Skip to main content
Log in

Highlighting the effects of land-use change on a threatened amphibian in a human-dominated landscape

  • Original article
  • Published:
Population Ecology

Abstract

In Western Europe, habitat loss and landscape fragmentation has led to significant population decline in various animal groups, including amphibians. The extinction of the last natural populations of the yellow-bellied toad in Belgium, Luxembourg and several regions of southern and western France suggests a widespread decline. By using site-occupancy models and adding covariates corresponding to the human-influenced features of the landscape, we tried to identify the relative effects of different land-use types on the species’ distribution pattern in a man-made environment (the Alsatian Rhine floodplain in France). We recorded presence–absence data in 150 forest sample plots (300 × 300 m) and then modeled species distribution while taking into account detection errors in the field. Land-use was recorded on two spatial scales: within the forest sample plots and in a 1500 m radius buffer area around the forest plots. In the forest plots, toad occurrence was negatively correlated with loss of forest cover to agricultural land. In contrast, occurrence is positively correlated with the density of human-made rutted dirt paths and tracks, which provide semi-natural breeding sites. In the 1500 m radius buffer zones around forest plots, toad occurrence was negatively correlated with the density of urbanization and road networks. These results can be used to plan conservation strategies for amphibians in human-dominated landscapes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allentoft ME, O’Brien J (2010) Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity 2:47–71

    Article  Google Scholar 

  • Andrews KM, Gibbons JW, Jochimsen DM (2008) Ecological effects of roads on amphibians and reptiles: a literature review. In: Mitchell JC, Jung Brown RE, Bartholomew B (eds) Urban herpetology. Society for the Study of Amphibians and Reptiles, Salt Lake City, pp 121–143

    Google Scholar 

  • Babik W, Rafinski J (2001) Amphibian breeding site characteristics in the Western Carpathians, Poland. Herpetol J 11:41–51

    Google Scholar 

  • Bailey LL, Simons TR, Pollock KH (2004) Estimating site occupancy and species detection probability parameters for terrestrial salamanders. Ecol Appl 14:692–702

    Article  Google Scholar 

  • Barandun J (1990) Reproduction of yellow-bellied toads Bombina variegata in a man-made habitat. Amphibia-Reptilia 11:277–284

    Article  Google Scholar 

  • Barandun J, Reyer HU (1998) Reproductive ecology of Bombina variegata: habitat use. Copeia 1998:497–500

    Article  Google Scholar 

  • Becker CG, Fonseca CR, Haddad CFB, Batista RF, Prado PI (2007) Habitat split and the global decline of amphibians. Science 318:1775–1777

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Brady SP (2012) Road to evolution? Local adaptation to road adjacency in an amphibian (Ambystoma maculatum). Sci Rep 2:235. doi:10.1038/srep00235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New-York

    Google Scholar 

  • Canessa S, Oneto F, Ottonello D, Arillo A, Salvidio S (2013) Land abandonment may reduce disturbance and affect the breeding sites of an endangered amphibian in northern Italy. Oryx 47:280–287

    Article  Google Scholar 

  • Carr LW, Fahrig L (2001) Effect of road traffic on two amphibian species of differing vagility. Conserv Biol 15:1071–1078

    Article  Google Scholar 

  • Cayuela H, Cheylan M, Joly P (2011) The best of a harsh lot in a specialized species: breeding habitat use by the yellow-bellied toad (Bombina variegata) on rocky riverbanks. Amphibia-Reptilia 32:533–539

    Article  Google Scholar 

  • Cayuela H, Besnard A, Bechet A, Devictor V, Olivier A (2012) Reproductive dynamics of three amphibian species in Mediterranean wetlands: the role of local precipitation and hydrological regimes. Freshwater Biol 57:2629–2640

    Article  Google Scholar 

  • Cayuela H, Besnard A, Joly P (2013) Multi-event models reveal the absence of interaction between an invasive frog and a native endangered amphibian. Biol Invasions 15:2001–2012

