Conservation Genetics

, Volume 15, Issue 1, pp 11–21 | Cite as

Environmental niche factor analysis (ENFA) relates environmental parameters to abundance and genetic diversity in an endangered amphibian, the fire-bellied-toad (Bombina bombina)

  • N. Dolgener
  • L. Freudenberger
  • M. Schluck
  • N. Schneeweiss
  • P. L. Ibisch
  • Ralph Tiedemann
Research Article


Increasing attempts are made to understand the factors responsible for both the demographic and genetic depletion in amphibian populations. Landscape genetics aims at a spatially explicit correlation of genetic population parameters to landscape features. Using data from the endangered fire-bellied toad Bombina bombina in Brandenburg (Northeastern Germany), we performed an environmental niche factor analysis (ENFA), relating demographic (abundance) and genetic (diversity at 17 microsatellite loci and partial sequences of the mitochondrial control region in 434 individuals from 16 populations) parameters to ecological and anthropogenic variables such as temperature, precipitation, soil wetness, water runoff, vegetation density, and road/traffic impact. We found significant correlations between road disturbance and observed heterozygosity and between soil wetness and mitochondrial diversity. As the influences of the environmental variables can differ between different indicators for genetic diversity, population size and abundance data, our ENFA-based landscape genetics approach allows us to put various aspects of long- versus short term effective population size and genetic connectivity into an ecological and spatially explicit context, enabling potentially even forecast assessment under future environmental scenarios.


Distribution modelling ENFA Genetic diversity Fire-bellied toad Landscape genetics Road disturbance 



We like to thank all volunteers who supported us with the field work. We thank Valerio Ketmaier for critically commenting on the manuscript, the Potsdam Institute for Climate Impact Research, especially Ylva Hauf, Anne Holsten and Manfred Stock, for providing climate, runoff and soil-wetness data and Julia Sauermann for the preparation of the Brandenburg map. Funding was provided by the Ministry of Science, Research and Culture of the state of Brandenburg, the European Social Fund, and the University of Potsdam. This is a publication of the graduate program “Adaptive Nature Conservation under Climate Change”.

Supplementary material

10592_2013_517_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 kb)
10592_2013_517_MOESM2_ESM.docx (17 kb)
Supplementary material 2 (DOCX 16 kb)
10592_2013_517_MOESM3_ESM.docx (151 kb)
Supplementary material 3 (DOCX 150 kb)


