Published in the United States of America

2013 • VOLUME 6 • NUMBER 2

AMPHIBIAN & REPTILE

Editor

Raul E. Diaz

University of Kansas, USA

Craig Hassapakis

Berkeley, California, USA

Associate Editors

Howard O. Clark, Jr. Erik R. Wild

Garcia and Associates, USA University of Wisconsin-Stevens Point, USA

Assistant Editors

Alison R. Davis

University of California, Berkeley, USA

Daniel D. Fogell

Southeastern Community College, USA

Editorial Review Board

David C. Blackburn

California Academy of Sciences, USA

Bill Branch

Port Elizabeth Museum, SOUTH AFRICA

Jelka Crnobrnja-Isailovc

IBISS University of Belgrade, SERBIA

C. Kenneth Dodd, Jr.

University of Florida, USA

Lee A. Fitzgerald

Texas A&M University, USA

Adel A. Ibrahim

Ha’il University, SAUDIA ARABIA

Harvey B. Lillywhite

University of Florida, USA

Julian C. Lee

Taos, New Mexico, USA

Rafaqat Masroor

Pakistan Museum of Natural History, PAKISTAN

Peter V. Lindeman

Edinboro University of Pennsylvania, USA

Henry R. Mushinsky

University of South Florida, USA

Elnaz Najafimajd

Ege University, TURKEY

Jaime E. Pefaur

Universidad de Los Andes, VENEZUELA

Rohan Pethiyagoda

Australian Museum, AUSTRALIA

Nasrullah Rastegar-Pouyani

Razi University, IRAN

Jodi J. L. Rowley

Australian Museum, AUSTRALIA

Peter Uetz

Virginia Commonwealth University, USA

Larry David Wilson

instituto Regional de Biodiversidad, USA

Allison C. Alberts

Zoological Society of San Diego, USA

Michael B. Eisen

Public Library of Science, USA

Russell A. Mittermeier

Conservation International, USA

Advisory Board

Aaron M. Bauer

Villanova University, USA

James Hanken

Harvard University, USA

Robert W. Murphy

Royal Ontario Museum, CANADA

Walter R. Erdelen

UNESCO, FRANCE

Roy W. McDiarmid

USGS Patuxent Wildlife Research Center, USA

Eric R. Pianka

University of Texas, Austin, USA

Antonio W. Salas

Environment and Sustainable Development, PERU

Dawn S. Wilson

AMNH Southwestern Research Station, USA

Carl C. Gans

(1923-2009)

Honorary Members

Joseph T. Collins

(1939-2012)

Cover :

Agalychnis lemur (SMF 89959), Cerro Negro, PNSF, Veraguas [Reference this issue: 6(2): 9-30 (e46)]. Photo by Arcadio Carrizo.

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Amphibian & Reptile Conservation 6(2):2-4.

Short Communication

New records of the Dice snake, Natrix tessellata, in the Suez

Canal zone and Sinai

ADEL A. IBRAHIM

Department of Environmental Sciences, Faculty of Science, Suez Canal University, 43527 Suez, EGYPT

Abstract . — Ten years of herpetological surveys in the Suez Canal zone revealed that Natrix tessel-

lata was most common in fresh water irrigation canals. It is recorded herein for the first time in Port

Said and Suez provinces and discovered in Sinai.

Key words. Dice snake, Natrix tessellata, Suez Canal, Sinai, new records

Citation: Ibrahim AA. 2012. New records of the Diced snake, Natrix tessellata, in the Suez Canal zone and Sinai. Amphibian & Reptile Conservation

6(2):2-4(e42).

The Dice snake ( Natrix tessellata-. Figs. 1 and 2) was

long known from the northern part of the Nile Delta

(Anderson 1898; Flower 1933; Marx 1968; Saleh 1997),

and its distribution extended in the lower extremes of

the River Nile as far as A1 Wasta in Bani Suef province

(Baha El Din 2011). However, no record of A. tessellata

was known from Sinai, and its distribution in the Suez

Canal zone was lacking.

The Dice snake (. Natrix tessellata) was first reported

from the Suez Canal zone by Werner (1983) referring to

an individual collected by Tortonese in 1948 from Qas-

sasin, 35 km west of the Suez Canal in the Ismailia prov-

ince, and two other individuals, one found eight km south

of Ismailia and the other, west of Bitter Lakes. Recently,

N. tessellata was reported from several different locali-

ties in the Suez Canal area (all in the Ismailia region).

Stein and Helmy (1994) reported the snake from Ismailia

gardens; they also recorded an individual from Balir A1

Baqar, a town in Sharqiya province, not Port Said prov-

ince as they claimed (the town is located 35 km west

of the Suez Canal). Two snakes were collected by the

author from Ferdan (10 km N. Ismailia), and Ain Ghos-

sain (15 km S. Ismailia) and deposited in the Museum

National d’Historire Naturelle, Paris (MNHN 2000.5147

and 2000.5148). Baha El Din (2011) reported this spe-

cies 48 km south of Port Said and associated it with Port

Said; however, a locality at the stated distance actually

is in Ismailia province. A ten-year herpetological survey

in the Suez Canal region by the author revealed that N.

tessellata is wide-spread in fresh water irrigation canals,

which constitute a huge irrigation web along the Suez

Canal west bank, from Port Said to Suez (Table 1 and

Fig. 3), thus documenting its first record from both Port

Correspondence. Email: dolaibrahim@yahoo.com

Said and Suez provinces. At Al-Ganayen of Suez, it ap-

proaches the Red Sea within five km. The Dice snake is

well-known to Suez Canal farmers as a non-venomous

snake; however, many people still continue to kill them

unnecessarily.

The Dice snake was transported to the east bank of

the Suez Canal through the fresh water canal connecting

west to east (Sinai) at Deversoir. At Meet Abul Koum Al-

Jadidah, a road-killed snake was first observed in 2008

documenting its first occurrence in Sinai. This species is

now widely distributed in fresh water canals irrigating

newly cultivated lands east of Bitter Lakes in Sinai.

Acknowledgments. — I thank Dr. Mohammad Here-

her for drawing the location map, and Craig Hassapa-

kis for editing the early draft of this manuscript. Many

thanks are due to the reviewers, John Simmons and Dr.

Konrad Mebert for their valuable comments and sugges-

tions.

Literature cited

Anderson J. 1898. Zoology of Egypt. Volume 1. Reptilia

and Batrachia. Quaritch, London. 370 p.

Baha El Din S. 2011. Distribution and recent range ex-

tension of Natrix tessellata in Egypt. Mertensiella

18:385-387.

Flower SS. 1933. Notes on the recent reptiles and am-

phibians of Egypt, with a list of the species recorded

from that kingdom. Proceedings of the Zoological So-

ciety of London 103(3):735-851.

amphibian-reptile-conservation.org

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March 2012 | Volume 6 | Number 2 | e42

Ibrahim

Figure 1. Natrix tessellata, Ismailia city, 7 August 2007. Photo: Adel A. Ibrahim.

Figure 2. Natrix tessellata, Deversoir, 24 May 2008. Photo: Adel A. Ibrahim.

amphibian-reptile-conservation.org

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March 2012 | Volume 6 | Number 2 | e42

New Dice snake record

Marx H. 1968. Checklist of the Reptiles and Amphibians

of Egypt. U.S. Naval Medical Research Unit No. 3,

Cairo. 51 p.

Saleh MA. 1997. Amphibians and Reptiles of Egypt.

Publication of National Biodiversity Unit (Egypt) No.

6. 234 p.

Stein K, Helmy I. 1994. Some new distribution records

for the snakes of Egypt (Squamata: Serpentes). Bul-

letin of the Maryland Herpetological Society 3: 15-26

Werner YL. 1983. Lizards and snakes from eastern low-

er Egypt in the Hebrew University of Jerusalem and

Tel Aviv University, with range extensions. Herpeto-

logical Review 14(1):29-31.

Manuscript received: 27 January 2012

Accepted: 26 February 2012

Published: 13 March 2012

Table 1. Locations of Natrix tessellata in the Suez Canal zone

and Sinai.

Location

Date

Coordinates

1

8 km S. Port Said

25.5.2009

31° 10' 54"

'N,

32° 18' 12'

'E

2

Abu Khalifa Ezbet Attawwab

31.7.2002

30° 46’ 30"

'N,

32° 15' 41'

'E

3

Km 17, N.W. Ismailia

13.5.2009

30° 44’ 00"

'N, 32° 13' 42"

E

4

Qaryat Assama’ana

9.5.2005

30° 43’ 23"

'N,

32° 15' 34'

'E

5

Ferdan

11.5.2000

30° 39’ 42"

'N, 32° '19' 49"E

6

Km 8, N.W. Ismailia

25.5.2009

30° 39’ 41"

'N,

32° 15' 31'

'E

7

Km 6, N.W. Ismailia

24.6.2008

30° 38’ 35"

'N, 32° 15' 07"

E

8

4 km N.W. Ismailia

23.7.2004

30° 37’ 43"

'N,

32° 14' 30'

'E

9

Ismailia City

7.8.2007

30° 35’ 19"

'N,

32° 16' 56'

'E

10

Al-Manayef

5.3.2006

30° 33’ 13"

'N,

32° 11' 54”

'E

11

Ain Ghosain

16.7.1999

30° 30’ 45"

'N,

32° 18' 13'

'E

12

Meet Abul Koum Al-Jadidah, S.

25.5.2008

30° 25’ 28"

'N,

32° 24' 47'

'E

13

Al-Aqqadah

1.6.2001

30° 26’ 01"

'N,

32° 20' 13'

'E

14

Deversoir

24.5.2008

30° 25’ 33"

'N,

32° 20' 49'

'E

15

Jeneeva

8.5. 2002

30° 12’ 23"

'N,

32° 25' 43'

'E

16

Al-Ganayen, Suez

31.5.2001

29° 59’ 53"

'N,

32° 33' 07'

'E

32°0'0"E 32°20'0"E

1 1 “ 1

32°0'0”E 32°20'0"E

Figure 3. Distribution of N. tessellata in the Suez Canal zone

and Sinai.

ADEL IBRAHIM is associate professor of zoology (herpetologist), was previously head of the De-

partment of Environmental Sciences, Suez Canal University, Suez, Egypt, and is currently a visiting

professor at Ha’il University, Saudia Arabia. Adel has published 33 scientific papers (all in the field of

herpetology), and currently two chapters in Amphibians of Egypt and Amphibians of Libya (In press).

Adel has researched the herpetofauna of Sinai since 1987 and the Suez Canal zone for more than 10

years. Adel is an avid photographer having contributed about 40 photos of reptile species to the Reptile

Database: http://www.reptile-database.org/. He is member of the International Herpetological Com-

mittee Advisory Board 2005-2012 (elected at the 5 th World Congress of Herpetology, South Africa).

amphibian-reptile-conservation.org

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March 2012 | Volume 6 | Number 2 | e42

Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the

original author and source are credited.

Amphibian & Reptile Conservation 6 ( 2 ): 5 - 8 .

Books to Read

“Books to Read” is Amphibian and Reptile Conservation's recommended book section that pres-

ents and publicizes books related to the “Sustainable Management of Amphibian and Reptile Bio-

diversity” and related topics. Information given is on author(s) or editor(s), publisher, copyright,

dimensions, cover art, and International Serial Book Number (ISBN). Short descriptions and book

reviews will be presented where possible. For potential book reviews and listing in “Books to

Read” address email to Craig Hassapakis at: arc.publisher@gmail.com. To assist our tracking

please email subject heading as“Book Review” with date as “dd/mm/yyyy.” Postal mail book(s)

for review and publicity to: Craig Hassapakis, 2525 Iowa Avenue, Modesto, California 95358-

9467, USA.

