Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-05T00:42:05.990Z Has data issue: false hasContentIssue false
  • English
  • Français

Identifying a key host in an acanthocephalan-amphipod system

Published online by Cambridge University Press:  25 August 2015

ALEXANDRE BAUER  and
THIERRY RIGAUD
ALEXANDRE BAUER*
Affiliation:
Laboratoire Biogéosciences, CNRS UMR CNRS 6282, Université de Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
THIERRY RIGAUD
Affiliation:
Laboratoire Biogéosciences, CNRS UMR CNRS 6282, Université de Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
*
*Corresponding author. Laboratoire Biogéosciences, CNRS UMR CNRS 6282, Université de Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Trophically transmitted parasites may use multiple intermediate hosts, some of which may be ‘key-hosts’, i.e. contributing significantly more to the completion of the parasite life cycle, while others may be ‘sink hosts’ with a poor contribution to parasite transmission. Gammarus fossarum and Gammarus roeseli are sympatric crustaceans used as intermediate hosts by the acanthocephalan Pomphorhynchus laevis. Gammarus roeseli suffers higher field prevalence and is less sensitive to parasite behavioural manipulation and to predation by definitive hosts. However, no data are available on between-host differences in susceptibility to P. laevis infection, making it difficult to untangle the relative contributions of these hosts to parasite transmission. Based on results from estimates of prevalence in gammarids exposed or protected from predation and laboratory infections, G. fossarum specimens were found to be more susceptible to P. laevis infection. As it is more susceptible to both parasite infection and manipulation, G. fossarum is therefore a key host for P. laevis transmission.

Keywords

Multi-host parasitesprevalencehost specificityhost qualitytransmissioninfectivity
Type
Research Article
Information
Parasitology , Volume 142 , Issue 13 , November 2015 , pp. 1588 - 1594
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

