, Volume 693, Issue 1, pp 157–167 | Cite as

Using ecological niche modeling to predict the distributions of two endangered amphibian species in aquatic breeding sites

Primary Research Paper


Amphibians are among the most threatened taxonomic groups worldwide. A fundamental step in species conservation is identifying the habitat requirements of the target species. However, this determination can often be problematic in endangered species because, by definition, they often only occupy a very limited number of sites. Moreover, when found, they are often in low abundance, and thus their detectability is low, yielding false “absence” data. Maximum entropy niche modeling provides a tool using only the presence data to predict potential habitat distributions of endangered species whose distributions have become highly limited. We provide two examples in the current study for the fire salamander, Salamandra infraimmaculata, and the green toad, Bufo viridis. S. infraimmaculata is considered endangered in Israel and near endangered worldwide. B. viridis is classified as locally endangered in Israel. Soil type was the most important predictor of the distribution of S. infraimmaculata and, to a lesser extent, also predicted the distribution of B. viridis. In addition, S. infraimmaculata larvae were also associated with high elevation areas. B. viridis was negatively associated with distance to urban areas and low solar radiation level. The potential distribution maps determined for S. infraimmaculata and B. viridis can help in planning future wetland use management around its existing populations, discovering new populations, identifying top-priority survey sites, or set priorities to restore its natural habitat for more effective conservation.


Bufo viridis Maxent Salamandra infraimmaculata Small sample size Species distribution model 



This study was funded by ISF grant 961-2008 awarded to Leon Blaustein and Shirli Bar-David and a scholarship provided by the Israel Council for Higher Education awarded to Lior Blank. The authors thank Miska Luoto, Rami Zaidenberg, Asaf Sadeh, and Arik Kershenbaum for fruitful discussions, two anonymous reviewers for improving the manuscript, and Ori Segev for valuable help in fieldwork. Field surveys of S. infraimmaculata and B. viridis larvae were conducted with permission from the Israel Nature and Parks Authority (permit 2009/36565).


  1. Attias, N., D. S. L. Raices, F. S. Pessoa, H. Albuquerque, T. Jordao-Nogueira, T. C. Modesto & H. G. Bergallo, 2009. Potential distribution and new records of Trinomys species (Rodentia: Echimyidae) in the State of Rio de Janeiro. Zoologia (Curitiba, Impresso) 26: 305–315.CrossRefGoogle Scholar
  2. Austin, M. & J. Meyers, 1996. Current approaches to modelling the environmental niche of eucalypts: implication for management of forest biodiversity. Forest Ecology and Management 85: 95–106.CrossRefGoogle Scholar
  3. Bar-David, S., O. Segev, N. Peleg, N. Hill, A. R. Templeton, C. B. Schultz & L. Blaustein, 2007. Long-distance movements by Fire Salamanders (Salamandra Infraimmaculata) and implications for habitat fragmentation. Israel Journal of Ecology and Evolution 53: 143–159.Google Scholar
  4. Bennie, J., B. Huntley, A. Wiltshire, M. O. Hill & R. Baxter, 2008. Slope, aspect and climate: spatially explicit and implicit models of topographic microclimate in chalk grassland. Ecological Modelling 216: 47–59.CrossRefGoogle Scholar
  5. Beven, K. J. & M. J. Kirkby, 1979. A physically based, variable contributing area model of basin hydrology/Un modèle à base physique de zone d’appel variable de l’hydrologie du bassin versant. Hydrological Sciences Journal 24: 43–69.Google Scholar
  6. Billeter, R., J. Liira, D. Bailey, R. Bugter, P. Arens, I. Augenstein, S. Aviron, J. Baudry, R. Bukacek & F. Burel, 2008. Indicators for biodiversity in agricultural landscapes: a pan European study. Journal of Applied Ecology 45: 141–150.CrossRefGoogle Scholar