Reptile Biodiversity: Standard

Methods for Inventory and

Monitoring

Editors, Roy W. McDiarmid, Mercedes S.

Foster, Craig Guyer, J. Whitfield Gibbons, and

Neil Chemoff. University of California Press,

Berkeley, California. First edition, January 12,

2012.

Product dimensions: 11.1 x 8.4 x 1.1 inches,

xii + 412 pages. Hardcover: US$67.00. ISBN:-

13: 978-0-520-26671-1.

Amphibians and Reptiles: An

Introduction to Their Natural

History and Conservation

By Marty Crump. The McDonald & Wood-

ward Publishing Company, Granville, Ohio.

September 20,2011.

Product dimensions: 8.9 x 6.9 x 0.7 inches.

Children 5th to 8th grade and older, ix + 249

pages. Paperback: US$29.95. ISBN-13: 978-1-

935778-20-2.

amphibian-reptile-conservation.org

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April 2012 | Volume 6 | Number 2 | e40

Hassapakis

Patterns of

Distribution of

Amphibians

A GLOBAL PUSFIt

I t I 1 ! B

William E. Duellman

Patterns of Distribution

of Amphibians: a Global

Perspective

Editor, William Duellman. The John Hopkins

University Press, Baltimore, Maryland. First

edition, July 20, 1999.

Product dimensions: 10.3 x 7.4 x 1.5 inches.

648 pages. Hardcover: US$90.00. ISBN- 13:

978-0-8018-6115-4.

Measuring and Monitoring

Biological Diversity: Standard

Methods for Amphibians

(Biological Diversity Handbook)

Editor, W. Ronald Heyer. Smithsonian Books,

Washington, D.C. First edition, February 17,

1994.

Product dimensions: 6.9 x 0.8 x 1.0 inches.

364 pages. Paperback: US$23.87. ISBN-13:

978-1-56098-284-5.

amphibian-reptile-conservation.org

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April 2012 | Volume 6 | Number 2 | e40

Books to Read

THE BIOLOGY OF ANURAN LARVAE

Edited by

Roy W MeDiarmid and Ronald Altig

Tadpoles: The Biology of Anuran

Larvae

Editors, Roy W. MeDiarmid and Ronald Altig.

University of Chicago Press, Chicago, Illinois.

First edition, October 1, 2000.

Product dimensions: 10.9 x 8.4 x 1.0 inches.

Hardcover: US$90.00; Paperback: US$47.50

ISBN-13: 978-0-226-55763-2.

A Natural History of

Amphibians

By Robert C. Stebbins and Nathan W. Cohen.

Princeton University Press, Princeton, New

Jersey. January 6, 1997.

Product dimensions: 9.1 x 6.0 x 0.8 inches.

332 pages. Paperback: US$31.95. ISBN- 13:

978-0-691-10251-1.

amphibian-reptile-conservation.org

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April 2012 | Volume 6 | Number 2 | e40

Hassapakis

The Chromosomes of

Terraranan Frogs

Insights into Vertebrate Cytogenetics

Editors

The Iguanid Lizards of Cuba

By Lourdes Rodriguez Schettino. University

Press of Florida, Gainesville, Florida. First

edition, December 31, 1999.

Product dimensions: 9.5 x 6.4 x 1.5 inches.

448 pages. Hardcover: US$85.00. ISBN-13:

978-0-8130-1647-4.

The Chromosomes of Terraranan

Frogs: Insights into Vertebrate

Cytogenetics

Editors, M. Schmid, Wiirzbur, J.P. Bogar, and

S.B. Hedge. S. Karger AG, Basel, Switzerland.

First edition, October 25, 2010.

Product dimensions: 11.1 x 8.6 x 1.2 inches.

568 pages. Hardcover: US$797.00. ISBN-13:

978-3-8055-9607-7.

Citation: Hassapakis C. 2012. Books to Read. Amphibian & Reptile Conservation 6(2):5-8(e40).

Published: 11 April 2012

amphibian-reptile-conservation.org

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April 2012 | Volume 6 | Number 2 | e40

Agalychnis lemur (SMF 89959), Cerro Negro, PNSF, Veraguas. Photo by AC.

amphibian-reptile-conservation.org

009

April 2012 | Volume 6 | Number 2 | e46

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original author and source are credited.

Amphibian & Reptile Conservation 6(2):9-30.

Field notes on findings of threatened amphibian species in

the central mountain range of western Panama

' 24 ANDREAS HERTZ, 12 SEBASTIAN LOTZKAT, 3 ARCADIO CARRIZO, 3 MARCOS PONCE,

'GUNTHER KOHLER, AND 2 BRUNO STREIT

department of Herpetology’, Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, Senckenberganlage 25, 60325 Frankfurt am Main,

GERMANY 2 Johann Wolfgang Goethe-University, Biologicum, Dept, of Ecology and Evolution, Max-von-Laue-Str. 13, 60438 Frankfurt am Main,

GERMANY 3 Institute de Ciencias Ambientales y Desarrollo Sostenible, Universidad Autonoma de Chiriqiu, David, PANAMA

Abstract . — During field work along a transect in the Cordillera Central of western Panama between

2008 and 2010, we detected several populations of amphibian species which are considered as

“Endangered” or “Critically Endangered” by the IUCN. Some of these species had suffered from

serious population declines, probably due to chytridiomycosis, but all are generally threatened by

habitat loss. We detected 53% of the Endangered and 56% of the Critically Endangered amphibian

species that have previously been reported from within the investigated area. We report on findings

of species that have not been found in Panama for many years, and provide locality data of newly

discovered populations. There is a need to create a new protected area in the Cerro Colorado area

of the Serrania de Tabasara, where we found 15% of the Endangered and Critically Endangered am-

phibian species known to Panama.

Resumen . — Durante trabajo de campo en un transecto a lo largo de la Cordillera Central en el oeste

de Panama entre 2008 y 2010, encontramos varias poblaciones de anfibios que son considerados

“En Peligro” o “En Peligro Critico” por la UICN. Algunas de estas especies habian sufrido serias

disminuciones de sus poblaciones, probablemente causadas por la quitridiomicosis, pero todas se

encuentran amenazadas por perdida de habitat. Detectamos el 53% de las especies En Peligro y el

56% de las especies En Peligro Critico que se habian reportado previamente en el area de estudio.

Reportamos hallazgos de especies que no se habian avistado en Panama por muchos ahos, asi

como localidades de poblaciones descubiertas por primera vez. Se requiere crear una nueva area

de proteccion en los alrededores del Cerro Colorado en la Serrania de Tabasara, donde se han en-

contrado 15% de los anfibios En Peligro y En Peligro Critico de todo Panama.

Key words. Anura, Batrachochytrium dentrobatidis ( Bd ), decline, Panama, Serrania de Tabasara, Serrania de Tala-

manca, Urodela

Citation: Hertz A, Lotzkat S, Carrizo A, Ponce M, Kohler G, Streit B. 2012. Field notes on findings of threatened amphibian species in the central range

of western Panama. Amphibian & Reptile Conservation 6(2):9-30(e46).

Introduction

Amphibian populations are declining or disappearing

around the globe at an alarming rate, and are the most

threatened vertebrate class on earth (Daszak et al. 1999;

Stuart et al. 2004; Gascon et al. 2007). The most obvi-

ous threat to tropical amphibians and to biodiversity in

general, comes from anthropogenic activities such as de-

forestation, habitat modification, and contamination. In

addition, from the late 1980s on, even amphibian popula-

tions in pristine, undisturbed habitats have begun to de-

cline enigmatically. These enigmatic declines have been

especially severe at upland sites of Australia (Campbell

1999) and the Neotropics (Young et al. 2001, 2004; Lips

et al. 2006). In particular, lower central America has suf-

Correspondence. Email: 4 ahertz@senckenberg.de

fered from multiple amphibian population declines that

were well documented (e.g., Crump et al. 1992; Young et

al. 2001; Lips 1999; Lips et al. 2006; Ryan et al. 2008).

After several experts have conducted research regard-

ing the causes, these enigmatic amphibian die-offs and

population declines could be clearly associated with, an

emerging infectious disease (EID) (Daszak et al. 2000)

caused by the fungus Batrachochytrium dendrobati-

dis (Bd) soon known as chytridiomycosis (Berger et al.

1998; Daszak et al. 1999; Ryan et al. 2008). The mortal-

ity rate of infected individuals can be as high as 100%

in some populations (Lips et al. 2003b), but not all spe-

cies have been affected equally. Due to the physiology of

Bd , which grows best at temperatures between 17-28 °C

(Piotrowski et al. 2004), populations in tropical moun-

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April 2012 | Volume 6 | Number 2 | e46

Hertz et al.

tainous habitats are more likely to be affected than those of extinction in the wild. Most species mentioned in this

in tropical lowlands (Longcore et al. 1999; Andre et al. paper are highly susceptible to Bd infection and have

2008). Montane riparian or lentic amphibian species are suffered dramatic population declines in Costa Rica and

at highest risk to Bd infection and population decline Panama, although their distribution areas comprise well-

(Lips et al. 2003b; Kriger and Hero 2007). Furthermore, protected areas like national parks and protected forests

degree of disease susceptibility of species depends on (IUCN 2011). Others have always been rare and are only

their particular immunologic defence in terms of quan- known from a few specimens. Almost all of these spe-

tity and quality of antimicrobial skin peptide mixtures cies have not been reported for many years and most of

(Woodhams et al. 2006). them are the only persisting populations known. We also

Chytridiomycosis first appeared in western Panama inspected some of the collected voucher specimens for

between 1993 and 1994 and spread in a wave-like man- chytrid infection by either histological examination of

ner south-eastward, crossing the Panama Canal in 2007 skin scrapings or PCR testing of skin swabbings. More-

(Lips et al. 2008; Woodhams et al. 2008). The disease over, we provide information on localities and contexts

has caused population declines and loss of amphibian of our findings and add brief ecological field notes on

diversity wherever it has been detected (Crawford et every species,

al. 2010a). Since Bd ’’ s arrival, many formerly abundant

species have disappeared or become rare. Only recently,

reports on rediscoveries or newly discovered popula- Material and methods

tions of amphibian species, which were thought to be

lost, have been reported (Puschendorf et al. 2005; Lotz- Between 2008 and 2010, we collected amphibian species

kat et al. 2007; Rodriguez-Contreras et al. 2008; Kolby along a transect which covered the continental divide

and McCranie 2009; Abarca et al. 2010; McCranie et al. mainly above 1000 m a.s.l., from the Costa Rican-Pana-

2010), but none from Panama. manian border to about 81 degrees of western longitude.

Our objective is to report on amphibian species found Only two findings were made prior to this project (see

in the central mountain range of western Panama facing Isthmohyla angustilineata and Oedipina grandis ac-

a high (IUCN category: Endangered, EN) to extremely counts) in 2006. An overview of the investigated area,

high (IUCN category: Critically Endangered, CR) risk with all localities sampled, is shown in Fig. 1 below.

82°30'W 82°0'W 8r30'W 81 o 0'W

82°30'W 82°0'W 81°30'W 81"0'W

Figure 1 . Sampled localities in the central mountain range of western Panama (Cross hatched area = transect, white dots = collect-

ing sites).

