Underground Occurences of Three Species of Amphibians and Reptiles with Special Emphasis on Rana Latastei (Amphibia: Anura)

Home , Agile frog, Italian agile frog, Pelobates syriacus

176 North-Western Journal of Zoology 13(1) / 2017

Key words: amphibia, faunistics, herpetofauna, Prespa, Balkan.

Article No.: e167501 Received: 19. November 2015 / Accepted: 27. February 2016 Available online: 30. March 2016 / Printed: June 2017

Márton SZABOLCS1,2,* and Edvárd MIZSEI3

1. Department of Tisza River Research, Danube Research Institute, Centre for Ecological Research, Hungarian Academy of Sciences, Bem tér 18/C, 4026 Debrecen, Hungary. 2. Pál Juhász-Nagy Doctoral School of Biology and Environmental Sciences, University of Debrecen, Egyetem tér 1, 4032 Debrecen, Hungary. 3. Department of Evolutionary Zoology & Human Biology, Univer- sity of Debrecen, Egyetem tér 1, 4032 Debrecen, Hungary. *Corresponding author, N. Szabolcs, E-mail: [email protected]

Figure 1. The location of Albania in Europe (A), a topog- raphical map of Albania, with main waterbodies, where the star indicates the new locality of Pelobates syriacus (B), and a photograph of the first P. syriacus found in Albania (C). Underground occurrences of three species of amphibians and reptiles

Acknowledgments. We thank the volunteers of the with special emphasis Greek Meadow Viper Working Group, especially Ádám on Rana latastei (Amphibia: Anura) Lovas-Kiss, for the help in the field trips. Traveling costs were provided by Balassi Institute, Hungary, Campus The Italian agile frog, Rana latastei Boulenger, 1879 Hungary Programme (B2/1CS/19196). Our efforts to map is an endemic species of the Padano-Venetian the herpetofauna of Albania was supported by the Societas Europea Herpetologica’s SEH Grant in plain, the Po plain hills, Canton Ticino and Istria Herpetology 2015 – Mapping and Distributions. (Barbieri & Bernini 2004). As a whole, the general distribution limits of this species are well known References (Bruno 1977, Grossenbacher 1982, Burlin & Dolce Bruno, S. (1989): Introduction to a study of the herpetofauna of Albania. British Herpetological Society Bulletin 29: 16-41. 1986, Gasc et al. 1997, Glasnović 2012), but the Budak, A., Göçmen, B. (2008): Herpetoloji (Herpetology), Ege borders of the distribution areas are not clear yet. Üniversitesi Fen Fakültesi Kitaplar Serisi, No. 194, Ege Distribution of R. latastei in Croatia is restricted to Üniversitesi Basimevi, Bornova-Izmir, 226p. Dhora, D. (2010): Register of species of the fauna of Albania. the central and northern part of Istria (Schmidtler Shkodër, Albania, Botimet Camaj-Pipa, 208p. 1977, Burlin & Dolce 1986, Gasc et al. 1997, Kul- Džukić, G., Beškov, V., Sidorocska, V., Cogălniceanu, D., Kalezić, jerić 2011). The Pazinčica river represents the M.L. (2008): Contemporary chorology of the spadefoot toads (Pelobates spp.) in the Balkan Peninsula. Zeitschrift für southernmost record of R. latastei (Kuljerić 2009, Feldherpetologie 15: 1-18. 2011). Haxhiu, I. (1994): The herpetofauna of Albania, Amphibia: species According to the known habitat requirements composition, distribution, habitats. Zoologische Jahrbuecher Systematik 17: 199-202. of R. latastei, it is restricted to lowlands and occu- Haxhiu, I. (1998): The reptilia of Albania: species composition, pies humid oak-hornbeam forest, hygrophilous distribution, habitats. Bonner Zoologische Beitrage 48(1): 35-57. woods of the Cladio-Fraxinetum angustifoliae asso- Jablonski, D. (2011): Reptiles and amphibians of Albania with new records and notes on occurence and distribution. Acta Societatis ciation and riparian woods (Barbieri & Mazzotti Zoologicae Bohemicae 75: 223-238. 2006). Sometimes it may be found in more open Mizsei, E., Jablonski, D., Végvári, Z., Lengyel, S., Szabolcs, M. areas such as peat bogs, sedge banks and swamps (2017): Distribution and diversity of reptiles in Albania: a novel database from a Mediterranean hotspot. Amphibia-Reptilia 38: (Jelić et al. 2012). During the biospeleological and 157-173. cave diving exploration into the Pazinska jama, Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., Crochet, three different amphibian and reptile species were P-A., Crnobrnja Isailović, J., Denoël, M., Ficetola, G.F., Gonçalves, J., Kuzmin, S., Lymberakis, P., de Pous, P., observed in the cave system, including the first re- Rodríguez, A., Sindaco, R., Speybroek, J., Toxopeus, B., Vieites, cord of R. latastei inside a Croatian cave. The only D.R., Vences, M., (2014): Updated distribution and other record of this species from inside a cave is biogeography of amphibians and reptiles of Europe. Amphibia- Reptilia 35: 1-31. from Italy (Bressi & Dolce 1999). The species is

