Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-29T13:04:59.542Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of ecological opportunity in shaping host–parasite networks

Published online by Cambridge University Press:  03 August 2020

Elvira D'Bastiani Open the ORCID record for Elvira D'Bastiani [Opens in a new window] ,
Karla M. Campião ,
Walter A. Boeger  and
Sabrina B. L. Araújo
Elvira D'Bastiani*
Affiliation:
Postgraduate program in Ecology and Conservation, Federal University of Paraná, Laboratory of Biological Interaction – Biological Sciences Sector, Caixa Postal (P.O. Box) 19031, CEP (Postal Code) 81531-990, Curitiba, PR, Brasil
Karla M. Campião
Affiliation:
Department of Zoology, Federal University of Paraná, Laboratory of Biological Interaction – Biological Sciences Sector, Caixa Postal (P.O. Box) 19031, CEP (Postal Code) 81531-990, Curitiba, PR, Brasil
Walter A. Boeger
Affiliation:
Department of Zoology, Federal University of Paraná, Laboratory of Biological Interaction – Biological Sciences Sector, Caixa Postal (P.O. Box) 19031, CEP (Postal Code) 81531-990, Curitiba, PR, Brasil
Sabrina B. L. Araújo
Affiliation:
Department of Physics, Federal University of Paraná, Laboratory of Biological Interaction – Biological Sciences Sector, Caixa Postal (P.O. Box) 19031, CEP (Postal Code) 81531-990, Curitiba, PR, Brasil
*
Author for correspondence: Elvira D'Bastiani, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite the great interest to quantify the structure of host–parasite interaction networks, the real influence of some factors such as taxonomy, host body size and ecological opportunity remains poorly understood. In this paper, we investigate the general patterns of organization and structure of interactions in two anuran–parasite networks in the Brazilian Pantanal (seasonally flooded environment) and Atlantic Forest (non-flooded forest). We present theoretical models to test whether the structures of these host–parasite interaction networks are influenced by neutrality, host taxonomy and host body size. Subsequently, we calculated metrics of connectance, nestedness and modularity to characterize the network structure. We demonstrated the structure networks were influenced mainly by body size and taxonomy of the host. Moreover, our results showed that the seasonally flooded environment present networks with higher connectance/nestedness and lower modularity compared to the other environment. The results also suggest that seasonal floods may promote ecological opportunities for new species associations.

