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Intra-phylum and inter-phyla associations among gastrointestinal parasites in two wild mammal species

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Abstract

A growing body of literature reveals that the interactions among the parasite community may be strong and significant for parasite dynamics. There may be inter-specific antagonistic interactions as a result of competition and cross-effective immune response, or synergistic interactions where infection by one parasite is facilitated by another one, either by an impoverishment of the host’s defenses, parasite-induced selective immunosuppression, or trade-offs within the immune system. The nature of these interactions may depend on how related are the parasite species involved. Here we explored the presence of associations among gastrointestinal parasites (coccidia and helminths) in natural populations of two wild mammal species, the capybara (Hydrochoerus hydrochaeris) and the guanaco (Lama guanicoe). The associations explored were between the oocyst outputs of a selected Eimeria species and the other coccidia of that parasite community, and between Eimeria spp. and the predominant nematodes. The statistical analysis included adjustment for potential confounders or effect modifiers. In guanacos, the prevailing interactions were synergistic among the coccidia and between coccidia and nematodes (Nematodirus spp.). However, in capybaras, the interaction between nematodes (Viannaiidae) and Eimeria spp. depended on environmental and host factors. The relationship was positive in some circumstances (depending on season, year, sex, or animal size), but it appeared to become antagonistic under different scenarios. These antagonist interactions did not follow a particular seasonal pattern (they occurred in autumn, spring, and summer), but they were predominantly found in females (when they depended on sex) or in 2010 and 2011 (when they depended on the sampling year). These results suggest that the relationship between coccidia and nematodes in capybaras may be context dependent. We propose that the context-dependent immune investment documented in capybaras may be the cause of these varying interactions.

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Acknowledgments

This study was funded by the Agencia Nacional de Promoción Científica y Tecnológica (PICT2010-2202), the Secretaría de Estado de Ciencia, Tecnología e Innovación de la Provincia de Santa Fe (SECTEI-21-08-12), and the Universidad Nacional del Litoral (CAI+D 002-009). PGM and ATE are fellows of CONICET.

We thank Pablo Carmanchahi, Carolina Marull, Virginia Rago, Sebastian Cirignoli, Daniel Zurvera, Valeria Debárbora, Natalia Schroeder, Paula Taraborelli, Pablo Gregorio, Pedro Insaurralde, the Payun Matru Cooperative, the Instituto Argentino de Investigación de las Zonas Áridas (IADIZA), and The Conservation Land Trust staff for their essential support during fieldwork.

The laboratory and field work was conducted in full compliance with the Bioethical Committee of the School of Veterinary Medicine of Universidad Nacional del Litoral.

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Authors and Affiliations

  1. Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral, Universidad Nacional del Litoral—Consejo Nacional de Investigaciones Científicas y Técnicas, RP Kreder 2805, 3080, Esperanza, Santa Fe, Argentina

    P. G. Moreno, M. A. T. Eberhardt, D. Lamattina & P. M. Beldomenico

  2. Grupo de Investigación en Ecofisiología de Fauna Silvestre, Mendoza, Argentina

    P. G. Moreno

  3. Departamento de Ciencias Naturales, Facultad de Humanidades y Ciencias, Universidad Nacional del Litoral, Santa Fe, Argentina

    M. A. Previtali

  4. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    M. A. Previtali & P. M. Beldomenico

Authors
  1. P. G. Moreno
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  2. M. A. T. Eberhardt
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  3. D. Lamattina
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  4. M. A. Previtali
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  5. P. M. Beldomenico
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Corresponding author

Correspondence to P. M. Beldomenico.

Additional information

P. G. Moreno and M. A. T. Eberhardt contributed equally to this work.

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Moreno, P.G., Eberhardt, M.A.T., Lamattina, D. et al. Intra-phylum and inter-phyla associations among gastrointestinal parasites in two wild mammal species. Parasitol Res 112, 3295–3304 (2013). https://doi.org/10.1007/s00436-013-3509-x

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  • DOI: https://doi.org/10.1007/s00436-013-3509-x

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