Correspondence –Notes 177 listed as Vulnerable (VU) in the IUCN Red List (Sindaco et al. 2009) and as a strictly protected species in Appendix II of the Convention on the Conservation of European Wildlife and Natural Habitats (Bern Convention) and in Annexes II and IV of the Directive on the Conservation of Natural Habitats of Wild Fauna and Flora. A few other taxa that are usually epigeous are regularly found inside caves (B. bufo, R. italica) (Lunghi et al. 2014). Caves are not closed systems, and species move between cave and outdoor environments (Manenti et al. 2015). The first speleological research of Pazinska jama was conducted by the French caver Martel (1896), who also prepared the first topographic Figure 1. Pazin river and the collecting site (green dot). draft of the cave together with W. Putick from Ljubljana. The entrance into the cave is under a After detailed research of the lake, siphons and vertical cliff and is followed by a hundred meter channels, the olm was not found, but the author long channel, which expands into a hall (80 ×20 m) counted 20 individuals of the Italian agile frog with the large subterranean Martel Lake. The lake each day (Fig. 2). Firstly, one group of individuals is full of logs that have been deposited by strong was detected along the channel, approximately 40 floods. m from the entrance. The surrounding habitat was light-influenced and a slight stream of water was The herpetological research and speleological exploration present. Secondly, a larger group was observed in of Pazinska jama (X:5416357 ; Y:5011182, 185 m a.s.l.) was the deepest dry part of the cave, along the sandy carried out on 14 and 15 April 2015 with the main pur- pose of finding the olm (Proteus anguinus Laurenti, 1768) edge of the Martel lake, but also on logs in the wa- and making a sketch of the underground system. Pazin- ter. This part is the zone of complete darkness. ska jama is located in Pazin (Istria, Croatia) where the Other recorded species included two indi- 16.5 km long Pazinčica river disappears into a sinkhole viduals of Bufo bufo and one Emys orbicularis. Bufo (Fig. 1). During the visit, the cave fauna was surveyed for bufo was observed in a dry part of the cave near approximately five hours each day. Last day, after the the lake while E. orbicularis was noticed in Martel channels were checked, we used a boat to survey the un- Lake. Both species were lighter in colour than derground lake. Animals were caught by hand, photo- graphed and released as soon as possible at the site of usual (Fig. 3 & 4). This kind of coloration in B.bufo capture. had already been observed in Croatia, but not

Figure 2. Sketch of the underground system Pazinska jama, authors SK HAD, SD Istra and SO HPD Željezničar, show- ing the exact locality of amphibian species in the research area (red dots – R. latastei; green dots – B. bufo; yellow dots – E. orbicularis).