    Article  Google Scholar 

  • Cayuela H, Besnard A, Bonnaire E, Perret H, Rivoalen J, Miaud C, Joly P (2014) To breed or not to breed: past reproductive status and environmental cues drive current breeding decisions in a long-lived amphibian. Oecologia 176:107–116

    Article  PubMed  Google Scholar 

  • Collins SJ, Russell RW (2009) Toxicity of road salt to Nova Scotia amphibians. Environ Pollut 157:320–324

    Article  CAS  PubMed  Google Scholar 

  • Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:231–240

    Article  Google Scholar 

  • Delaney KS, Riley SP, Fisher RN (2010) A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS One 5:e12767. doi:10.1371/journal.pone.0012767

    Article  PubMed Central  PubMed  Google Scholar 

  • Di Cerbo AR, Biancardi CM (2004) Seasonal activity and thermobiology of Bombina v. variegata in Lombardy (Seriana Valley, northern Italy). Ital J Zool 71:143–146

    Article  Google Scholar 

  • Dickman CR, Doncaster CP (1987) The ecology of small mammals in urban habitats. I. Populations in a patchy environment. J Anim Ecol 56:629–640

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol S 34:487–515

    Article  Google Scholar 

  • Fiske I, Chandler R (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Softw 43:1–23

    Google Scholar 

  • Gaggiotti OE (2004) Ecology, genetics, and evolution of metapopulations. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Hamer AJ, Parris KM (2011) Local and landscape determinants of amphibian communities in urban ponds. Ecol Appl 21:378–390

    Article  PubMed  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, New-York

    Google Scholar 

  • Hartel T (2008) Movement activity in a Bombina variegata population from a deciduous forested landscape. Northwest J Zool 4:79–90

    Google Scholar 

  • Hartel T, von Wehrden H (2013) Farmed areas predict the distribution of amphibian ponds in a traditional rural landscape. PLoS One 8:e63649. doi:10.1371/journal.pone.0063649

    Article  PubMed Central  PubMed  Google Scholar 

  • Hartel T, Nemes S, Mara G (2007) Breeding phenology and spatio-temporal dynamics of pond use by the yellow-bellied toad (Bombina variegata) population: the importance of pond availability and duration. Acta Zool Lituanica 17:56–63

    Article  Google Scholar 

  • Hazell D, Cunnningham R, Lindenmayer D, Mackey B, Osborne W (2001) Use of farm dams as frog habitat in an Australian agricultural landscape: factors affecting species richness and distribution. Biol Conserv 102:155–169

    Article  Google Scholar 

  • Hitchings SP, Beebee TJ (1997) Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127

    Article  PubMed  Google Scholar 

  • Homan RN, Windmiller BS, Reed JM (2004) Critical thresholds associated with habitat loss for two vernal pool-breeding amphibians. Ecol Appl 14:1547–1553

    Article  Google Scholar 

  • Hossack BR, Corn PS (2007) Responses of pond-breeding amphibians to wildfire: short-term patterns in occupancy and colonization. Ecol Appl 17:1403–1410

    Article  PubMed  Google Scholar 

  • Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755

    Article  CAS  PubMed  Google Scholar 

  • Janin A, Léna JP, Joly P (2011) Beyond occurrence: body condition and stress hormone as integrative indicators of habitat availability and fragmentation in the common toad. Biol Conserv 144:1008–1016

    Article  Google Scholar 

  • Joly P, Morand A (1994) Theoretical habitat templets, species traits, and species richness: amphibians in the Upper Rhone River and its floodplain. Freshwater Biol 31:455–468

    Article  Google Scholar 

  • Joly P, Miaud C, Lehmann A, Grolet O (2001) Habitat matrix effects on pond occupancy in newts. Conserv Biol 15:239–248

    Article  Google Scholar 

  • Karraker NE, Gibbs JP, Vonesh JR (2008) Impacts of road deicing salt on the demography of vernal pool-breeding amphibians. Ecol Appl 18:724–734

    Article  PubMed  Google Scholar 

  • Kendall WL, White GC (2009) A cautionary note on substituting spatial subunits for repeated temporal sampling in studies of site occupancy. J Appl Ecol 46:1182–1188

