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  • Amphibian Biology

  • Amphibian BiologyEdited by

    Harold Heatwoleand

    John W. Wilkinson

    Volume 11

    Status of Conservation and Decline of Amphibians: Eastern Hemisphere

    Part 4

    SOUTHERN EUROPE AND TURKEY

  • Published by Pelagic Publishingwww.pelagicpublishing.comPO Box 725, Exeter, EX1 9QU

    Amphibian Biology, Volume 11: Status of Conservation and Decline of Amphibians: Eastern Hemisphere, Part 4: Southern Europe and Turkey

    ISBN 978-1-907807-53-4 (Pbk)ISBN 978-1-907807-54-1 (ePub)ISBN 978-1-907807-55-8 (Mobi)ISBN 978-1-78427-038-4 (PDF)

    Copyright © 2015 Pelagic Publishing

    This book should be quoted as Heatwole, H. and Wilkinson, J.W. (eds) (2015) Amphibian Biology, Volume 11: Status of Conservation and Decline of Amphibians: Eastern Hemisphere, Part 4: Southern Europe and Turkey. Exeter: Pelagic Publishing.

    All rights reserved. No part of this document may be produced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise without prior permission from the publisher. While every effort has been made in the preparation of this book to ensure the accuracy of the information presented, the information contained in this book is sold without warranty, either express or implied. Neither the author, nor Pelagic Publishing, its agents and distributors will be held liable for any damage or loss caused or alleged to be caused directly or indirectly by this book.

    British Library Cataloguing in Publication Data.

    A catalogue record for this book is available from the British Library.

    Cover image: A calling male Bombina bombina in Hungary. Photograph by Bálint Halpern.

  • Table of contents of volume 11, Amphibian Biology: Eastern Hemisphere, Part 4 (Southern Europe and Turkey)

    39 The amphibians of the Italian region: A review of conservation status 1Franco Andreone

    40 Amphibian conservation and declines in Malta 17Patrick J. Schembri

    41 Conservation and declines of amphibians in Croatia 25Olga Jovanović and Dušan Jelić

    42 Conservation and declines of amphibians in Slovenia 32David Stanković, Martina Lužnik, and Katja Poboljšaj

    43 Conservation and decline of European amphibians: The Republic of Serbia 45Jelka Crnobrnja-Isailović and Momir Paunović

    44 Amphibian declines and conservation in Montenegro 56Ruža Ćirović

    45 Status of amphibians in Bosnia and Herzegovina 62Avdul Adrović

    46 Conservation and protection status of amphibians in Macedonia 67

    Bogoljub Sterijovski

    47 Amphibians of Albania 74

    Idriz Haxhiu

    48 Declines and conservation of amphibians in Greece 80Konstantinos Sotiropoulos and Petros Lymberakis

    49 Amphibian conservation and decline in Romania 87Dan Cogălniceanu and Laurenţiu Rozylowicz

    50 Conservation and decline of amphibians in Hungary 99Judit Vörös, István Kiss, and Miklós Puky

    51 Conservation and declines of amphibians in Bulgaria 131Nikolay Dimitrov Tzankov and Georgi Sashev Popgeorgiev

    52 Amphibian conservation and decline in Turkey 140Kurtuluş Olgun and Nazan Üzüm

    53 Conservation of amphibians in Cyprus 148Petros Lymberakis, Haris Nicolaou, and Konstantinos Sotiropoulos

    Index 152

  • Contents of previous parts of volume 11, Amphibian Biology: Eastern Hemisphere

    Part 1. Asia (edited by Harold Heatwole and Indraneil Das) 2014, Natural History Publications (Borneo), Kota Kinabalu, Malaysia1 Changes in amphibian populations in the Commonwealth of Independent States

    (Former Soviet Union)

    Sergius L. Kuzmin and C. Kenneth Dodd Jr.

    2 Status of conservation and decline of amphibians of MongoliaSergius L. Kuzmin

    3 Diversity and conservation status of Chinese amphibiansJianping Jiang, Feng Xie, and Cheng Li

    4 The Conservation of Amphibians in KoreaDaesik Park, Mi-Sook Min, Kelly C. Lasater, Jae-Young Song, Jae-Hwa Suh, Sang-Ho Son, and Robert H. Kaplan

    5 Conservation status of Japanese amphibiansMasafumi Matsui

    6 Status and decline of amphibians of AfghanistanIndraneil Das

    7 Amphibians of Pakistan and their conservation statusMuhammad Sharif Khan

    8 Status and decline of amphibians of IndiaIndraneil Das and Sushil K. Dutta

    9 Sri Lankan amphibians: Extinctions and endangermentRohan Pethiyagoda, Kelum Manamendra-Arachchi, and Madhava Meergaskumbura

    10 Amphibians of the Maldives ArchipelagoIndraneil Das

    11 Status, distribution, and conservation issues of the amphibians of NepalKaran B. Shah

    12 Status of amphibian studies and conservation in BhutanIndraneil Das

    13 Status, distribution and conservation of the amphibians of BangladeshA.H.M. Ali Reza

    14 Amphibian conservation: MyanmarGuinevere O.U. Wogan

  • 15 Decline of amphibians in ThailandYodchaiy Chuaynkern and Prateep Duengkae

    16 Amphibian conservation in Vietnam, Laos, and CambodiaJodi J.L. Rowley and Bryan L. Stuart

    17 Conservation status of the amphibians of Malaysia and SingaporeIndraneil Das, Norsham Yaakob, Jeet Sukumaran, and Tzi Ming Leong

    18 Conservation status of the amphibians of Brunei DarussalamT. Ulmar Grafe and Indraneil Das

    19 Status and conservation of Philippine amphibiansArvin C. Diesmos, Angel C. Alcala, Cameron D. Siler, and Rafe Brown

    20 Human impact on amphibian decline in IndonesiaDjoko T. Iskandar

    21 Amphibians of Timor-Leste: A small fauna under pressure.Hinrich Kaiser, Mark O’Shea, and Christine M. Kaiser

    22 Status and diversity of the frogs of New GuineaAllen Allison

    Part 2. North Africa (edited by Stephen D. Busack and Harold Heatwole) 2014, Basic and Applied Herpetology, Asociación Herpetológica Española, Madrid

    23 IntroductionHarold Heatwole and Stephen D. Busack

    24 Amphibian conservation in MauritaniaJosé Manuel Padial, Pierre-André Crochet, Philippe, Geniez, and José Carolos Brito

    25 Amphibians of Morocco, including Western Sahara: A status reportRicardo Reques, Juan M. Pleguezuelos, and Stephen D. Busack

    26 Diversity and conservation of Algerian amphibian assemblagesJosé A. Mateo, Philippe Geniez, and Jim Pether

    27 Conservation status of amphibians in TunisiaNabil Amor, Mohsen Kalboussi, and Khaled Said

    28 Amphibians in Libya: A status reportAdel A. Ibrahim

    29. Amphibians of Egypt: A troubled resourceAdel A. Ibrahim

  • Part 3. Western Europe (edited by Harold Heatwole and John W. Wilkinson) 2013

    31 Infectious diseases that may threaten Europe’s amphibiansTrent W.J. Garner, An Martel, Jon Bielby, Jaime Bosch, Lucy G. Anderson, Anna Meredith, Andrew A. Cunningham, Matthew C. Fisher, Daniel A. Henk, and Frank Pasmans

    32 Conservation and declines of amphibians in IrelandFerdia Marnell

    33 Amphibian declines and conservation in BritainJohn W. Wilkinson and Richard A. Griffiths

    34 Conservation and declines of amphibians in The NetherlandsAnton H.P. Stumpel

    35 Amphibian declines and conservation in BelgiumGerald Louette and Dirk Bauwens

    36 Amphibian declines and conservation in FranceJean-Pierre Vacher and Claude Miaud

    37 Conservation and declines of amphibians in SpainCesar Ayres, Enrique Ayllon, Jaime Bosch, Alberto Montori, Manuel Ortiz-Santaliestra, and Vicente Sancho

    38 Conservation and declines of amphibians in PortugalRui Rebelo, Maria José Domingues Castro, Maria João Cruz, José Miguel Oliveira, José Teixeira, and Eduardo Crespo

