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Threatening levels and extinction risks based on distributional, ecological and life-history datasets (DELH) versus IUCN criteria: example of Serbian reptiles

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Abstract

Recent studies on the world reptiles’ extinction risks pointed out that about 20 % of species are threatened, with another 20 % are data-deficient following IUCN criteria. IUCN set up criteria for assessment of extinction risk at global and regional scales, relying on distribution data, population parameters and quantitative analyses. Only 12 % of reptilian species were listed as globally threatened upon population data. Long-term population studies are time-consuming, thus it would be practical to use some other parameters for estimations of extinction risks. Threatening level (and extinction risks) of Serbian reptiles have never been investigated. We aimed to scrutinize species threatening level (thus set up conservation priorities) on the basis of distributional, ecological and life-history datasets (DELH). We estimated which traits are the most important for the conservation of species. Separately, we used IUCN criteria for regional level to assess extinction risk and compared them with the results obtained by analyses of DELH datasets. The two types of criteria gave similar estimates for the chelonian species. In snakes, two species exhibited higher conservation scores by DELH than by IUCN criteria, the opposite being true for two other species. In lizards, only two species had higher extinction risks by IUCN whereas five lizards were more threatened according to DELH. Our intention was not discredit the values of IUCN criteria for setting regional (or national) extinction risks, but to suggest that use of additional features other than IUCN could be valuable for estimation of threatening level and setting conservation priorities for cases where precise distribution and population data are not available.

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References

  • Agasyan A, Avci A, Tuniyev B, Crnobrnja-Isailović J, Lymberakis P, Andrén C, Cogalniceanu D, Wilkinson J, Ananjeva N, Üzüm N, Orlov N, Podloucky R, Tuniyev S, Kaya U, Böhme W, Ajtić R, Tok V, Ugurtas IH, Sevinç M, Crochet PA, Nettmann HK, Krecsák L (2009a) Darevskia praticola. In: The IUCN red list of threatened species, version 2014.2. www.iucnredlist.org

  • Agasyan A, Avci A, Tuniyev B, Crnobrnja-Isailović J, Lymberakis P, Andrén C, Cogalniceanu D, Wilkinson J, Ananjeva N, Üzüm N, Orlov N, Podloucky R, Tuniyev S, Kaya U, Böhme W, Nettmann HK, Joger U, Cheylan M, Pérez-Mellado V, Borczyk B, Sterijovski B, Westerström A, Schmidt B (2010b) Zootoca vivipara. In: The IUCN red list of threatened species, version 2014.2. www.iucnredlist.org

  • Ajtić R (2009) Morfološke, biogeografske i ekološke odlike Kočijevog gekona (Cyrtodactylus kotschyi Steindachner, 1870 Gekkonidae) sa kopnenog dela areala. Master Thessis, Prirodno-matematički fakultet Univerziteta u Nišu

  • Ajtić R, Tomović L (2001) First record of Kotschy’s gecko Cyrtodactylus kotschyi (Steindachner, 1870) (Gekkonidae, Lacertilia) in FR Yugoslavia. Arch Biol Sci 53:23–24

    Google Scholar 

  • Andreone F, Luiselli L (2000) The Italian batrachofauna and its conservation status: a statistical assessment. Biol Conserv 96:197–208

    Article  Google Scholar 

  • Berglind S-Å (2004) Area-sensitivity of the sand lizard and spider wasps in sandy pine heath forests—umbrella species for early successional biodiversity conservation? Ecol Bull 51:189–207

    Google Scholar 

  • Bertolero A, Cheylan M, Hailey A, Livoreil B, Willemsen RE (2011) Testudo hermanni (Gmelin 1789)—Hermann’s tortoise. In: Rhodin AGJ, Pritchard CH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB, Mittermeier RA (eds) Conservation Biology of freshwater turtles and tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian research monographs No. 5, Lunenburg, pp 059.1–059.20

    Google Scholar 

  • Böhm M, Collen B, Baillie JEM et al (2013) The conservation status of the world’s reptiles. Biol Conserv 157:372–385

    Article  Google Scholar 

  • Böhme W, Lymberakis P, Ajtić R, Haxhiu I, Crnbrnja-Isailović J, Sindaco R (2009a) Algyroides nigropunctatus. In: IUCN red list of threatened species, version 2013.1. www.iucnredlist.org

