eo Rear:

FMNH 138687 Kapit District, Sarawak F isniea are uneage

FMNH 239948 Kota Mardu, Sabah F paar aga.

AFS 9815 Songkhla, Thailand

FMNH 239959 Mendolong, Sabah F = ;

FMNH 243943 Mendolong, Sabah F senna Siler ia toa

FMNH 230064 Danum Valley, Sabah F Base ee

FMNH 230063 Danum Valley, Sabah F AFS/KLS indicate wild caught specimens examined under anaesthesia.

Hon = =a << = a oS Sd Se ee Sd Se Se ed SS Se

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 113-121 Issued 28 November 2002

Underwood’s classification of the geckos: a 21*

century appreciation

ANTHONY P. RUSSELL

Department of Biological Sciences, University of Calgary, 2500 University Drive N.W., Calgary, Alberta,

Canada, T2N 1N4. email: arussell@ucalgary.ca

AARON M. BAUER

Biology Department, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085-1699, USA

SYNOPSIS. The publication in 1954 of Underwood’s ‘On the classification and evolution of geckos’ was the first comprehensive

attempt to understand the systematics, evolution and biogeography of this group of lizards. Combining the use of the exploration

of novel characters with a global overview of geckos, Underwood erected hypotheses of relationship and patterns of distribution.

In the 48 years since that landmark publication much has changed, but much has stayed the same. Underwood's division of geckos

into four major clusters is still recognised today, although the sphaerodactyls are now regarded as a group derived from within

the gekkonines, and the diplodactylines have been diminished by the removal of several genera and their placement in the

gekkonines. The framework that Underwood established has resulted in generic and/or species level phylogenies being generated

for the eublepharids, some sphaerodactyls, the carphodactyline diplodactylines and some clusters within the gekkonines. The

latter group, because of its size, has remained intractable to detailed systematic analysis at the generic level, although the

recognition of many discrete monophyletic clusters within the Gekkonidae (the Gekkoninae of Underwood) holds out the

possibility that greater levels of intergeneric resolution are close to realisation.

Underwood's initial approach to the systematic analysis of geckos was distinguished by its use of novel characters of the visual

system that led to new insights. It is possible that the next breakthrough in higher level systematic analysis of geckos may again

come from the exploitation of new character sources. Some examples of these possibilities are discussed.

INTRODUCTION

‘| We] would like to make a distinction between how [Dr. Underwood]

thought about the classification of [gekkotans] and what he thought,

since in [our] view how a man thinks is far more important than what

he thinks ... [we] suggest that how [Underwood] thought about

classification survives untarnished to this day. Does what he thought

about it bear critical scrutiny nearly fifty years later?’ With these

words (bracketed modifications aside) Garth Underwood (197 1a)

began his A Modern Appreciation of Camp’s ‘Classification of the

Lizards.’ Nearly 50 years after its publication we here consider

Underwood’s classification of the Gekkota, its central position in the

study of these lizards, its influence on subsequent work in the field

and how its conclusions have been modified over the intervening

decades. This work was Underwood’s first substantial contribution

- to squamate evolution, preceding other major contributions to the

systematics of pygopods (Underwood, 1957) and snakes

(Underwood, 1967) and establishing the way he was to think about

and employ character analysis in approaches to what had previously

been regarded as rather intractable problems.

Garth Underwood was interested in both the theory and practice

of systematics and also in the evolutionary morphology of the

organisms that he chose as the subjects of his systematic analyses.

He was bold in embracing novel sources of data for his systematic

analyses, put forward hypotheses of relationship in the hopes that

they would be scrutinised and evaluated by others, and frequently

returned to systematic problems that he had already published some

years earlier to bring fresh insights and approaches. Specimens

always figured prominently as a primary source of inspiration and

new data.

A comparison of the lizard families recognised by Boulenger

(1885), Camp (1923), and most modern workers (e.g., Macey er al.,

1997; Harris et al., 1999) reveals almost no discrepancies. The

gekkotan lizards, however, are an exception. Until the middle of the

20" century, lizard systematists variously recognised the

Eublepharidae and Uroplatidae as entities distinct from the

Gekkonidae. Different classificatory schemes reflected not only

different interpretations of characters, but alternative views of the

systematic meaning of novel morphologies. For most of the time

after the description of the first gecko genera by Laurenti (1768),

gecko systematics was dominated by alpha systematic treatments

and the allocation of newly discovered species to an ever growing

number of genera, defined chiefly by externally discernible digital

features. This reliance on digital characters as almost the sole

determinant of affinity resulted in the widespread recognition of

composite genera constituted by digitally convergent taxa. Further,

the focus on foot structure did little to resolve higher order relation-

ships among gekkotans, as the digital characters then recognised

suggested many discrete clusterings of species, but provided few

putative links between them.

Garth Underwood was led to the topic of gecko classification,

which he (1954:469) characterised as ‘far from stable’, through his

research on the reptilian eye. His earlier work on retinal morpholog

(Underwood 1951a) and pupil shape (Underwood 1951b) had both

highlighted the distinctiveness of the gecko eye and suggested that

ophthamological characters could be of use in the resolution of

higher order relationships among the many gecko genera.

Underwood’s optimism that the eye could provide useful characters

was bolstered by the then recent work of Bellairs (1948), who had

conclusively demonstrated that the true eyelids of the eublepharid

geckos were primitive to the derived condition of a well-developed

114

brille and lack of moveable lids typical of other geckos. Further,

Walls (1942) and Prince (1949) had examined the eyes of some

geckos in their broader ophthamological treatments, suggesting

avenues for further research.

Walls’ (1942) comprehensive treatment of the vertebrate eye led

Underwood to hypothesise that this organ system could yield useful

and stable associations of characters. The general recognition of the

retinal characteristics of the eyes of geckos as evidence of secondary

nocturnality, and a preliminary survey (Underwood 1951b) of the

form of the pupil suggested that a more intensive survey of pupil

form may provide a means by which gekkonids could be subdivided

into more manageable and meaningful subsets reflective of their

evolutionary history. Underwood (1954) set himself the task of

surveying a moderately comprehensive collection of preserved

geckos at the Museum of Comparative Zoology, Harvard Univer-

sity, and to analyse the resulting data. He used these data to erect the

first modern generic level analysis of gekkotan relationships. He

recognised potential problems with character state interpretation

caused by state of preservation and the limitations of a single-

character classification, but nonetheless regarded pupil character

states to be sufficiently discrete for the purpose of establishing a

workable classification of geckos, which would be subject to modifi-

cation as additional data became available. Werner (1977) later

demonstrated that pupil shape and dilation change with differing

light levels, and these observations have helped refine Underwood’s

(1954) initial conclusions (see below).

UNDERWOOD’S CLASSIFICATION OF THE

GECKOS

Underwood (1954) recognised three families of gekkotan lizards.

The Eublepharidae was characterised by true eyelids, the lack of a

spectacle and vertical pupils reflective of the nocturnal adaptations

of the family. The five genera he included were those subsequently

placed by Kluge (1967a) in his Eublepharinae, and by Kluge (1987)

and Grismer (1988) in the Eublepharidae. [Note: The current alloca-

tion of taxa employed in this article is based upon Kluge, 2001].

Underwood (1954) considered Aeluroscalabotes as the most primi-

tive member of the family. It has subsequently been regarded as the

sister group of all remaining eublepharids (Grismer, 1988).

Underwood’s Sphaerodactylidae was supported by the presence

of around, diurnal-type pupil (or eliptical or straight vertical pupil in

some cases), the existence of a fovea, and the presence of a specta-

cle. He included five genera therein, corresponding to Kluge’s

(1967a) Sphaerodactylinae and later Sphaerodactylini (Kluge 1987,

1995).

All remaining genera were placed in the Gekkonidae, character-

ised by a spectacle and lack of a fovea. Pupil shape was variable.

Within the Gekkonidae he recognised two subfamilies, the

Diplodactylinae and the Gekkoninae. The former had vertical pupils

with straight margins, or circular pupils. He included 22 genera in

this group. Among them are all of the genera now assigned to the

Diplodactylinae by Kluge (1967a) except for Eurydactylodes,

Pseudothecadactylus, and Crenadactylus. Underwood had doubts

about the placement of the first of these genera (see below), speci-

mens of which he had not examined himself, and changed its

allocation the following year (Underwood 1955). Crenadactylus

ocellatus was examined but was included with Phyllodactylus in the

Gekkoninae by Underwood (1954). The Diplodactylinae was subse-

quently retained by Kluge (1987) and Bauer (1990a), although its

affinities with the Pygopodidae were uncertain (see below).

A.P. RUSSELL AND A.M. BAUER

Stephenson and Stephenson (1956) regarded New Zealand geckos

(Hoplodactylus and Naultinus) as the most primitive forms on the

basis of Underwood's (1955) revised view that amphicoelous verte-

bral centra are primitive within lizards and within the Gekkota.

Furthermore, Stephenson (1960) rejected Underwood’s (1954)

ophthamalogical division of the Gekkonidae into two subfamilies as

it was inconsistent with osteological characters, but neither

Underwood nor Stephenson ‘correctly’ placed all Australian genera.

Also included in Underwood’s Diplodactylinae were several

genera not now regarded as closely allied to the Australo-Pacific

diplodactylines: Aristelliger, Chondrodactylus, Colopus,

Gymnodactylus, Palmatogecko, Phelsuma, Ptenopus, Rhoptropella,

Rhoptropus, Saurodactylus, and Teratoscincus. Four of these,

Chondrodactylus, Colopus, Rhoptropus, and Palmatogecko, share

many features in common with each other and with Pachydactylus

(placed by Underwood [1954] in the Gekkoninae). Kluge (1967a)

moved these taxa to the Gekkoninae, and Russell (1972) and Haacke

(1976) established the affinities of these forms as part of the Pachy-

dactylus group (see below).

Two other taxa, Rhoptropella and Phelsuma, have also been

regarded as being closely related to one another (see below). Both of

these genera, as well as all remaining ones, were moved to the

Gekkoninae by Kluge (1967a) and have remained there since, with

Teratoscincus as the sister group of all other gekkonines. The

affinities of Gymnodactylus have remained problematic (Abdala

1988, 1996; Abdala and Moro 1996), as have those of Aristelliger

(Russell and Bauer 1993), and Ptenopus (Bauer 1990b), whereas

Saurodactylus has been considered allied to the sphaerodactyline

lineage (Kluge 1995). Underwood’s Phyllurus also included within

it a species now assigned to the gekkonine genus Nactus.

The Gekkoninae were characterised by Gekko-type pupils or

secondarily circular pupils. Underwood’s (1954) Gekkoninae, al-

though lacking the taxa mentioned above (and with the addition of

Eurydactylodes, and Crenadactylus as Phyllodactylus ocellatus)

otherwise included all of the genera placed in the group by Kluge

(1967a). This grouping also included Uroplatus, which by virtue of

a large suite of autapomorphic features had been accorded separate

familial status by many previous workers (see Bauer and Russell

1989 for a review). In this regard, Underwood’s (1954) results were

similar to those of Wellborn (1933), who had based her conclusions

on osteological data. Underwood did not rely entirely on the pupil

character, however, as Lygodactylus, with round pupils, was placed

in the Gekkoninae on the basis of other (digital) similarities with

Hemidactylus.

Nine genera were not assigned to family or subfamily by

Underwood. Five of these were unplaced due to lack of material.

The remaining four were taxa with round pupils that were regarded

as secondarily diurnal gekkonids, but which Underwood consid-

ered, on the basis of existing data, could not be allocated to one or the

other of his two subfamilies. Of the latter, one genus, Ancylodactylus,

has been synonymized with another, Cnemaspis. The other two were

Quedenfeldtia and Pristurus. Of the genera not examined,

Ceramodactylus has since been subsumed in Stenodactylus, and

Dravidogecko has been synonymized with Hemidactylus.

Underwood also recognised some instances of convergence among

geckos. Specifically he addressed the allocation of species of leaf-

toed geckos (then chiefly distributed in Diplodactylus and

Phyllodactylus), and bent-toed geckos (then mostly placed in

Gymnodactylus). Among the leaf-toed geckos, pupil shape sug-

gested the transfer of several species of African Diplodactylus to

Phyllodactylus. These geckos are now regarded as members of the

genus Urocotyledon (Kluge, 1983) and are, as Underwood indicated,

correctly assigned to the Gekkonidae rather than the Diplodactylidae.

GECKO CLASSIFICATION

Diplodactylyus, as recognised by Underwood, corresponds to two

currently recognised genera, Diplodactylus and Strophurus. His

reconstituted Phyllodactylus included forms now placed in that

genus as well as Asaccus, Afrogecko, Euleptes, Christinus,

Crenadactylus, Paroedura and Urocotyledon (based on his list of

specimens examined). He also separated Narudasia from

Quedenfeldtia, and divided the then cosmopolitan Gymnodactylus

into four genera: Gymnodactylus (restricted to South America),

Phyllurus (corresponding to the current Phyllurus and Saltuarius,

but also including the species vankampeni, now allocated to the

gekkonine genus Nactus), Cyrtodactylus (including representatives

of Cyrtodactylus, Geckoella, Tenuidactylus, Mediodactylus, Nactus),

and Wallsaurus (the latter now synonymized with Homonota, a

genus listed as unexamined by Underwood).

STEPS TOWARDS FURTHER SYSTEMATIC

RESOLUTION

Underwood’s (1954) classification provided a springboard for sub-

sequent systematic work on geckos. The four large units he

established were ‘corrected’ by Kluge (1967a), but remained as the

chief elements in Kluge’s higher order treatment of the group.

Moffat (1973) generally accepted Kluge’s (1967a) allocation of

genera to subfamilies but disagreed with his methodology and his

pattern of subfamilial relationships.

Eublepharidae

The most stable unit has been the Eublepharidae. This group was

retained intact by Kluge (1967a), although reduced to subfamilial

rank. All subsequent researchers have accepted the monophyly of

this group and more recent treatments have reflected the phylogenetic

position of the Eublepharidae as the sister-group of all other gekkotans

by again according it familial rank (e.g. Grismer 1988). Further,

patterns of relationship within the eublepharids have been estab-

lished at the generic and species levels (Grismer, 1988, 1991, 1994;

Grismer et al., 1999; Ota et al., 1999). In this instance, Underwood

(1954) chiefly used primitive features in diagnosing the family (e.g.

true eyelids present, etc.) but subsequent research has identified

numerous synapomorphies that support the reality of this mono-

phyletic unit (Grismer, 1988; Ota ef al., 1999).

Sphaerodactylidae

The Sphaerodactylidae of Underwood has remained unchanged in

terms of generic content. Kluge (1967a) recognised the group as a

subfamily and considered it to be highly derived, in contrast to

Underwood (1954), who interpreted it as a primitively diurnal group

and a relatively early offshoot of the gekkotan lineage. Subsequently

Kluge (1987) demonstrated that sphaerodactyls are derived from

within gekkonines, confirming their monophyly while obviating

their recognition as a higher order group, as such recognition would

render the Gekkoninae paraphyletic. This arrangement also re-

ceived support from reproductive characters including the restriction

of the calcareous eggshell to gekkonines and sphaerodactylines

(Bustard 1968; Werner 1972). Kluge (1995) later conducted an

explicit investigation of the phylogeny of the sphaerodactyls, yield-

ing a fully resolved generic level pattern for the group. Kluge (1995)

regarded the gekkonine Pristurus as the immediate sister group of

the sphaerodactyls and considered Quedenfeldtia, Cnemaspis,

Narudasia and Saurodactylus as other appropriate outgroup taxa for

his analysis (see below). Of these outgroup genera, Underwood

115

examined material of only Narudasia and Saurodactylus. Species

level analyses within individual sphaerodactyl genera are ongoing

and have been attempted for the largest genus, Sphaerodactylus

(Hass 1991, 1996).

Diplodactylinae

The composition of the Diplodactylinae has changed most signifi-

cantly. Kluge (1967a, b) removed a large number of genera from this

group to the Gekkoninae, leaving only forms with parchment-

shelled eggs in his Diplodactylinae, and provided a generic level

hypothesis of relationships among the remaining forms. Bauer

(1990a) erected a species level hypothesis of relationships among

the Carphodactylini, one of two tribal groups established by Kluge

(1967a). Additional hypotheses at the species level have been

presented by Good et al. (1997) and Vences ef al. (2001). The

Diplodactylini, also established by Kluge (1967a), has yet to be

investigated phylogenetically at the species level, although Kluge

(1967b) erected a generic level hypothesis of relationships and King

(1987b) suggested a species level phylogeny of Diplodactylus based

on several karyotypic characters. Underwood (1954) had purged the

genus Diplodactylus of two taxa with Gekko-type pupils, rendering

a cluster of taxa still accepted as monophyletic. However, he re-

tained in Phyllodactylus the species ocellatus, which has since been

recognised as a diplodactyline and placed in the genus Crenadactylus.

Although the content of Underwood’s (1954) Diplodactylinae as

a whole has changed little, argument persists over patterns of

internal relationship. In particular, the monophyly of the

Carphodactylini has been called into question (Donnellan ef al.

1999) and the relationship of New Zealand taxa has also been re-

evaluated (Chambers ef al. 2001). King (1987b) and King and

Mengden (1990), based on chromosomal data, argued that Oedura

was more closely allied to the Carphodactylini than to other

Diplodactylini, and that pygopods are also allied to the

carphodactylines. Donnellan et al. (1999), based on molecular data

(12SRNA, c-mos), regarded the Diplodactylini , including Oedura,

as monophyletic, but suggested that the Carphodactylini is

paraphyletic. They found pygopods to be the sister group of all

Diplodactylines.

Patterns of relationship within the Diplodactylinae have further

been complicated by the recognition that pygopods are more closely

related to this group (or some component thereof) than to other

gekkotans (Kluge 1987). On this basis, Kluge (1987) recognised a

redefined Pygopodidae for the group that includes diplodactyline

geckos plus pygopods. Good ef al. (1997), based in part on argu-

ments presented by Bauer (1990a), proposed an alternative higher

level scheme, recognising the Diplodactylidae as a family level

group. Based on the patterns of relationship retrieved by Donnellan

et al. (1999), the Diplodactylidae and Pygopodidae are sister taxa.

As mentioned above, the genus Eurydactylodes proved particu-

larly problematic to Underwood (1954) and he only included it in his

Diplodactylinae in the following year (Underwood, 1955). For a

variety of reasons, this genus has continued to be enigmatic, exhib-

iting an odd mosaic of characteristics. Although Eurydactylodes

appears to be a member of a monophyletic New Caledonian

carphodactyline radiation (Bauer 1990a), it possesses a number of

features that are problematic and, at least superficially, link it to

other groups of geckos. One such feature is the tail-squirting appa-

ratus. Members of this genus have caudal glands that secrete a sticky

substance as a defensive mechanism. Such mechanisms have been

widely reported in arthropods (Deslippe ef al. 1996), and amphi-

bians (Arnold 1982), but among amniotes have been noted only for

geckos of the Australian diplodactyline genus Strophurus (Rosenberg

116

and Russell 1980) and Eurydactylodes (BOhme and Sering 1997).

Although the secretion has not been characterised, it is likely similar

to that of Strophurus spp., which is proteinaceous (Rosenberg et al.

1984) and is effective in detering at least some small predators, such

as spiders, which become entangled in the secretion (Minton 1982).

However, both the anatomy of the gland and the ejection mechanism

of secretion differ between the two gecko genera, suggesting that the

apparatus in convergent (BOhme and Sering 1997). Eurydactylodes

is also convergent with Strophurus in its bright yellow-orange

mouth coloration. Most geckos have unpigmented buccal linings.

Eurydactylodes also shares some features with gekkonid geckos.

Most notable is the presence of extracranial endolymphatic sacs in

the neck region, especially in juveniles and reproductive females.

These calcium-storing structures frequently form conspicuous bulges

on the necks of gekkonids, but in diplodactylids are intracranial and

contain little calctum. Eurydactylodes is an exception in that very

large sacs are often present, in some individuals artificially increas-

ing the apparent size of the head (Bauer 1989). Perhaps related to

this, the eggshells of Eurydactylodes, although similar in most

regards to those of typical carphodactylines, are covered by a

calcified outer surface (Bauer and Sadlier 2000), which otherwise

typifies gekkonids (Bustard, 1968; Werner, 1972).

Gekkoninae

The Gekkoninae was the most heterogeneous and unwieldy of

Underwood’s higher order groups and it has remained largely

intractable to this day. Indeed, as a result of the resolution of the

content of the Diplodactyinae, the Gekkoninae has grown signifi-

cantly. Further, the vast majority of all new or resurrected genera

since 1954 are gekkonines. Underwood (1954) initiated the process

of dismantling some of the larger gekkonid genera that he recog-

nised as polyphyletic assemblages of digitally convergent taxa. In

particular he addressed the composition of Phyllodactylus and

Gymnodactylus, two of the largest and most cosmopolitan taxa.

Subsequent reduction of Phyllodactylus occurred with the removal

of Crenadactylus and its shift to the Diplodactylinae (Dixon and

Kluge 1964), and the placement of several geographically coherent

gekkonine leaf-toed forms into Paroedura (Dixon and Kroll 1974),

Asaccus (Dixon and Anderson 1973), Urocotyledon (Kluge 1983),

and Christinus (Wells and Wellington 1983). All remaining Old

World leaf-toed geckos were removed from the now strictly American

Phyllodactylus by Bauer et al. (1997), who erected Haemodracon,

Dixonius, Afrogecko, Cryptactites and Goggia, and resurrected

Euleptes. Nussbaum et al. (1998) further provided a new generic

name for the elongate-bodied leaf-toed geckos of Madagascar,

Matoatoa. Arnold and Gardner (1994) also provided a species level

phylogeny for Asaccus, using a variety of Old and New World leaf-

toed geckos as outgroup taxa, but without explicit justification. Both

these authors and Nussbaum ef al. (1998) suggested that at least

some phyllodactyl taxa might be closely related.

A similar dismantling of Gymnodactylus was begun by Underwood

(1954), who removed Phyllurus to the Diplodactylinae and recog-

nised the genera Gymnodactylus, Cyrtodactylus and Wallsaurus for

a subset of the naked-toed geckos. Subsequently Golubev and

Szczerbak (1981) and Szczerbak and Golubev (1984) divided the

Old World forms placed by Underwood in Cyrtodactylus, which

they regarded as polyphyletic, into several genera, including the

Palearctic Tenuidactylus, Cyrtopodion, Mesodactylus, Carinato-

gecko, Mediodactylus and Asiocolotes. Tropical forms were divided

into Cyrtodactylus, Geckoella and Nactus (Kluge 1983).

The effect of these actions has been to dismantle several larger,

clearly polyphyletic groups and to instead recognise a larger number

A.P. RUSSELL AND A.M. BAUER

of smaller, but putatively monophyletic, genera. The problem re-

mains, however, that relationships among these genera are poorly

resolved. While the identification of monophyletic units is a neces-

sary first step in the resolution of gekkotan relationships, the increase

in the number of such units increases the sampling required in order

to erect a hypothesis of relationship across all members of the group.

This has been the major stumbling block in the phylogenetic inter-

pretation of the Gekkoninae: any attempt to resolve relationships

among some subset of genera of necessity requires an analysis of

virtually all other genera. The sheer diversity of the group has been

an impediment to its resolution.

Despite the difficulty of determining relationships among

gekkonines, some clusters of genera that appear to be monophyletic

have been identified. These groups are chiefly those that share

highly distinctive and generally restricted derived conditions. Thus,

such groups have typically been identified on the basis of informa-

tion intrinsic to themselves rather than on the basis of outgroup

comparison. Indeed, when outgroup analysis has been attempted,

the choice of outgroup has been based on geography (e.g., Joger

1985; Bauer 1990b; Abdala 1996; Macey er al. 2000) or on some

preconceived notion of similarity, usually based on digital anatomy

(e.g., Arnold and Gardner 1994; Macey et al. 2000). Chromosomal

characteristics of gekkonids are highly heterogeneous (King 1987c),

but such variation may occur within genera and thus has contributed

little to the resolution of higher order relationships.

One of the most substantially supported subgroups of gekkonines

is the Pachydactylus group. This is a cluster of genera sharing the

unique feature of hyperphalangy of digit I of both the manus and pes.

The group includes the chiefly Mediterranean genera Tarentola and

Geckonia and the southern Africa forms Pachydactylus, Rhoptropus,

Chondrodactylus, Colopus, and Palmatogecko. Underwood (1954)

recognised the relationship of all of these except Pachydactylus

itself, placing them in the Diplodactylinae and identifying a peculiar

pupil shape, the Rhoptropus-type, that all shared. Several species of

Pachydactylus (e.g., P. austeni, P. kochi) are strikingly similar, even

in external appearance, to Colopus and Palmatogecko. By chance,

however, Underwood’s (1954) list of taxa examined reveals that he

did not examine any of these species. Hyperphalangy had previ-

ously been identified in some members of the group by Wellborn

(1933), but her sampling was inadequate to highlight the potential

phylogenetic value of the feature. Russell (1972, 1976) and Haacke

(1976) recognised the significance of hyperphalangy and argued

convincingly that this was evidence of the relatedness of these taxa.

Virtually all subsequent workers (Bauer 1990b, 2000; Kluge and

Nussbaum 1995; Lamb and Bauer 2002; but see Joger 1985) have

agreed that these seven genera (including collectively approxi-

mately 80 species) form a monophyletic group. With closely related

taxa thus identified, species level phylogenies have been possible

within constituent genera (e.g., Rhoptropus: Bauer and Good 1996,

Lamb and Bauer 2001; Pachydactylus: Lamb and Bauer 2000,

2002).

Other clusterings, although less well investigated, have also been

proposed, although not necessarily tested. The Gekko group, con-

sisting of Gekko, Gehyra, Hemiphyllodactylus, Lepidodactylus,

Luperosaurus, Perochirus, Pseudogekko, and Ptychozoon, all share

similarities of digital structure (Kluge 1968; Russell 1972, 1976)

and are probably a monophyletic group, although particular patterns

of intergeneric relationship remain untested.

The large and heterogeneous genus Hemidactylus seems to be

related to a number of much smaller genera that are also similar

digitally, and are united by synapomorphies of size and shape of the

intermediate phalanges (Russell, 1977a). Dravidogecko, for example,

has been synonymized with Hemidactylus on the basis of digital

Can a

the Ga <a,

GECKO CLASSIFICATION

morphology (Bauer and Russell 1995). In addition, Cosymbotus,

Briba and Teratolepis are also very similar and are almost certainly

share a common ancestry with Hemidactylus, or are derived from

within it.

Bauer (1990b) found some evidence for the recognition of a

Madagascan radiation including several genera of leaf and fan-toed

geckos including Uroplatus, Ebenavia and Paroedura. Kluge and

Nussbaum (1995) did not retrieve identical patterns of relationship,

but these genera nonetheless grouped closely when only Afro-

Malagasy geckos were included in the analysis. An expanded Indian

Ocean lineage, including these taxa plus Ailuronyx, Blaesodactylus,

Homopholis, and Geckolepis was retrieved by Bauer (1990b), al-

though not by Kluge and Nussbaum (1995).

Another putatively monophyletic group is the Lygodactylus com-

plex (Pasteur 1964), which includes two additional genera, at least

one of which, Millotisaurus, is probably derived from within

Lygodactylus (Pasteur, 1995; Kriiger, 2001). Lygodactylus itself

clustered with Phelsuma in analyses constrained to include only

Afro-Malagasy genera (Bauer 1990b; Kluge and Nussbaum 1995).

Kriiger (2001) also clustered Lygodactylus and Phelsuma together.

Although some genera have been revised at the alpha level, and

numerous new taxa have been erected, most revisions have merely

proposed species groups, without providing explicit hypotheses of

relationship (e.g. Pasteur 1964; Brown and Parker 1977; Nussbaum

and Raxworthy 2000). These, like many of the other groups, share

digital similarities and geographic cohesiveness. Among those gen-

era for which some idea of relationships exist, there are several for

which species level phylogenies have been proposed, including

Uroplatus (Bauer and Russell 1989) and Gehyra (selected species

only; King 1979, 1983).

Rhoptropella has been associated with several different genera by

different authors. Russell (1977b) used digital morphology to argue

that it was in fact a Phelsuma, with no direct affinities to Rhoptropus,

with which it had previously been associated (e.g. Boulenger 1885).

Russell and Bauer (1990) found additional support for this from

histological investigations and Good and Bauer (1995) presented

allozyme evidence for Rhoptropella’s links to Phelsuma. Both

Bauer (1990b) and Kluge and Nussbaum (1995) found the two

genera to be sister taxa when a generic analysis was conducted.

Rosler (2001), discussing pholidosis, also concluded that Phelsuma

and Rhoptropella are sister taxa. ROll (1999), however, using oph-

thalmological and digital surface data, interpreted it as displaying

features of both Rhoptropus and Phelsuma, which, if true, could

suggest affinities between the chiefly African Pachydactylus group

and the putatively monophyletic Indian Ocean complex. A variety

of character types also suggest that Bogertia and Thecadactylus may

be allied (Russell and Bauer 1988; Abdala and Moro 1996).

Cnemaspis, Narudasia, Quedenfeldtia, Saurodactylus and

Pristurus have been proposed as gekkonine taxa basal to the

sphaerodactyl lineage (Arnold 1993; Kluge 1995), demonstrating

the paraphyly of the Gekkoninae. Although Kluge (1995) did not

claim any specific relationships among these taxa, his analysis did

yield patterns in which Pristurus was the sister group of the

sphaerodactyls, and Narudasia, Saurodactylus and Cnemaspis

formed a clade. Arnold (1993) advocated the pattern ((((Pristurus,

Quedenfeldtia) sphaerodactyls) Saurodactylus) Narudasia). Behav-

ioural apomorphies unique to this cluster were documented by

Résler and Wranik (2001), who noted reproductive morphological

apomorphies shared by Quedenfeldtia and the sphaerodacty]s to the

exclusion of Pristurus. Arnold (1993) provided a species level

phylogeny for Pristurus. The African members of this group were

also clustered together in an anlysis of Afro-Malagasy taxa by Kluge

and Nussbaum (1995). RGIl and Schwemer (1999) identified a

iM /

unique crystallin ligand common to several of these taxa (plus

Lygodactylus), that they interpreted as synapomorphic. This was

subsequently found in Cnemaspis (RGIl, in press), but whether this

indicates affinity or convergence among secondarily diurnal forms

remains to be determined.

The naked-toed geckos have proved especially difficult to deal

with. Szczerbak and Golubev (1984, 1986) provided evidence of

relationship among some Palearctic forms, such as Tenuidactylus,

Mediodactylus, Asiocolotes, and Cyrtopodion. Macey et al. (2000)

found evidence for the monphyly of Cyrtopodion and Mediodactylus

and hypothesized relationships among a small number of species in

each group. The generic allocation of certain Himalayan members

of the group has proved especially problematic (Khan 1993; Khan

and Rosler 1999).

Another group of naked-toed geckos including Agamura, Bunopus,

Alsophylax, Crossobamon, Microgecko, and Tropiocolotes has been

even less well investigated (Leviton and Anderson 1972; Szczerbak

and Golubev 1977; Golubev 1984; Golubev and Szczerbak 1985).

The New World naked toed forms, Gymnodactylus and Homonota,

have been included in analyses by Abdala (1996) and Abdala and

Moro (1996) but these investigations included only South American

gekkonines. Abdala (1988) also provided a species level phylogeny

for Homonota (see also Vanzolini 1968).

While some degree of resolution for the gekkonine taxa outlined

above has been reached, certain other gekkonines remain enigmatic

and without any sound indication of affinities. Teratoscincus is

highly unusual in its morphology, and appears to be the sister group

of all remaining gekkonines (Kluge 1987). A species level phylogeny

for this group has been generated (Macey et al. 1999). Stenodactylus

has sometimes been considered to be allied to Teratoscincus (Kluge

1967a; Kluge and Nussbaum 1995), but its position remains equivo-

cal (Arnold 1980).

Another perplexing padless genus is Prenopus, asouthern African

endemic. Both Bauer (1990b) and Kluge and Nussbaum (1995)

found little evidence for particular affinities, and constrained or

retrieved a basal placement among African gekkonines. Ptenopus

possesses a large number of autapomorphic traits (Haacke 1975;

Rittenhouse et al. 1998: Russell et al. 2000). This mirrors the

situation that plagued analyses of Uroplatus in that many features

segregate these geckos from other taxa, but those traits that are

shared are chiefly primitive ones.

Four pad-bearing genera, which appear unrelated to one another

and have no obvious affinities to previously discussed groups, are

also problematic. These are Afroedura, Aristelliger, Calodactylodes,

and Paragehyra. Paragehyra was long known from a single speci-

men of a single species, but a second species was recently discovered

(Nussbaum and Raxworthy 1994). The availability of additional

material allowed the relationships of the genus to be investigated in

more detail, but this has not yielded any definitive statements about

its position within the Gekkoninae (Kluge and Nussbaum 1995),

although Nussbaum and Raxworthy (1994) noted the similarity of

the digits of this form to those of another enigmatic taxon, the West

Indian Aristelliger.

Russell (1972) grouped Afroedura and Calodactylodes in the

same digitally defined cluster. Loveridge (1944) had initially segre-

gated Afroedura from the Australian Oedura, and this was reflected

in Underwood’s (1954) placement of the genera in different sub-

families. Some question as to the distinctiveness of these taxa

remained, however, until Cogger (1964) conducted detailed osteo-

logical comparisons. Despite some similarities in digital design,

Russell and Bauer (1989) concluded that Calodactylodes and

Afroedura were more likely convergent than related. Bauer and Das

(2000) noted some superficial similarity and geographic proximity

118

to Asaccus, but again concluded that the relationships of

Calodactylodes were obscure.

Aristelliger was one of the taxa regarded as enigmatic by

Underwood (1954). He placed it in the Diplodactylinae and re-

garded it as an archaic form, possibly unable to compete with the

gekkonines, which he regarded as more derived. Indeed, he regarded

it as being a basal gekkonnid, retaining oil droplets in the eyes and

displaying vertebral amphicoely. In part, Underwood’s (1954) as-

sessment of this genus may have been influenced by the fact that he

was, at the time, based in the West Indies and had more information

about it than most other geckos, and certainly more than any that he

also placed in the Dioplodactylinae. Aristelliger has been employed

ina variety of evolutionary (Hecht 1952) and morphological (Ruibal

and Ernst 1965) studies, probably because of ease of availability.

These studies, however, have helped little to clarify the position of

the taxon. Although it has rather complex external digital structure,

anatomically it reveals a quite simple architecture. Thus more

detailed studies of the digits (Russell 1976, 1979; Russell and Bauer

1990, 1993) have not assisted in placing it with other genera that

typically show a more complex anatomy.

BIOGEOGRAPHIC AND EVOLUTIONARY

IMPLICATIONS OF UNDERWOOD’S

CLASSIFICATION OF THE GECKOS

Underwood (1954) pioneered a comprehensive approach to gecko

systematics. As a result of this, he was faced with issues of biogeog-

raphy and evolution that begged an explanation. For geckos, this

was essentially uncharted territory and the recognition of clusters,

especially within his Gekkoninae, generated new biogeographic and

evolutionary problems. Chief among these was the need to explain

the biogeography and evolution of his Diplodactylinae. This proved

especially challenging because, as noted above, this cluster of taxa

later proved to be the least stable of Underwood’s (1954) proposed

units.

Underwood (1954) interpreted eublepharids, with their scattered

distribution, as an ancient radiation with its own specialisations,

chiefly to arid conditions, rather than as a cluster of relicts. He

viewed the eublepharids as the primary, ancient Northern Hemi-

sphere radiation of the Gekkota.

