Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-26T01:33:01.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of host diet and phylogeny on parasite sharing by fish in a diverse tropical floodplain

Published online by Cambridge University Press:  09 December 2015

L. B. LIMA ,
S. BELLAY ,
H. C. GIACOMINI ,
A. ISAAC  and
D. P. LIMA-JUNIOR
L. B. LIMA*
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso, Campus de Nova Xavantina, BR 158, Km 148 – CEP: 78690-000 – Caixa Postal 08 – Nova Xavantina – MT, Brasil Laboratório de Ecologia e Conservação de Ecossistemas Aquáticos, Universidade Federal de Mato Grosso, Rodovia MT 100, Km 3,5 Setor Universitário CEP: 78698 – 000 – Pontal do Araguaia, MT, Brasil
S. BELLAY
Affiliation:
Universidade Estadual de Maringá, Centro de Ciências Biológicas, Avenida Colombo, 5790 bloco G90 sala 011, Zona 7, CEP: 87020-900 – Maringá, PR, Brasil
H. C. GIACOMINI
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Office RW 520B, 25 Harbord St., Toronto, ON, M5S 3G5l, Canada
A. ISAAC
Affiliation:
Universidade Federal do Paraná, Setor Palotina. Rua Pioneiro, 2153, Jardim Dallas, CEP: 85950-000, Palotina, PR-Brasil
D. P. LIMA-JUNIOR
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso, Campus de Nova Xavantina, BR 158, Km 148 – CEP: 78690-000 – Caixa Postal 08 – Nova Xavantina – MT, Brasil Laboratório de Ecologia e Conservação de Ecossistemas Aquáticos, Universidade Federal de Mato Grosso, Rodovia MT 100, Km 3,5 Setor Universitário CEP: 78698 – 000 – Pontal do Araguaia, MT, Brasil
*
*Corresponding author: Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso, Campus de Nova Xavantina, BR 158, Km 148 – CEP: 78690-000 – Caixa Postal 08 – Nova Xavantina – MT, Brasil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The patterns of parasite sharing among hosts have important implications for ecosystem structure and functioning, and are influenced by several ecological and evolutionary factors associated with both hosts and parasites. Here we evaluated the influence of fish diet and phylogenetic relatedness on the pattern of infection by parasites with contrasting life history strategies in a freshwater ecosystem of key ecological importance in South America. The studied network of interactions included 52 fish species, which consumed 58 food types and were infected with 303 parasite taxa. Our results show that both diet and evolutionary history of hosts significantly explained parasite sharing; phylogenetically close fish species and/or species sharing food types tend to share more parasites. However, the effect of diet was observed only for endoparasites in contrast to ectoparasites. These results are consistent with the different life history strategies and selective pressures imposed on these groups: endoparasites are in general acquired via ingestion by their intermediate hosts, whereas ectoparasites actively seek and attach to the gills, body surface or nostrils of its sole host, thus not depending directly on its feeding habits.