  • Böhme W, Lymberakis P, Ajtić R, Disi AMM, Werner Y, Tok V, Ugurtas IH, Sevinç M, Hraoui-Bloquet S, Sadek R, Crochet PA, Haxhiu I, Corti C, Sindaco R, Kaska Y, Kumlutaş Y, Avci A, Üzüm N, Yeniyurt C, Akarsu F, Crnobrnja-Isailović J (2009b) Mediodactylus kotschyi. In: IUCN red list of threatened species, version 2013.2. www.iucnredlist.org

  • Böhme W, Lymberakis P, Ajtić R, Tok V, Ugurtas IH, Sevinç M, Crochet PA, Haxhiu I, Sterijovski B, Krecsák L, Crnobrnja-Isailović J, Kaska Y, Kumlutaş Y, Avci A, Jelić D (2009c) Ablepharus kitaibelii. In: IUCN red list of threatened species, version 2014.2. www.iucnredlist.org

  • Böhme W, Lymberakis P, Ajtić R, Tok V, Ugurtas IH, Sevinç M, Crochet PA, Haxhiu I, Krecsák L, Sterijovski B, Crnobrnja-Isailović J, Podloucky R, Cogalniceanu D, Avci A (2009d) Podarcis tauricus. In: The IUCN red list of threatened species, version 2014.2. www.iucnredlist.org

  • Breininger DR, Mazerolle MJ, Bolt MR, Legare ML, Drese JH, Hines JE (2012) Habitat fragmentation effects on annual survival of the federally protected eastern indigo snake. Anim Conserv 15:361–368

    Article  Google Scholar 

  • Conway-Gómez K (2007) Effects of human settlements on abundance of Podocnemis unifilis and P. expansa turtles in northeastern Bolivia. Chelonian Conserv Biol 6:199–205

    Article  Google Scholar 

  • Cox NA, Temple HJ (2009) European red list of reptiles. Office for Official Publications of the European Communities, Luxembourg

    Google Scholar 

  • Crnobrnja-Isailović J, Aleksić I (1999) First record of Coluber najadum Eichwald (1831) in Serbia. Arch Biol Sci 51:47–48

    Google Scholar 

  • Crnobrnja-Isailović J, Ajtić R, Tomović L (2007) Activity patterns of the sand viper (Vipera ammodytes) from the central Balkans. Amphibia-Reptilia 28:582–589

    Article  Google Scholar 

  • Crnobrnja-Isailović J, Ajtić R, Vogrin M, Corti C, Pérez Mellado V, Sá-Sousa P, Cheylan M, Pleguezuelos JM, Lymberakis P, Sindaco R, Romano A, Jelić D (2009a) Elaphe quatuorlineata. In: IUCN red list of threatened species, version 2013.2. www.iucnredlist.org

  • Crnobrnja-Isailović J, Vogrin M, Corti C, Sá-Sousa P, Cheylan M, Pleguezuelos JM, Tomović L, Sterijovski B, Joger U, Westerström A, Borczyk B, Schmidt B, Meyer A, Sindaco R, Jelić D (2009b) Vipera berus. In: IUCN red list of threatened species, version 2013.2. www.iucnredlist.org

  • Diamond WJ (2010) Population decline in the endangered grassland earless dragon in Australia: identification, causes and management. Dissertation, University of Canberra

  • Dury C (1910) The passenger pigeon. J Cincinnati Soc Nat Hist 21:52–56

    Google Scholar 

  • Džukić G, Kalezić ML (2004) The biodiversity of amphibians and reptiles in the Balkan Peninsula. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity: pattern and process in the European hotspot. Kluwer Academic Publishers, Dordrecht, pp 167–192

    Google Scholar 

  • Džukić G, Pasuljević G (1979) O rasprostranjenju ljuskavog gustera Algyroides nigropunctatus (Dumeril et Bibron, 1839) (Reptilia, Lacertidae). Biosistematika 5:61–70

    Google Scholar 

  • Džukić G, Purger J (1988) Significance of adder, Vipera berus (Linnaeus, 1758) presence in Vojvodina. Arch Biol Sci 40:13–14

    Google Scholar 

  • Filippi E, Luiselli L (2000) Status of the Italian snake fauna and assessment of conservation threats. Biol Conserv 93:219–225

