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Amphibian and Reptile Conservation 4(1):3-11.

DOI: 10.151 4/journal. arc. 004001 5 (1504KB PDF)

Crocker Range National Park, Sabah, as a refuge for

Borneo’s montane herpetofauna

INDRANEIL DAS 1

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

Abstract.— Crocker Range National Park in Sabah (East Malaysia), northern Borneo, is an exceptional area for

herpetological diversity. Inventories of the Park are incomplete, but show high diversity, as well as regional

endemicity shared with the adjacent and more well-known Gunung Kinabalu National Park. The montane

ecosystem of the Range offers refuge for a number of rare herpetofaunal taxa, including Stoliczkia borneen-

sis, Rhabdophis murudensis, Oligodon everetti, Philautus bunitus, Ansonia anotis, Sphenomorphus aes-

culeticola, and undescribed species of squamates of the genera Sphenomorphus and Gongylosoma. The 59

species of amphibians and 45 species of reptiles now recorded from the Range represent 39 and 16.2 per cent

of the total Bornean amphibian and reptile fauna, respectively. The high levels of deforestation of the sur-

rounding regions of Borneo, particularly lowland rainforests, highten the importance of protection of primary

forests of northern Borneo’s Crocker Range.

Key words. Crocker Range National Park, Sabah, Malaysia, herpetofauna, conservation

Citation: Das, Indraneil. 2006. Crocker Range National Park, Sabah, as a refuge for Borneo’s montane herpetofauna. Amphib. Reptile Conserv. 4(1):3-

11 (el 5).

Introduction

Borneo, one of four major islands of the great Indo-

Malayan Archipelago (along with Sumatra, Java and

Sulawesi), is situated on the eastern edge of the Sunda

Shelf between coordinates 04° S to 07° N and from

109-119° E. It is the second largest tropical island in the

world (after New Guinea), covering a land area of approx-

imately 743,380 sq km. During the Pleistocene glaciation,

sea levels fell between 120-200 m below current levels,

uniting the islands of the Sundas (Morley and Flenley

1987). Palynological evidence reveals that during the last

glacial maxima, upland plant species moved down, in

response to temperature changes (Flenley 1997; Newsome

and Flenley 1988).

Vegetational zonation for Borneo is arguably best

known from Gunung Kinabalu (Kitayama 1991), the north-

ern edge of Crocker Range, which has a largely intact

vegetation. At about 1,200 m is the upper boundary of low-

land rainforest, where the majority of emergent trees,

comprises primarily the dipterocarps, disappear from the

canopy (Beaman and Beaman 1998). The lower montane

forest is five-layered, lacking emergents. The upper limit of

the lower montane forest is 2,000-2,350 m, that of the upper

montane forest, between 2,800-3,000 m. The upper mon-

tane forest has a dense herbaceous layer. The upper limit of

the lower subalpine coniferous forests is 3,400 m, which is

sparse in undergrowth and lower in height. Unfortunately,

not much is known of the ecological distribution of the

montane fauna within these altitudinal ranges and even less

so of their conservation status. Montane regions, particular-

ly ranges at 1,200 m above sea level, because of their

Paleohistory, have been centers for speciation and

endemism. Because of the inaccessible nature of montane

regions in terms of logistics, these have also remained one

of the least known, and most generalizations stem from

studies conducted in Gunung Kinabalu, the highest moun-

tain in Borneo (see MacKinnon et al. 1996).

Adjacent to the Gunung Kinabalu National Park is the

Crocker Range National Park, although the Kinabalu region

is geologically and floristically part of the same range.

Situated in northwestern Sabah, this is the largest protected

area in East Malaysia, covering an area of 1,399 sq km. The

Park is named for William Maunder Crocker (7-1899), a

British administrator with the Rajah Brooke’s Sarawak

Civil Service, who introduced British administrative prac-

tice in what was then British North Borneo (now the

Malaysian State of Sabah). The altitudinal variation of this

Park is remarkable, in rising from near sea level to 1,670 m

and extending from the base of Gunung Alab to the town of

Tenom. The higher slopes are dominated by moss forests

and by a profusion of rhododendrons and orchids. A gener-

al description of the site is in Briggs (1997:68). Preliminary

studies on the herpetofauna of the Crocker Range National

Correspondence. 1 Email: idas@ibec.unimas.my

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December 2006 I Volume 4 I Number 1 I el 5

Indraneil Das

Figure 1. Map of Borneo, showing the location of Crocker Range National Park, Sabah. Map generated with the MICRODEM map-

ping program written by Peter Guth of the U.S. Naval Academy, using the GTOPO30 data set and edited by the author using

Photoshop version 6.0.

DOI: 10.151 4/journal.arc.004001 5g001

Park, at low elevations (290-410 m) have been conducted

by Tan (1992), resulting in the discovery of new species by

Inger (1989) and in general ecological studies of amphib-

ians by Inger and Stuebing (1992). As predicted by Inger

(1966) and Inger and Stuebing (1989), the fauna of both

Sabah and of Borneo had continued to grow through new

collections and better laboratory and field techniques. An

assessment of the herpetological biodiversity of Crocker

Range, Sabah, was conducted 2000-2001, in order to gath-

er baseline data on species occurrence and habitat use. The

present manuscript, written in 2001, was delayed in press,

and two subsequent field collections from the Crocker

Range have now been published- Ramlah et al. (2001) and

Hee et al. (2004) both reported anuran amphibians collected

from the Range. Their lists have been included in the pres-

ent inventory.

Methodology

Field work was conducted between the years 1999-2001, dur-

ing both the dry and wet months. Collecting techniques

included netting for aquatic amphibians (adults as well as the

larval stages), and “cruising” collection, including walking

along forest trails or streams at all times of the day, and par-

ticularly after dusk, following evening showers. Potential

microhabitats (e.g., under fallen trunks and branches and but-

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December 2006 I Volume 4 I Number 1 I e15

Crocker Range National Park

Table 1. Checklist of the herpetofauna of Crocker Range (the National Park and associated lowlands).

Amphibians

Bufonidae

Ansonia anotis Inger, Tan & Yambun, 2001

Ansonia hanitschi Inger, 1960

Ansonia leptopus (Gunther, 1872)

Ansonia longidigita Inger, 1960

Ansonia spinulifer (Mocquard, 1 890)

Bufo asper Gravenhorst, 1 829

Bufo juxtasper Inger, 1964

Laptop hryne borbonica (Kuhl & van Hasselt, 1 827)

Pedostibes maculatus (Mocquard, 1890)

Pedostibes rugosus Inger, 1958

Megophryidae

Leptobrachella baluensis Smith, 1931

Leptobrachella parva Dring, 1983

Leptobrachium montanum Fischer, 1885

Leptolalax cf. gracilis (Gunther, 1872)

Leptolalax cf .pictus Malkmus, 1992

Megophrys nasuta (Schlegel,1858)

Megophrys cf. kobayashii Malkmus & Matsui, 1997

Microhylidae

Chaperina fusca Mocquard, 1 892

Kalophrynus heterochirus (Boulenger, 1900)

Kalophrynus pleurostigma Tschudi, 1838

Kalophrynus subterrestris Inger, 1966

Kaloula pulchra Gray, 1831

Metaphrynella sundana (Peters, 1867)

Microhyla borneensis Parker, 1926

Ranidae

Fejervarya limnocharis (Wiegmann, 1835)

Huia cavitympanum (Boulenger, 1893)

Ingerana baluensis (Boulenger, 1896)

Limnonectes finchi (Inger, 1966)

Limnonectes ingeri (Kiew, 1978)

Limnonectes kuhlii (Tschudi, 183 8)

Limnonectes leporinus (Andersson, 1923)

Limnonectes palavanensis (Boulenger, 1894)

Meristogenys kinabaluensis (Inger, 1966)

Meristogenys orphnocnemis (Matsui, 1986)

Meristogenys poecilus (Inger & Grids, 1983)

Meristogenys whiteheadi (Boulenger, 1887)

Occidozyga baluensis (Boulenger, 1896)

Rana erythraea (Schlegel, 1837)

Rana hosii Boulenger, 1891

Rana luctuosa (Peters, 1871)

Rana raniceps (Peters, 1871)

Rana signata (Gunther, 1 872)

Staurois latopalmatus (Boulenger, 1887)

Staurois natator (Gunther, 1858)

Staurois tuberilinguis Boulenger, 1918

Rhacophoridae

Nyctixalus pictus (Peters, 1871)

Philautus aurantium Inger, 1989

Philautus bunitus Inger, Stuebing & Tan, 1995

Philautus hosii (Boulenger, 1895)

Philautus mjobergi Smith, 1925

Continued on page 007.

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Indraneil Das

Plate 1. A view of forests of the Crocker Range National Park at 16th Mile, on the Papar-Keningau Pass.

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Plate 2. Megophrys nasuta.

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Plate 3. Nyctixalus pictus.

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Plate 4. Staurois natator.

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Plate 5. Limnonectes palavanensis.

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December 2006 I Volume 4 I Number 1 I e15

Crocker Range National Park

Table 1. Continued.

Amphibians

Philautus petersi (Boulenger, 1900)

Polypedates leucomystax (Gravenhorst, 1 829)

Polypedates macrotis (Boulenger, 1891)

Polypedates otilophus (Boulenger, 1893)

Rhacophorus angulirostris Ahl, 1927

Rhacophorus baluensis Inger, 1954

Rhacophorus everetti Boulenger, 1 894

Rhacophorus gauni (Inger, 1966)

Rhacophorus pardalis Gunther, 1858

Reptiles

Agamidae

Bronchocela cristatella (Kuhl, 1 820)

Draco haematopogon Boie in: Gray, 1831

Phoxophrys borneensis Inger, 1960

Phoxophrys cephalum (Mocquard, 1 890)

Eublepharidae

Aeluroscalabotes felinus (Gunther, 1 864)

Gekkonidae

Cosymbotus platyurus (Schneider, 1792)

Cyrtodactylus baluensis (Mocquard, 1890)

Cyrtodactylus matsuii Hikida, 1 990

Scincidae

Apterygodon vittatus Edeling, 1864

Mabuya sp.

Sphenomorphus sp.

Tropidophorus mocquardii Boulenger, 1894

Colubridae

Ahaetulla prasina (Boie, 1827)

Asthenodipsas laevis (Boie, 1 827)

Asthenodipsas malaccanus Peters, 1864

Amphiesma flavifrons (Boulenger, 1887)

Amphiesma saravacense (Gunther, 1872)

Calamaria leucogaster Bleeker,1860

Calamaria suluensis Taylor, 1922

Coelognathus flavolineatus (Schlegel, 1827)

Gongylosoma baliodeirum (Boie, 1827)

Gongylosoma longicauda (Peters, 1871)

Gongylosoma sp.

Gonyophis margaritatus (Peters, 1871)

Hydrablabes periops (Gunther, 1 872)

Lepturophis albofuscus (Dumeril, Bibron & Dumeril, 1854)

Lycodon effraenis Cantor, 1 827

Lycodon subcinctus Boie, 1 827

Oligodon everetti Boulenger, 1 893

Pareas nuchalis (Boulenger, 1900)

Psammodynastes pulverulentus (H. Boie in F. Boie, 1827)

Pseudorabdion albonuchalis (Gunther, 1 896)

Ptyas fusca (Gunther, 1858)

Rhabdophis chrysargos (Schlegel, 1 827)

Rhabdophis conspicillatus (Gunther, 1 872)

Rhabdophis murudensis (Smith, 1925)

Sibynophis geminatus (Boie, 1826)

Sibynophis melanocephalus (Gray, 1825)

Continued on page 009.

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December 2006 I Volume 4 I Number 1 I e15

Plate 6. Rhacophorus everetti. Plate 7. Meristogenys kinabaluensis.

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Plate 8. Meristogenys whiteheadi.

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Plate 9. Rana hosii.

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Plate 10. Leptophryne borbonica.

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Plate 12. Phoxophrys cephalum.

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Plate 1 1 . Phoxophrys borneensis.

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Plate 13. Aeluroscalabotes felinus.

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December 2006 I Volume 4 I Number 1 I e15

Crocker Range National Park

Table 1. Continued.

Colubridae

Stoliczkia borneensis Boulenger, 1899

Crotalidae

P arias sumatranus (Raffles, 1 822)

Popeia sabahi (Regenass & Kramer, 1981)

Trimeresurus borneensis (Peters, 1872)

Tropidolaemus wagleri Wagler, 1830

Elapidae

Calliophis intestinalis (Laurenti, 1768)

Ophiophagus hannah (Cantor, 1836)

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Table 2. Geographical statistics for Borneo. *Total land area figures for Indonesia and Malaysia represent only the sum of

the Bornean components (Brunei Darussalam, Malaysia, and Indonesia). Data from Smythies and Davison (1999:6).

Land

Area

(km 2 )

Human

Population

(1990)

Population

Density

(km 2 )

Forested

Area (km 2 ) in

1990

Percent

Forest

Cover

*Brunei Darussalam

5,760

300,000

52.1

4,360

75.7

*Malaysia

198,160

3,527,200

17.8

134,214

67.7

Sabah

73,710

1,808,800

24.5

44,367

60.2

Sarawak

124,450

1,718,400

13.8

89,847

72.2

Indonesia

539,460

9,096,000

16.9

396,100

73.4

West Kalimantan

146,760

3,228,000

22.0

87,000

59.3

Central Kalimantan

152,600

1,396,000

9.1

111,100

72.8

South Kalimantan

37,660

2,597,000

69.0

8,000

21.2

East Kalimantan

202,440

1,875,000

9.3

180,000

88.9

Total

743,380

12,923,200

17.4

534,674

71.9

DOI: 1 0.1 51 4/journal. arc.004001 5t002

tresses of tree trunks) were searched. Data on specimens taken

from systematic institutions have also been collated. These

include the Natural History Museum, London; Field Museum

of Natural History, Chicago; Zoological Museum, Gunung

Kinabalu National Park Headquarters; “Borneensis

Collection” of Universiti Malaysia Sabah, Kota Kinabalu; and

the Sabah State Museum, Kota Kinabalu.

Data recorded for each capture include species, sex, stage

of growth, and reproductive condition. Voucher specimens

were retained to verify identification and eventual deposition

in appropriate systematic institutions. Dietary and microhabi-

tat data was recorded in standard pro forma. All species and

colour morphs were photographed in life using color slide

transparency film, for use in talks, field manuals, and for pro-

duction of publicity material.

Results and discussions

The known amphibian fauna includes the families Bufonidae

(ten species), Megophryidae (seven species), Microhylidae

(seven species), Ranidae (21 species), and Rhacophoridae (14

species). The reptile fauna recorded thus far includes

Agamidae (four species), Eublepharidae (one species),

Gekkonidae (three species), Scincidae (four species),

Colubridae (27 species), Crotalidae (four species), and

Elapidae (two species). Table 1 lists the herpetofauna of the

Crocker Range as known at present.

As may be expected, a large number of species are exclu-

sively montane in distribution. These include Ansonia anotis,

A. hanitschi, A. longidigita, Leptobrachella baluensis, L.

parva, Leptobrachium montanum, Leptolalax cf. pictus,

Kalophynus subterrestris, Huia cavitympanum, Ingerana

baluensis , Meristogenys kinabaluensis, M. orphnocnemis, M.

poecilus, M. whiteheadi, Rana signata, Philautus bunitus, P.

petersi, Rhacophorus angulirostris, R. baluensis, R. everetti,

and R. gauni, among amphibians. A few widespread species

occur in the lowlands of the Range, including the human-com-

mensal, Kaloula pulchra. The number and proportion of

reptiles that are essentially montane at this site seemed slight-

ly lower: Draco haematopogon, Phoxophrys borneensis , P.

cephalum, Cyrtodactylus baluensis, C. matsuii,

Sphenomorphus sp., Tropidophorus mocquardii, Amphiesma

saravacense, Stoliczkia borneensis, and Popeia sabahi. On

the other hand, there were relatively more lowland species,

including human commensals among the reptiles, and these

include: Bronchocela cristatella, Aeluroscalabotes felinus,

Cosymbotus platyurus, Apterygodon vittatus, Mabuya sp.,

Ahaetulla prasina, and Coelognathus flavolineatus.

Of the ecological types (habitat + use of diel time) repre-

sented among the amphibian fauna, 36 are exclusively riparian

and/or utilize riparian habitats for breeding and 23 are non-

riparian. All are active at night, and some (including Staurois

latopalmatus and Ansonia longidigita) also found abroad dur-

ing the day. Among the reptiles, only four species can be

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December 2006 I Volume 4 I Number 1 I e15

Indraneil Das

Plate 14. Amphiesma saravacense.

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Plate 15. Sphenomorphus sp.

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Plate 16. Stoliczkia borneensis.

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Plate 17. Logging in the lowlands of the Crocker Range.

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classified as riparian, the rest non-riparian. The reptile fauna of

the Range could also be divided into a diurnal community (19

species) and a nocturnal one (25 species); the activity patterns

of a few (e.g., the sit-and-wait viperid snakes, as well as their

non-venomous colubrid mimic, the so-called Mock Viper,

Psammodynastes pulverulentus ) are difficult to classify into

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December 2006 I Volume 4 I Number 1 I e15

Crocker Range National Park

either of these two categories. Divided into categories based on

microhabitat use, 17 were exclusively arboreal, 24 primarily

terrestrial, one primarily fossorial, and three aquatic.

A number of rare taxa are known from the Range. These

include the third specimen known of the montane colubrid

snake, Stoliczkia borneensis, hitherto known only from

Gunung Kinabalu and Trus Madi (and most recently, from

Sarawak’s Gunung Murud); Oligodon everetti, also known

solely from the Gunung Kinabalu massif; and Rhabdophis

murudensis, known from Gunung Murud, to the south of

Crocker Range. Additional specimens of a Crocker Range

frog endemic, Philautus bunitus, were collected. New species

collected from the range include a semi-fossorial skink of the

genus Sphenomorphus and the colubrid snake of the genus

Gongylosoma. Another species of snake collected, Popeia

sabahi, was until recently referred to the mainland Asian pop-

ulation of Trimeresurus popeiorum. The 59 species of

amphibians and 45 species of reptiles recorded to date from

the Range represent 39 and 16.2 percent of the total Bornean

amphibian and reptile fauna, respectively.

The high levels of deforestation of countries within

Borneo (excluding Brunei Darussalam; see Das 1994) are a

cause for concern (Primack and Hall 1992; Table 2). Most of

the productive forests of East Malaysia, for instance, have

either been already logged or placed under logging conces-

sions (MacKinnon et al., 1996:398).

The uncertain future of tropical rainforests of Borneo in

the long term places great importance of protection of mon-

tane forests of northern Borneo, such as the Crocker Range of

Sabah, for the survival of biodiversity.

Acknowledgments. — I thank Sabah Parks, and its

Scientific Officer, Jamili Nais for permission and facilities to

work in the Crocker Range National Park. Collections from the

Park were made under permit number TS/PTD/5/5Jld. 14(76).

Field work was supported by a research grant (UNIMAS

192/99 [4]) administered by Universiti Malaysia Sarawak. I

thank Prof. Ghazally Ismail, former Deputy Vice Chancellor,

UNIMAS, and Datuk Lamri Ali, Director of Sabah Parks for

invitation to participate in the Crocker Range Scientific

Expedition (1999); Fatimah Abang and Andrew Alek Tuen,

successive Directors at the Institute of Biodiversity and

Environmental Conservation (UNIMAS), for support and

facilities, and colleagues, past and current, at IBEC (Stuart

James Davies, and Nicolas Pilcher) for support. For field com-

panionship, I thank Christopher Cowell Austin, Heok Hui Tan,

and Kelvin Kok Peng Lim.

For permission and facilities to examine specimens under

their care, I thank the staff of the Field Museum of Natural

History, Chicago (Robert Frederick Inger, Alan Resetar, and

Cassandra Redhed); Sabah Parks Zoological Museum,

Gunung Kinabalu National Park Headquarters (Jamili Nais

and Maklarin Fakim); Sabah State Museum, Kota Kinabalu

(Anna Wong), and the Borneensis Collection of Universiti

Malaysia Sabah, Kota Kinabalu (Maryati Mohammed, Ahmed

Sudin, and Fucy Kimsui). Gary Geller, Jet Propulsion

Faboratory, National Aeronautics and Space Administration,

helped generate the base map of Borneo.

Finally, I’d like to thank Aaron Bauer and Fee Grismer

for comments on the manuscript.

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Manuscript received: 18 February 2002; Accepted: 21 July 2004;

Published: 26 December 2006

Amphib. Reptile Conserv. | http://www.herpetofauna.org 011

December 2006 I Volume 4 I Number 1 I e15

Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any

medium, provided the original author and source are credited.

Amphibian and Reptile Conservation 4(1):1 7-21 .

DOI: 10. 151 4/journal. arc. 004001 7 (7300KB PDF)

A Brazilian anuran (Hylodes magalhaesi:

Leptodactylidae) infected by Batrachochytrium

dendrobatidis : a conservation concern

L. F. TOLEDO 15 , C. F. B. HADDAD 1 , A. C. O. Q. CARNAVAL 2 ’ 3 , AND F. B. BRITTO 4

l Departamento de Zoologia, Institute) de Biociencias, Unesp, Rio Claro, Sao Paulo, Caixa Postal 199, CEP 13506-970, BRAZIL 2 The Field

Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA 3 Museum of Vertebrate Zoology, Valley Life Science Building, University

of California, Berkeley, California 94720, USA 4 Depart amento de Biologia, Instituto de Biociencias, Unesp, Rio Claro, Sao Paulo, Caixa Postal

199, CEP 13506-970, BRAZIL

Abstract.— Several studies have associated the chytrid fungus Batrachochytrium dendrobatidis with anuran

population declines worldwide. To date, the fungus has been found in Africa, the Americas, Australia, and

Europe. However, it has never been reported to occur in the Atlantic forest or Brazil. Based on morphologi-

cal, histological, and molecular data, we encountered evidence of B. dendrobatidis infection in a high-altitude

stream-dwelling Brazilian anuran species, Hylodes magalhaesi (Leptodactylidae). One population

(Municipality of Camanducaia, State of Minas Gerais) was surveyed from 2001 to 2005. Tadpoles lacking teeth

were observed and collected in 2004. Histological and molecular analyses identified infection by B. dendro-

batidis. Although infected tadpoles seem nowadays to co-exist with the disease, our results are alarming due

to the highly endangered situation of the Brazilian Atlantic forest and its fauna. Effects of the chytrid infec-

tion on the studied population are still unknown. Further investigations are needed to provide information on

its distribution in relation to other populations of H. magalhaesi.

Key words. Batrachochytrium dendrobatidis, Hylodes, anuran decline , conservation , Atlantic forest , Brazil

Citation: Toledo, L. F., Haddad, C. F. B., Carnaval, A. C. O. Q., and Britto, F. B. 2006. A Brazilian anuran (Hylodes magalhaesi : Leptodactylidae) infect-

ed by Batrachochytrium dendrobatidis : a conservation concern. Amphib. Reptile Conserv. 4(1):17-21(e17).

Introduction

Brazil currently figures as the most species-rich country in the

world with regard to amphibian diversity (Young et al. 2004;

Silvano and Segalla 2005), encompassing two biomes of con-

servation concern: the Cerrado and the Atlantic forest (Myers

et al. 2000). Notwithstanding its striking percentage of

endemic species, the Atlantic forest has been seriously threat-

ened by human intervention, reduced to approximately 7% of

its original distribution (Morellato and Haddad 2000), and

therefore, considered one of the most important biodiversity

hotspots for conservation (Myers et al. 2000, Conservation

International 2005). Such intense habitat change and fragmen-

tation have been tied to local amphibian population

fluctuations and declines (for a recent review, see Eterovick et

al. 2005). However, at a global scale, several factors other

than habitat disturbance have been associated to amphibian

population crashes (Collins and Storfer 2003), particularly

emerging infectious diseases such as chytridiomycosis,

caused by the fungus Batrachochytrium dendrobatidis

(review in Daszak et al. 2003). This chytrid fungus is global-

ly widespread (Speare and Berger 2000) and has been tied to

amphibian declines in Australia, the Americas, and Europe

(Berger et al. 1998, 1999a; Bosch et al. 2001). To date, there

have been no reports of B. dendrobatidis occurring in the

Atlantic forest or in Brazil. Based on morphological, histolog-

ical, and molecular data, we document infection in Hylodes

magalhaesi — a high-altitude stream-dwelling leptodactylid

endemic to the Brazilian Atlantic rainforest.

Methods

Field survey

From 2001 to 2005, we followed a population of H. magal-

haesi through yearly 10-day trips to Vila de Monte Verde,

Municipality of Camanducaia, State of Minas Gerais

(22°52'37.9"S, 46°02'01.8"W, ca. 1,600 m above sea level).

Adults and tadpoles of H. magalhaesi were observed along a

fast rivulet in this montane forest. Males were observed dur-

ing the day while calling from the water margin (Fig. 1);

tadpoles were observed under debris or in crevices under

water. Adults were collected by hand during the day. Tadpoles

(stage 25 sensu Gosner 1960) were collected with wicker fish

traps, using raw meat as bait. Specimens were deposited in

Celio F. B. Haddad anuran collection, Departamento de

Zoologia, Instituto de Biociencias, Universidade Estadual

Paulista, Rio Claro, State of Sao Paulo, Brazil (CFBH 8287:

tadpole lot for molecular analysis, collected in January 2005;

CFBH 8288: tadpole lot for histological analysis, collected in

Correspondence. 5 Email: toledolf2@yahoo.com

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December 2006 I Volume 4 I Number 1 I el 7

L. F. Toledo et al.

Figure 1. Adult male of Hylodes magalhaesi. Municipality of Camanducaia, State of Minas Gerais, Brazil.

Photo: Celio F. B. Haddad.

DOI: 10.151 4/journal. arc.004001 7g001

January 2002). A collecting permit was provided by Instituto

Brasileiro do Meio Ambiente e dos Recursos Naturais

Renovaveis (IBAMA 02001.002792/98-03).

Histology

Four tadpoles with deformed oral disks were fixed in 10%

formaldehyde solution for 24 hours (h), and their mouthparts

were then transferred to a buffer sodium phosphate solution

(pH 7.4), where they were kept for an additional 24 h.

Mouthparts were dehydrated through 30-minute (min) immer-

sion in each ethanol solution of a series of increasing

concentrations (70, 80, 90, and 95%), then embedded in Leica

resin for 24 h at 4°C before inclusion. Resin polymerization

was performed in a 37°C chamber. Sections (5 Im thick) were

stained with two techniques: hematoxylin and eosin (HE)

were first used to document the general morphologic aspects

of the tissue, and periodic acid Schiff (PAS) was subsequent-

ly used to enable better visualization of glycogen, mucin,

basal membranes, and the fungus (Junqueira and Junqueira

1983).