  7. Blaustein, L. & S. S. Schwartz, 2001. Why study ecology in temporary pools? Israel Journal of Zoology 47: 303–312.CrossRefGoogle Scholar
  8. Blaustein, A. R. & D. B. Wake, 1995. The puzzle of declining amphibian populations. Scientific American 272: 52–57.CrossRefGoogle Scholar
  9. Bradford, D. F., A. C. Neale, M. S. Nash, D. W. Sada & J. R. Jaeger, 2003. Habitat patch occupancy by toads (Bufo punctatus) in a naturally fragmented desert landscape. Ecology 84: 1012–1023.CrossRefGoogle Scholar
  10. Calsbeek, R., J. N. Thompson & J. E. Richardson, 2003. Patterns of molecular evolution and diversification in a biodiversity hotspot: the California Floristic Province. Molecular Ecology 12: 1021–1029.PubMedCrossRefGoogle Scholar
  11. Carmel, Y. & L. Stoller-Cavari, 2006. Comparing environmental and biological surrogates for biodiversity at a local scale. Israel Journal of Ecology and Evolution 52: 11–27.CrossRefGoogle Scholar
  12. Costa, G. C., C. Nogueira, R. B. Machado & G. R. Colli, 2010. Sampling bias and the use of ecological niche modeling in conservation planning: a field evaluation in a biodiversity hotspot. Biodiversity and Conservation 19: 883–899.CrossRefGoogle Scholar
  13. Davies, Z. G., R. J. Wilson, S. Coles & C. D. Thomas, 2006. Changing habitat associations of a thermally constrained species, the silver spotted skipper butterfly, in response to climate warming. Journal of Animal Ecology 75: 247–256.PubMedCrossRefGoogle Scholar
  14. Dayton, G. H., R. E. Jung & S. Droege, 2004. Large-scale habitat associations of four desert anurans in Big Bend National Park, Texas. Journal of Herpetology 38: 619–627.CrossRefGoogle Scholar
  15. Degani, G., 1996. Salamandra salamandra at the Southern Limit of Its Distribution. Laser Pages Publication, Kazrin, Israel.Google Scholar
  16. deMaynadier, P. G. & M. L. Hunter, 1998. Effects of silvicultural edges on the distribution and abundance of amphibians in Maine. Conservation Biology 12: 340–352.CrossRefGoogle Scholar
  17. Diller, L. V. & R. L. Wallace, 1999. Distribution and habitat of Ascaphus truei in streams on managed, young growth forests in north coastal California. Journal of Herpetology 33: 71–79.CrossRefGoogle Scholar
  18. Dolev, A. & A. Perevolotsky, 2004. The Red Book – Vertebrates in Israel. Israel Nature and Parks Authority and The Society for the Protection of Nature in Israel, Jerusalem, Israel.Google Scholar
  19. Elith, J., C. H. Graham, R. P. Anderson, M. Dudík, S. Ferrier, A. Guisan, R. J. Hijmans, F. Huettmann, J. R. Leathwick & A. Lehmann, 2006. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29: 129–151.CrossRefGoogle Scholar
  20. Elith, J., S. J. Phillips, T. Hastie, M. Dudík, Y. E. Chee & C. J. Yates, 2011. A statistical explanation of MaxEnt for ecologists. Diversity and Distributions 17: 43–57.CrossRefGoogle Scholar
  21. Elron, E., A. Gasith & S. Gaphny, 2005. Increased occupancy of the green toad (Bufo viridis), a possible syndrome of a population in trouble. Israel Journal of Zoology 51: 63.Google Scholar
  22. Engler, R., A. Guisan & L. Rechsteiner, 2004. An improved approach for predicting the distribution of rare and endangered species from occurrence and pseudo absence data. Journal of Applied Ecology 41: 263–274.CrossRefGoogle Scholar
  23. Ensabella, F., S. Loriga, P. Formichetti, R. Isotti & A. Sorace, 2003. Breeding site selection of Bufo viridis in the city of Rome (Italy). Amphibia Reptilia 24: 396–399.CrossRefGoogle Scholar
  24. Ferrier, S., G. Watson, J. Pearce & M. Drielsma, 2002. Extended statistical approaches to modelling spatial pattern in biodiversity in northeast New South Wales. I. Species-level modelling. Biodiversity and Conservation 11: 2275–2307.CrossRefGoogle Scholar