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April 2012 | Volume 6 | Number 2 | e46

Threatened amphibian species in western Panama

We collected all specimens (adults and larvae) dur-

ing opportunistic searches mostly at night. We obtained

coordinates and altitude of the study sites using a Gar-

min GPS Map 60 CSx GPS receiver or alternatively a

Garn i i n Etrex Summit, both with integrated barometric

altimeters. For preservation and preparation of voucher

specimens we follow the recommendations of Kohler

(2001). We assigned tadpoles to Gosner stages (Gosner

1960) prior to identification. We identified specimens to

the species level using the dichotomous keys of Kohler

(2011), Savage (2002), and Duellman (2001), and if nec-

essary original species descriptions. We deposited vouch-

er specimens (listed in Appendix I) in the collection of

the Senckenberg Forschungsinstitut und Naturmuseum

Frankfurt, Germany (SMF), those labelled with AH field

numbers will be included into the Museo Herpetologico

de Chiriqui (MHCH), the herpetological collection of the

Universidad Autonoma de Chiriqui, David, Panama.

We created all maps using ArcGIS 10, and calculat-

ed mean distances of populations to the next Protected

Area with the “Near” tool in the “Proximity” folder. We

obtained map layers from the map server of the Smith-

sonian Tropical Research Institute (STRI) (URF: http://

map server, str i . si.edu/ geonetwork/srv/en/ main, horn e) .

All maps and coordinates are in the geographic coordi-

nate system and WGS 1984 datum. We rounded coordi-

nates to the second decimal place; elevations are rounded

to the next tenth.

Some of the detected specimens have been tested for

infection with Batrachochytrium dentrobatidis. There-

fore, we gently rubbed a cotton swap over the ventral

surfaces of the pelvic patch and inner thighs following

the sampling guidelines of Hyatt et al. (2007). Testing

for Bd was performed by real-time Taqman PCR assay

following the protocol of Boyle et al. (2004). Because

this technique was not available to us prior to 2010, we

did not take PCR samples from all specimens. Further,

we examined 10 specimens collected before 2010 by

histological examination of stained skin scrapings, for

detection of Bd thalli and sporangia. We took skin scrap-

ings from the ventral surface of the inner left thigh of

preserved animals and stained them with 0.01% solution

of Congo Red dye dissolved in PBS buffer (pH 7.4) and

stained for 20 minutes (Briggs and Burgin 2003, 2004).

Stained scrapings were examined with bright-field mi-

croscopy using a Bresser Biolam optical microscope.

Since the most recently published list of amphibian

species known to occur in Panama (Jaramillo et al. 2010),

ongoing investigation has led to some changes and ad-

ditions to this list. To get an updated list (Appendix II)

of the amphibian species that are currently known to be

native in Panama we updated and revised the list of Jara-

millo et al. (2010). First we included all species that have

been added to the Panamanian herpetofauna after 2010.

These are (with references in parentheses): Agalychnis

annae (Hertz et al. 2011), Craugastor evanesco (Ryan et

al. 2010b), Incilius karenlipsae (Mendelson and Mulca-

hy 2010), Pristimantis adnus (Crawford et al. 2010b) and

P. educatoris (Ryan et al. 2010a). Moreover, we includ-

ed Bolitoglossa pygmea and B. robinsoni (Bolanos and

Wake 2009) not found in Jaramillo et al. (2010). Because

of taxonomic changes we exchanged Rhinella granulosa

for R. centralis (Narvaes and Rodriguez 2009), and ex-

cluded Agalychnis lithodryas that we treat as a synonym

of A. spurelli (Ortega- Andrade 2008). We follow Kohler

2011 and list Lithobates taylori in place of L. pipiens

complex. Although Hyalinobatrachium vireovittatum

might be a synonym of H. talamancae (Kubicki 2007;

Hertz et al. 2011) we decided to list both species until

further investigation has been conducted. The same deci-

sion was taken for Relictivomer pearsei that might be a

synonym of Elachistocleis ovalis, and both taxa are listed

as present in Panama. Further, we excluded the three in-

troduced species Eleutherodactylus antillensis, E. jolm-

stonei , and E. planirostris (Crawford et al. 2011).

In the following text we use the abbreviation PA for

“Protected Areas” and abbreviations for Panamanian PAs

(in parentheses) reflect their original names in Spanish:

Parque Internacional Fa Amistad (PIFA); Parque Nacio-

nal Volcan Baru (PNVB); Reserva Forestal Fa Fortuna

(RFFF); Bosque Protector Palo Seco (BPPS); Parque

Nacional Santa Fe (PNSF). Abbreviations of IUCN cat-

egories follow IUCN (201 1).

Results

We now count 206 native species of amphibians known

to occur in Panama. Of these, 23 species (11%) are con-

sidered Endangered (EN) and 22 (11%) Critically Endan-

gered (CR) as defined by the IUCN (Fig. 2).

LC

53 %

Figure 2. Percentage of Panamanian amphibian species in each

IUCN category.

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Hertz et al.

In total 33 (73%) of those 45 species, in detail 17

(74%) of the 23 species in the EN and 16 (73%) of the

22 species in the CR categoiy, are known to occur within

the investigated area (Appendix II). During this study we

found 18 (55%) of these 33 species, on which we report

below. We further present the positive results of analysis

of skin swabbings and histological examination for pres-

ence of Bd illustrated in an overview map (Fig. 3).

Individual species accounts of species catego-

rized as Endangered (EN)

We found a total of nine EN species within the inves-

tigated areas representing 4% of all amphibian species

known to occur in Panama. Furthermore, 39% of the

Panamanian species in the EN category, and 53% of the

EN species that are known to occur within the transect.

We made all but three findings within the boundaries of

PAs, except one at Santa Clara ( Ptychohyla legleri ), and

two in the Cerro Colorado region ( Agalychnis annae and

Pristimantis museosus). The former two species could

not be reported from any of Panama’s PAs (Appendix II).

Agalychnis annae (Duellman 1963): This species,

formerly considered as a Costa Rican endemic, has been

only recently recorded from Panama (Hertz et al. 2011).

Between 1980 and 1990, Agalychnis annae disappeared

from all PAs in Costa Rica and was subsequently listed as

EN. In Costa Rica, it is only found near heavily polluted

streams in the metropolitan region of San Jose. Pounds

et al. (2008) hypothesized that the frog and its tadpoles

may be less susceptible to water pollution than the chy-

trid fungus, so it survives only at disturbed and polluted

sites. We found a single female during daytime surveys

inactive on a leaf by the side of a dirt road. The area is in-

habited and fit for agricultural use, though streams in the

area did not appear to be heavily polluted. Admittedly,

we did not conduct chemical analysis. We furthermore

cannot tell whether a reproductive population exists.

Thus, further monitoring is strongly needed.

Ecnomiohyla fimbrimembra (Taylor 1948): This spe-

cies is associated with primary humid montane forest. It

is an obligatory canopy dweller that lives and reproduces

principally in tree crowns. Ecnomiohyla fimbrimembra

is very rarely observed and collected, and there are no

dependable data on its population status (Savage 2002).

However, it is presumed to have a decreasing population

trend, because it is strongly associated with mature pri-

mary forests, which are endangered by human activities.

The first and formerly only specimen from Panama was

an adult male collected in 1982 at Cerro Horqueta, PILA,

Chiriqui (Ibanez et al. 1991).

We collected an adult male during a rainy night on

the north-eastern slopes of Volcan Baru. This expands the

known distribution of E. fimbrimembra in Panama to a

second PA, the PNVB, and represents the second male

specimen in a scientific collection (Savage 2002; Men-

delson et al. 2008).

Ptychohyla legleri (Taylor 1958): This species is

considered moderately common in appropriate habitats

(Solis et al. 2008). We found only a single froglet near a

small creek at Santa Clara in extreme western Panama,

where the first Panamanian specimens were collected in

1966 (Duellman 2001). Despite intensive search efforts

we carried out at different tunes of the year at this site,

it remained the only encountered specimen. Even though

it was found on an organic farm, the surroundings are

dominated by intensive coffee plantations nowadays. As

a stream breeder it faces a potential risk of chytrid infec-

tion, but there are no reports on population declines of

this species due to chytridiomycosis yet. Santos-Barrera

et al. (2008) recorded P. legleri from the San Vito region

in Costa Rica, near Santa Clara, but found no evidence

for Bd in that area. However, former studies have proved

the presence of Bd at this site (Lips et al. 2003a; Picco

and Collins 2007). In addition, we collected a male glass

frog ( Cochranella granulosa ) at the same creek in Santa

Clara, which tested positive for Bd by PCR.

Pristimantis museosus (Ibanez, Jaramillo, and Arose-

mena 1994): This species can be characterised as uncom-

mon. We found it on the Caribbean slopes along the cen-

tral mountain range wherever pristine forest was present.

Ibanez et al. (1994) collected the type material at pristine

premontane wet forest and lower montane rainforest life

zones (Holdridge 1967). Likewise, we never found it in

degraded habitats and therefore suspect it of being very

sensitive to deforestation.

Bolitoglossa magnifica Hanken, Wake, and Savage

2005: The type material of this species was collected on

the lower slopes of Volcan Baru, Chiriqui, Panama in

1975. This species was first assigned to B. nigrescens un-

til the revision of the B. nigrescens complex by Hanken

et al. (2005). It has not been collected or observed since.

It is listed as EN because of its small known distribution

range and a general loss of habitat. In fact, inadequate

data allow only a restrained assessment of this species.

We collected four individuals during the day only a few

kilometres away from the species’ type locality at PNVB

while ascending from the town of Boquete to the peak by

car. In a relatively short period of time (approximately 1 5

min), we found all four individuals under a pile of wood

by the side of the road. Further research is needed, but it

seems to be common at certain sites.

Bolitoglossa compacta Wake, Brame, and Duellman

1973: This is a rather uncommon species (Savage 2002)

with a small distribution between the Costa Rican-Pan-

amanian border and Volcan Barn. The type material was

collected on the northern slope of Cerro Pando between

1920 and 1970 m a.s.l. in undisturbed cloud forest (Wake

et al. 1973). It was first recorded from Costa Rica by Lips

(1993), who did not give much information on its habitat,

but described the vegetation at this site as lower montane

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Threatened amphibian species in western Panama

rainforest in a later work (Lips 1998). Although little is

known about the species’ environmental demands, it is

assumed to inhabit relatively undisturbed lower montane

rainforest, and therefore is threatened by habitat loss due

to logging.

We found a single specimen on the south-eastern

slope of Volcan Barn, within the boundaries of PNVB,

under a rotten trunk by the side of the road.

Bolitoglossa marmorea (Tanner and Brame 1961):

This species has almost the same distribution as Bolito-

glossa compacta, but inhabits slightly higher elevations.

Specimens collected during this study were, just as the

type material, found in montane rainforest at the edge of

the timberline and pluvial paramo above timberline. The

ability to live in open habitats is probably the reason why

it persists also in degraded habitats. There is a need for

further studies as these are the first records of the species

in more than ten years (IUCN 2010).

Still it seems to be a common species at the peak of

Volcan Barn. In only one morning, we collected five

specimens by turning a couple of rocks near the summit

of the volcano.

Bolitoglossa minutula Wake, Brame, and Duellman

1973: This seems to be still a quite common species

where unspoiled forest exists. Nevertheless, its known

distribution area is small and it is assumed to be threat-

ened by deforestation. We collected at least nine speci-

mens of B. minutula at PILA and PNVB. Especially near

the continental divide on both southern and northern

slopes of Cerro Pando (PILA), it appears to be the most

common salamander.

Oedipina grandis Brame and Duellman 1970: This

elongate, fossorial salamander was easily found in the

early 1990s, but then decreased in abundance for un-

known reasons (Lips 1998). We detected a single, adult

female in January 2006 at night in Jurutungo on the edge

of PILA. The specimen was crawling between recently

cut Heliconia leaves, on a small trail leading to a water

intake point of a small stream. It remained the only indi-

vidual taken during this study.

