Analele tiinifice ale Universitii Al. I. Cuza Iai, s.

Biologie animal, Tom LVI, 2010

SFNTU GHEORGHE (TULCEA, ROMANIA): AN IMPORTANT HERPETOLOGICAL AREA

tefan R. ZAMFIRESCU, Alexandru STRUGARIU, Iulian GHERGHEL and Oana ZAMFIRESCU
Al. I. Cuza Iasi University, Faculty of Biology, Carol I, 20A, 700505, Iasi, Romnia. e-mail: zamfi@uaic.ro

Abstract. Amphibians and reptiles are endangered at European level. The aim of the study is to present the detailed distribution of the herpetofauna of the area surrounding the village of Sfntu Gheorghe. We identified 7 amphibian and 6 reptile species of which only one is not legally protected. The main threats for the amphibians and reptiles are the habitat alteration and killing. Keywords: amphibians, reptiles, habitats, Danube Delta, Directive 92/43/EEC. Rezumat. Sfntu Gheorghe (Tulcea, Romnia): o zon de importan herpetofaunistic. Amfibienii i reptilele sunt specii ameninate la nivel European. Scopul acestui studio este de a prezenta distribuia detaliat a heretofaunei din mprejurimile satului Sfntu Gheorghe. Am identificat 7 specii de amfibieni i 6 specii de reptile, dintre care doar una nu se afl sub protecia legii. Principalele ameninri pentru amfibieni i reptile sunt degradarea habitatului i uciderea. Cuvinte cheie: amfibieni, reptile, habitate, Delta Dunrii, Directiva 92/43/EEC.

Introduction The amphibians and reptiles are one of the most endangered animals. At European level, almost a quarter of the amphibians and nearly one fifth of the reptiles are considered threatened (Cox & Temple, 2009; Temple & Cox, 2009). These animals also play an important part in the protection of nature. According to Romanian and European environmental regulations, the presence of some of these species constitutes arguments for the continuous protection of certain areas (European Council Directive 92/43/EEC, transposed as Romanian Government Ordinance no. 57/20.06.2007). Therefore, the identification and monitoring of areas were these species concentrate is very important. Such an area is the Danube Delta, especially the part near the coast, which offers a great variety of habitats and environmental conditions. Although a biosphere reserve, the delta is not deprived of human influence and alteration. The area around Sfntu Gheorghe is representative in this respect for putting together wilderness and civilisation in various degrees. Thus, we aim to present the herpetofauna of the area surrounding the village of Sfntu Gheorghe, emphasising on species with protective value and their habitats. Even though there are several herpetofaunistic records for the locality Sfntu Gheorghe, our study presents for the first time a detailed distribution of the species. Material and Methods The study area (Fig. 1) lies in the south-eastern tip of the Srturile natural marine levee, which is an economical zone of the Danube Delta Biosphere Reserve. It is also included in the Natura 2000 network of protected areas as ROSCI0065 Delta Dunrii (The Danube Delta) established through the Order of the Minister of Environment and Durable Development 776/05.09.2007. The area is a mosaic of natural and anthropogenic habitats: permanent and temporal ponds and channels, flat areas, dykes and beach. Average altitude is around 0 m.
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The sandy substratum is covered with vegetation that varies from hydrophilous to xerophilous. The climate of the area is semi-arid, with mean annual temperatures and precipitations of 11.4oC and 403.6 mm, respectively (Gtescu & tiuc, 2006). The study zone it is considered as formed of 4 areas: the village, which includes anthropic habitats, the area to the north-west of the village (Fig. 2), includes small temporary ponds and elevated terraces covered mostly by Juncus sp., the area to the east of the village (Fig. 3), includes marshes and sand dykes, and the seashore, which includes small dunes with scares vegetation (Fig. 4).

Figure 1. The study area.

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Analele tiinifice ale Universitii Al. I. Cuza Iai, s. Biologie animal, Tom LVI, 2010

Figure 2. The north-western area.

Figure 3. The eastern area.

Figure 4. The small dunes of the beach.