Keywords

Body sizecommunitydispersal limitationendoparasite–anurantaxonomy
Type
Research Article
Information
Parasitology , Volume 147 , Issue 13 , November 2020 , pp. 1452 - 1460
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Adlard, RD, Miller, TL and Smit, NJ (2015) The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends Parasitology 31, 160–166.CrossRefGoogle ScholarPubMed
Agosta, SJ (2006) On ecological fitting, plant–insect associations, herbivore host shifts, and host plant selection. Oikos 114, 556–565.CrossRefGoogle Scholar
Agosta, SJ and Klemens, JA (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecology Letters 11, 1123–1134.CrossRefGoogle ScholarPubMed
Agosta, SJ, Janz, N and Brooks, DR (2010) How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia Curitiba 27, 151–162.CrossRefGoogle Scholar
Agostinho, AA, Thomaz, SM, Minte-Vera, CV and Winemiller, KO (2000) Biodiversity in the high Paraná River Floodplain. In Gopal, B, Junk, WJ and Davis, JA (eds), Biodiversity in Wetlands: Assessment, Function and Conservation. Leiden: Backhuys Publishers, pp. 89–118.Google Scholar
Almeida-Neto, M, Guimaraes, P, Guimaraes, PR Jr, Loyola, RD and Ulrich, W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.CrossRefGoogle Scholar
Araujo, SB, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS ONE 10, e0140577 (1/12).CrossRefGoogle ScholarPubMed
Bascompte, J, Jordano, P, Melián, CJ and Olesen, JM (2003) The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences 100, 9383–9387.CrossRefGoogle ScholarPubMed
Bozelli, RL (1992) Composition of the zooplankton community of Batata and Mussurá Lakes and of the Trombetas River, State of Pará, Brazil. Amazoniana: Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas 12, 239–261.Google Scholar
Brooks, DR and Hoberg, EP (2007) How will global climate change affect parasite–host assemblages? Trends in Parasitology 23, 571–574.CrossRefGoogle ScholarPubMed
Brooks, DR, León-Règagnon, V, McLennan, DA and Zelmer, D (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, S76–S85.CrossRefGoogle ScholarPubMed
Brooks, DR, Hoberg, EP, Boeger, WA, Gardner, SL, Galbreath, KE, Herczeg, D and Dursahinhan, AT (2014) Finding them before they find us: informatics, parasites, and environments in accelerating climate change. COPA 81, 155–164.Google Scholar
Brooks, DR, Hoberg, EP and Boeger, WA (2019) The Stockholm Paradigm: Climate Change and Emerging Disease. Chicago and London: University of Chicago Press.Google Scholar
Campiao, KM, de Aquino Ribas, AC, Morais, DH, da Silva, RJ and Tavares, LER (2015) How many parasites species a frog might have? Determinants of parasite diversity in South American anurans. PLoS ONE 10, e0140577 (1/12).CrossRefGoogle ScholarPubMed
Campião, KM, da Silva, ICO, Dalazen, GT, Paiva, F and Tavares, LER (2016) Helminth parasites of 11 anuran species from the Pantanal Wetland, Brazil. Comparative Parasitology 83, 92–100.CrossRefGoogle Scholar
Clark, NJ, Clegg, SM, Sam, K, Goulding, W, Koane, B and Wells, K (2018) Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Diversity and Distributions 24, 13–23.CrossRefGoogle Scholar
Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0. Available at http://www.R-project.org/.2018.Google Scholar
Dallas, T, Hall, RJ and Drake, JM (2016) Competition-mediated feedbacks in experimental multispecies epizootics. Ecology 97, 661–670.Google ScholarPubMed
Dormann, CF and Strauss, R (2014) A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5, 90–98.CrossRefGoogle Scholar
Dormann, CF, Gruber, B and Fründ, J (2008) Introducing the bipartite package: analysing ecological networks. Interaction 1.Google Scholar
Dormann, CF, von Riedmatten, L and Scherer-Lorenzen, M (2017) No consistent effect of plant species richness on resistance to simulated climate change for above-or below-ground processes in managed grasslands. BMC Ecology 17, 23.CrossRefGoogle ScholarPubMed
Eklöf, A, Jacob, U, Kopp, J, Bosch, J, Castro-Urgal, R, Chacoff, NP and Lomáscolo, SB (2013) The dimensionality of ecological networks. Ecology Letters 16, 577–583.CrossRefGoogle ScholarPubMed
Frost, DR (2020) Amphibian Species of the World: an Online Reference. Version 6.0. American Museum of Natural History, New York, USA.Google Scholar
Gonzalez, CE and INÉS, HM (2015) Checklist of nematode parasites of amphibians from Argentina. Zootaxa 3980, 451–476.CrossRefGoogle ScholarPubMed
González, AMM, Ornelas, JF, Dalsgaard, B, Márquez-Luna, U and Lara, C (2018) Meta-networks for the study of biogeographical traits in ecological networks: the Mexican hummingbird-plant assemblage. The Science of Nature 105, 9–10.Google Scholar
Graça, RJ, Oda, FH, Lima, FS, Guerra, V, Gambale, PG and Takemoto, RM (2017) Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil. Journal of Natural History 51, 705–729.CrossRefGoogle Scholar
Hadfield, JD, Krasnov, BR, Poulin, R and Nakagawa, S (2014) A tale of two phylogenies: comparative analyses of ecological interactions. The American Naturalist 183, 174–187.CrossRefGoogle ScholarPubMed
Hoberg, EP and Brooks, DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 1533–1550.CrossRefGoogle Scholar
Hoberg, EP and Zarlenga, DS (2016) Evolution and biogeography of Haemonchus contortus: linking faunal dynamics in space and time. In Hoberg, EP and Zarlengathe, DS (eds), Advances in Parasitology, Vol. 93. Bethesda, United States: Academic Press, pp. 1–30.Google Scholar
