Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T23:13:29.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Pairing success and sperm reserve of male Gammarus pulex infected by Cyathocephalus truncatus (Cestoda: Spathebothriidea)

Published online by Cambridge University Press:  03 August 2011

MATTHIAS GALIPAUD ,
ZOÉ GAUTHEY  and
LOÏC BOLLACHE
MATTHIAS GALIPAUD*
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
ZOÉ GAUTHEY
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
LOÏC BOLLACHE
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
*
*Corresponding author: Equipe Ecologie Evolutive, UMR CNRS Biogéosciences 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France. E-mail: matthias.galipaud@u-bourgogne.fr
Get access Rights & Permissions [Opens in a new window]

Summary

Manipulative parasites with complex life cycles are known to induce behavioural and physiological changes in their intermediate hosts. Cyathocephalus truncatus is a manipulative parasite which infects Gammarus pulex as intermediate host. G. pulex males display pre-copulatory mate guarding as a response to male-male competition for access to receptive females. In this paper, we tested the influence that C. truncatus-infection might have on male G. pulex sperm number and pairing success. We considered 3 classes of G. pulex males in our experiments: (i) uninfected males found paired in the field, (ii) uninfected males found unpaired in the field, or (iii) infected males found unpaired in the field. Both infected males and uninfected unpaired males paired less with a new female than uninfected paired males did. Furthermore, infected males appear to be at a strong disadvantage when directly competing for females with a healthy rival male, and had fewer sperm in their testes. We discuss the potential effect of male and female mating strategies on such male host mating alteration.

Keywords

manipulative parasitemale-male competitionpathogenic effectsgammaridstapeworm
Type
Research Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1429 - 1435
Copyright
Copyright © Cambridge University Press 2011

