, Volume 726, Issue 1, pp 229–244 | Cite as

A multi-scale analysis of breeding site characteristics of the endangered fire salamander (Salamandra infraimmaculata) at its extreme southern range limit

Primary Research Paper


Understanding species’ distributions often requires taking into consideration the characterization of the environment at different spatial scales. The habitat characteristics of the endangered fire salamander, S. infraimmaculata, have received little attention. In this study, at this species’ most peripheral and xeric limit (Mt. Carmel, Israel), we examined predictors of the larval distribution of S. infraimmaculata at aquatic-breeding sites at both local and landscape scales. We investigated the predictive power of environmental variables using two methods: generalized linear models and conditional inference trees (CTREE). Both multi-model approaches yielded similar results. At the local site scale, hydroperiod predicted breeding site use. At the landscape scale, Salamandra presence was best predicted by proximity to other breeding sites. In addition, our study indicates that sites selected for breeding are far from roads and agricultural fields. Overall, this study demonstrates that ultimately, both local and landscape scale predictors are necessary to understand properly a species’ habitat requirements and thus can help in planning future management around the breeding sites.


Conditional inference trees Generalized linear models Land-use Scale 



This study was funded by the Israel Science Foundation grant 961-2008 awarded to Leon Blaustein, Deustche-Israel Project DIP 10 awarded to Leon Blaustein, Alan R. Templeton, Sebastian Steinfartz and Arne Nolte, and a scholarship provided by the Israel Council for Higher Education awarded to Lior Blank. We thank Alan R. Templeton, Juha Merilä, Iftah Sinai, Arik Kershenbaum, Asaf Sadeh, and Ori Segev for fruitful discussion and Arik Kershenbaum for comments on the manuscript. Field surveys of S. infraimmaculata larvae were conducted with permission from the Israel Nature and Parks Authority (permit 2009/36565).


  1. Allen, T. F. H. & T. B. Starr, 1982. Hierarchy: Perspectives for Ecological Complexity. University of Chicago Press, Chicago.Google Scholar
  2. 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.CrossRefGoogle Scholar
  3. Beck, C. W. & J. D. Congdon, 2000. Effects of age and size at metamorphosis on performance and metabolic rates of Southern Toad, Bufo terrestris, metamorphs. Functional Ecology 14: 32–38.CrossRefGoogle Scholar
  4. Beja, P. & R. Alcazar, 2003. Conservation of Mediterranean temporary ponds under agricultural intensification: an evaluation using amphibians. Biological Conservation 114: 317–326.CrossRefGoogle Scholar
  5. Bishop, C. A., N. A. Mahony, J. Struger, P. Ng & K. E. Pettit, 1999. Anuran development, density and diversity in relation to agricultural activity in the Holland River watershed, Ontario, Canada (1990–1992). Environmental Monitoring and Assessment 57: 21–43.CrossRefGoogle Scholar
  6. Blank, L. & L. Blaustein, 2012. Using ecological niche modeling to predict the distributions of two endangered amphibian species in aquatic breeding site. Hydrobiologia 693: 157–167.CrossRefGoogle Scholar
  7. Blank, L., R. Linker & Y. Carmel, 2013a. A multiscale analysis of herbaceous species richness in a Mediterranean ecosystem. Journal of Plant Ecology 6: 113–121.CrossRefGoogle Scholar
  8. Blank, L., I. Sinai, I. Bar-David, N. Peleg, O. Segev, A. Sadeh, N. M. Kopelman, A. R. Templeton, J. Merilä & L. Blaustein, 2013b. Genetic population structure of the endangered fire salamander (Salamandra infraimmaculata) at the southernmost extreme of its distribution. Animal Conservation 16: 412–421.CrossRefGoogle Scholar
