Skip to main content
SpringerLink
Log in

Factors regulating the invasive success of an alien frog: a comparison of the ecology of the native and alien populations

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

We examined niche occupancy of Discoglossus pictus, an anuran recently established in Europe, comparing the niches of native (North Africa) and alien populations (south-western Europe) at two spatial scales to determine whether adaptive divergence had occurred between these two populations. Additionally, we determine whether the alien species showed a wider larvae niche and higher phenotypic variability compared with co-occurring anurans. We characterized the breeding habitats and the climatic space occupied by native and alien groups of populations of D. pictus and examined morphological traits of D. pictus and sympatric anuran larvae. Our results revealed no divergence in breeding habitat use between native and alien populations. A shift was observed between the realized niches occupied by the native and alien populations, but this shift might only reflect cryptic niche conservatism. The range of reproductive habitats selected by D. pictus was not wider than those of most native species. In the invaded range, D. pictus showed morphological overlap with some native species and broader phenotypic variability, but the adaptive advantages of this latter attribute were uncertain. Our results suggest that the invasive capacity of this species depends on favourable abiotic conditions rather than on its adaptive advantages over native anurans.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altig, R., 2007. A primer for the morphology of anuran tadpoles. Herpetological Conservation and Biology 2: 71–74.

    Google Scholar 

  • Altig, R. & G. F. Johnston, 1989. Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetological Monographs 3: 81–109.

    Article  Google Scholar 

  • Anderson, M. J., 2005. PERMANOVA: a computer program for permutational multivariate analysis of variance. Department of Statistics-University of Auckland, Auckland.

    Google Scholar 

  • Anderson, R. P. & I. Gonzalez, 2011. Species-specific tuning increases robustness to sampling bias in models of species distributions: an implementation with MaxEnt. Ecological Modelling 222: 2796–2811.

    Article  Google Scholar 

  • Angetter, L. S., S. Loetters & D. Roedder, 2011. Climate niche shift in invasive species: the case of the brown anole. Biological Journal of the Linnean Society 104: 943–954.

    Article  Google Scholar 

  • Ben Hassine, J. & S. Nouira, 2009. Diet of Discoglossus pictus Otth, 1837 (Anura, Alytidae) and Pelophylax saharicus (Boulenger in Hartert, 1913) in the oases of Kettana (Gabes, Tunisia). Bulletin de la Société Zoologique de France 134: 321–332.

    Google Scholar 

  • Ben Hassine, J. & S. Nouira, 2012. Répartition géographique et affinités écologiques des Amphibiens de Tunisie. Revue d’Écologie (Terre & Vie) 67: 437–457.

    Google Scholar 

  • Bosch, J. & Í. Martínez-Solano, 2003. Factors influencing occupancy of breeding ponds in a montane amphibian assemblage. Journal of Herpetology 37: 410–413.

    Article  Google Scholar 

  • Boix, D., J. Sala, X. D. Quintana & R. Moreno-Amich, 2004. Succession of the animal community in a Mediterranean temporary pond. Journal of the North American Benthological Society 23: 29–49.

    Article  Google Scholar 

  • Broennimann, O., U. A. Treier, H. Müller-Schärer, W. Thuiller, A. T. Peterson & A. Guisan, 2007. Evidence of climatic niche shift during biological invasion. Ecology Letters 10: 701–709.

    Article  CAS  PubMed  Google Scholar 

  • Broennimann, O., M. C. Fitzpatrick, P. B. Pearman, B. Petitpierre, L. Pellissier, N. G. Yoccoz, W. Thuiller, M. J. Fortin, C. Randin, N. E. Zimmermann, C. H. Graham & A. Guisan, 2012. Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography 21: 481–497.

    Article  Google Scholar 

  • Buckley, L. B. & W. Jetz, 2007. Environmental and historical constraints on global patterns of amphibian richness. Proceedings of the Royal Society B: Biological Sciences 274: 1167–1173.