Individual species accounts of species catego-

rized as Critically Endangered (CR)

We found a total of nine CR species within the investigat-

ed area. That is 4% of all Panamanian amphibian species,

41% of all Panamanian amphibian species in the CR cat-

egory, and 56% of all Panamanian CR amphibians that

are known to occur within the transect. We made most

of the records within the boundaries of PAs, except three

species ( Isthmohyla debilis, I. graceae, and I. tica ) from

°0'N

°30'N

82°30'W

82°0'W

81 °30'W

81 “O'W

Figure 3. Map of localities referred to in Table 1. (hatched areas = PAs; cross hatched area = Cerro Colorado region, with Cerro

Sagui massive in the western and Cerro Santiago in the eastern portion; black dots indicate positive Bd results).

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Hertz et al.

the CeiTo Colorado region. We could not find the former

two in any of Panamas PAs, while the latter one was also

present in PILA (Appendix II).

Atelopus varius (Lichtenstein and von Martens 1 856):

This eye-catching harlequin toad once was a common

species in Costa Rica and Panama, but has suffered dra-

matic population declines throughout its range (Crump et

al. 1992; Pounds and Crump 1994; Lips 1998, 1999; Lips

et al. 2003b; La Marca et al. 2005). Although there have

been sporadic sightings of this species, it is believed to be

still in serious decline. We observed four individuals, all

at Cerro Negro (PNSF), Veraguas. All adults were found

sleeping on low riparian vegetation and a single tadpole

(Gosner stage: 36) was found in a mountain stream.

None of the collected individuals appeared to be sick.

We conducted histological examination of skin scrap-

ings from two adults, which yielded no evidence for Bd.

These specimens are probably part of a small population

that still persists at Cerro Negro.

Agalychnis lemur (Boulenger 1882): This used to be

a quite common species in Costa Rica and Panama, but

has become rare in recent years, probably due to chy-

tridiomycosis. It is suspected that A. lemur is more resis-

tant to Bd than is other species (Woodhams et al. 2006).

There is no doubt that deforestation is a major threat to

this species as well. We collected a single specimen at

Cerro Negro (PNSF), Veraguas. The frog was found in a

small creek where it was sitting on a rock. Although we

visited Cerro Negro between 2008 and 2009 seven times

at different seasons of the year, this remained the only

detected specimen.

Duellmanohyla uranochroa (Cope 1875): This spe-

cies was once common in the RFLF, but has become rare

after severe declines (Lips 1999; Pounds et al. 2008). We

collected the first four tadpoles (Gosner stages: 26-29)

from a small creek on the south-western slope of Cerro

Pata de Macho (RFLF) in 2008, where several more tad-

poles were present in slow-moving water puddles along

the creek. In the following years, tadpoles have been

observed in this creek during several times of the year.

In 2009, we found two adults: one from vegetation near

the collection site of the tadpoles, and a second at BPPS,

Comarca Ngobe-Bugle, only a few km from the former

adult. This individual was also arranged in riparian veg-

etation, about three m above the ground. The latter one

appeared meagre and feeble and we found it to be para-

sitized by a large nematode that moved under its skin.

Both adults tested negative for the presence of Bd. All

of the collected tadpoles showed mouthpart deformations

ranging from slight folding of the oral disc to complete

loss of keratine in denticles and beak. A skin scraping

we took from a tadpole’s oral disc tested positive for Bd

by histological examination. D. uranochroa is currently

known from Monteverde and Tuis de Turrialba, Costa

Rica (IUCN 2010). Our records represent the only recent

findings of this species in Panama.

Hyloscirtus colymbci (Dunn 1931): This species has

undergone drastic population declines in western and

central Panama (Lips 1999; Lips et al. 2006; Crawford

et al. 2010a). We made the first record in 2008, collect-

ing four tadpoles from a fast-moving stream near Alto de

Piedra, Veraguas. A few weeks later, we found a single

adult male, and in 2009 we encountered an adult female.

Then, in 2010 we collected four adult specimens, two

males and two females, in both forest and streams, and

some more tadpoles. One male was calling from riparian

vegetation, and we heard several additional males calling

along the stream. Although field work has been earned

out in Alto de Piedra between 1998 and 2004, e.g., by

Brem and Lips (2008), this population was only recent-

ly discovered in the course of this project (Hertz et al.

2011). One of the individuals we collected in 2010 at first

sight appeared to be sick tested positive for Bd by PCR.

This confirms that Bd is still present within the habitat.

All other collected specimens were also tested, but ap-

peared to be healthy and we did not find any evidence for

a Bd infection.

Isthmohyla angustilineata (Taylor 1952): This has al-

ways been an uncommon species (Savage 2002). There

are only sparse data available on geographic distribution

and population status. The most recent record comes

from Costa Rica at Braulio Carillo National Park near

Volcan Barva (Nishida 2006). At Monteverde it has de-

clined drastically but is still found sporadically, whereas

there are no recent records from Cerro Chompipe and

Tapanti (IUCN 2010). In Panama there is little informa-

tion on its distribution and population status. The spe-

cies was first reported from Panama by Arosemena and

Ibanez (1991), who collected three specimens in 1990

at Cerro Horqueta, PILA, the only published record for

Panama until now. In 2006, we collected an adult female

at almost the same locality; the frog was sitting in a shrub

in an inundated pasture. The current population status at

this site is unknown.

Isthmohyla debilis (Taylor 1952): This small frog is

an uncommon species collected at a few locations (Sav-

age 2002). In 1996 and 1997, the populations of this spe-

cies collapsed at RFLF (Lips 1999). In Panama, I. cle-

bilis was last detected in 1998 from neighboring BPPS

(Hofer and Bersier 2001; IUCN 2010). In Costa Rica it

had equally declined, and there are no recent findings in

this country. We collected two calling males at La Nevera

on the western slopes of Cerro Santiago, Comarca Ngo-

be-Bugle, in 2008. The frogs were only traceable by fol-

lowing their cricket-like calls, as they sat in very dense

vegetation overhanging a stream. In 2009, we collected

another male near Llano Tugri on the eastern slopes of

Cerro Santiago, Comarca Ngobe-Bugle. This one was

not hidden in vegetation nor was it calling, but sat ex-

posed on a rock in a mountain stream. In the same year,

we collected two more male specimens, one of which

was found calling in bushes at the margin of a mountain

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Threatened amphibian species in western Panama

stream at La Nevera; the other one sat in the same bush,

moving towards its calling conspecific. Only two days

later we found an additional calling male, but for con-

servation reasons refrained from collecting it. The frog

cowered well-concealed between the leaves of a fallen

tree overhanging a mountain stream. Our findings rep-

resent the only recent records of this species within its

native range. Accordingly, there are no known lingering

populations within the boundaries of any PA. These re-

cords also extend the known geographic distribution of

the species about 30 to 40 km to the east from its nearest

collecting site at Rio Chiriqui, RFLF, Chiriqui (Myers

andDuellman 1982).

Isthmohyla graceae (Myers and Duellman 1982):

Since there were drastic declines of the species reported

from RFLF, Chiriqui (Lips 1999) this Panamanian en-

demic has disappeared from all well-known sites. De-

spite many search efforts, it is uncertain if any of these

populations now survive (IUCN 2010). Although the

Cerro Colorado area is the type locality of this species,

previous search efforts concentrated mainly on PAs. In

2010, at the south-eastern slopes of Cerro Sagui, Comar-

ca Ngobe-Bugle, close to the species’ type locality, we

detected various calling males and tadpoles at a marshy

headwater of Rio Cricamola between pasture and forest.

We collected four adult males and one tadpole as repre-

sentative samples. All four collected adults were tested

for Bd using swab samples for PCR; three with negative

and one with a uncertain result(s). Like in the previous

species, this represents the only known population that so

far persists, and there are no recent records from any PA.

Isthmohyla rivularis (Taylor 1952): This species once

was veiy common (Savage 2002), but declined through-

out its range in the 1990s. In Panama, the last records date

back to 1996 (IUCN 2010). In 2007, it was rediscovered

at Monte verde, Costa Rica (Andrew Gray, pers. comm.

2011), where it was last seen in 1989. We collected a to-

tal of six adult males and one adult female around Cerro

Pando, PILA, Chiriqui and Bocas del Toro. Six speci-

mens were obtained from the Pacific slopes and one from

the Caribbean slopes. The first individual was detected

in 2008 by coincidence at night near a small mountain

stream. In one of the ensuing nights, after heavy rain

falls, we located three more males by the side of an un-

paved road by following their calls. Calling site was very

dense vegetation, intermingled with leaf litter that was

overhanging a small creek. The calling males were sitting

near ground level, well-hidden between plant material. In

the same night, we heard more males calling from differ-

ent creeks in the surrounding area. In 2009, we collected

another calling male from the bank of a mountain creek,

where it was perched on a leaf near a small cascade. In

the same night, and only about 100 m away from the lat-

ter specimen, we detected a female on a broad-leaved

plant in a waterless anabranch. In November 2009, we

found another individual, when crossing over the con-

tinental divide to the Caribbean slopes of Cerro Pando.

It was sitting in a bush, about 1.5 m above ground level,

near a fast-moving mountain creek. The abundance of

this species in the surroundings of Cerro Pando indicates

that there is a surviving population. None of the collected

specimens appeared to be sick. Histological examination

of skin scrapings did not provide any evidence of a chy-

trid infection.

Isthmohyla tica (Starrett 1966): This stream-breeder

has also been a common species in Costa Rica and Pan-

ama (Savage 2002), until it dramatically declined at all

known sites. In Panama, it had been collected at mul-

tiple sites between PILA and RFLF in the 1980s and 90s

(Tejera and Dupuy 2003). These populations collapsed

in 1 997 and there were no recent sightings in Costa Rica

or Panama. In July 2010, we collected a male specimen

at Rio Changena, northern slope of Cerro Pando, PILA,

Bocas del Toro. The cricket-like call drew our attention

to the frog that was sitting well-hidden about three m

above the water line in a bush. We heard another male

from the opposite side of the river, but could not find it.

Later in the same month, we found a specimen at the up-

per reaches of Rio Hacha, Comarca Ngobe Bugle. This

individual was not calling, but sitting about 3.5 m above

the water in a small tree.

Discussion

The Panamanian Central Cordillera is an area where Bd

driven amphibian declines have been especially severe

(Young et al. 2001) and where declines were exception-

ally well documented (Lips 1998, 1 999; Lips et al. 2006).

At all of these sites certain species, mainly hylids, bufo-

nids, and stream-associated craugastorids, have not been

found since these documented decline events. While in

neighboring Costa Rica recent surveys have led to sev-

eral rediscoveries of lost species (Garcia-Rodruiguez et

al. 2012), upland sites in western Panama were not fre-

quently visited by herpetologists. The majority of present

amphibian research in Panama is earned out east of El

Cope following the Bd wave and little attention has been

paid to post decline sites. Accordingly, to date the pres-

ent paper is the only information on relict populations

of rare amphibians, and shall serve as a basis for future

studies. There is a paucity of data for many species in

general, as indicated by the high number of species listed

as Data Deficient by the IUCN. In Panama, there are 34

species (more than 16% of all Panamanian amphibians;

Fig. 2) for which more information is required to assess

their population status and conservation trend.

The absence of chytrid at a certain site could explain

why a population persists. We took chytrid samples from

several specimens and various localities. Though, the

sample size presented here is not large enough to prove

the absence of Bd at an investigated site, and we can-

not identify refuge areas free of Bd: this will require fur-

ther investigation. However, our presence data together

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Hertz et al.

Table 1 . Visited areas, protection status, and percentage of all EN/CR species found.