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The herpetofaunistic study consisted of extensive, visual and aural, transect surveys (Coglniceanu, 1997; Sutherland, 2006) carried out during spring and summer of the following periods: May 2007, July 2008 and May and August 2010. The specimens were identified following the literature (Fuhn, 1960; Fuhn & Vancea, 1961; Nllert & Nllert, 1995; Coglniceanu, 2000; Arnold & Burton, 2002) and photographed. Species protection status has been set according to Directive 92/43 EEC, RGO 57/2007 and the Red Data Book of Romanian Vertebrates (Iftime, 2005) Habitat situation has been assessed through vegetation analysis. The vegetation study was done according to the Braun-Blanquet methodology (Braun-Blanquet, 1964, Cristea et al. 2004). Results and Discussion Species account During the investigations we recorded 7 amphibian species and 6 reptile species. Bombina bombina (Fig. 5) have been cited previously from the study area (Fuhn, 1971; Coglniceanu et al., 2000; Szkely et al., 2009). We found it in channels and temporary and permanent ponds especially during the reproduction period. The individuals prefer the habitats with shallow water and lush aquatic vegetation. The species is distributed everywhere in the area, except for the beach. Pelobates fuscus (Fig. 6). The records of this species are relatively old (Fuhn, 1971; Oel, 1992). The situation may be due to its nocturnal activity pattern. Indeed, we observed numerous individuals after dusk when they were emerging from the sand to forage. During the day we accidentally sow a few specimens. The highest densities for the species were observed on the sand dykes covered that cross the wet area between the village and the beach. It seems that the individuals prefer the sands with vegetation, and avoid the barren ones, as they are absent on the sands near the sea shore.

Figure 5. Bombina bombina

Figure 6. Pelobates fuscus

Bufo viridis (Fig. 7) has been previously recorded from the area (Fuhn, 1971; Oel, 1992; Szkely et al., 2009). We found it mainly in and around the village, in anthropogenic habitats. Hyla arborea. This species is diffusely distributed in the area. We manage to record its presence mainly by hearing its calls that occur especially during the sunset. The individuals were recorded from the habitat in the north of the village and from the flat area towards the sea (Fig. 8). The species was previously mentioned from Sfntu Gheorghe (Oel, 1992).

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Figure 7. Bufo viridis

Figure 8. Hyla arborea

Pelophylax esculentus complex. The green frogs are present in every body of water, especially permanent ones (in the channel in that surrounds the village, the one that borders the study area to the west, and in the marshes between the village and the sea, to the east). All the three species have been recorded previously from the area: Pelophylax lessonae (Oel, 2000), Pelophylax kl. esculentus and Pelophylax ridibundus (Fuhn, 1960; Popescu, 1973; Oel, 1992; Coglniceanu et al., 2000; Szkely et al., 2009). Whereas P. kl. esculentus and P. ridibundus have a constant presence, P. lessonae is less frequent and we observed it in the eastern marshes. Species identification was carried out through the pulse structure and duration of the calls: very jerky for P. ridibundus, jerky and relatively short for P. kl. esculentus, and smooth and relatively longer for P. lessonae (Zamfirescu, 2004). Emys orbicularis (Fig. 9) has been previously recorded from the area (Fuhn, 1971). We saw individuals near the marshes between the village and the sea. In the area to the north-west from the village and in the village we found dead individuals (Fig. 10). Probably, they were killed by vehicles.

Figure 9. Emys orbicularis

Figure 10. Emys orbicularis killed specimen

Eremias arguta (Fig. 11) appears only on some small dunes with vegetation, on the beach. It was previously recorded from the area (Fuhn, 1971).The lizards are active only during the day, especially in spring. They may coexist with Lacerta agilis in the same habitats. Lacerta agilis has been previously and recently recorded from the study area as L. agilis euxinica. (Fuhn, 1971, Trk, 1999, 2004; Gherghel & Strugariu, 2009). We found the individuals of in large numbers in the area to the north-west from the village. Fewer individuals have been observed on the small vegetated dunes near the sea shore
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together with the previous species. Our observations confirm also the presence of the erythronotus morph (Fig. 12).

Figure 11. Eremias arguta

Figure 12. Lacerta agilis euxinica erythronotus morph

Natrix natrix is constantly present in the study area towards north-west, in the village, and to the seashore. The species has been recorded in the past, as well (Fuhn, 1971; Trk, 2004). The snakes live near the ponds and channels, but they can also be found relatively far from water. We encountered many dead specimens, which were probably killed by vehicles, humans or boats (Fig. 13). In the study area there are two morphs, apart from the normal one, i.e. persa (Fig. 14) and melanistic (Fig. 15).

Figure 13. Natrix natrix killed specimen

Figure 14. Natrix natrix persa morph

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Figure 15. Natrix natrix melanic morph

Analele tiinifice ale Universitii Al. I. Cuza Iai, s. Biologie animal, Tom LVI, 2010

Natrix tessellata although previously observed (Fuhn, 1971) it is quite rare in the study area. We could see only one dead specimen in the village channel (Fig. 16).