The sphaerodactylids were biogeographically non-problematic

as all occur in the New World. Underwood (1954) viewed them as an

early New World offshoot of the Gekkota, based on his belief that

they were primitively diurnal, retaining certain plesiomorphic

lacertilian ophthalmological features. Kluge’s (1967) demonstra-

tion that the sphaerodactyls are derived from within the gekkonines,

and subsequent recognition of secondary diurnality in the

sphaerodactylines (ROll, in press) has resulted in a reinterpretation

of sphaerodactyl biogeography and evolutionary history, with north

African affinities being supported by more recent systematic inves-

tigations (Arnold, 1993; Kluge, 1995).

Underwood (1954) undertook to explain the distribution of the

Diplodactylinae which, in his view, included a large core of Australo-

Pacific taxa, but also genera from Africa and the Americas. He noted

that no genus occupied more than one continent and that most genera

had rather limited or patchy distributions. Only Arvistelliger and the

New Zealand taxa did not co-occur with Gekkonines. He felt that

ovoviviparity might explain their ability to survive in New Zealand.

In the case of Aristelliger, he noted that its occurrence was basically

complementary to that of gekkonines, and suggested that 1t may

have formerly had a broader distribution but had subsequently

A.P. RUSSELL AND A.M. BAUER

withdrawn in the face of competition with gekkonine geckos. He

viewed the gekkonines as a more modern, expanding group that was

displacing diplodactylines from areas of previous occupancy. He

regarded New Caledonia as marking the periphery of the range of

the gekkonines, with Lepidodactylus and Eurydactylodes being

relatively recent invaders into diplodactyline (Rhacodactylus and

Bavayia) territory. He believed that Phelsuma, being chiefly insular,

diurnal, and arboreal, was ecologically segregated from the

gekkonines with which it co-occurs. He regarded its occurrence in

mainland East Africa as a recent event. Its arrival on islands of the

Indian Ocean was hypothesised to be as a nocturnal stock, an

offshoot of the southern African cluster of diplodactylines, with a

subsequent change in life style enabling it to coexist with gekkonines.

He regarded most continental diplodactylines as being terrestrial,

with arboreal forms being peripheral.

The foregoing rather tortuous scenario developed by Underwood

(1954) to account for diplodactyline biogeography and evolution

was the direct result of the recognition of, as it was formulated at the

time, a polyphyletic assemblage. Removal of Aristelliger, Phelsuma

and a variety of other taxa (see above) from the Diplodactylinae

(Kluge, 1967) and inclusion of Eurydactylodes within it (Underwood,

1955) rendered biogeographic and evolutionary consideration of the

remaining diplodactylids more tractable (Bauer, 1990a), but left the

Gekkonidae (Underwood’s Gekkoninae) yet more unwieldy. That

some gekkonine genera were present on multiple continents sug-

gested to Underwood (1954) that this was the dominant group. He

recognised four major digital morphologies among gekkonines, and

believed that each had reached most areas of the world and that most

had radiated in situ in each area, giving rise to numerous regionally

endemic genera. Thus, while expansion was an important theme in

the evolution of gekkonines, there was significant within-region

evolution as well. These ideas were obviously heavily influenced by

those of Darlington (1948) and by the idea of competitive exclusion

(a more ecological than historical view). He noted the waif dispersal

capabilities of some geckos and opined that this complicated the

picture of dispersal via land bridges that served as his main para-

digm. The issue of waif dispersal, though recognised as being

restricted to certain taxa, remains to this day as a confounding factor

in the interpretation of the evolution of gekkonid spatial patterns.

Further systematic consideration (see above) has resulted in an

increased complement of gekkonid genera, but has also resulted in

some level of internal resolution, which, in turn, has influenced

some aspects of biogeographic interpretation. For many regions,

local radiations of monophyletic clusters of genera have been recog-

nised, but resolution of pattern between these clusters remains

poorly understood.

CONCLUSIONS

Underwood’s (1954) systematic, biogeographic and evolutionary

considerations of geckos marked the first attempt to comprehen-

sively assess this circumglobal and highly diverse cluster. His

analyses brought some degree of order to a previously very poorly

understood set of problems, and his choice of ophthalmological

characters as those of primary consideration resulted in the estab-

lishment of a basic pattern that has survived to the present in

modified form. Although Underwood (1968, 1970, 1971b, 1977a,b)

revisited the gekkotan eye repeatedly, the promise of phylogenetic

utility originally held out by ophthalmolgical data has not, until

recently, been pursued. ROll (1995, 1997, 1999) and R6ll and

Schwemer (1999) have demonstrated that many diurnal geckos are

GECKO CLASSIFICATION

unable to modify pupil shape and instead regulate light through

absorbance by crystallins in the lens. Although Roll and Schwemer

(1999) assumed that the use of particular crystallins was likely to

have evolved only once, there is no evidence that all diurnal gekkonids

are allied (e.g. Phelsuma + Lygodactylus and Sphaerodactylus +

Quedenfeltia + Narudasia + Saurodactylus; Kluge and Nussbaum

1995). This avenue of approach, however, suggests that at the

anatomical and molecular level, data from the visual system may yet

be of significance in assisting in the resolution of pattern between

nocturnal and secondarily diurnal clusters of gekkonids (including

sphaerodactyls).

Despite attempts to move away from digital architecture as a

primary means of identifying suprageneric clusters, this has contin-

ued to play a role and has been instrumental, by way of examination

of internal architecture, in assisting in the circumscription of a

number of apparently monophyletic assemblages (Russell, 1976).

Pedal anatomy remains a primary determinant of generic allocation

and a major clue to potential higher order relationships (e.g.,

Nussbaum and Raxworthy 1994).

Changes in generic alignment and more modern views of plate

tectonics have necessitated a rethinking of Underwood’s (1954)

biogeographic hypotheses. Essentially the eublepharids appear to

represent an ancient Laurasian radiation, in keeping with Under-

wood’s (1954) ideas. The remaining gekkotans are now regarded as

being of Gondwanan origin and to consist of an essentially east

Gondwanan diplodactylid radiation and a west Gondwanan gekkonid

radiation, with the latter having given rise, in turn, to the New World

sphaerodactyls.

Interpretation of patterns of relationship must now deal with the

recognition that the age of the Gekkota is much greater than was

believed in 1954 and that many genera might be quite ancient.

Hence, generic body plans may have been established for very long

periods, making them rather discrete from one another and render-

ing it difficult to erect hypotheses of relationship. Even among the

sphaerodacyls, generic differentiation is estimated to have occurred

as much as 40 million years ago (Hass 1991). King (1987a, 1987b),

on the basis of chromosomal and immunological data correlated

with tectonic history of the Australian region, estimated a minimum

divergence of 66 my between the two major clades of diplodactylines,

and at least 120 my for the origin of the gekkotans.

Despite the magnitude of the problem, only patterns of relationship

within the rather amorphous Gekkonidae (Underwood’s Gekkoninae)

remainrelatively unassailed. Even here, however, large, circumglobal

unwieldy genera have been broken into smaller, more geographically

circumscribed taxa and there is now an opportunity to begin to make

inroads into the determination of the patterns of interrelationship of

suprageneric clusters of gekkonid taxa. This may best be broached by

taking exemplars, appropriately selected (Bininda-Emonds er al.

1998) from the putative clusters and the enigmatic genera, and

investigating a combination of morphological and molecular data.

Given the magnitude of the problem, this will be an iterative process

and will necessitate frequent cross-checking within and between

clusters. The boldness of Garth Underwood’s approach will have to

be adopted in selecting novel sources of data to allow new approaches

to be taken and insights to be revealed.

REFERENCES

Abdala, V. 1988. Anilisis cladistico de las especies del género Homonota (Gekkonidae).

Revista Espanola de Herpetologia 12: 55-62.

1996. Osteologia craneal y relaciones de los geconinos sudamericanos

(Reptilia:Gekkonidae). Revista Espanola de Herpetologia 10: 41-54.

119

& Moro, S. 1996. Cranial musculature of South American Gekkonidae. Journal

of Morphology 229: 59-70.

Arnold, E.N. 1980. A review of the lizard genus Stenodactylus (Reptilia: Gekkonidae).

Fauna of Saudi Arabia 2: 368-404.

1993. Historical changes in the ecology and behaviour of semaphore geckos

(Pristurus, Gekkonidae) and their relatives. Journal of Zoology, London 229: 353—

384.

—— & Gardner, A.S. 1994. A review of the Middle Eastern leaf-toed geckoes

(Gekkonidae: Asaccus) with descriptions of two new species from Oman. Fauna of

Saudi Arabia 14: 424-441.

Arnold, S.J. 1982. A quantitative approach to antipredator performance: salamander

defense against snake attack. Copeia 1982: 247-253.

Bauer, A.M. 1989. Extracranial endolymphatic sacs in Eurydactylodes (Reptilia:

Gekkonidae), with comments on endolymphatic function in lizards in general.

Journal of Herpetology 23: 172-175.

1990a. Phylogenetic systematics and biogeography of the Carphodactylini (Rep-

tilia: Gekkonidae). Bonner zoologische Monographien 30: 1-217.

1990b. Phylogeny and biogeography of the geckos of southern Africa and the

islands of the western Indian Ocean: a preliminary analysis. pp.275—284. In: Peters,

G. and Hutterer, R. (eds). Vertebrates in the Tropics. Zoologisches Forschungsinstitut

und Museum A. Koenig, Bonn.

2000. Evolutionary scenarios in the Pachydactylus group geckos of southern

Africa: new hypotheses. African Journal of Herpetology 48: 53-62.

—— & Das, I. 2000. A review of the gekkonid genus Calodactylodes (Reptilia:

Squamata) from India and Sri Lanka. Journal of South Asian Natural History 5: 25—

35.

— & Good, D.A. 1996. Phylogenetic systematics of the day geckos, genus Rhoptropus

(Reptilia: Gekkonidae), of south-western Africa. Journal of Zoology, London 238:

635-663.

& Russell, A.P. 1989. A systematic review of the genus Uroplatus (Reptilia:

Gekkonidae), with comments on its biology. Journal of Natural History 23: 169-

203.

& 1995. The systematic relationships of Dravidogecko anamallensis

(Giinther 1875). Asiatic Herpetological Research 6: 30-35.

& Sadlier, R.A. 2000. The Herpetofauna of New Caledonia. Society for the Study

of Amphibians and Reptiles, Ithaca, NY.

, Good, D.A. & Branch, W.R. 1997. A taxonomy of the Southern African leaf-

toed geckos (Squamata: Gekkonidae), with a review of Old World ‘Phyllodactylus’

and the description of five new genera. Proceedings of the California Academy of

Sciences 49: 447-497.

Bellairs, A.d’A. 1948. The eyelids and spectacle in geckos. Proceedings of the

Zoological Society of London 118: 420-425.

Bininda-Emonds, O.R.P., Bryant, H.N. & Russell, A.P. 1998. Supraspecific taxa as

terminals in cladistic analysis: implicit assumptions of monophyly and errors in

phylogenetic inference. Biological Journal of the Linnean Society 64: 101-133.

Bohme, W. & Sering, M. 1997. Tail squirting in Eurydactylodes: independent evolu-

tion of caudal defensive glands in a diplodactyline gecko (Reptilia, Gekkonidae).

Zoologischer Anzeiger 235: 225-229.

Boulenger, G.A. 1885. Catalogue of the Lizards in the British Museum (Natural

History). 2nd ed. Vol. 1. Trustees of the British Museum, London.

Brown, W.C. & Parker, F. 1977. Lizards of the genus Lepidodactylus (Gekkonidae) from

the Indo-Australian Archipelago and the islands of the Pacific, with descriptions of new

species. Proceedings of the California Academy of Sciences, 4" ser. 61: 253-265.

Bustard, H.R. 1968. The egg-shell of gekkonoid lizards: a taxonomic adjunct. Copeia

1968: 162-164.

Camp, C.L. 1923. Classification of the lizards. Bulletin of the American Museum of

Natural History 48: 89-481.

Chambers, G.K., Boon, W.M., Buckley, T.R., & Hitchmough, R.A. 2001. Using

molecular methods to understand the Gondwanan affinities of the New Zealand

biota: three case studies. Australian Journal of Botany 49: 377-387.

Cogger, H.G. 1964. The comparative osteology and systematic status of the gekkonid

genera Afroedura Loveridge and Oedura Gray. Proceedings of the Linnean Society

of New South Wales 89: 364-372.

Darlington, P.J., Jr. 1948. The geographical distribution of cold-blooded vertebrates.

Quarterly Review of Biology 23: 1-26, 105-123.

Deslippe, R.J., Jelinski, L., & Eisner, T. 1996. Defense by use of a proteinaceous glue:

woodlice vs. ants. Zoology 99 (1995/96):205—210.

Dixon, J.R. & Anderson, $.C. 1973. A new genus and species of gecko (Sauria:

Gekkonidae) from Iran and Iraq. Bulletin of the Southern California Academy of

Sciences 72: 155-160.

& Kluge, A.G. 1964. A new gekkonid lizard genus from Australia. Copeia 1964:

174-180.

— & Kroll, J.C. 1974. Resurrection of the generic name Paroedura for the

phyllodactyline geckos of Madagascar, and description of a new species. Copeia

1974: 24-30

Donnellan, S.C., Hutchinson, M.N. & Saint, K.M. 1999. Molecular evidence for the

phylogeny of Australian gekkonoid lizards. Biological Journal of the Linnean

Society 67: 97-118.

120

Golubev, M.L. 1984. Structure of the genus Tropiocolotes (Reptilia, Gekkonidae) [in

Russian]. Vestnik Zoologii 1984(6): 12.

& Szezerbak, N.N. 1981. Carinatogecko gen. n. (Reptilia, Gekkonidae) a new

genus of gecko lizards from Southwest Asia [in Russian]. Vestnik Zoologii 1981(5):

3441.

& Szezerbak, N.N. 1985. On the relationships of two Palearctic gecko genera:

Tenuidactylus | Agamura (Reptila, Gekkonidae) [in Russian]. pp.59-60. In: Prob-

lems of Herpetology. Sixth All-Union Herpetological Conference Abstracts, Tashkent.

Nauka, Leningrad.

Good, D.A. & Bauer, A.M. 1995. The Namaqua day gecko revisited: allozyme

evidence for the affinities of Phelsuma ocellata. Journal of the Herpetological

Association of Africa 44: 1-9.

; & Sadlier, R.A. 1997. Allozyme evidence for the phylogeny of giant New

Caledonian geckos (Squamata: Diplodactylidae: Rhacodactylus), with comments on

the status of R. leachianus henkelii. Australian Journal of Zoology 45: 317-330.

Grismer, L.L. 1988. Phylogeny, taxonomy, classification, and biogeography of

eublepharid geckos. pp.369-469. In: Estes, R. and Pregill, G. (eds). Phylogenetic

Relationships of the Lizard Families: Essays Commemorating Charles L. Camp.

Stanford University Press, California.

1991. Cladistic relationships of the lizard Eublepharis turcmenicus (Squamata:

Eublepharidae). Journal of Herpetology 25: 251-253.

1994. Phylogeny, classification, and biogeography of Goniurosaurus kuroiwae

(Squamata: Eublepharidae) from the Ryukyu Archipelago, Japan, with description of

a new subspecies. Zoological Science 11: 319-335.

, Viets, B.E. & Boyle, L.J. 1999. Two new continental species of Goniurosaurus

(Squamata: Eublepharidae) with a phylogeny and evolutionary classification of the

genus. Journal of Herpetology 33: 382-393.

Haacke, W.D. 1975. The burrowing geckos of Southern Africa, 1. (Reptilia:

Gekkonidae). Annals of the Transvaal Museum 29: 197-243.

Haacke, W.D. 1976. The burrowing geckos of Southern Africa, 5. (Reptilia:

Gekkonidae). Annals of the Transvaal Museum 30; 71-89.

Harris, D.J., Sinclair, E.A., Mercader, N.L., Marshall, J.C. & Crandall, K.A. 1999.

Squamate relationships based on c-mos nuclear DNA sequences. Herpetological

Journal 9: 147-151.

Hass, C.A. 1991. Evolution and biogeography of West Indian Sphaerodactylus (Sauria:

Gekkonidae): a molecular approach. Journal of Zoology, London 225: 525-561.

1996. Relationships among West Indian geckos of the genus Sphaerodactylus: a

preliminary analysis of mitochondrial 16s ribosomal RNA sequences. pp.175-194.

In: Powell, R. & Henderson, R.W. (eds). Contributions to West Indian Herpetology:

A Tribute to Albert Schwartz. Society for the Study of Amphibians and Reptiles,

Ithaca, New York.

Hecht, M.K. 1952. Natural selection in the lizard genus Aristelliger. Evolution 6: 112—

124.

Joger, U. 1985. The African gekkonine radiation — preliminary phylogenetic results,

based on quantitative immunological comparisons of serum albumins. pp.479-494.

In: Schuchmann, K.-L. (ed). African Vertebrates: Systematics, Phylogeny and

Evolutionary Ecology. Zoologisches Forschungsinstitut und Museum A. Koenig,

Bonn.

Khan, M.S. 1993. A new angular-toed gecko from Pakistan, with remarks on the

taxonomy and a key to the species belonging to the genus Cyrtodactylus (Reptilia:

Sauria: Gekkonidae). Pakistan Journal of Zoology 25: 67-73.

& Rosler, H. 1999. Redescription and generic redesignation of the Ladakhian

gecko Gymnodactylus stoliczkai Steindachner. 1969 [sic]. Asiatic Herpetological

Research 8: 60-68.

King, M. 1979. Karyotypic evolution in Gehyra (Gekkonidae: Reptilia). I. The Gehyra

variegata-punctata complex. Australian Journal of Zoology 27: 373-393.

1983. Karyotypic evolution in Gehyra (Gekkonidae: Reptilia). II. The Gehyra

australis complex. Australian Journal of Zoology 31: 723-741.

1987a. Origin of the Gekkonidae: chromosomal and albumin evolution suggests

Gondwanaland. Search 18: 252-254.

1987b. Chromosomal evolution in the Diplodactylinae (Gekkonidae: Reptilia). I.

Evolutionary relationships and patterns of change. Australian Journal of Zoology

35: 507-531.

1987c. Monophyleticism and polyphyleticism in the Gekkonidae: a chromosomal

perspective. Australian Journal of Zoology 35: 641-654.

& Mengden, G. 1990. Chromosal evolution in the Diplodactyinae (Gekkonidae:

Reptilia). II. Chromosomal variability between New Caledonian species. Australian

Journal of Zoology 38: 219-226.

Kluge, A.G. 1967a. Higher taxonomic categories of gekkonid lizards and their

evolution. Bulletin of the American Museum of Natural History 135: 1-60, pls. 1-5.

1967b. Systematics, phylogeny, and zoogeography of the lizard genus

Diplodactylus Gray (Gekkonidae). Australian Journal of Zoology 15: 1007-1108.

— 1968. Phylogenetic relationships of the gekkonid lizard genera Lepidodactylus

Fitzinger, Hemiphyllodactylus Bleeker, and Pseudogekko Taylor. The Philippine

Journal of Science 95:331-352.

—— 1983. Cladistic relationships among gekkonid lizards. Copeia 1983: 465-475.

— 1987. Cladistic relationships in the Gekkonoidea (Squamata, Sauria). Miscellane-

A.P. RUSSELL AND A.M. BAUER

ous Publications, Museum of Zoology, University of Michigan (173): i-iv + 1-54.

1995. Cladistic relationships of sphaerodacty] lizards. American Museum Novitates

(3139): 1-23.

— 2001. Gekkotan lizard taxonomy. Hamadryad 26:1-209.

— & Nussbaum, R.A. 1995. A review of African-Madagascan gekkonid lizard

phylogeny and biogeography (Squamata). Miscellaneous Publications, Museum of

Zoology, University of Michigan (183): i-v + 1-20.

Kriiger, J. 2001. Die madagassischen Gekkoniden. Tiel I]: Die Geckos der Gattung

Lygodactylus Gray, 1864 (Reptilia: Sauria: Gekkonidae). Gekkota 3: 3-28.

Lamb, T. & Bauer, A.M. 2000. Relationships of the Pachydactylus rugosus group of

geckos (Reptilia; Squamata: Gekkonidae). African Zoology 35: 55-67.

& 2001. Mitochondrial phylogeny of Namib day geckos (Rhoptropus) based

on cytochrome b and 16S rRNA sequences. Copeia 2001: 775-780.

& 2002. Phylogenetic relationships of the large-bodied members of the

African lizard genus Pachydactylus (Reptilia: Gekkonidae). Copeia, in press.

Laurenti, J.N. 1768. Specimen Medicum, Exhibens Synopsin [sic] Reptilium

Emendatam cum Experimentis circa Venena et Antidota Reptilium Austriacorum.

Trattnern, Vienna.

Leviton, A.E. & Anderson, S.C. 1972. Description of a new species of Tropiocolotes

(Reptilia: Gekkonidae) with a revised key to the genus. Occasional Papers of the

California Academy of Sciences 96: 1-7.

Loveridge, A. 1944. New geckos of the genera Afroedura, new genus, and Pachydactylus

from Angola. American Museum Novitates 1254: 14.

Macey, J.R., Ananjeva, N.B., Wang, Y. & Papenfuss, T.J. 2000. Phylogenetic

relationships among Asian gekkonid lizards formerly of the genus Cyrtodactylus

based on cladisitic analyses of allozymic data: monophyly of Cyrtopodion and

Mediodactylus. Journal of Herpetology 34: 258-265.

, Larson, A., Ananjeva, N.B., & Papenfuss, T.J. 1997. Replication slippage may

cause parallel evolution in the secondary structures of mitochondrial transfer RNAs.

Molecular Biology and Evolution 14: 30-39.

, Wang, Y., Ananjeva, N.B., Larson, A. & Papenfuss, T.J. 1999. Vicariant

patterns of fragmentation among gekkonid lizards of the genus Teratoscincus

produced by the Indian collision: a molecular phylogenetic perspective and an

area cladogram for Central Asia. Molecular Phylogenetics and Evolution 12:

320-332.

Minton, S.A. 1982. Highlights in herpetology: it’s not all snakes. Proceedings of the

Indiana Academy of Sciences 92: 70-76.

Moffat, L.A. 1973. The concept of primitiveness and its bearing on the phylogenetic

classification of the Gekkota. Proceedings of the Linnean Society of New South

Wales 97: 275-301.

Nussbaum, R.A. & Raxworthy, C.J. 1994. The genus Paragehyra (Reptilia: Sauria:

Gekkonidae) in southern Madagascar. Journal of Zoology, London 232: 37-59.

— & 2000. Systematic revision of the genus Paroedura Giinther (Reptilia:

Squamata: Gekkonidae), with the description of five new species. Miscellaneous

Publications, Museum of Zoology, University of Michigan (189): i-iv + 1-26.

5 & Pronk, O. 1998. The ghost geckos of Madagascar: a further revision of

the Malagasy leaf-toed geckos (Reptilia, Squamata, Gekkonidae). Miscellaneous

Publications, Museum of Zoology, University of Michigan (186): i-1v + 1-26.

Ota, H., Honda, M., Kobayashi, M., Sengoku, S. & Hikida, T. 1999. Phylogenetic

relationships of eublepharid geckos (Reptilia: Squamata): a molecular approach.

Zoological Science 16: 659-666.

Pasteur, G. 1964. Recherches sur 1’ évolution des lygodactyles, lézards Afro-Malgaches

actuels. Travaux de I'Institut Scientifique Chérifien. Série Zoologie 29:1—132 + 12

plates.

1995. Biodiversité et reptiles: diagnoses de sept nouvelles espéces fossiles et

actuelles du genre de lézards Lygodactylus (Sauria, Gekkonidae). Dumerilia 2: 1-21.

Prince, J.H. 1949. Visual development 1. E. & S. Livingstone, Edinburgh.

Rittenhouse, D.R., Russell, A.P. & Bauer, A.M. 1998. The larynx and trachea of the

barking gecko, Prenopus garrulus maculatus (Reptilia: Gekkonidae) and their

relation to vocalization. South African Journal of Zoology 33: 23-30.

Roll, B. 1995. Crystallins in lenses of gekkonid lizards (Reptilia, Gekkonidae).

Herpetological Journal 5: 298-304.

1997. Photoreceptors of diurnal and nocturnal geckos. In: Elsner, N. and Wassle,

H. (eds), Proc. 25 Géttingen Neurobiology Conference Vol. II, 502. Thieme, Stutt-

gart.

1999. Biochemical and morphological aspects of the relationship of the Namaqua

day gecko to Phelsuma and Rhoptropus (Reptilia, Gekkonidae). Zoology 102: 50-

60.

In press. Cnemaspis: tertiarily diurnal (Reptilia, Gekkonidae). Herpetological

Journal.

& Schwemer, J. 1999. L-Crystallin and vitamin A, isomers in lenses of diurnal

geckos. Journal of Comparative Physiology A 185: 51-58.

Rosenberg, H.I. & Russell, A.P. 1980. Structural and functional aspects of tail

squirting: a unique defense mechanism of Diplodactylus (Reptilia: Gekkonidae).

Canadian Journal of Zoology 58: 865-881.

7 & Kapoor, M. 1984. Preliminary characterization of the defensive secre-

tion of Diplodactylus (Reptilia: Gekkonidae). Copeia 1984: 1025-1028.

GECKO CLASSIFICATION

Rosler, H. 2001. Zur Rumpfbeschuppung der Gattung Phelsuwma Gray, 1825:

Zoogeographische Aspekte (Sauria: Gekkonidae). Gekkota 3: 47-73.

— & Wranik, W. 2001. Bemerkungen zur Fortpflanzungsbiologie von Geckonen —

2. Untersuchungen zur Reprpoduktion von Pristurus obsti R6sler & Wranik, 1999

und Pristurus sokotranus Parker, 1938 im Vergleich zu anderen Geckos (Sauria:

Gekkonidae). Gekkota 3: 125-182.

Ruibal, R. & Ernst, V. 1965. The structure of the digital setae of lizards. Journal of

Morphology 117: 271-294.

Russell, A.P. 1972. The foot of gekkonid lizards: a study in comparative and functional

anatomy. Unpublished Ph.D. thesis, University of London, England.

1 976. Some comments concerning interrelationships amongst gekkonine geckos.

pp.217-244. In: Bellairs, A.d’A. & Cox, C.B. (eds). Morphology and Biology of

Reptiles. Linnean Society Symposium Series 3. Academic Press, London.

1977a. The phalangeal formula of Hemidactylus Oken, 1817 (Reptilia:

Gekkonidae): a correction and a functional explanation. Anatomia Histologia

Embryologia 6: 332-338.

— 1977b. The genera Rhoptropus and Phelsuma (Reptilia: Gekkonidae) in Southern

Africa: a case of convergence and a reconsideration of the biogeography of Phelsuma.

Zoologica Africana 12: 393-408.

— 1979. Parallelism and integrated design in the foot structure of gekkonine and

diplodactyline geckos. Copeia 1979: 1-21.

& Bauer, A.M. 1988. Paraphalangeal elements of gekkonid lizards: a compara-

tive survey. Journal of Morphology 197: 221-240.

& 1989. The morphology of the digits of the golden gecko, Calodactylodes

aureus (Reptilia: Gekkonidae) and its implications for the occupation of rupicolous

habitats. Amphibia-Reptilia 10: 125—140.

—& 1990. Digit I in pad-bearing gekkonine geckos: alternate designs and the

potential constraints of phalangeal number. Memoirs of the Queensland Museum

29:453-472.

& 1993. Aristelliger Cope. Caribbean geckos. Catalogue of American

Amphibians and Reptiles 565.14.

, Rittenhouse, D.R. & Bauer, A.M. 2000. Laryngotracheal morphology of Afro-

Madagascan geckos — a comparative survey. Journal of Morphology 245: 241-268.

Stephenson, N.G. 1960. The comparative osteology of Australian geckos and its

bearing on their morphological status. Transactions of the Royal Society of New

Zealand 84: 341-358.

& Stephenson, E.M. 1956. The osteology of the New Zealand geckos and its

bearing on their morphological status. Transactions of the Royal Society of New

Zealand 84: 341-358.

Szezerbak, N.N. & Golubev, M.L. 1977. Systematics of the Palearctic geckos (genera

Gymnodactylus, Bunopus, Alsophylax) [in Russian]. Trudy Zoologiiskogo Instituta

Akademiya Nauk USSR 74: 120-133.

—& 1984. On generic assignement of the Palearctic Cyrtodacrylus lizard

species (Reptilia, Gekkonidae) [in Russian]. Vestnik Zoologii 1984(2); SO-S6.

121

& 1986. Gecko Fauna of the USSR and Contiguous Regions [in Russian].

Naukova Dumka, Kiev.

Underwood, G. 1951a. Reptilian retinas. Nature 167: 183.

1951b. Pupil shape in certain geckos. Copeia 1951: 211-212.

1954. On the classification and evolution of geckos. Proceedings of the Zoologi-

cal Society of London 124: 469-492.

1955. Classification of geckos. Nature 175: 1089.

1957. On lizards of the family Pygopodidae. A contribution to the morphology

and phylogeny of the Squamata. Journal of Morphology 100:207-268.

1967. A Contribution to the Classification of Snakes. British Museum (Natural

History) Publication No. 653. Trustees of the British Museum (Natural History),

London. 179pp.

—— 1968. Some suggestions concerning vertebrate visual cells. Vision Research 8:

483-488.

1970. The eye. pp. 1-97. In: Gans, C. & Parsons, T. (eds). Biology of the Reptilia,

vol. X. Academic Press, London.

1971a. A modern appreciation of Camp’s ‘Classification of the lizards.’ Pp. vii—

xvii In Camp, C.L., Classification of the Lizards. Society for the Study of Amphibians

and Reptiles, Lawrence, Kansas.

1971b. Vertebrate comparative anatomy at the cellular level: visual cells and

phylogeny. pp.64—69. In: Hecht, M. (ed). Vertebrate Evolution: Mechanism and

Process. Report of the NATO Advanced Study Institute, Robert College, Istanbul,

Turkey 4-15 August, 1969. NATO.

1977a. Simplification and degeneration in the course of evolution of squamate

reptiles. Colloques internationaux C.N.R.S. N° 266 — Mécanismes de la

Rudimentation des Organes chez les Embryons de Vertébrés. pp.341-351.

1977b. Comments on phyletic analysis of gekkotan lizards. NATO Advanced

Studies Institute Series (Life Sciences) 14: 53-55.

Vanzolini, P.E. 1968.Geography of the South American Gekkonidae. Arquivos de

Zoologia 17: 85-112.

Vences, M., Henkel, F.-W. & Seipp, R. 2001. Molekulare Untersuchungen zur

Phylogenie und Taxonomie der Neukaledonischen Geckos der Gattung Rhacodactylus

(Reptilia: Gekkonidae). Salamandra 37: 73-82.

Walls, G.L. 1942. The Vertebrate Eye, Cranbrook Institute Scientific Bulletin 19,

Bloomfield Hills, Michigan.

Wellborn, V. 1933. Vergleichende osteologische Untersuchungen an Geckoniden,

Eublephariden and Uroplatiden. Sitzungsberichte der Gesellschaft Naturforschender

Freunde zu Berlin 1933: 126-199.

Wells, R.W. & Wellington, C.R. 1983. A synopsis of the class Reptilia in Australia.

Australian Journal of Herpetology 1: 73-129.

Werner, Y.L. 1972. Observations on eggs of eublepharid lizards, with comments on the

evolution of the Gekkonoidea. Zoologische Mededelingen 47: 21\—224, pl. I.

1977. Ecological comments on some gekkonid lizards of the Namib Desert, South

West Africa. Madoqua 10: 157-169.

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 123-130

Issued 28 November 2002

The skull of the Uropeltinae (Reptilia,

Serpentes), with special reference to the otico-

occipital region

OLIVIER RIEPPEL

Department of Geology, The Field Museum, 1400 S Lake Shore Drive, Chicago, IL 60605-2496, U.S.A. e-mail:

rieppel @ fieldmuseum.org

HUSSAM ZAHER

Universidade de Sao Paulo, Instituto de Biociencias, Departamento de Zoologia, Rua do Matao, Travessa 14,

Cidade Universitaria, OSSO8-900, Sao Paulo, SP, Brazil

Synopsis. The skull anatomy of uropeltines is reviewed, and new data is presented on the highly derived otico-occipital region.

A phylogenetic analysis of uropeltine interrelationships using parsimony is performed using characters derived from skull

structure. The basal position of the genus Melanophidium is confirmed; Pseudotyphlops is a relatively derived uropeltine, in spite

of its relatively large size. The monophyly of the genera Melanophidium and Rhinophis requires further testing.

INTRODUCTION

Uropeltinae (Nopesa 1923. The name is here used as by Kluge 1991,

Fig. 4; see also Cundall et al. 1993) remain an enigmatic group of

basal alethinophidian snakes. This is largely due to their burrowing

habits and restricted distribution, and the consequent scarcity of

material available in public repositories. We have studied the

uropeltine skulls from the collections of The Natural History Mu-

seum, London, which permitted us to review the highly derived skull

structure in this monophyletic clade of snakes.

The first detailed description of a uropeltine skull was given by

Baumeister (1908) in a monograph on the genus Rhinophis. Peculi-

arities of the cranio-vertebral joint in the group were dealt with by

Williams (1959), Underwood (1967), and Hoffstetter & Gasc (1969).

Some aspects of the skull of uropeltines were described by Rieppel

(1977, 1978, 1983), Bellairs & Kamal (1981), and Wever (1978),

but none of these studies addressed details of the morphology of the

otico-occipital complex. The lower jaw of uropeltines was described

by Rieppel & Zaher (2000). In their detailed analysis of the cranial

anatomy and phylogenetic relationships of Anomochilus, Cundall &

Rossman (1993), and Cundall et al., (1993), comment on various

aspects of the skull structure of uropeltines, and their functional as

well as phylogenetic significance. In particular, Cundall & Rossman

(1993; see also Cundall & Greene 2000) recognized a fundamen-

tally different design of skull adaptation to burrowing habits in

scolecophidians and uropeltines (Fig. 1). The phylogenetic relation-

ships of uropeltines within snakes were discussed in cladistic terms

by Cundall et al. (1993), Scanlon & Lee (2000), and Tchernov et al.,

(2000). Only one study has appeared so far that dealt with uropeltine

interrelationships, based on microcomplement fixation techniques

(Cadle et al. 1990). In this paper, we review the skull anatomy of

uropeltines, adding new detail to previous descriptions (Rieppel

1977, 1978) and providing new data on the detailed morphology of

the otico-occipital complex. These morphological characters are

used in a phylogenetic analysis of uropeltine interrelationships,

which will be compared to the results obtained by Cadle er al.

(1990). This study is presented in honor of Dr. Garth Underwood,

who more than 20 years ago introduced the senior author to the study

of the skull of ‘henophidian’ snakes.

MATERIAL EXAMINED

The present study is based on the investigation of the skull of the

following taxa (generic names used in the manuscript refer only to

the specimens here listed), arranged as outgroup taxa and in-group

(uropeltine) taxa.

Institutional abbreviations

BMNH, British Museum (Natural History), now The Natural His-

tory Museum; FMNH, Field Museum of Natural History, now The

Field Museum.

Outgroup taxa: Anilius scytale (FMNH 35683); Cylindrophis

maculatus (BMNH_ 1930.5.8.48); Cylindrophis ruffus (FMNH

179033); Boa constrictor (FMNH 22435, 22438): Calabaria

reinhardtii (FMNH 31372); Candoia aspera (FMNH 13915);

Candoia b. australis (FMNH 22997); Lichanura roseofusca (FMNH

31565); Python molurus (FMNH 223198); Tropidophis pardalis

(FMNH 233).