Name of area

Land cover (ha)

Protection status

Number of EN

species found

Number of

CR species

found

Percentage of EN/CR

species in transect

PILA

207,000 (Panama

only)

Transboundary Protected Area;

UNESCO World Heritage Site

3

18%

BPPS

167,410

Conservation Forest

1

7%

PNSF

72,636

National Park

1

3

12%

RFLF

19,500

Forest Reserve

0

1

3%

PNVB

14,322

National Park

5

0

15%

Cerro Colo-

rado Area

at least 14,000

unprotected

i

3

15%

Santa Clara

N.A.

unprotected

1

0

3%

with other studies (e.g., Kilburn et al. 2011) show that

at a large-scale this pathogen is still present at sites in

Panama where chytridiomycosis once emerged (Fig 3).

Further research on chytridiomycosis in wild amphibian

populations should focus on populations at post-decline

sites.

Altitudinal distribution of a species may also be a rea-

son for a species to persist. There is evidence that popula-

tions of species that inhabit a vast altitudinal range may

at least persist at lower altitudes where mean temperature

is higher (Berger et al. 2004), or could even actively keep

Bd infections low by exploration to warm microclimate

(Daskin et al. 2011). The same is imaginable with species

having wide horizontal distributions, with populations

persisting in climatic refuges, e.g., drier and warmer re-

gions (Puschendorf et al. 2005). Unfortunately, lowland

forests are facing a higher deforestation risk due to a bet-

ter accessibility and higher agricultural value. For exam-

ple, nowadays there are almost no remainders of pristine

pacific lowland forest in western Panama.

Notwithstanding, habitat loss by means of modifica-

tion, fragmentation, and destruction is still the biggest

threat to amphibians and wildlife in general (Gardner et

al. 2007; Young et al. 1999, 2004). About 44% of Pan-

ama’s land mass is still covered by forests. Compared

to other Central American countries, Panama showed a

relatively low deforestation rate of -1.2% in the period

between 1990 and 2000 (total Central America -1.6%),

and an even lower -0.4% between 2000 and 2010 (total

Central America -1.2%; data taken from FAO 2011). But

deforestation rates in Panama are not equally distributed,

and some forests are under higher anthropogenic pres-

sure than others. By far the highest deforestation rate

among Panamanian provinces is found in the Comarca

Ngobe-Bugle (-21.8%, 1992-2000) followed by the cen-

tral-eastern provinces of Darien (-13.9%), and Panama

(-12.2%) (ANAM 2009). A great portion of the Cordil-

lera Central, almost the whole part known as Serrania

de Tabasara, is located within the limits of the Comarca

Ngobe-Bugle. In addition, the Cordillera Central is home

to 73% of the EN and CR amphibian species in Panama.

Consequently, there is a general need for more well-pro-

tected areas in this mountain range. During this study, we

identified the Cerro Colorado region as one of the most

important unprotected areas for amphibian conservation

in Panama. The minimum convex polygon drawn around

our collection points would comprise around 14,000 ha

and could include at least 15% of Panamas EN and CR

amphibian species (Table 1). Two Critically Endangered

species, Isthmohyla debilis on the slopes of Cerro San-

tiago and /. graceae on the slopes of Cerro Sagui, both of

which had not been detected since the late 1 990s, do oc-

cur here. These are the only known populations of those

two species that now persist. Additionally, it is the only

place in Panama where the Endangered Agalychnis an-

nae is known, and beside La Amistad, the only additional

place across its whole distribution area where the Criti-

cally Endangered I. tic a can still be found. As presumed

by the restricted time we spent in field, these findings are

better understood as only a limited sample of an estimat-

ed apparent higher species diversity, including certainly

many undescribed species, signifying important diver-

sity of other non-herpetological organisms possibly as

well. Unfortunately, Cerro Colorado is under increased

anthropogenic pressure, especially through international

mining companies that wish to establish a copper mine

at this site. At present time, the current Panamanian gov-

ernment is attempting to ease the solicitation process for

foreign countries to get concessions (Nakoneczny and

Whysner 2010). From all that we know, mining at Cerro

Colorado will cause severe environmental damage and

reduce Panamanian amphibian fauna once more. Thus,

we strongly recommend to Panamanian authorities, both

the government of Panama and traditional authorities of

Ngobe-Bugle, to assign the Cerro Colorado area, includ-

ing Cerro Santiago, Cerro Sagui, and the whole moun-

tain ridge in between, an area of approximately 65,400

ha (Fig. 3), as PA in order to preserve this highly diverse

area for future generations.

Unfortunately, even PAs are not always successful in

their ability to control deforestation. This is especially

severe in PILA and BPPS, where deforestation of mature

forest was high, despite the protection status (Oestreich-

er et al. 2009). Currently, the discussion on new roads

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Threatened amphibian species in western Panama

through remote areas of different PAs, including PILA,

PNVB, and BPPS, has come up again. The Panamanian

government expects an increase of tourism and trade to

be triggered by these projects. However, costs to build

and maintain roads in tropical mountainous forests are

usually high, making it doubtful that economic aims will

be achieved (Reid and Hanily 2003). Beside other effects

these roads will exacerbate deforestation by facilitating

the access to formerly well-protected sites (Young 1994;

Chomitz and Gray 1996; Nelson and Hellerstein 1997).

It is further questionable if new roads in PAs rather an-

noy tourists, who are predominantly looking for pure na-

ture, than stimulating them to make a visit, in particular

if there is no forest left to see when driving through a

park. There is a general need for comprehensive manage-

ment plans, better demarcation of PAs, and year-round

personnel to stop ongoing deforestation in areas that are

supposed to be protected.

Acknowledgments. — Collecting permits SE/A-30-

08, SC/A-8-09, SC/A-28-09, and SC/A-21-10, as well as

the corresponding exportation permits, were provided by

Direccion de Areas Protegidas y Vida Silvestre of the Au-

toridad Nacional del Ambiente (ANAM), Panama City,

Panama. Querube D. Fuenmayor and Victor Martinez,

Panama City, Panama, provided valuable assistance with

acquisition of these permits. Additional collecting per-

missions for the Comarca Ngobe-Bugle were provided

by Cacique General Rogelio Moreno, San Felix, Pana-

ma. For assistance in the field, we thank Abel Batista,

Andreas Uselis, Caroline Judith, Falk Ortlieb, Frank

Hauenschild, Joe-Felix Bienentreu, Feonard Stadler, and

Nadim Hamad. For transportation to Santa Fe National

Park we thank Rafael Gonzalez, and to Smelin Abrego

we are grateful for field assistance at that site. For lo-

gistical support, we are grateful to the park rangers of

PIFA and PNVB, as well as to Andrew Bennett, Gabriel

Palacios, Meike Piepenbring, Patrick McGreer, Porfirio

Yangiiez, Marciano Montezuma, and the families Cace-

res and Pena Solis. We thank Tobias Eisenberg for ex-

amination of skin swabbings for Bd infection. This paper

is based upon work funded to AH by the FAZIT-Stiftung,

and to SF by the Studienstiftung des deutschen Vollces,

and the Freunde und Forderer der Universitat Frankfurt.

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Accepted: 27 March 2012

Published: 21 April 2012

Appendix I

Voucher specimens

Anura: Agalychnis annae: Comarca Ngobe-Bugle:

Cerro Colorado, N8.53, W81.81, 1600 m a.s.l.: SMF

89791; Agalychnis lemur. Veraguas: PNSF, Cerro Ne-

gro, N8.57, W81.10, 690 m a.s.l.: SMF 89959; Atelopus

varius : Veraguas: PNSF, Cerro Negro, N8.57, W81.10,

730-1090 m a.s.l.: SMF 89822-3, 89917, AH 218; Du -

ellmanohyla uranochroa : Chiriqui: RFLF, western

slopes of Cerro Pata de Macho, N8.67, W82.20. 1420

m a.s.l.: SMF 89824, 89826, AH 195; Comarca Ngobe-

Bugle: BPPS, continental divide, street to Petrotenni-

nal, N8.79, W82.21, 1060-1080 m a.s.l.: SMF 89825,

89827; Ecnomiohylafimbrimembra : Chiriqui: Boquete,

Bajo Mono, north-eastern slopes of Volcan Bam, N8.83,

W82.50, 1820 m a.s.l.: SMF 89857; Hyloscirtus colym-

ba: Veraguas: Alto de Piedra, N8.51, W81.12, 880-940

m a.s.l.: SMF 89794, 89828-32, AH 059, AH 547; Isth-

mohyla angustilineata : Chiriqi: PILA, Cerro Horqueta,

N8.85, W82.42, 1800 m a.s.l.: MHCH 483; Isthmohyla

debilis: Comarca Ngobe-Bugle: La Nevera, western

slopes of Cerro Santiago, N8.50, W81.77, 1540-1650 m

a.s.l.: SMF 89833, 89835, AH 166, AH 347; Llano Tugri,

eastern slopes of Cerro Santiago, N8.50, W81.72, 1570

m a.s.l.: SMF 89834; Isthmohyla graceae: Comarca

Ngobe-Bugle: Cerro Sagui, Finca Alto Cedro, N8.56,

W81.82, 1710 m a.s.l.: SMF 8936-8, AH All, AH 478;

Isthmohyla rivularis : Chiriqui: PILA, Jumtungo, south-

ern slopes of Cerro Pando, N8.91, W82.72, 1870-2070 m

a.s.l.: SMF 89839-43, AH 138, AH 139; northern slopes

of Cerro Pando near continental divide, N8.93; W82.71,

2290 m a.s.l.: SMF 89843; Isthmohyla tica: Bocas del

Toro: PILA, Rio Changena, northern slopes of Cerro

Pando, N8.98, W82.69, 1620 m a.s.l.: SMF 89845; Co-

marca Ngobe-Bugle: Caribbean slopes of Cordillera de

Tabasara, valley of Rio Hacha, N8.52, W81.79, 1220 m

a.s.l.: SMF 89846; Pristimantis museosus : Bocas del

Toro: PILA, Rio Changena, northern slopes of Cerro

Pando, N8.98, W82.69, 1650 m a.s.l.: SMF 89859; Pri-

vate Reserve Willi Mazu, N8.79, W82.20, 690 m a.s.l.:

SMF 89860; Comarca Ngobe-Bugle: La Nevera, west-

ern slopes of Cerro Santiago, N8.50, W81.77, 1590 m

a.s.l.: SMF 89858; Veraguas: Alto de Piedra, N8.51,

W81.12, 940-1000 m a.s.l.: SMF 89861-2, AH 555;

PNSF, Cerro Negro, N8.57, W81.10, 770 m a.s.l.: SMF

89864 , Ptychohyla legleri: Chiriqui: Santa Clara, N8. 83,

W82.78, *1200 m a.s.l.: SMF 89863.