Bauer, A., Trouvé, S., Grégoire, A., Bollache, L. and Cézilly, F. (2000). Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. International Journal for Parasitology 30, 1453–1457.CrossRefGoogle ScholarPubMed
Bollache, L., Kaldonski, N., Troussard, J.-P., Lagrue, C. and Rigaud, T. (2006). Spines and behaviour as defences against fish predators in an invasive freshwater amphipod. Animal Behaviour 72, 627–633.Google Scholar
Cézilly, F., Thomas, F., Médoc, V. and Perrot-Minnot, M.-J. (2010). Host-manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26, 311–317.Google Scholar
Chovet, M. and Lécureuil, J. (1994). Répartition des Gammaridae épigés (Crustacés, Amphipodes) dans la Loire et les rivières de la Région Centre (France). Annales de Limnologie 30, 11–23.Google Scholar
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago.Google Scholar
Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E. and Rigaud, T. (2011). Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 2692–2698.CrossRefGoogle ScholarPubMed
Dunn, A. M. and Dick, J. T. A. (1998). Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography 21, 593–598.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Franceschi, N., Bauer, A., Bollache, L. and Rigaud, T. (2008). The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. International Journal for Parasitology 38, 1161–1170.Google Scholar
Franceschi, N., Cornet, S., Bollache, L., Dechaume-Moncharmont, F.-X., Bauer, A., Motreuil, S. and Rigaud, T. (2010). Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution 64, 2417–2430.Google Scholar
Hall, S., Becker, C., Simonis, J. and Duffy, M. (2009). Friendly competition: evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology 90, 791–801.Google Scholar
Jazdzewski, K. (1980). Range extensions of some gammaridean species in European inland waters caused by human activity. Crustaceana (Suppl. 6), 84–107.Google Scholar
Johnson, P. T. J., Lund, P. J., Hartson, R. B. and Yoshino, T. P. (2009). Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proceedings of the Royal Society, Series B, Biological Sciences 276, 1657–1663.Google Scholar
Kaldonski, N., Perrot-Minnot, M.-J. and Cézilly, F. (2007). Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Animal Behaviour 74, 1311–1317.Google Scholar
Kaldonski, N., Lagrue, C., Motreuil, S., Rigaud, T. and Bollache, L. (2008). Habitat segregation mediates predation by the benthic fish Cottus gobio on the exotic amphipod species Gammarus roeseli . Naturwissenschaften 95, 839–844.Google Scholar
Kennedy, C. R. (2006). Ecology of the Acanthocephala. 1st Edn. Cambridge University Press, New York.Google Scholar
Kopp, K. and Jokela, J. (2007). Resistant invaders can convey benefits to native species. Oikos 116, 295–301.Google Scholar
Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. The American Naturalist 140, 854–867.Google Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts’ behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847.Google Scholar
Lagrue, C., Wattier, R., Galipaud, M., Gauthey, Z., Rullmann, J.-P., Dubreuil, C., Rigaud, T. and Bollache, L. (2014). Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes. Freshwater Biology 59, 2555–2570.Google Scholar
Médoc, V., Rigaud, T., Motreuil, S., Perrot-Minnot, M.-J. and Bollache, L. (2011). Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften 98, 825–825.Google Scholar
Moore, J. K. (1984). Altered behavioural responses in intermediate hosts – An acanthocephalan parasite strategy. The American Naturalist 123, 572–577.Google Scholar
Moret, Y., Bollache, L., Wattier, R. and Rigaud, T. (2007). Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context. International Journal for Parasitology 37, 637–644.Google Scholar
Perrot-Minnot, M.-J., Sanchez-Thirion, K. and Cézilly, F. (2014). Multidimensionality in host manipulation mimicked by serotonin injection. Proceedings of the Royal Society, Series B, Biological Sciences 281, 20141915. doi:10.1098/rspb.2014.1915 Google Scholar
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. In Advances in the Study of Behavior (ed. Mitani, J., Brockmann, H. J., Roper, T., Naguib, M. and Wynne-Edwards, K.), pp. 151–186. Elsevier, Burlington. doi:10.1016/S0065-3454(10)41005-0 Google Scholar
Rigaud, T. and Moret, Y. (2003). Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 127, 571–577.Google Scholar
Rigaud, T., Perrot-Minnot, M.-J. and Brown, M. J. F. (2010). Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society, Series B, Biological Sciences 277, 3693–3702.Google Scholar
Rousset, F., Thomas, F., De Meeûs, T. and Renaud, F. (1996). Inference of parasite-induced host mortality from distributions of parasite loads. Ecology 77, 2203–2211.Google Scholar
Ruiz-González, M., Bryden, J., Moret, Y., Reber-Funk, C., Schmid-Hempel, P. and Brown, M. J. F. (2012). Dynamic transmission, host quality, and population structure in a multihost parasite of bumblebees. Evolution 66, 3053–3066.Google Scholar
Streicker, D. G., Fenton, A. and Pedersen, A. B. (2013). Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecology Letters 16, 975–984.CrossRefGoogle Scholar
Telfer, S., Bown, K. J., Sekules, R., Begon, M., Hayden, T. and Birtles, R. (2005). Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130, 661–668.Google Scholar
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 1851–1899.Google Scholar
Weinreich, F., Benesh, D. P. and Milinski, M. (2013). Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective. Parasitology 140, 129–135.Google Scholar
Westram, A. M., Baumgartner, C., Keller, I. and Jokela, J. (2011 a). Are cryptic host species also cryptic to parasites? Host specificity and geographical distribution of acanthocephalan parasites infecting freshwater Gammarus . Infection, Genetics and Evolution 11, 1083–1090.Google Scholar
Westram, A. M., Jokela, J., Baumgartner, C. and Keller, I. (2011 b). Spatial distribution of cryptic species diversity in European freshwater Amphipods (Gammarus fossarum) as revealed by pyrosequencing. PLoS ONE 6, 1–6.Google Scholar