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

Able, D. J. (1996). The contagion indicator hypothesis for parasite-mediated sexual selection. Proceedings of the National Academy of Sciences, USA 93, 2229–2233.CrossRefGoogle ScholarPubMed
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–352.CrossRefGoogle ScholarPubMed
Bierbower, S. M. and Sparkes, T. C. (2007). Parasite-related pairing success in an intermediate host, Caecidotea intermedius (Isopoda): Effects of male behavior and reproductive physiology. Journal of Parasitology 93, 445–449.CrossRefGoogle Scholar
Bollache, L., Gambade, G. and Cézilly, F. (2000). The influence of microhabitat segregation on size assortative pairing in Gammarus pulex (L,) (Crustacea, Amphipoda). Archive für Hydrobiologie 147, 547–558.CrossRefGoogle Scholar
Bollache, L., Gambade, G. and Cézilly, F. (2001). The effects of two Acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus Minutus on pairing success in male Gammarus pulex (Crustacea: Amphipoda). Behavioral Ecology and Sociobiology 49, 293–303.Google Scholar
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two Acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102–110.CrossRefGoogle ScholarPubMed
Borgia, G. (1986). Satin bowerbird parasites: a test of the male bright hypothesis. Behavioral Ecology and Sociobiology 19, 355–358.CrossRefGoogle 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 Scholar
Carmichael, L. M., Moore, J. and Bjostad, L. J. (1993). Parasitism and decreased response to sex pheromones in male Periplaneta americana (Dictyoptera: Blattidae). Journal of Insect Behavior 6, 25–32.CrossRefGoogle Scholar
Clayton, D. H. (1991). The influence of parasites on host sexual selection. Parasitology Today 7, 329–334.CrossRefGoogle ScholarPubMed
Cothran, R. D. (2008 a). The mechanistic basis of a large male mating advantage in two freshwater amphipod species. Ethology 114, 1145–1153.CrossRefGoogle Scholar
Cothran, R. D. (2008 b). Direct and indirect fitness consequences of female choice in a crustacean. Evolution 62, 1666–1675.CrossRefGoogle Scholar
Dunn, A. M. (2005). Parasitic manipulation of host life history and sexual behaviour. Behavioural Processes 68, 255–258.CrossRefGoogle ScholarPubMed
Dunn, A. M., Andrews, T., Ingrey, H., Riley, J. and Wedell, N. (2006). Strategic sperm allocation under parasitic sex-ratio distortion. Biology Letters 2, 78–80.CrossRefGoogle ScholarPubMed
Elwood, R. W., Gibson, J. and Neil, S. (1987). The amorous Gammarus: size assortative mating in G. pulex. Animal Behaviour 35, 1–6.CrossRefGoogle Scholar
Ferreira, S. M., Jensen, K. T., Martins, P. A., Sousa, S. F., Marques, J. C. and Pardal, M. A. (2005). Impact of microphallid trematodes on the survivorship, growth, and reproduction of an isopod (Cyathura carinata). Journal of Experimental Marine Biology and Ecology 318, 191–199. doi: 10.1016/j.jembre.2004.12.018.CrossRefGoogle Scholar
Forbes, M. R. L. (1991). Ectoparasites and mating success of male Enallagma ebrium damselflies (Odonata: Coenagrionidae). Oikos 60, 336–342.CrossRefGoogle Scholar
Franceschi, N., Lemaître, J. F., Cézilly, F. and Bollache, L. (2010). Size-assortative pairing in Gammarus pulex (Crustacea: Amphipoda): a test of the prudent choice hypothesis. Animal Behaviour 79, 911–916. doi: 10.1016/j. anbehav.2010.01.002.CrossRefGoogle Scholar
Franceschi, N., Rigaud, T., Moret, Y., Hervant, F. and Bollache, L. (2007). Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex. Parasitology 134, 1839–1847.CrossRefGoogle ScholarPubMed
Galipaud, M., Dechaume-Moncharmont, F.-X., Oughadou, A. and Bollache, L. (2011). Does foreplay matter? Gammarus pulex females may benefit from long-lasting precopulatory mate guarding. Biology Letters 7, 333–335. doi: 10.1098/rsbl.2010.0924.CrossRefGoogle ScholarPubMed
Geffard, O., Xuereb, B., Chaumot, A., Geffard, A., Biagianti, S., Noël, C., Abbaci, K., Garric, J., Charmantier, G. and Charmantier-Daures, M. (2010). Ovarian cycle and embryonic development in Gammarus fossarum. Evironmental Toxicology and Chemistry 29, 2246–2259.Google ScholarPubMed
Grafen, A. and Ridley, M. (1983). A model of mate guarding. Journal of Theoretical Biology 102, 549–567.CrossRefGoogle Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Hou, M. L. and Sheng, C. F. (1999). Fecundity and longevity of Helicoverpa armigera (Lepidoptera: Noctuidae): effects of multiple mating. Journal of Economic Entomology 92, 569–573.CrossRefGoogle Scholar
Howard, R. D. and Minchella, D. J. (1990). Parasitism and mate competition. Oikos 58, 120–122.CrossRefGoogle Scholar
Hunte, W., Myers, R. and Doyle, R. (1985). Bayesian mating decisions in an amphipod, Gammarus lawrencianus Bousfield. Animal Behaviour 33, 366–372.CrossRefGoogle Scholar
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.CrossRefGoogle ScholarPubMed
Hynes, H. B. N. (1954). The ecology of Gammarus duebeni Lilljeborg and its occurrence in fresh water in western Britain. Journal of Animal Ecology 23, 38–84.CrossRefGoogle Scholar
Jormalainen, V. (1998). Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. The Quarterly Review of Biology 73, 275–304.CrossRefGoogle Scholar
Kendall, M. S. and Wolcott, T. G. (1999). The influence of male mating history on male-male competition and female choice in mating associations in the blue crab, Callinectes sapidus (Rathbun). Journal of Experimental Marine Biology and Ecology 239, 23–32.CrossRefGoogle Scholar
Keymer, A. E. and Read, A. F. (1991). Behavioural ecology: the impact of parasitism. In Parasite–Host Associations, Coexistence or Conflict (ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), Oxford Scientific Publications, Oxford, UK.Google Scholar