  1. Beebee TJC, Griffiths R (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285CrossRefGoogle Scholar
  2. Braunisch V, Bollmann K, Graf RF, Hirzel AH (2008) Living on the edge—modelling habitat suitability for species at the edge of their fundamental niche. Ecol Model 214:153–167CrossRefGoogle Scholar
  3. Briggs L (1996) Populationsdynamische Untersuchungen an Rotbauchunkenpopulationen mit verschiedenen Landbiotopen. In: Krone A, Kühnel KD (eds) RANA Sonderheft 1: Die Rotbauchunke (Bombina bombina), Ökologie und Bestandssituation. Natur & Text, Rangsdorf, pp 32–46Google Scholar
  4. Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519CrossRefGoogle Scholar
  5. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  6. de Knegt HJ, van Langevelde F, Skidmore AK et al (2010) The spatial scaling of habitat selection by African elephants. J Anim Ecol 80:270–281PubMedCrossRefGoogle Scholar
  7. Dolgener N, Schröder C, Schneeweiss N, Tiedemann R (2012) Genetic population structure of the Fire-bellied toad Bombina bombina in an area of high population density: implications for conservation. Hydrobiology 689:111–120CrossRefGoogle Scholar
  8. Dormann CF, McPherson JM, Araújo MB et al (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609–628CrossRefGoogle Scholar
  9. Epps CW, Palsbøll PJ, Wehausen JD et al (2005) Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecol Lett 8:1029–1038CrossRefGoogle Scholar
  10. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedCentralGoogle Scholar
  11. Farr TG, Rosen PA, Caro E et al (2007) The shuttle radar topography mission. Rev Geophys 45:1–33CrossRefGoogle Scholar
  12. Freudenberger L, Hobson P, Rupic S, Schluck M, Sauermann J, Kreft S, Selva N, Ibisch PL (2013) Spatial Road Disturbance Index (SPROADI) for conservation planning: a novel landscape index, demonstrated for the state of Brandenburg, Germany. Landsc Ecol. doi: 10.1007/s10980-013-9887-8
  13. Gharadjedaghi B, Heimann R, Lenz K et al (2004) Verbreitung und Gefährdung schutzwürdiger Landschaften in Deutschland. Natur und Landschaft 79:71–81Google Scholar
  14. Goudet J (1995) Fstat version 1.2: a computer program to calculate F statistics. J Hered 6:485–486Google Scholar
  15. Graham CH, Ron SR, Santos JC et al (2004) Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution 58:1781–1793PubMedGoogle Scholar
  16. Grinnell J (1917) The niche-relationships of the California Thrasher. Auk 34:427–433CrossRefGoogle Scholar
  17. Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186CrossRefGoogle Scholar
  18. Günther R, Schneeweiss N (1996) Rotbauchunke—Bombina bombina (LINNAEUS 1761). In: Günther R (ed) Die Amphibien und Reptilien Deutschlands. Gustav Fischer Verlag, Jena, pp 215–232Google Scholar
  19. Hansen M, DeFries R, Townshend JR et al (2003) Vegetation Continuous Fields. MOD44B, 2001 Percent Tree Cover, Collection 3. University of Maryland, College ParkGoogle Scholar
  20. Hauswaldt JS, Schröder C, Tiedemann R (2007) Nine new tetranucleotide microsatellite markers for the fire-bellied toad (Bombina bombina). Mol Ecol Notes 7:49–52CrossRefGoogle Scholar
  21. Hedrick P (2005) Large variance in reproductive success and the Ne/N ratio. Evolution 59:1596–1599PubMedGoogle Scholar
  22. Hirzel AH, Le Lay G (2008) Habitat suitability modelling and niche theory. J Appl Ecol 45:1372–1381CrossRefGoogle Scholar
  23. Hirzel AH, Hausser J, Chessel D, Perrin N (2002) Ecological-niche factor analysis: how to compute habitat suitability maps without absence data? Ecology 83:2027–2036CrossRefGoogle Scholar
  24. Hofman S, Spolsky C, Uzzell T et al (2007) Phylogeography of the fire-bellied toads Bombina: independent pleistocene histories inferred from mitochondrial genomes. Mol Ecol 16:2301–2316PubMedCrossRefGoogle Scholar
  25. Holderegger R, Di Giulio M (2010) The genetic effects of roads: a review of empirical evidence. Basic Appl Ecol 11:522–531CrossRefGoogle Scholar
  26. Holsten A, Vetter T, Vohland K, Krysanova V (2009) Impact of climate change on soil moisture dynamics in Brandenburg with a focus on nature conservation areas. Ecol Model 220:2076–2087CrossRefGoogle Scholar
  27. Hoskin CJ, Goosem MW (2010) Road impacts on abundance, call traits, and body size of rainforest frogs in northeast Australia. Ecol Soc 15(3):15Google Scholar
  28. Houlahan JE, Findlay CS, Schmidt BR et al (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755PubMedCrossRefGoogle Scholar
  29. Huang S, Krysanova V, Österle H, Hattermann FF (2010) Simulation of spatiotemporal dynamics of water fluxes in Germany under climate change. Hydrol Process 24:3289–3306CrossRefGoogle Scholar
  30. Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427CrossRefGoogle Scholar
  31. Jaeger JAG (2000) Landscape division, splitting index, and effective mesh size: new measures of landscape fragmentation. Landsc Ecol 15:115–130CrossRefGoogle Scholar
  32. LIFE-Project: "Management of fire-bellied toads in the Baltic region” LIFE04NAT/DE/00028Google Scholar
  33. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  34. Orlowsky B, Gerstengarbe F-W, Werner PC (2008) A resampling scheme for regional climate simulations and its performance compared to a dynamical RCM. Theor Appl Climatol 92:209–223CrossRefGoogle Scholar
  35. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  36. Rowe G, Beebee TJC (2003) Population on the verge of a mutational meltdown? Fitness costs of genetic load for an amphibian in the wild. Evolution 57:177–181PubMedGoogle Scholar
  37. Schneeweiss N (1996) Zur Verbreitung und Bestandsentwicklung der Rotbauchunke in Brandenburg. In: Krone A, Kühnel KD (eds) RANA Sonderheft 1: Die Rotbauchunke (Bombina bombina), Ökologie und Bestandssituation. Natur & Text, Rangsdorf, pp 87–103Google Scholar
  38. Schneeweiss N, Zbierski H (2009) Artenschutzprogramm Rotbauchunke und Laubfrosch. MLUV, Ministerium für Ländliche Entwicklung. Umwelt und Verbraucherschutz des Landes Brandenburg, Potsdam, p 88. Accessed 12 July 2013
  39. Sokal RR, Rohlf FJ (1995) Biometry. State University of New York, Stony BrookGoogle Scholar
  40. Stuart SN, Chanson J, Cox N et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786PubMedCrossRefGoogle Scholar
  41. Stuckas H, Tiedemann R (2006) Eight new microsatellite loci for the critically endangered fire-bellied toad Bombina bombina and their cross-species applicability among anurans. Mol Ecol Notes 6:150–152CrossRefGoogle Scholar
  42. Sutherland RW, Dunning PR, Baker WM (2010) Amphibian encounter rates on roads with different amounts of traffic and urbanization. Conserv Biol 24:1626–1635PubMedCrossRefGoogle Scholar
  43. van Oosterhout C, Hutchinson WF, Willis D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  44. Wahlund S (1928) Zusammensetzung von Population und Korrelationserscheinung vom Standpunkt der Vererbungslehre aus betrachtet. Hered 11:65–106Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • N. Dolgener
    • 1
  • L. Freudenberger
    • 2
  • M. Schluck
    • 2
  • N. Schneeweiss
    • 3
  • P. L. Ibisch
    • 2
  • Ralph Tiedemann
    • 1
  1. 1.Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry and BiologyUniversity of PotsdamPotsdamGermany
  2. 2.Centre for Econics and Ecosystem Management, Faculty of Forest and EnvironmentUniversity for Sustainable Development EberswaldeEberswaldeGermany
  3. 3.Landesamt für Umwelt, Gesundheit und VerbraucherschutzNaturschutzstation RhinluchLinumGermany

Personalised recommendations