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Diversity and patterns of interaction of an anuran–parasite network in a neotropical wetland

Published online by Cambridge University Press:  07 October 2015

K. M. CAMPIÃO ,
A. RIBAS  and
L. E. R. TAVARES
K. M. CAMPIÃO*
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal Paraná, Curitiba, Brazil
A. RIBAS
Affiliation:
Faculdade de Computação, Universidade Federal do Mato Grosso do Sul, Brazil
L. E. R. TAVARES
Affiliation:
Departamento de Biologia, Universidade Federal do Mato Grosso do Sul, Brazil
*
*Corresponding author: Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal Paraná, 81531-980, Curitiba, Brazil. E-mail: karla_mcamp@yahoo.com.br
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Summary

We describe the diversity and structure of a host–parasite network of 11 anuran species and their helminth parasites in the Pantanal wetland, Brazil. Specifically, we investigate how the heterogeneous use of space by hosts changes parasite community diversity, and how the local pool of parasites exploits sympatric host species of different habits. We examined 229 anuran specimens, interacting with 32 helminth parasite taxa. Mixed effect models indicated the influence of anuran body size, but not habit, as a determinant of parasite species richness. Variation in parasite taxonomic diversity, however, was not significantly correlated with host size or habit. Parasite community composition was not correlated with host phylogeny, indicating no strong effect of the evolutionary relationships among anurans on the similarities in their parasite communities. Host–parasite network showed a nested and non-modular pattern of interaction, which is probably a result of the low host specificity observed for most helminths in this study. Overall, we found host body size was important in determining parasite community richness, whereas low parasite specificity was important to network structure.