  • Contributors to Part 4 (Southern Europe and Turkey)

    EDITORSHeatwole, Harold, Department of Biology, North Carolina State University, Raleigh, NC 27695-7617, USA [email protected], John W., Amphibian and Reptile Conservation, 655A Christchurch Road, Boscombe, Bournemouth, BH1 4AP, Dorset, [email protected]

    AUTHORSAndreone, Franco, Museo Regionale di Scienze Naturali, Sezione di Zoologia, Via G. Giolitti, 36, I-10123 Torino, [email protected]ć, Avdullahu, Univerzitet u Tuzli, Univerzitetska 4, 75000 Tuzla, Bosna i [email protected]Ćirović, Ruža, Environmental Protection Agency of Montenegro, Department for Monitoring, Analysis and Reporting, No. 19 IV Proleterske, 81,000 Podgorica, [email protected]ălniceanu, Dan, Ovidius University of Constanţa, Faculty of Natural Sciences, Aleea Universităţii nr. I, Corp B, 900470 Constanţa, [email protected]ć, Jekla, Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, 18000 Niš, [email protected], Idriz, Herpetofauna Albanian Society, Rruga Myslym Shyri, P.10, Sh.1, Ap.3 Cel: 00355 68, 200 3235, [email protected]ć, Dušan, Croatian Institute for Biodiversity, Croatian Herpetological Society Hyla, I. Breznička 5a, 10000 Zagreb, [email protected]ć, Olga, Department of Biology, Josip Juraj Strossmayer University of Osijek, Cara Had-rijana 8/A, 31000 Osijek, [email protected], István, Department of Zoology and Animal Ecology, Szent István University, 2103 Gödöllő, Páter Károly u. 1., [email protected]žnik, Martina, Faculty of Mathematics, Natural Sciences and Information Technologies, Uni-versity of Priomorska, Glagoljaška 8, SI-6000, Koper, [email protected], Petros, Natural History Museum of Crete, University of Crete, 71409 Herakleio, [email protected]

  • Nicolaou, Haris, Forestry Department, Ministry of Agriculture, Natural Resources and Environ-ment, 1414 Nicosia, [email protected], Kurtuluş, University of Adnan Menderes, Faculty of Science and Art, Biology Department, Kepez, 09010 Aydin, [email protected]ć, Momir, Institute for Biological Research “Siniša Stanković”, Bulevar Despota Stefana 142, 11000 Beograd, [email protected]šaj, Katja, Center for Cartography of Fauna and Flora, Antoličičeva 1, SI-2204 Miklavž na Dravskem polju, Sloveniakatja.poboljš[email protected], Georgi Sashef, Regional Natural History Museum, 34 Hristo G. Danov str., 4000, Plovdiv, [email protected], Miklós, Danube Research Institute of the Hungarian Academy of Sciences, 2131 Göd, Jávorka Sándor u. 14, [email protected], Laurenţiu, University of Bucharest, Bd. Nicolae Balcescu, 1, cod 010041, Bucharest, [email protected], Patrick J., Department of Biology, University of Malta, Msida, [email protected], Konstantinos, Department of Biological Applications and Technologies, School of Science and Technology, University of Ioannina, GR 451 10 University Campus of Ioannina, [email protected]ć, David, Department of Animal Science, Biotechnical Faculty, University of Ljubljana, Groblje 3, SI-1230 Domžale, [email protected], Bogoljub, Macedonian Ecological Society, Faculty of Natural Sciences, Blvd. ‘Kuzman Josifovski – Pitu’ 28/3-7 1000 Skopje, [email protected], Nikolay, Vertebrates Department, National Museum of Natural History, 1 Tsar Osvo-boditel blvd., Sofia 1000, [email protected]Üzüm, Nazan Taşkın, University of Adnan Menderes, Faculty of Science and Art, Biology Depart-ment, Kepez, 09010 Aydin, [email protected]örös, Judit, Hungarian Natural History Museum, 1088 Budapest, Baross u. 13, [email protected]

  • Editors’ prefaceDifferent authors agree to varying extents with some of the proposed changes in amphibian nomenclature and no consensus on European taxa has currently been reached. Consequently, no attempt has been made to completely standardize nomenclature and so names of some taxa will vary from one chapter to another. In time, perhaps a greater agreement will be reached than is possible at the present moment.

  • 39 The amphibians of the Italian region: A review of conservation status

    Franco Andreone

    Abbreviations and acronyms used in the text or references:Bd Batrachochytrium dendrobatidisEN EndangeredEU European UnionISPRA Italian National Institute for Environmental Protection and ResearchIUCN International Union for Conservation of NatureNIS Non-indigenous invasive speciesNT Near ThreatenedSHI Societas Herpetologica ItalicaSUV Sport utility vehicleVU VulnerableWWF World Wide Fund for Nature

    I. IntroductionWith 52 species, of which 25 are endemic, the Italian geographic region, including the Italian Peninsula and satellite islands and islets, Sardinia, and Sicily (Italy), Corsica and the surroundings of Nice (France), Ticino Canton (Switzerland), Istria and surrounding islands (Slovenia and Croatia), the Maltese Archipelago (Malta), San Marino, and Vatican City (according to Lanza et al. 2007, 2009), is an exceptional biodiversity hotspot. This is due mainly to its varied biogeographical composition, which includes elements that represent all major zoogeographic components. Considering the whole Italian region, the amphibian fauna is richer than the one present within the strict political boundaries of Italy: the edible frogs Pelophylax perezi and P. kl. grafi are present next to Nice (France), while Salamandra corsica, Discoglossus montalentii, and

    I. Introduction

    II. The status of the Italian amphibian fauna

    III. Threats affecting the Italian batrachofauna

    A. Habitat alteration and urbanization

    B. The chytrid fungus in Italy and its significance for amphibian conservation

    C. The introduced species

    1. Fishes

    2. Amphibians

    3. The red swamp crayfish

    IV. Conservation measures and monitoring programmes

    V. Conclusions

    VI. Acknowledgements

    VII. Addendum

    VIII. References

  • 2 Amphibian Biology

    Euproctus montanus are present in Corsica (France). In the other extra-Italian territories, the species are usually not different from those present within the Italian political boundaries, although P. bedriagae was reported, as an introduced species, for Gozo in the Maltese Archipelago (Sciberras and Schembri 2006; Schembri 2014).

    This high species diversity is determined by several factors such as the geological history of the Italian Peninsula, including its geographic position and structure, the orography, and the bioclimatic conditions. Vegetation formations evolved in a geographical context and climate influ-enced by the presence of two large mountain ranges (the Alps and Apennines), and a large conti-nental flood plain (the Po Plain), which allowed a succession of very different ecosystems over time and the stabilization of multiple phytocoenoses. The orographic characteristics are featured by an extensive coastline with a large number of small islands and islets, in addition to the large Tyrrhenian islands, all with Mediterranean xeric formations. Moreover, the large number of islands, the peninsular effect and the mountain ranges, together with Quaternary climatic change, have caused isolation that has led to a number of specific or subspecific differentiations.

    Many parts of Italy acted historically as biogeographic refugia, such as for newts (Scillitani and Picariello 2000), spectacled salamanders (Mattoccia et al. 2011), and spadefoot toads (Crottini et al. 2007). Most of these lineages generated endemisms that are strictly confined to the Italian region, as shown by the recent phylogeographic papers that identified endemic clades (e.g. Canestrelli et al. 2006; Verardi et al. 2009).

    Table 39.1 List of the amphibian species present in Italy, as considered by the assemblage of the Italian political boundaries and nearby territories (see text).Abbreviations and symbols:ALB = Albania; ALG = Algeria; COR = Corsica (France); CRO = Croatia; CYP = Cyprus; DEN = Denmark; EGY = Egypt; FRA = France; GRE = Greece; ISR = Israel; ITA = Italy (including Sicily and small islands); JOR = Jordan; LEB = Lebanon; LYB = Lybia; MAL = Maltese Archipelago; MON = Montenegro; MOR = Morocco; OEC = other European countries (see AmphibiaWeb for an exhaustive list); ONAC = other North African and Middle Eastern countries (see AmphibiaWeb for an exhaustive list); OWC = other countries in the world (see AmphibiaWeb for an exhaustive list); POR = Portugal; SAR = Sardinia (Italy); SER = Serbia; SLO = Slovenia; SPA = Spain; SYR = Syrian Arab Republic; TUN = Tunisia; TUR = Turkey; UK = United Kingdom; # Introduced (non-indigenous) species; * Species endemic to the Italian region. Note: the generic nomenclature for the cave salamanders follows Lanza et al. (2007, 2009).