    Article  Google Scholar 

  • Franco D, Akani GC, Ebere N, Luiselli L (2013) Using the river Niger delta local communities’ ecological knowledge to support the scientific evidence of snake declines. Herpetozoa 25:133–142

    Google Scholar 

  • Galán P (2004) Structure of a population of the lizard Podarcis bocagei in northwest Spain: variations in age distribution, size distribution and sex ratio. Anim Biol 54:57–75

    Article  Google Scholar 

  • Gerlach J (2008) Fragmentation and demography as causes of population decline in Seychelles freshwater turtles (genus Pelusios). Chelonian Conserv Biol 7:78–87

    Article  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, Déjà Vu Amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Goiran C, Shine R (2013) Decline in sea snake abundance on a protected coral reef system in the New Caledonian Lagoon. Coral Reefs 32:281–284

    Article  Google Scholar 

  • Gvoždík V, Jandzik D, Lymberakis P, Jablonski D, Moravec J (2010) Slow worm, Anguis fragilis (Reptilia: Anguidae) as a species complex: Genetic structure reveals deep divergences. Mol Phylogenet Evol 55:460–472

    Article  PubMed  Google Scholar 

  • Hagman M, Elmberg J, Karvemo S, Lowenborg K (2012) Grass snakes (Natrix natrix) in Sweden decline together with their anthropogenic nesting-environments. Herpetol J 22:199–202

    Google Scholar 

  • Hailey A, Willemsen RE (2003) Changes in the status of tortoise populations in Greece 1984–2001. Biodivers Conserv 12:991–1011

    Article  Google Scholar 

  • Ihlow F, Dambach J, Engler JO, Flecks M, Hartmann T, Nekum S, Rajaei H, Rödder D (2012) On the brink of extinction? How climate change may affect global chelonian species richness and distribution. Global Change Biol 18:1520–1530

    Article  Google Scholar 

  • IUCN (2001) IUCN red list categories and criteria: version 3.1. IUCN Species Survival Commission, IUCN, Gland. https://portals.iucn.org/library/efiles/documents/RL-2001-001-2nd.pdf

  • IUCN (2003) Guidelines for application of IUCN criteria at regional levels. Version 4.0. IUCN Species Survival Commission, IUCN, Gland. https://portals.iucn.org/library/efiles/documents/RL-2012-002.pdf

  • Jelić D, Ajtić R, Sterijovski B, Crnobrnja-Isailović J, Lelo S, Tomović L (2012a) Distribution of the genus Vipera in the western and central Balkans (Squamata: Serpetntes: Viperidae). Herpetozoa 25:109–132

    Google Scholar 

  • Jelić D, Kuljerić M, Koren T, Treer D, Šalamon D, Lončar M, Podnar-Lešić M, Janev-Hutinec B, Bogdanović T, Mekinić S, Jelić K (2012b) Crvena knjiga vodozemaca i gmazova Hrvatske. Ministarstvo zaštite okoliša i prirode, Državni zavod za zaštitu prirode, Republika Hrvatska

  • Joger U, Crnobrnja-Isailović J, Vogrin M, Corti C, Sterijovski B, Westerström A, Krecsák L, Pérez Mellado V, Sá-Sousa P, Cheylan M, Pleguezuelos JM, Sindaco R (2009) Vipera ursinii. In: IUCN 2013, IUCN red list of threatened species. version 2013.2. www.iucnredlist.org

  • Jović D (2000) Populacione karakteristike i zaštita planinskog gustera Zootoca vivipara (Jacquin, 1787) centralnog dela Balkanskog poluostrva. Master Thesis, Univerzitet u Novom Sadu

  • Lampinen R (2001) Universal transverse mercator (UTM) and military grid reference system (MGRS). http://www.fmnh.helsinki.fi/english/botany/afe/map/utm.htm

  • Ljubisavljević K, Jović D, Džukić G (2010) Morphological variation of the common lizard (Zootoca vivipara Jacquin, 1787) in the central Balkans. Arch Biol Sci 62:791–798

    Google Scholar 

  • Ljubisavljević K, Džukić G, Kalezić ML (2011) An overview of the trade issues concerning the true tortoises (Testudo spp.) in the former Yugoslavia. North-West J Zool 7:250–260

    Google Scholar 

  • Ljubisavljević K, Džukić G, Vukov TD, Kalezić ML (2014) Distribution patterns of Hermann’s tortoise Testudo hermanni Gmelin, 1789, in the region of former Yugoslavia (Testudines: Testudinidae). Herpetozoa 26:125–138

