Skip to main content

Repeated reduction in parasite diversity in invasive populations of Xenopus laevis: a global experiment in enemy release

Abstract

The introduction of species to multiple continents creates natural experiments suited to the evaluation of ecological hypotheses. For the Enemy Release Hypothesis (ERH), which postulates that the success of invasive populations hinges upon release from the effects of their natural enemies, assessments of parasite loss during invasion across independent geographical replicates are scarce. This study is the first to test the ERH for a globally invasive amphibian, Xenopus laevis, a successful invader on four continents with a well-described parasite fauna. In this study, the metazoan parasite communities of X. laevis from 20 invasive and 27 native sites in five countries and three continents were compared. An overall pattern of reduced parasite diversity in invasive X. laevis was not yet countered by acquisition of novel parasites. Invasive X. laevis harboured impoverished parasite communities that were distinct from those of native X. laevis from undisturbed habitats. Conversely, parasite communities from native X. laevis from disturbed habitats were similar to those from the invasive range. Accompanying parasites were common in the native range and included both generalists with indirect and specialists with direct life cycles. Our findings emphasise that parasite loss is characteristic of the invasion process of X. laevis and possibly contributes to its success as a global invader. The ERH is supported in terms of metazoan parasites as natural enemies, irrespective of the geographical origin, climatic conditions and invasion history of the host populations. This study also draws attention to parasites that co-invade with their hosts as invaders in their own right.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

Download references

Acknowledgements

The authors would like to express their sincere thanks to a number of persons who assisted in the collection of the frogs. Guénolé le Peutrec helped with the collection in France. In South Africa, several farm owners graciously gave permission for collection to take place on their properties and provided lodging for the research team: Fanus and Olga Kritzinger, William and Christa van Zyl, Dave Schlebusch, Fanus and Carin Oberholzer, Danie and Annalise Marais, Johan Hamann, Tobie Bielt, Gert Bench, Stoffel Labuschagne, Jannie and Susan van Rensburg, Jan Meintjies, Marthinus Hartman, Douw and Louise de Jager, Ernest de Villiers, and Danie and René Botha. Lastly, Mathys Schoeman, Annemie de Klerk, Clarke Scholtz, Andrea Darvall, Willie Landman, Ferdi de Lange and Roxanne Viviers assisted with the collection of frogs at the remainder of the localities in South Africa. A.L.S. received funding from the DST-NRF Centre of Excellence for Invasion Biology (South Africa). The utilisation of the frogs and the research protocols were approved by the Animal Care, Health and Safety in Research Ethics (AnimCare) Committee of the Faculty of Health Sciences of the North-West University (ethics number: NWU-0380-16-A5-01). Animals from the native South African populations were sampled under the permits 0056-AAA007-00224 (CapeNature) and FAUNA 1343-2017 (Northern Cape) provided by the Department of Economic Development, Environmental Affairs and Tourism.

Author information

Authors and Affiliations

Authors

Contributions

All authors were involved in initial conception, study design and data collection, as well as in editing and revision of the manuscript. A.L.S. generated the molecular data, performed the statistical analyses, prepared the tables and figures and led the manuscript writing.

Corresponding author

Correspondence to Anneke Lincoln Schoeman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 28 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schoeman, A.L., Kruger, N., Secondi, J. et al. Repeated reduction in parasite diversity in invasive populations of Xenopus laevis: a global experiment in enemy release. Biol Invasions 21, 1323–1338 (2019). https://doi.org/10.1007/s10530-018-1902-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-018-1902-1

Keywords

  • African clawed frog
  • Enemy Release Hypothesis
  • Globally invasive amphibians
  • Invasion ecology
  • Natural experiments
  • Parasite loss