    Article  PubMed  PubMed Central  Google Scholar 

  • Buskirk, J. V. & R. A. Relyea, 1998. Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biological Journal of the Linnean Society 65: 301–328.

    Article  Google Scholar 

  • Capula, M., 2007. Discoglossus pictus. In Lanza, B., F. Andreone, M. A. Bologna, C. Corti & E. Razzetti (eds), Fauna d’Italia: Amphibia. Calderini, Bologna.

    Google Scholar 

  • Chessel, D., A. Dufour & S. Dray, 2012. Ade4. R Package, version 1.5.1.

  • Chovanec, A., 1992. The influence of tadpole swimming behaviour on predation by dragonfly nymphs. Amphibia-Reptilia 13: 341–349.

    Article  Google Scholar 

  • Cleland, E. E., C. M. Clark, S. L. Collins, J. E. Fargione, L. Gough, K. L. Gross, S. C. Pennings & K. N. Suding, 2011. Patterns of trait convergence and divergence among native and exotic species in herbaceous plant communities are not modified by nitrogen enrichment. Journal of Ecology 99: 1327–1338.

    Article  CAS  Google Scholar 

  • Davidson, A. M., M. Jennions & A. B. Nicotra, 2011. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters 14: 419–431.

    Article  PubMed  Google Scholar 

  • Davis, M. A., K. Thompson & J. Philip Grime, 2005. Invasibility: the local mechanism driving community assembly and species diversity. Ecography 28: 696–704.

    Article  Google Scholar 

  • Denver, R. J., N. Mirhadi & M. Phillips, 1998. Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology 79: 1859–1872.

    Google Scholar 

  • Díaz-Paniagua, C., C. Gómez-Rodríguez, A. Portheault & W. de Vries, 2005. Los anfibios de Doñana. Organismo Autónomo Parques Nacionales, Madrid.

    Google Scholar 

  • Dolédec, S., D. Chessel & C. Gimaret-Carpentier, 2000. Niche separation in community analysis: a new method. Ecology 81: 2914–2927.

    Article  Google Scholar 

  • Dutra, S. L. & M. Callisto, 2005. Macroinvertebrates as tadpole food: importance and body size relationships. Revista Brasileira de Zoologia 22: 923–927.

    Article  Google Scholar 

  • Elton, C. S., 1958. The Ecology of Invasions by Animals and Plants. Methuen, London.

    Book  Google Scholar 

  • Escoriza, D. & D. Boix, 2012. Assessing the potential impact of an alien species in a Mediterranean amphibian assemblage: a morphological and ecological approach. Hydrobiologia 680: 233–245.

    Article  Google Scholar 

  • Escoriza, D., D. Espejo & M. M. Comas, 2007. Nuevo límite altitudinal para Discoglossus pictus Otth, 1837 (Anura: Discoglossidae) en el nordeste de Cataluña. Boletín de la Asociación. Herpetológica Española 18: 24–25.

    Google Scholar 

  • Fox, M. G., A. Vila-Gispert & G. H. Copp, 2007. Life-history traits of introduced Iberian pumpkinseed Lepomis gibbosus relative to native populations. Can differences explain colonization success? Journal of Fish Biology 71: 56–69.

    Article  Google Scholar 

  • Freeman, E., 2012. PresenceAbsence. R Package, version 1.1.9.

  • Friday, L. E., 1987. The diversity of macro invertebrate and macrophyte communities in ponds. Freshwater Biology 18: 87–104.

    Article  Google Scholar 

  • García-París, M., A. Montori & P. Herrero, 2004. Amphibia, Lissamphibia. In Ramos, M. A., et al. (eds), Fauna Ibérica, Vol. 24. Museo Nacional de Ciencias Naturales-CSIC, Madrid.

    Google Scholar 

  • Geniez, P. & V. Fradet, 2013. Discoglossus pictus. In Lescure, J. & J. C. De Massary (eds), Atlas des amphibiens et reptiles de France. Biotope editions, Mèze.