  9. Blaustein, L., J. Friedman & T. Fahima, 1996. Larval Salamandra drive temporary pool community dynamics: evidence from an artificial pool experiment. Oikos 76: 392–402.CrossRefGoogle Scholar
  10. Blaustein, L., J. E. Garb, D. Shebitz & E. Nevo, 1999. Microclimate, developmental plasticity and community structure in artificial temporary pools. Hydrobiologia 392: 187–196.CrossRefGoogle Scholar
  11. Bosch, J., L. Boyero & I. Martinez-Solano, 2004. Spatial scales for the management of amphibian populations. Biodiversity and Conservation 13: 409–420.CrossRefGoogle Scholar
  12. Boyero, L., 2003. Multiscale patterns of spatial variation in stream macroinvertebrate communities. Ecological Research 18: 365–379.CrossRefGoogle Scholar
  13. 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
  14. Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York.Google Scholar
  15. Calcagno, V., 2010. glmulti: an R Package for easy automated model selection with (generalized) linear models. Journal of Statistical Software 34: 1–29.Google Scholar
  16. Carlson, A. & P. Edenhamn, 2000. Extinction dynamics and the regional persistence of a tree frog metapopulation. Proceedings of the Royal Society of London Series B: Biological Sciences 267: 1311–1313.PubMedCrossRefGoogle Scholar
  17. 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
  18. Degani, G., 1996. Salamandra salamandra at the Southern Limit of its Distribution. Laser Pages Publication, Kazrin.Google Scholar
  19. Denoël, M. & G. F. Ficetola, 2008. Conservation of newt guilds in an agricultural landscape of Belgium: the importance of aquatic and terrestrial habitats. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 714–728.CrossRefGoogle Scholar
  20. Denoël, M. & A. Lehmann, 2006. Multi-scale effect of landscape processes and habitat quality on newt abundance: implications for conservation. Biological Conservation 130: 495–504.CrossRefGoogle Scholar
  21. Denoėl, M., G. F. Ficetola, R. Cirovic, D. Radovic, G. Dzukic, M. L. Kalezic & T. D. Vukov, 2009. 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.CrossRefGoogle Scholar
  22. Doherty, P. F., G. C. White & K. P. Burnham, 2012. Comparison of model building and selection strategies. Journal of Ornithology 152: 317–323.CrossRefGoogle Scholar
  23. 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
  24. Dorchin, A. & U. Shanas, 2010. Assessment of pollution in road runoff using a Bufo viridis biological assay. Environmental Pollution 158: 3626–3633.PubMedCrossRefGoogle Scholar
  25. Dufour-Dror, J., 2002. A quantitative classification of Mediterranean mosaic-like landscapes. Journal of Mediterranean Ecology 3: 3–12.Google Scholar
  26. Egea-Serrano, A., F. J. Oliva-Paterna & M. Torralva, 2006. Breeding habitat selection of Salamandra salamandra (Linnaeus, 1758) in the most arid zone of its European distribution range: application to conservation management. Hydrobiologia 560: 363–371.CrossRefGoogle Scholar
  27. Eitam, A., L. Blaustein & M. Mangel, 2005. Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146: 36–42.PubMedCrossRefGoogle Scholar
  28. Fahrig, L. & T. Rytwinski, 2009. Effects of roads on animal abundance: an empirical review and synthesis. Ecology and Society 14: 21.Google Scholar
  29. Ficetola, G. F., R. De Manenti, F. Bernardi & E. Padoa-Schioppa, 2011a. Can patterns of spatial autocorrelation reveal population processes? An analysis with the fire salamander. Ecography 35: 693–703.CrossRefGoogle Scholar
  30. Ficetola, G. F., L. Marziali, B. De Rossaro, F. Bernardi & E. Padoa-Schioppa, 2011b. Landscape–stream interactions and habitat conservation for amphibians. Ecological Applications 21: 1272–1282.PubMedCrossRefGoogle Scholar