    Google Scholar 

  • Luiselli L (2003) Comparative abundance and population structure of sympatric Afrotropical tortoises in six rainforest areas: the differential effects of ‘‘traditional veneration’’ and of ‘‘subsistence hunting’’ by local people. Acta Oecol 24:157–163

    Article  Google Scholar 

  • Luiselli L (2009) A model assessing the conservation threats to freshwater turtles of sub-Saharan Africa predicts urgent need for continental conservation planning. Biodivers Conserv 18:1349–1360

    Article  Google Scholar 

  • Luiselli L, Capula M, Burke RL, Rugiero L, Capizzi D (2014) Sighting frequency decreases over two decades in three populations of Testudo hermanni from central Italy. Biodivers Conserv. doi:10.1007/s10531-014-0766-7

    Google Scholar 

  • Lymberakis P, Ajtić R, Tok V, Ugurtas IH, Sevinç M, Crochet P-A, Disi AMM, Hraoui-Bloquet S, Sadek R, Haxhiu I, Böhme W, Agasyan A, Tuniyev B, Ananjeva N, Orlov N (2009a) Platyceps najadum. In: IUCN red list of threatened species, version 2013.2. www.iucnredlist.org

  • Lymberakis P, Crnobrnja-Isailović J, Ajtić R, Vogrin M, Böhme W (2009b) Podarcis erhardii. In: IUCN red list of threatened species, version 2013.2. www.iucnredlist.org

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pasuljević G (1965) Ritam dnevne i sezonske aktivnosti Ablepharus kitaibelii (Bibron et Bory) u Jugoslaviji. Glas Prir Muzeja Beogr B 20:311–314

    Google Scholar 

  • Pasuljević G (1966) Prilog poznavanju ekologije Ablepharus kitaibelii (Bibron et Bory). Zb filoz Fak Prištini 3:459–463

    Google Scholar 

  • Peterman WE, Feist SM, Semlitsch RD, Eggert LS (2013) Conservation and management of peripheral populations: spatial and temporal influences on the genetic structure of wood frog (Rana sylvatica) populations. Biol Conserv 158:351–358

    Article  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Stastistical Computing, Vienna

    Google Scholar 

  • Ralev A, Popović M, Ružić M, Shurulinkov P, Daskalova G, Crnobrnja-Isailović J (2012) A new record of Testudo graeca ibera PALLAS, 1814, in southern Serbia. Herpetozoa 25:151–153

    Google Scholar 

  • Reading CJ, Luiselli LM, Akani GC, Bonnet X, Amori G, Ballouard J-M, Filipii E, Naulleau G, Pearson D, Rugiero L (2010) Are snake populations in widespread decline? Biol Lett 6:777–780

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ristić N, Tomović L, Ajtić R, Crnobrnja-Isailović J (2006) First record of the four-lined snake Elaphe quatuorlineata (Lacépède, 1789) in Serbia. Acta Herpetol 1:135–139

    Google Scholar 

  • Sinervo B, Méndez-de-la-Cruz F, Miles DB et al (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899

    Article  CAS  PubMed  Google Scholar 

  • Smith MJ, Cogger H, Tiernan B, Maple D, Boland C, Napier F, Detto T, Smith P (2012) An oceanic island reptile community under threat: the decline of reptiles on Christmas Island, Indian ocean. Herpetol Conserv Biol 7:206–218

    Google Scholar 

  • Speybroeck J, Beukema W, Crochet P-A (2010) A tentative species list of the European herpetofauna (Amphibia and Reptilia)—an update. Zootaxa 2492:1–27

    Google Scholar 

  • Stevanović V, Stevanović B (1995) Basic climatic, geological and pedological factors of the diversity of terrestrial ecosystems in Yugoslavia. In: Stevanović V, Vasić V (eds) Biodiversity of Yugoslavia with review of internationally important species. Ecolibri, Biološki fakultet, Beograd, pp 75–95

    Google Scholar 

  • Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger HL, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Townsend Peterson A, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148

    Article  CAS  PubMed  Google Scholar 

  • Tomović L, Ajtić R, Đoković Đ, Antić S (2004) Records of Testudo graeca ibera Pallas, 1814 in Serbia and Montenegro. Herpetozoa 17:189–191

