Amphibian Biology: Status of Conservation and Decline of Amphibians: Eastern Hemisphere: Southern Europe & Turkey (Vol. 11/4) (Amphibian Biology, Vol. 11/4) [Illustrated] 1907807535, 9781907807534

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Amphibian Biology

Amphibian Biology Edited by Harold Heatwole and John W. Wilkinson Volume 11

Status of Conservation and Decline of Amphibians: Eastern Hemisphere

Part 4

SOUTHERN EUROPE AND TURKEY

Published by Pelagic Publishing www.pelagicpublishing.com PO 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

1

Franco Andreone

40 Amphibian conservation and declines in Malta

17

Patrick J. Schembri

41 Conservation and declines of amphibians in Croatia

25

Olga Jovanović and Dušan Jelić

42 Conservation and declines of amphibians in Slovenia

32

David Stanković, Martina Lužnik, and Katja Poboljšaj

43 Conservation and decline of European amphibians: The Republic of Serbia

45

Jelka Crnobrnja-Isailović and Momir Paunović

44 Amphibian declines and conservation in Montenegro

56

Ruža Ćirović

45 Status of amphibians in Bosnia and Herzegovina

62

Avdul Adrović

46 Conservation and protection status of amphibians in Macedonia

Bogoljub Sterijovski

47 Amphibians of Albania

67 74

Idriz Haxhiu

48 Declines and conservation of amphibians in Greece

80

Konstantinos Sotiropoulos and Petros Lymberakis

49 Amphibian conservation and decline in Romania

87

Dan Cogălniceanu and Laurenţiu Rozylowicz

50 Conservation and decline of amphibians in Hungary

99

Judit Vörös, István Kiss, and Miklós Puky

51 Conservation and declines of amphibians in Bulgaria

131

Nikolay Dimitrov Tzankov and Georgi Sashev Popgeorgiev

52 Amphibian conservation and decline in Turkey

140

Kurtuluş Olgun and Nazan Üzüm

53 Conservation of amphibians in Cyprus

148

Petros 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, Malaysia 1 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 Mongolia Sergius L. Kuzmin

3

Diversity and conservation status of Chinese amphibians Jianping Jiang, Feng Xie, and Cheng Li

4

The Conservation of Amphibians in Korea Daesik 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 amphibians Masafumi Matsui

6

Status and decline of amphibians of Afghanistan Indraneil Das

7

Amphibians of Pakistan and their conservation status Muhammad Sharif Khan

8

Status and decline of amphibians of India Indraneil Das and Sushil K. Dutta

9

Sri Lankan amphibians: Extinctions and endangerment Rohan Pethiyagoda, Kelum Manamendra-Arachchi, and Madhava Meergaskumbura

10 Amphibians of the Maldives Archipelago Indraneil Das

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

12 Status of amphibian studies and conservation in Bhutan Indraneil Das

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

14 Amphibian conservation: Myanmar Guinevere O.U. Wogan

15 Decline of amphibians in Thailand Yodchaiy Chuaynkern and Prateep Duengkae

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

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

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

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

20 Human impact on amphibian decline in Indonesia Djoko 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 Guinea Allen Allison

Part 2. North Africa (edited by Stephen D. Busack and Harold Heatwole) 2014, Basic and Applied Herpetology, Asociación Herpetológica Española, Madrid 23 Introduction Harold Heatwole and Stephen D. Busack

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

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

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

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

28 Amphibians in Libya: A status report Adel A. Ibrahim

29. Amphibians of Egypt: A troubled resource Adel A. Ibrahim

Part 3.Western Europe (edited by Harold Heatwole and John W. Wilkinson) 2013 31 Infectious diseases that may threaten Europe’s amphibians Trent 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 Ireland Ferdia Marnell

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

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

35 Amphibian declines and conservation in Belgium Gerald Louette and Dirk Bauwens

36 Amphibian declines and conservation in France Jean-Pierre Vacher and Claude Miaud

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

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

Contributors to Part 4 (Southern Europe and Turkey) EDITORS Heatwole, Harold, Department of Biology, North Carolina State University, Raleigh, NC 276957617, USA [email protected] Wilkinson, John W., Amphibian and Reptile Conservation, 655A Christchurch Road, Boscombe, Bournemouth, BH1 4AP, Dorset, UK [email protected]

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

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

Editors’ preface Different 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 I. Introduction

3. The red swamp crayfish

II. The status of the Italian amphibian fauna

IV. Conservation measures and monitoring programmes

III. Threats affecting the Italian batrachofauna

V. Conclusions

A.  Habitat alteration and urbanization B. The chytrid fungus in Italy and its significance for amphibian conservation

VI. Acknowledgements VII. Addendum VIII. References

C.  The introduced species 1. Fishes 2. Amphibians Abbreviations and acronyms used in the text or references: Bd Batrachochytrium dendrobatidis EN Endangered EU European Union ISPRA Italian National Institute for Environmental Protection and Research IUCN International Union for Conservation of Nature NIS Non-indigenous invasive species NT Near Threatened SHI Societas Herpetologica Italica SUV Sport utility vehicle VU Vulnerable WWF World Wide Fund for Nature

I.  Introduction With 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

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 influenced by the presence of two large mountain ranges (the Alps and Apennines), and a large continental 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). IUCN Red List Categorization Family

Species

Distribution

Global

National

Vulnerable

Vulnerable

CRO, ITA, MON, SER, SLO SAR

Habitat Directive Listing

PROTEIDAE 1

Proteus anguinus

II, IV

PLETHODONTIDAE 2

Atylodes genei*

Vulnerable

Vulnerable

3

Speleomantes ambrosii*

Vulnerable

Near Threatened SAR

II * II *, IV

4

Speleomantes flavus*

Vulnerable

Vulnerable

SAR

II *, IV

5

Speleomantes imperialis*

Near Threatened

Near Threatened SAR

II *, IV IV

6

Speleomantes italicus*

Near Threatened

Least Concern

ITA

7

Speleomantes sarrabusensis*

Vulnerable

Vulnerable

SAR

8

Speleomantes strinatii*

Near Threatened

Least Concern

ITA, FRA

IV

9

Speleomantes supramontis*

Endangered

Vulnerable

SAR

II *, IV

Least Concern

-

COR

IV

SALAMANDRIDAE 10

Euproctus montanus*



The Amphibians of the Italian Region: A Review of Conservation Status3 IUCN Red List Categorization Family

Species

Global

National

Distribution

Habitat Directive Listing IV

11

Euproctus platycephalus*

Endangered

Endangered

SAR

12

Ichthyosaura alpestris

Least Concern

Least Concern

ITA, OEC ITA

13

Lissotriton italicus*

Least Concern

Least Concern

14

Lissotriton vulgaris

Least Concern

Near Threatened ITA, OEC

15

Salamandra atra

Least Concern

Least Concern

ITA, OEC

16

Salamandra corsica*

Least Concern

-

SAR

17

Salamandra lanzai

Vulnerable

Vulnerable

ITA, FRA

18

Salamandra salamandra

Least Concern

Least Concern

ITA, OEC

19

Salamandrina perspicillata*

Least Concern

Least Concern

ITA ITA

IV IV IV

20

Salamandrina terdigitata*

Least Concern

Least Concern

21

Triturus carnifex

Least Concern

Near Threatened ITA, OEC

II, IV

Least Concern

Endangered

ITA, OEC

IV

Least Concern

Endangered

ITA, OEC

II, IV

PELOBATIDAE 22

Pelobates fuscus

PELODYTIDAE 23

Pelodytes punctatus

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 FRA, SPA

44

Pelophylax grafi

Least Concern

-

45

Pelophylax lessonae

Least Concern

Least Concern

ITA, OEC

46

Pelophylax perezi

Least Concern

-

FRA, SPA, POR, UK

IV

4

Amphibian Biology IUCN Red List Categorization

Family

Species

Global

National

Distribution

Habitat Directive Listing

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

Xenopus laevis#

Least Concern

-

ITA, OWC

PIPIDAE 52

II.  The status of the Italian amphibian fauna An 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, Pelophylax 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 Status5

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 urbanization

Most 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 Florence, 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 conservation

One 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 Status7

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 species 1.  Fishes Fish 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.  Amphibians Non-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 province 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 crayfish The 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 Status9

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 programmes The 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). Metaanalysis 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.  Conclusions In 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 (including 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 Status11

VI.  Acknowledgements I 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.  Addendum A 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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Valley as a major source of genetic variability. Molecular Ecology 16: 2734–2754. Cruz, M.J. and Rebelo, R., 2005. Vulnerability of Southwest Iberian amphibians to an introduced crayfish, Procambarus clarkii. Amphibia-Reptilia 26 (3): 293–303. Cruz, M.J., Rebelo, R. and G. Crespo, E., 2006. Effects of an introduced crayfish, Procambarus clarkii, on the distribution of south‐western Iberian amphibians in their breeding habitats. Ecography 29 (3): 329–338. Cruz, M.J., Pascoal, S., Tejedo, M. and Rebelo, R., 2006. Predation by an exotic crayfish, Procambarus clarkii, on natterjack toad, Bufo calamita, embryos: Its role on the exclusion of this amphibian from its breeding ponds. Copeia, 2006 (2): 274–280. Dell’Acqua, A., 1994. Rana verde maggiore, Rana ridibunda Pallas, 1771. In Atlante degli Anfibi e Rettili della Liguria, ed. G. Doria and S. Salvidio. Regione Liguria, Servizio Beni Ambientali e Naturali; Cataloghi dei Beni Naturali n. 2. Pp. 70–71. Denoël, M., Dzukic, G. and Kalezic, M.L., 2005. Effects of widespread fish introductions on paedomorphic newts in Europe. Conservation Biology 19 (1): 162–170. Di Rosa, I., Simoncelli, F., Fagotti., A. and Pascolini R., 2007. The proximate cause of frog declines? Nature 447: E4–E5. Di Tizio, L., Fiacchini, D. and Ferri V. (eds.), 2011. Quarto convegno “Salvaguardia Anfibi”, Riassunti e programma: 19. Faraone, F.P., Lillo, F., Giacalone, G. and Lo Valvo, M., 2008. The large invasive population of Xenopus laevis in Sicily (Italy). Amphibia-Reptilia 29: 405–412. Fattizzo, T. and Nitti, N., 2007. Prima segnalazione di Lithobates catesbeianus (Shaw, 1802) in Basilicata (Italia meridionale). Pianura 21: 201–207. Federici, S., Clemenzi, S., Favelli, M., Tessa, G., Andreone, F., Casiraghi, M. and Crottini, A., 2008. Identification of the pathogen Batrachochytrium dendrobatidis in amphibian populations of a plain area in the Northwest of Italy. Herpetology Notes 1: 33–37.

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and Fisher, M.C., 2006. The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biological Letters 2: 455–459. Gherardi, F., 2006. Crayfish invading Europe: The case study of Procambarus clarkii. Marine and Freshwater Behaviour and Physiology 39 (3), 175–191. Gherardi, F., Renai, B. and Corti, C., 2001. Crayfish predation on tadpoles: A comparison between a native (Austropotamobius pallipes) and an alien species (Procambarus clarkii). Bulletin Français de la Pêche et de la Pisciculture 361: 659–668. Hein, C.L.,Vander Zanden, M.J. and Magnuson, J.J., 2007. Intensive trapping and increased fish predation cause massive population decline of an invasive crayfish. Freshwater Biology 52: 1134–1146. Huner, J.V., 2002. Procambarus. In Biology of Freshwater Crayfish, ed. D.M. Holdich. Blackwell, Oxford. Pp. 541–584. IUCN, 2010. IUCN Red List of Threatened Species. Version 2010.1 (accessed at http://www.iucnredlist.org). Jesu R., Richard J., Mattioli F. and Mamone A., 2002. Due diverse strategie di allevamento di Pelobates fuscus insubricus. Atti del terzo Convegno “Salvaguardia Anfibi”, Lugano, 23–24 giugno 2000 – Cogecstre Ediz., Penne, 2002: 115–122. Knapp, R.A., 2005. Effects of nonnative fish and habitat characteristics on lentic herpetofauna in Yosemite National Park, USA. Biological Conservation 121 (2): 265–279. Lanza, B., 1962. On the introduction of Rana ridibunda Pallas and Rana catesbeiana Shaw in Italy. Copeia 1962 (3): 642–643. Lanza, B., Andreone, F., Bologna, M.A., Corti, C. and Razzetti, E., 2007. Fauna d’Italia. Amphibia. Calderini. Lanza, B., Nistri, A. and Vanni, S., 2009. Anfibi d’Italia. Quaderni di Conservazione della Natura; Numero 29. Ministero dell’Ambiente e della Tutela del Territorio e del Mare, ISPRA, Grandi and Grandi Editori.



The Amphibians of the Italian Region: A Review of Conservation Status15

Lillo, F., Faraone, F.P. and Lo Valvo, M., 2010. Can the introduction of Xenopus laevis affect native amphibian populations? Reduction of reproductive occurrence in presence of the invasive species. Biological Invasions 13 (7): 1533–1541. Litvinchuk, S.N., Crottini, A., Federici, S., De Pous, P., Donaire D., Andreone, F., Kalezic, M.L., Dzukic, G., Lada, G.A., Borkin, L.J. and Rosanov, J.M., 2013. Phylogeographic patterns of genetic diversity in the common spadefoot toad, Pelobates fuscus (Anura: Pelobatidae), reveals evolutionary history, postglacial range expansion and secondary contact. Organisms, Diversity & Evolution 13: 433–451. Livigni F. and Licata F., 2011. Waterfrog (Pelophylax sp.) found near Domusnovas in southwestern Sardinia, Italy. Herpetozoa 24 (1/2): 101–103. Mattoccia, M., Marta, S., Romano, A. and Sbordoni, V. 2011. Phylogeography of an Italian endemic salamander (genus Salamandrina): glacial refugia, postglacial expansions, and secondary contact. Biological Journal of the Linnean Society 104 (4): 903–992. Piazzini, S., Caruso, T., Favilli, L. and Manganelli, G., 2011. Role of predators, habitat attributes, and spatial autocorrelation on the distribution of eggs in the northern spectacled salamander (Salamandrina perspicillata). Journal of Herpetology 45 (3): 389–394. Romano, A., Ventre, N., De Riso, L., Pignataro, C. and Spilinga, C., 2010. Amphibians of the “Cilento e Vallo di Diano” National Park (Campania, Southern Italy): Updated check list, distribution and conservation notes. Acta Herpetologica 5 (2): 233–244. Rondinini, C., Battistoni, A., Peronace, V. and Teofili, C. (eds), 2013. Lista Rossa IUCN dei Vertebrati Italiani. Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Roma. Scalera, R., 2003. Anfibi e rettili italiani. Elementi di tutela e conservazione. Collana verde, 104. Corpo Forestale dello Stato. Ministero delle Politiche Agricole e Forestali. Roma.

Schembri, P.J., 2014. Amphibian Conservation and Declines in Malta. This volume, pp. 17–24. Sciberras, A. and Schembri, P.J., 2006. Geographic distribution. Rana bedriagae. Herpetological Review 37: 102. Scillitani, G. and Picariello, O., 2000. Genetic variation and its causes in the crested newt, Triturus carnifex (Laurenti, 1768), from Italy (Caudata: Salamandridae). Herpetologica 56 (1), 119–130. Scoccianti, C., 2001. Amphibia: aspetti di ecologia della conservazione [Amphibia: Aspects of conservation ecology]. WWF Italia, Sez. Toscana. Guido Peschino Grafica, Firenze. Scoccianti, C., 2004. Amphibians: threats and conservation. The Italian Journal of Zoology 71 (supplement 1): 9–15. Simoncelli, F., Fagotti, A., Dall’Olio, R., Vagnetti, D., Pascolini, R. and Di Rosa, I., 2005. Evidence of Batrachochytrium dendrobatidis infection in water frogs of the Rana esculenta complex in Central Italy. Ecohealth 2: 307–312. Societas Herpetological Italica, 2011. Assessing the status of amphibian breeding sites in Italy: a national survey. Acta Herpetologica 6 (1): 119–126, 2011. Solìs, R., Lobos, G., Walker, S.F., Fisher, M. and Bosch, J., 2010. Presence of Batrachochytrium dendrobatidis in feral populations of Xenopus laevis in Chile. Biological Invasions. Stagni, G., Scoccianti, C. and Fusini, R., 2002. Segnalazione di chytridiomicosi in popolazioni di Bombina pachypus (Anura, Bombinatoridae) dell’Appennino toscoemiliano. Abstracts IV Congresso della Societas Herpetologica Italica. Societas Herpetologica Italica, Napoli. Stagni, G.R. Dall’Olio, U. Fusini, S. Mazzotti, C. Scoccianti and A. Serra, 2004. Declining populations of Appenine yellow-bellied toad Bombina pachypus in northern Apennines, Italy: is Batrachochytrium dendrobatidis the main cause? Italian Journal of Zoology 71 (Supplement 1): 151–154. Tessa, G., Angelini, C., Bielby, J., Bovero, S., Giacoma, C., Sotgiu, G. and Garner, T.W.J., 2013. The pandemic pathogen of amphibians,

16 Amphibian Biology Batrachochytrium dendrobatidis (Phylum Chytridiomycota), in Italy. Italian Journal of Zoology 80 (1): 1–11. Tiberti R. and von Hardenberg A., 2012. Impact of introduced fish on Common frog (Rana temporaria) close to its altitudinal limit in alpine lakes. Amphibia-Reptilia 33: 303–307. Tiberti, R., von Hardenberg, A. and Bogliani G., 2013. Ecological impact of introduced fish in high altitude lakes: A case of study from the European Alps. Hydrobiologia. Tockner, K., Klaus, I., Baumgartner, C. and Ward, J.V., 2006. Amphibian diversity and nestedness in a dynamic floodplain river (Tagliamento, NE-Italy). Hydrobiologia 565 (1): 121–133. Van Buskirk, J., 2005. Local and landscape influence on amphibian occurrence and abundance. Ecology, 86 (7), 1936–1947. Verardi, A., Canestrelli, D. and Nascetti, G., 2009. Nuclear and mitochondrial patterns of introgression between the parapatric European treefrogs Hyla arborea and H. intermedia. Annales Zoologici Fennici 46: 247–258. Vorburger, C. and Reyer, H.U., 2003. A genetic mechanism of species replacement in European waterfrogs? Conservation Genetics 4 (2): 141–155. Weldon, C., Du Preez, L.H., Hyatt, A.D., Muller, R. and Speare, R. 2004. Origin of the amphibian chytrid fungus. Emerging Infective Diseases 12: 2100–2105. Woodhams, D.C., Rollins-Smith, L.A., Alford, R.A., Simon, M.A. and Harris R.N., 2007. Innate immune defenses of amphibian skin: antimicrobial peptides and more. Animal Conservation 10 (4): 425–428.

40 Amphibian conservation and declines in Malta Patrick J. Schembri I. Introduction

V. Conclusions

II.  Maltese amphibians

VI. Acknowledgements

III.  Conservation status and threats

VII. References

IV. Conservation measures and monitoring programmes

I.  Introduction The 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

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 amphibians Against 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 Malta19

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 threats Surprisingly, 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 environment 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 taxXlendi (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 programmes In 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 Malta21

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.  Conclusions The 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.  Acknowledgements I 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 Malta23

VII.  References Anderson, 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”. Publikazzjonijiet 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 (available at: http://cdr.eionet.europa.eu/Converters/convertDocument?file=mt/eu/art17/ envrflrpw/general-report.xml&conv=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. Conservation 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. Vertebrates 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. “Background Note on the Exploitation of Wildlife” [Environment Report 2005]. Malta Environment and Planning Authority, Floriana, Malta (available at www.mepa.org.mt/file. aspx?f=2142). MEPA (Malta Environment & Planning Authority), 2010. The Environment Report 2008. Sub-Report 8 Biodiversity. Malta Environment and Planning Authority, Floriana, Malta. NSO (National Statistics Office), 2010. Demographic Review 2009. National Statistics Office, Valletta, Malta. NSO (National Statistics Office), 2012. Malta in Figures 2012. National Statistics Office, Valletta, Malta. Pedley, M., Hughes Clarke, M. and Galea, P., 2002. Limestone Isles in a Crystal Sea: The Geology of the Maltese Islands. Publishers Enterprises Group, San Gwann, Malta. Sammut, M. and Schembri, P.J., 1991. Observations on the natural history of the painted frog Discoglossus pictus pictus (Amphibia: Anura: Discoglossidae) in the Maltese Islands (Central Mediterranean). Animalia [Catania, Italy] 18: 71–87. Savona Ventura, C., 1984. The fossil herpetofauna of the Maltese Islands; a review. Naturalista Siciliano (serie 4) 8: 93–106. Schembri, P.J., 1983. The painted frog ‘iz-zring’. Civilization [Malta] 5: 126–127. Schembri, P.J., 1997. The Maltese Islands: climate, vegetation and landscape. GeoJournal 41: 115–125. Schembri, P.J., 2003. Current state of knowledge of the Maltese non-marine fauna. In Malta Environment and Planning Authority Annual Report and Accounts 2003. Malta Environment

24 Amphibian Biology and Planning Authority, Floriana, Malta. Pp. 33–65. Schembri, P.J. and Sultana, J. (eds), 1989. Red Data Book for the Maltese Islands. Department of Information, Valletta, Malta. Sciberras, A. and Schembri, P.J., 2006. Occurrence of the alien Bedriaga’s frog (Rana bedriagae Camerano, 1882) in the Maltese Islands, and implications for conservation. Herpetological Bulletin 95: 2–5. Trump, D.H., 2002. Malta Prehistory and Temples. Midsea Books, Malta. Zangari, F., Roberta, C. and Giuseppe, N., 2006. Genetic relationships of the western Mediterranean painted frogs based on allozymes and mitochondrial markers: evolutionary and taxonomic inferences (Amphibia, Anura, Discoglossidae). Biological Journal of the Linnean Society 87 (4): 515–536.

41 Conservation and declines of amphibians in Croatia Olga Jovanović and Dušan Jelić I. Introduction A. General pressures on amphibian populations in Croatia

II. Conservation measures and monitoring programmes

III.  Red List IV. Summary V. Acknowledgements VI. References

Abbreviations or acronyms used in the text or references: CHS Hyla Croatian Herpetological Society Hyla EC European Commission EU European Union IPA Instrument for Pre-Accession Assistance MANMON Natura Management and Monitoring Project in Croatia (as part of IPA 2009) NSAP The National Strategy and Action Plan for the Protection of Biological and Landscape Diversity SINP State Institute for Nature Protection

I.  Introduction Croatia is a southern European country that ecologically includes four biogeographical regions: Continental, Alpine, Mediterranean, and Pannonian (Anonymous 2004). Due to the fact that the Pannonian Region in Croatia includes only a very small part of the east of Croatia, it has been proposed and accepted by the Standing Committee of the Bern Convention to include the Pannonian Region within the Continental Region (to allow easier and better management) (Anonymous 2010). During its geological history Croatia has acted as a glacial and interglacial refugium for northern European species, and its geographical position at the intersection of two regions has resulted in high biodiversity and endemism. The geographical position of Croatia also determines its climate, which is influenced mostly by the Adriatic Sea, the Dinarides’ orography, its elevation and position relative to the prevailing airflow, the openness of its northeastern parts to the Pannonian Plain, and the diversity of vegetation. Continental Croatia has a temperate continental climate due to its geographical position and to maritime influence; mean annual temperature ranges from 3°C in the highest mountainous areas to 17°C along the coast and on the islands of the middle and southern Adriatic. The lowland part of continental Croatia shows mild differences in mean annual air temperature, the most dominant temperature being about 11°C. Higher mean annual air temperatures (12°C) have been recorded only in the easternmost part of Croatia as a result of very warm summers in this, the most continental part of Croatia, and in the Zagreb area because of it being an urban heat island (a metropolitan area that is significantly warmer than its surrounding rural areas due to human activities). The mean annual amount of precipitation in Croatia ranges from

26 Amphibian Biology 300 mm to slightly over 3,500 mm. The smallest annual amounts fall on the outer islands of the southern Adriatic (Palagruža, 311 mm). The largest annual amounts of precipitation in Croatia fall in Gorski Kotar, on Mount Velebit, and on the northeastern slopes of the Konavle Plain (Konavosko polje) (from 3,000 mm to 3,500 mm). The annual amount of precipitation in continental Croatia decreases from west to east (Zaninović 2008). Table 41.1 List of recognized amphibian taxa in Croatia, with associated IUCN categories (from Jelić et al. 2012). DD = Data Deficient; EN = Endangered; LC = Least Concern; NE = Not Evaluated; NT = Near Threatened; VU = Vulnerable. Family

Genus

Species

Common Name

National / European IUCN Category

1

Salamandridae

Ichthyosaura

alpestris

Alpine Newt

LC / LC

2

Salamandridae

Lissotriton

vulgaris

Smooth Newt

LC / LC

Salamandridae

Lissotriton

vulgaris graecus

Greek Smooth Newt

LC / NE

3

Salamandridae

Triturus

carnifex

Italian Crested Newt

NT / LC

4

Salamandridae

Triturus

dobrogicus

Danube Crested Newt

NT / NT

5

Salamandridae

Salamandra

atra

Alpine Salamander

DD / LC

6

Salamandridae

Salamandra

salamandra

Fire Salamander

LC / LC

7

Proteidae

Proteus

anguinus

Olm

EN / VU

Proteidae

Proteus

anguinus ssp.n. Parzefall, Durand and Sket, 1999

Istrian Olm

EN / NE

8

Bombinatoridae

Bombina

bombina

Fire-bellied Toad

NT / LC

9

Bombinatoridae

Bombina

variegata variegata

Yellow-bellied Toad

LC / LC

variegata kolombatovici

Yellow-bellied Toad

NT / NE

10

Bufonidae

Bufo

bufo

Common Toad

LC / LC

11

Bufonidae

Bufotes

viridis

Green Toad

LC / LC

12

Pelobatidae

Pelobates

fuscus

Common Spadefoot

DD / LC

13

Hylidae

Hyla

arborea

Common Tree Frog

LC / LC

14

Ranidae

Pelophylax

kl. esculentus

Edible Frog

LC / LC

15

Ranidae

Pelophylax

lessonae

Pool Frog

LC / LC

16

Ranidae

Pelophylax

ridibundus

Marsh Frog

LC / LC

17

Ranidae

Rana

arvalis

Moor Frog

LC / LC

18

Ranidae

Rana

dalmatina

Agile Frog

LC / LC

19

Ranidae

Rana

latastei

Italian Agile Frog

EN / VU

20

Ranidae

Rana

temporaria

Grass Frog

LC/ LC

Despite its relatively small surface area (56,542 km2), Croatia has a high biodiversity that is reflected in the diversity of its amphibians; this is due to its geographical position and aforementioned biogeography. In Europe, 74 native amphibian species are recorded (Speybroeck et al. 2010). Of these, 20 are recognized from Croatia (Table 41.1, after Jelić et al. 2012; Jelić 2013), which represent about 25% of European species, some of which are endemic to the Dinaric Arc (e.g. the olm) (Jelić et al. 2012). Fortunately, the widespread, introduced and invasive American bullfrog (Lithobates catesbeianus) is still not recorded from Croatia. The amphibian fauna of Croatia can be divided into two separate ‘herpetological’ regions: 1) Continental-Alpine, and 2) Mediterranean (Figure 41.1). The Continental-Alpine Region corresponds to the floristic separation of the western Pannonian, eastern Pannonian, and Alpine macro-regions.



Conservation and Declines of Amphibians in Croatia27

Fig. 41.1 Map of the two herpetological regions in Croatia: (A) the continental and mountainous region, and (B) the Mediterranean region. From Jelić et al. (2012).

The Mediterranean region (with a Mediterranean macro-climate) was described by Nikolić and Topić (2005). The Continental-Alpine Region is inhabited by a total of 19 species of amphibians, 11 of which are closely linked only to this region: the alpine newt (Ichthyosaura alpestris), alpine salamander (Salamandra atra), fire salamander (S. salamandra), Italian crested newt (Triturus carnifex), Danube crested newt (T. dobrogicus), fire-bellied toad (Bombina bombina), common spadefoot (Pelobates fuscus), edible frog (Pelophylax kl. esculentus), pool frog (P. lessonae), moor frog (Rana arvalis), and grass frog (R. temporaria). The Mediterranean Region is inhabited by a total of 9 species of amphibians, with only a single species being closely linked to this region: the Italian agile frog (R. latastei) (Jelić et al. 2012). In total, examining amphibian diversity across the regions in Croatia, the most important area is the western part of the Continental-Alpine Region (Gasc et al. 1997), which has the highest diversity and importance.

A.  General pressures on amphibian populations in Croatia

Diversity and quality of habitats are important prerequisites for high species diversity. Croatia still harbours many freshwater habitats that are rarely found in most developed countries, and which represent important habitats for amphibians. Despite this, the majority of these habitats are under pressure. Floodplains, flooded forests, oxbow lakes, and tributaries of rivers face the threat of traditional water management practices that focus on technical measures, such as embankment, cutting of meanders, and melioration of floodplains. These habitats in Croatia are mostly found around the Drava, Sava, Danube, and Mura Rivers, and are important habitats for the fire-bellied toad, Danube crested newt, and common spadefoot (Jelić et al. 2012). Apart from that, landmanagement practices also pose threats to amphibian habitats, e.g. pollution, inappropriate use of pesticides, negligence of artificial ponds, habitat fragmentation, and urbanization (Janev-Hutinec

28 Amphibian Biology et al. 2006; Jelić et al. 2012). The valley of the karst River Mirna in Istria, inhabited by the Italian agile frog, is under great pressure from various human activities, such as intensive agriculture, use of pesticides, and inadequate infrastructure and regulations (Jelić et al. 2012). Other types of habitat that are probably the most threatened in Croatia are the small artificial karst ponds that were used for livestock and agriculture in the karst areas, where bodies of water are otherwise almost non-existent. Nowadays, when extensive grazing practices are abandoned, these ponds are not maintained and either are filled in and destroyed, or dry up. When these ponds represent the only bodies of water in which amphibian species can breed, their disappearance represents the greatest threat to the persistence of amphibians in these areas (Jelić et al. 2012). All these threats are representative of most threats already recognized globally for amphibians (Stuart et al. 2004; Beebee and Griffiths 2005; McCallum 2007) and reptiles (Reading et al. 2010). In addition, in some areas of Croatia (e.g. the Gorski Kotar region), the illegal poaching of frogs still occurs and threatens the existence of brown frog populations (Rana dalmatina and R. temporaria) in that area (personal observation by O.J. 2010). Another factor influencing amphibian populations in Croatia is introduced fish species that inhabit stagnant freshwater habitats and predate amphibian larvae. The most famous amphibian species found in Croatia and also the only true vertebrate stygobiont, the olm (Proteus anguinus), is threatened by such disturbance of karst cave systems as spring capping and pollution (Janev-Hutinec et al. 2006). Submerged underground systems, inhabited by the olm, are most threatened by the leaking of inorganic and organic pollutants into the karst systems, as well as by direct illegal dumping into caves (Jelić et al. 2012). The worldwide spread of the fungal disease caused by Batrachochytrium dendrobatidis (Bd), has not yet been confirmed in Croatia (Vörös and Jelić 2011). The Croatian Herpetological Society (CHS) Hyla began sampling and monitoring during 2009 in cooperation with Dr. Judit Vörös, from the Hungarian Natural History Museum, and this is still taking place. Proteus anguinus was also tested for the presence of Bd in order to determine whether it can survive in cold cave water (4–8°C). All tests have so far proven negative.

II.  Conservation measures and monitoring programmes Until recently, all amphibian species in Croatia were protected by law (Nature protection Act, and Ordinance on the proclamation of protected and strictly protected wild taxa; Official Gazette (OG) 99/09). However, new Ordinance (not yet implemented) recognizes only the strictly protected species, i.e. threatened and endemic species, species included under those categories in the EU legislation, and species included in International Conventions that have been adopted by Croatia. According to this new Ordinance, 13 species should be strictly protected. Conservation of amphibians is also included in The National Strategy and Action Plan for the Protection of Biological and Landscape Diversity (NSAP), which is the fundamental strategic document for nature conservation in the Republic of Croatia (OG 81/99, OG 143/08). Despite the fact that amphibians in Croatia are legally protected, the aforementioned illegal poaching still represents a threat. Luckily, with the involvement of local communities and The Directorate for Inspection of Nature Protection, this practice is becoming less frequent, and the protection of frogs in this region is being promoted through an annual Frog Night that includes a frog-jumping contest, and a Frog Museum, both located in the small town of Lokve. At present there are no organized monitoring programs for the majority of amphibian species in Croatia. Since 2012, however, the PROTEUS project was launched, dealing with the conservation and monitoring of P. anguinus in Croatia. Through this project, the first national amphibian monitoring program was established: 1) Four cave systems are monitored four times each year and P. anguinus individuals are counted on marked transects during cave-diving; DISTANCE



Conservation and Declines of Amphibians in Croatia29

software is used to estimate density and 2) environmental DNA methodology is used to monitor the presence of P. anguinus in inaccessible cave systems (traces of DNA are registered in water samples). In the period from 2005 to 2010, CHS Hyla carried out a project on the monitoring of R. latastei in Istria. Apart from that, CHS Hyla conducted several inventories and established monitoring projects on certain amphibian species, but mostly this was not carried out continuously (e.g. a Road Call Count in the Baranja region; Salamandra atra on Žumberak Hills and in the Gorski Kotar area; Rana arvalis in the Sava River floodplains). In addition, CHS Hyla is collecting records of all herpetofaunal encounters in Croatia and provides these data to SINP. Since 2011, CHS Hyla is also publishing an online bulletin (Hyla Herpetological Bulletin 2011–2013) with the emphasis on research of local importance in the South East European region, especially biodiversity, distribution mapping, and conservation. During the end of 2008, SINP organized and conducted the first freshwater restoration project in Croatia, with the main goal of conserving amphibian species. Restoration covered a system of three ponds in Mrkopalj (Sungerski lug, Gorski Kotar), two of which were filled in by garbage, wood dust, and communal waste. During 2009, a detailed survey of the restoration site was carried out and 10 amphibian species were found in this habitat (Salamandra salamandra, Triturus carnifex, Ichthyosaura alpestris, Lissotriton vulgaris, Rana temporaria, R. dalmatina, Pelophylax ridibundus, Bombina variegata, Bufo bufo, and Hyla arborea). This demonstration project showed a very positive effect of pond restoration on the populations of amphibians present in the area (Jelić and Marchand 2009). Additionally, some sites are being monitored locally for amphibian fauna in the spring, especially in the areas with high road mortality, e.g. Koprivnica (Samardžić 2004) and Nedelišće – with the emphasis on Bufo bufo and other species encountered during migrations – (Janev-Hutinec et al. 2013). However, national monitoring protocols (schemes and programmes) were developed for three species, Rana latastei, Triturus carnifex, and T. dobrogicus in 2013 by SINP in collaboration with CHS Hyla, through the IPA MANMON project. These protocols will be implemented from 2014 until 2019 when Croatia is due to give its first Natura 2000 monitoring report. A monitoring protocol for Proteus anguinus is also currently being prepared through the PROTEUS project in Croatia (www.proteus.hibr.hr). Within the next two to three years, it is planned to develop national monitoring protocols for other amphibian species listed on Appendices II and IV of the Habitats Directive, either for each species separately, or combined. In compliance with that, the monitoring will be carried out by experts who will report their findings back to SINP. A Management Plan, including an Action Plan for the conservation of Proteus anguinus in Croatia, is projected for 2014–2015. It will be prepared by SINP in collaboration with CHS Hyla. The new Red List of amphibians and reptiles of Croatia (Jelić et al. 2012) describes in detail all main threats to amphibians, as well as many local and species-specific problems. For each species, a list of precise conservation activities is given which should be carried out to decrease threats. This enables managers of protected areas, policy makers, and conservation practitioners at all levels (local and national) to adopt this in their yearly plans, and to follow the prescribed activities. One of the obstacles in the development of legal instruments is a general lack of basic distributional data at a national level, not only for amphibians, but also for the Croatian fauna in general. In that context, in 2014 Croatia will receive a loan from the World Bank to finance a project run by the Croatian Ministry of Environmental and Nature Protection called “EU Natura 2000 Integration Project: Field research and laboratory processing for collecting new inventory data for taxonomic groups: Actinopterygii and Cephalaspidomorphi, Amphibia and Reptilia, Aves, Chiroptera, Decapoda, Lepidoptera, Odonata, Plecoptera, Trichoptera”. The goal of this project is to collect basic data on the distribution of selected faunal groups, including amphibians. All data collected within

30 Amphibian Biology this project will be stored in a Nature Protection Information System by SINP and used for the purpose of conserving nature.

III.  Red List Preparation for the first Red List of amphibians and reptiles in Croatia started in the year 2000, and the first edition was published in 2006 (Janev-Hutinec et al. 2006); a second edition was prepared by Jelić et al. in 2012. According to the revised Red List, out of the total of 23 amphibian taxa reported in Croatia, 3 are Endangered (Rana latastei, Proteus anguinus, and P. anguinus spp. n), 4 are Near Threatened (Triturus carnifex, T. dobrogicus, Bombina bombina, and B. variegata kolombatovici), 14 are of Least Concern and 2 are Data Deficient (Salamandra atra and Pelobates fuscus) (Table 41.1). On a global scale, two Croatian amphibian species are considered threatened: Proteus anguinus and Rana latastei (Jelić et al. 2012).

IV.  Summary Croatia, as a southeastern European country, is home to 20 amphibian species (13 anurans and 7 caudates), which is a relatively high diversity on the European scale and considering its relatively small area. However, the amphibian fauna of Croatia faces severe threats (as elsewhere on the global scale) and that has resulted in the legal protection of a majority of its taxa. Major causes of amphibian decline are technical interventions in natural freshwater habitats, agriculture and land management, and pollution. Fortunately, chytridiomycosis has not yet been observed in Croatia. Although there is no organized monitoring of amphibians on a national scale, national monitoring protocols have been prepared for three species (Rana latastei, Triturus carnifex, and T. dobrogicus) and the monitoring is planned to start in 2014. Action plans for amphibians in Croatia do not yet exist, but the first one is already in preparation (for Proteus anguinus). Generally, despite the fact that the situation for amphibians in Croatia is not perfect, Croatia is in the process of becoming a full member of the EU and is now responsible to the European Commission (EC), not just to the Croatian citizenry. Hopefully, the situation will improve significantly in the future, as is already heralded by the implementation of EC Directives.

V.  Acknowledgements We thank Patricija Gambiroža, from the State Institute for Nature Protection, for providing valuable data.



Conservation and Declines of Amphibians in Croatia31

VI.  References Anonymous, 2004. Emerald Network Pilot Project in Croatia – Final Report. Convention on the conservation of European wildlife and natural habitats. Croatian Ministry of Environmental Protection and Physical Planning, Strasbourg. Anonymous, 2010. Biogeographical Regions’ map. Convention on the conservation of European wildlife and natural habitats. Directorate of Culture and Cultural and Natural Heritage in collaboration with Marc Roekaerts. Strasbourg. Beebee, T.J.C. and Griffiths, R.A., 2005. The amphibian decline crisis: A watershed for conservation biology? Biological Conservation. 125: 271–285. Gasc, J-P., Cabela, A., Crnobrnja-Isailović, J., Dolmen, D., Grossenbacher, K., Haffner, P., Lescure, J., Martens, H., Martinez-Rica, J.P., Maurin, H., Oliveira, M.L., Sofianidou, T.S., Veith M. and Zuiderwijk, A. (eds), 1997. Atlas of Amphibians and Reptiles in Europe. Societas Europaea Herpetologica & Museum Nationall d’ Histoire Naturelle (IEGB/SPN), Paris. Hyla Herpetological Bulletin 2011–2013 (accessed at http://www.hhdhyla.hr/index. php/en/publikacije/hyla-herpetoloski-bilten). Janev-Hutinec, B., Jovanović, O., Šafarek, G., Janković, S., 2013. Žaba, kača, kuščarvodozemci i gmazovi u Međimurju. (Amphibians and Reptiles in Međimurje Region). Međimurska Priroda – Public Institution for Nature Protection. Međimurska County, Croatia. Janev-Hutinec, B., Kletečki, E., Lazar, B., Podnar Lešić, M., Skejić, J., Tadić, Z. and Tvrtković, N., 2006. Red Book of Amphibians and Reptiles of Croatia. Ministry of Culture, State Institute for Nature Protection, Croatia. Jelić, D., 2013. Checklist of Amphibians and Reptiles of Croatia with bibliography of 250 years of research. Natura Sloveniae (in press). Jelić, D. and Marchand, M.A., 2009. Restoration and conservation of small ponds as important habitat for amphibians – example of ponds in Sungerski lug forest. Book of Abstracts 10th Croatian Biological Aongress, Osijek: 306–307.

Jelić, D., Kuljerić, M., Koren, T., Treer, D., Šalamon, D., Lončar, M., Podnar-Lešić, M., Janev-Hutinec, B., Bogdanović, T. and Mekinić, S., 2012. Red Book of Amphibians and Reptiles of Croatia. Ministry of Environmental and Nature Protection, State Institute for Nature Protection, Zagreb, Croatia. Pp. 232. McCallum, M.L., 2007. Amphibian decline or extinction? Current declines dwarf background extinction rate. Journal of Herpetology 41: 483–491. Nikolić, T. and Topić, J., 2005. The Red Book of Vascular Flora of Croatia. Ministry of Culture, State Institute for Nature Protection, Zagreb, Croatia. Parzefall, J., Durand, J.P. and Sket, B. 1999. Proteus anguinus Laurenti, 1768 – Grottenolm. In Grossenbacher, K. and Thismeier, B. (eds), Schwanzlurche I, Handbuch der Reptilien und Amphibien Europas. Aula Verlag, Wiesbaden. Pp. 57–76. Reading, C.J., Luiselli, L.M., Akani, G.C., Bonnet, X., Amori, G., Ballouard, J.M., Filippi, E., Naulleau, G., Pearson, D. and Rugiero, L., 2010. Are snake populations in widespread decline? Biology Letters, rsbl20100373. Samardžić, M., 2004. Ah, te žabe! Ecological Society Koprivnica, Croatia. Speybroeck, C., Beukema, W. and Crochet, P.-A., 2010. A tentative species list of the European herpetofauna (Amphibia and Reptilia)— an update. Zootaxa 2492: 1–27. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. and Waller. R.W., 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786. Vörös, J. and Jelić, D., 2011. First steps to survey chytrid fungus in Croatia. HYLA 2011 (1): 31–34. Zaninović, K. (eds), 2008. Climate atlas of Croatia: 1961–1990: 1971–2000. Meteorological and Hydrological Service, Zagreb, Croatia.

42 Conservation and declines of amphibians in Slovenia David Stanković, Martina Lužnik, and Katja Poboljšaj I. Introduction II.  Declining species A. General pressures on amphibian populations in Slovenia B. Declining amphibian species and species of special conservation concern

III. Conservation measures and monitoring programmes

A. Historical background of conservation measures and legislation for protecting amphibian species in Slovenia B.  Conservation measures C.  Monitoring activities

IV.  Red List of Slovenian amphibians V. Conclusion VI. Acknowledgements VII. References

Abbreviations or acronyms used in the text or references: EU NGO CKFF SEA SHS

European Union Non-governmental Organization Centre for Cartography of Fauna and Flora Strategic Environmental Assessment Societas Herpetologica Slovenica

I.  Introduction Slovenia is situated partly in Central Europe and partly in the northern Balkan Peninsula and straddles the junction of four main biogeographical regions – Alpine, Dinaric, Mediterranean, and Pannonian. This makes Slovenia a contact zone whose nature is influenced by all these regions and the transitions between them, which is also reflected in its herpetofauna. With 20 reported species of native amphibians (including Pelophylax kl. esculentus), Slovenia ranks among the richest of Palaeactic countries in terms of its amphibian diversity (Anthony et al. 2008), especially considering its small size. Because of the mountainous character of the Alpine and Dinaric regions, Slovenia’s average elevation is slightly above 556 m (Perko and Orožen Adamič 1999). The Alpine region in the northern and western parts of the country (42.1% of the country’s total area) includes the highest mountains and the highest valleys of the major rivers; while high plateaus, deep and narrow valleys, and flat karst poljes (karstic plains) characterize the physical relief of the Dinaric region (28.1%) in the south (Verovnik et al. 2012). The karst poljes with their intermittent rivers and lakes are the only surface wetlands in most of this region; in addition there are subterranean caves. Towards the east of the country, the average elevation drops as the mountainous terrain of the Alpine and Dinaric region turns into the Pannonian lowland. This region (21.2%) is comprised of



Conservation and Declines of Amphibians in Slovenia33

the lower reaches of major rivers that dissect wide plains and smaller hilly landscapes. As this region is also covered by numerous fishponds, gravel pits, reservoirs, and other artificial bodies of water, it is the richest in terms of surface wetlands. The average elevation also drops in the southwestern part of the country towards the Adriatic Sea, where the Mediterranean region starts. The Mediterranean region is characterized by plains and low hills. A Mediterranean climate prevails along the coast, but its impact reaches further inland. This region has higher temperatures and is under a strong Mediterranean influence; it also had favourable conditions during the Quaternary glaciations when the region acted as a refugium for at least some amphibian species (Garner et al. 2004; Canestrelli et al. 2012; Wielstra et al. 2013). Throughout history, human activities have played a very important role in terms of amphibian distribution and richness. Besides the negative effects, which are more obvious, human activities also have some positive effects on amphibians in Slovenia, e.g. the construction of karst ponds in limestone areas of southwestern Slovenia. As surface water is very rare there, ponds enable amphibians and other water-dependent species to breed and inhabit areas that were previously not suitable.

