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Landscape influences on dispersal behaviour: a theoretical model and empirical test using the fire salamander, Salamandra infraimmaculata

  • Behavioral ecology - Original research
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Abstract

When populations reside within a heterogeneous landscape, isolation by distance may not be a good predictor of genetic divergence if dispersal behaviour and therefore gene flow depend on landscape features. Commonly used approaches linking landscape features to gene flow include the least cost path (LCP), random walk (RW), and isolation by resistance (IBR) models. However, none of these models is likely to be the most appropriate for all species and in all environments. We compared the performance of LCP, RW and IBR models of dispersal with the aid of simulations conducted on artificially generated landscapes. We also applied each model to empirical data on the landscape genetics of the endangered fire salamander, Salamandra infraimmaculata, in northern Israel, where conservation planning requires an understanding of the dispersal corridors. Our simulations demonstrate that wide dispersal corridors of the low-cost environment facilitate dispersal in the IBR model, but inhibit dispersal in the RW model. In our empirical study, IBR explained the genetic divergence better than the LCP and RW models (partial Mantel correlation 0.413 for IBR, compared to 0.212 for LCP, and 0.340 for RW). Overall dispersal cost in salamanders was also well predicted by landscape feature slope steepness (76 %), and elevation (24 %). We conclude that fire salamander dispersal is well characterised by IBR predictions. Together with our simulation findings, these results indicate that wide dispersal corridors facilitate, rather than hinder, salamander dispersal. Comparison of genetic data to dispersal model outputs can be a useful technique in inferring dispersal behaviour from population genetic data.

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References

  • Adriaensen F, Chardon J, De Blust G, Swinnen E, Villalba S, Gulinck H, Matthysen E (2003) The application of least-cost modelling as a functional landscape model. Landsc Urban Plann 64:233–247

    Article  Google Scholar 

  • Bar-David S, Segev O, Peleg N, Hill N, Templeton AR, Schultz CB, Blaustein L (2007) Long-distance movements by fire salamanders (Salamandra infraimmaculata) and implications for habitat fragmentation. Isr J Ecol Evol 53:143–159

    Article  Google Scholar 

  • Bartumeus F, Da Luz M, Viswanathan G, Catalan J (2005) Animal search strategies: a quantitative random-walk analysis. Ecology 86:3078–3087

    Article  Google Scholar 

  • Blank L, Blaustein L (2012) Using ecological niche modeling to predict the distributions of two endangered amphibian species in aquatic breeding sites. Hydrobiologia 693:157–167

    Article  Google Scholar 

  • Blank L, Blaustein L (2014) 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

    Article  Google Scholar 

  • Blank L, Sinai I, Bar-David S, Peleg N, Segev O, Sadeh A, Kopelman NM, Templeton AR, Merilä J, Blaustein L (2013) Genetic population structure of the endangered fire salamander (Salamandra infraimmaculata) at the southernmost extreme of its distribution. Anim Conserv 16:412–421

    Article  Google Scholar 

  • Brady SP (2013) Microgeographic maladaptive performance and deme depression in response to roads and runoff. PeerJ 1:e163

    Article  PubMed Central  PubMed  Google Scholar 

  • Bunn A, Urban DL, Keitt T (2000) Landscape connectivity: a conservation application of graph theory. J Environ Manage 59:265–278

    Article  Google Scholar 

  • Cain ML (1985) Random search by herbivorous insects: a simulation model. Ecology 66:876–888

    Article  Google Scholar 

  • Degani G (1996) Salamandra salamandra at the southern limit if its distribution. Laser Pages, Jerusalem

    Google Scholar 

  • Dingle H, Drake VA (2007) What is migration? Bioscience 57:113–121

    Article  Google Scholar 

  • Dobzhansky T, Powell JR, Taylor CE, Andregg M (1979) Ecological variables affecting the dispersal behavior of Drosophila pseudoobscura and its relatives. Am Nat 114:325–334

    Article  Google Scholar 

  • Edwards AM, Phillips RA, Watkins NW, Freeman MP, Murphy EJ, Afanasyev V, Buldyrev SV, da Luz MG, Raposo EP, Stanley HE (2007) Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449:1044–1048

    Article  CAS  PubMed  Google Scholar 

  • Fournier A, Fussell D, Carpenter L (1982) Computer rendering of stochastic models. Commun Assoc Comp Mach 25:371–384

    Google Scholar 

  • Galpern P, Manseau M, Wilson P (2012) Grains of connectivity: analysis at multiple spatial scales in landscape genetics. Mol Ecol 21:3996–4009