    Family SpeciesIUCN Red List Categorization

    Distribution Habitat Directive ListingGlobal National

    PROTEIDAE

    1 Proteus anguinus Vulnerable Vulnerable CRO, ITA, MON, SER, SLO

    II, IV

    PLETHODONTIDAE

    2 Atylodes genei* Vulnerable Vulnerable SAR II *

    3 Speleomantes ambrosii* Vulnerable Near Threatened SAR II *, IV

    4 Speleomantes flavus* Vulnerable Vulnerable SAR II *, IV

    5 Speleomantes imperialis* Near Threatened Near Threatened SAR II *, IV

    6 Speleomantes italicus* Near Threatened Least Concern ITA IV

    7 Speleomantes sarrabu-sensis*

    Vulnerable Vulnerable SAR

    8 Speleomantes strinatii* Near Threatened Least Concern ITA, FRA IV

    9 Speleomantes supramontis*

    Endangered Vulnerable SAR II *, IV

    SALAMANDRIDAE

    10 Euproctus montanus* Least Concern - COR IV

  • The Amphibians of the Italian Region: A Review of Conservation Status 3

    Family SpeciesIUCN Red List Categorization

    Distribution Habitat Directive ListingGlobal National

    11 Euproctus platycephalus* Endangered Endangered SAR IV

    12 Ichthyosaura alpestris Least Concern Least Concern ITA, OEC

    13 Lissotriton italicus* Least Concern Least Concern ITA IV

    14 Lissotriton vulgaris Least Concern Near Threatened ITA, OEC

    15 Salamandra atra Least Concern Least Concern ITA, OEC IV

    16 Salamandra corsica* Least Concern - SAR

    17 Salamandra lanzai Vulnerable Vulnerable ITA, FRA IV

    18 Salamandra salamandra Least Concern Least Concern ITA, OEC

    19 Salamandrina perspicillata*

    Least Concern Least Concern ITA

    20 Salamandrina terdigitata* Least Concern Least Concern ITA II, IV

    21 Triturus carnifex Least Concern Near Threatened ITA, OEC II, IV

    PELOBATIDAE

    22 Pelobates fuscus Least Concern Endangered ITA, OEC IV

    PELODYTIDAE

    23 Pelodytes punctatus Least Concern Endangered ITA, OEC

    BOMBINATORIDAE

    24 Bombina pachypus* Endangered Endangered ITA

    25 Bombina variegata Least Concern Least Concern ITA, OEC II, IV

    ALYTIDAE

    26 Discoglossus montalentii* Near Threatened - COR II, IV

    27 Discoglossus pictus Least Concern Least Concern AL, FRA, ITA, MAL, SPA, TUN

    IV

    28 Discoglossus sardus* Least Concern Vulnerable SAR, ITA, FRA II, IV

    HYLIDAE

    29 Hyla arborea Least Concern - ITA, OEC IV

    30 Hyla intermedia* Least Concern Least Concern ITA (IV)

    31 Hyla meridionalis Least Concern Least Concern ALG, FRA, ITA, MOR, POR, SPA

    IV

    32 Hyla sarda* Least Concern ITA, FRA IV

    BUFONIDAE

    33 Bufo bufo Least Concern Vulnerable ITA, OEC

    34 Bufotes balearicus* Least Concern Least Concern ITA, COR, SPA (IV)

    35 Bufotes boulengeri Least Concern Vulnerable ITA, SPA, ONAC (IV)

    36 Bufotes siculus* Least Concern Least Concern SIC

    37 Bufotes viridis* Least Concern Least Concern ITA, OEC IV

    RANIDAE

    38 Lithobates catesbeianus# Least Concern - ITA, OWC

    39 Pelophylax bedriagae# Least Concern - MAL, ONAC

    40 Pelophylax bergeri* Least Concern Least Concern ITA, COR, SAR

    41 Pelophylax hispanicus* Least Concern Least Concern ITA

    42 Pelophylax kl. esculentus Least Concern Least Concern ITA, OEC

    43 Pelophylax kurtmuelleri# Least Concern - ALB, DEN, FRA, GRE, ITA

    44 Pelophylax grafi Least Concern - FRA, SPA

    45 Pelophylax lessonae Least Concern Least Concern ITA, OEC IV

    46 Pelophylax perezi Least Concern - FRA, SPA, POR, UK

  • 4 Amphibian Biology

    Family SpeciesIUCN Red List Categorization

    Distribution Habitat Directive ListingGlobal National

    47 Pelophylax ridibundus Least Concern - ITA, OEC

    48 Rana dalmatina Least Concern Least Concern ITA, OEC IV

    49 Rana italica* Least Concern Least Concern ITA IV

    50 Rana latastei* Vulnerable ITA, SWI, SLO, CRO

    II, IV

    51 Rana temporaria Least Concern Vulnerable ITA, OEC

    PIPIDAE

    52 Xenopus laevis# Least Concern - ITA, OWC

    II. The status of the Italian amphibian faunaAn overview of the conservation status for the Italian species, also including the overall legislative framework operating at national level, is reported in Table 39.1. For considerations of the regional laws, information is reported by Scalera (2003), while for indications of the ecological constraints on conservation sensitivities, see Andreone and Luiselli (2000). Six amphibians from the Italian region are shown in Figure 39.1. In terms of taxonomy we followed the list provided by Rondinini et al. (2013). The main annotations are that, according to Frost (2014) we used the genus Bufotes rather than Pseudepidalea for the species assemblage of the viridis group. Then, we considered present in the Italian territory four species, B. balearicus, B. boulengeri, B. siculus, and B. viridis, respectively. The presumed subspecies Pelobates fuscus insubricus is here not considered as valid, according to the data presented by Litvinchuk et al. (2013).

    Of the 52 treated species (including the exotic/introduced species Lithobates catesbeianus, Pelophy-lax kurtmuelleri, P. bedriagae, and Xenopus laevis) 9 species are threatened, i.e. 6 (Proteus anguinus, Atylodes genei, Speleomantes ambrosii, S. flavus, S. sarrabusensis, and Salamandra lanzai) are included in the Vulnerable (VU) category, and 3 (Speleomantes supramontis, Euproctus platycephalus, and Bombina pachypus) are Endangered (EN) (IUCN, 2010). This number equates to 18.75% of the authchthonous amphibian fauna of the Italian region (48 species) or 20.45% of the amphibians of political Italy (44 indigenous species). If the subspecies and populations present in the Italian territory are considered and a regional approach is applied, some further taxa especially worthy of conservation interest are identified. More recently, a list was provided by Rondinini et al. (2013), with the following threatened species: EN = Euproctus platycephalus, Ichtyosaura alpestris inexpectata, Bombina pachypus, Pelobates fuscus, and Pelodytes punctatus; VU = Atylodes genei, Speleomantes flavus, S. sarrabusensis, S. supramontis, Proteus anguinus, Salamandra lanzai, Bufo bufo, Bufotes boulengeri, and Rana latastei (Table 39.1). Some threatened subspecies were also taken into account such as follows: Ichthyosaura alpestris apuana (NT), Ichthyosaura alpestris inexpectata (EN), Salamandra atra aurorae (VU), and S. a. pasubiensis (EN).

    In the present contribution, considerations of some of the most relevant threats to Italian amphibian species and populations are summarized, with a focus on habitat alteration, emerging pathologies, and introduction of alien species. For a more general overview and indications of pollution and other threats, see Scoccianti (2001, 2004).