  25. Fielding, A. H. & J. F. Bell, 1997. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24: 38–49.CrossRefGoogle Scholar
  26. Gaston, K. J. & P. H. Williams, 1996. Spatial patterns in taxonomic diversity. In Gaston, K. J. (ed.), Biodiversity: A Biology of Numbers and Difference. Blackwell Science Ltd., Oxford, UK: 202–229.Google Scholar
  27. Geiger, R., 1965. The Climate Near the Ground. Harvard University Press, Cambridge, MA.Google Scholar
  28. Gessler, P., O. Chamran, F. Althouse & L. Holmes, 2000. Modeling soil–landscape and ecosystem properties using terrain attributes. Soil Science Society of America Journal 64: 2046.CrossRefGoogle Scholar
  29. Gibbs, J. P., 1998. Amphibian movements in response to forest edges, roads, and streambeds in southern New England. The Journal of Wildlife Management 62: 584–589.CrossRefGoogle Scholar
  30. Gibson, L., B. Wilson, D. Cahill & J. Hill, 2004. Spatial prediction of rufous bristlebird habitat in a coastal heathland: a GIS based approach. Journal of Applied Ecology 41: 213–223.CrossRefGoogle Scholar
  31. Goldberg, T., O. Pearlson, E. Nevo & G. Degani, 2007. Mitochondrial DNA analysis of Salamandra infraimmaculata larvae from habitats in northern Israel. Progrese şi Perspective in Medicina Veterinară – Lucrări ştiinţifice 50: 23–31.Google Scholar
  32. Guerry, A. D. & M. L. Hunter Jr, 2002. Amphibian distributions in a landscape of forests and agriculture: an examination of landscape composition and configuration. Conservation Biology 16: 745–754.CrossRefGoogle Scholar
  33. Guisan, A. & W. Thuiller, 2005. Predicting species distribution: offering more than simple habitat models. Ecology Letters 8: 993–1009.CrossRefGoogle Scholar
  34. Guisan, A. & N. E. Zimmermann, 2000. Predictive habitat distribution models in ecology. Ecological Modelling 135: 147–186.CrossRefGoogle Scholar
  35. Guisan, A., C. H. Graham, J. Elith, F. Huettmann & the NCEAS Species Distribution Modelling Group, 2007. Sensitivity of predictive species distribution models to change in grain size. Diversity and Distributions 13:332–340.Google Scholar
  36. Hall, J. K., R. Weinberger, S. Marco & G. Steinitz, 1999. Test of the Accuracy of the DEM of Israel. Geological Survey of Israel, Jerusalem.Google Scholar
  37. Hamer, A. J. & M. J. McDonnell, 2008. Amphibian ecology and conservation in the urbanising world: a review. Biological Conservation 141: 2432–2449.CrossRefGoogle Scholar
  38. Hardy, R., 1945. The influence of types of soil upon the local distribution of some mammals in southwestern Utah. Ecological Monographs 15: 71–108.CrossRefGoogle Scholar
  39. Hartel, T., S. Nemes, L. Demeter & K. Ollerer, 2008. Pond and landscape characteristics which is more important for common toads (Bufo bufo)? A case study from central Romania. Applied Herpetology 5: 1–12.CrossRefGoogle Scholar
  40. Hartel, T., O. Schweiger, K. Öllerer, D. Cogalniceanu & J. W. Arntzen, 2010. Amphibian distribution in a traditionally managed rural landscape of Eastern Europe: probing the effect of landscape composition. Biological Conservation 143: 1118–1124.CrossRefGoogle Scholar
  41. Hendrickx, F., J. P. Van Maelfait, W. Wingerden, O. Schweiger, M. Speelmans, S. Aviron, I. Augenstein, R. Billeter, D. Bailey & R. Bukacek, 2007. How landscape structure, land use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. Journal of Applied Ecology 44: 340–351.CrossRefGoogle Scholar
  42. Henkin, Z., N. Seligman, U. Kafkafi & D. Prinz, 1998. End-of-season soil water depletion in relation to growth of herbaceous vegetation in a sub-humid Mediterranean dwarf-shrub community on two contrasting soils. Plant and Soil 202: 317–326.CrossRefGoogle Scholar
  43. Hermosilla, C., F. Rocha & V. D. Valavanis, 2011. Assessing Octopus vulgaris distribution using presence-only model methods. Hydrobiologia 670: 35–47.CrossRefGoogle Scholar