    Article  PubMed  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G ST and D: forget G ST but not all of statistics! Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Giordano AR, Ridenhour BJ, Storfer A (2007) The influence of altitude and topography on genetic structure in the long-toed salamander (Ambystoma macrodactylum). Mol Ecol 16:1625–1637

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2002) FSTAT version 2.9.3.2. Institute of Ecology, Lausanne

  • Grinstead CM, Snell JL (1997) Chapter 11: Markov chains. In: Grinstead CM, Snell JL (eds) Introduction to probability. American Mathematical Society, Providence, pp 405–470

    Google Scholar 

  • Hall J, Weinberger R, Marco S, Steinitz G (1999) Test of the accuracy of the DEM of Israel. Geological Survey of Israel, Jerusalem

    Google Scholar 

  • Hendrix R, Hauswaldt JS, Veith M, Steinfartz S (2010) Strong correlation between cross-amplification success and genetic distance across all members of ‘True salamanders’ (Amphibia: Salamandridae) revealed by Salamandra salamandra-specific microsatellite loci. Mol Ecol Res 10:1038–1047

    Article  CAS  Google Scholar 

  • Jaquiéry J, Broquet T, Hirzel A, Yearsley J, Perrin N (2011) Inferring landscape effects on dispersal from genetic distances: how far can we go? Mol Ecol 20:692–705

    Article  PubMed  Google Scholar 

  • Jost L (2009) D vs. GST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091

    Article  Google Scholar 

  • Kershenbaum A, Kershenbaum A, Blaustein L (2011) Rock hyrax (Procavia capensis) den site selection: preference for artificial sites. Wildl Res 38:244–248

    Article  Google Scholar 

  • Khalil HK, Grizzle J (1992) Nonlinear systems. Macmillan, New York

    Google Scholar 

  • Lee-Yaw JA, Davidson A, McRae BH, Green DM (2009) Do landscape processes predict phylogeographic patterns in the wood frog? Mol Ecol 18:1863–1874

    Article  PubMed  Google Scholar 

  • Lovász L (1993) Random walks on graphs: a survey. Combinatorics, Paul Erdos is Eighty, vol 2. Keszthely, Hungary, pp 1–46

  • Lowe WH, Likens GE, McPeek MA, Buso DC (2006) Linking direct and indirect data on dispersal: isolation by slope in a headwater stream salamander. Ecology 87:334–339

    Article  PubMed  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104:19885–19890

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Munshi-South J (2012) Urban landscape genetics: canopy cover predicts gene flow between white-footed mouse (Peromyscus leucopus) populations in New York city. Mol Ecol 21:1360–1378

    Article  PubMed  Google Scholar 

  • Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA 105:19052–19059

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neteler M, Mitasova H (2008) Open source GIS: a GRASS GIS approach, 3rd edn. Kluwer, New York

    Book  Google Scholar 

  • Okubo A, Levin SA (2002) Diffusion and ecological problems. Springer, New York

    Google Scholar 

  • Phillips CA, Sexton OJ (1989) Orientation and sexual differences during breeding migrations of the spotted salamander, Ambystoma maculatum. Copeia 1989:17–22

    Article  Google Scholar 

  • Pinto N, Keitt TH (2009) Beyond the least-cost path: evaluating corridor redundancy using a graph-theoretic approach. Landsc Ecol 24:253–266

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Richardson JL (2012) Divergent landscape effects on population connectivity in two co-occurring amphibian species. Mol Ecol 21:4437–4451

    Article  PubMed  Google Scholar 

  • Roitberg BD, Mangel M (2010) Mosquito biting and movement rates as an emergent community property and the implications for malarial interventions. Isr J Ecol Evol 56:297–312

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Row JR, Blouin-Demers G, Lougheed SC (2010) Habitat distribution influences dispersal and fine-scale genetic population structure of eastern foxsnakes (Mintonius gloydi) across a fragmented landscape. Mol Ecol 19:5157–5171

    Article  PubMed  Google Scholar 

  • Sawyer SC, Epps CW, Brashares JS (2011) Placing linkages among fragmented habitats: do least-cost models reflect how animals use landscapes? J Appl Ecol 48:668–678

    Article  Google Scholar 

  • Schwartz MK, Copeland JP, Anderson NJ, Squires JR, Inman RM, McKelvey KS, Pilgrim KL, Waits LP, Cushman SA (2009) Wolverine gene flow across a narrow climatic niche. Ecology 90:3222–3232

    Article  PubMed  Google Scholar 

  • Segev O, Blaustein L (in press) Influence of water velocity and predation risk on fire salamander (Salamandra infraimmaculata) larval drift between temporary pools in ephemeral streams. Freshwater Sci