    Google Scholar 

  • Kéry M, Schmidt BR (2008) Imperfect detection and its consequences for monitoring for conservation. Community Ecol 9:207–216

    Article  Google Scholar 

  • Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681–684

    Article  CAS  PubMed  Google Scholar 

  • Knutson MG, Richardson WB, Reineke DM, Gray BR, Parmelee JR, Weick SE (2004) Agricultural ponds support amphibian populations. Ecol Appl 14:669–684

    Article  Google Scholar 

  • Kopecky O, Vojar J, Denoël M (2010) Movements of Alpine newts (Mesotriton alpestris) between small aquatic habitats (ruts) during the breeding season. Amphibia-Reptilia 31:109–116

    Article  Google Scholar 

  • Lengagne T (2008) Traffic noise affects communication behaviour in a breeding anuran, Hyla arborea. Biol Conserv 141:2023–2031

    Article  Google Scholar 

  • Lesbarrères D, Primmer CR, Lodé T, Merilä J (2006) The effects of 20 years of highway presence on the genetic structure of Rana dalmatina populations. Ecoscience 13:531–538

    Article  Google Scholar 

  • Lescure J, Pichenot J, Cochard PO (2011) Régression de Bombina variegata (Linné, 1758) en France par l’analyse de sa répartition passée et présente. B Soc Herpetol Fr 137:5–41 (in French with English abstract)

    Google Scholar 

  • MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle AJ, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255

    Article  Google Scholar 

  • MacKenzie DI, Bailey LL, Hines JE, Nichols JD (2011) An integrated model of habitat and species occurrence dynamics. Method Ecol Evol 2:612–622

    Article  Google Scholar 

  • Marzluff JM, Bowman R, Donnelly R (2001) Avian ecology and conservation in an urbanizing world. Springer, Boston

    Book  Google Scholar 

  • Massemin D, Cheylan M (2001) Eléments bibliographiques sur le statut passé et actuel du Sonneur à ventre jaune Bombina variegata (L.) (Anura; Discoglossidae) en région méditerranéenne française. B Soc Herpetol Fr 97:41–47 (in French with English abstract)

    Google Scholar 

  • Mazerolle MJ (2004) Amphibian road mortality in response to nightly variations in traffic intensity. Herpetologica 60:45–53

    Article  Google Scholar 

  • Mazerolle MJ, Desrochers A, Rochefort L (2005) Landscape characteristics influence pond occupancy by frogs after accounting for detectability. Ecol Appl 15:824–834

    Article  Google Scholar 

  • Mohneke R, Schneider H (1979) Effect of temperature upon auditory thresholds in two anuran species, Bombina v. variegata and Alytes o. obstetricans (Amphibia, Discoglossidae). J Comp Physiol 130:9–16

    Article  Google Scholar 

  • Morand A (1997) Stabilité relative des habitats de développement larvaire et de reproduction de Bombina variegata et Bufo calamita: l’insuffisance des Modèles rK et rKA. Geobios 30:23–36

    Article  Google Scholar 

  • Noël S, Ouellet M, Galois P, Lapointe FJ (2007) Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander. Conserv Genet 8:599–606

    Article  Google Scholar 

  • Oseen KL, Wassersug RJ (2002) Environmental factors influencing calling in sympatric anurans. Oecologia 133:616–625

    Article  Google Scholar 

  • Pellet J, Schmidt BR (2005) Monitoring distributions using call surveys: estimating site occupancy, detection probabilities and inferring absence. Biol Conserv 123:27–35

    Article  Google Scholar 

  • Pichenot J (2008) Contribution à la Biologie du Sonneur à ventre jaune (Bombina variegata, L.), Ecologie spatiale et approche multi-échelle de la sélection de l’habitat en limite septentrionale de son aire de répartition, PhD Thesis, University of Champagne-Ardennes, Reims (in French with English abstract)

  • Piha H, Luoto M, Merilä J (2007) Amphibian occurrence is influenced by current and historic landscape characteristics. Ecol Appl 17:2298–2309

    Article  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. URL http://www.R-project.org/