II.  Declining species A.  General pressures on amphibian populations in Slovenia

From 1970 onwards, a significant decline in the diversity of landscapes and habitats has been witnessed (Verovnik et al. 2012). This is mostly the result of urbanization and intensive agriculture. Consequently, the fragmentation of suitable habitats has increased, raising the risk of extinction, especially for less common amphibian species. Here, the main causes of amphibian decline in the country are described. Many aquatic ecosystems are degraded because of an uncontrolled and dispersed urbanization pattern. More than half of the country’s population live in settlements with less than 2,000 inhabitants and, furthermore, between 400 and 600 hectares of land are lost to urbanization annually. If population densities were similar to those in other comparable countries, the proportion of urbanized areas could decrease by more than one third (Drozg 1999). This dispersed and uncontrolled pattern of settlement is also the reason for urbanization of floodplains and marshlands. Intensive urbanization of these areas started after the Second World War and today more than 3% of all buildings are located there (Gašperič 2004; Komac et al. 2008). To secure the inhabitants and infrastructure of such urban areas from flooding, huge resources have been devoted to the regulation and hydromorphological modification of watercourses and their riparian buffer zones (e.g. regulation of riverbanks; construction of levees; deepening of the watercourse). This also has led to the disappearance of many amphibian habitats in the Slovenian lowlands. An additional problem of dispersed settlement is nutrient and organic pollution, as dispersed urbanization requires a larger sewage infrastructure (Vodopivec 2001; Vrhovšek and Kroflič 2007). In terms of amphibian conservation in the Dinaric region, the dispersed settlement pattern also has a negative effect on subterranean ecosystems. Pollution and changes in levels of underground-waters and ground-waters threaten populations of Europe’s only cave-adapted vertebrate, the olm (Proteus anguinus) (Aljančič et al. 1993). As the olm’s biology and ecology is still nearly unknown, other direct threats that could affect this species are not yet adequately recognized. Especially after joining the European Union, road transport in Slovenia has increased threefold. The growth can be ascribed to the increase in domestic transport as well as to the transit arising from the geographical position of Slovenia (Ministrstvo za okolje in prostor 2002). There are more

34 Amphibian Biology than 1,500 amphibian hotspots of road mortality in the country and mitigation measures are implemented only at a few (Sopotnik et al. 2013). The introduction of exotic predators, especially fish, has been reported to cause severe declines in many amphibian populations (Collins and Storfer 2003; Denoel et al. 2005; Orizaola and Braña 2006). Over past centuries, fish were introduced to many Slovenian mountain lakes. Only in one lake do fish and amphibians co-occur currently (Veenvliet and Kus Venvlieet 2008). Furthermore, the introduction of ornamental fish to ponds is becoming a serious problem, since there are increasingly fewer ponds without fish. Introduction of salmonids and other fish to karst springs could also represent a serious problem for the olm, as anglers occasionally report that Proteus is preyed upon by trout and rainbow trout (Lupinc 2012; Aljančič et al. 2013). The introduction of non-native amphibian species could also represent a problem. In 2007 the Balkan frog (Pelophylax kurtmuelleri) was reported at one pond in western Slovenia (Bressi 2007). No nationwide screening for the presence of chytridiomycosis or other amphibian disease is conducted regularly; however, in 2005, 29 amphibian samples tested negative (Garner et al. 2005). Because this disease has been recorded in all neighbouring countries (Spitzen van der Sluijs and Zollinger 2010; Spitzen-van der Sluijs et al. 2011), the possibility of its presence is very high. Other causes for amphibian decline in Slovenia are: (1) disappearance of ponds, especially in karst areas where surface watercourses are very rare; (2) draining of wetlands and other “worthless areas” to increase their economic potential; (3) illegal collecting for the food and pet trade. The extent of illegal collecting is not known, but attempts to trade in native amphibian populations have been registered – here special care should be focused on the olm, as its price on the black market is very high (Poboljšaj 2001).

B.  Declining amphibian species and species of special conservation concern

In Slovenia all native amphibian species are protected by law. Nevertheless, special concern should be focused on endemic, rare, and endangered species, as well as on genetically diverse species and unique populations. The olm or the cave salamander is not only a unique Slovenian amphibian, but it also has played a significant role in the nation’s history and has become one of its most recognized trademarks. In Slovenia, it inhabits subterranean habitats of the Dinaric bioregion, where so far it has been recorded at almost 200 localities. Most of those are included in the Natura 2000 network. At the moment, two subspecies have been recognized, the nominate subspecies and P. a. parkelj, a black subspecies. The black subspecies is known only at a few karst springs in Bela Krajina in southern Slovenia (Sket 1997). However, according to phylogenetic and phylogeographic analysis of mitochondrial DNA, the olm should be considered as a group of species and not a single one (Gorički and Trontelj 2006; Trontelj et al. 2007). In Slovenia at least two distinct lineages can be recognized and they do not correspond to the currently-recognized (white and black) subspecies. In the Rules on the inclusion of threatened plant and animal species in the Red List, the white olm is defined as a vulnerable subspecies, while the black subspecies is defined as a rare subspecies that is potentially at risk because of high endemism or limited range. Key threats for both taxa are all types of pollution of underground karst areas, causing deterioration in the quality of the olm’s habitat (Aljančič et al. 1993; Hudoklin 2011). In recent years, new negative impacts, that are to a large extent the consequence of intensive agriculture and unregulated disposal of municipal waste, have been documented in addition to unremediated existing impacts (Hudoklin 2011). The Italian agile frog (Rana latastei) is an endemic species of the Padano Venetian plain (Barbieri and Bernini 2004). Slovenian populations are found mainly in the Vipava valley in the west; however, the recent confirmation of this species along the Dragonja River Valley in Istra was not surprising (Glasnović 2012; Stanković and Poboljšaj 2013). As this species is present only in a small



Conservation and Declines of Amphibians in Slovenia35

part of the country and inhabits lowland river forests that are under severe pressure, it is regarded as endangered by the National Red List of amphibians. According to Garner et al. (2004) populations east of the River Adige (Italy), including Slovenian and Croatian ones, hold the highest genetic variability across the entire geographic range. We could therefore count Slovenian populations among the most valuable and important in Europe and therefore worthy of special protection. Species and populations that are characteristic of the Pannonian lowlands of southeastern and northeastern Slovenia also require special conservation attention, as habitats in this region have been strongly affected by intensive agriculture, regulations of rivers, and construction of infrastructure. The common spadefoot toad (Pelobates fuscus), the fire-bellied toad (Bombina bombina) and the moor frog (Rana arvalis), together with the Danube crested newt (Triturus dobrogicus), reach their southwestern distributional limit in Slovenia. Of these amphibians, P. fuscus and B. bombina are classified as endangered by the Red List. The threat of their local extirpation appears to be even higher in the lowlands of southeastern Slovenia, where especially P. fuscus appears to be very rare (Kink 2011; Vogrin 1997). On the other hand, B. bombina and its hybrids with B. variegata can still be found in both lowlands, but their distribution is poorly known and hybridization has been estimated only from morphological characters (Poboljšaj et al. 2011). Even though R. arvalis is not classified as endangered, the population from central Slovenia, recently discovered, should receive special attention. It appears that this population is still quite numerous despite the fact that it can be found only in a few isolated localities in the marshes near the capital city, where they are threatened by human activities such as urbanization, intensive farming, and recreational activities (Stanković and Cipot 2013). Furthermore, T. dobrogicus was also recently discovered in Slovenia. Its known distribution is currently restricted only to a few oxbow lakes of the River Mura in the northeastern part of the country (Stanković and Delić 2012). Special attention should also be given to populations of the Italian crested newt (T. carnifex) and of the smooth newt (Lissotriton vulgaris) from the Istra region in southwestern Slovenia, where several unique mitochondrial haplotypes have been discovered (Lužnik 2013; Lužnik et al. 2011a), as well as to the alpine newt (Ichthyosaura alpestris). The northern border of the glacial refugium for the alpine newt runs into Slovenia, which is reflected in the high genetic diversity of this species in the country (Lužnik et al. 2011b). Two additional subspecies or forms of the alpine newt from the montane lakes of the Eastern Julian Alps were described by Seliškar and Pehani (1935): I. a. lacusnigri from Črno jezero Lake, and the predominantly paedomorphic I. a. lacustris from the Jezero na Planini pri jezeru Lake. Presumably both subspecies became extinct when fish were introduced to both localities. In 2008, Veevnliet and Kus Veenvliet showed that individuals resembling I. a. lacusnigri can still be found at Črno jezero Lake. However, a molecular genetic analysis of museum samples showed that the subspecific status of this form is questionable (Lužnik et al. 2011b). The last group of species that deserves special concern are amphibians whose distribution and biology in Slovenia are poorly known and are therefore presumably rare. These are the alpine salamander (Salamandra atra) and the green toad (Bufotes viridis). It is known that S. atra inhabits the Alpine and the Dinaric bioregion, but its distribution is not well known (Poboljšaj & Stanković 2011). Preliminary results indicate that genetic diversity is quite high in the Slovenian populations (Razpet 2011, 2012). On the other hand, there has been no research whatsoever focusing on Slovenian populations of B. viridis. Most records come from the lowlands and the great majority of recorded breeding sites are urban habitats.

36 Amphibian Biology

III.  Conservation measures and monitoring programmes A.  Historical background of conservation measures and legislation for protecting amphibian species in Slovenia

The protection of Slovenian amphibians has been implemented into national legislation only in recent decades. Nevertheless, the first attempts to protect amphibians can be traced back to a Memorandum of the section for nature conservation and nature monuments at the Museum Society (Beuk 1920). Unfortunately, this national programme for nature conservation was never fully implemented. Among other things, the authors demanded protection of caves and their fauna, which also included the olm; establishment of protected areas, such as Ljubljana moor; and protection of a whole list of species, including toads. The first amphibian checklist was presented by Sket (1967) and the first Red List of threatened amphibians in 1992 by Sket (1992); the Red List was updated in 2002. With Slovenia’s independence, new legislation was adopted, and ever since 1993 all amphibian species are protected by the Decree on the protection of endangered animal species. Even though the current legislation is very good, the implementation is weak, since the government has not shown a great deal of interest in active conservation of amphibians.

B.  Conservation measures

In recent years a few NGOs and some governmental agencies have carried out different projects and amphibian conservation activities. Most of them have dealt with the mortality of amphibians on roads, restoration of ponds, raising public awareness, and education of youth. Amphibian mortality on roads was recognized as a serious threat to biodiversity relatively early; however, this problem is still not addressed adequately (Sopotnik et al. 2013). The first mitigation measures to reduce amphibian mortality from traffic took place during the construction of the Ljubljana–Kranj motorway in the early 1980s, when an amphibian underpass and a substitute breeding pond were constructed. Regrettably, the system stopped functioning over time due to lack of maintenance (Poboljšaj 2007). Afterwards, it took almost two decades until construction of underpasses and other mitigation measures countering amphibian mortality on roads became a common practice in the construction of new motorways, and it still needs improvement. In the past decade, the activities of NGOs, especially the Centre for Cartography of Fauna and Flora (CKFF) and Societas Herpetologica Slovenica (SHS), have helped raise public awareness of this issue. This, in turn, led to the establishment and organization of several volunteer groups for carrying out amphibian road-crossing patrols during spring migrations. Since 1997, when the SHS and Natural History Museum of Slovenia organized the first such action near the city of Koper in western Slovenia, the number of volunteer groups has increased substantially. In 2013, temporary fences for amphibians were erected at seven locations, while about ten additional groups carried amphibians over the road without the help of fences. Besides the CKFF and SHS, various local animal welfare societies also participate in the coordination and organization of volunteers. In addition, guidelines for volunteer groups have been prepared and published (Veenvliet and Kus Veenvliet 2010) and web pages for coordination of volunteers have been started. Based on the reports of the volunteer groups, more than 45,000 amphibians were carried over roads in 2013. After reforming the Environment Protection Act and implementation of the Protocol for Strategic Environmental Assessment (SEA), assessment of environmental impacts has become obligatory for every proposed project that could have a significant effect on the environment. However, because there is lack of knowledge among planners and contractors, the mitigation measures for amphibians often are not properly planned and carried out. Another large problem with amphibian mitigation measures is the absence of control and monitoring of the measures put in place. This also has been the case with amphibian underpasses and fences on newly constructed motorways.



Conservation and Declines of Amphibians in Slovenia37

In the past 15 years, much effort has been focused on collecting data on hotspots of amphibian mortality on roads. So far, data on more than 1,500 hotspots on more than 10,000 km of roads have been collected (Poboljšaj et al. 2000; Sopotnik 2013; Sopotnik et al. 2013). Most of the data were collected during 2005–2007 when the CKFF conducted an INTERREG (cross-border) SloveniaAustria project “Protection of bats and amphibians in the Region of Alpe-Adria”. The project also focused on collecting data on amphibian distribution, restoration of amphibian breeding sites, and general education about amphibian conservation and protection. One of the more important amphibian conservation activities is the inventory of breeding sites. In 2000, the project “Karst ponds as a network of aquatic biotopes” was carried out in collaboration with various NGOs from Slovenia and abroad. The main purpose of the project was assessing the condition of breeding grounds and setting up a database of ponds; this database is still growing. This was a starting point for future projects in the area, and elsewhere in Slovenia, where ponds are an important feature of the landscape. Between 2002 and 2005 the University of Primorska conducted a LIFE (European Union conservation) project: “Conservation of endangered habitats and species in the Karst region”. The project concentrated on the Karst’s edge, a transitional area connecting the Slovenian coast with the Karst plateau. Besides making inventories of endangered habitats and species, including amphibians, specific management plans were elaborated (Poboljšaj 2005). Several ponds were also restored, and detailed and clear management guidelines were written for the landowners. This work has been continued within the INTERREG Slovenia-Italy project BioDiNet (Network for the protection of biodiversity and cultural landscape). At the same time another follow-up project, which included monitoring of Triturus carnifex and Lissotriton vulgaris in ponds, and a study of their genetic makeup, was conducted in the same area (Lužnik 2013; Lužnik and Kryštufek 2013). The Mediterranean bioregion hosted another international project dealing with karst ponds between 2005–2007. The INTERREG Slovenia-Italy project “1001 ponds – 1001 life stories” was conducted by The Institute of the Republic of Slovenia for Nature Conservation, in collaboration with CKFF. The project focused on conservation and improvement of the pond network on the Karst plateau and the protection of amphibians. The project was a success, as it fully engaged the local community, especially by involving them in the activities and in training them as “pond wardens”. Almost sixty wardens qualified, over 1,700 ponds were recorded, and a dozen were restored in the traditional way. The activities continued after the project finished and even today local communities still restore and manage their ponds. Actions aimed at raising public awareness are one of the more important conservation activities because they have a long-term impact and focus on modification of human behaviour. Leaflets are published regularly to inform the general public on declining amphibian populations and amphibian conservation activities. Other public awareness activities include public lectures and excursions, while special attention is given to the education of youth through summer camps and workshops in schools, kindergartens, and in the field. Since the foundation of the SHS in 1995, data on amphibian distribution have been gathered systematically. The database is run by the CKFF and is not publicly available; the collected data will be presented in an atlas of the amphibians of Slovenia, which will be published sometime in the next few years. The database includes information both on the distribution of amphibians and on phenological observations (e.g. spawning; calling; larvae; courtship). Upon joining the European Union in 2004, the Slovenian government committed to adapting national legislation to that of the EU. The implementation of the Natura 2000 network, with its Habitats and Birds directives, has represented the biggest shift in Slovenian policy on nature and biodiversity and has significantly raised national standards regarding amphibian conservation

38 Amphibian Biology and protection. At the moment, there are 354 designated Natura 2000 sites, which encompass 37% of the country; 57 of these sites, which correspond to 24% of the country’s area, include at least one of the qualifying amphibian species (P. anguinus, R. latastei, B. bombina, B. variegata, T. carnifex, and T. dobrogicus).

C.  Monitoring activities

At the moment there is no national amphibian monitoring program in Slovenia. However, a first attempt to set up a monitoring scheme for Habitats Directive Annex II species of amphibian was recently carried out. In 2010 and 2011 the CKFF carried out a government-funded project to set up the monitoring of the target surface amphibian species; T. carnifex, R. latastei, B. variegata, and B. bombina (Poboljšaj et al. 2013). The proposed schemes for the monitoring of these species include recording species’ distributions and monitoring the sizes of populations. Since there are significant differences in the selected species’ distributions and ecologies, an individual approach in designing the schemes has been taken. Also, at present there are no separate monitoring schemes for different bioregions (Cipot et al. 2011; Poboljšaj et al. 2011). For B. variegata, the proposed scheme includes monitoring of the distribution of isolated populations, while additional records can be collected through monitoring of the Italian crested newt and other monitoring efforts. The proposed scheme also includes monitoring populations on 22 preselected sites, where population size is to be estimated by mark-release-recapture methods. As the distribution of B. bombina is less well known and the hybridization zone between the two species appears to be wider than previously believed, monitoring of populations and distributions cannot currently be set up; therefore, additional research is recommended (Poboljšaj et al. 2011). The proposed monitoring scheme for R. latastei suggests monitoring at sixteen different sites in western Slovenia. At six areas monitoring should be carried out annually, with the other areas being monitored biannually; also additional areas to be surveyed over longer periods of time will be selected (Lešnik et al. 2011). Research also should be focused on assessing the species’ distribution outside its core area, where its presence has been confirmed recently (Glasnović 2012; Stanković and Poboljšaj 2013). Even though T. carnifex is generally present in most of Slovenia, detailed knowledge on this species’ distribution is still insufficient. Therefore, monitoring of its distribution cannot currently be set up and additional research is recommended. However, the proposed scheme includes population monitoring at 27 preselected sites, while 3 more sites are to be added after additional research (Cipot et al. 2011). The biggest flaw in the proposed monitoring schemes is that there is still no national monitoring scheme for P. anguinus. However, the Society for Cave Biology, in cooperation with the Slovenian Academy of Science and Art, and the University of Ljubljana Biotechnical Faculty, are developing a methodology for monitoring the olm using detection of environmental DNA sampled from ground water (Aljančič et al. 2013).

IV.  Red List of Slovenian amphibians In the context of preparing the Biodiversity Conservation Strategy of Slovenia (Ministrstvo za okolje in prostor 2002), an analysis was made of the status of biodiversity, including a chapter on amphibians (Poboljšaj 2001). The result was a proposal for the new Red List, which consequently was published as new legislation in 2002 – Rules on the inclusion of endangered plant and animal species in the Red List, Official Gazette of the Republic of Slovenia No 82/2002 (Table 42.1). Since T. dobrogicus was just recently discovered in Slovenia, it does not yet have proper evaluation under either the Red List or protective legislation.



Conservation and Declines of Amphibians in Slovenia39

Table 42.1 Red list of Slovenian amphibians with their protection and conservation status. RL: Rules on the inclusion of endangered plant and animal species in the Red List, Official Gazette of the Republic of Slovenia No 82/2002, 42/2010. Ex - Probably extinct species or subspecies; E - Endangered species; V - Vulnerable species; R - Rare species; O - species with a low risk of becoming endangered; O1 - subcategory O, species protected by the Decree on protected wild animal species, Official Gazette of the Republic of Slovenia No.57/1993 which are not endangered now but have the potential of becoming endangered. DPA: Decree on protected wild animal species. Official Gazette of the Republic of Slovenia No. 46/04, subsequent corrections. 1A - Annex 1 (section A) protected native animals; 2A - Annex 2 (section A) protected native animals with habitat management protection; 2*A - priority species for conservation where the EU has a particular responsibility in relation to the proportion of their natural range, which lies within the European Union; 2B - Annex 2 (section A) protected non-native animals with habitat management protection. HD: European directive on conservation of natural habitats and of wild fauna and flora (Annex II - vulnerable/ sensitive species which could become endangered in the near future if the factors of threat continue to act; Annex IV - species that require strict protection; Annex V - species breeding and for which exploitation could be a matter of management); *priority species. Bern: Bern Convention on conservation of European wild flora, fauna, and natural habitats (II - Strictly protected animal species, III - Protected animal species). Species

Common Names

RL

DPA

HD

Bern

Proteus anguinus

Olm

V

1A, 2A*

II*, IV

II

Proteus anguinus parkelj

Black Olm

R

1A, 2A*

II*, IV

II

Salamandra salamandra

Fire Salamander

O

1A

/

III

Salamandra atra

Alpine Salamander

O1

1A, 2A

IV

II

Ichthyosaura alpestris

Alpine Newt

V

1A, 2A

/

III

Ichthyosaura alpestris lacusnigri

Alpine Newt

Ex

1A, 2A

/

III

Lissotriton vulgaris

Smoth Newt

V

1A, 2A

/

III

Triturus carnifex

Italian Crested Newt

V

1A, 2A

II, IV

II

Triturus dobrogicus

Danube Crested Newt

/

2B

II, IV

II

Bombina bombina

Fire-bellied Toad

E

1A, 2A

II, IV

II

Bombina veriegata

Yellow-bellied Toad

V

1A, 2A

II, IV

II

Pelobates fuscus

Common Spadefoot Toad

E

1A, 2A

IV

II

Bufo bufo

Common Toad

V

1A, 2A

/

III

Bufotes viridis

Green Toad

V

1A, 2A

IV

II

Hyla arborea

Tree Frog

V

1A, 2A

IV

II

Rana arvalis

Moor Frog

V

1A, 2A

IV

II

Rana temporaria

European Common Frog

V

1A

/

/

Rana dalmatina

Agile Frog

V

1A, 2A

IV

II

Rana latastei

Italian Agile Frog

E

1A, 2A

II, IV

II

Pelophylax ridibundus

Marsh Frog

V

1A, 2A

/

III

Pelophylax lessonae

Pool Frog

V

1A, 2A

IV

III

Pelophylax kl. esculentus

Edible Frog

V

1A, 2A

/

III

V.  Conclusion Slovenia is characterized by a rich herpetofauna; so far 7 species of tailed amphibians and 13 anuran species (including P. kl. esculentus) have been recorded. Even though the national legislation related to conservation and protection of amphibians and their habitat is good, the implementation is weak, as the government and its agencies do not demonstrate the necessary interest in active conservation of amphibians. In recent years, the implementation of the Natura 2000 network has contributed significantly to raising national standards regarding amphibian conservation. Currently,

40 Amphibian Biology 57 Natura 2000 sites include at least one of the qualifying amphibian species, which corresponds to more than 24% of the country’s surface. The major threats to amphibian populations in Slovenia are mostly related to uncontrolled and dispersed urbanization, regulation and hydromorphological modification of watercourses, nutrient and organic pollution, road transport, the introduction of non-native fish, and the disappearance of ponds. The risks related to infectious diseases could also represent a serious threat; however, no regular nationwide screening is conducted presently. In recent years, a few NGOs and some governmental agencies have carried out different projects and amphibian conservation activities. Most of them have dealt with mortality on roads, restoration of ponds, raising public awareness, and education of youth. In Slovenia, special consideration should also be given to Europe’s only cave-adapted vertebrate Proteus anguinus, for which changes in levels of pollution of ground-waters and subterranean waters also represent a key threat. One of the main current shortcomings of amphibian conservation in Slovenia is the lack of a regular nationwide monitoring programme. Nevertheless, some progress has been made. A first attempt to set up a monitoring scheme for species of amphibians in Habitats Directive Annex II was carried out recently, but unfortunately Proteus was excluded.

VI.  Acknowledgements We are grateful to the Centre for Cartography of Fauna and Flora and to Societas Herpetologica Slovenica and all its members, volunteers, and supporters for their help with amphibian conservation activities.



Conservation and Declines of Amphibians in Slovenia41

VII.  References Aljančič, M., Bulog, B., Kranjc, A., Josipovič, D., Sket, B. and Skoberne, P., 1993. Proteus: The Mysterious Ruler of Karst Darkness. Vitrum. Ljubljana. Aljančič, G., Gorički, Š., Magdalena, N., Stanković, D. and Kuntner, M., 2013. Endangerend Proteus: Combining DNA and GIS analyses for its conservation. In First International Workshop on Dinaric Karst Poljes as Wetlands of National and International Importance, ed. P. Sackl. Naše Ptice with Euronatur and Naša baština. Livno. Pp. 16–17. Anthony, B., Arntzen, J.W., Baha El Din, S., Böhme, W., Cogălniceanu, D., Crnobrnja-Isailovic, J., Crochet, P.-A., Corti, C., Griffiths, R., Kaneko, Y., Kuzmin, S., Wai Neng Lau, M., Li, P., Lymberakis, P., Marquez, R., Papenfuss, T., Pleguezuelos, J.M., Rastegar, N., Schmidt, B., Slimani, T., Sparreboom, M., Uğurtaş, İ., Werner, Y. and Xie, F., 2008. Amphibians of the Palaearctic Realm. In Threatened Amphibians of the World, ed. S.N. Stuart, M. Hoffmann, J.S. Chanson, N.A. Cox, R.J. Berridge, P. Ramani and B.E. Young. Lynx Edicions with IUCN – The World Conservation Union, Conservation International and Nature Serve. Barcelona. Pp. 106–111. Barbieri, F. and Bernini, F., 2004. Distribution and status of Rana latastei in Italy (Amphibia, Ranidae). Italian Journal of Zoology 71: 37–41. Beuk, S., 1920. Odsek za varstvo prirode in prirodnih spomenikov Muzejskega društva za Slovenijo, 1920. Spomenica Odseka za varstvo prirode in prirodnih spomenikov. Glasnik Muzejskega društva za Slovenijo 1: 69–75. Bressi, N., 2007. Pelophylax ridibundus (Pallas, 1771) in Italia, dalla rarefazione all’espansione e Pelophylax kurtmuelleri (Gayda, 1940), nuova specie per la Slovenia. Atti del museo civico di storia naturale di Trieste 53: 3–10. Canestrelli, D., Salvi, D., Maura, M., Bologna, M. A. and Nascetti, G., 2012. One species, three Pleistocene evolutionary histories: phylogeography of the Italian crested newt, Triturus carnifex. PloS One 7: e41754.

Cipot, M., Govedič, M., Lešnik, A., Poboljšaj, K., Skaberne, B., Sopotnik, M. and Stanković, D., 2011. Vzpostavitev monitoringa velikega pupka (Triturus carnifex) – Končno poročilo. Center za kartografijo favne in flore, Miklavž na dravskem polju. Collins, J. and Storfer, A., 2003. Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9: 89–98. Denoel, M., Dzukic, G. and Kalezic, M., 2005. Effects of widespread fish introductions on paedomorphic newts in Europe. Conservation Biology 19: 162–170. Drozg, V., 1999. Razpršena poselitev in okolje. In Mesta in Urbanizacija, ed. V. Prezml. Svet za varstvo okolja Republike Slovenije, Ljubljana. Pp. 16–19. Garner, T.W.J., Pearman, P.B. and Angelone, S., 2004. Genetic diversity across a vertebrate species’ range: a test of the central-peripheral hypothesis. Molecular Ecology 13: 1047–53. Garner, T.W.J., Walker, S., Bosch, J., Hyatt, A.D., Cunningham, A.A. and Fisher, M.C., 2005. Chytrid fungus in Europe. Emerging infectious Diseases 11: 1639–41. Gašperič, P., 2004. The expansion of Ljubljana onto the Ljubljansko barje moor. Acta Geographica Slovenica 44: 7–25. Glasnović, P., 2012. On the occurrence of the Italian agile frog (Rana latastei Boulenger, 1879) in the Slovenian part of Istria. Natura Sloveniae 14: 39–42. Gorički, Š. and Trontelj, P., 2006. Structure and evolution of the mitochondrial control region and flanking sequences in the European cave salamander Proteus anguinus. Gene 378: 31–41. Hudoklin, A., 2011. Are we guaranteeing the favourable status of the Proteus anguinus in the Natura 2000 network in Slovenia. In Pressures and Protection of the Underground Karst: Cases from Slovenia and Croatia = Pritiski in varovanje podzemnega krasa: primeri iz Slovenije in Hrvaške = Pritisci i zaštita podzemnog krša: primjeri iz Slovenije i Hrvatske, ed. M. Prelovšek, N. Zupan Hajna. Inštitut za raziskovanje Krasa ZRC SAZU. Postojna. Pp. 169–181.

42 Amphibian Biology Kink, B., 2011. Herpetološke značilnosti in naravovarstven pomen Krakovskega gozda – Herpetological characteristic and significance of the Krakovo forest. Varstvo narave 25: 71–86. Komac, B., Natek, K. and Zorn, M., 2008. Širjenja urbanizacije na poplavna območja. Geografski vestnik 80: 33–34. Lešnik, A., Cipot, M., Govedič, M. and Poboljšaj, K., 2011. Vzpostavitev monitoringa laške žabe (Rana latastei) – Končno poročilo. Center za kartografijo favne inflore. Miklavž na Dravskem polju. Lupinc, A., 2012. Človeška ribica. Ribič 71: 211. Lužnik, M., 2013. Ohranitveni status velikega (Triturus carnifex) in navadnega pupka (Lissotriton vulgaris) v sistemu izoliranih kraških vodnih teles – doktorska disertacija – Conservation status of Italian crested newt (Triturus carnifex) and smooth newt (Lissotriton vulgaris) in a system of isolated carstic ponds – Doctoral Dissertation. Univerza v Ljubljani, Biotehniška fakulteta, Ljubljana. Lužnik, M. and Kryštufek, B., 2013. Three years of population monitoring of newts (Lissamphibia, Salamandridae) in isolated karstic ponds. In Programme & Abstracts/17th European Congress of Herpetology, Veszprém, Hungary, University of Pannonia 22–27 August 2013. Societas Europaea Herpetologica. Veszprém. Pp. 262. Lužnik, M., Bužan, E.V. and Kryštufek, B. 2011a. Mitochondrial DNA reveals new lineage of the smooth newt Lissotriton vulgaris in SW Slovenia and Istria. In SEH European Congress of Herpetology & DGHT Deutscher Herpetologentag, Luxembourg and Trier, 25th to 29th September 2011. Societas Europaea Herpetologica and Deutsche Gesellschaft für Herpetologie und Terrarienkunde, Luxembourg and Trier. Pp. 110–111. Lužnik, M., Bužan, E.V. and Kryštufek, B., 2011b. Mitochondrial sequences do not support the independent taxonomic position of the extinct alpine newt subspecies Mesotriton alpestris lacusnigri. Amphibia-Reptilia 32: 435–440.

Ministrstvo za okolje in prostor – Ministry of the Environment and Spatial Planning, 2002. Strategija ohranjanja biotske raznovrstnosti v Sloveniji – Biodiversity conservation strategy of Slovenia. Ministrstvo za okolje in prostor. Ljubljana. Orizola, G. and Braña, F., 2006. Effect of salmonid introduction and other environmental characteristics on amphibian distribution and abundance in mountain lakes of northern Spain. Animal Conservation 9: 171–178. Perko, D. and OrozÏen AdamicÏ, M., 1998. Slovenija Ð Pokrajine in Ljudje. Mladinska Knjiga, Ljubljana. Poboljšaj, K., 2001. Analiza Stanja Biotske Raznovrstnosti: Dvoživke (Amphibia). Center za kartografijo favne in flore. Miklavž na Dravskem polju. Poboljšaj, K., 2005. Amphibians on Karst. In Diversity and Conservation of Karst Landscapes: Valencian and Slovenian Experiences, ed. E. Laguna, V. Deltoro, B. Lipej, M. Kaligarič and A. Sovinc. Generalitat Valenciana, Conselleria de territori i Habitatge, Valencia. Pp. 115–116, 152. Poboljšaj, K., 2007. Dvoživke in ceste – pregled stanja in tehničnih rešitev v Sloveniji. Ali smo v koraku z Evropo? In Varsto dvoživk v Regiji Alpe-Jadran: Zbornik prispevkov mednarodnega srečanja, 6–8. Junij 2007, Terme Radenci, Radenci, Slovenija, ed. K. Poboljšaj. Center za kartografijo favne in flore, Miklavž na Dravskem polju. Poboljšaj, K., Cipot, M., Govedič, M., Grobelnik, V., Lešnik, A., Skaberne, B. and Sopotnik, M., 2011. Vzpostavitev monitoringa hribskega (Bombina variegata) in nižinskega urha (Bombina bombina) –­ Končno poročilo. Center za kartgrafijo favne in flore. Miklavž na Dravskem polju. Poboljšaj, K., Cipot, M., Lešnik, A. and Govedič, M., 2013. First attempt to set up the national monitoring scheme for four target amphibian species in Slovenia. In Programme & abstracts/17th European Congress of Herpetology, Veszprém, Hungary, University of Pannonia 22–27 August 2013. Societas Europaea Herpetologica. Veszprém. Pp. 78.



Conservation and Declines of Amphibians in Slovenia43

Poboljšaj, K., Kotarac, M., Lešnik, A., Šalamun, A., Vesna, G. and Jakopič, M., 2000. Dvoživke in Ceste – Končno poročilo. Center za kartografijo favne in flore. Miklavž na Dravskem polju. Poboljšaj, K. and Stanković, D., 2011 The overview of genus Salamandra in Slovenia. In Alpine and Fire Salamanders Meeting, October 21st 2011, Hohenwerfen Fortress (Werfen), ed. V. Helfer. Razpet, A., 2011. Genetic diversity of alpine salamanders in Slovenia. In Alpine and Fire Salamanders Meeting, October 21st 2011, Hohenwerfen Fortress (Werfen), ed. V. Helfer. Razpet, A., 2012. Genska raznovrstnost planinskega močerada Salamandra atra. Acta triglavensia 1: 42. Seliškar, A. and Pehani, H., 1935. Limnologische Beiträge zum Problem der Amphibienneotenie (Beobachtungen an Tritonen der Triglavseen). Verhandlungen der Internationalen Vereinigung für theoretische und angewandte Limnologie 7: 263–294. Sket, B., 1967. Ključi za določanje živali – Dvoživke. Inštitut za biologijo Univerze v Ljubljani in Društvo biologov. Ljubljana. Sket, B., 1992. Rdeči seznam ogroženih vrst dvoživk (Amphibia) v Sloveniji. Varstvo narave 17: 45–49. Sket, B., 1997. Distribution of Proteus (Amphibia: Urodela: Proteidae) and its possible explanation. Journal of Biogeography 24: 262–280. Sopotnik, M., 2013. Popis črnih točk za dvoživke v Krajinskem parku Ljubljansko barje. Herpetološko društvo – Societas herpetologica slovenica. Ljubljana. Sopotnik, M., Jagar, T., Kirbiš, N., Lešnik, A., Ostanek, E., Petrovič, I., Poboljšaj, K., Rozman, A., Rozman, L., Stanković, D., Vamberger, M., Vlačič, D. and Žagar, A., 2013. Societas Herpetologica Slovenica’s activities for helping amphibians at road crossings. In Programme & abstracts /17th European Congress of Herpetology, Veszprém, Hungary, University of Pannonia 22–27 August 2013. Societas Europea Herpetologica, Veszprém. Pp. 291.

Spitzen van der Sluijs, A.M. and Zollinger, R., 2010. Literature review on Batrachochytrium. A report by RAVON for Invasive Alien Species Team (TIE); Ministry of Agriculture, Nature and Food Quality (Netherlands). http://ravon.nl/Portals/0/Pdf/Lit%20 studie%20Bd%20Def.pdf Stanković, D. and Cipot, M., 2013. Distribution and status of Rana arvalis in Central Slovenia. In Programme & abstracts/17 th European Congress of Herpetology, Veszprém, Hungary, University of Pannonia 22–27 August 2013. Societas Europea Herpetologica. Veszprém. Pp. 294. Stanković, D. and Delić, T., 2012 Morphological evidence for the presence of the Danube Crested Newt, Triturus dobrogicus (Kiritzescu, 1903), in Slovenia. Natura Sloveniae 14 (1): 23–29. Stanković, D. and Poboljšaj, K., 2013. New data on the distribution of the Italian agile frog (Rana latastei Boulenger, 1879) in Slovenian Istra. Natura Sloveniae 15 (2): 51–55. Trontelj, P., Gorički, Š., Polak, S., Verovnik, R., Zakšek, V. and Sket, B., 2007. Age estimates for some subterranean taxa and lineages in the Dinaric karst. Acta Carsologica 36: 183–189. Veenvliet, P. and Kus Veenvliet, J., 2008. Amphibians of the Eastern Julian Alps (Slovenia) with special attention to endemic forms of the alpine newt (Mesotriton alpestris). Zeitschrift für Feldherpetologie 15: 49–60. Veenvliet, P. and Kus Veenvliet, J., 2010. Smernice za akcije reševanja dvoživk z začasnimi ograjami ­– Različica 1.0 z dne 4.2.2010. Zavod Symbiosis, Metulje. Verovnik, R., Rebeušek, F. and Jež, M., 2012. Atlas dnevnih metuljev (Lepidoptera: Rhopalocera) Slovenije, Atlas of butterflies (Lepidoptera: Rhopalocera) of Slovenia. Atlas faunae et florae Sloveniae. Center za kartografijo favne in flore. Miklavž na Dravskem polju. Vodopivec, R., 2001. Pregled gradnje čistilnih naprav za čiščenje komunalnih odpadnih vod v Sloveniji – Overview of the construction of municipal wastewater treatment plants in Slovenia. Ekolist 1: 2–6.

44 Amphibian Biology Vogrin, N., 1997. A new record of the Common Spadefoot Pelobates fuscus fuscus (Laurenti, 1768), in Slovenia (Anura: Pelobatidae). Herpetozoa 10: 89–90. Vrhovšek, D. and Kroflič, B., 2007. Ekološka in ekonomska upravičenost rastlinskih čistilnih naprav na območjih razpršene poselitve. Geografski Obzornik 54: 13–16. Wielstra, B., Baird, A. B. and Arntzen, J.W., 2013. A multimarker phylogeography of crested newts (Triturus cristatus superspecies) reveals cryptic species. Molecular Phylogenetics and Evolution 67: 167–75.

43 Conservation and decline of European amphibians: The Republic of Serbia Jelka Crnobrnja-Isailović and Momir Paunović I. Introduction A. General pressures on amphibian populations

II. Declining species and species of special concern for conservation A.  Declining amphibian species B. Species of special concern for conservation

III. Conservation measures and monitoring programmes IV.  Species’ status V. Summary VI. Acknowledgements VII. References

Abbreviations and acronyms used in the text or references: CLC Corine Land Cover CORINE Coordination of Information on the Environment DTD Danube-Tisza-Danube ICPDR International Commission for the Protection of the Danube River IEGB/SPN Institut d’ Écologie et de Gestion de la Biodiversité / Service du Patrimoine Naturel IUCN International Union for the Conservation of Nature NGO non-governmental organization P protected PE Population Equivalent SP strictly protected WWTP wastewater treatment plant UN United Nations

I.  Introduction The area of The Republic of Serbia (including two autonomous provinces: Vojvodina in the north, and Kosovo and Metohija in the south) ranks with the top 20 countries of the Palearctic region in terms of amphibian species richness (Anthony et al. 2006). Unfortunately, amphibian populations in most of these countries are threatened. The foremost factors are loss, degradation, and fragmentation of habitat, followed by pollution and by competition from invasive non-native species (Sommerwerk et al. 2009), increased predatory pressure from domestic animals, and emerging infectious diseases such as chytridiomycosis (Baha el Din et al. 2006). The Republic of Serbia is situated partly in central Europe and partly in the central part of the Balkan Peninsula. Three distinct areas can be distinguished in the macro-relief of this region: the

46 Amphibian Biology

Fig. 43.1 Map of southern Europe with inset of a hydrographic map of The Republic of Serbia showing the locations of rivers, wetlands, and standing waters.

Pannonian Lowlands north of the Danube and Sava Rivers, Peripannonean lowlands as remnants of the southern bay of the ancient Pannonian Sea, and the mountains to the south. The mountainous area (parts of the Dinarides, Karpato-Balkan, and Rhodopi mountains) dominates, with a few large river valleys and a number of smaller watercourses. More than 86% of the area’s wetlands and standing waters are situated north of the Sava and the Danube Rivers (Figure 43.1). Wetlands cover approximately 314 km2, while standing waters (lakes, bogs, fish ponds, oxbow lakes, and disconnected river channels) cover about 142 km 2. According to the CORINE Land Cover Database (CLC 2006), inland waters (running and standing) cover approximately 1.09% of the total territory of the country, while wetlands cover about 0.28% of its total surface area. Wetlands/floodplains and their connection to adjacent rivers play an important role in the functioning of aquatic ecosystems. Despite the fact that nearly 80% of floodplains have been lost during the past 100 years, the area around large lowland rivers still incorporates a variety of wetlands, and some of them are protected by national legislation and international agreements e.g. Gornje Podunavlje, Koviljsko-Petrovaradinski rit; Obedska Bara; Zasavica; Stari Begej – Carska Bara. The climate is generally a moderate continental one and is influenced by relief; a boreal climate occurs at some higher elevations. According to the classification by Thornthwaite (1948), the majority of the area is characterized by a subhumid climate, while limited portions of the western



Conservation and Decline of European Amphibians: The Republic of Serbia47

and southwestern parts have a humid climate (Anonymous 2005). During the period 1961–1990, at elevations between 300 and 500 m, the average annual temperature was about 10°C; at 1,000 m elevation the corresponding value was about 6.0°C. The mean annual precipitation for the whole area is 896 mm with a predominantly continental pattern of greater amounts in the warmer period of the year. Most rain falls in May and June, while February and October has the least precipitation. The southwestern part has a Mediterranean precipitation pattern with maxima in November– January, and minima in August (Karadžić and Mijović 2007). From the end of World War II to the end of the twentieth century, the Serbian economic structure was characterized by a high degree of industrial development and irrational management of the environment, which led to the exhaustion of natural resources and to the accumulation of great amounts of industrial waste (Karadžić and Mijović 2007). As the country moved to a market economy, a new problem arose – responsibility for environmental protection within the context of a process of privatization.

A.  General pressures on amphibian populations

Aquatic ecosystems in the region are subject to considerable anthropogenic pressures, such as different types of hydrogeomorphological modifications (e.g. damming, regulation of rivers, and extraction of sand and gravel), and pollution by organic materials and nutrients, as well as by hazardous substances (Tripković et al. 2003, 2004; Lazarević et al. 2010; Simonovič et al. 2010). In addition, non-native species may be having considerable influence on aquatic communities (Paunović et al. 2004; Arbačiuskas et al. 2008; Pavlović et al. 2008; Panov et al. 2009; Zorić et al. 2011). All of these pressures can negatively influence amphibian assemblages. Furthermore, agricultural and urban land drainage, as well as flood-protection projects, have considerably reduced suitable habitats for amphibians in the past. Among the general threats to amphibians in the region, fragmentation, degradation, and loss of suitable habitats, together with pollution, are the most prominent. The northern part of the area (part of the Pannonian plain) is intersected by numerous watercourses (e.g. the Danube; Sava; Tisza; Tamiš; Begej), artificial canals of the Danube-Tisza-Danube (DTD) system, ponds, and stagnant tributaries (Figure 43.1). Along these bodies of water there are levees that protect the surrounding lowlands from floods, considerably reduce the surface area of floodplains and marshlands, and play a role in the self-purification of water. A similar situation exists in the valleys of the major rivers (e.g. the Morava and Kolubara) in central Serbia, where all major cities and significant industrial facilities are located in potentially floodable areas and require the construction of levees for flood control. Most of the communities do not have wastewater treatment plants and a number of existing ones are not operational. The most significant sources of municipal pollution include the cities of Belgrade, Novi Sad, and Niš, with an emission level higher than 150,000 PE (Population Equivalent, or unit per capita loading – a common expression used in waste-water monitoring and treatment for the organic biodegradable load having a five-day biochemical oxygen demand of 60 g of oxygen per day). These sources discharge untreated wastewater and exert significant pressures with regard both to organic matter and nutrient load. Cities having wastewater treatment plants (WWTPs) with capacities higher than 100,000 PE include Subotica and Kragujevac. The importance of small-sized and moderate-sized bodies of water in maintaining local amphibian assemblages in the area is neither understood nor appreciated by the public (CrnobrnjaIsailović et al. 2005). In historical times, ponds in this area were frequently created by humans for storage of water for cattle. Progressively, these ponds also became suitable sites for amphibian reproduction. With increased industrialization, intense migrations of people from the countryside into urban areas, and changes in livestock husbandry, these bodies of water lost their original

48 Amphibian Biology function and, consequently, are frequently used as dumping places for all kinds of domestic and industrial waste, or simply are drained, either intentionally by the land owners, or by natural means. Another negative impact from the point of view of persistence of amphibians is the transformation of their breeding sites into private fishponds. Because of the lack of communication between wilderness authorities and sectors responsible for water management and fisheries, private owners can easily still introduce stock fish into local amphibian breeding sites for their own use. It may be years before the damage is detected, when it is already too late for a remedy. Competition pressure from invasive, non-native species on amphibian populations has not been detected specifically in the area under consideration, although it is confirmed for the entire Danube Basin (Sommerwerk et al. 2009). Risk of predation from invasive fish has not been confirmed in the area so far, but occurs in the general Danube Basin (Reshetnikov 2003, 2004). Increased predation by domestic animals is a threat in areas surrounding large, and still growing, cities. By contrast, the rest of the area is undergoing depopulation. The fungal disease, chytridiomycosis, as a new threat, has not been officially detected in the area. Observations, however, point to the presence of some skin pathogens, probably of viral origin, in a few local amphibian populations (Crnobrnja-Isailović and Paunović, unpublished). Karadžić and Mijović (2007) reported additional factors as main causes of amphibian decline in The Republic of Serbia: roadkills and illegal collecting for commercial purposes. Previous construction of roads included no obligation to build passages for amphibians where roads cross migration routes. Environmental impact assessments are frequently carried out prior to construction of roads, but have usually provided only recommendations, not an obligation for mitigation. Illegal collecting for commercial purposes almost exclusively involves green frogs (Pelophylax esculentus, P. ridibundus, and P. lessonae). There are no historical records that describe the exploitation of frogs for food in Serbia, even in poor years, except targeted extermination that began with the development of fisheries, some 200 years ago in the territory of Vojvodina (Džukić et al. 2003a). The commercial export of green frogs from the area started in about 1928. Governmental control of the exploitation of these species began only in 1991, but basic, efficient state controls were designed and implemented only after the year 2000 (Džukić et al. 2003a,b). Table 43.1 Status of amphibian species in the Republic of Serbia according to various authorities. Taxon

National Conservation Status

IUCN Red List1

Bern Convention

Salamandra salamandra

LC

III

SP2

Salamandra atra

LC

II

SP2

Lissotriton vulgaris

LC

III

SP2

LC

III

SP2

CAUDATA Salamandridae

Icthyosaura alpestris Triturus ivanbureschi

NE

II

SP2

Triturus macedonicus 5

NE

II

SP2

Triturus cristatus

LC

II

SP2

Triturus dobrogicus

NT

II

SP2

Bombina bombina

LC

II

SP2

Bombina variegata

LC

II

SP2

4

ANURA Bombinatoridae

Bufonidae



Conservation and Decline of European Amphibians: The Republic of Serbia49

Taxon

IUCN Red List1

Bern Convention

National Conservation Status

Rana temporaria

LC

III

SP2

Bufo bufo

LC

III

SP2

Bufotes viridis

LC

II

SP2

LC

II

SP2

Pelobates fuscus

LC

II

SP2

Pelobates syriacus

LC

II

SP2

Pelophylax kl. esculentus

LC

III

P3

Pelophylax lessonae

LC

III

P3

Pelophylax ridibundus

LC

III

P3

Rana dalmatina

LC

II

SP2

Rana graeca

LC

III

SP2

Hylidae Hyla arborea Pelobatidae

Ranidae

Global and European status. Anonymous (2010b). Anonymous (2010c). 4 Wielstra et al. (2013). 5 A recent study (Wielstra and Arntzen 2011) demonstrated that it is Triturus macedonicus (Karaman 1922) that occurs in The Republic of Serbia, not Triturus carnifex, but some documents of international and national legislation still list T. carnifex. 1 2

3 

II.  Declining species and species of special concern for conservation The total number of amphibian species recorded from The Republic of Serbia is 21 (Table 43.1), which constitutes 78% of the total number of amphibian taxa reported for the Danube River Basin: 27, according to Somerwerk et al. (2009). Two thirds of the amphibian species recorded within the Danube basin prefer riverine landscapes, mostly at elevations below 300 m. Thus, the northern part of The Republic of Serbia (Figure 43.1) can be characterized as particularly important for amphibian conservation, although all species inhabiting Vojvodina can be found in the Balkan part of the country as well, mostly in the Peripannonian area. In addition, due to the fact that the lowland areas are the most densely populated, anthropogenic pressures are most intensive there in comparison to the southern part of the country. On the other hand, the Balkan part belongs to one of three main southern European centres of biodiversity and is also an important “transitional area” for historical migrations of amphibian species (Crnobrnja-Isailović 2007). Local populations there harbour more genetic diversity, due to patchy distributions, and should be considered when dealing with issues of conservation.