    Google Scholar 

  • Gómez-Rodríguez, C., C. Díaz-Paniagua, L. Serrano, M. Florencio & A. Portheault, 2009. Mediterranean temporary ponds as amphibian breeding habitats: the importance of preserving pond networks. Aquatic Ecology 43: 1179–1191.

    Article  Google Scholar 

  • Gosner, K. L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.

    Google Scholar 

  • Hansen, M. J. & A. P. Clevenger, 2005. The influence of disturbance and habitat on the presence of non-native plant species along transport corridors. Biological Conservation 125: 249–259.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones & A. Jarvis, 2005. Very high resolution interpolated global terrestrial climate surfaces. International Journal of Climatology 25: 1965–1978.

    Article  Google Scholar 

  • Hijmans, R. J., L. Guarino, C. Bussink, I. Barrantes & E. Rojas, 2011. DIVA-GIS, version 7.5.

  • Jackson, A. L., R. Inger, A. C. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.

    Article  PubMed  Google Scholar 

  • Jakob, C., G. Poizat, M. Veith, A. Seitz & A. J. Crivelli, 2003. Breeding phenology and larval distribution of amphibians in a Mediterranean pond network with unpredictable hydrology. Hydrobiologia 499: 51–61.

    Article  Google Scholar 

  • Kozak, K. H. & J. Wiens, 2006. Does niche conservatism promote speciation? A case study in North American salamanders. Evolution 60: 2604–2621.

    Article  PubMed  Google Scholar 

  • Lardner, B., 2000. Morphological and life history responses to predators in larvae of seven anurans. Oikos 88: 169–180.

    Article  Google Scholar 

  • Lawler, S. P. & P. J. Morin, 1993. Food web architecture and population dynamics in laboratory microcosms of protists. American Naturalist 141: 675–686.

    Article  CAS  PubMed  Google Scholar 

  • Layman, C. A. & J. E. Allgeier, 2011. Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in The Bahamas. Marine Ecology Progress Series 448: 131–141.

    Article  Google Scholar 

  • Liu, C., P. M. Berry, T. P. Dawson & R. G. Pearson, 2005. Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28: 385–393.

    Article  Google Scholar 

  • Llorente, G. A., A. Montori, X. Santos & M. A. Carretero, 1995. Atlas dels Amfibis i Rèptils de Catalunya i Andorra. El Brau, Figueres.

    Google Scholar 

  • Martínez-Solano, Í., 2004. Phylogeography of Iberian Discoglossus (Anura: Discoglossidae). Journal of Zoological Systematics and Evolutionary Research 42: 298–305.

    Article  Google Scholar 

  • Martínez-Solano, I. & M. García-París, 2002. Discoglossus jeanneae Busack, 1986. Sapillo pintojo meridional. In Pleguezuelos, J. M., R. Márquez & M. Lizana (eds), Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica Española, Madrid.

    Google Scholar 

  • McCollum, S. A. & J. D. Leimberger, 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole color, span ratio, and growth rate. Oecologia 109: 615–621.

    Article  Google Scholar 

  • Montori, A., G. Llorente, A. Richter-Boix, D. Villero, M. Franch & A. Garriga, 2007. Colonización y efectos potenciales de la especie invasora Discoglossus pictus sobre las especies nativas. Munibe 25: 14–27.

    Google Scholar 

  • Mooney, H. A. & E. E. Cleland, 2001. The evolutionary impact of alien species. Proceedings of the National Academy of Sciences 98: 5446–5451.

    Article  CAS  Google Scholar 

  • Ordonez, A., I. J. Wright & H. Olff, 2010. Functional differences between native and alien species: a global-scale comparison. Functional Ecology 24: 1353–1361.