  44. Hernandez, P. A., C. H. Graham, L. L. Master & D. L. Albert, 2006. The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29: 773–785.CrossRefGoogle Scholar
  45. Hernandez, P. A., I. Franke, S. K. Herzog, V. Pacheco, L. Paniagua, H. L. Quintana, A. Soto, J. J. Swenson, C. Tovar & T. H. Valqui, 2008. Predicting species distributions in poorly-studied landscapes. Biodiversity and Conservation 17: 1353–1366.CrossRefGoogle Scholar
  46. Herrmann, H. L., K. J. Babbitt, M. J. Baber & R. G. Congalton, 2005. Effects of landscape characteristics on amphibian distribution in a forest-dominated landscape. Biological Conservation 123: 139–149.CrossRefGoogle Scholar
  47. Kirk, T. A. & W. J. Zielinski, 2009. Developing and testing a landscape habitat suitability model for the American marten (Martes americana) in the Cascades mountains of California. Landscape Ecology 24: 759–773.CrossRefGoogle Scholar
  48. Knutson, M. G., J. R. Sauer, D. A. Olsen, M. J. Mossman, L. M. Hemesath & M. J. Lannoo, 1999. Effects of landscape composition and wetland fragmentation on frog and toad abundance and species richness in Iowa and Wisconsin, USA. Conservation Biology 13: 1437–1446.CrossRefGoogle Scholar
  49. Kovács, É. H. & S. A. S. István, 2010. Aspects of breeding activity of Bufo viridis in an urban habitat: a case study in Oradea, Romania. Biharean Biologist 4: 73–77.Google Scholar
  50. Kuemmerle, T., K. Perzanowski, O. Chaskovskyy, K. Ostapowicz, L. Halada, A. T. Bashta, I. Kruhlov, P. Hostert, D. M. Waller & V. C. Radeloff, 2010. European bison habitat in the Carpathian Mountains. Biological Conservation 143: 908–916.CrossRefGoogle Scholar
  51. Lefkaditou, E., C. Y. Politou, A. Palialexis, J. Dokos, P. Cosmopoulos & V. D. Valavanis, 2008. Influences of environmental variability on the population structure and distribution patterns of the short-fin squid Illex coindetii (Cephalopoda: Ommastrephidae) in the Eastern Ionian Sea. Hydrobiologia 612: 71–90.CrossRefGoogle Scholar
  52. Lehtinen, R. M., S. M. Galatowitsch & J. R. Tester, 1999. Consequences of habitat loss and fragmentation for wetland amphibian assemblages. Wetlands 19: 1–12.CrossRefGoogle Scholar
  53. Liu, C., P. M. Berry, T. P. Dawson & R. G. Pearson, 2005. Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28: 385–393.CrossRefGoogle Scholar
  54. Lobo, J. M., A. Jiménez-Valverde & R. Real, 2008. AUC: a misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography 17: 145–151.CrossRefGoogle Scholar
  55. McCune, B., D. Keon & R. Marrs, 2002. Equations for potential annual direct incident radiation and heat load. Journal of Vegetation Science 13: 603–606.CrossRefGoogle Scholar
  56. Navarro Cerrillo, R. M., J. E. Hernández Bermejo & R. Hernández Clemente, 2011. Evaluating models to assess the distribution of Buxus balearica in southern Spain. Applied Vegetation Science 14: 256–267.CrossRefGoogle Scholar
  57. Nevo, E., 1995. Asian, African and European biota meet at ‘Evolution Canyon’ Israel: local tests of global biodiversity and genetic diversity patterns. Proceedings: Biological Sciences 262: 149–155.CrossRefGoogle Scholar
  58. Nevo, E. & S. Y. Yang, 1979. Genetic diversity and climatic determinants of tree frogs in Israel. Oecologia 41: 47–63.CrossRefGoogle Scholar
  59. Oke, T. R., 1987. Boundary Layer Climates, 2nd edn. Methuen, London.Google Scholar
  60. Olsson, O. & D. Rogers, 2009. Predicting the distribution of a suitable habitat for the white stork in Southern Sweden: identifying priority areas for reintroduction and habitat restoration. Animal Conservation 12: 62–70.CrossRefGoogle Scholar
  61. Pahkala, M., A. Laurila & J. Merilä, 2000. Ambient ultraviolet B radiation reduces hatchling size in the common frog Rana temporaria. Ecography 23: 531–538.CrossRefGoogle Scholar
  62. Papenfuss, T., 2008. Salamandra infraimmaculata. In: IUCN 2008. Red List of Threatened Species. http://www.iucnredlist.org/details/59466.