  • The Amphibians of the Italian Region: A Review of Conservation Status 5

    Fig. 39.1 Representative amphibians from the Italian region. A) Sardinian brook salamander Euproctus platycephalus (Sette Fratelli Massif, Sardinia); B) Northern spectacled salamander Salamandrina perspicillata (Borbera Valley, Alessandria Province, Piedmont); C) Lanza’s salamander Salamandra lanzai (Upper Po Valley, Piedmont); D) Spadefoot toad Pelobates fuscus (South of Turin, Piedmont); E) Italian treefrog Hyla intermedia (South of Turin, Piedmont); F) Sardinian painted frog Discoglossus sardus (Sette Fratelli Massif, Sardinia) (all photos by the author).

    III. Threats affecting the Italian batrachofauna

    A. Habitat alteration and urbanizationMost threats to Italian amphibians are common to those in other parts of the world and are mostly due to habitat alteration and anthropogenic actions (Scoccianti 2004). The increasing urbanization of Italy and intensive agricultural practices represent the major threats for Italian amphibians. This is especially true when species living around the larger metropolitan towns of Italy, such as Flor-ence, Genoa, Milan, Rome, and Turin are considered. In particular, habitat alteration, human demographic increase, and general pollution are particularly intense in the Po Plain, N. Italy. Two species of particular conservation interest live only there: Pelobates fuscus (with the putative endemic subspecies P. f. insubricus) and Rana latastei. Their worrying and threatened status reflects the

  • 6 Amphibian Biology

    habitat alteration and related effects caused by the intense human pressure (pollution, urbanization, agriculture) affecting the Po Plain, which has about twenty million human inhabitants.

    In the remaining part of the Italian Peninsula, the overall orography is hilly and montane, and consequently the conservation threats are less directly tied to urbanization and the local pollution. Notwithstanding this, even in the Alps and Apennines the human impact is locally intense and threatening for amphibian populations. Many tourist localities receive thousands of visitors every year, and sometimes the access to these localities is facilitated by the construction of asphalted roads, which allow the passage of vehicles (e.g. trail motorbikes; SUV cars). In these cases, traffic therefore becomes an important threat. One largely Italian endemic species, Salamandra lanzai, is particularly vulnerable to road mortality and many individuals are killed each year by car traffic on mountain roads (F. Andreone, personal observation; Andreone et al. 2007). This species has been also affected by flood alleviation activities which have reduced the natural habitats of the species considerably (Andreone et al. 2007). Evidence of habitat alterations follows the intense use of mountain slopes for skiing and for the construction of ski lodges. In some Alpine and Apennine areas, the abandonment of traditional practises has led to the disappearance of important bodies of water, such as watering points for cattle and small fountains where species used to breed (Romano et al. 2010).

    Table 39.2 Review of the occurrence of chytridiomycosis in Italy, based upon published information.

    Authors and Date Species Area Argument

    Adams et al. 2008 Several species Several areas Presence of Bd in Italy

    Bielby et al. 2009 Discoglossus sardus Sardinia Evidence of mass mortality in Sardinia

    Bovero et al. 2008a Euproctus platycephalus Sardinia Evidence of Bd on the species

    Bovero et al. 2008b Several species Sardinia Emergence of Bd in Sardinia

    Di Rosa et al. 2007 Pelophylax lessonae Umbria Occurrence of Bd in central Italy over several years

    Federici et al. 2008 Several species Turin surroundings Occurrence of Bd in Piedmont

    Ficetola et al. 2011 Several species Po delta Occurrence of Bd in the Po delta

    Garner et al. 2004 Rana latastei. N. Italy Decline of R. latastei and its link with Bd

    Garner et al. 2006 Lithobates catesbeianus N. Italy The bullfrog as a Bd vector

    Simoncelli et al. 2005 Pelophylax esculentus complex

    Umbria Occurrence of Bd in central Italy

    Stagni et al. 2002 Bombina pachypus Tusco-Emilian Apennines Mortality of B. pachypus due to Bd

    Stagni et al. 2004 Bombina pachypus Tusco-Emilian Apennines Mortality of B. pachypus due to Bd

    B. The chytrid fungus in Italy and its significance for amphibian conservationOne of the most invoked causes of amphibian extinctions around the world is the appearance of the fungus Batrachochytrium dendrobatidis (traditionally abbreviated as chytrid or Bd), known to be the etiologic agent responsible for lethal chytridiomycosis and implicated in global amphibian declines (Collins and Crump 2009). So far, the situation of Bd in Italy is not yet well-documented, although there are already several reports, sadly due to the results of single researchers and not on the basis of a coordinated action. While this report has been in press a review was published by Tessa et al. (2013), to which we also refer for reporting the state of the Bd research in Italy (Table 39.2).

    The first documented chytridiomycosis in wild Italian amphibian populations dates back to 2001 (Stagni et al. 2004). Later, it was reported in Umbrian populations of the Pelophylax esculentus complex (possibly P. bergeri or P. kl. hispanicus) (Simoncelli et al. 2005; Di Rosa et al. 2007) and has

  • The Amphibians of the Italian Region: A Review of Conservation Status 7

    also been detected in Rana latastei (Garner et al. 2004), Lithobates catesbeianus (Garner et al. 2006; Adams et al. 2008), and Pelophylax esculentus complex (Adams et al. 2008; Federici et al. 2008) of northern Italy (Piedmont), and in Sardinian populations of the endemic Euproctus platycephalus and Discoglossus sardus (Bovero et al. 2008a).

    Up to now, however, observations of mass mortalities have been limited to Discoglossus sardus in Sardinia, while further data of its presence in mainland populations are urgently needed to get information on the effects on survival (Bielby et al. 2009).

    C. The introduced species1. FishesFish introduction is a well-known cause of the extirpation of many amphibian populations around the world (Scoccianti 2004). In particular, direct predation by alien fish can also cause reproductive failure and the extirpation of amphibian populations (Denoël et al. 2005; Knapp 2005). This is especially true when the introduction is done in areas where fish were formerly absent, as is the case for many Alpine and Apennine lakes, especially for the introduction of Salmo fontinalis (Tiberti and von Hardenberg 2012; Tiberti et al. 2013). This is also true for the Italian situation, where the disappearance of alpine populations of Rana temporaria was often reported as a consequence of the introduction of salmonid fish for sportive fishing. At the same time, presence of fish has been reported as the cause of the disappearance of paedomorphic newts in many areas of Europe, including Italy (Denoël et al. 2005). The influence of the introduced Salmo trutta on Salamandrina perspicillata was also analysed by Piazzini et al. (2011).2. AmphibiansNon-indigenous invasive species (NIS) can threaten native amphibian species through predation, competition, and toxicity. Three exotic amphibian species are present and acclimatized in Italy, and currently represent serious threats for the native species: Lithobates catesbeianus, Pelophylax kurtmuelleri, and Xenopus laevis. In the Italian region we should also report P. bedriagae in Gozo (Schembri 2014). They have been introduced for human consumption, in the case of the frogs, while the introduction of the clawed frog was likely due to the release of laboratory animals or for the pet trade (Weldon et al. 2004).

    The American bullfrog (Lithobates catesbeianus) is currently present in the Po Valley (N. Italy), as a result of repeated introductions, and became established between 1932 and 1937 in the prov-ince of Mantua. In the following years it was also documented in other provinces of Lombardy (Cremona, Brescia, Bergamo, and Pavia), Veneto (Verona and Rovigo, delta of Po River) and Emilia-Romagna (Piacenza, Reggio Emilia, Modena, Bologna, and Ferrara), probably as a result of both active introductions and the expansion of populations already naturalized. In the early 1960s, the bullfrog was also introduced into Lower Friuli (Udine), and later, between 1965 and 1975, into Tuscany (province of Pistoia and Florence), Latium (near Rome), where, however, its presence has not been confirmed since 1996, and Basilicata (Fattizzo and Nitti 2007).

    Since the 1980s, following further introductions, the bullfrog has spread to Piedmont (NW Italy) in the provinces of Asti and Turin (after an active and volunteer introduction), but apparently it did not become acclimatized in the ricefields of Vercelli and Novara, where it was introduced for some time, probably because of the unfavorable characteristics of these temporary (anthropogenic) aquatic habitats. Little is known of the species’ impact on autochthonous Italian species, although sporadic observations suggest that it could be responsible for the disappearance of the local amphibians, as a consequence of direct predation and competition (as happens in France), and it may be a transmission vehicle for the chytrid.

