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A host-endoparasite network of Neotropical marine fish: are there organizational patterns?

Published online by Cambridge University Press:  19 August 2011

SYBELLE BELLAY ,
DILERMANDO P. LIMA Jr ,
RICARDO M. TAKEMOTO  and
JOSÉ L. LUQUE
SYBELLE BELLAY
Affiliation:
Programa de Pós-Graduação em Ecologia de Ecossistemas Aquáticos Continentais, Universidade Estadual de Maringá, Maringá, PR, Brazil
DILERMANDO P. LIMA Jr
Affiliation:
Programa de Pós-Graduação em Ecologia de Ecossistemas Aquáticos Continentais, Universidade Estadual de Maringá, Maringá, PR, Brazil
RICARDO M. TAKEMOTO
Affiliation:
Programa de Pós-Graduação em Ecologia de Ecossistemas Aquáticos Continentais, Universidade Estadual de Maringá, Maringá, PR, Brazil
JOSÉ L. LUQUE*
Affiliation:
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
*
*Corresponding author: Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Cx. Postal 74508, Seropédica, RJ, CEP 23851-970, Brazil. Tel./fax: +55 21 26821617. E-mail: [email protected]
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Summary

Properties of ecological networks facilitate the understanding of interaction patterns in host-parasite systems as well as the importance of each species in the interaction structure of a community. The present study evaluates the network structure, functional role of all species and patterns of parasite co-occurrence in a host-parasite network to determine the organization level of a host-parasite system consisting of 170 taxa of gastrointestinal metazoans of 39 marine fish species on the coast of Brazil. The network proved to be nested and modular, with a low degree of connectance. Host-parasite interactions were influenced by host phylogeny. Randomness in parasite co-occurrence was observed in most modules and component communities, although species segregation patterns were also observed. The low degree of connectance in the network may be the cause of properties such as nestedness and modularity, which indicate the presence of a high number of peripheral species. Segregation patterns among parasite species in modules underscore the role of host specificity. Knowledge of ecological networks allows detection of keystone species for the maintenance of biodiversity and the conduction of further studies on the stability of networks in relation to frequent environmental changes.

Keywords

networkendoparasitesnestednessmodularityco-occurrencenull models
Type
Research Article
Information
Parasitology , Volume 138 , Issue 14 , December 2011 , pp. 1945 - 1952
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Almeida-Neto, M., Guimarães, P. R. Jr and Lewinsohn, T. M. (2007). On nestedness analyses: rethinking matrix temperature and anti-nestedness. Oikos 116, 716–722. doi: 10.1111/j.0030-1299.2007.15803.x.Google 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. doi: 10.1111/j.0030-1299.2008.16644.x.Google Scholar
Bascompte, J., Jordano, P. and Olesen, J. M. (2006). Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431–433. doi: 10.1126/science.1123412.CrossRefGoogle ScholarPubMed
Bascompte, J., Jordano, P., Melian, C. J. and Olesen, J. M. (2003). The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences, USA 100, 9383–9387. doi: 10.1073/pnas.1633576100.CrossRefGoogle ScholarPubMed
Bastolla, U., Fortuna, M. A., Pascual-García, A., Ferrera, A., Luque, B. and Bascompte, J. (2009). The architecture of mutualistic networks minimizes competiton and increase biodiversity. Nature, London 458, 1018–1021. doi: 10.1038/nature07950.CrossRefGoogle Scholar