  63. Papeş, M. & P. Gaubert, 2007. Modelling ecological niches from low numbers of occurrences: assessment of the conservation status of poorly known viverrids (Mammalia, Carnivora) across two continents. Diversity and Distributions 13: 890–902.CrossRefGoogle Scholar
  64. Pearson, R. G., T. P. Dawson & C. Liu, 2004. Modelling species distributions in Britain: a hierarchical integration of climate and land-cover data. Ecography 27: 285–298.CrossRefGoogle Scholar
  65. Pearson, R. G., C. J. Raxworthy, M. Nakamura & A. T. Peterson, 2007. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography 34: 102–117.CrossRefGoogle Scholar
  66. Penman, T., M. Mahony, A. Towerton & F. Lemckert, 2007. Spatial models of giant burrowing frog distributions. Endangered Species Research 3: 115.CrossRefGoogle Scholar
  67. Peterson, A. T., 2006. Uses and requirements of ecological niche models and related distributional models. Biodiversity Informatics 3: 59–72.Google Scholar
  68. Phillips, S. J. & M. Dudik, 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31: 161–175.CrossRefGoogle Scholar
  69. Phillips, S. J., R. P. Anderson & R. E. Schapire, 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231–259.CrossRefGoogle Scholar
  70. Pulliam, H. R., 2000. On the relationship between niche and distribution. Ecology Letters 3: 349–361.CrossRefGoogle Scholar
  71. Puschendorf, R., A. C. Carnaval, J. VanDerWal, H. Zumbado-Ulate, G. Chaves, F. Bolanos & R. A. Alford, 2009. Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Diversity and Distributions 15: 401–408.CrossRefGoogle Scholar
  72. Richter, K. O. & A. L. Azous, 1995. Amphibian occurrence and wetland characteristics in the Puget Sound Basin. Wetlands 15: 305–312.CrossRefGoogle Scholar
  73. Ryan, T. J., 2007. Hydroperiod and metamorphosis in small-mouthed salamanders (Ambystoma texanum). Northeastern Naturalist 14: 619–628.CrossRefGoogle Scholar
  74. Sadeh, A., N. Truskanov, M. Mangel & L. Blaustein, 2011. Compensatory development and costs of plasticity: larval responses to desiccated conspecifics. PLoS ONE 6: e15602.PubMedCrossRefGoogle Scholar
  75. Schiller, G., E. D. Ungar, S. Cohen & N. Herr, 2010. Water use by Tabor and Kermes oaks growing in their respective habitats in the Lower Galilee region of Israel. Forest Ecology and Management 259: 1018–1024.CrossRefGoogle Scholar
  76. Segev, O., N. Hill, A. R. Templeton & L. Blaustein, 2010. Population size, structure and phenology of an endangered salamander at temporary and permanent breeding sites. Journal for Nature Conservation 18: 189–195.CrossRefGoogle Scholar
  77. Shoemaker, V. H., 1988. Physiological ecology of amphibians in arid environments. Journal of Arid Environments 14: 145–153.Google Scholar
  78. Stav, G., B. P. Kotler & L. Blaustein, 2010. Foraging response to risks of predation and competition in artificial pools. Israel Journal of Ecology and Evolution 56: 9–20.CrossRefGoogle Scholar
  79. Stratman, D. 2000. Using Micro and Macrotopography in Wetland Restoration. Indiana Biology Technical Note 1. U.S. Department of Agriculture, Natural Resources Conservation Service, Indianapolis, IN.Google Scholar
  80. Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman & R. W. Waller, 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783.PubMedCrossRefGoogle Scholar
  81. Suzuki, N., D. H. Olson & E. C. Reilly, 2008. Developing landscape habitat models for rare amphibians with small geographic ranges: a case study of Siskiyou Mountains salamanders in the western USA. Biodiversity and Conservation 17: 2197–2218.CrossRefGoogle Scholar
  82. Swets, J. A., 1988. Measuring the accuracy of diagnostic systems. Science 240: 1285–1293.PubMedCrossRefGoogle Scholar
  83. Tarkhnishvili, D., I. Serbinova & A. Gavashelishvili, 2009. Modelling the range of Syrian spadefoot toad (Pelobates syriacus) with combination of GIS-based approaches. Amphibia-Reptilia 30: 401–412.CrossRefGoogle Scholar
  84. Tovar-Pescador, J., D. Pozo-Vázquez, J. A. Ruiz-Arias, J. Batlles, G. López & J. Bosch, 2006. On the use of the digital elevation model to estimate the solar radiation in areas of complex topography. Meteorological Applications 13: 279–287.CrossRefGoogle Scholar
  85. Van Buskirk, J., 2005. Local and landscape influence on amphibian occurrence and abundance. Ecology 86: 1936–1947.CrossRefGoogle Scholar
  86. Vos, C. C. & A. H. P. Stumpel, 1996. Comparison of habitat-isolation parameters in relation to fragmented distribution patterns in the tree frog (Hyla arborea). Landscape Ecology 11: 203–214.CrossRefGoogle Scholar
  87. Weiss, S. B. & A. D. Weiss, 1998. Landscape-level phenology of a threatened butterfly: a GIS-based modeling approach. Ecosystems 1: 299–309.CrossRefGoogle Scholar
  88. Wisz, M. S., R. Hijmans, J. Li, A. T. Peterson, C. Graham & A. Guisan, 2008. Effects of sample size on the performance of species distribution models. Biodiversity Letters 14: 763–773.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Institute of Evolution and Department of Evolutionary and Environmental Biology, Faculty of Natural SciencesUniversity of HaifaHaifaIsrael

Personalised recommendations