B&AH nº 27 [2013]

Revista EspaĂąola de HerpetologĂ­a

Journal of the Spanish Herpetological Society (AHE) Volumen 27 (2013) http://bah.herpetologica.es bah@herpetologica.org

Amphibian Biology Volume 11. Status of Conservation and Decline of Amphibians: Eastern Hemisphere Part 2. Northern Africa Editors: Stephen D. Busack, Harold Heatwole

BASIC & APPLIED HERPETOLOGy REVISTA ESPAÑOLA DE HERPETOLOGÍA

Spanish Herpetological Society (AHE) President: Juan Manuel Pleguezuelos Gómez Vice-President: Jaime Bosch Pérez General Secretary: Miguel Ángel Carretero Fernández Vice-General Secretary: José Antonio Mateo Miras Vocals: Enrique Ayllón López (Management) César Ayres Fernández (Conservation) Francisco Javier Diego Rasilla (Web page and promotion) Andrés Egea Serrano (Editor, Boletín de la AHE) Gustavo A. Llorente Cabrera (Atlas) Adolfo Marco Llorente (Marine turtles) Alber Montori Faura (Atlas) Manuel E. Ortiz Santaliestra (Editor, Basic & Applied Herpetology) Ana Perera Leg (Editor, Basic & Applied Herpetology) Alex Richter Boix (Editor, Boletín de la AHE) Xavier Santos Santiró (Editor, Boletín de la AHE & Treasurer) Daniel Villero Pi (Atlas)

Basic & Applied Herpetology (Editors) Manuel E. Ortiz Santaliestra (Amphibians) Institute for Environmental Sciences University of Koblenz-Landau Fortstraße 7, Building C1, Room 101b 76829 Landau (Germany) ortiz@uni-landau.de

Ana Perera Leg (Reptiles) CIBIO-Universidade do Porto.

Campus Agrário de Vairão.

Rua Padre Armando Quintas-Castro 4485-661 Vairão (Portugal) perera@cibio.up.pt

Asociación Herpetológica Española Museo Nacional de Ciencias Naturales Cl. José Gutiérrez Abascal, 2 28006 Madrid http://www.herpetologica.es

ISSN 2255 - 1468 Impresión: igrafic. Url: www.igrafic.com

Depósito Legal: M-38882-2012 Maquetación: Marcos Pérez de Tudela. Url: www.marcos-pdt.com

BASIC & APPLIED HERPETOLOGy REVISTA ESPAÑOLA DE HERPETOLOGÍA

CONTENTS Volume 27 (2013)

Pag. Editorial

5

Chapter 23. Introduction H. Heatwole, S.D. Busack

7

Chapter 24. Amphibian conservation in Mauritania J.M. Padial, P.-A. Crochet, P. Geniez, J.C.Brito

11

Chapter 25. Amphibians of Morocco, including Western Sahara: a status report R. Reques, J.M. Pleguezuelos, S.D. Busack, P. de Pous

23

Chapter 26. Diversity and conservation of Algerian amphibian assemblages J.A. Mateo, P. Geniez, J. Pether

51

Chapter 27. Conservation status of amphibians in Tunisia N. Amor, M. Kalboussi, K. Said

85

Chapter 28. Amphibians in Libya: a status report A.A. Ibrahim

101

Chapter 29. Amphibians of Egypt: a troubled resource A.A. Ibrahim

107

Cover illustration: Moroccan Spadefoot Toad (Pelobates varaldii) in the sand in Mamora Forest, Morocco (January, 2009) (see article by Reques et al. in this volume). Author: Philip de Pous.

BASIC & APPLIED HERPETOLOGy REVISTA ESPAÑOLA DE HERPETOLOGÍA

CONTENIDOS Volumen 27 (2013)

Pag. Editorial

5

Capítulo 23. Introducción H. Heatwole, S.D. Busack

7

Capítulo 24. Conservación de anfibios en Mauritania J.M. Padial, P.-A. Crochet, P. Geniez, J.C.Brito

11

Capítulo 25. Los anfibios de Marruecos, incluyendo Sáhara Occidental: Informe sobre su situación R. Reques, J.M. Pleguezuelos, S.D. Busack, P. de Pous

23

Capítulo 26. Diversidad y conservación del conjunto de anfibios argelinos J.A. Mateo, P. Geniez, J. Pether

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Capítulo 27. Estado de conservación de los anfibios en Túnez N. Amor, M. Kalboussi, K. Said

85

Capítulo 28. Anfibios en Libia: informe sobre su situación A.A. Ibrahim

101

Capítulo 29. Anfibios de Egipto: un recurso en problemas A.A. Ibrahim

107

Ilustración de portada: Sapo de Espuelas marroquí (Pelobates varaldii) en la arena en el bosque de Mamora, Marruecos (Enero 2009) (véase artículo de Reques et al. en este volumen). Autor: Philip de Pous.

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This year's volume of Basic & Applied Herpetology is dedicated entirely to publication of Part 2 of volume 11 of the book series Amphibian Biology. In 2013, the editors of this part, Stephen Busack and Harold Heatwole, posed to the editorial board of Basic & Applied Herpetology the challenge of publishing the Status of Conservation and Decline of Amphibians in North Africa. After a long process of editing and revision we are happy to present this treatise, organized in an introduction and six chapters, each chapter dedicated to a single North African country, including Mauritania, Morocco, Algeria, Tunisia, Libya, and Egypt, and written by some of the most relevant researchers in these countries.

The Spanish Herpetological Society, both as an institution and through some of its members in particular, has traditionally maintained an active focus on the North African herpetofauna. Now, we are proud to contribute to the publication of this work, which constitutes a valuable update for information regarding amphibians from this region as well as some novel information.

We wish to thank the authors of the chapters and the editors of the series for their understanding, patience, and effort in updating these manuscripts with the latest available information. We believe that members of the Spanish Herpetological Society and readers of the journal will appreciate the valuable information presented in this volume.

The editorial board

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Basic and Applied Herpetology 27 (2013): 7-10

Chapter 23 Introduction Harold Heatwole1,*, Stephen D. Busack2 1 2

Department of Biology, North Carolina State University, Raleigh, North Carolina, USA. North Carolina Museum of Natural Sciences, Raleigh, North Carolina, USA.

*Correspondence: Department of Biology, North Carolina State University, Raleigh, NC 27695-7617, USA. Phone: +1 (919) 515-3122, Email: harold_heatwole@ncsu.edu

Received: 10 January 2013; accepted: 10 January 2013.

Previous studies have treated the status of decline and conservation in amphibians, generally and on a country-by-country basis, for the Western Hemisphere. The present volume presents a series of papers for the Eastern Hemisphere, and this issue covers North Africa. An annotated checklist to current nomenclature of regional taxa is also provided.

Key words: amphibians; conservation; decline; North Africa.

Introducción. En estudios anteriores se han tratado el declive y la conservación de los anfibios del hemisferio occidental, tanto de manera general como país por país. El presente volumen presenta una serie de artículos correspondientes al hemisferio oriental, y este número en particular versa sobre el norte de África. Se aporta además una lista con la nomenclatura actualizada de los taxones de la región.

Key words: anfibios; conservación; declive; norte de África.

Amphibian skin is a bare, thin, and moist accessory respiratory organ endowed with a plentiful blood supply, attributes that make it a poor barrier against desiccation, noxious chemicals, and various other stresses (HEATWOLE et al., 1994). Exacerbating this basic ecological vulnerability is an emergent fungal disease, chytridiomycosis, that attacks the skin and larval mouthparts of amphibians and to which most species are highly susceptible (BERGER et al., 2009; MARTEL et al., 2013). Anthropogenic changes to the environment, such as fragmentation and destruction of habitat; pollution by endocrine disruptors and industrial, agricultural, and household waste; depletion of the ozone layer and concomitant elevation of ultraviolet radiation; acidification; climatic change; and road kills have contributed to the assault on

amphibians (HEATWOLE & WILKINSON, 2009, 2012). As a result, populations of many species around the world have been declining on an unprecedented scale, and many extinctions have occurred (LANNOO, 2005; WILSON et al., 2010; HEATWOLE, 2013).

The series Amphibian Biology (HEATWOLE et al., 1994 et seq.) variously published or in press by Surrey Beatty & Sons (Chipping Norton, later Baulkham Hills, Australia); Natural History Press (Kota Kinabalu, Sabah); Pelagic Press (Exeter, UK); Herpetological Monographs; and the present chapters by Basic and Applied Herpetology, has devoted three volumes to amphibian decline and extinction, two of which (Volumes 8 and 10) treated causes and potential remedies for these phenomena. Volumes

This chapter should be cited as: Heatwole, H. & Busack, S.D. (2013). Introduction. Chapter 23 in Part 2. Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 7-10.

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9 and 11, being published in parts as chapters become available, provide assessments of decline and extinction on a country-bycountry basis for the Western and Eastern Hemispheres, respectively. Volume 9, Parts 1 (Paraguay, Chile and Argentina [2010]), 2 (Uruguay, Brazil, Ecuador and Colombia [2011]) and 3 (Venezuela, Guyana, Suriname, and French Guiana [2012]) have been issued (HEATWOLE et al. 2010, 2011, 2013); Bolivia and Peru (Part 4) are under review. Parts on Central America, the Caribbean, and North America are pending.

The present contribution to the Amphibian Biology series represents Part 2 (Mauritania, Morocco, Algeria, Tunisia, Libya, and Egypt) of Volume 11. Part 1 covers all of Asia (HEATWOLE & DAS, 2014) and Part 3 deals with Western Europe (HEATWOLE & WILKINSON, 2013).

Various websites provide amphibian status at particular times and places; these websites change as population status of considered amphibian species changes. Without reference to previous conditions, however, it is not possible to assess the extent and rate of amphibian decline.

Amphibian Biology serves as an internationally available historical reference with which future assessment may be compared – a sort of time capsule. In one sense, because species of amphibians are going extinct while chapters are being written and put to press, any static publication may be out of date by the time it is published. An established benchmark, however, is timeless and necessary for temporal comparisons.

While some amphibian taxonomic rearrangements first proposed by FROST et al. (2006) have been widely accepted without argument, some rearrangements have been modified and others remain controversial (for updates see FROST, 2013). Until a more comprehensive consensus is

reached and nomenclature regarding all species becomes stabilized, it seems unwise to dictate any particular scheme for use in the Amphibian Biology series and authors have been allowed to exercise professional judgment regarding choice of nomenclature. As Part 2 of Volume 11 was in final review one species was reassigned (Bufotes boulengeri is now the recommended name) and the genus Barbarophryne was described (now the recommended name for Barbarophryne brongersmai) (BEUKEMA et al., 2013). As taxonomic allocations in poorly-understood species assemblages continue to receive attention, additional reallocations are possible.

Because it is important that information regarding conservation status be provided to herpetologists, government professionals in conservation and law enforcement, ecologists, and other interested parties in an unambiguous manner, the following annotated “checklist” to species in the areas covered in this issue is presented by family and arranged following nomenclatural choice of the authors. We hope it serves as a convenient checklist for species treated in this issue.

ORDER ANURA Family Alytidae Alytes maurus Pasteur and Bons, 1962 (Morocco, Algeria).

Discoglossus pictus Otth, 1837 (Morocco, Algeria, Tunisia).

Discoglossus scovazzi Camerano, 1878 (Morocco, Algeria).

Family Bufonidae Amietophrynus kassasii (Baha El Din, 1993) (Egypt).

Amietophrynus mauritanicus (Schlegel, 1841) (Morocco, Algeria, Tunisia).

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INTRODUCTION

Amietophrynus regularis (Reuss, 1833) (Mauritania, Egypt).

Amietophrynus xeros (Tandy, Tandy, Keith & Duff-Mackay, 1976) (Mauritania, Morocco, Algeria, Libya).

Barbarophryne brongersmai Hoogmoed, 1972 (Morocco, Algeria).

Bufo spinosus Daudin, 1803 (Morocco, Algeria, Tunisia) .

“Bufo” pentoni Anderson, 1893 (Mauritania).

Bufotes boulengeri (Lataste, 1879) (Morocco, Algeria, Libya, Tunisia, Egypt).

Duttaphrynus dodsoni (Boulenger, 1895) (Egypt).

Family Dicroglossidae Hoplobatrachus occipitalis (Günther, 1858) (Mauritania, Morocco, Algeria, Libya*).

Family Hylidae Hyla meridionalis Boettger, 1874 (Morocco, Algeria, Tunisia).

Hyla savignyi Audouin, 1827 (Egypt).

Family Hyperoliidae Kassina senegalensis (Duméril & Bibron, 1841) (Mauritania).

Family Pelobatidae Pelobates varaldii Pasteur and Bons, 1959 (Morocco).

Family Phrynobatrachidae Phrynobatrachus natalensis (Smith, 1849) (Mauritania).

Family Ptychadenidae Ptychadena bibroni (Hallowell, 1845) (Mauritania).

Ptychadena mascareniensis (Duméril & Bibron, 1841) (Mauritania, Egypt).

Ptychadena trinodis (Boettger, 1881) (Mauritania).

Ptychadena schillukorum (Werner, 1908) (Egypt).

Family Pyxicephalidae Pyxicephalus edulis Peters, 1854 (Mauritania)

Tomopterna cryptotis (Boulenger, 1907) (Mauritania).

Family Ranidae Pelophylax bedriagae (Camerano, 1882) (Egypt).

Pelophylax saharicus (Boulenger, 1913) (Morocco, Algeria, Libya, Tunisia, Egypt). *Although historically cited, the current presence of Hoplobatrachus occipitalis in Libya has not been confirmed in recent surveys.

ORDER CAUDATA Family Salamandridae Pleurodeles nebulosus (Guichenot, 1850) (Algeria, Tunisia).

Pleurodeles poireti (Gervais, 1835) (Algeria) Pleurodeles waltl Michahelles, 1830 (Morocco).

Salamandra algira Bedriaga, 1883 (Morocco, Algeria).

REFERENCES BERGER, L.; LONGCORE, J.F.; SPEARE, R.; HyATT, A. & SKERRATT, L.F. (2009).

Fungal diseases of amphibians, In H. Heatwole & J.W. Wilkinson (eds.)

Amphibian Decline: Diseases, Parasites, Maladies and Pollution.

Series: Amphibian Biology, vol. 8. Surrey Beatty & Sons, Baulkham Hills, Australia, pp.

2986-3066.

BEUKEMA, W.; DE POUS, P.; DONAIREBARROSO, D.; BOGAERTS, S.; GARCIAPORTA, J.; ESCORIzA, D.; ARRIBAS, O.J.; EL MOUDEN, E.H. & CARRANzA, S. (2013).

Review of the systematics, distribution, biogeography and natural history of Moroccan amphibians. Zootaxa 3661: 1-60.

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FROST, D.R. (2013). Amphibian Species of the World: an Online Reference. Version 5.6 (9 January 2013). American Museum of Natural History, New york, USA. Available at http://research.amnh.org/vz/herpetology/am phibia/index.html. Retrieved on 11/07/2013.

FROST, D.R.; GRANT, T.; FAIVOVICH, J.; BAIN, R.H.; HAAS, A.; HADDAD, C.F.B.; DE SA, R.O.; CHANNING, A.; WILKINSON, M.; DONNELLAN, S.C.; RAXWORTHy, C.J.; CAMPBELL, J.A.; BLOTTO, B.L.; MOLER, P.; DREWES, R.C.; NUSSBAUM, R.A.; LyNCH, J.D.; GREEN, D. M. & WHEELER, W.C. (2006). The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1-370.

HEATWOLE, H. (2013). Worldwide decline and extinction of amphibians, In K. Rohde (ed.)

The Balance of Nature and Climate Change.

Cambridge University Press, Cambridge, United Kingdom, pp. 259-278.

HEATWOLE, H. & DAS, I. (2014). Asia. Part 1 in Status of Conservation and Decline of Amphibians: Eastern Hemisphere. Series: Amphibian Biology, vol. 11, Natural History Publications, Kota Kinabalu, Sabah.

HEATWOLE, H. & WILKINSON, J.W. (2009).

Amphibian Decline: Diseases, Parasites, Maladies and Pollution. Series: Amphibian Biology, vol. 8. Surrey Beatty & Sons, Baulkham Hills, Australia.

HEATWOLE, H. & WILKINSON, J.W. (2012).

Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management. Series: Amphibian Biology, vol. 10.

Surrey Beatty & Sons, Baulkham Hills, Australia.

HEATWOLE, H. & WILKINSON, J.W. (2013).

Western Europe. Part 3 in Status of Conservation and Decline of Amphibians: Eastern Hemisphere.

Series: Amphibian Biology, vol. 11, Pelagic Publishing, Exeter, United Kingdom.

HEATWOLE, H.; BARTHALMUS, G.T. & HEATWOLE, A.y. (1994). The Integument.

Series: Amphibian Biology, vol. 1. Surrey Beatty & Sons, Chipping Norton, Australia.

HEATWOLE, H.; BARRIO-AMOR贸S, C.L. & WILKINSON, J.W. (2010) Paraguay, Chile and Argentina. Part 1 in Status of Decline of Amphibians: Western Hemisphere. Series: Amphibian Biology, vol. 9, Surrey Beatty & Sons, Baulkham Hills, Australia.

HEATWOLE, H.; BARRIO-AMOR贸S, C.L. & WILKINSON, J.W. (2011) Uruguay, Brazil, Ecuador and Colombia. Part 2 in Status of Decline of Amphibians: Western Hemisphere.

Series: Amphibian Biology, vol. 9, Surrey Beatty & Sons, Baulkham Hills, Australia.

HEATWOLE, H.; BARRIO-AMOR贸S, C.L. & WILKINSON, J.W. (2013) Venezuela, Guayana, Suriname and French Guayana. Part 3 in Status of Decline of Amphibians: Western Hemisphere.

Series: Amphibian Biology, vol. 9, Surrey Beatty & Sons, Baulkham Hills, Australia.

LANNOO, M. (2005). Amphibian Declines.

The Conservation Status of United States Species. University of California Press, Berkeley, California, USA. MARTEL, A.; SPITzEN-VAN DER SLUIJS, A.; BLOOI, M.; BERT, W.; DUCATELLE, R.; FISHER, M.C.; WOELTJES, A.; BOSMAN, W.; CHIERS, K.; BOSSUyT, F. & PASMANS, F. (2013). Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America 110: 15325-15329.

WILSON, L.D.; TOWNSEND, J.H. & JOHNSON, J.D. (2010). Conservation of Mesoamerican Amphibians and Reptiles.

Eagle Mountain Publishing Company, Eagle Mountain, Utah, USA.

Basic and Applied Herpetology 27 (2013): 11-22

Chapter 24 Amphibian conservation in Mauritania José Manuel Padial1,*, Pierre-André Crochet2, Philippe Geniez3, José Carlos Brito4 Section of Amphibians and Reptiles, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, USA. CNRS-UMR 5175 Centre d'Ecologie Fonctionnelle et Evolutive, Montpellier, France.

3 EPHE-UMR 5175 Centre d'Ecologie Fonctionnelle et Evolutive, Montpellier, France.

4 Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Instituto de Ciências Agrárias de Vairão, Vairão, Portugal.

1 2

*Correspondence: Section of Amphibians and Reptiles, Carnegie Museum of Natural History, 4400 Forbes Avenue, Pittsburgh, Pennsylvania, 15213-4080 USA. Phone: +1 412 622 4691, Email: padialj@CarnegieMNH.org

Received: 10 January 2013; received in revised form: 30 September 2013; accepted: 1 October 2013.

Only eleven species of amphibians (all anurans) have been found in Mauritania so far. Nonetheless, large areas of the country remain unexplored and the taxonomic status of several species remains uncertain, suggesting that additional species may be found in the future, especially in the Sahel savannahs of the southern part of the country. Within the Saharan realm, amphibians occur in isolated springs, “wadis” (temporary streams), and “gueltas” (ponds) in montane regions (Adrar and Tagant plateaus), while the Sahel savannahs contain innumerable bodies of water where all species listed in the country have been recorded despite only a small portion of the area having been sampled. No information on population trends is available, but the Sahel is threatened by intensive wood harvesting, agro-pastoral utilization, and uncontrolled use of pesticides.

Mountain populations in the Sahara are isolated and likely small, with high vulnerability to drought and global warming. Priority research needs include: (1) data on distribution and diversity for action by local conservation agencies; (2) determination of environmental change and the effect of population dynamics on genetic diversity and local populations; and (3) clarification of the taxonomic status of existing populations and the identification of reservoirs of genetic diversity.

Key words: amphibians; conservation; decline; distribution; Mauritania.

Conservación de anfibios en Mauritania. Hasta la fecha sólo once especies de anfibios (todas ellas anuros) han sido citadas en Mauritania. Sin embargo, todavía quedan en el país áreas extensas sin explorar y el estatus taxonómico de algunas especies es incierto, lo que sugiere que en el futuro podrían sumarse más especies, sobre todo en las sabanas del Sahel en la parte sur del país. En el área del Sáhara, los anfibios aparecen en manantiales aislados, “wadis” (arroyos temporales) y “gueltas” (charcas) en zonas de montaña (mesetas de Adrar y Tagant), mientras que las sabanas del Sahel contienen numerosas masas de agua en las que se han hallado todas las especies presentes en el país pese a que sólo se ha muestreado una pequeña parte de este área. No hay información disponible acerca de las tendencias poblacionales, pero el Sahel está amenazado por la explotación maderera intensiva, el uso agro-pastoral y la aplicación incontrolada de plaguicidas. Las poblaciones montanas en el Sáhara aparecen aisladas y probablemente son pequeñas y con una elevada vulnerabilidad a la sequía y el calentamiento global. Las necesidades prioritarias en cuanto a investigación incluyen: (1) toma de datos de distribución y diversidad para promover acciones por parte de las agencias locales de conservación, (2) determinación de cambios ambientales y del efecto de las dinámicas poblaciones sobre la diversidad genética y las poblaciones locales, y (3) aclaración del estado taxonómico de las poblaciones existentes e identificación de reservorios de diversidad genética.

Key words: anfibios; conservación; declive; distribución; Mauritania.

This chapter should be cited as: Padial, J.M., Crochet, P-A, Geniez, P. & Brito, J.C. (2013). Amphibian conservation in Mauritania. Chapter 24 in Part 2. Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 11-22. DOI: http://dx.doi.org/10.11160/bah.13002/

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Three quarters of Mauritania’s one million square kilometers belong to the Sahara Desert, which translates into low amphibian diversity relative to adjacent areas such as the Mediterranean and the Sahel. Only eleven widely-distributed anuran species have been so far recorded for the country (Table 1) (NICKEL, 2003; PADIAL & DE LA RIVA, 2004), and all of them are categorized as species of Least Concern by the IUCN (2013). Large areas of the Mauritanian territory remains, however, poorly explored, especially in the north, east, and south of the country. Considering the distribution of amphibians in adjacent areas of neighbouring countries, at least 17 additional species might occur in these unexplored areas of Mauritania. In addition, the taxonomy of some species currently considered broadly-distributed, including those cited for Mauritania (Ptychadena spp.

[Ptychadenidae], Hoplobatrachus occipitalis [Dicroglossidae], Tomopterna spp. [Pyxicephalidae], and Phrynobatrachus spp. [Phrynobatrachidae]), is often unreliable. Resolution of taxonomic problems may change the composition of the species-list and some species currently considered widely-distributed may eventually be found to consist of species complexes, each component species of which exhibiting a more restricted distribution.

Saharan Mauritania harbours relict populations of some Afrotropical species, several hundred kilometres distant from the closest area with large populations of such species, the Senegal basin. These nowisolated populations were likely connected to source populations as recently as 4000 years ago when more benign conditions

supported continuous savannah extending further north to southern Morocco, Western Sahara, and northern Mauritania, and where the now-relict anuran populations dwelled among elephants, giraffes, and lions (LE HOUĂŠROU, 1997). As relatively recent, and extremely rapid, climatic change led to desertification (GASSE, 2000; FOLEy et al., 2003), most large mammals disappeared from arid areas, while some amphibian, reptilian, and fish populations became isolated along basins of retreating rivers and interior water courses, forming pockets of local survivors (PADIAL & DE LA RIVA, 2004; PADIAL, 2006; TRAPE, 2009; BRITO et al., 2011). At least 20 localities within the Mauritanian Sahara, many connected by fossil river basins that may have acted as corridors for exchange of individuals during wet periods, are still inhabited by two to three anuran species. Anurans inhabiting other localities, particularly those on the Adrar and Tagant plateaus, are completely isolated by dunes or expanses of rock from conspecific populations. These areas constitute a natural laboratory for studying effects of climatic change on natural populations (DUMONT, 1982). Topics such as the effect of population size and degree of isolation on genetic diversity and survival, the effect of species-specific physiological plasticity to environmental change, and the effect of allopatry and local adaptation in diversification, could be optimally studied in Saharan isolates (WARD, 2009).

Biodiversity is usually managed at the level of nations and more inclusive administrative units (PLEGUEzUELOS et al., 2010) and it is therefore important to maintain as

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AMPHIBIAN CONSERVATION IN MAURITANIA

Table 1: Geographical areas (see also Fig. 1) and taxonomic status of anuran species recorded from Mauritania. Nomenclature and classification follow FROST (2013); taxonomic status follows RöDEL (2000).

Family

Species

Bufonidae

“Bufo” pentoni Amietophrynus regularis

Amietophrynus xeros

Dicroglossidae

Hoplobatrachus occipitalis

Hyperoliidae

Kassina senegalensis

Phrynobatrachidae Phrynobatrachus natalensis Ptychadenidae

Ptychadena bibroni Ptychadena mascareniensis Ptychadena trinodis

Pyxicephalidae

Pyxicephalus edulis Tomopterna cryptotis

Distribution and population status Scattered localities across the Sahelian savannah; locally abundant.

Scattered localities across the Sahelian savannah and along the coast; locally abundant.

Taxonomic status Stable.

Unstable; several synonyms across its broad distribution, coupled with large genetic divergence between East Africa versus Central and West Africa (VASCONCELOS et al., 2010) present the possibility of future change in status.

Most Saharan bodies of water; Unstable; several synonyms across its broad distribution locally abundant. present the possibility of future change in status.

Unstable; possible species Most Saharan bodies of water and across the Sahelian savannah; complex. locally abundant but possible local extirpations have occurred.

Scattered localities across the Unstable; possible species complex.

Sahelian savannah; scarce.

Unstable; possible species Known only from a single locality in the Sahelian savannah; complex. no data on abundance.

Known from two localities in Stable. the Sahelian savannah; no data on abundance.

Unstable; possible species Known only from a single locality in the Sahelian savannah; complex. no data on abundance.

Known from two localities in Stable. the Sahelian savannah; no data on abundance.

Scattered localities across the Unstable; possible species complex.

Sahelian savannah; probably locally abundant.

Unstable, possible species Scattered localities across the Sahelian savannah; also recorded complex. from the coast and in some Saharan bodies of water; rare.

much genetic diversity as possible within national borders. Recent surveys of fishes in central Mauritania indicate that localities supporting populations of several species in the 1950s (DEKEySER & VILLIERS, 1956) have now completely dried, leading to local

extirpations (TRAPE, 2009). Although anurans are more tolerant than fish to periods of drought, populations of some anurans may have been extirpated while others may have already crossed the population size threshold necessary for long-term survival.

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DIVERSITy AND DISTRIBUTION All species occurring in Mauritania are present in the Sahelian savannah (Table 1; Figs. 1-2), a pattern partially explained by humidity and temperature conditions. Species present in Saharan isolates occur along springs, “wadis” (temporary streams), and “gueltas” (ponds) in montane regions, and are also generally abundant and widely-distributed in the Sahel (Fig. 1), a pattern also explained by humidity and temperature but coupled with elevation. This simple pattern suggests that the Saharan populations are not Saharan in origin but are instead the product of colonization from the Sahelian savannah.

In contrast to the situation of other Saharan massifs further north, such as Hoggar or Tassili N’Ajjer, no amphibian species of Mediterranean affinities reaches Mauritania.

Within the Saharan realm of Mauritania, H. occipitalis (Dicroglossidae) and Amietophrynus xeros (Bufonidae) are the most conspicuous representatives, although Tomopterna cryptotis (Pyxicephalidae) can also be found in a few Saharan localities. Amietophrynus regularis, A. xeros (Bufonidae), and T. cryptotis are also found along the Saharan Atlantic coast, although large populations occur only in the Sahelian wetlands of Diawling National Park, near the mouth of the Senegal River. Kassina senegalensis (Hyperoliidae), Phrynobatrachus natalensis (Phrynobatrachidae), Ptychadena mascareniensis, Ptychadena trinodis, Ptychadena bibroni (Ptychadenidae), and Pyxicephalus edulis (Pyxicephalidae) are restricted to the Sahelian savannah (Fig. 2) of southern Mauritania.

Important areas for Saharan populations are on the Adrar and Tagant plateaus (Fig. 1), where rocky areas form networks of seasonal

rivers (“wadis”) with many temporary and permanent springs and small pools (“gueltas”) along streams (CAMPOS et al., 2012) (Fig. 3).

The Adrar plateau contains more than 20 such permanent bodies of water (Fig. 1). The Tagant plateau, situated south of the Adrar plateau, is transitional between Saharan and Sahelian environments. This mountainous area of about 2000 km2 forms an inner drainage that empties into a marshland formed by Gabou Lake (Fig. 3c) and other minor lakes, or into several “wadis” in the Senegal River basin. This area harbours more suitable sites for amphibians than does the Adrar, and includes typical components of the Sahelian savannah such as K. senegalensis.

Many other montane areas remain poorly explored in Mauritania. Sampling has been most intense in the Adrar and Tagant areas, especially because they are more easily accessible by car.

Nonetheless, other montane areas of Mauritania have been comparatively less sampled than the Tagant and the Adrar and may contain important populations of amphibians. The Assaba and Afollé Mountains, located south and east of the Tagant, respectively, also hold important populations of H. occipitalis, A. xeros, K. senegalensis, and T. cryptotis.