A.  Declining amphibian species

Except for green frogs, which have been the subject of detailed studies (Džukić et al. 2003a,b; Krizmanić 2006), there has been no regular monitoring of quantitative changes in the population status of amphibians in The Republic of Serbia. The first broad overview of distributions appeared in the Atlas of Amphibians and Reptiles in Europe (Gasc et al. 1997), in which many species were represented as scarce, merely because of the inadequacy of published data. The lack of a Red List of amphibians for the country has been a consequence of many factors, including inefficient ministerial coordination and the inability of experts to cope with their own, sometimes conflicting, visions of the task. Herein, however, is an attempt to identify the most endangered amphibians on the basis of the present authors’ own knowledge and field experience.

50 Amphibian Biology Among tailed amphibians, the crested newt species complex (Triturus cristatus superspecies) is generally the most susceptible to the previously mentioned threats because of its habitat specialization (Crnobrnja-Isailović et al. 2005). The green frogs of the country probably faced very serious declines during the last decade of the 20th century, due to the poor economic and political situation, the isolation of The Republic of Serbia (and The Republic of Montenegro, as constituents of the same federal state at that time), and lack of efficient governmental control (Džukić et al. 2003a). Statistics indicate that the former Yugoslavia was exporting green frogs for human consumption in quantities from 1 to even 420 tonnes in the years 1953 to 1991, with more than 6,000 tonnes exported in total over the assessed period. It was not known how many green frogs were exported from just The Republic of Serbia, until the beginning of the 1990s when the former Yugoslavia was separated into smaller countries. Due to an accident, it was revealed that two tonnes of green frogs were exported from The Republic of Serbia for commercial purposes in one single year, 1996 (Džukić et al. 1996). After a change of political system in the year 2000, both legislative and custom control became more efficient in regulating the exploitation of green frogs, although the negative influences of corruption and of economic transition are still prevalent. There are some indications that yellow-bellied toad (Bombina variegata) populations are in decline in the country, particularly in urban and semi-urban areas (present authors’ personal observations, based on comparison of numbers of adult toads seen in certain localities recently, as compared to 20 years ago). Another anuran species that may be endangered by anthropogenic changes is the treefrog (Hyla arborea). Treefrogs need specific bodies of water for mating. These are usually rather shallow ones that persist long enough throughout the season to enable tadpoles to complete development. Recently, it was recorded that at certain localities some bodies of water dry out soon after the start of the treefrogs’ breeding season. Sometimes spadefoot toads are restricted by lack of suitable habitat. Džukić et al. (2008) considered the distribution and chorology of Pelobates fuscus and Pelobates syriacus in the Balkan Peninsula and considered their narrow ecological niches and possible declines in the area as due, mostly, to anthropogenic influences and global warming.

B.  Species of special concern for conservation

All amphibian species in The Republic of Serbia are of conservation concern and are protected by national legislation. Although not all species are considered to be declining, those that are particularly rare or that are genetically very diverse can be considered to be of national conservation concern. One of these is undoubtedly the alpine salamander (Salamandra atra). It is a very peculiar and secretive species, perhaps rather from the human point of view, because in the Balkans it inhabits very high and humid mountainous areas where humans are infrequently present because of the harsh conditions (Andreone et al. 2008). This species occurs in isolated populations and may be suffering from the effects of construction of new ski resorts, even in the wildest parts of the Balkan Mountains, as well as from climatic change. A unique crested newt population group has been recognized in the central Balkans (Eastern Bosnia, Montenegro, Albania, Western Macedonia, and most of The Republic of Serbia) (Wielstra and Arntzen 2011), in an area previously assigned as occupied by the Italian crested newt, Triturus carnifex (Crnobrnja-Isailović et al. 1997; Kalezić et al. 1997; Arntzen 2003; Romano et al. 2008). That distinct evolutionary significant unit of the crested newt superspecies is named the Macedonian crested newt (Triturus macedonicus) after Karaman (1922). Furthermore, very restricted parts of The Republic of Serbia contain central western Triturus karelinii populations (Arntzen et al. 2008b; Wielstra and Arntzen 2011), recently named as T. ivanbureschi (Wielstra et al. 2013), and these



Conservation and Decline of European Amphibians: The Republic of Serbia51

deserve proper care as they contribute to the overall amphibian species richness in Serbia. Additionally, Danube crested newt (Triturus dobrogicus) populations in the country require conservation attention as their global and European IUCN status has been defined as Near Threatened (Arntzen et al. 2008a). Recently, an exhaustive phylogeographic study of the alpine newt, Icthyosaura alpestris, formerly Mesotriton alpestris (Sotiropoulos et al. 2007), revealed the existence of a population in southeastern Serbia with a unique mtDNA haplotype, again a species of value for conservation in regard to the overall richness of genetic diversity of the national amphibian fauna. The widely distributed European common frog (Rana temporaria) is not very common in Serbia. As an inhabitant of rather humid and cool habitats, it is restricted mostly to the highlands where it could suffer from the effects of global warming in this southernmost part of its range. Additionally, the species’ distribution is rather fragmented, with a big gap between western and eastern population groups along the Morava river valley. The Greek frog (Rana graeca) is a Balkan endemic specializing in fast-running waters. It deserves appropriate conservation measures because of its susceptibility to anthropogenic changes, such as inappropriate stream management, that could disrupt its reproductive potential (see Wheeler and Welsh 2008).

III.  Conservation measures and monitoring programmes Amphibians in the Republic of Serbia have been somewhat protected by national legislation since the second half of the nineteenth century, mainly as an intrinsic part of the wildlife in areas managed for fisheries. According to Džukić et al. (2003a,b), amphibians were not specifically protected in the former Yugoslavia until the end of the 1990s. The Convention on Biological Diversity and international legislation supports the conservation of amphibians as a generally threatened group (Alford and Richards 1999). Being a signatory to that convention, The Republic of Serbia has legal obligations not only relating to species diversity, but also to components of species’ genetic diversity, e.g. to the persistence of specific populations or population groups characterized by unique or rare haplotypes. The genetic diversity of amphibians in Serbia has been evaluated in national (Krizmanić 2006) and regional (Kalezić 1984; Kalezić et al. 1987; Crnobrnja et al. 1989) studies, as well as within large-scale phylogeographic research (Babik et al. 2005; Sotiropoulos et al. 2007 and papers reviewed by Crnobrnja-Isailović 2007), but not for all species. Most of the efforts concerning conservation of aquatic habitats in the country are focused on birds and fishes (ICPDR National Report 2005) and the protection of specific habitats important for the conservation of amphibians are not adequately addressed. Although the general protection of inland water habitats and wetlands contributes to the conservation of amphibians, the specific small-sized habitats of particular importance for amphibians should be identified and protected. Thus, further identification, mapping and classification of those habitats according to their importance should be carried out in order to propose and implement conservation measures. Monitoring of amphibian populations in The Republic of Serbia has not been conducted regularly. Green frogs have been monitored mainly through annual statistics of their catch in different districts but the first detailed overview that included protection and conservation of green frogs was carried out in 2003 (Džukić et al. 2003a). The survey of breeding sites of the crested newt (Crnobrnja-Isailović et al. 2005) has also become a good starting point for future actions. From 2002 onwards, the monitoring of amphibian breeding sites has been incorporated into particular projects funded by the national ministry in charge of science (2002 to 2005 within the scope of the project “Evolution in heterogeneous environments”) and the environment (Ivanović and Krizmanić 2004). Recently, the NGO “Protego” from Subotica has begun a set of activities focused on the monitoring

52 Amphibian Biology of small bodies of water and their wildlife, including amphibians, in Vojvodina (see http://www. protego-org.org/).

IV.  Species’ status The Republic of Serbia has no official Red List of amphibian species yet, although species-lists can be found in various publications (see Vukov et al. 2013). The newest regulations have categorized all the wildlife of the country into strictly protected (SP) (Anonymous 2010b), protected (P) (Anonymous 2010c), and those not included in either of those designations. All amphibian species, except green frogs, should now be considered as strictly protected (Table 43.1). Species in this category are considered especially important for the conservation of biodiversity, whether extirpated from just part, or all, of the territory, extirpated but now reintroduced, critically endangered or endangered, relict, locally endemic or stenoendemic, or globally threatened and globally protected wild species (Anonymous 2010a). Protected species include all wild species that are currently not threatened with becoming extinct or critically endangered, but which may be recognized as vulnerable, endemic, indicator species, key and umbrella species, relict species, or globally important and protected wild species. Protected species also include those that are not threatened but for which the phenotypic appearance is similar to strictly protected ones (Anonymous 2010a). Green frogs are categorized as protected species (Anonymous 2010c), which means that, under certain rules, their commercial exploitation may be permitted. Most amphibians in The Republic of Serbia are not globally threatened according to IUCN criteria, except the Danube crested newt (Triturus dobrogicus), which is assigned to Near Threatened at both global (Arntzen et al. 2008) and European levels (Temple and Cox 2009). Additionally, all species listed are protected by European legislation (Bern Convention).

V.  Summary Although rich in species diversity in European terms (8 species of tailed amphibians and 13 species of anurans described so far), the amphibian fauna of The Republic of Serbia faces very severe threats, including inappropriate alteration of native habitats (fragmentation, deterioration, and destruction), increased and uncontrolled pressure from transportation infrastructure projects, environmental pollution, exploitation, and global climatic change. There is also risk of the spread of emerging infectious diseases such as chytridiomycosis, although no cases have yet been detected in the country. The inappropriate treatment of small and moderate-sized bodies of water, as well as their frequent conversion into fishponds, is the major obstacle to the maintenance of rich amphibian diversity in The Republic of Serbia and could lead to extirpation of valuable components of genetic diversity or of evolutionarily significant units. The monitoring of amphibians is not widespread in the area and must be intensified, together with proper and frequent education about the importance of amphibian conservation, not just through ordinary educational programmes but also among citizens in general. Recent history and current problems with political transitions make conservation of biodiversity even more difficult than before, and present economic pressures mean that, without direct economic incentive, the people of the area will not be motivated to preserve amphibians’ breeding sites.

VI.  Acknowledgements We would like to thank Ariadne Angulo and Rebecca Miller from IUCN, as well as anonymous reviewers, for valuable comments. Our colleagues Vladica Simić and Predrag Simonović helped with data from the literature. This work was supported by Grant no. 173025 from the Ministry of Education and Science of The Republic of Serbia.



Conservation and Decline of European Amphibians: The Republic of Serbia53

VII.  References Alford, A.R., Richards and J.S., 1999. Global amphibian declines: A problem in applied ecology. Annual Review of Ecology and Systematics 30: 133–165. Andreone, F., Denoël, M., Miaud, C., Schmidt, B., Edgar, P., Vogrin, M., Crnobrnja Isailović, J., Ajtić, R., Corti, C. and Haxhiu, I., 2008. Salamandra atra. In IUCN 2011: IUCN Red List of Threatened Species. Version 2011.1. www. iucnredlist.org. Anonymous, 2005. “Environmental Report”. Ministry of environmental protection of Republic of Serbia – Environmental protection agency, Beograd [in Serbian]. Anonymous, 2010a. Regulation on proclamation and protection of strictly protected and protected plant, animal and fungi species. Official Gazette RS 5/10 [in Serbian]. Anonymous, 2010b. Regulation on proclamation and protection of strictly protected and protected plant, animal and fungi species. Appendix 1. Strictly protected species. Official Gazette RS 5/10 [in Serbian]. Anonymous, 2010c. Regulation on proclamation and protection of strictly protected and protected plant, animal and fungi species. Appendix 2. Protected species. Official Gazette RS 5/10 [in Serbian]. Anthony, B., Arntzen, J.W., Baha El Din, S., Böhme, W., Cogălniceanu, D., Crnobrnja-Isailović, J., Crochet, P.-A., Corti, C., Griffiths, R., Kaneko, Y., Kuzmin, S., Wai Neng Lau, M., Li, P., Lymberakis, P., Marquez, R., Papenfuss, T., Pleguezuelos, J.M., Rastegar, N., Schmidt, B., Slimani, T., Sparreboom, M., Ugurtas, I., Werner, Y. and Xie, F., 2006. Amphibians of the Palaearctic realm. In Threatened Amphibians of the World, ed. S.N. Stuart, M. Hoffmann, J.S. Chanson, N.A. Cox, R.J. Berridge, P. Ramani and B.E. Young. Lynx Edicions, with IUCN – The World Conservation Union, Conservation International and NatureServe, Barcelona. Pp. 10 /1–/213. Arntzen, J.W., 2003. Triturus cristatus superspecies – Kammolch Artenkreiss, including T. cristatus (Laurenti, 1768) – Northern crested

newt, T. carnifex (Laurenti, 1768) – Italian crested newt, T. dobrogicus (Kiritzescu, 1903) – Danube crested newt and T. karelinii (Strauch, 1870) – Southern crested newt. In Handbuch für Amphibien und Reptilien Europas, ed. K. Grossenbacher and B. Thiesmeier. Aula Verlag, Wiesbaden. Pp. 421–514. Arntzen J.W., Kuzmin, S., Jehle, R., Denoël, M., Anthony, B., Miaud, C., Babik, W., Vogrin, M., Tarkhnishvili, D., Ishchenko, V., Ananjeva, N., Orlov, N., Tuniyev, B., Cogălniceanu, D., Kovács, T. and Kiss, I., 2008. Triturus dobrogicus. In IUCN 2011: IUCN Red List of Threatened Species. Version 2011.1. www. iucnredlist.org. Arntzen, J.W., Papenfuss, T., Kuzmin, S., Tarkhnishvili, D., Ishchenko, V., Tuniyev, B., Spareboom, M., Rastegar-Pouyani, N., Ugurtas, I. H., Anderson, S., Babik, W., Miaud C. and Crnobrnja-Isailović, J., 2008. Triturus karelinii. In IUCN 2010. IUCN Red List of Threatened Species. Version 2010.4. www.iucnredlist.org. Babik, W., Branicki, W., Crnobrnja-Isailović, J., Cogălniceanu, D., Sas, I., Olgun, K., Poyarkov, N., Garcia-Paris, M. and Arntzen, J.W., 2005. Phylogeography of two European newt species – discordance between mtDNA and morphology-based specific and subspecific boundaries. Molecular Ecology 14: 2475–2491. Baha el Din, S., Bohme, W., Corti, C., Crnobrnja-Isailović, J., Lymberakis, P., Marquez, R., Miaud, C., Slimani, T., Ugurtas, I. and Werner, Y.L., 2006. The Status and Distribution of Amphibians in the Mediterranean Basin. In Threatened Amphibians of the World, ed. S.N. Stuart, M. Hoffmann, J.S. Chanson, N.A. Cox, R.J. Berridge, P. Ramani and B.E. Young. Lynx Edicions, with IUCN – The World Conservation Union, Conservation International and NatureServe, Barcelona. Pp. 113. CLC, 2006. CORINE Land Cover 2000 Database for Serbia & Montenegro. EvroGeomatika d.o.o, Belgrade, Geological Survey of Montenegro, Podgorica. Crnobrnja, J., Kalezić, M.L. and Džukić, G., 1989. Genetic divergence in the crested newt (Triturus cristatus complex) from Yugoslavia. Biosistematika 15: 81–92.

54 Amphibian Biology Crnobrnja-Isailović, J., 2007. Cross-section of a refugium: genetic diversity of amphibian and reptile populations in the Balkans. In Phylogeography of Southern European Biodiversity, ed. S. Weiss and N. Ferrand. Springer Verlag, Berlin. Pp. 327–337. Crnobrnja-Isailović, J., Aleksić, I. and Arntzen, J.W., 2005. The status of great crested newt breeding sites in Serbia. Froglog 67: 2–3. Crnobrnja-Isailović, J., Džukić, G., Krstić, N. and Kalezić, M.L., 1997. Evolutionary and paleogeographical effects on the distribution of the Triturus cristatus superspecies in the central Balkans. Amphibia-Reptilia 18: 321–332. Džukić, G., Kalezić, M., Aleksić, I. and Crnobrnja-Isailović, J., 1996. Green frogs are exploited in the former Yugoslavia. Froglog 19: 3­–4. Džukić, G., Kalezić, M. and Ljubisavljević, K., 2003a. “Protection and Conservation of Green Frogs in Serbia and Montenegro”. Federal Ministry of Labour, Health and Social Care, Department of Environment, Beograd [in Serbian]. Džukić, G., Kalezić, M. and Ljubisavljević, K., 2003b. Green frogs are greatly endangered in Serbia and Montenegro. Froglog 58: 2–3. Džukić, G., Beškov, V., Sidorovska, V., Cogalniceanu, D. and Kalezić, M.L., 2008. Contemporary chorology of the spadefoot toads (Pelobates spp.) in the Balkan Peninsula. Zeitschrift für Feldherpetologie 15: 61–78. Gasc, J-P., Cabela, A., Crnobrnja-Isailović, J., Dolmen, D., Grossenbacher, K., Haffner, P., Lescure, J., Martens, H., Martinez-Rica, J.P., Maurin, H., Oliveira, M.L., Sofianidou, T.S., Veith, M. and Zuiderwijk, A. (eds), 1997. “Atlas of Amphibians and Reptiles in Europe”. Societas Europaea Herpetologica & Museum National d’ Histoire Naturelle (IEGB/SPN), Paris. ICPDR National Report, 2005. National Report of Serbia and Montenegro – ICPDR Roof Report, Part B. www.icpdr.org. Ivanović, A. and Krizmanić, I., 2004. “Monitoring of Green Frogs (Rana synklepton esculenta) Metapopulation System in Southeastern Part of Pannonian Plain in Serbia: Final

Report”. Ministry of Protection of Natural Resources and Environment, and biological faculty of the University of Belgrade [in Serbian]. Kalezić, M.L., 1984. Evolutionary divergences in the smooth newt, Triturus vulgaris (Urodela: Salamandridae): Electrophoretic evidence. Amphibia-Reptilia 5: 22–230. Kalezić, M.L., Džukić, G., Crnobrnja, J. and Tvrtković, N., 1987. On the Triturus vulgaris schreiberi problem: electrophoretic data. Alytes 6: 18–22. Kalezić, M.L., Džukić, G., Mesaroš, G. and Crnobrnja-Isailović, J., 1997. The crested newt (Triturus cristatus superspecies) in ex-Yugoslavia: Morphological structuring and distribution patterns. University Thought, Natural Science, Priština IV: 39–46. Karadžić, B. and Mijović, A. (eds), 2007. “Environment in Serbia: an Indicator-based Review”. First Edition. Ministry of Science and Environmental Protection and Environmental Protection Agency, Republic of Serbia. Karaman, G., 1922. Beiträge zur Herpetologie von Mazedonien. Glasnik der Kroatien Naturwissenschaften Gesellschaft Zagreb 34: 1–22. Krizmanić, I., 2006. “Population Systems of Green Frogs (Rana synklepton esculenta), their Distribution and Protection in Republic of Serbia”. PhD Thesis, Faculty of Biology, University of Belgrade [in Serbian, with English summary]. Reshetnikov, A.N., 2003. The introduced fish, rotan (Perccottus glenii), depresses populations of aquatic animals (macroinvertebrates, amphibians, and a fish). Hydrobiologia 510: 83–90. Reshetnikov, A.N., 2004. The fish Perccottus glenii: history of introduction to western regions of Eurasia. Hydrobiologia 522: 349–350. Romano A., Arntzen, J.W., Denoël, M., Jehle, R. Andreone, F., Anthony, B., Schmidt, B., Babik, W., Schabetsberger, R., Vogrin, M., Puky, M., Lymberakis, P., Crnobrnja Isailović, J., Ajtić R. and Corti, C., 2008. Triturus carnifex. In IUCN 2011: IUCN Red List of Threatened Species. Version 2011.1. www.iucnredlist.org.



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Sommerwerk, N., Hein, T., Schneider-Jakoby, M., Baumgartner, C., Ostojić, A., Paunović, M., Bloesch, J., Siber, R. and Tockner, K., 2009. The Danube River Basin. In Rivers of Europe, ed. K. Tockner, U. Uehlinger and C.T. Robinson. Academic Press, San Diego. Chapter 3 (pp. 59–112). Sotiropoulos, K., Eleftherakos, K., Džukić, G., Kalezić, M.L., Legakis, A. and Polymeni, R. M., 2007. Phylogeny and biogeography of the alpine newt Mesotriton alpestris (Salamandridae, Caudata), inferred from mtDNA sequences. Molecular Phylogenetics and Evolution 45: 211–226. Temple, H.J. and Cox, N.A., 2009. “European Red List of Amphibians”. Office for Official Publications of the European Communities, Luxembourg. Thornthwaite, C.W., 1948. An approach toward a rational classification of climate. Geographical Review, New York 38: 55–94. Vukov, T., Kalezić, M.L., Tomović, L.J., Krizmanić, I., Jović, D., Labus, N. and Džukić, G., 2013. Amphibians in Serbia – distribution and diversity patterns. Bulletin of the Natural History Museum 6: 90–112. Wheeler, C.A. and Welsh, H.H. Jr., 2008. Mating strategy and breeding patterns of the foothill yellow-legged frog (Rana boylii). Herpetological Conservation and Biology 3: 128–142. Wielstra, B. and Arntzen, J.W., 2011. Unravelling the rapid radiation of crested newts (Triturus cristatus superspecies) using complete mitogenomic sequences. Bio Med Central Evolutionary Biology 11: 162. Wielstra, B., Litvinchuk, S.N., Naumov, B., Tzankov, N. and Arntzen, J.W., 2013. A revised taxonomy of crested newts in the Triturus karelinii group (Amphibia: Caudata: Salamandridae), with the description of a new species. Zootaxa 3682: 441–452.

44 Amphibian declines and conservation in Montenegro Ruža Ćirović I. Introduction II. General pressures on amphibian populations worldwide

D. Over-harvesting

III. Species of special conservation concern in Montenegro

B.  Introduced and invasive species

IV. Conservation measures and monitoring programmes

C.  Climatic change

V. References

A.  Habitat destruction

Abbreviations and acronymns used in the text or references: CANU Crnogorska Akademija Nauka i Umjetnosti (Montenegrin Academy of Sciences) EPA Environmental Protection Agency EU European Union GIZ Deutsche Gesellschaft für Internationale Zussameranbeit IUCN International Union for the Conservation of Nature

I.  Introduction The geographic position, climate and spatial characteristics of Montenegro, as well as its natural resources and their distribution, make it an exceptional European country in many ways. In just under 14,000 square kilometres there are exceptional natural areas, such as the Boka Kotorska Bay and sandy beaches of the southern part of the Adriatic coast; the biggest lake in the Balkans, Skadar Lake; the pristine Tara Canyon and mountains in the northern region; numerous glacial lakes; and peaks of up to 2,500 meters above sea level. Nature, including a rich diversity of biota and landscapes, and its cultural value, represents one of Montenegro’s greatest treasures. In terms of the number of different species per unit of surface area, Montenegro is one of the top countries in Europe and, at the same time, is home to numerous endemic species. National legislation currently protects 7.7% of the territory (five National Parks as well as areas with a lower level of protection). Forest and water resources represent some of the most significant natural resources that Montenegro has and they are very important for sustainable development. Forests cover approximately 45% of the territory. Despite the fact that the hydrological situation varies significantly – from areas without water, with no springs or surface flows of water, to areas where there is plenty of water – Montenegro as a whole has rich aquatic resources. A special natural resource is the ca. 300 km-long coastline, narrow coastal zone, and seacoast, which comprise a specific ecosystem and offer significant potential for development. Although Montenegro does not have great land resources, there is substantial unused potential for development of agriculture.



Amphibian Declines and Conservation in Montenegro57

The most important region in Montenegro is the holokarst region whose main characteristics are the scarcity of water and paucity of aquatic ecosystems. The aquatic ecosystems present in this region are ponds, stone basins, and collapsed sinkholes. These are the only habitats with paedomorphic populations of Triturus spp. The important areas for amphibians include a southeastnorthwest area from the Albanian border to the border with Bosnia and Herzegovina, the Skadar lake coast, and the Lukavica and Vojnik mountains in the north. Recognizable representative localities, or modules, are biologically diverse and serve as indicators of environmental conditions.

II.  General pressures on amphibian populations worldwide Amphibians are in decline globally and this is primarily due to emergent diseases and negative anthropogenic influences such as loss and alteration of habitat, introduction of invasive species, climatic change, UV radiation, environmental pollution, and overharvesting (Heatwole and Wilkinson 2009, 2012; Heatwole 2013). Those most important are now treated in turn.

A.  Habitat destruction

Anthropogenic alternation of habitats is widely considered as the single most important threat to amphibians globally (Lemckert et al. 2012). The main effect of habitat loss is reduction in population size, through reduced breeding and recruitment, reduced foraging opportunities, reduced opportunities for refuge leading to exposure to predators or harsh conditions, and unsuccessful hibernation. Human pressure on global ecosystems is intensifying as global populations rise, settlements expand, and extraction of natural resources accelerates. Furthermore, degradation and fragmentation of habitat reduces the quality of what remains. It is now estimated that humans have altered between one third and one half of the Earth’s land surface (Vitousek et al. 1997). Factors such as forestry and agriculture have major effects on endangered species’ populations. Roads, fields, and urban areas represent significant barriers to movement (Puky 2012), and may also result in unnaturally high population densities for the available food supplies. Of longer-term importance is the probability of inbreeding and loss of genetic variation in small isolated populations. Combined, these factors make populations extremely vulnerable to other threats such as disease and environmental catastrophes. The damming of rivers and the reduction in the quality of bodies of water can be extremely detrimental to the survival of many water-dependent species.

B.  Introduced and invasive species

Humans have spread a great many non-native animals and plants around the world and these have had an impact on amphibian species (Lemckert et al. 2012). The establishment and spread of non-native or “exotic” species are a major threat to worldwide biodiversity, and many species have been greatly impacted by introduced species through direct predation, competition, and the introduction of diseases. Communities of species develop over a long period of time, and survive in delicately balanced ecosystems. The movement of species between separate ecosystems can cause great upset, especially if an exotic species rapidly reproduces, establishes itself competitively within the new system, and becomes “invasive”.

C.  Climatic change

Amphibians are especially vulnerable to desiccation – the vast majority of species must maintain moist skin surfaces because a significant amount of their breathing occurs through their skin. Their eggs do not have hardened protective shells and accordingly are susceptible to drying out. Even the amphibians found in deserts are dependent upon seasonal rains and temporary sources of water for breeding.

58 Amphibian Biology The timing of breeding by amphibians is governed by environmental factors such as temperature and availability of water. It is thought that if global warming occurs, frogs will start breeding earlier in the season. This is already happening, with frogs coming out of hibernation and breeding earlier (Beebee 1995) and being more susceptible to sudden changes in the weather. There are also predictions that, in the second half of this century, carbon dioxide levels will double, which may increase the Earth’s mean surface temperature by 4°C (e.g. Rahmstorf 2008). The sea level could then rise by over 2 meters, inundating most of the world’s coastal wetlands – there will be an alteration of rainfall patterns and more frequent and intense droughts. Table 44.1 Status of Montenegrin amphibians according to European criteria. RL = IUCN European Red List (LC = Least Concern; EN = Endangered); HD = EU Habitats Directive on the Conservation of Natural Habitats and of Wild Fauna and Flora (Annex II – vulnerable/sensitive species that could become endangered in the near future if the factors of threat continue to act; Annex IV – species that require strict protection); Bern = Bern Convention on Conservation of European Wild Flora, Fauna, and Natural Habitats (II – Strictly protected animal species; III – Protected animal species). Scientific Name

RL

HD

Bern

Bombina variegata

LC

II, IV

II

Bufo bufo

LC

/

III

Bufotes viridis

LC

IV

II

Hyla arborea

LC

IV

II

Pelophylax kl. esculentus

LC

/

III

Pelophylax lessonae

LC

IV

III

Pelophylax ridibundus

LC

/

III

Pelophylax shqipericus

EN

/

III

Rana dalmatina

LC

IV

II

Rana graeca

LC

/

III

Rana temporaria

LC

/

/

Ichthyosaura alpestris

LC

/

III

Lissotriton vulgaris

LC

/

III

Triturus carnifex

LC

II, IV

II

Triturus macedonicus

/

/

/

Salamandra atra

LC

IV

II

Salamandra salamandra

LC

/

III

D.  Over-harvesting

Harvesting of amphibians has made inroads into populations in various parts of the world (Kusrini 2012; Kusrini et al. 2012). Many amphibian species are highly attractive and have become popular among collectors in the pet trade. Generally, the more rare the species the higher the demand for it. Furthermore, some species are used in traditional medicines or harvested for their various properties. Another possible cause of global decline is the collection of frogs as a food source. Elimination of frogs as predators of pest insects may lead to more extensive use of insecticides and cause considerable damage to delicate ecosystems, including the further destruction of amphibian populations.

III.  Species of special conservation concern in Montenegro None of the 17 species of Montenegrin amphibians can be regarded as common, and some of them are considered to be declining and can be considered to be of national or regional conservation



Amphibian Declines and Conservation in Montenegro59

concern. The current status of Montenegrin amphibians according to European criteria are given in Table 44.1. The alpine salamander (Salamandra atra) inhabits very high mountains and it occurs in isolated populations. In Montenegro the first records were on Bogićevica Mountain (National Park “Prokletije”). This species is endangered because of the construction of new ski resorts as well as from harvesting by collectors. The recent introduction of fish has been the cause of an alarming disappearance of newt populations in Montenegro (Džukić et al. 2005). This is especially true in lakes at high elevations (Bukumirsko, Zminičko, Visitor, and Hridsko lakes). Introduced salmonid fish are predators of newts at all life stages, from egg to adult individuals. Additionally, these fish are in competition with newts for the limited resources of food in oligotrophic lakes. The larvae of both species feed mainly on small shrimps and chironomid larvae. Restocking the lake often leads to irreversible change in the structure of the zooplankton, which significantly reduces the survival of newts. Montenegro appears to be a hotspot for paedomorphosis (Denoël et al. 2009b) because of the high density of paedomorphic populations of newts (Ichthyosaura alpestris, Lissotriton vulgaris, and Triturus macedonicus), all three species of which present this alternative life-history trait. Spatial autocorrelation of populations with paedomorphs shows that some areas are particularly favorable for expression of this polyphenism (Ćirović et al. 2008). However, these populations and the hotspot as a whole have critical conservation issues. From a conservation point of view, it may be too late to restore intraspecific biodiversity in some populations, particularly after a long time of selection against paedomorphosis. However, recent works have shown that amphibian populations can rebound after fish have been removed. There is thus the potential for recovery in ponds where fish were introduced recently or where paedomorphic populations have remained in nearby aquatic sites, but this remains to be determined. Netting or drying could help remove current fish stocks but this is not an easy task, particularly for small fish in large Alpine lakes (Denoël et al. 2009a,b).

IV.  Conservation measures and monitoring programmes Various investigations of the population dynamics of amphibians provide a basis for improving and implementating laws, agreements, and management plans for conserving biodiversity and sustainable use. Prerequisite to protection of amphibians are studies that monitor the status of their populations (Dodd et al. 2012). All amphibians in Montenegro are protected by national legislation (“Sl. list RCG” br.36/82,”Sl. list RCG” br.76/06). Investigation of the population dynamics of amphibians in Montenegro is aimed at improving the implementation of laws, agreements, and management plans to conserve biodiversity and sustainable use. Monitoring of amphibian populations has been conducted every year by national Ministries and the Environmental Protection Agency (EPA) through the project “Monitoring of Biodiversity”. Green frogs have been monitored by the project “Monitoring of Amphibians and Reptiles of Lake Skadar, Montenegro” financed by the Deutsche Gesellschaft für Internationale Zussameranbeit (GIZ) (see Ćirović 2011). The survey of alpine newts in high montane lakes has also been an initial impetus for future actions. From 2013 onwards, monitoring of newts’ breeding sites in the holokarst of Montenegro has been incorporated into particular projects funded by the EPA and the United Nations Development Programme (project “Revalidation of Ecological Values and Management Arrangements of Existing Protected Areas”) (Ćirović 2005). The NGOs from Podgorica have also initiated activities focused on the monitoring of some amphibian species. Further conservation actions should focus, among other things, on improvement of connectivity among groups of breeding sites by restoring dispersal corridors. Loss of aquatic habitat often is

60 Amphibian Biology seen as having the most damaging impact on populations, but the loss of terrestrial habitat can also have serious consequences. If urgent measures are not taken soon, an important kind of intraspecific biodiversity will disappear. Some sites with large populations should be closely protected and surveyed to assure persistance of those populations. Legislation should designate some of the important amphibian populations as conservation units. Management measures should also be taken to restore disturbed habitats.



Amphibian Declines and Conservation in Montenegro61

V.  References Beebee, T.J.C., 1995. Amphibian breeding and climate. Nature 374 (21): 9–220. Ćirović, R., 2005. The newts (Triturus spp., Salamandridae) in karst of Montenegro: protection and conservation programs. Water resources and environmental problems in karst, Cvijic. Belgrade – Kotor, 2005: 843–849. Ćirović, R., 2011. Herpetofauna of the Lake Skadar region: Diversity and importance of protection. Medjunarodni naučni skup “Skadarsko jezero – stanje i perspektive”. Crnogorska Akademija Nauka i Akademija Nauka Albanije, 19–21 Jun 2010. Godine, Podgorica-Skadar. CANU, Naučni skupovi, knjiga 105: 119–127. Ćirović, R., Radović, D. and Vukov, T.D., 2008. Breeding site traits of European newts (Triturus macedonicus, Lissotriton vulgaris and Mesotriton alpestris, Salamandridae) in the Montenegrin karst region. Archives of Biological Sciences (Belgrade) 60: 459–468. Denoël, M., Ficetola, G.F., Ćirović, R., Džukić, R. and Kalezić, M.L., 2009a. Ecological modelling and paedomorphosis: a study case in Montenegrin newts. 15th European Congress of Herpetology, 28 September–2 October, Kuşadasi, Turkey, Book of Absracts, p. 129. Denoël, M., Ficetola, G.F., Ćirović, R., Džukić, R., Kalezić, M.L. and Vukov, T.D., 2009b. A multi-scale approach to facultative paedomorphosis of European newts (Salamandridae) in the Montenegrin karst: Distribution pattern, environmental variables and conservation. Biological Conservation 142: 509–517. Dodd, C.K. Jr., Loman, J, Cogãlniceanu, D. and Puky, M., 2012. Monitoring amphibian populations. In Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management ed. H. Heatwole and J.W. Wilkinson, Vol. 10 in Amphibian Biology. Surrey Beatty & Sons. Baulkham Hills. Chapter 11 (pp. 3577–3635). Džukić, G., Ćirović, R., Denoël, M. and Kalezić, M.L., 2005. Fish introduction is a major cause of paedomorphosis extinction in European newts (Triturus spp.). Froglog 69: 3–4. Heatwole, H., 2013. Worldwide decline and extinction of amphibians. In The Balance of

Nature and Human Impact, ed. K. Rohde. Cambridge University Press. Cambridge. Chapter 18 (pp. 259–278). Heatwole, H. and Wilkinson, J.W., 2009. Amphibian Decline: Diseases, Parasites, Maladies and Pollution. Vol. 8 in Amphibian Biology, ed. H. Heatwole. Surrey Beatty & Sons. Baulkham Hills. Heatwole, H. and Wilkinson, J.W., 2012. Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management. Vol. 10 in Amphibian Biology, ed. H. Heatwole. Surrey Beatty & Sons. Baulkham Hills. Kusrini, M.D., 2012. International trade in amphibians. In Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management ed by H. Heatwole and J.W. Wilkinson, Vol. 10 in Amphibian Biology. Surrey Beatty & Sons. Baulkham Hills. Chapter 5 (pp. 3494–3504). Kusrini, M.D., H. Heatwole and Davenport, D., 2012. Harvesting of amphibians for food. In Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management ed by H. Heatwole and J.W. Wilkinson, Vol. 10 in Amphibian Biology. Surrey Beatty & Sons. Baulkham Hills. Chapter 4 (pp. 3469–3493). Lemckert, F., Hecnar, S.J. and Pilliod, D.S., 2012. Destruction, loss and modification of habitat. In Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management ed. H. Heatwole and J.W. Wilkinson, Vol. 10 in Amphibian Biology. Surrey Beatty & Sons. Baulkham Hills. Chapter 1 (pp. 3291– 3342). Puky, M., 2012. Road kills. In Conservation and Decline of Amphibians: Ecological Aspects, Effect of Humans, and Management ed. H. Heatwole and J.W. Wilkinson, Vol. 10 in Amphibian Biology. Surrey Beatty & Sons. Baulkham Hills. Chapter 6 (pp. 3505–3521). Rahmstorf, S., 2008. Anthropogenic climate change: Revisiting the facts. In Global Warming: Looking Beyond Kyoto, ed. E. Zedillo. Brookings Institution Press, Washington. Vitousek, P.M., Mooney, H.J., Lubchenco, J. and Melillo, J.M., 1997. Human domination of Earth’s ecosystems. Science 277: 494–499.

45 Status of amphibians in Bosnia and Herzegovina Avdul Adrović I. Introduction II.  Freshwater habitats A.  The Black Sea Basin B.  The Adriatic Basin

III. The amphibians of Bosnia and Herzegovina A. Pressures on the amphibian fauna

IV. References

C. Lakes D. Wetlands E.  Pressures on wetland ecosystems

I.  Introduction The country of Bosnia and Herzegovina occupies the central part of the Balkan Peninsula and shares borders with Croatia, Serbia, and Montenegro. The longest border is with Croatia in the north, northwest, and south and extends for 932 km. To the east and northeast the border with Serbia is 312 km. To the east and southeast there is a border of 215 km with Montenegro. In the south, Bosnia and Herzegovina has a coastal length of about 25 km bordering the Adriatic Sea. The total area of the country is 51,129 km2. The boundaries of Bosnia and Herzegovina are mostly natural and are formed by the rivers Drina, Sava, and Una. The country is mostly mountainous. The landscape of Bosnia and Herzegovina is varied and the unique flora and fauna exhibit great diversity and a high degree of endemism. There are a great variety of human cultures that reflect the diversity of all components of the environment (Redžić et al. 2008). The physiographic diversity of Bosnia and Herzegovina results from the country’s complex geology, topography, and climate. The country is moderately wet and its river courses belong to the basins of the Black Sea and Adriatic Sea.

II.  Freshwater habitats Thanks to its favorable natural conditions of climate, topography, vegetation, and geological features, Bosnia and Herzegovina has abundant fresh water in the form of rivers, lakes, and wetlands. A peculiarity is a network of underground rivers and streams in karst regions. In hydrographic terms, Bosnia and Herzegovina belongs to the Black Sea (Danube) Basin and the Adriatic Basin. About 70% of the total area of Bosnia and Herzegovina belongs to the Black Sea Basin, and about 30% to the Adriatic Basin.

A.  The Black Sea Basin

That part of the Black Sea Basin within the territory of Bosnia and Herzegovina is 38,719 km2, and contains the largest rivers. The main catchment areas are: (1) the immediate basin of the river Sava (total area 5,506 km2); (2) the Una, Korana, and Glina basin in Bosnia and Herzegovina (total area



Status of Amphibians in Bosnia and Herzegovina63

9,130 km2); (3) the Vrbas River Basin (total area 6,386 km2); the Bosna River Basin (total area 10,457 km2); and (4) that part of the Drina River Basin that lies in Bosnia and Herzegovina (total area 7,240 km2). The mountainous area of the Dinarides River is a watershed that feeds a large number of rivers and streams flowing to the north and to the south.

B.  The Adriatic Basin

The Adriatic Basin comprises southern and southwestern Bosnia and Herzegovina. The total catchment area is about 12,410 km2 which is about 24.3% of the territory of the country. The main catchments are: (1) the confluence of the river Neretva with the Trebisnjica River Basin (combined area of 10,110 km2) and (2) the confluence of the Cetina River with the Suica, Sturba, Zabljak, Bistrica, Brina, Plovuca, Jaruga, and Ricina (total area 2,300 km2). The river Neretva is the only river tributary making its way into the Adriatic Sea entirely via surface flow, as opposed to subterranean rivers.

C.  Lakes

Both natural and artificial lakes occur in Bosnia and Herzegovina. Natural lakes are represented at all elevations; they are mainly related to morphosculptural forms of relief, but also to tectonic predisposition. Natural lakes are abundant in the mountainous regions where they were formed around pits and abysses downstream and by different erosional processes upstream. A second type of natural lake occurs in karstic fields. Artificial “lakes” are built on large rivers such as the Drina, Vrbas, Neretva, and Trebisnjica, as well as in karst fields. On the Drina River there are three artificial reservoirs built to produce electricity. On the Neretva River there are five reservoirs and on the Trebisnjica River there are two. In Livno field are several reservoirs, e.g. Lake Bresinsko and Buško Blato (Lake Buško), that is one of the largest artificial reservoirs. Modrac reservoir, located on the Spreca River in the alluvial plain of Spreca, was built for the needs of industry.

D.  Wetlands

The wetland ecosystems of Bosnia and Herzegovina are located in natural depressions and on flat terrain. They were formed from sediments originating from different rivers and lakes and are located along major rivers such as the Una, Sava, Vrbas, Drina, and Neretva. In these, a variety of plant assemblages has developed that serve as habitats for amphibians. Particular types of wetlands are located around the montane springs and streams and, in some places, these form peatlands. At lower elevations, low basophilic peat is formed. In small, wet depressions in premontane zones, quagmires form a special type of lowland peat. Wetlands also are present in Bosnia-Herzegovina’s karst areas. At the present time, wetlands constitute the most endangered ecosystem in the world, including those in Bosnia and Herzegovina. These ecosystems are the habitat of organisms, including amphibians, that represent an extremely valuable genetic resource; their conservation deserves high priority.

