Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-23T12:45:27.269Z Has data issue: false hasContentIssue false
  • English
  • Français

Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective

Published online by Cambridge University Press:  20 August 2012

F. WEINREICH ,
D. P. BENESH  and
M. MILINSKI
F. WEINREICH*
Affiliation:
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany
D. P. BENESH
Affiliation:
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany
M. MILINSKI
Affiliation:
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany
*
*Corresponding author: Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany. Tel: +49 4522763348. Fax: +49 4522763310. E-mail: weinreich@evolbio.mpg.de
Get access Rights & Permissions [Opens in a new window]

Summary

Trophically-transmitted parasites generally need to undergo a period of development in the intermediate host before reaching infectivity. During this vulnerable period, manipulation of the host to reduce susceptibility to predation would be advantageous for parasites, because it increases the probability of surviving until infectivity and thus the probability of transmission. We tested this ‘predation suppression’ hypothesis in 2 parasite species that use copepods as first hosts: the tapeworm Schistocephalus solidus and the nematode Camallanus lacustris. In a series of prey choice experiments, we found that copepods harbouring uninfective, still-developing worm larvae were less frequently consumed by stickleback predators than uninfected copepods. The levels of predation suppression were similar in the two parasite species, suggestive of convergent evolution. Additionally, copepods harbouring 2 worms of a given species were not more susceptible to predation than those with 1 worm, suggesting that excessive larval parasite growth does not increase host susceptibility to predation. Our results support the idea that parasites can suppress intermediate host susceptibility to predation while uninfective, but we also note that the available studies suggest that this effect is weaker than the frequently observed enhancement of host predation by infective helminth larvae.

Keywords

anti-predator behaviourconvergent evolutionGasterosteus aculeatusgrowth costshost manipulationMacrocyclops albiduspredation enhancementpredation suppressiontransmission
Type
Research Article
Information
Parasitology , Volume 140 , Issue 1 , January 2013 , pp. 129 - 135
Copyright
Copyright © Cambridge University Press 2012