Keywords

Ecological networksphylogenetic signalhost–parasite interactions
Type
Research Article
Information
Parasitology , Volume 143 , Issue 3 , March 2016 , pp. 343 - 349
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abelha, M. C., Agostinho, A. A. and Goulart, E. (2001). Plasticidade trófica em peixes de água doce. Acta Scientiarum 23, 425–434.Google Scholar
Agosta, S. J., Janz, N. and Brooks, D. R. (2010). How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia 27, 151–162.Google Scholar
Agostinho, A. A., Gomes, L. C. and Pelicice, F. M. (2007 a). Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. EDUEM, Maringá.Google Scholar
Agostinho, A. A., Pelicice, F. M., Petry, A. C., Gomes, L. C. and Júlio, H. F. (2007 b). Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquatic Ecosystem Health and Management 10, 174–186.Google Scholar
Agostinho, A. A., Pelicice, F. M. and Gomes, L. C. (2008). Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazil Journal Biology 68, 1119–1132.Google Scholar
Beaulieu, J. M., Ree, R. H., Cavender-Bares, J., Weiblen, G. D. and Donoghue, M. J. (2012). Synthesizing phylogenetic knowledge for ecological research. Ecology 93, S4–S13.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, 1945–1952.Google Scholar
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
Bellay, S., de Oliveira, E. F., Almeida-Neto, M., Mello, M. A. R., Takemoto, R. M. and Luque, J. L. (2015 a). Ectoparasites and endoparasites of fish form networks with different structures. Parasitology 142, 901–909.Google Scholar
Bellay, S., de Oliveira, E. F., Almeida-Neto, M., Abdallah, V. D., de Azevedo, R. K., Takemoto, R. M. and Luque, J. L. (2015 b). The patterns of organisation and structure of interactions in a fish-parasite network of a Neotropical river. International Journal for Parasitology 45, 549–557.Google Scholar
Benesh, D. P., Chubb, J. C. and Parker, G. a. (2014). The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths. Proceedings of the Royal Society B: Biological Sciences 281, 20141462.Google Scholar
Bersier, L.-F. and Kehrli, P. (2008). The signature of phylogenetic constraints on food-web structure. Ecological Complexity 5, 132–139.CrossRefGoogle Scholar
Braga, M. P., Razzolini, E. and Boeger, W. a. (2015). Drivers of parasite sharing among Neotropical freshwater fishes. Journal of Animal Ecology 84, 487–497.CrossRefGoogle ScholarPubMed
Brown, S. P., Renaud, F., Guégan, J. F. and Thomas, F. (2001). Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.Google Scholar
Cattin, M.-F., Bersier, L.-F., Banašek-Richter, C., Baltensperger, R. and Gabriel, J.-P. (2004). Phylogenetic constraints and adaptation explain food-web structure. Nature 427, 835–839.Google Scholar
Chen, H.-W., Liu, W.-C., Davis, A. J., Jordán, F., Hwang, M.-J. and Shao, K.-T. (2008). Network position of hosts in food webs and their parasite diversity. Oikos 117, 1847–1855.Google Scholar
Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: why add intermediate hosts? American Naturalist 162, 172–181.Google Scholar
Dallas, T. and Presley, S. J. (2014). Relative importance of host environment, transmission potential and host phylogeny to the structure of parasite metacommunities. Oikos 123, 866–874.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. 1), 11482–11489.CrossRefGoogle ScholarPubMed
Foitzik, S., Fischer, B. and Heinze, J. (2003). Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance. Behavioral Ecology 14, 80–88.CrossRefGoogle Scholar
Gido, K. B. and Franssen, N. R. (2007). Invasion of stream fishes into low trophic positions. Ecology of Freshwater Fish 16, 457–464.Google Scholar
Graça, W. J. and Pavanelli, C. S. (2007). Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. EDUEM, Maringá.Google Scholar
Harms, C. and Turingan, R. (2012). Dietary flexibility despite behavioral stereotypy contributes to successful invasion of the pike killifish, Belonesox belizanus, in Florida, USA. Aquatic Invasions 7, 547–553.Google Scholar
Hayden, B., Massa-gallucci, A., Harrod, C., O'grady, M., Caffrey, J. and Kelly-quinn, M. (2014). Trophic flexibility by roach Rutilus rutilus in novel habitats facilitates rapid growth and invasion success. Journal of Fish Biology 84, 1099–1116.CrossRefGoogle ScholarPubMed
Hoeinghaus, D. J., Agostinho, A. A., Gomes, L. C., Pelicice, F. M., Okada, E. K., Latini, J. D., Kashiwaqui, E. A. L. and Winemiller, K. O. (2009). Effects of river impoundment on ecosystem services of large tropical rivers: embodied energy and market value of artisanal fisheries. Conservation Biology 23, 1222–1231.CrossRefGoogle ScholarPubMed
Isaac, A., Fernandes, A., Ganassin, M. J. M. and Hahn, N. S. (2014). Three invasive species occurring in the diets of fishes in a Neotropical floodplain. Brazilian Journal of Biology 74, S016–S022.Google Scholar
Joannes, A., Lagrue, C., Poulin, R. and Beltran-Bech, S. (2014). Effects of genetic similarity on the life-history strategy of co-infecting trematodes: are parasites capable of intrahost kin recognition? Journal of Evolutionary Biology 27, 1623–1630.CrossRefGoogle ScholarPubMed
Júlio-Júnior, H. F., Tós, C. D., Agostinho, Â. A. and Pavanelli, C. S. (2009). A massive invasion of fish species after eliminating a natural barrier in the upper Rio Paraná basin. Neotropical Ichthyology 7, 709–718.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.Google Scholar
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2009 a). Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology 54, 1805–1818.Google Scholar
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2009 b). Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 2047–2056.Google Scholar