The savannah in southern Mauritania contains innumerable bodies of water (CAMPOS et al., 2012) (Fig. 3). In addition to the eleven species recorded from this most diverse area of the country, PADIAL & DE LA RIVA (2004) suggested that several species were expected to occur in the country because they had been reported in neighbouring areas of Mali or Senegal. While none of these species has yet been recorded for Mauritania, we report this (taxonomically updated) list of expected species here:

AMPHIBIAN CONSERVATION IN MAURITANIA

15

Figure 1: Localities for Mauritanian anurans occurring in both Saharan isolates and Sahelian savannahs depicted over (top) elevation, and (bottom) environmental variability derived by Principal Components Analysis, where PC1 (red; 48.1% of variation): annual average temperature and maximum temperature of the hottest month; PC2 (green; 20.7%): minimum temperature of the coldest month; and PC3 (blue; 16.4%): slope. Environmental factors from Worldclim database (www.worldclim.org) at 2.5 arcsecond resolution. Photograph of Amietophrynus regularis courtesy of Mark-Oliver Rรถdel.

16

PADIAL ET AL.

Hemisotidae (Hemisus marmoratus); Hyperoliidae (Afrixalus fulvovittatus, Afrixalus weidholzi, Hyperolius spatzi, Kassina cassinoides, and Kassina fusca); Arthroleptidae (Leptopelis bufonides); Microhylidae (Phrynomantis microps); Pipidae (Xenopus muelleri); Ranidae (Hylarana galamensis); Phrynobatrachidae (Phrynobatrachus latifrons, Phrynobatrachus francisci, and Phrynobatrachus natalensis); Ptychadenidae (Ptychadena schillukorum, Ptychadena oxyrhynchus, Ptychadena pumilio, and Ptychadena tellinii).

CONSERVATION STATUS Although amphibians are declining worldwide, and amphibian extinctions are a major source of concern in many tropical countries (STUART et al., 2004), none of the anurans currently known in Mauritania is considered globally endangered (IUCN, 2013). This conclusion is, however, based on an incomplete survey of most African regions, and utilizes incomplete taxonomic knowledge. There is evidence suggesting that many African nominal species of the genera Ptychadena, Tomopterna, and Phrynobatrachus could in fact constitute species complexes (VENCES et al., 2004; PICKERSGILL, 2007; RöDEL et al., 2009). Future taxonomic research may well lead to changes in the perception of the level of endemicity and, hence, in the conservation needs of many species, including those occurring in Mauritania.

Although no evidence was found to indicate any population decline of anurans in Mauritania due to human pressure, an adequate assessment cannot be made because the relevant data are lacking. Some populations in the Sahel might be suffering negative effects

from intense harvesting of wood and from agro-pastoral use, two activities that enhance desertification, as well as from the uncontrolled use of pesticides (NATIONAL RESEARCH COUNCIL, 1981). Other important consequences for amphibians of agro-pastoral use in Mauritania could be the contamination of water by cattle faeces and the exploitation of bodies of water. Availability of many bodies of water within the Sahel Plateau (CAMPOS et al., 2012), however, should continue to provide refuge for healthy populations of anurans, at least in the short term.

Most Saharan populations are nonetheless vulnerable to extirpation. In fact, there has been a decline of relict fish populations in the Adrar Mountains related to intense drought (35% reduction in precipitation) since the 1970s (FOLEy et al., 2003), and some of them already have disappeared (TRAPE, 2009), suggesting that some local Saharan anuran populations may also be declining. While one might expect that a much higher tolerance to aridity would help anurans survive episodes of severe drought, and that metapopulation connectivity may be enhanced during favourable years, Saharan isolates of H. occipitalis, A. xeros, and T. cryptotis should be considered locally endangered, as well as other waterdependent reptiles and mammals (BRITO et al., 2011; VALE et al., 2012). Especially vulnerable are the northernmost populations of the Adrar Plateau. In fact, the permanent and deep (5 m) Guelta of Molomhar (near Atar) dried completely in March 2008, an unprecedented event according to local guides. This “guelta” had been historically inhabited by A. xeros, H. occipitalis, and at least three species of fish (Clarias anguillaris, Afropuntio pobeguini, and Tilapia zillii); all may have disappeared.

AMPHIBIAN CONSERVATION IN MAURITANIA

17

Figure 2: Localities for Mauritanian anurans occurring exclusively in the savannahs of the Sahel. See Fig. 1 for an explanation of Principal Components Analysis. All symbols for Ptychadena species are in blue because identifications in the literature are ambiguous.

18

PADIAL ET AL.

a

b

c

d

e

f

Figure 3: Representative localities occupied by anurans in Mauritania. (a) Guelta Toumbahjît (Adrar) supports relict populations of Amietophrynus xeros and Hoplobatrachus occipitalis. (b) Guelta Molomhar (Adrar), previously supported A. xeros and H. occipitalis but was found to be completely dry in March 2008 (see text). (c) Gabou Lake (Tagant) contains populations of A. xeros, H. occipitalis, Tomopterna cryptotis, and Kassina senegalensis. (d) Tâmoûrt Goungel (Hodh el Gharbi) where H. occipitalis, K. senegalensis, Ptychadena spp., and T. cryptotis are frequently found. (e) Mountainous areas of the Sahel south of Kiffa (Assaba), and Guelta Oumm Lebare where Ptychadena trinodis was found. (f) Tamourt Bougari (Assaba), a swamp inhabited by A. xeros and H. occipitalis, and probably Amietophrynus regularis, T. cryptotis, and K. senegalensis.

The major factor determining survival of Saharan amphibian populations is their capacity to resist episodic drought and their chance to experience occasional episodes of

populational connectivity during favourable years. Use of water by humans, especially for watering cattle, may increase the risk of local extirpation, especially during extremely dry

19

AMPHIBIAN CONSERVATION IN MAURITANIA

periods. The most effective conservation measure in this case is the provision of guidance for better management of water resources in oases, “wadis”, “gueltas”, and springs. Human populations have been historically living in close contact with anuran populations, and despite the intense droughts of the 1970s some amphibian populations survived. Nonetheless, human populations are increasingly relying on ground water for agriculture, including the raising of cattle, and for domestic use, which may eventually reduce the impact they may have had to date on some surface water.

Conservation measures for Saharan populations may be desirable because they present an ideal scenario for studying and testing hypotheses on effects of on-going environmental change on survival, local adaptation, and genetics of small and isolated populations. The Sahara Desert has probably suffered gradual xerification (with intermediate wet periods) since the Holocene, that, when considered along with more recent episodes of dramatic climatic change (GASSE, 2000; FOLEy et al., 2003), could be behind the current genetic and population structure of water-dependent organisms. Comparing the genetic structure of anurans in Saharan isolates with those of more continuously distributed populations in the Sahel should provide information about the role of population size, population dynamics, distance among populations, and time since separation, on the genetic structure of species in isolated populations. The current scenario available in Mauritania provides a perfect opportunity to study how population size, gene flow, speciesspecific characteristics, and environmental change affect local adaptation and extinction.

RECOMMENDATIONS A list of localities important to anurans in Mauritania is provided in Table 2. The conservation status and population trends of this fauna are currently unknown but we list the following series of actions that should lead to better understanding of the situation of amphibian populations and provide a frameTable 2: Important localities for anurans in Mauritania (coordinates in decimal degrees [WGS84 datum]).

Locality Wilaya Adrar Guelta Handoum Guelta Molomhar Guelta Toûngâd Iriji Kanoal, Oued Séguelil Terjît Toumbahjît Wilaya Assaba Aouînet Nanâga Bou Bleï'îne Bougari Guelta Oumm Lebare Guelta Metraucha Oumm Icheglâne Wilaya Brakna Aleg Wilaya Hodh Ech Chargui Mahmûdé Lake Wilaya Hodh El Gharbi Ain El Berbera Chegg el Mâleh source Guelb Samba Tâmchekket Tâmoûrt Goungel Wilaya Tagant Gabou Lake Guelta el Gheddiya El Housseînîya Guelta Fanar Guelta Garaouel Guelta Matmata Wilaya Trarza Diawling National Park

Coordinates

N20.323193 N20.580946 N20.061001 N20.516667 N20.303600 N20.252804 N20.236826

W13.142101 W13.136361 W13.132806 W13.050000 W13.197283 W13.088188 W13.004978

N17.152482 N17.126067 N16.546667 N16.579150 N16.538033 N17.070297

W12.199115 W10.990067 W10.792333 W10.704550 W10.741550 W12.207848

N17.053333 W13.916117 N16.499483 W7.715183 N16.691103 N16.515562 N16.654987 N17.249855 N16.403148

W9.716622 W10.452908 W9.707835 W10.667613 W9.559860

N18.260000 N17.834850 N17.737962 N18.015850 N17.451667 N17.887298

W12.360000 W11.557833 W12.245253 W12.174967 W12.394850 W12.110844

N16.440000 W16.340000

20

PADIAL ET AL.

work for defining future research and conservation priorities: (1) evaluate the status of Saharan isolates, especially the more vulnerable northern populations (i.e. Adrar and historical localities in Tiris zemmour), and extend field surveys to Saharan localities having a potential for supporting amphibian populations, e.g., Wilayas Assaba, Brakna, Guidimaka, Gorgol, Hodh El Gharbi, Hodh Ech Chargui, and Trarza in the Senegal basin and, especially, in the mountain ranges of Assaba and Gorgol in the Sahel, regions suspected of having the highest anuran diversity in Mauritania; (2) inventory amphibian populations, with special emphasis on exploration of poorly known areas (eastern Atar, Tagant, Tiris zemmour, and Hodh Ech Chargui), and provide resultant data regarding anuran distribution and diversity to national and international conservation agencies for use in future proposals regarding wildlife management and conservation; (3) conduct assessments of water quality and threats to populations, particularly in populations restricted to isolated montane pools; (4) from all populations collect tissue samples for molecular studies aimed at (a) assessing the effect of environmental change and population dynamics on genetic diversity and local extinction, (b) evaluate the phylogeographic structure of all anuran species present in Mauritania in order to identify large-scale patterns of genetic diversity, isolation, and gene flow, and (c) clarify the taxonomic status of Mauritanian populations through integration of Mauritanian samples into systematic studies of African anurans. In addition, a conservation measure that could potentially have an important impact on the conservation of amphibians would consist of the pro-

vision of guidance to local inhabitants for better management of water resources in oases, “wadis”, “gueltas”, and springs.

Acknowledgement José M. Padial received financial assistance for fieldwork from Asociación Amigos de Doñana; the drafting of this manuscript was made possible by a Gerstner Postdoctoral Fellowship through the Richard Gilder Graduate School of AMNH. José C. Brito’s work was supported by the Fundação para a Ciência e Tecnologia (Programme Ciência 2007), Portugal, by grants 7629-04 and 8412-08 from the National Geographic Society, and by project PTDC/BIABEC/099934/2008 (EU Programme COMPETE). Mark-Oliver Rödel critically read an earlier draft of the manuscript and kindly provided photographs.

REFERENCES BRITO, J.C.; MARTíNEz-FREIRíA, F.; SIERRA, P.; SILLERO, N. & TARROSO, P. (2011).

Crocodiles in the Sahara desert: an update of distribution, habitats and population status for conservation planning in Mauritania. PLoS ONE 6: e14734.

CAMPOS, J.C.; SILLERO, N. & BRITO J.C. (2012). Normalized Difference Water Indexes have dissimilar performances in detecting seasonal and permanent water in the Sahara-Sahel transition zone.

Journal of Hydrology 464-465: 438-446.

DEKEySER, P.L. & VILLIERS, A. (1956).

Contribution à l’étude du peuplement de la Mauritanie. Notations écologiques et biogéographiques sur la faune de l’Adrar.

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Mémoires de l’Institut Français d’Afrique Noire 44: 1-222.

DUMONT, H.J. (1982). Relict distribution patterns of aquatic animals: another tool in evaluating late Pleistocene climate changes in the Sahara and Sahel.

Palaeœcology of Africa 14: 1-24.

FOLEy, J.A.; COE, M.T.; SCHEFFER, M. & WANG, G. (2003). Regime shifts in the Sahara and Sahel: interactions between ecological and climatic systems in Northern Africa. Ecosystems 6: 524-539.

FROST, D.R. (2013). Amphibian Species of the World: an Online Reference. Version 5.6.

American Museum of Natural History; New york, USA. Available at http://research.amnh.org/herpetology/am phibia/index.html.

Retrieved on 01/09/2013.

GASSE, F. (2000). Hydrological changes in the African tropics since the last glacial maximum. Quaternary Science Reviews 19: 189-211.

IUCN (2013). The IUCN Red List of Threatened Species, v. 2013.2. International Union for Nature Conservation and Natural Resources, Gland, Switzerland.

Available at http://www.iucnredlist.org.

Retrieved on 02/03/2014.

LE HOUéROU, H.N. (1997). Climate, flora and fauna changes in the Sahara over the past 500 million years. Journal of Arid Environments 37: 619-647.

NATIONAL RESEARCH COUNCIL (1981).

Environmental Degradation in Mauritania. National Academy Press, Washington, DC, USA. NICKEL, H. (2003). Ökologische Untersuchungen zur Wirbeltierfauna im südöstlichen Mauretanien: zwei Fallstudien unter beson-

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derer Berücksichtigung der Krokodile.

Deutsche Gesellschaft für Technische zusammenarbeit, Eschborn, Germany.

PADIAL, J.M. (2006). Commented distributional list of the reptiles of Mauritania. Graellsia 62: 159-178.

PADIAL, J.M. & DE LA RIVA, I. (2004).

Annotated checklist of the amphibians of Mauritania (West Africa). Revista Española de Herpetología 18: 89-99.

PICKERSGILL, M. (2007). Frog search. Results of expeditions to southern and eastern Africa from 1993-1999. Frankfurt Contributions to Natural History 28: 1-575.

PLEGUEzUELOS, J.M.; BRITO, J.C.; FAHD, S.; FERICHE, M.; MATEO, J.A.; MORENORUEDA, G.; REQUES, R. & SANTOS, X. (2010). Setting conservation priorities for the Moroccan herpetofauna: the utility of regional red listing. Oryx 44: 501-508.

RöDEL, M.-O. (2000). Herpetofauna of West Africa, Vol. I: Amphibians of the West African Savanna. Edition Chimaira, Frankfurt am Main, Germany.

RöDEL, M.-O.; BOATENG, C.O.; PENNER, J. & HILLERS, A. (2009). A new cryptic Phrynobatrachus species (Amphibia: Anura: Phrynobatrachidae) from Ghana, West Africa. Zootaxa 1970: 52-62.

STUART, S.N.; CHANSON, J.S.; COX, N.A.; yOUNG, B.E.; RODRIGUES, A.S.L.; FISCHMAN, D.L. & WALLER, R.W. (2004). Status and trends of amphibian declines and extinctions worldwide.

Science 306: 1783-1786.

TRAPE, S. (2009). Impact of climate change on the relict tropical fish fauna of Central Sahara: threat for the survival of Adrar mountains fishes, Mauritania. PLoS ONE 4: e4400.

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VALE, C.G.; ร LVARES, F. & BRITO, J.C. (2012).

Distribution, suitable areas and conservation status of the Felou gundi (Felovia vae Lataste 1886). Mammalia 76: 201-207.

VASCONCELOS , R.; F ROUFE , E.; B RITO , J.C.; C ARRANzA , S. & H ARRIS , D.J. (2010). Phylogeography of the African common toad, Amietophrynus regularis, based on mitochondrial DNA sequences: inferences regarding the Cape Verde population and biogeo-

graphical patterns. African Zoology 45: 291-298.

VENCES, M.; KOSUCH, J.; RรถDEL, M.-O.; LรถTTERS, S.; CHANNING, A.; GLAW, F. & BรถHME, W. (2004). Phylogeography of Ptychadena mascareniensis suggests transoceanic dispersal in a widespread African-Malagasy frog lineage. Journal of Biogeography 31: 593-601.

WARD, D. (2009). The Biology of Deserts.

Oxford University Press, New york, USA.

Basic and Applied Herpetology 27 (2013): 23-50

Chapter 25 Amphibians of Morocco, including Western Sahara: a status report Ricardo Reques1,*, Juan M. Pleguezuelos2, Stephen D. Busack3, Philip de Pous4 Departamento de Ecología Evolutiva, Estación Biológica de Doñana, Sevilla, Spain.

Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Granada, Spain.

3 North Carolina Museum of Natural Sciences, Raleigh, North Carolina, USA. 4 Faculty of Life Sciences and Engineering, Departament de Producció Animal (Fauna Silvestre), Universitat de Lleida, Lleida, Spain.

1 2

* Correspondence: Departamento de Ecología Evolutiva, Estación Biológica de Doñana, Cl. Americo Vespucio, s/n, 41092, Isla de la Cartuja, E-41092 Sevilla, Spain. Phone: +34 616810551, Email: reques@telefonica.net

Received: 10 January 2013; received in revised form: 30 September 2013; accepted: 21 October 2013.

Morocco has one of the highest rates (28.6%) of amphibian endemism among countries bordering the Mediterranean Sea and, while large areas of Morocco are crucial for conserving amphibian biodiversity, some areas are not afforded legal protection. We examine biodiversity, identify immediate anthropogenic threats, discuss critical habitat for the conservation of amphibian diversity and the role of currently protected areas in meeting conservation goals within Morocco, Western Sahara included. The study area harbours 14 amphibian species, eight of which are assigned to the categories of Endangered (Pelobates varaldii), Vulnerable (Salamandra algira, Amietophrynus xeros, and Hoplobatrachus occipitalis) or Near Threatened (Pleurodeles waltl, Alytes maurus, Bufo spinosus, and Barbarophryne brongersmai) using IUCN criteria at the regional level of the study area.

Habitat loss and degradation due to conversion of land for agriculture, urbanization, or industry are major threats, but infrastructure for tourism, freshwater pollution by chemicals, introduction of non-native species to aquatic ecosystems (Gambusia holbrooki), pathogens (Batrachochytrium dendrobatidis), road-kills, and natural disasters (drought), are also rapidly increasing threats. In addition, consequences from global warming must also be considered. The present Conservation Area Network (CAN) does not include distributional ranges of some amphibian species, and a more complete CAN in Atlantic and desert areas is suggested. The northwestern Atlantic, Rif-Middle Atlas, Central Atlantic, and Tiris regions should be considered priorities for conservation because of amphibian endemism and/or the existence of isolated amphibian populations.

Key words: amphibian decline; conservation planning; Morocco; survival threats; Western Sahara.

Los anfibios de Marruecos, incluyendo Sáhara Occidental: Informe sobre su situación. Marruecos posee una de las tasas más elevadas de anfibios endémicos (28.6%) entre los países de la cuenca mediterránea y, a pesar de que extensas áreas de Marruecos son fundamentales para la conservación de la biodiversidad de anfibios, otras zonas no gozan de protección legal. En este estudio examinamos la biodiversidad, identificamos las amenazas antropogénicas más inmediatas y discutimos el hábitat crítico para la conservación de la diversidad de anfibios y el papel de las áreas actualmente protegidas en el cumplimiento de los objetivos de conservación en Marruecos, Sáhara Occidental incluido. El área de estudio alberga 14 especies de anfibios, ocho de las cuales se asignan a las categorías de En Peligro (Pelobates varaldii), Vulnerable (Salamandra algira, Amietophrynus xeros y Hoplobatrachus occipitalis) o Casi Amenazada (Pleurodeles waltl, Alytes maurus, Bufo spinosus y Barbarophryne brongersmai), utilizando criterios de la UICN a nivel regional en la zona de estudio. La pérdida de hábitat y la degradación debido a la conversión de terrenos para la agricultura, urbanismo o industria son las principales amenazas, pero las infraestructuras relacionadas con el turismo, la contaminación de agua dulce por productos químicos, la introducción de especies exóticas en los ecosistemas acuáticos (Gambusia holbrooki), la llegada de patógenos (Batrachochytrium dendrobatidis), los atropellos y los desastres naturales (sequía), también son amenazas en rápido aumento. Del mismo modo, también deben tenerse en cuenta las consecuencias del calentamiento global. La actual Red de Áreas de Conservación (CAN) no incluye ranThis chapter should be cited as: Reques R., Pleguezuelos J.M., Busack S.D. & de Pous, P. (2013). Amphibians of Morocco, including Western Sahara: A Status Report. Chapter 25 in Part 2. Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 23-50. DOI: http://dx.doi.org/10.11160/bah.13003/

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REQUES ET AL.

gos de distribución de algunas de las especies de anfibios, por lo que se sugiere una red de conservación más completa incluyendo zonas del Atlántico y el desierto. Las regiones del Atlántico Noroeste, Rif-Atlas Medio, Atlántico Centro y Tiris deben ser consideradas prioridades de conservación debido a los endemismos presentes y/o la existencia de poblaciones aisladas de anfibios.

Key words: amenazas para la supervivencia; declive de anfibios; Marruecos; planificación de conservación, Sáhara Occidental.

Morocco (including Western Sahara), with an area of 705 850 km2, is biogeographically within the Maghreb. In the north, mild and wet winters alternate with long, hot and increasingly dry summers as one progresses southward and eastward. Annual rainfall averages 950 mm in the north (Tangier), 430 mm along the Atlantic Coast (Casablanca), and less than 100 mm in most of the Western Sahara.

Four mountain ranges, the Rif (Jebel Tidighine, 2456 m), the Middle Atlas (Jebel Bou Naceur, 3356 m), the High Atlas (Jebel Toubkal, the highest peak in North Africa at 4167 m) and the Anti-Atlas (Jebel Siroua, 3304 m) traverse the country from north to south. The Sahara Desert begins south of the Anti-Atlas and High Atlas and extends east for more than 800 km and south for more than 1000 km to 21º N latitude.

Morocco probably has the most complete dataset regarding amphibian distribution and status across northern Africa, and BONS & GENIEz (1996), SCHLEICH et al. (1996), MATEO et al. (2003), and GENIEz et al. (2004) have been relied upon heavily for summaries of distribution and habitat preferences. While this manuscript was in review BEUKEMA et al.

(2013) described a third subspecies within Salamandra algira (S. a. splendens) and provided natural history data separately for the three Moroccan subspecies; supplemental natural history data for other amphibian taxa are also provided throughout this paper.

Morocco has only 14 of Africa’s 993 amphibian species (Table 1) (IUCN, 2009).

One of these species, Pelobates varaldii, is endemic but three other species, Discoglossus scovazzi, Alytes maurus, and Barbarophryne brongersmai, may be considered quasi-endemic because most of their distributional area is within Morocco and only isolated populations are known from within Algeria. Morocco, therefore, has almost exclusive responsibility for global Table 1: Moroccan amphibian species.

CAUDATA Salamandridae Pleurodeles waltl Michahelles, 1830 Salamandra algira Bedriaga, 1883 ANURA Alytidae Alytes maurus Pasteur and Bons, 1962 Discoglossus pictus Otth, 1837 Discoglossus scovazzi Camerano, 1878 Pelobatidae Pelobates varaldii Pasteur and Bons, 1959 Hylidae Hyla meridionalis Böttger, 1874 Bufonidae Amietophrynus mauritanicus (Schlegel, 1841) Amietophrynus xeros (Tandy, Tandy, Keith and Duff-Mackay, 1976) Bufotes boulengeri Lataste, 1879 Barbarophryne brongersmai (Hoogmoed, 1972) Bufo spinosus Daudin, 1803 Dicroglossidae Hoplobatrachus occipitalis (Günther, 1858) Ranidae Pelophylax saharicus (Boulenger, 1913)

25

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

conservation of these four amphibians.

Proximity to the Iberian Peninsula has provided Morocco with the greatest European influence on its amphibian fauna among all African countries; two species (Pleurodeles waltl and Bufo spinosus) and some genera (Salamandra, Discoglossus, Alytes, Pelobates, Pelophylax) are of European origin. Because of greater habitat diversity, higher rainfall, and lower rates of evaporation, amphibian species richness is highest in the north while large areas within the Sahara lack amphibians (BAHA EL DIN et al., 2008).

The global conservation status of Moroccan amphibians has been assessed quite recently (Table 2; see also COX et al., 2006) and while large areas of Morocco are crucial to conserving amphibian biodiversity (Table 3), many significant areas are not afforded legal protection (RONDININI et al., 2006; DE POUS et al., 2011).

Threatened amphibian species and populations are found in southern desert and savannah, and

Table 2: Red List status (IUCN categories) for amphibians of Morocco (PLEGUEzUELOS et al., 2010). CR=Critically Endangered; EN=Endangered; VU=Vulnerable; NT=Near Threatened; LC=Low Concern; NSp=number of species; End=number of endemic species; for comparative purposes global data for the amphibians of the Mediterranean Basin are included (COX et al., 2006).

CR EN VU NT LC NSp End Morocco, Anura 1 Morocco, Caudata Morocco, Amphibia 1 Mediterranean, Amphibia 2 13

2 1 3 13

3 6 12 1 1 2 0 4 6 14 1 17 61 106 68

in northern wetlands and mountains, but these habitat types are not always well-represented in the current Conservation Area Network (CAN, MINISTèRE DE L’AGRICULTURE, 1994).

Currently, no amphibian species is legally protected in Morocco.

Table 3: Precipitation and attributes of the distributional ranges of amphibians in Morocco (including Western Sahara). See text for procedure.

Species

Alytes maurus Amietophrynus mauritanicus Amietophrynus xeros Barbarophryne brongersmai Bufo spinosus Bufotes boulengeri Discoglossus pictus Discoglossus scovazzi Hoplobatrachus occipitalis Hyla meridionalis Pelobates varaldii Pelophylax saharicus Pleurodeles waltl Salamandra algira All Species Morocco

Range within Percentage of global Morocco (km2) range within Morocco 5 500 395 300 12 300 95 100 183 200 438 600 5 300 190 600 525 240 900 7 000 398 300 60 500 10 800

~95 47.88 0.21 ~ 95 1.16 22.44 2.22 ~ 95 0.01 31.67 100 28.21 14.11 48.74

Minimum

Precipitation Maximum

700 < 100

> 2000 2000

250 500 250 150 350

600 > 2000 > 2000 600 2000

300 600 < 100 500 800

2000 800 2000 2000 > 2000

Mean 995.7 466.1 < 100 293.7 541.9 441.9 270.6 614.9 < 100 580.8 710.7 463.7 733.2 943.9 441.8 413.1

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Figure 1: Major habitats utilized by amphibians at the regional level (from PLEGUEzUELOS et al., 2010).

In the following pages amphibian biodiversity in Morocco is examined, the most important habitats (Fig. 1) and the role of protected areas are discussed, and immediate threats to this biodiversity are identified. It is hoped that this information will assist environmental and conservation planning in Morocco by identifying non-random threats to diversity in terms of speciesâ&#x20AC;&#x2122; associations or ecological preferences.

In addition, this treatment provides important information on a group of terrestrial vertebrates under-represented in the CAN of most countries and frequently neglected in conservation policy (MILNER-GULLAND et al., 2006).

IUCN RED LIST STATUS OF MOROCCAN AMPHIBIANS (2009) Endangered Pelobates varaldii: The Moroccan spadefoot toad (Fig. 2a), an endemic, is locally distributed within the northwestern coastal plain among cork oak and other forested habitat and in areas

of uncultivated sandy soil next to temporary ponds; DE POUS et al. (2012) provided 134 georeferenced localities. Spawning sites are ephemeral ponds and dayas (Fig. 3a); modified habitats are avoided, and it is the most stenoecious Moroccan amphibian (BEUKEMA et al., 2013).

The northernmost locality is a small, forested area just south of the Tangier airport, easternmost localities are Khemisset and south of Ouezzane, and the southernmost locality is in the vicinity of Oualidia. Suitable areas for this species along most of the Moroccan Atlantic coastline, into the Souss Valley and southwards, and discontinuously along the Mediterranean coast east to the Algerian border, potentially do exist.

ESCORIzA & BEN HASSINE (2013) have reported a newly-discovered population of Pelobates varaldii, represented by a tadpole from one of 21 ponds surveyed in March 2013, in the Ben Slimane region. They suggest this population likely demonstrates the relictual nature currently found in a formerly continuous distribution through northern Moroccoâ&#x20AC;&#x2122;s Atlantic coastal plain.

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

a

b

c

d

e

f

27

Figure 2: Portraits of some Moroccan amphibians: (a) Pelobates varaldii (Mamora cork oak forest). (b) Salamandra algira (yebel Musa). (c) Alytes maurus (Chefchaouen). (d) Discoglossus scovazzi (Beni Snassene). (e) Amietophrynus xeros (Atar, Mauritania). (f) Bufotes boulengeri (Aïn Leuh). Photo credits: (a) P. de Pous, (b) S. yubero, (c) S.D. Busack, (d) R. Reques and (e & f) J.M. Pleguezuelos.

Current major threats to survival derive from loss and degradation of habitat due to conversion of suitable land to pasture for, and water pollution by, livestock. Survival is contingent upon sandy soil, and industrial farming is expanding into coastal areas (DE POUS et al., 2012). Populations are often restricted to temporal ponds where hydroperiods may not be sufficient for completion of larval development (developmental period is unstudied, but is dependent upon water depth, temperature, and availability of food; four to six months is likely). Tadpoles remaining in permanent bodies of water are disappearing because of introduced predatory fish (Gambusia holbrooki; see also SALVADOR, 1996 and STUART et al., 2008) and sudden draining during the larval period. Additional discovery (November 2008, DE POUS et al., 2012) of an indeterminate species of Procambarus (photographic documentation is suggestive of P. [Ortmannicus]

lophotus rather than P. clarkii [fide John Cooper, North Carolina State Museum, in litt., October 2010]) in a pond east of Larache (35.08122°N, 6.06908°W) signals an additional threat to this and other species. Invasive crayfish present an increasingly serious threat to aquatic organisms, including amphibian larvae, wherever they become established (COOPER & ARMSTRONG, 2007).