178 North-Western Journal of Zoology 13(1) / 2017

by the water flow. There are two possible explana- tions how the amphibians and reptiles reported in this study got into the underground. The first is that they were drifted by floods into the cave, while the second possibility is the intentional entrance of the individuals because of some ecological parameters such as constant humidity, a lack of predators or a lack of competition for food, or as breeding sites. Considering the large number of R. latastei specimens present on the site, and the fact that this was the only visit to the cave with the aim of finding herpetofauna, additional records are

necessary in order to evaluate if this is only an in- Figure 3. R. latastei from Pazinska jama (photo made on cidental occurrence or part of a trend in using the April 15 2015). underground system. Regardless, this is a very

important record because Pazin is on the edge of the R. latastei distribution and until now, there had only been information about several spawns be- longing to this species, but the adults were never observed in the area (Koren, Zagreb, pers. comm. 2015). The results of this study contribute to the knowledge of the occurrence and distribution of R. latastei and also indicate the possible residency and usage of the subterranean habitats. Karst covers 26 000 km2 (46%) of the Croatian territory (Gottstein 2010) and accordingly represents an important habitat for both land dwelling as well as underground animals. The usage of karstic caves,

sinkholes or other structures by amphibians is un- Figure 4. B. bufo from Pazinska jama (photo made on derstudied, and further research is needed. Re- April 15 2015). cently it has been recorded that caves can be

breeding sites for Salamandra salamandra (Mananti within caves (Jelić 2011). There was no indication 2009a, 2009b, 2011, Manenti & Ficetola 2013), so that the individuals were malnourished. there is also a possibility that other amphibian The occurrence of amphibians in underground species use caves as breeding sites. In this regard, habitats is reported in both herpetological and it is also important to visit this area again, to verify biospeleological literature (Manenti et al. 2009, whether the species breed in the cave systems. Ianc et al. 2012), but without systematic review about their presence in caves. As well as the cave Acknowledgements. I would like to thank Mladen Jekić who was the leader of the speleological-diving expedition finding in Italy, Pazinska jama represents a habitat “Pazinska jama 2015”. I also thank the 28 speleologists which is clearly different from the currently and cave-divers who participated in the expedition for known preferences of R. latastei mentioned in pre- their help in the field. They are members of SO Velebit vious papers (Barbieri & Mazzotti 2006, Mazzotti Zagreb, SO Liburnija Zadar, SO Željezničar Zagreb,SD & Pellizzari 2000, Bressi & Dolce 1999, Jelić et al. Istra, SD Buje, SD Ćićarija, SU Pula, SK Had Vrsar. My 2012). In their research on the Fire salamander, thanks also go to Antonio Ciceran for sharing the draft of Salamandra salamandra (Linnaeus, 1758), Manenti et Pazinska jama. Toni Koren and Dušan Jelić (Croatian Herpetological Society – Hyla, Zagreb, Croatia) are al. (2009) mentioned multiple mechanisms which thanked for helpful suggestions and comments on the could explain the underground presence of am- manuscript. phibians: subterranean habitats can be winter shel- ters, hiding places during the active season, and References feeding habitats, or caves sometime act as natural Arnold, N., Ovenden, D. (2002): A field guide to the reptiles and amphibians of Britain and Europe. Harper Collins Publishers, traps where amphibians fall in or are transported London, United Kingdom.