Borrett, S. R. and Salas, A. K. (2010). Evidence for resource homogenization in 50 trophic ecosystem networks. Ecological Modelling 221, 1710–1716.CrossRefGoogle Scholar
Braicovich, P. E. and Timi, J. T. (2008). Parasites as biological tags for stock discrimination of the Brazilian flathead in the South West Atlantic. Journal of Fish Biology 73, 557–571. doi:10.1111/j.1095-8649.2008.01948.x.CrossRefGoogle Scholar
Bush, A. O., Fernández, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
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 ScholarPubMed
Chambers, C. B., Cribb, T. H. and Malcolm, J. K. (2000). Tetraphyllidean metacestodes of teleosts of the Great Barrier Reef, and the use of in vitro cultivation to identify them. Folia Parasitologica 47, 285–292.Google Scholar
Chandler, A. C. (1935). Parasites of fishes in Galveston Bay. Proceedings of the United States National Museum 83, 123–157.CrossRefGoogle Scholar
Chávez, R. A., González, M. T., Oliva, M. E. and Valdivia, I. M. (2011). Endoparasite fauna of five Gadiformes fish species from the coast of Chile: host ecology versus phylogeny. Journal of Helminthology (available on CJO 2011). doi: 10.1017/S0022149X10000921.Google ScholarPubMed
Cribb, T. H., Bray, R. A., Wright, T. and Pichelin, S. (2002). The trematodes of groupers (Serranidae: Epinephelinae): knowledge, nature and evolution. Parasitology 124, S23–S42. doi. 10.1017/S0031182002001671.CrossRefGoogle ScholarPubMed
Fellis, K. J., Negovetich, N. J., Esch, G. W., Horak, I. G. and Boomker, J. (2003). Patterns of association, nestedness, and species co-occurrence of helminth parasites in the greater kudu, Tragelaphus strepsiceros, in the Kruger National Park, South Africa, and the Etosha National Park, Namibia. Journal of Parasitology 89, 899–907. doi: 10.1645/GE-3189.CrossRefGoogle ScholarPubMed
Figueiredo, J. L. and Menezes, N. A. (1978). Manual de Peixes Marinhos do Sudeste de Brasil II. Teleostei (1). Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Figueiredo, J. L. and Menezes, N. A. (1980). Manual de Peixes Marinhos do Sudeste de Brasil III. Teleostei (2). Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Figueiredo, J. L. and Menezes, N. A. (2000). Manual de Peixes Marinhos do Sudeste de Brasil VI. Teleostei (5). Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Fortuna, M. A., Popa-Lisseanu, A. G., Ibanez, C. and Bascompte, J. (2009). The roosting spatial network of a bird-predator bat. Ecology 90, 934–944. doi: 10.1890/08-0174.1.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. doi: 10.1111/j.1365-2656.2010.01688.x.CrossRefGoogle ScholarPubMed
Froese, R. and Pauly, D. (2010). FishBase. World Wide Web electronic publication. www.fishbase.org, version (05/2010).Google Scholar
Gotelli, N. J. (2000). Null model analysis of species co-occurrence patterns. Ecology 81, 2606–2621. doi: 10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2.CrossRefGoogle Scholar
Gotelli, N. J. and Entsminger, G. L. (2001). EcoSim: Null Models Software for Ecology. Version 7.0. Acquired Intelligence Inc.: Kesey-Bear. http://homepages.together.net/~gentsmin/ecosim.htm.Google Scholar
Gotelli, N. J. and Rohde, K. (2002). Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 86–94. doi: 10.1046/j.1461-0248.2002.00288.x.CrossRefGoogle Scholar
Guimerà, R. and Amaral, L. A. N. (2005 a). Cartography of complex networks: modules and universal roles. Journal of Statistical Mechanics: Theory and Experiment P02001, 1–13. doi: 10.1088/1742-5468/2005/02/P02001.Google Scholar
Guimerà, R. and Amaral, L. A. N. (2005 b). Functional cartography of complex metabolic networks. Nature, London 433, 895–900.doi: 10.1038/nature03288.CrossRefGoogle ScholarPubMed