E.  Pressures on wetland ecosystems

Strong anthropogenic pressures are exerted on wetland ecosystems that risk compromising their structure and stability. These include dangers such as global climatic change and its concomitant temperature extremes. Such situations lead to increased eutrophication, the level of which is affected by accumulation of large amounts of different forms of organic matter, transported via

64 Amphibian Biology surface waters. Acidic rain changes the pH of aquatic habitats and leads to the disappearance of stenovalent species. Alteration of habitats exerts one of the most drastic negative effects. There are numerous examples of violations of habitats that lead to irreversible changes with far-reaching consequences. One such negative example is the cutting of littoral vegetation in the area of the Bardaca Wetland. Another example is the exploitation of peat in the area of Bosansko Grahovo. Interest has been expressed in the development of hunting and fishing in the area of Hutovo Blato and Buško Blato, as well as at other important locations. There are numerous examples of the intensive extraction of sand and gravel from streams or from littoral areas. All the major waterways in Bosnia and Herzegovina, described above, are exposed to such exploitation to varying extents. Concessionaires gain concessions without prior studies having been conducted on the environmental impact; thus, the negative consequences of those developments are extremely difficult to track. The problem of draining wetlands and the diversion of streams that feed the wetlands should receive special attention. Table 45.1 Species and status of amphibians in Bosnia and Herzegovina. Data from Arntzen et al. (2007), Temple and Cox (2009), and Lelo and Vesnić (2011). LC = Least Concern; NE = Not Evaluated; NT = Near Threatened; VU = Vulnerable. Order/Family

Species

IUCN Red List Status

Bombina bombina

LC

Bombina variegata

LC

Pelobatidae

Pelobates fuscus

LC

Bufonidae

Bufo bufo

LC

Bufotes viridis

LC

Hylidae

Hyla arborea

LC

Ranidae

Rana dalmatina

LC

Rana graeca

LC

Rana temporaria

LC

Pelophylax kl. esculentus

LC

Pelophylax lessonae*

LC

Pelophylax ridibundus

LC

Proteidae

Proteus anguinus

VU

Salamandridae

Salamandra atra

LC

Salamandra salamandra

LC

Lissotriton vulgaris

LC

Ichthyosaura alpestris

LC

Triturus carnifex

LC

Triturus dobrogicus

NT

Triturus macedonicus **

NE

ANURA Discoglossidae

CAUDATA

* May be present in the north of the country. ** A relatively recently-recognized species present in the east.



Status of Amphibians in Bosnia and Herzegovina65

III.  The amphibians of Bosnia and Herzegovina The country of Bosnia and Herzegovina is characterized by a rich amphibian fauna that has been insufficiently studied. The first written records of its amphibians date from the second half of the nineteenth century (Werner 1898). The National Museum of Bosnia and Herzegovina was established in Sarajevo in 1888 and marks the beginning of the collection of amphibian specimens and the systematic processing of data. Later, a number of works were published by Bolkay (1919, 1922, 1924, 1929). More complete data were provided by Radovanović (1951) who, in his book Amphibians and Reptiles of Our Country, displayed data on 15 species of amphibians recorded from Bosnia and Herzegovina. Mihailinović (1963) provided information on the amphibian fauna of Mount Kozara; new localities of Proteus anguinus were registered by Čučković (1967), and he, Pocrnjić and Solaja (1987), and Miksić (1969) published data on the chorology of Proteus anguinus, Salamandra atra, and Ichthyosaura alpestris. At the time the treatises by Ðjurović et al. (1979) and Škrijelj and Korjenić (2000) were published, the known amphibian fauna of the country was only 18 species, with 5 subspecies. More recently, Redžić et al. (2008) reported an increase in the known diversity to 21 species in 7 families. Other contemporary investigations (Arntzen et al. 2007; Lelo and Vesnić 2011; see also Jablonski et al. 2012) suggest that the number of amphibian species currently recognized from Bosnia and Herzegovina may be 20 (see Table 45.1). Of the amphibians of Bosnia and Herzegovina, only Proteus anguinus is considered Vulnerable, whereas Triturus dobrogicus is Near Threatened (Temple and Cox 2009). In addition, however, the Prenj salamander, Salamandra atra prenjensis and Reiser’s alpine newt (Ichthyosaura alpestris reiseri) may be distinct taxa and are endemic to Bosnia and Herzegovina.

A.  Pressures on the amphibian fauna

Among the threats to the amphibians of Bosnia and Herzegovina are anthropogenic pressures, the most significant of which are those that change the quality of the habitat of sensitive species. Negative anthropogenic pressures are manifest by an increase in the pollution of water by organic and inorganic materials. Intense deforestation leads to alteration of hydrothermal regimes and habitats. The effects of global climatic change and acidic rain also negatively affect the number of amphibian populations and the quality of their habitat. The immediate problem is intensive eutrophication of standing water, primarily ponds and swamps, followed by uncontrolled hunting of ranid frogs, as well as the trade in species that are rare or have a restricted distribution in the country. A special problem is the introduction of fish that prey upon, or compete with, species of newts in the montane lakes. The sustainable use of amphibian resources through artificial propagation has not yet begun in Bosnia and Herzegovina (Redžić et al. 2008).

66 Amphibian Biology

IV.  References Arntzen, J.W., Espregueira Themudo, G. and Wielstra, B., 2007. The phylogeny of crested newts (Triturus cristatus superspecies): nuclear and mitochondrial genetic characters suggest a hard polytomy, in line with the paleogeography of the centre of origin. Contributions to Zoology 76: 261–287. Bolkay, S., 1919. Herpetological finds in the western part of the Balkan Peninsula. Journal of the National Museum of Bosnia and Herzegovina 31: 1–38 [in Serbian]. Bolkay, S., 1922. Table for determining the amphibians of Yugoslavia. Vol. 34 of the Journal of Croatian Society of Natural Sciences, Zagreb [in Croatian]. Bolkay, S., 1924. List of amphibians and reptiles, which are located in Bosnia – Herzegovina’s National Museum in Sarajevo, with morphological, biological and zoogeographical notes. Monument of the Serbian Royal Academy 41: 1–29 [in Serbian]. Bolkay, S., 1929. Ein Beitrag zur Verbreitung des geographischen Proteus anguinus carrarae Fitzinger. Journal of the National Museum of Bosnia-Herzegovina 41: 27–28. Čučković, S., 1967. New localities for the olm (Proteus anguinus Laur.) in the area of Trebinje in Herzegovina. Journal of the National Museum of Bosnia-Herzegovina PN 6: 223­–225 [in Bosnian]. Ðjurović, E., Vuković, T. and Pocrnjić, Z., 1979. Amphibians of Bosnia and Herzegovina: A key to the determination. National Museum of Bosnia Herzegovina, Sarajevo. Jablonski, D., Zandzik, D. and Gvoždík, V., 2012. New records and zoogeographic classification of amphibians and reptiles from Bosnia and Herzegovina. North-Western Journal of Zoology 8: 324–337. Lelo, S. and Vesnić, A., 2011. Revision of the checklist of amphibians (Vertebrata, Amphibia) of Bosnia and Herzegovina. Natura Montenegrina 10: 245–257. Mihailinović, M., 1963. The amphibians and reptiles of Mount Kozara. Journal of the

National Museum of Bosnia Herzegovina (PN) NS 2: 7 3–80 [in Bosnian]. Miksić, S., 1969. A new subspecies of the alpine salamander (Salamandra atra prenjensis nov.). Journal of the National Museum of Bosnia Herzegovina (PN) NS 8 (8): 3–86. Radovanovic, M., 1951. Amphibians and Reptiles of Our Country. Scientific Book, Belgrade. Redžić, S., Barudanović, S. and Radević, M., 2008. “Bosnia and Herzegovina – Land of Diversity”. First national Report of Bosnia and Herzegovina for the Convention on Biodiversity, Federal Ministry of Environment and Tourism, Sarajevo. Pp. 164. Pocrnjić, Z. and Solaja, M., 1987. Fauna tailed amphibians in Bosnia and Herzegovina. In Proceedings of the Gathering Minerals, Rocks, Extinct and Living World of Bosnia and Herzegovina. National Museum of Bosnia Herzegovina, Sarajevo. Pp. 559–562. Škrijelj, R. and Korjenić, E., 2000. “Biodiversity of Amphibians and Reptiles of Bosnia and Herzegovina”. Soros Foundation – Open Society Fund Bosnia and Herzegovina, Sarajevo. Temple, H.J. and Cox, N.A., 2009. “European Red List of Amphibians.” Luxembourg: Office for Official Publications of the European Communities. Werner, F., 1898. Contributions to knowledge of the reptile and amphibian fauna of the Balkan Peninsula. Journal of the National Museum of Bosnia Herzegovina 10 (13): 1–156 [in Bosnian].

46 Conservation and protection status of amphibians in Macedonia Bogoljub Sterijovski I. Introduction A.  Geographic features

III. Species of special concern for conservation

B. Amphibian species in the FYR of Macedonia

IV. Conservation measures and monitoring programmes

C. Assessment

V. Conclusions

II.  Threats to amphibians

VI. References

Abbreviations or acronyms used in the text or references: asl EU FYR IUCN NGO

above sea level European Union Former Yugoslav Republic International Union for the Conservation of Nature Non-governmental Organization

I.  Introduction A.  Geographic features

The Former Yugoslav Republic (FYR) of Macedonia is situated in the central part of the Balkan Peninsula. It covers a surface area of 25,713 km2. The relief is represented by montane massifs, intersected by plains (some of them filled with tectonic lakes) and river valleys. Macedonian mountains belong to three groups according to their elevation: high mountains (above 2,000 m), medium-high mountains (1,500–2,000 m), and low mountains (below 1,500 m). There are five mountains over 2,500 m asl (Korab, Shar Planina, Pelister, Jakupica, and Nidze). The highest peak is Golem Korab (2,753 m) on Korab Mountain; followed by Titov Vrv (or Turcin – 2,748 m) on the Shar Planina; Pelister (2,601 m) on Pelister Mountain; Solunska Glava (2,540 m) on Mokra (Jakupica) Mountain; and Kajmakcalan (2,520 m) on Nidze Mountain. There are seven more high mountains: Galicica, Stogovo, Jablanica, Osogovo, Kozuf, Bistra, and Belasica. The 16 medium-high mountains are Plakenska Planina, Vlaina, Suva Gora, Kozjak, Malesevo, Karaorman, Buseva Planina, Plackovica, Babuna, Ograzden, Selecka Planina, Skopska Crna Gora, Dren, German, Golak, and Bukovik. The low-mountain group consists of ten mountains: Zeden, Serta, Klepa, Gradeska Planina, Plaus, Smrdes, Mangovica, Gradistanska Planina, Ruen, and Kara Balija. The largest plain in Macedonia is Pelagonia (3,682 km2). Other important plains (valleys) are Ovce Pole, Skopje, Radovis-Strumica, Polog, Ohrid-Struga, Kumanovo, Veles, Delcevo-Berovo, Kocani, Gevgelija-Valandovo, Debar, Kicevo, Slaviste, and Prespa (Kolčakovski 2004). The greatest numbers of caves are found in Treska Gorge and Porece Basin, Mt. Jakupica, Mt. Galicica, Radika Valley, and Crn Drim Valley; the largest number of sinkholes is registered for Mt. Jakupica.

68 Amphibian Biology There are four tectonic zones: Vardar Zone (along the River Vardar), Pelagonian Horstanticlinorium (east of the Vardar zone), West-Macedonian Zone (westernmost parts and bordering Merdita Zone in Albania), and Serbian-Macedonian Massif (east of Vardar Zone and continuing to the east in Bulgaria with transition into the Rhodopes). In general, there are three different types of climate in Macedonia (Lazarevski 1993): modified Mediterranean, moderate continental climate, and montane climate: •

•

•

The modified Mediterranean climate is characterized by warm and dry summers and mild and rainy winters. It is typical of the area south of the Vardar River Valley (Dojran and Gevgelija-Valandovo to Demir Kapija) and the Strumica-Radovis Valley along the Struma and Strumica rivers. Some influence is detectable in the Skopje Plain, Bregalnica River Valley to Kočani. A weak Mediterranean impact also can be noted in the Drim Watershed. The moderate-continental climate is characterized by relatively cold and humid winters, and dry and warm summers (Malesevo, Slaviste, Kumanovo Valley, Ovce Pole, Skopje Valley, Polog, Kicevo, Prespa, and Pelagonia). The montane climate is characteristic of mountains higher than 1,000 m. Winters are long, cold, and snowy. Summers are short and cold.

The average annual air temperature is 11.1°C. The highest annual precipitation of 1,400 mm is recorded in the River Radika Valley (western Macedonia). The lowest annual precipitation of less than 500 mm is characteristic of central Macedonia (the Gradsko, Ovce Pole, and Veles areas). Regional differences in precipitation are mainly a result of the mountainous relief. Drought is a specific feature of the Macedonian climate. There is at least a 30-day period of drought every year. The duration of the drought period is up to 80 days (Lazarevski 1993). Macedonian rivers belong to the watersheds of the Aegean Sea (87%), Adriatic Sea (13%), and Black Sea (only 44 km2). The longest river of the Aegean Sea watershed is the Vardar with its tributaries (Pcinja, Bregalnica, and Crna Reka). The watershed of the Adriatic Sea includes the rivers Radika and Crn Drim (Ohrid Lake and Prespa Lakes also belong here). Only the small river Binacka Morava at Mt. Skopska Crna Gora represents the Black Sea’s watershed. There are eight climate-vegetation-soil zones in Macedonia (Filipovski et al. 1996). These zones represent the diversity of biomes in Macedonia: from the pseudomaquis in the lowest region to tundra-like habitats on the highest parts of the mountains. However, continental oak and beech forests constitute the dominant vegetation. There are 44 wetlands in the FYR of Macedonia, including 19 artificial lakes or reservoirs, eight marshes, 6 glacial lakes, 3 fish ponds, 3 natural lakes, 1 temporary water, 2 rivers, 1 wetland, and 1 spring. These cover 2.23% of the total area of the territory (Micevski 2002). Table 46.1 Amphibian species recorded from the FYR of Macedonia. List of Species CAUDATA

ANURA

1

Salamandra salamandra (Linnaeus, 1758)

6

Bombina variegata (Mertens and Muller, 1928)

2

Triturus karelinii (Strauch, 1870)

7

Pelobates syriacus (Boettger, 1889)

3

Triturus macedonicus (Karaman, 1922)

8

Bufo bufo (Mertens and Muller, 1928)

4

Ichthyosaura alpestris (Laurenti, 1768)

9

Bufotes viridis (Laurenti, 1768)

5

Lissotriton vulgaris (Linnaeus, 1758)

10

Hyla arborea (Linnaeus, 1758)

11

Rana dalmatina (Bonaparte, 1840)

12

Rana graeca (Boulenger, 1891)

13

Pelophylax ridibundus (Pallas, 1771)

14

Rana temporaria (Linnaeus, 1758)



Conservation and Protection Status of Amphibians in Macedonia69

B.  Amphibian species in the FYR of Macedonia

Due to the variety of the relief and climate, the FYR of Macedonia supports 14 species of amphibians (Table 46.1). In general, data on them are lacking. Since the beginning of the twentieth century, however, there have been several studies for some localities and regions (Doflein 1921; Karaman 1922, 1928, 1931, 1937, 1939; Buresch and Zonkow 1934; Dimovski 1959, 1960, 1963, 1964, 1966, 1971, 1981; Radovanović 1941, 1951, 1957, 1964; Džukić 1972; Džukić et al. 1998, 2001). Intensive research on amphibians started in the year 1999 to obtain basic faunistic data for the distribution of this class in the country, and to create a National Atlas of Amphibians. The data that have been collected so far cover more than 80% of the country and are in the process of publication. Table 46.2 Assessment of amphibian species in the FYR of Macedonia. Bern – Bern Convention on Conservation of European Wild Flora, Fauna and Natural Habitats (II – Strictly protected animal species, III – Protected animal species); HD – European Directive on the Conservation of Natural Habitats and of Wild Fauna and Flora (Annex II – vulnerable/sensitive species which could become endangered in the near future if threat factors continue to act; Annex IV – species that require strict protection); IUCN: IUCN assessment status (LC – Least Concern); MK: II – second tier list of protected wild species of the Republic of Macedonia. Amphibian Species in FYR of Macedonia

Conventions, Protected Lists, and Endemism Bern

HD

IUCN MK

Endemism

CAUDATA 1

Salamandra salamandra

III

/

LC

/

2

Triturus karelinii

II

IV

LC

II

3

Triturus macedonicus

III

II

/

II

4

Ichthyosaura alpestris

III

/

LC

/

5

Lissotriton vulgaris

III

/

LC

/

6

Bombina variegata

II

IV

LC

II

7

Pelobates syriacus

II

IV

LC

II

8

Bufo bufo

III

/

LC

/

9

Bufotes viridis

II

IV

LC

II

10

Hyla arborea

II

IV

LC

II

11

Rana dalmatina

II

IV

LC

II

12

Rana graeca

III

IV

LC

II

13

Pelophylax ridibundus

III

/

LC

/

14

Rana temporaria

III

/

LC

/

Balkan endemic

ANURA

C.  Assessment

Balkan endemic

The assessment of Macedonian amphibian species is carried out according to international conventions for the protection of threatened species on a European Level that includes the Convention on the Conservation of European Wildlife and Natural Habitats (known as the Bern Convention) and the EU Habitats Directive (Directive 92/43/EEC), the IUCN Red List (ver. 2013.1) and the List of protected wild species of the FYR of Macedonia (Macedonian Nature Protection Law/Protection of wild species in RM 139/11) (Table 46.2). All amphibians are listed under the Bern Convention (Appendices II and III) and regarded as Least Concern (except for T. macedonicus which is not evaluated) by the IUCN Red List (Table 46.2). Eight species are on the Habitats Directive and the List of Protected Wild Species of the FYR of Macedonia. Also, two species are regarded as Balkan endemics (Table 46.2), due to small ranges restricted to wetlands, and a fragmented distribution in the Balkan Peninsula.

70 Amphibian Biology

II.  Threats to amphibians Generally speaking, the threats to amphibians in the FYR of Macedonia are direct and indirect threats to wetland habitats and, in almost all cases, are caused by anthropogenic influence. Modification and fragmentation of amphibian habitats has been a historical threat and remains so today. These processes have become more intensive, especially in the past three decades (see Ministry of Environment and Physical Planning 2003a). Conversion of land and loss of natural habitats due to that conversion are most evident within aquatic habitats, particularly swamps and marshes. Since the end of the Second World War, almost all of the bigger swamps and marshes have been drained, mainly to gain new agricultural areas and to combat malaria. This is the principal reason why the marshland communities have become endangered, fragmented, or threatened, such as at Monospitovo Marsh, in the southern part of the country (Melovski et al. 2008). Modification and fragmentation of habitat also are caused by construction of artificial lakes or reservoirs. This is still the case, especially in the construction of the mini hydroelectric power dams in the western parts of the country (in the mountains of Bistra, Korab, and Shar Planina). Many small rivers and springs are diverted in order to fill up the new artificial lakes without concern for the necessary biological minimum of the water level. This is directly impacting amphibian populations and other biodiversity. Fragmentation of aquatic habitats (e.g. the upper and middle courses of rivers and streams) is common in the country. During the construction of major roads, the main migratory routes of the amphibians were not taken into consideration (Ministry of Environment and Physical Planning 2003a), resulting in cases of massive road kills (in Kacanicka Gorge; Demir Kapija Gorge; Istibanska Gorge; Matka Gorge; Debar – Struga region). In addition, the conversion of natural habitats into agricultural ones also represents a serious threat to biodiversity, especially in the southern parts of the country (e.g. Monospitovo marsh, where local people drained the marsh, burned the reeds, and subsequently took over the area for agricultural land). Pollution of water and soil pollution pose serious threats to biodiversity, especially from pesticides and fertilizers (in the past), and the improper disposal of waste water. This is the case in the Prespa region, where Prespa Lake is situated, the Dojran Lake region and the Strumica region near Monospitovo Marsh, where orchards and agriculture are important local industries (Ministry Environment and Physical Planning 2003a). Climatic change is also an indirect danger to amphibian populations in the FYR of Macedonia. The areas most sensitive to climatic changes are the refugia such as Taor Gorge; Treska River Gorge; Crna River, including the gorges of the Raec and Blasnica Rivers; Jama; Mavrovo-Radika region; Mt. Pelister; Ohrid-Prespa region; and Nidze-Kozuf mountains (Ministry Environment and Physical Planning 2003b). Due to climatic changes (e.g. increase in temperature), the aforementioned zones will be impacted directly by distributional changes in precipitation, additionally influencing the entire hydrology. Other factors that influence amphibians in the FYR of Macedonia are: • • • • • • •

lack of, or inappropriate, legal regulation of the conservation of biodiversity; lack of enforcement of the legal regulations that do exist; low public and institutional awareness of the importance of biodiversity of amphibians; almost no awareness among non-governmental organizations (NGOs); lack of field data and a National Red List for endangered species; no trained personnel in inspection services and customs; no monitoring of any amphibian species in any part of the country which could provide the necessary data for conservation and protection of amphibians.



Conservation and Protection Status of Amphibians in Macedonia71

III.  Species of special concern for conservation According to the list of endangered wild animals in the FYR of Macedonia (Macedonian Nature Protection Law/Protection of wild species in RM 139/11), eight amphibian species are listed as endangered within Macedonia. The lack of national distributional data and monitoring programmes means that current designations do not represent the status of species within the FYR of Macedonia. According to the available distributional data (Sterijovski unpublished), populations of T. karelinii, T. macedonicus, I. alpestris, L. vulgaris, P. syriacus, and R. temporaria are rare and therefore can be considered as endangered at a national level. Furthermore, for all amphibian species, the population status is unknown so there is no current way of verifying whether or not populations are declining.

IV.  Conservation measures and monitoring programmes At the present time, no conservation measures for amphibians in the FYR of Macedonia have been introduced or implemented (with the exception of the List of Protected Species). In 1999, comprehensive field research started on amphibians and reptiles in order to gain detailed distributional data of these two classes. Except for the few monitoring programmes that are present in the national parks (which do not include amphibians) there is currently no systematic monitoring.

V.  Conclusions In the FYR of Macedonia, 7.11% of the territory is protected (Ministry Environment and Physical Planning 2004). Almost all amphibian species are widely distributed throughout the country. At the time of writing, 14 species of amphibians have been recorded in the FYR of Macedonia and 8 of them are on the List of Protected Species. The visible causes of threat to this group of species are in almost all cases influenced by humans. Survival for most species depends on the protection of habitats, which are extremely important in the life cycle of amphibians. The lack of implementation of protective legislation has, in practice, disabled monitoring of the effects of modification and fragmentation of habitat, conversion of natural habitats, pollution of water and soil, and the effect of climatic change in the FYR of Macedonia. Furthermore, the lack of educated experts still creates problems in establishing protection for species in this group. Due to the lack of population studies and monitoring programmes in Macedonia the conservation status of amphibians in the FYR of Macedonia currently cannot be assessed accurately. This will need to be achieved before national priorities in amphibian conservation can be established.

72 Amphibian Biology

VI.  References Buresch, I. and Zonkow, J., 1934. Untersuchungen über die Verbreitung der Reptilien und Amphibien in Bulgarien und auf der Balkanhalbinsel. 2. Schlangen (Serpentes). Mitteilungen aus den Königlich naturwissenschaftlichen Instituten in Sofia 7: 106–188 [in Bulgarian, with German summary]. Dimovski, A., 1959. I prilog kon herpetofaunata na Makedonija (Beitrag zur Herpetofauna Mazedoniens). Fragmenta Balcanica 3: 1–4 [in Macedonian, with German summary]. Dimovski, A., 1960. Biogeografska i ekološka karakteristika na Skopskata kotlina. Unpublished doctoral dissertation, University of Skopje. Dimovski, А., 1963. Herpetofauna na skopska kotlina. I ­– zoogeografski i ekološki pregled. Godišen zbornik Prirodno-matematičkog fakulteta, Univerziteta u Skoplju, Skoplje, knjiga 14, Biologija 2: 189–221. Dimovski, A., 1964. II Prilog kon herpetofaunata na Makedonija (II Beitrag zur herpetofauna Mazedoniens). Fragmenta Balcanica 5: 19–22. Dimovski, А., 1966. Herpetofauna na skopska kotlina. II – faunistički del. Godišen zbornik Prirodno-matematičkog fakulteta, Univerziteta u Skoplju, Skoplje, knjiga 16, Biologija 4: 179–188. Dimovski, A., 1971. Zoocenološki istražuvanja na stepskite predeli vo Makedonija. Godišen zbornik Prirodno-matematičkog fakulteta, Univerziteta u Skoplju, Skoplje, knjiga 23, Biologija 4: 25–54. Dimovski, A., 1981. Vodozemci i vlečugi na Nacionalnot park Galičica. (Amphibies et reptiles du park national de Galitchitsa). Macedonian Academy of Scienses and Arts, Skopje II: 63–74 [in Macedonian, with French summary]. Doflein, F., 1921. Mazedonien, Erlebnisse und beobachtungen eines Naturforschers im gefolge des Deutschen heeres. Verlang von Gustav Fischer, Jena. Džukić, G., 1972. Herpetološka zbirka Prirodnjačkog muzeja u Beogradu (Herpetological collection of the Belgrade Museum of Natural

History). Glasnik Prirodnjačkog muzeja Beograd, Ser. B 27: 165–180. Džukić, G.,. Kalezić, M. L., Petkovski, S. and Sidorovska V., 1998. Batrachofauna and Herpetofauna of Balkan Peninsula: General remarks. Proceeding of the Second International Congress of the Biodiversity, Ecology and Conservation of the Balkan Fauna. Bioecco 2. Sept 16–20, 1998, Ohrid, Macedonia. Džukić, G., Kalezić, M.L., Petkovski, S. and Sidorovska, V., 2001. General remarks on Batracho- and Herpetofauna of the Balkan Peninsula. In 75 years of the Macedonian Museum of Natural History ed. T. Boškova. Prirodonaučen Muzej na Makedonija, Skopje. Pp. 195–204. Filipovski, Gj., Rizovski, R. and Ristevski, P., 1996. The characteristics of the climate vegetation soil zones (regions) in the Republic of Macedonia. MASA, Skopje. Karaman, S., 1922. Beiträge zur Herpetologie von Mazedonien. Glasnik Hrvatskog Prirodoslovnog društva, Zagreb 34: 278–299. Karaman, S., 1928. III Prilog herpetologiji Jugoslavije. Glasnik Skopskog Naučnog Društva, Skopje 4: 129–143 [in Serbian]. Karaman, S., 1931. Zoološke prilike Skopske kotline. Glasnik Skopskog Naučnog Društva, Skopje 10: 214–241 [in Serbian]. Karaman, S., 1937. Fauna južne Srbije. Spomenica, Skoplje [in Serbian]. Karaman, S., 1939. Über die Verbreitung der Reptilien in Jugoslavien. Annales Musei Serbiae Meridionalis, Skoplje 1: 1–20. Kolčakovski, D., 2004. Geotectonic characteristics of the relief in the Republic of Macedonia. Bulletin of the Department of Physical Geography, 1: 7–23. Lazarevski, A., 1993. Klimata vo Makedonija. Kultura, Skopje [in Macedonian]. Melovski, Lj., Ivanov, Gj., Angelova, N., Velevski, M. and Hristovski, S., 2008. Monospitovsko swamp – the last swamp in Macedonia. Municipality of Bosilovo. Bosilovo [in Macedonian].



Conservation and Protection Status of Amphibians in Macedonia73

Micevski, B., 2002. Inventory of Macedonian Wetlands. Bird Study and Protection Society of Macedonia, Skopje. Ministry of Environment and Physical Planning, 2003a. Country Study of Biodiversity of the Republic of Macedonia, First National Report. Ministry of Environment and Physical Planning, Skopje. Ministry of Environment and Physical Planning, 2003b. Macedonia’s First National Communication under the United Nations Framework Convention on Climate Change. Ministry of Environment and Physical Planning, Skopje. Ministry Environment and Physical Planning, 2004. Republic of Macedonia’s Spatial Plan. Ministry Environment and Physical Planning, Skopje. Radovanović, M., 1941. Zur Kenntnis der Herpetofauna des Balkans. Zoologischer Anzeiger 136: 145–159. Radovanović, M., 1951. Vodozemci i gmizavci naše zemlje. Naučna knjiga, Beograd. Radovanović, M., 1957. Einige Beobachtungen an Amphibien und Reptilien in Jugoslawien. Zoooglischer Anzeiger 159: 130–137. Radovanović, M., 1964. Die Verbreitung der Amphibien und Reptilien in Jugoslawien. Senckenbergiana Biologica, Frankfurt am Main 45: 553–561.

47 Amphibians of Albania Idriz Haxhiu I. Introduction II. Amphibian population declines in Albania III. Conservation measures and monitoring programmes

IV. Summary of the species present in Albania and their status V. Conclusions VI. Acknowledgements VII. References

I.  Introduction Some early studies on Albanian amphibians either were based solely on preserved material in museums (Kopstein and Wettstein 1921; Gayda 1940) or were summaries quoted from other authors (Calabresi 1932; Radovanovic 1951; Dimovski 1959, 1964; Bruno 1988, 1989). Those that were based directly on field observations mainly were conducted by foreigners during short excursions (De Fejervary 1923; Cei 1943; Frommhold 1959) or on extralimital populations in nearby regions of Montenegro or Greece (Hotz and Uzzell 1982; Schneider et al. 1984, 1992; Uzzell et al. 1987; Schneider and Joermann 1988; Sofianidou and Schneider 1989). More recently, field studies have been carried out by Albanian researchers (e.g. Dani 1970; Haxhiu 1982, 1983, 1986a,b, 1987, 1990, 1991, 1994; Haxhiu and Alimehilli 1987; Schnieder and Haxhiu 1992, 1994; Haxhiu and Oruci 2004; Haxhiu and Vrenozi 2009). This chapter summarizes the result of many years of observations in many different regions of Albania on a number of native species along with their biogeography, habitats, and conservation status; in particular, it establishes unequivocally the presence of a number of species thought by foreign authors not to inhabit Albania. This chapter summarizes field observations made between 1976 and 2010 by the author and about 30 collaborators during the course of numerous expeditions to many areas of Albania from the lowlands to elevations up to 2,000 m. In addition to recording traditional data on location, habitat, elevation, terrain, and surrounding vegetation, bio-acoustic techniques were utilized for clarification of taxonomic and biogeographic issues (Schnieder and Haxhiu 1992, 1994). These bio-acoustic studies have occasioned a precise evaluation of the Albanian anurans, especially the species of green frogs present in Albania. Three species (Pelophylax balcanicus; P. lessonae; P. epeiroticus) and their hybrids are present in Albania. The geographic distribution of P. epeiroticus in a restricted area of southwestern Albania (Figure 47.1) and in Greece (Schneider et al. 1992; Schnieder and Haxhiu 1992, 1994; Haxhiu and Oruci 2004) is related to the influence of the macroclimate and microclimate of the habitats characteristic of these areas. The presence of P. epeiroticus only in the Lowland of Saranda is a classic example of geographic isolation. The Lowland of Saranda is surrounded by high, rocky mountains that have geographically isolated this species. From Saranda to Vlora, along the Jon Coast, there are high, craggy, rocky, and stony mountains with scarce, temporary bodies of water where P. epeiroticus is absent but P. balcanicus can be found. The latter species has a higher ecological valence and distribution in comparison with P. epeiroticus. Pelophylax lessonae has a more northwestern distribution in the western lowlands near the Adriatic Sea, from Shkodra Lake to Orikum. The distribution of this species is related to the influence of macroclimate and microclimate and to the characteristic habitats of this area.



Amphibians of Albania75 Fig. 47.1 The administrative districts of Albania: 1. Shkodër; 2. Tropoje; 3. Pukë; 4. Kukës; 5. Lezhe; 6. Miridite; 7. Dibër; 8. Krujë; 9. Mat; 10 Durrës;. 11 Tirana; 12. Kavajë; 13. Lushnje; 14. Elbasan; 15. Librazhd; 16. Berat; 17. Gramsh; 18. Pogradec; 19. Fier; 20. Konçë; 21. Vlorë; 22. Tepelenë; 23. Skrapar; 24. Përmet; 25. Ersekë; 26. Gjirokastër; 27. Sarandë.

II.  Amphibian population declines in Albania A variety of anthropogenic influences have affected the Albanian landscape over different geographic and temporal scales. The most important of these is the destruction of the Albanian habitats in which amphibians live, e.g. a reduction in the area of lowland aquatic habitats. Construction of large drainage channels since the 1950s has resulted in the desiccation of thousands of hectares of marshland and its transformation into agricultural land. The reduction of aquatic habitat has a great impact on the distribution and frequency of various species of amphibians. Thus, in the lowlands of Saranda, Triturus cristatus, Lissotriton vulgaris, Bufo bufo, Bufotes viridis, Hyla arborea, Pelophylax epeiroticus, P. balcanicus, and Rana dalmatina formerly populated aquatic habitats, but no longer have them available. These species, however, have been able to colonize some of the new drainage channels and remain in a few remnant marshes and riverine areas. Largescale drainage also has taken place in the West Lowland of the Adriatic Sea where P. lessonae, P. balcanicus, T. cristatus, L. vulgaris, B. bufo, B. viridis, H. arborea, and R. dalmatina occur. Drainage of marshlands also has occurred in the areas of Korca, Pogradeci, Gjirokastra, Lezha, and Shkodra. Another action that has damaged the habitats of amphibians in Albania has been the diverting of the courses of most Albanian rivers, especially the mouths of the Drini, Mati, Ishmi, Bistrica, Kalasa, Pavllo, and Semani rivers. A serious problem for most amphibians has been (and still is) the alteration of too many such riverbeds in Albania, especially in the western lowland. The vegetation structure along these diverted rivers has been damaged and the riverbeds have been converted into coastal marshes that are now almost valueless as a habitat for amphibians. The use of agricultural chemicals and pesticides for crop protection in Albania has polluted aquatic habitats and as a result has damaged populations of various species of amphibians. Collection and exportation of green frogs (Pelophylax balcanicus, P. epeiroticus, and P. lessonae and their hybrids) over about 40 years has been a direct threat to these species. Especially during the past 20 years, many urban aquatic habitats have been polluted by sewage, detergents, and other chemicals, and rivers, lakes, and reservoirs have been used for irrigation. Also during this time, the beds of the rivers throughout Albania have been used intensively for the extraction of construction materials. This has reduced amphibian diversity, especially in and around cities.

76 Amphibian Biology

III.  Conservation measures and monitoring programmes Recently, the Albanian government enacted laws for the protection of animals and of biodiversity in Albania. Unfortunately these laws are not enforced and pollution and destruction of habitats continue without consideration for the environment. Also, the massive migration of people from mountains and other rural areas has resulted in unregulated construction of buildings in areas where, 20 years ago, there were only natural habitats. During the past 20 years, various projects for monitoring the Albanian fauna, including amphibians, have been realized but they have been few in number and have suffered interruptions. The Albanian government enacted laws that prohibit the collection of Pelophylax epeiroticus for export (from the Saranda district). For other species, such as P. balcanicus and P. lessonae and their hybrids, there are laws prohibiting collection before spawning. For all these rules, abuses have been continuous and the laws are never enforced. There are, however, an increasing number of reservoirs for irrigation and hydroelectric projects in hilly and mountainous areas that provide aquatic habitats for amphibians. These now number about 700 throughout Albania and they collectively cover thousands of hectares and have helped conserve some species of Albanian amphibians.

IV.  Summary of the species present in Albania and their status Two Red Books on the conservation status of the Albanian fauna have been published (Misja 2006). The data from those on amphibians are summarized in Table 47.1. Table 47.1 The status and distribution of amphibian species among the various administrative districts of Albania. Districts are numbered as shown in Figure 47.1. Code to generic names: B. = Bufo; Bo. = Bombina; Bt. = Bufotes; H. = Hyla; I. = Ichthyosaura; L.= Lissotriton; P. = Pelophylax; R. = Rana; S. = Salamandra; T. = Triturus. Code to conservation status: DD = Data Deficient; LR = Lowest Risk; VU = Vulnerable; cd = Conservation Dependent; lc = Least Concern; nt = Near Threatened. Species

Status Districts of Albania

S. atra

LRnt

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

27

+ + +

S. salamandra

DD

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

I. alpestris

DD

+ + + +

T. macedonicus

LRlc

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

+

+

L. vulgaris

LRlc

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

Bo. variegata

LRcd

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

B. bufo

LRnt

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

Bt. viridis

LRnt

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

H. arborea

LRlc

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

P. balcanicus*

VU

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

P. epeiroticus

VU

P. lessonae**

VU

+

+ + + + + + + + + + + + + + + + + + + + + + + + + + +

R. dalmatina

LRlc

R. graeca

LRnt

R. temporaria

LRcd

+ +

+

+ + + + + + + + + +

+ +

+ + +

+

+

+ + + +

+ +

+ +

+ + + + + + + +

+

+

+ +

+

+

+ +

* Considered by some to be a junior synonym of Pelophylax kurtmuelleri; other authors (e.g. Jablonski 2011) consider these taxa to be synonymous with P. ridibundus. ** Albanian populations now often designated as P. shqipericus.



Amphibians of Albania77

V.  Conclusions Despite the small size of Albania, the amphibian fauna numbers 15 species. Nine occur throughout the country, while others inhabit particular regions. The causes for restriction to limited areas reflect preferences for special habitats within the available diversity of landscapes, climates, and natural water resources. The species of the family Ranidae are especially restricted to specific distributions and they have the added threat of being of scientific and commercial interest. Since 1950, there have been increasing anthropogenic interventions that nowadays are exerting even more influence, especially on Albania’s declining aquatic habitats. The increased human population in urban areas has exacerbated urban and chemical pollution, especially where developments are in hilly terrain. In some areas, Albanian amphibians are able to utilize the newer habitats provided by irrigation and by hydroelectric reservoirs. These sources of water, however, have not compensated for the widespread loss of traditional marshlands.

VI.  Acknowledgements I wish to express my heartfelt gratitude to Prof. Dr. Hans Schneider, Bonn University, Germany, for his help and collaboration over about 20 years, especially in bioacoustic studies of the anurans of Albania. I am very grateful also to Dr. John W. Wilkinson and Prof. Harold Heatwole for correction of the manuscript.

78 Amphibian Biology

VII.  References Bruno, S., 1988. L’erpetofauna delle isole di Grex, Krk e Ada (Jugoslavia – Albania). Bulletin d’Ecologie 19: 265–281. Bruno, S., 1989. Introduction to a study of the herpetofauna of Albania. British Herpetological Society Bulletin 29: 16–41. Calabresi, E., 1932. Anfibi e Rettili d’Albania. Atti della Accademia Scientifica Veneto-TrentinoIstriana 23: 83–86. Cei, G., 1943. Sopra una piccola raccolta erpetologica fatta dal Sig. L. Cardini nei dintorni di Butrinto (Albania). Atti della Societa Toscana di Scienze Naturali residente in Pisa 523: 5–39. Dani, P., 1970. Fauna e amfibeve ne Myzeqe. Buletini i Shkencave te Natyres, Tirane 1: 39–43. Dimovski, A., 1959. Beitrag zur Herpetofauna Mazedoniens. Fragmenta Balcanica 3: 1–4. Dimovski, A., 1964. Beitrag zur Herpetofauna Mazedoniens. Fragm. Balc. 5: 19–22. De Fejervary, G.J., 1923. “Explorationes zoologicae ab E. Csiki in Albania peractae. Pars l. Batrachians and Reptiles.” Magyar Tudományos Akadémia Balkán-Kutatásainak t u d o m á n y o s e r e d m é n ye i : M a g ya r Tudományos Akadémia, Budapest. Frommhold, E., 1959. Als Tiergartner und Herpetologe in Albanien. Aquarium Terrarium 6: 115–118, 144–147, 170–182, 214–217. Gayda, H.S., 1940. Su alcuni anfibi e rettili dell’Albania esistenti nel Museo Zoologico di Bedino. Atti della Società Italiana di Scienze Naturali 79: 263–272. Haxhiu, I., 1982. “Percaktues i amfibeve te Shqiperise”. Universiteti i Tiranes, Tirana. Haxhiu, I., 1983. Fauna e vendit tone pasuri e madhe per ekonomine. Kultura Masive, Tirane 3: 71–81. Haxhiu, I., 1986a. Studim per bretkosat e gjelbra te vendit tone. Buletini i Shkencave te Natyres, Tirane 3: 47–55. Haxhiu, I., 1986b. Studim per bretkosat e gjelbra te vendit tone. Buletini i Shkencave te Natyres, Tirane 4: 80–84. Haxhiu, I., 1987. Studim per bretkosat e gjelbra te vendit tone. Buletini i Shkencave te Natyres, Tirane 1: 105–114.

Haxhiu, I., 1990. Te ushqyerit dhe riprodhimi e thithlopes (Bufo bufo) ne kushtet e vendit tone. Buletini i Shkencave te Natyres, Tirane 3: 34–40. Haxhiu, I., 1991. Donnees Bioecologiques Sur La Grenouille Des Torrents: Rana graeca Boulenger (Amphibia Anura) en Albanie. Biologia Gallo-Helenica 16: 171–176. Haxhiu, I., 1994. The Herpetofauna of Albania: Amphibia: Species Composition, Distribution, Habitats. Zoologische Jahrbuecher Systematik 121: 109–115. Haxhiu, I. and Alimehilli Xh., 1987. Emertime te amfibeve ne shqipen popullore. Studime Filologjike, Tirane 1: 185–189. Haxhiu, I. and Oruci, S., 2004. Amfibofauna e Sarandes. Monografi, Tirane. Pp. 101. Haxhiu, I. and Vrenozi, B., 2009. Species of Amphibians and Reptilians of Lake Ohrid with notes in their Ecology. Proceedings of International Conference. Botimet EMAL. Pp. 382–387. Hotz, H. and Uzzell, T., 1982. Biochemically detected sympatry of two frog species. Two different cases in the Adriatic Balkans (Amphibia, Ranidae). Proceedings of the Academy of Natural Sciences of Philadelphia 143: 50–79. Jablonski, D., 2011. Reptiles and amphibians of Albania with new records and notes on occurrence and distribution. Acta Societatis Zoologicae Bohemicae 75: 223–238. Kopfstein, F. and Wattstein, O., 1921. Reptilien und Amphibien aus Albanien. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 70: 387–457. Misja, K., 2006. “Libri i kuq i faunes” (“Red Book of Albanian Fauna”). MMPAU, Tirane. Uzzell, T., Gunther, R., Tunner H.-G. and Heppich, S., 1987. Rana shqiperica a new European water frog species from the Adriatic Balkans (Amphibia, Salientia, Ranidae). Notulae Naturae of the Academy of Natural Sciences of Philadelphia 468: 1–3. Radovanovic, M., 1951. “Vodozemci i Gmizavi Nase Zemlje (Amphibien und Reptilien Jugoslawiens)”. Naucna Knjiga, Beograd.

Schneider, H. and Haxhiu, I., 1992. The distribution of the Epeirus frog (Rana epeirotica) in Albania. Amphibia-Reptilia 13: 29–295. Schneider, H. and Haxhiu I., 1994. Mating call analysis and taxonomy of water frogs (Ranidae, Anura) in Albania. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere 121: 248–262. Schneider, H. and Joermann, G., 1988. Mating calls of water frogs (Ranidae) of Lake Skutari, Yugoslavia, and the relationship to water frogs of other regions. Journal of Zoological Systematics and Evolutionary Research 26: 261–275. Schneider, H., Sofianidou, T.S. and Kyriaropoulou‐Sklavounou, P., 1984, Bioacoustic and morphometric studies in water frogs (genus Rana) of Lake Ioannina in Greece, and description of a new species (Anura, Amphibia). Journal of Zoological Systematics and Evolutionary Research 22 (4): 349–366. Schneider, H., Sinsch, U. and Sofianidou, T.S., 1992. The water frogs of Greece: Evidence for a new species. Journal of Zoological Systematics and Evolutionary Research 31: 47–63. Sofianidou, T.S. and Schneider, H., 1989. Distribution range of the Epeirus frog Rana epeirotica (Amphibia: Anura) and the composition of the water frog populations in western Greece. Zoologischer Anzeiger 223 (1–2): 13–25.

Amphibians of Albania79

48 Declines and conservation of amphibians in Greece Konstantinos Sotiropoulos and Petros Lymberakis I. Introduction II. Species of special conservation concern A.  Pelophylax cerigensis (Beerli et al. 1994) B.  Bombina bombina (Linnaeus 1761)

F.  Rana temporaria (Linnaeus 1758) G.  Lyciasalamandra helverseni (Pieper 1963)

III. Conservation measures and monitoring programmes

C. Pelophylax cretensis (Beerli et al.1994)

IV. Conclusions

D.  Lyciasalamandra luschani (Steindachner 1891)

V. References

E.  Ichthyosaura alpestris (Laurenti 1768)

I.  Introduction The amphibian fauna of Greece comprises 22 species out of 85 found in Europe, a significant number given the small size of the country (Temple and Cox 2009). The most commonly invoked explanation for the richness and peculiarity of the Greek amphibian fauna is the geographic location of the Hellenic region and its geological history (Lymberakis and Poulakakis 2010 and references therein). Among the species constituting this fauna, three are insular endemics, Lyciasalamandra helverseni, occurring on three southeastern Aegean islands (Karpathos, Kasos, and Saria), Pelophylax cretensis on Crete, and Pelophylax cerigensis on Karpathos. In addition, the Greek amphibian fauna includes species with a wider European distribution, but with the southern tip of their geographic range extending into Greece (e.g. Rana temporaria in northern Greece; Bombina bombina in the region of the river Evros), as well as Anatolian species whose westernmost limit of distribution is Greece (e.g. Pelophylax bedriagae in the East Aegean Islands and Lyciasalamandra luschani on Megisti island). Finally, the Greek populations of the alpine newt (Ichthyosaura alpestris) and of the Cretan tree frog (Hyla arborea) are considered as distinct endemic subspecies (I. a. veluchiensis and H. a. cretensis respectively). Degradation of habitat and loss of breeding sites constitute the major threats to Greek amphibian populations, either as a result of intense climatic changes (increasing average temperatures, decreasing rainfall; prolonged drought), or as a result of human activities (agricultural and industrial pollution of inland waters; livestock farming; residential development and tourism; over-watering; recreational activities) (Sotiropoulos 2010). Handrinos (1992) estimated a loss of 61% of Greek wetlands between 1910 and 1991. There are no indications that this trend has decreased since. Other significant threats to local amphibian populations are forest fires and the collection of rare and endemic species for research and educational purposes; the latter can lead target species to extinction. A further risk is the introduction of the American bullfrog Lithobates catesbeianus into Crete; this invasive species can displace local populations of the Cretan waterfrog (P. cretensis) and in the long-term might lead to its extinction. Finally, a possible future threat to



Declines and Conservation of Amphibians in Greece81

Greek amphibians is attack by the fungus Batrachochytrium dendrobatidis, which is responsible for mass deaths of amphibians on four continents (Berger et al. 1998, 2009; Bosch et al. 2001; Stuart et al. 2004; Garner et al. 2005). So far, all 88 Greek specimens that have been screened have been negative (Garner et al. 2005). Table 48.1 Status of amphibian species present in Greece. CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near Threatened; L = Least Concern; NE = Not Evaluated.