Molecular analysis

We used specific DNA-based assay of Annis et al. (2004) to

detect infection by B. dendrobatidis in two tadpoles preserved

in ethanol (100%). From each tadpole, we extracted DNA

from a 2 x 2 mm piece of mouth tissue corresponding to

approximately half of the oral disk. We dried the material for

1 h at 55°C to allow for ethanol evaporation, then added 20 pi

of polymerase chain reaction (PCR) buffer (Perkin-Elmer),

and 2 pi of proteinase-K (10 mg/ml), crushing the tissue with

a pipette tip to increase the contact surface between the mate-

rial and the solution. We incubated this mixture for 3 h at

55°C, mixing occasionally. After centrifuging for a few sec-

onds (s) at 6,000 RPM, we incubated the material for 5 min at

100°C as described in Annis et al. (2004). For DNA extrac-

tion, we added 20 pi of GeneReleaser (BioVentures) and

followed a thermocycle program per manufacturer’s protocols

on a Peltier Thermal Cycler 200 (PTC-200, MJ Research).

After centrifuging samples for 1 min at 6,000 RPM, the DNA-

bearing supernatant was transferred to a new tube. To control

for contamination, a blank extraction was carried out in a tube

containing no sample.

PCR was performed to determine the presence of B. den-

drobatidis in the extracted material, using primers Bdla and

Bd2a of Annis et al. (2004). We added 3 pi of extracted DNA,

19 pi of water, and 1.5 pi of each primer (10 pM solution) to

a tube of PuReTaq Ready-To-Go PCR Beads (Amersham

Biosciences). These primers are known to bind specifically to

B. dendrobatidis DNA as opposed to that of other

Chytridiomycota and are expected to result in the amplifica-

tion of a fragment of approximately 300 base pairs (bp)

containing B. dendrobatidis 5.8S ribosomal RNA and flank-

ing internal transcriber spacer regions ITS 1 and ITS2 (Annis

et al. 2004). For amplification, we used a PCR thermocycle

program comprising a denaturation step at 95°C for 5 min, 35

cycles of 94°C for 45 s, 60°C for 45 s, and 72°C for 1 min, and

final extension at 72°C for 10 min. To ensure that no false

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December 2006 I Volume 4 I Number 1 I e17

Chytrid fungus in a Brazilian anuran

positives were generated due to contamination during the

amplification step, we used the blank extraction as a negative

control.

We evaporated all amplification products to bring them

to final volumes of 10 pi, which were run on a 1% low-melt

low-EDTA agarose gel for band visualization. We cut and

incubated the bands of interest with 1 pi of GELase (Epicentre

Technologies) for 5 min at 50°C, subsequently leaving them

at 45 °C overnight. We performed cycle sequencing reactions

using 2 pi of template, 3 pi of water, 1 pi of BigDye

Terminators ver. 3.0 (ABI Prism), 3 pi of BigDye Buffer, and

1 pi of primer. Cycle sequencing profiles comprised a denatu-

ration step at 96°C for 1 min and 25 cycles of 96°C for 10 s,

50°C for 5 s, and 60°C for 4 min. We precipitated final prod-

ucts in ethanol and resuspended in 10 pi of Hi-Di formamide

(ABI Prism) per manufacturer’s protocols. Sequencing reac-

tions were run on a 3730 Genetic Analyzer (Applied

Biosystems). We used Sequencer version 4.1.2 (Gene Codes

Corporation) to visualize sequences and to align them to par-

tial sequences of ITS1 and adjacent 5.8S ribosomal RNA

sequence of B. dendrobatidis available in GenBank

(http://www.ncbi.nlm.nih.gov/Genbank/index.html; accession

numbers AY598034 and AY997031). We used MegaBLAST

(http://www.ncbi.nlm.nih.gov/BLAST/) to align and compare

them to sequences of all fungi species available in GenBank.

To that end, we retained all alignments with identity percent-

age higher than 60%, setting log-odd match and mismatch

scores to 1 and - 1 , respectively. Only alignments larger than

40 bp in length and with E-scores equal or smaller than e-04

were considered for the purposes of sequence comparison.

Results

Field survey

The population did not seem to vary in abundance along the

rivulet where calling males were found, or over the years of

observation. However, no count data were collected to docu-

ment these observations. Adults showed no apparent physical

or behavioral abnormalities. Five tadpoles were collected in

2004, all showing deformed or incomplete mouthparts, with

total or partial teeth loss. Most tadpoles also lacked kera-

tinized jaw sheaths or showed partially keratinized jaw

sheaths. Gut content observation nonetheless suggests that the

lack of keratinized mouthparts seemed not to interfere with

feeding ability. All four tadpoles collected in 2005 had com-

pletely keratinized mouthparts.

Histology

Fungal structures consistent with B. dendrobatidis occurred in

the oral region of all four tadpoles, in the epidermis adjacent

to tooth rows. Four stages of B. dendrobatidis were identified

(Fig. 2A and 2B); an early phase containing a central spheri-

cal basophilic mass, a zoospore-filled phase with 4-10 round

or oval basophilic zoosphores in cross section, empty spheri-

cal zoosporangia with internal septa, as well as later stage

where the empty zoosporangium had collapsed into an irregu-

lar shape. These structures stained strongly with PAS.

Zoosporangia were present at greater density in the areas of

the epidermis of tooth rows and jaw sheaths that showed the

most abnormal histology, consisting of hyperkeratosis and

loss of superficial epidermis (Fig. 2C). The prominent keratin

plate that forms the jaw sheath in healthy tadpoles was almost

completely destroyed (Fig. 2D).

Molecular Analysis

DNA was successfully extracted from the material sampled.

No contamination was found in the blank extraction. As

expected under the scenario of infection by B. dendroba-

tidis, the PCR procedure resulted in a bright band of

approximately 300 bp in both tadpoles (Fig. 3). No amplifi-

cation was obtained in the negative control tube, thus

excluding the possibility of contamination. Direct sequenc-

ing of the amplified band resulted in a chromatogram with

several multiple peaks, which is not surprising given that

these are tandem repeats of ribosomal DNA that are not

identical. Yet, a 114-bp piece located at the 5’ end of the

sequence, excluding primer Bdla, did not include multiple

peaks and was easily aligned to portions of the ITS 1+5. 8 S

B. dendrobatidis sequences available in GenBank. In total,

MegaBLAST encountered 21 GenBank records that aligned

to this 114-bp query sequence. All of them correspond to

fungi species. The obtained sequence was 100% identical to

known partial sequences B. dendrobatidis and differed from

all remaining fungi species by more than 9% in sequence

composition (91% to 67% sequence identity). Based on data

available in GenBank, sequences of congeneric species of

Chytridiomycota can differ by approximately 5% in compo-

sition at this locus.

Discussion

The identification of B. dendrobatidis was confirmed by the

fact that the morphology of the fungal structures was consis-

tent with previous descriptions, particularly the presence of

zoosporangia in four stages of development and the occur-

rence of colonial morphology in the zoosporangia (Berger et

al. 1998, 1999b; Longcore et al. 1999; Pessier et al. 1999;

Fellers et al. 2001). The morphological identification as B.

dendrobatidis was confirmed by PCR showing a match with a

partial sequence of the ITS 1+5. 8S sequence in GenBank.

Hylodes magalhaesi is an Atlantic forest endemic frog

restricted to areas of high elevations in southeastern Brazil (>

1,500 m above sea level). To date, it has been known solely

from its type locality (Municipality of Campos do Jordao,

State of Sao Paulo; Bokermann 1964; Frost 2004). Our obser-

vations provide the second population record of the species,

which extends its distribution approximately 50 km north-

ward. They also provide the first record of this species in the

State of Minas Gerais. The data represent the first report of the

presence of B. dendrobatidis in Brazil and in the Atlantic for-

est. Furthermore, this is one of the southernmost reports of a

natural population infected by B. dendrobatidis in the

Americas (see also Herrera et al. 2005).

Our data are alarming with regard to the status of H.

magalhaesi given the lack of information about this species

( H . magalhaesi is classified under the World Conservation

Union (IUCN) “Data Deficient” category, AmphibiaWeb

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December 2006 | Volume 4 | Number 1 | e17

L. F. Toledo et al.

moutti opening

/3 374 LlflT^

Figure 2. Mouthpart section of H. magalhaesi tadpole; keratinized epidermis with various stages of Bd. (A) Detail of

sporangia as shown by HE technique: immature sporangium (is), sporangium with zoospores (sz), empty sporangium

(es), and sporangium with internal septum (sd); dec = denticle epithelial cell. (B) Detail of sporangia as shown by PAS

technique. (C) Fungus infection as shown by PAS technique, arrows point to sporangia (s); de = denticle epidermis;

n = nucleus of epithelial cells. (D) Region of irregular epidermal surface (*) evidenced by HE technique. Arrow shows

remaining keratinized denticle surface.

DOI: 10.151 4/journal. arc. 004001 7g002

10GO bp-

500 bp-

im bp-

Figure 3. Gel image of PCR results using Bd - specific primers

Bdla and Bd2a. A reference DNA ladder is presented (RL).

Results obtained with a negative control (extraction blank),

DNA template from specimen CFBH 8287.1 (A), and DNA tem-

plate from specimen CFBH 8287.2 (B) are provided.

DOI: 10.151 4/journal. arc.004001 7g003

2005), particularly given the increased rate of deforestation

faced by the Brazilian Atlantic forest (Myers et al. 2000;

Morellato and Haddad 2000). Population declines have been

reported for other species of Hylodes endemic to this biome

( H . asper, H. babax, H. phyllodes, and H. lateristrigatus ).

For H. asper and H. phyllodes, local extinctions have been

attributed to climate change (Heyer et al. 1988; Bertoluci

and Heyer 1995). Other decline-leading factors have been

suggested for the remaining species of Hylodes, as well as

for other mountain- stream frogs (cycloramphines, cen-

trolenids, hylids, and dendrobatids), including infectious

diseases (Weygoldt 1989). Observations by Weygoldt

(1989) of the metamorphosis of individuals of H. babax led

him to suggest the occurrence of bacterial infections in this

species. However, there is a great probability that they could

not complete their development due to B. dendrobatidis

infection, as observed in other infected species (see Berger

et al. 1998, 1999a).

Even though we have noticed no apparent decline in the

abundance of adult H. magalhaesi over the last five years,

additional and more intensive studies are necessary to deter-

mine the dynamics of the infected population. Tadpoles of H.

magalhaesi seem to be able to feed normally with unkera-

tinized tooth rows, which could be caused by the presence of

the chytrid (see also Berger et al. 1999a) and may represent a

pathogen reservoir (Collins and Storfer 2003), with potential

consequences for other less resistant anuran hosts in Brazil

(see Daszak et al. 2004). The following questions shall be

answered in future studies: Do apparently normal tadpoles

also carry B. dendrobatidis ? Are there differences concerning

the trophic ecology of toothless and normal tadpoles? Does B.

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December 2006 I Volume 4 I Number 1 I e17

Chytrid fungus in a Brazilian anuran

dendrobatidis infect other stages of tadpole development? Do

infected tadpoles metamorphose and reach adult sizes? Are

post-mctamorphic individuals infected? Are populations of H.

magalhaesi declining at the study site? What other syntopic

high-altitude stream-dwellers are also infected?

Acknowledgments. — C. R. B. Haddad and A. M. Haddad

assisted in the field work. C. Hassapakis, R. Speare, R. W. R.

Retallick, and an anonymous reviewer greatly improved the

manuscript with their comments. DNA-based assays were car-

ried out in the Field Museum Pritzker Laboratory for

Molecular Systematics and Evolution thanks to permits issued

by Brazil’s Conselho de Gestao do Patrimonio Genetico

(CGEN licenses 037/2004 and 023/2004; deliberation pub-

lished in Diario Oficial da Uniao, 19/08/2004, section 1, page

116). E. O’Neill provided valuable assistance with the molec-

ular work. FAPESP (proc. 01/13341-3) and CNPq supported

the Herpetology lab, Departamento de Zoologia, Unesp, Rio

Claro, Sao Paulo, Brazil. The authors also thank CNPq,

CAPES, FAPESP, the National Science Foundation, Idea

Wild, and Neotropical Grassland Conservancy for grants,

scholarships, and equipment donation.

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Published: 26 December 2006

December 2006 | Volume 4 | Number 1 | e17

Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in

any medium, provided the original author and source are credited.

Amphibian and Reptile Conservation 4(1):22-45.

DOI: 10.151 4/journal. arc. 004001 8 (1 754KB PDF)

Biodiversity in a forest island: reptiles and amphibians

of the West African Togo Hills

ADAM D. LEACHE 1 ’ 5 , MARK-OLIVER RODEL 2 , CHARLES W. LINKEM 3 , RAUL E. DIAZ 3 ,

ANNIKA HILLERS 4 , AND MATTHEW K. FUJITA 1

1 Museum of Vertebrate Zoology and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley,

California 94720-3160, USA 2 Department of Animal Ecology and Tropiccd Biology, Biocenter of the University, Am Hublci nd, D-97074

Wiirzburg, GERMANY 3 Division of Herpetology, Natural History Museum & Biodiversity Research Center and Department of Ecology and

Evolutionary Biology, 1345 Jayhawk Boulevard, The University of Kansas, Lawrence, Kansas 66045-7561, USA 4 Institute of Biodiversity and

Ecosystem Dynamics, University of Amsterdam, Kruislaan, 318, 1098, SM Amsterdam, THE NETHERLANDS

Abstract .— Our recent surveys of the herpetological diversity of the West African Togo Hills documented a

total of 65 reptile and amphibian species, making Kyabobo National Park one of the most diverse sites sur-

veyed in Ghana. We provide accounts for all species recorded along with photographs to aid in identification.

We recorded 26 amphibians, including six new records for Kyabobo N. P., one of which is a record for the

Togo Hills. Our collection of reptile species (22 lizards, 16 snakes, and one crocodile) also provides new

records and range extensions for Kyabobo N. P., such as the first observation of the dwarf crocodile,

Osteolaemus tetraspis. Amphibian species still lacking from our surveys in the Togo Hills include several

species that are adapted to fast running water or large closed forests, like the Togo toad, Bufo togoensis and

the slippery frog, Conraua derooi. Appropriate habitat for such species still remains in Kyabobo, highlighting

the need for additional survey work. We draw attention to the importance of conserving forest stream habi-

tats, which will in turn help ensure the persistence of forest-restricted species. We also highlight those

species that may prove most useful for evolutionary studies of West African rain forest biogeography.

Key words. Ghana, reptiles, amphibians, biogeography, conservation, biodiversity, Dahomey Gap, West Africa, Togo Hills,

Kyabobo National Park

Citation: Leache, A. D., Rodel, M.-O., Linkem, C. W., Diaz, R. E., Hillers, A., and Fujita, M. K. 2006. Biodiversity in a forest island: reptiles and amphib-

ians of the West African Togo Hills. Amphib. Reptile Conserv. 4(1):22-45(e18).

Introduction

The Guinean rain forest of Western Africa is a center of bio-

logical diversity with considerable endemism (Myers et al.

2000). The percentage of reptile and amphibian species

endemic to this region far exceeds that of other tetrapod

groups (reptiles = 33% and amphibians = 77% versus mam-

mals = 8% and birds = 18%; Myers et al. 2000).

Concomitant with this impressive diversity is an alarming

rate of habitat loss. In Ghana alone, natural forests have

diminished to about 11.8-14.5% of their former cover

(UICN 1996; Poorter et al. 2004). Worldwide, habitat loss

and forest fragmentation are recognized as key factors driv-

ing the global extinction of genetically distinct populations

and species (Bierregaard et al. 1992; Hughes et al. 1997;

Brooks et al. 1999; Stuart et al. 2004).

While the host of factors driving wildlife declines in the

Guinean rain forest ecosystem involve some of the usual sus-

pects (i.e., logging and land use conversion for agriculture),

several studies have demonstrated that hunting of wildlife for

human consumption through the bushmeat trade is among the

most immediate threats (Milner-Gulland et al. 2003;

Brashares et al. 2004; Cowlishaw et al. 2005). Although these

studies focused primarily on mammals and birds, it is clear

that reptiles are also harvested for human consumption (Fa et

al. 2000; Luiselli 2003). Additional human pressures with

possible adverse effects on reptile and amphibian diversity

include the collection of animals for medical uses, the pet

trade, and the killing of snakes, poisonous or not, out of fear.

It is interesting to compare the current trend of habitat

loss with the historical oscillations of the rain forest distribu-

tion. The forest probably formed a large belt of continuous

habitat extending from West to Central Africa during the early

Holocene and the last interglacial (Maley 1991; Dupont et al.

2000). During the last glacial maximum, the expansion of dry

forest and savannah resulted in a very restricted and patchy

distribution of rain forest (Dupont et al. 2000). Currently, the

large West African rain forest blocks are separated by the

Dahomey Gap, a stretch of dry savannah extending from cen-

tral Ghana, through Togo, Benin, and western Nigeria (Fig. 1).

Correspondence. 5 Tel: (510) 642-7928; fax: (510) 643-8238; email: leache@berkeley.edu

Amphib. Reptile Conserv. | http://www.herpetofauna.org 022

December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

Table 1. Frogs (Anura), Lizards (Squamata), Snakes (Squamata), and Crocodiles (Archosauria) recorded at Kyabobo National Park

and the surrounding areas. Habitat classification types are as follows: S=savannah; F=forest; FB=farmbush.

Family

Scientific Name

Common Name

Habitat

Frogs

Arthroleptidae

Arthroleptis cf. poecilonotus

West African Screeching Frog

FB, F

Bufonidae

Bufo mciculcitus

Flat-backed Toad

S, FB

Bufo regularis

Square-marked Toad

S, FB

Hemisotidae

Hemisus cf. marmoratus

Marbled Shovel-nosed Frog

S, FB

Hyperoliidae

Afrixalus dorsalis

Cameroon Leaf-folding Frog

Afrixalus vittiger

Savannah Leaf-folding Frog

S, FB

Afrixalus weidholzi

Weidholz’s Leaf-folding Frog

Hyperolius baumanni

Baumann’s Reed Frog

F, FB

Hyperolius concolor

Variable Reed Frog

S, FB

Hyperolius fusciventris burtoni

Lime Reed Frog

Hyperolius nasutus

Long-nosed Reed Frog

Hyperolius nitidulus

West African Reed Frog

Hyperolius torrentis

Ukami Reed Frog

Kassina senegalensis

Senegal Running Frog

S, FB

Leptopelis hyloides

Gbanga Tree Frog

F, FB

Leptopelis viridis

Rusty Tree Frog

Petropedetidae

Phrynobatrachus accraensis

Accra Puddle Frog

S, FB

Phrynobatrachus calcaratus

Horned Puddle Frog

F, FB

Phrynobatrachus natalensis

Natal Puddle Frog

Phrynobatrachus plicatus

Coast Puddle Frog

Ranidae

Amnirana albolabris

White-lipped Frog

Amnirana galamensis

Galam White-lipped Frog

Hoplobatrachus occipitalis

Crowned Bullfrog

S, FB

Ptychadena bibroni

Broad-banded Grass Frog

S, FB

Ptychadena oxyrhynchus

Sharp-nosed Grass Frog

Ptychadena pumilio

Medine Grass Frog

S, FB

Lizards

Agamidae

Agama agama

Rainbow Lizard

S, FB

Agama sankaranica

Senegal Agama

Chamaeleonidae

Chamaeleo senegalensis

Senegal Chameleon

Eublepharidae

Hemitheconyx caudicinctus

Fat-tail Gecko

Gekkonidae

Hemidactylus brookii

Brooke’ s House Gecko

S, FB

Hemidactylus fasciatus

Banded Leaf-toed Gecko

Hemidactylus mabouia

House Gecko

Hemidactylus muriceus

Guinea Leaf-toed Gecko

Lygodactylus gutturalis

Uganda Dwarf Gecko

S, FB

Gerrhosauridae

Gerrhosaurus major

Rough-scaled Plated Lizard

S, FB

Lacertidae

Holaspis guentheri

Sawtail Lizard

Scincidae

Cophoscincopus cf. simulans

Keeled Water Skink

Lygosoma brevicaudis

Short-tailed Writhing Skink

Lygosoma guineensis

Guinea Writhing Skink

S, FB

Panaspis togoensis

Togo Lidless Skink

Continued on page 26

Amphib. Reptile Conserv. | http://www.herpetofauna.org 023 December 2006 | Volume 4 | Number 1 | e18

A. D. Leache et al.

Figure 1. Satellite image of Western Africa. The disjunct distribution of the major blocks of African rain forest (wet lowland and drier

and mixed types) and the Togo Hills is highlighted in green (adapted from Schiotz 1967 and Lawson 1968). Kyabobo National Park,

located in the center of the Dahomey Gap in the Togo Hills, is highlighted by the red box and shown in figure 2. Base map down-

loaded from Google Earth (Google, Inc.).

DOI: 10.151 4/journal. arc.004001 7g001

Although the Dahomey Gap became established during the

late Holocene, it has also experienced fluctuations in range

and only reached its current extent within the last 1,100 years

(Salzmann and Hoelzmann 2005).

The Dahomey Gap is thought to be a major biogeo-

graphic border separating forest faunas restricted to blocks

of rain forest in West and Central Africa (Booth 1958;

Schiptz 1967; Hamilton 1976). Situated in the center of the

Dahomey Gap are the Togo Hills, a mountainous area with

peaks reaching 800 m that receives a substantial amount of

rain and includes vegetation composed of moist semi-decid-

uous forest and montane ravine forest. Thus, the Togo Hills

are a virtual “island” of lush forest surrounded by savannah

and contain many forest species that are isolated from the

more expansive rain forest blocks to the west and east (Fig.

1). The presence of relatively few rainforest endemics in the

Togo Hills (e.g., Togo slippery frog Conraua derooi,

Baumann’s reed frog Hyperolius baumanni, Ukami reed

frog H. torrentis) corroborates geological data suggesting

that this region has not been isolated for a long period of

time and is consistent with the hypothesis that the area

served as a forest refugium during dryer periods associated

with glacial maximum (Haffer 1982).

Ghana has an excellent national park system that encom-

passes the major habitat types located in the country. Located

in Eastern Ghana, bordered by the Koue River and Togo to the

east and the villages of Nkwanta and Shiare to the south, is

Kyabobo National Park (Fig. 2). Although Kyabobo is rela-

tively small (-380 km 2 ) compared to other national parks in

Ghana, it is important in terms of biodiversity conservation

and biogeography. Situated in the Dahomey Gap, Kyabobo

contains much of the residing large tracts of semi-deciduous

forest habitat remaining in the Togo Hills. It is crucial to cat-

alog and study the forest species of Kyabobo and the

immediate surrounding areas as an important first step toward

understanding the evolutionary history and biogeography of

the entire West African rain forest ecosystem.

Despite the clear understanding of the Togo Hills as an

important area for biodiversity conservation and biogeogra-

phy, it is surprising that so little is known about the reptiles

and amphibians of the area. Ghana has a fascinating history of

herpetological research beginning with the exportation of

specimens to European countries during the 1800s (Hughes

1988). The most comprehensive synopsis of the reptiles and

amphibians of Ghana is a checklist of species compiled by

Barry Hughes (1988), but this list is by no means definitive.

New country records and new species are still being discov-

ered (Leache 2005; Rodel et al. 2005).

A recent survey of amphibians of the Togo Hills con-

cluded that, with 31 amphibian species, the area is more

diverse than previously assumed and probably contains at

least 41 amphibian species (Rodel and Agyei 2003). The

periphery of Kyabobo National Park was also surveyed and

found to contain a total of 20 frog species (Rodel and Agyei

2003). The reptiles of the area have never been targeted for

biological survey.

Here, we summarize the results of our herpetological sur-

veys of Kyabobo National Park. We provide accounts for ah

species recorded along with photographs to aid in identifica-

tion. We draw attention to the importance of conserving forest

stream habitats, which will in turn help ensure the persistence

of forest-restricted species. We also highlight those species

that may prove most useful for evolutionary studies of West

African rain forest biogeography.

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December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

Table 1. Continued.

Family

Scientific Name

Common Name

Habitat

Scincidae (cont.)

Trachylepis affinis

Senegal Mabuya

S, FB, F

Trachylepis buettneri

Buettneri’ s Long-tailed Mabuya

S, FB

Trachylepis maculilabris

Speckle-lipped Mabuya

FB, F

Trachylepis perrotetii

Teita Mabuya

S, FB

Varanidae

T rachylepis quinquetaeniata

Rainbow Mabuya

S, FB

Varanus exanthematicus

Savannah Monitor

Varanus niloticus

Nile Monitor

S, FB, F

Snakes

Atractaspididae

Polemon acanthias

Reinhardt’s Snake-eater

Colubridae

Afronatrix anoscopus

African Brown Water Snake

S, FB, F

Crotaphopeltis hotamboeia

Herald Snake

S, FB

Gonionotophis klingi

Matschie’s African Ground Snake

Lamprophis lineatus

Striped House Snake

S, FB

Lycophidion nigromaculatum

Blotched Wolf Snake

Natriciteres variegata

Forest Marsh Snake

FB, F

Philothamnus heterodermus

Variable Green Snake

FB, F

Philothamnus semivariegatus

Spotted Bush Snake

S, FB

Psammophis phillipsi

Olive Grass Racer

S, FB

Psammophis rukwae

Rukwa Sand Racer

Rhamnophis aethiopissa

Large-eyed Green Treesnake

Elapidae

Naja melanoleuca

Black Forest Cobra

S, FB, F

Pythonidae

Python regius

Royal Python

S, FB

Typhlopidae

Typhlops punctatus

Spotted Blind Snake

S, FB, F

Viperidae

Causus maculatus

Spotted Night Adder

S, FB, F

Crocodiles

Crocodylidae

Osteolaemus tetraspis

Dwarf Crocodile

DOI: 10.151 4/journal. arc.004001 7t001

Methods

We surveyed six general areas located inside or on the periph-

ery of Kyabobo National Park (Plates 1-6) on three occasions

spanning a 5-year period, each during the rainy season. These

surveys were conducted on an eight-day visit from 15-22

August, 2001, a nine-day visit from 10-18 June, 2004, and a

20-day visit from 23 June-12 July, 2005. Kyabobo is situated

on the boundary between woodland and semi-deciduous for-

est zones and is extremely hilly (peaks reaching 800 m) with

vegetational changes occurring over short distances. Apart

from the ridge tops, which are almost bare of trees, the park is

generally densely wooded or forested. A small amount of

farming activity is still taking place in the park, but most farm-

ers have relocated. We sampled from as many distinct

microhabitats as possible at each general survey area includ-

ing streams, rivers, ponds, savannah grassland, savannah

woodland, transition woodland, semi-deciduous rain forest,

riparian forest, farm bush, and urbanized areas.

Specimens were found by visual encounter surveys

(Heyer et al. 1994; Rodel and Ernst 2004) supplemented with

acoustic searching for frogs, turning rocks and logs, peeling

bark, digging through leaf litter, and excavating burrows and

termite mounds. Surveys were conducted during the day and

night to detect both diurnal and nocturnal species. We collect-

ed voucher specimens for future systematic and genetic

studies. We primarily collected specimens by hand, but many

fast moving lizards were captured by blowgun using blunt,

plastic plugs as ammunition. Snake tongs were used to capture

poisonous snakes. Pitfall trap arrays were installed at four

locations (Laboum outpost near Odome, South Repeater

Station, Middle Control Camp, and the new Wildlife

Headquarters outside of Nkwanta) and monitored over a five-

day period. Each pitfall array consisted of five-gallon plastic

buckets (seven total) dug into the ground flush with the sur-

face, one-foot-tall plastic drift fence connecting the buckets,

and six wire-mesh snake traps set adjacent to the drift fence.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 025

December 2006 I Volume 4 I Number 1 I e18

A. D. Leache et al.

Togo

— — 'Kano ">

Kyabobo

National Park

G h n n a

■P l i

Shunt 1

Odome

N h vy.ri n in

J ‘ -

.■! >*■

M i|ir [ r»|-l- .-Irl.r

■ viur e - JMt'J ti-lhtil

Figure 2. Satellite image of Kyabobo National Park in the Togo Hills, Volta Region, Ghana. White boxes outline key survey sites, and

are numbered according to habitat photograph Plates 1-6. Base map downloaded from Google Earth (Google, Inc.).

DOI: 10.151 4/journal. arc.004001 7g002

Pitfall traps were left open continuously and monitored in the

morning and evening.

Digital photographs were taken of representatives of

each species and habitats at 5.0 or 6.1 megapixels (Nikon

D-70). When possible, calling frogs were recorded using a

digital video camcorder (Sony DCR DVD-203) coupled

with a directional zoom microphone (Sony ECM-HGZ1).

Geographic coordinates for each survey site were deter-

mined in the field with a Garmin GPS 72 or a Garmin eTrex

receiver. Coordinates were recorded as latitude and longi-

tude in decimal degrees, and referenced to the WGS84

(World Geodetic System of 1984) datum. Voucher speci-

mens and tissue samples are deposited at the Museum of

Vertebrate Zoology, University of California, Berkeley, or

within the personal collection of Mark-Oliver Rodel.

Complete voucher specimen information for most species,

including specific locality data and GPS coordinates, is

available online at the Museum of Vertebrate Zoology,

University of California, Berkeley website (http://mvz.

berkeley.edu/).

We identified specimens using the following litera-

ture: tree frogs (Schiptz 1967, 1999), savannah frogs

(Rodel 2000), Ghanaian amphibians (Rodel and Agyei

2003; Rodel et al. 2005), snakes (Hughes and Barry 1969;

Chippaux 1999), lizards (Spawls et al. 2002), skinks

(Horton 1973; Hoogmoed 1974; Greer et al. 1985; Bohme

et al. 2000), geckos (Henle and Bohme 2003), and croco-

dilians (Spawls et al. 2002).

Species list

We recorded a total of 65 species in Kyabobo National Park,

including 26 frogs, 22 lizards, 16 snakes, and one crocodile

(Table 1). Voucher specimens representing 61 of these

species were collected. The records for the savannah moni-

tor ( Varanus exanthematicus ), sawtail lizard ( Holaspis

guentheri ), Buettneri’s long-tailed mabuya ( Trachylepis

buettneri ), and dwarf crocodile ( Osteolaemus tetraspis ) are

based on observations.

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December 2006 I Volume 4 I Number 1 I e18

Plate 1. DOI: 10.1514/journal.arc.0040017g003

Plate 3. DOI: 10.151 4/journal.arc.004001 7g005

Plate 5." ^ DOI: 1 0.151 4/journal.arc.004001 7g007

Plate 7A. DOI: 10.151 4/journal.arc.004001 7g009

Plate 4. DOI: 10.1 51 4/journal. arc. 004001 7g006

Plate 6. DOI: 10.1 51 4/journal. arc. 004001 7g008

Plate captions: 1. Savannah and farmbush habitat at the Laboum Outpost entrance to Kyabobo. The western edge of the Togo Hills is

shown in the background. 2. Stream (originating from a waterfall) flowing through semi-deciduous forest vegetation at the southern end

of Kyabobo. 3. Savannah vegetation at South Repeater Station in Kyabobo, Togo Hills mountain-top at -800 meters elevation. The

Togo Hills are shown in the background extending to the south. 4. Semi-deciduous forest and stream adjacent to Middle Control Camp

located on the Western edge of Kyabobo. 5. Overview of the canopy of semi-deciduous forest bordering a stream viewed from Bad-

legged Man Camp in Kyabobo. 6. Shiare Village. Photograph by Martin Weinbrenner (www.eyelustrate.com). 7A. West African

Screeching Frog Arthroleptis of. poecilonotus, amplectant pair, South Repeater Station. 7B. Arthroleptis of. poecilonotus, male with

elongated third toe, South Repeater Station.

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December 2006 I Volume 4 I Number 1 I e18

Plate 8A. DOI: 10.151 4/journal.arc.004001 7g01 1

Plate 9. DOI: 10.151 4/journal.arc.004001 7g01 3

Plate 11. DOI: 1 0.1 51 4/journal.arc.004001 7g01 5

Plate 13. DOI: 10.1514/journal.arc.0040017g017

Plate 8B. DOI: 10.151 4/journal.arc.004001 7g001 2

Plate 12. DOI: 10.1514/journal.arc.0040017g016

Plate 14. DOI: 10.1514/journal.arc.0040017g018

Plate captions: 8A. Flat-backed Toad Bufo maculatus, South Repeater Station. 8B. Bufo maculatus, calling male, Pawa. 9. Square-

marked Toad Bufo regularis, Accra. 10. Marbled Shovel-nosed Frog Hemisus cf. marmoratus, Odome. 11. Cameroon Leaf-folding Frog

Afrixalus dorsalis, Pawa. 12. Savannah Leaf-folding Frog Afrixalus vittiger, calling male, Pawa. 13. Weidholz’s Leaf-folding Frog Afrixalus

weidholzi, Pawa. 14. Baumann’s Reed Frog Hyperolius baumanni, Middle Control Camp.

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December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

Frogs (Anura)

Arthroleptidae

West African Screeching Frog Arthroleptis cf. poecilonotus

Peters 1863 (Plate 7A and 7B). Arthroleptis are the most com-

mon leaf litter frogs in the Togo Hills. They inhabit degraded

forests and farmbush habitats. Their taxonomic status is

uncertain (Rodel and Agyei 2003). It is clear that they do not

belong to A. brevipes Ahl, 1923 (compare Rodel et al. 2005).

They might be conspecific with either A. zimmeri (Ahl 1925)

or A. poecilonotus, both described from southern Ghana.

However, most West African frogs of the genus Arthroleptis

(and Schoutedenella ) cannot be distinguished by morphologi-

cal criteria, although they are clearly distinct taxa based on

genetic and acoustic characters that cannot be assigned to

available names (Rodel and Bangoura 2004; Rodel et al.

2005). The frogs from the Togo Hills exhibited the variability

in dorsal coloration typical for most of their congeners includ-

ing: brown or reddish brown dorsal coloration with or without

a dark hourglass pattern, a vertebral stripe, or pale dorsolater-

al bands. The exact range of A. poecilonotus is uncertain given

this taxonomic confusion, but is reported from southern Sudan

westward to Guinea (Rodel 2000).

Bufonidae

Flat-backed Toad Bufo maculatus Hallowell 1854 (Plate 8A

and 8B). This medium-sized toad is brown or red in appear-

ance, with dark blotches on its warty back. Males in breeding

condition are uniform yellowish (Rodel 2000). The parotoid

glands are large, yet can be indistinct because they are covered

with warts, causing their appearance to blend with the skin.

Bufo maculatus inhabits savannah and degraded forests, but

never primary forest. Bufo maculatus has a wide distribution,

encompassing most of sub-Saharan Africa.

Square-marked Toad Bufo regularis Reuss 1833 (Plate

9). This is a large, robust toad with prominent, long, and

smooth parotoid glands. Its dorsal coloration is typically

brown with irregular dark blotches. This toad inhabits savan-

nah and frequently occurs in water-filled ditches around

human habitations. Its distribution includes sub-Saharan West

and East Africa.

Hemisotidae

Marbled Shovel-nosed Frog Hemis us cf. mannoratus (Peters 1854)

[Plate 10]. The subterranean Hemisus species with their squat bodies

and pig-shaped snouts are unmistakable, but are rarely encountered.

Two species are known to occur in West Africa including the forest

dwelling H. guineensis Cope 1865 and the savannah-dwelling H. mar-

moratus. However, the morphological criteria, as defined by Laurent

(1972), are not sufficient for species delimitation (M.-0. Rodel et al.,

unpublished data). Our species assignment should be taken as tenta-

tive. Hemisus marmoratus is distributed throughout savannah regions

south of the Sahara (Rodel 2000).

Hyperoliidae

Cameroon Leaf-folding Frog Afrixalus dorsalis (Peters

1875) [Plate 11]. This is a small frog that inhabits degraded

forests and farmbush habitats in the forest zone, and gallery

forests in the savannah zone (Schiptz 1967; Rodel 2000).

Most frogs have two broad yellowish dorsolateral bands and a

brownish back. Occasionally, specimens with a pale vertebral

band occur. The latter might be confused with the next species

that, however, has a much more slender body shape. Afrixalus

dorsalis is distributed from Sierra Leone to Angola (Schiptz

1999) .

Savannah Leaf-folding Frog Afrixalus vittiger (Peters

1876) [Plate 12], Two distinct forms of striped Afrixalus

occur in West Africa. They seem to occur in different habi-

tats, namely savannah and degraded forests or forest edges.

The forest form exhibits a fine black line within the paler

longitudinal stripes on the back and is considered A. ful-

vovittatus Cope 1860 by Perret (1976) and Rodel (2000).

The savannah species lacks the fine black lines and is con-

sidered A. vittiger by Perret (1976) and Rodel (2000).

Schiptz (1999) considered these forms A. fulvovittatus “type

A” and “type B”. Afrixalus vittiger (or A. fulvovittatus type

A) occurs in Kyabobo, and is widely distributed throughout

savannah regions of West Africa.

Weidholz’s Leaf-folding Frog Afrixalus weidholzi

(Mertens 1937) [Plate 13]. A tiny savannah frog with a yel-

low-gold back and often with a black vertebral line and

brownish flanks with minute white spots. Males call from

higher grasses several meters from open water. Their buzzing

advertisement call can easily be mistaken for an insect (Rodel

2000) . It ranges from Senegal into Central Africa.

Baumann’s Reed Frog Hyperolius baumanni Ahl 1931

(Plate 14). This frog is one of the few endemic species of the

Togo Hills. It prefers degraded forests and forest edges, where

it often occurs in high densities. Males have brownish backs

and whitish dorsolateral bands that begin on the snout and ter-

minate at the groin.

Variable Reed Frog Hyperolius concolor Rapp 1842

(Plate 15 A and 15B). This is a very common medium-sized

reed frog that inhabits farmbush and other open forest habi-

tats. Males often have an indistinct hourglass pattern on their

brownish backs, whereas females are most often grass-green.

The venter of both sexes is white. At night their dorsal color

is more or less uniform yellow. Hyperolius concolor is dis-

tributed from Guinea to Cameroon.

Lime Reed Frog Hyperolius fusciventris burtoni

Schiptz 1967 (Plate 16). Hyperolius fusciventris burtoni was

reported to occur from western Ghana to eastern Nigeria

(Schiptz 1967). Recently, this subspecies and H.f lamtoensis

have been reported to occur in sympatry in southwestern

Ghana (Rodel et al. 2005). In western Ivory Coast the latter

occurs in sympatry with the nominate form (Rodel and Ernst

2004). We thus think that all three subspecies would be more

appropriately treated as full species. Males from the Togo

Hills frequently have pale dorsolateral bands. We recorded

green and brown males. Brown specimens always had yellow

gular flaps, whereas green males have green ones. Most call-

ing sites are right at the border to open water.

Long-nosed Reed Frog Hyperolius nasutus Gunther

1864 (Plate 17). These small, green reed frogs are common

around ephemeral savannah ponds. They might be confused

with H. fusciventris, but the latter inhabits very different habi-

tats. In comparison, H. nasutus has a more slender body shape

and a longer, more pointed snout. The taxonomic situation of

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December 2006 I Volume 4 I Number 1 I e18

Plate 15A.

Plate 16.

Plate 18.

Plate 20.

DOI: 10.151 4/journal. arc. 004001 7g025

DOI: 10.151 4/journal. arc. 004001 7g01 9 Plate 15B.

DOI: 10.151 4/journal. arc. 004001 7g020

DOI: 10.151 4/journal. arc. 004001 7g021 Plate 1 7.

DOI: 10.151 4/journal. arc. 004001 7g022

^ 5

DOI: 10.151 4/journal. arc. 004001 7g023 Plate 19.

DOI: 10.151 4/journal. arc. 004001 7g024

— ■

Plate 21 A.

'# f “ b

DOI: 1 0.1 51 4/journal.arc.004001 7g026

Plate captions: 15A. Variable Reed Frog Hyperolius concolor, male, Pawa. 15B. Hyperolius concolor, female, Pawa. 16. Lime Reed

Frog Hyperolius fusciventris burtoni, calling male, Wli, Volta Region, Ghana. 17. Long-nosed Reed Frog Hyperolius nasutus, Comoe,

Ivory Coast. 18. West African Reed Frog Hyperolius nitidulus, male, Pawa. 19. Ukami Reed Frog Hyperolius torrentis, female, forest

stream southwest of South Repeater Station. 20. Senegal Running Frog Kassina senegalensis, Laboum outpost. 21A. Gbanga Tree

Frog Leptopelis hyloides, male, Wli, Volta Region, Ghana.

Amphib. Reptile Conserv. | http://www.herpetofauna.org

030

December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

this species group is not resolved (compare Channing et al.

2002; Rodel and Ernst 2003; Amiet 2005; Rodel et al., in

press). We therefore continue to apply the name H. nasutus.

Hyperolius nasutus is widely distributed south of the Sahara

(Rodel 2000).

West African Reed Frog Hyperolius nitidulus Peters

1875 (Plate 18). Hyperolius nitidulus is the most abundant

savannah tree frog in West Africa. The brownish frogs are

most conspicuous due to their xylophone like sounds of their

choruses around all kinds of vegetated, stagnant savannah

waters. Hyperolius nitidulus is widely distributed in savannah

regions from Senegal to Cameroon (Rodel 2000).

Ukami Reed Frog Hyperolius torrentis Schiptz 1967

(Plate 19). Hyperolius torrentis is so far believed to be

endemic to eastern Ghana and adjacent Togo (Schiptz

1967; Rodel and Agyei 2003). We have unpublished evi-

dence that this species may range along the Togolese

mountains into northern Benin (photo record by T. Moritz).

This large reed frog exhibits a variety of color patterns

(compare Schiptz 1967, 1999; Rodel and Agyei 2003).

From the similar sized H. concolor, it can be best distin-

guished by its yellowish to greenish venter; from H.

baumanni, it most conspicuously differs by larger size and

the lack of pale dorsolateral bands. Hyperolius torrentis

seems to occur exclusively on the forested borders of rap-

idly flowing streams.

Senegal Running Frog Kassina senegalensis

(Dumeril and Bibron 1841) [Plate 20]. This is a small to

medium-sized frog that typically inhabits savannah in most

of sub-Saharan Africa. Its dorsal coloration is a very pale

brown, with five longitudinal stripes. The three central

stripes are usually uninterrupted, while the two lateral

stripes have a fragmented pattern starting from the snout

and extending to the vent. The only specimen we found was

inside a hole three meters high in a tree trunk during the

day. Kassina senegalensis is widely distributed throughout

sub-Saharan Africa (Schiptz 1999).

Gbanga Tree Frog Leptopelis hyloides (Boulenger

1906) [Plate 21 A and 2 IB], A small (male) to medium- sized

(female) forest tree frog that is generally brownish in color

with a darker hour-glass pattern on the dorsum. The eyes are

prominent and contain red pigmentation, a distinguishing

character from the savannah species Leptopelis viridis.

Leptopelis hyloides also has more extensive webbing com-

pared to L. viridis. A proper name for this species is lacking,

since the type specimen actually represents L. viridis

(Schiptz 1999). Leptopelis hyloides is distributed throughout

the forest belt of West Africa west of the Cross River in

Nigeria (Schiptz 1999).

Rusty Tree Frog Leptopelis viridis (Gunther 1869)

[Plate 22], This fairly large hyperoliid has a compact appear-

ance, with large eyes and a general coloration of light to

reddish brown. Darker patches of color form a triangle on the

head and continue to form an irregular, and often broken, cir-

cle pattern on the back. On each side of its face is a dark mask

that starts at the tip of snout and continues to the forelimb. We

found individuals at night moving on the ground in savannah

habitat, and often heard their “chuck” call from low-lying

bushes. This species is abundant throughout West Africa

(Schiptz 1999).

Amphib. Reptile Conserv. | http://www.herpetofauna.org 031

Petropedetidae

Accra Puddle Frog Phrynobatrachus accraensis Ahl 1923

(Plate 23). This is a small and extremely common species that

occurs in almost all stagnant waters from dry savannah to dis-

turbed rainforest. It is best differentiated from similar puddle

frogs by its call and the combination of yellow throats in

breeding males, a well-developed webbing, and the lack of an

eyelid cornicle. Phrynobatrachus accraensis is distributed

throughout West Africa.

Horned Puddle Frog Phrynobatrachus calcaratus

(Peters 1863) [Plate 24]. This widespread West and Central

African forest frog differs from other puddle frogs in the

Togo Hills by the presence of an eyelid cornicle.

Furthermore, the vocal sac of males is dark violet to black.

The frogs almost completely lack webbing. The dorsum can

be uniform brown or bear a reddish longitudinal or transverse

band. Phrynobatrachus calcaratus is distributed from

Senegal to Cameroon.

Natal Puddle Frog Phrynobatrachus natalensis

(Smith 1849) [Plate 25]. This widespread savannah frog

probably comprises several cryptic species (Rodel 2000;

Crutsinger et al. 2004). They most often inhabit and breed in

small puddles almost devoid of vegetation. They differ from

the similar P. accraensis in having a larger size, more com-

pact body, and black throats on breeding males.

Phrynobatrachus natalensis is widely distributed throughout

Africa south of the Sahara.

Coast Puddle Frog Phrynobatrachus plicatus (Gunther

1859) [Plate 26]. This is a widespread West African forest

frog (Famotte 1966). It differs from all other West African

puddle frogs by its large size, exceeding 30 mm snout-vent

length, and two very long dorsal ridges that form an “X” pat-

tern. Males have a dark black throat. They most often breed in

small ponds in swampy forest or in small puddles on forest

roads. This species is distributed from Guinea to Nigeria.

Ranidae

White-lipped Frog Amnirana albolabris (Hallowell 1856)

[Plate 27], This is a large, slender frog with enlarged toe discs,

noticeably webbed hind feet, and a brown dorsal coloration,

often with distinct black spots. The skin appears smooth but is

covered with minute spines (Rodel and Bangoura 2004). A

white stripe along the upper lip does not extend much past the

tympanum, though speckles of white can occur along the sides

of the body. We found these frogs near streams and creeks

well within forested areas, often clinging to overhanging veg-

etation and rocks. Amnirana albolabris is common in West

and Central Africa forests.

Galam White-lipped Frog Amnirana galamensis

(Dumeril and Bibron 1841) [Plate 28]. This is a relatively

large ranid frog, typically brown to light brown above with

striking golden dorsolateral ridges. Both the upper and lower

lips are cream-colored; the stripe on the upper lip continues

along the side of the body. We found A. galamensis in savan-

nah habitat; at night, they were active and moving on land, and

during the day we heard vocalization in pools of water. We

also found adults underneath piles of bricks and concrete rub-

bish near ponds. This wide-ranging frog occurs in West, East,

and Central Africa.

December 2006 I Volume 4 I Number 1 I e18

Plate 21 B. DOI: 10.151 4/journal.arc.004001 7g027

Plate 23. DOI: 10.151 4/journal.arc.004001 7g029

Plate 25. DOI: 10.151 4/journal.arc.004001 7g031

Plate 27. DOI: 10.151 4/journal.arc.004001 7g033

Plate 22. DOI: 10.151 4/journal.arc.004001 7g028

Plate 24. DOI: 10.151 4/journal.arc.004001 7g030

Plate 26. DOI: 10.151 4/journal.arc.004001 7g032

Plate 28. DOI: 10.151 4/journal.arc.004001 7g034

Plate captions: 21 B. Leptopelis hyloides, female, Middle Control Camp. 22. Rusty Tree Frog Leptopelis viridis, male, Pawa. 23. Accra

Puddle Frog Phrynobatrachus accraensis, gravid female, Middle Control Camp. 24. Horned Puddle Frog Phrynobatrachus calcaratus,

female, note the eyelid cornicle, South Repeater Station. 25. Natal Puddle Frog Phrynobatrachus natalensis, Middle Control Camp. 26.

Coast Puddle Frog Phrynobatrachus plicatus, Bad-legged Man Camp. 27. White-lipped Frog Amnirana albolabris, forest stream south-

west of South Repeater Station. 28. Galam White-lipped Frog Amnirana galamensis, Accra.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 032

December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

Togo Slippery Frog Conraua derooi Hulselmans 1972

(Plate 29 A and 29B). This large aquatic frog is one of the few

amphibian species that is endemic to the Togo Hills. It is only

known from the type locality in Bismarckburg (Misahohe),

Togo (Hulselmans 1971), and a few localities in southeastern

Ghana (Schiptz 1967; Rodel and Agyei 2003). This species

was not recorded in the Volta region by Rodel and Agyei

(2003), and we did not record it in Kyabobo. However, we

were informed by people in Shiare village that the frog might

live in nearby Togo (large blackish frogs in flowing water

with very slimy skin). Very recently, C. derooi was rediscov-

ered in the Volta Region, including voice recordings from

Amedzofe and Biakpa (A. Hillers et al., unpublished data).

Hence its potential occurrence in Kyabobo should be further

investigated.

Crowned Bullfrog Hoplobatrachus occipitalis

(Gunther 1859) [Plate 30]. This large frog is highly aquatic

and extremely common. It mainly lives in savannah habitats,

but penetrates the forest zone in disturbed areas (Rodel 2000).

This species inhabits almost all kinds of waters, ranging from

small, sun-heated puddles to cold, fast-flowing streams. We

found several individuals in small puddles in residential areas,

large ponds, and slow-moving streams. The largest specimen

measured was a female (124 mm). They are very shy but eas-

ily recognized by their furious flights during which they partly

run over water. They are olive-green above with dark mot-

tling, and generally pale below. Their dorsally positioned

eyes, warty back (but particularly slimy skin), light interor-

bital stripe, and full webbing of their hind feed are suitable

criteria for determination. At night they can be traced by their

reflective red eye-shine. This species is not threatened.

However, in some areas it is harvested for human consump-

tion. Its range includes much of Africa south of the Sahara

(except southern Africa).

Broad-banded Grass Frog Ptychadena bibroni

(Hallowell 1845) [Plate 31]. A common, medium-sized,

West African grass frog that inhabits degraded forests and

moist savannahs. A reddish vertebral band is most often

present. Pale dorsolateral ridges are absent or fragmented

into a few warts.

Sharp-nosed Grass Frog Ptychadena oxyrhynchus

(Smith 1849) [Plate 32], A large (snout- vent length 40-68

mm) frog with an extremely pointed snout and enormous

hind legs. A pale dorsolateral ridge is present and not inter-

rupted. Breeding frogs most often call from small puddles

in open surrounding. This frog is widely distributed

throughout Africa.

Medine Grass Frog Ptychadena pumilio (Boulenger

1920) [Plate 33]. A widespread frog that inhabits degraded

forests and moist savannahs. It is characterized by its small

size, uninterrupted pale dorsal ridges, well-developed web-

bing and a comparatively compact body shape. Ptychadena

pumilio is distributed from Senegal to Ethiopia, and south to

Zambia (Rodel 2000).

Lizards (Squamata)

Agamidae

Rainbow Lizard Agama agama (Linnaeus 1758) [Plate 34A

and 34B], An extremely common diurnal lizard found in most

types of habitats except for dense primary rain forest and can

be found in particularly high abundance around human set-

tlements. Sexual dimorphism in this species is striking. At

Kyabobo, adult males are dark blue in coloration with bright

orange-red heads and tails, although the color on the tail

gradually grades to white and appears as a “rainbow.” Adult

females are drab grey or brown with distinctive paired orange

markings on the back. Agama agama are widely distributed

in Africa from Senegal to Egypt and south to Tanzania

(Spawls et al. 2002).

Senegal Agama Agama sankaranica Mocquard 1905

(Plate 35). A common diurnal lizard found in savannah habi-

tats. It is strictly terrestrial and often spotted darting between

clumps of vegetation. Both sexes are brown with a thin yellow

vertebral line extending from the neck to the base of the tail.

Some specimens have iridescent blue scales on the sides of

their face and around their ear openings. The local name for A.

sankaranica is the “bush agama.” Agama sankaranica is dis-

tributed across West Africa from Senegal to Cameroon.

Chamaeleonidae

Senegal Chameleon Chamaeleo senegalensis Daudin 1802

(Plate 36). A large green arboreal chameleon with a slightly

raised casque at the back of the head and a prehensile tail.

Found in moist savannah habitats. They are active during the

day and can be found on the ground crossing roads, although

they are more easily found at night in bushes and small trees

where the reflection of their bodies contrasts with the sur-

rounding vegetation. Possibly threatened by bush fires and

collecting for local medicinal use. Chamaeleo senegalensis is

distributed from Senegal to Cameroon.

Eublepharidae

Fat-tail Gecko Hemitheconyx caudicinctus (Dumeril 1851)

[Plate 37], A medium-sized terrestrial gecko that can be dis-

tinguished from other geckos by the presence of eyelids and

the lack of toe-pads. Laterally banded with yellow and black

with white bands on the tail. A savannah species distributed

throughout West Africa.

Gekkonidae

Brooke’s House Gecko Hemidactylus brookii Gray 1845

(Plate 38). A common nocturnal gecko that is abundant

around anthropogenic habitats. Usually found on building sur-

faces near cracks or in rafters. Resembles H. mabouia, but is

distinguishable by a shorter snout and the inability to make a

defensive “squeak” sound (Gramentz 2000). It has dorsal

tubercles that continue down the tail, but regenerated tails lack

tubercles. Hemidactylus brookii has a broad distribution

throughout West and Central Africa.