Holmes, J. C. and Price, P. W. (1986). Communities of parasites. In Community Ecology: Pattern and Process (ed. Kikkawa, J. and Anderson, D.J.), pp. 187–213. Blackwell Scientific Publication, Oxford, UK.Google Scholar
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385. doi: 10.1016/j.tree.2006.04.007.CrossRefGoogle Scholar
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
Krasnov, B. R., Matthee, S., Lareschi, M., Korallo-Vinarskaya, N. P. and Vinarski, M. V. (2010). Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents. Oikos 119, 120–128. doi: 10.1111/j.1600-0706.2009.17902.x.Google Scholar
Legendre, P. and Legendre, L. (1998). Numerical Ecology 2nd Edn. Elsevier Science, Amsterdam, The Netherlands.Google Scholar
Lewinsohn, T. M., Loyola, R. D. and Prado, P. I. (2006 a). Matrizes, redes e ordenações: a detecção de estrutura em comunidades interativas. Oecologia brasiliensis 10, 90–104.CrossRefGoogle Scholar
Lewinsohn, T. M., Prado, P. I., Jordano, P., Bascompte, J. and Olesen, J. M. (2006 b) Structure in plant-animal interaction assemblages. Oikos 113, 174–184. doi: 10.1111/j.0030-1299.2006.14583.x.CrossRefGoogle Scholar
Luque, J. L. and Poulin, R. (2004). Use of fish as intermediate hosts by helminth parasites: A comparative analysis. Acta Parasitologica 49, 353–361.Google Scholar
Manly, B. F. J. (2004). Multivariate Statistical Methods: a Primer, 3rd Edn. Chapman & Hall/CRC, Boca Raton, Fl, USA.CrossRefGoogle Scholar
Marchiori, N., da, C., Magalhães, A. R. M. and Pereira, J. Jr (2010). The life cycle of Bucephalus margaritae Ozaki & Ishibashi, 1934 (Digenea, Bucephalidae) from the coast of Santa Catarina State, Brazil. Acta Scientiarum. Biological Sciences 32, 71–78. doi. 10.4025/actascibiolsci.v32i1.5596.CrossRefGoogle Scholar
Menezes, N. A. and Figueiredo, J. L. (1980). Manual de Peixes Marinhos do Sudeste de Brasil IV. Teleostei (3). Museu de Zoologia, Universidadede São Paulo, São Paulo, Brazil.Google Scholar
Menezes, N. A. and Figueiredo, J. L. (1985). Manual de Peixes Marinhos do Sudeste de Brasil V. Teleostei (4). Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Morand, S., Poulin, R., Rohde, K. and Hayward, C. (1999). Aggregation and species coexistence of ectoparasites of marine fishes. International Journal for Parasitology 29, 663–672. doi: 10.1016/S0020-7519(99)00029-6.CrossRefGoogle ScholarPubMed
Mouillot, D., George-Nascimento, M. and Poulin, R. (2005). Richness, structure and functioning in metazoan parasite communities. Oikos 109, 447–460. doi: 10.1111/j.0030-1299.2005.13590.x.CrossRefGoogle Scholar
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. (2010). Vegan: Community Ecology Package. http://cran.r-project.org/web/packages/vegan/index.html.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, USA 104, 19891–19896. doi. 10.1073/pnas.0706375104.CrossRefGoogle ScholarPubMed
Pimm, S. L. and Lawton, J. H. (1980). Are food webs divided into compartments? Journal of Animal Ecology 49, 879–898.Google Scholar
Poulin, R. (2005). Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology 130, 109–115. doi:10.1017/S0031182004006304.CrossRefGoogle ScholarPubMed
Poulin, R. (2010). Network analysis shining light on parasite ecology and diversity. Trends in Parasitology 26, 492–498. doi: 10.1016/j.pt.2010.05.008.CrossRefGoogle ScholarPubMed
Poulin, R. and Luque, J. L. (2003). A general test of the interactive-isolationist continuum in gastrointestinal parasite communities of fish. International Journal for Parasitology 33, 1623–1630. doi:10.1016/j.ijpara.2003.09.005.CrossRefGoogle ScholarPubMed
Rezende, E. L., Albert, E. M., Fortuna, M. A. and Bascompte, J. (2009). Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecology Letters 12, 779–788. doi: 10.1111/j.1461-0248.2009.01327.x.Google Scholar
