Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-22T01:46:43.492Z Has data issue: false hasContentIssue false
  • English
  • Français

Facultative and obligate parasite communities exhibit different network properties

Published online by Cambridge University Press:  07 August 2013

TIMOTHÉE POISOT ,
MICHAL STANKO ,
DANA MIKLISOVÁ  and
SERGE MORAND
TIMOTHÉE POISOT*
Affiliation:
Université du Québec à Rimouski, Rimouski, Canada Quebec Center for Biodiversity Science, McGill University, Montréal, Canada
MICHAL STANKO
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia
DANA MIKLISOVÁ
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia
SERGE MORAND
Affiliation:
Institut des Sciences de l'Évolution, Université Montpellier 2, Montpellier, France
*
*Corresponding author: Université du Québec à Rimouski, Rimouski, Canada. E-mail: timothee_poisot@uqar.ca
Get access Rights & Permissions [Opens in a new window]

Summary

Network theory is gaining momentum as a descriptive tool in community ecology. Because organisms with the same lifestyle can still exhibit ecological differences, it is crucial to determine the scale at which networks should be described. Here we show that networks of hosts (mammals) and parasites (ectoparasitic gamasid mites) differ when either facultative or obligatory parasites only are considered. More importantly, the structure of these networks is opposed, with obligatory parasites networks being more modular, and facultative parasites networks being more nested. Our results have consequences for the way we define which species to include in ecological networks, which we discuss in the light of community ecology and epidemiology.

Type
Parasitology Express
Information
Parasitology , Volume 140 , Issue 11 , September 2013 , pp. 1340 - 1345
Copyright
Copyright © Cambridge University Press 2013 