Banded Leaf-toed Gecko Hemidactylus fasciatus Gray

1842 (Plate 39A and 39B). A medium-bodied nocturnal forest

gecko. Juveniles have distinct lateral black bands with yellow

borders and a banded white tail. As adults, the black and white

bands fade and the yellow bands remain resulting in a uniform

dark purple body with thin yellow bands. Commonly found

near streams on large rocks and fallen logs, but can also be

found on mountaintops away from water. In other areas they

Amphib. Reptile Conserv. | http://www.herpetofauna.org 033

December 2006 I Volume 4 I Number 1 I e18

Plate 34A. DOI: 1 0.1 51 4/journal.arc.004001 7g041

Plate 31 . DOI: 1 0.151 4/journal.arc.004001 7g038

Plate 33. DOI: 1 0.1 51 4/journal.arc.004001 7g040

Plate 34B. DOI: 1 0.1 51 4/journal.arc.004001 7g042

Plate captions: 29A. Togo Slippery Frog Conraua derooi, Biakpa, Volta Region, Ghana. 29B. Conraua derooi, Biakpa, Volta Region,

Ghana. 30. Crowned Bullfrog Hoplobatrachus occipitalis, Koue River. 31. Broad-banded Grass Frog Ptychadena bibroni, Mole N.P.,

Ghana. 32. Sharp-nosed Grass Frog Ptychadena oxyrhynchus, Comoe, Ivory Coast. 33. Medine Grass Frog Ptychadena pumilio,

Comoe, Ivory Coast. 34A. Rainbow Lizard Agama agama, male, Nkwanta. 34B. Agama agama, female, South Repeater Station.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 034

December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

are common on large forest trees and even in houses within

forests (M.-O. Rodel, unpublished data). A forest species dis-

tributed throughout West Africa.

House Gecko Hemidactylus mabouia (Moreau De

Jonnes 1818) [Plate 40]. Often referred to as the tropical house

gecko. Hemidactylus mabouia is commonly seen feeding near

light sources and is capable of producing a “squeak” sound

used for defense (Gramentz 2000). Similar in appearance and

behavior to H. brookii, but has a longer snout-to-eye distance.

This species is distributed throughout Africa, Madagascar,

and the Seychelles, and is also found in South and North

America (Spawls et al. 2002).

Guinea Leaf-toed Gecko Hemidactylus muriceus

Peters 1870 (Plate 41). A small forest gecko that prefers ter-

restrial habitat. Commonly found in leaf debris and under

logs. Partially diurnal and forages in fine vegetation (Branch

and Rodel 2003). The dorsal surface is highly tuberculate. Its

small body size distinguishes it from H. mabouia and H.

brookii. Henle and Bohme (2003) provide characters for iden-

tifying H. muriceus from species with which it is often

confused. Hemidactylus muriceus is distributed throughout

West and Central Africa.

Uganda Dwarf Gecko Lygodactylus gutturalis (Bocage

1873) [Plate 42], A very small gecko (maximum size up to 9

cm) lacking a claw on the thumb. Mostly diurnal and prefers

arboreal habitats. Their cryptic coloration and small size make

them difficult to detect on trees. This species is distributed

throughout West and Central Africa.

Gerrhosauridae

Rough-scaled Plated Lizard Gerrhosaurus major

Dumeril 1851 (Plate 43). A large lizard with prominently

keeled and armor-like scales. The dorsal surface is laterally

striped yellow and black, whereas the flanks are red and the

ventral surface is cream-colored. The limbs and tail are very

powerful. Can be seen basking on termite mounds in which

they commonly live. This species has been split into an east-

ern and western subspecies, G. m. major, Dumeril, 1851,

and G. m. bottegoi, Del Prato, 1895, respectively.

Gerrhosaurus major is widely distributed throughout Africa

south of the Sahara.

Scincidae

Keeled Water Skink Cophoscincopus cf. simulans (Vaillant

1884) [Plate 44], A small, secretive skink that is the only

semi-aquatic skink in the region. Dark brown and black in

color with a keeled back and tail. Occurs in muddy seeps of

water near streams. Based on their intermediate morphology,

it is unclear whether the specimens at Kyabobo represent C.

simulans or the recently described C. greeri (Bohme et al.

2000). Cophoscincopus simulans is distributed from Sierra

Leone to the Togo Hills.

Short-tailed Writhing Skink Lygosoma brevicaudis

Greer et al. 1985 (Plate 45). A medium-sized skink with

reduced limbs and a thick, chunky appearance, and an espe-

cially truncated tail with a tapering end. A savannah species

that inhabits seasonally variable and xeric habitat (Greer et al.

1985). Our record of Lygosoma brevicaudis in Kyabobo rep-

resents a northeastern range extension of -330 kilometers

based on specimen distributions presented in Greer et al.

(1985). Formerly known from central Ivory Coast to western

and southern Ghana.

Guinea Writhing Skink Lygosoma guineensis (Peters

1879) [Plate 46]. A medium-sized leaf litter skink with

reduced limbs and a cylindrical body. Easily distinguished

from L. brevicaudis by the presence of a longer, narrower tail.

Greer et al. (1985) note that L. guineensis is primarily a forest

species that is capable of penetrating more open savannah

under certain mesic conditions. Distributed throughout West

and Central Africa.

Togo Lidless Skink Panaspis togoensis (Werner 1902)

[Plate 47], A small, slim, leaf-litter skink with well developed

limbs. This species has a moveable lower eyelid with a trans-

parent disk. The color is a dull grey-brown above that

changes to a rusty red color at the hind limbs and tail.

Taxonomic changes based on morphological and ecological

similarities initiated by Broadley (1989) and followed by

Haft (1993) placed many West African species of lidless

skinks into the genus Leptosiaphos, including P. togoensis. A

recent molecular phylogenetic analysis by Schmitz et al.

(2005) based on specimens from Cameroon clarifies the evo-

lutionary relationships of these groups and recommends the

use of P. togoensis. Panaspis togoensis is distributed across

West and Central Africa.

Senegal Mabuya Trachylepis affinis (Gray 1838)

[Plate 48]. A medium-sized skink with a moderately long tail

and fully developed limbs. Adults have a brown back with

dark-brown spots arranged in two pairs of longitudinal rows,

and males have an immaculate white throat. The sides of the

head and neck can have a dull red color. This species may

have a white stripe extending from the upper lip to the groin,

but we did not see this condition in any specimens at

Kyabobo. They are found in a variety of forested and open

savannah habitats. The taxonomic status of T. blandingii, T.

raddonii, and T. ajfinis is unclear (Hoogmoed 1974), and a

rigorous phylogenetic study including all West African

Trachylepis is needed. Trachylepis ajfinis is distributed

across West and Central Africa.

Buettneri’s Long-tailed Mabuya Trachylepis buet-

tneri (Matschie 1893) [Plate 49]. A medium-sized lizard with

a long, slender body and limbs. The tail can reach up to four

times the length of the body. Found in small bushes, rocks

and vegetation in savannah habitat. Distributed from Ivory

Coast to Cameroon.

Speckle-lipped Mabuya Trachylepis maculilabris

(Gray 1845) [Plate 50]. A medium-sized, heavy built skink

with well-developed limbs and a long tail. Dorsal scales of

adults have five to seven keels. Adults are brown with dark

brown to black flanks with a white stripe extending from

under the eye to the forelimbs. The throat is yellow. Diurnal

and found in forested areas or around human settlements.

Trachylepis maculilabris occurs throughout Africa south of

the Sahara.

Teita Mabuya Trachylepis perrotetii (Dumeril and

Bibron 1839) [Plate 51]. A large, heavy skink with short, thick

limbs and a long tail. The color is olive-brown above, and

adults generally have red flanks. Commonly found in savan-

nah areas in grass or basking on low branches and tree trunks.

They usually run up trees when chased, but have also been

Amphib. Reptile Conserv. | http://www.herpetofauna.org 035

December 2006 I Volume 4 I Number 1 I e18

Plate 37.

DOI: 10.151 4/journal. arc. 004001 7g045

Plate 35. DOI: 10.151 4/journal.arc.004001 7g043

Plate 39A. DOI: 10.151 4/journal.arc.004001 7g047

Plate 40. DOI: 10.151 4/journal.arc.004001 7g049

Plate 36. DOI: 10.151 4/journal.arc.004001 7g044

Plate 38. DOI: 10.151 4/journal.arc.004001 7g046

Plate 39B. DOI: 10.151 4/journal.arc.004001 7g048

Plate 41 . DOI: 1 0.151 4/journal.arc.004001 7g050

Plate captions: 35. Senegal Agama Agama sankaranica, Odome. 36. Senegal Chameleon Chamaeleo senegalensis, female, Hoehoe.

37. Fat-tail Gecko Hemitheconyx caudicinctus, Laboum Outpost. 38. Brooke’s House Gecko Hemidactylus brookii, South Repeater

Station. 39A. Banded Leaf-toed Gecko Hemidactylus fasciatus, gravid female, South Repeater Station. 39B. Hemidactylus fasciatus,

juvenile, Middle Control Camp. 40. House Gecko Hemidactylus mabouia, Laboum Outpost. 41. Guinea Leaf-toed Gecko Hemidactylus

muriceus, South Repeater Station.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 036 December 2006 | Volume 4 | Number 1 | e18

Herpetofauna of the Togo Hills

observed to escape into water (Rodel et al. 1997). Distributed

throughout West and Central Africa.

Rainbow Mabuya Trachylepis quinquetaeniata

(Lichtenstein 1823) [Plate 52], A medium-sized skink with

well-developed limbs and long tail. Juveniles and females

have a black dorsum with five white lines extending from

behind the head to base of the tail. The tail is bright blue.

Adult males lose this color pattern and become brown and

acquire a black-blue throat. They are common in savannah

habitats and abundant around human settlements, but not

found in forested areas (Hoogmoed 1974). Trachylepis quin-

quetaeniata is distributed throughout Africa.

Lacertidae

Sawtail Lizard Holaspis guentheri Gray 1863. A small arbo-

real lacertid with a long head and pointed snout. The body and

tail are extremely flattened to aid in gliding between trees in

the forest (Spawls et al. 2002). The dorsum is black with

cream stripes down the sides that fade into a blue tail with

black crossbars. We encountered one specimen in Kyabobo

that was first spotted on the trunk of a large tree near a stream

before it retreated into the forest canopy. Holaspis guentheri

is widely distributed throughout West and Central Africa

(Spawls et al. 2002).

Varanidae

Savannah Monitor Varanus exanthematicus (Bose 1792)

[Plate 53]. This large monitor lizard has a broad head with

prominent ocular ridges. Varanus exanthematicus prefers

savannah habitat and can be spotted in agricultural areas

around Kyabobo. Active diurnally, mostly terrestrial but can

be found under rocks, in termite mounds, and in trees where it

rests. We observed one specimen basking on a termite mound

near Laboum Outpost. This species is CITES appendix II pro-

tected due to its popularity in the pet and skin trade (de

Buffrenil 1993). Distributed from Senegal to western Ethiopia

(Bayless 2002).

Nile Monitor Varanus niloticus (Linnaeus 1758)

[Plate 54], A large black monitor with 6-11 yellow cross-

bars or ocelli on the body (Dunger 1967; Spawls et al.

2002). The tail is laterally compressed with a prominent

vertebral ridge. Commonly found at night sleeping on veg-

etation overhanging streams or pools. Active diurnally, they

are very quick and wary. This species is CITES appendix II

protected due to its popularity in the pet and skin trade (de

Buffrenil 1993). A study by Bayless and Luiselli (2000)

shows microhabitat differences between V. niloticus and V.

ornatus in Nigeria, with the latter being primarily a forest

species. Varanus niloticus is broadly distributed throughout

Africa from Egypt to South Africa, and West to Senegal

(Bayless 2002).

Snakes (Squamata)

Atractaspididae

Reinhardt’s Snake-eater Polemon acanthias (Reinhardt

1860) [Plate 55]. A rare nocturnal burrowing snake with

smooth scales and a short, sharp tail. Polemon acanthias has

grooved rear fangs and is ophiophagous, but probably not dan-

gerous to humans. Many aspects of their natural history

remain unknown due to their secretive habits. Lives in forest

habitats close to water. Conservation status is uncertain, but is

possibly vulnerable due to forest destruction. This snake is

distributed from Guinea to Nigeria (Chippaux 1999).

Colubridae

African Brown Water Snake Afronatrix anoscopus (Cope

1861) [Plate 56]. A medium-sized snake with an overall

olive coloration with yellow ventral coloration. Round and

robust in appearance, A. anoscopus is an aquatic snake

found along streams where it hunts for small vertebrate

prey, mainly frogs. Individuals can be found resting under

rocks in the stream or basking along the bank in forest and

savannah habitat wherever water is available. When cap-

tured, individuals do not hesitate to strike and release musk

from their cloaca. This snake is distributed from Senegal to

Cameroon (Chippaux 1999).

Herald Snake Crotaphopeltis hotamboeia (Laurenti

1768) [Plate 57], A small dark-colored snake, usually black,

grey or olive-green with rear fangs. Transverse rows of small

white spots are present dorsally. Scales on this species tran-

sition from smooth to keeled posteriorly. Commonly active

at night, we observed this species feeding on small frogs of

the genus Phrynobatrachus (in the lab, frogs became inca-

pacitated after being bitten by this snake). Individuals were

found in savannah habitat near bodies of water. Defensive

displays for this snake include an intricate combination of

flattening the head into a triangular form (viper-shaped) fol-

lowed by hissing and striking (Spawls et al. 2002). This

snake is distributed broadly throughout Africa south of the

Sahara (Spawls et al. 2002).

Matschie’s African Ground Snake Gonionotophis

klingi Matschie 1893 (Plate 58). Gonionotophis klingi is

small, dark, and subtriangular in cross section with a

prominent longitudinal row of dorsal vertebral scales.

Body scales are keeled with ventral scales lighter in col-

oration than dorsal scales. Members of the genus

Gonionotophis differ from the very similar and closely

related genus Mehelya through the presence of a continu-

ous row of maxillary teeth (Loveridge 1939). These snakes

are slow-moving and nocturnal. Their diet consists mostly

of terrestrial amphibians. Possibly threatened due to

destruction of forest habitat. This snake is distributed from

Guinea to Nigeria (Chippaux 1999).

Striped House Snake Lamprophis lineatus (Dumeril et

al. 1854) [Plate 59]. A medium-sized snake with smooth

scales, a triangular- shaped head and relatively large eyes with

vertical pupils. They are nocturnal and feed primarily on

lizards and frogs, but occasionally eat small mammals

(Chippaux 1999). Lamprophis lineatus is distributed through-

out West and Central Africa.

Blotched Wolf Snake Lycophidion nigromaculatum

(Peters 1863) [Plate 60]. A small terrestrial forest snake with

a distinct broad head and vertical pupils. The body is sub-tri-

angular in cross section. Individuals are orange dorsally with

black diamond- shaped markings staggered down their back.

The venter is dark grey. The head and “neck” region are

Amphib. Reptile Conserv. | http://www.herpetofauna.org 037

December 2006 I Volume 4 I Number 1 I e18

Plate 44. DOI: 10.151 4/journal.arc.004001 7g053

Plate 48. DOI: 10.151 4/journal.arc.004001 7g057

Plate 43. DOI: 10.151 4/journal.arc.004001 7g052

Plate 45. DOI: 10.151 4/journal.arc.004001 7g054

Plate 47. DOI: 10.151 4/journal.arc.004001 7g056

Plate 49. DOI: 10.151 4/journal.arc.004001 7g058

Plate captions: 42. Uganda Dwarf Gecko Lygodactylus gutturalis, Nkwanta. 43. Rough-scaled Plated Lizard Gerrhosaurus major, Mole

N. P., Ghana. 44. Keeled Water Skink Cophoscincopus cf. simulans, Waterfall east of Laboum Outpost. 45. Short-tailed Writhing Skink

Lygosoma brevicaudis, South Repeater Station. 46. Guinea Writhing Skink Lygosoma guineensis, Middle Control Camp. 47. Togo

Lidless Skink Panaspis togoensis, Comoe, Ivory Coast. 48. Senegal Mabuya Trachylepis affinis, Tai, Ivory Coast. 49. Buettneri’s Long-

tailed Mabuya Trachylepis buettneri, Comoe N. P., Ivory Coast.

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December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

retracted backward onto the body to form an S-shape, which

they maintain when striking at a predator. Leston and Hughes

( 1 968) revived this species from synonymy with L. irroratum.

Lycophidion nigromaculatum is distributed from Guinea to

Ghana (Chippaux 1999).

Forest Marsh Snake Natriciteres variegata (Peters

1861) [Plate 61]. A harmless snake with a small head, round

pupils, and relatively short tail. Semi-aquatic and eats frogs.

We found one juvenile specimen (116 mm snout- vent length;

1.1 g) under leaf litter in the forest. The range spans from

Guinea to Cameroon (Hughes and Barry 1969).

Variable Green Snake Philothamnus heterodermus

(Hallowell 1857) [Plate 62], A green arboreal snake with

large, round pupils and a slightly upturned lip. Scales are

smooth with 15 midbody scale rows and a relatively long tail

(approximately 25% total length). Body scales have a con-

cealed white spot. According to Hughes and Barry (1969), P.

heterodermus can be distinguished from congeners by the

presence of an entire anal plate along with 2+ temporal

scales. This is a slender and fast species with both green and

brown phases. Spawls et al. (2002) mention a Ghanaian sur-

vey of this species where brown individuals spent more time

on the ground while green individuals spent more time on

trees during the dry season. This is a diurnal snake whose

main food consists of frogs. Distribution ranges from Guinea

to Uganda and Angola.

Spotted Bush Snake Philothamnus semivariegatus

(Smith 1847) [Plate 63]. A large, slender snake with black

dorsal crossbars. The appearance of an eyebrow is given by

the presence of its raised supraocular scale. Body is cylindri-

cal with a long tail, ranging from 25-35% of total body

length. Scales are smooth with 15 midbody scale rows.

Hughes and Barry (1969) diagnose this species from its con-

geners by the presence of 183-199 ventral scales with 1 +

temporal scales. Ventral scales are yellowish or bright green.

Ventral scales are also strongly keeled. This is a diurnal

snake that is very agile in trees, bushes and shrubs. According

to Spawls et al. (2002), the diet of this snake consists mainly

of lizards. This snake is widely distributed throughout Africa

south of the Sahara.

Olive Grass Racer Psammophis phillipsi (Hallowell

1844) [Plate 64], A large, fast diurnal snake that feeds pri-

marily on lizards. Found in savannah habitats and around

villages and agricultural areas. This species, as well as oth-

ers belonging to the genus, have the ability to “break off’

their tail when in danger as an escape mechanism (without

regeneration). Psammophis phillipsi has been considered by

many to be a complex of species due to its wide range

throughout Africa and seemingly diagnosable characters for

groups within.

Rukwa Sand Racer Psammophis rukwae Broadley

1966 (Plate 65). A fast-moving, rear-fanged diurnal snake

that is both terrestrial and arboreal. It is slender with a long

tail. Scales are smooth with 17 midbody scale rows and 148

to 183 ventrals. Anal plate is divided. This species is diag-

nosed from its congeners by its very fine black ventral lines

and by having the first five lower labials usually in contact

with the anterior sublinguals (Spawls et al. 2002). This

species is mainly a savannah inhabitant and distributed from

Senegal to Tanzania.

Large-eyed Green Treesnake Rhamnophis

aethiopissa Gunther 1862 (Plate 66). A slender arboreal

snake with a relatively short snout and large prominent eyes

with round pupils and a golden iris. The lip curves upward

posteriorly, giving the snake the impression of smirking.

Each scale has a black border, which gives the snake a

striped or checkered appearance. This snake reaches a

length of over one meter, and the tail is approximately 33%

of the total length. This species inhabits primary forest.

When in defensive posture, this snake laterally compresses

its neck, hisses, and strikes. It is suspected to be primarily a

frog eater. Distributed throughout West and Central Africa

(Chippaux 1999).

Elapidae

Black Forest Cobra Naja melanoleuca Hallowell 1857

(Plate 67). A large, thick-bodied cobra reaching 2.5 m with a

large head and yellow throat with black crossbars. The chin

and ventral parts of the belly are cream and/or white. In Ghana

it is found in well-forested habitat. This snake is agile and

active day and night. It can be found hiding among piles of

brush, rocks, hollow logs, and holes. A very deadly snake,

which can be aggressive when approached. It eats a wide vari-

ety of vertebrates, from frogs to monitor lizards and

mammals. Possibly threatened due to intense pressure from

humans who view the cobra as a threat and go out of their way

to kill them. This snake is widely distributed across the

afrotropics (Spawls et al. 2002).

Pythonidae

Royal Python Python regius (Shaw 1802) [Plate 68]. A very

muscular snake that is relatively small (reaching just over one

meter) with an elongate snout that is broader at the jaws. The

iris is yellow with vertical pupils and has black with golden-

yellow marbling dorsally. The tail is short, and males possess

spurs lateral to the cloacal opening. It is a slow-moving snake

that is active at night when it comes out to hunt for small

warm-blooded prey, which it sees with its heat-sensing

infrared pits that line its upper lip. This species is mainly

found in dry grassland habitat or moist savannahs. It is dis-

tributed throughout West and Central Africa and is commonly

exported for the pet trade (Spawls et al. 2002).

Typhlopidae

Spotted Blind Snake Typhlops punctatus (Leach 1819)

[Plate 69]. A small and secretive fossorial snake. Its natural

history still remains elusive, except for the fact that they are

one of the largest typhlopids, reaching up to 66 cm total

length. It has an obvious eye under the ocular scale and has 30

to 32 midbody scale rows with 374-465 scales in a mid-dor-

sal longitudinal series (Spawls et al. 2002). The coloration is

dark brown to grey dorsally with a yellow spot on the posteri-

or margin of each scale. Mainly fossorial, but can be found at

night when they are active on the surface. Although primarily

considered a lowland savannah inhabitant, we found speci-

mens on mountain tops (-800 m) predominated by savannah

vegetation. Presumed to feed on termites like other members

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December 2006 I Volume 4 I Number 1 I e18

Plate 50. DOI: 10.151 4/journal.arc.004001 7g059

Plate 52. DOI: 10.151 4/journal.arc.004001 7g061

Plate 54. DOI: 10.151 4/journal.arc.004001 7g063

Plate 56. DOI: 10.151 4/journal.arc.004001 7g065

Plate 51 . DOI: 1 0.151 4/journal.arc.004001 7g060

Plate 53. DOI: 10.151 4/journal.arc.004001 7g062

Plate 55. DOI: 10.151 4/journal.arc.004001 7g064

Plate 57. DOI: 10.151 4/journal.arc.004001 7g066

Plate captions: 50. Speckle-lipped Mabuya Trachylepis maculilabris, South Repeater Station. 51. Teita Mabuya Trachylepis perrotetii,

Mole N. P., Ghana. 52. Rainbow Mabuya Trachylepis quinquetaeniata, South Repeater Station. 53. Savannah Monitor Varanus exan-

thematicus, Mole N.P., Ghana 54. Nile Monitor Varanus niloticus, Laboum Outpost. 55. Reinhardt’s Snake-eater Polemon acanthias,

forest stream near Laboum Outpost. 56. African Brown Water Snake Afronatrix anoscopus, Laboum Outpost. 57. Herald Snake

Crotaphopeltis hotamboeia, Comoe, Ivory Coast.

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December 2006 I Volume 4 I Number 1 I e18

Herpetofauna of the Togo Hills

of its family. For a summary of the taxonomic discussion of

the T. punctatus complex see Branch and Rodel (2003). This

snake is distributed throughout West and Central Africa.

Viperidae

Spotted Night Adder Causus maculatus (Hallowell 1842)

[Plate 70]. A stout, thick-bodied viper with a short tail, round

pupils, and a rounded snout. Predominantly found in savan-

nah habitat, but it can also be found in forests. Its dorsal

coloration is light brown, dark tan or light olive with dark,

diamond-shaped vertebral markings. A V-shape is present on

the top of the head with the apex oriented anteriorly. The

head is slightly differentiated from the girth of the body, not

a distinctive triangular head like most vipers. Nine large

scales are present on the top of the head, unlike most vipers

(Spawls et al. 2002). Scales are lightly keeled. Belly is white

or cream in coloration. Locomotion is very slow, and it is

active at various times of the day and night. It inhabits many

human disturbed areas and is responsible for many snake

bites of humans. Distributed throughout West Africa to

Angola (Chippaux 1999).

Crocodiles (Archosauria)

Dwarf Crocodile Osteolaemus tetraspis Cope 1861 (Plate

71). Combined with its small size, robust appearance, and

broad snout, Osteolaemus tetraspis is easily distinguishable

from other crocodilians. It inhabits small rivers, and we

observed one individual in a remote forest stream in

Kyabobo. This is the first report of this CITES appendix I

species for Kyabobo National Park. This species is wide-

spread in the forests of West and Central Africa (Spawls et

al. 2002).

Results and discussion

With a total of 65 reptile and amphibian species, Kyabobo

National Park is one of the most diverse sites surveyed in

Ghana. Raxworthy and Attuquayefio (2000) surveyed the

herpetofaunal community at Muni Lagoon in the Volta

Region of Ghana during the peak of the rainy season and

found up to 26 species at a site. Leache (2005) surveyed

three sites located in the Northern, Brong-Ahafo, and

Greater Accra Regions of Ghana during the dry season and

found up to 30 species at a site. While surveys that focused

specifically on amphibian diversity in southwestern Ghana

documented up to 47 species, they were not restricted to a

single site, but rather encompassed a broad geographic area

(Rodel and Agyei 2003; Rodel et al. 2005). All of these stud-

ies predicted higher species abundance at their sites based on

non-asymptotic species accumulation curves and/or compar-

isons to historical data. Additional species, especially

snakes, certainly inhabit Kyabobo National Park. Their

absence from our survey does not necessarily indicate that

they are not present, but rather that they are secretive and/or

difficult to find. Long-term herpetological surveys in the

neotropics indicate that a great deal of effort is necessary to

detect every species at a site (Duellman 2005; Myers and

Rand 1969). In addition, we only surveyed during the rainy

season, and seasonality has some effect on the abundance of

different species of reptiles and amphibians in Ghana

(Hughes 1988). Thus, continued survey work in Kyabobo

National Park is warranted.

A recent biodiversity survey of amphibians of the entire

Volta Region recorded 31 amphibian species, including 20

species from the area including Kyabobo National Park

(Rodel and Agyei 2003). We found 26 frogs at Kyabobo. Of

the six new records, five are a subset of the 31 recorded

throughout the entire Volta Region ( Hemisus sp.,

Phrynobatrachus plicatus, Hyperolius baumanni, H. fusciven-

tris, and Afrixalus dorsalis ), and one ( Afrixalus weidholzi ) is a

new record for the Togo Hills. The amphibians absent from

our surveys in the Togo Hills include some that are adapted to

fast-running water or large closed forests, like Conraua derooi

and Bufo togoensis. Recently, C. derooi was discovered in the

Togo Hills (A. Hillers et al., unpublished data). In addition,

we have unconfirmed reports from people in Shiare village

that a frog fitting the description of C. derooi might live in

nearby Togo. Hence, the presence of suitable habitat in

Kyabobo makes the detection of these highly threatened

species possible.

We recorded 39 species of reptiles in our survey (22

lizards, 16 snakes, and one crocodile). Unfortunately, a lack

of historical data on the diversity of reptiles in the Togo Hills,

and no records from Kyabobo National Park, make area com-

parisons difficult. Some of the reptile species we found at

Kyabobo were not surprising, given their occurrence in a

broad variety of habitats and wide distribution throughout

West Africa. However, we did detect nine forest-restricted

reptiles in Kyabobo known primarily from other West African

forest blocks (Table 1). In general, we can assume that many

of our records are new for the area and therefore represent

range extensions. For instance, our observation of the dwarf

crocodile ( Osteolaemus tetraspis ) is the first report of this

CITES appendix I species for Kyabobo National Park, and our

record of Lygosoma brevicaudis in Kyabobo represents a

range extension of -330 kilometers based on specimen distri-

butions presented in Greer et al. (1985).