Batrachochytrium dendrobatidis, a globally distributed fungus responsible for chytridiomycosis and mass mortality among amphibians worldwide (HEATWOLE, 2013), has recently been reported from P. varaldii in Morocco. One of ten larvae sampled in April 2009, from ± 20.5 km SE Larache (35.038110°N, 6.029248°W) demonstrated a 0.4-genome equivalent infection intensity of this pathogen (EL MOUDEN et al., 2011). This finding, while suggesting a low prevalence of infection, warrants additional investigation. Populations of

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a

b

c

d

e

f

g

h

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

these amphibians are decreasing and there is urgent need for conservation and management; additional protected areas within its current range, coupled with management actions for conservation, are needed to mitigate continued population reduction.

The Evolutionary Distinct and Globally Endangered (EDGE) program at the zoological Society of London (http://www.edgeofexistence. org/) recently listed P. varaldii at number 36 on their global amphibian top 100.

Vulnerable Salamandra algira: The range of the North African fire salamander (Fig. 2b) is widely fragmented throughout northern, rather wet, mountain ranges in Morocco and Ceuta, Spain (MARTíNEz et al., 1997; ESCORIzA et al., 2006; BOGAERTS et al., 2007; ESCORIzA & COMAS, 2007; BEUKEMA et al., 2010, 2013). Recent morphological, genetic, and ecological studies suggest that there are different genotypes and phenotypes with parapatric distributions within Moroccan Salamandra, and further taxonomic study is

Figure 3: Habitats for some of Morocco’s amphibian species. (a) Nufar pool, Kasr-el-Kebir; P. varaldii. (b) Stream, Talassemtane, Bab Taza; S. algira, A. maurus, and B. spinosus. (c) Temporary pond, Asilah.

Breeding habitat, P. waltl. (d) Urban habitat, Chefchaouen, S. algira, A. maurus, D. scovazzi, and P. saharicus. (e) Spur of the Anti-Atlas, west of Agdz; B. brongersmai. (f ) Lanasser pool, Rif Mountains, H. meridionalis, A. mauritanicus, and P. saharicus. (g) Fort Bou Cherif, B. boulengeri. (h) Dayet Sjri, Merzouga, Tafilalt, A. mauritanicus.

Photo credits: (a) D. Donaire, (b & f ) R. Reques, (c & d) S.D. Busack, (e, g, & h) J.M. Pleguezuelos.

29

warranted (STEINFARTz et al., 2000; DUBOIS & RAFFAëLLI, 2009; BEUKEMA et al., 2010, 2013). Salamandra algira populations occurring within the Rif and northern border of the Middle Atlas have been partitioned into two subspecies, S. a. splendens Beukema, de Pous, Donaire-Barroso, Bogaerts, GarciaPorta, Escoriza, Arribas, El Mouden & Carranza 2013 and S. a. tangitana DonaireBarroso & Bogaerts 2003. Some populations of Salamandra are ovoviviparous (DONAIREBARROSO & BOGAERTS, 2003a; BEUKEMA et al., 2013). Viviparous populations from the Tingitane Peninsula have also been proposed for species status (as S. tingitana; DUBOIS & RAFFAëLLI, 2009). The population in Beni Snassen is assigned to S. algira spelaea, which is more related to the Algerian populations.

The species is locally common in the western and central Rif Mountains as well as in the Middle Atlas (FAHD et al., 2006; BEUKEMA et al., 2010, 2013), in habitat associated with humid, montane areas of Atlas Cedar (Cedrus atlantica), Pyrenean Oak (Quercus pyrenaica), and mixed forest (Abies, Cedrus, Pinus, and Quercus) with an abundance of montane streams (MARTíNEz-MEDINA, 2001) (Fig. 3b), and has been cited in caves (AELLEN, 1951; DONAIRE BARROSO & BOGAERTS, 2001). Salamandra algira occurs between 100 and 2100 m above sea level.

Populations are threatened by habitat loss due to the agriculture of Cannabis sativa in the Rif, deforestation, alteration and channelization of water, overgrazing by livestock throughout its range and, locally, by road-kill (TAIQUI, 1997; TAIQUI & MARTíNCANTARINO, 1997). The pet trade, climatic change, and the chytrid fungus are emerging concerns (BOGAERTS, 2007).

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Near Threatened Pleurodeles waltl: The Sharp-ribbed newt is distributed mainly throughout the coastal plain of northwestern Morocco (GARCíA-PARIS et al., 2004; BEUKEMA et al., 2013) within a roughly triangular area connecting the Tingitane Peninsula, Souk Jemaa des Oulad Abbou, and Anosseur, but three recorded localities (Talamrhecht, Safi, Île d'Mogador) fall outside this area. In general, P. waltl inhabits ponds, lakes, ditches, and slow-moving streams with non-permanent water (Fig. 3c) and adjusts to habitat modified by cultivation (BEUKEMA et al., 2013); populations are quite fragmented and are declining throughout the country (BEJA et al., 2009).

This species is Near Threatened because of a general decline in population numbers (almost 30% over ten years) and widespread loss of habitat (BEJA et al., 2009). Main threats to survival are agrochemical pollution and eutrophication caused by livestock, loss of aquatic habitat through drainage, and loss and fragmentation of terrestrial habitats (BAHA EL DIN et al., 2008).

Alytes maurus: The Moroccan midwife toad (Fig. 2c) is often found in association with larvae-bearing populations of S. algira (DONAIRE-BARROSO et al., 2006; BEUKEMA et al., 2013). It has a discontinuous distribution throughout humid areas in montane-karst and forested areas (mainly Q. pyrenaica) close to water sources in the western and central Rif Mountains (Fig. 3b) between 200 and 2050 m above sea level (Jebel Tazekka) (see DE POUS et al., 2013). Its distribution in the Middle Atlas is poorly known (LIBIS, 1985; DONAIRE-BARROSO et al., 2006). A recent

genetic analysis shows that A. maurus presents low levels of mtDNA variability with no clear geographical structuring (DE POUS et al., 2013). Its current, fragmented range is likely a result of increasing temperatures throughout the Quaternary, as a fossil record likely attributable to A. maurus suggests a much wider historical distribution (BEUKEMA et al., 2013; DE POUS et al., 2013).

Populations in the Chefchaouen district are threatened by pollution due to human activity (Fig. 3d) and by introduction of the invasive Eastern mosquito fish (Gambusia holbrooki) (DONAIRE-BARROSO et al., 2009a).

In the Middle Atlas some breeding localities in the Jebel Bou Iblane region are within protected areas (site of bio-ecological interest, priority 1) but pressure from cattle grazing, deforestation, canalization of mountainwater, and soil erosion are increasing threats outside of protected areas (DONAIREBARROSO et al., 2006). Additional threats to this species include the potential spread of recently detected chytrid fungus (EL MOUDEN et al., 2011) as well as the effects of climatic change. Due to its reduced distribution (about 30 known localities in an area of less than 5000 km2), the species has been listed as Near Threatened (DONAIRE-BARROSO et al., 2009a).

Barbarophryne brongersmai: The genus Barbarophryne was recently published (BEUKEMA et al., 2013) to reduce polyphyly within the “green toad group” by removing this species from the genera Bufo, Bufotes, or Pseudepidalea to which it has been variously assigned. Brongersma’s toad is found from 5 m to 1000 m above sea level in suitable habitat south of Casablanca (HOOGMOED, 1972;

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

GENIEz et al., 2000; BEUKEMA et al., 2013) where it inhabits semiarid areas of Argania spinosa, Euphorbia, grass-like vegetation, and ploughed fields. Temporary ponds where it breeds are generally located in rocky areas (Fig. 3e), and the species has been observed in artificial bodies of water (GARCíA-MUñOz et al., 2009). It is threatened by increased aridity and pollution and drainage of breeding habitat throughout much of its range.

Although present in the Parc National de Souss-Massa, the species is probably in decline, and at a loss rate of almost 30% over ten years makes it close to qualifying for Vulnerable status (SALVADOR et al., 2006).

Populations in the Souss Valley, Ifni, and Low Draa and Tekna regions, and those in northern Western Sahara, are being negatively affected by the proliferation of cisterns being built to water cattle. Toads, attracted by the humidity, fall into these underground cisterns and die when these watering structures dry up (GARCíA-MUñOz et al., 2009).

One-meter-deep decantation chambers linked to these cisterns are frequently used by breeding toads and, while post-metamorphic toads can probably climb the vertical walls, adults are less likely to escape in this manner (L. García-Cardenete, personal communication).

Least Concern Discoglossus scovazzi: The white-bellied painted frog (Fig. 2d) inhabits suitable habitat in Morocco and the Spanish territory of Ceuta at elevations from near sea level to 2650 m above sea level in the High Atlas Mountains (see Fig 9 in BEUKEMA et al., 2013) (DUBOIS, 1982; MARTíNEz-MEDINA,

31

2001; zANGARI et al., 2006). Abundant in sub-humid and humid bioclimatic zones, but also in semiarid zones around Casablanca, this frog inhabits temporal and ephemeral ponds of fresh or slightly brackish water and montane streams (BEUKEMA et al., 2013).

Localized loss of breeding sites through agricultural development in inland areas and increasing salinity in lagoons are the main threats (SALVADOR et al., 2009); it is presumed that the species can resist light modification of its habitat by deforestation.

Chytrid fungus, B. dendrobatidis, recently has been reported from D. scovazzi at two localities in Tétouan Préfecture. One metamorphic individual sampled in November, 2006, from Agnane (near Tétouan at 35.535881°N, 5.386177°W) presented an infection intensity of 29.9 genome equivalents and one adult sampled in February, 2007, approximately 18.5 km SE Larache (35.043940°N, 6.046156°W) presented an infection intensity of 60.3 genome equivalents (EL MOUDEN et al., 2011). Additional research regarding the actual extent of the distribution of this fungus is of paramount importance.

Discoglossus pictus: The western limit of distribution for the common painted frog is unclear. In Morocco apparently it is limited to a strip from the Cap des Trois Fourches Peninsula (Melilla included) to Morocco’s northern border with Algeria and possibly extending westward beyond the Moulouya Basin (BEUKEMA et al., 2013). It breeds in most types of still water, including temporal ponds, marshes, and brackish water. Habitat alteration, including changes in traditional land-use and urbanization (BOSCH et al., 2009), is its principal threat.

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Hyla meridionalis: Mediterranean treefrogs are widely distributed throughout the western Mediterranean (TEJEDO & REQUES, 2002); northern Mediterranean locations appear to have been colonized recently from Africa (RECUERO et al., 2007; but see STöCK et al., 2012). Widespread in Morocco from coastal wetlands to montane habitats, it inhabits most areas adjacent to still or moving water (Fig. 3f); current gaps in its apparent range in many parts of northeastern Morocco and the Middle-Atlas and High Atlas are likely due to a lack of distributional research (BEUKEMA et al., 2013). Loss of terrestrial and aquatic habitats is the major threat, but populations remain locally abundant. One of ten H. meridionalis larvae sampled in April, 2009, approximately 18.5 km SE Larache (Tétouan Préfecture; 35.043940°N, 6.046156°W) demonstrated a 395.9 genome equivalent infection intensity of the fungus B. dendrobatidis (EL MOUDEN et al., 2011).

tus based on mitochondrial DNA (see STöCK et al., 2006, 2008; BEUKEMA et al., 2013).

Inhabiting forested areas, shrubland, dry grassland, semi-desert, and desert at elevations from near sea level to 2670 m above sea level (Fig. 3g), Boulenger’s toad is one of the most widespread amphibians in Morocco. The main threat facing the species appears to be loss of breeding habitat through drainage of wetlands, management of natural water sources, and water pollution (IUCN, 2006). In the southern belt of its Moroccan distribution B. boulengeri is the species most likely to die inside modern underground cisterns built for watering cattle (L. GarcíaCardenete, personal communication).

Amietophrynus xeros: The desert toad (Fig. 2e) has been recorded from the extreme south of Western Sahara. The population found in temporal pools at Aouadi, a well close to Wadi Aïn Ascaf, is probably relictual and adversely impacted by regional drought; in areas near and within Adrar Atar (Mauritania) the species is always present around natural, temporal, small reservoirs. Listed as Least Concern at the global level, at the regional level of Morocco it could be considered Vulnerable (PLEGUEzUELOS et al., 2010).

Bufo spinosus: The common toad is a European species with genetically distinct relictual populations in Morocco (GARCíAPORTA et al., 2012). Isolated populations are found along Mediterranean mountains and in other mountains except the Anti-Atlas (FAHD et al., 2006; BEUKEMA et al., 2013). It inhabits very humid areas near permanent water, mostly in mountainous regions (Fig. 3b), and attains an elevation of 2750 m on Jebel Tinergouet in the High Atlas. Populations might be locally impacted by deforestation, water pollution, and draining of traditional breeding places (IUCN, 2006). While not threatened at the global level (AGASyAN et al., 2009), at the regional level of Morocco it can be considered Near Threatened (PLEGUEzUELOS et al., 2010).

Bufotes boulengeri: Previously considered a member of the Palearctic green toad complex as Bufo viridis, this toad (Fig. 2f) has been recently reassigned independent species sta-

Amietophrynus mauritanicus: The Mauritanian toad is a Maghrebian endemic with a wide distribution from the northern Sahara Desert to the Mediterranean coast, but its presence

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

in Western Sahara is unconfirmed (DONAIREBARROSO et al., 2009b). It frequents nearly any water source (Figs. 3f, 3h), including temporary ponds used for crops or cattle at elevations from sea level to 2650 m above sea level in the High Atlas (DUBOIS, 1982). This may be the most abundant and widely distributed amphibian in Morocco and it currently does not require conservation action.

Some populations, however, are affected by habitat loss and casualties due to motor vehicles (FAHD et al., 2002) and, attracted by humidity, some individuals die inside underground cisterns in the southern limit of its Moroccan distribution (J.M. Pleguezuelos, personal observation).

Hoplobatrachus occipitalis: The groovecrowned bullfrog, widely distributed further south in Africa, recently has been found in Western Sahara. Known only from the southwestern margin of Western Sahara (GleĂŻb Ladjir) it survives in temporary ponds of fresh water in regions with a Sahelian climate.

The principal threat to Western Saharan populations is its dependence on water; at the regional level of Morocco it could be considered Vulnerable (PLEGUEzUELOS et al., 2010).

Pelophylax saharicus: Populations of the Saharan green frog are generally widespread in Morocco from sea level to 2670 m above sea level in the Middle Atlas but fragmented in the desert because of patchy availability of habitat (oases). Locally abundant where wetland habitat exists, P. saharicus is one of the most commonly recorded amphibians in Morocco. An aquatic species that inhabits irrigation ditches, ponds, springs, rivers, and temporary pools, and with high tolerance to

33

alteration of its habitat (Figs. 3d, 3g), this species is presumed to have no major threats to survival. Survival, in fact, appears assisted in some regions by artificial ponds installed for agricultural purposes.

ECOLOGICAL

FACTORS AFFECTING

DISTRIBUTION

Understanding environmental factors and ecological requirements for survival of amphibian populations is key to developing management strategies for conservation (SEMLITSCH & ROTHERMEL, 2003).

Amphibian species richness is influenced by latitude within Africa, with maximum values at the Equator and minimum values at northern and southern continental extremes (RONDININI et al., 2006). Other factors accounting for African amphibian richness are the presence of suitable breeding places, rainfall, and terrestrial habitats used during nonbreeding periods; below we review these factors within Morocco.

With the exception of the ovoviviparous S. a. tingitana in mountains north and west of TĂŠtouan (DONAIRE BARROSO & BOGAERTS, 2001; BEUKEMA et al., 2010), the presence of every native species is contingent upon aquatic habitat for larval development. Mediterranean wetlands and other suitable breeding areas are highly temporal and unpredictable, and Morocco has suffered considerable degradation and loss of wetlands (RAMDANI et al., 2009); ecological monitoring of 24 wetlands and adjacent habitat (4529 ha) recorded a shrinkage in area of 25% from 1978 to 1999 (MORGAN, 1982; BIRKS et al., 2001; RAMDANI et al., 2001; GREEN et al., 2002). Oligohaline ponds (along the Atlantic coast), montane lakes (in the

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Middle Atlas) and temporal wetlands (both in Saharan and coastal areas), habitats considered most threatened, are precisely the habitats most important for amphibian reproduction.

Degradation resulting from hydrological alteration (in Atlantic plains), siltation (in some eastern semiarid areas), pollution by cattle and domestic sources (mainly in Atlantic plains) via processes very similar to those which have occurred in southern Spain (GREEN et al., 2002; REQUES, 2009) are common, yet only 10 of 47 wetlands with areas greater than two hectares surveyed between 1997 and 1999 by GREEN et al.

(2002) have been provided legal protection.

Alteration or loss of pools, streams, and gullies suitable for amphibian reproduction frequently goes unnoticed because of the small size and temporal character of these areas (OERTLI et al., 2005; REQUES, 2009) yet temporary wetlands with extended hydroperiods facilitate breeding success for most amphibians (PECHMANN et al., 1989; ROWE & DUNSON, 1995; WEyRAUCH & GRUBB, 2004).

Permanent wetland habitat is threatened by frequent introduction of non-native species (mainly fish) that feed upon amphibian eggs

Figure 4: Amphibian species richness in relation to rainfall classes. See text for data collection protocol.

and tadpoles (STUART et al., 2004), and desiccation of temporal pools results in loss of eggs and tadpoles (PECHMANN et al., 1991) in amphibian populations in arid regions (SEMLITSCH et al., 1996; BEJA & ALCAzAR, 2003). In general, all habitat modification reducing hydroperiod in breeding areas affects survival of amphibian populations.

Annual rainfall influences distribution and abundance (BORKIN, 1999) and in Morocco annual average rainfall is approximately 400 mm for most of the country, increasing to between 1500 mm and 2000 mm in northern mountains and decreasing to about 50 mm in the Sahara. Data on rainfall were obtained from GLOBCOVER (2008; full resolution mode, spatial resolution of 300 m), amphibian distributional data were obtained from the Global Amphibian Assessment (IUCN, 2006) and both datasets were entered into ArcGIS 9.2速 (ENVIRONMENTAL SySTEMS RESEARCH INSTITUTE, 2006) to obtain precipitation ranges and means for distributional areas of the 14 species in Morocco. As the boundaries between D. pictus and D. scovazzi are currently not clear (see Fig. 9 in BEUKEMA et al. 2013), we deal with this uncertainty by considering all populations of painted frogs from Cap des Trois Fourches Peninsula east to Algeria (including the Beni Snassen) as D. pictus. Most species are distributed throughout northern and western Morocco in localities where annual precipitation ranges between 400 mm and 1000 mm. Only two species, H. occipitalis and A. xeros in the extreme south, are found in localities with an annual rainfall of less than 150 mm. Together with A. mauritanicus, B. boulengeri, B. brongersmai, and P. saharicus, these species represent the only Moroccan species inhabiting the desert. At the opposite

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

extreme, S. algira and A. maurus inhabit areas with an annual precipitation greater than 600 mm (DONAIRE-BARROSO & BOGAERTS, 2003b) (Table 3, Fig. 4).

With the exception of P. saharicus and most populations of P. waltl, Moroccan amphibians can be considered terrestrial, and that is significant for conservation. Little is known about microhabitat use by most Moroccan amphibians (but see EL HAMOUMI et al., 2007; DE POUS et al., 2012; BEUKEMA et al., 2013) and any analysis must be performed within the framework of major habitats. Landscape ecology can highlight relationships among species and landscapes, follow shifts in relationships through time, and monitor the influence of anthropogenic changes in the landscape (NAUGLE et al., 2005). Data on the distributional area of major habitat types within the range of each species were obtained from GLOBCOVER (2008; see above), and the frequency of habitat use for each amphibian species analyzed by correspondence analysis (STATSOFT, 2001), which allowed assessment of relationships between landscape variables and amphibian species (P茅REz-L贸PEz, 2005) (Fig. 5). Hoplobatrachus occipitalis and A. xeros, associated with barren areas typical of desert regions, were again identified as isolated from the remaining species. At the opposite extreme were A. maurus and S. algira, both of which occur in forested or shrubland areas of northern Morocco. Other associations of conservation interest were those of P. varaldii with P. waltl, and of D. scovazzi and/or D. pictus with H. meridionalis.

Anurans of the genera Bufo, Bufotes, Barbarophryne, and Pelophylax utilized the landscape in an eclectic manner.

35

Figure 5: Correspondence between amphibian distribution and habitat type. Rc = Rainfed croplands; Ba =Bare areas; Mo1 = Mosaic cropland, 50-70% vegetation/20-50% grassland-shrubland-forest; Mo2 = Mosaic vegetation, 50-70% grasslandshrubland-forest/20-50% cropland; Co: Closed to open, >15% broadleaved or needle-leaved evergreen or deciduous, <5m shrubland; Sp = Sparse, <15% vegetation; Ot= Other. Data from GlobCover dataset (GLOBCOVER, 2008). Alymau = Alytes maurus; Amimau = Amietophrynus mauritanicus; Amixe = Amietophrynus xeros; Barbro = Barbarophryne brongersmai; Bufspi = Bufo spinosus; Bufbou = Bufotes boulengeri; Dispic = Discoglossus pictus; Dissco = Discoglossus scovazzi; Hopocc = Hoplobatrachus occipitalis; Hylmer = Hyla meridionalis; Pelvar = Pelobates varaldii; Pelsah = Pelophylax saharicus; Plewal = Pleurodeles waltl; Salalg = Salamandra algira.

PROSPECTS FOR CONSERVATION Synthesis of Threats to Amphibian Assemblages Survival problems faced by Moroccan amphibians can be attributed to environmental change of anthropogenic origin (IUCN, 2009); habitat loss is the major threat (Fig. 6).

The negative effect of human replacement of natural habitats with agricultural, urban, or industrial sites involves loss both of suitable habitat for breeding and of connectivity

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REQUES ET AL.

Figure 6: Major threats to Moroccan amphibians (from PLEGUEzUELOS et al., 2010).

between patches of suitable habitat (LAURANCE, 2001; STUART et al., 2008); the last is an increasing threat in Morocco, because of the spreading network of paved roads. These threats are particularly harmful to species with restricted distributions or ecological requirements, such as S. algira, P. varaldii, and A. maurus. Some species, however, do benefit from anthropogenic change; deforestation increases open habitat that may be rapidly colonized by generalist species such as A. mauritanicus and H. meridionalis.

Anurans also adapt well to agricultural landscapes if habitat change is not extreme; new and modified habitats can provide artificial, but suitable, breeding habitat in the form of irrigation ponds for P. saharicus and A. mauritanicus (STUART et al., 2004). Currently only four amphibian species, A. mauritanicus, B. boulengeri, P. saharicus and, to a lesser extent, H. meridionalis (because of overall resilience) exhibit relatively high tolerance to human-induced change to the landscape (deforestation and agriculture in particular).

Other recent threats include loss of suitable coastal habitat due to increasing development for tourism (affecting mainly P. varaldii along the Atlantic and Discoglossus species along the Mediterranean), and spread of other develop-

ments that modify natural water sources. Since construction of the Ouarzazate reservoir on the Oued Drâa, regular flooding ceased and oases that formerly provided suitable breeding places for A. mauritanicus, B. brongersmai, H. meridionalis, and B. boulengeri disappeared. Due to the high number of species affected, four of them threatened, intrinsic factors of the species should be considered the second major threat to Moroccan amphibians (Fig. 6). Restricted distributional area and low population density place Moroccan populations of S. algira, P. waltl, A. maurus, P. varaldii, A. xeros, B. spinosus, and H. occipitalis, all species with reduced dispersal capacity, in very sensitive situations.

Amphibians cannot escape natural effects resulting from climatic change (PARMESAN et al., 1999; CAREy & ALEXANDER, 2003) as changes in temperature and humidity affect physiology and phenology of the reproductive process (WALTHER et al., 2002; ROOT et al., 2003; READING, 2007) in addition to promoting loss and fragmentation of habitat (TEWKSBURy et al., 2008). Earlier estimates that at least four Endangered species and 13 Vulnerable species within Africa, most inhabiting the northern half of the continent, would be affected by climatic change (IPCC, 2007) have been reinforced by MARTíNEzFREIRíA et al. (2013) who predict a reduction in suitable area for 50% of Moroccan reptilian species in the future, suggesting a serious potential threat to amphibians as well.

Natural disasters like the current drought affecting Western Sahara (BENASSI, 2008) could hamper survival of A. xeros and H. occipitalis, species living in desert habitats at the southern extreme of Western Sahara.

Batrachochytrium dendrobatidis, the globally distributed fungus responsible for

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

chytridiomycosis and mass mortality among amphibians worldwide (HEATWOLE, 2013), has recently been reported in populations of P. varaldii, D. scovazzi, and H. meridionalis from Tétouan Préfecture. While opportunistically sampling 51 sites on the Gharb plain and in the Rif and Middle Atlas mountains between 2005 and 2009, EL MOUDEN et al.

(2011) examined 203 amphibian specimens for presence of chytrid fungus. Three sites (6%; all north of latitude 35.038°N) proved positive for chytrid fungus. While sample sizes for individuals determined to carry the fungus were low (one P. varaldii tadpole of 10 sampled, one adult H. meridionalis of four sampled, and two D. scovazzi [a metamorph and an adult] from each of two sites; see IUCN Red List Status, above) and infection rates cannot be accurately determined from the data obtained, the presence of this fungus in northern Morocco introduces another serious threat to the survival of native amphibians.

When ranked by number of species affected by each major threat to Moroccan amphibians, pollution placed third (Fig. 6). Chemical pollution of freshwater has been recognized as a serious global threat to amphibian populations (BRIDGES & SEMLITSCH, 2000; SPARLING et al., 2000) but while there are data concerning the effect of some pesticides on the Northern Bald Ibis (Geronticus eremita; ARMESTO et al., 2006) in Morocco, data are lacking on the effect of pesticides upon amphibians. Pollutants in favourable breeding habitat in Morocco are generally nitrogenous derivatives from agricultural fertilizer, but urban and cattle waste also contribute.

Although the relationship between pollutant level and amphibian richness is generally neg-

37

ative (BOONE & BRIDGES, 2003), different species do respond differently (BRIDGES & SEMLITSCH, 2000). Low pollution levels can increase trophic resources (BOONE & JAMES, 2005), and the relative abundance of some generalist species (P. saharicus, A. mauritanicus, and H. meridionalis) residing on the outskirts of urban areas, such as Chefchaouen, Ifrane, Goulimine, and Ouarzazate (FAHD et al., 2006, 2007) may be artificially high because of pollution. Species such as S. algira, however, cannot tolerate this kind of pollution (DONAIRE-BARROSO & BOGAERTS, 2003a).

Non-native species in aquatic ecosystems can pose serious threats to native amphibian populations (MOUSLIH, 1987; KATS & FERRER, 2003; KIESECKER, 2003). Mosquito fish (G. holbrooki), for example, are known to be detrimental to amphibian breeding success (SEGEV et al., 2009) and recent introductions of mosquito fish into numerous montane springs may compromise populations of A. maurus and other species (DONAIRE-BARROSO & BOGAERTS, 2003b; BEUKEMA et al., 2013). Discovery of New World crayfish Procambarus cf lophotus (DE POUS et al., 2012) suggests impending threats to aquatic amphibians in this area as well. “Once established, no methods exist by which a non-indigenous crayfish can be exterminated without unacceptable harm to native crayfishes and other organisms” (LODGE et al., 2000).

Road-kills may cause local extirpation of populations when traffic levels in proximity to breeding areas are high (DODD & SMITH, 2003; HOULAHAN et al., 2006). There are no data on such an impact on Moroccan amphibians, but the threat from traffic is presumed to be increasing because the number of roads and vehicles continues to increase.

38

REQUES ET AL.

An increasing threat to amphibian assemblages in arid areas of the south (Souss Valley, Ifni, Low Draa, Tekna) is the building of more and more reinforced concrete cisterns by shepherds. These deep, underground and covered structures with one or two uncovered decantation chambers positioned at the bottom of lightly sloping valleys accumulate humidity and attract amphibians. Individuals fall into decantation chambers or cisterns, both of which serve as death-traps (e.g. GARCíA-MUñOz et al., 2009). Although some B. brongersmai may breed in decantation chambers, others are subjected to predation or to dehydration as these structures become empty (L. García-Cardenete, personal communication). This increasing threat could rapidly deplete Saharan populations of A. mauritanicus, B. brongersmai and, particularly, B. boulengeri, in regions where they currently are scarce because of arid conditions.

This hazard can be corrected easily by installation of evacuation slides.

Priority Areas The Mediterranean Basin is considered a global hotspot for amphibian diversity and endemism (STUART et al., 2008).

Biogeographically, this eco-region includes four mountain chains and the northern half of the Moroccan lowlands and, as with other Mediterranean areas, Moroccan habitats are highly degraded and scarcely protected (BROOKS et al. 2004; WILSON et al., 2007; DE POUS et al., 2011). Gap analysis of diversity and distribution of amphibians, mammals, and protected areas in Africa illustrated the convenience of broadening protected areas around the western Rif, western Middle Atlas, and some localities along the Atlantic coast (RONDININI et al., 2005, 2006).

Figure 7: Priority areas (shaded) for amphibian conservation (see text).

Protection of places of interest, with amphibians acting as umbrella species, would conserve other vertebrates as well (RONDININI & BOITANI, 2006). Using models for 11 amphibian and 86 reptilian species, DE POUS et al. (2011) defined priority areas into which the existing protected areas could be extended.

Amphibians occur in most major habitats in Morocco, and threatened species are notably present in wetlands as expected, but also in shrublands, savannahs, and deserts (Fig. 1).

