Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Jun 22;270(1521):1309–1314. doi: 10.1098/rspb.2003.2358

Parasite-mediated predation between native and invasive amphipods.

Calum MacNeil 1, Jaimie T A Dick 1, Melanie J Hatcher 1, Rebecca S Terry 1, Judith E Smith 1, Alison M Dunn 1
PMCID: PMC1691366  PMID: 12816645

Abstract

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0-90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single-species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed-species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.

Full Text

The Full Text of this article is available as a PDF (300.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrams-Ogg A. C., Kruth S. A., Carter R. F., Dick J. E., Valli V. E., Kamel-Reid S., Dubé I. D. Clinical and pathological findings in dogs following supralethal total body irradiation with and without infusion of autologous long-term marrow culture cells. Can J Vet Res. 1993 Apr;57(2):79–88. [PMC free article] [PubMed] [Google Scholar]
  2. Baker M. D., Vossbrinck C. R., Didier E. S., Maddox J. V., Shadduck J. A. Small subunit ribosomal DNA phylogeny of various microsporidia with emphasis on AIDS related forms. J Eukaryot Microbiol. 1995 Sep-Oct;42(5):564–570. doi: 10.1111/j.1550-7408.1995.tb05906.x. [DOI] [PubMed] [Google Scholar]
  3. Basilico V., Ricciardi L., Giani S. La misura della velocità dell'onda sfigmica. Boll Soc Ital Biol Sper. 1979 Sep 15;55(17):1759–1765. [PubMed] [Google Scholar]
  4. Bauer A., Trouvé S., Grégoire A., Bollache L., Cézilly F. Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. Int J Parasitol. 2000 Dec;30(14):1453–1457. doi: 10.1016/s0020-7519(00)00138-7. [DOI] [PubMed] [Google Scholar]
  5. Carius H. J., Little T. J., Ebert D. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution. 2001 Jun;55(6):1136–1145. doi: 10.1111/j.0014-3820.2001.tb00633.x. [DOI] [PubMed] [Google Scholar]
  6. Ebert D., Herre E. A. The evolution of parasitic diseases. Parasitol Today. 1996 Mar;12(3):96–101. doi: 10.1016/0169-4758(96)80668-5. [DOI] [PubMed] [Google Scholar]
  7. Gatehouse H. S., Malone L. A. The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J Invertebr Pathol. 1998 Mar;71(2):97–105. doi: 10.1006/jipa.1997.4737. [DOI] [PubMed] [Google Scholar]
  8. Herre E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science. 1993 Mar 5;259(5100):1442–1445. doi: 10.1126/science.259.5100.1442. [DOI] [PubMed] [Google Scholar]
  9. Mooney H. A., Cleland E. E. The evolutionary impact of invasive species. Proc Natl Acad Sci U S A. 2001 May 8;98(10):5446–5451. doi: 10.1073/pnas.091093398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Vossbrinck C. R., Baker M. D., Didier E. S., Debrunner-Vossbrinck B. A., Shadduck J. A. Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. J Eukaryot Microbiol. 1993 May-Jun;40(3):354–362. doi: 10.1111/j.1550-7408.1993.tb04928.x. [DOI] [PubMed] [Google Scholar]
  11. Weiss L. M., Zhu X., Cali A., Tanowitz H. B., Wittner M. Utility of microsporidian rRNA in diagnosis and phylogeny: a review. Folia Parasitol (Praha) 1994;41(2):81–90. [PubMed] [Google Scholar]
  12. Zaret T. M., Paine R. T. Species Introduction in a Tropical Lake: A newly introduced piscivore can produce population changes in a wide range of trophic levels. Science. 1973 Nov 2;182(4111):449–455. doi: 10.1126/science.182.4111.449. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES