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

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Abstract

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.

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References

  • Allen, T. F. H. & T. B. Starr, 1982. Hierarchy: Perspectives for Ecological Complexity. University of Chicago Press, Chicago.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Beja, P. & R. Alcazar, 2003. Conservation of Mediterranean temporary ponds under agricultural intensification: an evaluation using amphibians. Biological Conservation 114: 317–326.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Blaustein, L., J. Friedman & T. Fahima, 1996. Larval Salamandra drive temporary pool community dynamics: evidence from an artificial pool experiment. Oikos 76: 392–402.

    Article  Google Scholar 

  • Blaustein, L., J. E. Garb, D. Shebitz & E. Nevo, 1999. Microclimate, developmental plasticity and community structure in artificial temporary pools. Hydrobiologia 392: 187–196.

    Article  Google Scholar 

  • Bosch, J., L. Boyero & I. Martinez-Solano, 2004. Spatial scales for the management of amphibian populations. Biodiversity and Conservation 13: 409–420.

    Article  Google Scholar 

  • Boyero, L., 2003. Multiscale patterns of spatial variation in stream macroinvertebrate communities. Ecological Research 18: 365–379.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York.

    Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Degani, G., 1996. Salamandra salamandra at the Southern Limit of its Distribution. Laser Pages Publication, Kazrin.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Doherty, P. F., G. C. White & K. P. Burnham, 2012. Comparison of model building and selection strategies. Journal of Ornithology 152: 317–323.

    Article  Google Scholar 

  • 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.

  • Dorchin, A. & U. Shanas, 2010. Assessment of pollution in road runoff using a Bufo viridis biological assay. Environmental Pollution 158: 3626–3633.

    Article  CAS  PubMed  Google Scholar 

  • Dufour-Dror, J., 2002. A quantitative classification of Mediterranean mosaic-like landscapes. Journal of Mediterranean Ecology 3: 3–12.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Eitam, A., L. Blaustein & M. Mangel, 2005. Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146: 36–42.

    Article  PubMed  Google Scholar 

  • Fahrig, L. & T. Rytwinski, 2009. Effects of roads on animal abundance: an empirical review and synthesis. Ecology and Society 14: 21.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Geiger, R., 1965. The Climate Near the Ground Harvard University Press. Massachusetts, Cambridge.

    Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Graham, M. H., 2003. Confronting multicollinearity in ecological multiple regression. Ecology 84: 2809–2815.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Hothorn, T., K. Hornik & A. Zeileis, 2006. Unbiased recursive partitioning: a conditional inference framework. Journal of Computational and Graphical Statistics 15: 651–674.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Jha, S. & J. Vandermeer, 2010. Impacts of coffee agroforestry management on tropical bee communities. Biological Conservation 143: 1423–1431.

    Article  Google Scholar 

  • Joly, P., C. Miaud, A. Lehmann & O. Grolet, 2001. Habitat matrix effects on pond occupancy in newts. Conservation Biology 15: 239–248.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 

  • Landis, J. R. & G. G. Koch, 1977. The measurement of observer agreement for categorical data. Biometrics 33: 159–174.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • McCune, B., D. Keon & R. Marrs, 2002. Equations for potential annual direct incident radiation and heat load. Journal of Vegetation Science 13: 603–606.

    Article  Google Scholar 

  • McGarigal, K. & S. A. Cushman, 2002. Comparative evaluation of experimental approaches to the study of habitat fragmentation effects. Ecological Applications 12: 335–345.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Nagelkerke, N. J. D., 1991. A note on a general definition of the coefficient of determination. Biometrika 78: 691–692.

    Article  Google Scholar 

  • Nally, R. M. & C. J. Walsh, 2004. Hierarchical partitioning public-domain software. Biodiversity and Conservation 13: 659–660.

    Article  Google Scholar 

  • 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.

  • Papenfuss, T. 2008. Salamandra infraimmaculata. In IUCN 2008. Red List of Threatened Species. http://www.iucnredlist.org/details/59466.

  • Pearce, J. & S. Ferrier, 2000. Evaluating the predictive performance of habitat models developed using logistic regression. Ecological Modelling 133: 225–245.

    Article  Google Scholar 

  • Peleg, N. 2010. Studies on the conservation of the fire salamander Salamandra Infraimmaculata in Israel. PhD thesis. University of Haifa, Haifa, Israel.

  • Pineda, E. & G. Halffter, 2004. Species diversity and habitat fragmentation: frogs in a tropical montane landscape in Mexico. Biological Conservation 117: 499–508.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ryan, T. J., 2007. Hydroperiod and metamorphosis in small-mouthed salamanders (Ambystoma texanum). Northeastern Naturalist 14: 619–628.

    Article  Google Scholar 

  • Sadeh, A., N. Truskanov, M. Mangel & L. Blaustein, 2011. Compensatory development and costs of plasticity: larval responses to desiccated conspecifics. PLoS One 6: e15602.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saltz, D., 2011. Statistical inference and decision making in conservation biology. Israel Journal of Ecology and Evolution 57: 309–317.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Skelly, D. K., E. E. Werner & S. A. Cortwright, 1999. Long-term distributional dynamics of a Michigan amphibian assemblage. Ecology 80: 2326–2337.

    Article  Google Scholar 

  • Skelly, D., L. Freidenburg & J. Kiesecker, 2002. Forest canopy and the performance of larval amphibians. Ecology 83: 983–992.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Swets, J. A., 1988. Measuring the accuracy of diagnostic systems. Science 240: 1285–1293.

    Article  CAS  PubMed  Google Scholar 

  • Tavernini, S., 2008. Seasonal and inter-annual zooplankton dynamics in temporary pools with different hydroperiods. Limnologica 38: 63–75.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Van Buskirk, J., 2005. Local and landscape influence on amphibian occurrence and abundance. Ecology 86: 1936–1947.

    Article  Google Scholar 

  • Voss, S. R., 1993. Relationship between stream order and length of larval period in the salamander Eurycea wilderae. Copeia 1993: 736–742.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Wells, K. D., 2007. The Ecology and Behavior of Amphibians. University of Chicago Press, Chicago, IL.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

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Acknowledgments

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).

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Blank, L., Blaustein, L. A multi-scale analysis of breeding site characteristics of the endangered fire salamander (Salamandra infraimmaculata) at its extreme southern range limit. Hydrobiologia 726, 229–244 (2014). https://doi.org/10.1007/s10750-013-1770-8

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