Threatened Moroccan amphibians have very restricted ranges, but ranges of the most threatened species include portions of the ranges of most other remaining species. Well-designed conservation area networks (CAN) will include most threatened species and much of Morocco’s amphibian species richness (Fig. 7; see also DE POUS et al., 2011). In northern Morocco, for example, protection of the entire range of A. maurus will protect eight additional species; DE POUS et al. (2011) showed that only about 7% of the distribution of A. maurus falls inside protected areas (e.g. National and Natural Parks of Jebel Bou Hachem, Bou Iblane, Talassemtane, Koudiat Tidighine, Al

39

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

Jabha Tazekka), although remaining populations are in areas so rugged that alteration is not imminent (DONAIRE-BARROSO & BOGAERTS, 2003b). In western Morocco, protection of the range of P. varaldii would include partial ranges of six additional species. This CAN would not include B. brongersmai, A. xeros, or H. occipitalis; conservation of the latter two species requires management action in the southern extreme of Western Sahara, areas currently suffering extreme drought and political problems.

Expansion of areas under protection would benefit A. maurus and other species of concern in Morocco, e.g. S. algira and B. spinosus. Because P. varaldii has not been confirmed within limits of the Merja zerga Biological Reservation recently, it apparently

does not occur in any protected area (DE POUS et al., 2011, 2012). The Mamora cork oak forest and surrounding area is the only locality where it is still common, and here it is highly threatened by overgrazing, logging, exotic tree plantations, and industrial development. Reduction of these negative effects and avoidance of further fragmentation (DE POUS et al., 2012) is essential, while establishing protected areas within this part of the range is urgent. Such action would also benefit P. waltl, D. scovazzi, H. meridionalis, B. boulengeri, A. mauritanicus, and P. saharicus.

The CAN in Morocco does not currently include all amphibian species, and a more complete network including remaining species is advisable (DE POUS et al., 2011). Some threat-

Table 4: Characteristics of regions having priority for amphibian conservation. For approximate regional areas, currently-protected areas, and percentages of major habitats within regions, see GLOBCOVER (2008) and text for details. Cost.A.R. = Coastal Atlantic Region; R.A.M.R. = Rif-Middle Atlas Mountain Region; Cent.A.R. = Central Atlantic Region; T.R. = Tiris Region.

Approximate regional area (km2) Currently-Protected areas

Cost.A.R.

R.A.M.R.

Cent.A.R.

5782

15 608

15 416

Merja zerga, Talassantane, Souss-Massa Sidi Boughaba Tazekka

T.R. > 211 576 None

Rainfed cropland

15.8

6.9

13.1

0

Mosaic cropland (50-70%) / other vegetation (grassland / shrubland / forest) (20-50%)

36.3

24.0

16.0

0

Mosaic vegetation (grassland / shrubland / forest) (50-70%) / cropland (20-50%)

25.7

23.0

26.2

0

Closed broadleafed deciduous forest (> 40% of the area with trees > 5m in height)

0.7

6.0

0

0

Mosaic forest or shrubland (50-70%) / grassland (20-50%)

4.4

10.6

8.4

0

11.7

19.3

4.6

0

Sparse (< 15% cover) vegetation

2.4

4.3

20.7

100

Bare areas

0.6

2.2

9.4

0

Closed to open (> 15%) (broad-leafed or needle-leafed, evergreen or deciduous) / shrubland (< 5 m)

40

REQUES ET AL.

ened species are found in desert and savannah but neither habitat type is well represented in the current CAN. Areas of high priority for protection are those in which historical ecological processes continue to function and in which climatic changes forecasted for the future may be mitigated (PARRISH et al., 2003; LOVEJOy, 2006; DE POUS et al., 2011). It is proposed here that the northwestern Atlantic, Rif-Middle Atlas, central Atlantic, and Tiris regions be considered as priorities for amphibian conservation (Fig. 7; see also RONDININI et al., 2005, 2006; CARVALHO et al., 2011; DE POUS et al., 2011). Currently protected areas in the first three regions should be enlarged (Table 4) and protection should be established for the Tiris region. Each of these regions contains habitat meeting ecological requirements (GLOBCOVER, 2008; see above) for the survival of Moroccan amphibians (Table 4).

NEW ECOLOGICAL STAGES AFFECTING MOROCCAN AMPHIBIANS Morocco will achieve significant human population increase and economic amelioration in the near future (AFRICAN DEVELOPMENT BANK, 2012), both of which likely will have negative effects on natural ecosystems.

Predicting how these changes will affect the amphibian fauna is difficult. One cannot rely upon modelling because time-series data for these effects on amphibian populations are not available, and one can only hypothesize future relationships between environmental change and amphibian populations. Knowledge of the ability of Moroccan amphibians to adapt to, and survive, human-induced environmental change is also lacking; some degraded habitats,

abandoned quarries, or deforested areas for example, may become suitable habitat for some amphibian species.

Besides foreseeable change in land use and pollutant levels, consequences from climatic change must also be considered. The Intergovernmental Panel on Climate Change (IPCC) predicts Morocco will be severely affected by an increase in temperature and a decrease in rainfall in the near future (HULME et al., 2001; IPCC, 2007; KLAUSMEyER & SHAW, 2009; LOARIE et al., 2009; MARTĂ­NEz-FREIRĂ­A et al., 2013). A 15% decrease in average annual rainfall has been recorded in Morocco during the past 30 years, with periods of drought increasing in duration and intensity (BENASSI, 2008). Following this scenario, Mediterranean wetlands will face altered hydroperiods, and wetlands currently permanent will become seasonal while wetlands currently temporal will disappear (REQUES, 2005; IPCC, 2007).

Shortening of the hydroperiod would affect species like P. varaldii, a threatened species with a relatively long larval period. It would also have negative consequences for other species through population and community effects (SCHNEIDER, 1997; MOREy, 1998). Scarcity of freshwater would hardly affect availability of water for humans (IPCC, 2007); competition for available water will increase between humans and amphibians and the loser in this competition will always be the non-humans.

Many aspects of the biology and ecology of Moroccan amphibians remain unknown (BEUKEMA et al., 2013); to foresee climatic and anthropogenic effects of global change upon amphibians it is necessary to understand the natural history and tolerance of each species to environmental change. Amphibian decline occurring on the southern Iberian Peninsula

STATUS OF MOROCCAN AND WESTERN SAHARAN AMPHIBIANS

because of increasing aridity (unpublished data) is probably very similar to that occurring in Morocco. Effective measures in Spain included restoring habitat in important breeding areas and creating new breeding areas (BEEBEE, 1996; SEMLITSCH & ROTHERMEL, 2003; REQUES & TEJEDO, 2008). The most suitable breeding places for amphibians in Mediterranean regions are temporal, spatially heterogeneous, and with extended hydroperiods (BEJA & ALCAzAR, 2003; TEWS et al., 2004). Species-specific conservation effort is needed in several cases, such as in the temporary coastal breeding ponds of P. varaldii and for some marginal, isolated, and scarce populations of S. algira and A. maurus (DE POUS et al., 2012, BEUKEMA et al., 2013).

Amphibians have survived dramatic episodes of climatic change for millions of years. Their future now depends upon humans.

If measures are not undertaken to minimize the impact of humans and the harsh effect of climatic change on amphibians, some species will not survive, particularly those in countries with large arid areas like Morocco.

Acknowledgement P. de Pous received financial support from FI-DGR grant 2013FI_B1 00110, Generalitat de Catalunya, Spain, during preparation of this manuscript. We thank L. Boyero, J.E. Cooper, D. Donaire-Barroso, S. Fahd, J. Fetzner, L. García-Cardenete, and J.A. Mateo, whose comments improved the manuscript, and extend our appreciation to those who came before us, to those who continue to respect and study the amphibians of Morocco, and to those currently engaged in protecting this most unique and valuable resource.

41

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Basic and Applied Herpetology 27 (2013): 51-83

Chapter 26 Diversity and conservation of Algerian amphibian assemblages José Mateo1,*, Philippe Geniez2, Jim Pether3 Servei de Protecció d’Especies, Govern de les Illes Balears, Palma de Mallorca, Spain.

CNRS, Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier, France.

3 Centro de Investigaciones Herpetológicas, Gáldar, Spain.

1 2

*Correspondence: Servei de Protecció d’Especies, Govern de les Illes Balears, 07011-Palma de Mallorca, Spain. Phone: +34 630491672, Fax: +34 971176678, Email: mateosaurusrex@gmail.com

Received: 10 January 2013; received in revised form: 14 October 2013; accepted: 7 November 2013.

Fourteen amphibian species representing six families inhabit Algeria: Salamandridae (Pleurodeles nebulosus, Pleurodeles poireti, and Salamandra algira), Alytidae (Alytes maurus, Discoglossus pictus, and Discoglossus scovazzi), Bufonidae (Amietophrynus mauritanicus, Amietophrynus xeros, Barbarophryne brongersmai, Bufo spinosus, and Bufotes boulengeri), Hylidae (Hyla meridionalis), Ranidae (Pelophylax saharicus), and Dicroglossidae (Hoplobatrachus occipitalis). The presence of some of them, like A. maurus, D. scovazzi, and H. occipitalis, is punctual. Areas of distribution conform to predictable patterns of biogeography; almost all species are present only in the Mediterranean region, while the Sahara Desert relegates a few frog species to isolation in mountain areas and oases with sufficient water.

Amphibian community origins are directly related to climatic changes in North Africa throughout the Holocene.

Many relict populations can be explained by comparison of the former layout and structure of hydrographic networks with those currently reduced to dry beds and, on occasion, suffering hyper-saline conditions. Relatively close phylogenetic relationships between species in the north of Algeria, portions of the Iberian Peninsula, Moroccan Atlas Mountains, Mediterranean islands and the Italian Peninsula, demonstrate that Algerian amphibian communities have as their origins the same Tertiary geological events that gave rise to today’s Mediterranean Sea. In the northern Mediterranean region, human overpopulation of coastal areas is affecting water quality and amphibian species diversity. The relict character of many amphibian populations in the desert regions, along with the rarity of stable water due to a combination of natural climatic changes, over-exploitation of aquifers, and eutrophication or pollution, justifies considering all species to be in danger to one extent or another. Using IUCN-proposed criteria as a guide, we herein suggest a catalogue of threatened amphibian species, provide a preliminary list of areas of interest, and suggest appropriate action necessary for amphibian conservation in Algeria. Of the 14 amphibian species known from Algeria P. poireti, a newt found only in the Edough mountains, the Guerbes-Sendhadja wetlands, and the Mekhada marshes, and A. maurus, a toad whose only known population in Algeria is in the Tlemcen mountains, must be considered Critically Endangered according to our suggested catalogue. We also consider P. nebulosus to be Threatened and S. algira to be Vulnerable, each due to continued loss of habitat, rarity, and population fragmentation. Finally, all amphibian populations south of 32°N latitude should be considered Near Threatened.

Key words: Algeria; amphibians; conservation; population decline.

Diversidad y conservación del conjunto de anfibios argelinos. Catorce especies de anfibios de seis familias diferentes viven en Argelia: Salamandridae (Pleurodeles nebulosus, Pleurodeles poireti y Salamandra algira), Alytidae (Alytes maurus, Discoglossus pictus y Discoglossus scovazzi), Bufonidae (Amietophrynus mauritanicus, Amietophrynus xeros, Barbarophryne brongersmai, Bufo spinosus y Bufotes boulengeri), Hylidae (Hyla meridionalis), Ranidae (Pelophylax saharicus) y Dicroglossidae (Hoplobatrachus occipitalis). La presencia de algunas de ellas como A. maurus, D. scovazzi y H. occipitalis, es puntual. Las areas de distribución coinciden con los patrones biogeográficos predecibles; casi todas las especies están presentes únicamente en la region mediterránea, mientras que sólo unas pocas especies aparecen en el desierto del Sáhara quedando aisladas en zonas de montaña y oasis con agua suficiente. Los orígenes de la comuThis chapter should be cited as: Mateo, J., Geniez, P. & Pether, J. (2013). Diversity and conservation of Algerian amphibian assemblages. Chapter 26 in Part 2. Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 51-83. DOI: http://dx.doi.org/10.11160/bah.13004/

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nidad de anfibios están relacionados con los cambios climáticos acontecidos en el norte de África durante el Holoceno. La existencia de muchas poblaciones relictas se explica al comparar la disposición y estructura de las antiguas cuencas hidrográficas con las actuales, reducidas a lechos secos y en ocasiones expuestas a condiciones hipersalinas. Las relaciones filogenéticas relativamente estrechas entre las especies del norte de Argelia con las de algunas partes de la península Ibérica, montañas del Atlas marroquí, islas del Mediterráneo y península Itálica, demuestran que las comunidades de anfibios de Argelia tienen el mismo origen Terciario que los eventos geológicos que dieron lugar al actual mar Mediterráneo. En la región mediterránea, al norte, la superpoblación humana en áreas costeras afecta a la calidad del agua y a la diversidad de especies de anfibios. El carácter relicto de muchas poblaciones de anfibios en las regiones desérticas, junto a la escasez de masas estables de agua como resultado de una combinación entre cambios climáticos naturales, sobreexplotación de acuíferos, eutrofización y contaminación, justifica que todas las especies se consideren, en algún grado, amenazadas. Guiándonos en los criterios propuestos por la UICN, sugerimos un catálogo de anfibios amenazados, aportamos una lista preliminar de áreas de interés y sugerimos las acciones necesarias para la conservación de los anfibios de Argelia. De las 14 especies conocidas en Argelia, P. poireti, un triton presente solo en las montañas de Edough, los humedales de Guerbes-Sendhadja y las marismas de Mekhada, así como A. maurus, un sapo cuya única población conocida en Argelia está en las montañas de Tlemcen, deben considerarse en peligro crítico según el catálogo que aquí sugerimos. También consideramos a P. nebulosus como amenazado y a S. algira como vulnerable, en ambos casos como consecuencia de la continua pérdida de hábitat, enrarecimiento y fragmentación de poblaciones. Finalmente, todas las poblaciones de anfibios al sur del paralelo 32°N deberían considerarse como casi amenazadas.

Key words: anfibios; Argelia; conservación; declive de poblaciones.

In spite of its size (2 381 740 km2) Algeria (Fig. 1) has populations of only 14 species of amphibians (SALVADOR, 1996; SCHLEICH et al., 1996) (Table 1). Its species diversity for this group of vertebrates is one of the poorest in Africa. Amphibian assemblages rarely contain more than five species, and more than half of Algeria is territory considered uninhabitable for salamanders, toads, or frogs (SALVADOR, 1996; SCHLEICH et al., 1996; COX et al., 2006). Such limited amphibian diversity has as its origin major climatic changes affecting all of North Africa during the Pleistocene and the Holocene. Historical changes, coupled with today’s scarce and unpredictable precipitation in almost the entire country, continue to limit suitable environments for amphibians (FAURE, 1985; PETIT MAIRE, 1985, 1986; DUBIEF, 2001; AUMASSIP & FERHAT, 2002; COX et al., 2006; LE QUELLEC, 2006).

HABITAT Geology, climate, and vegetation within Algeria allow characterization of two well-differentiated areas (Mediterranean Algeria and Saharan Algeria), each separated geographically from the other by the Sub-Atlasic Fault,

Figure 1: Main regions in Algeria.

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a large east-to-west-oriented geological fault near latitude 33ºN (ASKRI et al., 1995). This geographic separation has been used to explain floral and faunal differentiation within Algeria (BONS, 1967; WHITE, 1976; QUEzEL, 1978; SCHULz, 1979; LAMBERT, 1984; WICKENS, 1984; OzENDA, 1991; BOBROV, 2000) and provides a convenient framework for a discussion of amphibian assemblages and the threats they face.

The Mediterranean Located to the north of the great SubAtlasic Fault, the Mediterranean area, also known as Alpine Algeria (ASKRI et al., 1995), has an approximate area of 280 000 km2. The geological origin of this region is tied directly to the history of the Mediterranean Sea and to Tertiary folds that gave rise to many of the mountain ranges in southern Europe and northern Africa (MALDONADO, 1985); two of these Tertiary mountain ranges cross contemporary northern Algeria from east to west.

The northern slope of the Tell, or Tellian Atlas (with “Djebel” Lalla Khedidja, at 2308 m, the highest point), coincides almost completely with the Mediterranean coastline and is composed of several individual mountains (Tlemcen, Chréa and Kabylia) that behave as authentic “interior islands” in that these contain some of the largest concentrations of threatened amphibians in the entire Mediterranean region (COX et al., 2006; STUART et al., 2008).

Climatic conditions in the Tell are typically Mediterranean (humid to sub-humid; average annual precipitation > 400 mm, with dry summers and generally moderate temperatures) coinciding with Köppen’s climatic region “Csa” (KöPPEN, 1936). This area is the most humid region in Algeria and some meteorological stations, Djurjura, Babor, and El Tarf for example, record total annual precipitation of > 1000 mm (GRIFFITHS & SOLIMAN, 1972).

Vegetation in this area is comprised of sclerophyllous forests and heathlands adapted to hot dry summers. Holm oaks (Quercus ilex) accompanied or replaced by Kermes oaks (Q. coccifera),

Table 1: Biogeographic characteristics of the amphibian species of Algeria.

Species Pleurodeles nebulosus Pleurodeles poireti Salamandra algira Alytes maurus Discoglossus pictus Discoglossus scovazzi Hyla meridionalis Amietophrynus mauritanicus Amietophrynus xeros Barbarophryne brongersmai Bufo spinosus Bufotes boulengeri Pelophylax saharicus Hoplobatrachus occipitalis

Biogeographic region

Biogeographic affinity

Palaeartic Palaeartic Palaeartic Palaeartic Palaeartic Palaeartic Palaeartic Palaeartic Ethiopian Palaeartic Palaeartic Palaeartic Palaeartic Ethiopian

Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Sahelian Arid Mediterranean Eurosiberian Arid Mediterranean Mediterranean Soudanian

Regional presence in Algeria Tell Eastern Tell (Edough) Tell Western Tell Tell Saoura Valley Tell Tell+Hauts Plateaux Tassili’n’Ajjer and Hoggar Saharan Atlas Tell All - rare Northeastern extreme All Tassili'n'Ajjer

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Aleppo pines (Pinus halepensis), Carob trees (Ceratonia siliqua), or Sandarac gum cypress (Tetraclinis articulata) in the least humid areas, Cork oaks (Q. suber) in areas with soil of low pH, deciduous oaks (Q. canariensis, Q. faginea and Q. afares) in the most humid areas, or firs and cedars (Abies nummidica and Cedrus atlantica) in the cooler and humid mountains, provide tree cover (SCHULz, 1979; OzENDA, 1991).

To the south of the Tellian Atlas, and north of the Sub-Atlasic Fault (HERKAT & GUIRAUD, 2006), is the Saharan Atlas, a range of small, isolated mountains rising to 2000 m above sea level. Between the Tellian Atlas and the Saharan Atlas are the Hauts Plateaux and Aïn Regada platform, two plateaus separated by the solid massif of the Aurès.

The Saharan Atlas plateaus have climates that are basically Mediterranean but resemble Saharan climates in that annual precipitation rarely exceeds 200 mm. These areas coincide with the Steppic-Northern African domain defined by QUEzEL (1978) and only a few summits, such as the mountains around Aïn Sefra and “Djebel” Ksel, present a somewhat more humid climate, resembling those characterizing the Tellian Atlas (OzENDA, 1991).

The more humid conditions in the Tellian Atlas and the Aurès support the most complex amphibian assemblages in Algeria (COX et al., 2006). The Hauts Plateaux, Aïn Regada platform, and most of the Saharan Atlas support a less diverse fauna, their geographic ranges being more localized.

The Sahara South of the Sub-Atlasic Fault, the Saharan platform is larger and more geologically stable than in Alpine Algeria (WILLIAMS, 1984;

ASKRI et al., 1995). This fault line coincides closely with isohyets of 100 mm annual rainfall and, for climatologists and biogeographers alike, this fault line is the northern limit of the Saharan warm desert (Fig. 2) (GRIFFITHS & SOLIMAN, 1972; LAMBERT, 1984, SMITH, 1984; BOBROV, 2000). In addition to variation in volume of rain, different parts of the Sahara also differ in their seasonal pattern of rainfall (GRIFFITHS & SOLIMAN, 1972).

Approximately to the south of latitude 23°N precipitation occurs during summer (monsoon), while to the north of latitude 23°N the pattern of rainfall is similar to that of the Mediterranean region (Fig. 2). The variations in patterns of precipitation within the Sahara Desert significantly affect the biogeography of the entire region.

A large portion of the Saharan platform sits directly on the North-African Craton, a Precambrian shield about 1.5 billion years

Figure 2: Rainfall pattern in Algeria. Dotted line separates areas with Mediterranean-type precipitation (concentrated in the cool months of the year) from those with monsoon-type precipitation (concentrated during the summer). Modified from GRIFFITHS (1972) and GRIFFITHS & SOLIMAN (1972).

CONSERVATION OF ALGERIAN AMPHIBIANS

old and partitioned into several large, complex, sedimentary basins (WILLIAMS, 1984; ASKRI et al., 1995). Today, this area presents a monotonous, extremely arid and denuded landscape, for the most part not favourable for amphibian populations (LAMBERT, 1984; BORKIN, 1999). The Sahara Desert however, is not only the “Empty Quarters” of MONOD’s (1958) or EMBERGER et al.’s (1962) extensive desert areas, totally free of amphibians, and with an average annual precipitation of 5 mm, e.g., Tanezrouf or Ténéré (Fig. 2) (MONOD, 1958; DUBIEF, 1968); there are also less harsh districts in which some amphibians find favourable microhabitats (GRIFFITHS & SOLIMAN, 1972; LARMUTH, 1984).

In the Algerian Sahara, the monotony of the desert is interrupted by southern mountains and oases. The Targui shield, a socle associated with the Pan-African fold, includes the Hoggar and the plateaus (“tassilis”) surrounding it (WILLIAMS, 1984; ASKRI et al., 1995). These mountains, attaining elevations of up to 3000 m in the Adrar Tahat, receive more precipitation, and are subject to lower rates of evaporation than surrounding areas (Fig. 2) (GRIFFITHS & SOLIMAN, 1972). This moisture regimen, coupled with the existence of deep canyons able to support and maintain stable bodies of water, allows the southern mountains to behave as floral and faunal refuges of the first order (LHOTE, 1972; OzENDA, 1991; BOUMEzBEUR, 2001).

Oases are remnants of a hydrographic network that, fewer than six thousand years ago, supported extensive savannahs with varied faunas (DRAKE & BRISTOW, 2006; LE QUELLEC, 2006). Despite current hyper-arid conditions, the composition and differing thicknesses of silt and the varying elevations of certain areas

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Figure 3: Hydrographic basins of the Central Sahara (main rivers and lakes during the last humid period, about 8000 years ago). 1: Lake of Tidikelt, 2: Melhir / El Djedid mega-lake, 3: Chad megalake, 4: Fezzan mega-lake. Modified from DRAKE & BRISTOL (2006).

continue to partition the central Sahara into hydrological basins. These basins, in part, determine the distributions of oases and of amphibian species continuing to inhabit the Algerian Sahara. The most important basins are “wadis” Tafassasset, Tamanrasset and Tin Tarabine, the Tidikelt depression, and the ephemeral water-filled basins in the large “chotts” of the northeast (Fig. 3).

Large northeastern “chotts” (Melhir in Algeria and Djerid in Tunisia) formed ChottMegalake (a lake of about 30 000 km2 that captured waters from the central and eastern Saharan Atlas, the eastern mountains of Nementcha and Tebessa, the subsidiary basins of Hodna and Aurès, and from basins along “wadi” Mya and in the Gassi Touil

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Valley, all of which originate north of the Hoggar and the Tademaït Plateau) a few thousand years ago (DAMNATI, 2000).

Water for the Tidikelt depression mainly originates from the Moroccan High Atlas, Middle Atlas, and the western Saharan Atlas, supplemented by water from the western side of the Hoggar and the southern slope of the Cretaceous Tademaït Plateau (DRAKE & BRISTOW, 2006; FERHAT, 2006). At present, water still flows regularly, reaching Abadla, the valley of the Saoura / Messaoud and continuing to the oases of Touat, resulting in a relatively benign corridor between the Grand “Erg” Occidental and the “Erg” Er Raoui.

The eastern Hoggar, the Tassili’n’Ajjer and, partially, the Aïr Mountains provide water for the Tafassasset basin and flow on to the Ténéré basin (Niger), a subsidiary basin in turn of the Paleo-Chad. This great inland sea had a surface area the size of France, but at the present time is reduced to little more than 10 000 km2.

The Tamanrhasset and Tin Tarabine rivers occasionally receive water from the southern and western slopes of the Hoggar, water generally lost to the deserts of northern Mali and Niger. In the recent past, however, these rivers, tributaries of the Niger, facilitated migration of numerous sub-Saharan water-associated species to the north. Mega-Fezzan, a lake exceeding 100 000 km2, located in southwestern Libya, continues to receive much of its water from the eastern slopes of the Tassili’n’Ajjer (DRAKE & BRISTOW, 2006).

Amphibian Fauna Estimates of the number of amphibian species in Algeria historically have been limited to between eight and ten (LAMBERT, 1984;

SALVADOR, 1996; SCHLEICH et al., 1996; BORKIN, 1999) but recent molecular investigations have led to discovery of species previously unnoticed (COX et al., 2006). DNA analysis has demonstrated that newts of the Edough are well-differentiated from those in the rest of the country and should be considered different species (Pleurodeles poireti and P. nebulosus) (CARRANzA & ARNOLD, 2004; CARRANzA & WADE, 2004) and that painted frogs from most of Algeria are representative of a complex containing two species, Discoglossus pictus and D. scovazzi (PABIJAN et al., 2012; BEUKEMA et al., 2013), although the presence of D. scovazzi appears to be restricted to isolated populations in the Saoura Valley (HUGHES & HUGHES, 1992).

Populations of two species previously unknown in Algeria have also been discovered.

The African Midwife Toad (Alytes maurus), the nearest viable population of which was only known from several hundred kilometres to the west in Morocco, has been recently found in the mountains of Tlemcen (first specimens caught by J. Peña in 1990; confirmed 2009).

Barbarophryne brongersmai, previously known from Figuig, Morocco, a few kilometres from the border with Algeria (BONS & GENIEz, 1996), recently has been found in four towns in the Saharan Atlas of northwestern Algeria (first specimens caught by Jesús Peña in 1990, and J.A. Mateo, personal observation).

Nomenclature for Algeria’s amphibians (Table 1) follows that proposed by CARRANzA & WADE (2004) for caudate species, and BEUKEMA et al. (2013) for anuran species. Of the 14 species of Algerian amphibians, three are caudates (Fig. 4) in the family Salamandridae (two species of Pleurodeles [one endemic] and one species of Salamandra) and 11 are anurans (Figs. 5-8) in the families Alytidae (one species

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Table 2: Species-complexes, species, and subspecies of amphibians occurring in the Messinian biogeographic regions.

South of the Iberian Peninsula

Rif + Moroccan Atlas

Salamandra salamandra longirostris Pleurodeles waltl

S. algira tingitana and others P. waltl

Alytes dickhillenii Discoglossus jeannae D. galganoi Hyla meridionalis H. arborea Bufo spinosus Pelophylax perezi

Tellian Atlas

Sicily + Calabria S. salamandra -

A. maurus D. scovazzi

S. algira algira P. nebulosus P. poireti A. maurus D. pictus auritus

H. meridionalis

H. meridionalis

H. intermedia

B. spinosus P. saharicus riodeoroi

B. spinosus P. saharicus saharicus

B. bufo P. esculentus

of Alytes, two species of Discoglossus), Bufonidae (two species of Amietophrynus and one species each of Barbarophryne, Bufo, and Bufotes), Hylidae (one species of Hyla), Ranidae (one species of Pelophylax), and Dicroglossidae (one species of Hoplobatrachus).

Two species reported in the literature (Amietophrynus regularis and Ptychadena sp.) (LE BERRE, 1989; SALVADOR, 1996; SCHLEICH et al., 1996) have not been found in recent years and are no longer considered members of the Algerian fauna. Both species, reported from southern Algeria, were very likely confused with Amietophrynus xeros and Hoplobatrachus occipitalis, two species present in the mountains of the Tassili and the Hoggar (COX et al., 2006).

FAMILy SALAMANDRIDAE: NEWTS AND “TRUE” SALAMANDERS This Palearctic family is represented by two genera (Pleurodeles and Salamandra), and three species (P. nebulosus, P. poireti, and S. algira).

Pleurodeles nebulosus (Guichenot, 1850): Algerian Newt (Fig. 4). This species is endemic

D. pictus pictus

to the Maghreb of Algeria and northern Tunisia.

In Algeria this species is present in humid, subhumid, and semi-arid Mediterranean areas in the north, but absent from the northwest, with Sig (“Wilaya” of Mascara) being its westernmost known locality (KOLAR, 1955; LE BERRE, 1989; SCHLEICH et al., 1996; CARRANzA & WADE, 2004; VEITH et al., 2004). This newt prefers stagnant waters.

Pleurodeles poireti (Gervais, 1835): Edough’s Newt (Fig. 4). This species is an Algerian endemic (SAMRAOUI & DE BéLAIR, 1997; CARRANzA & WADE, 2004), smaller (up to 129 mm total length) but otherwise very similar in external appearance to P. nebulosus. In addition to genetic differences, it differs from P. nebulosus in external morphometric characters and in the configuration of the vomerine teeth (PASTEUR, 1958; CARRANzA & WADE, 2004). Edough’s Newt has a very restricted distribution, being found only in the coastal massif of Edough, the Guerbes-Sendhadja wetlands and the Mekhada marsh (“Wilayas” of Annaba and Skikda) (SAMRAOUI et al., 2012).

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Figure 4: Distributional ranges and bi-dimensional approximation to bioclimatic range for species of Caudata.

Bioclimatic approximation utilizes Embergerâ&#x20AC;&#x2122;s ombroclimatic index (Q = 2000 P / M2 â&#x20AC;&#x201C; t2), an indicator of degree of Mediterranean feel in temperate climates (OzENDA, 1964), where P is annual rainfall in mm, M is the average maximum temperature of the hottest month and t is the average minimum temperature during the coldest month (see DAGET, 1977). hum: humid; shu: sub-humid; sdr: sub-dry; sah: Saharan.