  • 8 Amphibian Biology

    A rather similar situation is known for the introduction of another frog species, the Balkan green frog Pelophylax cf. kurtmuelleri. In Italy this NIS is currently dominant in many areas of the provinces of Savona and Imperia (Ligury: Capocaccia et al. 1969; Dell’Acqua 1994) and is increasing in the provinces of Cuneo, Asti, and Alessandria (Piedmont: Andreone 1999). The origin and expansion of Ligurian populations likely derived from individuals imported in 1941 from northern Albania (Lanza 1962). In the following years this frog spread throughout the Impero and Prino Caramagna rivers (Bologna 1972) and later on in almost all streams of the River Basin to the Imperia Bevera river (a few kilometers from the French border) to the west, and in the province of Savona to the east (Ferri and Dell’Acqua 1985; Dell’Acqua 1994). The Piedmontese populations (Alessandria, Cuneo, Asti) originated probably from the expansion to the north of the Ligurian nuclei, and partly by introduction and acclimatization of individuals of unknown origin (Andreone 1999). In Piedmont the populations are currently expanding rapidly, and in this region, the eastern boundary of the species is identified by a report from the Rio Gorzente. In Friuli Venezia-Giulia the species was introduced in 1990 (Bressi 1995). A more recent update was provided by Bellati et al. (2012).

    Vorburger and Reyer (2003) demonstrated that, after introduction, P. kurtmuelleri easily replaces the native P. esculentus and P. lessonae in many areas of western Europe, due to a phenomenon of genetic pollution, with an expulsion of the lessonae genome. Thus, P. kurtmuelleri will increase in numbers in the population at the expense of both native taxa, leading even to pure populations of P. kurtmuelleri. This genetic pollution is worrying, because in theory the spread of P. kurtmuelleri in natural populations can lead to sterilization of the lessonae-esculenta complex. If so, the disappearance of native green frogs from neighbouring areas is a possibility and will only be prevented by geographical and physical barriers. Unluckily, new records of introduced green frogs in Sardinia and Sicily may also lead to the diffusion of populations on islands with a population of endemic species (Livigni and Licata 2011).

    A further NIS worthy of special concern in recent years is the African clawed frog, Xenopus laevis, in Sicily. To date, the Sicilian populations of X. laevis have a distribution of about 300 km2 (Faraone et al. 2008) and its expansion is ongoing and rapid, using streams as corridors and agricultural ponds as breeding ponds (Lillo et al. 2010). The area of distribution of this invasive species will cover the entire western portion of the island in a few years (Lillo et al. 2010). The decline of some Sicilian native amphibian populations (such as Discoglossus pictus, Hyla intermedia, and P. kl. esculentus) is possibly associated with the presence of X. laevis (Lillo et al. 2010) and, although the direct causes of the decline of native amphibian populations are not clarified, there is a concern that these events are due to the capability of X. laevis to be, as demonstrated elsewhere (Weldon et al. 2004; Solìs et al. 2010), a vector for Bd dispersal.3. The red swamp crayfishThe red swamp crayfish, Procambarus clarkii, a native freshwater crustacean of Eastern North America and Mexico, has been introduced for aquaculture on all continents except Antarctica and Australia (Huner 2002). It is currently present in most countries of Western Europe, and large territories have been invaded in the Iberian Peninsula, France, and Italy (Gherardi 2006). Procambarus clarkii can predate the larvae of several species of European amphibians (Gherardi et al. 2001; Cruz and Rebelo 2005; Cruz et al. 2006a). In general, its presence can exclude amphibians from potentially suitable reproductive areas (Cruz et al. 2006a; Cruz et al. 2006b).

    Unfortunately, the complete eradication of P. clarkii populations appears extremely difficult (not to say impossible), and would require the application of multiple approaches and techniques (Aquiloni et al. 2009, 2010). Intensive trapping may reduce its abundance (Hein et al. 2007), but this would be extremely expensive and cannot be applied on a large scale. Management actions can

  • The Amphibians of the Italian Region: A Review of Conservation Status 9

    be applied to specific areas with the highest conservation priority, to mitigate impacts. Such an approach might be more effective in areas where the environmental suitability for P. clarkii is limited.

    A recent study by Ficetola et al. (2012) showed that for P. clarkii, suitability and habitat adaptation is higher in the largest, permanent bodies of water, while amphibian species richness was highest in wetlands with intermediate size and hydroperiod. This likely occurs primarily because only species with fast larval development can successfully reproduce in ephemeral wetlands (e.g. Hyla intermedia and the green toad Bufotes viridis were not detected in the visited wetlands) (Van Buskirk 2003; Ficetola and De Bernardi 2005). Therefore, these wetlands tend to have assemblages with low species richness. Secondly, large permanent wetlands often have high abundance of predators (both fish and invertebrates) (Baber et al. 2004; Werner et al. 2007);

    IV. Conservation measures and monitoring programmesThe interest of the scientific community towards the conservation of Italian amphibians has led in recent decades to the increase of safeguarding actions, especially for some selected species.

    A first and general overview of threats to the Italian amphibian fauna was provided by Bruno (1983), but it was especially with the research on the spadefoot toad (Pelobates fuscus) that public attention was oriented towards amphibians. In the 1990s, the Italian populations of the spadefoot toad were monitored and became the object of conservation efforts, also because they were considered as belonging to an endemic subspecies, P. f. insubricus (Andreone et al. 2004a). In reality, as stressed by Andreone et al. (1993) and more recently evidenced by Crottini et al. (2007) and Crottini and Andreone (2007), little was known about the real phylogenetic differentiation of the Italian populations of this species, which is widespread in Europe. According to Litvinchuk et al. (2013), the validity of the insubricus subspecies is questionable and should be rejected based upon a strong genetical basis, although the Italian populations are characterized by a conspicuous haplotype richness and diversity (Crottini et al. 2007; Litvinchuk et al. 2013) that should be taken into account for future conservation programmes. The inclusion of such a putative subspecies in the EU Habitats Directive, and its asterisked status, has resulted in supporting studies and conservation actions on the species. These include the production of an action plan (Andreone, 2000) and, more recently, of some specific EU LIFE projects that allowed detailed actions. As stressed elsewhere, the conservation actions were often irregular (due to lack of continuity in financing) and provided results mainly in the field of awareness and in the short-term management of some populations, such as those living in the Parco Regionale del Ticino and in the Site of Community Importance “Poirino-Favari” (Crottini and Andreone 2007). The long-term effectiveness of these actions, which were ultimately quite expensive and with limited outputs, have yet to be assessed (see Crottini and Andreone 2007).

    Other species-specific actions regarding threatened species were carried out on the Italian agile frog, Rana latastei. As summarized by Scali and Gentilli (2007), most of the initiatives were directed towards population monitoring, rescue actions, and captive breeding. As reported by Tockner et al. (2006), however, the species, although considered one of those at the highest risk and threat (Andreone and Luiselli 2000), is also locally abundant and quite adaptable.

    Lanza’s salamander Salamandra lanzai has been studied for several years in most of its historical localities, mainly for aspects regarding its distribution and phenology (Andreone et al. 2004b) and for providing practical guides for its management (Andreone et al. 2007). Similarly, the Sardinian brook salamander Euproctus platycephalus is still the object of intense studies due to the fact that little is known regarding its distribution (Bovero et al. 2005), and because the chytrid has been detected in some of its populations. Similarly, Aurora’s alpine salamander (Salamandra atra aurorae)

  • 10 Amphibian Biology

    and the recently described S. a. pasubiensis were the subjects of another EU LIFE project (Brakels and Beukema 2008).

    Attempts at captive breeding of threatened species should also be noted. As far as we know, three threatened species have been the subject of such attempts: Pelobates fuscus, Rana latastei, and Euproctus platycephalus (Andreone 2000; Ficetola and De Bernardi 2006; Garcia 2010). Apart from some developments in husbandry science (e.g. Jesu et al. 2002) such projects were not particularly successful (e.g. P. fuscus and R. latastei).