  31. Freeman, E. 2007. PresenceAbsence: An R Package for Presence–Absence Model Evaluation. USDA Forest Service, Rocky Mountain Research Station, 507 25th street, Ogden, UT, USA.Google Scholar
  32. Fuller, T. E., K. L. Pope, D. T. Ashton & H. H. Welsh Jr, 2011. Linking the distribution of an invasive amphibian (Rana catesbeiana) to habitat conditions in a managed river system in Northern California. Restoration Ecology 19: 204–213.CrossRefGoogle Scholar
  33. Garriga, N., X. Santos, A. Montori, A. Richter-Boix, M. Franch & G. A. Llorente, 2012. Are protected areas truly protected? The impact of road traffic on vertebrate fauna. Biodiversity and Conservation 21: 2761–2774.CrossRefGoogle Scholar
  34. Geiger, R., 1965. The Climate Near the Ground Harvard University Press. Massachusetts, Cambridge.Google Scholar
  35. Goldberg, T., E. Nevo & G. Degani, 2009. Breeding site selection according to suitability for amphibian larval growth under various ecological conditions in the semi-arid zone of northern Israel. Ecologia Mediterranea 35: 65–74.Google Scholar
  36. Goldberg, T., E. Nevo & G. Degani, 2011. Genetic diverseness and different ecological conditions in Salamandra infraimmaculata larvae from various breeding sites. Animal Biology Journal 2: 37–49.Google Scholar
  37. Gomez-Garcia, D., J. Azorin & A. J. Aguirre, 2009. Effects of small-scale disturbances and elevation on the morphology, phenology and reproduction of a successful geophyte. Journal of Plant Ecology 2: 13–20.CrossRefGoogle Scholar
  38. Gonzalez-Mirelis, G. & M. Lindegarth, 2012. Predicting the distribution of out-of-reach biotopes with decision trees in a Swedish Marine Protected Area. Ecological Applications 22: 2248–2264.PubMedCrossRefGoogle Scholar
  39. Graham, M. H., 2003. Confronting multicollinearity in ecological multiple regression. Ecology 84: 2809–2815.CrossRefGoogle Scholar
  40. Gu, W. & R. K. Swihart, 2004. Absent or undetected? Effects of non-detection of species occurrence on wildlife-habitat models. Biological Conservation 116: 195–203.CrossRefGoogle Scholar
  41. Hamer, A. J., S. J. Lane & M. J. Mahony, 2002. Management of freshwater wetlands for the endangered green and golden bell frog (Litoria aurea): roles of habitat determinants and space. Biological Conservation 106: 413–424.CrossRefGoogle Scholar
  42. Harless, M. L., C. J. Huckins, J. B. Grant & T. G. Pypker, 2011. Effects of six chemical deicers on larval wood frogs (Rana sylvatica). Environmental Toxicology and Chemistry 30: 1637–1641.PubMedCrossRefGoogle Scholar
  43. Hothorn, T., K. Hornik & A. Zeileis, 2006. Unbiased recursive partitioning: a conditional inference framework. Journal of Computational and Graphical Statistics 15: 651–674.CrossRefGoogle Scholar
  44. Jakob, C., A. Seitz, A. J. Crivelli & C. Miaud, 2002. Growth cycle of the marbled newt (Triturus marmoratus) in the Mediterranean region assessed by skeletochronology. Amphibia-Reptilia 23: 407–418.CrossRefGoogle Scholar
  45. Jha, S. & J. Vandermeer, 2010. Impacts of coffee agroforestry management on tropical bee communities. Biological Conservation 143: 1423–1431.CrossRefGoogle Scholar
  46. Joly, P., C. Miaud, A. Lehmann & O. Grolet, 2001. Habitat matrix effects on pond occupancy in newts. Conservation Biology 15: 239–248.Google Scholar
  47. 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
  48. Kundu, S., Y. S. van Aulchenko, C. M. Duijn & A. C. J. W. Janssens, 2011. PredictABEL: an R package for the assessment of risk prediction models. European Journal of Epidemiology 26: 261–264.PubMedCentralPubMedCrossRefGoogle Scholar
  49. Kutiel, H., 2012. Weather conditions and forest fire propagation: the case of the Carmel fire, December 2010. Israel Journal of Ecology & Evolution 58: 113–122.Google Scholar