In-group taxa: Melanophidium punctatum (BMNH 1930.5.8.119);

Melanophidium wynaudense (BMNH _ 1930.5.8.124—-125); Platy-

plecturus madurensis (BMNH 1930.5.8.111); Plecturus perroteti

(BMNH 1930.5.8.105); Pseudotyphlops philippinus (BMNH

1978.1092); Rhinophis drummondhayi (BMNH 1930.5.8.67—68);

Rhinophis sanguineus (BMNH _ 1930.5.8.59); Teretrurus rhodo-

gaster (BMNH_ 1930.5.8.98); Uropeltis woodmansoni (BMNH

1930.5.8.73-74);

Abbreviations used in the figures

ang, angular; bo, basioccipital; com, compound bone; d, dentary;

ec, ectopterygoid; f, frontal; Is, laterosphenoid; m, maxilla; n, nasal;

0c, otic capsule; op-eo, opisthotic-exoccipital; p, parietal; pl, pala-

tine; pm, premaxilla; po.vc, posterior opening of Vidian canal; prf,

prefrontal; pro, prootic; pro.c, prootic canal; pro.r, preorbital ridge;

pt, pterygoid; q, quadrate; sm, septomaxilla; so, supraoccipital; sp,

splenial; tr-f.r, transverse frontal ridge; v, vomer; II, optic foramen;

Ne trigeminal foramen (maxillary branch); Vy trigeminal foramen

(mandibular branch); VII, facialis foramen; X, jugular foramen;

XII, hypoglossal foramen.

124

Fig. 1 The skull and mandible of Pseudotyphlops philippinus (BMNH

1978.1092) in left lateral view.

GENERAL ASPECTS OF THE SKULL

The premaxilla of uropeltines is characterized by a single premaxil-

lary foramen (Fig. 2). The vomerine processes of the premaxilla

meet the vomer in a well-defined contact. The premaxilla of

uropeltines shows characteristic variation within the group (Rieppel

1977; Cundall & Rossman 1993). The anterior margin of its trans-

verse process is more or less evenly rounded in Melanophidium,

which correlates with a gentle anteromedial curvature of the anterior

end of the maxilla (Fig. 2A). The two bones closely approach each

other, or barely establish contact. This genus therefore retains a

plesiomorphic configuration of the snout, which is also inferred to

be present in Platyplecturus (the specimen BMNH 1930.5.8.111

lacks the premaxilla, but retains the maxilla which shows an

anteromedially curved anterior end), and which represents a con-

dition similar to that seen in Anomochilus (Cundall & Rossman

1993). The other uropeltines have a similar premaxilla, which

carries an anteriorly projecting, bipartite rostrum. The straight ‘trans-

verse’ processes point posterolaterally, and meet the straight maxilla

O. RIEPPEL AND H. ZAHER

in a shizarthrosis (Cundall & Rossman 1993; Fig. 2B—E). These two

elements define the lateral margins of the strongly ‘telescoped’

(Haas 1930), i.e., tapering and pointed snout (see also Cundall &

Rossman 1993, Fig. 25B).

The maxilla of basal alethinophidians carries an anterior medial

process (Rieppel 1977; Scanlon & Lee 2000), which is particularly

well developed in uropeltines, where it participates in the formation

of a broadly overlapping contact between maxilla, premaxilla, and

vomer. In Melanophidium, the anterior medial process of the maxilla

is not engaged in any such contact, but freely underlaps the

septomaxilla. In Pseudotyphlops, the anterior medial process of the

maxilla overlaps a medially extending horizontal flange of the

transverse process of the premaxilla in a complex, interlocking

premaxillary — maxillary contact (Fig. 2B, D-E). Rhinophis and

Uropeltis are unique in that the anterior medial process of the

maxilla forms a well-defined sutural contact with an anterior lateral

process of the vomer in front of the opening for Jacobson’s organ.

The medial or choanal processes of the palatines of uropeltines

are broad, arching over the choanal tubes and projecting ventrally

again medial to the choanal tubes. Their ventral tips are embraced

anteriorly by the posterior ends of the vomers, as is also the case in

other basal alethinophidians (Cundall & Rossman 1993; Cundall et

al. 1993; Rieppel 1983; Fig. 2, 3). The parasphenoid forms a sagittal

interchoanal process that lies between the choanal processes of the

palatines, as is also the case in Anomochilus and Cylindrophis

(Cundall & Rossman 1993; Cundall et al. 1993). The dorsal lamina

of the nasal is variously developed in uropeltines, but tends to be

relatively broad and notched anterolaterally in species with a rounded

snout, but slender and tapering to a fine tip in species with a strongly

telescoped snout.

The snout complex is suspended from the rest of the skull at the

naso-frontal joint (see Rieppel 1978, for details) and through the link

provided by the prefrontal (Fig. 3). The maxilla of uropeltines

carries a well-developed ascending process that is in a firm planar

(i.e., not interdigitating) contact with the prefrontal. Medial to the

ascending process, the superior alveolar nerve canal is open dorsally

in uropeltines, appearing as a groove on the dorsal surface of the

Fig.2 A-E The palate in uropeltine snakes. A, Melanophidium wynaudense (BMNH 1930.5.8.124); B, Pseudotyphlops philippinus (BMNH 1978.1092):

C, Rhinophis sanguineus (BMNH 1930.5.8.59); D-E, Pseudotyphlops philippinus (BMNH 1978.1092).

SKULL OF UROPELTINAE

B 2mm

Fig. 3 The snout complex of Pseudotyphlops philippinus (BMNH 1978.1092).

maxilla, a unique condition among snakes (Fig. 4). The suspension

of the snout complex from the braincase is more elaborate in

uropeltines than it is in other basal alethinophidians (Rieppel 1978).

The parietal of uropeltines forms distinct anterolateral, 1.e.,

supraorbital processes which may or may not contact the prefrontal

(Fig. 3). In Cylindrophis maculatus and in Anomochilus (Cundall &

Rossman 1993), as well as in Melanophidium punctatum, the

supraorbital process of the parietal participates in the suspension of

the prefrontal. In other uropeltines, the contact between parietal and

prefrontal may be reduced or absent, due to a relatively shorter

supraorbital process of the parietal (this character is bilaterally

variable in the skull of Platyplecturus). The optic foramen is located

between the frontal and parietal in Melanophidium and Platy-

plecturus, but within the frontal in Plecturus, Rhinophis, and

Uropeltis (Underwood, 1967: 64). In Pseudotyphlops (Fig. 3A) and

Teretrurus, the optic foramen is a slit-like opening in the posterior

margin of the frontal. The parietal carries a low sagittal crest in the

relatively large Pseudotyphlops (Fig. 5C). In the other species with

smaller skulls, such a sagittal crest is at best very faintly developed

in the posterior part of the parietal (Fig. 5SA—B). In some uropeltines

such as Rhinophis and Uropeltis (Fig. 5B), the parietals are not

completely fused in their posterior part. A supratemporal is absent in

uropeltines, and the quadrate is suspended from the otic capsule ina

relatively low position. The suprastapedial process of the quadrate is

very elaborate in uropeltines, and as in Anomochilus (Cundall &

Rossman 1993), it exceeds the shaft of the quadrate in length.

In Anomochilus, the anterior end of the edentulous palatine shows

some elaboration into a broader structure that receives the medial

(palatine) process of the maxilla in a deep facet (Cundall & Rossman

1993, Fig. 2B). In uropeltines, the anterior process of the palatine is

modified to form a broad wing which establishes a broad ventral

overlap with the posterolateral part of the vomer, and which receives

the well developed medial process of the maxilla in a deeply

recessed lateroventrally facing facet (Fig. 2). The infraorbital nerve

(maxillary division of the trigeminal nerve) pierces the bottom of

this recessed facet to become the superior alveolar nerve. The

morphology of the palatine in Anomochilus is intermediate between

that of Cylindrophis on the one hand, and that of uropeltines on the

other (Cundall & Rossman 1993). Palatine teeth are absent in

Anomochilus and uropeltines with the exception of Melanophidium

wynaudense. The ectopterygoid and pterygoid are reduced in

uropeltines (and even more so in Anomochilus: Cundall & Rossman

1993), and the pterygoid is edentulous.

The para-basisphenoid is relatively broad in uropeltines, gradually

becoming narrower anteriorly and tapering to a pointed tip between

the choanal processes of the palatines. The ventral surface of the

para-basisphenoid is distinctly convex in Pseudotyphlops resulting

in the formation of ventrolateral ridges. These are at best weakly, or

only very faintly, developed in other, smaller, species with a para-

basisphenoid that has a flat or even slightly convex ventral surface.

Along the lateral edge of the para-basisphenoid the ossified crista

trabecularis ends behind the anterior margin of the laterally descend-

ing flange of the parietal in most taxa except for Teretrurus and

Rhinophis drummondhayi, where it ends at the anterior margin of the

126

C 1mm

Fig.4 A-C A, The left maxilla of Cylindrophis maculatus (BMNH

1930.5.8.48) in lateral and dorsal views; B, The left maxilla of

Melanophidium wynaudense (BMNH 1930.5.8.124) in lateral and dorsal

views; C, The left maxilla of Pseudotyphlops philippinus (BMNH

1978.1092) in lateral and dorsal views.

laterally descending flange of the parietal. In Rhinophis sanguineus

and Uropeltis, the crista trabecularis extends further anteriorly and

terminates below the optic foramen that is located in the frontal. In

front of the ossified crista trabecularis, the cartilaginous trabecula

cranii is embedded in all taxa in a deep furrow located between the

lateral margin of the parasphenoid and the ventrally projecting margin

of the frontal. Tiny fontanelles may persist along the line of fusion of

the basisphenoid and basioccipital in Rhinophis and Uropeltis.

THE OTICO-OCCIPITAL COMPLEX

The otico-occipital complex is here considered to include the prootic,

opisthotic-exoccipital, supraoccipital, and basioccipital. These brain-

O. RIEPPEL AND H. ZAHER

case elements show a variable degree of fusion with each other

among the specimens examined (Fig. 6). All braincase elements

except the opisthotic and exoccipital remain separate from one

another in Melanophidium. All braincase elements are fused with

one another in Plecturus, Pseudotyphlops, Rhinophis and Uropeltis,

but the basioccipital remains separate from the basisphenoid in

Teretrurus. The exoccipitals and basioccipital are always fused in

the occipital condyle. The stalk of the occipital condyle is short in

Melanophidium, Platyplecturus, and Teretrurus, but distinctly elon-

gated in the other taxa investigated, such that the depression of the

basioccipital housing the brainstem is exposed in dorsal view (Fig.

5). The exoccipitals define the dorsal margin of the foramen mag-

num, and their posterolateral corners are either deeply notched, or

perforated by a foramen.

A laterosphenoid is always present in uropeltines, but while it

remains a relatively narrow element in Melanophidium (Fig. 6A—B)

and Pseudotyphlops (Fig. 6C), it becomes distinctly broadened in

the other taxa investigated.

The plesiomorphic condition of the posterior opening of the

Vidian canal and its relation to the facial nerve branches is exempli-

fied by Melanophidium among uropeltines (Fig. 6A—B). The

hyomandibular and palatine branches of the facial nerve exit from

separate foramina opening into an obliquely oriented recess located

on the prootic closely behind the foramen for the mandibular branch

of the trigeminal nerve in Melanophidium punctatum (Fig. 6A), and

incompletely separated from the posterior margin of the mandibular

branch foramen in Melanophidium wynaudense (Fig. 6B). The

recess housing the facialis foramina becomes deeper ventrally, as it

connects with the posterior opening of the Vidian canal that is

located on the prootic — basisphenoid suture. This condition is

closely comparable to that in Cylindrophis and Anomochilus (Cundall

& Rossman 1993), except that the posterior opening of the Vidian

canal is located more (Anomochilus: Cundall & Rossman 1993, Fig.

4) or less (Cylindrophis maculatus) below the prootic — basisphe-

noid suture. In Pseudotyphlops (Fig. 6C) and Rhinophis sanguineus

(Fig. 6F), the palatine branch of the facial nerve enters directly into

a canal within the prootic which connects ventrally with the Vidian

canal, and which opens dorsally within the posteriorly expanded

recess of the mandibular branch foramen. This prootic canal appears

to be a modification of the condition observed in Melanophidium by

the lateral closure of the prootic recess that houses the facialis nerve

foramina. In Pseudotyphlops and Rhinophis sanguineus the Vidian

canal retains no separate posterior opening; the internal carotid

enters directly into the opening of the prootic canal. In all other taxa

investigated (e.g., Uropeltis, Fig. 6D; Rhinophis drummondhayi,

Fig. 6E), the palatine branch of the facial nerve enters again a prootic

canal which is completely separated from the mandibular branch

foramen however, and which opens anteroventral to the anterior

corner of the juxtastapedial recess. The internal carotid enters the

prootic canal on its way to the sella turcica. The anterior opening of

the Vidian canal lies on the suture between para-basisphenoid and

parietal in front of the dorsolateral wings of the para-basisphenoid

(McDowell 1967).

The juxtastapedial recess is well developed in uropeltines, which

all except Pseudotyphlops share with Anilius and Cylindrophis the

presence of a fenestra pseudorotunda (Rieppel 1979a). The shaft of

the stapes is directed posterolaterally as it connects with the elon-

gated suprastapedial process of the quadrate via the stylohyal (Rieppel

1980; see also Wever 1978). As in scolecophidians and basal

alethinophidians, the juxtastapedial recess is open posteriorly, and

the jugular foramen is exposed in lateral view (Tchernov et al. 2000;

Fig. 6). The posteroventral corner of the crista circumfenestralis is

enlarged to form a gliding surface for the quadrate ramus of the

SKULL OF UROPELTINAE 127

pro

pro-op-eo

bo bo

Atmm_ B_tmmS Cimm

Fig.5 A-C The otico-occipital region of uropeltine snakes in dorsal views. A, Melanophidium wynaudense (BMNH 1930.5.8.124); B, Uropeltis

woodmansoni (BMNH 1930.5.8.73); C, Pseudotyphlops philippinus (BMNH 1978.1092).

pro.c

Cimm VII V3 D

op-eo/so

aaa proc Is Pt Feeds 21 I 4 vil a

P pro.c

Fig.6 A-—F The otico-occipital region of uropeltine snakes in right lateral views. A, Melanophidium punctatum (BMNH 1930.5.8.119); B,

Melanophidium wynaudense (BMNH 1930.5.8.124); C, Pseudotyphlops philippinus (BMNH 1978.1092); D, Uropeltis woodmansoni (BMNH

1930.5.8.73); E, Rhinophis drummondhayi (BMNH 1930.5.8.67—68); F, Rhinophis sanguineus (BMNH 1930.5.8.59).

128

pterygoid in Melanophidium (Fig. 6A—B) and Pseudotyphlops (Fig.

6C), a surface that is ‘rounded off’ to a variable degree in smaller

species, and reduced in Rhinophis drummondhayi (Fig. 6E). By the

fact that the braincase elements remain separate in Melanophidium,

it is possible to ascertain that the prootic, opisthotic-exoccipital, and

basioccipital contribute to this enlarged posteroventral part of the

crista circumfenestralis. In the plesiomorphic condition, the

juxtastapedial recess is wide open laterally (Cylindrophis,

Anomochilus: Cundall & Rossman 1993), and such is also the case

in Melanophidium (Fig. 6A—B), Platyplecturus and Teretrurus. In

other uropeltines, the lateral opening of the juxtastapedial recess is

closed to a narrow slit, most extremely so in Uropeltis (Fig. 6D) and

Rhinophis (Fig. 6E-F), where the dorsal and ventral lips of the crista

circumfenestralis closely approach each other, or may even estab-

lish a restricted contact with each other. Never is the juxtastapedial

recess fully closed laterally, however, as is the case in Liotyphlops

(Haas 1964), typhlopids and leptotyphlopids (Rieppel 1979b). The

jugular foramen is internally subdivided in most uropeltines (except

in Pseudotyphlops, Teretrurus and Uropeltis), and it is located either

behind the juxtastapedial recess (plesiomorphic), or in the

posteroventral corner of the latter (in Platyplecturus, Plecturus,

Teretrurus and Uropeltis). The exoccipital is pierced by two hy-

poglossal foramina in Melanophidium punctatum (Fig. 6A), but by

a single, enlarged hypoglossal foramen in the other taxa investi-

gated.

PHYLOGENETIC INTERRELATIONSHIPS

Recent cladistic analyses hypothesized that Anomochilus is the

sister-group of uropeltines (Scanlon & Lee 2000; Tchernov et al.

2000), and Cylindrophis is the sister-group of uropeltines plus

Anomochilus (YTchernov et al. 2000; see also McDowell 1987;

Cundall et al. 1993, osteological data only). The addition of soft

anatomy characters by Cundall et al. (1993) resulted in a different

p 6

4? oY y N

” v { & \ 0) ‘

Ce ae ee Wee

AY | y U \y \ 0 (° RY,

ie 8 mn.

NY RY Ny Ry W AN x” ny £

\" " Ay “ RY 5 RY) s 0

Bs Sg gic SANs, a0 Ree eae peel

Cl Pee en a

CE Oe Ae aaa

Ls 7 The phylogenetic interrelationships of Uropeltinae. See text for

urther discussion.

O. RIEPPEL AND H. ZAHER

Table 1. The data matrix used in the analysis of the phylogenetic

interrelationships of Uropeltinae. Character definitions are given in

Appendix I.

12345 67891 11111 11112 22222 22223 333

0 12345 67890 12345 67890 123

00000 01000 00000 00022 11111 11111 111

00100 00000 00000 10022 11111 11111 111

01100 00111 12011 10122 11111 11121 111

bali lalaly 7Zontital atzalal(oynlatwgzy afilabaist abstilaal alital

10L00 TLI10 12001 10222 1IAT) Tae Aa

11111 LAA 312110 19222 TAT Ae a

1A, ZOU SAAT) W222 Ae a Ae els

PATOL OOLT 127 AOA 2S eet 2 ected

21200 O1L11. OLL01, 11222 L111 eae Ae

00100 01000 0000? 00011 11111 11120 000

00000 00000 00000 00010 00001 11110 000

if a

00000 00000 00000 00000 00000 00010 000

Melanoph. punctatum

Melanoph. wynaud.

Platyplecturus

Uropeltis

Teretrurus

Rhinophis drum.

Rhinophis sang.

Plecturus

Plseudotyphlops

Anomochilus

Cylindrophis

Anilius

cladogram, which still reproduces the monophyly of Alethinophidia

and Macrostomata respectively, but which shows anilioids (Rieppel

1977, 1988) to be paraphyletic. The sound transmitting apparatus

was found to be ‘similar’ in Typhlops and Rhinophis by Wever

(1978: 705), but a sister-group relationship of scolecophidians and

uropeltines has so far never been recovered through cladistic analy-

sis of morphological data (Cundall etal. 1993; Kluge, 1991; Scanlon

and Lee 2000; Tchernov et al. 2000), and it was specifically rejected

by Cadle et al. (1990; see also Cundall & Rossman 1993).

Previous work (Tchernoy et al. 2000), and the description of the

uropeltine skull presented above, allows the delimitation of 33

phylogenetically potentially informative characters (Appendix I

and Table 1) for an analysis of uropeltine interrelationships. Given

the currently controversial relationships of Anilius and Anomochilus

relative to uropeltines, these two taxa together with Cylindrophis

were used as paraphyletic outgroup in the analysis of uropeltine in-

group relationships (characters 25 through 28 are uninformative

using this rooting procedure, and were ignored in the analysis). The

analysis was performed using PAUP version 3.1.1. (Swofford 1991,

Swofford & Begle 1993). All multistate characters were unordered,

and the branch-and-bound search option was implemented. Character

optimization is based on the DELTRAN routine.

A single most parsimonious tree was obtained (TL = 49; CI =

0.796; RI = 0.877) with fully resolved uropeltine relationships.

Given the scarcity of characters, it is not surprising that some nodes

among uropeltines are rather poorly supported (with the minimal

decay index or Bremer support index [Bremer 1988]: +1). Neverthe-

less, the tree (Fig. 7) suggests some interesting preliminary results.

The basal position of Melanophidium among uropeltines was

expected (Rieppel 1977; McDowell 1987), and is reproduced here.

However, there is a signal for paraphyly of the genus Melanophidium.

Melanophidium wynaudense appears to be more closely related to

other uropeltines than it is to Melanophidium punctatum (decay

index: +1) on the basis of the presence of a single (enlarged)

hypoglossal foramen behind the jugular foramen (16[1]; ci=1).

Evidently, the monophyly of the genus Melanophidium must be

tested by the addition of other characters, including soft anatomy,

because the result obtained here may be nothing more than the

reflection of the fact that as coded, Melanophidium punctatum is

plesiomorphic relative to all other uropeltines in all characters that

SKULL OF UROPELTINAE

are informative for the analysis of uropeltine interrelationships

(unfortunately, Melanophidium was not included in the analysis

performed by Cadle er al. [1990]).

The genera Teretrurus, Platyplecturus, Pseudotyphlops, Plecturus,

Uropeltis, and Rhinophis form a monophyletic clade that is very

strongly supported on the basis of 7 characters (decay index: +6).

This represents a strong corroboration of the basal position of the

genus Melanophidium (unequivocal synapomorphies are designated

with an asterisk): *8(1), supraoccipital fused to opisthotic —

exoccipital; *9(1) prootic fused to opisthotic — exoccipital; 11(1)

laterosphenoid broad (reversal implied); 12(2) palatine branch of

facial nerve enclosed in prootic canal which is separate from man-

dibular branch foramen; 15(1) jugular foramen single (reversals

implied); 18(2) posteroventral process of dentary absent (reversal

implied); 29(2) gliding surface for pterygoid posteroventral to

juxtastapedial recess ‘rounded off’ (reversal implied). The

monophyly of all uropeltines except Melanophidium is the most

strongly supported clade on the basis of this data set.

Within that clade, Platyplecturus is the sister-taxon of a clade that

includes (Pseudotyphlops (Plecturus (Rhinophis, Uropeltis))) on

the basis of 2 characters (decay index: +1): *2(1) nasals narrow

anteriorly, gradually tapering to pointed tip; *10(1) basioccipital

fused to basisphenoid. Pseudotyphlops is the sister-taxon of a clade

that includes (Plecturus (Rhinophis, Uropeltis)) on the basis of three

characters (decay index: +1): 1(1) transverse process of the premax-

illa points posterolaterally, and meets the straight maxilla in a

shizarthrosis (convergent in Jeretrurus); *13(1) narrow lateral open-

ing of the juxtastapedial recess; *17(1) stalk of the occipital condyle

elongated. Plecturus shares with the (Rhinophis, Uropeltis) — clade

three characters (decay index: +2): 5(1) optic foramen fully enclosed

by frontal; 14(1) jugular foramen recessed within posteroventral

corner of juxtastapedial recess; 15(0), jugular foramen internally

subdivided (reversal).

The clade that includes Rhinophis and Uropeltis (decay index:

+1) is diagnosed by a well-defined buttressing contact between the

processus medialis anterior of the maxilla and an anterior lateral

process of the vomer (*4 [1]). Interestingly, there is a signal for the

paraphyly of the genus Rhinophis, because Rhinophis sanguineus

appears to be more closely related to Uropeltis than to Rhinophis

drummondhayi on the basis of two characters (decay index: +1):

6(2) crista trabecularis ends in front of lateral fronto-parietal suture;

7(0) supraorbital process of parietal does not contact prefrontal

(reversal).

DISCUSSION AND CONCLUSIONS

The monophyly of Uropeltinae has not previously been questioned

(Rieppel 1977; Cadle et al. 1990; Cundall eral. 1993; Scanlon & Lee

2000; Tchernovy ef al. 2000) and is here corroborated by six un-

equivocal synapomorphies (decay index: +3): *19(2), exoccipitals

and basioccipital fused in occipital condyle; *20(2), anterior denti-

gerous process of palatine modified into expanded lamina; *30(1),

occipital condyle modified as described by Williams (1959) and

Hoffstetter & Gasc (1969); *31(1), the superior alveolar nerve canal

in the maxilla is open dorsally; *32(1), frontals at least twice as long

as broad; *33(1), supratemporal absent.

The phylogenetic analysis of the interrelationships among

Uropeltinae corroborates the hypothesized basal position of the

genus Melanophidium, the latter possibly paraphyletic. The clade

comprising Jeretrurus and the Indian species of Uropeltis that 1s

consistently obtained on the basis of allozyme data (Cadle et al.

129

1990) is not supported here. By contrast, the possible paraphyly of

the genus Rhinophis indicated by molecular data (Cadle et al. 1990)

is also found here, although far less species were included in the

morphological analysis.

Pseudotyphlops is larger that all other uropeltines included in the

analysis, and it shows characters of cranial anatomy that appear in

outgroup taxa such as Anilius and Cylindrophis, but not in other

uropeltines. In the adult skull of Anilius and Cylindrophis, the part of

the para-basisphenoid located behind the optic foramen has a con-

cave ventral surface, which results in the formation of distinct lateral

ventral ridges (Tchernov et al. 2000). This character is also observed

in the relatively large skull of adult Pseudotyphlops. In the much

smaller skull of other uropeltines, the ventral surface of the para-

basisphenoid is at best very weakly concave, flat, or even slightly

convex, and ventral lateral ridges are very faintly indicated

(Melanophidium, Platyplecturus, Plecturus, Uropeltis, Rhinophis),

or absent (Jeretrurus; also in Anomochilus: Cundall & Rossman

1993). The same observation relates to the presence of a sagittal

ridge on the parietal, well expressed in adult Anilius, Cylindrophis,

and in Pseudotyphlops among uropeltines, much reduced and re-

stricted to the posterior part of the parietal or absent in Anomochilus

and smaller uropeltines. Given its relative size, and the presence of

relatively plesiomorphic features in the skull, a basal position of

Pseudotyphlops relative to other uropeltines might have been

expected, but was not corroborated by cladistic analysis, although

the genus is still outside the (Plecturus (Rhinophis, Uropeltis))

clade.

The morphological transformation that is implied in the descrip-

tion of the Vidian canal in uropeltines (and in its coding; the

character was used unordered) is also contradicted by the cladistic

analysis discussed above. The description suggests that the indi-

vidualization of the prootic canal (which receives the palatine

branch of the facial nerve and into which enters the internal carotid)

follows its formation in association with the recess of the mandibu-

lar branch foramen, the cladistic analysis suggests otherwise. The

incorporation of the opening of the prootic canal into the recess of

the mandibular branch foramen is a secondary development that

occurred convergently in Pseudotyphlops and Rhinophis sanguineus.

ACKNOWLEDGEMENTS. We would like to thank E.N. Arnold and C.

McCarthy (BMNH), as well as Harold Voris and Alan Resetar (FMNH) for

permission to study the collections under their care. D. Cundall and two

anonymous reviewers offered helpful criticism on earlier drafts of this paper.

REFERENCES

Baumeister, L. 1908. Beitrage zur Anatomie und Physiologie der Rhinophiden.

Zoologische Jahrbiicher, Abteilung fiir Anatomie und Ontogenie der Tiere, 26: 423-

526.

Bellairs, A.d’A. & Kamal, A. 1981. The chondrocranium and the development of the

skull in Recent reptiles. pp 2-263. In: Gans, C. & Parsons, T.S. (eds). Biology of the

Reptilia. Vol. 2. Academic Press, London.

Bremer, K. 1988. The limits of amino acid sequence data in angiosperm phylogenetic

reconstruction. Evolution 42: 795-803.

Cadle, J.E., Dessauer, H.C., Gans, C. & Gartside, D.F. 1990. Phylogenetic relation-

ships and molecular evolution in uropeltid snakes (Serpentes: Uropeltidae): allozymes

and albumin immunology. Biological Journal of the Linnean Society 40; 293-320.

Cundall, D. & Greene, H.W. 2000. Feeding in snakes. pp. 293-333. In Schwenk, K.

(ed). Feeding: Form, Function, and Evolution in Tetrapod Vertebrates. Academic

Press, San Diego.

& Rossman, D.A. 1993. Cephalic anatomy of the rare Indonesian snake

Anomochilus weberi. Zoological Journal of the Linnean Society 109: 235-273.

Wallach, V. & Rossman, D.A. 1993. The systematic relationships of the snake

genus Anomochilus. Zoological Journal of the Linnean Society 109: 275-299.

130

Frazzetta, T.H. 1966. Studies on the morphology and function of the skull in the

Boidae (Serpentes). Part 2. Morphology and function of the jaw apparatus in Python

sebae and Python molurus. Journal of Morphology 118: 217-296.

Haas, G. 1930. Uber die Kaumuskulatur und die Schidelmechanik einiger

Wiihlschlangen. Zoologische Jahrbiicher, Abteilung fiir Anatomie und Ontogenie

der Tiere 52: |-94.

Hoffstetter, R. & Gasc, J.-P. 1969. Vertebrae and ribs of Modern reptiles. pp. 201-310.

In: Gans, C., Parsons, T.S. & Bellairs, A.d°A. (eds). Biology of the Reptilia Vol. 1.

Academic Press, London.

Kluge, A.G. 1991. Boine snake phylogeny and research cycles. Miscellaneous Publi-

cations Museum of Zoology, University of Michigan, 178: 1-58.

McDowell, S.B. 1967. Osteology of the Typhlopidae and Leptotyphlopidae: a critical

review. Copeia 1967: 686-692.

1987. Systematics. pp 3—SO. In: Seigel, R.A., Collins, J.T. & Novak, S.S. (eds).

Snakes. Ecology and Evolutionary Biology. Macmillan Publ., New York.

Nopesa, F.v. 1923. Die Familien der Reptilien. Fortschritte der Geologie und

Paldontologie 2: 1-210.

Rieppel, O. 1977. Studies on the skull of the Henophidia (Reptilia, Serpentes). Journal

of Zoology, London 181: 145-173.

1978. The evolution of the naso-frontal joint in snakes and its bearing on snake

origins. Zeitschrift fiir zoologische Systematik und Evolutionsforschung 16: 14-27.

1979a. The evolution of the basicranium in the Henophidia (Reptilia, Serpentes).

Zoological Journal of the Linnean Society 66: 411-431.

1979b. The braincase of Typhlops and Leptotyphlops (Reptilia, Serpentes).

Zoological Journal of the Linnean Society, 65: 161-176.

1980. The sound transmitting apparatus of primitive snakes and its phylogenetic

significance. Zoomorphology 96: 45-62.

1983. A comparison of the skull of Lanthanotus borneensis (Reptilia: Varanoidea)

with the skull of primitive snakes. Zeitschrift fiir zoologische Systematik und

Evolutionsforschung 21; 142-153.

—— 1988. A review of the origin of snakes. Evolutionary Biology 22: 37-130.

& Zaher, H. 2000. The intramandibular joint in squamates, and the phylogenetic

relationships of the fossil snake Pachyrhachis problematicus Haas. Fieldiana (Geol-

ogy), n.s. 43: 1-69.

Scanlon, J.D. & Lee, M.S.Y. 2000. The Pleistocene serpent Wonambi and the early

evolution of snakes. Nature 403: 416-420.

Swofford, D.L. 1990. PAUP — Phylogenetic Analysis Using Parsimony, Version 3.0.

Illinois Natural History Survey, Champaign.

— & Begle, D.P. 1993. PAUP — Phylogenetic Analysis Using Parsimony, Version

3.1. Laboratory of Molecular Systematics, Smithsonian Institution, Washington DC.

Tchernov, E., Rieppel, O., Zaher, H., Poleyn, M.J. & Jacobs, L.J. 2000. A new fossil

snake with limbs. Science 287: 2010-2012.

Underwood, G. 1967. A Contribution to the Classification of Snakes. British Museum

(Natural History) Publication No. 653 Trustees of the British Museum (Natural

History), London. 179pp.

Wever, E.G. 1978. The Reptile Ear. Princeton University Press, Princeton. 1024pp.

Williams, E.E. 1959. The occipito-vertebral joint in the burrowing snakes of the family

Uropeltidae. Breviora 106: 1-10.

Appendix I List of Characters used in the

phylogenetic analysis

1. Anterior tip of maxilla turned medially, closely approaching or

touching transverse process of premaxilla (0); anterior tip of

maxilla straight, contact with premaxilla shizarthrotic (1).

2. Nasals relatively broad anteriorly, notched (0); nasals gradually

tapering to pointed tip anteriorly (1).

Teeth on palatine present (0), absent (1).

4. A distinct and well defined buttressing contact between the

processus medialis anterior of the maxilla and an anterior lateral

process of the vomer is absent (0), or present (1).

Parietal enters optic foramen (0), optic foramen fully enclosed

entirely within frontal (1).

6. Crista trabecularis ends behind the (lateral) fronto-parietal su-

ture (0), at the (lateral) fronto-parietal suture (1), in front of the

(lateral) fronto-parietal suture (2).

7. Supraorbital process of parietal does not (0), or does (1) participate

in suspension of prefrontal (contacts prefrontal above the orbit).

O. RIEPPEL AND H. ZAHER

8. Supraoccipital separate (0), or fused (1).

9. Prootic and opisthotic-exoccipital separate (0), or fused (1).

10. Basisphenoid — basioccipital separate (0), or fused (1).

11. Laterosphenoid narrow (0), broad (1).

12. Facial nerve branches open into a recess behind the mandibular

branch foramen which connects with the posterior opening of

the Vidian canal (0); facial nerve branches open into a prootic

canal which opens within the recession of the mandibular branch

foramen and connects with the posterior opening of the Vidian

canal (1); facial nerve branches open into a prootic canal which

opens behind the mandibular branch foramen and connects with

the posterior opening of the Vidian canal (2).

13. Juxtastapedial recess wide open laterally (0; fenestra pseudo-

rotunda may be exposed in lateral view), distinctly restricted by

approximation of dorsal and ventral margin (1; fenestra

pseudorotunda never exposed in lateral view).

Jugular foramen behind juxtastapedial recess (0), recessed within

juxtastapedial recess (1).

15. Jugular foramen internally subdivided (0), single (1).

16. More than one hypoglossal foramina (0), single but enlarged

hypoglossal foramen (1).

Stalk of occipital condyle short, depression in basioccipital for

brainstem not visible in dorsal view (0), stalk of occipital

condyle elongate, depression in basioccipital for brainstem

visible in dorsal view (1).

Posteroventral process of dentary distinct (0), reduced (1),

absent (2).

19. Exoccipitals not in contact dorsal to basioccipital in occipital

condyle (0); exoccipitals in contact dorsal to basioccipital in

occipital condyle (1); exoccipitals and basioccipital fused in

occipital condyle (2).

20. Anterior dentigerous process of palatine slender and straight (0),

broadened anteriorly (1), modified into expanded lamina (2).

21. Pterygoid teeth present (0), absent (1) (Tchernov et al. 2000).

22. Suprastapedial process of stapes is not (0), or is (1) distinctly

longer than shaft of stapes (Tchernov et al. 2000).

Quadrate suspension close to dorsal margin of otic capsule (0),

shifted anteroventrally on otic capsule (1) (Tchernov er al.

2000).

Retroarticular process unmodified (0), wrapping around poste-

rior aspect of mandibular condyle of quadrate (1) (Cundall et al.

1993).

25. Premaxillary teeth present (0), absent (1).

26. Contact between premaxilla and vomer overlapping (0), or in

well defined recess (1).

Preorbital ridge on frontal (Frazzetta 1966) does not (0), does (1)

project beyond anterior margin of dorsally exposed surface of

frontal.

28. Interchoanal process of parasphenoid absent (0), present (1).

29. Posteroventral part of crista circumfenestralis does not (0), or

does (1) form a distinctly enlarged gliding surface for the

quadrate ramus of the pterygoid, or this gliding surface is

present but “rounded off” (2).

