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Ectoparasites and endoparasites of fish form networks with different structures

Published online by Cambridge University Press:  16 March 2015

S. BELLAY ,
E. F. DE OLIVEIRA ,
M. ALMEIDA-NETO ,
M. A. R. MELLO ,
R. M. TAKEMOTO  and
J. L. LUQUE
S. BELLAY*
Affiliation:
Departamento de Ciências Biológicas, Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá, Av. Colombo, Bloco G90, Sala 13, 87020-900, Maringá, Paraná, Brazil
E. F. DE OLIVEIRA
Affiliation:
Departamento de Engenharia Ambiental, Programa de Pós-Graduação em Engenharia Ambiental, Universidade Tecnológica Federal do Paraná, Campus Londrina, Londrina, Brazil
M. ALMEIDA-NETO
Affiliation:
Departamento de Ecologia, Programa de Pós-Graduação em Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Brazil
M. A. R. MELLO
Affiliation:
Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
R. M. TAKEMOTO
Affiliation:
Departamento de Ciências Biológicas, Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá, Av. Colombo, Bloco G90, Sala 13, 87020-900, Maringá, Paraná, Brazil
J. L. LUQUE
Affiliation:
Departamento de Parasitologia Animal, Programa de Pós-Graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro, Seropédica, Brazil
*
*Corresponding author. Departamento de Ciências Biológicas, Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá, Av. Colombo, 5790, Bloco G90, Sala 13, 87020-900, Maringá, Paraná, Brazil. E-mail: sybellebellay@yahoo.com.br
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Summary

Hosts and parasites interact with each other in a variety of ways, and this diversity of interactions is reflected in the networks they form. To test for differences in interaction patterns of ecto- and endoparasites we analysed subnetworks formed by each kind of parasites and their host fish species in fish–parasite networks for 22 localities. We assessed the proportion of parasite species per host species, the relationship between parasite fauna composition and host taxonomy, connectance, nestedness and modularity of each subnetwork (n = 44). Furthermore, we evaluated the similarity in host species composition among modules in ecto- and endoparasite subnetworks. We found several differences between subnetworks of fish ecto- and endoparasites. The association with a higher number of host species observed among endoparasites resulted in higher connectance and nestedness, and lower values of modularity in their subnetworks than in those of ectoparasites. Taxonomically related host species tended to share ecto- or endoparasites with the same interaction intensity, but the species composition of hosts tended to differ between modules formed by ecto- and endoparasites. Our results suggest that different evolutionary and ecological processes are responsible for organizing the networks formed by ecto- and endoparasites and fish.