Most reptiles and amphibians in Kyabobo National Park

that are connected to forest habitats should be considered

threatened. While many reptiles and amphibians thrive in

human-disturbed areas, others are restricted to specific micro-

habitat types and do not persist in the face of habitat

destruction. Given this setting, preserving sensitive habitats is

the most effective method of conserving reptiles and amphib-

ians. In particular, the forest habitats in Kyabobo, and

specifically the forests bordering the streams and rivers,

should be considered sensitive areas. Some frogs appear to

inhabit and breed exclusively in these areas (e.g., Hyperolius

torrentis, Phrynobatrachus plicatus , Amnirana albolabris,

and Leptopelis hyloides ). We can assume that these species

once had widespread distributions throughout the Togo- Volta

highlands, but habitat modification has all but eliminated them

from most areas. Successful conservation of these species

equates to protecting their forest stream habitats. Any destruc-

tion to this habitat type, such as clearing of forest or increasing

sedimentation in the water, could have damaging effects on

the herpetofauna, especially to the breeding amphibian popu-

lations. Thus, focusing attention on this specific habitat type

could benefit multiple species simultaneously.

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December 2006 I Volume 4 I Number 1 I e18

Plate 58. DOI: 10.151 4/journal.arc.004001 7g067

Plate 60. DOI: 10.151 4/journal.arc.004001 7g069

Plate 62. DOI: 10.151 4/journal.arc.004001 7g071

Plate 64. DOI: 10.151 4/journal.arc.004001 7g073

Plate 61 . DOI: 1 0.151 4/journal.arc.004001 7g070

Plate 63. DOI: 10.151 4/journal.arc.004001 7g072

Plate captions: 58. Matschie’s African Ground Snake Gonionotophis klingi, forest habitat northeast of South Repeater Station. 59.

Striped House Snake Lamprophis lineatus, Comoe, Ivory Coast. 60. Blotched Wolf Snake Lycophidion nigromaculatum, Middle Control

Camp. 61. Forest Marsh Snake Natriciteres variegata, forest stream near Laboum Outpost. 62. Variable Green Snake Philothamnus het-

erodermus, Tai, Ivory Coast. 63. Spotted Bush Snake Philothamnus semivariegatus, near Laboum Outpost. 64. Olive Grass Racer

Psammophis phillipsi, male, Nkwanta. 65. Rukwa Sand Racer Psammophis rukwae, Nkwanta.

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December 2006 I Volume 4 I Number 1 I e18

Plate 67. DOI: 1 0.1 51 4/journal.arc.004001 7g076

Plate 68. DOI: 1 0.1 51 4/journal.arc.004001 7g077 Plate 69. DOI: 1 0.1 51 4/journal.arc.004001 7g078

Plate 70. DOI: 1 0.1 51 4/journal.arc.004001 7g079 Plate 71 . DOI: 1 0.1 51 4/journal.arc.004001 7g080

Plate captions: 66. Large-eyed Green Treesnake Rhamnophis cf. aethiopissa, Ankasa National Park, Ghana. 67. Black Forest Cobra

Naja melanoleuca, Comoe, Ivory Coast. 68. Royal Python Python regius, Keri. 69. Spotted Blind Snake Typhlops punctatus, South

Repeater Station. 70. Spotted Night Adder Causus maculatus, Nkwanta. 71. Dwarf Crocodile Osteolaemus tetraspis, Comoe, Ivory

Coast.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 043 December 2006 | Volume 4 | Number 1 | e18

Herpetofauna of the Togo Hills

Figure 3. The three resolved phylogenetic hypotheses for the

evolutionary history of forest-restricted species in Western

Africa, assuming exclusivity of each forest block.

DOI: 1 0.1 51 4/journal.arc. 004001 7g081

Compared to the 47 amphibian species documented in the

southwestern forests of Ghana (Rodel et al. 2005), the Togo Hills

harbor less diversity with 26 species. The climatological and geo-

logical history of the forests themselves may explain present day

patterns of organismal diversity. During the last glacial maximum

the expansion of dry forest and savannah fragmented rain forests

reduced the size and extent of rain forest habitat within the Togo

Hills to a minimum (Dupont et al. 2000). Larger blocks of forest

persisted along the coast to the west of Ghana and in Central

Africa. These areas may have experienced less retraction and

therefore maintained higher species diversity. Thus, a positive

correlation may exist between forest patch size during the

Pleistocene and present-day biodiversity. This hypothesis should

be scmtinized more closely using genetic data from multiple, co-

distributed forest species restricted to forest habitat, but with

distributions spanning West Africa. Feasible target species fitting

these criteria include Leptopelis hyloides, Phrynobatrachus pli-

catus, Amnirana albolabris, Hemidactylus fasciatus, Panaspis

togoensis, Gonionotophis klingi, Rhamnophis aethiopissa, and

Osteolaemus tetraspis. Genetic data will provide a more sensitive

measure of diversity for these forest-restricted species and facili-

tate the estimation of divergence dates between lineages. In

addition, a comparative phylogeographic approach will enable us

to determine whether co-distributed forest species have shared

evolutionary histories (Fig. 3). Our surveys have contributed to

the sampling essential for comparative biogeographic research of

the herpetofauna in this complex biodiversity hotspot.

Acknowledgments. — We thank the Wildlife Division in

Accra for granting us permission to conduct research in the

National Parks of Ghana. We are grateful to Peter Howard, Pete

Hartley, and Phil Marshall at the IUCN for their help coordi-

nating and funding our survey work in 2005. We thank John

Mason, Executive Director of the Nature Conservation

Research Centre, for providing logistical support in Accra. We

are also grateful to the Museum of Vertebrate Zoology for sup-

porting our 2004 expedition. We especially want to thank

Baturi Ali and Anne Leache for their help collecting and prepar-

ing specimens. We thank Mark Bayless, Robert Drewes, Craig

Hassapakis, Jim McGuire, Ted Papenfuss, and Jack Sites for

useful discussions and comments on this manuscript.

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Manuscript received: 8 November 2005; Accepted: 20 December

2005; Published: 26 December 2006

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the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduc-

tion in any medium, provided the original author and source are credited.

Amphibian and Reptile Conservation 4(1):46-59.

DOI: 10.151 4/journal. arc. 004001 4 (2407KB PDF)

Land use and anuran biodiversity in southeast

Kansas, USA

LEWIS R. ANDERSON AND JOSEPH A. ARRUDA 1

Department of Biology’, Pittsburg State University, Pittsburg, Kansas 66762-7552, United States of America

Abstract .— The relationship of anuran breeding site biodiversity to land use was examined in southeast

Kansas, USA. Eight breeding pools or temporary ponds were sampled from March to July 1995. Each site has

some adjacent woodland, but varied in the remaining adjacent land use. Two sites were relatively unimpact-

ed reference or “natural” sites, two were impacted by abandoned coal or lead/zinc mines, and four were

impacted by cropland. Adult density was determined with visual and audio censuses. Tadpoles were exam-

ined for malformations and density was estimated. Eggs were collected from the sites, hatched in the

laboratory, and examined for malformations. Total audio anuran density was statistically higher (ANOVA,

P<0.05) in natural area breeding pools (1,048.7/ha) compared to pools in agricultural (519.0/ha) and mined

areas (164.8/ha). Visual densities followed the same pattern (459.9/ha natural > 31 5.1 /ha agricultural >

262.0/ha mined) but were not statistically different. Tadpole densities were significantly (P<0.05) higher in nat-

ural area breeding pools (137.6/m 2 ) compared to agricultural (59.4/m 2 ) and mined areas (28.5/m 2 ). The

percentage of tadpoles with malformations was significantly lower (P<0.05) in natural areas (0.4%) compared

to agricultural (4.6%) and mining (8.3%). Malformations found in the field included spinal cord, optic, edemas,

and tumors. Eggs incubated from natural sites had significantly (P<0.05) higher percentages of eggs hatch-

ing successfully (98.8%) and lower percentages of tadpoles with malformations (17.5%) than did eggs from

agricultural (88.2% and 51.0%, respectively) and mined areas (40.4% and 76.1%, respectively). Eggs incubat-

ed from natural sites also had the lowest malformation rate (17.5%) compared to eggs from agricultural sites

(51.0%) and mined sites (76.1%), but these differences were not statistically different. These data provide evi-

dence for the link between land use and the individual and population characteristics of anurans in breeding

pools.

Key words. Amphibian, anuran, land use, tadpole, watershed, biodiversity, malformations

Citation: Anderson, L. R. and Arruda, J. A. 2006. Land use and anuran biodiversity in southeast Kansas, USA. Amphib. Reptile Conserv. 4(1):46-59(e14).

Introduction

The reasons for declines in amphibian populations (Blaustein

and Wake 1990; Wake 1991) are complex, and include dis-

eases, ultraviolet radiation, pollutants, and habitat

modifications (Alford and Richards 1999). In spite of many

changes to the natural landscape and land use in southeast

Kansas, the region supports a greater diversity of anurans —

17 species — than the rest of the state (Conant and Collins

1993). Hecnar and M’Closkey (1996) showed regional differ-

ences in amphibian species richness related to land use history.

Southeast Kansas is also an ecotone between eastern decidu-

ous forests and prairie, and is at the edge of distribution for

many anuran species. Anuran populations that reside in

peripheral areas such as this are of considerable interest to

many biologists and geneticists who study divergence and spe-

ciation (Ptacek 1984).

The conversion of the rural landscape in southeast

Kansas, as elsewhere, from pre-settlement conditions may

adversely affect breeding and nonbreeding habitats and water

quality in anuran breeding pools. Small wetlands are important

to juvenile recruitment and their loss and increased isolation

can have a negative effect on rescue efforts (Semlitsch and

Bodie 1998). Such isolation influences the probability of dis-

persal among wetlands and is one of the critical factors in

managing aquatic-breeding amphibians (Semlitsch 2000).

Development of road networks, such as the many rural roads

constructed on section lines (Public Land Survey System) in

Kansas, can be responsible for fragmentation as well as direct

mortality (Fahrig et al. 1995; Vos and Chardon 1998). But

direct water quality impacts on breeding pools can occur as

well. Agricultural runoff can carry fertilizers, pesticides, and

sediments. Underground and strip-mining of coal, lead, and

zinc earlier this century in southeast Kansas has left piles of

mine tailings. Leachate from mined areas can be acidic and

contain elevated concentrations of metals.

The goal of this project was to assess the relationship

between adjacent land use and the biodiversity of anurans

inhabiting breeding pools. The specific objectives were to (1)

identity breeding pools with different surrounding land uses,

(2) estimate adult anuran density, (3) estimate the density of

and malformation rates in tadpoles, and (4) estimate the hatch-

Correspondence. 1 Tel: (602) 235-4738, fax: (620) 235-4194, email: jarruda@pittstate.edu

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Land use and anuran biodiversity

Figure 1. Locations of study sites in southeast Kansas.

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Plate 1. View of site N1 in Bourbon County, Kansas. A shallow

artificial pond chiefly fed by a small ephemeral stream that

originates in and runs through a meadow and a wooded area.

DOI: 10.151 4/journal. arc. 004001 4g002

ing success of eggs and the malformation rates of their

hatched tadpoles incubated in the laboratory.

Plate 2. View of site N2 in Cherokee County, Kansas. A shal-

low artificial pond fed by runoff from a mature woodland area.

DOI: 1 0.1 51 4/journal. arc. 004001 4g003

Plate 3. View of site A1 in Bourbon County, Kansas. A shallow

man-made pond adjacent to a plowed crop field.

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Plate 4. View of site A2 in Cherokee County, Kansas. A natu-

ral wetland surrounded on three sides by a plowed crop field.

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Methods

Study area and sites

The study area is located in the Osage Cuestas physio-

graphic region in three counties in southeast Kansas USA

(Figure 1). Site selection focused on finding anuran breed-

ing pools located in “micro-watersheds” with different

immediate surrounding land uses. Three land uses were

considered: agricultural, mined, and natural. Agricultural

areas were plowed fields and row crops. Areas with live-

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December 2006 I Volume 4 I Number 1 I e14

L. R. Anderson and J. A. Arruda

Plate 5. View of site A3 in Cherokee County, Kansas. A natural pool on the edge of a plowed crop field.

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Plate 6. View of site A4 in Cherokee County, Kansas. An artifi-

cial wetland in the middle of a plowed crop field.

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stock were not used. Mined areas were on land that had

clear signs of previous mining activity, including mine tail-

ings. Natural areas were defined as lands with no

cultivation, grazing, or mining activities occurring within

the micro-watershed now or in the recent past, and approx-

imating an undisturbed vegetative cover.

Over 70 potential sites were evaluated according to water

depth, vegetation, percentage of the land use category in the

micro- watershed, and availability of adjacent non-breeding

habitats. The final sites chosen included eight sites in three

Plate 7. View of site Ml in Crawford County, Kansas. A shal-

low pool chiefly fed by a small ephemeral stream that

originates in and runs through land that was previously mined

for coal.

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land use categories: four agricultural sites, two mined land

sites, and two natural sites. All sites, except one (Al ), are on

private property.

The first natural site (Nl ) is a shallow artificial pond

(Plate 1). The pond is fed by a small ephemeral stream that

originates in and runs through a meadow and a wooded area

before entering the pond. Runoff from the surrounding wood-

ed area also feeds the pond. The area around the pond is

undergoing succession and consists of dense cedars, brush,

small and medium sized trees, and grasses. Mature forest lies

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December 2006 I Volume 4 I Number 1 I e14

Land use and anuran biodiversity

just to the south and the area has never been cultivated. N2 is

a shallow artificial pond (Plate 2). The pond is fed by runoff

from a surrounding mature woodland area. An area of grasses

mixed with small trees and dense brush is located just north of

the pond and a grassed area is located to the south.

The first agricultural site, Al, is a shallow man-made

pond adjacent to a plowed crop field on the Hollister Wildlife

Area owned by the State of Kansas (Plate 3). The pond is fed

by runoff from the field where sunflowers were grown.

Adjacent to the other sides of the pond are a prairie, a dense-

ly wooded area, and an ephemeral stream. This site is

probably the least intensively cultivated site of all the agricul-

tural sites. Agricultural site A2 is a natural wetland (Plate 4)

fed by runoff from a crop field where soybeans were grown.

The field surrounds the wetland on three sides while small to

medium sized trees, aquatic and wet soil plants, and grasses

are adjacent to the wetland on the fourth side. Woodlands are

nearby to the east and west. Agricultural site A3 is a natural

pool at the edge of a plowed crop field (Plate 5). The pool is

fed by runoff from the field where soybeans were grown. On

the opposite side of the pool from the crop field is a grassed

area with dense brush and small trees. Adjacent to the north

end are mature woodlands next to a creek. The last agricultur-

al site, A4, is an artificial wetland in the middle of a plowed

crop field (Plate 6). The wetland is fed by runoff from the field

where soybeans were grown in 1995. A dense growth of small

trees is present on both sides in the wetland. A grassed area is

adjacent to the wetland, and woodlands lie adjacent to the

south, the east, and the west.

The first mined site, Ml, is a shallow pool fed by a small

ephemeral stream (Plate 7) located on a partially reclaimed

coal mine now managed by Pittsburg State University as part

of the Monahan Outdoor Education Center. The stream origi-

nates in and runs through land that was previously mined for

coal and by smaller amounts of runoff from the immediate

wooded area. The area adjacent to the pool is undergoing suc-

cession with trees of varying sizes and dense brushy

vegetation. Native grass areas are adjacent. The last mined

site, M2, is a man-made pool at the edge of a pile of mining

spoils (chat) left over from lead and zinc mining activities that

occurred earlier in this century (Plate 8). The pool is fed by

runoff from the chat piles. Adjacent to the pool are cattails,

dense brush, grasses, and trees of varying sizes. A wooded

area next to a creek is just west of the pool.

Sample collection

Sampling started on 13 March 1995 with each site sampled

at two-week intervals for a total of seven samples per site

ending on 30 June 1995. Sampling took place in the

evenings starting approximately one hour after sunset. All

tasks were performed in the same order by the same person

during each sample event at each site. A miner’s head light

was used for illumination.

At each site, the pool was approached quietly with the

light dimmed in order to tape record the calls of adult anuran

males and count them. If the number of calling anurans was

low, it was possible to stand in one or a few spots and count

the different individuals. If the number of calling anurans was

high, multiple parallel transects were slowly walked with the

light dimmed as much as possible (modified from Heyer et al.

1994). Every attempt was made to avoid counting the same

individual twice. Anurans were recorded by species and num-

ber of individuals in order to estimate density.

Visual census of adults consisted of walking along mul-

tiple parallel transects and counting the anurans encountered

on both sides of the transect (modified from Heyer et al.

1994). Transects were approximately two meters apart.

Anurans were recorded by species and number of individuals

in order to estimate density.

During sample period three, the tadpoles in the pools had

reached a size large enough to be handled briefly and were

sampled. Tadpole sampling was performed throughout the

remainder of night sampling periods and in addition, each site

was visited and tadpoles sampled during the daylight twice in

July approximately two weeks apart.

Tadpole sampling was performed along the edges of

two adjacent sides of each sample site. The other two sides

of each sample site were sampled during alternate sampling

events. Tadpole sampling was performed every five meters

(m) at smaller sites and every 10 m at larger sites. Five m

is the minimum distance recommended to avoid sampling

the same tadpoles more than once (Heyer et al. 1994).

Tadpoles were trapped with a plastic storage container with

its bottom cut out (24.5 by 38 centimeters, cm). They were

removed with a dipnet, counted, examined for malforma-

tions, and released. Numbers of individual tadpoles and

numbers and types of malformations were recorded.

Malformations were classified based on the system in the

Frog Embryo Teratogenesis Assay Xenopus (FETAX,

Bantle et al. 1991).

When found, the eggs of non-threatened and non-endan-

gered species were collected, brought back to the laboratory,

and incubated at 18°C. The eggs were kept in glass beakers

with water collected from the site. Water was changed daily

using site water kept in a refrigerator (Bantle 1995). Necrotic

eggs were removed at the same time.

After the eggs hatched, any remaining necrotic eggs

were removed and counted, followed by fixation in 10% for-

malin for 24 hours (Hull 1995) and preservation in 70%

ethanol to preserve them. Newly hatched tadpoles were

killed using tricaine methanesulfonate (MS-222) added

directly to the beaker to relax the tadpoles and avoid unnat-

ural contortions. Tadpoles were fixed and preserved as for

the necrotic eggs.

Preserved tadpoles were then counted and examined for

malformations at 15X. Malformation types and number of indi-

viduals were recorded in order to calculate the percent of tadpoles

hatching successfully and the percent with malformations.

Fixation, examination methods, malformation types, and malfor-

mation data sheets were modeled after Bantle et al. (1991).

Data analysis

Adult density and field tadpole data were analyzed as a two-

way ANOVA with interaction using land use group (natural,

agricultural, mined) and sampling period (seven biweekly

samples) as main effects. Audio and visual counts (the total

count or by individual species) were expressed as density

(numbers per hectare, ha) using average breeding pool area.

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December 2006 I Volume 4 I Number 1 I e14

L. R. Anderson and J. A. Arruda

Table 1. Species present (X) with species richness at each site and land use group. Site codes are mapped in Figure 1.

Species

Mined

Agricultural

Natural

Acris crepitans

Bufo americanus

Gastrophryne carolinensis

Hyla versicolor/chrysoscelis

Pseudacris crucifer

Pseudacris triseriata

Rana areolata

Rana catesbeiana

Rana sphenocephala

TOTAL

LAND USE

DOI: 10.151 4/journal. arc.004001 4t001

Field tadpole data included tadpole density (numbers per

square meter, m 2 ) and the percentage of field tadpoles with

malformations.

Laboratory tadpole data included both percent eggs

hatched and percentage tadpoles malformed. These data were

analyzed with a one-way ANOVA using land use group as the

main effect. Laboratory tadpole data from different sample

periods were pooled by site because eggs were not consistent-

ly found at all sites in all sample periods. The percentages of

types of specific malformations were pooled by land use and

so were not analyzed statistically.

All percentage data were arcsine transformed before

analysis (Zar 1996). As a result, standard errors from percent-

age data are asymmetrical and both lower and upper standard

errors are presented in data tables. The general linear models

procedure in SAS was used for all analyses (SAS 1988) and a

significance level of 0.05 was used, except as noted.

Results

Species found

Nine species of anurans were found during visual and audio

sampling of adults (Table 1). Overall, agricultural and natural

sites both yielded the same nine species but the species pres-

ent varied at each site. At agricultural sites, species richness

varied from three to eight, and while species richness was

Table 2. Adult density by land use group. Data are numbers per hectare. C is census type: A = audio, V = visual. Within each line,

means with different lower case letters are significantly different (P<0.05, except for northern spring peeper where P=0.06).

Species

Mined

Mean (SE)

Agricultural

Mean (SE)

Natural

Mean (SE)

Rana sphenocephala

23.2 (29.8) a

77.2 (21.1) a

59.7 (29.8) a

47.0 (39.8) a

102.7 (28.2) a

65.9 (39.8) a

Pseudacris triseriata

3.4 (12.6) a

38.5 (8.9) b

0.0 (12.6) a

3.4 (7.1) a

17.7 (5.0) a

1.9 (7.1) a

Bufo americanus

8.4 (24.0) a

29.0 (17.0) a

43.4 (24.0) a

42.1 (19.1) a

28.8 (13.5) a

33.9 (19.1) a

Acris crepitans

129.8 (148.0) a

250.9 (104.7) a

546.4 (148.0) a

126.8 (48.6) a

91.0 (34.4) a

186.8 (48.6) a

Pseudacris crucifer

0.0 (62.9) b

4.2 (44.5) b

177.1 (62.9) a

0.0 (9.6) b

1.4 (6.8) b

50.5 (9.6) a

Hyla versicolor/chrysoscelis

0.0 (41.0) b

106.6 (29.0) a

202.0 (41.0) a

0.0 (13.1) c

38.6 (9.3) b

100.3 (13.1) a

Rana catesbeiana

0.0 (7.5) a

7.7 (5.3) a

9.1 (7.5) a

42.7 (13.9) a

28.1 (9.9) a

12.4 (13.9) a

Rana areolata

0.0 (5.1) a

4.2 (3.6) a

9.5 (5.1) a

0.0 (4.9) a

6.3 (3.4) a

5.7 (4.9) a

Gastrophryne carolinensis

0.0 (0.8) a

0.5 (0.5) a

1.7 (0.8) a

0.0 (0.8) a

0.5 (0.5) a

1.7 (0.8) a

Total density

164.8 (198.3) b

519.0 (140.2) b

1048.7 (198.3) a

262.0 (86.0) a

315.1 (60.8) a

459.0 (86.0) a

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December 2006 I Volume 4 I Number 1 I e14

Land use and anuran biodiversity

Plate 8. View of site M2 in Cherokee County, Kansas. A man-

made pool at the edge of a pile of mining spoils (chat) left over

from lead and zinc mining.

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All landscape photos by Lewis Anderson (Plates 1-8).

seven at both natural sites. The mined sites had only five

species, four at one site and five at the second. Only one agri-

cultural site (Al) had more than six species.

Based on overall occurrences, there may be three clusters

of species. Cluster one included species generally found at all

three groups of sites: the southern leopard frog ( Rana spheno-

cephala ), western chorus frog ( Pseudacris triseriata ),

American toad (Bufo americanus ), Blanchard’s cricket frog

( Acris crepitans), and the bullfrog ( Rana catesbeiana) [Table

1], Cluster two included species not found at the mined sites,

less common at the agricultural sites, and common at the nat-

ural sites: northern spring peeper ( Pseudacris crucifer) and

gray treefrog (Hyla versicolor / chiysoscelis). Cluster three

included species uncommon at all sites: northern crawfish

frog ( Rana areolata) and eastern narrowmouth toad

( Gastrophryne carolinensis).

Adult density

Total audio density was significantly greater in natural sites

(1048.7 / ha) than in the agricultural and mined sites (Table 2),

but there was no significant difference between the agricultural

(519.0 / ha) and mined (164.8 / ha) sites. Total visual density

did not vary significantly among the groups of sites, but the

rank order was the same as for audio density. Overall, estimates

of audio density were about twice the visual densities at agri-

cultural and natural sites, but just over half at the mined sites.

The densities of some species varied with land use group.

P. triseriata audio density was significantly higher in agricul-

tural sites than in mined and natural sites (Table 2). Natural

sites had no P. triseriata in the audio census. Visual density

was also higher at the agricultural sites, but not significantly

so, and P. triseriata were found during the visual census at

one natural site. The density of R. sphenocephala was also

higher at agricultural sites in both audio and visual census

(Table 2), although the differences were not significant.

Visual density of the H. versicolor! chrysoscelis complex

was significantly higher in natural sites compared to agricul-

tural sites (Table 2). The same pattern existed for audio

density, but was not significant. Audio and visual density of

Plate 9. Eastern Narrowmouth Toad, Gastrophryne carolinensis.

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December 2006 I Volume 4 I Number 1 I e14

L. R. Anderson and J. A. Arruda

Table 3. Field tadpole density (per m2) and percent malformations by land use category. Standard errors for percentage data are

asymmetrical upper and lower standard errors. Within each line, means with different lower case letters are significantly different

(P<0.05).

Mined

Agricultural

Natural

Mean (SE)

Density (per m2)

28.5 (11.1) c

59.4 (7.7) b

137.6 (11.8) a

% Malformed

8.3 (2.2/1. 9) b

4.6 (0.8/0. 8) b

0.4 (0.5/0. 1) a

DOI: 10.151 4/journal. arc. 004001 4t003

Table 4. Percentages of types of malformations in field tad-

poles from each land use category.

Category

Notochord

Spinal Cord

Head/

Face

Edema

Stunted

Severe

Mined

48.8

2.4

4.9

41.5

2.4

Agricultural

46.8

1.1

9.6

33.5

9.0

Natural

26.9

8.5

36.2

19.2

9.2

DOI: 1 0.1 51 4/journal. arc.004001 4t006

within 2.5 minutes in the lymphatic system and the plasma of

a chronically catheterized Bufo marinus (Wentzell 1993).

Wentzell (1993) also noted the kidney is the first organ

exposed to the incoming ambient water. Atrazine has been

shown to bioconcentrate in northern leopard frogs ( Rana pip-

iens ), but no impacts were observed (Allran and Karasov

2000). Russell et al. (1997) surveyed the distribution of the

accumulation of PCBs and DDT metabolites in green frogs

( Rana clamitans ) and found variation in the amounts and

kinds of contaminants accumulated. Bishop and Gendron

(1998) reviewed literature on contaminant levels and effects

in amphibians for the Great Lakes basin and reported some

population declines could be influenced by exposures to envi-

ronmental contaminants.