    Article  Google Scholar 

  • Pabijan, M., A. Crottini, D. Reckwell, I. Irisarri, J. Susanne-Hauswaldt & M. Vences, 2012. A multigene species tree for Western Mediterranean painted frogs (Discoglossus). Molecular Phylogenetics and Evolution 64: 690–696.

    Article  PubMed  Google Scholar 

  • Parnell, A. & A. Jackson, 2013. Package ‘siar’ vs 4.2.

  • Pearson, R. G., C. J. Raxworthy, M. Nakamura & A. T. Peterson, 2007. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography 34: 102–117.

    Article  Google Scholar 

  • Phillips, B. L., G. P. Brown & R. Shine, 2010. Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. Journal of evolutionary biology 23: 2595–2601.

    Article  CAS  PubMed  Google Scholar 

  • Phillips, S., M. Dudik & R. Schapire, 2012. MaxEnt 3.3.3k. AT & T Labs-Research, Princeton University.

    Google Scholar 

  • Qian, H., X. Wang, S. Wang & Y. Li, 2007. Environmental determinants of amphibian and reptile species richness in China. Ecography 30: 71–482.

    Article  Google Scholar 

  • R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Relyea, R. A., 2004. Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 85: 172–179.

    Article  Google Scholar 

  • Rödder, D. & S. Lötters, 2009. Niche shift versus niche conservatism? Climatic characteristics of the native and invasive ranges of the Mediterranean house gecko (Hemidactylus turcicus). Global Ecology and Biogeography 18: 674–687.

    Article  Google Scholar 

  • Rodríguez, M. A., J. A. Belmontes & B. A. Hawkins, 2005. Energy, water and large-scale patterns of reptile and amphibian species richness in Europe. Acta Oecologica 28: 65–70.

    Article  Google Scholar 

  • Sakai, A., F. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, D. E. Mc Cauley, P. O’Neill, I. M. Parker, J. N. Thompson & S. G. Weller, 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332.

    Article  Google Scholar 

  • Sancho, V., 2000. Datos sobre la distribución y estatus del sapillo pintojo (Discoglossus jeanneae) en la Comunidad Valenciana. Revista d’Observació i Estudi de la Natura 1: 13–16.

    Google Scholar 

  • Sax, D. F. & S. D. Gaines, 2003. Species diversity: from global decreases to local increases. Trends in Ecology & Evolution 18: 561–566.

    Article  Google Scholar 

  • Sax, D. F., J. J. Stachowicz, J. H. Brown, J. F. Bruno, M. N. Dawson, S. D. Gaines, R. K. Grosberg, A. Hastings, R. D. Holt, M. M. Mayfield, M. I. O’Connor & W. R. Rice, 2007. Ecological and evolutionary insights from species invasions. Trends in Ecology and Evolution 22: 465–471.

    Article  PubMed  Google Scholar 

  • Schulte, U., A. Hochkirch, S. Lötters, D. Rödder, S. Schweiger, T. Weimann & M. Veith, 2012. Cryptic niche conservatism among evolutionary lineages of an invasive lizard. Global Ecology and Biogeography 21: 198–211.

    Article  Google Scholar 

  • Simberloff, D., J. L. Martin, P. Genovesi, V. Maris, D. A. Wardle, J. Aronson, F. Courchamp, B. Galil, E. García-Berthou, M. Pascal, P. Pyšek, R. Sousa, E. Tabacchi & M. Vilà, 2012. Impacts of biological invasions: what’s what and the way forward. Trends in Ecology and Evolution 28: 58–66.

    Article  PubMed  Google Scholar 

  • Skelly, D. K., 2001. Distributions of pond-breeding anurans: an overview of mechanisms. Israel Journal of Zoology 47: 313–332.

    Article  Google Scholar 

  • Smith, K. G., 2005. Effects of nonindigenous tadpoles on native tadpoles in Florida: evidence of competition. Biological Conservation 123: 433–441.