Keywords

networknestednessparasiteamphibianhelminth
Type
Research Article
Information
Parasitology , Volume 142 , Issue 14 , December 2015 , pp. 1751 - 1757
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Aho, J. M. (1990). Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and process. In Parasite Communities Patterns and Process (eds. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 157–190. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Almeida-Neto, M. and Ulrich, W. (2011). A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software 26, 173–178.CrossRefGoogle Scholar
Almeida-Neto, M., Guimarães, P., Guimarães, P. R. Jr, Loyola, R. D. and Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.CrossRefGoogle Scholar
Anderson, R. M. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission, 2nd Edn. CABI Publishing, Wallingford, Oxon, UK. 650 pp.CrossRefGoogle Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–6. http://CRAN.R-project.org/package=lme4.Google Scholar
Bellay, S., Lima, D. P., Takemoto, R. M. and Luque, J. L. (2011). A host–endoparasite network of neotropical marine fish: are there organizational patterns? Parasitology 138, 1945–52.CrossRefGoogle ScholarPubMed
Bellay, S., De Oliveira, E. F., Almeida-Neto, M., Lima Junior, D. P., Takemoto, R. M. and Luque, J. L. (2013). Developmental stage of parasites influences the structure of fish–parasite networks. PLoS ONE 8, e75710.CrossRefGoogle ScholarPubMed
Bellay, S., De Oliveira, E. F., Almeida-Neto, M., Mello, M. A. R., Takemoto, R. M. and Luque, J. L. (2015). Ectoparasites and endoparasites of fish form networks with different structures. Parasitology 142, 901–909.CrossRefGoogle ScholarPubMed
Brito, S. V., Corso, G., Almeida, A. M., Ferreira, F. S., Almeida, W. O., Anjos, L. A., Mesquita, D. O. and Vasconcellos, A. (2014). Phylogeny and micro-habitats utilized by lizards determine the composition of their endoparasites in the semiarid Caatinga of Northeast Brazil. Parasitology Research 113, 3963–3972.CrossRefGoogle ScholarPubMed
Brooks, D. R., León-Règagnon, V., Mclennan, D. A. and Zelmer, D. (2006). Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, 76–85.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Campião, K. M., Morais, D. H., Dias, O. T., Aguiar, A., Toledo, G., Tavares, L. E. R. and da Silva, R. J. (2014). Checklist of helminth parasites of amphibians from South America. Zootaxa 30, 1–93.CrossRefGoogle Scholar
Csardi, G. and Nepusz, T. (2006). The igraph software package for complex network research. International journal of complex systems 1695. http://igraph.sf.net.Google Scholar
Dormann, C. F., Gruber, B. and Fründ, J. (2008). Introducing the bipartite package: analysing ecological networks. R News 8, 8–11.Google Scholar
Fortuna, M. A., Stouffer, D. B., Olesen, J. M., Jordano, P., Mouillot, D., Krasnov, B. R., Poulin, R. and Bascompte, J. (2010). Nestedness vs modularity in ecological networks: two side of the same coin? Journal of Animal Ecology 79, 811–817.CrossRefGoogle Scholar
Goater, T. M. and Goater, C. P. (2001). Ecological monitoring and assessment network: protocols for measuring biodiversity: parasites of amphibians and reptiles Available at website http://www.emanrese.ca/eman/ecotools/protocols/terrestrial/herpparasites/intro.htm.Google Scholar
Graham, S. P., Hassan, H. K., Burkett-Cadena, N. D., Guyer, C. and Unnasch, T. R. (2009). Nestedness of ectoparasite-vertebrate host networks. PLoS ONE 4, 1–8.CrossRefGoogle ScholarPubMed
Guimarães, P. R. Jr. and Guimarães, P. (2006). Improving the analyses of nestedness for large sets of matrices. Environmental Modelling and Software 21, 1512–1513.CrossRefGoogle Scholar
Guimarães, P. R., Rico-Gray, V., Oliveira, P. S., Izzo, T. J., Dos Reis, S. F. and Thompson, J. N. (2007). Interaction intimacy affects structure and co-evolutionary dynamics in mutualistic networks. Current Biology 17, 1797–1803.CrossRefGoogle Scholar
Hamann, M. I., Kehr, A. I. and González, C. E. (2013). Biodiversity of trematodes associated with amphibians from a variety of habitats in corrientes province, argentina. Journal of Helminthology 87, 286–300.CrossRefGoogle ScholarPubMed
Joppa, L. N. and Williams, R. (2013). Modeling the building blocks of biodiversity. PLoS ONE 8, e56277.CrossRefGoogle ScholarPubMed
Joppa, L. N., Montoya, J. M., Solé, R., Sanderson, J. and Pimm, S. L. (2010). On nestedness in ecological networks. Evolutionary Ecology Research 12, 35–46.Google Scholar
Kamiya, T., O'Dwyer, K., Nakagawa, S. and Poulin, R. (2014). What determines species richness of parasitic organisms? a meta-analysis across animal, plant and fungal hosts. Biological Reviews 89, 123–134.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Fortuna, M. A., Mouillot, D., Khokhlova, I. S., Shenbrot, G. I. and Poulin, R. (2012). Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. American Naturalist 179, 501–511.CrossRefGoogle ScholarPubMed
Lima, D. P. Jr, Giacomini, H. C., Takemoto, R. M., Agostinho, A. A. and Bini, L. M. (2012). Patterns of interactions of a large fish–parasite network in a tropical floodplain. Journal of Animal Ecology 81, 905–913.CrossRefGoogle Scholar
Luque, J. L. and Poulin, R. (2008). Linking ecology with parasite diversity in neotropical fishes. Journal of Fish Biology 72, 189–204.CrossRefGoogle Scholar
Marquitti, F. M. D., Guimarães, P. R., Pires, M. M. and Bittencourt, L. F. (2014). MODULAR: software for the autonomous computation of modularity in large network sets. Ecography 37, 221–224.CrossRefGoogle Scholar
Mcquaid, C. F. and Britton, N. F. (2013). Coevolution of resource trade-offs driving species interactions in a host–parasite network: an exploratory model. Theoretical Ecology 6, 443–456.CrossRefGoogle Scholar
Neuwirth, E. (2011). RColorBrewer: ColorBrewer palettes. http://CRAN.R-project.org/package=RColorBrewer.Google Scholar
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. (2013). Vegan: community ecology package. R package version 2. 0–6. http://CRAN.R-project.org/package=vegan.Google Scholar
Olesen, J. M., Bascompte, J., Dupont, Y. L. and Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America 104, 19891–19896.CrossRefGoogle ScholarPubMed
Paradis, E. et al. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.CrossRefGoogle ScholarPubMed
Poulin, R. (1996). Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia 105, 545–551.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites from Individuals to Communities, 2nd Edn. Princeton University Press, NJ, USA.CrossRefGoogle Scholar
Poulin, R. (2010). Network analysis shining light on parasite ecology and diversity. Trends in Parasitology 26, 492–498.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2004). Parasite Biodiversity, Smithsonian Institution Books, Washington, D.C., USA.Google Scholar
Proulx, S. R., Promislow, D. E. L. and Phillip, P. C. (2005). Network thinking in ecology and evolution. Trends in Ecology and Evolution 20, 345–353.CrossRefGoogle ScholarPubMed
Pyron, A. and Wiens, J. (2011). A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61, 543–583.CrossRefGoogle Scholar
R Development Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/.Google Scholar
Sabagh, L. T., Ferreira, V. L. and Rocha, C. F. D. (2010). Living together, sometimes feeding in a similar way: the case of the syntopic hylid anurans Hypsiboas raniceps and Scinax acuminatus (Anura: Hylidae) in the Pantanal of Miranda, Mato Grosso do Sul State, Brazil. Brazilian Journal of Biology 70, 955–959.CrossRefGoogle Scholar
Ulrich, W., Almeida-Neto, M. and Gotelli, N. J. (2009). A consumer's guide to nestedness analysis. Oikos 118, 3–17.CrossRefGoogle Scholar
Vázquez, D. P., Poulin, R., Krasnov, B. R. and Shenbrot, G. I. (2005). Species abundance and the distribution of specialization in host – parasite interaction networks. Journal of Animal Ecology 74, 946–995.CrossRefGoogle Scholar
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