In agricultural areas, pesticides may be present in breed-

ing pools. Several organophosphates caused abnormal

pigmentation, abnormal gut development, notochord defects,

and reduced growth to embryos of the African clawed frog

Xenopus laevis (Snawder and Chambers 1989).

Organochlorine pesticides impaired the peripheral or central

nervous system by the likely inhibition of enzymes or metabo-

lites by substances normally destroyed during nerve action

(Livingston 1977). Fenitrothion and carbaryl showed effects

such as microcephaly, edema, altered external morphology,

heart abnormalities, and notochord / spinal cord abnormalities

inX. laevis (Elliot-Feeley 1982).

R. pipiens larvae were exposed to atrazine and nitrates in

the lab and no significant growth or developmental effects

were noted except for slowed larval growth due to nitrates

(Allran and Karasov 2000). Bridges and Semlitsch (2000)

found significant variation in the time to death among tad-

poles of nine species of Rana and ten subpopulations of R.

sphenocephala exposed to carbaryl. Significant variation in

the tolerance to carbaryl was found within a population of H.

versicolor tadpoles (Semlitsch et al. 2000).

At Pelee Island in Canada, hybrid toads ( B . woodhousii

X B. americanus) have disappeared from agricultural areas

with heavy chemical use (Green 1989). Cooke (1981) caged

tadpoles in a potato field sprayed with oxamyl, a carbamate

nematicide, and found a very high incidence of deformities of

the tail and hind limbs, and high mortality among the

deformed tadpoles.

R. pipiens embryos exposed to paraquat in a laboratory

situation showed abnormal tail development, reduced muscu-

lar response, abnormal swimming behavior, and stunted

growth (Dial and Bauer 1984). The types of malformations

found in these studies are consistent with those found in agri-

cultural areas in this study including notochord / spinal cord

malformations (sometimes also referred to as tail abnormali-

ties or malformations), microcephaly (head/face), and stunted

growth (Tables 4 and 6).

In mined areas, problems can arise from the leaching of

metals such as lead and zinc, and from low pH. Smelters also

have been active in southeast Kansas in the past, sometimes

close to mines. Lead concentrations found in tadpoles living in

water subject to deposition from smelters and lead mine efflu-

ent are much higher than in tadpoles found residing in

roadside ditches (Birdsall et al. 1986). Because of differences

in the feeding habits of larval and adult amphibians, tadpoles

living in roadside drainage accumulate more lead than the

adults (Birdsall et al. 1986). Also, B. americanus tadpoles

have shown no avoidance of water containing lead in octago-

nal fluvarium tests (Vial 1992).

Niethhammer et al. (1986) showed that R. catesbeiana

had much higher levels of lead, zinc, and cadmium in their tis-

sues than did reptiles, birds, or mammals collected from a

river impacted by metal pollution from abandoned mine tail-

ing piles. Khangarot and Ray (1987) showed that amphibians

exposed to heavy metals display a variety of adverse effects

such as erratic body movements, slower growth and develop-

ment rates, morphological deformities and death.

Rowe et al. (1996) found oral deformities in tadpoles

from a basin contaminated by coal ash. Loumbourdis et al.

(1999) noted a tendency for retarded growth in tadpoles of R.

ridibunda exposed to cadmium. The metamorphosis of R.

luteiventrus tadpoles was delayed when they were exposed

to soils contaminated with heavy metals (Lefcort et al.

1998). Freda (1991) pointed out the influential roles of pH,

Amphib. Reptile Conserv. | http://www.herpetofauna.org 054

December 2006 I Volume 4 I Number 1 I e14

Land use and anuran biodiversity

Plate 12. Gray Treefrog, Hyla versicolor/chrysoscelis. DOI: 10.1514/journal.arc.0040014g013

Plate 13. Northern Cricket Frog, Acris crepitans. DOI: 10.1514/journal.arc.0040014g014

Amphib. Reptile Conserv. | http://www.herpetofauna.org 055 December 2006 | Volume 4 | Number 1 | e14

L. R. Anderson and J. A. Arruda

hardness, dissolved organic carbon, developmental stage,

and species on the impact of aluminum toxicity.

Additionally, Freda (1991) noted the endpoints of toxic

effects may vary from early egg mortality to sperm motility

or to the success of fertilization.

Tests on anuran embryos under acidic conditions indi-

cate a high survival rate to a certain threshold, and then the

survival rate drops drastically. Embryos that do hatch often

display developmental abnormalities and more abnormali-

ties at lower pH (Pierce et al. 1984). Larvae of R. sylvatica

showed greater tolerance to acidic conditions but toxicity of

the acidic water does have adverse effects (Pierce et al.

1984). Preest (1993) showed that low pH disrupts osmoreg-

ulation in Ambystoma maculatum larvae causing slower

growth and ultimately reducing fecundity and increasing

exposure to predation.

At M2, the lead/zinc mined site, no tadpoles were found

during any sample event nor were any tadpoles found during

two intensive searches of the entire pool. Tadpoles with

stunted growth comprised 41.5% of the total malformations

found from eggs originating from mined sites in this study

compared to 33.5% at agricultural sites and 19.2% at natural

sites (Table 6).

Since land use likely affects water quality, water quality

provides a possible explanation for the higher rate of tadpoles

with malformations, the lower percentage of eggs hatching

successfully, and potentially, the lower density of tadpoles in

agricultural and mined land breeding pools. It is less clear

what the relative role of water quality is in producing the

lower adult anuran densities and species richness in agricul-

tural and mined land breeding pools compared to physical

habitat availability or quality.

The application of metapopulation dynamics (Gilpin and

Hanski 1991, Fiedler and Jain 1992) and the concepts of

sources and sinks to amphibians has been recognized by

Hecnar and M’Closkey (1996) and Alford and Richards

(1999). Considering the relationship of spatial scale to the

species status of green frogs (R. clamitans ), Hecnar and

M’Closkey (1997) detected differences in occupancy and

abundance at various spatial scales and concluded that the sta-

tus of the green frog was dependent on the scale used.

Overall, the higher diversity of amphibians seen in the

region of southeast Kansas may be maintained by a hetero-

geneous landscape, where losses in impacted areas are

balanced by survival and recruitment from unimpacted

areas. The analysis of Alford and Richards (1999) that

habitat patch isolation may be of greater significance on

populations of amphibians, compared to other animals is

relevant to the consideration of the status of amphibians in

southeast Kansas. Alford and Richards (1999) concluded

that the dynamics of pond use was primarily affected by

breeding pond isolation. The amphibian landscape of

southeast Kansas contains many isolated patches of breed-

ing pools, pools isolated not only by physical distance, but

by the distance generated by patches of poor water quality.

These pools have varied breeding and nonbreeding habitats

as well, cast against a background of dispersal pathways

and environments.

Even when adult anurans from neighboring populations

migrate into an impacted breeding patch, low juvenile recruit-

ment due to poor tadpole survivorship can result in reduced adult

density and diversity in the patch. Freda (1991), Bishop and

Gendron (1998) and Loumbourdis et al. (1999) show the key role

of pollutants on the tadpole stage. If water quality is sufficiently

poor over a larger regional area, there may be no immigration at

all into central breeding pools and overall biodiversity may

decrease as observed by Hecnar and M’Closkey (1996) for the

effect of habitat loss. Species having shorter life spans may be the

first to disappear from an area and any differential tolerances of

the adults, larvae, and eggs from different species (Bridges and

Semlitsch 2000 and Semlitsch et al. 2000) may also play a role.

The limited travel range of anurans and the consideration that

some tend to be patrophilic may explain localized extirpations of

anuran populations such as observed here.

Acknowledgments. — We wish to thank Dan VanLeeuwen

for assistance in both the field and laboratory and Drs. James

Triplett and Alexander Bednekoff for assistance in guiding the

project. The project would not have been possible without

access to land owned or managed by: Vernon and Carmen

Anderson, Kate Wade, and Verne Leeper, the Terry Best fam-

ily, the Brewster brothers, Augustus Clark, the Pittsburg State

University Biology Department, the Kansas Department of

Wildlife and Parks, and the Farmers Home Administration.

This project was funded by the Kansas Department of

Wildlife and Parks. Suzanne Collins and Joseph Collins of

The Center for North American Herpetology graciously pro-

vided species images.

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L. R. Anderson and J. A. Arruda

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Manuscript received: 30 September 1997; Accepted: 27 October

2001; Published: 26 December 2006

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December 2006 I Volume 4 I Number 1 I e14

the Creative Commons Attribution License, which permits unrestricted use, distribution, and repro-

duction in any medium, provided the original author and source are credited.

Amphibian and Reptile Conservation 4(1):60-87.

DOI: 10.151 4/journal. arc. 004001 6 (2329KB PDF)

The authors are responsible for the facts presented in this article and for the opinions expressed there-

in, which are not necessarily those of UNESCO and do not commit the Organisation. The authors

note that important literature which could not be incorporated into the text has been published follow-

ing the drafting of this article.

Conservation of amphibians and reptiles in Indonesia:

issues and problems

DJOKO T. ISKANDAR 1 * AND WALTER R. ERDELEN 2

1 School of Life Sciences and Technology, Institut Teknologi Bandung, 10, Jalan Ganesa, Bandung 40132 INDONESIA

2 Assistant Director-General for Natural Sciences, UNESCO, 1, rue Miollis, 75732 Paris Cedex 15, FRANCE

Abstract . — Indonesia is an archipelagic nation comprising some 17,000 islands of varying sizes and geologi-

cal origins, as well as marked differences in composition of their floras and faunas. Indonesia is considered

one of the megadiversity centers, both in terms of species numbers as well as endemism. According to the

Biodiversity Action Plan for Indonesia, 16% of all amphibian and reptile species occur in Indonesia, a total of

over 1,100 species. New research activities, launched in the last few years, indicate that these figures may be

significantly higher than generally assumed. Indonesia is suspected to host the worldwide highest numbers

of amphibian and reptile species. Herpetological research in Indonesia, however, has not progressed at a rate

comparable to that of neighboring countries. As a result, the ratio of Indonesian species to the entirety of

Southeast Asian and Malesian species has “declined” from about 60% in 1930 to about 50% in 2000, essen-

tially a result of more taxa having been described from areas outside Indonesia. Many of these taxa were

subsequently also found in Indonesia. In the last 70 years, 762 new taxa have been described from the

Southeast Asia region of which only 262 were from Indonesia. In general, the herpetofauna of Indonesia is

poorly understood compared to the herpetofauna of neighboring countries. This refers not only to the taxo-

nomic status, but also to the basic biological and ecological characteristics of most of the species. Moreover,

geographic distribution patterns for many species are only poorly known. In view of the alarming rate of for-

est loss, measures for more effective protection of the herpetofauna of Indonesia are urgently required. The

status of virtually all of the Indonesian species, e.g. in terms of IUCN categories, remains unknown, and no

action plans have been formulated to date. In addition, research results on Indonesia’s amphibian and reptile

fauna have often not been made available in the country itself. Finally, there is a clear need to organize

research activities in such a way that a larger segment of the Indonesian population becomes aware of the

importance of the herpetofauna as an essential component of the country’s biodiversity. To address these

issues, this paper (1) gives an overview of the herpetofauna as part of Indonesia’s biodiversity, (2) outlines the

history of herpetological research in the region, (3) identifies major gaps in our knowledge of the Indonesian

herpetofauna, and (4) uses this framework for discussing issues and problems of the conservation of amphib-

ians and reptiles in Indonesia. In particular, the contents and shortcomings of compilations of lists of

protected or threatened species by national and international authorities are discussed, major threats to the

Indonesian herpetofauna or certain components thereof are described, and a set of measures for better long-

term conservation is proposed.

Abstrak . — Indonesia adalah suatu negara kepulauan yang terdiri dari sekitar 17.000 pulau dengan ukuran

bervariasi dan mempunyai asal usul geoiogi yang kompleks seperti yang terlihat dalam komposisi tumbuhan

dan hewannya. Indonesia, sebagai salah satu pusat keanekaragaman yang terbesar di dunia, baik dari segi

kekayaan alam jenisnya maupun dari segi tingkat endemisitasnya. Menurut Biodiversity Action Plan for

Indonesia, 16% dari amfibi dan reptil dunia terdapat di sini, dengan jumlah lebih dari 1100 jenis. Kegiatan

penelitian yang dilaksanakan pada masa yang baru lalu menunjukkan bahwa jumlah tersebut di atas masih

jauh di bawah keadaan yang sebenarnya. Indonesia mungkin sekali sebuah negara yang mempunyai jumlah

amfibi dan reptil terbesar di dunia. Yang patut menjadi pertimbangan ialah bahwa penelitian amfibi dan rep-

til di Indonesia jauh lebih lambat di bandingkan dengan kemajuan di negara tetangga. Sebagai gambaran,

jumlah jenis di Indonesia apabiia dibandingkan dengan jumlah jenis di seluruh Asia Tenggara dalam kurun

waktu 70 tahun telah merosot dari 60% menjadi 50%. Hal ini terjadi karena jumlah taksa baru kebanyakan

ditemukan di luar Indonesia. Banyak diantara jenis-jenis tersebut kemudian ditemukan di Indonesia. Dalam

70 tahun terakhir, 762 jenis taksa dipertelakan dari luar Indonesia dan hanya 262 pertelaan dari Indonesia.

Correspondence. * 1 Tel/ fax: + +62-22-250.0258, email: iskandar@sith.ith.acdd 2 Tel: +33 (0) 1 45 68 40 78, email: w.erdelen@unesco.org;

Corresponding author.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 060

December 2006 I Volume 4 I Number 1 I e16

Indonesian amphibian and reptile conservation

Pada umumnya herpetofauna Indonesia tidak banyak dikenal, baik dari segi taksonomi, ciri-ciri biologi

maupun ciri-ciri ekologinya. Daerah penyebaran suatu jenis sangat sedikit diketahui. Meninjau dari cepatnya

penebangan dan pengalihan fungsi hutan, usaha untuk melindungi komponen biologi (dalam hal ini amfibi dan

reptil) sangat diperlukan. Hampir semua status perlindungan baik secara nasional maupun dengan mengiku-

ti kategori IUCN atau CITES tidak banyak diketahui atau dipahami. Kebanyakan informasi mengenai

organisme Indonesia sulit diperoleh di dalam negeri. Sebagai akibat, maka diperlukan suatu mekanisme

untuk mengatur kegiatan penelitian sedemikian rupa sehingga timbul kesadaran bahwa amfibi dan reptil

merupakan salah satu komponen yang sangat berharga dari kekayaan keaneka-ragaman Indonesia. Makalah

ini memberikan (1) gambaran komponen biodiversitas herpetofauna Indonesia, (2) memaparkan sejarah

perkembangan herpetologi di Indonesia, (3) mengidentifikasi kekosongan dalam pengetahuan herpetologi di

Indonesia, (4) memaparkan masalah dan jalan keluar dalam konseravsi keanekaragaman herpetofauna

Indonesia. Daftar herpetofauna Indonesia yang dilindungi undang-undang, CITES dan IUCN dibahas, hewan-

hewan yang mulai terancam dan kiat untuk melindunginya dibahas.

Key words. Conservation, biodiversity, current knowledge, Indonesia, Amphibia, Reptilia, IUCN

Citation: Iskandar, D. T. and Erdelen, W. R. 2006. Conservation of amphibians and reptiles in Indonesia: issues and problems. Amphib. Reptile

Conserv. 4(1 ):60-87(e1 6).

Introduction

Indonesia, an archipelagic nation with a population of some 210

million people, comprises about 17,000 islands of varying sizes

and geological origins, as well as marked differences in com-

position of their floras and faunas. Indonesia is one of the 17

megadiversity countries (Mittermeier and Mittermeier 1997)

with two of the world’s 25 hotspots for conservation priorities,

viz. Sundaland and Wallacea (Mittermeier et al. 1999; Myers et

al. 2000), important ecoregions and endemic bird areas.

According to the biodiversity action plan for Indonesia (BAP-

PENAS 1993), 16% of the world’s amphibian and reptile

species occur in Indonesia, a total of over 1100 species.

One of the earliest comprehensive descriptions of the

herpetofauna of Indonesia, formerly referred to as Dutch East

India or the Dutch East Indies, is the two volume work by de

Rooij (1915, 1917). The first volume covers the lizards, tur-

tles, and crocodiles; 267 species of lizards, 35 chelonians, and

four species of crocodilians are described. The second volume

on snakes lists 84 genera and 318 species. De Rooij ’s nomen-

clature is based on the catalogues of the British Museum

published in several volumes by Boulenger (see Das 1998, for

references). The region covered in this work is the Indo-

Australian Archipelago, stretching from Sumatra in the west

to New Guinea and the Solomon Islands in the east. The next

landmark publication on the herpetofauna of the Indo-

Australian Archipelago was the work of van Kampen (1923)

on amphibians. This work was an extension of his earlier

work — he had published a list of 194 amphibian species for

the same region in 1907 — which brought the total number of

amphibian species described to 254 species. In 1950, more

than 30 years after de Rooij ’s publication (de Rooij 1917), de

Haas published a checklist of the snakes of the Indo-

Australian Archipelago (de Haas 1950). This checklist

contained additions to the snake fauna and also some nomen-

clatorial changes. De Haas (1950) stressed the imperfect

knowledge of the geographic distribution of many species,

even from Java, where much of the early research had been

earned out. This, to some extent, was covered by van Hoesel’ s

work on the snakes of Java (van Hoesel 1959). Later work

either focused on specific taxonomic groups or on parts of the

Indonesian region or neighboring countries (Iskandar 1998,

2000). As a consequence, discussed in further detail below,

much of our increasing knowledge of the Indonesian herpeto-

fauna was a result of work performed outside of Indonesia

itself. Only within the last decade new work on the Indonesian

herpetofauna has appeared, e.g., on turtles and crocodiles

(Iskandar 2000), the snakes of Sumatra (David and Vogel

1996), the snakes of Borneo (Stuebing and Inger 1999), the

snakes of Sulawesi (de Lang and Vogel 2005), the amphibians

of Java and Bali (Iskandar 1998), the lizards of Borneo (Das

2004), and the amphibians and reptiles of the Sunda region

(Manthey and Grossmann 1997). Checklists of all amphibian

and snake species of Southeast Asia and New Guinea have

been compiled (Iskandar and Colijn 2000, 2002); the other

reptile checklists are still in press. Other publications of

regional relevance include work on Philippine amphibians

(Alcala and Brown 1998), on the herpetofauna of Sabah (Inger

and Stuebing 1989; Inger and Tan 1996), and publications

focusing on Borneo (e.g., Inger and Stuebing 1997; ITTO

1998), peninsular Malaysia and Thailand (Chan-Ard et al.

1999; Cox et al. 1998), peninsular Malaysia and Borneo (Lim

and Das 1999), and Singapore (Lim and Lim 1992).

Das (1998) and recently Iskandar and Colijn (2003), pub-

lished a comprehensive bibliography of herpetological

publications about Indonesia (excluding the Moluccas and

New Guinea). These bibliographies clearly illustrate how dif-

ficult it is to compile the relevant published material for

certain taxonomic groups. Moreover, updating of taxonomic

and systematic relationships of certain amphibian and reptile

species groups occurring in Indonesia faces a few other prob-

lems as well. Some of the most crucial points are discussed

more in detail below. The fact that new amphibians and rep-

tiles are still being described from Indonesia, not only from

lesser known areas such as Papua (formerly known as Irian

Jaya) and from more remote islands, but also from Java

(examples for amphibians in Iskandar (1998) and a lizard in

Iskandar (1994)), clearly underscores our fragmentary knowl-

edge of the heipetofauna of Indonesia.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 061

December 2006 I Volume 4 I Number 1 I e16

D. T. Iskandar and W. R. Erdelen

Concern about conservation of Indonesian species is

quite a recent phenomenon. An exception may be early focus

on the Komodo dragon ( Varanus kotnodoensis ), the first

Indonesian reptile species for which protection and population

management were considered vital for its survival (e.g.,

Hoogerwerf 1953). Conservation activities have always been

biased toward better known and more showy bird and mam-

mal species. Amphibians and reptiles have largely been

ignored. This changed only recently, after it was noticed that

some reptile species, particularly from Indonesia, were heavi-

ly exploited for their skins and other products such as meat,

gall bladders, etc., and when evidence for a worldwide and

poorly understood decline of amphibian species became avail-

able. To the general public in Indonesia, however, amphibians

and reptiles are not considered groups that are in specific need

of protection. As a result of the bias of conservation-related

research in Indonesia, again toward larger mammal and par-

ticular bird species, our data on the herpetofauna of Indonesia

are still poor. This applies despite the fact that Indonesia har-

bors the second-most, if not the most diverse herpetofauna

worldwide. Our ignorance is not only limited to amphibians

and reptiles. In the Agenda 21 -Indonesia, it is estimated that

30% of the plant species and 90% of the animal species of

Indonesia have not been adequately described and scientifi-

cally documented (State Ministry for Environment 1997).

Trained herpetologists are virtually non-existent in Indonesia,

and conservation and management activities only occasional-

ly extend to amphibian and reptile species. More recent work

on the ecology of certain islands or island groups within the

Indonesian archipelago (e.g., Monk et al. 1997; Whitten et al.

1996) and work on amphibians and reptiles in trade (Erdelen

1998a; Erdelen 1998b), however, indicate that amphibians

and reptiles are gaining momentum as groups that need to be

considered important components of Indonesia’ s biodiversity.

This paper ( 1 ) gives an overview of the herpetofauna as

part of Indonesia’ s biodiversity, (2) outlines the history of her-

petological research in the region, (3) identifies major gaps in

our knowledge of the Indonesian herpetofauna, and (4) uses

this framework for discussing issues and problems of the con-

servation of amphibians and reptiles in Indonesia. In

particular, the contents and shortcomings of compilations of

lists of protected or threatened species by national and inter-

national authorities are discussed, major threats to the

Indonesian herpetofauna or certain components thereof are

described, and a set of measures for better long-term conser-

vation is proposed.

Knowledge of amphibians and reptiles of Indonesia:

a historical perspective

As already indicated above, with the publications of de Rooij

(1915, 1917) and van Karnpen (1923), for the first time, over-

views of the herpetofauna of the Indo-Australian Archipelago

were available. Therefore, our analysis starts with the year 1930

(Fig. 1-3). During the last 70 years, the number of Malesian

(Insular Southeast Asia and New Guinea) reptile species,

described principally from outside Indonesia, increased from

942 to 1238 species. During the same period comparatively few

taxa were described from Indonesia. This discrepancy in species

described is even more evident in the amphibians; whereas the

Malesian and the whole Southeast Asian taxa show a marked

increase, especially after 1955, the Indonesian “increment” in

taxa is only between one-half and one-third of the Malesian and

of the whole Southeast Asian figures (Fig. 1-3).

Comparatively little new information was added during

World War II and during the periods of major political unrest

in Indonesia, i.e., between 1940 and 1960 (Fig. 1-3: data

points at the mid-intervals of 1945 and 1955). The decade

1960 to 1970 is characterized by the description of many new

taxa from the Malesian region. Most of these taxa had been

described from studies that were not earned out in Indonesia

but in neighboring countries (especially from Malaysia,

Philippines, Papua New Guinea and the Solomon Islands).

This indirectly contributed to the increase in our knowledge of

the Indonesian herpetofauna after many of these new forms

were also found in Indonesia.

A closer look shows that not only new species of moni-

tor lizards (Bohme et al. 2002; Bohme and Jacobs; 2001;

Bohme and Ziegler 1997, 2005; Harvey and Barker 1998;

Jacobs, 2003; Philipp et al. 1999; Sprackland 1999; Ziegler et

al. 1999) but also new species of land and freshwater tortois-

es (McCord et al. 1995; McCord and Pritchard, 2002; van

Dijk 2000; Rhodin 1994) were described from Indonesia.

Figures for total species numbers will probably still increase

(Rhodin and Genorupa 2000). For instance, some of the so-

called better known species may comprise species complexes

(e.g., Limnonectes macrodon), and quite a few new taxa are

already known but still await their scientific description

(Emerson et al. 2000; Evans et al. 2003).

Need for conservation of Indonesian amphibians

and reptiles

Threatened species, CITES, and protected species,

iUCN, CITES, and PKA lists: a comparison

Three major compilations give an outline of the present status

of national and international conservation and protection

measures. These are the 2000 IUCN Red List of Threatened

Animals (Baillie and Groombridge 1996), into which the new

IUCN categories and criteria are incorporated (as adopted by

IUCN in 1994), the CITES lists of species listed in the appen-

dices, and the list of Indonesian protected species (Ministry of

Forestry 2004). The 1996 IUCN list comprises a total of 30

reptile species occurring in Indonesia (Table 1). Of these rep-

tile species, 22 are considered threatened, i.e., belonging to the

category “critically endangered,” “endangered,” or “vulner-

able.” The remaining eight species are either grouped under

“data deficient” (five species) or “lower risk” (three species).

These threat categories differ only in quantitative aspects, e.g.,

in population decline rates.

The 2000 IUCN Red List (IUCN 2000) shows a dra-

matic increase in the numbers of turtle species included

(Table 1). This has largely been due to information and rec-

ommendations from a workshop on conservation and trade

of freshwater turtles and tortoises in Asia (van Dijk et al.

2000). In the IUCN Red List (IUCN 2000), no turtle species

is further listed as data deficient, and nearly all Indonesian

and New Guinean species are included, in addition to a

number of other Asian turtle and tortoise species. The pres-

Amphib. Reptile Conserv. | http://www.herpetofauna.org 062

December 2006 I Volume 4 | Number 1 | e16

Indonesian amphibian and reptile conservation

Frog species known from Indonesia,

Malesia and Southeast Asia (1 930-2000)

No. of Species

Figure 1. DOI: 10. 151 4/journal. arc. 004001 4g001

Snake species known from Indonesia,

Malesia and Southeast Asia (1 930-2000)

No. of Species

800

700 - _

600 -

500 -

400 -

300 -

200 -

100 -

o +LLL — ! ■ - .,1111 — ■ .,11111 — I - - 1,1111 — ■ , m il — I ' ■ 1, 1 111 — • I , .11 II — I - ■ ■,11111 — UOJ

1930 1940 1950 1960 1970 1980 1990 2000

Figure 2. DOI: 10. 151 4/journal. arc. 004001 4g002

Lizard species known from Indonesia,

Malesia and Southeast Asia (1 930-2000)

No. of Species

800 -|

700

600 -

500 -

400 -

300 -

200 ; . . . . . ; . ;

loo- ;

o — ' I I m — • i ^ — — Lj-W — i • ' 1 1 m — 1 ' • — • i — • ^ L

1930 1940 1950 1960 1970 1980 1990 2000

Figure 3. DOI: 10. 151 4/journal. arc. 004001 4g003

Amphib. Reptile Conserv. | http://www.herpetofauna.org 063 December 2006 | Volume 4 | Number 1 | e16

n Indonesia

□ Malesia

u Southeast Asia

□ Indonesia

□ Malesia

□ Southeast Asia

D. T. Iskandar and W. R. Erdelen

Table 1. Indonesian reptiles listed in the IUCN Red Lists of threatened animals (Baillie and Groombridge 1996; IUCN 2000), in the

CITES Appendices I or II, and protection status in Indonesia. For comparison, threat proposals of the Asian turtle trade workshop

(ATT 1999, see van Dijk et al. 2000) are included. IUCN categories of threat: CR = critically endangered, DD = data deficient, EN =

endangered, LR = lower risk: near threatened, VU = vulnerable, — = not listed. CL = listed in CITES Appendices (I, II; - = not listed).