30. Occipital condyle is not (0), or is (1) modified as described by

Williams (1959) and Hoffstetter & Gasc (1969).

31. The superior alveolar nerve canal in the maxilla is closed (0), or

open (1) dorsally.

32. Frontals are not (0), are (1) at least twice as long as broad.

33. Supratemporal present (0), absent (1).

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 131-142

Issued 28 November 2002

The Cretaceous marine squamate Mesoleptos

and the origin of snakes

MICHAEL S. Y. LEE AND JOHN D. SCANLON

Department of Palaeontology, The South Australian Museum, North Terrace, Adelaide SA 5000, Australia. e-

mail Lee.Mike @ saugov.sa.gov.au

Department of Environmental Biology, The University of Adelaide, Adelaide SA 5005, Australia

SyNopsiIs. The poorly known marine squamate Mesoleptos is reassessed based on two previously known specimens and a

newly referred specimen. The three specimens of Mesoleptos zendrinii share unique characters such as long, posteriorly tapering

centra and distally straight but non-pachyostotic ribs. Mesoleptos had a narrow neck (and presumably small head), long laterally

compressed body, and small fore- and hindlimbs. Phylogenetic analysis suggests that Mesoleptos is the nearest relative of snakes;

this phylogenetic position is consistent with its morphology being intermediate between typical marine squamates (e.g.

mosasauroids) and primitive marine snakes (pachyophiids). However, this interpretation remains tentative because Mesoleptos

is very poorly known, and many of the characters uniting it with mosasauroids and primitive snakes are correlates of marine habits

and/or limb reduction.

INTRODUCTION

Whereas sea snakes (Laticaudinae and Hydrophiinae) and marine

iguanas (Amblyrhynchus) are the only truly marine squamates living

today, there was a more diverse and very different radiation of such

forms during the Cretaceous. These extinct marine squamates

included the large monitor-like aigialosaurs and mosasaurs, the

small, long-necked dolichosaurs, and the medium-sized limbed

snakes Pachyrhachis, Pachyophis, and Haasiophis. These forms

were suggested by workers in the late nineteenth and early twentieth

centuries to be closely related to each other and to modern snakes

(e.g. Cope, 1869; Boulenger, 1891; Gorjanovic-Kramberger, 1892;

Nopesa, 1908, 1923), a view which has been supported by some

recent phylogenetic analyses (e.g. Scanlon, 1996; Caldwell 1999;

Lee and Scanlon 2002; but see Tchernov ef al. 2000; Rieppel and

Zaher 2000).

One poorly known form that has been associated with this radia-

tion is Mesoleptos zendrinii (Cornalia and Chiozza, 1852;

Gorjanovic-Kramberger, 1892; Calligaris, 1988). M. zendrinii was a

marine squamate with a rather elongated body, long ribs, and well-

developed but rather small hindlimbs. It has been repeatedly

associated with other contemporary marine squamates, largely on

the basis of common habitat rather than any detailed analysis of

morphology. Cornalia and Chiozza (1852) suggested affinities with

“Raphiosaurus’, based on a specimen (BMNH R32268) figured

under this name by Owen (1842) but later referred to Dolichosaurus

(Owen 1850a, 1851). Subsequent workers have commented on

errors in the original description, though a full redescription of the

type specimen has not appeared. Gorjanovic-Kramberger (1892)

referred an additional specimen to Mesoleptos cf. zendrinii, dis-

cussed below, and referred this genus to the Varanidae, although

acknowledging that it differed from other varanids in being highly

aquatic. Nopcsa (1903) referred it tentatively to Aigialosauridae,

and suggested that the moderate elongation of the trunk region

relative to other known aigialosaurs was analogous to the independ-

ent elongation of the body in some mosasaurs such as Clidastes.

Later, Nopesa (1923) compared M. zendrinii with Eidolosaurus

trauthi, including both in a subfamily Mesoleptinae within his

broadly conceived Dolichosauridae (Mesoleptinae, Aigialosaurinae,

Dolichosaurinae). He regarded the Mesoleptinae as intermediate

between two main lineages, one consisting of the Aigialosaurinae

plus their probable descendants the Mosasauridae, and the other

consisting of the Dolichosaurinae plus their probable nearest rela-

tives — though not direct descendants — the snakes. Nopcsa’s (1903,

1923) classifications still represent the most complete discussion of

these forms to date, and are summarised by Calligaris (1988).

However, no unambiguous derived characters have been proposed

linking Mesoleptos with any of the other marine groups or with

snakes, and these interpretations need to be critically examined.

Here, we identify a new specimen of Mesoleptos, compare it to

previously known specimens, and use the combined material to infer

the phylogenetic relationships and palaeoecology of Mesoleptos.

Mesoleptos emerges as on the stem lineage leading to snakes, lying

phylogenetically between marine lizards (mosasauroids,

dolichosaurs, Adriosaurus) and primitive limbed snakes

(Pachyrhachis, Pachyophis, Haasiophis). Garth Underwood’s ear-

liest research interests included the origin and evolution of snakes,

and he has contributed to possibly the two most influential papers on

this topic (Bellairs and Underwood 1951; Underwood 1967). The

current paper is thus a small contribution to a field of inquiry that

Garth Underwood helped establish.

Institutional abbreviations

HUJ PAL, Hebrew University of Jerusalem Palaeontological Col-

lection; MCSNT, Museo Civico di Storia Naturale di Trieste; MNHN,

Musée Nationale d’ Histoire Naturelle, Paris; SAM, South Austral-

ian Museum.

DESCRIPTION OF NEW SPECIMEN

Material and horizon

The specimen consists of part and counterpart, but all morphological

information is preserved on the part (Fig. 1A). Anterior vertebral

column, ribs, shoulder girdle, and partial forelimbs. Locality: “Ein

Jabrud (Ain Yabrud), 7 km north-east of Ramallah (West Bank,

Palestine) and 20 km north of Jerusalem. Stratigraphic horizon: Bet-

Meir Formation (Lower Cenomanian; earliest Upper Cretaceous).

Catalogued as HUJ-PAL EJ699.

132

M.S.Y. LEE AND J.D. SCANLON

Vertebrae

An articulated series of thirteen vertebrae (here referred to as

vertebrae 1-13) is preserved, along with an isolated element on the

lower left (vertebra 14). All vertebrae are exposed ventrally only;

the surfaces of vertebrae 1—7 are weathered, while that of vertebra 11

is broken. The series 1-13 represents the anterior presacral part of

the column. Vertebra 1, the anteriormost, is the smallest; size then

increases gradually along the series such that the last is approxi-

mately twice the dimension of the first. The cervical-dorsal boundary

cannot be precisely determined because the cartilaginous sternal

contacts are not preserved. However, in typical lizards (anonymous

referee, pers. comm.), the cervical-dorsal boundary lies slightly

behind an abrupt increase in rib length. There is an abrupt change in

the size and shape of the ribs between preserved vertebrae 5 and 6

(see below), suggesting the cervical-dorsal boundary was slightly

behind this region, perhaps between vertebrae 7 and 8. Both shoulder

girdles, however, are preserved around the level of vertebra 5,

suggesting a slightly more anterior cervical-dorsal boundary.

The centra are all elongate, the length being approximately three

times the width across the middle of each vertebra. They narrow

sharply behind the transverse processes, and then more gradually

posteriorly. All centra are procoelous; the anterior cotyle is deeply

concave and the posterior condyle strongly convex. The articular

surfaces of the condyles face posteriorly; part of the surface is

sometimes exposed in ventral view, so they were at most only

slightly inclined dorsally.

Subcentral foramina are visible on the ventral surface of most

vertebrae: two are present on vertebrae 6 to 9, and one is present on

vertebrae 10 and 12. They were presumably present on the other

vertebrae but are not visible due to weathering and/or damage.

Where two foramina are present on a single vertebrae, they are never

bilaterally symmetrical and are often both on the same side of the

midline.

A sagittal keel, extending along the posterior half of the centrum,

is present on vertebrae | to 7. The keel terminates posteriorly in a

prominent knob-shaped hypapophysis, which is, however, partly

weathered away on all except vertebrae 6 and 7. The keels and

(where preserved) the hypapophyses are more prominent on the

anteriormost vertebrae and gradually decrease in size posteriorly.

On vertebra 8, there is no keel. A weak hypapophysis may have been

present, but this cannot be confirmed due to breakage. Both the keel

and hypapophysis are absent from vertebrae 9 to 13, and the ventral

surface is completely smooth.

A pair of transverse processes extend laterally from the anterior

end of each centrum. These processes extend proportionally further

laterally in the more posterior vertebrae: the diameter across the

transverse processes is slightly less than the length of the centrum in

the anteriormost vertebra, but slightly more in the posteriormost

vertebra (Table 1). Most of the tranverse processes on the anterior

vertebrae are weathered ventrally, but at least one is complete on

most of the posterior vertebrae. The articular surfaces of the proc-

esses are not fully exposed, but appear to have been single based on

the morphology of the proximal ends of the ribs.

The isolated vertebra ‘14’ does not fit onto either end of the

Fig. 1 (A) Photograph of the third known individual of Mesoleptos (HUJ-

PAL 699). (B) Specimen drawing. The anterior end of the specimen is to

the top right. Unstippled areas represent areas repesent broken bone.

Scale bar = 2cm. Abbreviations: cor, coracoid; sea, scapula; cla,

clavicle; hum, humerus; ep, epiphyseal ossification; v1 first

(anteriormost) preserved vertebra; p.vert, isolated posterior vertebra; r5,

rib of fifth preserved vertebra; hyp, hypapophysis.

MESOLEPTOS AND THE ORIGIN OF SNAKES

Table 1. Measurements of HUJ-PAL EJ699: midline length between rims

of cotyle and condyle; width across transverse processes; straight-line

length of rib. The vertebrae are numbered from the first preserved

centrum.

Vertebra no. Centrum length Greatest width Rib length

1 22 16 ~

2 20.5 19 -

3 22 20 -

4 - - 19.5

5 19 20 20

6 20 20.5 4]

Vl 21 20 49

8 (16+) 23 49

9 22 23 59

10 2a 24 73

11 (23+) (24+) 89

12 25 31 (92+)

13 26 39 121

= = - 132

- ~ 139

14 23 34.5 -

articulated series. It is too large to fit next to vertebra 1, and

furthermore could not be a cervical as it lacks the mid-ventral keel

and hypapophysis. However, it is too small to fit next to vertebra 13.

As in most squamates, after reaching maximum size (at or past

vertebra 13), the centra must have again gradually decreased in size

towards the posterior end of the dorsal region. The isolated vertebra

appears to belong to this region. Its surface is worn in a manner that

suggests there were laterally paired ventral mounds or processes

defining a median longitudinal trough on the posterior part of the

centrum.

Ribs

Ribs are preserved in association with vertebrae 4 to 13. Only the left

rib (right in ventral view) of vertebra 4 is preserved. Both ribs are

preserved in association with vertebrae 5 to 8. Only the left ribs are

associated with vertebrae 9 to 11. Both ribs are associated with

vertebrae 12 and 13, but the right ribs are displaced so that they

overlie the left ribs and point anteriorly. Three additional ribs

belonging to the next three (missing) dorsal vertebrae are also

preserved; these are presumably right ribs based on their similar

orientation to the right ribs of the last two preserved vertebrae.

The anteriormost preserved rib is associated with the 4th vertebra.

It is short (only as long as the centrum) and smoothly curved. The

shaft is oval in cross-section and uniformly thick throughout its

length. Slightly longer ribs, of similar shape, are associated with the

Sth vertebra. The next pair of ribs, associated with the 6th vertebra,

are much longer and quite different in shape. The distal end of the

left rib (right in ventral view) is weathered away; the right rib is

complete and its proximal half is smoothly curved, but the distal half

is nearly straight. The more posterior ribs are similar in shape,

except that the curved proximal portion occupies progressively less

and less of the shaft. By vertebra 13, the curved portion only

occupies the proximal one-fifth of the shaft.

The articular surfaces are visible on the left ribs associated with

vertebrae 7, 8, 10 and 13, and on the second of the three isolated ribs.

The ribs are all single-headed. The anterior ribs are flared at the

proximal end and then nearly uniformly thick thoughout their

length, while more posterior ones have a distinct neck proximally

before becoming thickened in the region of greatest curvature, then

gradually tapering distally in the straight part of the shaft. The distal

ends are truncated squarely where they joined the costal cartilages,

133

which are not preserved.

Approximate measurements of the vertebrae and ribs (Table 1)

show a more or less steady increase in dimensions from vertebra | to

13, continued in the ribs belonging to the next two missing vertebrae

(both ends of the last known rib are incomplete or obscured and its

length is therefore not measurable). As noted above, the posteriormost

preserved ribs cannot belong to vertebra 14, which is from the

posterior trunk (abdominal) region.

Shoulder girdle and forelimb

Both scapulocoracoids are preserved in medial view. The right is

complete except for the dorsal scapular blade, while the left is partly

covered by a rib and is missing the distal (anterior) end of the

procoracoid process. A curved strip of bone adjacent to the left

scapulocoracoid is probably the left clavicle. The left humerus is

preserved in proximal dorsal view. All appendicular elements are

very small in proportion to the axial elements.

The scapula is a simple, rectangular plate; the scapular blade is

short. Its anterior margin is weakly concave; a scapulocoracoid

emargination was thus present. The coracoid is single and bears two

processes, and two emarginations. The more dorsal process is much

longer and extends anterodorsally, forming the ventral margin of the

scapulocoracoid foramen and the dorsal margin of the coracoid

emargination that represents the anterior coracoid foramen. The

ventral process is shorter and expanded distally. It forms the ventral

border of the anterior coracoid foramen and the dorsal border of the

emargination representing the posterior coracoid foramen. The ven-

tral margin of the coracoid is smoothly convex, and the posterior

margin is drawn out into a posteroventral spur. The probable clavicle

is a tiny curved rod, tapered at each end. There is no ventromedial

expansion or foramen. The humerus is relatively large compared to

the shoulder elements, though still small compared to the axial

elements. The proximal end is expanded and flattened. The entire

articular surface is occupied by a large, semilunar epiphysis which

caps the humerus. The distal end of the humerus is weathered.

COMPARISONS WITH SIMILAR TAXA

The specimen is clearly a squamate, as it possesses all the

synapomorphies of squamates (Estes et al., 1988) for which it can be

coded: single-headed ribs, cervical vertebrae with hypapophyses,

procoelous vertebrae, presence of anterior coracoid emargination.

Admittedly, these are relatively few because the specimen is very

incomplete, but still sufficient to make a firm identification. Among

squamates, it is clearly different from most groups in possessing

distally straight ribs. The only taxa that possess such ribs are

Mesoleptos, Adriosaurus, Acteosaurus, and various groups of aquatic

snakes. The specimen here is compared to these forms, and to some

other superficially similar taxa to which it might be related.

Mesoleptos zendrinii

HUJ-PAL EJ699 is extremely similar to Mesoleptos, which is

known from two specimens. The type of Mesoloptos zendrinii, from

the Upper Cretaceous of Comen, Slovenia, is an articulated series of

dorsal, sacral and anterior caudal vertebrae with ribs and a partial

hindlimb. The specimen has been illustrated as a lithographic plate

(Cornalia and Chiozza, 1852: pl. 3) and an interpretive line drawing

(Calligaris, 1988: fig. 2). Cornalia (in Cornalia and Chiozza, 1852)

considered the specimen to be exposed in dorsal view, while

Gorjanovic-Kramberger (1892) maintained it was exposed ventrally,

134

Table 2. Measurements of Mesoleptos zendrinii holotype (based on

Cornalia and Chiozza, 1852: pl. 3), for comparison with data in Table 1.

The vertebrae are numbered from the first preserved rib.

Vertebra no. Centrum length Greatest width Rib length

1 - - 45

D) = = we

2 - - Ws

4 12 - 90

>) 13 — 116

6 12 - 120

7 12 18 125

8 12 20 119+

9 20* 23 124+

10 15 24 120+

11 IS) 25 120+

12 15 22 114

* there may be inaccuracies with the outlines of some vertebrae in the original

figure, or this anomalous high value could reflect longitudinal separation of two

adjacent vertebrae during partial disarticulation of the skeleton before fossilisation.

but in any case most of the vertebrae are bisected by the broken

surface of the slab and are thus seen as cross-sections at various

levels. The intervertebral articulations are not clearly exposed, and

Cornalia found no indication that the vertebrae were procoelous,

though Gorjanovic-Kramberger (1892) and later authors assumed

that they must have been similar to the specimen in the Novak

collection (discussed below). The type specimen could not be

located in recent times: Calligaris (1988) was unable to confirm it

was still in the Museo Civico di Storia Naturale de Milano (Milan).

The most anterior parts preserved of the type are strongly curved

ribs which probably contacted the sternum, and the first vertebral

fragments are associated with the fourth visible rib. Some small

elements and fragments visible between the anterior ribs may include

parts of the shoulder girdle and/or forelimb. Apart from the first few,

the ribs are weakly curved proximally and nearly straight for the

distal two-thirds of their length. The ribs are widest at the proximal

articulation and are otherwise slender, with no trace of thickening

(pachyostosis) more distally. Ribs in the posterior half of the trunk

are displaced to point anteriorly, corresponding to bloating and

maceration of the carcass proceeding most rapidly in the area of the

viscera, and the most posterior ribs are either lost or not exposed.

The outlines of the first 12 preserved vertebrae are nearly triangular,

indicating that they are split horizontally through the middle or

lower part of the centrum. From about the 13th preserved vertebra

the outlines of the trunk vertebrae are expanded posteriorly as well

as anteriorly and the neural canal is exposed, indicating a more

dorsal position of the break; after the 22nd there is not much visible

of the vertebral centra themselves. Prominent transverse processes

are visible on vertebrae 24—27, and transverse grooves on the 24th

and 26th vertebrae resemble lymph channels seen on the ventral

surface of the sacral and anterior caudal vertebrae in Varanus,

suggesting that the skeleton is exposed ventrally, and that the 24th

and 25th preserved vertebrae are the sacrals. After the first two

caudals (26-27), represented by broad transverse processes of one

side, there are indeterminate fragments of two more vertebrae, then

indications of four vertebrae in lateral view showing elongate, near-

vertical chevrons and a tall but antero-posteriorly narrow, slightly

back-sloping neural spine. Traces of longitudinal elements under the

transverse processes of the 25th—26th probably represent the ilium,

slightly displaced posteriorly, medially and (if the orientation is

correct) dorsally from its natural position. The femur is level with

the probable sacrals; the tibia and fibula are articulated, but incom-

plete distally.

M.S.Y. LEE AND J.D. SCANLON

The two referred specimens consist of HUJ-PAL EJ699 and

another specimen in the Museo Civico di Storia Naturale, Trieste

(MCSNT 9962: locality and other collection details undetermined).

The latter consists of a shorter but similar section of the skeleton to

that in the type, exposed dorsally (Calligaris, 1988). Comparisons of

the vertebrae are difficult due to the different parts and orientations

of the skeleton in the different specimens, but all three specimens

might share the derived character of unusually long, and posteriorly

tapering, trunk centra. The shape of the centrum in the type can be

inferred from the cross-sectional views of the vertebrae, which in

some parts of the trunk show a similar outline to the ventral views in

HUJ-PAL EJ699, being wide across the transverse processes and

narrowing steeply behind them to be almost parallel-sided posteriorly.

In MCSNT 9962, where only the upper part of the neural arch and

postzygapophyses are visible, the vertebrae are about 3/4 as long

(between successive neural arches) as wide (across

postzygapophyses), which is similar to proportions in the more

posterior part of HUJ-PAL EJ699.

All three specimens share a distinctive feature of the ribs in that

the distal portion, representing most of their length, is nearly straight.

This is interpreted as a derived condition corresponding to lateral

compression of the trunk region, as in the pachyophiids and some

other groups of thoroughly aquatic snakes. All three specimens also

exhibit, as far as can be seen, complete but small girdles and limbs.

The development of the forelimb and shoulder girdle in the current

specimen matches the development of the pelvis and hindlimb in the

type and MCSNT specimens of Mesoleptos. The shoulder girdle and

forelimb in HUJ-PAL EJ699 are relatively small, but complete in

that all major elements are present. All ossified shoulder girdle

elements except the interclavicle are preserved, while (based on the

size and ossification of the humerus) most of the distal forelimb

bones were present. This is consistent with the small but well

developed (though incompletely preserved) sacrum, pelvis and

hindlimb in the two previously known specimens of Mesoleptos.

The observation that the shoulder girdle and forelimb in HUJ-PAL

EJ699 are both reduced in size but complete, as is the pelvis and

hindlimb in Mesoleptos, further suggests they are the same or

closely related species.

Thus, HUJ-PAL EJ699 can be associated with the two known

specimens of Mesoleptos because (1) they exhibit no significant

differences from each other, though they all differ from all other

squamates, (2) they have derived similarities in the ribs (otherwise

found only in very different forms) and, less certainly, in the

vertebrae and limbs.

‘Mesoleptos’ cf. zendrinii

Gorjanovic-Kramberger (1892: pl. III, fig. 4) reported a specimen in

I. Novak’s collection showing several articulated vertebrae with

ribs, and fragments of some other elements, which he referred to

Mesoleptos, close to M. zendrinii. The collection consisted of

material from Cretaceous deposits of Isola di Lesina (Italian name

for Hvar Island), Croatia (Gorjanovic-Kramberger, 1892). This was

held after his death by his widow Antonia Novak (Kornhuber, 1901:

19) but the present location of this material is unknown (Calligaris,

1988). Gorjanovic-Kramberger interpreted the specimen as exposed

ventrally, but the shape of contacts between condyles and cotyles

visible in his figure suggest that the vertebra may actually be

exposed in dorsal view but sectioned horizontally at the base of the

neural canal; this would invalidate comparisons based on the sup-

posed ventral surface, though not the overall outline, of the centrum.

The shape of the centrum in the most complete vertebra is very

similar to vertebrae 9-13 of HUJ-PAL EJ699. The elongate and

MESOLEPTOS AND THE ORIGIN OF SNAKES

posteriorly narrow centra have been regarded as diagnostic of

Mesoleptos, and are not found in any other limbed squamates,

though a similarly shaped centrum is present in some primitive

snakes (e.g. Lapparentophis, Hoffstetter, 1960; Patagoniophis,

Scanlon, 1993; Coniophis, Gardner and Cifelli, 1999).

Girdle and limb elements are also present in the Novak specimen;

Gorjanovic-Kramberger (1892: 99) describes ‘indistinct impres-

sions’ of the humerus, radius, ulna and two metacarpals, altogether

measuring 93.3 mm in length. This must be less than the total length

of the forelimb, because the elements are incompletely represented

(the ends of the long bones are obscured and the humerus can not be

compared in detail with HUJ-PAL EJ699), but it can be concluded

that a forelimb was present and equivalent in length to between three

and four thoracic vertebrae, just as in the HUJ specimen. Plate-like

structures are also shown just anterior to the supposed humerus in

Gorjanovic-Kramberger’s figure, suggesting the posterior margins

of a scapula and coracoid like those of the HUJ specimen, although

no useful details can be compared.

On the other hand the ribs, although long, are curved throughout

their length. While the centrum length of the one well-preserved

vertebra is about 31.5 mm, the length of the most complete rib

(belonging to the preceding vertebra) is over 90 mm (Gorjanovic-

Kramberger, 1892). These proportions seem to indicate a position

deep within the dorsal region. In HUJ-PAL EJ699, curved ribs only

occur up to the anterior dorsal region while more posterior ribs are

straight. Thus the Novak specimen apparently lacks this apomorphy

shared by the type of Mesoleptos zendrinii with the MCSNT and

HUJ specimens (neither Gorjanovic-Kramberger nor subsequent

writers have commented on this difference). It should therefore not

be referred to Mesoleptos, but might possibly represent.a species

closely related to either Mesoleptos or the Mesoleptos-snake clade

(see below).

Adriosaurus, Acteosaurus

Adriosaurus suessi Seeley, 1881 (Lee and Caldwell, 2000) and

Acteosaurus tommasinii von Meyer, 1860 (considered identical by

Nopcsa, 1923) are small marine lizards with distally straight ribs and

thus, laterally compressed bodies. Adriosaurus is known from two

specimens, from Upper Cretaceous deposits of Comen, Slovenia

and Lesina (=Hvar), Croatia, while Acteosaurus is known from a

single specimen from Comen. However, they both differ from

Mesoleptos in lacking the distinctly small cervicals (relative to

dorsals), in possessing proportionally larger limbs, proportionally

shorter and wider dorsal vertebrae, and in exhibiting heavy

pachyostosis of both dorsal vertebrae and ribs. They are also much

smaller than Mesoleptos.

Eidolosaurus trauthii

Nopesa (1923) described Eidolosaurus trauthii from a near-com-

plete skeletal impression found during the demolition of a house in

the Istrian region, i.e. in the same general region as Comen, but

possibly within the present borders of either Slovenia, Croatia, or

Italy (more precise locality details were not provided). This speci-

men is currently housed in the Geologische Staatsanstalt, Vienna but

has yet to be completely prepared. Fragments of the skull are present

in articulation with the vertebral column, so that the total number of

presacral vertebrae can be determined as 34. Short, slender ribs were

present on at least three posterior cervicals, but on the basis of a

sharp increase in length and thickness between adjacent ribs (as

there is no trace of the sternum), Nopcsa counted 11 cervical and 23

dorsal vertebrae. Two sacral and 48 or more postsacral vertebrae

were also present. Nopcsa interpreted the type of Mesoleptos zendrinii

135

as also having 23 dorsal vertebrae. The numbers of cervical and

trunk vertebrae in Mesoleptos and Eidolosaurus are therefore com-

parable. The relative femur length is similar in both, corresponding

to the length of three middle dorsal vertebrae. However, there are

also considerable differences: in Eidolosaurus the centra of trunk

vertebrae are as wide as long, with no indication of a posterior taper;

there is a median groove between paired ridges on the ventral

surface throughout the trunk (the groove further divided by a median

ridge in posterior vertebrae); all trunk ribs are strongly and uni-

formly curved and greatly thickened; and both the vertebrae and ribs

are pachyostotic.

Nopcsa (1923: 107, footnote) also mentions ‘An undescribed

fossil discovered by Professor Jakel, which came to my attention

while this work was in press, shows 18 posteriorly tapering vertebral

centra, which bear long, slightly curved, proximally club-shaped

ribs. The specimen is 28 cm long. The vertebral centra show a

shallow but well developed median longitudinal groove. The ante-

rior centra are almost triangular and wider than long. The general

habitus is Mesoleptos-like, but the ribs are somewhat pachyostotic.

Probably this form is related to Eidolosaurus.’ This may have been

the specimen collected by Prof. O. Jakel at Lesina which Kornhuber

(1901: 3) mentioned and referred to Carsosaurus. It would be

particularly interesting to compare this specimen with HUJ-PAL

EJ699, which also resembles Mesoleptos but has somewhat thick-

ened ribs, but no illustration was provided and again the present

location of the specimen is unknown (Calligaris, 1988: 117).

Dolichosaurs: Dolichosaurus, Coniosaurus,

Pontosaurus

Dolichosaurus longicollis Owen, 1850a from the English Chalk

(Owen, 1842, 1851; Caldwell, 2000) and Pontosaurus lesinensis

(Kornhuber, 1873) from Hvar, Croatia, are elongate, Cenomanian

marine squamates known from two or more articulated partial

skeletons, and are thus important for comparison with Mesoleptos.

They both clearly differ from HUJ-PAL EJ699 and the other

Mesoleptos specimens in the shape of the ribs (distally curved rather

than straight), the more gradual changes in rib length and vertebral

dimensions along the trunk, and greater number of dorsal vertebrae,

all of which correspond to a more slender and cylindrical body form.

Individual mid-trunk vertebrae of Dolichosaurus differ from those

of Mesoleptos in being less massive, and having proportionally

larger condyles and cotyles. Otherwise, they are similar in possess-

ing broad transverse processes, a posteriorly cylindrical centrum,

well-developed zygosphenes, a long neural spine, and absence of

pachyostosis. Vertebral morphology of Pontosaurus can not yet be

adequately compared because the specimens remain incompletely

prepared (Calligaris, 1988). Coniosaurus crassidens Owen, 1850a

(Coniasaurus Caldwell and Cooper, 1999, invalid emendation or

sustained lapse) and Coniosaurus gracilodens Caldwell, 1999, oc-

cur in the same deposits as D. longicollis but comparisons are more

problematic. Only very incomplete postcranial remains of

Coniosaurus are known; the vertebrae are very similar to those of

Dolichosaurus, and the two species are diagnosed by features of the

jaws and teeth unknown in Dolichosaurus. Thus, one of the species

of Coniosaurus might be synonymous with Dolichosaurus (Caldwell,

2000).

Pachyvaranus crassispondylus

Pachyvaranus was described from the Maastrichtian of Morocco

(Arambourg and Signeux, 1952: 288-91, pl. 41) based on a small

number of isolated vertebrae (MNHN PMC 1-4) and two doubtfully

associated osteoderms (PMC 5-6), and originally referred to

136

Aigialosauridae. However, it has narrower condyles and cotyles,

relatively longer centra and more prominent transverse processes

than known aigialosaurs. This suggests it should be compared with

HUJ-PAL EJ699, which it resembles in size. The Pachyvaranus

specimens are from marine phosphate deposits, and differ from

HUJ-PAL EJ699 in the thick and compact ossification of the verte-

brae (pachyostosis). The vertebrae also differ in that the centrum of

Pachyvaranus is triangular, tapering rather than nearly parallel-

sided posteriorly, but this could be a result of pachyostosis; in other

pachyostotic reptiles the centra are further expanded posterolaterally,

and nearly rectangular. Further, the reported ‘zygosphene’ is only a

small triangular projection comparable to that of Varanus, which

does not bear facets for articulation with a zygantrum on the

preceding vertebra. Arambourg and Signeux considered possible

affinities with dolichosaurs (ruled out by the lack of true zygosphenal

articulations in Pachyvaranus) as well as aigialosaurs (noting differ-

ences including the narrower condyles). The lack of zygosphenes in

Pachyvaranus also rules out affinities with aigialosaurs, since recent

studies (Carroll and DeBraga, 1992) have demonstrated the pres-

ence of well-developed zygosphenes in aigialosaurs. However,

affinities with Mesoleptos were not considered. No material other

than trunk vertebrae (and doubtfully associated osteoderms) has

been described for Pachyvaranus, and conversely the vertebrae of

Mesoleptos are not fully known ‘in the round’, so that it is not yet

possible to make detailed comparisons.

Pachyophiidae

Three long-bodied, limb reduced Cretaceous marine squamates

have been referred to Pachyophiidae: Pachyophis woodwardi

Nopcsa, 1923 (Lee et al., 1999), Mesophis nopcsai Bolkay, 1925,

and Pachyrhachis problematicus Haas, 1979 (Haas, 1980; Lee and

Caldwell, 1998; Zaher and Rieppel, 1999). Haas (1979) originally

included Pachyrhachis in Simoliophiidae, as did McDowell (1987)

who also added Pachyophis; but of the two family-group names

proposed by Nopcsa (1923), Pachyophiidae has page priority. There

is now agreement that pachyophiids are snakes but their exact

position within snakes remains debated (Zaher and Rieppel, 1999;

Tchernovy et al. 2000; Lee and Scanlon, 2002). These three taxa are

extremely similar, and possess small heads, heavily pachyostotic

mid-body vertebrae and ribs, and distally straight ribs indicating

lateral compression of the trunk. Radovanovic (1935: 411) postu-

lated that Mesophis was a terrestrial snake in which the very slender

distal parts of the ribs had been straightened by pressure during

fossilization. However, this hypothesis is very unlikely because ribs

of similar shape occur consistently in otherwise undistorted speci-

mens of larger pachyophiids, namely Pachyophis and Pachyrhachis,

as well as in other marine taxa (see below).

The specimen described here is clearly not a pachyophiid because

in all known pachyophiids the forelimbs and shoulder girdle are

completely absent, and the mid-trunk ribs are heavily swollen

(pachyostotic). Also, the centra are long and taper posteriorly, unlike

the pachyophiid condition of short centra that are of constant width

throughout. The transverse processes also extend much further

laterally than they do in pachyophiids.

Haasiophis

A new limbed Cretaceous marine snake, Haasiophis, has been

described and interpreted to have affinities with Pachyrhachis

(Tchernovy et al., 2000) and by implication with pachyophiids as a

group. However, certain cranial elements were apparently

misidentified, and a reassessment of the morphology suggests that

these taxa are not closely related, but are successive outgroups to

M.S.Y. LEE AND J.D. SCANLON

crown-clade snakes (Lee and Scanlon 2002). The postcranial ele-

ments of Haasiophis have yet to be properly described, making

comparisions with Mesoleptos difficult. However, Haasiophis dif-

fers from HUJ-PAL EJ699 in possessing heavy pachyostosis of the

vertebrae, many more trunk vertebrae, and in completely lacking a

shoulder girdle and forelimb.

Palaeogene Marine Snakes

HUJ-PAL EJ699 can be confidently excluded from the following

groups of Tertiary snakes with distally straight ribs based on pres-

ence of forelimbs and very different vertebrae. Archaeophis

(Archaeophiinae) has long, proximally curved but distally straight

ribs (Janensch, 1906), and the ribs of Palaeophis share this morphol-

ogy (Owen, 1850b). However, the neural arch is narrow and high,

the centrum approximately cylindrical and the transverse processes

relatively small (Rage, 1984). In the complete skeleton of

Archaeophis proavus there are over 450 trunk vertebrae and no

traces of limbs or girdles (Janensch, 1906), and there is no indication

of their presence in other less completely known species.

Anomalophis (Anomalophiidae) has similar ribs (Janensch, 1906;

Auffenberg, 1959) and also small transverse processes. However,

the centra are long and gradually tapering, and the neural arches are

narrow and depressed, except for a backsloping neural spine. Verte-

brae of other early aquatic snakes (Nigerophiidae and

Russellophiidae; Rage, 1984, Averianov, 1997) have features re-

sembling the palaeophiids, acrochordids and colubroids to a varying

extent, but no ribs or articulated skeletons are known and their

relationships remain obscure.

Thus, the specimen HUJ-PAL EJ699 can be associated most

closely with Mesoleptos. However, it differs from the type of M.

zendrinii (as described by Cornalia and Chiozza, 1852; compare

Tables 1 and 2) in the ribs of the anterior thoracic region being

considerably shorter relative to vertebral length or width: the ribs are

also thick in the curved middle portion of the shaft rather than

uniformly slender. This region of the body is not preserved in the

other referred (MCSNT) specimen. If confirmed, these differences

would indicate a considerable variation in body shape (analogous to

the differences among known specimens of aigialosaurids) which

might justify erection of a new species. However, the location and

condition of the type and some other important specimens are

currently unknown, and the putative differences cannot be directly

confirmed. There remains a possibility that the description and

figure of the type are inaccurate, as they seem questionable in a

number of details, and that the two specimens are identical. Thus, we

have refrained from any formal taxonomic decisions pending a more

comprehensive search for the type, and simply refer the current

specimen to Mesoleptos sp. indet.