Keywords

host–parasite metazoan networksantagonistic networksconnectancenestednessmodularity
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 901 - 909
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Almeida-Neto, M. and Ulrich, W. (2011). A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software 26, 173–178.Google Scholar
Almeida-Neto, M., Guimarães, P., Guimarães, P. R., Loyola, R. D. and Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.Google Scholar
Arai, H. P. and Mudry, D. R. (1983). Protozoan and metazoan parasites of fishes from the headwaters of the Parsnip and McGregor Rivers, British Columbia: a study of possible parasite transfaunations. Canadian Journal of Fisheries and Aquatic Sciences 40, 1676–1684.Google Scholar
Arthur, J. R. and Te, B. Q. (2006). Checklist of the Parasites of Fishes of Viet Nam. FAO Fisheries Technical paper 369/2. Food and Agriculture Organization of the United Nations, Rome, Italy. Available from: http://www.fao.org/docrep/009/a0878e/a0878e00.htm Google Scholar
Arthur, J. R., Margolis, L. and Arai, H. P. (1976). Parasites of fishes of Aishihik and Stevens Lakes, Yukon Territory, and potential consequences of their interlake transfer through a proposed water diversion for hydroelectrical purposes. Journal of the Fisheries Research Board of Canada 33, 2489–2499.Google Scholar
de Azevedo, R. K., Abdallah, V. D. and Luque, J. L. (2010). Acanthocephala, Annelida, Arthropoda, Myxozoa, Nematoda and Platyhelminthes parasites of fishes from the Guandu river, Rio de Janeiro, Brazil. Check List 6, 659–667.Google Scholar
Bellay, S., Lima, D. P. Jr., Takemoto, R. M. and Luque, J. L. (2011). A host–endoparasite network of Neotropical marine fish: are there organizational patterns? Parasitology 138, 1945–1952.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.Google Scholar
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.Google Scholar
Bush, A. O., Fernández, J. C., Esch, G. W. and Seed, J. R. (eds.) (2001). Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge.Google Scholar
Chemes, S. B. and Takemoto, R. M. (2011). Diversity of parasites from Middle Paraná system freshwater fishes, Argentina. International Journal of Biodiversity and Conservation 3, 249–266.Google Scholar
Chinniah, V. C. and Threlfall, W. (1978). Metazoan parasites of fish from the Smallwood Reservoir, Labrador, Canada. Journal of Fish Biology 13, 203–213.Google Scholar
Choudhury, A., Hoffnagle, T. L. and Cole, R. A. (2004). Parasites of native and nonnative fishes of the Little Colorado River, Grand Canyon, Arizona. Journal of Parasitology 90, 1042–1053.Google Scholar
Dechtiar, A. O. (1972). Parasites of fish from Lake of the Woods, Ontario. Journal of Fisheries Research Board of Canada 29, 275–283.Google Scholar
Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America 105(Suppl), 11482–11489.Google Scholar
Fonseca, C. R. and John, J. L. (1996). Connectance: a role for community allometry. Oikos 77, 353–358.Google Scholar
Fontaine, C., Guimarães, P. R., Kéfi, S., Loeuille, N., Memmott, J., van der Putten, W. H., van Veen, F. J. F. and Thébault, E. (2011). The ecological and evolutionary implications of merging different types of networks. Ecology Letters 14, 1170–81.CrossRefGoogle ScholarPubMed
Fortuna, M. A., Stouffer, D. B., Olesen, J. M., Jordano, P., Mouillot, D., Krasnov, B. R., Poulin, R. and Bascompte, J. (2010). Nestedness versus modularity in ecological networks: two sides of the same coin? Journal of Animal Ecology 79, 811–817.CrossRefGoogle ScholarPubMed
Froese, R. and Pauly, D. (2013). FishBase. World Wide Web electronic publication. http://www.fishbase.org Google Scholar
Garrido-Olvera, L., Arita, H. T. and Pérez-Ponce De León, G. (2012). The influence of host ecology and biogeography on the helminth species richness of freshwater fishes in Mexico. Parasitology 139, 1652–1665.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, e7873.Google Scholar
Guimarães, P. R. Jr. and Guimarães, P. R. (2006). Improving the analyses of nestedness for large sets of matrices. Environmental Modelling and Software 21, 1512–1513.Google 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 coevolutionary dynamics in mutualistic networks. Current Biology: CB 17, 1797–1803.Google Scholar
Guimerà, R. and Amaral, L. A. N. (2005). Functional cartography of complex metabolic networks. Nature 433, 895–900.Google Scholar