  • Simberloff D, Farr JA, Cox J, Mehlman DW (1992) Movement corridors: conservation bargains or poor investments? Conserv Biol 6:493–504

    Article  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Slatkin M, Voelm L (1991) F (ST) in a hierarchical island model. Genetics 127:627–629

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Soule ME, Gilpin ME (1991) The theory of wildlife corridor capability. In: Saunders DA, Hobbs RJ (eds) The role of corridors in nature conservation. Surrey Beatty & Sons, Chipping Norton, pp 3–8

    Google Scholar 

  • Southwood A, Avens L (2010) Physiological, behavioral, and ecological aspects of migration in reptiles. J Comp Physiol B 180:1–23

    Article  PubMed  Google Scholar 

  • Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564

    Article  CAS  PubMed  Google Scholar 

  • Steinfartz S, Kuesters D, Tautz D (2004) Isolation and characterization of polymorphic tetranucleotide microsatellite loci in the fire salamander Salamandra salamandra (Amphibia: Caudata). Mol Ecol Notes 4:626–628

    Article  CAS  Google Scholar 

  • Takahata N, Nei M (1984) FST and GST statistics in the finite island model. Genetics 107:501–504

    CAS  PubMed Central  PubMed  Google Scholar 

  • Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, New Jersey

    Book  Google Scholar 

  • Thiesmeier B, Schuhmacher H (1990) Causes of larval drift of the fire salamander, Salamandra salamandra terrestris, and its effects on population dynamics. Oecologia 82:259–263

    Article  Google Scholar 

  • Viswanathan G, Buldyrev SV, Havlin S, Da Luz M, Raposo E, Stanley HE (1999) Optimizing the success of random searches. Nature 401:911–914

    Article  CAS  PubMed  Google Scholar 

  • Warburg MR (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 

  • Warburg MR (2007) The phenology of a rare salamander (Salamandra infraimmaculata) in a population breeding under unpredictable ambient conditions: a 25 year study. Acta Herpetol 2:147–157

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wright S (1949) The genetical structure of populations. Ann Hum Genet 15:323–354

    Google Scholar 

  • Zollner PA, Lima SL (1999) Search strategies for landscape-level interpatch movements. Ecology 80:1019–1030

    Article  Google Scholar 

Download references

Acknowledgments

We thank Shirli Bar David, Arne Nolte, Sebastian Steinfartz and Ori Segev for fruitful discussion, and three anonymous reviewers for their detailed suggestions. This research was carried out under Israel National Parks Authority permit number no. 2009/36565. It was partly funded by Israel Science Foundation (ISF) grant 961-2008 awarded to Leon Blaustein, Shirli Bar-David, and Alan Templeton, and by an Academy of Finland Grant awarded to Juha Merilä. Arik Kershenbaum was provided with a doctoral scholarship by the University of Haifa and by the ISF grant. Part of this work was conducted while Arik Kershenbaum was a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, an institute sponsored by the National Science Foundation (NSF), the US Department of Homeland Security, and the US Department of Agriculture through NSF award no. EF-0832858, with additional support from the University of Tennessee, Knoxville. This study was partially funded by the Deutsch-Israel Project no. BL 1271/1-1 awarded to Leon Blaustein, Alan Templeton, Sebastian Steinfartz and Arne Nolte.

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Authors and Affiliations

  1. Community Ecology Lab, Department of Evolutionary and Environmental Ecology and the Institute of Evolution, Faculty of Natural Sciences, University of Haifa, 31905, Haifa, Israel

    Arik Kershenbaum, Lior Blank, Iftach Sinai, Leon Blaustein & Alan R. Templeton

  2. National Institute for Mathematical and Biological Synthesis (NIMBioS), Knoxville, TN, USA

    Arik Kershenbaum

  3. Israel National Parks Authority, 95463, Jerusalem, Israel

    Iftach Sinai

  4. Ecological Genetics Research Unit, Department of Biosciences, University of Helsinki, 00014, Helsinki, Finland

    Juha Merilä

  5. Department of Biology, Washington University, St Louis, MO, USA

    Alan R. Templeton

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  1. Arik Kershenbaum
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  2. Lior Blank
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Correspondence to Arik Kershenbaum.

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Communicated by Jean-François Le Galliard.

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Kershenbaum, A., Blank, L., Sinai, I. et al. Landscape influences on dispersal behaviour: a theoretical model and empirical test using the fire salamander, Salamandra infraimmaculata . Oecologia 175, 509–520 (2014). https://doi.org/10.1007/s00442-014-2924-8

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