Figure 16. Natrix tessellata dead specimen

Vipera ursinii (Fig. 17) is the most documented reptile from the study area (e.g.: Fuhn, 1971, Trk, 2002, Halpern et al., 2007; see Krecsak & Zamfirescu, 2008 for a comprehensive review). The population is concentrated in the area toward the north-west from the village, and has a density estimated around 5 individual/ha and an estimated size of 321 individuals (Strugariu et al., 2011). The vipers occur on the slighted elevated terraces covered with vegetation formed of plant communities of the associations Juncetum maritimi (Rbel 1930) Pignatti 1953, Juncetum littoralis Popescu et Sanda 1976, and Agropyretum elongati I. erbnescu 1968. This vegetation has a coverage between 50% and 100% that insures optimal conditions in terms of thermoregulation and refuge against predators. The population might cover a larger area that spans almost near the beach. This hypothesis is supported by the finding of a dead specimen on the path to the beach (Fig. 18). The specimen might have been carried to that location, but other observations (I. Popescu, pers. comm.) increase the likelihood of our hypothesis. Some species we have not observed have been recorded from the study area in the past: Lissotriton vulgaris (Fuhn, 1971), Triturus dobrogicus (Fuhn, 1971).

Fugure 17. Vipera ursinii

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Figure 18. Vipera ursinii killed specimen

Anthropogenic impact and conservation Eleven of the identified species are included in the annexes of the Directive 92/43/EEC/1992 (Table 1.). One amphibian and two reptiles are species of Community interest whose conservation requires the designation of special conservation area. Other four species of amphibians and two species of reptiles are species of Community interest in need of strict protection. Of the 13 identified species 12 are included in the annexes of the RGO 57/2007. From the Romanian Red List perspective, three are vulnerable, one is endangered and one is critically endangered. The threats for the studied species fall into two main categories: habitat alteration and killing with or without intention (see Figs. 10, 13, 16, 18). The most evident habitat alteration consists of construction (Fig. 19) littering (Fig. 20), which alters the very area where Vipera usrinii, the critically endangered species exists.

Figure 19. Construction site in the habitat of Vipera urinii.

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Figure 20. Village dump site in the habitat of Vipera urinii.

Analele tiinifice ale Universitii Al. I. Cuza Iai, s. Biologie animal, Tom LVI, 2010

Table 1. Identified amphibian and reptile species and protection status.

Class Order Family Bombinatoridae Bufonidae Hylidae Pelobatidae Species Bombina bombina Bufo viridis Hyla arborea Pelobates fuscus Pelophylax ridibundus Pelophylax kl. esculentus Pelophylax lessonae Emys orbicularis Eremias arguta Lacerta agilis Natrix natrix Natrix tessellata Vipera ursinii Directive 92/43/EEC 1992 2a 4a 4a 4a 5a 5a 4a 2a 4a 4a 2a RGO 57/2007 3a 4Aa 4Aa 3a 5Aa 5Aa 4Ba 3a 4Ba 4Aa 4Aa 3a Red list (Iftime 2005) Nearly threatened Nearly threatened Vulnerable Vulnerable Vulnerable Endangered Nearly threatened Critically endangered

Amphibia

Anura

Ranidae

Chelonii

Emydidae Lacertidae

Reptilia

Squamata

Colubridae Viperidae

Directive 92/43/EEC/1992 2a Annex IIa: Animal species of Community interest whose conservation requires the designation of special areas of conservation 4a Annex IVa: Animal species of Community interest in need of strict protection 5a Annex Va: Animal species of Community interest whose taking in the wild and exploitation may be subject to management measures RGO 57/2007 3 Annex 3a: Animal species of Community interest whose conservation requires the designation of special areas of conservation 4Aa Annex 4Aa: Animal species of Community interest in need of strict protection 4Ba Annex 4Ba: Animal species of national interest in need of strict protection 5Aa Annex 5a: Animal species of Community interest (except birds) whose taking in the wild and exploitation may be subject to management measures

Because of the high number of protected species, the studied area is important for the protection of amphibians and reptiles at national and European level, and therefore efficient protective measures must be taken to reduce the above mention threats. Acknowledgements This work was supported by CNCSIS-UEFISCSU, project PNII-IDEI 2098/2008. We express our gratitude to CMN and INDD for issuing the research permits. We wish to thank Mihail V. Huuleac-Volosciuc, Andrei Mizeru and Valentina Moraru, Anca Pavel, Tiberiu C. Sahlean and Cristina Strugariu for their valuable assistance during fieldwork.
References Arnold, E. N., Burton, J. A., 2002. Gia de campo de los reptiles y amfibios de Espaa y Europa. Vives, V. Trans. Ediciones Omega, Barcelona. Braun-Blanquet, J., 1964. Pflanzensoziologie, Grundzge der Vegetationskunde. 2nd edition, Springer Verlag, Wien-New York. Coglniceanu, D., 1997. Practicum de ecologie a amfibienilor: Metode i tehnici n studiul ecologiei amfibienilor. Ed. Universitii Bucureti. Coglniceanu, D., Aioanei F., Matei B. 2000 Amfibienii din Romnia. Determinator. Ed. Ars Docendi, Bucureti.