Kirjušina, M. and Vismanis, K. (2007). Checklist of the Parasites of Fishes of Latvia. FAO Fisheries Technical paper 369/3. Food and Agriculture Organization of the United Nations, Rome, Italy. Available from: http://www.fao.org/docrep/010/a1078e/a1078e00.htm Google Scholar
Koehler, A. V., Brown, B., Poulin, R., Thieltges, D. W., Fredensborg, B. L. (2012). Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evolutionary Ecology 26, 1497–1512.Google Scholar
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. The American Naturalist 179, 501–511.Google Scholar
Leong, T. S. and Holmes, J. C. (1981). Communities of metazoan parasites in open water fishes of Cold Lake, Alberta. Journal of Fish Biology 18, 693–713.Google Scholar
Lewinsohn, T. M. and Prado, P. I. (2006). Structure in plant–animal interaction assemblages. Oikos 113, 174–184.Google Scholar
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.Google Scholar
Mello, M. A. R., Marquitti, F. M. D., Guimarães, P. R. Jr., Kalko, E. K. V., Jordano, P. and de Aguiar, M. A. M. (2011). The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS ONE 6, e17395.Google Scholar
Muzzall, P. M. and Whelan, G. (2011). Parasites of Fish from the Great Lakes: A Synopsis and Review of the Literature, 1871–2010. Great Lakes Fishery Commission Miscellaneous Publication 2011–01. Ann Arbor, MI. Available from: http://www.glfc.org/pubs/SpecialPubs/2011-01.pdf.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. (2014). Vegan: Community Ecology Package. http://cran.r-project.org/web/packages/vegan/index.html Google Scholar
Paradis, E., Claude, J. and Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.Google Scholar
Pimm, S. L. (1982). Food Webs. Chapman & Hall, London.Google Scholar
Poisot, T., Stanko, M., Miklisová, D. and Morand, S. (2013). Facultative and obligate parasite communities exhibit different network properties. Parasitology 140, 1340–1345.Google Scholar
Poulin, R. (1998). Evolutionary Ecology of Parasites. First. Chapman & Hall, London.Google Scholar
Poulin, R. and Leung, T. L. F. (2011). Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166, 731–738.Google Scholar
Poulin, R., Krasnov, B. R., Pilosof, S. and Thieltges, D. W. (2013). Phylogeny determines the role of helminth parasites in intertidal food webs. The Journal of Animal Ecology 82, 1265–1275.Google Scholar
R Development Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/ Google Scholar
Rezende, E. L., Lavabre, J. E., Guimarães, P. R., Jordano, P. and Bascompte, J. (2007). Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448, 925–928.Google Scholar
Statsoft, Inc. (2005). Statistica (data analysis software system), version 7.1. http://www.statsoft.com Google Scholar
Strona, G., Galli, P. and Fattorini, S. (2013). Fish parasites resolve the paradox of missing coextinctions. Nature Communications 4, 1718.Google Scholar
Suweis, S., Simini, F., Banavar, J. R. and Maritan, A. (2013). Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500, 449–452.Google Scholar
Takemoto, R. M., Pavanelli, G. C., Lizama, M. A. P., Luque, J. L. and Poulin, R. (2005). Host population density as the major determinant of endoparasite species richness in floodplain fishes of the upper Paraná River, Brazil. Journal of Helminthology 79, 75–84.Google Scholar
Takemoto, R. M., Pavanelli, G. C., Lizama, M. A. P., Lacerda, A. C. F., Yamada, F. H., Moreira, L. H. A., Ceschini, T. L. and Bellay, S. (2009). Diversity of parasites of fish from the upper Paraná River floodplain, Brazil. Brazilian Journal Biology 69, 691–705.Google Scholar
Thébault, E. and Fontaine, C. (2008). Does asymmetric specialization differ between mutualistic and trophic networks? Oikos 117, 555–563.Google Scholar
Thompson, J. N. (1994). The Coevolutionary Process. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Timi, J. T., Rossin, M. A., Alarcos, A. J., Braicovich, P. E., Cantatore, D. M. P. and Lanfranchi, A. L. (2011). Fish trophic level and the similarity of non-specific larval parasite assemblages. International Journal for Parasitology 41, 309–316.CrossRefGoogle ScholarPubMed
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, 946–955.Google Scholar
Violante-González, J. and Aguirre-Macedo, M. L. (2007). Metazoan parasites of fishes from Coyuca Lagoon, Guerrero, Mexico. Zootaxa 1531, 39–48.Google Scholar
Violante-González, J., Aguirre-Macedo, M. L. and Mendoza-Franco, E. F. (2007). A checklist of metazoan parasites of fish from Tres Palos Lagoon, Guerrero, Mexico. Parasitology Research 102, 151–161.Google Scholar
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