PI = protection status of species in Indonesia (P = protected; - = not protected). Quota = Quota issued by PKA for skin trade (QS)

and live export or pet trade (QL). Note: Quota categories given according to major use category. *) Including Cyclemys oldhami. **)

Export stopped since 1994 (see text for details). Note: At least three new species of the chelid genus Elseya, none of them listed here,

will be described from New Guinea. ***)The different subspecies of Python curtus are now in the process of being split into three dis-

tinct species. Note: Since this table was prepared several new species and subspecies have been described, including Chitra vandjiki

and Chitra chitra javanensis (McCord and Pritchard 2002), Varanus bohmei (Jacobs 2003), V. macraei (Bohme and Jacobs 2001), V.

reisingeri (Eidenmuller and Wicker 2005), and V. zugorum (Bohme and Ziegler 2005), Pelochelys signifera (Webb 2001), Candoia

paulsoni and Candoia superciliosa (Smith et al. 2001)

Taxon

IUCN

ATT

IUCN

Quota

1996

1999

2000

Testudines - Turtles and Tortoises

Carrettochelyidae

Carrettochelys insculpta

Chelidae

Chelodina mccordi

Chelodina novaeguineae

Chelodina parkeri

Chelodina reimanni

Chelodina siebenrocki

Elseya branderhorstii

Elseya novaeguineae

Emydura subglobosa

Cheloniidae

Caretta caretta

Chelonia mydas

Eretmochelys imbricata

Lepidochelys olivacea

Natator depressus

Dermochelyidae

Dermochelys coriacea

Bataguridae

Batagur baska

Callagur borneoensis

Cuora amboinensis

Cyclemys dentata *)

Heosemys spinosa

Leucocephalon yuwonoi

Malay emys subtrijuga

Notochelys platynota

Orlitia borneensis

Siebenrockiella crassicollis

Testudinidae

Indotestudo forstenii

“Indotestudo elongata ”

Manouria emys

Trionychidae

Amyda cartilaginea

Chitra chitra

Pelochelys bibroni

Pelochelys cantorii

Crocodylia - Crocodiles

Crocodylidae

Crocodylus mindorensis

Crocodylus novaeguineae

Continued on page 065.

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December 2006 I Volume 4 I Number 1 I e16

Indonesian amphibian and reptile conservation

Table 1. Continued.

Taxon

IUCN

ATT

IUCN

Quota

1996

1999

2000

Crocodylia - Crocodiles

Crocodylidae

Crocodylus porosus

Crocodylus raninus

Crocodylus siamensis

Tomistoma schlegelii

Sauria - Lizards

Agamidae

Chlamydosaurus kingii

Hydrosaurus amboinensis

Hypsilurus dilophus

Lanthanotidae

Lanthanotus borneensis

Scincidae

Tiliqua gigas

Varanidae

Varanus aujfenbergi

Varanus beccarii

Varanus bengalensis nebulosus

Varanus caerulivirens

Varanus cerambonensis

Varanus doreanus

Varanus dumerilii

QLL

Varanus indicus

Varanus jobiensis

Varanus komodoensis

Varanus melinus

Varanus “panoptes” (gouldii)

Varanus prasinus

Varanus rudicollis

Varanus salvadorii

Varanus salvator

Varanus salvator togianus

Varanus timorensis

Varanus yuwonoi

Serpentes - Snakes

Anomochilidae

Anomochilus leonardi

Boidae

Candoia aspera

Candoia carinata

Colubridae

Iguanognathus werneri

Ptyas mucosa

Elapidae

Naja sputatrix

Naja sumatrana

Ophiophagus hannah

Pythonidae

Apodora papuana

Leiopython albertisii

Lias is Jus cus

Liasis mackloti

(QS)**)

Continued on page 066.

Amphib. Reptile Conserv. | http://www.herpetofauna.org

065

December 2006 I Volume 4 I Number 1 I e16

D. T. Iskandar and W. R. Erdelen

Table 1. Continued.

Taxon

IUCN

1996

ATT

1999

IUCN

2000

Quota

Serpentes - Snakes

Pythonidae

Morelia amethistina

Morelia boeleni

Morelia clastolepis

Morelia nauta

Morelia spilota variegata

Morelia tracyae

Morelia viridis

Python curtus ***)

Python molurus bivittatus

Python reticulatus

Python timoriensis

DOI: 1 0.1 51 4/journal.arc.004001 6t001

ent list contains 85 species, of which 3 1 species, including

most turtles and crocodiles, are considered threatened. For

other reptile groups such as varanid lizards and pythons,

however, we urgently need assessment of their status.

Except for highly localized knowledge of some of the most

common species such as Varanus salvator, Python curtus,

and Python reticulatus, we hardly know anything about the

other Indonesian species.

None of the Indonesian amphibian species was listed in

the 2000 IUCN Red List of Threatened Animals. However,

by the 2004 Red List of Threatened Species, the status of

amphibians had changed dramatically, and the report noted

that they “are currently the most threatened class of verte-

brates on the IUCN Red List” (Baillie et al. 2004, p. 1 1). This

is reflected in the 2006 Red List, which lists 39 threatened

amphibian species in Indonesia (IUCN 2006). All this new

information on amphibians certainly requires further detailed

analysis, which could not be earned out for this paper.

The IUCN criteria and subcriteria provide information

on the underlying reasons why a species may be threatened.

Lor the Indonesian taxa, most are given criterion A, i.e., pop-

Plate 1 . DOI: 1 0.1 51 4/journal.arc.004001 6g005

ulations are declining. Subcriteria 1 and 2 (for criterion A)

indicate that decline has been observed or suspected in the

past (subcriterion 1) or will be in the future (subcriterion 2).

Subcriteria a and b only point out the evidence available, i.e.,

direct observation or an index of abundance. More important

is that subcriteria c and/or d are listed for virtually all of the

Plate 2. DOI: 10.1 51 4/journal. arc. 004001 6g004

Plate 3. DOI: 10.1 51 4/journal. arc. 004001 6g006

Plate captions: 1 . Ingerophrynus celebensis. 2. Pelophryne signata. 3. Litoria infrafrenata.

Species plates 1-3 taken by Djoko T. Iskandar.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 066 December 2006 | Volume 4 | Number 1 | e16

Plate 4. DOI: 10. 151 4/journal. arc. 004001 6g007

Plate 6. DOI: 10. 151 4/journal. arc. 004001 6g009

Plate 8. DOI: 10.1514/journal.arc.0040016g011

Plate 10. DOI: 10.1514/journal.arc.0040016g013

Plate 7. DOI: 10.1514/journal.arc.0040016g010

Plate 9. DOI: 1 0.1 51 4/journal.arc.004001 6g01 2

Plate 11. DOI: 10.1514/journal.arc.0040016g014

Plate captions: 4. Litoria sp. 5. Leptolalax hamidi. 6. Leptobachium hasseltii. 7. Limnonectes sp. with a black tympanum.

8. Limnonectes cf modestus. 9. Limnonectes sp. that laid tadpoles. 10. Limnonectes shompenorum. 11. Limnonectes modestus.

Species plate 6-9 taken by Jim A. McGuire. Species plates 4-5, 10, & 11 taken by Djoko T. Iskandar.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 067

December 2006 I Volume 4 I Number 1 I e16

D. T. Iskandar and W. R. Erdelen

threatened taxa; that is, either the area occupied by the

species is shrinking or the habitat quality is decreasing {sub-

criterion c ) or the species is heavily exploited {subcriterion

d). In the case of the Komodo monitor, it is well-known that,

except for Flores, the species is restricted only to a few small-

er islands, Komodo being the most extensive, and that the

Flores populations are threatened (for distributional details

see Auffenberg 1981, Murphy et al. 2002; Ciofi and de Boer

2004). The species under criterion D and subcriterion 2 all

have susceptible populations. For instance, the chelid turtle

Chelodina mccordi occurs only on Roti Island, south of

Timor (Rhodin 1994), and Chelodina parkeri seems to have

a very restricted distribution in Irian Jaya (Iskandar 2000;

Samedi and Iskandar 2000). The colubrid snake

Iguanognathus werneri is known only from a single speci-

men from Sumatra. Leucocephalon (formerly Heosemys)

yuwonoi from northern Sulawesi, was only described within

the last decade or so (McCord et al. 1995; McCord et al.

2000). The false gharial {Tomistoma schlegelii ), in the 1996

IUCN list classified as DD is now (IUCN 2000) considered

endangered. This change in threat status is supported by

many studies in Sumatra, Borneo, and peninsular Malaysia

(Bezujien et al., 1998; Ramono and Rahardjo 1993; Ross et

al. 1996; Simpson et al. 1998; Stuebing et al. 1998).

In sum, as already indicated in the IUCN list (Baillie

1996), the overall conservation status of amphibians and rep-

tiles cannot be assessed. As a consequence, this also applies

to the lower national level of this analysis. The IUCN list

largely reflects the fact that of the six orders of reptiles only

the crocodiles (Crocodylia), the tuataras (Rhynchocephalia),

and, at least in part, the turtles (Testudines) have been

assessed. However, the majority of the reptile species, i.e.,

the lizards and snakes, do not fall into any of these groups.

This bias in available assessment data is also clearly seen in

the list for the Indonesian species. The majority of the

species are turtles of which all of the species found in

Indonesia are listed. Of the six crocodile species found in

Indonesia, three appear in the IUCN list, all are listed in

Appendix I or II of CITES (Table 1). Of the lizards, only the

Komodo monitor, being the largest extant lizard species, is

mentioned. As an endemic flagship species, it has the high-

est protection status among Indonesia’s reptiles. The

speciose group of snakes is only represented by a single

python species {Python molurus ) and a single colubrid snake

species {Iguanognathus werneri).

By definition, CITES covers international trade issues.

Therefore, the IUCN and CITES lists are not congruent but

have only certain species in common (Table 1). For example,

except for one species of monitor lizard {Varanus bengalen-

sis), all species of CITES Appendix I are also listed as

Plate 14. DOI: 1 0.1 51 4/journal. arc. 004001 6g01 7 Plate 15. DOI: 10.1514/journal.arc.0040016g018

Plate captions: 12. Limnonectes cf. gruriniens. 13. Occidozyga lima. 14. Rhacophorus gauni. 15. Nyctixalus pictus.

Species plates 13 & 15 taken by Jim A. McGuire. Species plate 12 & 14 taken by Djoko T. Iskandar.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 068

December 2006 I Volume 4 | Number 1 | e16

Plate 16. DOI: 10.1514/journal.arc.0040016g019

Plate 19. DOI: 10.151 4/journal. arc. 004001 6g022 Plate 18. DOI: 1 0.1 51 4/journal. arc. 004001 6g021

Plate captions: 16. Nyctixalus margaritifer. 17. Rhacophorus edentulus. 18. Rhacophorus margaritifer. 19. Staurois guttatus.

Species plate 18 taken by Jim A. McGuire. Species plates 16 & 19 taken by Djoko T. Iskandar. Species plate 17 taken by

Graeme Gillespie.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 069

December 2006 I Volume 4 I Number 1 I e16

Plate 22. DOI: 10.1514/journal.arc.0040016g025

Plate 24. DOI: 1 0.1 51 4/journal. arc. 004001 6g027

Plate 26. DOI: 1 0.1 51 4/journal.arc.004001 6g029

Plate 21. DOI: 10.1 51 4/journal. arc. 004001 6g024

Plate 23. DOI: 10.1514/journal.arc.0040016g026

Plate 25. DOI: 10.1514/journal.arc.0040016g028

Plate 27. DOI: 1 0.1 51 4/journal.arc.004001 6g030

Plate captions: 20. Sylvirana picturata. 21. Hydrophylax chalconota. 22. Odorrana hosii. 23. Hydrophylax nicobariensis. 24. Sylvirana

celebensis. 25. Kaloula baleata. 26. Kaloula pulchra. 27. Microhyla achatina.

Species plate 20 taken by Djoko T. Iskandar. Species plates 21-27 taken by Jim A. McGuire.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 070

December 2006 I Volume 4 I Number 1 I e16

Plate 28.

DOI: 1 0.1 51 4/journal.arc.004001 6g031

Plate 29. DOI: 10.1514/journal.arc.0040016g032

Plate 30. DOI: 10.1514/journal.arc.0040016g033

Plate 31.

DOI: 1 0.1 51 4/journal. arc. 004001 6g034

Plate 32. DOI: 10.151 4/journal. arc. 004001 6g035 Plate 33. DOI: 10.1 51 4/journal. arc. 004001 6g036

Plate 34. DOI: 1 0.1 51 4/journal.arc.004001 6g037 Plate 35. DOI: 1 0.1 51 4/journal.arc.004001 6g038

Plate captions: 28. Oreophryne sp. 29. Bronchocela jubata. 30. Gonocephalus kuhlii. 31. Gonocephalus grandis (male).

32. Bronchocela cristatella. 33. Draco bourouniensis. 34. Draco haematopogon. 35. Cyrtodactylus jellesmae.

Species plate 31 taken by Djoko T. Iskandar. Species plates 29, 30, & 32-35 taken by Jim A. McGuire. Species plate 28 taken by

Graeme Gillespie.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 071 December 2006 | Volume 4 | Number 1 | e16

D. T. Iskandar and W. R. Erdelen

threatened by IUCN. For Tomistoma schlegelii this has

applied only since the IUCN 2000 list was published (see

Table 1). As shown in Table 1, except for species protected in

Indonesia (P) and Crocodylus raninus and C. mindorensis,

both species virtually unknown by Indonesian authorities to

occur in Indonesia, all species listed under CITES are subject

to quota that limit the annual catch. These may be quota refer-

ring to skin trade (QS) or quota for trade of live specimens

(QL). In addition, a few species of reptiles are protected in

Indonesia but appear neither in the IUCN list nor in the CITES

appendices. These are two species of side-necked turtles

(Chelidae), three showy and large species of agamid lizards,

the monotypic genus Lanthanotus, and the scincid species

Tiliqua gigas. The agamids belong to the genera

Chi amydosa u nts , Hydrosaurus, and Hypsilurus. These are

either species with restricted ranges within Indonesia

( Hydrosaurus amboinensis ) or are elements of the Australian

realm, found in Indonesia only in Papua and on small islands

on the Sahul Shelf ( Chlamydosaurus kingii and Hypsilurus

dilophus).

Conclusions

Internationally protected species such as marine turtles may

experience considerable exploitation in Indonesia. Species not

adequately considered by any national or international regula-

tions are exploited in enormous numbers in Indonesia. This

presently particularly applies to freshwater turtles (’’freshwa-

ter turtles” or “tortoises” — tortoises by definition do not occur

in the water). The taxonomic status of many species is neither

clear to scientists nor, as a consequence, to Indonesian con-

servation authorities. For instance, what is considered

Indotestudo elongata is in fact I. forsteni, which shows

intraspecific variation in presence or absence of nuchal scales,

the major character by which the two species are distinguished

by CITES. The species complex of Crocodylus siamensis and

the taxonomic status of C. raninus are only poorly understood

although recorded from Brunei Darussalam (Das and Charles

2000). In addition, varanid nomenclature is presently under-

going such rapid modification that the official authorities

cannot keep pace with revisions published and new species

described in the scientific literature (Pianka et al. 2004).

Moreover, traders have identified the need for more taxonom-

ic studies as specimens were collected that showed significant

deviation from “classical” species descriptions (see, e.g.,

Yuwono 1998, for more specific information). In extreme

cases, taxa later described as new species have already (under

other names) been traded for some time before they were offi-

cially described in the literature. This, for instance, applies to

virtually all recently described new species such as, among

reptiles, the monitor lizards, pythons, and turtles.

Threats to Indonesian amphibians and reptiles

General remarks

Most of the information needed for conservation measures

for the amphibians and reptiles of Indonesia is not available.

In particular, habitat requirements are little known, popula-

tion sizes are unknown for virtually all species, and, as a

consequence, recent trends in population sizes also remain

unknown. Generally, most of the fundamental data on

species biology and ecology are lacking. Our knowledge,

however, is not zero. We do know that certain species are

typical forest dwellers and that habitat destruction and trade

have affected species and local populations. Some of the

potential threatening factors, however, we are only begin-

ning to understand. These are, for instance, the questions as

to what extent the global decline in amphibian species also

applies for Indonesian species and to what extent extreme

climatic fluctuations, mostly associated with El Nino

Southern Oscillation (ENSO) events, cause disturbances in

natural reproductive patterns in amphibians that may affect

population sizes and densities in the long run. A study in

Papua New Guinea, for instance, has shown that drought

conditions affect frogs with terrestrial breeding modes and

with direct development to such an extent that reproduction

almost ceased (Bickford 1998). In addition, it was found that

rare and uncommon arboreal species descend from their

arboreal sites and frog densities seem to increase near

streams. The effects of the latter two phenomena on the

respective communities remain unknown. A similar situation

may be expected for frogs in other parts of Indonesia, not

only for the Indonesian part of New Guinea (Papua).

Studies in Kalimantan have shown that, as a result of the

intense fires during the long drought in 1998 and the con-

comitant haze that affected the whole region, amphibian

reproductive cycles normally triggered by the moon phases

may have been completely out of synchronization with natu-

ral cues, and it is possible that reproduction may not have

taken place (Iskandar et al. 1999). Similar observations have

been made for other taxonomic groups such as birds and pri-

mates, which showed very limited activities and reduced

vocalizations during such periods (Gurmaya et al. 1999,

Raharjaningtrah and Prayogo 1999).

Habitat destruction

Habitat destruction and the resulting fragmentation of popu-

lations is the most important factor affecting the indigenous

amphibian and reptile species of Indonesia. For instance,

Sumatra has experienced a drastic loss of lowland forests

during the past two decades. Many of the Indonesian

endemics are species occurring in forests. We do not know

to what extent these species can tolerate human impacts

without severe population reductions. This situation is par-

ticularly acute in those parts of Indonesia where island sizes

are small and, as a consequence, extension of natural vege-

tation and absolute numbers of individuals for most of the

species are already low. This applies, for instance, to eastern

Indonesia, e.g., the Lesser Sunda Islands and the Moluccas.

But even on the larger islands such as Sumatra, Kalimantan,

Sulawesi, and Irian Jaya, localized endemism and species

with narrow geographical ranges are automatically prone to

extinction. This applies to most of the New Guinean micro-

hylid frogs such as the genera Oreophryne and

Xenobatrachus and most tree frogs of the genus Litoria. In

many cases, species are known only from the type specimen

or species have not been found again for decades. Examples

of such very poorly known species are the amphibians

Ichthyophis hypocyaneus, Rana debussyi, R. persimilis, and

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December 2006 I Volume 4 I Number 1 I e16

Plate 36.

DOI: 1 0.1 51 4/journal. arc. 004001 6g039

Plate 37. DOI: 10.1514/journal.arc.0040016g040

Plate 38.

DOI: 1 0.1 51 4/journal. arc. 004001 6g041 Plate 39.

DOI: 1 0.1 514/journal.arc.004001 6g042

Plate 40. DOI: 10. 151 4/journal. arc. 004001 6g043 Plate 41. DOI: 10.1 514/journal. arc. 004001 6g044

Plate 42. DOI: 1 0.1 51 4/journal. arc. 004001 6g045 Plate 43. DOI: 1 0.1 51 4/journal. arc. 004001 6g046

Plate captions: 36. Cyrtodactylus sp. 37. Gehyra mutilata. 38. Gekko smithi. 39. Gekko vittatus. 40. Lepidodactylus lugubris.

41. Cyrtodactylus sp. 42. Ptychozoon kuhlii. 43. Tribolonotus gracilis.

Species plates 36-38, 40 & 42 taken by Jim A. McGuire. Species plate 39 taken by Alain Compost. Species plates 41 & 43 taken

by Djoko T. Iskandar.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 073 December 2006 | Volume 4 | Number 1 | e16

D. T. Iskandar and W. R. Erdelen

Philautus jacobsoni; the lizards Harpesaurus tricinctus, H.

modigliani, and Thaumatorhynchus brooksv, and the snakes

Iguanognathus werneri and Anoplohydrus aemulans.

The present rate of habitat destruction in Indonesia is

alarming. In 1996, logging concessions covered an area of

about 54 million hectares (Sunderlin and Resosudarmo 1996),

and earlier reports by the United Nations Food and

Agriculture Organisation and the World Bank estimated an

increase in annual deforestation from 300,000 hectares in the

1970s to about 1 million hectares in 1990. In 1998, logging

activities were still estimated to cover an area of some 51.5

million hectares, carried out by over 421 private companies,

most of them operating under 33 leading business groups

(Jakarta Post, 15 January 1999).

Agenda 21 -Indonesia estimates that up to 1.3 million

hectares of forest are cleared annually in Indonesia and that

habitat loss in Java and Bali is about 91% (State Ministry for

Environment 1997). Between 1985 and 1997 about 18 mil-

lion hectares of forest have been lost in Indonesia, mostly

lowland rain forests. It is estimated that by the year 2010

Kalimantan will have lost all of its lowland forests, as has

largely occurred on Sumatra.

Studies in man-made habitats have shown that these con-

tain only a small segment of the original diversity in

amphibian and reptile species. Even in oil palm plantations

which superficially resemble forests, i.e., in terms of shade

conditions and microclimate, most of the amphibian and rep-

tile taxa found are typical human commensals or species

occurring in agricultural landscapes. For instance, no typical

forest-dwelling species was found in oil palm plantations

studied in north Sumatra (Gaulke et al. 1997, 1998).

Accordingly, conversion of natural forest to agroecosystems

or urban areas will result in the extermination of most of the

species that formerly occurred in the given area.

Trade

General remarks on wildlife trade in Indonesia

Indonesia has a long history of wildlife trade, particularly in

birds, live reptiles, reptile skins, and corals. Indonesia ranks

among the world’s leading nations in export of wildlife and

wildlife products (Nash 1993). Early conservationists in

Indonesia already saw a considerable danger for certain wild

species through the largely uncontrolled export of wild animal

species in those days, particularly the export of mammal and

bird skins (e.g., Dammerman 1928). Trade in live plants and

animals in Indonesia has received critical attention by the

international community for many years. This particularly

applies to trade in mammals, birds, and reptiles. For instance,

enormous quantities of reptile skins were exported from

Indonesia in the 1980s (see Jenkins and Broad 1994), and live

export of birds and mammals had also reached new dimen-

sions. The 1991 figures for Indonesian wildlife exports, as

compiled by Nash (1993), list almost 80,000 parrots, 1.9 mil-

lion reptiles including reptile skins, over 14,000 primates, and

over 1 million pieces of coral. These figures certainly no

longer apply, but nevertheless the question as to whether trade

in certain species of Indonesian wild flora and fauna meets the

criterion of sustainability still persists. In this section a few of

the most important issues related to trade and conservation of

amphibians and reptiles in Indonesia are discussed. A thor-

ough analysis of the overall situation in wildlife trade in

Indonesia is, in our opinion, long overdue.

Since 1978, Indonesia has been party to CITES, the

Convention on International Trade in Endangered Species of

Fauna and Flora. Indonesian CITES authorities are the

Indonesian Institute of Sciences, the Scientific Authority

(LIPI: Lembaga Ilmu Pengetahuan Indonesia); and the

Directorate General of Protection and Nature Conservation

(PKA: Direktorat Jenderal Perlindungan dan Konservasi

Alam), the Management Authority.

CITES Appendix I species may be harvested for domes-

tic use (see e.g., the non-protected CITES Appendix I

species in Table 1). In international trade they are treated

according to the rules and regulations in CITES. Appendix II

species that are traded are subject to annual quota, i.e., PKA

determines the number of specimens that may be caught for

trade, both skin and live specimen trade (see Table 1 for

species under the quota regulation). This “annual allowable

catch” is determined newly for each calendar year. Quotas

are then set on a provincial level. At present 30 reptile

species are protected by Indonesian law, and, of these, quo-

tas are issued for 27 species (Table 1).

Since Indonesia has been party to CITES, concern has

been repeatedly stated over the implementation of Article IV of

the Convention (Nash 1993). Article IV refers to Appendix II

species and to the fact that export should not be detrimental to

the survival of the respective species (paragraph 2a) and that

export should “be limited in order to maintain that species

throughout its range at a level consistent with its role in the

ecosystems in which it occurs and well above the level at which

that species might become eligible for inclusion in Appendix I

...” (paragraph 3). Subsequently, several reviews of the trade

situation for particular species groups were earned out. For

Indonesia, the most important ones were on Asian monitor

lizards (Luxmoore and Groombridge 1990) and on Asian

pythons (Groombridge and Luxmoore 1991). Information on

trade in Indonesian lizards and snakes has been compiled doc-

umenting the many different facets of relevance for achieving

sustainable harvests of the species in question (Erdelen 1998b).

Still, the problem of setting appropriate quotas, as already dis-

cussed in Nash (1993), has not been solved for most of the taxa

in trade in Indonesia. Confusion is also widespread over the

term “non-detrimental” as given in the Convention (see

above). This is underscored by the holding of an IUCN work-

shop to develop guidance for CITES scientific authorities on

the making of “non- detriment findings”.

Amphibian and reptile trade in Indonesia: conserva-

tion implications

As indicated above, an overall analysis of wildlife trade in

Indonesia is not available. This also applies for the herpeto-

fauna of Indonesia. As pointed out in an IUCN workshop on

Asian turtles trade (van Dijk et al. 2000), determining trade

levels for a species that should not have short-term or long-

term negative effects on natural populations is a complex

subject. This is exacerbated in amphibians and reptiles

because of our lack of knowledge of their biology and ecolo-

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December 2006 I Volume 4 I Number 1 I e16

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Plate 46. DOI: 1 0.1 51 4/journal. arc. 004001 6g049

Plate 48. DOI: 10.1514/journal.arc.0040016g051

Plate 50. DOI: 10.1514/journal.arc.0040016g053

Plate 45. DOI: 10.1514/journal.arc.0040016g048

Plate 47. DOI: 10.1514/journal.arc.0040016g050

Plate 49. DOI: 10.1514/journal.arc.0040016g052

Plate 51. DOI: 10.1514/journal.arc.0040016g054

Plate captions: 44. Cryptoblepharus balinensis. 45. Emoia artrocostata. 46. Emoia caeruleocauda. 47. Lamprolepis smaragdinum. 48.

Eutropis multifasciata (male). 49. Eutropix rudis. 50. Glaphyromorphus nigricaudis. 51 . Papuascincus stanleyanus.