Taxon

National Red Data Book

IUCN (Mediterranean)

Annex EU

Presidential Bern Decree No Convention 67/1981

Remarks

CAUDATA Salamandridae Salamandra salamandra

NE

LC

Lyciasalamandra helverseni

NT/CR

VU

Lyciasalamandra luschani

VU

EN

Lissotriton vulgaris

NE

Ichthyosaura alpestris

VU/EN

Triturus karelinii

NT

LC

IV

II

Triturus macedonicus

LC

LC

IV

II

Bombina bombina

EN

LC

II/IV

II

Bombina variegata

LC

LC

II/IV

II

Bufo bufo

LC

LC

+

III

Bufotes viridis

LC

LC

IV

+

II

LC

LC

IV

+

II

NE

LC

IV

+

II

Pelophylax bedriagae

NE

LC

Pelophylax cerigensis

CR

EN

Endemic

Pelophylax cretensis

EN

EN

Endemic

Pelophylax kurtmuelleri

LC

LC

Pelophylax ridibundus

LC

LC

Pelophylax epeiroticus

NT

VU

Rana graeca

NE

LC

IV

Rana temporaria

VU

LC

V

Rana dalmatina

NE

LC

IV

+

III

+

II

LC

+

III

LC

+

III

Endemic II/IV

Anura Discoglossidae

Bufonidae

Hylidae Hyla arborea Pelobatidae Pelobates syriacus Ranidae

V

III III +

III III

82 Amphibian Biology

II.  Species of special conservation concern A.  Pelophylax cerigensis (Beerli et al. 1994)

Pelophylax cerigensis is endemic to Greece. It occurs in just a few locations on Karpathos Island, where it inhabits permanent or seasonal streams as well as temporary ponds and pools (Valakos et al. 2008). Although a significant population decline was observed during the past decade, it still can be considered as “common” where it occurs. Until recently, the species also was believed to exist on the island of Rhodes (Beerli et al. 1994, 1996). However, on the basis of more recent data Lymberakis et al. (2007) assigned the Rhodes’ population of water frogs to Pelophylax bedriagae. Degradation and destruction of habitats caused by residential and touristic development, groundwater pumping, and livestock operations are considered to be major threats to this species. Another potential threat is intensive collection for scientific and research purposes exacerbated by the limited and localized distribution of this species (Sotiropoulos 2010). The species is listed in Annex V of the Habitats Directive (92/43/EEC) and Annex III of the Bern Convention as Rana ridibunda. It is classified as Critically Endangered (CR) in the National Red List (Table 48.1).

B.  Bombina bombina (Linnaeus 1761)

Bombina bombina occurs in a small part of Evros prefecture (northeastern Greece) where it exhibits a fragmented distribution. Specifically, it is found in the river delta and in agricultural, low-lying areas either in permanent or seasonal wetlands, including shallow lakes and ponds, swamps and marshes, bogs, and irrigation and drainage channels (Helmer and Scholte 1985). Major threats include degradation and/or loss of terrestrial and aquatic habitats, especially its breeding sites, due to intensive farming, and agro-chemical and industrial pollution (Sotiropoulos 2010). The species is included in Annexes II and IV of the Habitats Directive (92/43/EEC) and Annex II of the Bern Convention. It is classified as Endangered (EN) in the National Red List (Table 48.1).

C.  Pelophylax cretensis (Beerli et al. 1994)

Pelophylax cretensis is endemic to Greece. It occurs on the island of Crete, where it exhibits a highly fragmented distribution exclusively in the lower areas of the island (Beerli et al. 1994). It is found both in permanent and temporary ponds, freshwater lakes, artificial drainage channels and wastewater oxidation tanks, and permanent and seasonal streams. In recent years a significant reduction in the extent and quality of habitat for the species in Crete has been observed. Major threats to the species are the degradation and destruction of habitat due to human activities (residential, industrial, and touristic development, groundwater pumping, livestock farming, and agriculture) and potentially due to global climatic change. Other significant threats to local populations include the introduction of alien species (e.g. Lithobates catesbeianus), and collection for scientific and research purposes. Its limited distribution increases its vulnerability (Sotiropoulos 2010). The species is listed in Annex V of the Habitats Directive (92/43/EEC) and Annex III of the Bern Convention as Rana ridibunda. It is classified as Endangered (EN) in the National Red List (Table 48.1).

D.  Lyciasalamandra luschani (Steindachner 1891)

Lyciasalamandra luschani inhabits the small island of Megisti (Kastelorizo), where it can be considered as common at the sites of occurrence (Polymeni 1988). The island is characterized by xeric habitats with dry pine forests, Mediterranean maquis, and phrygana. Salamanders are restricted to karstic limestone where they live almost exclusively in boulder fields formed at the foot of karstic rock (Veith et al. 2001), as well as near human settlements, inhabiting loose rock walls and ruins (Polymeni 1988, 1994).



Declines and Conservation of Amphibians in Greece83

Main threats to the species are degradation and/or habitat destruction resulting from demolition of stone walls, fences, and old stone buildings. Other threats include collection for scientific and research purposes, prolonged drought, and random extirpation as a result of its limited distribution (Sotiropoulos 2010). The species is included in Annexes II and IV of the Habitats Directive (92/43/ EEC), Annex II of the Bern Convention, and in Presidential Degree 67/81 (as Mertensiella luschani). It is classified as Vulnerable (VU) in the National Red List (Table 48.1).

E.  Ichthyosaura alpestris (Laurenti 1768)

The alpine newt (Ichthyosaura alpestris) is spreading in Greece in the high elevations of the Pindus massif, northern Peloponnisos, and Ropope, where it occurs in small and highly isolated local populations (Sotiropoulos et al. 1995). It inhabits a variety of permanent and seasonal wetlands, such as ponds and streams with cold, clear water found in woods and forest glades, alpine meadows, and sometimes in rocky and arid areas. It is often found in springs and animals’ drinking troughs (Bringsøe 1994; Breuil and Parent 1987, 1988). Recent genetic studies show that Peloponnesian populations differ significantly in both mtDNA and allozyme frequencies from the mainland ones and constitute a separate conservation unit (Sotiropoulos et al. 2007, 2008). Increasing habitat degradation and destruction due to climatic change (high temperatures, prolonged droughts) and human activities such as water abstraction, pollution, winter tourism, motor sports, and natural disasters, e.g. fires, are among the major threats for the species in Greece. Another potential threat is over-collection for scientific purposes (Sotiropoulos 2010). The species is included in Annex III of the Bern Convention and in Presidential Decree 67/81. It is found in the Northern Pindos National Park and areas of network Natura 2000. It is classified as Vulnerable (VU) in the National Red List, while Peloponnesian populations are considered as Endangered (EN) (Table 48.1).

F.  Rana temporaria (Linnaeus 1758)

Rana temporaria occurs in Greece in a small part of the Rhodope Mountains and in the northwestern part of the prefecture of Evros, mostly in forested habitats (deciduous and coniferous) and in montane meadows. Its presence has been confirmed in at least five locations, where it breeds in permanent and seasonal ponds, creeks and streams of permanent or periodic flow, springs, bogs, and swamps. However, it is likely present in more places in the Rhodopes (Asimakopoulos 1989, 1994). Major threats to the species include degradation and loss of terrestrial and aquatic habitat, particularly breeding sites, due to intensive logging and deforestation (Sotiropoulos 2010). The species is included in Annex III of the Bern Convention and Annex V of the Habitats Directive (92/43/EEC). It is found in areas of the Natura 2000 network. It is classified as Vulnerable (VU) in the National Red List (Table 48.1).

G.  Lyciasalamandra helverseni (Pieper 1963)

Lyciasalamandra helverseni is endemic to Greece, inhabiting three Dodecanese islands: Karpathos, Saria, and Kasos (Polymeni 1988; Veith et al. 2001). These islands are characterized by xeric habitats with dry pine and oak forests, Mediterranean maquis, and phrygana. Salamanders are restricted to karstic limestone boulder fields (Veith et al. 2001) and near human settlements where they inhabit loose rockwalls and ruins (Polymeni 1988, 1994). At the genetic level, the L. helverseni populations of Kasos constitute a distinct clade differing significantly from those of Karpathos and Saria, and are considered as a separate conservation unit (Eleftherakos et al. 2007). A major threat to the species is the degradation and destruction of habitat due to fires, residential and touristic development, and climatic change. Especially on the Island of Kasos, the species is threatened by over-grazing by livestock, which has greatly increased in recent years. Genetic studies show a high degree of inbreeding in isolated, local populations (Eleftherakos et al. 2007).

84 Amphibian Biology Another threat is over-collection for scientific and research purposes (Sotiropoulos 2010). The species is listed in Annexes II and IV of the Habitats Directive (92/43/EEC), Annex II of the Bern Convention, and in Presidential Degree 67/81 (as Mertensiella luschani). It is classified as Near Threatened (NT) in the National Red List, but on the island of Kasos it is considered as Critically Endangered (CR) (Table 48.1).

III.  Conservation measures and monitoring programmes The only conservation measure taken so far for Greek amphibians is the inclusion of many species under national legislation (Presidential Degree 67/1981) as well as in the National Red List (Table 48.1). Apart from a monitoring program of Karpathos’ populations of water frogs, by the managing authority of Karpathos-Saria during the past few years, no other official conservation and management activities have been provided for the protection of amphibian populations in Greece.

IV.  Conclusions The Amphibian fauna of Greece is amongst the richest in Europe, considering the limited area of the country. Among the 22 species, 7 have been included in the National Red List and are of special conservation concern. Among them, three are endemic to Greece. Major threats to local amphibian populations are loss of habitat and degradation of breeding-sites, destruction that is due to human activities, extensive isolation, climatic alterations, and to a lesser extent to natural disasters. Conservation measures that are required include (1) development and implementation of measures and actions to protect and preserve local populations at regional and national levels, (2) application of information and awareness programs at local and national levels, (3) development of research programs for a detailed study of the biology and ecology of the species, (4) precise identification and treatment of threats, (5) monitoring of local populations, (6) development and implementation of management programmes, (7) restoration of habitat types, and (8) re-introduction of species into restored areas.



Declines and Conservation of Amphibians in Greece85

V.  References Asimakopoulos, V., 1989. Die Vertbreitung des Grasfrosches Rana temporaria Linnaeus, 1758 in Griechenland. Salamandra 25: 291–294. Asimakopoulos, V., 1994. Distributional records for the amphibians of the Greek part of Rodope mountain range (East Macedonia and Thraki). Biologia Gallo-Hellenica 22: 23–36. Beerli, P., Hotz, H. and Uzzell, T., 1996. Geologically dated sea barriers calibrate a protein clock for Aegean water frogs. Evolution 50: 1676–1687. Beerli, P., Hotz, H., Tunner, H., Heppich, S. and Uzzell, T., 1994. Two new water frog species from the Aegean islands Crete and Karpathos (Amphibia, Salientia, Ranidae). Notulae Naturae of the Academy of Natural Sciences of Philadelphia, No. 470: 1–9. Berger, L., Longcore, J.F., Speare, R., Hyatt, A. and Skerratt, L.F., 2009. Fungal Diseases of Amphibians. In Amphibian Decline: Diseases, Parasites, Maladies and Pollution, ed. H. Heatwole and J.W. Wilkinson. Volume 8 in the series Amphibian Biology, ed. H. Heatwole. Surrey Beatty & Sons, Baulkham Hills, Australia. Chapter 2 (pp. 2986–3052). Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.D., McDonald, K.R., Hines, H.B., Lips, K.R., Marantelli, G. and Parkes, H., 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences (USA) 95: 9031– 9036. Bosch, J., Martinez-Solano, I. and Garcia-Paris, M., 2001. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biological Conservation 97: 331–337. Breuil, M. and Parent, G.H., 1987. Essai de caractérisation du Triton alpestre hellénique Triturus alpestris veluchiensis. I. Historique et présentation des nouvelles données. Alytes 6: 131–151.

Breuil, M. and Parent, G.H., 1988. Essai de caractérisation des populations du Triton alpestre hellénique. II. Relations entre le Triton alpestre hellénique et la sous-espèce nominative. Alytes 7: 19–43. Bringsøe, H., 1994. New records of Triturus alpestris (Amphibia, Caudata) in south Greece, with information on feeding habits, ecology and distribution. Annales Musei Goulandris 9: 349–374. Eleftherakos, E., Sotiropoulos, K. and Polymeni, R.M., 2007. Conservation units in the insular endemic salamander Lyciasalamandra helverseni (Urodela, Salamandridae). Annales Zoologici Fennici 44: 387–399. Garner, T.W.J., Walker, S., Bosch, J., Hyatt, A.D., Cunningham, A.A. and Fischer, M.C., 2005. Chytrid fungus in Europe. Emerging Infectious Diseases 11: 1639–1640. Handrinos, G., 1992. Wetland loss and wintering waterfowl in Greece during the 20th century: A first approach. In Managing Mediterranean Wetlands and their Birds, ed. M. Finlayson, T. Hollis and T. Davis. Proceedings of an IWRB International Symposium, Grado, Italy. Pp. 183–187. Helmer, W. and Scholte, P., 1985. Herpetological research in Evros, Greece. Proposal for a biogenetic reserve. Societas Europaea Herpetologica. Pp. 139. Lymberakis P. and Poulakakis, N., 2010. Three continents claiming an archipelago: The evolution of Aegeans herpetofaunal diversity. Diversity 2: 233–255. Lymberakis, P., Poulakakis, N., Manthalou, G., Tsigenopoulos, C.S., Magoulas, A. and Mylonas, M., 2007. Mitochondrial phylogeography of Rana (Pelophylax) populations in the eastern Mediterranean region. Molecular Phylogenetics and Evolution 44: 115–125. Polymeni, R.M., 1988. Contribution to the study of the amphibian Mertensiella luschani (Steindachner, 1891) (Urodela, Salamandridae). Doctoral Thesis, Department of Biology, University of Athens [in Greek with English summary].

86 Amphibian Biology Polymeni, R.M., 1994. On the biology of Mertensiella luschani (Steindachner, 1891): A review. Mertensiella 4: 301–314. Sotiropoulos, K., 2010. Amphibians. In The Red Data Book of Threatened Animals of Greece, ed. A. Legakis and P. Maragou. Ministry for the Environment, Energy and Climate Change/ Hellenic Zoological Society, Athens. Pp. 161– 178. Sotiropoulos, K., Eleftherakos, K., Dzukic, G., Kalezic, M.L., Legakis, A. and Polymeni R.M., 2007. Phylogeny and biogeography of the alpine newt Mesotriton alpestris (Salamandridae, Caudata), inferred from mtDNA sequences. Molecular Phylogenetics and Evolution 45: 211–226. Sotiropoulos, K., Eleftherakos, K., Kalezic, M.L., Legakis, A. and Polymeni R.M., 2008. Genetic structure of the alpine newt, Mesotriton alpestris (Salamandridae, Caudata), in the southern limit of its distribution: implications for conservation. Biochemical Systematics and Ecology 36: 297–311. Sotiropoulos, K., Legakis, A. and Polymeni, R.M., 1995. A review of the knowledge on the distribution of the genus Triturus in Greece. Herpetozoa 8: 25–34. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. and Waller, R.W., 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786. Temple, H.J. and Cox, N.A., 2009. European Red List of Amphibians. Office for Official Publications of the European Communities, Luxembourg. Valakos, E.D., Pafilis, P., Sotiropoulos, K., Lymberakis, P., Maragou, P. and Foufopoulos, J., 2008. The Amphibians and Reptiles of Greece. Chimaira Editions, Frankfurt am Main. Veith, M., Baran, I., Godmann, O., Kiefer, A., Öz, M. and Tunç, M.R., 2001. A revision of population designation and geographic distribution of the Lycian Salamander Mertensiella luschani (Steindachner, 1891). Zoology in the Middle East 22: 67–82.

49 Amphibian conservation and decline in Romania Dan Cogălniceanu and Laurenţiu Rozylowicz I. Introduction A.  Human footprint B. Phylogeography

II. Species of special conservation concern A.  Taxonomic issues

III. Conservation measures and monitoring programmes A.  Legislation and conservation policy B.  Red Lists C.  Conservation and taxonomy D.  Conservation strategies

B. Hybridization

IV. Conclusions

C.  Major threats

V. Acknowledgements VI. References

Abbreviations and acronyms used in the text and references: asl EEC EU IUCN mtDNA RL

above sea level European Economic Community European Union International Union for the Conservation of Nature mitochondrial deoxyribonucleic acid Red List

I.  Introduction Romania is populated by 19 species, including a species complex of amphibians. The country comprises an area of 238,390 km2 that is divided somewhat evenly between plains and meadows (33%), hills and plateaus (36%), and mountains (31%). It is positioned in the southeastern part of Central Europe and is bounded by the Carpathian Mountains, the lower course of the Danube (for a distance of 1,075 km), and the Black Sea. On a global land-based map, Romania is positioned at a latitude of 45°N and longitude of 25°E, encompassing a land area measured at 525 km northsouth and 743 km east-west. The climate is temperate–continental, with multi-annual average temperatures of 8°C in the northern portion of the country, 11°C in the south, and a mean value of -2.5°C in the highest mountainous regions. Yearly precipitation decreases from west to east, from 600 mm in the Banat-Crişana Plain, to 500 mm in the Romanian Plain, and less than 400 mm along the coast of the Black Sea, while in the mountains annual precipitation reaches 1,000–1,400 mm (Rey et al. 2007). Romania is situated at the junction of five different biogeographic regions (alpine, continental, pannonian, Black Sea, and steppic) out of the ten regions recognized by the European Union (EU). There are 17 major types of terrestrial ecosystem in Romania, including all of Europe’s major ecosystems. These are designated as: boreal coniferous forests, mesophilous, hygrophilous,

88 Amphibian Biology xerothermic broadleaved forests, and various grasslands and shrubbery. Compared to the rest of Europe, Romania maintains a high proportion of natural and semi-natural ecosystems and habitats that cover 47% of the country, the rest being divided between agricultural land (45%) and built-up areas (8%) (National Institute of Statistics 2009). There is an abundance of semi-natural habitat created and maintained by low-intensity traditional farming (Cowell 2007). It is estimated that nearly 70% of Romania’s territory was covered by forests two centuries ago, and approximately 50% of the area was still forested a century ago (Giurescu 1975). There are only four countries with intact forest landscapes currently left in Europe – the three countries of Fennoscandia (Norway, Sweden, and Finland) and Romania (Greenpeace 2006). Virgin forests in Romania cover 218,500 ha in parcels larger than 50 ha and represent 3.43% of the total forested area of Romania (Biriş and Veen 2005).

A.  Human footprint

Romania has a relatively low population density of 90 inhabitants per km2 (National Institute of Statistics 2009). The road network is moderately developed, with about 80,000 km of roads, of which 20% are national. Thus, it has the lowest road density (0.33 km/km2) within the EU. The overall human impact is minimal due to a small human population density and an underdeveloped transportation highway network. Historically, humans tended to settle along large rivers that provided water, food, shelter, construction materials, and transportation routes. For centuries these humans attempted to control flood levels and subsequent erosion to protect their settlements and agricultural fields (Gren et al. 1995). Many such massive environmental transformations were implemented along the length of the Danube River and its major tributaries, leading to the destruction of nearly 450,000 ha of wetlands linked to the river floodplain out of a total floodplain area of 540,000 ha (Schneider et al. 2008). The Danube Delta was also affected, with approximately 20% of the delta being dyked or drained (Ştiucă et al. 2002). Damming and dyking, combined with the development of a complex irrigation network constructed until the late 1980s in the southern part of Romania, promoted the dispersal of amphibians. During the 1990s, the overall irrigation network was de-emphasized and essentially dismantled (Davidescu et al. 2010).

B.  Phylogeography

The present composition and distribution of Europe’s fauna was shaped by glaciation. A number of studies, and the increasing body of accumulating data, have allowed for the identification of several general patterns. The highest genetic diversity in many species, and highest species diversity, is reported to be in the southern refugia, a region that has remained unaltered by these climatic changes. Genetic evidence of multiple range expansions and retractions during the Pliocene–Pleistocene climatic oscillations are still observable in southeastern and central Europe but are minimally detectable in northern Europe, thus generating the present pattern of northern purity and southern richness (e.g. Hewitt 2004). Recent phylogenetic studies on amphibians point to multiple glacial refugia in Romania that contributed to the postglacial recolonization of central and northern Europe. The moor frog (Rana arvalis), being a lowland species, is restricted to humid habitats, with a broad Eurasian distribution. Babik et al. (2004) identified three main lineages in the Romanian Carpathian Basin. The balance of the species’ range is populated by a single lineage, suggesting that the other two lineages, which harbour high mitochondrial and morphological diversity, survived several glacial cycles in the Carpathian Basin. However, they have not expanded to the North, at least not within this present interglacial period. A phylogenetic study of the spadefoot toad (Pelobates fuscus) identified nearly all genetic polymorphism in populations from the south of Romania and Serbia, considered as a



Amphibian Conservation and Decline in Romania89

refugial zone (Eggert et al. 2006). Similarly, phylogenetic analysis of two newt species (Lissotriton vulgaris and L. montandoni) has shown that the older clades were found not only in the southern part of the range but also in central Europe (Babik et al. 2005). The Romanian lowlands, located northwest of the Black Sea, and the Carpathians are important refugial zones for Bombina bombina and B. variegata, respectively (Fijarczyk et al. 2011) and are far north of the Mediterranean areas usually regarded as glacial refugia, thereby highlighting the importance of these zones for ectothermic terrestrial species. Table 49.1 The list and status of Romanian amphibians according to the European Union Habitats Directive and Bern Convention annexes and three different Red Lists.

Taxon

Habitats Directive

Bern Convention

IUCN Red List Europe (2009)1

IUCN Red List Romanian Europe 27 (2009)1 Red List (2005)2

Triturus dobrogicus

3

2

NT

NT

EN

Triturus cristatus

3, 4A

2

LC

LC

VU

LC

LC

Lissotriton vulgaris

4B

3

Lissotriton vulgaris ampelensis

3, 4A

3

NT VU

Lissotriton montandoni

3, 4A

2

LC

LC

VU

Ichthyosaura alpestris

4B

3

LC

LC

VU

Salamandra salamandra

4B

3

LC

LC

VU

Bombina bombina

3, 4A

2

LC

LC

NT

Bombina variegata

3, 4A

2

LC

LC

NT

Pelobates fuscus

3, 4A

2

LC

LC

VU

Pelobates syriacus

4A

2

LC

NT

EN

Bufo bufo

4B

3

LC

LC

NT

Bufotes viridis

4A

2

LC

LC

NT

Hyla arborea

4A

2

LC

LC

NT

Rana dalmatina

4A

2

LC

LC

VU

Rana temporaria

4B, 5A

3

LC

LC

VU EN

Rana arvalis

4A

2

LC

LC

Pelophylax kl. esculentus

5A

3

LC

LC

Pelophylax lessonae

4B

3

LC

LC

Pelophylax ridibundus

5A

3

LC

LC

1 Temple and Cox (2009). 2 Iftime (2005).

II.  Species of special conservation concern A.  Taxonomic issues

Of the 19 species of amphibians in Romania, 7 (Lissotriton vulgaris, L. montandoni, Ichthyosaura alpestris, Bufotes viridis, Pelophylax ridibundus, P. lessonae, and P. kl. esculentus) have been affected by recent taxonomic changes (Cogălniceanu et al. 2013). The changes are not currently included in legislation, thus generating an inconsistency among managers, decision-makers, and taxonomists (Table 49.1). The nomenclature used in the present chapter is according to Speybroeck et al. (2010). There is uncertainty regarding the specific taxonomic status of Triturus dobrogicus after Litvinciuk and Borkin (2000) described two subspecies without precise range boundaries in Romania, a study unconfirmed later by Vörös and Arntzen (2010). Also, the presence of T. arntzeni (now T. ivanbureschi) indicated by a map in Vörös and Arntzen (2010) has not been confirmed.

90 Amphibian Biology

Fig. 49.1 The Romanian distribution of the amphibian species that reach their distributional limits within that country (grey areas) in relation to the distribution of the European Union’s Biogeographic regions there (see code). 1: Lissotriton montandoni; 2: Triturus dobrogicus – stippled gray range; 3: Lissotriton vulgaris ampelensis; 4: Triturus cristatus; 5: Salamandra salamandra; 6: Bombina variegata; 7: Pelobates syriacus; 8: Pelobates fuscus; 9: Rana dalmatina; 10: Rana arvalis.

More than half of the species found in Romania are at the limit of their geographic range and are of special importance for conservation (Cogălniceanu et al. 2013). Of these, five have a range restricted to a certain area or type of habitat (Popescu et al. 2013) (Table 49.2; Figure 49.1).

B.  Hybridization

Three pairs of related species hybridize extensively in Romania, the extent of the area of hybridization possibly having been increased by human-induced changes in their habitat. The two species of toads of the genus Bombina hybridize extensively (Szymura 1993). The pattern of the hybrid zones differs in Romania, either clinal (i.e. narrow contact zones) in the south and east, or extended mosaic hybrid zones in Transylvania (Vines et al. 2003). The two related small species of newt, Lissotriton vulgaris and L. montandoni, hybridize extensively within their areas of contact, usually at elevations of 500–1,000 m asl (e.g. Fuhn et al. 1975). A recent molecular study by Babik et al. (2005) reported a replacement of the original L. montandoni mtDNA by L. vulgaris mtDNA. This was most likely facilitated by reduction of the effective population size of L. montandoni in refugia during glacial periods. The two species of crested newts (Triturus cristatus and T. dobrogicus) also hybridize along narrow contact zones, the latter species being restricted to floodplains (Cogălniceanu et al. 2013).



Amphibian Conservation and Decline in Romania91

Table 49.2 Amphibian species that reach the limits of their distributional range in Romania. No.

Species

Limit of Distributional Range

Range Size

1

Lissotriton montandoni

Eastern and southern limit

Restricted

2

Triturus dobrogicus

Eastern limit

Restricted

3

Lissotriton vulgaris ampelensis

Endemic subspecies

Restricted

4

Triturus cristatus

Southern limit

Widespread

5

Salamandra salamandra

Eastern limit

Widespread

6

Bombina variegata

Eastern limit

Widespread

7

Pelobates syriacus

Northern limit

Restricted

8

Pelobates fuscus

Southern limit of contiguous range

Widespread

9

Rana dalmatina

Eastern limit

Widespread

10

Rana arvalis

Southern limit

Restricted

C.  Major threats

A recent evaluation has revealed major threats to amphibians in the Palaearctic region (Anthony et al. 2008). In their order of significance these are: habitat loss, land use changes, pollution, natural disasters, human disturbance, invasive species, accidental mortality, fire, and disease. Of these, habitat loss, pollution, and accidental mortality have been documented for Romanian amphibians. While industrial pollution has decreased over the past two decades, intensification of agriculture and ongoing improper treatment of wastewater are escalating (Patroescu et al. 2006) and both pose serious threats to lowland species (e.g. Triturus dobrogicus; Bombina bombina). The species in Romania that are most affected by habitat destruction are the habitat specialists: Rana arvalis, Pelobates sp., and Triturus dobrogicus. The moor frog Rana arvalis is widely distributed throughout Europe and considered of least concern, but its range is steadily decreasing. Roček and Sandera (2008) suggested that increased previous deforestation in Europe restricted its range to floodplains along rivers. This species is now severely threatened by habitat destruction as a result of damming and dyking and has already vanished from several localities (Sas et al. 2008). The two species of the genus Pelobates reach their ranges’ limits in Romania. The present-day range of P. syriacus seems to be much smaller than before. During the Pliocene era its range extended much farther north, into Central Europe. The fragmentation of the previously contiguous range within the Balkans limited its distribution to a few restricted refugial zones (Ugurtaş et al. 2002). Fossils of P. fuscus have been identified from the Middle Miocene onward within Central Europe (Venczel 1999). The last post-glacial invasion into central Europe occurred from southern Europe, a long-standing refugial zone (Eggert et al. 2006). Both species have faced a reduction in their range in the Balkans during the past century (Džukić et al. 2005). The range of P. syriacus has also undergone a recent contraction (Delfino et al. 2007), while P. fuscus is vanishing within Sweden (Nystrom et al. 2002) and Denmark (Fog et al. 1997). A recent study of the genetic diversity of P. syriacus in Israel (at the southern limit of its range) exposed an increase in genetic variability from the core of its range to the edge of its dispersal. This finding is explained by the much harsher climatic and abiotic conditions at the range’s edge, which must be tolerated over generations both by tadpoles and by post-metamorphic individuals in that region (Munwes et al. 2010). This result demonstrates the high conservation value of populations at the limits of their ranges.

92 Amphibian Biology

III.  Conservation measures and monitoring programmes A.  Legislation and conservation policy

Conservation within the EU member states is based on several conventions and directives: the Convention on Biological Diversity, the Bern Convention (Convention on the Conservation of European Wildlife and Natural Habitats, 1979), the Bonn Convention (Convention on Migratory Species, 1979), and the two directives: Birds, adopted in 1979 (Council Directive 79/409/EEC on the Conservation of wild birds), and Habitats, adopted in 1992 (Council Directive 92/43/EEC on the Conservation of natural habitats and of wild fauna and flora) (Pullin et al. 2009). At national levels, the conservation priorities are based on the annexes of protected species in the EU Directives and Conventions, as well as on a number of Red Lists. The percentage of protected areas in Romania has increased almost five times since 1989, from 4.1% to 19.29% of the national territory. These increases were the result of the creation of 27 National and Natural Parks and 382 protected areas as part of the EU Natura 2000 network (Iojă et al. 2010). A similar trend of rapid increases of protected areas worldwide has raised concerns about the capacity to manage them (Sutherland et al. 2009). The same applies to Romania, as well, where the efficiency of the extended network of protected areas is criticized as being comprised of unclear conservation goals and with a focus on protecting species and habitats of European-level concern (Iojă et al. 2010). The Birds and Habitats Directives originated from EU 12, and the lists of priority species and habitats from the annexes reflect the situation at the moment. The annexes were updated after each new expansion (in 1995, EU 15 when Finland, Austria, and Sweden joined the EU; EU 25, when 8 former communist countries, Malta, and Cyprus joined in 2004; and finally EU 27 in 2007 when Romania and Bulgaria joined). New species were added to the annexes, but never re-evaluated on the basis of their status in the enlarged EU. Thus, many amphibian species endangered in Western Europe are still common in central and southeastern Europe (e.g. Bombina spp.). The present priorities are European priorities, at a continental level. National priorities that are relevant at regional and local levels are still required in addition to the EU priorities. A critical reappraisal of priorities at both EU and national levels is proposed. This would involve up-scaling or down-scaling in priorities of species listed in the annexes, or in establishing targeted priorities at local and provincial levels. Monitoring is a requirement for Natura 2000 sites and must be conducted within each site by the administrator of that site. There are no standardized protocols and the results of the ongoing surveys do not allow detection of trends in population size. Long-term monitoring studies on amphibian populations and their habitats are carried out in central Romania (e.g. Hartel et al. 2010, 2011).

B.  Red Lists

In addition to the above-listed legislation, there is a wide range of Red Lists (RL) at global, European, regional (e.g. Witkowski et al. 2003), national, and local levels (Köppel et al. 2003). Many European countries still use different criteria in establishing National Red Lists (De Iongh and Bal 2007). While global and regional RL are constructed according to strict rules and criteria, national, and local RLs are prepared inadequately and mostly reflect the author’s opinion or bias, without criteria or even reasons given. As an example, the Romanian national RL (e.g. Botnariuc and Tatole 2005) and local RL (e.g. Oţel and Ciocarlan 2000) use only 9 categories while the IUCN recommends the use of 11 categories for regional assessments. These shortcomings limit the value and utility of national RLs that should be considered with caution for they do not allow further analyses or the detection of trends. Szekely et al. (2009) compared several national and regional RLs, with a focus on the Black Sea province of Dobrogea. Considerable differences were observed between the Red



Amphibian Conservation and Decline in Romania93

Lists, not only in the use of subjective rather than objective criteria, but also by different spatial scales, with some species locally abundant and others regionally rare or with a restricted distribution. Overall, many European countries still use different criteria in establishing national RLs (De Iongh and Bal 2007), thus requiring their harmonization within Europe. There are also significant differences in the conservation status of species listed within the various conventions, directives, and RLs (e.g. Batáry et al. 2007).

C.  Conservation and taxonomy

Over the past few decades, major changes have developed in the taxonomy and systematics of amphibians, with the number of recognized species of amphibians increasing 48.2% since 1985 (Frost et al. 2006). Most recent descriptions are new discoveries, while removal from synonymy represents only a small proportion (14%) of the newly recognized species (Köhler et al. 2008). Apart from the increasing rate of species description, there are major nomenclatural changes in amphibian taxonomy (e.g. Frost et al. 2006), and more changes are likely in the future. This shift is partly due to the major technological advances and to the increasing number of specialists worldwide that work on amphibians. The increasing number of herpetologists and their resulting publications is illustrated by the increase in the output of literature: 25% of all the publications on amphibians published were released during the past decade. This in turn has created a “herpetologist effect”, similar to the “botanist effect” (e.g. Pautasso and McKinney 2007), whereby more amphibian specialists result in increased sampling and in the recognition and description of new species. The significant increase in described species does not have a direct impact on Romania’s amphibians, since most newly described species are tropical (Cogălniceanu and Hartel 2009). A prolonged period of time is required to include taxonomic changes in legislation, which illustrates the slow process of assimilating new approaches and research findings into the management of biodiversity (Cogălniceanu and Cogălniceanu 2010). Thus, conservation is frequently hampered and delayed by taxonomic instability that makes regional and international cooperation difficult due to misunderstandings concerning the names of priority species (Isaac et al. 2004).

D.  Conservation strategies

The EU Habitats and Birds Directives are focused on favourable conditions for conservation. While overall management plans have to be tailored according to the species of conservation concern and to the specific conditions existing in the area, there are some broad generalities. Species that require particular protective measures can be included in two broad categories: 1.

2.

Species abundant in the past but now under threat from human activities such as habitat destruction and over-harvesting (e.g. Rana dalmatina; R. temporaria; Lissotriton vulgaris; Triturus cristatus; Hyla arborea; Bufo bufo). A ban on harvesting brown frogs for meat (frog legs) and the creation of ponds for reproduction are sufficient measures in the medium-term. Species that were rare in the past, or which have a small or fragmented range and low densities and population sizes, caused either by superior competitors, effective predators, or specific habitat requirements (e.g. Rana arvalis Pelobates syriacus; Triturus dobrogicus; Lissotriton montandoni). These species require more complex and active measures involving the preservation of their habitats, eliminating fish from some areas, providing migration corridors, while constantly monitoring their populations for change.

Additional studies on habitat use and population status of Romanian amphibians are required since Romania is extremely heterogeneous (e.g. covering five biogeographic regions), and has human impacts that vary regionally.

94 Amphibian Biology

IV. Conclusions The EU Common Agricultural Policy has triggered important socio-economic changes of traditional land use (Young et al. 2007). Many traditional land-use systems are presently affected either by abandonment of land or intensification of its use (Plieninger et al. 2006; Kuemmerle et al. 2009). After 1990, the use of pesticides and chemical fertilizers decreased steadily (Turnok 1996; Ciaian and Pokrivcak 2007), but an increase in their use is foreseeable in connection with the intensification of agricultural practices. The number of temporary ponds along dirt roads and of artificially-made aquatic habitats used for watering cattle is declining due to improved management and infrastructure of roads, and the spread of modern watering systems. The stocking of bodies of water with fish also has recently resumed and has resulted in the exclusion of amphibians from many habitats for breeding (e.g. Hartel et al. 2007). Despite the low density of roads, a steady increase in intensity of vehicular traffic has triggered higher death rates along roads and thereby contributes to fragmentation and isolation of habitats. The presence of the chytrid fungus was recently reported from Romania (Vörös et al. 2013), but no harmful effects were found in the populations studied. Overall, the conservation measures currently in place in Romania might not prevent or even reduce the expected decline in amphibians; more specific measures are required, targeted at preserving and managing aquatic habitats used for breeding.

V. Acknowledgements Special thanks to Jelka Crnobrnja-Isailovic and Tibor Hartel for helpful comments. This work was supported by two grants of the Romanian National Authority for Scientific Research, CNCS-UEFISCDI, PN-II-ID-PCE-2011-3-0173 (principal investigator Dan Cogălniceanu) and PN-II-RU-TE-2011-3-0183 (principal investigator Laurenţiu Rozylowicz).



Amphibian Conservation and Decline in Romania95

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Kuemmerle, T., Müller, D., Griffiths, P. and Rusu, M., 2009. Land use change in Southern Romania after the collapse of socialism. Regional Environmental Change 9: 1–12. Litvinchuk, S.N. and Borkin, L.J., 2000. Intraspecific taxonomy and nomenclature of the Danube crested newt, Triturus dobrogicus. Amphibia-Reptilia 21: 419–430. Munwes, I., Geffen, E., Roll, U., Friedmann, A., Daya, A., Tikochinski, Y. and Gafny, S., 2010. The change in genetic diversity down the core-edge gradient in the eastern spadefoot toad (Pelobates syriacus). Molecular Ecology 19: 2675–2689. National Institute of Statistics, 2009. “Romanian Statistical Yearbook”. http://www.insse.ro/ cms/rw/pages/anuarstatistic2009.ro.do Nystrom, P., Birkedal, L., Dahlberg, C. and Bronmark, C., 2002. The declining spadefoot toad Pelobates fuscus: Calling site choice and conservation. Ecography 25: 488–498. Oţel, V. and Ciocarlan, V. (eds), 2000. The Red List of Plant and Animal Species from the Danube Delta Biosphere Reserve Romania. Editura Fundaţia Aves. Tulcea. Patroescu, M.. Iojă, C.I., Patroescu-Klotz, I.V. and Necsuliu, R., 2006. Umweltqualität in Rumänien. In T. Kahl, K. Metheltin and A. Ungureanu (eds) Rumänien. Viena: LIT Verlag. Pp. 151–167. Pautasso, M. and McKinney, M.L., 2007. The Botanist effect revisited: Plant species richness, county area, and human population size in the United States. Conservation Biology 21: 1333–1340. Plieninger, T., Höchtl, F. and Spek, T., 2006. Traditional land-use and nature conservation in European rural landscapes. Environmental Science & Policy 9: 317–321. Popescu, V.D, Rozylowicz, L., Cogălniceanu, D., Niculae, I.M. and Cucu, A.L., 2013. Moving into protected areas? Setting conservation priorities for Romanian reptiles and amphibians at risk from climate change. PLOS One 8 (11): e79330. Pullin, A.S., Baldi, A., Can, O.E., Dieterich, M., Kati, V., Livoreil, B., Lovei, G., Mihok, B.,

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98 Amphibian Biology global biological diversity. Conservation Biology 23: 557–567. Székely, P., Plăiaşu, R., Tudor, M. and Cogălniceanu, D., 2009. The distribution and conservation status of amphibians in Dobrudja (Romania). Turkish Journal of Zoology 33: 147–156. Szymura, J.M., 1993. Analysis of hybrid zone with Bombina. In Hybrid Zones and Evolutionary Process, ed. R.G. Harisson. Oxford University Press, New York. Pp. 261–289. Temple, H.J. and Cox, N.A., 2009. European Red List of Amphibians. Luxembourg: Office for Official Publications of the European Communities. Turnok, D., 1996. The Rural Transition in Romania. Eastern European Countryside 2: 45–57. Ugurtaş, I.H., Ljubisavljevic, K., Sidorovska, V., Kalezic, M. and Dzukic, G., 2002. Morphological differentiation of Eastern Spadefoot toad (Pelobates syriacus) populations. Israel Journal of Zoology 48: 13–32. Venczel, M., 1999. Anurans from the Late Miocene of Tardosbanya (Hungary). Nymphaea (Folia naturae Biharie) 27: 82–90. Vines, T., Köhler, S., Thiel, M., Ghira, I., Sands, T., MacCallum, C., Barton, N. and Nürnberger, B., 2003. The maintenance of reproductive isolation in a mosaic hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution 57: 1876–1888. Vörös, J. and Arntzen, J.W., 2010. Weak population structuring in the Danube crested newt, Triturus dobrogicus, inferred from allozymes. Amphibia-Reptilia 31: 339–346. Vörös, J., Bosch, J., Dán, A. and Hartel, T., 2013. First record of Batrachochytrium dendrobatidis on amphibians in Romania. North Western Journal of Zoology. 9: 446–449. Witkowski, Z.J., Król, W. and Solarz, W. (eds), 2003. Carpathian List of Endangered Species. WWF and Institute of Nature Conservation, Polish Academy of Sciences, Vienna-Krakow. Young, J., Richards, C., Fischer, A., Halada, L., Kull, T., Kuzniar, A., Tartes, U., Uzunov, U. and Watt, A., 2007. Conflicts between

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50 Conservation and decline of amphibians in Hungary Judit Vörös, István Kiss and Miklós Puky B.  Mapping the Hungarian herpetofauna

I. Introduction A. The history of habitat destruction in Hungary

C.  Amphibian rescue actions

B. Legal protection of amphibian species in Hungary

E.  Monitoring programmes

II. Declining species of amphibians and species of special conservation concern A.  Salamandra salamandra

D.  Frog tunnels 1. Hungarian biodiversity monitoring system 2.  Survey of Natura 2000 species 3.  Monitoring of Caudata

B.  Triturus dobrogicus

4. Reconstruction and management of habitats

C.  Triturus carnifex

5.  Research on amphibians in Hungary

D.  Ichthyosaura alpestris

A. TAXONOMY

E.  Bombina variegata F.  Rana arvalis

B. ECOLOGICAL STUDIES ON AMPHIBIANS

G.  Rana temporaria

C.  MOLECULAR PHYLOGEOGRAPHY

III. Conservation measures and monitoring programmes A. Role of NGOs in protection of amphibians

D.  CHYTRIDIOMYCOSIS IN HUNGARY

IV. Conclusions V. Acknowledgements VI. References

Abbreviations and acronyms used in the text and references: Bd CB DAPTF ECNE EU MME mtDNA NGO NP SEH SSC UTM

Batrachochytrium dendrobatidis Carpathian Basin Declining Amphibian Populations Task Force Expertise Centre for Biodiversity and Sustainable Development European Union Hungarian Ornithological and Nature Conservation Society mitochondrial deoxyribonucleic acid non-governmental organization National Park European Herpetological Society Species Survival Commission Universal Transverse Mercator (a type of map)

100 Amphibian Biology

I.  Introduction Hungary, located in Central-Eastern Europe, lies in the Carpathian Basin and covers most of the Pannonian Biogeographical Region. This bioregion is a discrete unit with the following characteristics: Geomorphology: The topography consists of lowlands of 200–500 m above sea level surrounded by mountains up to 2,000 m high. A few mountains of low elevation emerge on the northern edge (Northern Middle Range, Transdanubian Middle Range), western border (Alpine foothills), and southern border (Mecsek Hills). Climate: Three climatic zones (Sub-mediterranean, Oceanic and Continental) converge in this region. Vegetation: This biogeographic region lies at the conjunction of two main vegetation zones – Broadleaved Forest and Forest-steppe. Zoogeography: The region has elements of Alpine, Carpathian, and Mediterranean biotas (Varga 1995; Illyés 2004; Varga 2009). The evolution of species in the Carpathian Basin was strongly influenced by the formation of the Danube catchment area as well as by the retreat of the Pannonian Inland Sea (Kovács et al. 2006; Vörös et al. 2006; Varga 2009; Vörös and Arntzen 2010). The Carpathian Basin has one of the highest biodiversities of Europe (Williams et al. 1999; Varga 2009). Due to the overlap of different climatic zones, during the Quarternary climatic fluctuations the region served as glacial refugia for several animal species (Varga 2009), including ectothermic vertebrates such as amphibians, e.g. the moor frog and the common newt (Babik et al. 2004, 2005). For this reason, most of the amphibian species inhabiting the Carpathian Basin show high genetic diversity, in many cases with an east-west split partitioned by the Danube river (Babik et al. 2004, 2005; Vörös et al. 2006; Vörös and Major 2007). The Hungarian amphibian fauna can be characterized by three groups of species: (1) species living in isolated montane populations in the low mountains of Hungary, separated from the main range of the species in the Carpathians or the Alps (Salamandra salamandra; Ichthyosaura alpestris; Triturus carnifex; Bombina variegata; Rana temporaria); (2) typical lowland species (Triturus dobrogicus; Rana arvalis; Pelobates fuscus; Bombina bombina; Pelophylax ridibundus; P. lessonae; P. kl. esculentus); and (3) widely distributed species occupying lowlands as well as hilly areas (Lissotriton vulgaris; Bufo bufo; Bufotes viridis; Hyla arborea; Rana dalmatina).