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

Ball, M. A., Parker, G. A. and Chubb, J. C. (2008). The evolution of complex life cycles when parasite mortality is size- or time-dependent. Journal of Theoretical Biology 253, 202–214.CrossRefGoogle ScholarPubMed
Barber, I., Walker, P. and Svensson, P. A. (2004). Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour 11, 1425–1440.CrossRefGoogle Scholar
Benesh, D. P. (2010 a). Developmental inflexibility of larval tapeworms in response to resource variation. International Journal for Parasitology 40, 487–497.CrossRefGoogle ScholarPubMed
Benesh, D. P. (2010 b). What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 162, 599–608.CrossRefGoogle Scholar
Benesh, D. P. (2011). Intensity-dependent host mortality: What can it tell us about larval growth strategies in complex life cycle helminths? Parasitology 138, 913–925.CrossRefGoogle ScholarPubMed
Benesh, D. P., Chubb, J. C. and Parker, G. A. (2011). Exploitation of the same trophic link favors convergence of larval life-history strategies in complex life cycle helminths. Evolution 65, 2286–2299.CrossRefGoogle ScholarPubMed
Bethel, W. M. and Holmes, J. C. (1974). Correlation of development of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with infectivity to definitive host. Journal of Parasitology 60, 272–274.CrossRefGoogle ScholarPubMed
Brattey, J. (1983). The effects of larval Acanthocephalus lucii on the pigmentation, reproduction, and susceptibility to predation of the isopod Asellus aquaticus. Journal of Parasitology 69, 1172–1173.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Christen, M. and Milinski, M. (2005). The optimal foraging strategy of its stickleback host constrains a parasite's complex life cycle. Behaviour 142, 979–996.Google Scholar
Clarke, A. S. (1954). Studies on the life cycle of the pseudophyllidean cestode Schistocephalus solidus. Proceedings of the Zoological Society of London 124, 257–302.CrossRefGoogle 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
Dubinina, M. N. (1980). Tapeworms (Cestoda, Ligulidae) of the Fauna of the USSR, Amerind Publishing Co. Pvt. Ltd., New Dehli, India.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.CrossRefGoogle ScholarPubMed
Franz, K. and Kurtz, J. (2002). Altered host behaviour: manipulation or energy depletion in tapeworm-infected copepods? Parasitology 125, 187–196.CrossRefGoogle ScholarPubMed
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J. C. and Parker, G. A. (2009). When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 1976–1986.CrossRefGoogle ScholarPubMed
Hammerschmidt, K. and Kurtz, J. (2005). Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proceedings of the Royal Society of London, B 272, 2511–2518.Google Scholar
Helluy, S. (1983). Relations hôtes-parasite du trématode Microphallus papillorobustus (rankin, 1940) ii-modifications du comportement des Gammarus hôtes intermédiaires et localisation des métacercaires. Annales de Parasitologie Humaine et Comparé 58, 1–17.CrossRefGoogle Scholar
Hurd, H. and Fogo, S. (1991). Changes induced by Hymenolepis diminuta (Cestoda) in the behavior of the intermediate host Tenebrio molitor (Coleoptera). Canadian Journal of Zoology-Revue Canadienne De Zoologie 69, 2291–2294.CrossRefGoogle Scholar
Hynes, H. B. N. (1950). The food of freshwater sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius) with a review of the methods used in studies of the food of fish. Journal of Animal Ecology 19, 36–58.CrossRefGoogle Scholar
Lefèvre, T., Adamo, S. A., Biron, D. G., Missé, D., Hughes, D. and Thomas, F. (2009). Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Advances in Parasitology 68, 45–83.CrossRefGoogle ScholarPubMed
Levri, E. P. (1998). The influence of non-host predators on parasite-induced behavioral changes in a freshwater snail. Oikos 531–537.CrossRefGoogle Scholar
Levri, E. P. and Lively, C. M. (1996). The effects of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum. Animal Behaviour 51, 891–901.CrossRefGoogle Scholar
Manly, B. F. J. (1974). A model for certain types of selection experiments. Biometrics 281–294.CrossRefGoogle Scholar
Médoc, V. and Beisel, J. N. (2008). An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators. Parasitology 135, 977–984.CrossRefGoogle ScholarPubMed
Médoc, V. and Beisel, J. N. (2011). When trophically-transmitted parasites combine predation enhancement with predation suppression to optimize their transmission. Oikos 120, 1452–1458.CrossRefGoogle Scholar
Médoc, V., Bollache, L. and Beisel, J. N. (2006). Host manipulation of a freshwater crustacean (Gammarus roeseli) by an acanthocephalan parasite (Polymorphus minutus) in a biological invasion context. International Journal for Parasitology 36, 1351–1358.CrossRefGoogle Scholar
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 39–57.CrossRefGoogle Scholar
Milinski, M. (1984). A predator's costs of overcoming the confusion-effect of swarming prey. Animal Behaviour 32, 1157–1162.CrossRefGoogle Scholar
Milinski, M. (1986). Constraints placed by predators on feeding behaviour. In The behaviour of Teleost Fishes (ed. Pitcher, T. J.), pp. 236–252. Croom Helm, London, UK.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, USA, New York, NY, USA.CrossRefGoogle Scholar
Moravec, F. S. (1969). Observations on the development of Camallanus lacustris (Zoega, 1776). Vèstnik Ceskoslovenské Zoologické Spolecnosti 33, 15–33.Google Scholar
Mouritsen, K. N. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043–1050.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. and Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution 63, 448–458.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature, London 425, 480–484.CrossRefGoogle ScholarPubMed
Ponton, F., Lefevre, T., Lebarbenchon, C., Thomas, F., Loxdale, H. D., Marché, L., Renault, L., Perrot-Minnot, M. J. and Biron, D. G. (2006). Do distantly related parasites rely on the same proximate factors to alter the behaviour of their hosts? Proceedings of the Royal Society of London, B 273, 2869–2877.Google ScholarPubMed
Poulin, R. (1995). “Adaptive” changes in the behaviour of parasitized animals: A critical review. International Journal for Parasitology 25, 1371–1383.CrossRefGoogle ScholarPubMed
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.CrossRefGoogle Scholar
Poulin, R., Curtis, M. A. and Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behavior of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265–271.CrossRefGoogle Scholar
Pulkkinen, K., Pasternak, A. F., Hasu, T. and Valtonen, E. T. (2000). Effect of Triaenophorus crassus (Cestoda) infection on behavior and susceptibility to predation of the first intermediate host Cyclops strenuus (Copepoda). Journal of Parasitology 86, 664–670.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2005). Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889–894.CrossRefGoogle Scholar
Seppälä, O., Valtonen, E. T. and Benesh, D. P. (2008). Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society of London, B 275, 1611–1615.Google ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle ScholarPubMed
Tierney, J. F., Huntingford, F. A. and Crompton, D. W. T. (1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and antipredator behavior of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 46, 603–605.CrossRefGoogle Scholar
Van der Veen, I. T. and Kurtz, J. (2002). To avoid or eliminate: cestode infections in copepods. Parasitology 124, 465–474.CrossRefGoogle ScholarPubMed
Wedekind, C. and Milinski, M. (1996). Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? An experimental analysis of behavioural resistance. Parasitology 112, 371–383.CrossRefGoogle Scholar