Species plates 44-49 taken by Jim A. McGuire. Species plates 50 & 51 taken by Djoko T. Iskandar.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 075 December 2006 | Volume 4 | Number 1 | e16

D. T. Iskandar and W. R. Erdelen

gy and the exploitation patterns, even in the so-called “better

known” species (Erdelen 1998a). How difficult it is to collect

the relevant field data to estimate sustainability was shown in

a study of three of the most heavily exploited reptiles in

Indonesia, the water monitor ( Varanus salvator), the reticulat-

ed python ( Python reticulatus ), and the blood python ( Python

curtus ) (Erdelen et al. 1997).

Reptile and amphibian trade is a comparatively recent

phenomenon in Indonesia. Before the late 1980s, Indonesia

had no professional collectors of live reptiles (Yuwono

1998). Generally, reptile trade may be subdivided into two

major components, i.e., skin trade, including trade in other

organs such as gall bladders, and pet trade. The former cov-

ers a few species harvested in large numbers, the latter

about 30 species of amphibians, about 18 species of non-

marine turtles, about 50 species of lizards, and about the

same number of snake species (for details, see Yuwono

1998). Skin trade, on the other hand, essentially comprised

five species in Indonesia, viz. the water monitor ( Varanus

salvator), two species of python (the reticulated python

Python reticulatus and the blood python P. curtus ), the rat

snake ( Ptyas mucosa ), and the spitting cobra ( Naja sputa-

trix ). In the case of cobras, however, most specimens are

caught for the food market, and skins are largely by-prod-

ucts (Saputra, pers. comm.). Since 1991, all quotas were

reduced for these species, and international concern about

the numbers of rat snakes harvested led to a total ban of

trade in this species in Indonesia in 1994. In 1998, LIPI

undertook a survey on Ptyas mucosa, and an EU project on

this species is currently on its way to providing data on

whether the international ban should be lifted or not. The

latest (for the year 2000) quota for the remaining four

species are 150,000 (Naja sputatrix), 46,400 ( Python cur-

tus), 176,000 ( Python reticulatus), and 496,000 ( Varanus

salvator). One of the major questions arising from studies

on the habitats from where specimens are collected is how

to evaluate whether a species is collected from anthro-

pogenic habitats such as paddy fields, rubber plantations or

oil palm plantations, or from natural forest. Of these

species, blood pythons are virtually exclusively collected

from rubber and especially oil palm plantations (see e.g.,

Erdelen et al. 1997), and cobras and rat snakes are collected

mostly from paddy field areas (Sugardjito et al. 1998).

However, to what extent reticulated pythons are caught in

forested areas or in open areas following deforestation

remains unknown. Moreover, these pythons often are

caught near human dwellings where they can easily find

prey (Auliya, pers. comm, and own observations). The same

applies for the water monitor, which may be caught in habi-

tats ranging from urban areas to mangrove forests (e.g.,

Erdelen 1991). Surprisingly, these high harvest rates have

obviously not led to large-scale extinctions of certain popu-

lations. This may be a result of high reproductive rates of

species such as the water monitor and the reticulated python

(Shine et al. 1998a, 1998b, 1998c, 1999a, 1999b).

This better understanding of the impact of harvesting on

the populations of species in the skin trade is in no way

matched by information available on the species used for live

exports for the pet trade. To meet the demands of the pet mar-

ket, however, rare species are captured only occasionally;

mostly common species are traded to ensure a constant supply

for the customers (see Yuwono 1998, for details).

International customers are more interested in species from

the Australian Realm rather than from the Southeast Asian

Realm of Indonesia. This is possibly related to the fact that

Australia and Papua New Guinea have rigorous export regu-

lations for amphibians and reptiles, and so the limited

availability increases the demand.

Toward improved conservation of amphibians and

reptiles in Indonesia

Summary of the present situation

General issues

Amphibians and reptiles in Indonesia remain a poorly under-

stood group. Although, in recent years, considerable effort has

been put into obtaining a better understanding of the compo-

sition, taxonomic relationships, and geographic distribution of

the amphibians and reptiles of Indonesia, we are still far from

a complete knowledge of species numbers and the basic bio-

geographic patterns and their evolution. In particular, we need

a better understanding of ( 1 ) the number of species occurring

in Indonesia, (2) their relationships to closely related taxa

found in the region, (3) the geographic distribution patterns

within the Indonesian archipelago, (4) the closeness of associ-

ation between certain species and specific vegetation or

ecosystem types, and (5) the habitat and particularly micro-

habitat requirements for most of the Indonesian amphibian

and reptile species.

These may appear as needs from a purely scientific per-

spective, but this information is also essential for

approaching the problem of long-term conservation of

Indonesian amphibians and reptiles. Conservation measures

need to be launched now, despite the fact that our knowledge

of the herpetofauna is still rather fragmentary. For instance,

71 amphibian species, 63 lizard species, 73 snake species,

and one crocodilian; i.e., a total of 208 species of herpetofau-

na, are known from fewer than ten specimens. In most cases,

these species are known only from the type specimens. How

this translates into the conservation status of these taxa is dif-

ficult to assess. For instance, many species listed may be

newly described taxa and not necessarily rare species. Others

have questionable taxonomic status such as some of the

species of the genus Ichthyophis and may also be naturally

rare. Most species known only from the type specimen were

collected from remote areas, and the status of these species

remains unknown. Other species, particularly snakes, may be

naturally rare but may have a wide geographic range within

Indonesia or on the island(s) where they are found.

Local aspects

Studies carried out in Indonesia have been largely conducted

by foreign scientists, in part due to the fact that there is a gen-

eral lack of trained herpetologists in Indonesia, as well as a

lack of funding facilities to conduct herpetological research.

Both issues need to be addressed by Indonesian universities.

Herpetology could, for instance, be much better represented in

the curricula.

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December 2006 I Volume 4 | Number 1 | e16

Plate 52. DOI: 10.1514/journal.arc.0040016g055

Plate 54. DOI: 10.1514/journal.arc.0040016g057

Plate 53. DOI: 1 0.151 4/journal.arc.0040016g056

Plate 55. DOI: 10.1514/journal.arc.0040016g058

Plate 56. DOI: 10.1514/journal.arc.0040016g059

Plate 57.

DOI: 1 0.1 514/joumal.arc.004001 6g060

Plate 58. DOI: 10. 151 4/journal. arc. 004001 6g061 Plate 59. DOI: 10. 1514/journal. arc. 0040016g062

Plate captions: 52. Sphenomorphus nigrilabris. 53. Tropidophorus baconi. 54. Varanus melinus. 55. Varanus indicus. 56. Typhlops lin-

eatus. 57. Cylindrophis melanotus. 58. Xenopeltis unicolor. 59. Chrysopelea rhodopleuron.

Species plates 52, 53, 55, 58, & 59 taken by Jim A. McGuire. Species plate 54 taken by Djoko T. Iskandar. Species plate 58 taken

by Graeme Gillespie. Species plate 56 taken by Alain Compost.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 077 December 2006 | Volume 4 | Number 1 | e16

D. T. Iskandar and W. R. Erdelen

Only slowly are projects and studies planned and carried

out that have amphibians and/or reptiles as the major target

group. Up to now, these were groups only occasionally sam-

pled within programs that were primarily aimed at broader

conservation issues as, for example, conservation of natural

forest ecosystems or wetlands in Indonesia. The only excep-

tion may have been trade-related surveys and studies and

some work on marine turtles.

Most of the work carried out by local organizations

involved species inventories. This work had to face problems

of species identification and comparisons with reference col-

lections. In this context, a strengthening of the role of the

leading museum in Indonesia, the Museum Zoologicum

Bogoriense, is urgently required. This refers to the setting up

of reference collections for researchers, better infrastructure,

and collection materials, and an increase in the number of

highly qualified staff for the different taxonomic groups.

There is still a lack of basic information materials such as

simple field guides or color guides for the most important taxa

of Indonesian amphibians and reptiles. This information is

urgently needed by various groups, especially the local com-

munities and the official authorities (such as PKA and

Customs Control). An internationally sponsored program for

writing local language field guides is a promising step toward

providing a better information basis for professionals, inter-

ested laymen, and the Indonesian authorities. Several agencies

have taken up this issue, including EMDI, Fauna Malesiana,

GEF Biodiversity, IUCN, and the World Bank. As a result,

books about mammals, birds, reptiles, and amphibians have

been published or are presently being prepared.

Taxa-specific issues

Amphibians

Most information about the status of amphibians in

Indonesia is based on studies from neighboring areas, such

as Sarawak, where Stuebing (1994, 1997) studied habitats

and microhabitats of the herpetofauna, including the

amphibian families Bufonidae, Megophryidae,

Microhylidae, Ranidae, and Rhacophoridae. Stuebing ’s

work is of particular relevance for Indonesia as it was car-

ried out in a proposed connected protected area system in

Sarawak and Kalimantan, jointly to be managed by

Malaysian and Indonesian authorities (Lanjak-Entimau and

Betung Kerihun, respectively; the latter until recently

known as Bentuang Karimun). Moreover, Stuebing (1994,

1997) had developed a management plan that focused on the

herpetofauna. Comparable work on the protected area man-

agement level is still lacking in Indonesia. A second

example is the study on the effects of ENSO events on frog

species in New Guinea (Bickford 1998), already discussed

above. To date, we have only cursory information on the

likely effects of prolonged droughts, fire, and haze on pop-

ulations of Indonesian amphibians and, in particular, on

impacts on reproductive cycles. For instance, Iskandar

(1998) described the decline in the endemic toad

Leptophryne cruentata (Bufonidae) from the slopes of

Gede-Pangrango (West Java), most likely caused by the

1981 eruptions of the volcano Mt. Galunggung which last-

ed for about six months. Detailed longitudinal studies of

population changes in Indonesian amphibian species have

not been carried out yet. Accordingly, we do not know

whether a general decline in amphibian numbers as

observed elsewhere is also taking place in Indonesia.

Because of our poor knowledge of the Indonesian amphib-

ian species, we do not have any information against which

to “calibrate” observed changes or trends. This database

needs to be created, possibly as a joint venture between

Indonesian universities and the Museum Zoologicum

Bogoriense. Moreover, there is a strong need for more

detailed taxonomic studies. This is best illustrated in the

frog leg trade (mostly Limnonectes macrodon and L. blythii )

for which actually many species are harvested; some of

them have not even been described scientifically (for details

see Emerson et al. 2000; Iskandar 1996).

Turtles and crocodiles

Although, among reptiles, sea turtles have received the most

attention by international conservation organizations, the situ-

ation of the domestic trade in Indonesia and the smuggling of

specimens or products from Indonesia still remain unknown.

This particularly refers to the green turtle ( Chelonia mydas ),

the species most commonly caught (Suwelo et al. 1995). In a

study by Limpus (1995) it is stated that the “largest slaughter

of green turtles globally occurs within the Australasian

region, including Indonesia" ...., that “ near-total egg harvest

still characterizes the green turtle nesting populations of

Indonesia ”, and that, for the hawksbill turtle ( Eretmochelys

imbricata ), “ substantial harvest for domestic consumption of

meat and scale continues in Cuba, Indonesia ” ... Mass collec-

tion of eggs of all marine turtle species still occurs throughout

Indonesia (Tomascik et al. 1997). With the present economic

situation in Indonesia these trends have been exacerbated and

have been underscored in numerous articles that have

appeared in the media. A national strategy and action plan for

the conservation of marine turtles, already outlined in the

early 1990s, has not been implemented, and current exploita-

tion of marine turtles and their eggs in Indonesia is not

sustainable (Tomascik et al. 1997). The conservation priority

issues compiled by Tomascik et al. include, among others,

improvement of fishing regulations and fishing techniques to

the benefit of marine turtles, better planning of coastal devel-

opment activities and avoidance of pollution in nesting areas,

law enforcement, research on basic biology and ecology, pro-

duction of education materials on conservation of marine

turtles for the general public, and the launching of the relevant

conservation programs by the Government of Indonesia.

Among turtles, least understood is the current situation

of the live export of non-marine chelonians. Already in 1988,

official export statistics for the Asiatic softshell turtle ( Amy da

cartilaginea ) reached 66,500 kg for Sumatra only (details in

Jenkins 1995; Shepherd 2000). During the past decade, vol-

ume in trade has reached enormous dimensions. The species

affected, their relative percentages in the shipments, and then-

precise origin within Indonesia are virtually unknown.

Moreover, to what extent protected or threatened species are

exported as “by-catch” is not known either. For 1994, Jenkins

(1995) listed quota for the Southeast Asian box turtle ( Cuora

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December 2006 I Volume 4 I Number 1 I e16

Plate 60. DOI: 10.1514/journal.arc.0040016g063

Plate 62. DOI: 10.1514/journal.arc.0040016g065

Plate 64. DOI: 10.1514/journal.arc.0040016g067

Plate 61. DOI: 10.1514/journal.arc.0040016g064

Plate 63. DOI: 10.1514/journal.arc.0040016g066

Plate 65. DOI: 10.1514/journal.arc.0040016g068

Plate 66. DOI: 1 0.1 51 4/journal. arc. 004001 6g069 Plate 67. DOI: 1 0.1 51 4/journal. arc. 004001 6g070

Plate captions: 60. Morelia tracyae. 61. Morelia boeleni. 62. Morelia viridis (juvenile). 63. Morelia viridis. 64. Python breitensteini. 65.

Boiga irregularis. 66. Calamaria sp. 67. Calamaria sp.

Species plates 60, 62, & 65 taken by Djoko T. Iskandar. Species plates 66 & 67 taken by Graeme Gillespie. Species plates 61,

63, & 64 taken by Alain Compost.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 079 December 2006 | Volume 4 | Number 1 | e16

D. T. Iskandar and W. R. Erdelen

amboinensis ) of 10,000 specimens, and for Amy da carti-

laginea of 50,000 specimens. However, other sources as

quoted in Jenkins (1995) indicate that the real and actual fig-

ures may be much higher. Annual exports for Cuora

amboinensis were estimated at 200,000 specimens or, more

precisely, plastrons, which were exported from Sulawesi to

Hong Kong as turtle paste (Samedi and Iskandar 2000).

The alarming trends in freshwater and marine turtle

exploitation, particularly in Southeast Asia, have drawn atten-

tion to more rigorous protection measures and implementation

of CITES, respectively. Although a first action plan for tor-

toises and freshwater turtles was already formulated more

than a decade ago (IUCN/SSC Tortoise and Freshwater Turtle

Specialist Group 1989), the situation has dramatically wors-

ened. As pointed out by Jenkins (1995), exploitation patterns

of non-marine chelonians have shifted from harvests for

domestic consumption to large-scale international trade,

mainly for meat consumption, covering hundreds of thou-

sands of individuals annually. Imports by mainland China are

increasing, including massive smuggling, and there are drasti-

cally increased exports from Indonesia, in particular from

Sumatra, Kalimantan, and Sulawesi.

In his introductory remarks to the proceedings of the

1993 international conference on conservation, restoration,

and management of tortoises and turtles, John Behler (1997),

chairman of the respective IUCN/SSC specialist group, stat-

ed that “The great Asian river turtles ( Batagur baska,

Callagur borneoensis, and Orlitia borneensis ) and the giant

softshells ( Chitra spp. and Pelochelys bibroni ) are seriously

depressed and will not long survive without heroic interven-

tion” and that “Today, there is no more serious turtle crisis

than that which is taking place in Southeast Asia and south-

ern China. Some species are very likely being lost in nature

before they can be described” (p. xix). Several of the papers

in the same proceedings addressed questions of tortoise and

non-marine turtle conservation in the Asian region, but not a

single paper dealt with an analysis of the situation in

Indonesia where populations are most heavily exploited for

these turtle groups. In a workshop on trade of freshwater tur-

tles and tortoises in Asia (van Dijk et al. 2000) a number of

recommendations to lessen impacts on natural populations

were formulated. The same appeal is addressed in the book

about the turtles and crocodiles of insular Southeast Asia

(Iskandar 2000). These are not repeated here, but it is hoped

that they will be implemented in the respective countries of

the region, thus reducing or eliminating collecting from the

wild and curtailing demand in consumer countries. If this

cannot be achieved in the near future, then the further exis-

tence of many of the species will be at stake.

Presently six species of crocodiles have been described

from Indonesia, viz. the estuarine crocodile ( Crocodylus poro-

sus ), the New Guinea crocodile (C. novaeguineae), the Bornean

crocodile (C. raninus, Ross et al. 1998), the Siamese crocodile

(C. siamensis ), and the tomistoma or false gharial ( Tomistoma

schlegelii ). The Philippine crocodile (C. mindorensis ) has been

sighted in East Sulawesi, and its occurrence in Indonesia has

been confirmed through observation of specimens in a crocodile

farm near Makassar (Iskandar- 1998, 2000). Crocodylus porosus

and C. novaeguineae are bred in captivity and caught from the

wild for the skin trade. The status of their wild populations

would need to be re-evaluated. Over ten years ago,

Thorbjarnarson (1992) had already found that the estuarine croc-

odile had become rare in Java and Sumatra and that more

information was needed about wild populations in Kalimantan

and the smaller island groups (see Ross et al. 1996, for discus-

sion). The status of C. raninus has been confirmed only recently,

and it remains unclear whether this “species” consists of a

species complex or not (for details see Ross et al. 1996).

Moreover, the status of this species in the wild in Indonesia is

unknown. The Siamese crocodile and Tomistoma were already

listed as endangered in the Conservation Action Plan for croco-

diles (Thorbjarnarson 1992). Next to Thailand, Indonesia was

considered the highest priority for action regarding these two

species. This is reflected in their protection status in Indonesia

(Table 1). The fact that Tomistoma schlegelii is now considered

endangered only indicates the need for further surveys on the

status of this species, particularly with regard to its occurrence in

Sulawesi. In addition, the status of C. siamensis in Indonesia - it

was only reported from Kalimantan in the mid-1990s (Ross et al.

1996) - is unknown. According to Ross et al. (1996) the Siamese

crocodile has not been “imported” to Kalimantan but occurs

there naturally. In sum, more work on the systematic status of

some of the Indonesian crocodilians as well as detailed studies

of the status of their wild populations are urgently needed.

Lizards and snakes

Probably the least understood groups among Indonesian amphib-

ians and reptiles are the lizards and snakes. Accordingly, for

these groups only scanty information that was available was

included into the lists compared here (Table 1 ). The reasons why,

for instance, only some of the larger agamid species have been

considered, remain unclear. For Lanthanotus no published evi-

dence exists (yet) that this species occurs in Indonesia. To date,

it has only been reported from Sarawak, in the East Malaysian

state of Borneo, but according to information from traders and

local people, it also occurs in West Kalimantan. Efforts are

presently being undertaken to publish a series of guides with

color photographs to facilitate identification of the most common

amphibian and reptile species utilized in Indonesia. Long-term

experience in the pet trade has shed light on taxonomic uncer-

tainties, especially in taxa that are distributed in eastern Indonesia

such as the Tiliqua gigas and T. scincoides species complex or

species (see Yuwono 1998; Shea, 2000). Candoia carinata had

been known as a very variable species, and is now split into three

species. Two of them have two subspecies and the other has six

subspecies (Smith et al. 2001). Morelia amethistina shows con-

siderable morphological and color variation (Yuwono 1998) and

was recently split into four species (Harvey et al. 2000). Most

new monitor lizards from East Indonesia that were described

after the year 1997 first appeared in trade under the identity of

other species due to the lack of regulation to control undescribed

species (i.e. Bohme et al. 2002; Bohme and Jacobs 2001 ; Bohme

and Ziegler 1997; Eidenmuller and Wicker 2005; Harvey and

Barker 1998; Jacobs, 2003; Philipp etal. 1999; Sprackland 1999;

Ziegler et al. 1999). The criteria that led to the inclusion of

lguanognathus werneri and Anomochilus leonardi into the

IUCN list remain unclear. There is virtually no information

available on these species, and quite a number of similarly poor-

ly known species should be included on the list if ignorance

Amphib. Reptile Conserv. | http://www.herpetofauna.org 080

December 2006 I Volume 4 | Number 1 | e16

Plate 68. DOI: 1 0.1 51 4/journal.arc.004001 6g071

Plate 69.

DOI: 1 0.1 51 4/journal. arc. 004001 6g072 Plate 70.

DOI: 1 0.1 514/joumal.arc.004001 6g073

Plate 71. DOI: 10. 1514/journal. arc. 0040016g074 Plate 72. DOI: 10.1 51 4/journal. arc. 004001 6g075

Plate captions: 68. Cerberus rynchops. 69. Candoia carinata. 70. Chrysopelea paradisii celebensis. 71. Dendrelaphis caudalineatus.

72. Dendrelaphis punctulatus.

Species plates 68-70, & 72 taken by Jim A. McGuire. Species plate 69 & 71 taken by Djoko T. Iskandar.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 081

December 2006 I Volume 4 I Number 1 I e16

Plate 77. DOI: 10.151 4/journal.arc.004001 6g080

Plate captions: 73. Elaphe erythrura. 74. Enhydris matannensis. 75. Rhabdophis chrysargoides. 76. Rhabdophis subminiatus.

77. Acantophis praelongus.

Species plates 74 & 76 taken by Djoko T. Iskandar. Species plates 73, 75, & 77 taken by Jim A. McGuire.

Amphib. Reptile Conserv. | http://www.herpetofauna.org

082

December 2006 I Volume 4 | Number 1 | e16

Plate 73. DOI: 1 0.1 51 4/journal.arc.004001 6g076

Plate 75. DOI: 1 0.1 51 4/journal.arc.004001 6g078

Plate 74. DOI: 1 0.1 51 4/journal. arc. 004001 6g077

Plate 76. DOI: 1 0.1 51 4/journal.arc.004001 6g079

Plate 78. DOI: 10.1514/journal.arc.0040016g081

Plate 79.

DOI: 10. 151 4/journal. arc. 004001 6g082 Plate 80.

DOI: 1 0.1 514/journal.arc.004001 6g083

Plate 83. DOI: 10.1514/journal.arc.0040016g086

Plate captions: 78. Stegonotus modestus. 79. Aspidomorphus mulleri. 80. Ophiophagus hannah. 81. Tropidolaemus wagleri.

82. Chelodina reimannii. 83. Chelodina siebenrocki.

Species plates 78, 79, 82, & 83 taken by Djoko T. Iskandar. Species plates 80 & 81 taken by Alain Compost.

Amphib. Reptile Conserv. | http://www.herpetofauna.org 083

December 2006 I Volume 4 I Number 1 I e16

D. T. Iskandar and W. R. Erdelen

about a taxon is a criterion for inclusion into IUCN Red Lists,

particularly as a threatened species.

As far as skin trade is concerned, further studies on

Ptyas mucosa are planned to eventually provide evidence that

skin trade in this species could be resumed again after the ban

in 1994. For skins that had been on stock for sometime,

export permits have recently been issued by PKA. Another

problem refers to the cobras. Whereas several species are list-

ed as one taxon in the IUCN list, only for one species (Naja

sputatrix ) are quota issued by the Indonesian authorities.

Although the greater number of specimens are certainly N.

sputatrix, nevertheless an unknown number of other cobra

species may be harvested from Sumatra and Kalimantan. In

short, although surveys on harvest levels of cobras have

already been undertaken (Boeadi et al. 1998; Sugardjito et al.

1998), we need more information for an overall assessment

of harvest levels, especially for the island of Java, where most

of the cobras are caught for the food market and skins are

used as byproducts.

A set of measures for the future

Generally, much more research is needed to provide better

information on which to base conservation measures for

amphibians and reptiles in Indonesia. This should be earned

out both by local and foreign scientists and should involve

both basic and applied research components. The latter should

place emphasis on conservation of herpetological diversity as

part of ongoing and future programs in biodiversity conserva-

tion and sustainable use in Indonesia. The most pressing

problems amphibians and reptiles in Indonesia are facing at

the moment are, in our opinion, either related to their conser-

vation and/or to their sustainable use. More specific

recommendations regarding the trade situation have been

made (Erdelen 1998b) and are not further discussed here.

A “research-coordinating” and “information-dissemi-

nating” body might be useful to identify research needs and

ensure that information on ongoing research and published

results are made available in Indonesia. This coordinating

body should consist of representatives of the official

Indonesian authorities such as LIPI and PKA, as well as rep-

resentatives of universities, nongovernmental organizations,

the trade community, and other interest groups (e.g., from the

industrial sector).

For future research programs and the dissemination of

information, as indicated above, an overview of project

reports and other unpublished materials, so-called “gray lit-

erature,” available from various Indonesian authorities, and

an analysis of conservation-related results already reported

in these sources might make further research more effective

by avoiding duplication of work already carried out earlier

in Indonesia. These efforts, however, would require the cre-

ation and management of a centralized database. Location

of this database, combined with a library that contains other

relevant published information, as well as staffing, would

need funding, the greater part of which would naturally

have to come from external sources. Several specific initia-

tives have been launched already, such as the LIPI database

which contains information on plants and animals in its col-

lections. In addition, Conservation International has

launched a CD-ROM with comprehensive environmental

information about Papua.

To develop necessary local expertise, Indonesian univer-

sities need to put more emphasis on teaching amphibian and

reptile biology and systematics. This might require changes in

the curriculum as well as good working groups in zoological

systematics. The major aim should be to train more students in

field techniques and methodology in zoological systematics

for later degree work in herpetology. Teaching needs could be

met either by Indonesian scientists only or in cooperation with

visiting foreign scientists.

A basis for regular exchange of information among all

people interested in herpetology in Indonesia is clearly need-

ed. This may eventually lead to the development of public

awareness programs aimed at making amphibians and rep-

tiles a more ’’popular 44 group of animals in Indonesia. This

exchange of information could be arranged by the formation

of a herpetological working group and/or by providing and

exchanging this information through the Internet.

Conclusions and outlook

Without doubt we need to put more efforts in improving our

understanding of the composition, the geographic distribution,

and habitat and microhabitat requirements of the herpetofauna

of Indonesia. In addition, however, amphibians and reptiles

need to be seen as an important component of the megadiversi-

ty of Indonesia and thus need to be more explicitly included into

conservation measures such as setting aside protected areas or

giving species a particular protection status. The more we learn

about the herpetofauna, the more we will probably realize that

many species comprise genetically different units, which should

be the target of conservation genetic approaches to biodiversity

conservation. Last, but certainly not least, amphibians and rep-

tiles with their general low mobility and great evolutionary age

may prove to be key groups toward an understanding of the bio-

geography of the world’s largest archipelago.

Acknowledgments. — The authors are grateful to Aaron

Bauer, Wolfgang Bohme, L. Anathea Brooks, Indraneil Das,

Alfred Gramstedt, Bob Inger, and Tony Whitten for providing

useful information and for constructive comments on earlier

drafts of the manuscript. We thank Linny Ayunahati and Pilar

Chiang-Joo for drawing the figure and Boeadi, Ed Colijn,

George Saputra, and Frank Yuwono for many discussions on

issues raised in our paper. We wish to express our sincere

gratitude to Alain Compost, Graeme Gillespie, and Jim

McGuire who provided many of the excellent color photo-

graphs.

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Manuscript received: December 2001; Accepted: 2005; Published:

26 December 2006

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