A.  The history of habitat destruction in Hungary

In Hungary, as globally, the most important factors leading to population decline of amphibians are destruction, alteration, and fragmentation of habitats, pollution of the environment, and the increasing impact of human activities. Information about the country-wide distribution of the 17 amphibian species was recorded only over the past few decades, while long-term monitoring and data on population biology are available only from about the past ten years. The most dramatic habitat losses affecting Hungary’s amphibian fauna occurred during the nineteenth century. This period is called “the noisy habitat loss”. In the mid nineteenth century, Hungary began intensive regulation of rivers in order to develop shipping potential, to prevent floods, and to integrate its floodplains into agriculture. Due to these actions, the hydrography of Hungary changed significantly. Regulation of the two main rivers (Danube and Tisza), drying of marshes and swamps, as well as prevention of regular floods, resulted in the loss of 97% of Hungary’s wetlands. The remaining area of forest cover, after the development of the Carpathian Basin, is estimated at 40–60%. At the beginning of the nineteenth century, forest cover remained at 30%; during the twentieth century it shrank to 11.8% and now only 7% of the country is forested. Within the European Union, the area



Conservation and Decline of Amphibians in Hungary101

for agricultural use is 41% on average, while in Hungary it is 62%. Seventy-eight percent of the agricultural land is arable land and 17% is grassland. Beginning in the middle of the twentieth century, arable areas became dominated by large monocultures with significant initial use of chemical fertilizers. In addition, agricultural ownership of farming structures and land were transformed following the change of the communist regime. Although the use of chemical fertilizers decreased significantly due to lack of funds, many previously unused areas that had been taken over by nature were farmed anew. In the past few decades, there has been a slow destruction of the remaining wetlands, forests, and grasslands that were suitable for hibernation and foraging for amphibians. This period could be called “the silent habitat loss”. The construction of roads and highways disconnected remaining amphibian populations and created barriers between their hibernation and breeding sites. Greenfield investments of industrial facilities and the expansion of residential areas at the expense of green areas have decreased the number of potential habitats even further. The use of EU funds has resulted in the initiation of projects that altered habitats, and will lead to an increase in the level of human disturbance in the long-term (ecotourism; changes in usage of water). The agricultural policy of the European Union had a dual impact. The effect of the EU-funded agri-environmental programmes proved to be positive as these support environment-friendly production, including the conversion of arable lands into grasslands, and the creation of wetlands. On the other hand, the EU-funded Single Area Payment Scheme (SAPS) had a negative impact as it facilitated the conversion of areas previously abandoned for up to several decades, and providing adequate feeding or hibernation sites for amphibians, into arable lands. The Hungarian amphibian fauna has no invasive elements; so far, the introduction of alien species (e.g. Lithobates catesbeianus) has been prevented. However, several alien fish and reptilian species have become established in Hungary; these prey on the tadpoles, larvae, and even adults of native amphibians. Despite all the above risks, in numerous respects the natural state of Hungary in general, and in individual smaller areas, is better than in many other countries of the EU. Table 50.1 List of amphibian species present in Hungary with a summary of their status. Hungarian Common Protection Status Name in Hungary

Population Sizes and Trends

Salamandra salamandra

Foltos szalamandra

Protected

Stable in general, locally decreasing

Needed

At some localities

Triturus carnifex

Alpesi tarajosgőte

Strictly Protected

Stable in general, locally decreasing

Needed

At all known localities

Triturus dobrogicus

Dunai tarajosgőte

Protected

Stable in general, locally decreasing

Needed

At some localities

Ichthyosaura alpestris Alpesi gőte

Protected

Stable in general, locally decreasing

Conservation At some plan available localities

Lissotriton vulgaris

Pettyes gőte

Protected

Common

Not necessary

No surveys

Bombina bombina

Vöröshasú unka

Protected

Very different population sizes

Not necessary

At some localities

Bombina variegata

Sárgahasú unka

Protected

Small local populations

Needed

At some localities

Pelobates fuscus

Barna ásóbéka

Protected

With large population sizes at some localities

Not necessary

At some localities

Bufo bufo

Barna varangy

Protected

Common

Not necessary

At some localities

Scientific Name

Action Plan

PopulationLevel Survey

102 Amphibian Biology

Scientific Name

Hungarian Common Protection Status Name in Hungary

Population Sizes and Trends

Bufotes viridis

Zöld varangy

Protected

Common

Not necessary

No surveys

Hyla arborea

Zöld levelibéka

Protected

Common

Not necessary

No surveys

Pelophylax lessonae

Kis tavibéka

Protected

Distribution and population size not known

Not necessary

No surveys

Pelophylax ridibundus Nagy tavibéka

Protected

Common

Not necessary

No surveys

Pelophylax kl. esculentus

Kecskebéka

Protected

Common

Not necessary

No surveys

Rana arvalis

Mocsári béka

Protected

Rare in general, but with significant population sizes at some localities

Needed

At some localities

Rana dalmatina

Erdei béka

Protected

Common

Not necessary

At some localities

Rana temporaria

Gyepi béka

Protected

Stable in general, decreasing in some areas, but spreading in some other areas

Needed

No surveys

Action Plan

PopulationLevel Survey

B.  Legal protection of amphibian species in Hungary

The protection of amphibians (as well as of nature in general) is regulated by Act LIII of 1996 for the protection of the natural environment; this act has been amended and supplemented on several occasions. According to this Act, it is prohibited to disturb, damage, torture, or kill any individual of a protected animal species, or to endanger its breeding or other activity, or to destroy or damage sites it uses for feeding, breeding, resting, or hiding. Permission from the Nature Conservation Authority is required to (1) regulate the stock of protected animal species, (2) collect, capture, kill, own, breed, or mount individuals, (3) own mounted specimens, (4) keep any individual in a collection of living animals, (5) introduce individuals from foreign stands into domestic stands of that animal species, (6) exchange genes artificially between stands, (7) exchange, sell, or purchase its individuals, (8) transfer to, or import from, a foreign country or transport such individuals, or (9) re-introduce or introduce any individual. In Hungary, all species of amphibians are protected, and only one species (Ichthyosaura alpestris) is included in the “Strictly Protected” category (Decree 100/2012 (IX. 28.) VM) (Table 50.1). Designations are only generally defined due to lack of the necessary research and data, even though there are considerable differences in nature conservation value, as expressed in monetary terms. The lists of the European Union‘s Directive 92/43/EEC on the conservation of natural habitats (the Habitats Directive) contain 14 of the Hungarian amphibian species (Table 50.1). This represents almost 78% of the species found in Hungary.

II.  Declining species of amphibians and species of special conservation concern Based on data provided by the 10 national park directorates, of the 17 amphibian species occurring in Hungary, 10 (Lissotriton vulgaris; Bombina bombina; Hyla arborea; Pelobates fuscus; Bufo bufo; Bufotes viridis; Rana dalmatina; Pelophylax ridibundus; Pelophylax lessonae; Pelophylax kl. esculentus) can be considered common and mostly have stable populations countrywide. More attention must be



Conservation and Decline of Amphibians in Hungary103

focused on conservation of the seven species that are rare, or which have an isolated or patchy distribution.

A.  Salamandra salamandra

In Hungary the fire salamander lives in island-like populations in hilly and mountainous areas of the Northern Middle Range and in Western Transdanubia. Data about the distribution of the species have been collected over the past 100 years (Dely 1966; Vörös et al. 2010) but long-term monitoring has occurred only for the past decade. Within the framework of the Hungarian Biodiversity Monitoring System, salamander populations from three regions of Hungary (Őrség-Vendvidék; Aggtelek Karst region; Zemplén Mountains) have been subjected to continuing surveys by Dankovics and Bakó (Kiss et al. 2001, 2002, 2003, 2004, 2005, 2006a, 2007, 2008, 2009, 2011, 2012). Due to the communitybased (not species-based) methods of the monitoring system, the presence of the fire salamander is detected regularly at the survey sites but unfortunately the results do not indicate the population size. Some other attempts by national parks or individual researchers were made to study the species in Hungary. Dankovics (2001, 2002, 2004, 2005, 2006, 2007, 2008) surveyed a salamander population in the Sopron Mountains, Western Transdanubia, between 2001 and 2008 and each year found only 3–10 adult individuals; however, the maximum number of larvae he counted was 844 in 2005. Csilléry and Lengyel (2004) studied the density dependence of S. salamandra larvae in streams in the Aggtelek National Park region and found that larvae responded to high density by increasing their body length. Vörös et al. (unpublished data) carried out a molecular phylogeographic study to reveal the genetic pattern of Hungarian salamander populations. Salamandra salamandra was thought to have become extirpated in the past 90 years from the Buda Hills that encircle the city of Budapest. The occurrence of the species was last reported there Fig. 50.1 Distribution of juvenile and adult specimens of Salamandra salamandra in the recently discovered Buda Hills locality in 2010 (Balogh 2012). The animals live around the 500 m section of a slow-flowing stream (blue line) surrounded by family houses. The specimens were located mainly under rocky walls but sometimes appeared in gardens. Blue dots = males; red dots = females; green dots = juveniles.

104 Amphibian Biology

Fig. 50.2 Seasonal activity of a Salamandra salamandra population in the Buda Hills in 2010 (Balogh 2012). The first activity peak was related to deposition of larve in early spring, and a second activity wave was experienced in the autumn, presumably related to breeding. Each successful observation was made during or after rain.

in 1918 by Lajos Méhely and it was not subsequently detected (Méhely 1918). At the end of 2008, however, a new population was discovered on the outskirts of Budapest, in a cool, afforested valley, surrounded by buildings, in and around a watercourse near the Buda Landscape Protection Area (Szelényi et al. 2010; Vörös et al. 2010). Since then, the population has been surveyed intensively; its habitat has been mapped, a mark-recapture study initiated, and population genetic studies carried out (Balogh 2012; Vörös et al. 2011a,b; Kiss et al. 2013). Within the first 3 years more than 700 individuals were identified with a 17% recapture rate (Figures 50.1, 50.2). Another unknown population was found in 2010 in the Pilis-Visegrádi Mountains (Vörös et al. 2010). The main factors threatening S. salamandra populations are disappearance and alteration of habitats, and desiccation of the streams suitable for larval development. Several observations prove that where clean water bodies are lacking, salamanders tend to use polluted waters, temporary ponds, or even wallows for depositing larvae. For the protection of the species in Hungary the most important step would be the conservation of breeding sites of the small, isolated populations in the Buda Hills, Pilis-Visegrádi Mountains, and Naszály area.

B.  Triturus dobrogicus

Hungary covers most of the Pannonian range of Triturus dobrogicus so that this country is responsible for conservation of the largest population (30–50%) of the Danube crested newt (Puky 2000; Arntzen et al. 2009). The distribution of the species in Hungary is mainly associated with the Danube, Tisza, and Drava river drainages and their tributaries, but it can be found in lakes and channels with relatively permanent water in lowlands and hilly areas (Vörös and Major 2007). Gubányi et al. (2010) recently summarized and compared the previously published data and recently recorded locality records of the species in Hungary and concluded that in the past 30 years, T. dobrogicus has disappeared from several breeding sites due to drying of the habitat or because of construction by humans. The number of identified localities of the Danube crested newt has increased significantly in the past decade due to Natura 2000-related projects, the Hungarian Biodiversity



Conservation and Decline of Amphibians in Hungary105

Fig. 50.3 Maximum number of newts among sampling occasions in a given year (diamonds and black line) and average number of newts/successful sampling occasion (squares and grey line) within ten years during the Triturus carnifex survey at Pityerszer locality in Őrség National Park. The number of newts increased from 2001 to 2007 and slightly dropped in 2008, but the population seems to remain stable (based on surveys by Dankovics, unpublished). The similar pattern of the two datasets suggests that both sampling methods are adequate for detecting similar tendencies.

Monitoring System, and increased monitoring efforts in the ten national parks, but knowledge about the precise range of the species is still far from complete. The main threat to this species is habitat fragmentation (Vörös et al. in prep.) and the disappearance of breeding sites (Puky et al. 2005). The population dynamics and habitat use of Triturus dobrogicus was investigated at the breeding site near the town of Hatvan (Deák et al. 2012). The results showed that even a small, isolated water body surrounded by agricultural land can serve as refugia for significant newt populations. Molecular studies based on analyses of allozymes and microsatellites showed that gene-flow is high among Pannonian populations (Vörös and Arntzen 2010), but higher along the Tisza River than along the Danube River (Vörös et al. in prep.). This process may be caused by the strong regulation of the Danube that can hinder migration of newts. Until recently, T. cristatus was considered to be a member of the Hungarian amphibian fauna. It was believed to be distributed in the Northern Mountain Range in norteastern Hungary (Puky et al. 2005). Vörös and Major (2007) studied mitochondrial ND2 fragments and 7 microsatellite loci at 22 localities throughout the country and proved that pure T. dobrogicus populations occur in the whole of Hungary, except at the western border with Austria where T. carnifex lives. Triturus cristatus is represented only by a hybrid population in the Aggtelek Karst region, where Hungarian populations of T. dobrogicus meet the southern border of the distribution of T. cristatus in Slovakia. These results were confirmed by Mikuliček et al. (2004), who showed that the closest population to this hybrid locality (Domica) is a mixed T. dobrogicus-like population. Hybridization between T. dobrogicus and other species of crested newts has been detected at contact zones (Wallis and Arntzen 1989).

C.  Triturus carnifex

The populations of T. carnifex in Hungary represent the northeastern border of the species‘ distributional range. In Hungary the occurrence of the species is well mapped; it occurs only in Western Transdanubia in the Alpine foothills covering six UTM squares (10 x 10 km) (Gubányi et

106 Amphibian Biology

Fig. 50.4 The most suitable period for sampling Triturus carnifex populations is shown according to the surveys carried out between 2001 and 2007 in the framework of the Hungarian Biodiversity Monitoring System. The number of individuals shown are pooled numbers, regardless of year. The black stripe indicates the most suitable period for sampling (based on surveys by Dankovics, unpublished).

al. 2010). In 1998, a specimen was found in the Kőszegi Mountains (Tartally et al. 2001) that was later identified by molecular analyses as a hybrid (Vörös, unpublished). Triturus carnifex usually occupies permanent or temporary bodies of still water, but sometimes breeds in streams or slowly moving rivers (Puky et al. 2003). It often can be found in artificial waters in gardens, or in sand-pits with little or no vegetative cover. Monitoring of T. carnifex populations has been carried out during the past ten years within the frame of the Hungarian Biodoversity Monitoring System (Figure 50.3). As the surveys show, the best season for monitoring Triturus carnifex is from the end of March through mid-May. This was taken into consideration when sampling events were scheduled. Due to variation in microclimatic conditions of the survey areas, however, the most suitable periods for monitoring may vary (Figure 50.4). The surveys suggest that T. carnifex has low population sizes in Hungary. Threats to the survival of the species are the eutrophication, succession, desiccation, and destruction of breeding sites (e.g. via pollution and introduction of fish). Some of the breeding ponds are located near tourist destinations (e.g. the village museum of Pityerszer) that negatively affect newt populations. Terrestrial habitats have been destroyed by construction of roads and parking lots, thereby causing fragmentation of populations. In the past few years, several known breeding sites of T. carnifex have been reconstructed, and new sites have been created in the area of the Őrség National Park. Soon after the sites were established, newts occupied the ponds. Most of the breeding sites are located on private lands that are maintained by the owners, but some of them are still filled with mud and require ongoing management.

D.  Ichthyosaura alpestris

The alpine newt occurs in five isolated mountane populations in Hungary and is one of the rarest amphibian species in the country (Bakó and Korsós 1999). It is found in Őrség-Vendvidék, Bakony



Conservation and Decline of Amphibians in Hungary107

Fig. 50.5 Changes in population size of Ichthyosaura alpestris in the Grajka stream valley, Szakonyfalu, Őrség National Park. The target study site was a dirt road with temporary ponds, but the surrounding area was surveyed as well. From 2001 the number of newts significantly decreased along the road (diamonds and black line), especially from 2008, when fewer ponds were created by tracks, and existing breeding sites were not properly maintained. However, in the surrounding bodies of water, the number of newts increased (squares and grey line) which suggests that the population migrated to different breeding ponds. The low numbers of newts in the past few years were a consequence of dry breeding seasons (based on surveys by Dankovics, unpublished).

Mountains, Mátra Mountains, Bükk Mountains, and Zemplén Mountains (Dely 1967, Molnár et al. 2001). Due to their small area of distribution and small population size, the Hungarian populations are endangered (Molnár et al. 2000). The nominotypical subspecies (I. alpestris alpestris) is found in Hungary. Based on osteological examinations, Dely (1959a) described four new subspecies (Ichthyosaura alpestris bakonyiensis, I. a. bükkiensis, I. a. carpathicus and I. a. sátoriensis) within Hungary but these forms have not been accepted as valid taxa (Gasc et al. 1997; Korsós and Vörös 2004), and recent morphometrical studies have also not confirmed this geographical pattern (Molnár 2001). The species usually can be found above 500 m elevation. Despite the lower elevation of Western Transdanubia (Őrség-Vendvidék), the species is present there because of the cool, alpine climate. Ichthyosaura alpestris favours beech forests where small ponds are used for breeding. It often can be found in bodies of water with no vegetation (e.g. channels; ponds in dirt roads) (Molnár 2001). In the past few decades, mostly faunistic and taxonomic surveys were carried out on this species (Dely 1959a,b, 1960a,b, 1962; Molnár 2001; Dankovics 2003). Lately, within the frame of the Hungarian Biodiversity Monitoring System (Kiss et al. 2001, 2002, 2003, 2004, 2005, 2006a, 2007, 2008, 2009, 2011, 2012) and through individual actions in national parks, significant amounts of data have been collected about the population size of I. alpestris in some regions (Figure 50.5). The most important threats to the species are destruction and desiccation of breeding sites, increasing number of predators (e.g. wild boar; fish), improper wildlife management, and use of forests, tourism, and the spread of technical sports. In the 1990s, some alpine newt populations of the Northern Middle Range suffered serious declines (Szitta 1991, 1995; Molnár 2004); therefore an action plan for the protection of I. alpestris populations was prepared (Kiss et al. 2006b). Following the action plan, two national parks (Őrség

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Fig. 50.6 Changes in number of Rana arvalis in Ócsa wetland area between 2001–2010 (based on surveys by Kiss, unpublished). Diamaonds on thin line = all observed frogs; squares on thin line = number of frogs calculated by the egg clutches; thick line = observed and calculated number of frogs combined.

and Bükk National Park) have started reconstruction of habitat to conserve alpine newt populations in Hungary.

E.  Bombina variegata

The yellow-bellied toad occurs in Hungary in island-like populations in the low mountains of the Northern Middle Range, the Transdanubian Middle Range, the hilly ranges in southeastern Transdanubia, and the foothills of the Western Transdanubian Alps (Szabó 1956, 1960; Solti and Varga 1988; Dankovics 1995; Dely 1996; Marián 1998; Gubányi 1999; Vörös 2008). This species favours temporary ponds, but sometimes can be found around streams. The yellow-bellied toad is active from early April through mid-October. The distribution of the species in Hungary is relatively well-known; however, new findings still can be expected as, in 2005, a small isolated population was found in the Pilis-Visegrád Mountains close to Budapest (Kiss et al. 2005). The populations of B. variegata are surrounded by those of B. bombina in the lowlands, and hybridization of the two species occurs in several regions. Hybridization between the two Bombina species has been reported since the early twentieth century, based on morphological (Méhely 1904; Sipos 1986; Dely 1996; Vörös et al. 2002), bioacoustical (Hock et al. 2010) and molecular (Gollmann et al. 1986; Gollmann 1987; Vörös et al. 2006) evidence. Szymura et al. (2000) described two well-differentiated sister mtDNA lineages (differing by 4.7–5.2% of their mtDNA nucleotides) within B. variegata. Vörös et al. (2006) confirmed that populations of both mtDNA lineages are present in Hungary. Bombina variegata from the Northern Middle Range belong to the Carpathian clade, and populations from the Transdanubian Middle Range, hilly ranges in southeastern Transdanubia, and the Western Transdanubian Alpine foothills are of Alpine origin (Vörös et al. 2006). The Danube River seems to be the barrier between the two lineages within the Carpathian Basin, except in the case of the



Conservation and Decline of Amphibians in Hungary109

Pilis-Visegrád Mountains where the newly discovered population, despite its Transdanubian position, has a Carpathian origin (Vörös 2007). The yellow-bellied toad is protected by law in Hungary. It is not threatened at a national level but some of the small populations need special conservation, and management of breeding sites is necessary for the long-time survival of the species (Puky et al. 2005). Due to the drying of temporary ponds, there is a regular loss of tadpoles (Péchy and Haraszthy 1997). Long-term monitoring of the species has been carried out in three regions of the country: Őrség, Aggtelek (Kiss et al. 2001, 2002, 2003, 2004, 2005, 2006a, 2007, 2008, 2009, 2011, 2012) and Bakony (Vörös 2007, 2008a) mountains. In the past few years, country-wide surveys of the amphibian chytrid fungus, Batrachochytrium dendrobatidis, showed that Bombina variegata is one of the affected species. Presence of the chytrid fungus on B. variegata was proved in six out of seven surveyed regions populated by the species (Balaž et al. 2013). Although high prevalence (56%) was detected in some of the juveniles in B. variegata populations, no sign of infection was noticed on any of the affected individuals and no chytridiomycosis-related population declines has been reported from the affected regions (Vörös et al. 2009). Despite these findings, the population size of B. variegata should be monitored countrywide, and special care taken of the relatively small populations.

F.  Rana arvalis

The moor frog has significant populations in northeastern Hungary along the northern section of the Tisza River, in southern Transdanubia, and along the Drava River, and is present in different corners of the country as small isolated populations. It favours marshes and also swamp forests of the lowlands; some small populations can be found in hilly areas (Puky and Schád 2008). The subspecies Rana arvalis wolterstorffi was described from Hungary (Fejérváry 1919; Dely 1953, 1964). Babik and Rafinski (2000) studied the morphometry of R. arvalis in Central Europe and found no difference in body size between the two subspecies (R. a. arvalis and R. a. wolterstorffi); however, they detected that Hungarian populations differed from the nominal form in relative length of the hind limbs. The morphometric differentiation was not concordant with the genetic (allozyme) pattern that showed a northern-southern separation in Central Europe (Rafinski and Babik 2000). Babik et al. (2004) inferred the phylogeography of R. arvalis and found high diversity of mtDNA within the Carpathian Basin. They recognized three divergent haplotype groups, of which two occur in Hungary. Considering the complex, discordant pattern of morphology, nuclear genetic markers, and mtDNA, the taxonomic status of the Hungarian populations should be revised and should have a high priority for conservation. The greatest threat for the species is the desiccation of swamps and marshes. Significant population decline was reported in the Ócsa wetland area (Péchy and Haraszthy 1997) and was confirmed by long-term monitoring of the Hungarian Biodiversity Monitoring System (Kiss et al. 2001, 2002, 2003, 2004, 2005, 2006a, 2007, 2008, 2009, 2011, 2012). In the past few years, low rainfall at the end of winter has resulted in low reproductive success in many populations. Population size further decreased because of fewer frogs surviving to maturity and laying eggs (Figure 50.6). Dankovics (2001, 2002, 2004, 2005, 2006, 2007, 2008) surveyed a R. arvalis population in Figurák, Lébény, Fertő-Hanság National Park between 2000 and 2008 and recorded the number of adults, juveniles, and egg clutches. He observed a high number of egg clutches (5,000) in 2001 but then the population collapsed due to an increasing population of wild boars and an extremely dry season. In 2011 he detected only 50–100 clutches. Because of the decreasing number of breeding sites and the increasing number of predators (wild boars; storks; herons), local protection of populations of this species is necessary.

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Fig. 50.7 Changes in population size of Rana temporaria at Hársas Lake, Szentgotthárd-Máriaújfalu, Őrség National Park between 2001 and 2010. Although the number of frogs and egg clutches showed significant fluctuations over periods of three years, the population has still been growing (based on surveys by Dankovics, unpublished). Diamonds = all observed frogs; squares = number of frogs calculated by the egg clutches; triangles = observed and calculated number of frogs combined.

G.  Rana temporaria

In Hungary, the common frog occurs in island-like populations at low elevations in the mountains of Western Transdanubia, the Pilis Mountains, and the Northern Middle Range. It favours cool and humid valleys and mountain meadows. Vági et al. (2013) surveyed the breeding characteristics of ten amphibian species in the Pilis Mountains and found that occurrence of Rana temporaria was positively related to mixed hornbeam-oak forest, beech forest, and depth of ponds. There is very little population-level information about the species in Hungary; most data are derived from road kills and amphibian rescue actions at roads (Puky 1989). Within the framework of the Hungarian Biodiversity Monitoring System, four regions of Hungary have been surveyed in the past ten years (Őrség-Vendvidék, Pilis Mountains, Aggtelek Karst, and Zemplén Mountains) (Kiss et al. 2001, 2002, 2003, 2004, 2005, 2006a, 2007, 2008, 2009, 2011, 2012). Among the four regions, the most significant population was found at Hársas Lake in Szentgotthárd-Máriaújfalu, Őrség National Park (Figure 50.7). Threats to this species are destruction and desiccation of breeding sites, as well as cessation of flooding and disappearance of cut-off meanders due to the decreasing volumetric flow from springs. The first occurrence of the amphibian chytrid fungus, Batrachochytrium dendrobatidis, on Rana temporaria was described from the Pilis Mountains (Vörös et al. 2009). The specimen that later tested positive for Bd was collected in July 2004 and showed no sign of infection (Hettyey, personal communication). The distribution and abundance of Bd in the Pilis Mountains are not mapped but no population decline has been observed in the region, which suggests that the species might only carry the desease.

III.  Conservation measures and monitoring programmes A.  Role of NGOs in protection of amphibians

NGOs have been involved in herpetology in Hungary since the first conservation organizations were formed. Regional surveys, often with publication or description of unique phenomena as a



Conservation and Decline of Amphibians in Hungary111

Fig. 50.8 Sites of amphibian surveys in Hungary.

final result, are the most typical activities they carry out. However, since the 1980s, the activity of NGOs has developed gradually in three directions. They promote conservation of nature in general and the designation of sites of special interest, as well as the conservation of amphibian populations and assemblageas through active management. Especially since 2000, amphibian rescues at road crossings have become relatively frequent, including 25–30 sites every year with several independent groups organizing these activities. Research (in most cases local surveys) is another activity of NGOs, and has resulted in the production of the national herpetological atlas of Hungary organiszd by Varangy Akciócsoport Egyesület (Puky et al. 2005). The third area in which amphibian-oriented NGOs are active is education. There are diverse activities ranging from traditional methods such as talks, children‘s competitions, in some cases with participation from other Carpathian Basin countries (Végváriné Pongrácz et al. 2001), production of information brochures on the local herpetofauna (Andrési 2011), and frog concerts, i.e. interactive scientific programmes with frogrelated music and literature (Puky and Lukács 2008). In the best projects, such as the international award-winning International Salamander Year organized by Varangy Akciócsoport Egyesület, all these elements are combined and they mutually enchance each other. By 2010, there were some herpetological sections of larger NGOs in Hungary engaged in conservation of amphibians, as well as entire NGOs specifically founded for that purpose. This suggests that public participation will increase in the coming decades, likely in co-operation with other organizations, such as zoos. One of the most popular organizations focusing on conservation of amphibians is the Amphibian and Reptile Conservation Group of the MME/Birdlife Hungary that was founded in 1993. The group aims to collect data about the distribution of Hungarian amphibians and reptiles, conduct species conservation programmes, and coordinate local population surveys; these activities will involve a large number of volunteers (www.khvsz.mme.hu).

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Fig. 50.9 Average number of amphibian species during the 10 years of surveys at 16 sites in the framework of the Hungarian Biodiversity Monitoring System (Kiss et al. unpublished).

B.  Mapping the Hungarian herpetofauna

The description of amphibian distribution has long been the topic of Hungarian herpetologists (e.g. Méhely 1904; Fejérváryné-Lángh 1943; Dely 1967). Their publications, however, either describe the fauna of a smaller area (e.g. Szabó 1956, 1960; Marián 1966, 1968; Solti and Varga 1981; Marián 1988, 1998; Dely 1990; Dankovics 1995; Hegyessy 2006) or discuss the national or Carpathian Basin distribution of a single species (e.g. Dely 1964, 1966; Schäffer and Purger 2005; Vörös 2008; Gubányi et al. 2010; Vörös et al. 2010). The joint project between the Hungarian Natural History Museum and five national parks resulted in significant progress towards mapping the distribution of Hungarian species of amphibians. Owing to this cooperation, the herpetofauna was described by Dely (1981, 1987, 1996) for the Hortobágy NP, Bükk NP, and Kiskunsági NP, by Gubányi (1999) for the Aggtelek NP, and by Gubányi et al. (2002) for the Fertő-Hanság NP. The first modern, 10 km x 10 km UTM square-based mapping project was launched by the MME/Birdlife Hungary in 1988. Based on approximately 3,200 records, Bakó (1992) and Bakó and Korsós (1999) compiled UTM atlases for the country and suggested a system for evaluating species according to their distribution. In 2001 the Amphibian and Reptile Conservation Group started a new survey to collect data using considerably smaller units (2.5 km x 2.5 km UTM square units) (Péchy 2001). Péchy and Haraszthy (1997) increased interest in amphibians by publishing a herpetological book oriented toward conservation and including European distribution maps. Recently, a web-based mapping project was introduced by the Amphibian and Reptile Conservation Group of MME/Birdlife Hungary, that made it possible for both volunteers and specialists to upload their observations about the amphibian and reptilian species of Hungary (herpterkep.mme.hu). The project offers different data interfaces for “basic” and “advanced” users, and the data are validated by a scientific committee before being used for scientific or conservational purposes. The project started in April 2011 and within 3 years received nearly 17,000 records. The data were provided for the mapping project of the European Herpetological Society (SEH); in the case of two species



Conservation and Decline of Amphibians in Hungary113

Fig. 50.10 Cumulative number of individuals for the 16 observed species plus Bombina hybrids between 2001 and 2006 at 6 study sites (Őrség-Vendvidék; Pilis-Visegrádi Mts.; Ócsai-turjánvidék; Gödöllői-dombság; Kardoskút; Aggteleki Karst) (Kiss et al. unpublished). Abbreviations: S. sal = Salamandra salamandra; B. vir. = Bufotes viridis; T. car. = Triturus carnifex; T. dob. = Triturus dobrogicus; B. var. = Bombina variegata; R. tem. = Rana temporaria; T. alp. = Ichthyosaura alpestris; P. fus. = Pelobates fuscus; H. arb. = Hyla arborea; B. bom. = Bombina bombina; R. arv. = Rana arvalis; B. hybr. = Bombina hybrids; P. rid. = Pelophylax ridibundus; L. vul. = Lissotriton vulgaris; P. kl. esc. = Pelophylax kl. esculentus; R. dal. = Rana dalmatina; B. buf. = Bufo bufo.

(Salamandra salamandra and Hyla arborea) the “Herptérkép” project works in conjunction with “Vadonleső”, a wide-scale governmental education project of the Ministry for Rural Development, founded in 2009 and focusing on easily recognizable protected and Natura 2000 species (www. vadonleso.hu). Varangy Akciócsoport Egyesület, also serving as IUCN/SSC Declining Amphibian Populations Task Force (DAPTF) Hungary, launched its intensive herpetofaunal mapping project in 2001 which, expressed in 10 km x 10 km UTM squares, resulted in a database of more than 16,000 records from 96.2% of Hungary, published in the form of a herpetological atlas for Hungary in 2005 (Puky et al. 2005). By 2011, this database grew to nearly 30,000 records representing each 10 km x 10 km UTM square. Other attempts involving the general public are being made to collect distributional data for Hungarian amphibian species, e.g. the photography grant by the Varangy Akciócsoport Egyesület (www.varangy.hu), whereby pictures accompanied by dates of observation and description of sites in Carpathian Basin can be sent in for determination (Tóth and Puky 2012).

C.  Amphibian rescue actions

There is an insufficient number of frog tunnels under busy roads at many Hungarian localities; therefore amphibian rescue actions are needed. These actions are mainly organized by national park directorates, but several NGO‘s and numerous volunteers actively participate in saving frogs from road kill. Some of the locations have a long history of amphibian rescues, such as Hont (since 1987), Farmos (Danube Ipoly National Park), or Fertőboz-Hidegség (Fertő-Hanság National Park).

114 Amphibian Biology The majority of amphibian rescues take place in the administrative areas of the Danube-Ipoly and Bükk National Park Directorates. About 35 rescue events are organized each year, but this number might be an underestimation as several small NGO‘s initiate such actions without involving the media or registering their activities. The location of the rescues are shown in Figure 50.8. In the past few years several frog tunnels have been constructed due to EU-funded projects (Faggyas and Puky 2012; Mechura et al. 2012).

D.  Frog tunnels

Routes of animal migrations initially were not taken into consideration when construction of roads and motorways began in Hungary. The number of motorways increased rapidly in the 1980s and so far there are 1,300 km of motorways, approximately 7,000 km of primary and secondary roads, and 23,000 km of regional and local roads fragmenting the country. New construction of motorways is now subject to environmental impact assessment in order to designate the most appropriate locations for animal tunnels (Kovács et al. 2010) but on many primary and secondary roads the tunnels are established only after the roads have been built. Some of these post hoc constructions have led to problems due to improper design or construction or to lack of maintenance (Puky 2003; Puky and Vogel 2004). Several EU-funded projects helped national parks install new frog tunnels. According to estimations, at least 140 frog tunnels function under roads and motorways in Hungary, and several others are under construction. Some of these tunnels also facilitate the crossing of other vertebrate groups (Puky et al. 2007). The use of tunnels by amphibians along three motorways was examined by Kovács et al. (2010).

E.  Monitoring programmes 1.  Hungarian biodiversity monitoring system Herpetological studies of the past 100 years focused primarily on faunistic surveys and did not provide information about changes in species composition or population size. In 2001, a biodiversity monitoring system was started that aimed to conduct long-term, assemblage-level surveys on amphibians and reptiles. The project was coordinated by the Ministry of Environment and Water (now Ministry for Rural Development). The intent of this long-term monitoring system between 2001 and 2013 was to survey a certain sampling unit and collect data about the species, such as stage of development, sex, and number of individuals, characteristics of the site, and the threats facing them. The standardized methodological protocol (Kiss et al. 2007) was revised periodically. In 2011, a new protocol system based on species-level monitoring was set up for Salamandra salamandra (Bakó et al. 2011), Triturus carnifex (Dankovics and Kiss 2011b), Triturus dobrogicus (Dankovics and Kiss 2011a), Bombina bombina (Vörös 2011b), Bombina variegata (Vörös 2011a), Rana temporaria (Kovács 2011), and Rana dalmatina (Kovács 2011). With the coordination of the ministry, monitoring started at 2–6 sites of 5 national park directorates (Őrség; Danube-Ipoly; Balaton Uplands; Aggtelek; Körös-Maros) in 2001, but the number of surveyed sites has increased continously and, in 2010, 41 sites were already being studied (Figure 50.8). Some of the national park directorates were able to join the monitoring project or to increase the number of studied sites from their own budget (Danube-Dráva; Balaton Uplands; Fertő-Hanság). For monitoring newts, funnel-trapping has proved to be the most efficient method. It is timeconsuming but cost-efficient. For the rest of the amphibian species, visual observations were made during the day, or at night using torches. Five to seven sampling occasions were completed that mainly occured during the breeding season of amphibians. When surveying breeding adults was not possible, counting egg clutches was a good complementary method for estimating population size (Rana temporaria; Rana dalmatina; Rana arvalis). Counts of egg clutches were carried out only when that procedure did not damage the habitat. The protocol did not support identification of



Conservation and Decline of Amphibians in Hungary115

tadpoles because of damage caused by handling the animals. It was suggested only for species for which presence-absence could not be detected any other way. The experiences of the twelve years of monitoring showed that data from one or a few years are not enough to characterize a region's species diversity. In certain areas, the number of detected species was not changed by involving new study sites, but at sites that have been surveyed for ten years the number of detected species increased with time (Figure 50.9). Long-term monitoring is necessary for the detection of rare species. The most common species were Lissotriton vulgaris, Hyla arborea, and Pelophylax spp. Except in one case, Bufo bufo, Bufotes viridis, Pelobates fuscus, and Rana dalmatina occurred on every study site. Bufo bufo was observed in the highest numbers (Figure 50.10). The practice and results gained from the long-term amphibian monitoring (e.g. seasonal activity of species) have already provided an important basis for several conservation projects in Hungary.

2.  Survey of Natura 2000 species The project “Preparation of monitoring system according to Birds Directive (79/409/EK) and Habitats Directive (92/43/EK)” (2006/018–176–02–01) aimed to make a comprehensive analysis of the distribution of three amphibian species of importance to the community, Triturus carnifex, Triturus dobrogicus, and Bombina bombina, and to confirm their presence on the basis of empirical research in ten Natura 2000 sites in Hungary. The survey was performed in ten national park directorates in 2008 (Figure 50.8). The study focused in particular on recent taxonomic revisions. In addition to the data presented in the National Report of 2006, required by Article 17 of the Habitat Directive, there is a considerable amount of published and unpublished data on the distributions of the species studied. On the basis of these published and unpublished data and the results of our surveys, the distribution maps were redrawn on a UTM grid. While distributional data for T. carnifex covered two UTM squares in the National Report of 2006, the present survey indicated a distribution of six UTM squares. Triturus dobrogicus could be found in 18.6% of the 1,045 UTM squares of the country (coverage of 26.3%), while Bombina bombina appeared in 663 (~84%) UTM squares (Puky et al. 2004; Gubányi et al. 2010). The other goal of the project was to provide methodology and guidelines for a long-term monitoring of these species in the field in order to enable Hungary to comply with its obligations under the EU's Birds Directive and Habitat Directive. Funnel-trapping was used as the standard method for Triturus dobrogicus and for Bombina bombina; visual observations in daylight were conducted. Visual observations using torches at night and, in the case of B. bombina, acoustic observations, were used as supplementary methods. The two methods gave different results in different habitats; use of these methods in parallel is suggested for demonstrating the presence of these species and for the estimation of their population sizes. Both methods are suitable for collection of quantitative data. Acoustic observation, however, is suitable only for detecting the presence of a particular species, but should be used in parallel with the other methods. All data on the 4,500 observed individuals of the three species were entered into the Hungarian Nature Conservation Information System Database (Kiss et al. 2010).

3.  Monitoring of Caudata The Bureau for Nature Conservation of the Ministry of Environment and Water (now Ministry for Rural Development) initiated systematic monitoring of caudates in every national park directorate in Hungary. The surveys were carried out by rangers. Funnel-trapping was used as the standard method for capturing Triturus dobrogicus, T. carnifex, Ichthyosaura alpestris, and Lissotriton vulgaris. The action led to several new observations regarding the distribution of Hungarian Caudata, and was appropriate for determining presence/absence of newts, but did not provide population-level results.

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4.  Reconstruction and management of habitats Very few data are available on the local protection of Salamandra salamandra populations. Kiss et al. (2013) reported significant losses of larvae due to heavy rainfall in the newly discovered population at Buda Hills. Mortality of larvae could be reduced by forming small artificial pools along the section of river used by salamanders for breeding. Several successful projects designed for the protection of Ichthyosaura alpestris have been carried out over the past few years. Existing breeding sites were surveyed, cleaned, and refilled with water, and new breeding ponds were built. The Bükk National Park Directorate has taken special care in managing the breeding sites of I. alpestris over the past 15 years (Balogh 1992; Salétli 1999; Molnár 2001). Breeding ponds were cleaned (e.g. Pisztrángos Lake in the Mátra Mountains, Jávorkúti Lake in the Bükk Mountains) and ponds with threatened populations were fenced (Jávorkúti Lake). It is well known that temporary puddles in wheel tracks provide a suitable environment for several amphibian species. In these, however, significant mortalities can occur when forestry operations resume, thus destroying established amphibian populations. In Őrség National Park and Bükk National Park, artificial ponds were created next to the road and I. alpestris were relocated to the new sites. These ponds were monitored regularly and re-migrating individuals were captured and relocated again. After the serious drought in 2000, the Őrség National Park Directorate created several artificial ponds for amphibians. After the first year Ichthyosaura alpestris, Lissotriton vulgaris, Triturus carnifex, and Bombina variegata had successfully occupied the ponds. In Ócsa wetland, which is inhabited by one of the most significant populations of Rana arvalis in Hungary, in order to save the species, the channel system that encompasses the area, has been modernized. In order to create breeding habitats for Rana temporaria, meanders of the Ménes-völgyi streambed were cleared in the Aggtelek National Park.

5.  Research on amphibians in Hungary A.  TAXONOMY Besides the above-mentioned taxonomic studies on Ichthyosaura alpestris, the Triturus cristatus superspecies, Bombina species, and Rana arvalis (Fejérváry 1919; Dely 1953, 1964; Sipos 1986; Molnár 2001; Vörös et al. 2002), and other significant works on the taxonomy of newts (Bolkay 1910, 1911, 1927, 1928), Pelophylax species have been the main target of herpetological research in Hungary for a considerable length of time. Bolkay (1907) discussed the validity of P. ridibundus as a distinct species, Dely and Stohl (1972) investigated the interspecific hybrid P. kl. esculentus. Gubányi (1990, 1992), Gubányi et al. (1992), and Gubányi and Korsós (1992) carried out a complex study on the genetic composition and distribution of the P. kl. esculentus complex. Tunner and Tunner (1992) and Tunner and Kárpáti (1997) described a new population system of the P. kl. esculentus complex from Hungary between the Neusiedler See and the Danube. In the past ten years, with the increased availabilty of molecular methods, amphibian taxonomic research in Hungary has turned to characterization of the native fauna with the help of genetic markers. Genetic differentiation was revealed within the country in Bombina bombina and B. variegata (Vörös et al. 2006), Triturus dobrogicus (Vörös and Major 2007), Bufo bufo (Recuero et al. 2012), Salamandra salamandra (Vörös et al. 2011), and Ichthyosaura alpestris (Vörös and Szabó 2013). The Bombina variegata populations representing the two ancient mitochondrial lineages were studied in combination with bioacoustic and morphological methods (Hock et al. 2010).

B.  ECOLOGICAL STUDIES ON AMPHIBIANS Only a few population-level studies have been conducted on amphibians in Hungary. Kiss and Laár (1992) investigated the changes in population size of a Bufo bufo population in the Babat area.



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Kiss and Nagy (1997) and Kiss (1999) studied how tadpole development in Bufo bufo and Rana dalmatina is influenced by inconstant water levels. Muraközy and Kiss (2006) investigated alteration of the breeding characteristics of Bufo bufo by weather conditions. Rédly (2003) examined the breeding characteristics and migrating pattern of a Lissotriton vulgaris population in Babatpuszta. Spawning preference of Rana dalmatina was studied by Kecskés and Puky (1992) on the floodplain of the Ipoly River, and the long-term spawning of this species was also investigated along the River Danube (Puky et al. 2006). Breeding biology and habitat use of seven amphibian species (L. vulgaris; B. bombina; B. bufo; R. dalmatina; R. temporaria; P. ridibundus; H. arborea) were studied by Hettyey et al. (2003) in the Pilis Mountains. The migration pattern of amphibians was investigated by Schád et al. (1999) at Naplás Lake, Budapest. Puky and Oertel (1987, 1997) and Simon et al. (2007, 2010, 2012) studied the accumulation of heavy metals by several anuran species in Hungary. The effect of road traffic on different amphibian communities was investigated by Puky and Kecskés (1992), Puky (2006), and Puky et al. (2007), with over 20 years of data at the sites studied longest. Amphibian deformities were detected in 12 species (up to 70% frequency in one species, Bombina bombina) by Fodor and Puky (2002), Puky and Fodor (2002), and Henle et al. (2012). Mester et al. (2013) discovered facultative paedomorphosis in T. dobrogicus. Anthony and Puky (2001) and Tóth and Puky (2010a,b) developed, tested, and improved an aural protocol for monitoring amphibians in Hungary. Hettyey and Török (2005) and Hettyey et al. (2009) carried out behavioural/ecological (sperm competition) experiments on Bufo bufo under laboratory conditions. The breeding behaviour of Rana dalmatina was studied by Hettyey et al. (2005). The composition of the diets of the Pelophylax kl. esculentus complex and of Rana arvalis (Lőw and Török 1998), Hyla arborea (Kovács and Török 1997) and eight other amphibian species (Kovács and Török 1992, 1997) were investigated in the Kis-Balaton Nature Protection Area. Hettyey et al. (2010) performed experiments on Rana dalmatina tadpoles to ascertain the antipredator responses induced by direct and indirect cues. Tadpoles of the same species were studied to reveal the strength of phenotypic responses to predators of different qualities (Hettyey et al. 2011).