Huang, S, Bininda-Emonds, OR, Stephens, PR, Gittleman, JL and Altizer, S (2014) Phylogenetically related and ecologically similar carnivores harbour similar parasite assemblages. Journal of Animal Ecology 83, 671–680.CrossRefGoogle ScholarPubMed
Janzen, DH (1985) On ecological fitting. Oikos 45, 308–310.CrossRefGoogle Scholar
Jones, KE, Patel, NG, Levy, MA, Storeygard, A, Balk, D, Gittleman, JL and Daszak, P (2008) Global trends in emerging infectious diseases. Nature 451, 990–993.CrossRefGoogle ScholarPubMed
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, BR, Fortuna, MA, Mouillot, D, Khokhlova, IS, Shenbrot, GI and Poulin, R (2012) Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. The American Naturalist 179, 501–511.CrossRefGoogle ScholarPubMed
Krishna, A, Guimaraes, PR Jr, Jordano, P and Bascompte, J (2008) A neutral-niche theory of nestedness in mutualistic networks. Oikos 117, 1609–1618.CrossRefGoogle Scholar
Lafferty, KD (2009) The ecology of climate change and infectious diseases. Ecology 90, 888–900.CrossRefGoogle ScholarPubMed
Leung, TL and Koprivnikar, J (2016) Nematode parasite diversity in birds: the role of host ecology, life history and migration. Journal of Animal Ecology 85, 1471–1480.CrossRefGoogle ScholarPubMed
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2013) Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122, 73–83.CrossRefGoogle Scholar
MacArthur, RH, Diamond, JM and Karr, JR (1972) Density compensation in island faunas. Ecology 53, 330–342.CrossRefGoogle Scholar
Malcicka, M, Agosta, SJ and Harvey, JA (2015) Multi level ecological fitting: indirect life cycles are not a barrier to host switching and invasion. Global Change Biology 21, 3210–3218.CrossRefGoogle Scholar
May, RM (2019) Stability and Complexity in Model Ecosystems, vol. 1. Princeton university press.CrossRefGoogle Scholar
Morand, S (2015) (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. International Journal for Parasitology 4, 80–87.Google ScholarPubMed
Morse, SS, Mazet, JA, Woolhouse, M, Parrish, CR, Carroll, D, Karesh, WB and Daszak, P (2012) Prediction and prevention of the next pandemic zoonosis. The Lancet 380, 1956–1965.CrossRefGoogle ScholarPubMed
Naisbit, RE, Rohr, RP, Rossberg, AG, Kehrli, P and Bersier, LF (2012) Phylogeny versus body size as determinants of food web structure. Proceedings of the Royal Society B: Biological Sciences 279, 3291–3297.CrossRefGoogle ScholarPubMed
Nylin, S, Agosta, S, Bensch, S, Boeger, WA, Braga, MP, Brooks, DR and Schäpers, A (2018) Embracing colonizations: a new paradigm for species association dynamics. Trends in Ecology & Evolution 33, 4–14.CrossRefGoogle ScholarPubMed
Olesen, JM, Bascompte, J, Dupont, YL and Jordano, P (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences 104, 19891–19896.CrossRefGoogle ScholarPubMed
Poisot, T, Stouffer, DB and Gravel, D (2015) Beyond species: why ecological interaction networks vary through space and time. Oikos 124, 243–251.CrossRefGoogle Scholar
Poulin, R (2004) Parasites and the neutral theory of biodiversity. Ecography 27, 119–123.CrossRefGoogle Scholar
Ramalho, WP, Machado, IF and Vieira, LJS (2018) Do flood pulses structure amphibian communities in floodplain environments? Biotropica 50, 338–345.CrossRefGoogle Scholar
Rezende, EL, Jordano, P and Bascompte, J (2007) Effects of phenotypic complementarity and phylogeny on the nested structure of mutualistic networks. Oikos 116, 1919–1929.CrossRefGoogle Scholar
Rezende, EL, Albert, EM, Fortuna, MA and Bascompte, J (2009) Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecology Letters 12, 779–788.CrossRefGoogle Scholar
Scordato, ES and Kardish, MR (2014) Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. Journal of Animal Ecology 83, 1387–1397.CrossRefGoogle ScholarPubMed
Stigall, AL (2014) When and how do species achieve niche stability over long time scales? Ecography 37, 1123–1132.Google Scholar
Stigall, AL, Bauer, JE, Lam, AR and Wright, DF (2017) Biotic immigration events, speciation, and the accumulation of biodiversity in the fossil record. Global and Planetary Change 148, 242–257.CrossRefGoogle Scholar
Thomaz, SM, Roberto, MDC and Bini, LM (1997) Caracterização limnológica dos ambientes aquáticos e influência dos níveis fluviométricos. In Anna Emília ADeM, V, Angelo A, Agostinho and Norma, SH (eds), A Planície de Inundação do Alto rio Paraná: Aspectos Físicos, Biológicos E Socioeconômicos, Vol. 1. EDUEM, pp. 73–102.Google Scholar
Valverde, S, Vidiella, B, Montañez, R, Fraile, A, Sacristán, S and García-Arenal, F (2020) Coexistence of nestedness and modularity in host–pathogen infection networks. Nature Ecology & Evolution, 1–10.Google ScholarPubMed
Vanbergen, AJ, Woodcock, BA, Heard, MS and Chapman, DS (2017) Network size, structure and mutualism dependence affect the propensity for plant–pollinator extinction cascades. Functional Ecology 31, 1285–1293.CrossRefGoogle Scholar
Vázquez, DP, Chacoff, NP and Cagnolo, L (2009) Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90, 2039–2046.CrossRefGoogle ScholarPubMed
Wright, SJ (1980) Density compensation in island avifaunas. Oecologia 45, 385–389.CrossRefGoogle ScholarPubMed
Zar, JH (1999) Biostatistical Analysis, 4th Edn. Upper Saddle River, NJ, USA: Prentice-Hall, p. 931.Google Scholar
Supplementary material: File

D'Bastiani et al. Supplementary Materials

D'Bastiani et al. Supplementary Materials

Download D'Bastiani et al. Supplementary Materials(File)
File 689.1 KB