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Salamandra algira Bedriaga, 1883: Algerian Salamander (Fig. 4). In Algeria this species is restricted to very humid places in the northern mountains (SCHLEICH et al., 1996; MARTíNEz-MEDINA et al., 1997; DONAIRE & BOGAERTS, 2003; MATEO et al., 2003).

DOUMERGUE (1901) documented a population at Rhar-el-Maden (near Remchi) in Oran and this population is the westernmost known from Algeria (BONS & GENIEz, 1996). There are confirmed records from the mountains of Constantine, Edough, Medjerda, Traras, Tlemcen, and the Blidah Atlas; the majority of literature citations are from the Grande and Petite Kabylia regions (JOGER & STEINFARTz, 1995; ESCORIzA et al., 2006).

Larvae may occur in puddles and in creeks with slow moving currents and clear, clean water but adults frequent very humid and rocky areas and are associated with deciduous forests. Salamandra a. algira is the subspecies found in Algeria (DONAIRE & BOGAERTS, 2003) and it is probable that the extreme fragmentation to which the species is subjected masks genetic differentiation exceeding the species-subspecies threshold.

FAMILy ALyTIDAE: PAINTED FROGS With a Mediterranean distribution, this anuran family is comprised of two genera and 11 species (SAN MAURO et al., 2005). There are three species in Algeria: Alytes maurus, Discoglossus pictus, and D. scovazzi (HUGHES & HUGHES, 1992; PABIJAN et al., 2012).

Alytes maurus Pasteur and Bons, 1962: African Midwife Toad (Fig. 5). Holocene fossil remains found near Oran suggest that the African Midwife Toad had a considerably

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wider distribution a few thousand years ago (MATEO et al., 2003), and the presence of this species in northwestern Algeria was considered likely according to models of potential distributions (POUL et al., 2013).

In 1990 two adults of this species were captured in an artificial reservoir in the Hafir Forest (1170 m, 34°46’12’’ N / 1°27’23’’ W) by Jesús Peña and colleagues. Because these specimens had been incorrectly identified and labeled in the collection of the Asociación de Amigos de Doñana they went unnoticed until 2006 when they were re-identified by José A. Mateo. A visit to the Hafir Forest area by Mateo in May, 2009, allowed for detection of Alytes larvae. Numbers, however, were low and some individuals presented deteriorated horny beaks, an unequivocal sign they were infected by the fungus Batrachohytrium dendrobatidis (ALFORD et al., 2007). Chytridiomycosis, whose presence in North Africa has been confirmed (EL MOUDEN et al., 2011), is considered a prime cause for extinction of numerous amphibian species and it virulently affects adults and larvae of Alytes (BOSCH et al., 2013). A visit to the area during summer, 2013, provided no evidence of Alytes in the original artificial reservoir or vicinity.

Adults of A. maurus are not very aquatic, and the species is restricted to regions of humid Mediterranean climate.

Discoglossus pictus Otth, 1837: Algerian Painted Frog (Fig. 5). This species is relatively terrestrial and generally found in wellwatered, highly humid areas. It is present in all relatively humid Mediterranean regions of northern Tunisia, Algeria and north-eastern Morocco, Sicily, Malta, the Galita islands, and in French Roussillon and Spanish Catalonia (as an introduced species with an

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Figure 5: Distributional ranges and bi-dimensional approximation to bioclimatic range for species of Alytidae. See Fig. 4 legend for details.

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Figure 6: Distributional ranges and bi-dimensional approximation to bioclimatic range for species of Amietophrynus. See Fig. 4 legend for details.

expanding distribution) (LANzA & BRUzzONE, 1960; VEITH & MARTENS, 1997; PLEGUEzUELOS, 2002; FRANCH et al., 2007; BEUKEMA et al., 2013).

In Algeria, populations have been documented from the entire Tell, and from the vicinity of Oran to the border with Tunisia.

It is relatively common in the Hauts Plateaux and has been found in the oasis of zibans and in the Saharan Atlas (KOLAR, 1955; S URA , 1983; S ALVADOR , 1996).

VEITH & MARTENS (1997) assigned Algerian populations to the subspecies D. p. auritus Héron-Royer, 1888.

Discoglossus scovazzi (Camerano, 1878): Moroccan Painted Frog (Fig. 5). This species, found in humid and sub-humid areas, is represented by a relict population in the Saoura Valley (HUGHES & HUGHES, 1992). The Saoura Valley is formed from the confluence of some intermittent rivers originating in the Moroccan Atlas Mountains, where D. scovazzi is common (authors' personal observation).

FAMILy BUFONIDAE: “TRUE” TOADS Five species (Amietophrynus mauritanicus, A. xeros, Barbarophryne brongersmai, Bufo

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spinosus, and Bufotes boulengeri) from this family are known in Algeria (SALVADOR, 1996; SCHLEICH et al., 1996; COX et al., 2006).

Amietophrynus mauritanicus (Schlegel, 1841): Berber Toad (Fig. 6). Exclusive to the Maghreb, the Berber toad is quite common in humid, subhumid, and semi-arid areas with a Mediterranean climate in the north and northwest of Algeria (SALVADOR, 1996; SCHLEICH et al., 1996). It is found along the entire coastal area, in the Tellian Atlas, the Hauts Plateaux, region of zibans, the Saharan Atlas near the river Guir, and the Drâa (KOLAR, 1955; BALOzET, 1957; SIBOULET, 1968; ALTES & SIBOULET, 1977; SURA, 1983; LE BERRE, 1989; SALVADOR, 1996; SCHLEICH et al., 1996). References to A. mauritanicus in the south of Algeria (Hoggar and Tassili’n’Ajjer) (ANGEL & LHOTE, 1938; LE BERRE, 1989) are erroneous; the species found there is A. xeros. Amietophrynus mauritanicus lives in close proximity to temporary or permanent bodies of water that generally are deeper than those used by other Algerian bufonids.

Amietophrynus xeros (Tandy, Tandy, Keith and Duff-MacKay, 1976): Savannah Toad (Fig. 6). Typically a Sahelian species of arid savannahs, dry “wadies”, oases, and similar areas, the Savannah Toad is restricted to the Hoggar and Tassili’n’Ajjer mountains (ANGEL & LHOTE, 1938; CEI, 1973; JOGER, 1981; SALVADOR, 1996; SCHLEICH et al., 1996; RöDEL, 2000) of southern Algeria.

Barbarophryne brongersmai Hoogmoed, 1972: Brongersma’s Toad (Fig. 7). GENIEz et al. (2004) suggested that Brongersma’s toad was a possible species to be found in north-

western Algeria and, recently, it has been discovered in four towns in the Saharan Atlas within Algeria (Jesús Peña and José A. Mateo, unpublished). The species also may actually occur in other areas of this mountain range where it could have been confused with B. boulengeri. It is not a very aquatic toad, and lives near humid areas (e.g., “wadies”, ditches, oases, orchards, gardens) in arid areas of Mediterranean climate.

Bufo spinosus Daudin, 1803: Common Toad (Fig. 7). The common toad is not very abundant in Algeria and its distribution is fragmented. It is found only in humid and subhumid areas of Mediterranean climate in the north; it is well-documented from the Tellian Atlas (SALVADOR, 1996; SCHLEICH et al., 1996; AGASyAN et al., 2008). According to GARCIA-PORTA et al. (2012) common toads of North Africa should be considered a nondescribed subspecies.

Bufotes boulengeri (Lataste, 1879): NorthAfrican Green Toad (Fig. 7). This species is relatively common in the north, but rare in the more humid areas there (SALVADOR, 1996; SCHLEICH et al., 1996). It is present in varying densities in the oases and relatively humid areas of central and southern Algeria. It is absent from the Kabylia mountains but relatively common in the Hauts Plateaux, other semi-arid and arid regions of the Saharan Atlas, and the southern slope of the Aurès and Tebessa Mountains (SEURAT, 1930; SALVADOR, 1996). SAMRAOUI et al. (2012) have found some isolated populations of this species in Numidia (northwestern Algeria), where it is rare. In the central Sahara, North-African Green Toads are associated with oases (SCHLEICH et al., 1996) or with temporary

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Figure 7: Distributional ranges and bi-dimensional approximation to bioclimatic range for Bufotes boulengeri, Barbarophyne brongersmai (Moroccan individual), and Bufo spinosus. See Fig. 4 legend for details.

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watercourses (BONS & GENIEz, 1996). In the south, this species is probably the most common amphibian and is known from the Mouydir Mountains and the massifs of the Hoggar and Tassili’n’Ajjer (SCHLEICH et al., 1996).

This toad is associated with seasonal ponds of shallow depth in areas of very arid climates but in other geographical areas their preferences can vary.

FAMILy HyLIDAE: TREEFROGS RECUERO et al. (2007) and STöCK et al.

(2008) demonstrated that tree frogs in Tunisia and northeastern Algeria are genetically different from those in Morocco and northern and northwestern Algeria but no taxonomic changes have yet been introduced.

Hyla meridionalis Boettger, 1874: Stripeless Treefrog (Fig. 8). This anuran is associated with bodies of water with dense vegetation in humid regions with a Mediterranean climate along the entire Algerian coast, in the Tell, along the Cheliff Valley, and in the northern half of the Aurès (LLABADOR, 1947; SURA, 1983; BONS & GENIEz, 1996; SALVADOR, 1996; SCHLEICH et al., 1996).

FAMILy RANIDAE: “TRUE” FROGS True frogs are represented in Algeria only

by Pelophylax saharicus.

Pelophylax saharicus (Boulenger, 1913): NorthAfrican Green Frog (Fig. 8). By far the most common and widely distributed anuran throughout North Africa (BONS & GENIEz, 1996; SCHLEICH et al., 1996; GENIEz et al., 2004; BAHA EL DIN, 2006; DONAIRE-BARROSO

et al., 2008), two subspecies of the NorthAfrican Green Frog, P. s. saharicus (BOULENGER, 1891) and P. s. riodeoroi (SALVADOR & PERIS, 1975), are currently recognized. Pelophylax s. riodeoroi can be found in the northwest around Tlemcen and Aïn Sefra, in western “hamadas” along the Oueds Guir, Saoura and zousfana, in the Touat Oasis up to Timimoun, and in the valley of the Drâa.

Pelophylax s. saharicus is present in the Tellian Atlas, central and eastern Sahara, Hauts Plateaux, Kabylia, Aurès, the region of Tebessa, along the Ghardaia-El Golea corridor, on the Tademaït Plateau, and in oases (ARANO et al., 1998).

In the north its distribution is continuous and this aquatic species inhabits creeks and ponds from the Mediterranean coast down to the Saharan Atlas (HEMMER et al., 1980; LE BERRE, 1989; SALVADOR, 1996; SCHLEICH et al., 1996). More to the south, and in the centre and east of the country, it is restricted to dayas and oases (BOULENGER, 1891; ANGEL & LHOTE, 1938; COX et al., 2006). In the massifs of Hoggar and Tassili’n’Ajjer it is relatively common in deep gorges and close to bodies of relatively stable water (ANGEL & LHOTE, 1938).

FAMILy DICROGLOSSIDAE: FORKED TONGUED FROGS Recent separation of this group from the family Ranidae is based on molecular evidence and no anatomical characterization is yet available (FROST et al., 2006). The only African representative of this newly-formulated family is Hoplobatrachus occipitalis.

Hoplobatrachus occipitalis (Günther, 1859): African Bullfrog (Fig. 8). Algerian populations

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Figure 8: Distributional ranges and bi-dimensional approximation to bioclimatic range for Hyla meridionalis, Pelophylax saharicus, and Hoplobatrachus occipitalis. See Fig. 4 legend for details.

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of this widely-distributed bullfrog are restricted to Tassili’n’Ajjer, where several populations have been found in the vicinity of Iherir (25°24’ N, 8°44’ E), zaouatallaz (24°52’ N, 8°26’ E), in aguelman of Ifedil (24°33’ N, 9°31’ E), and at the head of the “wadi” Iddo (25°13’ N, 9°44’ E) (SEURAT, 1930; SCORTECCI, 1937; ANGEL & LHOTE, 1938; RöDEL et al., 2006).

African Bullfrogs are very aquatic and inhabit rivers and temporary ponds of subSaharan savannahs; in the Tassili’n’Ajjer they can be found only near stable sources of water and have suffered significant decreases in recent decades. In 1990 they had disappeared from some “gueltates” in which they were formerly abundant (Isidro Corea, personal communication).

BIOGEOGRAPHy Geology and bioclimatic conditions partition Algeria into three regions of biogeographic importance for amphibians: the Mediterranean Tell (with humid or subhumid conditions), a transition zone between Mediterranean Tell and the Sahara Desert (with arid or semi-arid conditions), and the Sahara Desert (Fig. 2).

The Tell Coincidence of distribution for several species or species-complexes in the Tellian region with those of the Moroccan Atlas, the north of Tunisia, the Iberian Peninsula, or the south of Italy suggests that amphibian distribution in these areas sharing a Mediterranean climate can be partially explained by the “Messinian Model” (Table 2) (BUSACK, 1986; MATEO et al., 2003; BUSACK & LAWSON, 2008). This biogeographical model, initially

proposed by BOCQUET et al. (1978) to explain floristic coincidences, relates distributional patterns to intercontinental connections during desiccation and rehydration of the Mediterranean Sea during the Messinian (Upper Miocene) “Salinity Crisis”. The cooccurrence of several species is related to disappearance and re-appearance of a marine barrier resulting from fragmentation of Pangaea. Conformation of current regional amphibian assemblages with circumstances initiated by this series of events has been broadly explained in the works of BUSACK (1986), ARANO et al. (1998), MATEO et al.

(2003), CARRANzA & ARNOLD (2004), FROMHAGE et al. (2004), RECUERO et al.

(2007), and BUSACK & LAWSON (2008).

Research demonstrates that genetic diversity in various complexes (Table 2) is explained by the closure and re-opening of the Strait of Gibraltar. BUSACK (1986), for example, demonstrated significant differences in genetic distances between some species considered vicariant from one side to the other of the Strait of Gibraltar. Other workers (ARANO et al., 1998; CARRANzA & WADE, 2004; FROMHAGE et al., 2004; MARTíNEz-SOLANO et al., 2004; VEITH et al., 2004) have also discovered genetic discontinuities of the same order of magnitude. BARBADILLO et al.

(1997), and later CARRANzA & WADE (2004) and PAULO et al. (2008), presented very convincing hypotheses based on fragmentation of basal populations, before and during the Messinian Crisis, to explain discontinuities.

These authors suggested that the area now comprising the coast of northwestern Africa and the southern Iberian Peninsula once belonged to a series of islands belonging to a geologic complex named Alkapeca (MICHARD

CONSERVATION OF ALGERIAN AMPHIBIANS

et al., 2002). Each of these islands could, over a long period of time, harbour isolated populations of amphibians currently represented in the region by allopatric species. ARANO et al.

(1998), CARRANzA & ARNOLD (2004), FROMHAGE et al. (2004), MARTíNEz-SOLANO et al. (2004), and RECUERO et al. (2007) have described genetic discontinuity considered appropriate for supporting taxonomic changes among North-African amphibians in the genera Pelophylax, Alytes, Discoglossus, Pleurodeles, and Hyla. Mountainous massifs of Edough, connected for a few thousand years to the mainland, remained totally isolated over a period of several millions of years and represent the last of the islands of the Alkapeca complex; the newt from Edough represents one additional example of allopatric speciation (CARRANzA & ARNOLD, 2004; CARRANzA & WADE, 2004).

In addition to faunal distributions attributable, in part, to Messinian events the Tell region also has contemporary differences in climate. Eastern and western areas along the Mediterranean Sea have areas of varying humidity and, while northwestern Algeria is relatively arid, the Kabilya area (GRIFFITHS, 1972) and some areas to the east of Alger, in the mountains of the Tell, are humid. Some northwestern slopes (Tlemcen Mountains, Aricha Plateau) drain into the Moulouya.

The valley through which this river flows provides a gradual northern corridor of desert and provides a pathway through which some species with clear Saharan affinities can approach to within less than 20 km of the Mediterranean Sea (BONS & GENIEz, 1996).

Two endemic species of the genus Pleurodeles, along with two species with Eurosiberian affinity (B. spinosus and S. algira),

67

are more common in these more humid regions. Bufotes boulengeri is, however, almost absent from this region.

On occasion, north-south and east-west humidity gradients (described above) are interrupted by elevations or depressions. The relative aridity of northwestern Algeria is partially ameliorated in the mountains behind Tlemcen, thereby creating a haven for Mediterranean sub-humid vegetation and sheltering several faunal relics that appear again only in the Middle Atlas, Rif, or Kabilya Mountains (SCHLEICH et al., 1996). Alytes maurus is one such faunal vestige that merits a mention.

The Transition Zone While maintaining a strong climatic affinity with the Mediterranean, the transition zone has continental thermal conditions and a mean annual rainfall of 100-250 mm; this produces an aridity that reduces amphibian species richness. Included in this zone are the entire Hauts Plateaux, the Aïn Regada platform, the Saharan Atlas, and the southern slopes of the Aurès and Tebessa Mountains.

The batrachian fauna of the transition zone is characteristically Mediterranean; creeks, ponds, “dayas”, and humid steppes in the area provide shelter for some of the more common anurans of the Tell. Discoglossus pictus, A. mauritanicus, B. boulengeri, and P. saharicus are species that can be found in the area (SALVADOR, 1996; SCHLEICH et al., 1996; BRUNET et al., 2009).

Also in the transition zone, but very near the desert in the Saharan Atlas, some summits (including, among others, Morhad at 2137 m, Makter at 2063 m, Aissa at 2236 m, and Ksel at 2009 m) serve as relatively humid havens surrounded by arid steppes.

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MATEO ET AL.

Assemblages of up to four different amphibian taxa can be found in these areas, including species otherwise occurring much further to the north (DOUMERGUE, 1901; SCHLEICH et al., 1996). These populations, now in danger of extirpation, are relicts from a not too distant time when precipitation was more abundant (PETIT-MAIRE, 1985; AUMASSIP, 2004; LE QUELLEC, 2006).

The only amphibian characteristic of the transition zone is B. brongersmai whose distribution in Algeria is believed to extend into desert regions of the western Hauts Plateaux and western steppe of the Saharan Atlas.

The Sahara Strictly Saharan amphibians do not exist (BONS, 1973; BORKIN, 1999). Of the six species of frogs and toads occurring south of 33ºN, four have Mediterranean, and therefore Palaearctic, affinities (D. scovazzi, B. boulengeri, A. mauritanicus, and P. saharicus), while the other two (H. occipitalis and A. xeros) are Ethiopian. Unlike reptiles or mammals, amphibians in the Sahara Desert face a hostile environment and an almost impassable biogeographic barrier. Requiring surface water, most frogs and toads have physiological and ecological requirements that preclude their survival over more than 99% of this great desert’s surface area (COX et al., 2006). Locations providing humid microclimates, regardless of size, serve to explain species’ distributions (LARMUTH, 1984); only where water exists on the surface, or seasonally, as in some mountain “gueltates” and “dayas” in the region of Laghouat, and some wells and oases, are amphibians found.

Hydrographic basins, almost always dry, may be used as basic geographic units

(PALOMO & ANTúNEz, 1992); their distribution and extent can offer interesting insight into the origin and affinity of the amphibian populations for which they provide refuge (see summary by DRAKE & BRISTOW, 2006).

Isolation of D. scovazzi, A. mauritanicus, and P. saharicus in different tracts of the Saoura Valley (BONS & GENIEz, 1996) likely began 6000 years ago as water from Saharan slopes of the Great Atlas and Middle Atlas drained into the basin of Tidikelt, of which the Saoura forms a part (HUGHES & HUGHES, 1992; DRAKE & BRISTOW, 2006).

The presence of A. xeros and H. occipitalis on the southern slopes of Tassili’n’Ajjer and, to a lesser extent, the Hoggar, is understandable because these slopes are associated with the Niger River and the Lake Chad basins, areas where both species are still abundant (LE BERRE, 1989; SALVADOR, 1996; RöDEL, 2000). Today’s Saharan batrachofauna is a pale memory of what it would have been only a few thousand years ago when the region was dotted by lakes and interior deltas, and traversed by large rivers. During that time Paleolithic artists of the Tassili, Drâa Valley, and the Eglabs region found inspiration in the hippopotamus, crocodile, and other vertebrates associated with water, in places where even dromedary camels find it difficult to survive today (VERNET, 1995; AUMASSIP, 2004; LE QUELLEC, 2006).

CONSERVATION PROBLEMS The same skin that allows an exchange of gases and ions with the environment makes amphibians extraordinarily susceptible to chemical contaminants, ultraviolet radiation, and infection. Increasing levels of various

CONSERVATION OF ALGERIAN AMPHIBIANS

kinds of pollutants (HEATWOLE & WILKINSON, 2009) and UV-radiation (MARCO et al., 2009) have been registered in recent decades, and there has been a globalization of pathogenic viruses, bacteria, and fungi (BERGER et al., 2009; HEMINGWAy et al., 2009) that in the past were limited to resistant and geographically-restricted species (STUART et al., 2004; ALFORD et al., 2007).

Amphibians may serve as an “early-warning” taxon for potential threats to other species, including humans, and they deserve programmed and continuous monitoring (COX et al., 2006; DODD et al., 2012).

The monitoring carried out during the past three decades by the University of Annaba has revealed significant reduction in numbers of P. poireti in recent years, and determined that this newt can be found only in Algeria. This species has come to be regarded as one of the most threatened amphibians in the Mediterranean region (SAMRAOUI et al., 2012). Unfortunately, monitoring programs of Algerian amphibian populations were restricted to localized areas (SAMRAOUI & DE BéLAIR, 1997; ROUAG, 2006; ROUAG & BENyACOUB, 2006) and the effects that acid rain, contaminated aquifers, or illnesses transmitted by ranaviruses or chytrid fungi (Batrachochytrium) may be having on amphibians in Algeria is only beginning to be understood.

The presence of chytrid fungi in North Africa had been predicted by earlier models (RON, 2005), and now has been confirmed in Morocco (EL MOUDEN et al., 2011). Chytrid fungus had gone completely unnoticed in Algeria, but evidence of infection found in midwife toad larvae in the region of Tlemcen suggests that chytridiomycosis is affecting some amphibian popula-

69

tions in this country. The recently discovered Algerian population of A. maurus is already in extreme danger of extirpation.

Shortage and unpredictability of precipitation make most of Algeria a territory in which permanent and semi-permanent bodies of water are rare. In the north, the only region in which rainfall is relatively plentiful, water quality is often compromised by high human population density and the enormous volume of waste that industry and urbanization generate (MIMOUNI & CHIBANE, 1989). In the arid Sahara to the south, human presence occasionally has fostered survival of some amphibian species, thanks to construction of channels and “fogharas” and to the maintenance of palm groves (e.g., the Ramsar reserve at the Ouled Saïd Oasis). It is possible that small populations of D. scovazzi detected in the Saoura Valley (HUGHES & HUGHES, 1992) survive precisely because of this contribution of water.

In other cases, however, presence of humans has resulted in eutrophication of “gueltates” and wells, and extirpation of fragile amphibian populations. Regardless of location, being it the north, central, or south of Algeria, amphibians continue to lose suitable areas in which to live.

COX et al. (2006) published conclusions regarding distributions and state of conservation for Mediterranean amphibians as expressed by experts from 18 countries.

Three of the 12 batrachian species then known from Algeria were listed as threatened under criteria established by the International Union for the Conservation of Nature (IUCN, 2010) (Table 3). While the evaluation summarized by COX et al. (2006) was global, application of the same IUCN criteria then used has been applied at the regional

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Table 3: Conservation status of Algerian amphibian species. R%: percentage of the species’ worldwide distribution corresponding to Algeria (ASTUDILLO & ARANO, 1995); IUCN Med: estimated level of threat, according to IUCN criteria, in countries bordering the Mediterranean Sea (COX et al., 2006); IUCN Algeria: level of threat proposed after the present updated review for Algerian populations, including species newly-recorded for the country; Criteria according to IUCN (2010) for species catalogued in Algeria as VU, EN or CR. LC: Least Concern; NT: Near threatened; VU: Vulnerable; EN: Endangered; CR: Critically Endangered. No Algerian species is included in category DD: Deficient Data.

Species

R%

IUCN Med

IUCN Algeria

Criteria

Pleurodeles nebulosus Pleurodeles poireti Salamandra algira Alytes maurus Discoglossus pictus Discoglossus scovazzi Hyla meridionalis Amietophrynus mauritanicus Amietophrynus xeros Barbarophryne brongersmai Bufo spinosus Bufotes boulengeri Pelophylax saharicus Hoplobatrachus occipitalis

68 100 42 4 57 1 47 48 1 37 6 5 42 1

VU EN VU NT LC LC LC LC LC LC LC LC LC LC

VU CR VU CR LC NT LC LC NT LC VU LC / NT* LC / NT* NT

B 1ab (ii) + 2 ab (iii) B 2ab (iii) B 1ab (ii) + 2 ab (iii) B 1ab +D 2

B 1ab (v) -

*Saharan populations south of 32°N latitude

level (GAERDENFORS et al., 2001; IUCN, 2010) to the 14 species currently known to occur in Algeria (Table 3) and this assessment allows completion of the Algerian catalog of threatened species, and provides a basis for making recommendations to appropriate governmental authorities (see PLEGUEzUELOS et al., 2010). Reference to the protection of autochthonous fauna, and the necessity of legislation dedicated specifically for that purpose, is published in Algeria’s Constitution, but none of the lists of threatened Algerian fauna published since Algeria’s independence has included amphibians (DUPUy, 1966; WORLD LAW GUIDE, 2010).

Table 3 provides information about the level of threat to each of the 14 amphibian species known to occur in Algeria.

THREATENED AMPHIBIANS Pleurodeles poireti. Because of its small geographic range (restricted to the Massif of Edough, the Guerbes-Sendhadja wetlands, and the Mekhada wetlands; SAMRAOUI & DE BéLAIR, 1997; CARRANzA & WADE, 2004; SAMRAOUI et al., 2012), and the proven regression of this species (SAMRAOUI et al., 2012), Edough’s Newt is considered the most threatened amphibian in Algeria. Because the species is an endemic, Algeria’s responsibility for its conservation is a high priority.

These newts are threatened by water pollution, overgrazing, and drying out of habitat due to agricultural and sanitary development (COX et al., 2006). A wetland area at GuerbesSenhadja, including almost all the lagoons and

CONSERVATION OF ALGERIAN AMPHIBIANS

swamps near Annaba, and encompassing more than half of the known distribution of this species, has been declared a Ramsar reserve, which, at least in theory, provides a territorial base for which a recovery plan can be developed. This plan should include procedures based on the species’ biology and basic requirements as a means of formulating management measures (SAMRAOUI et al., 2012).

Pleurodeles nebulosus. The Algerian Newt has a much less limited distribution than Edough’s Newt. Lagoons and other bodies of fresh water in its distributional range, however, have suffered direct human impact, from draining of land for sanitary reasons, loss of land to cultivation, contamination of land by agriculture or industry, and decrease in residual water volume associated with growth of Algeria’s human population over the past three centuries.

Concern for wetlands has increased in the past few decades and that concern has been translated into numerous Ramsar reserves.

These reserves, especially the complex of lagoons (Lac des Oiseaux and Lake Fetzara) that are part of El Kala National Park, have helped this species. As with Edough’s Newt, more information about this species’ biology and of the actions required to guarantee its conservation, is urgently needed (SAMRAOUI et al., 2012).

Salamandra algira. The range of the Algerian Salamander is discontinuous in mountains with significant rainfall and high water quality, and studies of the genetic variability of North African populations should be undertaken (BOGAERTS & DONAIRE-BARROSO, 2003). Loss of habitat due to deforestation

71

and cultivation, as well as loss from overgrazing and water contamination, are considered serious areas of concern within Algeria (IUCN, 2005, unpublished report). Some habitats of the Algerian Salamander already possess some level of protection (Chréa, Djurdjura, and El Kala National Parks; Babor Natural Reserve), yet many areas in the Grande and Petite Kabilya and in the Constantine Mountains should also be considered areas of interest for conservation.

Alytes maurus. The only well-known haven for the African Midwife Toad is in the Tlemcen Mountains, a good part of which is at present included in Tlemcen National Park (LOUKKAS, 2006). Loss of habitat associated with deforestation, contamination of water, and emergent illness are among the main threats. Algeria has limited responsibility for conservation of this species because Tlemcen populations represent only the eastern edge of a wider distribution in Morocco.

Application of some basic and inexpensive conservation measures in Tlemcen National Park could guarantee its survival. If, as seems to be happening, chytridiomycosis is affecting the population of Midwife Toads from Tlemcen, urgent measures need be taken to preserve this species in Algeria.

Bufo spinosus. The Common Toad is a widespread species not considered globally threatened (COX et al., 2006) but that, in Algeria, has a highly fragmented distribution associated with mountainous areas (SAMRAOUI et al., 2012). This pattern of distribution and progressive deterioration of populations support the conclusion that the species is Vulnerable.

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Table 4: Areas of special interest for amphibians in Algeria.