Caudata: Bolitoglossa compacta: Chiriqui: PNVB, Vol-

can Barn, road from Boquete to summit, N8.80, W82.52,

3000 m a.s.l.: SMF 89849; Bolitoglossa magnifica :

Chiriqui: PNVB, Volcan Barn, road from Boquete to

summit, N8.80, W82.51, 2350 m a.s.l.: SMF 89847-8,

AH 323, AH 325; Bolitoglossa marmorea : Chiriqui:

PNVB, Volcan Barn, summit region of volcano, N8.81,

W82.54, 3340-3400 m a.s.l.: SMF 89850-2, AH 328, AH

329; Bolitoglossa minutula: Chiriqui: PILA, Jumtungo,

southern slopes of Cerro Pando, N8.91, W81.72, 1960-

2030 m a.s.l.: SMF 89854, AH 141; northern slopes of

Cerro Pando near continental divide, N8.93, W82.71,

2320 m a.s.l.: SMF 89855, AH 277; PNVB, Sendero Los

Quezales, northern slope of volcano, N8.85, W82.51,

2130 m a.s.l.; SMF89856; PNVB, Volcan Barn, road

from Boquete to summit, Camp Mamecillos, N8.80,

W82.51, 2600 m a.s.l.: SMF 89853; Oedipina grandis:

Chiriqui: PILA, Jumtungo, southern slopes of Cerro Pan-

do, N8.54, W82.43, 2060 m a.s.l.: SMF 85076.

amphibian-reptile-conservation.org

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Threatened amphibian species in western Panama

APPENDIX II

List of amphibians known to occur in Panama

Amphibian species reported

for Panama

IUCN

Category

EN/CR

known from

transect

EN/CR detected

during this study

Distance of detected

population to nearest PA

(km)

Name of nearest

PA

Order Anura

Family Aromobatidae

Allobates talamancae

LC

Family Bufonidae

Atelopus certus

EN

A. chiriquiensis

CR

X

A. glyphus

CR

A. limosus

EN

A. varius

CR

X

0

PNSL

A. zeteki

CR

Crepidophryne epiotica

LC

Incilius aucoinae

LC

1. coniferus

LC

1. fastidiosus

LC

1. karenlipsae

NE

1. melanochlorus

LC

1. peripatetes

CR

X

1. signifer

LC

Rhaebo haematiticus

LC

Rhinella acrolopha

DD

R. alata

DD

R. centralis

NE

R. marina

LC

Family Centrolenidae

Cochranella euknemos

LC

C. granulosa

LC

Espadarana prosoblepon

LC

Hyalinobatrachium

NT

aureoguttatum

H. chirripoi

LC

H. colymbiphyllum

LC

H. fleischmanni

LC

H. talamancae

LC

H. valerioi

LC

H. vireovittatum

DD

Sachatamia albomaculata

LC

S. ilex

LC

Teratohyla pulverata

LC

T. spinosa

LC

Family Craugastoridae

Craugastor azueroensis

EN

C. bransfordii

LC

C. catalinae

CR

X

C. crassidigitus

LC

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Hertz et al.

Amphibian species reported

for Panama

IUCN

Category

EN/CR

known from

transect

C. emcelae

CR

X

C. evanesco

NE

C. fitzingeri

LC

C. gollmeri

LC

C. gulosus

EN

X

C. jota

DD

C. longirostris

LC

C. megacephalus

LC

C. melanostictus

LC

C. monnichorum

DD

C. noblei

LC

C. obesus

EN

X

C. opimus

LC

C. podiciferus

NT

C. polyptychus

LC

C. punctariolus

EN

X

C. raniformis

LC

C. ranoides

CR

X

C. rhyacobatrachus

EN

X

C. rugosus

LC

C. stejnegerianus

LC

C. tabasarae

CR

C. talamancae

LC

C. taurus

CR

Family Dentrobatidae

Ameerega maculata

DD

Colostethus latinasus

DD

C. panamansis

LC

C. pratti

LC

Dendrobates auratus

LC

Hyloxalus chocoensis

DD

Oophaga arborea

EN

X

O. granulifera

VU

O. pumilio

LC

O. speciosa

EN

X

O. vicentei

DD

Phyllobates lugubris

LC

Ranitomeya claudiae

DD

R. fulgurita

LC

R. minuta

LC

Silverstoneia flotator

LC

S. nubicola

NT

Family Eleutherodactylidae

Diasporus diastema

LC

D. hylaeformis

LC

D. quidditus

LC

D. vocator

LC

EN/CR detected

during this study

Distance of detected

population to nearest PA

(km)

Name of nearest

PA

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Threatened amphibian species in western Panama

Amphibian species reported

for Panama

IUCN

Category

EN/CR

known from

transect

EN/CR detected

during this study

Distance of detected

population to nearest PA

(km)

Name of nearest

PA

Family Hemiphractidae

Gastrotheca cornuta

EN

X

G. nicefori

LC

Hemiphractus fasciatus

NT

Family Hylidae

Agalychnis annae

EN

X

30

BPPS

A. callidryas

LC

A. lemur

CR

X

0

PNSF

A. spurelli

LC

Anotheca spinosa

LC

Cruziohyla calcarifer

LC

Dendropsophus ebraccatus

LC

D. microcephalus

LC

D. phlebodes

LC

D. subocularis

LC

Duellmanohyla lythrodes

EN

X

D. uranochroa

CR

X

0

BPPS; RFLF

Ecnomiohyla fimbrimembra

EN

X

0

PNVB

E. miliaria

VU

E. rabborum

CR

E. thysanota

DD

Hyloscirtus colymba

CR

X

0

PNSF

H. palmeri

LC

Hypsiboas boans

LC

H. crepitans

LC

H. pugnax

LC

H. rosenbergi

LC

H. rufitelus

LC

Isthmohyla angustilineata

CR

X

0

PILA

1. calypsa

CR

X

1. debilis

CR

X

36

BPPS

1. graceae

CR

X

27

BPPS

1. infucata

DD

1. lancasteri

LC

1. picadoi

NT

1. pseudopuma

LC

1. rivularis

CR

X

0

PILA

1. tica

CR

X

0

PILA

1. zeteki

NT

Phyllomedusa venusta

LC

Ptychohyla legleri

EN

X

7

PILA

Scinax altae

LC

S. boulengeri

LC

S. elaeochrous

LC

S. rostratus

LC

S. ruber

LC

Smilisca phaeota

LC

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Hertz et al.

Amphibian species reported

for Panama

IUCN

Category

EN/CR

known from

transect

EN/CR detected

during this study

Distance of detected

population to nearest PA

(km)

Name of nearest

PA

S. sila

LC

S. sordida

LC

Trachycephalus venulosus

Family Leiuperidae

LC

Engystomops pustulosus

LC

Pleurodema brachyops

Family Leptodactylidae

LC

Leptodactylus bolivianus

LC

L. fragilis

LC

L. fuscus

LC

L. melanonotus

LC

L. poecilochylus

LC

L. savagei

Family Microhylidae

LC

Chiasmocleis panamensis

LC

Elachistocleis ovalis

LC

Nelsonophryne aterrima

LC

Relictivomer pearsei

LC

Family Pipidae

Pipa myersi

Family Ranidae

EN

Litobathes taylori

LC

L. vaillanti

LC

L. vibicarius

CR

X

L. warszewitschii

LC

Family Strabomantidae

Pristimantis achatinus

DD

P adnus

NE

P altae

NT

P caryophyllaceus

NT

P cerasinus

LC

P cruentus

LC

P educatoris

NE

P gaigei

LC

P moro

LC

P museosus

EN

X

0

PILA; BPPS;

PNSF

P pardalis

NT

P pirrensis

DD

P ridens

LC

P taeniatus

LC

Strabomantis bufoniformis

LC

S. laticorpus

DD

Order Caudata

Family Plethodontidae

Bolitoglossa anthracina

DD

B. biseriata

LC

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Threatened amphibian species in western Panama

Amphibian species reported

for Panama

IUCN

Category

B. bramei

DD

B. colonnea

LC

B. compacta

EN

B. copia

DD

B. cuna

DD

B. gomezi

DD

B. lignicolor

VU

B. magnifica

EN

B. marmorea

EN

B. medemi

VU

B. minutula

EN

B. phalarosoma

DD

B. pygmaea

DD

B. robinsoni

DD

B. robusta

LC

B. schizodactyla

LC

B. sombra

VU

B. taylori

DD

Oedipina alfaroi

VU

O. alleni

LC

O. collaris

DD

O. complex

LC

O. cyclocauda

LC

O. fortunensis

NE

O. gracilis

EN

O. grandis

EN

O. maritima

CR

O. pacificensis

LC

O. parvipes

LC

Order Gymnophiona

Family Caeciliidae

Caecilia isthmica

DD

C. leucocephala

LC

C. nigricans

LC

C. volcani

DD

Dermophis glandulosus

DD

D. gracilior

DD

D. parviceps

LC

Gymnophis multiplicata

NE

Oscaecilia elongata

DD

O. ochrocephala

LC

EN/CR

known from

transect

X

EN/CR detected

during this study

Distance of detected

population to nearest PA

(km)

Name of nearest

PA

X

0

PNVB

X

0

PNVB

X

0

PNVB

X

0

PILA; PNVB

X

0

PILA

Total 206

33

18

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Hertz et al.

APPENDIX III

Representative species

Agalychnis annae (SMF 89791), Cerro Colorado, Comarca

Ngobe-Bugle. Photo by SL.

Atelopus varius (AH 218), Cerro Negro, PNSF, Veraguas.

Photo by AH.

Bolitoglossa magnified (AH323), Volcan Barn, PNVB,

Chiriqul. Photo by AH.

Bolitoglossa minutula (SMF 89855), valley of Jurutungo,

southern slope of Cerro Pando, PILA, Chiriqul. Photo by AH.

Agalychnis lemur (SMF 89959), Cerro Negro, PNSF, Vera-

guas. Photo by AC.

Bolitoglossa compacta (SMF 89849), Volcan Barn, PNVB,

Chiriqul. Photo by AH.

Bolitoglossa marmorea (SMF 89850), summit of Volcan Barn,

PNVB, Chiriqul. Photo by AH.

Duellmanohyla uranochroa (SMF 89824), western slope of

Cerro Pata de Macho, RFLF, Chiriqul. Photo by AH.

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Threatened amphibian species in western Panama

Back view of Duellmanohyla uranochroa (SMF 89825) with

large nematode under the skin, BPPS, Comarca Ngobe-Bugle.

Photo by AH.

Ecnomiohyla fimbrimembra (SMF 89857), Bajo Mono, east-

ern slope of Volcan Barn, PNVB, Chiriqui. Photo by AH.

Hyloscirtus colymba (SMF 89831) infected with chydridiomy-

cosis, note reddish coloration through vascular dilatation, Alto

de Piedra, PNSF, Veraguas. Photo by AH.

Isthmohyla debilis (AH 347), La Nevera, Comarca Ngobe-

Bugle. Photo by AH.

Tadpoles of Duellmanohyla uranochroa (AH 195) showing

complete loss of keratinized mouthparts (A) and deformation

of oral disk (B), western slope of Cerro Pata de Macho, RFLF,

Chiriqui. Photo by AH through dissecting microscope.

Hyloscirtus colymba (AH 547), Alto de Piedra, PNSF, Vera-

guas. Photo by AH.

Isthmohyla angustilineata (MHCH 483), El pianista, PILA,

Bocas del Toro. Photo by MP.

Isthmohyla graceae (SMF 89837), Cerro Sagui, Comarca

Ngobe-Bugle. Photo by AH.

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Hertz et al.

Isthmohyla rivularis (SMF 89843), northern slope of Cerro

Pando, PILA, Bocas del Toro. Photo by AH.

Oedipina grandis (SMF 85076), valley of Jurutungo, southern

slope of Cerro Pando, PILA, Chiriqul. Photo by GK.

Ptychohyla legleri froglet (SMF 89863), Santa Clara, Chiriqul.

Photo by AH.

Isthmohyla tica (SMF 89846), Rio Hacha, Comarca Ngobe-

Bugle. Photo by AH.

Pristimantis museosus (SMF89859), Rio Changena, northern

slopes of Cerro Pando, PILA Bocas del Toro. Photo by AH.

View of the Cerro Colorado area looking westward along the

continental divide, from La Nevera. Note road from San Felix

and cone-shaped peak of Cerro Sagui in the background (cp.

Fig. 1 in Myers and Duellman 1982). Photo by SL.

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Threatened amphibian species in western Panama

Andreas Hertz

Sebastian Lotzkat

Gunther Kohler

Arcadio Carrizo

Bruno Streit

Marcos Ponce

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April 2012 | Volume 6 | Number 2 | e46

Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License, which permits unrestricted use

for non-commercial and education purposes only provided the original author and source are credited.