    Euproctus platycephalus is currently the object of a captive breeding program in the Bioparco di Roma, which led to considerable reproductive success (L. Vignoli, personal communication 2013).

    Beside the actions directed towards threatened or iconic species, many citizen-based initiatives have been carried out in Italy. These were mainly focussed on rescue actions on roads during toads’ breeding migrations. This volunteer work has been often reported during the Societas Herpetologica Italica (SHI) and “Salvaguardia Anfibi” congresses (Di Tizio et al. 2011). Meta-analysis of most of the data of these migrations has shown that populations of the common toad (Bufo bufo) are declining (Bonardi et al. 2011). This is quite an alarming scenario, since it is one of the few studies providing quantitative evidence that amphibians are declining in Italy.

    The most recent series of herpetological talks launched under the “HerpeThon 2011” and “HerpeThon 2013” initiatives provided the intervention of several conferences and exhibits focussed on amphibian conservation (e.g. Garner and Andreone 2011; Andreone et al. 2013).

    V. ConclusionsIn terms of practical actions, it is important that the threatened species are subject to constant and on-going monitoring, and that tailored conservation actions are led by experienced teams. It is also crucial that the areas where the threatened species occur are put under strict conservation protection, and that the realization of infrastructures takes into consideration the presence of species reported in the EU Habitats Directive. I further recommend that the chytrid is monitored all through Italy and that probiotic strains are selected from the Italian species, particularly those that are more threatened or have the narrowest distributions (Woodhams et al. 2007).

    Unluckily, on many occasions, Italy (in its political and administrative sense) has not been respectful of European conservation standards. This was for example the case for the spadefoot toad in Turin Province, and for generalized habitat alterations which have occurred in the high Pellice and Germanasca Valleys, elective habitats of Salamandra lanzai (Andreone et al. 2004b). These habitat alterations were consequences of works carried out to the riverbed, and financed by local administrations, with the aim to limit the negative effects of extraordinary floods.

    As a general conclusion it is important to stress that, although research on amphibians, and particularly on their conservation, is quite abundant in Italy (especially thanks to the activism of the Italian herpetological community) there are only a few studies aiming to monitor the general trends of amphibians in Italy. An exception to this has been the recent monitoring work reported by SHI, but unluckily stopped due to lack of economic support (Societas Herpetologica Italica 2011). At the same time, an organized monitoring of the occurrence of chytrid is mostly absent. These kinds of initiatives should be supported by the state environmental agencies (notably by the Ministero dell’Ambiente e del Mare and/or by regions), but unfortunately this is not yet the case. Similarly, other actions directed towards the monitoring of exotic amphibian species (includ-ing control of the introduction of allochthonous green frogs for human consumption) are missing, and should be implemented in forthcoming years.

  • The Amphibians of the Italian Region: A Review of Conservation Status 11

    VI. AcknowledgementsI thank all the friends and colleagues who contributed in the past years with published and unpublished information, in particular: S. Bovero, P. Eusebio Bergò, A. Crottini, F. Fraticelli, F. Lillo, V. Mercurio, G. Tessa, R. Tiberti, and L. Vignoli. I thank J.W. Wilkinson for having invited me to prepare this contribution.

    VII. AddendumA recent contribution by Domeneghetti et al. (2013) showed the presence of MtDNA haplotype assigned to Pelophylax shqipericus in an individual sampled in Umbria, thus suggesting that this species too could be present in the Italian territory. [Domeneghetti, D., Bruni, G., Fasola, M., and Bellati A., 2013. Discovery of alien water frogs (gen. Pelophylax) in Umbria, with first report of P. shqipericus for Italy. Acta Herpetologica 8 (2): 171–176.]

  • 12 Amphibian Biology

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  • 40 Amphibian conservation and declines in Malta

    Patrick J. Schembri

    I. IntroductionThe Maltese Islands are amongst the smaller islands of the Mediterranean, yet they are practically unique in that they are an island state, the Republic of Malta, with a very high population density, which presently approximates to 1,317 persons km2, based on the resident population alone (NSO 2012). The islands have been more or less continuously inhabited for the past 7,500 years or so (Trump 2002). In recent years, the islands have received an influx of more than one million tourists per year (1.4 million in 2011) (NSO 2012), and they now also host a considerable population of temporary immigrants seeking access to mainland Europe (NSO 2010). As may be expected, the large human population and its activities over such a prolonged period of time have had severe impacts on the natural environment, including the herpetofauna.

    The Maltese group, lying more or less at the centre of the Mediterranean, about 96 km south of Sicily and 290 km north of the Libyan coast, comprises the three inhabited islands of Malta, Gozo, and Comino, respectively 246.5 km2, 65.8 km2, and 2.9 km2 in area, and a number of uninhabited islets and rocks none of which is larger than 10 hectares. Geologically, the islands are almost entirely made of carbonate rock and are the emerged high points of a vast block of limestone that spans from the coasts of Tunisia to southeastern Sicily. Most of this block is presently submerged but, during the great marine lowstand of the Messinian Salinity Crisis, a land connection existed between the Hyblean region of Sicily and North Africa. This connection resulted in the first episode of colonization by biota of what are today the Maltese Islands. Following the Zanclean transgression at the end of the Miocene epoch, the Maltese islands remained isolated from the surrounding lands until the marine regressions associated with the Quaternary glaciations either established temporary land bridges with Sicily or else narrowed considerably the channel between Malta and Sicily (Pedley et al. 2002). In both cases, immigration of biota to Malta from Sicily was facilitated. These repeated waves of colonization account for the large degree of similarity of the Maltese biota with that of Hyblean Sicily, whereas the periods of isolation of the Maltese Islands have resulted in the evolution of more or less distinct island forms of some biota, including a number of endemic species (Schembri 2003).

    Topographically, the islands are low-lying with a maximum elevation of only 253 m. The climate is strongly bi-seasonal, with hot, dry, and sunny summers and wet but mild winters during which falls some 85% of the mean annual rainfall of ca. 530 mm; this climatic regime defines a dry season from March to October and a wet season during the remaining months (Schembri 1997). While the mean temperature range is 12–26°C, very high maximum ground temperatures may occur in

    I. Introduction

    II. Maltese amphibians

    III. Conservation status and threats

    IV. Conservation measures and monitoring programmes

    V. Conclusions

    VI. Acknowledgements

    VII. References

  • 18 Amphibian Biology

    summer (sometimes up to 45°C); such conditions have profound implications for the biota (Schembri 1997; Cassar et al. 2008). Although rivers existed in the remote past, there are none today and the islands’ surface waters comprise a few springs and small ponds and a much larger number of artificial bodies such as reservoirs, ponds, and irrigation channels. During the wetter periods of the Pleistocene glacial cycles, when the islands had a much larger area than at present due to marine regression, the rivers that existed then incised river valleys into the limestone rock; these rivers are now extinct and the valleys, known as ‘widien’ in Maltese (singular: ‘wied’) now serve to drain runoff water from their catchment during the wet season (Anderson 1997). During the dry season, there is no flow in practically any of the widien and most have dry watercourses; the exceptions are those few widien that drain groundwater seeping out of aquifers to form minor springs (Schembri 1997; Cassar et al. 2008). However, due to tapping of such springs at source for irrigation, and massive extraction of groundwater from the aquifers supplying these springs, there are presently very few such perennial springs left. There are also no lakes or even large ponds in the Maltese Islands and the only standing bodies of water that exist, apart from completely artificial reservoirs, are natural or semi-natural depressions that fill with water during the wet season. Practically all of these dry up in the summer months, the exceptions being a few small ponds that also derive water from seepage of groundwater.