Area

Climate

Type of Habitat

Coordinates

Area (km2)

Lake Béni Belaïd

36º53’ N 6º05’ E

6

Mediterranean subhumid

Edough

36º51’ N 7º19’ E 36º56’ N 7º20’ E 36º47’ N 8º07’ E 36º47’ N 7º31’ E 36º45’ N 8º01’ E 36º51’ N 8º23’ E

700

Mediterranean subhumid

42

Mediterranean subhumid

9

Mediterranean humid

Marshes

90

Mediterranean humid

1.2

Mediterranean humid

Stable coastal lagoons, areas of seasonal flooding Freshwater lagoon

764

Mediterranean subhumid and humid

Tlemcen Mountains

34º36’ N 1º27’ W

82

Mediterranean semi-arid and subhumid

Chréa

36º26’ N 2º53’ E 36º19’ N 3º34’ E

266

Mediterranean subhumid

185

Mediterranean semi-arid and subhumid

36º30’ N 5º30’ E 33º54’ N 0º09’ E 33º37’ N 6º04’ E

17

Mediterranean humid

2550

Mediterranean Saharan

Humid area, coastal swamps and subhumid Mediterranean forest Mediterranean mountains with cork, pine, and oak forest Mediterranean mountains with oak and cedar forests Mediterranean mountains with cork forests, cedar and pine Mediterranean forests of Holm oak, cedar, and fir Arid Mediterranean areas

204

Saharan, precipitation in colder months

Oases, dunes, and “hamadas” Alignment of Oases, between “ergs” and “hamadas”

Guerbes-Senhadja Mekhada marshes Lake Fetzara Lac des Oiseaux El Kala National Park

Djurdjura

Djebel Babor Ksour Mountains and Djebel Ksel Oases of Wadi Igharghar

Guir / Saoura

29º54’ N 1º54’ W

11 000

Saharan, precipitation in colder months

Drâa Valley

29º31’ N 7º01’ W

4200

Saharan, precipitation in colder months

24°35’ N 09°31’ E (Djanet)

72 000

Tassili’n’Ajjer National Park

Saharan, precipitation in warmest months

Freshwater lake, adjacent humid areas and coastal dunes Mediterranean mountains and forest Coastal wetlands

Temporary “wadies”, isolated “gueltates”, and abandoned irrigation ditches Hyperarid plateaus and hills

Hoggar National Park

22°47’ N 5°31’ E (Tamanrhasset)

380 000

Saharan, precipitation in warmest months Mountainous Desert

*BR: Biosphere Reserve; NP: National Park; NR: Natural Reserve.

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CONSERVATION OF ALGERIAN AMPHIBIANS

Wilaya

Protection*

Nº Species

Threatened and NearThreatened species

Jijel

NR Ramsar site 1303

5

P. nebulosus

Rouag, 1997 in Boumezbeur & Naziha 2003; Boumezbeur & Naziha, 2002 Samraoui & de Bélair, 1997; Carranza & Wade, 2004 Samraoui et al., 2012

References

NR, Ramsar

7

Annaba Skikda

Ramsar site 1056

5

P. poireti S. algira P. poireti

El Tarf

Ramsar

5

P. poireti

Samraoui et al., 2012

Annaba

Ramsar site 1299

6

P. nebulosus

Boumezbeur, 2003

El Tarf

NR Ramsar site 975 NP, Ramsar sites 280, 281, 1293, 1301, 1305 and 1424 NP

5

P. nebulosus

Boumezbeur & Naziha, 2003

6

P. nebulosus B. spinosus

Rouag, 2006; Rouag & Benyacoub, 2006

A. maurus B. spinosus

Doumergue,1901; Loukkas, 2006

S. algira B. spinosus S. algira B. spinosus

Loukkas, 2006

El Tarf

Tlemcen

7 Blida

NP, BR

6

Bouira Tizi Ouzou

NP

6

Sétif

NR

6

Naama Bayadh

NP, Ramsar

5

El Oued

None

3

Bechar Adrar

None

4

Tindouf

None

4

Illizi

NP

4

Tamanrhas-set

NP

3

Loukkas, 2006

S. algira B. spinosus B. brongersmai

-

P. saharicus A. mauritanicus B. boulengeri P. saharicus A. mauritanicus B. boulengeri D. scovazzi B. boulengeri P. saharicus B. brongersmai?

A. xeros B. boulengeri H. occipitalis P. saharicus P. saharicus A. xeros B. boulengeri

-

-

Gauthier, 1967; Hughes & Hughes, 1992 Bons & Geniez, 1996

Le Berre, 1989; Hughes & Hughes, 1992; UNEP / WCMW, 2008 Hughes & Hughes, 1992; Boumezbeur, 2001

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MATEO ET AL.

NEAR-THREATENED SPECIES Three species, considered of Least Concern (LC) at the global level, have restricted and severely fragmented distributions in Algeria and are considered Near Threatened (NT) at the local level. Barbarophryne brongersmai is relatively common in semi-arid regions in portions of the Saharan Atlas, and both A. xeros and H. occipitalis have wide distributions in sub-Saharan Africa but are restricted to some areas of the Hoggar and the Tassili in Algeria. As with the previous species, water quality and loss of habitat are the main causes of their precarious state.

Pelophylax saharicus and B. boulengeri are not considered threatened at the global level (COX et al., 2006) and are relatively common in northern Algeria but isolated populations in the Saharan region are, on occasion, very threatened. For this reason, populations south of latitude 32ºN in Algeria can appropriately be considered as Near Threatened (NT).

benefitted some amphibian species. The most obvious examples of this are wetland areas protected by the Ramsar convention, areas originally mapped for ornithological reasons but that also serve as amphibian refuges. As noted above, protection of wetlands in the north of Algeria benefits species such as P. poireti and P. nebulosus; similarly, protection of mountainous areas, such as those of the Djurdjura, Tlemcen, or the Hoggar, serve as refuges for some threatened species and protect relict fauna like S. algira and A. maurus.

Not all areas important for amphibian conservation are found within the boundaries of a national park or reserve, however, but all deserve to be preserved, especially all Saharan water points whose amphibian communities are, by definition, threatened. We conclude this chapter with a preliminary listing of areas of importance to amphibians, including information on location, area, climate, habitat characteristics, and Threatened and Near Threatened species that can be found in these areas (Table 4).

AREAS OF SPECIAL INTEREST FOR AMPHIBIANS

Acknowledgement

Reports published in 2003 by Earth Trends identify 5.1% of Algeria’s surface as within limits of reserves, national parks, national monuments, or otherwise protected landscape.

Although amphibians are repeatedly considered excellent indicators of the ecological health of an area, they have rarely been considered when site mapping for these protected areas (BUTCHART et al., 2006). In addition to sites important for historical and landscape reasons, Algerian parks and reserves have targeted mainly the conservation of birds and large mammals (LOUKKAS, 2006). The protective measures adopted have, however, indirectly

Assistance and information were provided

by José Brito, Jesús Peña, Hipólito Guerrero, Eva Graciá and the curators of herpetological collections maintained by the Asociación Amigos de Doñana (Sevilla, Spain), the British Museum of Natural History, the Estación Biológica de Doñana (Sevilla, Spain), the Cornide de Saavedra Fund (Coruña, Spain), the Institut de Recherches (Rabat, Morocco), the Laboratoire de Biogéographie et écologie des Vertébrés (Montpellier, France), the Musée de la Wilaya d’Oran (Oran, Algeria), the Musée National d’Histoire Naturelle (Paris, France),

CONSERVATION OF ALGERIAN AMPHIBIANS

the Museo Nacional de Ciencias Naturales (Madrid, Spain), the Museum Alexander König (Bonn, Germany), and Paul Valéry University (Montpellier, France).

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Basic and Applied Herpetology 27 (2013): 85-100

Chapter 27 Conservation status of amphibians in Tunisia Nabil Amor1,2,*, Mohsen Kalboussi3, Khaled Said2 Center for Functional and Evolutionary Ecology and Biogeography of Vertebrates (EPHE), UMR5175 – CNRS Montpellier, France.

Unité de Recherche: Génétique, Biodiversité et Valorisation des Bioresources, Institut Supérieur de Biotechnologie de Monastir, Monastir, Tunisia.

3 Institut Sylvo-Pastoral, Tabarka, Tunisia.

Authors are listed in alphabetical order.

1 2

* Correspondence: Unité de Recherche: Génétique, Biodiversité et Valorisation des Bioresources, UR/09-30, Institut Supérieur de Biotechnologie de Monastir, Monastir 5000, Tunisia. Phone: +216 99904622, Fax: +216 71573526. Email: nabil.amor@gmail.com

Received: 10 January 2013; received in revised form: 17 September 2013; accepted: 18 September 2013.

The North African amphibian fauna was once regarded as limited in diversity, but increased field and laboratory research in the region has subsequently revealed considerable endemism and data such as these are necessary for making objective and justifiable recommendations for conservation. Our research, coupled with findings from the literature, allow an up-to-date analysis of distribution, status of populations, and actual and potential threats to the continued survival of all species within Tunisia. The Tunisian batrachofauna currently consists of seven species grouped in seven genera: Pleurodeles, Bufotes, Discoglossus, Bufo, Amietophrynus, Pelophylax, and Hyla. Whereas other species are characterized by wider distributions from north to south, Bufo spinosus appears restricted to the mountainous northwestern corner where major protected areas occur. Pleurodeles nebulosus and Hyla meridionalis appear restricted to humid, subhumid, and semi-arid localities in northern Tunisia, in the Khroumirie region, but also within the Mogod region, around Tunis and the Cap Bon Peninsula. Northern localities represent the most humid and temperate portion of the country and support the highest habitat and species diversity. Despite an increasing number of man-made habitats (irrigation canals), southern localities continue to suffer from lack of suitable habitat due to natural and human causes. There are no manmade ponds dedicated to protect amphibian species in Tunisia. Our observations confirmed that Tunisia is affected by amphibian population decline, due especially to loss and fragmentation of habitat. Principal threats to amphibian survival (uncontrolled urban extension, alteration and destruction of habitat, pollution, road kills, and introduction of several predator species) vary slightly from north to south. Implementation of stricter policies coupled with increased public education and awareness is recommended in order to preserve Tunisia’s amphibian fauna.

Key words: amphibians; conservation status; Tunisia.

Estado de conservación de los anfibios en Túnez. Tradicionalmente se consideraba a la fauna de anfibios del norte de África poco diversa, pero el aumento de los estudios de campo y laboratorio en esta región ha revelado un grado considerable de endemicidad, haciéndose necesarios más datos para elaborar recomendaciones para la conservación que sean objetivas y justificables. Nuestro trabajo, junto a otros hallazgos recopilados de la literatura, permite un análisis detallado de la distribución, estado de las poblaciones y amenazas reales y potenciales para la supervivencia de todas las especies de Túnez. La batracofauna tunecina consiste actualmente en siete especies en otros tantos géneros: Pleurodeles, Bufotes, Discoglossus, Bufo, Amietophrynus, Pelophylax e Hyla. Mientras que algunas especies se encuentran ampliamente distribuidas de norte a sur, Bufo spinosus se restringe a la región montañosa noroccidental donde se encuentran las principales áreas protegidas. Pleurodeles nebulosus e Hyla meridionalis se limitan a las localidades húmedas, subhúmedas y semiáridas del norte, en la región de Khroumirie, además de a la región de Mogod, el entorno de la capital y la península del cabo de Bon. Las localidades septentrionales constituyen la parte más húmeda y templada del país, albergando la mayor diversidad de hábitats y de especies. En las localidades meridionales, pese al incremento en el número de hábitats artificiales (canales de irrigación), existe una falta de hábitats apropiados como consecuencia de factores tanto This chapter should be cited as: Amor, N., Kalboussi, M. & Said, K. (2013). Conservation status of amphibians in Tunisia. Chapter 27 in Part 2.

Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 85-100. DOI: http://dx.doi.org/10.11160/bah.13006/

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naturales como artificiales. No existen en todo Túnez charcas artificiales destinadas a la protección de anfibios. Nuestras observaciones confirman que Túnez no es ajeno al declive de las poblaciones de anfibios, debido fundamentalmente a la pérdida y fragmentación del hábitat. Las principales amenazas para la supervivencia de los anfibios (expansión incontrolada de los núcleos urbanos, alteración y destrucción del hábitat, contaminación, atropellos e introducción de diferentes especies depredadoras) varían ligeramente de norte a sur. Recomendamos implementar políticas más estrictas, junto al incremento de la educación y concienciación social, para preservar la fauna de anfibios de Túnez.

Key words: anfibios; estado de conservación; Túnez.

Tunisia is the smallest north-African country, with an area of 164 000 km2. While some forest occurs in the centre of the country, broadly-forested areas are limited to the north; almost one-third of Tunisia’s surface area is covered by the Sahara Desert, and a major portion of the rest of the country is dominated by an arid climate characterized by annual and seasonal variation in rainfall (PEEL et al., 2007). The major ecological factor limiting amphibian survival in the country is scarcity of water (AMOR et al., 2010a,b).

Prior studies of the distribution of amphibians in Tunisia (POIRET, 1789; GERVAIS, 1835, 1853; LATASTE, 1881; BOULENGER, 1882, 1891; OLIVIER, 1894, 1896; DOUMERGUE, 1901; DE CHAIGNON, 1904; WOLTERSTORFF, 1901; MAyET, 1903; PELLEGRIN, 1927; GAUTHIER, 1928; MERTENS, 1929; MOSAUER, 1934; BLANC, 1935; GALLIEN, 1948; PASTEUR, 1958; DOMERGUE, 1959; SCHNEIDER, 1974, 1978; HEMMER et al., 1980; BLANC & NOUIRA, 1988; STEINWARz & SCHNEIDER, 1991; SCHLEICH et al., 1996; MEDDEB & CHENITI, 1998; NOUIRA & LESCURE, 1998; NOUIRA, 2001; ROMDHANE & MISSAOUI, 2001; JOGER, 2003; AzOUzI & TEKAyA, 2004, 2007; BEN HASSINE, 2007, 2011; MEDDEB et al., 2007) understandably were limited in geographical coverage and utilized the morphologically-based taxonomy in use at the time.

Updated contributions by AMOR et al. (2007,

2009, 2010a,b,c,d,e, 2011), SICILIA et al.

(2009), BEN HASSINE & NOUIRA (2012a,b), BEN HASSINE et al. (2013), and BOGAERTS et al.

(2013a,b) contribute toward a more complete understanding of the distribution and ecology of Tunisian amphibians.

FAUNAL COMPOSITION AND GENERAL DISTRIBUTION Pleurodeles nebulosus (Guichenot, 1850), the Algerian ribbed newt, is the only salamander represented in Tunisia (CARRANzA & WADE, 2004; VEITH et al., 2004; SICILIA et al., 2009; BEN HASSINE & NOUIRA, 2012a,b; BEN HASSINE et al., 2013). It has been recorded from north-central Algeria to the Cap Bon Peninsula (SMITH et al., 1998; PASMANS et al., 2002; SICILIA et al., 2009; BEN HASSINE & NOUIRA, 2012b; BEN HASSINE et al., 2013) but currently this Algero-Tunisian endemic appears restricted to the humid, subhumid, and semiarid localities in northern Tunisia: in the Khroumirie region, and at the Mogod region, around Tunis and the Cap Bon Peninsula (BEN HASSINE, 2012a; BEN HASSINE et al., 2013). In these places it is locally abundant in humid environments close to rivers (Ordha, southwest of Tabarka; the route between Aïn Sobh and the aeroport; near oued El Kebir, Tabarka), small watercourses, and stagnant bodies of water (in the vicinity of Tabarka; Barbra Dam

AMPHIBIAN STATUS IN TUNISIA

near the village of Hammam Bourguiba).

Individuals tend to congregate in groups of more than ten under the same shelter, probably in response to the lack of suitable shelters, but also they are often found solitary or in small groups. Aestivation during hot and dry periods of the year is accomplished by digging deeply into soil among plant roots. The species’ southern limit of distribution in Tunisia seems to be the Cap Bon Peninsula.

Hyla meridionalis Böttger, 1874, the Mediterranean treefrog, is the country’s only arboreal species of amphibian. Recent phylogeographic studies have shown that Tunisian H. meridionalis are highly divergent from Iberian and neighbouring populations, suggesting that the Tunisian populations could represent a new species (RECUERO et al., 2007; STöCK et al., 2008a), although the interpretation of this divergence could be exaggerated due to absence of samples from Algeria. The Mediterranean treefrog is limited to northern Tunisia, from the Algerian border (El Feija National Park) to Bizerte, south and north of Medjerda (BEN HASSINE & NOUIRA, 2012b), where it has a disjunct distribution and survives mainly around sources of water supporting woody vegetation; when not breeding or moving toward a suitable breeding pond, it usually is found perched on a tree or a bush.

The species may be locally abundant in the Khroumirie and Mogod regions during its breeding season, generally from the beginning of February to the end of March (SICILIA et al., 2009; BEN HASSINE & NOUIRA, 2012a).

In Tunisia, the species has not been found on coastal dunes (e.g. Bizerte), as is sometimes the case in southern Spain or northern Morocco (BUSACK, 1986), and its reported occurrence near the city of Tunis and Bardo’s

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gardens (MAyET, 1903) has not been confirmed (SICILIA et al., 2009; BEN HASSINE & NOUIRA, 2012b) .

Discoglossus pictus Otth, 1837, the painted frog, is widely distributed in Tunisia, but its geographic distribution is discontinuous. All eastern Maghrebian populations were formerly known as D. p. auritus, but the taxonomic validity of D. p. auritus for these populations, and D. p. pictus for Mediterranean island populations (Sicily, Malta, and Gozo) does not appear supported by recent genetic and karyological analyses (FROMHAGE et al., 2004; zANGARI et al., 2006; AMOR et al., 2007, 2010c,d,e). The painted frog inhabits a wide range of biotopes from montane forests to coastal areas. In northwestern Tunisia it may be found somewhat distant from any water (AMOR et al., 2010c,d). In southernmost localities D. pictus is confined to areas such as the oases of Gafsa, Chott El Djerid, Kebili, Chinini, and the Oued el Ferd and Kettana both in Gabès (BUSACK, 2006; BEN HASSINE & NOUIRA, 2009, 2012b; SICILIA et al., 2009; AMOR et al., 2010c,d). Higher densities may be found around the multiple dams in the country, especially during breeding seasons. BEN HASSINE & NOUIRA (2012b) considered the painted frog to be absent from all Sahel regions; however, we have recorded the presence of individuals from Gabès to Nabeul (AMOR et al., 2010c,d). Surveys within suitable habitats during the breeding season are necessary for verification of this species’ presence.

Pelophylax saharicus (Boulenger, 1913), the North African green frog, is the most abundant species in Tunisia (AMOR et al., 2007, 2009, 2010a,b). It inhabits oases, ponds (natural and artificial), and irrigation

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ditches throughout the country (including northern portions of the Sahara Desert), and population density is often very high (AMOR et al., 2009, 2010a,b). The taxonomy of this species has changed in the recent past (STEINWARz & SCHNEIDER, 1991; NOUIRA, 2001) from its former names Rana perezi (Seoane 1885) and R. ridibunda (Pallas 1771). BUCKLEy et al. (1994, 1996) and ARANO et al. (1998) distinguished between Iberian green frogs (Pelophylax perezi) and West African green frogs (P. saharicus), and within the latter identified two distinct clades separated by the river Moulaya: P. saharicus saharicus in Algeria and P. s. riodeoroi in Morocco. A recent morphological study described significant differentiation among Tunisian populations of P. saharicus (AMOR et al., 2009). However, using mitochondrial markers, AMOR et al. (2010a,b) revealed low genetic variation and the absence of structure within the species in Tunisia.

Bufo spinosus Daudin, 1803, the common toad, is confined to mountainous regions of northwestern Tunisia. A recent phylogeographic study, covering the entire distribution of the species complex, suggested the use of B. bufo ssp. for the African population and that this population might include two different subspecies, one in the Western Maghreb and another in the Eastern Maghreb (GARCIA-PORTA et al., 2012).

However, further studies have discovered that populations from northern Africa, as well as those from the Iberian Peninsula and southern France constitute a different species, B. spinosus (RECUERO et al. 2012; ARNTzEN et al., 2013). Bufo spinosus inhabits forested areas between Tabarka and Ouchtata and can sometimes be found near cities (Jendouba)

and archaeological sites in Bulla Regia, both of which may constitute local refuges for many amphibian and reptilian species, but it generally avoids proximity to humans.

SICILIA et al. (2009) and BOGAERTS et al.

(2013a) reported this species near Aïn Draham in an oak forest near the reservoir of Beni M’tir; BEN HASSINE & NOUIRA (2012a,b) also mention Beni Mtir, Ghardimou, and El Feija. Population densities were very low. In addition to localities specified by previous authors, we add maritime pine forests west of Melloula, mixed oak (zeen and cork oak) forests east of Tabarka, and oak forests south of Nefza (Bellif forests).

Amietophrynus mauritanicus (Schlegel, 1841), the Mauritanian toad, is an endemic species of the Maghreb. During our fieldwork we observed this species to be present in low densities throughout Tunisia where it inhabits rocky areas, meadows, bushes, cultivated fields, and some urban environments (Gafsa). In the south it is confined to the oases of Gafsa, Chott El Djerid, Tozeur, Kebili, and Ben Gardane (BOULENGER, 1891; JOGER, 2003; AMOR et al., 2007; SICILIA et al., 2009).

Bufotes boulengeri (Lataste, 1879), Boulenger’s toad, has recently become better understood in a phylogenetic context.

Previously considered a member of the Palearctic green toad complex as Bufo viridis, recently it has been reassigned independent species status based on mitochondrial DNA data (see STöCK et al., 2006, 2008b and BEUKEMA et al., 2013 for details). It is widely distributed throughout Tunisia and inhabits forest, meadow, and steppe environments (AMOR et al., 2011). Resistant both to

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drought and saline conditions, it prefers open terrain near water courses but in arid areas it lives close to irrigation ditches, springs, and oases (AMOR et al., 2011).

According to SICILIA et al. (2009), the southernmost breeding site is a temporary stream in the rocky desert (Hamada) near Tataouine. The species seems to be quite common on the Tunisian islands of Kerkennah and Djerba (STöCK et al., 2006; BEN HASSINE & NOUIRA, 2012b). Recent morphometric study of Tunisian Boulenger’s toad reported clinal variation in body size and weight that might result from phenotypic plasticity correlated with local environmental factors (AMOR et al., 2011).

The North African Fire Salamander, Salamandra algira (Bedriaga, 1883), occurs in isolated populations throughout the northern mountain ranges of north-western Africa (SCHLEICH et al., 1996). BLANC (1935) mentioned that S. algira might occur in Tunisia, as its type locality is found nearby in Algeria.

Despite the fact that BLANC (1935) encouraged searches for S. algira in the Khroumirie region, no subsequent records were provided.

Recently, after field trips conducted in northeastern Tunisia, BOGAERTS et al. (2013b) found no indications for the presence of S. algira in Tunisia. Additionally, phenotypic and morphological examinations of “Tunisian” S. algira museum specimens originating from the zoologisches Forschungsmuseum Alexander Koenig (zFMK), Germany, were carried out. The zFMK specimens of S. algira turned out to be most likely middle or eastern European Salamandra salamandra. These results do not support earlier statements on the presence of the species in Tunisia.

HABITAT DIVERSITy AND CURRENT STATUS

Northern localities Habitat diversity is highest between the Medjerda Mountains in the west and Cap Bon Peninsula in the east. Northwestern Tunisia (Khroumirie and Mogod regions) has the highest rainfall (650-1500 mm / year) (OMRANI & OUESSAR, 2008) and is the most humid and temperate portion of the country, dominated by forests of natural cork (Quercus suber) and zeen (Quercus canariensis) (LE FLOC’H et al., 2010). The northwest, with two national parks and four natural reserves, provides appropriate habitats for populations of all Tunisian amphibian species. Best known are the national parks, from which six species are reported (KAREM, 2003; SICILIA et al., 2009; BEN HASSINE & NOUIRA, 2012a,b; BEN HASSINE et al., 2013) but species commonly found in other parts of North Africa, such as B. spinosus and H. meridionalis, have not been found in either northern park or in the south of Tunisia.

Northern Tunisia is continuing to experience increasing rural populations with high human densities of 173-256 inhabitants / km2) (COELHO et al., 1999; GAFSI et al., 2008). Intense human activity and population growth over the past century have led to deforestation for agriculture and industry, overgrazing, forest fires, and pollution, resulting in significant loss of amphibian habitat (BOUSSAïD et al., 1999). The plain of Tunis suffers fragmentation of habitat resulting from urbanization, industrial pollution, and waste management. Many artificial lakes and dams have been created in the west in the

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past twenty years; while the water is used primarily for agriculture and some artificial wetlands may dry in summer, these artificial sites provide refuges and breeding areas for amphibians in a country where water is an important variable influencing amphibian survival. Natural habitats, however, often are damaged during construction because of alteration of the courses of rivers and streams.

Introduction of several species of fish (Mugil cephalus, Liza ramada, Rutilus rubilio, Scardinius erythrophtalmus, Gambusia affinis) into new dams may also lead to predation, mostly on eggs and larvae (GHRAB & BOUATTOUR, 1999; AMOR et al., 2009; BEN HASSINE & NOUIRA, 2012a). The impact of these lakes on local amphibian populations is yet to be studied.

Severe drought in 1987-1988 and 19881989 exacerbated habitat degradation in the wetlands on Cap Bon Peninsula (SMART & HOLLIS, 1989). At one site, Azmour, we found several P. saharicus specimens displaying morphological abnormalities (missing digits), probably stemming from intensive agricultural activity. In the same region, BEN HASSINE et al. (2011) reported high rates of malformation in populations of P. saharicus and D. pictus inhabiting an artificial dam (“lebna”).

Central localities Habitat destruction in this region is also increasing as a result of urban and industrial development. We observed high mortality of amphibians and reptiles on roadways throughout all visited localities; concentration of the textile industry in the Sahel region (Moknine, Monastir, Ksarhlel, and Sousse) has likely contributed to declines in species

abundance that we noted during field trips (2004-2013). In fact, disposal of large amounts of industrial waste at breeding sites caused massive pollution (CAR / PAP, 2005).

Southern localities The scarcity of suitable habitat for amphibians in southern Tunisia (AMOR et al., 2009, 2010a,b,c, 2011) is due both to natural and human causes: an increase in temperature, a decrease in annual rainfall (ALOUI, 2010) and, thus, an increase in the intensity of drought on the one hand, and the expansion of human activity on the other. Elevated temperatures can lead to early desiccation of breeding ponds and subsequent mortality of eggs and tadpoles and may also result in mortality of adults due to the increased rate of water loss associated with dry conditions (BLAUSTEIN et al., 2010). However, in southern agricultural regions where natural wetlands are scarce, irrigation channels may represent important breeding habitats for amphibians. In fact, we observed that all amphibian species were breeding in these man-made habitats.

Habitat fragmentation in extensive areas is also a significant negative factor influencing amphibian survival (BLAUSTEIN et al., 1994; FISHER & SHAFFER, 1996; GILLESPIE & HOLLIS, 1996; HECNAR & M’CLOSKEy, 1996). Plantations established on weakened soils in Gafsa are fragmenting the land and many natural water sources have run dry because of agricultural activities. An important problem facing amphibians in this area, however, is pollution of remaining freshwater and terrestrial habitats by mineral mining and wastewater (commonly known as

AMPHIBIAN STATUS IN TUNISIA

“margine”) from olive mills. Tailings from phosphate mining have polluted the Bay of Gafsa (Gafsa, Mitlaoui, Moularayes, Redaief, and Lala), thereby threatening coastal and fishing waters (Gabès and Sfax) and underground aquifers. The average volume of “margine” produced annually, at Sfax, during extraction of olive oil is estimated at 700 000 m3 (0.7 m3 / ton of fresh olives). Although its effects on the environment through pollution, corrosion, and blocking of sewage pipes have not been thoroughly documented, we have observed a

b

Figure 1: “Margine” waste generated during the process of olive (Olea europaea) oil extraction. (a) Ain Essoltan. (b) Gafsa (Oasis Nord).

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large quantities of “margine” and other kinds of waste being released into natural habitats (Fig. 1). Other sources of pollution are cement plants, chemical (M’dilla, Guetar, and Ksar-Gafsa) and steel manufacturing plants and petroleum refineries (HAMzA-CHAFFAI, 1993; HAMzA-CHAFFAI et al., 1997; SERBAJI, 2000; SMAOUI-DAMAK et al., 2003).

Discoglossus pictus has been found in the Oued el Ferd, Nefta (BOULENGER, 1891) and in the oases of the Chott El Djerid (MAyET, 1903). The southernmost sites where the species occurred were irrigation canals in Chott El Djerid and also in Chinini oasis near Gabés; in the same area from which it was recorded by Busack in March, 1972 (BUSACK, 2006), and by SICILIA et al. (2009). Discoglossus pictus was reported to occur in Gafsa, Kebili, and Kettana (BEN HASSINE & NOUIRA, 2009, 2012b; AMOR et al., 2010c,d). SCHNEIDER (1978) reported the occurrence of A. mauritanicus on the northern border of the Sahara Desert. Recent studies reveal that this species is confined to oases, especially Tozeur and Gafsa (JOGER, 2003; AMOR et al., 2007; SICILIA et al., 2009; BEN HASSINE & NOUIRA, 2012b). Bufotes boulengeri and P. saharicus appear remarkably adapted to extreme conditions in the southern part of Tunisia, occurring in irrigation channels and agricultural reservoirs in spite of high temperatures and elevated salinity (Tozeur, Ras El Ain). Plasticity in the annual reproductive cycle of P. saharicus (ESTEBAN et al., 1999), coupled with predation on tadpoles and juveniles of B. boulengeri, contribute to this species being the dominant amphibian in the south (MEDDEB & CHENITI, 1998).

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THREATS TO SURVIVAL In general, Tunisians do not like amphibians and avoid any contact with them. Toads are particularly disdained because of their large size and rough skin. Few people exhibit fear of these animals and amphibians are not deliberately killed unless found in close proximity to gardens and houses. No Tunisian species are objects of local trade or exploitation except, perhaps, frogs (P. saharicus mostly) used as model animals in the educational system.

In summary, major threats to amphibian survival in Tunisia currently include: - Deforestation and destruction of natural vegetation close to watercourses and ponds.

The decrease in natural vegetation is continuing, and large portions of natural forests are degraded. Hyla meridionalis, in particular, is negatively affected by such practices, and many local populations have declined or disappeared in the past few years because of habitat loss.

- Desiccation of wetlands, ponds, and meadows (El Mnagaa) due to agricultural activity and urban extension, especially in southern Tunisia (Ain Essoltan) (BEN AMOR, 2010).