Krasnov, B. R., Mouillot, D., Khokhlova, I. S., Shenbrot, G. I. and Poulin, R. (2012). Compositional and phylogenetic dissimilarity of host communities drives dissimilarity of ectoparasite assemblages: geographical variation and scale-dependence. Parasitology 139, 338–347.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Pilosof, S., Stanko, M., Morand, S., Korallo-Vinarskaya, N. P., Vinarski, M. V. and Poulin, R. (2014). Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering. Oikos 123, 63–70.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2009). Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 1659–1663.Google Scholar
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103, 11211–11216.Google Scholar
Legendre, P. and Legendre, L. (2012). Numerical Ecology, 3rd Edn. Elsevier, Oxford, UK.Google Scholar
Lima-Junior, D. P., 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
Locke, S. A., McLaughlin, J. D. and Marcogliese, D. J. (2013). Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122, 73–83.Google Scholar
Locke, S. A., Marcogliese, D. J. and Valtonen, E. T. (2014). Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia 174, 253–262.Google Scholar
Maddison, W. P. and Maddison, D. R. (2015). Mesquite: a Modular System for Evolutionary Analysis. Version 3.04. http://mesquiteproject.org Google Scholar
Magurran, A. E. (2004). Mesuring Biological Diversity. Blackwell Publishing, Carlton, Victória, Australia.Google Scholar
Mouillot, D., Krasnov, B. R., Shenbrot, G. I., Gaston, K. J. and Poulin, R. (2006). Conservatism of host specificity in parasites. Ecography 29, 596–602.Google Scholar
Naisbit, R. E., Rohr, R. P., Rossberg, a. G., Kehrli, P. and Bersier, L.-F. (2012). Phylogeny versus body size as determinants of food web structure. Proceedings of the Royal Society B: Biological Sciences 279, 3291–3297.Google Scholar
Oksanen, J., Blanchet, F. G., Kindt, R., Pierre, L., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. (2013). Vegan: Community Ecology Package. https://cran.r-project.org/web/packages/vegan/index.html Google Scholar
Pariselle, A., Boeger, W. A., Snoeks, J., Bilong Bilong, C. F., Morand, S. and Vanhove, M. P. M. (2011). The monogenean parasite fauna of cichlids: a potential tool for host biogeography. International Journal of Evolutionary Biology 2011, 1–15.Google Scholar
Pendleton, R. M., Hoeinghaus, D. J., Gomes, L. C. and Agostinho, A. A. (2014). Loss of rare fish species from tropical floodplain food webs affects community structure and ecosystem multifunctionality in a mesocosm experiment. PLoS ONE 9, e84568.Google Scholar
Poisot, T., Bever, J. D., Nemri, A., Thrall, P. H. and Hochberg, M. E. (2011). A conceptual framework for the evolution of ecological specialisation. Ecology Letters 14, 841–851.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. (1992). Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753–758.Google Scholar
Poulin, R. (1997). Species richness of parasite assemblages: evolution and Patterns. Annual Review of Ecology and Systematics 28, 341–358.Google Scholar
Poulin, R. (2010). Decay of similarity with host phylogenetic distance in parasite faunas. Parasitology 137, 733–741.Google Scholar
Poulin, R. and Forbes, M. R. (2011). Meta-analysis and research on host–parasite interactions: past and future. Evolutionary Ecology 26, 1169–1185.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., Mouillot, D. and Thieltges, D. W. (2011). The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society B: Biological Sciences 366, 2379–2390.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. Journal of Animal Ecology 82, 1265–1275.CrossRefGoogle ScholarPubMed
R Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna. http://www.r-project.org/ Google Scholar
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.Google Scholar
Seppälä, O. and Jokela, J. (2008). Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biology Letters 4, 663–666.Google Scholar
Stouffer, D. B. and Bascompte, J. (2011). Compartmentalization increases food-web persistence. Proceedings of the National Academy of Sciences of the United States of America 108, 3648–3652.Google Scholar
Stouffer, D. B., Sales-Pardo, M., Sirer, M. I. and Bascompte, J. (2012). Evolutionary conservation of species’ roles in food webs. Science 335, 1489–1492.Google Scholar
Strona, G. (2015). The underrated importance of predation in transmission ecology of direct lifecycle parasites. Oikos 124, 685–690.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 of Biology 69, 691–705.Google Scholar
Thatcher, V. E. (2006). Aquatic Biodiversity in Latin America: Amazon Fish Parasites, Vol. 1, 2nd Edn. Pensoft, Sofia, Bulgaria.Google Scholar
Thébault, E. and Fontaine, C. (2010). Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856.Google Scholar
Thieltges, D. W., Ferguson, M. A. D., Jones, C. S., Krakau, M., Montaudouin, X., Noble, L. R., Reise, K. and Poulin, R. (2009). Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160, 163–173.Google Scholar
Thieltges, D. W., Amundsen, P.-A., Hechinger, R. F., Johnson, P. T. J., Lafferty, K. D., Mouritsen, K. N., Preston, D. L., Reise, K., Zander, C. D. and Poulin, R. (2013). Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122, 1473–1482.Google Scholar
Tillberg, C. V., Holway, D. A., Lebrun, E. G. and Suarez, A. V. (2007). Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proceedings of the National Academy of Sciences of the United States of America 104, 20856–20861.Google Scholar
Wiens, J. J. and Graham, C. H. (2005). Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics 36, 519–539.Google Scholar
Woo, P. T. K. (2006). Fish diseases and Disorders: Protozoan and Metazoan Infections, Vol. 1, 2nd Edn. CAB International, Cambridge, UK.Google Scholar
Supplementary material: File

Lima supplementary material S1

Lima supplementary material

Download Lima supplementary material S1(File)
File 53.8 KB
Supplementary material: File

Lima supplementary material S2

Lima supplementary material

Download Lima supplementary material S2(File)
File 31.7 KB
Supplementary material: File

Lima supplementary material S3

Lima supplementary material

Download Lima supplementary material S3(File)
File 93.4 KB