RECONSTRUCTION AND PALAEOECOLOGY

Based on all three specimens, Mesoleptos can be reconstructed as

follows (Figs. 1 and 2). Depending on where one draws the cervical-

dorsal boundary, there are five to seven cervical vertebrae preserved

in HUJ-PAL EJ699, and as these do not include the atlas or axis there

must have been at least seven to nine cervicals, and possibly several

more. Seven to nine cervicals are plesiomorphic for squamates and

occur in most terrestrial varanoids, aigialosaurs and some mosasaurs,

while dolichosaurs, Eidolosaurus and some mosasaurs have increased

from this number (Nopesa, 1908, 1923; Caldwell, 2000). There are

23 trunk vertebrae in the type and thus at least 30 to 32 presacrals

altogether (cf. 34 in Eidolosaurus), but not many more than this

MESOLEPTOS AND THE ORIGIN OF SNAKES

137

Fig. 2 Reconstruction of Mesoleptos in dorsal and lateral views. The head and tail are not known in any specimen and are thus conjectural. Note the

long neck, long laterally compressed body, and short webbed limbs. Scale bar = 10cm.

unless the neck was unusually long. Short, curved ribs are present on

most of the cervical vertebrae, implying a narrow cylindrical neck,

which is similar to conditions in Eidolosaurus and some dolichosaurs,

rather than aigialosaurs which have longer ribs on most of the

cervicals. The cervical-thoracic boundary presumably lies around,

or immediately posterior to, the sharp increase in rib length.

The anterior thoracic ribs are straight distally, implying a lateral

flattening of the trunk region. Allowing for apparent variation

between the three known specimens in the proportional length of the

ribs, the ribs remain long throughout the mid-trunk region, where the

largest vertebrae occur. Vertebral and rib dimensions increase stead-

ily up to at least the tenth thoracic vertebra, are highest in mid-trunk

and decrease, apparently more slowly, in the last ten or so presacrals.

These size gradients are stronger than seen in measured skeletons of

Varanus and Heloderma (Scanlon, unpublished data), and far more

conspicuous than in any other marine varanoids described. Unlike

some aigialosaurs and all mosasaurs, there is not a long series of

shortened posterior dorsal ribs. Rather, long, distally straight ribs

continue at least to within the last five presacral vertebrae (as

indicated by the MCSNT specimen; the most posterior ribs have

been damaged or lost in both this and the type).

The cervical vertebrae bear prominent ventral keels and hypa-

pophyses, which are reduced on the first two thoracics and then

disappear. The centra of the following thoracic vertebrae are smooth

ventrally, but posterior trunk vertebrae apparently have laterally

paired keels defining a median trough, a feature that also occurs in

dolichosaurs, Eidolosaurus and some aigialosaurs (but often com-

mencing more anteriorly in the trunk). The sacral vertebrae (in the

MCSNT specimen at least) are shorter than the immediately preced-

ing trunk vertebrae, and are fused (or at least very tightly articulated)

together. Parts of the first few caudal vertebrae are present in the

type, indicating a laterally compressed tail with elongate but antero-

posteriorly narrow neural spines and chevrons.

The trends in vertebral size (length and width) and rib length

indicate an animal with a relatively small head and narrow neck in

relation to its body, similar to dolichosaurs and Eidolosaurus. The

curved cervical ribs indicate that the cervical region of the animal

was approximately round in cross-section. However, the distally

straight dorsal ribs indicate that the trunk region of the animal was

laterally compressed and very deep. These long ribs projected only

a short distance laterally from the vertebrae before curving to extend

downward (and obliquely backward) for most of their length. The

girdles and limbs were rather small, although most elements were

probably present; compared to adjacent vertebrae, both the femur

and humerus are relatively shorter than in aigialosaurs, but the

forelimb was not as reduced as in dolichosaurs or Eidolosaurus (Fig.

In comparison with the similar-sized aigialosaurs, Pontosaurus

and species of Varanus, trends in vertebral size within the column of

Mesoleptos are somewhat different. There is a local minimum of

centrum length in the posterior cervical region, but the elongation of

the anterior cervicals is much less pronounced than the condition in

most Varanus spp. (a derived condition within that genus). Gradi-

ents of vertebral length and width within the thoracic and dorsal

region are stronger than in any of the other taxa. The centrum is

narrower posteriorly than in aigialosaurs, Pontosaurus and Varanus,

indicating a condyle-cotyle joint of smaller diameter and surface

area. This in turn suggests weaker compressive forces within the

column, along with a less energetic style of locomotion and/or a

greater capacity for lateral flexion of the neck and trunk. On the

other hand, the combination of long transverse processes and long

narrow centra increases both leverage and space for muscles con-

necting successive transverse processes, such as the m.

interarticularis (cf. Mosauer, 1935; Gasc, 1974). These could then

be of increased importance in lateral undulation, perhaps taking over

in this role from longer muscles inserting on the ribs whose effec-

tiveness would be decreased by lateral compression of the trunk. If

the above interpretation of the affinities of the Novak specimen is

correct, the derived vertebral morphology evolved before the lateral

compression, so that this ‘takeover’ could happen via an intermedi-

ate where both sets of muscles were effective. Zygosphenes,

considered to be of biomechanical importance in limiting twisting

between adjacent vertebrae (Gasc, 1974), are well-developed (ex-

posed dorsally inthe MCNST specimen) and articulate with zygantra

in the preceding neural arches as in other aquatic varanoids and all

snakes.

Among living squamates, the only forms with distally straight

ribs (and thus laterally compressed bodies) are highly aquatic

caenophidian snakes, such as file snakes (acrochordids) and sea

snakes (laticaudine and hydrophiine elapids). This feature has rarely

been discussed in extant snakes; Hoffstetter and Gayrard (1965) do

not comment on any unusual features of the ribs in Acrochordus or

Enhydrina (Hydrophiinae), though it was described in ‘Enhydris’

(=Lapemis) hardwickii (Hydrophiinae) by Janensch (1906: 22). In

Acrochordus arafurae (SAM R26956, R26966) the anterior ribs are

robust and strongly curved, while those of the posterior half of the

body are much more slender and only weakly curved except near the

base. The pachyophiids — primitive marine snakes — also had a

138

similar morphology, which is functionally correlated with

anguilliform swimming (Scanlon et al., 1999; Lee et al., 1999). It

can thus be concluded that Mesoleptos was marine. This is also

supported by the morphology of the posterior ribs. While they do not

exhibit the histological features of true pachyostosis, they are never-

theless robust (in the MCSNT and HUJ specimens) and might have

served to reduce bouyancy, much like the pachyostotic ribs in other

marine reptiles. The type of M. zendrinii, from the Comen locality,

also comes from deposits dominated by marine fish (Gorjanovic-

Kramberger, 1892) and is associated with aigialosaurs, dolichosaurs

and pachyophiids. This also presumably applies to the MCSNT

specimen (although its collection details have not been recorded it is

probably from either Comen or Lesina). Marine habits of the present

specimen are also implied by the position of the “Ein Jabrud locality

far from the palaeoshoreline (Scanlon et al., 1999), and the articu-

lated nature of the preserved elements suggesting in situ preservation.

The laterally compressed body and small limbs suggest that

Mesoleptos swam primarily by lateral undulation, holding its limbs

against its flanks (Carroll 1985; Lee 1999). In such forms, most of

the propulsion occurs by movements of the tail, and to some extent

the posterior region of the trunk. This is consistent with the observa-

tion that the posterior trunk region is most laterally compressed in

Mesoleptos (the tail is unknown). The forelimbs and hindlimbs,

however, were still large and well ossified enough to have been

functional. They may have been used for slow locomotion (‘walk-

ing’) along the seabed, where (with the help of buoyancy) they could

have supported the body. Alternatively, or additionally, they may

have been used for forays on the shore.

PHYLOGENETIC RELATIONSHIPS OF

MESOLEPTOS

All previous interpretations of the morphology and relationships of

Mesoleptos were based either on poorly preserved and inadequately

described material (the type), or on a composite of the type with the

referred Novak specimen (Gorjanovic-Kramberger, 1892) which is

clearly distinct from M. zendrinii in rib morphology. Gorjanovic-

Kramberger’s inclusion of Mesoleptos in Varanidae was

‘phenetically’ based on its long ribs, as distinct from the shorter and

more uniform ribs of Aigialosaurus (as then interpreted) and

dolichosaurs. However, he recognised it as marine in habits and thus

by no means a typical varanid. Nopesa classified Mesoleptos doubt-

fully as an aigialosaur (1903), but later placed it in a separate

subfamily (Mesoleptinae) with Eidolosaurus, close to both

aigialosaurines and dolichosaurines within Dolichosauridae (1923).

McDowell and Bogert (1954) returned Mesoleptos and

Eidolosaurus, again doubtfully, to Aigialosauridae, but also briefly

considered that they might be related to the living earless monitor,

Lanthanotus. Hoffstetter (1955) also retained Mesoleptos as a poss-

ible aigialosaurid, while recognising Eidolosaurus as a dolichosaur

and suggesting that Pachyvaranus might represent a distinct family.

Romer (1956) placed both Mesoleptos and Eidolosaurus, with

question marks, in Dolichosauridae.

The current state of understanding of these groups is perhaps best

indicated by the fact that the systematic conclusion to Calligaris’

(1988) review was formed by a summary of Nopcsa’s (1923)

classification, without substantial additions or revisions. That these

groups have been poorly studied recently is highlighted by Carroll

and DeBraga’s (1992) statement that only five species had been

assigned to Aigialosauridae, and did not mention either Mesoleptos

(assigned to Aigialosauridae by Nopcsa, 1903, Camp, 1923, and

M.S.Y. LEE AND J.D. SCANLON

McDowell and Bogert, 1954), Eidolosaurus (assigned by Nopcsa,

1923, and McDowell and Bogert, 1954) or Pachyvaranus (assigned

by Arambourg and Signeux, 1952).

The relationships of Mesoleptos, therefore, remain unresolved.

While a robust assessment will have to await more complete material,

a preliminary analysis is undertaken here. Morphological informa-

tion from the MCSNT and HUJ specimens (based on examination of

specimens) and the type (based on published descriptions) was used

in order to evaluate its phylogenetic relationships. Mesoleptos was

added to the data matrix used in the most recent comprehensive

analysis of squamates (Lee 2002); this matrix includes 248 osteo-

logical characters, used here, and addresses recent criticisms of

various characters (Rieppel and Zaher 2000). Recently described (or

redescribed) elongate marine squamates were also included in this

matrix: Pachyrhachis (Lee and Caldwell, 1998), Pachyophis (Lee et

al., 1999), Adriosaurus (Lee and Caldwell, 2000) and dolichosaurs

(Coniosaurus and Dolichosaurus; Caldwell and Cooper, 1999;

Caldwell, 1999, 2000). Coniosaurus and Dolichosaurus are here

combined into a single taxon, Dolichosauridae sensu stricto, based

on the observations that the comparable parts of the two taxa appear

almost identical, they overlap stratigraphically, and as noted by

Caldwell (2000) one of the Coniosaurus species might be synony-

mous with D. longicollis. Character codings for all taxa (except

Haasiophis) in this matrix, including the marine fossil forms, are

based on direct examination of the material. As descriptions of the

remaining marine squamates discussed above are dated, and they

have yet to be restudied, they have not been included in the analysis.

The full matrix is presented elsewhere (Lee 2002) and only the

(new) character codings for Mesoleptos are listed here (Appendix

1). The full matrix (including Mesoleptos) used in this analysis has

been deposited in TreeBase (http://www.treebase.org/treebase/).

The enlarged data matrix with Mesoleptos was analysed using the

heuristic algorithm of PAUP* (Swofford, 1999) employing 100

random addition sequences. Two analyses were performed, with

multistate characters ordered according to morphoclines where

possible, or with all multistate characters unordered, to see if the

phylogenetic analyses were contingent on assumptions of character

state transitions. The degree of support for each grouping was

ascertained by the support index (Bremer, 1988), calculated in

PAUP using batch commands generated by TreeRot Version 2b

(Sorenson, 2000). These commands were modified so that each

heuristic search employed 100 rather than 20 random addition

sequences. Nonparametric bootstrapping (1000 heuristic replicates

each employing 100 random addition sequences) was also used to

assess the robustness of each clade. As there were no fully specified

a priori hypotheses for Mesoleptos and all other squamates,

Templeton tests are inappropriate and were not performed (Goldman

et al., 2000).

Phylogenetic affinities

In the ordered analysis, three most parsimonious trees were found,

each of length 672, consistency index = 0.46, retention index =0.71.

The strict consensus is shown in Fig. 3A, along with nodal supports.

In the unordered analysis, 4 most parsimonious trees were found

when only branches with unequivocal character support were re-

tained, each of length 639, consistency index = 0.48, retention index

= 0.71. The strict consensus is shown in Fig. 3B, along with nodal

supports.

The basic topologies of the ordered and unordered consensus

trees are similar to each other and largely unchanged from that the

previous study (Lee, 2002), so that diagnoses of all the clades within

Squamata are not repeated here. The characters diagnosing additional

MESOLEPTOS AND THE ORIGIN OF SNAKES 139

@ @ Red @ NS

Oe OL x PF FOS Ng

4) SS Re) \aPC “OP @ D S Ry CRS 7 9 S rs AAT

Le Oe x SF oo LW ae RS 2 SP .O » > OW .0? 2 Wh?

EEK SPM F KEES So & Px os SPY Or o A a soos FN”

SAS s N>’ AC OP 0 Ros CF BSP? 0” es A OA ee

DO PP SF Ph LE WO. PPO ES SO Wis & 4? Oo a? _«

SP FMF HTP SF PIF SH OHHH PO gregh BH po 092" go were

Hi ee Teele Clade D: 2,82

, 12,100 4,97 Mosasauroidea .

Acrodonta 1,49 a

6.88 6,100 Ophidia: 5,98

? 1,46 Varanidae

Gekkota 6.93 Clade C: 1,66

1,56 : ‘

1,33 Xenosauridae Clade B: 1,50

4,94 :

Lacertoidea Clade A: 3,70

Iguania: 2,69 2,74 Pythonomorpha: 7,99

Thecoglossa: 9,92

2,43 Varanoidea: 7,95

2,61

Anguimorpha: 4,75

1,35

Scleroglossa: 6,93 A.

se CAS

a) a) \ eS >

Rod See @ oY @ OM RS o 8 eg 2

@ s Ro SM 5? Ow e S S OF I 0? OL? 0

PELE SF SOE SNS eg go & CLL Oe KS eo 3 “oN a 8 ¢ sts "3° OFS

DQ PO FP LX BE OS PF OE LY Says « * y SS

SPF FHF HEE FFP LPP AF GPP OH SOW sss OP ph poh geo" 9 wes

Agamidae V

1,81 Acrodonta 10,100 1,49 a

3,81 7 AI ne

ae cea Melis paeniee Seige

1,36 i : Xenosauridae = Clade B: 1,46

5,97

Clade A: 5,79

Pythonomorpha: 7,99

Iguania 1,36 Thecoglossa: 7,85

1,63 Varanoidea: 7,91

1,51

Anguimorpha: 1,57

1,61

Scleroglossa: 8,93

Fig. 3. The phylogenetic affinities of Mesoleptos, based on cladistic analyses of 248 characters across squamates. (A) Analysis with multistate characters

ordered, strict consensus of 3 trees, length 672, consistency index 0.46, retention index 0.71. (B) Analysis with multistate characters unordered, strict

consensus of 3 trees, length 639, consistency index 0.48, retention index 0.71. First number next to each clade refers to branch support (Bremer, 1988);

second number refers to bootstrapping frequency. Clades immediately relevant to the affinities of Mesoleptos are in bold and are discussed in the text.

The other more inclusive clades are discussed in Lee (1998). Aquatic terminal taxa are indicated in bold.

140

clades of immediate relevance to Mesoleptos are listed below. The

character changes diagnosing these clades in the ‘ordered’ analysis

under delayed transformation optimisation are listed in Appendix 2;

the changes in the ‘unordered’ analysis are very similar, except that

some clades collapse (compare Figs 3A and B). Unequivocal changes,

i.e. those which occur under both delayed and accelerated

optimisation, are indicated with an asterisk (*). Note that most

characters diagnosing snakes (Ophidia) are equivocal because

Mesoleptos, the sister group of snakes, is poorly known and nearly

all the characters could apply to a more inclusive clade that also

contains Mesoleptos (clade C). As discussed below, the clades are

not strongly corroborated due to missing data and possible correla-

tion of the supporting characters, and are thus not yet named

formally.

EVOLUTIONARY IMPLICATIONS

The phylogenetic results imply that snakes arose from within a

plexus of marine varanoids, an idea suggested initially by Nopcsa

(1908, 1923) and later by Haas (1980). The aquatic hypothesis is

often ascribed to Cope (1869), but Cope never suggested that the

aquatic mosasaurs were ancestral to snakes: rather, he suggested that

both had a close common ancestor, which might even have been

terrestrial. However, critics subsequently misquoted Cope as sug-

gesting that snakes evolved directly from mosasaurs and thus had

marine ancestors, and then proceeded to argue that as snakes could

not have evolved from mosasaurs (which possess numerous

specialisations), they could not have had marine ancestors (e.g.

Owen, 1877; Dollo, 1903, 1904; Janensch, 1906; McDowell and

Bogert, 1954; Zaher and Rieppel, 1999). Nopcsa (1908, 1923)

recognised and addressed the erroneous arguments of Owen and

Janensch, and put forward a rigorous case for a marine stage in snake

ancestry. More recently, by interpreting aigialosaurs as probable

ancestors of snakes, McDowell and Bogert (1954) implicitly pro-

posed a marine ancestry. In describing the second specimen of

Pachyrhachis (=Ophiomorphus), Haas (1980: 191) stated that the

fossil ‘points to the fact that the snakelike body and loss of limbs did

develop in a marine surrounding’. Despite this, the aquatic theory

has in recent times been largely rejected in favour of the “fossorial

theory’, 1.e. that snakes evolved from small elongate burrowing

lizards (e.g. Janensch, 1906; Walls, 1940; Bellairs and Underwood,

1951; Underwood, 1967; Rieppel, 1988; Greene, 1997). Thus, few

modern studies rigorously surveyed marine varanoids and marine

ophiomorphs for possible relationships with modern snakes.

This analysis indicates that the closest four to eight outgroups to

modern (terrestrial) snakes are marine: the exact number varies

depending on how the polytomies are resolved. The most parsimo-

nious interpretation is that marine or at least semi-aquatic habits

were primitive for pythonomorphs, and that snakes evolved in a

marine or semi-aquatic environment and are secondarily terrestrial

(Nopcesa, 1908, 1923; McDowell and Bogert, 1954; Haas, 1980).

In order to maintain that the snake stem lineage was always terres-

trial, between four and eight convergent invasions of marine

habitats must be assumed to have occurred in mosasauroids,

dolichosaur-like taxa, and basal snakes. The analysis further sug-

gests that, of all the marine varanoids, Mesoleptos occupies a

crucial phylogenetic position, as the nearest relative of snakes

(Ophidia). If this is true, the similarities between Mesoleptos and

primitive snakes are not convergent; these include such traits as a

proportionally small head, long body, limb reduction, and lateral

body compression. In these features, Mesoleptos appears inter-

M.S.Y. LEE AND J.D. SCANLON

mediate between the typical lizard-like marine varanoids (e.g. mosa-

saurs) and primitive marine snakes.

Two substantial caveats must be added to this interpretation.

Apart from mosasaurs and aigialosaurs, all the marine varanoids are

very imperfectly known. For instance, Mesoleptos can be scored for

only 13% of characters, dolichosaurs for 35% and Adriosaurus for

38%. Such large amounts of missing information suggest that their

positions cannot be very robust, a view confirmed by low bootstrap

and Bremer supports. This missing information also reduces support

throughout the tree, as the poorly known taxa can fit into many

different places with only slight loss in parsimony. Additionally,

many of the characters that unite dolichosaurs, Adriosaurus and

Mesoleptos with mosasauroids and snakes, to the exclusion of other

varanoids, are correlates of marine adaptation. Within this group

(Pythonomorpha), many of the characters uniting dolichosaurs,

Aphanizocnemus, Adriosaurus and Mesoleptos with snakes to the

exclusion of mosasauroids are correlates of body elongation and

limb reduction. Thus, the position of these poorly known taxa close

to snakes might reflect a false signal caused by marine adaptation

and body elongation, both features found in basal snakes. More

complete fossil finds, and thus, information on characters not obvi-

ously correlated with habitat and body form, are required before

their phylogenetic relationships can be conclusively ascertained and

the early evolution of snakes clearly understood. The fundamental

questions investigated by Bellairs and Underwood (1951) and

Underwood (1967) regarding the affinities and ecological origins of

snakes still await convincing answers.

ACKNOWLEDGEMENTS. ML thanks Garth Underwood for assistance,

friendship, and inspiration during his visits to the Natural History Museum.

We also thank Harry Greene, David Cundall, Michael Caldwell, Jenny Clack

and Susan Evans for comments and/or discussion, and Eitan Tchernoy

(Hebrew University, Jerusalem) for hospitality in Israel and allowing study

and description of their specimen of Mesoleptos. Supported by an Australian

Research Council Senior (QEII) Fellowship and Research Grant to ML.

REFERENCES

Arambourg, C. & Signeux, J. 1952. Les vertébrés fossiles des gisements de phos-

phates (Maroc — Algérie — Tunisie). Service Géologique du Maroc, Notes et Mémoires

92: 1-359.

Auffenberg, W. 1959. Anomalophis bolcensis (Massalongo), anew genus of fossil snake

from the Italian Eocene. Breviora, Museum of Comparative Zoology 114: 1-16.

Averianovy, A.O. 1997. Paleogene sea snakes from the eastern part of Tethys. Russian

Journal of Herpetology 4: 128-142.

Bellairs, A. D’a. & Underwood, G. 1951. The origin of snakes. Biological Reviews of

the Cambridge Philosophical Society 26: 193-237.

Bolkay, S.J. 1925. Mesophis nopcsai n. g., n. sp.; ein neues, schlangendhnliches Reptil

aus der unteren Kreide (Neocom) von Bilek-Selista (Ost-Hercegovina). Glasnika

Zemaljskog Museja u Bosni i Hercegovini 37: 125-136.

Boulenger, G.A. 1891. Notes on the osteology of Heloderma horridum and H.

suspectum, with remarks on the systematic position of the Helodermatidae and on the

vertebrae of the Lacertilia. Proceedings of the Zoological Society of London 1891:

109-121.

Bremer, K. 1988. The limits of amino-acid sequence data in angiosperm phylogenetic

reconstruction. Evolution 42: 795-803.

Caldwell, M.W. 1999. Squamate phylogeny and the relationships of snakes and

mosasauroids. Zoological Journal of the Linnean Society 125: 115-147.

. 2000. On the aquatic squamate Dolichosaurus longicollis Owen, 1850

(Cenomanian, Upper Cretaceous), and the evolution of elongate necks in squamates.

Journal of Vertebrate Paleontology 20: 720-735.

, & Cooper, J. 1999. Redescription, palaeobiogeography, and palaeoecology of

Coniasaurus crassidens Owen, 1850 (Squamata) from the English Chalk (Creta-

ceous, Cenomanian). Zoological Journal of the Linnean Society 127: 423-452.

Calligaris, R. 1988. I rettili fossili degli ‘Strati calcarei ittiolotici di Comen’ e

dell’ Isola di Lesina. Atti del Museo Civico di Storia Naturale, Trieste 41: 85-125.

MESOLEPTOS AND THE ORIGIN OF SNAKES

Camp, C.L. 1923. Classification of the lizards. Bulletin of the American Museum of

Natural History 48: 289-481.

Carroll, R.L. 1985. Evolutionary constraints in aquatic diapsid reptiles. Special

Papers in Palaeontology 33:145-155.

Carroll, R.L. & Debraga, M. 1992. Aigialosaurs: mid-Cretaceous Varanoid lizards.

Journal of Vertebrate Paleontology 12: 66-86.

Cope, E.D. 1869. On the reptilian orders Pythonomorpha and Streptosauria. Proceed-

ings of the Boston Society of Natural History 12: 250-266.

Cornalia, E. & Chiozza, L. 1852. Cenni geologici sull’ Istria. Giornale dell’ I. R.

Instituto Lombardo 3: \-35.

Dollo, L. 1903. Les ancétres des Mosasauriens. Bulletin scientifique de France et

Belgique 38: 137-130.

1904. L’origine des Mosasauriens. Bulletin du Societé belgique de Geologie,

Hydrologie et Palaeontologie, Bruxelles 18: 217-222.

Estes, R., De Queiroz, K. & Gauthier, J. 1988. Phylogenetic relationships within

Squamata. In R. Estes and G. Pregill (eds), Phylogenetic relationships of the lizard

families. Stanford University Press, Stanford, California. Pp. 119-281.

Gardner, J.D. & Cifelli, R.L. 1999. A primitive snake from the Cretaceous of Utah.

Special Papers in Palaeontology 60: 87—100.

Gasc, J.-P. 1974. L’interprétation fonctionelle de l'appareil musculo-squelettique de

l’axe vertébral chez les serpents (Reptilia). Mémoires du Muséum nationale d'Histoire

naturelle, Séries A 83: 1-182.

Goldman, N, Anderson, J.P. & Rodrigo, A.G. 2000. Likelihood-based tests of

topologies in phylogenetics. Systematic Biology 49: 652-670.

Gorjanovic-Kramberger, C. 1892. Aigialosaurus, eine neue Eidechse aus die

Kreideschiefern der Insel Lesina mit Riicksicht auf die bereits beschriebenen

Lacertiden von Comen und Lesina. Glasnik huvatskoga naravoslovnoga drustva

(Societas historico-naturalis croatica) u Zagrebu 7: 74-106.

Greene, H.W. 1997. Snakes — The evolution of mystery in nature. University of

California Press, Berkeley.

Haas, G. 1979. On a new snakelike reptile from the lower Cenomanian of Ein Jabrud,

near Jerusalem. Bulletin du Muséum national d'Histoire naturelle, Paris (4), Section

C 1: 51-64.

— 1980. Remarks on a new ophiomorph reptile from the lower Cenomanian of Ein

Jabrud, Israel. In L. L. Jacobs (ed.), Aspects of vertebrate history: Essays in Honour

of E. H. Colbert. Museum of Northern Arizona Press: Flagstaff AZ. Pp. 177-202.

Hoffstetter, R. 1955. Squamates de type moderne. Traité de Paléontologie 5: 606-662.

1960. Un serpent terrestre dans le Cretacé inférieur du Sahara. Bulletin du Societé

géologique de France 7: 897-902.

& Gayrard, Y. 1965. Observations sur l’osteologie et la classification des

Acrochordidae (Serpentes). Bulletin du Muséum national d'Histoire naturelle, Paris

(series 2) 36: 677-696.

Janensch, W. 1906. Uber Archaeophis proavus Mass., eine Schlange aus dem Eociin

des Monte Bolca. Beitrtige zur Paléontologie und Geologie Osterreich-Ungarns

und des Orients 19:\—33.

Kluge, A.G. 1987. Cladistic relationships in the Gekkonoidea (Squamata, Sauria).

Miscellaneous Publications of the Museum of Zoology, University of Michigan 173:

1-54.

Kornhuber, A. 1873. Uber einen neuen fossilen Saurier aus Lesina. Abhandlungen der

k. k. geologischen Reichsanstalt 5: 75—90, 2 plates.

Kornhuber, A. 1901. Opetiosaurus bucchichi. Eine neue fossile Eidechse aus der

unteren Kreide von Lesina in Dalmatien. Abhandlungen der k. k. geologischen

Reichsanstalt 17: \-24.

Lee, M.S.Y. 1998 Convergent evolution and character correlation in burrowing rep-

tiles: towards a resolution of squamate phylogeny. Zoological Journal of the Linnean

Society 65: 369-453.

— 1999. Aquatic reptiles. In R. Singer and M. K. Diamond (eds), Encyclopedia of

Paleontology. Fitzroy Dearbon: London. Pp.96—101.

2002. Squamate phylogeny, taxon sampling, and data congruence. Herpetological

Monographs in review.

& Caldwell, M.W. 1998. Anatomy and relationships of Pachyrhachis

problematicus, a primitive snake with hindlimbs. Philosophical Transactions of the

Royal Society of London B 353: 1521-1552.

& 2000. Adriosaurus and the affinities of mosasaurs, dolichosaurs and

snakes. Journal of Paleontology 74: 915-937.

—. & Scanlon, J.D. 1999. A second primitive marine snake: Pachyophis

woodwardi from the Cretaceous of Bosnia-Herzegovina. Journal of Zoology, Lon-

don 248: 509-520.

& Scanlon, J.D. 2002. Snake phylogeny based on osteology, soft anatomy and

ecology. Biological Reviews of the Cambridge Philosophical Society 77, in press.

McDowell, S.B. 1987. Systematics. In R.A. Seigel, J.T.C. Collins and S.S. Novak

(eds.), Snakes: Ecology and Evolutionary Biology. MacMillan, New York. Pp. 1—S0.

& Bogert, C.M. 1954. The systematic position of Lanthanotus and the affinities

of the Anguimorphan lizards. Bulletin of the American Museum of Natural History

105: 1-154.

Mosauer, W. 1935. The myology of the trunk region of snakes and its significance for

ophidian taxonomy and phylogeny. University of California Publications in Biologi-

cal Sciences 1: 81-120.

141]

Nopesa, F. 1903. Uber die Varanusartigen Lacerten Istriens. Beitrége zur Paltontologie

und Geologie Osterreich-Ungarns und des Orients 15: 31-42.

1908. Zur Kenntnis der fossilen Eidechsen. Beitrdige zur Paldontologie und

Geologie Osterreich-Ungarns und des Orients 21: 33-62.

—— 1923. Eidolosaurus und Pachyophis. Zwei neue Neocom-Reptilien.

Palaeontographica 65: 99-154.

Owen, R. 1842. Description of the remains of a bird, tortoise and lizard from the Chalk

of Kent. Transactions of the Geological Society of London, Series 2, 6: 411-413.

1850a. Description of the fossil reptiles of the Chalk Formation. In F. Dixon (ed.),

The Geology and Fossils of the Tertiary and Cretaceous Formations of Sussex.

Longman, Brown, Green and Longman, London. Pp. 378-400, 403-404.

1850b. Monograph on the Reptilia of the London Clay. Part Ill. Order Ophidia.

British Museum: London

1851. A monograph on the fossil Reptilia of the Cretaceous formations. Part I.

The Palaeontological Society: London.

1877. On the rank and affinities of the reptilian class of the Mosasauridae,

Gervais. Quarterly Journal of the Geological Society of London 33: 682-715.

Radovanovic, M. 1935. Anatomische Studien am Schlangenkopf. Jenaische Zeitschrift

fiir Naturwissenschaft 69: 321-422.

Rage, J.C. 1984. Handbuch der Paldoherpetologie. Teil 11. Serpentes. Gustav Fischer,

Stuttgart.

Rieppel, O. 1988. A review of the origin of snakes. Evolutionary Biology 22: 37-130.

& Zaher, H. 2000. The intramandibular joint in squamates, and the phylogenetic

relationships of the fossil snake Pachyrhachis problematicus Haas. Fieldiana (Geol-

ogy) 43: 1-69.

Romer, A.S. 1956. Osteology of the reptiles. University of Chicago Press, Chicago.

Scanlon, J.D. 1993. Madtsoiid snakes from the Eocene Tingamarra Fauna of eastern

Queensland. Kaupia: Darmstddter Beitrige zur Naturgeschichte 3: 3-8.

1996. Studies in the palaeontology and systematics of Australian snakes. Unpub-

lished Ph.D. thesis, University of New South Wales, Sydney.

& Lee, M.S.Y. 2000. The Pleistocene serpent Wonambi and the early evolution of

snakes. Nature 403: 416-420.

. . Caldwell, M.W. and Shine, R. 1999. Ecology and taphonomy of the

primitive snake Pachyrhachis. Historical Biology 13: 127-150.

Seeley, H.G. 1881. On remains of a small lizard from the Neocomian rocks of Comén,

near Trieste, preserved in the Geological Musem of the University of Vienna.

Quarterly Journal of the Geological Society of London 37: 52-56.

Sorenson, M. 2000. TreeRot Version 2b. Computer program and documentation.

Distributed by the author, Boston University.

Swofford, D. L. 1999. PAUP*: Phylogenetic Analysis Using Parsimony (*and other

methods). Version 4. Sinauer Associates, Sunderland MA.

Tchernoy, E., Rieppel, O., Zaher, H., Poleyn, M. & Jacobs, L.L. 2000. A fossil snake

with limbs. Science 287: 2010-2012.

Underwood, G. 1967. A Contribution to the Classification of Snakes. British Museum

(Natural History) Publication No. 653. Trustees of the British Museum (Natural

History), London. 179pp.

von Meyer, H.V. 1860. Actaeosaurus tommasinii aus dem schwarzen Kreide-Schiefer

von Comen am Karste. Palaeontographica 7: 223-231.

Walls, G.L. 1940. Ophthalmological implications for the early history of snakes.

Copeia 1940: 1-8.

Zaher, H. & Rieppel, O. 1999. The phylogenetic relationships of Pachyrhachis

problematicus, and the evolution of limblessness in snakes (Lepidosauria, Squamata).

Comptes rendues de |’Académie des Sciences de Paris, Sciences de la terre et des

planétes 329: 831-837.

Appendix 1

Additions to the osteological data matrix of Lee (2002) used in this

cladistic analysis. Mesoleptos was added to the taxon list and could

be coded for the following characters.

Axial Skeleton

171. Centra. Not constricted anterior to condyle, i.e. condyle not

wider than posterior end of centrum (0); slightly constricted

anterior to condyle, i.e. condyle slightly wider than posterior

end of centrum (1); greatly constricted anterior to condyle, 1.e.

condyle much wider than posterior end centrum (2). Mesoleptos

172. Vertebral articular surfaces. Vertical, condyles (if present)

facing posteriorly, much of the articular surface is visible in

ventral view (0); slightly anterodorsal, condyles facing slightly

dorsally, only the ventral edge of the articular surface is visible

—

in ventral view (1); anterodorsal, condyles facing very dorsally,

none of the articular surface is visible in ventral view (2).

Mesoleptos 0.

. Centra. Notochordal, i.e. perforated by persistent notochord

in adults (0); not notochordal, i.e. not perforated by persistent

notochord in adults (1). Mesoleptos 1.

Centra. Amphicoelous (0); procoelous (1). Mesoleptos 1.

. Neural spines. Tall processes (0); low ridges (1). Mesoleptos 0.

Zygosphenes and zygantra. Present (0); absent (1).

Mesoleptos 0 (Visible on the MCSNT specimen).

. Intercentra on dorsal (thoracolumbar) vertebrae. Present

(0); absent (1). Mesoleptos 1.

. Number of presacral vertebrae. 23 to 25 (0); 22 or fewer (1);

26 (2); 27 to 50 (3); 50 to 119 (4); 120 to 150 (5), 150 or more

(6). Mesoleptos 3.

. Transverse processes of cervicals. On anterior end of cen-

trum (0); on middle of centrum (1). Mesoleptos 0.

. Hypapophyses on anterior presacrals. Only extending to the

posterior end of the sixth presacral at most (0); extending to the

seventh presacral or beyond (1). Mesoleptos 1.

. Anterior presacral vertebrae (excluding atlas and axis

intercentra). Not sutured or fused to preceding centrum (0);

sutured to preceding centrum (1); fused to preceding centrum

(2). Mesoleptos 2.

. Anterior presacral vertebrae Not sutured or fused to follow-

ing centrum (0); sutured to following centrum (1); fused to

following centrum (2). Mesoleptos 0.

. Pachyostosis of mid-dorsal vertebrae and ribs. Absent (0);

present (1). Mesoleptos 0.

. Body shape. Round, dorsal ribs smoothly curved (0); laterally

compressed, middle and distal regions of dorsal ribs totally

straight (1). Mesoleptos 1.

. Ribs. Proximal end without anteroventral pseudotuberculum

(0); proximal end with anteroventral pseudotuberculum (1).

Mesoleptos 0.

. Ribs. Proximal end without posterodorsal pseudotuberculum

(0); proximal end with posterodorsal pseudotuberculum (1).