    Article  Google Scholar 

  • Stephens, P. R. & J. J. Wiens, 2009. Bridging the gap between community ecology and historical biogeography: niche conservatism and community structure in emydid turtles. Molecular Ecology 18: 4664–4679.

    Article  CAS  PubMed  Google Scholar 

  • Thomson, J. A., M. R. Heithaus, D. A. Burkholder, J. J. Vaudo, A. J. Wirsing & L. M. Dill, 2012. Site specialists, diet generalists? Isotopic variation, site fidelity, and foraging by loggerhead turtles in Shark Bay, Western Australia. Marine Ecology Progress Series 453: 213–226.

    Article  Google Scholar 

  • Tingley, R., M. J. Greenlees & R. Shine, 2012. Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121: 1959–1965.

    Article  Google Scholar 

  • Trabucco, A. & R. J. Zomer, 2009. Global Aridity Index (Global Aridity) and Global Potential EvapoTranspiration (Global-PET) geospatial database. CGIAR Consortium for Spatial Information. Available at: http://www.cgiar-csi.org/.

  • Vences, M., M. Puente, S. Nieto & D. R. Vieites, 2002. Phenotypic plasticity of anuran larvae: environmental variables influence body shape and oral morphology in Rana temporaria tadpoles. Journal of Zoology 257: 155–162.

    Article  Google Scholar 

  • Wiens, J. J. & C. H. Graham, 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual review of ecology, evolution, and systematics 36: 519–539.

    Article  Google Scholar 

  • Wiens, J. J., D. D. Ackerly, A. P. Allen, B. L. Anacker, L. B. Buckley, H. V. Cornell, E. J. Damschen, T. J. Davies, J. A. Grytnes, S. P. Harrison, B. A. Hawkins, R. D. Holt, C. McCain & P. R. Stephens, 2010. Niche conservatism as an emerging principle in ecology and conservation biology. Ecology Letters 13: 1310–1324.

    Article  PubMed  Google Scholar 

  • Wintrebert, P., 1908. Présence à Banyuls-sur-Mer (Pyrénées-Orientales) du Discoglossus pictus Otth. Bulletin de la Société Zoologique de France 33: 54.

    Google Scholar 

  • Wu, Z., Y. Li, Y. Wang & M. J. Adams, 2005. Diet of introduced bullfrogs (Rana catesbeiana): predation on and diet overlap with native frogs on Daishan Island, China. Journal of Herpetology 39: 668–674.

    Article  Google Scholar 

Download references

Acknowledgments

Permits for field work were provided by the Tunisian Ministry of Agriculture and the Departament de Medi Ambient de Catalunya (ref. SF/574). The authors wish to thank Saïd Nouira (Faculty of Sciences of Tunis) and Ali Bouattour (Institute Pasteur, Tunis) for their assistance. We thank the staff of the Zona Volcànica de la Garrotxa Natural Park for providing access to unpublished data. This work was supported by a grant from the Spanish Ministerio de Ciencia e Innovación, Programa de Investigación Fundamental No Orientada (CGL2011-23907). The authors are also grateful to two anonymous reviewers whose comments have helped in improving the manuscript.

Author information

Authors and Affiliations

  1. Institute of Aquatic Ecology, University of Girona, Campus Montilivi, 17071, Girona, Spain

    Daniel Escoriza & Dani Boix

  2. Faculty of Sciences of Tunis, University Tunis El Manar, 2092, Tunis, Tunisia

    Jihène Ben Hassine

Authors
  1. Daniel Escoriza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jihène Ben Hassine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dani Boix
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel Escoriza.

Additional information

Handling editor: Lee B. Kats

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Escoriza, D., Ben Hassine, J. & Boix, D. Factors regulating the invasive success of an alien frog: a comparison of the ecology of the native and alien populations. Hydrobiologia 730, 127–138 (2014). https://doi.org/10.1007/s10750-014-1827-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-014-1827-3

Keywords

Search

Navigation