Amphibian & Reptile Conservation 6(2):31-34.

Habitat associations and conservation of Eremias

acutirostris (Boulenger, 1887) in the Sistan region, Zabol, Iran

r Seyyed Saeed Hosseinian Yousefkhani, 1 2 Hamzeh Oraei, 1>3 Azar Khosravani and 1 4 Eskandar

Rastegar-Pouyani

Arnnian Plateau Herpetology’ Research Group (IPHRG), Faculty of Science, Razi University, 67 14967346 Kermanshah, IRAN ^-Department of

Zoology >, Faculty of Biology, Tehran University, Tehran, IRAN 3 Department of Biology, Faculty of Science, Razi University, 6714967346 Kerman-

shah, IRAN ^Department of Biology, Faculty of Science, Hakim Sabzevari University, Sabzevar, IRAN

Abstract . — During a field survey in the Sistan region of Iran in October 2011, habitat of Eremias

acutirostris was surveyed and four specimens of the species were collected. We report a locality

situated along the road from Zabol to Doost Mohammad, near the town of Bonjar. The fragile habitat,

consist of immobile sand dunes, is situated in proximity to an industrial zone, placing this remnant

population under threat of pollution and other anthropogenic edge effects. We call the Zabol Envi-

ronmental Protection Agency to act and insure the species’ future in Iran.

Key words. Eremias acutirostris , Zabol, sand dune, Doost Mohammad, conservation

Citation: Hosseinian Yousefkhani SS, Hamzeh O, Khosravani A, Rastegar-Pouyani E. 2013. Habitat associations and conservation of Eremias acutiros-

tris (Boulenger, 1887) in the Sistan region, Zabol, Iran. Amphibian & Reptile Conservation 6(2):31-34(e60).

Introduction

Eremias is a widespread Lacertid genus that is distrib-

uted from China to eastern Europe and southward to the

Iranian plateau (Anderson 1999; Rastegar-Pouyani et al.

2007). The genus comprises approximately 15 species in

Iran. Eremias acutirostris (Fig. 1) occurs in Iran, Afghan-

istan, and Pakistan, and listed as “Least Concern” by the

IUCN (Anderson 1999, Rastegar-Pouyani et al. 2008).

As a specialist species, E. acutirostris requires a suitable

habitat, perhaps critical for its survival.

Within the distribution range of the species, its occur-

rence in Iran is limited to a small area (Zabol region)

(Fig. 2). This particular habitat, characterized by veg-

etated sand dunes, is consumedly degraded by the high

human population density in the area; main threats are

overgrazing and industrial activities. In this study, we ex-

amined the species’ habitat preferences and provide sug-

gestions about its conservation, in association to these

environmental problems.

Materials and methods

During a three day field survey in the Sistan region of

Iran in October 2011, we observed 12 specimens of E.

acutirostris in the field; four were collected and depos-

ited in the Hakim Sabzevari Zoological Museum (SUHC

1084, 1085, 1086, and 1087). The locality was in an arid

area of the Hamoon basin, approximately 20 km W of

Bonjar on the road between Zabol and Doost Mohammad

( N 31° 05’ 15.6”, E 061° 37’ 32.8”, elevation 440 m).

Correspondence. Email: mesaliria.watsonana@gmail.com

The habitat consisted of immobile sand dunes with large

shrubs ( Tamarix sp. and Haloxylon sp.) (Fig. 3). The

snake Echis carinatus and the gecko Bunopus tubercula-

tus were also observed and collected in the same habitat.

Results and discussion

Reptiles inhabit a diverse array of habitats, but are

known to be sensitive to habitat destruction and degrada-

tion (Goode et al. 1995). Lizards in the genus Eremias in-

habit xeric habitats in Iran, which are threatened mainly

by grazing and industrial development. Human activity

in the study area is evident and an industrial park has

recently been constructed along the road between the vil-

lages. The construction of the industrial township, with

all its accompanying structures, inevitably destroyed

some of the fragile habitat. Drought conditions result-

ing in loss of vegetation have deteriorated the habitat, as

shrubs are viable resources for food (via insect attraction)

and shelter (refuge from predators) for the lizards. We

presume that these recent modifications are negatively

affecting the species’ population within the area and may

possibly lead to extinction of this lizard in Iran, if not

restricted and protected.

Conservation of E. acutirostris and other rare species

that may occur in the studied habitat are significantly

depended on the decision making of the Department of

Environment of the region, and the establishment of pro-

tected area(s). We hope that publication of our findings

will improve the conservation of this rare species, with

its restricted distribution in Iran.

amphibian-reptile-conservation.org

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July 2013 | Volume 6 | Number 2 | e60

Hosseinian Yousefkhani et al.

Acknowledgments. — We thank Naser Sanchooli for

field assistance in the Zabol region and John D. Willson

for editing the manuscript for English. Our special thanks

go out to Roy Talbi, for kindly providing helpful com-

ments on the manuscript. We thank Craig Hassapakis for

helping to improve parts of the manuscript.

Literature cited

Anderson SC. 1999. The Lizards of Iran. Society for the

Study of Amphibians and Reptiles, Ithaca, New York,

USA. 137 text-figs., distribution maps [unnumbered],

25 col. pis., 442 p.

Goode MJ, Howland JM, Sredl MJ. 1995. Effects of

microhabitat destruction on reptile abundance in

Sonoran Desert rock outcrops. Nongame and En-

dangered Wildlife Program Heritage Report. Arizona

Game and Fish Department, Phoenix, Arizona, USA.

25 p.

Rastegar-Pouyani N, Johari M, Rastegar-Pouyani E.

2007. Field Guide to the Reptiles of Iran (Volume 1 :

Lizards). Razi University Press, Kennanshah, IRAN.

298 p.

Rastegar-Pouyani N, Kami HG, Rajabizadeh M, Shafiei

S, Anderson SC. 2008. Annotated checklist of am-

phibians and reptiles of Iran. Iranian Journal of Ani-

mal Biosystematics 4(l):43-66.

Received: 07 December 2012

Accepted: 21 February 2013

Published: 09 July 2013

Figure 1 . Adult male Eremias acutirostris from the Zabol region, Iran.

amphibian-reptile-conservation.org

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July 2013 | Volume 6 | Number 2 | e60

Habitat associations and conservation of Eremias acutirostris

45 * 50 * 55 * 60 ’ 65 "

RUSSI.

GEORGIA

TURKEY

TURKMENISTAN

Tabfiii..* tI

5 ** \

.ake Urmia T

i * <i \

) avand

TEHRAN

Kermanshah

Eatahar

Dezful."i^'

Advaz

Abadan

Bus he hr

OMAN

35 " -

40 ‘-

- 40 "

UZBEK STAN

B riandl AFGHANISTAN

SAUDI

ARABIA

45 '

50 *

55 "

60 "

65 °

Figure 2. Map of Iran and the location of limited population (A) of Eremias acutirostris in east of Iran.

Figure 3. Habitat of Eremias acutirostris along the road from Bonjar to Doost Mohammad, Sistan region, Iran.

amphibian-reptile-conservation.org

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July 2013 | Volume 6 | Number 2 | e60

Hosseinian Yousefkhani et al.

Seyyed Saeed Hosseinian Yousefkhani earned his B.Sc. in biological sciences from the Hakim Sabzevari

University. He received his M.S. in animal biosystematics from the University of Razi, Kermanshah, where he

researched the geographic variation of Mesalina watsonana (Sauria: Lacertidae) with morphological characters

in Iran. He currently a research colleague in several reptile projects in Iran.

Hamzeh Oraie is a Ph.D. student in the department of zoology at the University of Tehran. He received his B.S.

in biological sciences, and M.S. in animal biosystematics both from the University of Razi, Kermanshah. His

M.S. research focused on the gecko fauna of Iran. His current research interests include molecular systematics

and phylogeny of Ophisops elegans (Sauria: Lacertidae) in Iran.

Azar Khosravani earned her B.S. in biological sciences from the University of Zabol. She received her M.S.

in animal biosystematics from the University of Razi, Kermanshah, where she researched the geographic varia-

tion of Mesalina watsonana (Sauria: Lacertidae) in Iran. Currently, she is a Ph.D. student in the department of

biology at the University of Razi, Kermanshah. Her current research interests include molecular systematics and

phylogeny of the Genus Bunopus (Sauria: Gekkonidae) in Iran.

Eskandar Rastegar-Pouyani earned his B.S. in animal science from Tehran University, Iran in 1995 and his

M.S. in animal biosystematics from Teacher Training University of Tehran, Iran in 1997, where he studied the

herpetofauna of the Semnan Province, northeastern Iran. In 2007 he received his Ph.D. from the University of

Heidelberg, Germany under the advisement of Michael Wink and Ulrich Joger. His doctoral dissertation investi-

gated the molecular phylogeny and phylogeography of the genus Eremias (Sauria, Lacertidae).

amphibian-reptile-conservation.org

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July 2013 | Volume 6 | Number 2 | e60

Amphibian & Reptile Conservation 6(2): 35-39.

ative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License, which permits unrestricted use for

non-commercial and education purposes only provided the original author and source are credited. The official

publication credit source: Amphibian & Reptile Conservation at: amphibian-reptile-conseiyation.org

New country record and range extension of Eremias suphani

Ba§oglu & Hellmich, 1968 from Iran

15 Eskandar Rastegar-Pouyani, 2 Aziz Avci, 3 Yusuf Kumluta§, 3 Qetin llgaz,

and 4 Seyyed Saeed Hosseinian Yousefkhani

1 Department of Biology, Faculty of science, Hakim Sabzevari University, Sabzevar, IRAN 2 Adnan Menderes University Faculty of Science and

Arts, Department of Biology, Aydin-TURKEY 3 Dokuz Eyliil University, Faculty of Science, Department of Biology’, Buca, izmir-TURKEY A Young

Researchers and Elite Club, Shirvan Branch, Islamic Azad University, Shirvan, IRAN

Abstract . — Iran is located in an area that is bordered by several mountains and contains herpeto-

faunal constituents from adjacent countries such as Pakistan, Iraq, Afghanistan, and Turkey. We

surveyed several border provinces of Iran to more completely understand the Iranian herpetofauna.

During one survey in the northwestern part of Iran we found a species of the genus Eremias that can

be added to Iran’s herpetofauna. Previously, the distribution of Eremias suphani was limited to the

Van Lake in Turkey (type locality). We compared Iranian samples with E. suphani from Turkey using

a molecular marker (Cytochrome b) and confirmed that this species is also present in Iran. The new

record of this species is located on the road from Firoragh to Chaldoran in the west of the province

of Azarbaijan, Iran.

Key words. Eremias suphani, Iran, Turkey, new record, molecular marker

Citation: Rastegar-Pouyani E, Avci A, Kumluta§ Y, llgaz C, Hosseinian Yousefkhani SS. 2013. New country record and range extension of Eremias

suphani Ba§oglu & Hellmich, 1968 from Iran. Amphibian & Reptile Conservation 6(2): 35-39 (e73).

Introduction

The herpetofauna of Iran remains poorly documented

and in some isolated areas completely unknown (An-

derson 1999). Historically, the Iranian herpetofauna has

been studied by several foreign herpetologists (Mertens

1957; Anderson 1966, 1999; Leviton et al. 1992; Tuck

1971, 1974) who visited Iran, as well as by Iranian her-

petologists (Latifi 1991; Balouch and Kami 1995; Kami

and Vakilipoure 1996a, 1996b; Firouz 2000; Rastegar-

Pouyani et al. 2007). Nonetheless, herein we report the

presence of a previously undocumented species from

the country. According to the recent published data, 15

species of the genus Eremias exist in Iran (Hosseinian

Yousefkhani et al. 2013), to which we add another.