    II. Maltese amphibiansAgainst the background of a dearth of freshwater and the almost total lack of perennial bodies of water, it is hardly surprising that the amphibian fauna of the Maltese Islands is very impoverished indeed. There is presently only one native species of amphibian, the painted frog Discoglossus pictus Otth, 1837 (Lanfranco 1955; Lanza 1973; Baldacchino and Schembri 2002). Cave deposits of Upper Pleistocene age have yielded the remains of a toad identified as Bufo bufo, while much younger deposits (spanning from ca 7200 BCE to modern times) from the same cave included bones of another toad (identified as Bufo viridis) and of Discoglossus pictus (Savona Ventura 1984). The occurrence of a Pleistocene toad is consistent with the much wetter climate and the existence of permanent surface water in the Maltese Islands during pluvial periods. The younger remains of toads and frogs may result from introduction of these animals by humans or from mixing of the surface layers with deeper layers of the cave deposits where these remains were found; there was much scope for such mixing, given the history of excavations of the cave (Hunt and Schembri 1999). Whatever the identity and origin of the fossil and subfossil toads of Malta, these are now extinct and there is no historic record or scientific evidence that any species of amphibian other than the painted frog has existed on the Maltese Islands in historic times.

    In 1913, Giuseppe Despott, a Maltese naturalist, attempted to introduce into Malta several amphibians (Bufo bufo, Bufo viridis, Bufo calamita, Hyla arborea, and other unspecified species) (Despott 1913), but this experiment failed (Baldacchino and Schembri 2002). Over the years, a number of amphibians have been imported for the pet and aquarium trade but there are no reports that any have escaped into the wild. However, in the late 1990s a population of Bedriaga’s Frog Pelophylax bedriagae, of unknown provenance, became established on Gozo (Sciberras and Schembri 2006).

    As presently recognized, Discoglossus pictus occurs in Sicily, the Maltese Islands, Tunisia, and Algeria and it has been introduced to parts of southern France and northeastern Spain, most likely from North Africa (Fromhage et al. 2004; Zangari et al. 2006). The North African populations have been regarded as a distinct subspecies (Discoglossus pictus auritus) from the Sicilian and Maltese ones (Discoglossus pictus pictus); however, recent genetic studies (Fromhage et al. 2004; Zangari et al. 2006) have only demonstrated a weak differentiation between Siculo-Maltese and North African populations that probably does not warrant the designation of subspecies.

  • Amphibian Conservation and Declines in Malta 19

    The origin of the Maltese population of Discoglossus pictus may be autochthonous via dispersal from Sicily across land connections or by rafting across narrow marine channels during marine downstands in the Late Miocene era or during the Pleistocene era, or it may have been facilitated by humans, as the lack of fossil remains prior to the prehistoric phase of human colonization of the islands suggests. Whatever their origin, the Maltese populations of Discoglossus pictus are reproductively isolated from those of Sicily and are of special conservation concern, thus qualifying as ‘designatable units’ (DUs) sensu Green (2005). DUs are recognized when not all populations of a species have the same probability of extinction and therefore need different management strategies; DUs are defined on the basis of some morphological, genetic, or distributional element and must have differing conservation status, but need not be evolutionary units and may be determined by ecology and conservation status alone (Green 2005). Moreover, the Maltese painted frog has gained the status of an iconic species for environmental NGOs, being the nation’s only native amphibian and, since the 1960s, such NGOs have campaigned intensely for the conservation of this taxon.

    III. Conservation status and threatsSurprisingly, given its status as Malta’s only native amphibian, very few studies have been conducted on the painted frog in the Maltese Islands. Apart from studies related to taxonomy and to the phylogenetic relationships of the Maltese populations to other populations of Discoglossus in the Mediterranean area (Lanza et al. 1986; Fromhage et al. 2004; Zangari et al. 2006), there is only one study on the biology of the species. Sammut and Schembri (1991) showed that, in the Maltese Islands, the main factor limiting reproduction was the availability of freshwater in quantities and situations that permit successful spawning and larval development, that the frog is able to breed in any available freshwater, and that larval development is abbreviated, taking on average some six weeks, depending on temperature, but with some individuals completing metamorphosis in as little as 46 days from hatching; however, development time is related to population density and, at high densities, it may be as long as 130 days. This species of frog was found to be a facultative breeder with reproduction taking place at all times of the year that water is available, although given the general desiccation during the dry season, reproduction generally was limited to the wet season. Sammut and Schembri (1991) suggested that rain may act directly to cue spawning since they observed frogs to emerge within hours of the first substantial rainfall at the end of the dry period. This frog is most abundant where freshwater is plentiful for most of the year. Such places are key breeding grounds that serve to regenerate populations in other areas where water is less abundant (Baldacchino and Schembri 2002). Populations living in suboptimal environments become extirpated during extended periods of aridity and such marginal habitats are re-colonized by frogs that have survived in more optimal situations.

    No dedicated studies on the distribution and abundance of the painted frog in the Maltese Islands have been made and information on these aspects is mostly based on the more or less casual records by naturalists and members of environmental NGOs. Based on these observations, the frog occurs on the islands of Malta and Gozo, but there are no confirmed records from Comino or any of the smaller islets (Baldacchino and Schembri 2002). On the islands where it occurs, it is predictably found in valleys (‘widien’), pools and wetlands, wherever there are cisterns and reservoirs on agricultural land, and in ponds and other artificial bodies of water.

    Although no actual quantitative data exist, the general impression is that populations have declined over the years (MEPA Nature Protection Unit 2005; MEPA 2010) and in its 2007 report to the European Commission on the implementation of the Habitats Directive, the national environ-ment agency (the Malta Environment and Planning Authority) gave the conservation status of Discoglossus pictus as “Inadequate & Deteriorating” (EEA 2008). Such a negative status might well

  • 20 Amphibian Biology

    be expected given that natural wetlands have decreased over the years for a variety of reasons, chief of which are over-extraction of water from the aquifers that supply such wetlands, tapping of water at source, and habitat destruction through development (MEPA 2010). Although extremely variable from year to year, there is no evidence that there is any declining trend in annual rainfall over the islands (NSO 2010) and neither have there been any reports, even anecdotal ones, of malformations, disease, or other abnormal conditions in local frogs.

    One cause of decline of the painted frog at particular sites has been the establishment of the alien Pelophylax bedriagae. At the time the alien frog was initially reported from the pool at Ta’ Sarraflu in Gozo in 2006, native and alien frogs co-existed. However, subsequent non-systematic observations at this site showed a thriving population of Pelophylax bedriagae but no adults or young of Discoglossus pictus (Thomas Glinka and Torsten Ruf, personal communication 2011). Sciberras and Schembri (2006) observed predation by Pelophylax bedriagae on larval and juvenile Discoglossus on numerous occasions; hence, this might be the cause of the demise of the Painted Frog population in this pool. Similarly, an artificial pool close to Għajnsielem in Gozo, where a population of Pelophylax bedriagae has become established, did not appear to have any Discoglossus pictus in it (Jacqueline Galea personal communication 2009; Thomas Glinka and Torsten Ruf personal communication 2011). Apart from these two sites, Pelophylax bedriagae is known from a reservoir at Tax-Xhejma, Gozo (Caroline Camilleri Rolls, personal communication 2011), from Il-Wied tax-Xlendi (Sciberras and Schembri 2006) and from a deep artificial pool at Nadur, all on Gozo, and from a reservoir within the grounds of a tourist complex at Mellieha Bay on the island of Malta (Sciberras and Schembri 2006). It appears that, unlike Discoglossus pictus, Bedriaga’s Frog is not capable of traversing substantial expanses of arid ground, and remains confined to places where there is water for most of the year. It seems therefore, that the alien frog is spreading to new sites due to human transport. Sciberras and Schembri (2006) stated that they have seen children at the Ta’ Sarraflu pool capturing the frogs with nets, presumably to be kept as ‘pets’, one attraction of the alien species being its loud call.