  50. Landis, J. R. & G. G. Koch, 1977. The measurement of observer agreement for categorical data. Biometrics 33: 159–174.PubMedCrossRefGoogle Scholar
  51. Manenti, R., G. F. Ficetola & F. De Bernardi, 2009. Water, stream morphology and landscape: complex habitat determinants for the fire salamander Salamandra salamandra. Amphibia-Reptilia 30: 7–15.CrossRefGoogle Scholar
  52. 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
  53. McGarigal, K. & S. A. Cushman, 2002. Comparative evaluation of experimental approaches to the study of habitat fragmentation effects. Ecological Applications 12: 335–345.CrossRefGoogle Scholar
  54. Moning, C. & J. Muller, 2008. Environmental key factors and their thresholds for the avifauna of temperate montane forests. Forest Ecology and Management 256: 1198–1208.CrossRefGoogle Scholar
  55. Morand, A., P. Joly & O. Grolet, 1997. Phenotypic variation in metamorphosis in five anuran species along a gradient of stream influence. Comptes Rendus de l’Académie des Sciences-Series III-Sciences de la Vie 320: 645–652.CrossRefGoogle Scholar
  56. Nagelkerke, N. J. D., 1991. A note on a general definition of the coefficient of determination. Biometrika 78: 691–692.CrossRefGoogle Scholar
  57. Nally, R. M. & C. J. Walsh, 2004. Hierarchical partitioning public-domain software. Biodiversity and Conservation 13: 659–660.CrossRefGoogle Scholar
  58. 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.Google Scholar
  59. Papenfuss, T. 2008. Salamandra infraimmaculata. In IUCN 2008. Red List of Threatened Species. http://www.iucnredlist.org/details/59466.
  60. Pearce, J. & S. Ferrier, 2000. Evaluating the predictive performance of habitat models developed using logistic regression. Ecological Modelling 133: 225–245.CrossRefGoogle Scholar
  61. Peleg, N. 2010. Studies on the conservation of the fire salamander Salamandra Infraimmaculata in Israel. PhD thesis. University of Haifa, Haifa, Israel.Google Scholar
  62. Pineda, E. & G. Halffter, 2004. Species diversity and habitat fragmentation: frogs in a tropical montane landscape in Mexico. Biological Conservation 117: 499–508.CrossRefGoogle Scholar
  63. Ray, N., A. Lehmann & P. Joly, 2002. Modeling spatial distribution of amphibian populations: a GIS approach based on habitat matrix permeability. Biodiversity and Conservation 11: 2143–2165.CrossRefGoogle Scholar
  64. Rota, C. T., R. J. Fletcher Jr, R. M. Dorazio & M. G. Betts, 2009. Occupancy estimation and the closure assumption. Journal of Applied Ecology 46: 1173–1181.Google Scholar
  65. Rothermel, B. B. & T. M. Luhring, 2005. Burrow availability and desiccation risk of mole salamanders (Ambystoma talpoideum) in harvested versus unharvested forest stands. Journal of Herpetology 39: 619–626.CrossRefGoogle Scholar
  66. Rowe, C. L. & W. A. Dunson, 1995. Impacts of hydroperiod on growth and survival of larval amphibians in temporary ponds of central Pennsylvania, USA. Oecologia 102: 397–403.CrossRefGoogle Scholar
  67. Ryan, T. J., 2007. Hydroperiod and metamorphosis in small-mouthed salamanders (Ambystoma texanum). Northeastern Naturalist 14: 619–628.CrossRefGoogle Scholar
  68. Sadeh, A., N. Truskanov, M. Mangel & L. Blaustein, 2011. Compensatory development and costs of plasticity: larval responses to desiccated conspecifics. PLoS One 6: e15602.PubMedCentralPubMedCrossRefGoogle Scholar
  69. Saltz, D., 2011. Statistical inference and decision making in conservation biology. Israel Journal of Ecology and Evolution 57: 309–317.CrossRefGoogle Scholar
  70. 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
  71. Segev, O., M. Mangel, N. Wolf, A. Sadeh, A. Kershenbaum & L. Blaustein, 2011. Spatiotemporal reproductive strategies in the fire salamander: a model and empirical test. Behavioral Ecology 22: 670–678.CrossRefGoogle Scholar