C.  MOLECULAR PHYLOGEOGRAPHY Numerous studies have shown that the Carpathian Basin (CB) played an important role in Europe‘s biogeography, serving as a glacial refugium for invertebrate and vertebrate animal species (Varga 2009). Due to Hungary‘s transitional geomorphology, climate, vegetation, and zoogeography, several animal species show significant genetic diversity. The molecular phylogeography of the two Bombina species was studied by Vörös et al. (2006), who proposed recent expansion of populations of B. bombina within the CB along the Danube river, the existance of two old mitochondrial lineages of B. variegata within the isolated Hungarian populations, and low divergence between the isolated Transdanubian populations of B. variegata. The phylogeography of Triturus dobrogicus showed low genetic differentiation but high gene-flow among Hungarian populations (Vörös and Major 2007). Bufo bufo seems to have low genetic diversity within the CB but significant genetic structure through it‘s distribution range (Recuero et al. 2012). Molecular phylogeography and population genetic studies on Hungarian populations of Salamandra salamandra and Ichthyosaura alpestris are in progress (Vörös et al. 2011a,b; Vörös and Szabó 2013 respectively).

D.  CHYTRIDIOMYCOSIS IN HUNGARY The chytrid fungus, Batrachochytrium dendrobatidis was first detected in Hungary in 2004 in a specimen of Rana temporaria from the Pilis Mountains (Vörös et al. 2009). Since then the country has been surveyed systematically to reveal the distribution of the pathogen in Hungarian amphibians (Balaž et al. 2013). Out of 12 sampled regions, 7 were found to harbour the fungus (Soproni

118 Amphibian Biology Mountains; Köszegi Mountains; Örség; Bakony Mountains; Pilis Mountains; Mátra Mountains; Zemplén Mountains). The seven infected regions were at low elevations in the Western Hungarian Alpine foothills, Transdanubian Middle Range, and Northern Middle Range. However, Puky et al. (unpublished data) found Bd on the Hungarian Plain. We examined 13 species but only 3 of them (Rana temporaria; Bombina variegata; Pelophylax sp.) carried the disease. Bd was found on Bombina variegata from six regions, and on Rana temporaria and Pelophylax sp. from two regions. The highest prevalence was detected in Bombina variegata in juveniles from the Bakony Mountains, with 50% prevalence in 2009 (Vörös et al. 2009). A long-term survey of this population is under process (Vörös et al. unpublished), but preliminary results show that the pathogen has persisted in the pond and has a high infection rate, e.g. 44% in juveniles (Gál et al. 2012).

IV.  Conclusions Studies on Hungarian amphibians over the past 100 years have focused mainly on distribution and taxonomy. Most Hungarian herpetologists of the past two centuries – Lajos Méhely, GézaGyula Fejérváry, Aranka Fejérváry-Lángh, István Bolkay, Olivér Dely – expended a lot of effort in completing the taxonomic revision of the amphibian fauna, and in mapping distributions of the species. Unfortunately, the amphibian fauna has not been unable to cope with the speed of today‘s man-made changes, and the overall picture of amphibian distribution and population sizes have changed significantly and quickly. Therefore, the legal protection of amphibians has become necessary and, since 1996, all amphibian species are legally protected in Hungary. From the 1980s, herpetological research has turned in a more ecologically based direction, and in the past ten years amphibians have become the subject of evolutionary ecology, molecular systematics, and phylogeographical studies. Meanwhile, knowledge about the distribution of species has been enriched by several local faunistic surveys, modern mapping projects launched by different NGOs, and national monitoring. A deep, regionally based, knowledge of the distribution of species is crucial for research and for efficient conservation and management, and despite the small number of species living in the country it is still far from complete. Future amphibian research in Hungary should focus on (1) mapping the distribution of species, (2) long-term monitoring in order to determine demographic trends of populations and to be able to detect declines, (3) population dynamic studies in order to promote effective management, and (4) investigations of conservation genetics to reveal and maintain genetic diversity in the amphibian populations. In the past, management has prevented introduction of alien amphibian species, but nowadays several factors are threatening our amphibian fauna such as loss and modification of habitat, pollution, introduction of predators (e.g. fish), and diseases (e.g. chytridiomycosis). Therefore effective measures and habitat management are essential for the sustainable survival of the 17 species of Hungary. Nevertheless, the most challenging task is still to understand and recognize the need for basic research to develop effective long-term conservation programmes. Over the past decade, Hungary has made an outstanding effort to implement permanent channels of communication between researchers and policy makers while, at the same time, using recent research findings in shaping and enforcing future conservation policies. It is hoped that this joint effort will secure the future of the native amphibian populations, and at the same time promote the scientific study of the evolutionary processes that are constantly shaping the singular Hungarian biodiversity.



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V.  Acknowledgements We are grateful to Ágnes Gruber, István Szentirmai (ŐNPI), Gábor Takács (FHNPI), Judit Cservenka (BFNPI), Sándor Bérces (DINPI), Éva Kovács (KNPI), Dániel Molnár (DDNPI), Tibor Danyik (KMNPI), András Pozsonyi (BNPI), Attila Huber (ANPI), and Viktor Köbödöcz (HNPI) for providing data on amphibian surveys. Róbert Dankovics, János Farkas, and Tibor Kovács provided significant data and relevant literature, and Gabriella Ritti Simonné provided data on frog tunnels. We thank Olivér Váczi and Botond Bakó (Ministry for Rural Development) for technical help and for comments on the manuscript, and Mario García-París for helpful advice. Special thanks to Judit Cservenka and Zsuzsa Csaba for correcting and translating English. Studies on Bufo bufo, Salamandra salamandra, Ichthyosaura alpestris and chytridiomycosis in Hungary were supported by the Hungarian Research Fund (OTKA K77841 and OTKA K84071) and by the Bolyai János research scholarship of the Hungarian Academy of Sciences to JV.

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Varga, Z., 1995. Geographical patterns of biodiversity in the Palearctic and in the Carpathian Basin. Acta Zooogica Academiae Scientiarum Hungaricae 41: 71–92. Varga, Z., 2009. Extra-Mediterranean refugia, post-glacial vegetation history and area dynamics in Eastern Central Europe. In Relict species: Phylogeography and Conservation Biology, ed. J. Habel and Th. Assmann. Springer-Verlag, Heidelberg. Pp. 57–87. Végváriné Pongrácz, Á., Gémesi, D. and Puky, M., 2001., “Tiszatündérek” – egy komplex környezeti nevelési program módszertana, eredményei és tanulságai” (Tisza fairies” – methodology, result and lessons learned from a complex envvironmental education programme). Civilek a Tiszáért. Nimfea Természetvédelmi Egyesület. Piremont Press, Debrecen. Pp. 160–167. Vörös, J., 2007. “Morphological and genetic studies on Bombina bombina and Bombina variegata in Hungary, focusing on the phylogeography and the híbrid zones formed by the two species”. PhD dissertation. Eötvös Lóránd Tudományegyetem, Budapest [in Hungarian]. Pp. 1–82. Vörös, J., 2008. Distribution of the fire-bellied toad (Bombina bombina Linnaeus, 1761) and yellow-bellied toad (Bombina variegata Linnaeus, 1758) in Hungary. Természetvédelmi Közlemények 14: 45–59 [in Hungarian with English summary]. Vörös, J., 2011a. Sárgahasú unka (Bombina variegata) monitorozása monitorozása. Természetvédelmi Információs Rendszer. Központi protokoll (Monitoring of the yellow-bellied toad (Bombina variegata). Information system of nature conservation. Federal protocol) [in Hungarian]. Pp. 23–27. http://www.termeszetvedelem.hu/_user/browser/File/NBmR/keteltu-hullo Vörös, J., 2011b. Vöröshasú unka (Bombina bombina) monitorozása. Természetvédelmi Információs Rendszer. Központi protokoll (Monitoring of the fire-bellied toad (Bombina bombina). Information system of nature conservation. Federal protocol) [in Hungarian].

130 Amphibian Biology Pp. 18–22. http://www.termeszetvedelem. hu/_user/browser/File/NBmR/keteltu-hullo Vörös, J. and Arntzen, J.W., 2010. Weak population structuring in the Danube crested newt, Triturus dobrogicus inferred from allozymes. Amphibia – Reptilia 31: 339–346. Vörös, J. and Major, Á., 2007. Phylogeograhy and species composition of the two Bombina species and the Triturus cristatus species complex in the Carpathian Basin. In The Origin of the Fauna of the Carpathian Basin, ed. L. Forró L. Hungarian Natural History Museum, Budapest. Pp. 269–282. Vörös, J. and Szabó, K., 2013. Mitochondrial DNA diversity of the alpine newt, Mesotriton alpestris, in the Carpathian Basin. 17 th European Congress of Herpetology. Veszprém, Hungary. Programme and abstracts. Pp. 1–307. Vörös, J., Szalay, F. and Korsós, Z., 2002. A comparative morphological study on the two Hungarian discoglossid toad species Bombina spp. Biota 3: 171–177. Vörös, J., Alcobendas, M., Martínez-Solano, I. and García-París, M., 2006. Evolution of Bombina bombina and Bombina variegata (Anura: Discoglossidae) in the Carpathian Basin: a history of repeated mt-DNA introgression across species. Molecular Phylogenetics and Evolution 38: 705–718. Vörös, J., Dankovics, R., Harmos, K., Dobay, G. and Kiss, I., 2010. Distribution and conservation status of the fire salamander (Salamandra salamandra) in Hungary. Állattani Közlemények 95: 121–149 [in Hungarian with English summary]. Vörös, J., Hettyey, A., Sós, E., Dankovics, R. and Garner, T., 2009. Amphibian chytrid fungus in Hungary. Second European Congress of Conservation Biology, abstract book. Pp. 1–105. Vörös, J., Szabó, K., Kiss, I., Schweiger, S. and Jelic, D., 2011. Genetic structure of Salamandra salamandra in the Carpathian Basin. 16th European Congress of Herpetology, Luxembourg and Trier. Abstract book. Pp. 1–68.

Wallis, G.P. and Arntzen, J.W. 1989. Mitochondrial-DNA variation in the crested newt superspecies: limited cytoplasmatic gene flow among species. Evolution 43: 88–104. Williams, P., Humphries, C. and Araújo, M., 1999. Mapping Europe‘s biodiversity. In Facts and Figures on Europe‘s Biodiversity, State and Trends 1998–1999, ed. B. Delbaere. Expertise Centre for Biodiversity and Sustainable Development (ECNC), Tilburg. Pp. 12–20.

51 Conservation and declines of Amphibians in Bulgaria Nikolay Dimitrov Tzankov and Georgi Sashev Popgeorgiev I. Introduction A.  Species list and recent changes

III. Conservation measures and monitoring programmes

B.  Species’ distribution and richness

IV. Conclusions

II. Amphibian declines and species of special conservation concern

V. Acknowledgements VI. References

Abbreviations and acronyms used in the text and references: asl

above sea level

I.  Introduction A.  Species list and recent changes

A total of 19 amphibian species was listed by Stojanov et al. (2011) for the Bulgarian batrachofauna. Another three species are now also recognized: Pelophylax bedriagae (Camerano, 1882), P. lessonae (Camerano, 1882) and P. kurtmuelleri (Gayda, 1940), the latter very recently by Lukanov et al. (2013). The specific status of Lissotriton graecus (Wolterstorff, 1906) is still controversial. This taxon was elevated to specific status by Dubois and Raffaëlli (2009), but that decision was questioned by Speybroeck et al. (2010) on the grounds that the molecular data presented by Babik et al. (2005) recognized a contact zone between this species and L. vulgaris (Linnaeus, 1758) (sensu stricto), although the mitochondrial DNA of the closer species L .montandoni (Boulenger, 1880) was fully introgressed by that of the latter; thus, this demonstrates that it cannot be an argument against its status as a species. From the point of view of conservation policy, the specific status of L. graecus is more plausible as this taxon was included in the national Red Data Book of Bulgaria as vulnerable (VU). A new specific name for the eastern taxon of the T. karelinii group, replacing T. arntzeni Litvinchuk, Borkin, Džukić, and Kalezić, 1999 was proposed by Wielstra et al. (2013) – T. ivanbureschi (Wielstra and Arntzen, 2013). The species Hyla orientalis Bedriaga, 1890 mentioned for Bulgaria by Frost (2013), seems to have a contact zone with H. arborea in Bulgaria, as they co-occur in close proximity in Eastern Serbia and northeastern Greece (Stöck et al. 2012). Both taxa were recorded via bioacoustic research that is still in process (unpublished data). Finally, the generic name Bufotes Rafinesque, 1815 has been assigned to the green toads and even if the species B. viridis (Laurenti, 1768) was listed for Bulgaria (Stojanov et al. 2011; Frost 2013), the species B. variabilis (Pallas, 1769) seems also to be present. This taxon has already been confirmed for neighbouring countries – Greece and Turkey (Stöck et al. 2006; Van Bocxlaer et al. 2009). Additionally, there are two further taxa with subspecific status and local distribution – L. vulgaris schmidtleri (Raxworthy, 1988) and Salmandra salamandra beschkovi Obst, 1981 (for which the name S. s. werneri Sochurek and Gayda, 1941 seems to be more appropriate). Taking into consideration all these recent changes, the total number of amphibian species present in Bulgaria has risen to 25 or 27 taxa in total. This represents 29% of the European total of 85 species

132 Amphibian Biology (Temple and Cox 2009) and slightly more than 80% of the Balkan Peninsula’s batrachofauna. This high biodiversity is determined by the large-scale variability of Bulgarian natural habitats and by the palaeoclimatic and paleogeographic conditions during the last glaciation cycle during the Holocene. Table 51.1 Bulgarian amphibian species grouped according to their distribution. Kind of Distribution

Species

Distributed on a large scale

Lissotriton vulgaris, Triturus ivanbureschi, Bufo bufo, Bufotes viridis/ variabilis, Hyla arborea/orientalis, Rana dalmatina, Pelophylax ridibundus

Distributed over a large geographic region or regions

Salamandra salamandra, Bombina bombina, B. variegata, Pelobates fuscus, P. syriacus, R. temporaria

Distributed over a medium-sized geographic region or regions

Triturus dobrogicus, Ichthyosaura alpestris, Rana graeca, Pelophylax kl. esculentus

Confined to a small geographic region or regions

Lissotriton graecus, Triturus cristatus, T. macedonicus, Pelophylax bedriagae, P. kurtmuelleri, P. lessonae

Table 51.2 Conservation status, chorological types, and origin of Bulgarian amphibian species (L = local; SW = southwest; W = west; SE = southeast; E = east) and elevational range. When available, subspecific attribution has been stated in order to present more precise chorology. Abbreviations: BDA = Biological diversity act of Bulgaria (Annexes II, III, and IV). 92/43 = Council Directive 92/43/ EEC of 21 May 1992 of the Conservation of Natural Habitats and of Wild Fauna and Flora (Annexes II and III). Bern = Bern Convention (Appendices II and III). RDB = Red Data Book of the Republic of Bulgaria. IUCN = International Union for Conservation of Nature with categories (in columns RDB and IUCN) of LC (Least Concern), NT (Near Threatened) and VU (Vulnerable). Origin: L = local; SW = southwest; W = west; SE = southeast; E = east. Min = minimal elevation in m asl. Max = maximal elevation in m asl. Species

BDA

Ichthyosaura alpestris carpathica

III

Lissotriton graecus

III

Lissotriton vulgaris vulgaris

III

92/43

Bern

RDB

IUCN

Chorotype

Origin

Min Max

III

VU

LC

Balcano-Carpathian

L

873

2453

South-Balkanian

SW

106

1385

European

L

2

1854

Balcano-Anatolian

SE

–

–

European

L

100

2350

South-Balkanian

SW

280

1050

VU III

LC

Lissotriton vulgaris schmidtleri Salamandra salamandra salamandra

III

III

LC

Salamandra salamandra werneri Triturus cristatus

II, III

II, IV

II

VU

LC

European

L

154

1382

Triturus dobrogicus

II, III

II

II

VU

NT

Ponto-Panonnian

L

2

40

Triturus ivanbureschi

II, III

II, IV

II

LC

Balcano-Anatolian

SE

2

1800

Triturus macedonicus

III

II, IV

II

LC

South-Balkanian

SW

–

1650

Bombina bombina

II, III

II, IV

II

LC

Ponto-European

E

0

450

Bombina variegata scabra

II, III

II, IV

II

LC

Balkanian

L

45

2100

Pelobates fuscus

III

IV

II

LC

European

L

0

730

Pelobates syriacus balcanicus

III

IV

II

LC

Balcano-Anatolian

SE

0

600

Bufo bufo

III

III

LC

Europo-Anatolian

L

0

2000

Balcano-Westasiatic

E

–

–

Bufotes variabilis Bufotes viridis

III

IV

II

LC

European

W

0

2300

Hyla arborea

III

IV

II

LC

European

W

0

2300

Easteuropo-Westasiatic

E

–

–

LC

Anatolo-Caucasian

SE

2

595

LC

European

L

2

203

LC

South-Balkanian

SW

93

160

Hyla orientalis Pelophylax bedriagae Pelophylax kl. esculentus Pelophylax kurtmuelleri

IV

V

III



Conservation and Declines of Amphibians in Bulgaria133 Species

BDA

Pelophylax lessonae Pelophylax ridibundus

IV

Rana dalmatina

92/43

Bern

IUCN

Chorotype

Origin

Min Max

IV

III

RDB

LC

European

L

10

29

V

III

LC

European

L

0

2000

IV

II

LC

Europo-Anatolian

L

2

2000

Rana graeca

III

IV

III

LC

Balkanian

SW

129

1800

Rana temporaria

IV

V

III

LC

European

L

250

2505

B.  Species’ distribution and richness

The amphibian species present in Bulgaria can be assigned to four groups according to the extent of their distribution (Table 51.1). Species from the first group have a large-scale distribution across the country, being common from lowland areas to middle elevations in the mountains. Those belonging to the second group are in turn divided into two groups – species that are distributed in mountainous and hilly regions of the western, central, and southern part of the country (Salamandra salamandra, Bombina variegata, and Rana temporaria) and species distributed typically in the plains and lowlands (B. bombina, Pelobates syriacus, and P. fuscus – the latter found only in northern Bulgaria and on the Sofia Plain). In the third group, Ichthyosaura alpestris and R. graeca are confined to mountains (R. graeca only in the south-southwestern part) whereas T. dobrogicus and P. kl. esculentus live in lowlands along the Danube River and Durankulak Lake on the northern Black Sea coast (P. cf. kl. esculentus also occurs sporadically along the southern Black Sea coast). Those from the fourth group have limited distribution and are restricted to the southwesternmost areas (L. graecus, T. macedonicus, and P. kurtmuelleri), to the northwestern part of the country (T. cristatus), to the north-central region (P. lessonae), and the southeastern area (P. bedriagae).

Fig. 51.1 E levational distribution of the amphibians in Bulgaria. White bars indicate the upper range of the optimal elevation.

134 Amphibian Biology

Fig. 51.2 Amphibian species richness in ETRS 10 x 10 km grid cells.

According to chorological, biogeographic, and phylogeographic attribution, the Bulgarian amphibian fauna can be assigned to eleven chorotypes. Assignments of species’ status, chorotype, origin, and elevational range, amended after Stojanov et al. (2011) are presented in Table 51.2. Species richness strongly correlates with elevation; up to 500 m asl 21 species are present, 17 between 500 and 1,000 m asl, 14 between 1,000 and 1,500 m asl, 13 between 1,500 and 2,000 m asl, and only 6 between 2,000 and 2,500 m asl (Figure 51.1). When combining the available phylogeographic and palaeogeographic data, the present-day amphibian fauna can be assigned to three main groups. The largest is the local Balcanic group that includes 13 species probably having their glacial refugia in the country. Two smaller groups consist of seven species whose refugia were confined to the southwest/west or to the southeast/east with their post-glacial routes passing through the country or ending within the country (Table 51.2). To estimate geographic patterns of species richness, species occurrences according to Stojanov et al. (2011) with some additional data were plotted on the European (ETRS) 10 x 10 km² grids format (Figure 51.2). Regions with the highest number of species per grid cell are concentrated along the Danube River (Figure 51.3a), isolated regions related to wetland along the Black Sea coast (Figure 51.3b), along the river Maritsa in central Bulgaria or along the river Struma in southwestern Bulgaria and certain grids in the western mountainous part of the country (Figure 51.3c). In contrast, the regions with the lowest species richnesses are the highest parts of mountains, approximately above 2,000 m asl and the regions of Ludogorieto and Dobrudja in the northeast.



Conservation and Declines of Amphibians in Bulgaria135

II.  Amphibian declines and species of special conservation concern Mass agricultural activities and the deforestation of the lowlands, draining of the large inner country marshes, large-scale stocking, and industrial and urban pollution of water have affected amphibians heavily at a national level. In the lowlands of northern Bulgaria, species with declining populations are: L. vulgaris, T. cristatus – found in the country only in 2005 (Tzankov and Stojanov 2008) – T. dobrogicus, B. variegata, P. fuscus, P. syriacus, and P. lessonae. All these species are confined to small or medium-sized ponds. The last species was cited only for Lake Srebarna by Beschkov (1965) and not confirmed there by recent studies (Biserkov and Naumov 2012; personal observations). Recently P. lessonae was found near the town of Oryahovo by means of bioacoustic studies (unpublished data). This species seems to be affected strongly by afforestation along the Danube River and by the large-scale replacement of indigenous riparian forests by poplar plantations that support extremely low amphibian species diversity. In the high plains in western Bulgaria, especially the Sofia Plain, a significant decline of P. fuscus populations has been observed in recent decades, being confirmed in two of the five known localities. In the Thracian Plain, B. bombina populations are strongly declining due to intensive agriculture and to intensive collection of specimens in the region. The species is now present mainly in rice plantations and in highly fragmented natural or semi-natural habitats. Of the montane species, I. alpestris has a highly fragmented distribution and, even if a list of new locations were found during the past decade, the species would still be highly vulnerable and it deserves special conservation measures. Other mountane species are less affected but large-scale afforestation with coniferous trees accompanied by deforestation of native trees has a strong negative impact on their populations throughout the country. Local problems include the draining of bodies of water by private owners (e.g. the pond in Figure 51.3c was destroyed in 2008 but later has been recovering naturally) and their over-use by domestic animals (Livade, Slavianka mountains – until now the only known locality of T. macedonicus in the country).

III.  Conservation measures and monitoring programmes Historically, Bulgarian environmental legislation has developed in rate and scope similarly to other European legislation. At a relatively early stage, in 1931, the first protected area was established (Silkosia Reserve at Mt. Strandza), in 1934 the first natural park in the Balkan Peninsula was created (Vitosha), and in 1936, Bulgaria adopted the first legislation specifically dedicated to natural protection. Much later, in 1991, an Act for the protection of the environment was adopted, which has been amended repeatedly and was completely revised in 2002 as the Biological Diversity Act, wherein a list of protected species, including amphibians, was adopted. After joining the European Union in 2007, the categories are now equivalent to those of the Habitats Directive 92/43/EEC (Table 51.2). Currently, the network of protected areas, including National Parks (3), Nature Parks (10), Reserves (55), Maintained Reserves (35), Natural Landmarks (457), and Protected Localities (175) covers 5% of the national territory. The only specially designated protected area for the conservation of amphibians is Muhalnitsa Pond (1.9 ha) that protects a breeding site for R. temporaria, a species that undergoes one of the longest targeted breeding migrations in the world: 10 to 10.5 km (Beshkov and Angelova 1981; Beshkov 1988). The Bulgarian Natura 2000 sites network covers 34.34% of the territory of Bulgaria. Six amphibian species have high priority for conservation in Natura 2000 protected zones – T. cristatus, T. dobrogicus, T. ivanbureschi, T. macedonicus, B. bombina, and B. variegata. The first edition of the Bulgarian national Red Data Book (1985) was a first attempt towards focused protection of amphibians, although this document has no administrative power. This edition included only two

136 Amphibian Biology

Fig. 51.3 Habitats with greatest amphibian species numbers: a) wetlands along the Danube River – Srebarna lake (12 species): Lissotriton vulgaris, Triturus dobrogicus, Bombina bombina, Pelobates fuscus, Pelobates syriacus, Bufotes variabilis/viridis, Bufo bufo, Hyla arborea/orientalis, Rana dalmatina, Pelophylax kl. esculentus, Pelophylax lessonae, Pelophylax ridibundus; b) wetlands along the Black Sea coast – Arkutino lagoon marsh (11 species): Lissotriton vulgaris, Triturus ivanbureschi, Bombina bombina, Pelobates syriacus, Bufotes variabilis/viridis, Bufo bufo, Hyla arborea/orientalis, Rana dalmatina, Pelophylax bedriagae, Pelophylax cf. kl. esculentus, Pelophylax ridibundus; c) inner-country medium to small wetlands at lower elevations in the mountains – ponds and nearby small springs at Mt. Osogovo near v. Novo selo (11 species): Ichythyosaura alpestris, Lissotriton vulgaris, Triturtus ivanbureschi, Salamandra salamandra, Bombina variegata, Bufo bufo, Hyla arborea/orientalis, Rana dalmatina, Rana graeca, Rana temporaria, Pelophylax ridibundus.

species – I. alpestris and P. syriacus. The second edition (Golemanski 2011) listed four species of newts – L. graecus, I. alpestris, T. cristatus, and T. dobrogicus. Taking into account projects completed by the governmental and non-governmental organizations on habitat restoration, natural protection, and faunal research (including amphibians), a large list of mainly indirect conservation activities could be listed. Among these, the most important are the establishment of the Natura 2000 network and subsequent mapping project (2011/2012) of the priority species. During this project, large amounts of field data on faunistics, biology, and ecology were collected. Another important national initiative is the implementation of the National Biodiversity Monitoring System (NBMS), a comprehensive mechanism for long-term study and a summary of the changes in Bulgarian biodiversity. The system is managed by the Executive Environment Agency (ExEA). Six amphibian species are covered – I. alpestris, T. dobrogicus, B. bombina, P. fuscus, P. syriacus, and R. graeca, all of which were included since the preparatory period



Conservation and Declines of Amphibians in Bulgaria137

(2005–2006). A set of 13 polygons was designated for these species during the second period (2010/2011). This network will be optimized and an additional number of polygons added in the third period (2013/2014) to complement the polygons situated in and outside the Natura 2000 zones. All data collected are stored in a national database in ExEA, while the assessments are carried out at regional level by internal substructures such as Regional Inspectorates of the Environment and Waters (RIEW), or by other organizations like the Bulgarian Academy of Science (BAS). In the next period (2014–2020) a network of polygons for monitoring the priority species, as well as species covered by NBMS, will be implemented at a national level. Another important means of protecting amphibians is the management of places included in the Ramsar Convention. So far in Bulgaria, 11 Ramsar sites have been declared. Within the project “Life for the Bourgas Lakes supported by the financial instrument of the EU LIFE + Nature and Biodiversity”, a National Plan for the conservation of wetlands in Bulgaria from 2013 to 2022 has been proposed. It includeds threats and special measures for the protection of amphibians in the wetlands. Twenty-five further wetlands that are not listed as Ramsar sites, but meet one or more of the criteria, are proposed for further declaration. Since 1996, the Wild Nature Association “Balkans” has been taking care of the restoration and protection of the Dragoman Marshland – the largest karst swamp (350 ha) in Bulgaria and an important place for the southernmost population of P. fuscus and some other amphibian species.

IV.  Conclusions Although the general status of amphibian populations in Bulgaria seems to be stable for most of the species at a national level, this group does suffer from human pressures. Habitat destruction causes alteration, fragmentation, and isolation of the populations and this issue has become very topical with the mass execution of infrastructure projects throughout the country. Pollution and contamination of water are of fundamental importance for amphibian population declines. These are threats that are still not assessed adequately. Additionally, chytridiomycosis, an emerging disease which has caused amphibian declines elsewhere in Europe (overall summary by Whittaker and Vredenburg 2011), has still not been studied fully in the eastern part of the continent. Climatic change is another underestimated factor that will affect amphibians globally (Corn 2005; Heatwole 2013). The indirect effects of global warming, such as the availability of water, will likely be more deleterious than the effects of temperature alone (Araújo et al. 2006). Future problems with the effectiveness of already established protected areas and especially the Natura 2000 network (as the largest one) will be very relevant (Araújo et al. 2011). A series of action plans should be adopted in order to adequately respond to current, as well as predicted, future threats.

V.  Acknowledgements Special thanks to our colleagues and friends (listed in alphabetic order) Andrey Stojanov, Borislav Naumov, and Yurii Kornilev, and many others for their company and unforgettable moments in the field.

138 Amphibian Biology

VI.  References Araújo M.B., Thuiller W. and Pearson R.G., 2006. Climate warming and the decline of amphibians and reptiles in Europe. Journal of Biogeography 33: 1712–1728. Araújo, M.B., Alagador, D., Cabeza, M., NoguésBravo, D. and Thuiller, W., 2011. Climate change threatens European conservation areas. Ecology Letters 14: 484–492. Babik, W., Branicki W., Crnobrnja-Isailovic, J., Cogălniceanu, D., Sas, I., Olgun, K., Poyarkov, N.A., Garcia-Paris, M. and Arntzen, J.W., 2005. Phylogeography of two European newt species – discordance between mtDNA and morphology. Molecular Ecology 14: 2475–2491. Beschkov, V., 1965. Über das Vorkommen des Teichfrosches (Rana esculenta L.) in Bulgarien. Bulletin de l’Institut de Zoologie et Musée, Sofia 19: 45–54 [in Bulgarian; German summary]. Beshkov, V., 1988. The greatest periodic migration in the amphibian world. Priroda 37 (3): 4–29. Beshkov, V. and Angelova, B., 1981. One unusual breeding migration of the European common frog (Rana temporaria L.). Ekology 8: 34–42. Biserkov, V. and Naumov B., 2012. Changes after 1948 in the habitats of amphibians and reptiles in the area of the Srebarna lake biosphere reserve. In Ecosystems of the Biosphere Reserve Srebarna Lake, ed. Y. Uzunov, B. Georgiev, E. Varadinova, N. Ivanova, L. Pehlivanov and V. Vasilev. Professor Marin Drinov Academic Publishing House, Sofia. Pp. 163–183. Corn, P.S., 2005. Climate change and amphibians. Animal Biodiversity and Conservation 28: 59–67. Dubois, A. and Raffaëlli J., 2009. A new ergotaxonomy of the family Salamandridae Goldfuss, 1820 (Amphibia, Urodela). Alytes 26: 1–85. Frost, D.R., 2013. Amphibian Species of the World: An Online Reference. Version 5.6 (1 January 2013). Electronic Database accessible at http://research.amnh.org/herpetology/ amphibia/index.html. American Museum of Natural History, New York, USA. Golemanski, V., 2011. Red Data Book of the Republic of Bulgaria. Animals. Joint edition of

the Bulgarian Academy of Sciences and Ministry of Environment and Water, Sofia. Heatwole, H., 2013. Worldwide decline and extinction of amphibians. In The Balance of Nature and Human Impact, ed. K. Rohde. Cambridge University Press, Cambridge. Chapter 18 (pp. 259–278). Lukanov, S., Tzankov N. and SimeonovskaNikolova D., 2013. A comparative study of the mating call of Pelophylax ridibundus (Pallas, 1771) and Pelophylax kurtmuelleri (Gayda, 1940) from syntopic and allotopic populations. Journal of Natural History, available at: http://dx.doi.org/10.1080/002229 33.2013.791942 Speybroeck, J., Beukema W. and Crochet P.-A., 2010. A tentative species list of the European herpetofauna (Amphibia and Reptilia) – an update. Zootaxa 2492: 1–27. Stöck, M., Moritz, C., Hickerson M., Frynta, D., Dujsebayeva, T., Eremchencko, V., Macey, J.R., Papenfuss, T.J. and Wake, D.B., 2006. Evolution of mitochondrial relationships and biogeography of Palearctic green toads (Bufo viridis subgroup) with insights into their genomic plasticity. Molecular Phylogenetics and Evolution 41: 663–689. Stöck, М., Dufresnes, C., Litvinchuk, S.N., Lymberakis, P., Biollay, S., Berroneau, M., Borzée, A., Ghali, K., Ogielska, М. and Perrin, N., 2012. Cryptic diversity among Western Palearctic tree frogs: Postglacial range expansion, range limits, and secondary contacts of three European tree frog lineages (Hyla arborea group). Molecular Phylogenetics and Evolution 65: 1–9. Stojanov, A., Tzankov, N. and Naumov, B., 2011. Die Amphiben und Reptilien Bulgariens. Chimaira, Frankfurt am Main. Temple, H.J. and Cox N.A., 2009. European Red List of Amphibians. Office for Official Publications of the European Communities, Luxembourg. Tzankov, N. and Stoyanov, A., 2008. Triturus cristatus (Laurenti, 1768): A new species for Bulgaria from its southernmost known localities. Salamandra 44: 153–162.



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Van Bocxlaer, I., Biju, S.D., Loader, S.P. and Bossuyt, F., 2009. Toad radiation reveals into-India dispersal as a source of endemism in the Western Ghats-Sri Lanka biodiversity hotspot. BMC Evolutionary Biology 9: 131. Wielstra, B., Litvinchuk, S.N., Naumov, B., Tzankov, N. and Arntzen, J.W., 2013. A revised taxonomy of crested newts in the Triturus karelinii group (Amphibia: Caudata: Salamandridae), with the description of a new species. Zootaxa 3682: 441–453. Whittaker, K. and Vredenburg V., 2011. An Overview of Chytridiomycosis. AmphibiaWeb: Information on amphibian biology and conservation [web application]. Berkeley, California: AmphibiaWeb. Available at: http:// amphibiaweb.org/.

52 Amphibian conservation and decline in Turkey Kurtuluş Olgun and Nazan Üzüm I. Introduction

Lyciasalamandra fazilae

A.  Causes of species richness in Turkey

Lyciasalamandra flavimembris

B.  The amphibian species of Turkey

Lyciasalamandra luschani

II. Declining Turkish amphibians and species of special conservation concern

Mertensiella caucasica Neurergus strauchii

A.  Declining amphibian species in Turkey

Neurergus crocatus

B. The reasons for amphibian decline in Turkey

Rana holtzi

C. Amphibian species of special conservation concern in Turkey

Rana tavasensis

Lyciasalamandra billae Lyciasalamandra antalyana Lyciasalamandra atifi

III.  Conservation measures required IV. Summary V. References

I. Introduction A.  Causes of species richness in Turkey

Turkey, especially Anatolia, is a country of high floral and faunal diversity. The main reasons for the species diversity in Turkey are its geographical location and large area. These have combined to produce a variety of different geographical conditions, resulting in the formation of a wide variety of ecological environments, and consequently high species diversity. On the other hand, Anatolia also possesses mountain chains that play important roles as zoogeographical barriers. One of the most important barriers in Turkey is the Anatolian Diagonal (Davis 1971). It consists of an interrupted chain of mountains running diagonally from the Erzurum-Kars Plateau in the northeast toward the Amanos and Taurus mountains in the south and divides Anatolia into eastern and western portions that differ in environmental conditions and geological history. Botanists and zoologists both accept that this topographical feature has played an important role in the diversification of the Anatolian fauna and flora (Ekim and Güner 1986; Çıplak et al. 1993, 1996; Gülkaç and Yüksel 1999; Özkurt et al. 2002; Çıplak 2003, 2004, 2008; Rokas et al. 2003). It divides the biota of Anatolia into eastern and western elements, especially in taxa with limited capacity for movement and with low ecological valences. This mountainous region served as a centre of speciation. The evolutionary differentiation of many living groups arose as a result of isolation by these barriers, especially during glacial and post-glacial periods.

B.  The amphibian species of Turkey

In Turkey, class Amphibia has two orders, Caudata and Anura, collectively with 7 families: Salamandridae (18 species), Bombinatoridae (1), Bufonidae (4), Hylidae (2), Pelobatidae (1), Pelodytidae (1), and Ranidae (7), for a total of 34 species (Table 52.1). Thirteen species are endemic to Turkey and three to the general region.



Amphibian Conservation and Decline in Turkey141

Table 52.1 The amphibian species of Turkey and their conservation status according to IUCN categories and criteria. LC = Least Concern; NT = Near Threatened; VU = Vulnerable; EN = Endangered; CR = Critically Endangered. For definitions of Red-List criteria, see IUCN (2014). Species

Red List Category

Lissotriton vulgaris

LC

Red-List Criteria

Endemism

Lyciasalamandra antalyana

EN

Lyciasalamandra arikani

DD

B1ab(iii)

Endemic

Lyciasalamandra atifi

EN

B1ab(iii)

Endemic

Lyciasalamandra billae

CR

B1ab(iii)

Endemic

Lyciasalamandra fazilae

EN

B1ab(iii)

Endemic

Lyciasalamandra flavimembris

EN

B1ab(iii)

Endemic

Lyciasalamandra ifrani

DD

Lyciasalamandra luschani

VU

Lyciasalamandra yehudahi

DD

Mertensiella caucasica

VU

B2ab(ii,iii)

Regional Endemic

Neurergus crocatus

VU

B2ab(iii)

Regional Endemic

Neurergus strauchii

VU

B1ab(iii)

Endemic

Ommatotriton ophryticus

NT

Ommatotriton vittatus

LC

Salamandra infraimmaculata

NT

Salamandra salamandra

LC

Triturus karelinii

LC

Bombina bombina

LC

Bufo bufo

LC

Bufo verrucosissimus

NT

Bufotes variabilis

DD

Bufotes viridis

LC

Hyla orientalis

LC

Hyla savignyi

LC

Pelobates syriacus

LC

Pelodytes caucasicus

NT

Pelophylax bedriagae

LC

Pelophylax caralitanus

NT

Pelophylax ridibundus

LC

Rana dalmatina

LC

Rana holtzi

CR

Rana macrocnemis

LC

Rana tavasensis

EN

Endemic

Endemic B1ab(iii)

Endemic Endemic

B2ab(iii)

Regional Endemic Endemic

B2ab(iii,iv)

Endemic

B1ab(iii)+2ab(iii)

Endemic

142 Amphibian Biology

II.  Declining Turkish amphibians and species of special conservation concern A.  Declining amphibian species in Turkey

Many amphibian populations in Turkey are endangered for various reasons and serious declinies are evident. Studies of their ecology are lacking but are urgently needed. No amphibian species in Turkey have become extinct recently. However, 2 of 34 species were categorized as Critically Endangered (CR) according to the criteria of the IUCN Red List (IUCN 2014). One of these species, Lyciasalamandra billae (Akyarlar Salamander) occurs only in a very restricted area (about 15 km2). Although the habitat of this species is not under direct pressure from humans, a forest fire could cause a decline or even extinction. In addition, increasing touristic activities, especially in forested areas, and unsustainable commercial harvesting are now additional, important threats for this species. Another CR species, Rana holtzi (Taurus Frog), is endemic to the Bolkar Mountains of Central Anatolia and has one of the smallest distributional ranges of all the Western Palearctic amphibians. Within this small region it is patchily distributed. Until 2007 it was known only from two lakes, Karagöl and Çinigöl, at elevations of 2,500–2,600 m (Baran et al. 2007); however, the distributional range was extended by the discovery of another population at Eğrigöl (16 km southeast of Karagöl) in Çamlıyayla/Mersin at an elevation of 3,000 m. The introduction of predatory fishes (e.g. carp) into the lakes in the 1990s and overcollection for scientific and other purposes adversely affected the populations of this species for a long time. In recent years, thanks to successful conservation efforts, it has increased in number (Olgun personal observations). Owing to successful conservation efforts and the extension of its distributional range, this species’ Red List status can be changed from Critically Endangered (CR) to Endangered (EN). Five Turkish amphibian species are categorized as Endangered (EN) in the Red List. Four of them belong to the genus Lyciasalamandra and all of them have quite restricted distributions and very local populations. For all species, the major potential threats are habitat loss caused by forest fires, and overcollection for scientific and other purposes. Currently, the population density of humans is low in its distributional range and there is little touristic activity, but with ongoing development in the region, habitat loss could become more severe in the future (IUCN 2014). Another EN species that is totally dependent upon water is Rana tavasensis. It also has a very small distributional range and the densities of its populations are quite low. Four salamandrid species (Lyciasalamandra luschani; Mertensiella caucasica; Neurergus crocatus; Neurergus strauchii) are categorized as Vulnerable (VU) according to IUCN Red list criteria. Lyciasalamandra luschani has a naturally restricted range and a fragmented distribution. There is continuing decline in the extent and quality of its habitat (IUCN 2014). It has the same potential threats as other species of Lyciasalamandra. Mertensiella caucasica is only distributed in northeastern Anatolia in Turkey. It is a habitat specialist and prefers forested areas with small streams. Its distribution is fragmented by road construction and by tourism in summer. In addition, several dams are being constructed on streams and will be major threats for this species (IUCN 2014). Neurergus crocatus is restricted to Beytüşşebap (Şırnak) where its range is fragmented or being lost. Degradation of its habitat from pollution and drought also contributes to its decline. Neurergus strauchii also has a fragmented distribution. In general, this species lives at high elevations where there is a low human population and few threats, but, like N. crocatus, it is declining especially because of degradation of its habitat. From the above information, it is clear that 11 (32.4%) of the 34 species of amphibians in Turkey are under some degree of threat, a fact that emphasizes the need for expanded conservation efforts.



Amphibian Conservation and Decline in Turkey143

B.  The reasons for amphibian decline in Turkey

Of the 18 salamandrid species in Turkey, L. antalyana, L. atifi, L. billae, L. fazilae, L. flavimembris, L. arikani, L. irfani, L. luschani, and L. yehudahi are terrestrial species that do not need any bodies of water for breeding. This feature allows them to adapt successfully to extreme conditions. However, they need calcareous rocks with damp, cool crevices for refuges in hot and dry seasons. The vegetation of their habitat is also very important for their survival. These species are found in quite different environments and particularly prefer open areas that have resulted from overgrazing and cutting; rocky and bushy areas; flat farmlands; the edges of settlements; gardens; and pristine pine forests. Primary measures to ensure their survival include prevention of forest fires, effective control of tourism, and prevention of illegal harvesting for commercial purposes (Franzen et al. 2008). On the other hand, Pelophylax ridibundus is a strongly aquatic species found in lakes, ponds, or slowly flowing streams. Although it is very common in Turkey and no major threats to this adaptable species exist at present, loss of its breeding habitats and illegal collecting for various purposes, especially commercial exploitation (e.g. frog-leg trade) could create serious problems for populations of this species. In addition, while harvesting this species, its habitat generally is destroyed. For this reason, it is necessary to increase awareness of the public, strengthen controls by an authorized board, pass legislation against unauthorized collecting, and impose punishments for infringements of those laws. There are uncertainties about which institutions should intervene against the unauthorized and prohibited collection of specimens, and such uncertainties foster uncontrolled harvesting.

C.  Amphibian species of special conservation concern in Turkey Lyciasalamandra billae (Franzen and Klewen 1987) (Akyarlar Salamander) This species is listed as Critically Endangered (CR) in the IUCN 2014 Red List. It is an endemic species that is restricted to the vicinity of Akyarlar (Antalya) at about 15–230 m asl (Franzen and Klewen 1987; Veith et al. 2001). This habitat is free of frost during winter and has about 800–1,500 mm annual rainfall as in the habitats of other salamanders. These salamanders hide under stones or in the crevices of rocks during the day. Especially in rainy or humid weather, they can be seen at night on the surface of the soil or while climbing on rocks. Above-ground activities, such as breeding or feeding, of L. billae and other salamanders occurs mainly during the rainy winter months between November and March when the air temperature is between 5° and 15°C. However, near the coast these activities continue until April (Franzen et al. 2008). It is almost impossible to see these animals later in the year. However, in favourable weather they can be found on the surface or close to the surface until the beginning of May (Veith et al. 2001). Otherwise, they do not leave their habitats. Moreover, the genus Lyciasalamandra shows nest dependence (Olgun et al. 2001). This species is live-bearing, producing one or two fully metamorphosed young. Its habitat is somewhat remote from human influences but, since it is restricted to a very limited area (approximately 15 km2), it is still under threat (Franzen and Klewen 1987; Veith et al. 2001). The major potential threats are forest fires and increasing touristic activities in their distributional area and it needs protection from over-collection for commercial purposes.

Lyciasalamandra antalyana (Başoğlu and Baran, 1976) (Antalya Salamander) This species is listed as Endangered (EN) in the IUCN 2014 Red List. It is an endemic species. It only occurs in the vicinity of Kedetler (Antalya) with a vertical distribution of 120–650 m (Veith et al. 2001). It has the same ecological features as those of Lyciasalamandra billae. Its habitat is distant from human influences, but, since it occurs only in a very limited area (approximately 35 km2), it is still under threat (Veith et al. 2001). The major potential threats are

144 Amphibian Biology forest fires and increasing touristic activities in its distributional range. In addition, it requires protection from over-collection for commercial purposes.

Lyciasalamandra atifi (Başoğlu, 1967) (Akseki Salamander) This species is classified as Endangered (EN) in the IUCN 2014 Red List. It is an endemic species and its geographic range is limited to the vicinity of Alanya and Akseki (Antalya) at about 190–1,300 m asl (Veith et al. 2001). It has the same ecological features as those of Lyciasalamandra billae. Its habitat is beyond the range of most anthropocentric influences, but, since it occurs only in a very limited area (approximately 110 km2), it is still under threat (Veith et al. 2001). The major potential threats are forest fires and increasing touristic activities in its geographic range. In addition, it needs protection from over collection for commercial purposes.