    IV. Conservation measures and monitoring programmesIn 1989, the Department of Information of the Government of Malta published the first comprehensive assessment of the conservation status of Maltese biota in the form of the Red Data Book for the Maltese Islands (Schembri and Sultana 1989). This assessment made use of the IUCN’s threat categories and criteria operative at the time and included annotations and discussion of threats. In this publication, Discoglossus pictus pictus was assessed as ‘Vulnerable’ and as having a restricted distribution in the Mediterranean (since as recognized then, the subspecies pictus was considered a Siculo-Maltese endemic) and in the Maltese Islands (due to the dearth of freshwater habitats on which the frog depends for survival) (Lanfranco and Schembri 1989). The chief threats faced by the frog were given as habitat destruction, pollution, and persistent persecution, the latter referring to the then common practice of frog-collecting and tadpole-collecting by children as a recreational activity, sometimes as a formally organized event under adult supervision (Schembri 1983; MEPA Nature Protection Unit 2005). Although having no legal status, being an official Government publication and commissioned by the Government agency responsible for the environment, a listing in the Red Data Book for the Maltese Islands was given consideration in the granting of permits for development projects; publication of the Red Data Book coincided approximately with the time development projects started to be assessed for their environmental impact.

    In 1991 the Maltese Parliament enacted comprehensive environmental legislation in the form of the Environment Protection Act 1991, which amongst other things gave the Minister responsible for the environment the power to issue regulations protecting species. Regulations protecting the

  • Amphibian Conservation and Declines in Malta 21

    painted frog under this Act were first issued in 1993 in the form of the Fauna and Flora Protection Regulations 1993. Since that time, these regulations were amended several times and the Act itself was replaced by new legislation, in part necessitated by Malta becoming a Member State of the European Union; however, the painted frog has remained a protected species since. Currently, Discoglossus pictus is listed in Schedule V (Animal and plant species of community interest in need of strict protection) of the Flora, Fauna and Natural Habitats Protection Regulations, 2006. These regulations transpose the requirements of the European Union’s ‘Habitats Directive’ (Directive 92/43/EEC) to local legislation; Discoglossus pictus is listed in Annex IV (Animal and plant species of community interest in need of strict protection) of the ‘Habitats Directive’.

    Its listing as a protected species is the only direct conservation measure for this species in Malta. The main effect of this listing has been to deter the overt persecution and collection of frogs and tadpoles. It must be noted that this achievement was only possible due to an intensive publicity campaign by environmental NGOs, and the government environmental agency, highlighting the uniqueness of this species in the local context and promoting its conservation, and because the same themes feature in the environmental education curriculum of local schools.

    Natural and semi-natural wetlands of all types are rare habitats in the Maltese Islands and practically all the significant ones have been scheduled as ‘Special Areas of Conservation – Candidate Sites of International Importance’ (SACs) under the Flora, Fauna and Natural Habitats Protection Regulation, 2006; most such sites have since been accepted by the European Commission as Natura 2000 sites in terms of the European Union’s ‘Habitats Directive’. Acceptance of these sites as part of the Natura 2000 network affords them and the biota within them a high level of protection that will eventually benefit the painted frog. Unfortunately, at the present time there have been no approved management plans published, let alone implemented, for any SAC and therefore there is as yet no active conservation management of any Discoglossus pictus population. Monitoring of biota within Natura 2000 sites is also a requirement of the ‘Habitats Directive’; however, if any monitoring of the painted frog populations has been made by the competent authority, results have not been made public. No assessment of the conservation status of Discoglossus pictus at regional level (the geographical extent of the Maltese Islands) using the currently operative 2001 IUCN Red List categories and criteria (IUCN 2003) has been made.

    V. ConclusionsThe painted frog, Discoglossus pictus, is the only native amphibian in the Maltese Islands. The species is limited to localities where there is sufficient water available, at least during part of the year, to allow it to complete its life cycle. Because of the general dearth of freshwater habitats in the Maltese Islands, the frog has an overall restricted distribution. Localities with perennial or very abundant water are key habitats for the species as they are the source of individuals that re-colonize suboptimal habitats from where the frog becomes extirpated during periods of severe aridity.

    No detailed studies on the population of the species have been made but there are indications that populations are declining, mainly due to alterations in habitat that result in a reduced water supply. In particular localities Discoglossus pictus populations apparently have been extirpated by the recently introduced Pelophylax bedriagae; however, this alien frog does not seem to spread well in the arid Maltese environment and is presently limited to a few localities where there is a relatively permanent water supply, whereas the native frog is able to survive in areas that are practically dry during the summer months. The painted frog is a legally protected species and this has served to reduce its collection and persecution, which were previously key factors contributing to population decline. There are no direct management programmes for the species.

  • 22 Amphibian Biology

    There is a pressing need for a scientific survey of the distribution and abundance of the painted frog in the islands as a whole, and, depending on the results of this survey, study of the factors that are contributing to the decline of particular populations. Such information can serve as a basis on which to build conservation management actions aimed at reversing any negative population trends.

    VI. AcknowledgementsI am grateful to the following persons for providing information: Alfred E. Baldacchino, Mariella Camilleri, Caroline Camilleri Rolls, Jacqueline Galea, Thomas Glinka, Torsten Ruf, Arnold Sciberras, and Jeroen Speybroeck.

  • Amphibian Conservation and Declines in Malta 23

    VII. ReferencesAnderson, E.W., 1997. The wied: a representative

    Mediterranean landform. GeoJournal 44: 111–114.

    Baldacchino, A.E. and Schembri, P.J., 2002. “Amfibji, Rettili u Mammiferi”. Publikazz-jonijiet Indipendenza, Pieta, Malta [in Maltese].

    Cassar, L.F., Conrad, E. and Schembri, P.J., 2008. The Maltese archipelago. In Mediterranean Island Landscapes: Natural and Cultural Approaches, ed. I.N. Vogiatzakis, G. Pungetti and A.M. Mannion. Springer, Heidelberg, Germany. Pp. 297–322.

    Despott, G., 1913. I nostri rettili. Archivum Melitense [Malta] 2: 93–96.

    EEA (European Environment Agency), 2008. Report on Implementation Measures (Article 17, Habitats Directive) – Malta – 2007 (avail-able at: http://cdr.eionet.europa.eu/Convert-ers/convertDocument?file=mt/eu/art17/envrf lrpw/general -report .xml&con-v=rem_26).

    Fromhage, L., Vences, M. and Veith, M., 2004. Testing alternative vicariance scenarios in western Mediterranean discoglossid frogs. Molecular Phylogenetics and Evolution 31: 308–322.

    Green, D.M., 2005. Designatable units for status assessment of endangered species. Conserva-tion Biology 19: 1813–1820.

    Hunt, C.O. and Schembri, P.J., 1999. Quaternary environments and biogeography of the Maltese Islands. In Facets of Maltese Prehistory, ed. A. Mifsud and C. Savona Ventura. The Prehistoric Society of Malta, Malta. Pp. 41–75.

    IUCN, 2003. Guidelines for Application of IUCN Red List Criteria at Regional Levels: Version 3.0. IUCN Species Survival Commission, IUCN, Gland, Switzerland and Cambridge.

    Lanfranco, G., 1955. Reptiles, amphibians of the Maltese Islands. Malta Year Book 1995: 198–203.

    Lanfranco, G. and Schembri, P.J., 1989. Verte-brates other than birds. In Red Data Book for the Maltese Islands, ed. P.J. Schembri and J. Sultana. Department of information, Malta. Pp. 129–142.

    Lanza, B., 1973. Gli anfibi e i rettili delle isole circumsiciliane. Lavori della Società Italiana di Biogeografia (Nuova Serie) 3: 755–804.

    Lanza, B., Nascetti, G., Capula, M. and Bullini, L., 1986. Les discoglosses de la région Méditerranéenne Occidentale (Amphibia; Anura; Discoglossidae). Bulletin de la Sociétè Herpetologique de France 40: 16–27.

    MEPA Nature Protection Unit, 2005. “Back-ground Note on the Exploitation of Wildlife” [Environment Report 2005]. Malta Environ-ment and Planning Authority, Floriana, Malta (available at www.mepa.org.mt/file.aspx?f=2142).

    MEPA (Malta Environment & Planning Author-ity), 2010. The Environment Report 2008. Sub-Report 8 Biodiversity. Malta Environment and Planning Authority, Floriana, Malta.

    NSO (National Statistics Office), 2010. Demo-graphic Review 2009. National Statistics Office, Valletta, Malta.

    NSO (National Statistics Office), 2012. Malta in Figures 2012. National Statistics Office, Valletta, Malta.

    Pedley, M.