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tefan R. Zamfirescu et al. Cox, N.A., Temple, H.J., 2009. European Red List of Reptiles. Luxembourg: Office for Official Publications of the European Communities. Cristea, V., Gafta, D., Pedrotti, F., 2004. Fitosociologie. Ed. Presa Universitar Clujean, Cluj-Napoca. European Commission, 1992. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora (online). Official Journal L 206, 22/07/1992 P. 0007-0050. Consolidated version 01.01.2007. Available at: http://ec.europa.eu/ environment/ nature/ legislation/habitatsdirective /index_en.htm. Fuhn, I., Vancea, S., 1961, Fauna R.P.R. Reptilia (estoase, oprle, erpi). Vol. 14, Fasc. 2. Ed. Academiei R.P.R, Bucureti. Fuhn, I., 1960. Fauna R.P.R Amphibia. Vol. 14, Fasc. 1. Ed. Academiei R.P.R., Bucureti. Fuhn, I., 1971. Amfibii i reptile din Delta Dunrii. Peuce: Studii i Comunicri de tiinele Naturii, 373-378. Gtescu P., tiuc R. (eds.), 2006. Delta Dunrii Rezervaie a Biosferei. Editura Dobrogea, CD Press, Constana, pp. 451-455. Gherghel, I., Strugariu, A., 2009. Further Evidence of Phenotypic Plasticity in the Sand Lizard: The erythronotus colour morph in the Pontic Sand Lizard (Lacerta agilis euxinica). Herpetologica Romanica, 3: 77-79. Halpern, B., Major, ., Pchy, T., Marinov, E.M., Kiss, J.B., 2007. Genetic comparison of Moldavian Meadow Viper (Vipera ursinii moldavica) populations of the Danube-Delta. Scientific Annals of the Danube Delta Institute for Research and Development, Tulcea-Romania 13: 19-26. Iftime, A., 2005. Reptilia. Amphibia. In: Botnariuc, N., Tatole, V. (eds.), Cartea Roie a Vertebratelor din Romnia. Ed. Curtea Veche, Bucureti. Krecsak L., Zamfirescu .R.., 2008. Vipera (Acridophaga)ursinii in Romania: historical and present distribution. North-West. J. Zool. 4: 339359. Nllert, A., Nllert, C., 1995. Los amfibios de Europa: identificacin, amenazas, proteccin . Torres, E. Trans. Ediciones Omega, Barcelona. Oel, V., 1992. Investigaii herpetologice n rezervaia Biosferei Delta Dunrii (RBDD) n anul 1991. Analele tiinifice ale I.C.P.D.D., 1: 159-162. Oel, V. (ed.) 2000. The Red List of plant and animal species from the Danube Delta Biosphere Reserve Romania. Edit. Fundaia Aves, Tulcea. Popescu, M., 1973. Contribuii la cunoaterea hranei adulilor de Rana ridibunda ridibunda Pall. i Rana esculenta L. din judeul Tulcea. Peuce: Studii i Comunicri de tiinele Naturii, 397-408. Szkely, P., Pliau, R., Tudor, M., Coglniceanu, D., 2009. A preliminary record list of amphibians in Dobrudja (Romania). Analele tiinifice ale Universitii Al. I. Cuza Iai, s. Biologie Animal, 50: 145-153. Sutherland, W. J. (ed.), 2006. Ecological Census Techniques: A Handbook. 2nd edition. Cambridge University Press, New York. Strugariu, A., Zamfirescu, .R., Gherghel, I., Sahlean, T.C., Moraru, V., Zamfirescu, O., 2011. A preliminary study on population characteristics and ecology of the critically endangered meadow viper Vipera ursinii in the Romanian Danube Delta. Biologia, 66/1: DOI: 10.2478/s11756-010-0146-z. Temple, H.J., Cox, N.A., 2009. European Red List of Amphibians. Luxembourg: Office for Official Publications of the European Communities. Trk, Z., 1999. Contributions to the knowledge of the distribution of sand lizard ( Lacerta agilis euxinica Fuhn and Vancea 1964) in southeastern Romania. Analele tiinifice ale INDD, 7: 498-500. Trk, Z., 2002. Potential management plan for conservation of Vipera ursinii from the Danube Delta Biosphere Reserve (Romania). Analele tiinifice ale INDD. 9: 174-184. Trk, Z., 2004. Herpetological investigations in the Danube Delta Biosphere Reserve (Romania) in 2003. Analele tiinifice ale INDD, 10: 81-83. Zamfirescu, .R., 2004. Comparison between Water Frogs (Rana esculenta Complex) Mating Calls. Analele tiinifice ale Univ. Al.I. Cuza Iai, s. Biologie Animal, 50: 267-278.

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