Rohde, K. (1998). Is there a fixed number of niches for endoparasites of fish? International Journal for Parasitology 28, 1861–1865. doi: 10.1016/S0020-7519(98)00142-8.CrossRefGoogle Scholar
Rohde, K., Hayward, C. and Heap, M. (1995). Aspects of the ecology of metazoan ectoparasites of marine fishes. International Journal for Parasitology 25, 945–970. doi: 10.1016/0020-7519(95)00015-T.Google Scholar
Rossin, M. A., Poulin, R., Timi, J. T. and Malizia, A. I. (2005). Causes of inter-individual variation in reproductive strategies of the parasitic nematode Graphidioides subterraneus. Parasitology Research 96, 335–339. doi. 10.1007/s00436-005-1400-0.CrossRefGoogle ScholarPubMed
Scheffer, M., Carpenter, S. and Young, B. de (2005). Cascading effects of overfishing marine systems. Trends in Ecology and Evolution 20, 579–581. doi:10.1016/j.tree.2005.08.018.CrossRefGoogle ScholarPubMed
Solé, R. V. and Montoya, J. M. (2001). Complexity and fragility in ecological networks. Proceedings of the Royal Society of London, B 268, 2039–2045. doi: 10.1098/rspb.2001.1767.CrossRefGoogle ScholarPubMed
Stone, L. and Roberts, A. (1990). The checkerboard score and species distributions. Oecologia, 85, 74–79. doi: 10.1007/BF00317345.CrossRefGoogle ScholarPubMed
Stouffer, D. B. and Bascompte, J. (2011). Compartmentalization increases food-web persistence. Proceedings of the National Academy of Sciences, USA 108, 3648–3652. doi. 10.1073/pnas.1014353108.CrossRefGoogle ScholarPubMed
Tello, J. S., Stevens, R. D. and Dick, C. W. (2008). Patterns of species co-occurrence and density compensation: a test for interspecific competition in bat ectoparasite infracommunities. Oikos 117, 693–702. doi: 10.1111/j.0030-1299.2008.16212.x.CrossRefGoogle Scholar
Thébault, E. and Fontaine, C. (2010). Stability of ecological communities and thearchitecture of mutualistic and trophic networks. Science 329, 853–856. doi: 10.1126/science.1188321.CrossRefGoogle Scholar
Thompson, J. N. (1994). The Coevolutionary Process. University of Chicago Press, Chicago, Ill, USA.CrossRefGoogle Scholar
Thompson, J. N. (2005). The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago, Ill, USA.CrossRefGoogle Scholar
Thompson, J. N. (2006). Mutualistic webs of species. Science 312, 372–373. doi: 10.1126/science.1126904.CrossRefGoogle ScholarPubMed
Torres, P. and Soto, M. S. (2004). Hysterothylacium winteri sp. n. (Nematoda: Anisakidae), a parasite of Chilean rock cod, Eleginops maclovinus (Perciformes: Eleginopidae), from South Chile. Folia Parasitologica 51, 55–60.CrossRefGoogle Scholar
Ulrich, W., Almeida-Neto, M. and Gotelli, N. J. (2009). A consumer's guide to nestedness analysis. Oikos 118, 3–17. doi: 10.1111/j.1600-0706.2008.17053.x.CrossRefGoogle Scholar
Ulrich, W. and Gotelli, N. J. (2007). Disentangling community patterns of nestedness and species co-occurrence. Oikos 116, 2053–2061. doi: 10.1111/j.2007.0030-1299.16173.x.CrossRefGoogle Scholar
Vázquez, D. P., Melián, C. J., Williams, N. M., Blüthgen, N., Krasnov, B. R. and Poulin, R. (2007). Species abundance and asymmetric interaction strength in ecological networks. Oikos 116, 1120–1127. doi: 10.1111/j.2007.0030-1299.15828.x.Google 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, 946–955. doi: 10.1111/j.1365-2656.2005.00992.x.CrossRefGoogle Scholar
Wood, C. L., Lafferty, K. D. and Micheli, F. (2010). Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecology Letters 13, 761–775. doi: 10.1111/j.1461-0248.2010.01467.x.CrossRefGoogle ScholarPubMed
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Matrix of Host-Parasite Interaction

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