    Google Scholar 

  • Tomović L, Ajtić R, Ljubisavljević K, Urošević A, Jović D, Krizmanić I, Labus N, Đorđević S, Kalezić ML, Vukov T, Džukić G (2014) Reptiles in Serbia—Distribution and diversity patterns. Bull Nat Hist Mus Belgrade 7:129–158

    Google Scholar 

  • Tomović L, Urošević A, Ajtić R, Krizmanić I, Simović A, Labus N, Jović D, Krstić M, Đorđević S, Anđelković M, Golubović A, Džukić G (2015) Contribution to the knowledge of distribution of Colubrid snakes in Serbia. Ecol Montenegrina 2:162–186

    Google Scholar 

  • Turtle Conservation Coalition, Rhodin AGJ, Walde AD, Horne BD, Van Dijk PP, Blanck T, Hudson R (eds) (2011) Turtles in trouble: the world’s 25+ most endangered tortoises and freshwater turtles—2011. IUCN/SSC Tortoise and Freshwater Turtle Specialist Group, Turtle Conservation Fund, Turtle Survival Alliance, Turtle Conservancy, Chelonian Research Foundation, Conservation International, Wildlife Conservation Society, San Diego Zoo Global, Lunenburg

  • Uetz P, Hošek J (eds) (2014) The reptile database. http://www.reptile-database.org. Accessed 8 Dec 2014

  • Ursenbacher S, Schweiger S, Tomović L, Crnobrnja-Isailović J, Fumagalli L, Mayer W (2008) Molecular phylogeography of the nose-horned viper (Vipera ammodytes, (Linnaeus, 1758)): evidence for high genetic diversity and multiple refugia in the Balkan Peninsula. Mol Phylogenet Evol 46:1116–1128

    Article  CAS  PubMed  Google Scholar 

  • Vukov TD, Tomović L, Krizmanić I, Labus N, Džukić G, Jović D, Kalezić ML (2015) Conservation issues of Serbian Amphibians based on distributional, life history and ecological data. Acta Zool Bulg 67(1):105–116

    Google Scholar 

  • Whitfield SM, Bell KE, Philippi T, Sasa M, Bolaños F, Chaves G, Savage JM, Donnelly MA (2007) Amphibian and reptile declines over 35 years at La Selva, Costa Rica. PNAS 104:8352–8356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly supported by: Ministry of Education, Science and Technological Development of Republic of Serbia (Grant No. 173043). Many thanks to M. Andjelković, S. Antić, A. Golubović, A. Ivanović, M. Krstić, M. Marković, A. Simović, M. Slijepčević, M. Vujošević, and V. Žikić for generously providing field distribution data. We are grateful to four anonymous reviewers for valuable comments of the manuscript.

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Authors and Affiliations

  1. Faculty of Biology, University of Belgrade, Studentski trg 16, Belgrade, 11000, Serbia

    L. Tomović, I. Krizmanić & S. Đorđević

  2. Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar Despota Stefana 142, Belgrade, 11000, Serbia

    A. Urošević, T. Vukov, K. Ljubisavljević, M. L. Kalezić & G. Džukić

  3. Institute for Nature Conservation of Serbia, Dr Ivana Ribara 91, Belgrade, 11070, Serbia

    R. Ajtić

  4. Institute for Nature Conservation of Serbia, Vožda Karađorđa 14, Nis, 18000, Serbia

    D. Jović

  5. Biology Department, Faculty of Science and Mathematics, University of Priština, Lole Ribara 29, Kosovska Mitrovica, 38220, Serbia

    N. Labus

  6. Niger Delta Ecology and Biodiversity Conservation Unit, Department of Applied and Environmental Biology, Rivers State University of Science and Technology, PMB5080, Port Harcourt, Rivers State, Nigeria

    L. Luiselli

  7. Centre of Environmental Studies Demetra, Via Olona 7, 00198, Rome, Italy

    L. Luiselli

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  1. L. Tomović
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Communicated by Marcelo F. Tognelli.

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Tomović, L., Urošević, A., Vukov, T. et al. Threatening levels and extinction risks based on distributional, ecological and life-history datasets (DELH) versus IUCN criteria: example of Serbian reptiles. Biodivers Conserv 24, 2913–2934 (2015). https://doi.org/10.1007/s10531-015-0984-7

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