  • Riley SP, Busteed GT, Kats LB, Vandergon TL, Lee LF, Dagit RG, Kerby JL, Sauvajot RM (2005) Effects of urbanization on the distribution and abundance of amphibians and invasive species in southern California streams. Conserv Biol 19:1894–1907

    Article  Google Scholar 

  • Rota CT, Fletcher RJ, Dorazio RM, Betts MG (2009) Occupancy estimation and the closure assumption. J Appl Ecol 46:1173–1181

    Google Scholar 

  • Rotem G, Ziv Y, Giladi I, Bouskila A (2013) Wheat fields as an ecological trap for reptiles in a semiarid agroecosystem. Biol Conserv 167:349–353

    Article  Google Scholar 

  • Rubbo MJ, Kiesecker JM (2005) Amphibian breeding distribution in an urbanized landscape. Conserv Biol 19:504–511

    Article  Google Scholar 

  • Safner T, Miaud C, Gaggiotti O, Decout S, Rioux D, Zundel S, Manel S (2011) Combining demography and genetic analysis to assess the population structure of an amphibian in a human-dominated landscape. Conserv Genet 12:161–173

    Article  Google Scholar 

  • Sanzo D, Hecnar SJ (2006) Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica). Environ Pollut 140:247–256

    Article  CAS  PubMed  Google Scholar 

  • Schmidt BR (2005) Monitoring the distribution of pond-breeding amphibians when species are detected imperfectly. Aquat Conserv 15:681–692

    Article  Google Scholar 

  • Schmidt BR, Pellet J (2005) Relative importance of population processes and habitat characteristics in determining site occupancy of two anurans. J Wildlife Manage 69:884–893

    Article  Google Scholar 

  • Sewell D, Beebee TJ, Griffiths RA (2010) Optimizing biodiversity assessments by volunteers: the application of occupancy modelling to large-scale amphibian surveys. Biol Conserv 143:2102–2110

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Tanadini LG, Schmidt BR (2011) Population size influences amphibian detection probability: implications for biodiversity monitoring programs. PLoS One 6:e28244. doi:10.1371/journal.pone.0028244

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thiriet J, Vacher JP (2010) Atlas des Répartition des Amphibiens et Reptiles d’Alsace. Bufo, Colmar, Strasbourg (in French)

  • Vacher JP (2013) Le Sonneur à ventre jaune (Bombina variegata) en Alsace: statut, menaces et plan régional d’actions. Ciconia 37:52–62 (in French)

    Google Scholar 

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

    Article  Google Scholar 

  • van der Meer E, Fritz H, Blinston P, Rasmussen GS (2013) Ecological trap in the buffer zone of a protected area: effects of indirect anthropogenic mortality on the African wild dog Lycaon pictus. Oryx 48:285–293

    Article  Google Scholar 

  • Vos CC, Antonisse-De Jong AG, Goedhart PW, Smulders MJM (2001) Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 86:598–608

    Article  CAS  PubMed  Google Scholar 

  • Warren SD, Büttner R (2008) Relationship of endangered amphibians to landscape disturbance. J Wildlife Manage 72:738–744

    Article  Google Scholar 

  • Weir LA, Royle JA, Nanjappa P, Jung RE (2005) Modeling anuran detection and site occupancy on North American Amphibian Monitoring Program (NAAMP) routes in Maryland. J Herpetol 39:627–639

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Aurélien Besnard for his advice with the design of the protocol, Gaël Fellet and Julien Prinet from the French Forest Agency for facilitating the field work, Victoria Michel for helping us collecting data and for her help with the GIS software, Wendy Hahn and Stéphanie Kaempf for helping us with the GIS, and Anne Ganet, Fanny Gosselin, Adeline Haller, and Priscilla Illy for their help in the field.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hugo Cayuela.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 252 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cayuela, H., Lambrey, J., Vacher, JP. et al. Highlighting the effects of land-use change on a threatened amphibian in a human-dominated landscape. Popul Ecol 57, 433–443 (2015). https://doi.org/10.1007/s10144-015-0483-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-015-0483-4

Keywords

Navigation