Knudsen, R., Gabler, H. M., Kuris, A. M. and Amundsen, P. A. (2001). Selective predation on parasitized prey. A comparison between two helminth species with different life-history strategies. Journal of Parasitology 87, 941–945.Google Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111–115.CrossRefGoogle ScholarPubMed
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts’ behaviour by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847. doi: 10.1890/06-2105.1.CrossRefGoogle ScholarPubMed
Lefèvre, T., Roche, B., Poulin, R., Hurd, H., Renaud, F. and Thomas, F. (2008). Exploiting host compensatory responses: the ‘must’ of manipulation? Trends in Parasitology 24, 435–439.CrossRefGoogle ScholarPubMed
Lemaître, J. F., Rigaud, T., Cornet, S. and Bollache, L. (2009). Sperm depletion, male mating behaviour and reproductive time out in Gammarus pulex (Crustacea, Amphipoda). Animal Behaviour. 79, 911–916. doi: 10.1016/j.anbehav.2008.08.028.Google Scholar
MacNeil, C., Dick, J. T. A. and Elwood, R. W. (1999). The dynamics of predation on Gammarus spp. (Crustacea: Amphipoda). Biological Reviews 75, 375–395.CrossRefGoogle Scholar
Milinski, M. and Bakker, T. C. M. (1990). Female sticklebacks use male coloration in mate choice and hence avoid infected males. Nature, London 344, 330–333.CrossRefGoogle Scholar
Moore, J. (1984). Altered behavioural responses in intermediate hosts – an acanthocephalan parasite strategy. The American Naturalist 123, 572–577.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behaviour of Animals. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Nakagawa, S. and Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews 82, 591–605. doi: 10.1111/j.1469-185X.2007.00027.x.CrossRefGoogle ScholarPubMed
Oetinger, D. F. (1987). Effects of Acanthocephalus dirus (Acanthocephala) on morphometrics and reproduction of Caecidotea intermedius (Crustacea: Isopoda). Transactions of the American Microscopical Society 116, 240–248.CrossRefGoogle Scholar
Okaka, C. E. (1984). Studies on the biology of Cyathocephalus truncatus (Pallas, 1781) (Cestoda: Spathebothriidea) in the fish and crustacean host. Ph.D. thesis, University of Leeds, Leeds, UK.Google Scholar
Ortigosa, A. and Rowe, L. (2003). The role of mating history and male size in determining mating behaviours and sexual conflict in a water strider. Animal Behaviour 65, 851–858.CrossRefGoogle Scholar
Parker, G. A. (1974). Courtship persistence and female-guarding as male time investment strategies. Behaviour 48, 157–184.CrossRefGoogle Scholar
Plaistow, S. J., Bollache, L. and Cézilly, F. (2003). Energetically costly precopulatory mate guarding in the amphipod Gammarus pulex: causes and consequences. Animal Behaviour 65, 683–691.CrossRefGoogle Scholar
Poulton, M. J. and Thompson, D. J. (1987). The effects of the acanthocephalan parasite Pomphorhynchus laevis on mate choice in Gammarus pulex. Animal Behaviour 35, 1577–1578.CrossRefGoogle Scholar
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology, 109, 109–118.CrossRefGoogle ScholarPubMed
Rasmussen, E. (1959). Behaviour of sacculinized shore crabs (Carcinus maenas Pennant). Nature, London 183, 479–480.CrossRefGoogle Scholar
Read, A. F. (1990). Parasites and the evolution of host sexual behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. and Behnke, J. M.), pp. 117–157. Taylor & Francis, New York, USA.Google Scholar
Sadek, M. M. (2001). Polyandry in field-collected Spodoptera littoralis moths and laboratory assessment of the effects of male mating history. Entomologia Experimentalis et Applicata 98, 165–172.CrossRefGoogle Scholar
Sparkes, T. C., Keogh, D. P. and Orsburn, T. H. (2002). Female resistance and mating outcomes in a stream-dwelling isopod: effects of male energy reserves and mating history. Behaviour 139, 875–895.CrossRefGoogle Scholar
Sparkes, T. C., Weil, K. A., Renwick, D. T. and Talkington, J. A. (2006). Development-related effects of an acanthocephalan parasite on pairing success of its intermediate host. Animal Behaviour 71, 439–448. doi: 10.1016/j.anbehav.2005.06.006.CrossRefGoogle Scholar
Sutcliffe, D. W. (1992). Reproduction in Gammarus (Crustacea, Amphipoda): basic processes. Freshwater Forum 2, 102–128.Google Scholar
Tain, L., Perrot-Minnot, M. J. and Cézilly, F. (2006). Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society of London, B 273, 3039–3045.Google ScholarPubMed
Thomas, F., Renaud, F., Derothe, J. M., Lambert, A., Meeüs, T. and Cézilly, F. (1995). Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite. Oecologia 104, 259–264.CrossRefGoogle ScholarPubMed
Thompson, S. N. and Kavaliers, M. I. (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109, 119–139.CrossRefGoogle ScholarPubMed
van Son, T. C. and Thiel, M. (2006). Mating behaviour of male rock shrimp, Rhynchocinetes typus (Decapoda: Caridea): effect of recent mating history and predation risk. Animal Behaviour 71, 61–70.CrossRefGoogle Scholar
Ward, P. I. (1986). A comparative field study of the breeding behaviour of a stream and a pond population of Gammarus Pulex (Amphipoda). Oikos 46, 29–36.CrossRefGoogle Scholar
Wellborn, G. A. and Bartholf, S. E. (2005). Ecological context and the importance of body and gnathopod size for pairing success in two amphipod ecomorphs. Oecologia 143, 308–316.CrossRefGoogle ScholarPubMed
Zohar, S. and Holmes, J. C. (1998). Pairing success of male Gammarus lacustris infected by two acanthocephalans: A comparative study. Behavioral Ecology 9, 206–211.CrossRefGoogle Scholar