Eremias suphani (Suphan Racerunner) was consid-

ered to be confined to Turkey, where it was described

from Van Lake (Basoglu and Hellmich 1968), with some

additional populations of this species having been re-

corded from western Turkey (Bischof and Bohme 1980).

The species is morphologically similar to Eremias strau-

chi , its putative sister species, but there are differences in

scalation (Bischof and Bohme 1980).

Adults of Eremias suphani can be distinguished from

E. strauchi by the presence of a double or single row

of gular scales separating the scales of the third pair of

chin shields (third pair of chin shields in contact in E.

strauchi ), the presence of enlarged gular scales border-

ing the third pair of chin shields (no enlarged gulars in

Correspondence. 5 rastegarpouyani45@gmail.com

E. suphani ), and the presence of a ventrolateral row of

well-defined, large, round, white spots, that may be fused

to form a longitudinal band (diffuse small longitudinal

spots or a diffuse thin line in E. strauchi).

The distribution of these two sister species meet in

the Dogubayazit Depression in NE Turkey (Bischof and

Bohme 1980). In Iran, E. suphani is found on compact-

ed, loamy soil at the Iran-Turkey border. In Turkey, E.

suphani also lives on pebbly/sand substrates with sparse

vegetation (Franzen and Hecks 1999; Baran et al. 2012).

Amphibian and reptile species that have a sympatric

distribution with E. suphani include: Bufotes variabi-

Iis, Pelophylax ridibundus , Rana macrocnemis, Testudo

graeca, Trapelus lessonae, Ophisops elegans, and Lac-

erta media. Eremias suphani is listed as Least Concern

because, although its extent of occurrence is less than

20,000 km 2 , it is common with large population sizes,

no major threats, and it is unlikely to be declining fast

enough to qualify for listing in a more threatened cat-

egory (Kaska et al. 2013).

Herein we report a new Iranian country record for

E. suphani, confirmed using a molecular marker (Cyto-

chrome b).

Materials and Methods

The Iranian samples were collected during field trips to

the northwest of the country in June 2005 on the road

amphibian-reptile-conservation.org

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December 2013 | Volume 6 | Number 2 | e73

Rastegar-Pouyani et al.

Figure 1 . Habitat of Eremias suphani in NW Iran on the road from Firoragh to Chaldoran in Ali Sheykh village (Photo by Eskandar

Rastegar-Pouyani, 2005).

from Firoragh to Chaldoran, at the village of Alishekh

(Fig. 1) (E 44° 34' 78.4", N 38° 49' 22.1", elevation:

1934 m). Four specimens were collected (SUHC 310-

313) (Fig. 2) and deposited in the Sabzevar University

Herpetological Collection (SUHC), Iran. The sites of the

new records near the border of Iran-Turkey are provided

in Figure 3. Turkish specimens were collected from three

different localities in 2010 and 2012 (Aydtnlar Village,

Adilcevaz, Bitlis — between Tatvan and Bitlis km 4, Bit-

lis — Ho§ap, Giizelsu, Van). They were deposited in the

Biology Laboratories of Dokuz Eyliil University, izmir,

Turkey.

DNA was obtained from tissue samples (muscle or

liver) that were preserved in 96% ethanol (Rastegar-

Pouyani et al. 2010). DNA was extracted using a high salt

method (Kabir et al. 2006). Fragments of Cytochrome b

were amplified (PCR) using the primers Mtanew (5'-CTC

three specimens of E. strauchi and five specimens of E.

suphani from Turkey where compared with the Iranian

samples using MEGA 5.0 software (Table 1). The se-

quences have been deposited in the GeneBank with ac-

cession numbers from KF797802 to KF797813.

Results

Genetic distance (Table 2) indicates that the Iranian sam-

ples are very close to Eremias suphani of Turkey with

only about 2% of genetic distance. Distances between

Eremias strauchi population and both Eremias suphani

and Eremias sp. samples from Iran, are 16%. Eremias sp.

samples from Iran now confirmed as Eremias suphani.

In addition to previous studies on the Iranian herpe-

tofauna, our initial research in the NW comer of Iran

revealed the presence of Eremias suphani in Iran. We fo-

CCA GCC CCA TCC AAC ATC TCA GGA TGA TGA cused our search in NW Iran to the border of Turkey fo:

AAC-3') and Mtfsh (5 '-TAG TTG GCC AAT GAT GAT other localities, but in the other locations Eremias straw

GAA TGG GTG TTC TAC TGG-3'). Sequences from chi : has been recorded.

Table 1. Examined samples in this study along with their locality and coordinates.

Code

Species name

N

E

Elevation

Locality

Str-1

Eremias strauchi

39° 51' 57.1"

42° 29' 03.3"

864 m

Between Aralik and Giindogdu, Igdir

Str-2

Eremias strauchi

39° 51' 57.1"

42° 29' 03.3"

864 m

Between Aralik and Giindogdu, Igdir

Str-3

Eremias strauchi

39° 51' 57.1"

42° 29' 03.3"

864 m

Between Aralik and Giindogdu, Igdir

SU2-A

Eremias suphani

38° 18' 18.2"

43 ° 48' 46.4"

1,997 m

Ho§ap, Giizelsu, Van

SU2-B

Eremias suphani

38° 18' 18.2"

43 ° 48' 46.4"

1,997 m

Ho§ap, Giizelsu, Van

SU2-C

Eremias suphani

38° 18' 18.2"

43 ° 48' 46.4"

1,997 m

Ho§ap, Giizelsu, Van

SU1-B

Eremias suphani

38° 53' 55.2"

42° 55' 38.8"

2,000 m

Aydmlar village, Adilcevaz, Bitlis

SU1-C

Eremias suphani

38° 53' 55.2"

42° 55' 38.8"

2,000 m

Aydmlar village, Adilcevaz, Bitlis

SUHC 724

Eremias sp.

38° 49' 22.1"

44 ° 34 ' 78.4"

1,934 m

on the road from Firoragh to Chaldoran

SUHC 725

Eremias sp.

38° 49' 22.1"

44 ° 34 ' 78.4"

1,934 m

on the road from Firoragh to Chaldoran

SUHC 726

Eremias sp.

38° 49' 22.1"

44 ° 34 ' 78.4"

1,934 m

on the road from Firoragh to Chaldoran

amphibian-reptile-conservation.org

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December 2013 | Volume 6 | Number 2 | e73

New country record and range extension of Eremias suphani

Figure 2. General view of Eremias suphani from Iran. The color pattern of this species is different from Eremias strauchi strauchi

(Photo by EskandarRastegar-Pouyani, 2005).

Discussion

Specimens of Eremias collected from Ahlat, Bitlis, in

eastern Turkey were considered to be Eremias velox ssp.

by Ba§oglu and Hellmich (1959). In 1968, these authors

examined specimens from Ahlat, Sup ban Dagi, Mukus,

and Van and described a new subspecies, Eremias velox

suphani. Peters (1964) considered E. velox strauchi to be

a full species (E. strauchi ), whereas specimens collected

from Dogubayazit, Igdir, and Kagizman were considered

as E. velox by Clark and Clark (1973). Ba§oglu and Ba-

ran (1977) stated that E. suphani and E. strauchi are sub-

species of E. velox whereas Bischoff (1978) suggested

that E. suphani is a subspecies of E. strauchi. Finally,

E. velox suphani was regarded as a distinct species by

Bishoff and Bohme (1980).

Eremias suphani is considered to be endemic to east-

ern Turkey, where it is known from the vicinity of Lake

Van (Mulder 1995; Franzen and Heckes 1999; Baran et

al. 2012).

According to the previous studies on the Iranian her-

peto fauna (Leviton et al. 1992; Anderson 1999; Ras-

tegar-Pouyani et al. 2007, 2008), E. suphani has not been

recorded from Iran. During field trips to northwest Iran in

2005, four specimens from a population belonging to the

genus Eremias were collected that were not compatible

with diagnostic key of the Iranian species of Eremias, but

were comparable to E. strauchi. Considering these ob-

servations we assumed that these specimens represented

a new species of Eremias, and decided to compare the

specimens with individuals of other species of the genus

that were described and previously recorded from the re-

gion, specifically Eremias strauchi and Eremias suphani.

Genetic analysis revealed that the Iranian samples clus-

tered (with 2% distance) with E. suphani and not with E.

strauchi (16% distance). This new country record dem-

onstrates how the border regions of Iran have not been

carefully investigated, and that additional effort must be

made to document reptile diversity in these areas.

These results strongly suggest that the Iranian samples

are conspecific with Eremias suphani. Consequently, we

conclude that Eremias suphani is recorded for the first

time in Iran near the border with Turkey on the road from

Firoragh to Chaldoran in Ali Sheykh village.

Acknowledgments. — We thank Hamzeh Oraei and

Azar Khosravani for their efforts in providing the mo-

lecular data and Dr. Jim Bogart for his generous help in

improving the English of an earlier version of this manu-

script.

Table 2. Estimates of evolutionary divergence (p-distance) over sequence pairs between samples of Eremias in this study.

Eremias suphani Turkey

Eremias sp. Iran Firoragh

Eremias strauchi strauchi

Eremias suphani Turkey

—

0.022

0.193

Eremias sp. Iran Firoragh

0.022

—

0.166

Eremias strauchi strauchi

0.193

0.166

—

amphibian-reptile-conservation.org

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December 2013 | Volume 6 | Number 2 | e73

Rastegar-Pouyani et al.

TURKEY

w

lran-TurkeX^aer

IRAQ W

Type locality and Turkey records

IRAN

aw

Figure 3. Iran-Turkey map and localities of new records in Iran and the type locality of Eremias suphani around the Van Lake in

Turkey. Red circles relate to new country records in Iran and the blue circles are type localities of the Turkish samples.

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Received: 03 November 2013

Accepted: 08 November 2013

Published: 14 December 2013

Appendix I. List of the material examined in this study and their accession numbers.

Species name

Country

Accession Number

Eremias suphani

Turkey

KF797802

Eremias suphani

Turkey

KF797803

Eremias suphani

Turkey

KF797804

Eremias suphani

Turkey

KF797805

Eremias suphani

Iran

KF797806

Eremias suphani

Iran

KF797807

Eremias suphani

Iran

KF797808

Eremias suphani

Iran

KF797809

Eremias strauchi strauchi

Iran

KF797810

Eremias strauchi strauchi

Iran

KF797811

Eremias strauchi strauchi

Iran

KF797812

Eremias strauchi strauchi

Iran

KF797813

amphibian-reptile-conservation.org

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December 2013 | Volume 6 | Number 2 | e73

CONTENTS

Administration, journal information (Instructions to Authors), and copyright notice Inside front cover

Adel A. Ibrahim — New records of the Dice snake, Natrix tessellata, in the Suez Canal zone and Sinai 2

Craig Hassapakis — Books to Read 5

Andreas Hertz, Sebastian Lotzkat, Arcadio Carrizo, Marcos Ponce, Gunther Kohler, and Bruno St-

reit — Field notes on findings of threatened amphibian species in the central range of western Panama 9

Seyyed Saeed Hosseinian Yousefkhani, Hamzeh Oraei, Azar Khosravani and Eskandar Rastegar-Pouy-

ani — Habitat associations and conservation of Eremias acutirostris (Boulenger, 1887) in the Sistan region,

Zabol, Iran 31

Eskandar Rastegar-Pouyani, Aziz Avci, Yusuf Kumluta§, £etin Ilgaz, and Seyyed Saeed Hosseinian

Yousefkhani — New country record and range extension of Eremias suphani Ba§oglu & Hellmich, 1968

from Iran 35

Table of Contents Back cover

VOLUME 6

2013

NUMBER 2