Correspondence –Notes 179

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Revue Suisse de Zoologie 89: 607-615. Ianc, R., Cicort-Lucaciu, A.S., Ilies, D., Kovacs, E.H. (2012): Note on the presence of Salamandra salamandra (Amphibia) in caves from Two of the four European spadefoot toad species Padurea Craiului Mountains, Romania. North-Western Journal are present in Romania: the Common spadefoot of Zoology 8: 202–204. toad Pelobates fuscus (Laurenti 1768), with an ex- Jelić, D., Kuljerić, M., Koren, T., Treer, D., Šalamon, D., Lončar, M., Podnar Lešić, M., Janev Hutinec, B., Bogdanović, T., Mekinić, S., tensive range that covers most of the plains and Jelić, K. (2012): Crvena knjiga vodozemaca i gmazova Hrvatske. hilly regions (up to 700 m); and Eastern or Syrian Državni zavod za zaštitu prirode, Republika Hrvatska, Zagreb. spadefoot toad Pelobates syriacus Boettger, 1889, Jelić, M. (2011): Finding of Common toad (Bufo bufo) with predominant yellow body coloration. Hyla 2: 25. which is limited to the southern parts of the coun- Kuljerić, M. (2011): Italian agile frog, Rana latastei Boulenger, 1879 try at altitudes below 200 m a.s.l. (Fuhn 1960, Sos (Amphibia, Anura). Hyla 1: 3-20. 2008). The european distribution of P. syriacus in- Kwet, A. (2009): European Reptile and Amphibian Guide, 2nd ed. New Holland Publisher Ltd., London. cludes the south-eastern Balkans (Džukić et al. Lunghi, E., Manenti, R., Ficetola, G. F. (2014): Do cave features 2005, 2008); in SW Asia it occurs in eastern to affect underground habitat exploitation by non-troglobite south-eastern Transcaucasia, northern Iran, Tur- species? Acta Oecologica 55: 29-35. Manenti, R., Ficetola, G.F. De Bernardi, F. (2009a): Water, stream key and the Levant to Israel (Agasyan et al. 2009, morphology and landscape: complex habitat determinants for Székely et al. 2013). According to Sofianidou the fire salamander Salamandra salamandra. Amphibia-Reptilia (1997), the present range of P. syriacus is bounded 30: 7-15. Manenti, R., Ficetola, G.F., Bianchi, B., De Bernardi, F. (2009b): by the Pannonian Plain and the Danube River area Habitat features and distribution of Salamandra salamandra in in the north (but see Cogălniceanu et al. 2013, underground springs. Acta Herpetologica 4: 143-151. Székely et al. 2013), the Morava River valley in the Manenti, R., Ficetola, G.F., Marieni, A., De Bernardi, F. (2011): Caves as breeding sites for Salamandra salamandra: habitat west, the Mediterranean shoreline in the south, selection, larval development and conservation issues. North- and Transcaucasia in the east. In Romania the sub- Western Journal of Zoology 7(2): 304-309. species P. s. balcanicus Karaman, 1928 appears, Manenti, R., Ficetola, G.F. (2013): Salamanders breeding in subterranean habitats: Local adaptations or behavioural which has a distribution restricted to Macedonia, plasticity? Journal of Zoology 289: 182-188. Bulgaria, Romania, Greece and Turkey-in-Europe Manenti, R., Lunghi, E., Ficetola, G. F. (2015): The distribution of (Fuhn 1960, Ugurtas et al. 2002). cave twilight-zone spiders depends on microclimatic features and trophic supply. Invertebrate Biology 134(3): 1-10. P. syriacus is a highly specialized species, hav- Martel, E.A. (1896): Sur les siphons des sources et des rivières ing a narrow ecological niche. Terrestrial habitats souterraines. Comptes Rendus de l'Académie des Sciences 122: occupied are generally open uncultivated and also 1147-1150. Schmidtler, J.F. (1977): Amphibien aus Feuchtwaldern Istriens. cultivated arable land (Székely et al. 2013), steppe, Salamandra 13 (2): 114-116. coastal dunes (Fuhn 1960), semi-desert and rocky Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., Crochet, areas, heathlands and deciduous woodlands P.A., Isailović, J.C., Denoël, M., Ficetola, G.F., Gonçalves, J., Kuzmin, S. (2014): Updated distribution and biogeography of (Džukić et al. 2005), etc. According to Székely et al.