- Transformation, fragmentation, and destruction of suitable natural habitat due to grazing, farming, and urbanization.

Ecosystems have been changed dramatically during the past century, and the phenomenon is not likely to end in the near future. Plowing may constitute destruction of the habitat of P. nebulosus because this species aestivates in the soil during summer. In regions where intensive agricultural activity occurs, newts are restricted to the margins of cultivated land where soil is not turned over.

- Pollution derived from industry, such as mining (Gafsa), petroleum (Sfax), and textile

production (Monastir), or agriculture (Cap Bon) pose risks to freshwater and to the equilibrium of the ecosystem.

- Road kills: large numbers of amphibians, mainly toads, are killed on roads during the breeding season and after rains. Amphibians are constrained to move within their home ranges and must often cross roads, exposing them to vehicular traffic. There is no system of tunnels allowing safe movement from one place to another along the Tunisian national network of routes and highways.

CURRENT STATUS The network of protected areas in Tunisia is comprised of 17 national parks and 27 natural reserves, four faunal reserves, and 38 humid areas (Ramsar). During the past two years, many of these protected areas have been subjected to numerous degradations (e.g. cutting trees, fires, poaching) that have many consequences for the fauna inhabiting them.

Prior studies by SICILIA et al. (2009) and BEN HASSINE & NOUIRA (2012b) evaluated the conservation status of Tunisian amphibians.

In addition, we carried out recent fieldwork in more than 30 localities including different aquatic and terrestrial habitats (Table 1) and covering the entire speciesâ&#x20AC;&#x2122; ranges (AMOR et al., 2007, 2009, 2010a,b,c,d,e, 2011). On the basis of these surveys, we noted that D. pictus, P. saharicus, B. boulengeri, and A. mauritanicus are common and do not appear threatened, which, with the exception of D. pictus, accords with the observations made by BEN HASSINE & NOUIRA (2012b). On the other hand, species like B. spinosus, H. meridionalis, and P. nebulosus were believed to be represented only at a few scattered localities, although

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recent intensive surveys like those by SICILIA et al. (2009) and BEN HASSINE & NOUIRA (2012a,b) have confirmed their presence in some new localities, revealing a more continuous distribution. In the network of protected areas, no status report concerning amphib-

ian populations has been completed, and available data are not sufficient to provide an accurate status report for all species.

Salamandra algira, however, has been determined not to occur within Tunisia’s borders (BOGAERTS et al., 2013b).

Table 1: Geographic information and species detected in the localities recently surveyed. Pn: Pleurodeles nebulosus, Dp: Discoglossus pictus, Am: Amietophrynus mauritanicus, Bsp: Bufo spinosus, Bbo: Bufotes boulengeri, Hm: Hyla meridionalis, Ps: Pelophylax saharicus.

Region

Locality

Latitude (N)

Longitude (E)

Elevation (m)

Observed species

North

Azmour Beja Ghar Dimaou Grombalia Hammamet Kelibia Korba Lebna (1) Lebna (2) Nabeul Oued El Maleh Beja Bizert Barbra dam Oued Ezzarga Tunis

36°55’05.32’’ 36°43’58.48’’ 36°26’59.37’’ 36°36’10.95’’ 36°22’36.76’’ 36°50’58.75’’ 36°33’53.84’’ 36°44’27.08’’ 36°44’26.83’’ 36°27’32.37’’ 36°41’19.81’’ 37°19’45.31’’ 36°44’02.00’’ 36°38’34.22’’ 36°52’20.21’’

11°00’22.20’’ 9°11’00.69’’ 8°25’43.60’’ 10°29’38.41’’ 10°32’20.36’’ 11°06’49.49’’ 10°51’36.28’’ 10°55’20.03’’ 10°55’19.70’’ 10°44’07.44’’ 9°14’19.64’’ 9°48’50.87’’ 8°32’08.00’’ 9°12’59.33’’ 10°10’32.54’’

95 249 449 45 3 4 0 13 12 39 154 29 176 302 30

Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Pn, Dp, Am, Bsp, Bbo Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Hm, Ps Pn, Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Hm, Ps Pn, Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps

Centre

Kairouan (1) Kairouan (2) Kasserine Kasserine el Arich Monastir 1 Monastir 2

35°40’13.00’’ 35°43’22.02’’ 35°10’25.93’’ 35°12’00.61’’ 35°45’33.04’’ 35°42’03.04’’

10°5’57.72’’ 10°5’55.12’’ 8°49’36.37’’ 8°49’13.30’’ 10°48’49.35’’ 10°46’00.12’’

62 65 726 633 24 22

Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps

South

Ain Essoltan Ben Garden Gabès (Chenini) Gafsa Gafsa (Oasis Nord) Gafsa (Oasis Sud) Djerba Kebili Nefta Oued El Maleh Gafsa Tamerza Oasis 1 gk Tamerza Oasis 2 pk Tozeur Ras El Ain

34°23’15.16’’ 36°22’36.76’’ 33°52’33.59’’ 34°23’43.41’’ 34°23’12.21’’ 34°23’21.18’’ 33°49’40.70’’ 33°41’22.06’’ 36°50’58.75’’ 34°23’09.02’’ 34°23’04.68’’ 34°23’06.66’’ 33°55’20.59’’

8°49’42.13’’ 10°32’20.36’’ 10°04’39.68’’ 8°46’51.35’’ 8°46’12.15’’ 8°47’00.50’’ 11°01’04.83’’ 8°58’17.82’’ 11°06’49.49’’ 8°49’11.40’’ 7°56’24.36’’ 7°55’19.23’’ 8°07’58.93’’

278 3 44 270 271 283 0 38 4 270 291 270 92

Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps Dp, Am, Bbo, Ps

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All aspects of the biology and life history of amphibians in Tunisia require additional study and protection-oriented action. Priority should be given to localized populations and species with restricted ranges for implementation of conservation measures in the near future. In addition, implementation of stricter policies, especially for industrial and agricultural activities, is necessary to preserve the Tunisian amphibian fauna. Finally, there is a need to increase civic awareness and participation among the citizens of Tunisia with regard to the importance of protecting and preserving our natural heritage in order to reduce the rate at which the ecosystem is degrading.

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Basic and Applied Herpetology 27 (2013): 101-106

Chapter 28 Amphibians in Libya: a status report Adel A. Ibrahim* Department of Environmental Sciences, Faculty of Science, Suez University, Suez, Egypt. *Correspondence: Department of Environmental Sciences, Faculty of Science, Suez University, 43527 Suez, Egypt. Phone: +20-122-358-2798, Email: dolaibrahim@yahoo.com

Received: 10 January 2013; received in revised form: 29 November 2013; accepted: 9 December 2013.

Libya is mostly desert, has few water sources and only four amphibian species (all anurans) have been historically reported to occur there, although ancient reports of Hoplobatrachus occipitalis have not been confirmed in recent surveys. Amietophrynus xeros is confined to the Ghat area in the southwest, Pelophylax saharicus is restricted to the north and Bufotes boulengeri is found in various localities within the country. Although no quantitative data have been reported for amphibian population declines, some factors (habitat degradation, drought, and high temperatures contributing to disappearance of some bodies of water) seem to be behind the local decline of amphibian populations in Libya.

Key words: amphibians; conservation; Libya; population decline.

Anfibios en Libia: informe sobre su situación. Libia es mayoritariamente desierto, presenta pocas fuentes de agua y solo cuatro especies de anfibios (todas ellas anuros) se han citado históricamente, aunque las citas antiguas de Hoplobatrachus occipitalis no han podido confirmarse en muestreos recientes. Amietophrynus xeros está confinado al área de Ghat en el suroeste, Pelophylax saharicus se restringe al norte y Bufotes boulengeri aparece en varias localidades dentro del país. Aunque no existen datos cuantitativos de declives de poblaciones de anfibios, algunos factores (degradación de hábitat, sequía, y las elevadas temperaturas que contribuyen a la desaparición de algunas masas de agua) parecen estar detrás de los declives locales de poblaciones de anfibios en Libia.

Key words: anfibios; conservación; declive de poblaciones; Libia.

While most (~95 %) of the human population of Libya resides in the Mediterranean coastal region in the north, widely-scattered oases in the desert area to the south are also inhabited. Because of its vast desert and paucity of water sources Libya has only four documented amphibian species. Libyan amphibians, especially those inhabiting the south, are part of the worldwide declining amphibian phenomenon with one or more species threatened because of drastic changes in habitat (IBRAHIM, 2008). Population declines and / or extinctions throughout the country are difficult to prove, however, because of the effects of

annual variation in climate, normal fluctuation of populations, and lack of historical data.

FROST (2013) listed five species from Libya, but only three could be confirmed recently: (1) Amietophrynus xeros, which is very localized and found only near Ghat in the southwestern extreme; (2) Pelophylax saharicus, which appears to be confined to the north; and (3) Bufotes boulengeri, which is scattered throughout. Since the work of SCORTECCI (1937), these three species are the only ones reported in field-based studies (SCHNURRENBERGER, 1963; SCHLEICH, 1987; FRyNTA et al., 2000; IBRAHIM & INEICH, 2005; IBRAHIM, 2008).

This chapter should be cited as: Ibrahim, A.A. (2013). Amphibians in Libya: a status report. Chapter 28 in Part 2. Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 101-106. DOI: http://dx.doi.org/10.11160/bah.13005/

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Few articles have been published on the conservation status of Libyan amphibians. The main objectives of this study are to report on the current status of Libyan amphibians and to define the main causes for decline or extinction, in order to propose conservation measures.

recently. Extirpation of this frog from Ghat may be directly related to the disappearance of water and / or with this species’ general inability to cope with habitat variation due, in part, to its relatively large size.

Pelophylax saharicus (Boulenger, 1913)

THE AMPHIBIAN FAUNA Libyans do not discriminate among species and local Arabic names “Dhofda'a” and “Grana” (most likely derived from the Italian word “rana”) apply to all anuran taxa; taxonomy follows FROST (2013).

Hoplobatrachus occipitalis (Günther, 1858) This species was introduced to the Ghat area to control mosquitoes (SCHLEICH et al., 1996). SCORTECCI (1937) reported high abundance of this species in the Ghat area which, in addition to numerous wells, puddles, and small marshes, once formed a continuous oasis with about 20 springs within the city itself.

Presently, Ghat is no longer an oasis; with the exception of one spring still at Al-Berkah, most bodies of water have dried up. During a visit to this area in 2006 no remnant water source was observed; the whole area had completely changed because of urban expansion.

Intensive search in the Ghat area, particularly at Tunin where about 15 springs and several wells previously existed, produced no evidence of H. occipitalis. SALVADOR (1996) and RöDEL (2000) cited Libya as one of the countries where H. occipitalis was present but these reports seem to have been based on ancient literature. Therefore, the records of H. occipitalis are questionable and the presence of this species in Libya has not been confirmed

The Saharan frog has been reported in the northeast, from Barqa, Benghazi, Al-Marj, Shahhat and Al-Jabal Al-Akhdar (WERNER, 1909; GHIGI, 1920; zAVATTARI, 1922, 1937; CALABRESI, 1923; SCHLEICH, 1987; FRyNTA et al., 2000), and from Tripoli (Aïn Sarah) by WERNER (1909). IBRAHIM & INEICH (2005) reported it as common in freshwater springs and rain pools in Badr village (Nalut Province). Individuals were also collected from Aïn Al-Khenjari (8 km southeast of Badr) where they were active during part of the year, including sunny winter days. SCORTECCI (1934) cited a juvenile in Ghat, but was unable to find additional specimens despite extensive search. DUBOIS & OHLER (1995) reported the ten specimens deposited in the Museo Civico di Storia Naturale, Milan, as lost. Pelophylax saharicus has not been reported from Al-Berkah since Scortecci’s initial paper, and was not found there during the present study. JDEIDI (2008) noted a significantly different mating call in specimens from the northeast, suggesting the possibility of cryptic diversity within Libyan P. saharicus.

Amietophrynus xeros (Tandy, Tandy, Keith & Duff-Mackay, 1976) The Savannah toad is highly localized in Libya. IBRAHIM (2008) reported its occurrence in pools of local farms at Tunin and

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Figure 1: Map of Libya. 1: Brack, 2: Al-Fejij, 3: Qabroon, 4: Sabha, 5: Ghodwah, 6: Morzoq, 7: Taraghen, 8: Om Al-Araneb, 9: zowailah.

around the water station at Al-Berkah and suggested the Ghat area (Fig. 1) to be the only well-documented locality for the species in Libya. An intensive male chorus was heard in July 2006, and toads were occasionally found in swampy areas with dense vegetation at farms where it was difficult to catch an individual or to trace a toad by its call. Toads were commonly seen in highest densities just after sunset; diurnally, they concealed themselves under the vegetation stratum (up to 30 cm thick) at the bottom of the pool. In addition to intensive nocturnal activity, toads and tadpoles were observed swimming near the surface during the day, some of them close to the edges of the pool.

Bufotes boulengeri (Lataste, 1879) The Green toad is widespread, especially in the eastern part of the country and along the Mediterranean coastal belt where there is plenty of rainfall and the area is mostly green.

This species has been reported from Derna (WERNER, 1909), Al-Marj (zAVATTARI, 1922), Al-Jabal Al-Akhdar at Al-Bayda (SCHLEICH, 1987) in the northeast and in Benghazi Province (GHIGI, 1920; FRyNTA et al., 2000). Along the coast between Benghazi and Tripoli it has been recorded at Al-Khoms (ANDREUCCI, 1913) and Misratah (BOULENGER, 1914). In the extreme west it has been reported from Tripoli (WERNER, 1909; SCORTECCI, 1935), Sebratah (FRyNTA

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et al., 2000), and Badr village (IBRAHIM & INEICH, 2005). In the south, it has been reported from Al-Jofrah (Fig. 1) (zAVATTARI, 1937), Ain Ed-Dalaam, 5 km west of Sabha (Fig. 1, site 4), Brack oasis (Fig. 1, site 1) (SCHNURRENBERGER, 1963), Al-Fejij (Fig. 1, site 2) and Qabroon (Fig. 1, site 3) (FRyNTA et al., 2000). SCORTECCI (1934, 1935) reported B. boulengeri in Taraghen (Fig. 1, site 7), Morzoq (Fig. 1, site 6), Ghodwah (Fig. 1, site 5) and Al-Qatroun. IBRAHIM (2008) found a few individuals on the Taraghen agricultural project grounds and in the university dormitory in Taraghen.

Rehabilitation of the previously devastated agricultural project at Taraghen helped some individuals to survive. This toad was also common on green farms consisting of thousands of acres of cultivated vegetables, fruits, and fodder in Om Al-Araneb (Fig. 1, site 8).

THREATS, DECLINE AND CONSERVATION There are no quantitative data indicating the existence of decline or change in population dynamics of amphibians from Libya. It is clear, however, that degradation of habitat, especially in the south, has affected amphibians in this country.

Amphibians in the north are probably not as deeply threatened as in the south because gradual urban expansion is occurring mostly in the extensive green coastal sector, which has a permanent water supply. All previous herpetofaunal studies focusing on the north have reported B. boulengeri and P. saharicus, the two species currently existing there (e.g. WERNER, 1909; GHIGI, 1913; zAVATTARI, 1922; CALABRESI, 1923; S CHNURRENBERGER , 1963; S CHLEICH ,

1987; FRyNTA et al., 2000; IBRAHIM & INEICH, 2005; IBRAHIM, 2008). In the south the situation is different; amphibians are greatly threatened and already extirpated in some places. The main threat is destruction of wetland breeding sites thought to be caused by long-term climatic and environmental changes and / or a considerable lowering of the water table because of local extraction for agriculture, industry, and urban expansion.

Southern Libya is extremely dry; annual precipitation averages less than 20 mm and inter-annual variability is high (PALLAS, 1980); some areas receive no rainfall for several years at a time and, of course, without rain there is no opportunity for replenishing bodies of water. One of the causes for the disappearance of water in the south, especially in the Ghat area, is scarcity of rainfall. The south is also hot, especially during June, July, and August. In Sabha, for example, air temperature may exceed 50ยบC in summer. In addition, insolation is extreme and potential evaporation reaches, or exceeds, 4.5 m / year (HUGHES & HUGHES, 1992). Such climatic conditions likely contributed to the disappearance of some bodies of water.

The only amphibian species inhabiting the Ghat area (A. xeros) is threatened because it is confined to areas of very limited water sources in Tunin and Al-Berkah. In a similar manner, B. boulengeri populations in the Taraghen village that was once an oasis (SCORTECCI, 1934) are now threatened because they have become few in number and occur in places with a notable shortage of water.

Local human activities have also contributed to the reduction of the water table.

Currently one must dig a well at least 400 m

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deep to extract underground water in Ghat, while in Sabha the necessary depth ranges from 70 to 150 m, and occasionally from 1.5 to 2 km to get clear water (Al-Khair Saleh & Abid Ahmad, personal communication).

In some areas of southern Libya, amphibian habitats may be affected by loss of underground water as a result of the construction of the Great Man Made River, a river 1600 km long that conveys about 6.5 million cubic meters of water per day from southern aquifers to Libyans in the coastal belt. This tremendous use of underground water can result in considerable degradation of land within oases and causes severe damage to the cover of vegetation (WHITE et al., 2003).

Expansion of green fields in Om AlAraneb and zowailah (Fig. 1, site 9) has remarkably increased during the past decade.

Bufotes boulengeri could hardly find tiny pools for breeding sites in these agricultural projects watered by drip irrigation. The area of cultivated land, however, is still extremely limited compared to the vast area of surrounding desert. The small number of toads reported from agricultural projects in Morzoq and Ghodwah will be threatened if underground water decreases to the point that its extraction becomes too expensive and the necessity for alternative sources arises.

Acknowledgement I am grateful to Abid Ahmad (Faculty of Science, Sabha University) for providing facilities and data and to Roberto Sindaco (Istituto per le Piante da Legno e l’Ambiente, corso Casale, Torino) for providing essential literature for this review.

REFERENCES ANDREUCCI, A. (1913). Contributo alla fauna della Tripolitania. Bollettino della Società Entomologica Italiana 45: 185-202.

BOULENGER, G.A. (1914). Contributo allo studio della fauna libica. Materiali raccolti nelle zone di Misurata e Homs, 1912-13, dal dott. Alfredo Andreini, capitano medico. Rettili e Batraci. Annali del Museo Civico di Storia Naturale "G. Doria e R. Gestro", Genova 6: 79-80.

CALABRESI, E. (1923). Missione zoologica del Dr. E. Festa in Cirenaica. Bollettino dei Musei di Zoologia e Anatomia Comparata della R. Università di Torino 38: 1-28.

DUBOIS, A. & OHLER, A. (1995). Frogs of the subgenus Pelophylax (Amphibia, Anura, genus Rana): a catalogue of available and valid scientific names, with comments on name-bearing types, complete synonymies, proposed common names, and maps showing all type localities. Zoologica Poloniae 39: 139-204.

FROST, D.R. (2013). Amphibian Species of the World: an Online Reference, v. 5.6.

American Museum of Natural History, New york, USA. Available at http://research.amnh.org/herpetology/am phibia. Retrieved on 11/07/2013.

FRyNTA, D.; KRATOCHVíL, L.; MORAVEC, J.; BENDA, P.; DANDOVÁ, R.; KAFTAN, M.; KLOSOVÁ, K.; MIKULOVÁ, P.; NOVÁ, P. & SCHWARzOVÁ, L. (2000). Amphibians and reptiles recently recorded in Libya. Acta Societatis Zoologicae Bohemiae 64: 17-26.

GHIGI, A. (1913). Materiali per lo studio della fauna libica. Memorie della Reale Accademia delle Scienze dell’Istituto di Bologna, Classe di Scienze Fisiche, Sezione delle Scienze Naturali 6: 251-296.

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GHIGI, A. (1920). Vertebrati di Cirenaica raccolti dal Prof. Alessandro Ghigi nella escursione organizzata dal Touring Club Italiano, 15–24 Aprile 1920. Memorie della Reale Accademia delle Scienze dell’Istituto di Bologna, Classe di Scienze Fisiche, Sezione delle Scienze Naturali 7: 195-212.

HUGHES, R.H. & HUGHES, J.S. (1992). A Directory of African Wetlands. IUCN, UNEP, and WCMC, Gland, Switzerland, Nairobi, Kenya, and Cambridge, United Kingdom.

IBRAHIM, A. (2008). Contribution to the herpetology of southern Libya. Acta Herpetologica 3: 35-49.

IBRAHIM, A. & INEICH, I. (2005). Additional records to the herpetofauna of Nalut Province, Libya. African Herp News 38: 2-9.

JDEIDI, T.B. (2008). Structure and variation of Rana saharicus mating calls in Libya, In The Sixth World Congress of Herpetology.

Manaus, Brasil.

Available at http://www.intronet.com.br/clientes/rep/ index2.php?var=viewAbstract&id=65.

Retrieved on 12/09/2013.

PALLAS, P. (1980). Water resources in the Socialist People’s Libyan Arab Jamahiriya, In M.J. Salem & M.T. Busrewil (eds.) The Geology of Libya. Second Symposium on the Geology of Libya. Faculty of Science, University of Al-Fateh, Tripoli, Lybia, September 16-21, 1978. Academic Press, London, United Kingdom, pp. 539-591.

RöDEL, M.O. (2000). Herpetofauna of West Africa, Vol. I. Amphibians of the West African Savanna. Edition Chimaira, Frankfurt, Germany.

SALVADOR, A. (1996). Amphibians of northwest Africa. Smithsonian Herpetological Information Service 109: 1-43.

SCHLEICH, H. (1987). Contribution to the herpetology of Kouf national park and adjacent area. Spinixia 10: 37-80.

SCHLEICH, H.; KäSTLE, W. & KABISCH, K. (1996). Amphibians and Reptiles of North Africa. Koeltz Scientific Publishers, Koenigstein, Germany.

SCHNURRENBERGER, H. (1963). Fishes, amphibians, and reptiles of two Libyan oases. Herpetologica 18:270-273.

SCORTECCI, G. (1934). Cenni sui risultati di una campagna di ricerche zoologiche nel Fezzan. Natura, Rivista di Scienze Naturali 25: 93-103.

SCORTECCI, G. (1935). Cenni sugli anfibi della Tripolitania. Atti Secondo Congresso di Studi Coloniali, Firenze 13: 159-165.

SCORTECCI, G. (1937). Il Saharo Italiano. 1.

Il Fezzan e Oasi di Gat. La fauna del Fezzan. Reale Società Geografica Italiana, Roma 15: 211-239.

WERNER, F. (1909). Reptilien, Batrachier und Fische von Tripolis und Barka. Zoologische Jahrbücher (Systematik) 27: 595-646.

WHITE, K.; BROOKS, N. P. J.; DRAKE, N. A.; CHARLTON, M. & MCLAREN, S. J. (2003). Monitoring vegetation change in desert oases by remote sensing; a case study in the Libyan Fazzan. Libyan Studies 34: 153-166. zAVATTARI, E. (1922). Vertebrati di Cirenaica raccolti dal generale medico prof. Francesco Testi. Atti della Società dei Naturalisti e Matematici di Modena 8: 13-22. zAVATTARI, E. (1937). I Vertebrati della Libia, In Festschrift zum 60 Geburstage von Professor Dr. Embrik Strand, vol. 2.

University of Latvia, Riga (Izdevnieciba "Latvija"), pp. 526-532.

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Chapter 29 Amphibians of Egypt: a troubled resource Adel A. Ibrahim Department of Environmental Sciences, Suez University, Suez, Egypt. *Correspondence: Department of Environmental Sciences, Faculty of Science at Suez, Suez University, 43527 Suez, Egypt. Telephone: +20 1204800096, Email: dolaibrahim@yahoo.com

Received: 10 January 2013; received in revised form: 16 December 2013; accepted: 6 January 2014.

Amphibians in Egypt are represented by only nine species. Some species (Amietophrynus regularis, Bufotes boulengeri, Ptychadena mascareniensis, and Pelophylax bedriagae) are well-known and common. Distributions of Duttaphrynus dodsoni and Hyla savignyi are limited, Amietophrynus kassasii is common and restricted while Ptychadena schillukorum appears uncommon and localized. Egyptian amphibians are, in part, poorly studied; some are threatened, others have declined or disappeared at various localities. Over-harvesting, habitat destruction, predation, overuse of pesticides, and road-kills are main causes of population decline. In 2010 the Egyptian government issued a resolution prohibiting exportation of Pelophylax bedriagae taken from natural habitats for three years – at least – to allow rehabilitation of populations; the local CITES committee had previously issued a similar declaration in 2009. Limitation of quantities of Amietophrynus regularis used for dissection in Egyptian universities and scientific agencies was also requested by the Secretary of the Egyptian Environment. These decrees and declarations seem to have been successful during the past few years.

Key words: Amphibia; conservation; Egypt; population decline.

Los anfibios de Egipto: un recurso en problemas. Los anfibios en Egipto están representados únicamente por nueve especies. Algunas especies (Amietophrynus regularis, Bufotes boulengeri, Ptychadena mascareniensis y Pelophylax bedriagae) son bien conocidas y comunes. Las distribuciones de Duttaphrynus dodsoni e Hyla savignyi son limitadas, Amietophrynus kassasii es común y restricta mientras que Ptychadena schillukorum es poco común y también restricta. Los anfibios egipcios están, en parte, poco estudiados, algunos están amenazados, mientras que otros están en declive o han desaparecido en varias localidades. La sobreexplotación, destrucción de hábitat, depredación, excesivo uso de pesticidas y los atropellos son las principales causas del declive de las poblaciones. En 2010, el gobierno egipcio emitió una resolución prohibiendo la exportación de Pelophylax bedriagae capturadas en sus hábitats naturales durante tres años – por lo menos – para permitir la recuperación de las poblaciones; previamente el comité CITES local había emitido una declaración similar en 2009. Asimismo, la secretaría de ambiente de Egipto solicitó la restricción de las cantidades de Amietophrynus regularis utilizadas para disección en universidades egipcias y agencias científicas. Estos decretos y declaraciones parecen haber tenido éxito a lo largo de los últimos años.

Key words: Amphibia; conservación; declive de poblaciones; Egipto.

Most of Egypt is desert, and frogs inhabiting Egypt must share water resources with humans. Populations, both of humans and anurans, are concentrated along the River Nile Valley and Delta (which together represent less than 5% of Egypt's total area) and most anuran species are threatened. The paucity of suitable frog habitat, coupled with

the need for cohabitation with humans, may ultimately lead to the extinction of one or more species in many places in Egypt.

Egypt has a small (nine species), poorly-studied, amphibian fauna whose current status and need for conservation are not well known. Four species (Amietophrynus regularis, Bufotes boulengeri, Ptychadena mascareniensis, and Pelophylax

This chapter should be cited as: Ibrahim, A.A. (2013). Amphibians of Egypt: a troubled resource. Chapter 29 in Part 2. Mauritania, Morocco, Algeria, Tunisia, Libya and Egypt in Vol. 11. Conservation and Decline of Amphibians: Eastern Hemisphere of the series Amphibian Biology. Basic and Applied Herpetology 27: 107-117. DOI: http://dx.doi.org/10.11160/bah.13007/

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bedriagae) are considered relatively widespread and common, and three (Pelophylax saharicus in the west at Siwa Oasis [Fig. 1, site 2], Duttaphrynus dodsoni in the extreme southeast at Jabal Elba [Fig. 1, site 26], and Hyla savignyi in the extreme northeast of the Sinai Peninsula) are restricted to small areas. Amietophrynus kassasii is common and restricted, while Ptychadena schillukorum appears rare and localized (BAHA EL DIN, 2006). The goal of this contribution is to assess potential threats, current status, and distribution of Egyptian amphibians in order to recommend conservation management strategies.

THE FAUNA The taxonomy for this study follows Frost (2013).

Amietophrynus kassasii (Baha El Din, 1993).

Local name: Dofda'a Qassas.

Nile Valley Toads, previously identified as Bufo vittatus in Egypt (ANDRE 1909; FLOWER 1933), occur in the Nile Valley and Delta and in the Fayoum (Fig. 1, site 20) Depression.

SABER (2002) reported dense populations in bodies of freshwater south of Lake Burullus (Fig. 1, site 5). BAHA EL DIN (2006) suggested this species was common but localized and assumed it spread northward along reed swamps on both banks of the River Nile and its branching channels after construction of the Aswan Dam in the extreme south. It is recorded upstream as far as Luxor (Fig. 1, site 23).

Amietophrynus kassasii is mostly aquatic and is found in densely vegetated shallow or deep water, reed swamps, rice fields, overgrown canals, and water ways. It is seen only occasionally on land (BAHA EL DIN, 2006).

Figure 1: Map of Egypt and sites referred in the text. 1: As-Salloum; 2: Siwa Oasis; 3: Burg Al-Arab; 4: Alexandria; 5: Lake Burullus; 6: Ras El Barr; 7: Dumyat; 8: Faraskur; 9: Shirbin; 10: Lake Manzala; 11: Port SaĂŻd; 12: Al-Qantara; 13: Ismailia; 14: Meet Abul Koum Al Jadidah; 15: Bitter Lakes; 16: Suez; 17: Al-Arish; 18: Sheikh zowayid; 19: Rafah; 20: Fayoum; 21: Suhag; 22: Qena; 23: Luxor; 24: Edfu; 25: Aswan; 26: Jabal Elba.

Amietophrynus regularis (Reuss, 1833). Local name: Ad-Dofda'a Al-Masreyya Ar-Raqtaâ&#x20AC;&#x2122;a.