Mesoleptos 0.

. Distally forked cloacal ribs (‘lymphapophyses’). Absent (0);

present (1). Mesoleptos 0.

. Tail. Cylindrical or only slightly lateral compressed, trans-

verse processes well-developed, chevrons and neural spines

not elongated (0); very laterally compressed, transverse proc-

esses reduced anteriorly and absent posteriorly, chevrons and

neural spines elongated (1). Mesoleptos 1.

. Scapulocoracoid. Present and large (0); present but reduced

(1); absent (2). Mesoleptos 1.

. Emargination on anterodorsal edge of scapula. Absent (0);

present (1). Mesoleptos 0.

. Anterior (primary) coracoid emargination. Absent (0);

present (1). Mesoleptos 1.

. Posterior (secondary) coracoid emargination. Absent (0);

present (1). Mesoleptos 1.

. Clavicle. Present (0); absent (1). Mesoleptos 0 (see text for

discussion of identity of this element).

. Clavicles. Rod-like, at most only slightly expanded proxi-

mally and with no notch or fenestra (0); greatly expanded

proximally, usually with notch or fenestra (1). Mesoleptos 0

(see text for discussion of identity of this element).

. Forelimbs. Large (0); small (1), absent (2). Mesoleptos 1.

2. Pelvis. Present and large (0); present and small (1); absent (2).

Mesoleptos 1.

. Hindlimbs. Well-developed (0); reduced (1); absent (2).

M.S.Y. LEE AND J.D. SCANLON

Mesoleptos |.

234. Body proportions. Head moderately large with respect to

wide trunk region (0); head extremely small with respect to

wide trunk region (1). Mesoleptos 1.

235. Dorsal body osteoderms. Absent (0); present (1). Mesoleptos

236. Ventral body osteoderms. Absent (0); present (1). Mesoleptos

246. Epiphyses. Present on appendicular and axial skeleton (0);

present on appendicular, but absent on axial skeleton (1);

absent from both appendicular and axial skeleton. Mesoleptos

1. Note Haasiophis was incorrectly coded with state 1 in Lee

(2002); it has state 2.

Appendix 2 Synapomorphies for Clades A-D in Fig. 3A

Character number, consistency index and direction of change (if not

0 — 1) listed in parentheses.

Clade A: dolichosaurs, Adriosaurus, Mesoleptos, and

Ophidia

*More than ten cervical vertebrae (181, 0.6, 23), *Scapulocoracoid

reduced (203, 0.67), *interclavicle absent (210, 0.33), *forelimbs

small (218, 0.5), *pelvis reduced (222, 0.5), *hindlimbs small (228,

0.67).

Clade B: Adriosaurus, Mesoleptos, and Ophidia

*Premaxilla-maxilla contact mobile (5, 1.0), frontals paired (26,

0.14), postorbitofrontal ventral process large (36, 0.5, 10), su-

pratemporal superficial (52, 0.67, 10), *body laterally compressed

(196, 0.5), pubis not expanded distally (227, 1.0).

Clade C: Mesoleptos and Ophidia (snakes)

*Vertebral condyles facing posteriorly (172, 1.0, 10), *head small

with respect to trunk (234, 1.0).

Clade D: Ophidia (snakes)

Dorsal process of maxilla on middle or anterior of maxilla (8, 0.5,

1-30), posterior process of maxilla long (10, 0.33, 1-0), lacrimal

absent (11, 0.5), frontoparietal suture with sinuous contact (30, 0.2,

1-0), pineal foramen absent (40, 0.17), parietal table reduced to

sagittal crest (42, 0.22, 10), suspensorial ramus of parietal reduced

(44, 0.5), upper temporal arch incomplete (45, 0.25), tympanic crest

absent (57, 0.29, 0-2), parietal downgrowths contacing

parabasisphenoid (67, 1.0), optic foramina enclosed in bone (68, 1.0),

anterior brain cavity floored by frontals and cultriform process (69,

0.67, 0-2), trigeminal foramina bordered at least partly by parietal

(70, 1.0), supraoccipital on skull roof behind parietal (86, 0.5),

posttemporal fenestra closed (89, 0.5), opening of Jacobson’s organ

enclosed by vomer and septomaxilla only (94, 0.4, 12), vomer

medial to palatine (99, 1.0), palatine-vomer contact mobile (102,

1.0), palatine long (103, 0.33, 10), palatine with distinct rectangu-

lar process (105, 1.0), two or fewer mental foramina on lateral surface

of dentary (117, 1.0), posterior margin of lateral surface of dentary

deeply notched (123, 0.4, 12), dentary overlapped by surangular

(124, 1.0,0—2), surangular extends far over lateral surface of dentary

(134, 1.0, 23), articular fused with prearticular and surangular

(144, 0.25, 10), retroarticular process short (145, 1, O01), mar-

ginal teeth with medial and lateral carinae (153, 0.67, 12), palatine

teeth present (166, 0.33, 10), palatine teeth long fangs (167, 1.0),

*at least 120 presacral vertebrae (180, 0.6, 3-5), *lymphapophyses

present (200, 0.67).*shoulder girdle absent (203, 0.67, 12), *clavi-

cle absent (207, 0.33), ossified sternum absent (213, 1.0), *forelimbs

absent (218, 0.5, 12), scleral ossicles absent (241, 0.5), *appen-

dicular epiphyses absent (246, 0.67, 12).

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 143-154

Phallus morphology in caecilians (Amphibia,

Gymnophiona) and its systematic utility

DAVID J. GOWER AND MARK WILKINSON

Department of Zoology, The Natural History Museum, London SW7 SBD, UK.

email addresses: davig@nhm.ac.uk, marw @nhm.ac.uk

CONTENTS

MSTHEGHCLT CHUGH Et en tee cee tox cece conus t eee eet ev WERE ERE ce cor axes sasaeusccans<duacuaandeccdcacsancacedehisedvonciiticacusvuabemseticsdesdeesssesdidavauuceacioee 143

NE) LEM A O MINIS CUNIR LEM Un ane ct age cers textece et eaten en CreeeenWtane sexes eersssuorucmucsersesucussasesosvasascdaradsaversseases ... 144

Abbreviations used in figures ..... .. 144

Morphol a pyprerss.se-ccarcenns «sscrones-ceeees .. 144

Disposition of the cloaca ..... .. 144

PDAs Netra Sees nt Lea LOA Cleat anne eee toca MEO rare ets ce wat anete << dees ts ereneaiivedaasay¥saheen ies ec duoeaiVattot wtswasisecancebsvesessiesisiaasevecuseoneves 146

MUDch ch eevee cece ene ccaee a sane eas eta a ncarrs const asisnsiva ddaschnsddsczentsl lascagsteiae osdvecsassutvadedssvsvasancasesieassvssvessdeastnastacseusds 146

Stn US GN eeeeamenen seers cee essere eas esses sueteccut ties autos wavecyacsat<idsbastsenadiensceasevorsnusaswasscscuennsescepdeevall cosaete@inawrabuteisversoveneeouescesienevarseeeses 146

PSUNEC TLC Emp LALA CSCRS ULM eet ce tee eee ep er see eee cee = cone nn sc gh c¥as'dcebeyaxanWscdsttees=deeesestwce Gopdekevorhactrihenoraasbeas desttuaecessecseasieessaasuiases 147

FRGSTE yn peal LIM ow esreeca testerectax ne cxene ean hen cee cea’ eavupensedeapascncaasnaxandvovuasencravancasvarendsbis exaecvispasssdnsxaaadesdaunsoaracesoseaseecetcecesntens 148

Sy ea ML 6) COSA CV THTNANRNES MD UA CONN renee en cers anes cn ac cea a gndaed tapas piesa retndomsonwccasScteoaeaansadtep tatea cbs sa succnus mascapsnss<arveveverssvstseVuasseezs 148

OMPOSI LOMO 1s MAUL EAM SUNG LEME S brews vadaatex sc uuss taxa apes mess oan oaun- ap ten asnsenateemateas nc datas abek ser easensnule saeiwessadenaueansacesneuasens<cuxecrntsns 148

Relanonsiip Deiweeni theme verted Glodcaland the PMAMS ..-.2.cc:.c0-es+-ccecensancensepeeysdeteceaecesac-neseedenvsacedevonorosedtenssecasuessouseacees 149

RSYIS LeU cl LCS eNO ene pesca aan oes eter eee nee meres cn acs bats seatese terse azusvacs emasds oeeanesee wath acd dnasctucdcyacsevonvotensesivseinessaraccsssuntatvensvitt 149

ESF PALS MOND MOLOMYISMECIES SOE CHG 2 aavagsevensssssnsciessavasssesdees cacgnastaseasnesenssscxsuipestcdndp owas Avsvovexewasusuadsvesnvacertevsenedvavadesseencoeoe 149

RS Me ACURA AEN COMCANI CLUCNEATT LCR CLESTREN LN ian tara canoe ae asnceeceveo ouguvadeneassceteucaeeWWer,Pasderanicscxsansi cevanxeseazaueusipcesucesseiscestarsees 152

IB SYS UTS UST fret een eee ae ea ee hag sn stare seen coax css ensahisniveveanscaveadcnivatcedssisidesatcedseacseavescsccvasaceasaacsussuceadsdaessiaccesdnsewazecesese 152

PAOLO MLC SUSE St sete ete eee eee nt SNe cet Nase cc da cesionvsccvsnndsencus unsounareOetastvaceeaebvocsntsurtuecaUscestedeceesasucescenccdsneadanecee ee 153

FPG RENEDIC CS heres cc sect Nee taaeenwetrs tee enc tees eee meee aE cies suanas sunsibvcnn'ees dueron cul dtdaudesssuubudessetarsuetadustiaeseeascccesnvacecsatsucsassatuecsendusess 153

SYNOPSIS. The cloaca of male caecilian amphibians (Gymnophiona) is a tube that comprises an anterior urodeum and a posterior

phallodeum. The phallodeum everts (with the urodeum lying inside it) to form a phallus used for direct sperm transfer in

copulation. Phallodeal morphology is rich in detail and variation, and has therefore been considered a potentially useful and much

needed tool for caecilian phylogenetics and species-level taxonomy. Despite this, it has been almost entirely ignored in caecilian

systematics, there is confusion regarding some aspects of morphology, and variation within and among species is poorly

understood. A short review and reconsideration of phallus morphology is presented, and the systematic potential assessed. The

anterior part of the phallodeum appears to offer the most obvious systematic potential, and the morphology of longitudinal ridges

and their ornamentation here seem to have diagnostic and/or phylogenetic value for some taxa. Although there is evidence of

intraspecific variation, at least some of which is associated with ontogeny and reproductive condition, individuals of the same

species generally have a common pattern of phallodeal ridges and ornamentation, and congeners often share a similar pattern.

However, these patterns are not universally species specific, at least among uraeotyphlids. Although variation needs to be better

understood, the male cloaca offers great potential for caecilian systematics.

Issued 28 November 2002

INTRODUCTION

As in other amphibians, caecilians (Gymnophiona) possess a cloaca,

a chamber that opens to the exterior via the vent and into which open

the large intestine, the urogenital (Wolffian and Miillerian) ducts,

and the bladder. In contrast to other amphibians, the cloaca of male

caecilians can be everted through the vent (Fig. 1) to serve as an

intromittant organ, or phallus, used in copulation to effect direct

sperm transfer (e.g. Himstedt, 1996). It has long been recognised

that the external surface of the caecilian phallus and the correspond-

ing internal surface of the uneverted cloaca may bear distinctive

ridges and grooves, tuberosities and even spines (e.g. Duvernoy,

1849; Giinther, 1864; Spengel, 1876; Noble, 1931). There is consid-

erable interspecific variation in the complex patterns of these features,

but there have been few comparative studies.

Spengel (1876) compared cloacal features in males of six species

in what are now recognised as six genera from three families, and

aspects of cloacal morphology were compared further in some of

these species by Wiedersheim (1879). Tonutti (1931) provided a

very detailed documentation of the uneverted and everted cloaca of

the caeciliid Hypogeophis rostratus (Cuvier, 1829) and compared it

with the uneverted cloaca of the ichthyophiid /chthyophis glutinosus

(Linnaeus, 1758) and of the caeciliid Spihonops annulatus (Mikan,

1820). Tonutti (1933) expanded the comparative aspect of his study

of the caecilian phallus by incorporating detailed data on a further

Six species, including representatives of Scolecomorphidae and

Typhlonectidae. Tonutti’s work remains the most detailed to date.

Taylor (1968 and references therein) figured (though without labels

or orientation) everted phallodea and in situ dissections of 12 species

in eight genera and four families. The broadest comparative study of

the male cloaca was presented by Wake (1972), who examined

144

large —- cloaca

intestine

—-+—.urodeum ——+-——_ phallodeum —

<— anterior—> —posterior>

a vent

large intestine

urodeum

phallus

Fig. 1 Schematic sagittal section through the posterior of a male

caecilian showing (a) main divisions of the uneverted cloaca, and (b)

the everted phallus with the internal, lumenal surface of the phallodeum

on its exterior surface, and the urodeum forming its core.

34 caecilian species, including representatives of 20 currently recog-

nised genera and all six of the currently recognised families. Exbrayat

(1991) compared cloacae of single species from four genera in three

families. Wake (1998) provided comparative data on the cloacal

spines and spicules of the three nominate species of Scolecomorphus

Boulenger, 1883.

Species limits in caecilians are poorly understood and the tax-

onomy within many genera is best viewed as uncertain and potentially

unstable (Nussbaum and Wilkinson, 1989). The inadequate state of

current knowledge has been attributed to the group’s tropical distri-

bution, largely fossorial and secretive lifestyle, under-representation

in museum collections, lack of detailed study, and a relative paucity

of obvious external morphological features in association with their

limbless bodies, reduced or absent tails, and reduced head features

(e.g. Nussbaum & Wilkinson, 1989). Some 34 years after the

publication of Taylor’s (1968) taxonomic monograph, species level

caecilian systematics is still dominated by counts of annuli, verte-

brae, and teeth. Of the phallus, Taylor (1968: 31) was ‘certain that

most genera and many species could be identified by the characters

of this organ alone’ and Wake (1972: 353) stated that ‘the arrange-

ment of musculature and cloacal accessory structures is

species-specific in males.’ If correct, male cloacal morphology, with

its complex structure and many variations, should provide a much

needed tool for investigating species limits in and phylogenetic

relationships among caecilians. However, not much has changed

since Largen et al. (1972: 187) pointed out that ‘The value of penis

structure as a taxonomic character has yet to be fully investigated’.

D.J. GOWER AND M. WILKINSON

We have made observations of the cloacal morphology of a broad

range of caecilian species. Without assembling a thorough synthesis

of these observations, we draw upon them here to provide a descrip-

tion of the male cloaca that emphasises some features that can be

homologised across taxa, and that indicates the kind of variation that

occurs. It is hoped that this contribution will clarify some points of

confusion in the literature and be a stimulus to future research. Our

focus here is on the male cloaca only.

Abbreviations

Text

UMMZ: University of Michigan, Museum of Zoology.

Figures

a.ll anterior tuberosity of 1.1

a.md anterior tuberosity of md

ap anterior part of phallodeum

a.rdl anterior tuberosity of r.dl

a.rvl anterior tuberosity of r.vl

b bladder

bp blind pit

bs blind sac

c colliculus

cl copulator loop

c.md central tuberosity of md

cs cloacal sheath

ebs entrance to blind sac

eu entrance to urodeum

i intestine

l.bs left blind sac

l.dl left dorsolateral longitudinal ridge

Ll left lateral longitudinal ridge

lvl left ventrolateral longitudinal ridge

md mid-dorsal longitudinal ridge

Pp phallodeum

p.lvl posterior tuberosity of 1.vl

p.md posterior tuberosity of md

pp posterior part of phallodeum

p.rdl posterior tuberosity of r.dl

p.rl posterior tuberosity of r.l

p.rvl posterior tuberosity of r.vl

r.bs right blind sac

r.dl right dorsolateral longitudinal ridge

rl right lateral longitudinal ridge

rm retractor muscle

r.vl right ventrolateral longitudinal ridge

s sulcus

sph sphincter

u urodeum

ud urogenital duct

umd mid-dorsal ridge of urodeum

Vv small additional ventral tuberosity

vd vent denticulations

vp vascular plexus

MORPHOLOGY

DISPOSITION OF THE CLOACA. The cloaca of male caecilians is

essentially a tube that extends between the posterior end of the

intestines and the vent, and that may or may not have paired dorsal

diverticula or blind sacs. The intestines, the paired urogenital ducts

PHALLUS MORPHOLOGY IN CAECILIANS

Fig. 2 Uraeotyphlus cf. narayani (field tag MW 249). Phallodeal portion of undissected, uneverted cloaca exposed in the coelom by a mid-ventral

incision through the body wall. The phallodeum has been rotated about its long axis through 90° to show its right lateral aspect. Scale on drawing =

5 mm.

Fig. 3 Uraeotyphlus cf. narayani (field tag MW 249). Anterior phallodeal portion of undissected, uneverted cloaca exposed in the coelom by a mid-

ventral incision through the body wall. The phallodeum has been rotated about its long axis through 180° to show its dorsal aspect. See Fig. 2 for scale.

and bladder open, in close proximity, into the cloaca at its anterior

end. The openings of the ducts and bladder are in the dorsolateral

and ventral wall of the cloaca respectively. The Miillerian and

Wolffian ducts and the intestine may extend posterior to their points

of entry into the urodeum before turning back on themselves in U-

bends or copulator loops that facilitate the eversion of the phallus

(Duvernoy, 1849; Giinther, 1864; Spengel, 1876; Sawaya, 1942;

Wilkinson, 1990; this paper: Figs. 2, 3). As documented by, for

example, Rathke (1852), Giinther (1864), Spengel (1876),

Wiedersheim (1879: 89, Fig. 89) and Tonutti (1931, 1933: e.g. Fig.

32), the mature male cloaca sits within a membranous cloacal

sheath, to which it is unattached other than at its anterior and

146

posterior ends (e.g. Rathke, 1852; Tonutti, 1931; Exbrayat, 1996).

This loose association presumably also facilitates cloacal eversion

(e.g. Spengel, 1876; Wilkinson, 1990). The sheath is continuous

with the mesorchium and with the parietal peritoneum via a ventral

mesentary (e.g. Tonutti, 1933: Fig. 3a).

A musculus retractor cloacae that is unique to caecilians origi-

nates on the mid-ventral body wall and inserts posterior to its origin

on the lateral and ventral surface of the cloaca. In those taxa

possessing blind sacs, the insertion is bifid and is largely or perhaps

entirely on the sacs themselves (e.g. Ichthyophis Fitzinger, 1826

Tonutti, 1931: Fig. 30e; pers. obs.; Uraeotyphlus Peters, 1879, this

paper: Figs. 2, 3). This muscle is thought to retract the everted

phallodeum when contracted (e.g. Giinther, 1864; Spengel, 1876).

DIVISIONS OF THE CLOACA. The cloaca can be divided along its

long axis into two main regions (e.g. Duvernoy, 1849; Tonutti, 1931)

—an anterior cloacal chamber, or urodeum, and a posterior cloacal

chamber, or phallodeum (Fig. 1). The phallodeum of mature indi-

viduals is also broadly divisible into two regions, an anterior part

with pronounced ornamentation that forms the more distal part of

the everted phallus, and a structurally more simple posterior section

that forms the proximal stalk of the everted phallus. Giinther (1864)

and Wiedersheim (1879) discussed three regions in the male cloaca.

Their anterior region corresponds to the urodeum, and their middle

and posterior parts correspond to the anterior and posterior sections

of the phallodeum, respectively. Exbrayat (1991) also distinguished

three regions of the cloaca, but these do not correspond directly to

the partitions recognised by other authors. His middle section

includes the posterior part of the urodeum and the anterior

phallodeum.

The most obvious variations in cloacal morphology occur on the

internal, lumenal surface of the phallodeum, which corresponds to

the external surface of the phallus. The morphology of this surface

can be examined directly in caecilians preserved with the phallus

fully everted, or by dissection, serial sectioning or endoscopy

(Himstedt, 1996). Comparison of dissected cloacae is best effected

by maintaining an approximately standard approach. Figures of

dissected cloacae in the literature (e.g. Duvernoy, 1849; Giinther,

1864; Spengel, 1876; Taylor, 1968; Wake, 1972; this paper) are

mostly of cloacae opened with a longitudinal mid-ventral incision.

This procedure gives a clear view of the dorsal surface of the

phallodeum. Features of the urodeum must be determined by dissec-

tion, sectioning, or endoscopy. The caecilian phallus is sometimes

referred to as the phallodeum (e.g. Duellman & Trueb, 1986), but the

latter term is more properly reserved for the posterior cloacal

chamber. The urodeum, at least in part, also contributes to the

phallus by forming its core as it lies inside the everted phallodeum

(e.g. Tonutti, 1931: Fig. 22b; this paper: Fig. 1).

In the majority of caecilians, the distinction internally between

the urodeum and phallodeum is obvious in dissected specimens. The

relatively simple and narrow urodeum gives way posteriorly to the

broader phallodeum, which has pronounced longitudinal (and/or

oblique) ridges and deep sulci extending to the phallodeal-urodeal

border (e.g. see figures of Uraeotyphlus below). In most taxa, a mid-

dorsal protuberance marks the posterior end of the urodeum. This

protuberance is here termed colliculus (= little hill). The colliculus is

perhaps equivalent, at least in part, to the ‘bourrelet’? mentioned by

Duvernoy (1849; also Exbrayat, 1991). Typically the colliculus

projects into the phallodeal chamber to a varying degree, being

particularly large in some species (e.g. pers. obs. of Gegeneophis

ramaswamii Taylor, 1942, Herpele squalostoma (Stutchbury, 1834),

and Microcaecilia unicolor (Duméril, 1864)). In species with blind

sacs, these open into the phallodeum adjacent to its border with the

D.J. GOWER AND M. WILKINSON

urodeum. A major exception to this general pattern is apparently

restricted to the caeciliid genera Dermophis Peters, 1879 and

Gymnopis Peters, 1874 (MW, pers. obs.). In these caecilians, which

lack blind sacs, there is no definite colliculus and no clear differen-

tiation between urodeum and phallodeum. Given the apparently

universal presence of distinct phallodeal and urodeal chambers in all

other caecilians, including all non-caeciliids (outgroups), we inter-

pret its absence as a putative synapomorphy of Dermophis and

Gymnopis.

Wake (1972) made no use of a clear urodeum-phallodeum divi-

sion in her descriptions. She documented several features close to

the openings of the urogenital ducts, which are in the anterior

urodeum rather than the phallodeum. In our experience, this is a far

more irregular region in which gross morphological regularities are

less apparent and variation is harder to characterise than in the

phallodeum. Wake (1972) mostly examined partially opened

cloacae in which only the anterior part of the phallodeum could be

observed.

The absolute and relative sizes of the urodeum and phallodeum

may vary taxonomically but substantial variation within species

might be expected given that the cloaca must serve both reproduc-

tive and alimentary functions. Exbrayat (1991) has presented

evidence of seasonal variation correlated with the breeding cycle in

Typhlonectes compressicauda (Duméril and Bibron, 1841), and

short term changes might even occur with the passage of faeces. In

a sample of 11 preserved Hypogeophis rostratus, the phallodeum

ranged from 1.6 to 5.3 times the length of the urodeum (MW,, pers.

obs.), demonstrating considerable intraspecific variation in size in

this species.

URODEUM. The urodeum is a relatively simple and typically nar-

row chamber. Its dorsal surface is characterised by a pronounced

mid-dorsal longitudinal ridge (see figures of Uraeotyphlus below)

and seemingly irregular arrangements of other, less pronounced

ridges. The appearance of the lesser ridges can vary substantially

with state of preservation and possibly also in life. The colliculus is

an expansion of the posteriormost part of the mid-dorsal urodeal

ridge, and it shows variations in form that may be of systematic

value, as may differences in the overall shape of the urodeum (long

and narrow or short and somewhat broader). Additional lateral or

ventral more pronounced longitudinal ridges may also be present in

the urodeum (Wake, 1972). Wake (1972) described considerable

variation in the form of the urodeum at the points of entry of the

urogenital ducts, which are often depressed and may vary in their

relations to the mid-dorsal longitudinal ridge. She reported that

papillae associated with the openings of the urogenital ducts were

present only the typhlonectids (Typhlonectes compressicauda,

Chthonerpeton indistinctum (Reinhardt and Liitken, 1861) and C.

viviparum Parker and Wettstein, 1929) that she examined. However,

one of us (MW) has observed urogenital papillae in other species,

including taxa that Wake reported as lacking them (e.g. Grandisonia

sechellensis (Boulenger, 1909) and Geotrypetes seraphini (Dumeéril,

1859)). Systematically useful variation may occur in the urodeum

but we have not yet discerned clear patterns of variation.

BLIND SACS. Blind sacs (caecal appendage of Giinther, 1864;

Penisblindsack of Spengel, 1876; Blindsack of Wiedersheim, 1879;

Penissack of Tonutti, 1931) are paired anterior extensions of the

phallodeum that run parallel to the urodeum (Figs. 2, 3). Blind sacs

vary in size and they may be free or partially fused to the adjacent

urodeum (e.g. Wake, 1972). In species with blind sacs, these are a

feature of the mature cloaca and may be absent or less well devel-

oped in immature males (see discussion of Uraeotyphlus below). In

most cases, species within the same genus, or that are otherwise

PHALLUS MORPHOLOGY IN CAECILIANS

147

Fig. 4 Uraeotyphlus cf. narayani (field tag MW 207). Views of (a) right lateral, (b) dorsal, (c) distal and slightly ventral, and (b) ventral surfaces of

phallus (everted cloaca). Scale bar for Fig. 4b = 3 mm.

considered to be closely related, have blind sacs in a similar con-

dition, suggesting relatively stable and systematically informative

interspecific variation. Blind sacs are well developed in ichthyophiids

and uraeotyphlids, caecilians that Wake (1972) considered ‘primi-

tive’ in other reproductive characters, leading her to suggest that

well developed blind sacs are a general caecilian feature, with

reduction and loss being derived. In contrast, Tonutti (1931, 1933)

considered well developed blind sacs derived. Rhinatrematids are

believed to be the sister group of other extant caecilians on the basis

of a wide variety of evidence (e.g. Nussbaum, 1977; Hedges et al.,

1993; Wilkinson, 1996). Spengel (1876) and Wake (1972) docu-

mented blind sacs in the rhinatrematids Rhinatrema bivittatum

(Cuvier, 1829) and Epicrionops petersi Taylor, 1968 respectively,

but we note their absence (or minimal development) in mature

Epicrionops marmoratus Taylor, 1968 (MW, pers. obs.). This sug-

gests homoplasy and may complicate the interpretation of polarity.

ANTERIOR PHALLODEUM. The lumenal surface of the anterior

phallodeum bears the distinctive structures seen on the external

surface of the more distal part of the fully everted phallus (Figs. 1, 4

to 9). Much variation occurs here, but we discern a presumably

homologous pattern anteriorly that is common to almost all caecilians.

In this region there is a pair of deep dorsolateral grooves, one on

either side. Each of these sulci (Figs. 4 to 9) are bordered by a pair

of well developed, parallel dorsolateral longitudinal or oblique

ridges. A median mid-dorsal longitudinal ridge may or may not also

be present, a variation that appears to be species specific. In species

with blind sacs, the sulci and their bordering ridges run into the blind

sacs, extending to their distal tips. In species lacking blind sacs, the

ridges fade out and the sulci open out at the anterior of the phallodeum,

either side of the colliculus. In Hypogeophis rostratus, the sulci run

posteriorly and terminate blindly with the fusion of their associated

ridges (Tonutti, 1931: Fig. 20; pers. obs.), a pattern that is consistent

in the 11 specimens of this species examined by one of us (MW).

Similar ‘fusion’ of the dorsolateral longitudinal ridges occurs in

many caecilians (e.g. Uraeotyphlus, Figs. 6 to 9). Less commonly,

the posterior end of each sulcus is open, with the more medial

bordering ridge fading out or fusing with its antimere along the

dorsal midline (e.g. Grandisonia alternans (Stejneger, 1893),

Gegeneophis ramaswamii, Boulengerula boulengeri Tornier, 1896,

MW, pers. obs.). Additional major longitudinal ridges may or may

not be present lateral and/or ventral to those forming the sulci. In

uraeotyphlids (Figs. 4 to 9) and ichthyophiids, major longitudinal

ridges are broadly distributed, whereas in some caeciltids (pers. obs.

of e.g. Grandisonia Taylor, 1968 and Schistometopum Parker, 1941;

this paper: Fig. 10) the ridges are more restricted to the dorsal

surface of the phallodeum. Although we have discussed a single

main pair of sulci, there may be other, smaller, more or less

148

D.J. GOWER AND M. WILKINSON

Fig.5 Uraeotyphlus cf. narayani (field tag MW 207). Views of (a) dorsal, and (b) distal and slightly ventral surfaces of phallus (everted cloaca). For

scale see Fig. 4.

Fig. 6 Uraeotyphlus cf. narayani (field tag MW 254). Dissected cloaca

of mature male. The cloaca has been opened mid-ventrally and pinned

to reveal the lumenal surface of the phallodeum and posterior part of the

urodeum. The incision has longitudinally bisected the right ventrolateral

longitudinal ridge so that parts of it lie on each side of the open cloaca.

Scale = 3 mm.

longitudinal grooves at the anterior end of the phallodeum, at least

some of which may enter the blind sacs, where present (e.g.

Geotrypetes Peters, 1879, pers. obs.).

POSTERIOR PHALLODEUM. The distinction between the anterior

and posterior phallodeum is sometimes less clear cut than that

between the phallodeum and urodeum. Wake (1972) reported that

the longitudinal ridges of the anterior phallodeum continue

posteriorly to the vent. We find that the major longitudinal ridges

reduce greatly posteriorly, either abruptly or gradually, that they

may or may not extend as far as the vent, and that the pattern of

ridges within the posterior phallodeum is irregular or less obviously

regular than those of the anterior phallodeum. The phallodeum

narrows dramatically posteriorly, shows considerable variation in

length, and has its terminal portion surrounded by a sphincter of

variable size.

PHALLODEAL ORNAMENTATION. The major longitudinal ridges

of the anterior phallodeum may be more or less invested with, or

elaborated into, tuberosities, transverse ridges and grooves, longi-

tudinal crests, or spines that are often in distinctive patterns (e.g.

Figs. 6, 9). Isolated thickenings or other ornaments may also

occur in the spaces between the major longitudinal ridges. The

ridges associated with the dorsolateral sulci bear such features

only posterior to the sulci (e.g. Figs. 4, 7, 9). Both the shape and

arrangement of this ornamentation may be expected to provide

systematic characters, although there is also evidence of

intraspecific variation (e.g. Scolecomorphus, Wake, 1998). Species

appear to differ in whether the ridges within the posterior

phallodeum bear any ornamentation or not. Where present, as in

Typhlonectes compressicauda (Exbrayat 1996), they are not as

pronounced or distinctive as the structures of the anterior

phallodeum (distal phallus).

COMPOSITION OF PHALLODEAL STRUCTURES. The composition of

the main longitudinal ridges and their ornamentation is unclear from

PHALLUS MORPHOLOGY IN CAECILIANS

the literature and warrants further histological examination. Tonutti

(1931, 1933) viewed the longitudinal ridges as encompassing longi-

tudinal ’propulsor’ muscles but we are unable to verify this from his

figured sections. Wake (1972: 354) described the ridges as ‘longitu-

dinal muscles overlain by fibrous connective tissue’, but also warned

(p. 363) that ‘Caution must be exercised in interpreting the various

folds in the cloacal wall. They may often not be muscle but may be

ridges of connective tissue’. Wake (1998) referred to connective

tissue ridges in Scolecomorphus and made no mention of previous

reports that ridges are muscular (Tonutti, 1933; Wake, 1972). Wake

(1972) also referred to at least some phallodeal ornamentation as

transverse muscle ridges, whereas Wiedersheim (1879) stated that

the prominences are hardened parts of longitudinal folds of cloacal

mucosa. In at least one case it is clear that the prominences are not

muscular: large recurved calcified or cartilaginous spines are present

in Scolecomorphus uluguruensis Barbour and Loveridge, 1925

(Noble, 1931; Taylor, 1968; Nussbaum, 1985; Wake, 1998). Exbrayat

(1991) showed that tuberosities in the phallodeum of Typhlonectes

compressicauda are keratinous, and that their thickness varies with

the reproductive cycle. Exbrayat (1996) described smooth trans-

verse and striated longitudinal muscles in the wall of the cloaca of T.

compressicauda, with the latter forming the major longitudinal

ridges. Muscle therefore appears to be present in the longitudinal

phallodeal ridges of at least some species, but we find no clear

evidence that any of the tuberosities, crests etc found in the

phallodeum are muscular.

RELATIONSHIP BETWEEN THE UNEVERTED CLOACA AND THE PHALLUS.

There is some confusion in the literature regarding the positional

relationship between structures as seen on the internal surface of the

uneverted phallodeum, and the same structures when observed on

the external surface of the phallus. Wake (1972: 359, Fig. 13, 15)

described and figured the blind sacs as being positioned at the

proximal base of the everted phallodeum in a thickened ‘blind sac

sheath’. In the uneverted phallodeum, blind sacs, where present, are

pockets extending from the dorsal wall of the phallodeum, very

149

close to the border between the phallodeum and urodeum. The sacs

extend anteriorly from the anterior end of the phallodeum so that,

within the coelom, they can be seen running parallel to the posterior

end of the urodeum (e.g. Wiedersheim, 1879: Fig. 88; this paper:

Figs. 2, 3). Thus, the blind sacs must be positioned at, or inside, the

distal end of the everted phallus (Tonutti, 1931: e.g. Fig. 22b of

Hypogeophis rostratus) rather than at its base. This can be clearly

seen by comparing the figures shown here of the uneverted and

everted phallodeum of Uraeotyphlus (Figs. 2 to 9), where the

entrance to the blind sacs are seen right at the distal termination of

the everted phallus (Figs. 4, 5). Preserved specimens may show

various degrees of phallodeal eversion, and it is clear that Wake’s

figures are of partially everted organs, which may have misled her.

In our experience, the major dorsolateral sulci, their associated

ridges, and the colliculus are clearly visible at the distal end of a well

everted phallus, although the extent of phallodeal eversion during

copulation is unknown.

Bons (1986) and Exbrayat (1991) also figured what we consider

to be partially everted phallodea of 7yphlonectes compressicauda.

Typhlonectes have a distinctive ‘cloacal disc’ surrounding the vent

(Taylor, 1968) and Exbrayat’s figure 3 appears to show the cloacal

disk at the distal tip of the protruding phallus, and seemingly

detached from the adjacent skin. However, the disc is continuous

with the surrounding skin and must remain at the base of the phallus

because it is everted rather than telescopically extended.

SYSTEMATICS

IS PHALLUS MORPHOLOGY SPECIES SPECIFIC? The family

Uraeotyphlidae is monotypic, comprising five currently recognised

species of Uraeotyphlus endemic to peninsular India (Pillai &

Ravichandran, 1999). Uraeotyphlidae is the extant sister taxon of

the south and southeast Asian Ichthyophiidae (Wilkinson &

Nussbaum, 1996; Gower et al., 2002; Wilkinson et al., 2002). As

iy I.dl

( i I.

ie ~

p.rvl i |

A fly |

tet

Fig. 7 Uraeotyphlus cf. narayani (field tag MW 172). Anterior phallodeum of mature male, prepared as specimen shown in Fig. 6. Scale = 2 mm.