  72. Semlitsch, R. D., D. E. Scott & J. H. K. Pechmann, 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69: 184–192.CrossRefGoogle Scholar
  73. Silva, F. R., T. A. L. Oliveira, J. P. Gibbs & D. C. Rossa-Feres, 2012. An experimental assessment of landscape configuration effects on frog and toad abundance and diversity in tropical agro-savannah landscapes of southeastern Brazil. Landscape Ecology 27: 87–96.CrossRefGoogle Scholar
  74. Skelly, D. K., E. E. Werner & S. A. Cortwright, 1999. Long-term distributional dynamics of a Michigan amphibian assemblage. Ecology 80: 2326–2337.CrossRefGoogle Scholar
  75. Skelly, D., L. Freidenburg & J. Kiesecker, 2002. Forest canopy and the performance of larval amphibians. Ecology 83: 983–992.CrossRefGoogle Scholar
  76. Skelly, D. K., M. A. Halverson, L. K. Freidenburg & M. C. Urban, 2005. Canopy closure and amphibian diversity in forested wetlands. Wetlands Ecology and Management 13: 261–268.CrossRefGoogle Scholar
  77. Skidds, D. E. & F. C. Golet, 2005. Estimating hydroperiod suitability for breeding amphibians in southern Rhode Island seasonal forest ponds. Wetlands Ecology and Management 13: 349–366.CrossRefGoogle Scholar
  78. Snodgrass, J. W., M. J. Komoroski, A. L. Bryan & J. Burger, 2000. Relationships among isolated wetland size, hydroperiod, and amphibian species richness: implications for wetland regulations. Conservation Biology 14: 414–419.CrossRefGoogle Scholar
  79. Steinfartz, S., M. Veith & D. Tautz, 2000. Mitochondrial sequence analysis of Salamandra taxa suggests old splits of major lineages and postglacial recolonizations of Central Europe from distinct source populations of Salamandra salamandra. Molecular Ecology 9: 397–410.PubMedCrossRefGoogle Scholar
  80. Stephens, S. E., D. N. Koons, J. J. Rotella & D. W. Willey, 2004. Effects of habitat fragmentation on avian nesting success: a review of the evidence at multiple spatial scales. Biological Conservation 115: 101–110.CrossRefGoogle Scholar
  81. Swets, J. A., 1988. Measuring the accuracy of diagnostic systems. Science 240: 1285–1293.PubMedCrossRefGoogle Scholar
  82. Tavernini, S., 2008. Seasonal and inter-annual zooplankton dynamics in temporary pools with different hydroperiods. Limnologica 38: 63–75.CrossRefGoogle Scholar
  83. Trenham, P. C., W. D. Koenig, M. J. Mossman, S. L. Stark & L. A. Jagger, 2003. Regional dynamics of wetland-breeding frogs and toads: turnover and synchrony. Ecological Applications 13: 1522–1532.CrossRefGoogle Scholar
  84. Van Buskirk, J., 2005. Local and landscape influence on amphibian occurrence and abundance. Ecology 86: 1936–1947.CrossRefGoogle Scholar
  85. Voss, S. R., 1993. Relationship between stream order and length of larval period in the salamander Eurycea wilderae. Copeia 1993: 736–742.CrossRefGoogle Scholar
  86. Wang, I. J., J. R. Johnson, B. B. Johnson & H. B. Shaffer, 2011. Effective population size is strongly correlated with breeding pond size in the endangered California tiger salamander, Ambystoma californiense. Conservation Genetics 12: 911–920.CrossRefGoogle Scholar
  87. Warburg, M. R., 1994. Population ecology, breeding activity, longevity, and reproductive strategies of Salamandra salamandra during an 18-year long study of an isolated population on Mt. Carmel, Israel. Mertensiella 4: 399–421.Google Scholar
  88. Wells, K. D., 2007. The Ecology and Behavior of Amphibians. University of Chicago Press, Chicago, IL.CrossRefGoogle Scholar
  89. Werner, E. E. & K. S. Glennemeier, 1999. Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999: 1–12.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

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

Personalised recommendations