Egyptian Toads are very common around creeks, ponds, farms, and houses. They are found in the Nile Delta (especially AshSharqeyya, Ad-Daqahleyya, Al-Gharbeyya, Al-Qalubeyya, and Kafr Ash-Sheikh Governorates); the Nile Valley from upstream of Dumyat (Fig. 1, site 7) down to Abu Simbel south of Aswan City (Fig. 1, site 25); in Fayoum (Fig. 1, site 20); along the northwestern coast from Alexandria (Fig. 1, site 4) westward to As-Salloum (Fig. 1, site 1) near the border with Libya (ANDERSON, 1898; FLOWER, 1933; MARX, 1968;

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MICHAEL et al., 1992; BAHA EL DIN, 2006); at Lake Burullus (Fig. 1, site 5) (SABER, 2002); in newly-reclaimed areas in the western coastal desert (SALEH, 1997) and in Western Desert oases (BAHA EL DIN, 2006); the Suez Canal zone, and recently in Sinai 20 km west of Al-Arish (Fig. 1, site 17) (IBRAHIM, 2001a).

Very common around freshwater irrigation canals on the west bank of the Suez Canal from Port SaĂŻd (Fig. 1, site 11) to Suez (Fig. 1, site 16), this toad is often heard calling in gardens and around houses. Following introduction of water from the River Nile it has also become widespread on the east bank of the Suez Canal, especially in green fields east of the Bitter Lakes (Fig. 1, site 15) that extend up to ten km into Sinai (IBRAHIM, 2013).

Bufotes boulengeri (Lataste, 1879). Local name: Dofda'a Khadra.

The Green Toad occurs mainly in northern Egypt, but is infrequently found from Rafah (Fig. 1, site 19) at the northeastern extremity of the country to As-Salloum (Fig. 1, site 1) in the extreme west (BAHA EL DIN, 2006). It has been recorded from Lake Burullus (Fig. 1, site 5); Fayoum (Fig. 1, site 20); Alexandria and its environs (Fig. 1, site 4); Burg Al-Arab (Fig. 1, site 3); and Western Desert oases (FLOWER, 1933; MARX, 1968; MICHAEL et al., 1992; SALEH, 1997; SABER, 2002: Annex 6). MARX (1968) reported it from Al-Qantara (Fig. 1, site 12) and Anderson (1898) reported finding this species in Luxor, but there has been no record of this species in Upper Egypt since his report.

SALEH (1997) recorded this species from the Suez Canal zone but did not cite an exact

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locality; occurrence in the Suez Canal zone is doubtful. The only taxon of the family Bufonidae present on both sides of the Suez Canal is A. regularis (IBRAHIM, 2013), and A. regularis is not known to occur in sympatry with B. boulengeri (BAHA EL DIN, 2006). The local record from Shirbin (Fig. 1, site 9) in the Nile Delta (MARX, 1968) is also incorrect; this town has been visited many times since, and no green toads were found.

Amietophrynus regularis, along with Ptychadena mascareniensis, is, however, found there (personal observation).

In North Sinai, B. boulengeri is common, and found in small bodies of water, ponds, and irrigating freshwater creeks in Al-Arish (Fig. 1, site 17), Sheikh zowayid (Fig. 1, site 18), Rafah, and Sad Ar-Rawafaâ&#x20AC;&#x2122;a (HART, 1891; SCHMIDT & MARX, 1956; WERNER, 1982; GHOBASHI et al., 1990).

Duttaphrynus dodsoni Boulenger, 1895. Local name: Dofda'a Elba.

Dodson's Toad was first reported from Jabal (Mount) Elba (Fig. 1, site 26) at the extreme southeastern corner of Egypt (SCHMIDT & MARX, 1957). It is considered to be confined to this area, but southern Egypt has not been thoroughly surveyed and this toad may be found west of Jabal Elba at the Sudanese border. BAHA EL DIN (2006) observed that toads often perch in high positions on rocks and small boulders while looking for moving prey underneath. He also suggested that during long-lasting droughts they probably move to higher elevations where there is higher humidity, and that they can be found during winter and spring in or near wells at night.

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Hyla savignyi Audouin, 1827. Local name: Dofda'a Ash-shajar.

I discovered Savigny's Treefrog in Egypt for the first time in 1992 (BAHA EL DIN, 1994).

This species was confined to local farms, especially those near the beach, in Rafah (Fig. 1, site 19) at the Egypt-Israel border and in Sheikh zowayid (Fig. 1, site 18) where Savigny's Treefrogs were usually seen on trees on both banks of man-made canals (locally known as Thameela), and occasionally on the ground near shallow bodies of water.

The treefrog in northern Sinai is confined to an area not extending more than 20 km west of Rafah. Treefrogs are not found among peach (Prunus persica), almond (Amygdalis communis) or grape (Vitis vinifera) crops in Rafah (personal observation) because these crops depend upon rainwater which is relatively scant. Recently, however, a large number of drip-system-irrigated farms and orchards has been established from Rafah up to 10 km south and west of the city. While areas of pipe leakage and small man-made irrigation pools of varying size provide limited water resources for treefrogs, populations are large enough that local people are irritated by the noise made by calling frogs. Vocalizations increased in some areas and decreased in others as I drove southwest of Rafah; frogs were numerous in mandarin (Citrus x nobilis) orchards which represent almost 80% of these farms, and less numerous in olive (Olea europaea) and apple (Pyrus malus) orchards; olives and apples do not require as much water as mandarins.

I visited the agricultural project at AlKharrouba, about 15 km east of Al-Arish City (Fig. 1, site 17) in June 2009, and no treefrogs were seen despite the presence of water and

dense vegetation around both banks of the 450-m man-made canal. The canal depends upon a pump station which has been unused and neglected for a relatively long time, and salinity in the creek has increased to the point that it is no longer suitable for the frogs. While it has been assumed this frog might be found in Al-Arish (BAHA EL DIN, 2006), the AlKharrouba area apparently acts as a barrier to treefrog distribution as extensive surveys from Al-Kharrouba westward to Al-Arish did not produce this species.

Destruction of habitat and urbanization, especially at the beach, do not allow this species to spread west of Sheikh zowayid. An adult treefrog captured from the village of ArRoudha, 50 km west of Al-Arish, is deposited in the herpetological collection of zaranik protectorate. The collector assured me the specimen was captured in the village, but the treefrog, which may have been introduced to the area, no longer occurs there.

Pelophylax bedriagae (Camerano, 1882).

Local name: Gazza'a Akhdar.

Currently recorded from the Nile Valley and Delta, extreme northeast Sinai, Fayoum (Fig. 1, site 20) and Luxor (Fig. 1, site 23) (BAHA EL DIN, 2006), the Levant Green Frog was first recorded from Egypt when specimens were found in Giza by MARX (1968). BAHA EL DIN (2006) suggested that successive ecological changes downstream from the high Aswan Dam may be related to the occurrence of P. bedriagae in Upper Egypt. It is a common species at Lake Burullus (Fig. 1, site 5) (SABER, 2002: Annex 6).

This species was collected for the first time from Rafah (Fig. 1, site 19), North Sinai in 1987 (IBRAHIM, 2011). In Sinai, however,

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P. bedriagae is currently on the verge of extirpation. Once abundantly distributed in Rafah and Sheikh zowayid (Fig. 1, site 18) in the peninsula’s extreme northeast, it is now rarely observed, even during the breeding season (personal observation).

Levant Green Frogs were first observed in the Suez Canal zone six km northwest of Ismailia (Fig. 1, site 13), and a large number were heard vocalizing in natural swamps about three km southwest of Serapeum village during June, 2008. According to local people, these swamps were not present 30 years ago.

On the east bank of the Suez Canal, P. bedriagae were first recorded from a dense reed assemblage in a small swamp five km north of Ismailia East at Attaqaddom village (IBRAHIM, 2011). No additional east-bank localities for the species were listed (IBRAHIM, 2013).

This species is highly resistant to environmental pollution. In Ismailia Governorate, it has been found in a heavily littered swamp polluted by organic waste (Fig. 2). Some ponds considered the main source of mosquito proliferation in Ferdan (about 10 km north of Ismailia City) have been filled in recently.

Disappearance of ponds and urbanization of Ferdan may have caused this frog’s decline.

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Ptychadena mascareniensis (Duméril and Bibron, 1841). Local name: Gazza'a Mukhattat.

The Mascarene Ridged Frog (P. m. mascareniensis) is widespread throughout the Nile Valley and Delta. Dense populations are found in almost all Nile Delta Governorates, especially Dumyat, Ad-Daqahleyya, AlGharbeyya, Ash-Sharqeyya, Al-Menufeyya, and Al-Beheira. It is common in Lake Burullus (Fig. 1, site 5) (SABER, 2002: Annex 6) and regularly observed in the small canals irrigating cultivated fields (especially rice). It has spread upstream to Qena (Fig. 1, site 22), Edfu (Fig. 1, site 24), and Fayoum (Fig. 1, site 20) (ANDERSON, 1898; FLOWER, 1933; MARX, 1968) and has been recorded in reclaimed desert areas irrigated with Nile water (SALEH, 1997). This species is also wellknown on the west bank of the Suez Canal around Port Saïd (Fig. 1, site 11) and at Ferdan and Al-Qantara West (Fig. 1, site 12) in Ismailia Governorate, extending southwest to near Suez (Fig. 1, site 16) (IBRAHIM, 2013).

For the first time in Sinai, specimens (one each) were recorded on local farms 17 km south of Al-Arish (Fig. 1, site 17), and

Pelophylax saharicus (Boulenger, 1913). Local name: Gazza'a Sahrawy.

The Saharan Frog appears confined to the Siwa Oasis in the Western Desert (Fig. 1, site 2) (BAHA EL DIN, 2006). It is expected, however, that its range might extend further to the west, possibly to the Egypt-Libya border. It is a common frog; some individuals were captured from Siwa for identification and released at the site of capture during summer, 2007.

Figure 2: A view of a polluted natural swamp south of Ismailia.

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from Sheikh zowayid (Fig. 1, site 18). It has been suggested that these animals may have reached these areas accidentally via local transport carrying fodder and other commodities (IBRAHIM, 2001b). On the east bank of the Suez Canal this species has become common by following streams to recently cultivated lands east of Bitter Lakes (Fig. 1, site 15). Several frogs were observed and heard vocalizing in a pool alongside A. regularis at Meet Abul Koum Al Jadidah (Fig. 1, site 14) about seven km east of the Suez Canal (IBRAHIM, 2013). The local record of this species from Wadi Feiran, South Sinai, by SCHMIDT & MARX (1956) is likely to be erroneous and unreliable because this area is extremely arid and represents unsuitable habitat for the species.

Ptychadena schillukorum (Werner, 1908).

Local name: Gazza'a Sudani.

BAHA EL DIN (2005) reported the occurrence of the Schilluk Ridged Frog in Egypt based on two individuals, one from the western margin of Lake Manzala (Fig. 1, site 10) and the other from Fayoum (Fig. 1, site 20).

He provided an account for the Egyptian Nile Delta population and discussed confusion with P. mascareniensis. I visited the western area of Lake Manzala but could not locate this species. In Dumyat (Fig. 1, site 7), Ras El Barr area (Fig. 1, site 6), and Faraskur (Fig. 1, site 8) only three amphibian species are known, A. regularis, P. mascareniensis, and P. bedriagae (Gamal Abdulla, personal communication). Intensive search is needed to locate this species in view of the fact that it is localized to small areas and not well-known in Egypt (BAHA EL DIN, 2006).

THREATS, DECLINE AND CONSERVATION Ancient Egyptians have records of "the frog", finding it in shallow bodies of water around the River Nile. Toads, according to records from the Pharaohs, were so abundant that they were called "Khefen" (one hundred thousand) and the ancient Egyptians painted images of toads on the walls of temples and considered toads to be sacred. It is possible that, because of these images and a highly-visible productivity, the frog became a powerful symbol of self proliferation and regeneration of life.

The croaking of toads has always been a familiar sound to Egyptians. Two decades ago, toads were seen throughout the length of the River Nile and its Delta. Choruses were heard wherever a source of water was found, much to the annoyance of the people living nearby.

Recently, however, decrease in population numbers has become evident even to the public, and the sound has become less intensive than before.

The reasons for declining amphibian populations in Egypt can be summarized as follows: Over-harvesting One of the major threats confronting A. regularis and P. bedriagae is annual harvesting for teaching, research, and exportation. Up to two million A. regularis are taken from the wild each year to meet the needs of Egyptian universities and scientific research centres. Unfortunately, this toad is still used for dissection and animal dealers collect both adult and young toads; many toads, especially juveniles, die from poor handling and storage. Animal dealers who provide Egyptian universities with toads emphasized that there is a remarkable decline in

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amphibian populations, and in A. regularis in particular (personal observation). It is currently difficult to meet the needs of all universities and research agencies. Rashed Refaee, an animal dealer supplying Cairo University, stated that ten years ago he used to collect 1000 frogs in one hour; today four people now spend four days to collect 140 individuals. That dealer was supplying the University with approximately 250,000 toads per year collected over a nine-month period that included the mating season.

A large number of Levant Green Frogs, P. bedriagae, is exported each year to countries where it is used for food. These frogs were removed from the wild, mostly from Lake Manzala and Lake Burullus (Fig. 1, sites 10 and 5, respectively), but substantial quantities were also collected from Nile creeks, and from irrigating canals in Upper Egypt (Suhag, Qena [Fig. 1, sites 21 and 22, respectively]). Figure 3 clearly shows variation in quantities exported between 2000 and 2009, suggesting that frog numbers have likely declined due to over harvesting. No aquaculture for breeding frogs is

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known in Egypt, but there are man-made pools used for maintaining frogs until ready for export.

One frog dealer at Lake Manzala with whom I spoke emphasized that all sizes of frogs, including juveniles, are removed from the Lake between September and June; while hunters used to catch up to two metric tons of frogs from the Lake in one day during the breeding season, it is now difficult to catch two kilograms in one day. He also stated that breeding these frogs in captivity was once attempted, but the attempt failed because the frogs decreased in size and eventually died. Animal dealers in the Suez Canal zone similarly collect a large number of frogs from natural habitats.

All anurans listed above are species of "Least Concern" according to the IUCN (STUART et al., 2008), and none is locally threatened or endangered according to CITES. While these species may be classed as "Least Concern" on the scale of all of Egypt, many local populations are severely threatened through overexploitation or other anthropogenic effects (such

Figure 3: Estimate of the number of Pelophylax bedriagae individuals removed from natural habitats for exportation between 2000 and 2009 (data courtesy of Ragi Toma).

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as filling in ponds). While no studies on amphibian conservation have evaluated the real danger and challenges these species face, the Egyptian Secretary of the Environment (2 February 2010) approved a decree prohibiting exportation of Levant Green Frogs (P. bedriagae) taken from natural habitats for a period of at least three years to allow the species to recover and reproduce. Only farm-raised frogs may be exploited after conclusion of the specified three-year period and if, after three years, hunting is allowed, it will not be permitted during the reproductive season (March to July). The local CITES committee had issued a similar decree on 15 October 2009.

In addition, the Secretary of the Environment has requested that the Secretary of Higher Education and Scientific Research evaluate reducing the quantity of Egyptian toads (A. regularis) used for dissection in Egyptian universities and scientific agencies.

Destruction of Habitat Expansion of urbanization has caused severe degradation of amphibian habitats, especially at breeding sites. In the Nile Delta a vast area of green fields has been devastated because of human expansion at the expense of water sources that originally created breeding habitat for frogs. All anurans in the Delta are affected, particularly A. regularis and P. mascareniensis.

The same situation is evident along the western portion of the Mediterranean coast, where extensive human expansion, road projects, and other anthropocentric use of land has occurred during the past few decades, and destruction of shallow bodies of fresh water has damaged habitat and caused extirpation of populations of frogs in many places.

The dramatic decline of P. bedriagae in northern Sinai can be attributed to habitat destruction due to change from furrow-irrigation to drip irrigation. Furrow-irrigation was based on the establishment of permanent underground sources (man-made canals) that allowed frogs to live and reproduce. These canals have been neglected and most have either dried up or become salty while others have been filled in. Since P. bedriagae is highly aquatic, it gradually disappeared, and H. savignyi is no longer observed in Rafah City for the same reason. No treefrogs were observed on farms near the beach or close to the border and, during summer 2009, very few individuals of P. bedriagae or H. savignyi were observed in an irrigating canal about 7 km south of Rafah or in a small canal at Sheikh zowayid. Frogs in these canals are threatened as this habitat is expected to dry up because there is no more underground water feeding it. Pelophylax bedriagae is also threatened by localized loss of habitat through drainage of wetlands along the banks of the River Nile.

Predators The invasive red swamp crayfish (Procambarus clarkii) was unwisely and irresponsibly introduced to the River Nile at Giza in 1983 and represents a serious threat to anurans (A. regularis in particular) within the river system. This New-World crayfish, free from natural predators in Egypt, has spread rapidly throughout the Nile Valley from Dumyat to Aswan and small numbers have been recently recorded in northern Sinai (IBRAHIM & KHALIL, 2009).

While this crayfish feeds mainly on fishes, snails, and plants in its natural habitat, P. clarkii sub-

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stantially reduced larval survival in all anuran species in a southwest Iberian population to which it had been introduced in 1973 (CRUz & REBELO, 2005).

The obvious decline in frog populations coincident with widespread distribution of these crayfish suggests that this predator plays a key role in Egypt as well, but as yet there has been no direct evidence of predation recorded. One animal dealer with whom I spoke, however, stated that he had to travel to Upper Egypt to collect toads because (he believes) crayfish have greatly reduced toad populations in the Nile Delta. Crayfish are considerably less expensive than shrimp and red lobster and a great effort is being made to control this invasive animal by catching and selling large quantities to Egyptian and international markets, thus attempting to minimize its effect on fish and amphibians (Magdy Khalil, personal communication).

Tadpoles and frogs are also important food items for some snakes, such as the Diced Water Snake, Natrix tessellata (SALEH, 1997), and large lizards, such as the Nile Monitor, Varanus niloticus (LENz, 2004), inhabiting Egyptian freshwater systems.

Overuse of Pesticides Pesticides are used routinely and excessively. This excessive use has contributed substantially to contamination of the wetlands in which frogs breed, and may lead to extensive destruction of eggs and tadpoles. Puddles and swamps are normally sprayed with pesticides and petroleum hydrocarbons (e.g. kerosene and crude oil) to control mosquitoes and flies and, thus, anurans and their eggs are likely affected negatively.

Road-Kills During spring and summer several dead anurans are seen on main highways and connecting roads passing through villages and green fields (personal observation).

Acknowledgement I thank Dr. Nabil Sedqi, undersecretary of agriculture for Egyptian zoo and Wildlife, Dr. Ragi Toma, manager of wildlife, for providing data on frogs exported from Egypt over the past ten years, and Dr. Adel ElGazzar for identifying plants and reviewing an early draft of this manuscript. I am grateful to Mr. Sayed zaina for accompanying me on several field trips to the Nile Delta.

REFERENCES ANDERSON, J. (1898). Zoology of Egypt, Volume First, Reptilia and Batrachia. Bernard Quaritch, London, United Kingdom.

ANDRE, A. (1909). Bufo vittatus Blgr. in 채gypten. Bl채tter f체r Aquarien - und Terrarienkunde 20: 642-625.

BAHA EL DIN, S.M. (1994). A contribution to the herpetology of Sinai. The Herpetological Society Bulletin 48: 18-27.

BAHA EL DIN, S.M. (2005). On the occurrence of Ptychadena schillukorum (Werner 1907) in Egypt. Herpetozoa 18: 178-181.

BAHA EL DIN, S.M. (2006). A Guide to the Reptiles and Amphibians of Egypt. The American University in Cairo Press, Cairo, Egypt.

C RUz , M.J & R EBELO , R. (2005).

Vulnerability of southwest Iberian amphibians to an introduced crayfish,

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Procambarus clarkii. Amphibia-Reptilia 26: 293-303.

FLOWER, S.S. (1933). Notes on the recent reptiles and amphibians of Egypt, with a list of the species recorded from that kingdom. Proceedings of the Zoological Society of London 1933: 735-851.

FROST, D.R. (2013). Amphibian Species of the World: an Online reference, Version 5.6. (9 January 2013). American Museum of Natural History, New york. Available at http://research.amnh.org/vz/herpetology/amphibia/index.html. Retrieved on 12/14/2013.

GHOBASHI, A.; ABU EGLA, M.; TANTAWy, H. & IBRAHIM, A. (1990). Herpetofaunal survey of Al-Arish area (North Sinai), with special reference to their habitat and seasonal distribution. Proceedings of the Zoological Society, Arab Republic of Egypt 21: 273-290.

HART, H.C. (1891). Some account of the fauna and flora of Sinai, Petra, and Wadi Arabah. Alexander P. Watt (for the Committee of the Palestine Exploration Fund), London, United Kingdom.

IBRAHIM, A.A. (2001a). Geographic distribution.

Bufo regularis. Herpetological Review 32: 112.

IBRAHIM, A.A. (2001b). Geographic distribution.

Ptychadena mascareniensis.

Herpetological Review 32: 115.

IBRAHIM, A.A. (2011). First record of Pelophylax bedriagae (Amphibia: Ranidae) in the Suez Canal area, Egypt. Herpetology Notes 4: 331-332.

IBRAHIM, A. (2013). The herpetology of the Suez Canal zone. Vertebrate Zoology 63: 87-110.

IBRAHIM, A.M. & KHALIL, M.T. (2009). The red swamp crayfish in Egypt (A fast spreading freshwater invasive crustacean). Centre of

Research and studies of protectorates, Ain Shams University, Cairo, Egypt.

LENz, S. (2004). Varanus niloticus, In E. Pianka, D. King & R. King (eds.)

Varanoid Lizards of the World. Indiana University Press, Bloomington, Indiana, USA, pp. 133-138.

MARX, H. (1968). Checklist of the Reptiles and Amphibians of Egypt. Special Publication, United States Naval Medical Research Unit Number Three, Cairo, Egypt.

MICHAEL, M.I.; DEKINESH, S.I. & ALy, A.H. (1992). The herpetofauna of the north western coast of Egypt. Journal of the Egyptian German Society of Zoology (Comparative Physiology) 8: 81-99.

SABER, S. (2002). Amphibians and Reptiles & Reptile and Amphibian species recorded from Burullus Protected Area. In M. Kassas (ed) Management plan for Burullus Protected Area. Med Wet Coast, Global Environment Facility & Egyptian Environment Affairs Agency, Cairo, Egypt, pp. 37-38 & Annex 6, p 112. Available at http://vinc.s.free.fr/ article.php3?id_article=159. Accessed on 02/03/2014.

SALEH, M.A. (1997). Amphibians and Reptiles of Egypt. Publications of National Biodiversity Unit No. 6, Cairo, Egypt.

SCHMIDT, K.P. & MARX, H. (1956). The Herpetology of Sinai. Fieldiana Zoology 39: 21-40.

SCHMIDT, K.P. & MARX, H. (1957). Results of the NAMRU-3 Southeastern Egypt Expedition, 1954. Bulletin of the Zoological Society of Egypt 13: 16-28.

STUART, S.N.; HOFFMANN, M.; CHANSON, J.S.; COX, N.A.; BERRIDGE, R.J.; RAMANI, P. & yOUNG, B.E. (2008). Threatened Amphibians of the World. IUCN, Gland,

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Switzerland & Conservation International, Arlington, Virginia, USA. Werner, y.L. (1982). Herpetofaunal survey of the Sinai peninsula (1967-77), with emphasis on the Saharan sand communi-

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ty. In N.J. Scott, Jr (ed.) Herpetological Communities. Wildlife Research Report 13, United States Department of the Interior, Fish and Wildlife Service, Washington DC, USA, pp. 153-161.

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Figure captions: should be typed (double-spaced) and grouped together on a page separate from the figures. They should explain with clarity all the elements in the figure. Make figures understandable without reference to the text.

Figures: illustrations, whether maps, drawings, diagrams or photographs, should be kept to the minimum needed to clarify the text. They should be numbered consecutively in Arabic numerals arranged as they are quoted in the text and submitted on separate pages (one figure per page), each bearing the figure number and, if desired (e.g. in photographs), the name(s) of the figure author(s). If good-quality versions of figures are necessary to be examined during the review process, authors will include such version in the original submission, as separate files, according to the instructions given in the next paragraph. In the text, ‘Figure’ should be abbreviated (Fig. 2) except when beginning a sentence. Authors are encouraged to use a sans serif font (Helvetica, Arial, Geneva) for all text associated with figures. The labelling must be clearly legible and stand reduction to the final print size. Include a scale of distance or dimension where appropriate.

Once the manuscript is accepted for publication, good-quality versions of figures should be submitted in their original format with a minimum resolution of 300 dpi. For figures consisting in a picture modified with symbols, text, etc., authors will be requested to send the original, unmodified, good-quality picture once the manuscript is accepted. For figures not originally in a digital format (photographs, slides, drawings) authors are recommended to use a dedicated scanner or send the original to the editors by postal mail. In these cases, the originals will be returned to authors after digitalization. Given that B&AH assumes the costs of publishing colour prints and slides, these will be accepted only when they are strictly necessary at the editors’ discretion. In some cases, colour figures can be accepted only for the digital version, being displayed in greyscale format in the printed version.

REREFENCES For references in the text give full surnames of the first author followed by the publication year and separated by a comma (Pleguezuelos, 1997). For papers with two authors, use the term “&” to separate surnames (Semlitsch & Bodie, 2003). Papers with three or more authors will be quoted with the surname of the first author followed by ‘et al.’ (note italics) (Stuart et al., 2004). To distinguish between two papers by the same author(s) in the same year use lower-case letters (a,b) after the year, without space, arranged in alphabetical order as the references are quoted in the text (Harris et al., 2004a,b). List multiple citations in chronological order, using alphabetical order for citations within the same year. Separate citations with semicolons (Tyler, 1991; Wake, 1991; Blaustein et al., 1994a,b; Stuart et al., 2004). If the citation is part of the sentence, move the surname(s) of the author(s) out of the brackets and delete the comma.

“As pointed by Pleguezuelos (1997)” “Blaustein et al. (1994a) reviewed the situation of amphibians” The reference list should include all and only the references mentioned in the text, tables and figures. Cite references in the reference list in alphabetical order according to the authors' surnames. Multiple citations for the same author should be organized as follows: single citations first (in chronological order), two-author citations second (in alphabetical order), three or more authors third (in chronological order). Spell out (i.e. do not abbreviate) the names of all journals. The references should conform to the following formats:

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Articles in periodicals: • Stuart, S.N.; Chanson, J.S.; Cox, N.A.; young, B.E.; Rodrigues, A.S.L.; Fishman, D.L. & Waller, R.W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783-1786.

• Wiens, J.J. & Penkrot, T.A. (2002). Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology 51: 69-91.

Books: • Dodd, Jr., C.K. (ed.) (2009). Amphibian Ecology and Conservation. A Handbook of Techniques.

Oxford University Press, Oxford.

• Vitt, L.J. & Caldwell, J.P. (2009). Herpetology: An Introductory Biology of Amphibians and Reptiles, 3rd ed. Academic Press, Burlington, Massachusetts.

Book chapters: • King, R.B. (2009). Population and conservation genetics, In S.J. Mullin & R.A. Seigel (eds.)

Snakes: Ecology and Conservation. Cornell University Press, Ithaca, New york, pp. 78-122.

Web pages (authors are recommended to keep the use of web pages to a minimum; use peerreviewed literature instead when possible): • IUCN (2010). The IUCN Red List of Threatened Species, v. 2010.3. International Union for Nature Conservation and Natural Resources, Gland, Switzerland. Available at http://www.iucnredlist.org/. Retrieved on 10/31/2010.

SUPPORTING MATERIAL Authors can submit with their manuscripts supporting material related to the work (additional tables and figures, detailed protocols, data logs, audio and video recordings, etc.). The supporting material will be uploaded to the online site of B&AH with a reference code that will be used to quote such material in the final version of the article. In the initial version of the manuscript, supporting material should be quoted as “SM” followed by a number according to the same format as for tables and figures. Supporting material must be submitted as independent files. Name each file with the code used in the initial version of the manuscript (SM1, SM2, etc.). Authors may also refer to supporting material available from a different online site (e.g. GenBank, MorphoBank), in which case the exact access reference will be indicated in the final version of the article.

BIOETHICAL CONSIDERATIONS Because right animal use and care is an area of major concern to the AHE, authors must guarantee that all animals used for research purposes are treated ethically and in accordance with the laws and regulations established by governmental authorities and bioethics committees of each institution.

Therefore, authors are recommended to state in the Acknowledgement section that they have followed the corresponding regulation and legislation on animal care. Authors should cite in this section the information regarding collection permits and experimental protocols approved by bioethics or animal care committees. Editors might request from authors as much information as they consider necessary to confirm the fulfilment of such premises. Failure to comply with these bioethical principles will suppose immediate rejection of the article, regardless of the reviewers’ recommendation.

Las normas de publicación en castellano están disponibles para su consulta en la página web de Basic and Applied Herpetology (http://bah.herpetologica.es/)

BASIC & APPLIED HERPETOLOGY REVISTA ESPAÑOLA DE HERPETOLOGÍA

On behalf of the Spanish Herpetological Society, the editorial board of Basic and Applied Herpetology wants to acknowledge the work of the following experts who have worked as manuscript reviewers for the elaboration of the present volume (in alphabetical order): Jihène Ben Hassine (Tunis-El Manar University, Tunisia) Lior Blank (University of Haifa, Israel) José Carlos Brito (CIBIO-Universidade de Porto, Portugal) Pierre-André Crochet (Centre d'Ecologie Fonctionnelle et Evolutive-CNRS, France) El Hassan El Mouden (Université Cadi Ayyad, Morocco) Soumia Fahd (Université Abdelmalek Essaddi, Morocco) Sarig Gafny (Ruppin Academic Center, Israel) Tarek Bashir Jdeidi (Tripoli University) Fernando Martínez-Freiría (CIBIO-Universidade de Porto, Portugal) Daniele Salvi (CIBIO-Universidade de Porto, Portugal) Boudjéma Samraoui (University of Guelma, Algeria) Neftalí Sillero (CICGE-Universidade de Porto, Portugal) Roberto Sindaco (Istituto per le Piante da Legno e l'Ambiente, Italy) Yehudah Leopold Werner (Hebrew University of Jerusalem, Israel)

AHE

© 2013