150

D.J. GOWER AND M. WILKINSON

Fig. 8 Uraeotyphlus cf. narayani (UMMZ 139810). Cloaca of immature male, prepared as specimen shown in Fig. 6. Scale = 2 mm.

with many groups of caecilians, the taxonomy of Uraeotyphlus has

an inadequate basis, with some species known from only few

specimens, many with poor locality data. Few diagnostic characters

have been identified and current keys are not satisfactory, so that

caution needs to be exercised in applying names to individuals, and

in assuming species identity of groups of individuals. The following

discussion draws on the examination of the cloaca in more than 30

male Uraeotyphlus representing at least three distinct species. The

focus here is on features of the lumenal surface of the anterior

portion of the phallodeum, chiefly the longitudinal ridges and their

ornamentation.

Figures 4 to 8 show the morphology of the phallus and dissected

cloacae of four specimens. These are identified as Uraeotyphlus cf.

narayani Seshachar, 1939, but unpublished morphological and mole-

cular data have revealed previously unsuspected diversity in the

populations that these individuals are drawn from. It is not yet

apparent whether this diversity is indicative of previously unrecog-

nised specific or subspecific taxa. Whatever their true specific

identity, these four specimens share a common pattern in the major

features of the anterior phallodeum. There are seven major longitu-

dinal phallodeal ridges — a single mid-dorsal ridge, and pairs of

dorsolateral, lateral, and ventrolateral ridges. As in most other

caecilians, the anterior end of each dorsolateral ridge holds a major

longitudinal sulcus that extends into the corresponding blind sac

(Figs. 4, 5, 9). In mature individuals, each of the major longitudinal

ridges bear hardened transverse thickenings. When relatively small,

these thickenings bear an approximately transverse narrow line of

dense, opaque tissue that stands out against the more translucent

main body of longitudinal ridge. Where relatively large, the

thickenings are developed into tuberosities that can be irregular, and

that interlock in the uneverted cloaca. The mid-dorsal ridge bears

three such tuberosities and the other, paired longitudinal ridges two

each. The transverse thickenings of each major longitudinal ridge

are offset relative to each adjacent ridge, and they generally bear the

same spatial relationship to each other in each individual (Figs. 4 to

7). Of the paired ridges, the lateral ones are the least well developed,

and sometimes they are best located by their transverse thickenings.

Within this common pattern are some minor variations. In immature

males (Fig. 8), the main longitudinal ridges are less well developed

and bear no transverse thickenings or indications of hardened tissue,

but they can still be readily identified and homologised with those in

mature males. In addition, the blind sacs of immature males are not

developed. Instead, there is a pair of shallow pits in their place. The

relative size of the transverse thickenings or tuberosities also varies

lvl

Fig.9 Uraeotyphlus cf. oxyurus (field tag MW 469). Cloaca of mature

male prepared as specimen shown in Fig. 6. The incision has

longitudinally bisected the left ventrolateral longitudinal ridge so that

parts of it lie on each side of the opened cloaca. The left side of the

posterior end of the urodeum has been torn away from the anterior end

of the phallodeum so that retractor muscle is visible through the

resulting hole. Scale = 3 mm.

PHALLUS MORPHOLOGY IN CAECILIANS

Fig. 10 Schistometopum gregorii from Tanzania. Views of (a) dorsal, and (b) right lateral surface of phallus of field specimen MW 3257

and (d) ventral surface of phallus of field specimen MW 3251. Scale bars in mm.

Itsy

among individuals, but whether this variation is correlated with

taxonomy, ontogeny, and/or temporally within any possible repro-

ductive cycles is as yet unknown. Occasionally, minor variations in

the ornamentation are seen. For example, the individual shown in

Fig. 4 also has a single, poorly formed, transverse thickening

ventrally. In the individual shown in Fig. 6, the posteriormost

transverse thickening on the right dorsolateral longitudinal ridge

extends posterior to the posteriormost transverse thickening on the

mid-dorsal longitudinal ridge, whereas the reverse of this pattern (as

seen on the left of this individual) is more commonly encountered.

Finally, the transverse thickenings or tuberosities are sometimes

multipartite.

Figure 9 depicts the phallodeum of an individual identified as U.

cf. oxyurus (Duméril and Bibron, 1841). Although the precise

specific identity of this individual also is not entirely clear, we are

confident that it is referable to a species distinct from that (or those)

represented in Figs. 4 to 8. For example, the U. cf. oxyurus indi-

vidual comes from a population with substantially more vertebrae

(112-115, n = 18) than the populations represented by the other

figured specimens (93-110, n> 100). Despite their apparent specific

distinctness, the phallodea of U. cf. narayani (Figs. 4 to 8) and U. cf.

oxyurus (Fig. 9) share the same number and pattern of longitudinal

ridges and transverse ornamentation. Thus Wake’s (1972: 353)

claim that the phallodeal ridges and ‘cloacal accessory structures is

species-specific’ does not appear to hold — at least not at the level of

the presence, number, or topographical relations of major features. It

might yet hold for morphometric variations of phallodeal features

and/or for fine morphological details of the longitudinal ridges and

their ornamentation, but this needs further assessment.

That not all species of Uraeotyphlus share the same basic

phallodeal morphology is revealed by observation of U. cf.

malabaricus (Beddome, 1870), in which the number and arrange-

ment of longitudinal ridges and their ornamentation is markedly

different. Interestingly, analysis of mitochondrial DNA sequence

data strongly indicates that U. narayani and U. cf. oxyurus share a

more recent common ancestor with each other than either does with

U. cf. malabaricus (Gower et al., 2002).

SPECIES’ DIFFERENTIATION AND GENERIC IDENTITY. Nussbaum &

Pfrender’s (1998) recent revision of the caeciliid genus

Schistometopum recognised two species occurring on opposite sides

of the African continent. S. thomense (Barboza du Bocage, 1873) is

known from Sao Tomé island in the Gulf of Guinea, and S. gregorii

(Boulenger, 1894) from lowland coastal regions of Kenya and

Tanzania. The validity of the genus has not been seriously ques-

tioned, but it is currently diagnosed on a combination of characters,

with no known unique synapomorphies.

Wake (1972: 358) described the male cloaca of S. thomense as

having ‘four regularly spaced muscle bands on each side of the

cloaca’, presumably features of the urodeum, and that ‘the posterior

part of the cloaca [more the central region, as can be seen when the

cloaca is fully dissected] is arranged in three sets of transverse,

crescent-shaped muscles, one mid-dorsal, the other two ventro-

lateral.’ Tonutti (1933) described longitudinal phallodeal ridges as

dorsal rather than ventrolateral in S. thomense and we concur with

his assessment (see Fig. 10). Wake found the cloaca of S. gregorii to

have a similar morphology to that of S. thomense. Although we are

not convinced that the transverse ridges comprise muscle, we agree

that the two species share a similar morphology, and consider the

presence of three (though see discussion of S. gregorii below)

narrow and long longitudinal ridges with a characteristic ornamen-

tation of regularly spaced, scalloped transverse ridges and grooves

to be restricted to these two species among material we have

D.J. GOWER AND M. WILKINSON

a b

Fig. 11 Sketches showing disposition of major longitudinal ridges and

their ornamentation in the dorsal lumenal wall of the anterior part of the

phallodeum of (a) Schistometopum thomense (UMMZ 188027), and (b)

S. gregorii (UMMZ 147011) from Kenya. Compare with Tanzanian S.

gregorii shown in Fig. 10. Not drawn to scale.

observed. Thus, this phallodeal structure is potentially a unique

diagnostic character of Schistometopum.

Wake (1972) considered the phallodeal ridges of Schistometopum

to resemble the condition in Geotrypetes. However, the part of the

mid-dorsal longitudinal ridge that bears ornamentation in both S.

thomense (Fig. lla) and S. gregorii (Figs. 10, 11b) is relatively much

longer than the comparable ornamented area in Geotrypetes

seraphini, which 1s instead restricted to a small nubbin that lies at, or

slightly beyond, the level of the posterior end of the ornamented part

of the longitudinal ridges lateral to it (pers. obs. of e.g. UMMZ

172648). In addition, the ornamentation appears to be somewhat

different in the two genera, which otherwise also have quite differ-

ently organised cloaca (for example, Schistometopum lacks blind

sacs).

The phallodeum of a single specimen (UMMZ 147011) of S.

gregorii from Northern Kenya has been examined and a sketch of

the ornamented part of the longitudinal ridges is shown in Fig. 11b.

The figured morphology is largely similar to that seen in several

specimens of S. thomense (e.g. Fig. 11a), except that, in UMMZ

147011, there is not a single mid-dorsal ridge, but instead two

paramedian longitudinal ridges, one longer than the other. Both of

these ridges bear transverse crests, but they are shorter relative to the

dorsolateral longitudinal ridges than in the observed specimens of S.

thomense. The morphology of the mid-dorsal region of the phallo-

deum in two Tanzanian specimens of S. gregorii observed for this

study (Fig. 10) both bear a greater resemblance to the condition in S.

thomense (Fig. 11a) than to the single Kenyan S. gregorii (Fig. 11b)

examined. The sample size is small, but the observed morphological

variation is intriguing in light of Taylor’s (1968: 677) suggestion

that, based on differences in annulation, the Tanzanian and Kenyan

populations of S. gregorii might be specifically distinct.

DISCUSSION

The complex structure of the caecilian phallus offers great potential

for caecilian systematics, both as a source of diagnostic features for

species, and of characters for phylogenetics. However, to fully

exploit this potential requires a better understanding of the extent of

intraspecific variation that occurs within features that appear to vary

interspecifically. Of course, in this regard there is no difference

between the caecilian phallus and any other structure employed in

systematics, and we suggest that incomplete understanding of vari-

ation should temper but not discourage the use of cloacal characters

PHALLUS MORPHOLOGY IN CAECILIANS

in caecilian systematics. There is evidence of considerable ontoge-

netic variation in the development of blind sacs and phallodeal

ornamentation, emphasising the need for systematic comparisons to

be of co-ordinate developmental stages or of developmental trajec-

tories. There is also evidence of variation in adults in the sizes of the

urodeum and phallodeum, and the exact form of ridges, their orna-

mentation, and other phallodeal structures, at least some of which is

seemingly correlated with breeding cycles. Despite Wake’s (1998:

183) statement that the morphology of the phallodeum of

Scolecomorphus ‘is indeed consistent within the species’, the same

paper clearly documents intraspecific variation in the number of

phallodeal spines in Scolecomorphus uluguruensis and S. vittatus

(Boulenger, 1895). Functional considerations lead us to speculate

that additional intraspecific variation in phallodeal ornamentation

occurs because the phallodeum serves both reproductive and excre-

tory roles. In individuals with well-developed tuberosities, these can

interdigitate in situ to seemingly obstruct the cloacal lumen. We

hypothesise that in these species, at least, cloacal ornamentation

would be elaborated at times of courtship but reduced at other times.

If correct, differences in reproductive condition would need to be

taken into account in any systematic comparisons.

Our observations suggest that the pattern of major longitudinal

ridges and often also the number and position of phallodeal tuberosi-

ties or other ornamentation is mostly constant within species. The

same general pattern occurs in 1] specimens of Hypogeophis

rostratus, the largest sample of a single species that we have

examined in detail. However, detailed study of ontogenetic and

population variation is needed to test this constancy and to deter-

mine whether variations in the form of phallodeal ornamentation are

of systematic utility. Thus, future studies should attempt to increase

sample sizes for at least some species. Of the 33 species examined by

Wake (1972), her largest sample was 29 specimens of Gymnopis

proxima (Cope, 1877) whereas sample sizes for the remaining

species were low (mean = 1.7), providing little basis for assessing

variation. Wake (1972) did not discuss intraspecific variation in any

species.

Closely related species (e.g. congeners) tend to have similar

cloacal morphologies, providing a strong indication that the cloaca

will be a source of stable phylogenetic characters. For example, the

absence of a definitive colliculus or any other obvious division of the

cloaca into urodeal and phallodeal chambers is a very striking

putative synapomorphy of Dermophis and Gymnopis. These genera

have been considered closely related (e.g. Nussbaum & Wilkinson,

1989) but there are no previously reported uniquely derived

characters. Similarly, the general form of the longitudinal phallodeal

ridges and their ornamentation in Schistometopum thomense and S.

gregorii appears to offer the first known unique diagnostic character

for Schistometopum. On the other hand, congeners can sometimes

be readily distinguished by clear-cut, discrete differences in the

patterns of phallodeal ridges and topological relations in their

ornamentation.

Contrary to Wake (1972), our investigations of Uraeotyphlus

suggest that, in at least some cases, cloacal morphology may not be

species specific. Instead, it appears that some species that can be

clearly differentiated based on traditional morphological characters

have a common pattern of phallodeal ridges and ornamentation.

Species specific differences in these examples may yet be found in

the details of the form of phallodeal morphology, but additional

work is needed to test this.

In this survey we have concentrated upon the gross structural

features of the caecilian cloaca. The lumenal surface of the cloaca

appears to be also covered in many minor ridges and grooves

(striae). This micro-ornamentation may also yield useful systematic

153

data but, as with more macroscopic features, studies of this must

take into account potential intraspecific variation. In some cases,

where we have described major structures as terminating, it might be

more accurate to describe them as giving rise to, or being supplanted

by, striae. For example, in Hypogeophis rostratus, where the main

dorsolateral longitudinal ridges and their sulci ‘terminate’ anteriorly,

close to the colliculus, they more accurately continue into incon-

spicuous striae (MW, pers. obs.). These bend around the lateral

margins of the colliculus and open into channels running alongside

the main mid-dorsal urodeal ridge. We suspect this arrangement

constitutes the passage through which sperm travel from the urodeum

to the phallodeum, to be delivered to the female via the dorsolateral

sulci that are such a prominent feature of the phallus.

ACKNOWLEDGEMENTS. It is a pleasure to thank our esteemed colleague

and friend Garth Underwood for inspiring our research and for enlightening

discussions of systematics, cloacae and histology. The assistance in provision

of material of too many people to name individually has been indispensable

to this work, and is gratefully acknowledged. Thanks to Christian Klug and

Claudine Levasseur for assistance with translations, Alex Kupfer for helpful

discussions of cloacal form and function, and Harry Taylor for Fig. 10. MW

is grateful to Ron Nussbaum for fostering and encouraging his interest in

caecilian cloacae, and to David Sever for helpful discussion of amphibian

urogenital systems. This paper was improved by critiques from Barry Clarke,

Alex Kupfer, Simon Loader and Hendrik Miiller and supported in part by

NERC grants GST/02/832 and GR/9/2881, and an MRF award.

REFERENCES

Bons, J. 1986. Donnees histologiques sur le tube digestif de Typhlonectes

compressicaudus (Dumeril et Bibron, 1841) (amphibien apode). Mémoires de la

Société Zoologique de France 43: 87-90.

Duellman, W. E. & Trueb, L. 1986. Biology of amphibians. New York, 670pp.

Duvernoy, G. L. 1849. Cours d'histoire naturelle des corps organisés professé au

collége de France. Revue et magasin de Zoologie 1849: 179-189.

Exbrayat, J-M. 1991. Anatomie du cloaque chez quelques gymnophiones. Bulletin de

la Société Herpetologique de France 58: 3\-43.

1996. Croissance et cycle du cloaque chez Typhlonectes compressicaudus (Duméril

et Bibron, 1841), amphibien gymnophione. Bulletin de la Société Herpetologique de

France 121: 93-98.

Gower, D. J., Kupfer, A.. Oommen, O. V., Himstedt, W., Nussbaum, R. A., Loader,

S. P., Presswell, B., Miiller, H., Krishna, S. B., Boistel, R. & Wilkinson, M. 2002.

A molecular phylogeny of ichthyophiid caecilians (Amphibia: Gymnophiona:

Ichthyophiidae): Out of India or out of southeast Asia? Procceedings of the Royal

Society B 269: 1563-1569.

Giinther, A. C. L. G. 1864. Reptiles of British India. London, 452pp.

Hedges, S. B., Nussbaum, R. A., & Maxson, L. R. 1993. Caecilian phylogeny and

biogeography inferred from mitochondrial DNA sequences of the 12S rRNA and

16S rRNA genes (Amphibia: Gymnophiona). Herpetological Monogaphs 7: 64-76.

Himstedt, W. 1996. Die Blindwiihlen. Magdeburg, 160pp.

Largen, M. J., Morris, P. A. & Yalden, D. W. 1972. Observations on the caecilian

Geotrypetes grandisonae Taylor (Amphibia: Gymnophiona) from Ethiopia. Monitore

Zoologico Italiano, Supplemento IV 8: 185-205.

Noble, G. K. 1931. The biology of the Amphibia. New York, 577pp.

Nussbaum, R. A. 1977. Rhinatrematidae: a new family of caecilians (Amphibia:

Gymnophiona). Occasional Papers of the Museum of Zoology, University of Michi-

gan 682: 1-30.

1985. Systematics of Caecilians (Amphibia: Gymnophiona) of the family

Scolecomorphidae. Occasional Papers of the Museum of Zoology, University of

Michigan 713: 1-49.

— & Pfrender, M. E. 1998. Revision of the African caecilian genus Schistometopum

Parker (Amphibia: Gymnophiona: Caeciliidae). Miscellaneous Publications, Mu-

seum of Zoology, University of Michigan 187: 1-32.

& Wilkinson, M. 1989. On the classification and phylogeny of caecilians

(Amphibia: Gymnophiona), a critical review. Herpetological Monogaphs 3: 1-42.

Pillai, R. S. & Ravichandran, M. S. 1999. Gymnophiona (Amphibia) of India: a

taxonomic study. Records of the Zoological Survey of India, Occasional Paper 172:

1-117

154

Rathke, H. 1852. Bemerkungen uber mehrere Korpertheile der Coecilia annulata.

Archiv fiir Anatomie, Physiologie und Wissenschaftliche Medicin 1852: 334-350.

Sawaya, P. 1942. Sobre a cloaca des Siphonops. Universidade de Sao Paulo, Boletins

da Faculdade de Filosofia, Ciencias e Letras 25 (Zoologia no. 6): 3-55.

Spengel, J. W. 1876. Das Urogenitalsystem der Amphibien. I. Theil. Der anatomische

Bau des Urogenitalsystems. Arbeiten aus dem zoolog.-zootom. Institut in Wiirzburg

3: 51-114.

Taylor, E. H. 1968. The caecilians of the World. Lawrence, 848pp.

Tonutti, E. 1931. Beitrag zur Kenntnis der Gymnophionen. XV. Das Genitalsystem.

Morphologisches Jahrbuch 68: 151-292.

1933. Beitrag zur Kenntnis der Gymnophionen. XIX. Kopulationsorgane bei

weiteren Gymnophionenarten. Morphologisches Jahrbuch 72: 155-211.

Wake, M. H. 1972. Evolutionary Morphology of the caecilian urogenital system. IV.

D.J. GOWER AND M. WILKINSON

The cloaca. Journal of Morphology 136: 353-366.

—— 1998. Cartilage in the cloaca: Phallodeal spicules in caecilians (Amphibia:

Gymnophiona. Journal of Morphology 237: 177-186.

Wiedersheim, R. 1879. Die Anatomie der Gymnophionen. Jena, 101pp.

Wilkinson, M. 1990. The presence of a Musculus Retractor Cloacae in female

caecilians (Amphibia: Gymnophiona). Amphibia-Reptilia 11: 300-304.

1996. The heart and aortic arches of rhinatrematid caecilians (Amphibia:

Gymnophiona). The Zoological Journal of the Linnean Society 118: 135-150.

—— & Nussbaum, R. A. 1996. On the phylogenetic position of the Uraeotyphlidae

(Amphibia: Gymnophiona). Copeia 1996: 550-562.

——, Sheps, J. A., Oommen, O. V. & Cohen, B. L. 2002. Phylogenetic Relationships

of Indian caecilians (Amphibia: Gymnophiona) inferred from mitochondrial rRNA

gene sequences. Molecular Phylogenetics and Evolution 23: 401-407.

Bull. nat. Hist. Mus. Lond. (Zool.) 68(2): 155-163

Issued 28 November 2002

Holaspis, a lizard that glided by accident:

mosaics of cooption and adaptation in a

tropical forest lacertid (Reptilia, Lacertidae)

E.N. ARNOLD

Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 SBD.

SYNOPSIS. Holaspis is the most morphologically apomorphic lacertid taxon with 42 or more derived morphological features

arising on its exclusive lineage. Nearly all of these confer advantages in three specialised activities, or ameliorate problems

resulting from them. The activities are: climbing on the often vertical open surfaces on tree boles and branches, utilising very

narrow crevices in wood and beneath bark, and the ability, unique among lacertids, to glide from tree to tree. Although many of

the features related to these activities are likely to result from direct adaptation to the situations concerned, exaptation has been

critical in the development of gliding. Two behaviours present in the earliest lacertids have been coopted to this activity: rib

spreading associated with basking contributes to an effective aerofoil, and balance control associated with running helps maintain

appropriate posture in the air. Features originally developed in the context of crevice use also contribute to the aerofoil and a high

surface: weight ratio. So, while natural selection has moulded Holaspis for its present activities, multiple accidents of history have

also been important, as they also have in the evolution of bird flight.

INTRODUCTION

Sometimes there has been a flurry of adaptation on a lineage after a

long period of little or no obvious change. A plethora of apomorphies

may have been produced, often in association with shift into a new

and demanding niche or a succession of these. For instance, this

occurred in the lacertid lizard genus Meroles where apomorphies

accumulated in a series of increasingly extreme soft-sand environ-

ments (Arnold 1990, 1991). In other cases, not all the features that

confer performance advantage in such a selective regime necessar-

ily arose by natural selection in its context. In some instances,

features developed by natural selection in a different situation or by

some other means, and were only later coopted to a new function.

Darwin (1872) was aware of this process which was named exaptation

by Gould & Vrba (1982). Cases of exaptation are very widespread

(Arnold, 1994; Gould, 2002) and contribute to the ability of lineages

to enter new selective regimes. Usually, optimum survival in these

involves combining exaptations with new features that are built by

the new selective regime. Exaptations are typically a small propor-

tion of the necessary features, but there are examples where a

number of characters really critical to invading the new regime are

exaptations. A case in point is the aberrant lacertid genus, Holaspis,

the only member of the approximately 1700 species of Scincomorpha

known to glide regularly and effectively.

TAXONOMY AND RELATIONSHIPS

Until recently Holaspis was regarded as a single species with two

well-defined subspecies, but these are now each given species

status (Broadley, 2000) as Holaspis guentheri and H. laevis. H.

guentheri occurs in Sierra Leone, Ghana, Nigeria, Cameroon,

Congo, Uganda, Gabon and Angola, and H. /aevis in Tanzania,

southeast Congo, Malawi and Mozambique. H. laevis has six dark

longitudinal stripes on the body instead of eight and has on aver-

age fewer, larger scales comprising the semitransparent window

present in the lower eyelid which is generally rather better devel-

oped than in H. guentheri.

Within the Lacertidae, morphology indicates that Holaspis is a

member of the subfamily Eremiainae (Harris, Arnold & Thomas,

1998) and within this of the Equatorial African clade (Arnold,

1989a, b.), which is relatively basal and has a generally primitive

morphology, most of its members not differing much from members

of the generally primitive subfamilies, Lacertinae and Gallotiinae.

The Equatorial African clade is characterised by the following

combination of derived features: pineal foramen lacking; medial

area of the clavicle not markedly expanded; only one postnasal

scale; parietal scale extending laterally to the edge of parietal table

of the skull, and the tympanic scale small. All except Holaspis also

have the postorbital and postfrontal bones fused, the absence of this

condition in Holaspis being secondary (Arnold, 1989a). Among the

Equatorial clade, morphology suggests Holaspis is the sister group

of two species of Adolfus, A. africanus and A. vauereselli (Arnold

1989a). Studies of mitochondrial DNA sequence (Harris & Arnold,

pers. obs) corroborate this relationship, although with only low

bootstrap support.

MORPHOLOGY OF HOLASPIS

The following account concentrates on those characters that are

peculiar to Holaspis and derived within the Equatorial African

group, and usually within the Lacertidae as a whole. These

autapomorphies and are listed in Appendix 1. For illustrations of

living Holaspis see Schmidt, 1919 (reproduced in Arnold 1989a),

Schiotz (1960) and Branch (1998).

Holaspis are small lizards growing to a maximum of only about

53mm from snout to vent and a total length of 130mm. The whole

animal is extremely depressed, and more so than any other lacertid.

The index, head depth/ head width, measured on alcohol-preserved

specimens somewhat exceeds that found in most other flattened

lacertids (see for instance Arnold 1998a, p. 344), averaging about

0.54 when measured in adults (n = 10). This however does not give

156

Fig. 1 Head and skull of Holaspis. a. Head from above; b. Head from

side; c. Skull from above; d. Skull from side. fn frontonasal scale, fp

frontoparietal suture, pa palpebral bone, pm premaxilla, r rostral scale,

io inferior orbital foramen, so supraocular osteoderms, t triangular scale

covering area occupied by interparietal and paired frontoparietal scales

in most other lacertid lizards.

a full impression of the extent of the dorsoventral flattening, largely

because in fixed material shrinkage of the jaw muscles pulls the

kinetic skull into its most retracted position in which the vertical

extent is greatest (Arnold 1998a). Also, unlike other lacertids, the

whole of the limbs and tail are depressed in Holaspis.

HEAD. The parietal area of the head (Fig. la, b) is flat and

unarched and the snout is flattened above, being wedge-shaped in

lateral view. The rostral shield is large, extending far on to the top of

the snout and contacting the frontonasal scale very broadly. The

nostrils are placed on the sides of the snout and are set well back

from its tip. The area of the top of the head usually occupied by the

interparietal and paired frontoparietal scales in other lacertids is

covered in Holaspis by a single large triangular scale. The lower

eyelid has a ‘window’ composed of enlarged semi-transparent scales.

In H. guentheri these number 1—5 (mean 3.5, n = 15) while in H.

laevis there are usually 2-4 (mean 2.3, n = 8) that are sometimes

black-edged. The scales on the temporal area vary in size: dorsally

and posteriorly they are typically large and polygonal, whereas

anteriorly they are much smaller and diagonally elongated, running

backwards and downwards from behind the eye in irregular lines

that are separated by somewhat expansible hinge regions.

The low skull (Fig. 1c, d) is more delicately constructed and thin-

boned than in any other lacertid lizard and the roof of the parietal

region is so flexible in alcohol-preserved material that it can easily

be deflected downwards. As in other lacertids, comparatively im-

mobile sutures in the skull, such as that between the frontal and nasal

bones, show a considerable overlap between the elements involved,

giving a measure of rigidity in spite of the thinness of the compo-

nents. In contrast, the frontoparietal suture, one of the main sites of

Fig. 2 Scleral ossicles of left eye of lizards. a. Typical lacertid lizard; b.

Holaspis; c. Platysaurus (Cordylidae). Ossicles are numbered according

to the system of Gugg (1939); see Underwood (1970).

E.N. ARNOLD

cranial kinesis, is a relatively simple abutment without the complex

interdigitation found at this site in other lacertid lizards.

The body of the premaxilla is peculiar in forming a broad semicir-

cular boss that is convex above and supports the extensive rostral

scale. The nasal openings of the skull are situated posterior to this

boss and are extremely large. They extend backwards so that the

primary nasal cavities are broadly exposed dorsally. Of the bony

elements normally roofing the orbits of lacertid lizards, only the

palpebral bone is present in its entirety. The usual array of four

supraocular osteoderms is greatly reduced; the first being absent and

the others only present in adults, where they are limited to a narrow

medial fringe. The inferior orbital foramen is very large. Pterygoid

teeth are absent. The mandibles are slender and shallow and their

retroarticular processes are directed somewhat ventrally.

SCLERAL OSSICLES. In the eye, the scleral ossicles are reduced,

from the usual lizard number of fourteen that is present in all other

lacertids, to twelve. This is by the loss of two out of the sequence

made up of ossicles 5 to 9 (Fig. 2b). The twelve ossicles present are

so shaped and arranged that the scleral ring is incomplete peripher-

ally. Instead of extending from the area of the pupil to the vertical

equator of the eye, the ring is strongly emarginated above and below.

Dorsally this emargination is produced by the loss of the two

ossicles, their neighbours extending across the gap so formed and

overlapping only in the pupillar region. The ventral gap in the outer

part of the ring is largely a result of the peripheral, radially directed

part of ossicle 14 being missing but the peripheral sections of

ossicles | and 13 are also skewed away from the gap thus increasing

its extent.

Bopy. The neck of Holaspis is dorsoventrally flattened, with the

skin at the sides forming a prominent sharp-edged flap in many

preserved specimens that is also visible in live animals (Fig. 2,

Schigtz, 1960). The flap apparently gains some support from the

first branchial and hyoid horns of the hyoid apparatus and its edge is

sometimes marked by a longitudinally oval area of somewhat

enlarged scales. In other preserved material, in which the pharyngeal

cavity is expanded dorsoventrally, the flaps are barely apparent,

suggesting that they are homologous with the slight skin folds which

occur in this region in many lacertid lizards and which are necessary

for pharyngeal enlargement.

The body is strongly depressed and arched in transverse section,

being convex above and flat beneath. Posterior to the sternally

connected ribs, the trunk has an elongated oval outline when viewed

from above and the lateral edges of the body form distinct ridges.

The dorsal integument consists of two very different types of scaling

(Fig. 3a). Running along the vertebral region from nape to tail is a

band of enlarged, broad plates. These are arranged in two longitudi-

nal series, which are slightly staggered relative to each other. Each

plate slightly overlaps the one immediately behind it and also,

medially, the plate diagonally posterior to it in the other row. The

hinge regions between the plates allow flexibility in the vertical

plane but do not permit the plates to move much relative to each

other in the plane of the integument.

The lateral areas of the dorsal integument are made up of small

granular scales. At the broadest part of the dorsum, there are 30 to 41

of these on each side, between the vertebral and ventral plates. These

small scales often show a differentiation in arrangement between the

anterior and posterior regions of the back. On the neck and shoul-

ders, they are non-imbricate and firmly bonded together so that they

can only move slightly relative to one and other. Further back they

may gradually alter, so that beyond the sternally connected ribs the

scales are completely different in character. Here, they are lined up

in two directions: they are arranged in rows running steeply

EVOLUTION OF HOLASPIS

Fig. 3 Dorsal views of the left posterior trunk of Holaspis. a. Skin,

showing double vertebral band of enlarged scales and small lateral

scales (only three rows shown). b. Skeleton showing elongated anterior

free ribs with long cartilaginous tips; the tips usually overlap each other

to form a continuous edge to the ribs, but in this cleared and stained

specimen they have become partly separated.

posteriorly, and to a much lesser extent outwards from the vertebral

plates, and they also form transverse rows of which there are two or

three to each vertebral plate. These rows run slightly posteriorly

from their origin, but further out, they curve a little so that they run

more or less directly laterally and may turn slightly forwards before

they reach the perimeter of the dorsum (Fig. 3a). Each scale in a

transverse row strongly overlaps its neighbour on its medial flank,

but if the skin is pulled laterally, it stretches easily and extensively,

so that each scale is separated from its fellows (Fig. 4). It is then

sometimes apparent that the scales are interconnected by ‘bridges’.

These are often pigmented and not very elastic and apparently

contain alpha-keratin, as do the scales. They lie slightly below the

level of the scales themselves and fall into two groups. One series

runs approximately laterally from the posterior outer border of each

scale to insert beneath the inner border of its neighbour. The other

runs from the anterior inner border of every scale and joins it to the

posterior inner border of the scale which lies in front of it when the

skin is unstretched. These longitudinal bridges are the only ones

immediately visible in preserved material, the lateral ones being

hidden under the imbricating scales. When the skin is not stretched,

the bridges are slack and slightly folded. The regions between the

scales and their bridges are made up of soft, extensible skin,

a b

Fig. 4 Scales from right lateral skin of posterior trunk. a. Skin

unstretched, scales overlapping medially and longitudinal bridges

showing. b. Skin stretched showing lateral and longitudinal bridges and

expanded areas between the scales. The bridge system is not always

fully apparent. The arrow show direction of stretching.

157

presumably consisting largely of beta-keratin. The development of

this system of bridges shows very considerable variation among

specimens.

When the skin is stretched laterally, each scale moves in a

transverse direction, the excursion made by the outer scales being

much greater than that made by the inner ones. This results in the

originally curved transverse rows approximating more closely to a

straight line. These movements can produce at least 50% increase in

the area of skin. This ability of the skin to expand is not so highly

developed as in many snakes, but it is certainly unique among the

Lacertidae and probably among other lizard groups.

The dorsolateral skin, when unexpanded, has one or more longi-

tudinal folds on either side. The whole of the dorsal integument is

rather loosely attached to the underlying musculature by connective

tissue, as in other lacertids. The area of granular scales passes round

the sharp-edged lateral border of the body to contact the ventral

plates. These are large and arranged in six longitudinal rows, as in

many other lacertids, and are rectangular showing little imbrication.

The collar is straight-edged and again not strongly overlapping.

Holaspis has 25-26 presacral vertebrae in males and 25-27 in

females. These numbers are unexceptional for lacertids in which the

majority of species have 25—29 presacrals with extremes of 23 and

33 and show sexual difference in average number of dorsal verte-

brae. The vertebrae of Holaspis differ from those of other lacertids

in being distinctly depressed with virtually no neural crest or spine

In most lacertid lizards the dorsal ribs can be divided into three

groups: |. the thoracic ribs attached to the sternum and xiphister-

num; 2. the anterior free dorsal ribs which are unattached distally

and have prominent cartilaginous extensions at their tips; and 3. the

posterior free dorsal ribs which are usually about two-thirds the

length of the more anterior ribs and have no cartilaginous exten-

sions. In Holaspis, there are 7—8 anterior free ribs in males and 8-9

in females. They are markedly elongate compared with those of

other lacertids, being considerably longer than the thoracic ribs and

about twice as long as the posterior free dorsal ones. Their

cartilaginous extensions are also exceptionally long and are turned

backwards, each extending beneath the next posterior rib and run-

ning parallel with its own cartilaginous process (Fig. 3b). These

overlapping processes are bound together by loose connective tissue

and form a smooth border to the series of elongated ribs. It is this

border which forms the prominent edge of the body that runs slightly

ventrally and backwards to terminate just in front of the anterior

border of the hind leg. The termination is enclosed in a fold of loose

skin that connects it to the underside of the thigh.

The sternum of Holaspis has an extremely large central fontanelle

that occupies most of its area, and the scapulocoracoid plate has two

foramina compared with one in other lacertid lizards.

Holaspis is peculiar among lacertid lizards in having prominent

slips of the intercostalis scalaris muscle (Maurer 1896) running

from the tips of the anterior free ribs forwards and somewhat

inwards to insert on the upper surface of the rectus abdominis

muscle above the outer edge of the second row of ventral scales. The

muscle fibres to the more anterior free ribs form a single block but

those to the more posterior ones comprise separate slips.

TAIL. In nearly all lacertid lizards, the tail is cylindrical and at

most slightly flattened dorsoventrally at its base. It is covered by

whorls of numerous subequal scales there being two whorls to each

caudal vertebra. Deviations from this pattern are usually slight but

Holaspis differs radically. Its tail (Fig. 5) is somewhat dorsoven-

trally compressed and above has a double row of broad plates, which

is a direct continuation of the series on the body. These enlarged

scales differ from those on the back in being arranged in simple

158

Fig.5 Tail of Holaspis. a. Proximal segment from above; b. Proximal

segment from below; c. Transverse section.

lateral pairs instead of being staggered. The plates each have several

sense organs on their posterior border and, as the usual number of

sense organs per dorsal caudal scale in other lacertid lizards is one,

it is likely that the plates have replaced a number of smaller scales.