Lyciasalamandra fazilae (Başoğlu and Atatür 1974) (Lycian Salamander) This species is listed as Endangered (EN) in the IUCN 2014 Red List. It is an endemic species found only in the vicinity of Gökçeovacık, Dalyan, and Üzümlü (Muğla) at about 0–1,000 m asl (Kordges et al. 2005). It has the same ecological features as those of Lyciasalamandra billae. Its habitat is apart from human influences but, since it is confined in a very limited area (approximately 60 km2), it is still under threat (Kordges et al. 2005). The major potential threats are forest fires and increasing touristic activities in its area of occupancy. In addition, it needs protection from over-collection for commercial purposes.

Lyciasalamandra flavimembris (Mutz and Steinfartz, 1995) (Marmaris Salamander) This species is classified as Endangered (EN) in the IUCN 2014 Red List. It is an endemic species distributed only in the vicinity of Marmaris, Ula (Muğla) at about 80–620 m asl (Veith et al. 2001). It has the same ecological features as those of Lyciasalamandra billae. Its habitat is not near human influences, but, since it is found only in a very limited area (approximately 30 km2), it is still under threat (Veith et al. 2001). The major potential threats are forest fires and increasing touristic activities in its geographic range. In addition, it needs protection from over-collection for commercial purposes.

Lyciasalamandra luschani (Steindachner, 1891) (Luschan’s Salamander) This species is listed as Vulnerable (VU) in the IUCN 2014 Red List. It is an endemic species and distributed only in the area between the Eşen River (between Muğla and Antalya) and Finike (Antalya) at about 60–840 m asl (Franzen et al. 2008). It has the same ecological features to those of Lyciasalamandra billae. Its habitat is a bit far from human influences but since it is distributed in a very limited area (approximately 100 km2), it is still under threat (Franzen et al. 2008). The major potential threats are forest fires and increasing touristic activities in their distributional area. In addition, it must be protected from over-collection for commercial purposes.

Mertensiella caucasica (Waga, 1876) (Caucasian Salamander) This species is classified as Vulnerable (VU) on the IUCN Red List 2014. It occurs in northeastern Anatolia (the cities of Ordu Giresun, Rize, Trabzon, Artvin, Kars, Bayburt, and Gumushane), Turkey (Baran and Atatür 1998). Franzen (1985) reported it to be found very close to sea level, based on the larvae from Hopa at 25 m asl. It lives in forests or groves close to streams. Nocturnal in habit, it shelters under stones, logs, or bark by day. Sometimes it enters shallow water (Baran and Atatür 1998). There are very limited data on its biology. It shows activity between March and July, depending on elevation. However, its most active period is between April and June. It needs water for breeding. It can be either oviparous or ovoviviparous according to its habitat.



Amphibian Conservation and Decline in Turkey145

Neurergus strauchii (Steindacher, 1888) (Spotted Salamander) This species is classified as Vulnerable (VU) on the IUCN 2014 Red List. It inhabits suitable biotopes in the vicinity of Muş, Bitlis, and Malatya with a vertical distribution of 1,500–2,000 m. It is a montane form, and lives in cool and continously flowing streams. It spends the winter months on land under suitable stones, or in burrows (Baran and Atatür 1998).

Neurergus crocatus (Cope, 1862) (Urmiye Salamander) This species is classified as Vulnerable (VU) on the IUCN 2014 Red List. It occurs in the vicinity of Beytüşşebap (Şırnak), southeastern Anatolia. It has similar ecological characteristics to those of Neurergus strauchii.

Rana holtzi (Werner, 1898) (Taurus Frog) This species is classified as Critically Endangered (CR) on the IUCN Red List 2014. It is an endemic species and only lives in Akdağ, Tavas (Denizli). At Karagöl and Çinigöl it occurs at elevations of 2,500–2,600 m in the Bolkar Mountains of Central Anatolia and at Eğrigöl (16 km southeast of Karagöl) at an elevation of 3,000 m in Çamlıyayla/Mersin.

Rana tavasensis (Baran and Atatür, 1986) (Tavas Frog) This species is classified as Endangered (EN) on the IUCN Red List 2014. It is an endemic species and only lives in Akdağ, Tavas (Denizli).

III.  Conservation measures required The following conservation activities are needed to protect the amphibians of Turkey in their natural habitats. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.

Fostering public awareness. Preventing uncontrolled construction. Protecting water resources. Preventing habitat destruction. Preventing forest fires. Preventing uncontrolled hunting and harvesting. Promoting organic farming for the protection of natural habitats, especially those containing endangered and endemic species. Providing the effective implementation of legal measures against the removal of amphibian species for export abroad. Realizing research that would ensure keeping regular control of population dynamics, especially for endangered species. As a result of the above, determining necessary measures for ensuring the continuity of the species and checking the application of those measures at regular intervals. Reorganizing existing laws and legislation.

IV. Summary The native amphibian fauna of Turkey consists of 18 caudates and 16 anuran species, including 10 endemic to Turkey and 3 endemic to the region. These species recently were assessed against the IUCN Red List categories of threat and 11 (32.4 %) species (9 caudates and 2 anurans) have been listed as threatened species; 2 of them are categorized as Critically Endangered (CR), 5 amphibian species are categorized as Endangered (EN) and 4 species are listed as Vulnerable (VU) (IUCN 2014). Many amphibian populations in Turkey are endangered for various reasons. Ongoing studies in Turkey have recorded a continuing decline in the extent and quality of amphibians’

146 Amphibian Biology habitats (Kaya et al. 2009). Loss and degradation of habitats are by far the major threats. In addition, unsustainable commercial harvesting for food (especially of ranids such as Pelophylax ridibundus and Pelophylax caralitanus), predation, and introduced fish species are other important threats. The disease chytridiomycosis has been responsible for serious declines almost everywhere that amphibians occur (North, Central, and South America; Australia; Africa; Europe) (Van Sluys and Hero 2010; Heatwole 2013). Although there has been no report on the effect of chytridiomycosis on the amphibian species in Turkey up to now, this disease might be a major cause of declining amphibians in Turkey; monitoring studies for more than three years in the western part of the Aegean region of Turkey revealed serious declines in some caudate and anuran populations (Kaya et al. 2009). For these reasons, conservation measures should include: increased awareness of the public, enforcement of conservation legislation, protection of habitats for amphibians, and protection from unsustainable harvesting.



Amphibian Conservation and Decline in Turkey147

V. References Baran, İ. and Atatür, M.K., 1998. “Turkish Herpetofauna (Amphibians and Reptiles)”. Republic of Turkey Ministry of Environment, Ankara. Baran, İ., Ilgaz, Ç., Kumlutaş, Y., Olgun, K., Avcı, A. and İret, F., 2007. On new populations of Rana holtzi and Rana macrocnemis (Ranidae: Anura). Turkish Journal of Zoology 31: 241–247. Çıplak, B., 2003. Distribution of Tettigoniinae (Orthoptera, Tettigoniidae) bush-crickets in Turkey: The importance of the Anatolian Taurus Mountains in biodiversity and implications for conservation. Biodiversity and Conservation 12: 47–64. Çıplak, B., 2004. Biogeography of Anatolia: The marker group Orthoptera. Memorie della Societa Entomologica Italiana 82 (2): 357–372. Çıplak, B., 2008. The analogy between interglacial and global warming for the glacial relicts in a refugium: A biogeographic perspective for conservation of Anatolian Orthoptera. In Insect Ecology and Conservation, ed. S. Fattorini. Research Sign Post Kerala, India. Pp. 135–163. Çıplak, B., Demirsoy, A. and Bozcuk, A.N., 1993. Distribution of Orthoptera in relation to the Anatolian Diagonal in Turkey. Articulata 8 (1): 1–20., Çıplak, B., Demirsoy, A. and Bozcuk, A.N., 1996. Malatya (Türkiye) Ensifera (Orthoptera, Insecta) faunası. Turkish Journal of Zoology 20: 247–254. Davis, P.H., 1971. Distribution patterns in Anatolia with particular reference to endemism. In Plant life of South-West Asia, P.H. Davis, P.C. Harper and I.C. Hedge. Botanical Society of Edinburgh, Edinburgh. Pp.15–27. Ekim, T. and Güner, A., 1986. The Anatolian Diagonal: Fact or fiction? Proceedings of the Royal Society of Edinburgh 89B: 69–77. Franzen, M., 1985. Mertensiella caucasica (Waga, 1876) (Caudata: Salamandridae) in Meereshöhe. Salamandra 21 (1): 98–99. Franzen, M. and Klewen, R., 1987. Mertensiella luschani billae ssp. n. - eine neue Unterart des Lykischen Salamanders aus SW-Anatolien. Salamandra 23 (2/3): 132–141.

Franzen, M., Bußmann, M., Kordges, T. and Thiesmeier, B., 2008. “Die Amphibien und Reptilien der Südwest-Türkei”. LaurentiVerlag, Bielefeld. Gülkaç, M.D. and Yüksel, E., 1999. Türkiye’deki Spalax Tür ve Alttürlerinin Dağılımına ve Türleşmesine Coğrafik İzolasyonun Etkisi. Turkish Journal of Zoology 23 (Supp. 2): 491–496. Heatwole, H., 2013. Worldwide decline and extinction of amphibians. In The Balance of Nature and Human Impact, ed. K. Rohde. Cambridge University Press. Cambridge. Chapter 18 (pp. 259–278). IUCN, 2014. IUCN Red List of Threatened Species. Version 2014.1. www.iucnredlist.org. Kaya, U., Cox; N., Üzüm, N., Kumlutaş, Y., Avcı, A., Kaska, Y., Öz, M., Tunç, R. and Başkale, E., 2009. Threatened amphibians of Turkey: listing categories, monitoring studies, and conservation status. 15th European Congress of Herpetology, Kuşadası-Aydın/Turkey. Kordges, T.B., Thiesmeier, H., Meinig, H. and Eckstein, H.P., 2005. Beobachtungen am Lykischen Salamander (Mertensiella luschani fazilae) in der Südwest-Türkei. Zeitschrift für Feldherpetologie 12: 111–112. Olgun, K., Miaud, C. and Gautier, P., 2001. Age, size and growth of the terrestrial Salamander Mertensiella luschani in an arid environment. Canadian Journal of Zoology 79: 1559–1567. Özkurt, Ş., Yiğit, N. and Çolak, E., 2002. Karyotype variation in Turkish populations of Spermophilus (Mammalia: Rodentia). Z. Säugetierkunde 67: 117–119. Rokas, A., Atkinson, R.J., Webster, L.M.I., György, C. and Stone, G.N., 2003. Out of Anatolia: longitidunal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gallwasp Andricus quercustozae. Molecular Ecology 12: 2153–2174. Van Sluys, M., and Hero, J.M., 2010. How does chytrid infection vary among habitats? The case of Litoria wilcoxii (Anura, Hylidae) in SE Queensland, Australia. EcoHealth. Veith, M., Baran, İ., Godmann, O., Kiefer, A., Öz, M. and Tunç, R., 2001. A revision of population designation and geographic distribution of Mertensiella luschani (Steındachner, 1891). Fauna in the Middle East 22: 67–82.

53 Conservation of amphibians in Cyprus Petros Lymberakis, Haris Nicolaou, and Konstantinos Sotiropoulos I. Introduction II.  Cypriot amphibians A.  Hyla savignyi (Audouin 1829). Savigny’s Treefrog – lemon-yellow treefrog

C. Pelophylax bedriagae (Camerano 1882). Bedriaga’s frog – Levant water frog

III. Monitoring IV. References

B.  Bufotes viridis (Laurenti 1768). Green toad Abbreviations and acronyms used in the text and references: asl EIFAC

above sea level European Inland Fisheries Advisory Commission

I.  Introduction The Amphibian fauna of Cyprus is poor, comprising only three anuran species. This is to be expected, as Cyprus is an island of (biogeographically) oceanic origin, i.e. it has never been connected to adjacent landmasses (Pavlíček and Csuzdi 2006). This view, however, is equivocal. A main point challenging the hypothesis of complete isolation was presented by Böehme and Wiedl (1994) who noted the very low proportion of endemic or even differentiated forms in the Cypriot herpetofauna; actually there are only five endemic tetrapod species on the island (one snake, one lizard, one mammal, and two birds); see also Poulakakis et al. (2013). The three anuran species, Bufotes viridis, Hyla savignyi, and Pelophylax bedriagae appear to have affinities to populations on the adjacent coasts, especially so with the easternmost Mediterranean. All three species are characterized as Least Concern by the IUCN and are covered under the national law 153/2003 for the protection of the environment. Two species (Bufotes viridis and Hyla savignyi; under Hyla arborea) are included in annex IV of Directive 92/43. Anurans in Cyprus appear to have robust populations. There are problems locally mainly due to the exhaustive use of water. This is counteracted partially by the construction of water reservoirs that are readily colonized, provided they meet certain standards of suitability. Despite the few and cheap measures required for an artificial reservoir to host amphibians (e.g. accessibility; elementary shelters; environmental flow) these are not always achieved, mostly due to lack of information. Moreover, anticipating climatic change and given the history of droughts in Cyprus, the availability of suitable bodies of water for amphibians may be dramatically reduced in the future. Despite the lack of conclusive research specifically targeting the issue, several authors (Blosat 2008 and references therein) suggest that anuran populations suffer heavy predation from introduced, alien fish species either directly (predation of eggs, tadpoles, and/or adults) or indirectly, from herbivorous fish that do not allow the development of aquatic flora as refuges for amphibians.



Conservation of Amphibians in Cyprus149

This has a further impact as several species, such as the endangered snake Natrix natrix cypriaca, depend on anurans as their main food source. An impressive (albeit dated) list of freshwater species introduced into Cyprus (Dill 1990), including several of the worst invasive alien species (Blosat 2008), gives an indication of the magnitude of the problem, which, however, needs to be specifically addressed. Insect control (mainly for mosquitoes) is practiced in Cyprus by spraying insecticides along small torrents and streams as well as around the banks of larger bodies of water. This practice may constitute a severe threat in the long-term (Shah 2010). Actual impacts appear to be low, but have never been assessed. Finally, a potential future threat to the Amphibians of Cyprus is the amphibian chytrid fungus Batrachochytrium dendrobatoides (Bd) (Rosenblum et al. 2010). The fungus is responsible for massive amphibian declines in many parts of the world, and even in southern parts of Europe it has started to kill amphibians and reduce their populations (Garner et al. 2005). Rödder et al. (2009) modelled the potential distribution of Bd under current and anticipated climates. They showed that the entire Aegean and eastern Mediterranean area provides suitable climatic conditions for the fungus to grow.

II.  Cypriot amphibians A.  Hyla savignyi (Audouin 1829). Savigny’s Treefrog – lemon-yellow treefrog

The species was first recorded from Cyprus by Gunther (1879). Recent studies (Stöck et al. 2008; Gvoždίk et al. 2010) consider the Cypriot population of the species as an introduction by dispersal during the Pleistocene era, originating from mainland populations of southeastern Turkey and/or Syria. According to the same papers, Cypriot treefrogs are distinct from southern Levantine and southwestern Arabian populations. It is widespread throughout the island. The highest locality from which this species was recorded is 1,028 m asl (Baier et al. 2009). It is normally found close to bodies of water, e.g. streams, ponds, dams, and lakes. The loss of suitable habitats is certainly a threat to the species.

B.  Bufotes viridis (Laurenti 1768). Green toad

The Bufotes viridis species complex is under taxonomic revision. Stöck et al. (2006) suggested that the Cypriot population belongs to the eastern fraction of the species complex under the provisional name Bufotes variabilis. In the same study, an individual green toad from Cyprus was found to belong to the same single mitochondrial group that also occurs in all parts of Asia Minor. This same monophyletic mitochondrial group occurs not only in Asia Minor but reaches western Iran and the Levant and is also widespread in northeastern Europe and Northern Central Asia (Baier et al. 2009). It is widespread throughout the island with the highest record of approximately 700 m asl (Osenegg 1989). In Cyprus a wide variety of bodies of water are used for deposition of eggs, such as streams and dams, but also shallow brackish lakes (Osenegg 1989). The destruction of wetlands and other humid habitats is a major threat to this species.

C.  Pelophylax bedriagae (Camerano 1882). Bedriaga’s frog ­– Levant water frog

There is an ongoing discussion of the taxonomy and phylogenetics of eastern Mediterranean water frogs (Böehme and Wiedl 1994; Lymberakis et al. 2007; Akın et al. 2010; Plötner et al. 2010; Poulakakis et al. 2013) including the taxonomy of the Cypriot population of the genus. The water frogs of Cyprus show significant variations in colour. The back frequently varies from greyish to brown to olive to light green. In Cyprus, the species has large populations throughout the island, including in several protected areas, with the highest recorded elevation being 1,350 m asl. (Nicolaou,

150 Amphibian Biology unpublished data). When streams dry up during summer, water frogs are observed moving upstream to the remaining water. In spring, when there is water at lower elevations, they move downstream again. Although there is some loss of humid habitats, the populations of these frogs appear to be robust, hence the lack of any designation of threat for this species in Cyprus.

III.  Monitoring The Cypriot government announced a tender for the monitoring of the three anuran species of the island in October 2011. This has now been contracted, but it is on-going and results are still expected at the time of writing.



IV.  References Akın, C.¸ Bilgin, C.C., Beerli, P., Westaway, R., Ohst, T., Litvinchuk, S.N., Uzzell, T., Bilgin, M., Hotz, H., Guex, G.-D. and Plötner, J., 2010. Phylogeographic patterns of genetic diversity in eastern Mediterranean water frogs have been determined by geological processes and climate change in the Late Cenozoic. Journal of Biogeography 37: 2111–2124. Baier, F., Sparrow, D. and Wiedl, H., 2009. The Amphibians and Reptiles of Cyprus. Edition Chimaira, Frankfurt am Main. Blosat, B., 2008. Population status, threats and protection of the grass snake, Natrix natrix cypriaca (Hecht, 1930) on Cyprus. Mertensiella 17: 246–271. Böhme, W. and Wiedl, H., 1994. Status and zoogeography of the herpetofauna of Cyprus with taxonomic and natural history notes on selected species (Genera Rana, Coluber, Natrix, Vipera). Zoology in the Middle East 10: 31–52. Dill, W.A., 1990. Inland fisheries of Europe. EIFAC Technical Paper No. 52. Rome, FAO. pp. 1–471. Garner, T.W.J., Walker, S., Bosch, J., Hyatt, A.D., Cunningham, A.A. and Fisher, M.C., 2005. Chytrid fungus in Europe. Emerging Infectious Diseases 11: 1639–1641. Gunther, A., 1879. Notice of a collection of mammals and reptiles from Cyprus. Proceedings of the Zoological Society of London 1879: 741. Gvoždίk, V., Moravec, J., Klϋtsch, C. and Kotlίk, P., 2010. Phylogeography of the Middle Eastern tree frogs (Hyla, Hylidae, Amphibia) as inferred from nuclear and mitochondrial DNA variation, with a description of a new species. Molecular Phylogenetics and Evolution 55: 1146–1166. Lymberakis, P., Poulakakis, N., Manthalou, G., Tsigenopoulos, C.S., Magoulas, A. and Mylonas, M., 2007. Mitochondrial phylogeography of Rana (Pelophylax) populations in the eastern Mediterranean region. Molecular Phylogenetics and Evolution 44: 115–125. Osenegg, K., 1989. Die Amphibien und Reptilien der Insel Zypern. Diploma thesis, University of Bonn, unpublished.

Conservation of Amphibians in Cyprus151 Pavlíček, T. and Csuzdi, C., 2006. Species richness and zoogeographic affinities of earthworms in Cyprus. European Journal of Soil Biology 42: 111–116. Plötner, J., Uzzell, T., Beerli, P., Cigdem, A., Bilgin, C.C., Haefeli, C., Ohst, T., Köhler, F., Schreiber, R., Guex, G.-D., Litvinchuk, S.N., Westaway, R., Reyer, H.-U., Pruvost, N. and Hotz, H., 2010. Genetic divergence and evolution of reproductive isolation in eastern Mediterranean water frogs. In Evolution in Action, ed. M. Glaubrecht. Springer Verlag, Heidelberg. Pp. 373–403. Poulakakis, N., Kapli, P., Kardamaki, A., Skourtanionti, E., Göcmen, B., Ilgaz, Ç., Kumlutas, Y., Avci, A. and Lymberakis, P., 2013. Comparitive phylogeography of six herpetofauna species in Cyprus: Late Micene to Pleistocene colonization routes. Biological Journal of the Linnean Society 108: 619–635. Rödder, D., Kielgast, J., Bielby, J., Schmidtlein, S., Bosch, J., Garner, T.W.J., Veith, M., Walker, S., Fisher, M.C. and Lötters, L., 2009. Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 1: 52–66. Rosenblum, E.B., Voyles, J., Poorten, T.J. and Stajich, J.E., 2010. The deadly chytrid fungus: A story of an emerging pathogen. Plos Pathogens 6: 1–3. Shah, S., 2010. Behind mass die-offs, pesticides lurk as culprit. Yale Environment 360: http:// e360.yale.edu/content/topic.msp?id=248 Stöck, M., Dubey, S., Klόtsch, C., Litvinchuk, S. N., Scheidt, U. and Perrin, N., 2008. Mitochondrial and nuclear phylogeny of circum-Mediterranean tree frogs from the Hyla arborea group. Molecular Phylogenetics and Evolution 49: 1019–1024. Stöck, M., Moritz, C., Hickerson, M., Frynta, D., Dujsebayeva, T., Eremchenko, V., Macey, J. R., Papenfuss, T.J. and Wake, D.B., 2006. Evolution of mitochondrial relationships and biogeography of Palearctic green toads (Bufo viridis subgroup) with insights into their genomic plasticity. Molecular Phylogenetics and Evolution 41: 663–689.

152 Amphibian Biology Page numbers in italics indicate figures or tables. Please note that listings are under species name, not under family. A acid rain 64, 65 African clawed frog (Xenopus laevis) 4, 4, 7, 8 Agile frog see Rana dalmatina agriculture, intensification of 28, 33, 34, 35, 70, 75, 91, 94, 101, 135 Akseki salamander (Lyciasalamandra atifi) 141, 143, 144 Akyarlar salamander (Lyciasalamandra billae) 141, 142, 143 Albania administrative districts 75 conservation/monitoring 76 legal protection 76 overview 74 pressures/threats 75 species present and status 76 summary 77 alpine newt see Ichthyosaura alpestris alpine salamander see Salamandra atra American bullfrog (Lithobates catesbeianus) 3, 4, 6, 7, 80, 82, 101 Amphibian and Reptile Conservation Group, Hungary 111, 112–113 Antalya salamander (Lyciasalamandra antalyana) 141, 143, 143–144 Appenine yellow-bellied toad (Bombina pachypus) 3, 4, 6 Atylodes genei 2, 4 Aurora’s alpine salamander (Salamandra atra aurorae) 9–10 B Balkan frog see Pelophylax kurtmuelleri

Balkan green frog see Pelophylax kurtmuelleri Batrachochytrium dendrobatidis fungus (Bd) Bulgaria 137 Croatia 28 Cyprus 149 Greece 80–81 Hungary 109, 110, 117–118 Italy 6–7, 6, 10 Romania 94 Serbia 48 Slovenia 34 Turkey 146 Bedriaga’s Frog see Pelophylax bedriagae Bern Convention 52, 69, 92 Black olm (Proteus anguinus parkelj) 34, 39 Bombina bombina Bosnia and Herzegovina 64 Bulgaria 132, 133, 136 Croatia 26, 27, 30 Greece 80, 81, 82 Hungary 100, 101, 102, 113, 114, 115, 116, 117 Romania 89, 89, 91 Serbia 48 Slovenia 35, 39 Turkey 141 Bombina pachypus 3, 4, 6 Bombina variegata Albania 76 Bosnia and Herzegovina 64 Bulgaria 132, 133, 133, 135, 136 Croatia 26, 29 Greece 81 Hungary 100, 101, 108–109, 113, 114, 116, 117, 118 Italy 3 Macedonia 68, 69 Montenegro 58 Romania 89, 89, 90, 91 Serbia 48, 50 Slovenia 35, 38 Bombina variegata kolombatovici 26, 30

Bombina variegata scabra 132 Bombina variegata variegata 26 Bonn Convention 92 Bosnia and Herzegovina freshwater habitats 62–64 overview 62 pressures/threats 63–64, 65 species present and status 64, 65 Bufo bufo Albania 75 Bosnia and Herzegovina 64 Bulgaria 132, 133, 136 Croatia 26, 29 Greece 81 Hungary 100, 102, 101, 113, 115, 116–117 Italy 3, 4, 10 Macedonia 68, 69 Maltese Islands 18 Montenegro 58 Romania 89, 93 Serbia 49 Slovenia 39 Turkey 141 Bufo verrucosissimus 141 Bufotes balearicus 3, 4 Bufotes boulengeri 3, 4 Bufotes siculus 3, 4 Bufotes variabilis Bulgaria 131, 132, 133, 136 Cyprus 149 Turkey 141 Bufotes viridis Albania 75, 76 Bosnia and Herzegovina 64 Bulgaria 131, 132, 133, 136 Croatia 26 Cyprus 148, 149 Greece 81 Hungary 100, 102, 102, 113, 115 Italy 3, 4, 9, 18 Macedonia 68, 69 Montenegro 58 Romania 89 Serbia 49 Slovenia 35, 39 Turkey 141

Index153 Bulgaria conservation/monitoring 135–137 declining species/species of concern 135 habitats 136 legal protection 135 species distribution 132, 133–134, 133, 134 species present and status 131–132, 132–133 summary 137 C captive breeding projects 10 Caucasian salamander (Mertensiella caucasica) 141, 142, 144 Centre for Cartography of Fauna and Flora (CKFF) 36, 37, 38 chemical pollution 75, 77, 94, 101 chytrid fungus see Batrachochytrium dendrobatidis fungus (Bd) climatic change 50, 57–58, 63–64, 65, 70, 80, 137, 148 collecting/hunting/poaching Albania 75, 76 Bosnia and Herzegovina 65 Bulgaria 135 Croatia 28 Greece 80, 82, 83, 84 Maltese Islands 20 Montenegro 58 Romania 93 Serbia 48 Slovenia 34 Turkey 142, 143, 146 Comino 19 Common spadefoot see Pelobates fuscus Common toad see Bufo bufo Common tree frog see Hyla arborea conservation and monitoring Albania 76



Bulgaria 135–137 Croatia 28–30 Greece 84 Hungary 111–118, 111, 112, 113 Italy 9–10 Macedonia 71 Maltese Islands 20–21 Montenegro 59–60 Romania 92–93 Serbia 51–52 Slovenia 36–38 Cretan tree frog (Hyla arborea cretensis) 80 Cretan waterfrog (Pelophylax cretensis) 80, 81, 82 Croatia conservation/monitoring 28–30 herpetological regions 26–27, 27 legal protection 28 overview 25–26 pressures/threats 27–28 Red List 30 species present and status 26–27, 26 summary 30 Croatian Herpetological Society (CHS) Hyla 28, 29 Cyprus legal protection 148 monitoring 150 overview 148–149 species present 149–150 D Danube crested newt see Triturus dobrogicus designatable units (DUs) 19 Despott, Giuseppe 18 Discoglossus montalentii 1–2, 3 Discoglossus pictus Italy 3, 8 Maltese Islands 18–22 Discoglossus sardus 3, 5, 6, 7 diseases 40, 45, 48, 52, 57

see also Batrachochytrium dendrobatidis fungus (Bd) drainage impacts 34, 47, 48, 64, 70, 75, 135 E Edible frog see Pelophylax kl. esculentus EU Birds Directive 37, 92, 93, 115 EU Common Agricultural Policy 94, 101 EU Convention on Biological Diversity 51, 92 EU Habitats Directive 9, 10, 21, 29, 38, 40, 92, 135 see also Natura 2000 network EU LIFE projects 9, 10, 37, 137 Euproctus montanus 1–2, 2 Euproctus platycephalus 2, 4, 5, 6, 7, 9, 10 European common frog see Rana temporaria European Herpetological Society (SEH) 112 eutrophication 63, 65, 106 exotic species Croatia 28 Cyprus 148–149 Greece 80 Hungary 101 Italy 7–9 Maltese Islands 18, 20, 21 Montenegro 57 Serbia 45, 47, 48 Slovenia 34 F Fire salamander see Salamandra salamandra Fire-bellied toad see Bombina bombina fish 7, 28, 34, 48, 59, 65, 94, 101, 142, 148–149 flood-management impacts 6, 10, 27, 33, 47, 88, 100 floodplains 27, 33, 46 forest fires 80, 142, 143

154 Amphibian Biology G genetic pollution 8 Gozo 2, 7, 17, 18, 19, 20 see also Maltese Islands Grass frog see Rana temporaria Greece conservation/monitoring 84 legal protection 84 overview 80–81 pressures/threats 80–81 species of concern 82–84 species present and status 81 summary 84 Greek smooth newt (Lissotriton vulgaris graecus) 26 green frogs 8, 48, 50, 51, 52, 59, 74, 75 Green toad see Bufotes viridis H habitat alteration/destruction/ fragmentation Albania 75 Bosnia and Herzegovina 64, 65 Bulgaria 135, 137 Croatia 27, 28 Greece 80 Hungary 100–101, 105, 106 Italy 5–6 Macedonia 70 Maltese Islands 19–20 Montenegro 57 Romania 88, 91, 94 Serbia 45, 47, 47–48, 50 Slovenia 33, 34 Turkey 142, 143 harvesting see collecting/ hunting/poaching HerpeThon talks 10 Hungary conservation/monitoring 111–118, 111, 112, 113 declining species/species of concern 102–111 habitat alteration/ destruction 100–101 legal protection 102

overview 100 species present and status 101–102 summary 118 hunting see collecting/hunting/ poaching hybridization 35, 38, 90, 105, 108 Hyla arborea Albania 75, 76 Bosnia and Herzegovina 64 Bulgaria 131, 132, 133, 136 Croatia 26, 29 Greece 80, 81 Hungary 100, 102, 102, 113, 113, 115, 117 Italy 3 Macedonia 68, 69 Montenegro 58 Romania 89, 93 Serbia 49, 50 Slovenia 39 Hyla arborea cretensis 80 Hyla intermedia 3, 5, 8, 9 Hyla meridionalis 3 Hyla orientalis Bulgaria 131, 132, 133, 136 Turkey 141 Hyla sarda 3 Hyla savignyi Cyprus 148, 149 Turkey 141 I Ichthyosaura alpestris Albania 76 Bosnia and Herzegovina 64, 65 Bulgaria 132, 133, 133, 135, 136, 136 Croatia 26, 27, 29 Greece 80, 81, 83 Hungary 100, 101, 102, 106–108, 107, 113, 115, 116, 117 Italy 3 Macedonia 68, 69, 71 Montenegro 58, 59

Romania 89, 89 Serbia 48, 51 Slovenia 35, 39 Ichthyosaura alpestris alpestris 107 Ichthyosaura alpestris apuana 4 Ichthyosaura alpestris bakonyiensis 107 Ichthyosaura alpestris bükkiensis 107 Ichthyosaura alpestris carpathica 132 Ichthyosaura alpestris carpathicus 107 Ichthyosaura alpestris inexpectata 4 Ichthyosaura alpestris lacusnigri 35, 39 Ichthyosaura alpestris lacustris 35 Ichthyosaura alpestris reiseri 65 Ichthyosaura alpestris sátoriensis 107 Ichthyosaura alpestris veluchiensis 80 inbreeding 57, 83 insecticides 58, 149 Institute of the Republic of S l o ve n i a f o r N a t u r e Conservation 37 INTERREG (cross-border ) projects 37 introduced species see exotic species Istrian olm (Proteus anguinus spp. n.) 26, 30 Italian agile frog see Rana latastei Italian crested newt see Triturus carnifex Italian treefrog (Hyla intermedia) 3, 5, 8, 9 Italy conservation/monitoring 9–10 overview 1–2 pressures/threats 5–9, 6 representative species 5

Index155 species present and status 2–4, 4 summary 10 L Lanza’s salamander (Salamandra lanzai) 3, 4, 5, 6, 9, 10 Lemon-yellow treefrog (Hyla savignyi) 141, 148, 149 Levant water frog see Pelophylax bedriagae Lissotriton graecus 131, 132, 133, 133, 136 Lissotriton italicus 3 Lissotriton montandoni Bulgaria 131 Romania 89, 89, 90, 90, 91, 93 Lissotriton vulgaris Albania 75, 76 Bosnia and Herzegovina 64 Bulgaria 131, 132, 133, 135, 136 Croatia 26, 29 Greece 81 Hungary 100, 101, 102, 113, 115, 116, 117 Italy 3 Macedonia 68, 69, 71 Montenegro 58, 59 Romania 89, 89, 90, 90, 93 Serbia 48 Slovenia 35, 37, 39 Turkey 141 Lissotriton vulgaris ampelensis 89, 90, 91 Lissotriton vulgaris graecus 26 Lissotriton vulgaris schmidtleri 131, 132 Lissotriton vulgaris vulgaris 132 Lithobates catesbeianus Greece 80, 82 Hungary 101 Italy 3, 4, 6, 7 Luschan’s salamander (Lyciasalamandra luschani)

80, 81, 82–83, 141, 142, 143, 144 Lycian salamander (Lyciasalamandra fazilae) 141, 143, 144 Lyciasalamandra antalyana 141, 143, 143–144 Lyciasalamandra arikani 141, 143 Lyciasalamandra atifi 141, 143, 144 Lyciasalamandra billae 141, 142, 143 Lyciasalamandra fazilae 141, 143, 144 Lyciasalamandra flavimembris 141, 143, 144 Lyciasalamandra helverseni 80, 81, 83–84 Lyciasalamandra irjani 141 Lyciasalamandra luschani Greece 80, 81, 82–83 Turkey 141, 142, 143, 144 Lyciasalamandra yehudahi 141, 143 M Macedonia conservation/monitoring 71 overview 67–68 pressures/threats 70 species of concern 71 species present 68, 69 species status 69, 69 summary 71 Macedonian crested newt see Triturus macedonicus Malta see Maltese Islands Maltese Islands conservation/monitoring 20–21 legal protection 20–21 overview 17–18 pressures/threats 19–20 species present 18–19 species status 19–20 summary 21–22 Marmaris salamander (Lyciasalamandra flavimembris) 141, 143, 144

Marsh frog see Pelophylax ridibundus Mertensiella caucasica 141, 142, 144 molecular phylogeography 117 monitoring see conservation and monitoring Montenegro conservation/monitoring 59–60 legal protection 59 overview 56–57 pressures/threats 57–58 species of concern 58–59 species present and status 58 Moor frog see Rana arvalis N Natrix natrix cypriaca 149 Natura 2000 Integration Project 29–30 Natura 2000 network 21, 34, 37–38, 39–40, 92, 115, 135, 136 Neurergus crocatus 141, 142, 145 Neurergus strauchii 141, 142, 145 NGOs (non-governmental organizations) 19, 21, 36, 37, 51–52, 59, 110–111, 113 non-indigenous invasive species (NIS) 7–8 see also exotic species Northern spectacled salamander (Salamandrina perspicillata) 3, 5, 7 O Olm Black (Proteus anguinus parkelj) 34, 39 White see Proteus anguinus Ommatotriton ophryticus 141 Ommatotriton vittatus 141

156 Amphibian Biology P paedomorphosis 59, 117 painted frog (Discoglossus pictus) 3, 8, 18–22 Pelobates fuscus Bosnia and Herzegovina 64 Bulgaria 132, 133, 133, 135, 136, 136, 137 Croatia 26, 27, 30 Hungary 100, 101, 102, 113, 115 Italy 3, 4, 5–6, 5, 9, 10 Romania 88–89, 89, 90, 91, 91 Serbia 49, 50 Slovenia 35, 39 Pelobates fuscus insubricus 4, 5, 9 Pelobates syriacus Bulgaria 132, 133, 133, 135, 136, 136 Greece 81 Macedonia 68, 69, 71 Romania 89, 90, 91, 91, 93 Serbia 49, 50 Turkey 141 Pelobates syriacus balcanicus 132 Pelodytes caucasicus 141 Pelodytes punctatus 3, 4 Pelophylax balcanicus 74, 75, 76, 76 Pelophylax bedriagae Bulgaria 131, 132, 133, 133, 136 Cyprus 148, 149–150 Greece 80, 81, 82 Italy 2, 3, 4, 7 Maltese Islands 18, 20, 21 Turkey 141 Pelophylax bergeri 3, 6 Pelophylax caralitanus 141, 146 Pelophylax cerigensis 80, 81, 82 Pelophylax cretensis 80, 81, 82 Pelophylax epeiroticus Albania 74, 75, 76, 76 Greece 81 Pelophylax kl. esculentus Bosnia and Herzegovina 64 Bulgaria 132, 133, 133, 136



Croatia 26, 27 Hungary 100, 102, 102, 113, 116, 117 Italy 3, 6, 6, 7, 8 Montenegro 58, 59 Romania 89, 89 Serbia 48, 49, 50, 51, 52 Slovenia 32, 39, 39 Pelophylax grafi 1, 3 Pelophylax hispanicus 3 Pelophylax kurtmuelleri Bulgaria 131, 132, 133, 133 Greece 81 Italy 3, 4, 7, 8 Slovenia 34 Pelophylax lessonae Albania 74, 75, 76, 76 Bosnia and Herzegovina 64 Bulgaria 131, 132, 133, 133, 135, 136 Croatia 26, 27 Hungary 100, 102, 102 Italy 3, 6, 8 Montenegro 58, 59 Romania 89, 89 Serbia 48, 49, 50, 51, 52 Slovenia 39 Pelophylax perezi 1, 3 Pelophylax ridibundus Albania 76 Bosnia and Herzegovina 64 Bulgaria 132, 133, 136 Croatia 26, 29 Greece 81 Hungary 100, 102, 102, 113, 116, 117 Italy 3 Macedonia 68, 69 Montenegro 58, 59 Romania 89, 89 Serbia 48, 49, 50, 51, 52 Slovenia 39 Turkey 141, 143, 146 Pelophylax shqipericus Albania 76 Italy 11 Montenegro 58 pesticides 27, 70, 75, 94

poaching see collecting/ hunting/poaching pollution Albania 75, 77 Bosnia and Herzegovina 65 Bulgaria 137 Croatia 28 Greece 80, 82, 83 Italy 5, 6 Macedonia 70 Maltese Islands 20 Romania 91 Serbia 45, 47 Slovenia 33, 34, 40 Turkey 142 see also chemical pollution; wastewater ponds desiccation and/or drainage 28, 47–48, 109 eutrophication 65 restoration 29, 36, 37, 116 surveys 37 Pool frog see Pelophylax lessonae predators introduced 7, 8–9, 20, 28, 34, 48, 59, 101, 142, 148–149 native 45, 48, 107, 109, 149 Prenj salamander (Salamandra atra prenjensis) 65 Procambarus clarkii 8–9 Proteus anguinus Bosnia and Herzegovina 64, 65 Croatia 26, 28, 28–29, 29, 30 Italy 2, 4 Slovenia 33, 34, 38, 39, 40 Proteus anguinus parkelj 34, 39 Proteus anguinus spp. n 26, 30 PROTEUS project 28–29 R Ramsar Convention 137 Rana arvalis Croatia 26, 27, 29 Hungary 100, 102, 108, 109, 113, 114, 116, 117

Index157 Romania 88, 89, 90, 91, 91, 93 Slovenia 35, 39 Rana arvalis wolterstorffi 109 Rana dalmatina Albania 75, 76 Bosnia and Herzegovina 64 Bulgaria 132, 133, 136 Croatia 26, 28, 29 Greece 81 Hungary 100, 102, 102, 113, 114, 115, 117 Italy 4 Macedonia 68, 69 Montenegro 58 Romania 89, 90, 91, 93 Serbia 49 Slovenia 39 Turkey 141 Rana graeca Albania 76 Bosnia and Herzegovina 64 Bulgaria 132, 133, 133, 136, 136 Greece 81 Macedonia 68, 69 Montenegro 58 Serbia 49, 51 Rana holtzi 141, 142, 145 Rana italica 4 Rana latastei Croatia 26, 27, 28, 29, 30 Italy 4, 4, 5–6, 6, 7, 9, 10 Slovenia 34–35, 38, 39 Rana macrocnemis 141 Rana tavasensis 141, 142, 145 Rana temporaria Albania 76 Bosnia and Herzegovina 64 Bulgaria 133, 133, 135, 136 Croatia 26, 27, 28, 29 Greece 80, 81, 83 Hungary 100, 102, 102, 110, 110, 113, 114, 116, 117, 118 Italy 4, 7 Macedonia 68, 69, 71 Montenegro 58 Romania 89, 93

Serbia 49, 51 Slovenia 39 Red Lists, national 29, 30, 38, 39, 84, 89, 92–93 Red swamp crayfish (Procambarus clarkii) 8–9 Reiser’s alpine newt (Ichthyosaura alpestris reiseri) 65 reservoirs 70, 76, 148 rivers 10, 27, 46, 47, 57, 63, 70, 75, 100 road mortality 6, 29, 33–34, 48, 70, 94 road rescue actions 10, 36–37, 48, 111, 113–114 Romania conservation/monitoring 92–93 human footprint 88 legal protection 92 overview 87–88 phylogeography 88–89 pressures/threats 91 Red Lists 92–93 species at range limits 90, 90, 91 species of concern 89–91 species present and status 89 summary 94 S Salamandra atra Albania 76 Bosnia and Herzegovina 64, 65 Croatia 26, 27, 29, 30 Italy 3 Montenegro 58, 59 Serbia 48, 50 Slovenia 35, 39 Salamandra atra aurorae 4, 9–10 Salamandra atra pasubiensis 4, 10 Salamandra atra prenjensis 65 Salamandra corsica 1–2, 3 Salamandra infraimmaculata 141

Salamandra lanzai 3, 4, 5, 6, 9, 10 Salamandra salamandra Albania 76 Bosnia and Herzegovina 64 Bulgaria 132, 133, 133, 136 Croatia 26, 27, 29 Greece 81 Hungary 100, 101, 103–104, 103, 104, 113, 113, 114, 116, 117 Italy 3 Macedonia 68, 69 Montenegro 58 Romania 89, 90, 91 Serbia 48 Slovenia 39 Turkey 141 Salamandra salamandra beschkovi 131 Salamandra salamandra salamandra 132 Salamandra salamandra werneri 131, 132 Salamandrina perspicillata 3, 5, 7 Salamandrina terdigitata 3 Sardinian brook salamander (Euproctus platycephalus) 2, 4, 5, 6, 7, 9, 10 Sardinian painted frog (Discoglossus sardus) 3, 5, 6, 7 Savigny’s treefrog (Hyla savignyi) 141, 148, 149 Serbia conservation/monitoring 51–52 declining species 49–50 legal protection 51 map 46 overview 45–47 pressures/threats 45, 47–48 species of concern 50–51 species present and status 48–49, 52 summary 52

158 Amphibian Biology Slovenia conservation/monitoring 36–38 declining species/species of concern 34–35 legal protection 36, 37–38 overview 32–33 pressures/threats 33–34 Red List 38, 39 summary 39–40 Smooth newt see Lissotriton vulgaris Societas Herpetologica Italica (SHI) 10 Societas Herpetologica Slovenica (SHS) 36, 37 spadefoot toads see Pelobates species Speleomantes ambrosii 2, 4 Speleomantes flavus 2, 4 Speleomantes imperialis 2 Speleomantes italicus 2 Speleomantes sarrabusensis 2, 4 Speleomantes strinatii 2 Speleomantes supramontis 2, 4 Spotted salamander (Neurergus strauchii) 141, 142, 145



T Taurus frog (Rana holtzi) 141, 142, 145 Tavas frog (Rana tavasensis) 141, 142, 145 taxonomy 89, 93, 116 tourism impacts 6, 106, 142 Tree frog see Hyla arborea Triturus arntzeni 89, 131 Triturus carnifex Bosnia and Herzegovina 64 Croatia 26, 27, 29, 30 Hungary 100, 101, 105–106, 105, 106, 113, 114, 115, 116 Italy 3 Montenegro 58 Serbia 49, 50 Slovenia 35, 37, 38, 39 Triturus cristatus Albania 75

Bulgaria 132, 133, 133, 135, 136 Hungary 105, 116 Romania 89, 90, 90, 91, 93 Serbia 48, 50 Triturus dobrogicus Bosnia and Herzegovina 64, 65 Bulgaria 132, 133, 133, 135, 136, 136 Croatia 26, 27, 29, 30 Hungary 100, 101, 104–105, 113, 114, 115, 116, 117 Romania 89, 89, 90, 90, 91, 91, 93 Serbia 48, 51, 52 Slovenia 35, 38, 39 Triturus ivanbureschi Bulgaria 131, 132, 133, 135, 136 Romania 89 Serbia 48, 50 Triturus karelinii Bulgaria 131 Greece 81 Macedonia 68, 69, 71 Serbia 50 Turkey 141 Triturus macedonicus Albania 76 Bosnia and Herzegovina 64 Bulgaria 132, 133, 133, 135 Greece 81 Macedonia 68, 69, 69, 71 Montenegro 58, 59 Serbia 48, 49, 50, 51 tunnels 36, 113, 114 Turkey conservation measures required 145 declining species 142–143 overview 140 species of concern 143–145 species present and status 140, 141 summary 145–146

U urbanization 5–6, 33, 35, 40 Urmiye salamander (Neurergus crocatus) 141, 142, 145 V Va r a n g y A k c i ó c s o p o r t Egyesület 111, 113 W waste 29, 34, 47 wastewater 47, 70, 91 wetlands 9, 20, 46, 63, 64, 80, 100, 137 White olm see Proteus anguinus X Xenopus laevis 4, 4, 7, 8 Y Yellow-bellied toad (Bombina variegata kolombatovici/ variegata) 26, 30