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

Almeida-Neto, M., Guimaraes, P., Guimaraes, P. Jr., Loyola, R. and Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.CrossRefGoogle Scholar
Barber, M. (2007). Modularity and community detection in bipartite networks. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics 76, 066102.CrossRefGoogle ScholarPubMed
Bascompte, J. (2007). Networks in ecology. Basic and Applied Ecology 8, 485–490.CrossRefGoogle Scholar
Bascompte, J., Jordano, P., Melián, 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.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago, IL, USA.Google Scholar
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
Danon, L., Ford, A. P., House, T., Jewell, C. P., Keeling, M. J., Roberts, G. O., Ross, J. V. and Vernon, M. C. (2011). Networks and the epidemiology of infectious disease. Interdisciplinary Perspectives on Infective Diseases 2011, 284909.Google ScholarPubMed
Dormann, C. F., Frund, J., Blüthgen, N. and Gruber, B. (2009). Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecology Journal 2, 7–24.CrossRefGoogle Scholar
Dunne, J. A. (2006). The network structure of food webs. In Ecological Networks: Linking Structure and Dynamics (ed. Dunne, J. A. and Pascual, M.), pp. 27–86. Oxford University Press, Oxford, UK.Google Scholar
Espinosa-Soto, C. and Wagner, A. (2010). Specialization can drive the evolution of modularity. PLoS Computational Biology 6, e1000719.CrossRefGoogle ScholarPubMed
Flores, C. O., Meyer, J. R., Valverde, S., Farr, L. and Weitz, J. S. (2011). Statistical structure of host-phage interactions. Proceedings of the National Academy of Sciences USA 108, E288–E297.CrossRefGoogle ScholarPubMed
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, 1170–1181.CrossRefGoogle ScholarPubMed
Fortuna, M. A. and Bascompte, J. (2006). Habitat loss and the structure of plant–animal mutualistic networks. Ecology Letters 9, 281–286.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 78, 811–817.CrossRefGoogle Scholar
Haitlinger, R. (1977). Parasitological investigation of small mammals of Gory Sowie (Middle Sudetes). VI. Siphonaptera, Anoplura, Acarina. Polskiego Pisma Entomologicznegu 47, 429–492.Google Scholar
Jordano, P., Bascompte, J. and Olesen, J. M. (2003). Invariant properties in coevolutionary networks of plant–animal interactions. Ecology Letters 6, 69–81.CrossRefGoogle Scholar
Kéfi, S., Berlow, E. L., Wieters, E. A., Navarrete, S. A., Petchey, O. L., Wood, S. A., Boit, A., Joppa, L. N., Lafferty, K. D., Williams, R. J., Martinez, N. D., Menge, B. A., Blanchette, C. A., Iles, A. C. and Brose, U. (2012). More than a meal … integrating non-feeding interactions into food webs. Ecology Letters 15, 291–300.CrossRefGoogle ScholarPubMed
Koleff, P., Gaston, K. J. and Lennon, J. J. (2003). Measuring beta diversity for presence-absence data. Journal of Animal Ecology 72, 367–382.CrossRefGoogle Scholar
Krasnov, B. R., Stanko, M., Khokhlova, I. S., Shenbrot, G. I., Morand, S., Korallo-Vinarskaya, N. P. and Vinarski, M. V. (2010). Nestedness and -diversity in ectoparasite assemblages of small mammalian hosts: effects of parasite affinity, host biology and scale. Oikos 120, 630–639.CrossRefGoogle Scholar
Krasnov, B. R., Mouillot, D., Shenbrot, G. I., Khokhlova, I. S. and Poulin, R. (2011). Beta-specificity: the turnover of host species in space and another way to measure host specificity. International Journal for Parasitology 41, 33–41.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
Leung, T. L. F. and Poulin, R. (2008). Parasitism, commensalism, and mutualism: exploring the many shades of symbioses. Vie et Milieu 58, 107–115.Google Scholar
Liu, X. and Murata, T. (2010). Community detection in large-scale bipartite networks. Transactions of the Japanese Society for Artificial Intelligence 5, 184–192.Google Scholar
Mouillot, D., Krasnov, B. R., Shenbrot, G. I. and Poulin, R. (2008). Connectance and parasite diet breadth in flea-mammal webs. Ecography 31, 16–20.CrossRefGoogle Scholar
Mrciak, M., Daniel, M. and Rosický, B. (1966). Parasites and nest inhabitants of small mammals in the western Carpathians. I. Mites of the superfamily Gamasoidea (Parasitiformes). Acta Facultatis Rerum Naturalium Universitatis Comenianae 13, 81–116.Google Scholar
Newman, M. E. J. (2010). Networks: an Introduction. Oxford University Press, New York, USA.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Poisot, T., Canard, E., Mouquet, N. and Hochberg, M. E. (2012 a). A comparative study of ecological specialization estimators. Methods in Ecology and Evolution 3, 537–544.CrossRefGoogle Scholar
Poisot, T., Canard, E., Mouillot, D., Mouquet, N. and Gravel, D. (2012 b). The dissimilarity of species interaction networks. Ecology Letters 15, 1353–1361.CrossRefGoogle ScholarPubMed
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. (2000). The diversity of parasites. Quarterly Review of Biology 75, 277–293.CrossRefGoogle ScholarPubMed
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Poullain, V., Gandon, S., Brockhurst, M. A., Buckling, A. and Hochberg, M. E. (2008). The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62, 1–11.Google ScholarPubMed
Roche, B., Dobson, A. P., Guegan, J.-F. and Rohani, P. (2012). Linking community and disease ecology: the impact of biodiversity on pathogen transmission. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 2807–2813.CrossRefGoogle ScholarPubMed
Schleuning, M., Fründ, J., Klein, A.-M., Abrahamczyk, S., Alarcón, R., Albrecht, M., Andersson, G. K. S., Bazarian, S., Böhning-Gaese, K., Bommarco, R. et al. (2012). Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology 22, 1925–1931.CrossRefGoogle ScholarPubMed
Schoener, T. W. (1989). Food webs from the small to the large. Ecology 70, 1559–1589.CrossRefGoogle Scholar
Stanko, M., Miklisová, D., Goüy de Bellocq, J. and Morand, S. (2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295.CrossRefGoogle ScholarPubMed
Strogatz, S. H. (2001). Exploring complex networks. Nature 410, 268–276.CrossRefGoogle ScholarPubMed
Thebault, E. and Fontaine, C. (2010). Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856.CrossRefGoogle ScholarPubMed
Vazquez, 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.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.CrossRefGoogle Scholar
Veech, J. A. (2012). Significance testing in ecological null models. Theoretical Ecology 5, 611–616.CrossRefGoogle Scholar
Weitz, J. S., Poisot, T., Meyer, J. R., Flores, C. O., Valverde, S., Sullivan, M. B. and Hochberg, M. E. (2013). Phage–bacteria infection networks. Trends in Microbiology 21, 82–91.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. and Gowtage-Sequeria, S. (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11, 1842–1847.CrossRefGoogle ScholarPubMed