The wide double band is flanked by one or two (rarely three)

longitudinal rows of narrower scales, one row being frequent in H.

laevis and one or two in H. guentheri. The number of rows some-

times increases anteriorly and these scales are replaced by granules

on the tail base. The median part of the ventral surface of the tail is

formed by another row of wide, paired plates, again replacing

multiple small scales in other lacertid lizards.

The lateral edges of the tail are serrated and consist of a single row

of strongly modified scales. In transverse section, each of these

scales is more or less triangular, the broad base joining the tail, the

apex pointing outwards; in this plane, the lateral scales curve

downwards. Viewed from above, these scales are again approxi-

mately triangular, the point being directed obliquely backwards.

Proximally, the longitudinal axis of these scales is parallel with that

of the whole tail; distally, their anterior edges tend to be twisted

downwards so that their longitudinal section here runs backwards

and slightly upwards. Each lateral scale is capable of some move-

ment since it is connected with contiguous scales in its whorl by

flexible hinge regions. However, the motion is limited by the scale

interlocking with its anterior and posterior neighbours. On the

underside of each of these scales, parallel with and close to the

trailing edge, is a slit-shaped cavity. The anterior portion of the

following scale projects into this, giving the lateral fringes consider-

able stiffness.

LimBs. The spans of the fore and hind limbs approach equality

more closely than in any other lacertid lizard, the index, forelimb

span/hindlimb span, being 0.85 in males (n= 3), and 0.85 in females,

(n = 4) while the total range for the Lacertidae is 0.53—0.85 (Arnold

1998b).

The forelimbs are rather flattened and the single band of enlarged

scales, present on the anterior surface of the upper limb of most

lacertids, occurs in Holaspis too. However, instead of being continued

as a single band on the lower limb, it is replaced by two parallel ones,

one dorsal, the other ventral with their zig-zag line of contact forming

a forwardly directed edge that may sometimes be quite acute.

The hind leg is similarly markedly depressed and the proximal,

femoral segment has large plates above and below the leading edge;

E.N. ARNOLD

a b

Fig. 6 Right manus of lacertid lizards. a. A form frequently climbing on

steep open surfaces (Lacerta oxycephala); b. Holaspis guentheri.

only the lower series reaches the front of the crus. The greater part of

the trailing area of the hind leg is formed by a web of loose elastic

skin, which becomes taut when the leg is partly extended. This

‘patagium’ is continuous with a series of about four large sharp-

edged, sometimes interlocking, scales which make up the trailing

edge of the crus. These scales are generally similar in construction

and arrangement to those on the lateral edges of the tail

The manus and pes of Holaspis show strong development of a

syndrome of features characteristic of lacertid lizards that climb on

continuous open surfaces (Fig. 6; Arnold, 1998b) and many features

are better developed than in other forms. The longest digit is number

4 and all digits are strongly latero-mesially compressed; some digits

are flexed downwards at the articulation of phalanges | and 2 and in

most there is upward flexure at the penultimate articulation. Phalanges

are very slender, the penultimate ones being very long and markedly

curved downwards. In the manus intermediate phalanges of digits 3

and 4 are shorter than the ones bordering them and the same is true

of intermediate phalanges of digits 3 and 4 of the pes. The final

phalanx of each digit and the claw that covers it is short, deep and

recurved. The large ventral digital tendons are offset from the

articulations in the regions where digits can be abruptly flexed

downwards. The articulations within the digits, except the most

distal, are simple involving single cup and ball arrangement and the

digits are abruptly flexed in the horizontal plane, both mesially and

laterally, especially in the area of the penultimate articulation.

The manus of Holaspis has the following additional derived

features. Digits 2-5 are subequal in length, and numbers 3 and 4 are

conjoined for the length of their first phalanx. The shortening and

downward flexure of phalanx 2 digit 3 and phalanges 2 and 3 of digit

4 is much more marked than in other lacertid lizards.

Digits 3, 4 and 5 of the pes each have a lateral fringe of interlock-

ing triangular scales, which extends distally to the base of the

penultimate phalange. That on the fifth toe is continuous with the

similar scales on the trailing edge of the crus. Digits 4 and 5 also

have a similar mesial fringe.

COLOUR IN LIFE. In life, Holaspis is blue-black with several

longitudinal pale stripes on the dorsum, the two on the vertebral

plates being tinged blue posteriorly. The tail has a series of large,

light, intensely blue spots on its upper surface and its lateral fringes

are yellow, while the belly is red.

EVOLUTION OF HOLASPIS

BEHAVIOUR

Holaspis guentheri occurs especially in rain-forest situations while

H. laevis also extends into savannah. These lizards are nearly always

observed at some height on the trunks and branches of standing

trees, occurring at least up to 30m, and do not usually come down to

the ground (H. guentheri: H. Lang in Schmidt, 1919; Perret &

Mertens, 1957; Schigtz & Volsge, 1959; Laurent, 1964; Dunger,

1967; P. Agland, pers. comm. A. P. Mead, pers. comm. H. /aevis:

Barbour & Loveridge, 1928; Loveridge, 1951, 1953; De Witte,

1953; Branch, 1998; D. G. Broadley pers. comm.), although they

can occur on fallen timber (H. Lang in Schmidt, 1919). Holaspis

spp. are active hunters, constantly moving and searching and often

investigating crevices (P. Agland, pers. comm.) in which they also

frequently hide when disturbed and at night (H. Lang in Schmidt,

1919; Loveridge, 1951; Laurent, 1964; pers. obs. on captive ani-

mals). They are extremely agile, moving with ease on vertical and

overhanging surfaces (H. Lang in Schmidt, 1919). Holaspis appear

to thermoregulate and at times basks in patches of sunlight for at

least up to ten minutes (Dunger, pers comm.; P. Agland, pers

comm.). As in many other basking lacertid lizards, the body is

spread and flattened by the dorsal ribs being rotated forwards and in

Holaspis the body becomes as flat and round as a coin (Dunger pers.

comm., P. Agland pers comm.).

Holaspis is unique among lacertid lizards in being able to glide

between trees. This behaviour was first formally reported in H.

guentheri in Ghana by Schigtz & Volsge (1959) and subsequently

confirmed by P. Agland in Cameroun and A. P. Mead in Nigeria

(pers. comms). Earlier reports also provide some collaboration. C. J.

P. Ionides (quoted by Loveridge, 1955) noted that in Tanzania H.

laevis covers long distances in leaps between trees and Laurent

(1964) reported that local people in northern Angola said that H.

guentheri can fly. According to Schigtz & Volsée (1959), this lizard

starts from a head-downwards position, high on a tree trunk from

which it leaps outwards and glides steeply downwards. The trajec-

tory later becomes shallower, and just before the lizard alights, it

turns slightly upwards. For most of the glide, the lizard is orientated

with its sagittal axis along the direction of motion, but towards the

end this becomes perpendicular to it, the lizard stalling and reducing

speed by this means. In one measured leap a lizard travelled 10.5m

horizontally while dropping 9m, an overall angle of about 42° from

the horizontal. Holaspis appears capable of selecting a target before

launching itself, and of changing direction in mid-flight.

Among the H. guentheri observed by P. Agland (pers. comm.) one

glided 30m at an angle of 10—20°, another travelled 25m and a third

6m. Motion was fast and straight and again appeared to be directed.

In some cases there was an initial drop before the trajectory levelled

out but in one instance a lizard running horizontally on a branch

launched itself into the air without much fall before stabilising its

flight path. At the end of a dive animals again alighted head

upwards, landing very fast and sometimes immediately running

upwards. Holaspis clearly has the ability to maintain its belly-

downwards posture in the air with limbs spread and to change

orientation as appropriate.

FUNCTIONAL ANATOMY

In this section an assessment is made as to whether particular

morphological apomorphies of Holaspis could have evolved through

direct adaptation by natural selection in connection with one or more

of its special behaviours: frequent locomotion on very steep often

159

vertical open surfaces, use of very narrow crevices, and gliding.

Assessment is made on two criteria: 1. perceived functional benefit

of the apomorphies in the activities concerned; and 2. whether

similar apomorphies have appeared independently in other lizards

that have evolved similar behaviours. The second criterion is most

convincing if there are multiple independent origins of the apomorphy

and if these origins are correlated with appearance of the relevant

behaviour on the lineages of the taxa concerned. Even if there is a

prima facie case for functional advantage of an apomorphy in

connection with a particular behaviour, its absence in forms that

have evolved the behaviour independently raises the possibility that

it is not connected with the activity concerned. Alternatively, it may

represent one of several strategies with other taxa gaining similar

advantages in different ways.

LOCOMOTION IN TREE BOLES. The functional advantages of near-

equality in fore and hind limb spans, and of characteristic foot

architecture, in climbing on steep open surfaces has been discussed

elsewhere (Arnold 1998b). These features are particularly well

developed in Holaspis and presumably related to the abundance of

such surfaces in its environment. The unique manus features of

Holaspis suggest the forelimbs are sometimes used in parasagittal

planes (Arnold, 1998b). This may be when the lizard launches itself

from a head-downwards position on a steep surface. Extending the

forelimbs at this time would push the foreparts of the body out into

a more horizontal position, putting it closer to its orientation when

gliding and making an outward leap easier.

USE OF CREVICES. Features that confer advantages in crevice use

and the functional basis for this has already been surveyed (Arnold

1998a). Many derived features of Holaspis occur in other lacertids

that use rock crevices, having developed independently at least once

in archaeolacertas (Lacerta spp.), and in Omanosaura cyanura and

some populations of Podarcis hispanica. These forms show many

apomorphies similar to those of Holaspis although the features are

less developed than in this form, especially the degree of flattening

of the head, body and limbs. These low vertical dimensions enable

lizards to enter narrow crevices and a variety of cranial features

(Appendix 1, numbers 4, 6, 7, 8, 10 and 12) results in a deformable

skull that can be inserted into irregular spaces. Increased cranial

kinesis enables the skull to be flattened further by protraction on

entering a crevice and locked into place by subsequent retraction. As

a result of flattening of the skull, the eyes, which are large, project

well above it during normal activities and this potentially impedes

entry into crevices. However, in lacertids including Holaspis each

eye is pushed downwards as the lizard enters a crevice by contact

with the crevice roof so that its lower surface deflects the flexible

membrane crossing the greatly enlarged inferior orbital foramen.

This enables the lower part of the eye to project into the buccal

cavity, so that it can be housed within the depth of the head.

Reduction of the supraocular osteoderms increases the flexibility of

the skin over the eyes so that its geometry can alter during their

depression. Reduced overlap of collar and belly scales increase

smoothness enabling lizards to move easily both forwards and

backwards in crevices. Some or all these features are paralleled in

many non-lacertid crevice users including skinks (such as Mabuya

laevis and M. sulcata), xantusiids (Xantusia henshawi), geckos

(Afroedura) and iguanids (Sauromalus, Oplurus).

Holaspis has other features not found in other crevice-using

lacertids but present in the most extremely flattened exploiters of

rock crevices in other families, such as Platysaurus (Cordylidae)

and Tropidurus semitaeniatus (Iguaninidae, Tropidurinae) and prob-

ably functionally associated with such strong depression. Among

these is modification of the scleral ossicles, so that there is one or

160

more windows in the scleral ring (Fig. 2). These enable the eyeballs

to distort and flatten, so they can be housed in the narrow space

available within the head. Other shared features, which also contrib-

ute to low vertical dimensions, are depression of the body vertebrae

and reduction of the crests on their neural arches.

Shortening and consequent decrease in mass of the adductor

muscles associated with reduction in head height probably plays a

critical role in facilitating the evolution of this cranial morphol-

ogy. Curtailed mass reduces the power of the muscles, so a

particularly strong, thick arched parietal area of the skull is no

longer necessary to resist their action, and this also permits the

posterior skull roof to become thin and flat. Similarly the mandi-

bles are subjected to reduced forces in biting and can consequently

be more slender with smaller vertical dimensions. However, such

shortening of the muscles carries penalties in terms of reduced

efficiency in biting and prey handling (Arnold, 1998a). Change in

geometry of the skull during the retraction phase of cranial kinesis

ameliorates this effect by improving their angle of action on the

jaw and the length of their excursion. This phenomenon is promi-

nent in Platysaurus, which has an expansion area in the skin on

the anterior cheek that accommodates the changes involved in the

substantial kinetic movement. The similarly orientated hinge

regions of Holaspis, between the small scales found in this region,

indicates that its skull is similarly highly mobile, as does the

simplified fronto-parietal suture.

The downward flexion of the retroarticular process of the mandi-

ble may permit a longer and more efficient depressor mandibulae, in

spite of the flattened head, although this feature is not paralleled in

other very flattened crevice users. Other characteristics of Holaspis

could also plausibly be considered as adaptations to crevice use, but

are not repeated in functional analogues. Thus, the large plates along

the back which might possibly increase smoothness and so ease

mobility within crevices; although neither Platysurus or T.

semitaeniatus have this feature. The enlarged sternal fontanelle

could similarly be thought to increase flexibility in this region, but

Platysaurus has no fontanelle at all.

Another complex of Holaspis features may also be related to

use of crevices, specifically those beneath bark. This involves the

snout which is wedge shaped in lateral view (unlike that of rock

crevice dwellers), with the bizarre flattened boss formed from the

premaxilla, and nostrils set back from the snout tip and low on its

sides. Such features are not found even in extremely flattened

lizards using rock crevices, but they do occur in the flattened

lygosomine skink Aulacoplax, which habitually conceals itself in

the narrow interstices between the bases of the fronds of screw

pines (Pandanus spp.) (Brown and Fehlmann, 1958). This arrange-

ment may enable the skink to enlarge interstices so they are broad

enough to take the rest of the animal as it moves forwards.

Holaspis may possibly do the same when pushing beneath flexible

pieces of loose bark. The frequent presence of longitudinal

scratches on the dorsum of the head suggests this may be the case.

Fusion of the frontoparietal and interparietal scales may increase

strength and smoothness of the head surface but has no parallels

elsewhere.

GLIDING. Since Holaspis descends through the air in a controlled

way at relatively shallow angles it glides rather than parachutes.

Gliders depend on the possession of an aerofoil which extracts a lift

component as the animal moves through the air, the lift counteract-

ing the force of gravity. For gliding at shallow angles to be possible,

the ratio of surface: body weight needs to be high. Some other

gliding lizards have a specialised lift surface that provides this. In

the agamid Draco, this is formed from a membrane supported by the

E.N. ARNOLD

elongated abdominal ribs while in the gecko Ptychozoon there are

flaps attached to the sides of the belly that fold out, increasing

surface area. In Holaspis, itis the whole body that acts as an aerofoil

and some features that also confer performance advantage in using

crevices contribute to its formation. This is particularly true of

dorsoventral compression, but low ossification of the skull must

help increase the surface: weight ratio. Other features appear to be

specifically associated with gliding and are not found in crevice

dwellers, although they may occur in other gliders. Included here is

low ossification of the pectoral girdle and perhaps that of the

sternum and depression of the legs and tail. This last feature,

together with development of distinct trailing edges on the limbs,

also occurs in Draco and Ptychozoon, which do not enter very

narrow crevices. Surface area is further increased by the lateral flaps

on the neck and the webs of skin that form the trailing edge of the

proximal hind legs, both features again found in Draco and

Ptychozoon. The modified scales on the sides of the tail, on the

trailing edge of the crus and on the hind digits also increase surface

very efficiently, forming stiff lateral fringe-like extensions with

little increase in weight. They are exactly paralleled in structure and

function by scales on the hind side of the thigh and tail base in

Draco, while Ptychozoon has analogous cutaneous extensions along

the length of the tail.

Holaspis is able to produce further temporary increase in sur-

face area by lateral expansion of the abdominal region so that this

becomes almost disc-like. The increase in surface area is brought

about by the long free dorsal ribs being rotated forward around

their articulations with the body vertebrae, so that instead of being

directed diagonally backwards they project more laterally. In

Holaspis, the gain in surface area this produces is large because

the ribs are long. The overlapping flexible rib tips form a continu-

ous lateral edge to the area supported by the ribs and this maintains

its continuity and longitudinal orientation in spite of the move-

ments of the ribs themselves. The rotation of the ribs is

presumably partly brought about by the intercostal muscles, as

seems to be the case in Draco (Colbert, 1967). But it is likely that

the well-developed slips of the m. intercostalis scalaris also play a

part. As they run somewhat diagonally outwards and backwards

from the m. rectus abdominis to the rib tips, their contraction

would also help swing the ribs forwards; at the same time the ribs

would tend to bow laterally and bend distally downwards. The

contraction would also raise the m. rectus abdominis and with it

the ventral integument which is closely attached. These move-

ments would produce a more aerodynamically efficient transverse

section in which the dorsal surface was more strongly convex and

the belly flat or slightly concave.

The skin must stretch to allow for the increase in lateral area that

the rib movements produce. Its distinctive structure permits this, for

expansion occurs not only at the longitudinal lateral skin folds but

also at the extensible areas between the scales. The bridges that often

join the scales limit the direction and extent of expansion; they also

help distribute it evenly throughout the skin, discouraging wrinkling

and so contributing to a smooth surface. The looseness of the

connection between the skin and underlying structures usual in

lizards is also important in allowing skin tension to be evenly

distributed.

It is probable that the band of large broad plates in the vertebral

region also has a function in producing as good an aerofoil as

possible. As the hinge regions between the plates are virtually

inelastic, the whole area can be regarded as a single lamina which is

firmly fixed at the occiput and at the tail base. When such an

elongate lamina is stretched over a flat or convex surface, and placed

under tension, it becomes very resistant to lateral deformation. This

EVOLUTION OF HOLASPIS

effect is increased when the tension is both along and across the

lamina. It can be demonstrated by placing a strip of paper on plane

surface and putting it under longitudinal tension, after which dis-

placing the intermediate area laterally, even to a small extent,

becomes very difficult.

Such rigidity appears to be developed in the vertebral area of

Holaspis, which extends over the convex dorsum of the body.

Tension is generated by the lateral skin being pulled outwards during

rib spreading. This movement distorts the large plates and their

hinge regions slightly, so that there is a small widening and longitu-

dinal contraction of the vertebral band. As this is firmly attached at

the occiput and the tail, tension within it is thereby increased. The

slight movements of the plates exhaust the very limited internal

mobility of the band, increasing its lateral rigidity further. These

processes can be discerned in the detached dorsal skin of an alcohol-

preserved Holaspis. Lateral tension alone, produces a longitudinal

contraction of the vertebral band whereas, if it is applied when the

ends of the band are fixed to the substrate, the band becomes

laterally rigid.

The rigid vertebral band ensures that the extended lateral skin is

spread evenly on both sides of the body, again helping to avoid the

tendency of the tense skin to wrinkle. It may also act to keep the

body straight during gliding by restricting lateral bending. This

effect can be simulated by attaching a strip of adhesive paper tape

along the side of an elongate rubber balloon. When this is inflated,

the stretched wall of the balloon exerts tension on the paper strip,

which represents the vertebral band of Holaspis and the air pressure

provides support for this in an analagous manner to the body of the

lizard. A balloon modified in this way is substantially harder to bend

sideways than an unmodified one.

When the lateral skin of Holaspis is unstretched, the vertebral

band is slack and capable of rucking upwards at its hinges. This

permits the lizard a normal amount of lateral movement, when for

instance walking rather than gliding, since the band now lacks

lateral rigidity.

The surface: weight ratio (“wing’-loading) of Holaspis was roughly

assessed on the assumption the whole animal acts as an aerofoil.

Area was found by placing straightened preserved lizards belly

downwards on squared paper and tracing their outline; maximum

lateral extent of the body was then estimated by comparison with

photographs of animals basking with their bodies fully expanded,

and by stretching the lateral skin. Weight was calculated on the

assumption that live lizards weigh 10% more than alcohol preserved

ones (Colbert, 1967) The loadings for four individual adult Holaspis

varied between 0.26 and 0.37 gm/cm?. These are relatively small

figures when compared with those for Draco (Colbert, 1967). Such

low loading is probably necessary to compensate for the relatively

poor general aerodynamic shape of Holaspis.

FUNCTIONAL SIGNIFICANCE OF OTHER CHARACTERS. A minority

of derived features of Holaspis are not functionally associated

with its main distinctive behaviours The presence of a window in

the lower eyelid has developed in a wide range of small lizards

that bask directly in the sun in relatively dry microclimates

(Arnold, 1973; Greer, 1983). This means that such lizards can

reduce the extensive water loss associated with these situations by

closing their eyes but still retain vision to detect predators, pass-

ing food items etc. In agreement with this explanation, the window

is better developed in H. laevis which extends into relatively dry

savannah, than in H. guentheri which appears to be confined to

forest. Loss of pterygoid teeth in lacertids tends to correlate with

the general reduction in ossification found in Holaspis and may

be a concomitant of this.

161

EVOLUTION OF HOLASPIS

The order in which new features develop and the situations in which

they do so can often be reconstructed by examining states on side

branches on the lineage of the taxon concerned. This cannot be done

with many features of Holaspis as they have evolved within its

exclusive lineage, which by definition lacks side branches, so other

cues have to be used for these autapomorphies. However exam-

ination of the relatives of Holaspis does give some information.

Thus, a degree of climbing is widespread in lacertids as is a modest

amount of crevice use. This makes it most parsimonious to assume

these behaviours precede gliding, which is unique to Holaspis.

These activities and the morphological adaptations associated with

them are better developed in Holaspis itself. Improvement in climb-

ing modifications may possibly have begun first, as climbing steep

tree boles and branches must precede exploiting crevices in them.

Animal gliders and fliers can be stable or unstable. In stable ones,

there is a long lift surface behind the centre of gravity. This means

that, as an animal glides, any tendency to pitch in the sagittal plane

around the centre of gravity is self-correcting. In pitching, the long

posterior lift surface will rise or fall, but the air pressure produced by

forward locomotion will return it and the animal as a whole to its

original orientation. Unstable fliers with short lift surfaces behind

the centre of gravity gain in manoeuvrability but do not self-correct

and so require sophisticated neurological mechanisms to maintain

appropriate posture in the air, something that is unnecessary in stable

forms (Smith, 1952). Unsurprisingly, stable forms evolved before

unstable ones in most of the main groups of flying animals, namely

insects, pterosaurs and birds, and possibly bats too (Smith, 1952).

As might be expected from this, Holaspis is a stable glider. The

centre of gravity of preserved Holaspis appears to be just behind the

midpoint between the two pairs of legs. There is therefore a consid-

erable area of lift surface posterior to the centre of gravity, made up

of the hind body, hind limbs and tail. Experiments were conducted

with models made out of laminated cardboard and weighted to give

a wing loading and weight distribution similar to that of Holaspis.

When gently launched in the appropriate position, these glided well,

confirming that a glider of the dimensions and shape of Holaspis is

stable.

Given inherent stability, gliding ability seems to require only an

aerofoil and ability to reach and maintain an appropriate belly-down

posture with limbs slightly raised, as well as some ability to trim, at

least initially. In tree frogs Cott, (1926) found adoption of initial

posture very critical: Phrynohyas venulosa spread its limbs and

glided when dropped whereas Hyla arborea, which is morphologi-

cally similar, dropped vertically with legs flailing. It might be

expected that the ability to adopt the appropriate posture would be

confined to Holaspis among lacertids as it is the only known glider,

but when tests were carried out on a number of lacertids this

propensity was found to be widespread, being present in completely

terrestrial lizards such as Lacerta agilis and Acanthodactylus

erythrurus, as well as climbing ones (Arnold, 1989a). The wide

distribution of this ability suggests it confers advantage in another

more general context and may have arisen there. This context may

be terrestrial locomotion. Certainly running lacertids seem to have

to continuously adjust their body positions and, at some points in the

stride cycle, they may be balanced on only a single toe (Arnold

1998b), so good neurological control of posture seems to be essen-

tial in this activity.

The production of an aerofoil is likely to largely result from direct

adaptation, as many of the features of Holaspis appear to confer

advantage only in gliding. However rib spreading, like balance, is

162

coopted from an earlier activity. All lacertids, including Holaspis,

appear to spread their ribs when basking in relatively cool conditi-

ons, increasing surface area and rate of heat intake.

Permanent depression of the head, body and limbs of course also

contributes to the aerofoil and we can ask whether this is a special

feature of gliding or whether it is coopted from crevice use. As

already noted there is some phylogenetic evidence of its earlier

origin for crevice use, something that has occurred in many inde-

pendent lineages.

Modifications for gliding in Holaspis are quite extensive, several

organ systems being involved. It is therefore rather surprising that

Holaspis has not developed a more efficient aerofoil such as occurs

in Draco. However to do this would probably involve the develop-

ment of a delicate patagium or extensive lateral skin flaps. It is likely

that such structures would interfere with the lizard’s ability to enter

and move in the narrow crevices it regularly utilises. Consequently

Holaspis is restricted to using means of broadening the body that do

not project exteriorly.

As a stable glider, Holaspis is very dependent on its long tail, but

this can break easily, even close to its base where loss might make it

unstable in the air and reduce its ability to control its glide path.

Nonetheless the tail is lost and often regenerated in many individuals

(Arnold, 1984). This emphasises the importance of tail loss as an

antipredator device and suggests the cost: benefit ratio still favours

frequent tail loss in Holaspis even though locomotory costs may

well be high.

It might be thought that cases like Holaspis, where entrance into

a new life mode has been dependent on multiple exaptations, are

rare. But this phenomenon occurs in another instance where aerial

locomotion has been attained, that of birds where feathers and the

complex mechanism of wing folding arose long before gliding or

active flight (Gauthier & Gall, 2001).

ACKNOWLEDGEMENTS. [am grateful to P. Agland, D. Broadley, G. Dunger,

the late A. Loveridge, and A. P. Mead for information about the behaviour of

Holaspis in the field, and to Garth Underwood for helpful discussion. An

earlier version of this paper formed part of a D. Phil thesis submitted to the

University of Oxford. In connection with this I thank my supervisors, the late

A. J. Cain and the late N. Tinbergen, and the Scientific Research Council of

the United Kingdom for providing funding, 1963-1966.

REFERENCES

Arnold, E. N. 1973. Relationships of the Palaearctic lizards assigned to the genera

Lacerta, Algyroides and Psammodromus (Reptilia: Lacertidae). Bulletin of the

British Museum (Natural History) 25: 289-366.

1984. Evolutionary aspects of tail shedding in lizards and their relatives. Journal

of Natural History 18: 127-169

1988. Caudal autotomy as a defense. In C. Gans & R. B. Huey (eds) Biology of the

Reptilia 16B: Defense and Life History. Alan R, Liss, New York.

1989a. Systematics and adaptive radiation of Equatorial African lizards assigned

to the genera Adolfus, Bedriagaia, Gastropholis, Holaspis and Lacerta (Reptilia:

Lacertidae). Journal of Natural History 23: 525-555.

1989b. Towards a phylogeny and biogeography of the Lacertidae: relationships

within and an Old-World family of lizards derived from morphology. Bulletin of the

Natural History Museum London (Zoology) 55: 209-257.

1990. Why do morphological phylogenies vary in quality? An investigation based

on the comparative history of lizard clades. Proceedings of the Royal Society of

E.N. ARNOLD

London B 240: 135-172.

1991. Relationship of the South African lizards assigned to Aporosaura, Meroles

and Pedioplanis (Reptilia: Lacertidae). Journal of Natural History 25: 783-807.

1994. Investigating the origins of performance advantage: adaptation, exaptation

and lineage effects. In P. Eggleton & R. Vane-Wright (eds) Phylogenetics and

Ecology. Linnean Society of London and Academic Press, London. Pp. 123-168.

1998a. Cranial kinesis in lizards. Variations, uses and origins. Evolutionary

Biology 30: 323-357.

1998b. Structural niche, limb morphology and locomotion in lacertid lizards

(Squamata, Lacertidae); a preliminary survey. Bulletin of the Natural History Mu-

seum London (Zoology) 64: 63-89.

Barbour, T. & Loveridge, A. 1928. A comparative study of the herpetological faunae

of the Uluguru and Usumbara Mountains, Tanganyika Territory with descriptions of

new species. Memoirs of the Museum of Comparative Zoology 50: 84-265.

Branch, W. R. 1998. Field Guide to Snakes and Other Reptiles of Southern Africa.

Struik, Cape Town.

Broadley, D. 2000. Lacertidae. Holaspis laevis (Werner, 1895). Eastern serrate-toed

tree lizard. African Herp News 31: 13-14

Brown, W. C. & Fehlmann, A. 1958. A new genus and species of arboreal lizards from

the Palau islands. Occasional Papers, Natural History Museum, Stanford University

6: 1-7.

Colbert, E. H. 1967. Adaptations for gliding in the lizard Draco. American Museum

Novitates 2283: 1-20.

Cott, H. B. 1926. Observations on the life-habits of some batrachians and reptiles from

the lower Amazon: and a note on some mammals from Marajo island. Proceedings

of the Zoological Society of London 1926: 1159-1178.

Darwin, C. 1872. On the Origin of Species. 6" edition. John Murray, London.

De Witte, G. F. 1953. Exploration du Parc National de |’ Upemba 6: Reptiles. Brussels.

Dunger, G. T. 1967. The lizards and snakes of Nigeria, part 2: The Lacertids of Nigeria.

Nigerian Field 32: 117-130.

Gauthier, J. & Gall, L. F. (eds) 2001. New Perspectives on the Origin and Early

Evolution of Birds. Peabody Museum, New Haven, Connecticutt.

Gould, S. J. 2002. The Structure of Evolutionary Theory. Belknap, Harvard.

— & Vrba, E. 1982. Exaptation —a missing term in the science of form. Paleobiology

8: 4-15.

Greer, A. E. 1983. On the adaptive significance of the reptilian spectacle: the evidence

from scincid, teiid and lacertid lizards. In: A. G. J. Rhodin & K. Miyata (eds).

Advances in Herpetology, Essays in Honor of Ernest E. Williams. Museum of

Comparative Zoology, Cambridge, Massachusetts. Pp.213—221.

Gugg, W. 1939. Der Skleralring der plagiotremen Reptilien. Zoologische Jahrbiicher,

Abteilung fiir Anatomie 65: 339-416.

Harris, D. J., Arnold, E. N. & Thomas, R. H. 1998.Relationships of lacertid lizards

(Reptilia: Lacertidae) estimated from mitochondrial DNA sequences and morphol-

ogy. Proceedings of the Royal Society of London B 265: 1939-1948.

Laurent, R. F. 1964. Reptiles et amphibiens de I’ Angola. Companhia de Diamantes de

Angola: Publicacoes Culturais 67: 1-165.

Loveridge, A. 1951. On reptiles and amphibians from Tanganyika collected by C. J. P.

Ionides. Bulletin of the Museum of Comparative Zoology, Harvard 106: 175-204.

1953. Zoological results of a fifth expedition to East Africa III: Reptiles from

Nyasaland and Tete. Bulletin of the Museum of Comparative Zoology, Harvard 110:

143-487.

— 1955. On a second collection of reptiles and amphibians taken in Tanganyika

Territory by C. J. P. lonides. Journal of the East Africa Natural History Society 22:

168-198.

Maurer, F. 1896. Die ventrale Rumpfmuskulatur einiger Reptilien. Einer vergleichender-

anatomische Untersuchungen. Festschrift ftir Gegenbaur I: 183-256.

Perret, J. L. & Mertens, R. 1957. Etude dune collection herpétologique faite au

Cameroun de 1952 4 1955. Bulletin de I’ Institut Francais d’Afrique Noire 19: 548—

601.

Schigtz, A. 1960. Vestafrikas flyvende firben. Naturens Verden, July 1960.

& Vols¢e, H. 1959. The gliding flight of Holaspis guentheri Gray, a West African

lacertid. Copeia 1959: 259-260.

Schmidt, K. P. 1919. Contributions to the herpetology of the Belgian Congo based on

the collection of the American Congo Expedition 1909-1915. Part I: Turtles,

crocodiles, lizards and chameleons; with field notes by Herbert Lang and James P.

Chapin. Bulletin of the American Museum of Natural History 39: 385-624.

Smith, J. Maynard. 1952. Importance of the nervous system in evolution of animal

flight. Evolution 6: 127.

Underwood, G. L. 1970. The eye. In Gans, C. & Parsons, T. S. (eds). Biology of the

Reptilia 2: 1-97.

EVOLUTION OF HOLASPIS

Appendix 1

Derived features of Holaspis not found in immediate relatives in the

paraphyletic genus Adolfus. Most features are unique in the Lacertidae

as a whole and these are denoted by *. Separate postorbital and

postfrontal bones are primitive in the Lacertidae but fusion is the

usual condition in the African Equatorial group and separation in

Holaspis is a reversal (Arnold, 1989a). Most features appear to

confer a performance advantage in one or more of the characteristic

behaviours of Holaspis or ameliorate a problem associated with

them. The behaviours concerned are designated as follows: L —

locomotion on steep surfaces, C — use of crevices, G — gliding.

Brackets indicate a relatively minor role.

Proportions

1. Head, body, limbs and tail extremely depressed*

2. Snout sharply wedge-shaped in lateral view*

3. Fore and hind limbs approach equality in length*

Skeleton and musculature

4. Skull light and very thin-boned with some

deformability*

. Premaxilla forming a large semicircular boss*

6. Nasal openings of skull very large and widely

expose primary nasal chambers

7. Fronto-parietal suture a simple abuttment, not strongly

interdigitated*.

8. Postorbital and postfrontal bones separate

9. Supraocular osteoderms very reduced*

10. Inferior orbital foramen extremely large

11. Pterygoid teeth absent

12. Increased cranial kinesis

13. Ring of scleral ossicles reduced to twelve and

emarginated above and below*

14. Retroarticular process of mandible directed

somewhat ventrally*

15. Dorsal vertebrae depressed with very reduced neural

spines*

16. Anterior free ribs elongated with long cartilagenous

extensions at their tips*

17. Coracoid plate with an extra fontanelle*

18. Sternal fontanelle very large*

19. M. intercostalis scalaris well developed, consisting of

slips originating on tips of anterior free dorsal ribs

(

C(G)

(ele)

(KR (Gi (@liar fel ial (rer

20.

Pie

22:

23.

and running forwards and medially to insert on upper

surface of m. rectus abdominis, above outer margins

of second row of ventral scales*

Manus and pes have syndrome of features associated

with climbing on continuous open surfaces very

pronounced*.

Length and downward curvature of penultimate

phalanges of digits better developed than in other

lacertids*

Digits 2-5 of manus subequal in length*

In manus, shortening and downward flexure of phalanx

2 of toe, 3 and phalanges 2 and 3 of toe 4, very

pronounced*

External features

24.

2A:

26.

278

28.

phe).

Rostral scale very large, extending on to top of snout

with broad frontonasal contact*

Nostrils set back, on sides of snout*

Interparietal and paired frontoparietal scales all

replaced by a single triangular scale*

A window in the lower eyelid made up of 1—5 enlarged

semitransparent scales

Temporal scales differentiated with anterior ones

arranged in diagonal lines*

Neck with sharp-edged flap on each side when

pharynx not expanded*

. Cross section of body convex above and flat below

. A double series of very large flat scales along

vertebral region of body*

. Dorsal scales on sides of posterior trunk laterally

expandable*

. Lateral dorsal scales on posterior trunk sometimes

joined by a system of bridges*

. Collar and belly scales with very reduced imbrication

. Tail with two longitudinal rows of broad enlarged

scales above and below, the former with multiple

sensory pores*

Tail with lateral fringes of interconnected pointed scales*

. Two rows of large scales on front of forelimbs*

. A patagium behind the knee*

. A row of flat triangular scales on trailing edge of crus*

. Second and third fingers of manus conjoined at base*

. Digits 3-5 of pes with a fringe of interlocking

pointed scales*

. Distinctive colouring*

163

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