Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-28T02:00:34.277Z Has data issue: false hasContentIssue false
  • English
  • Français

Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan

Published online by Cambridge University Press:  25 February 2008

D. P. BENESH ,
E. T. VALTONEN  and
O. SEPPÄLÄ
D. P. BENESH*
Affiliation:
Department of Biological and Environmental Science, POB 35, FI-40014University of Jyväskylä, Finland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, POB 35, FI-40014University of Jyväskylä, Finland
O. SEPPÄLÄ
Affiliation:
EAWAG, Swiss Federal Institute of Aquatic Science and Technology, and ETH-Zürich, Institute of Integrative Biology (IBZ), Überlandstrasse 133, PO Box 611, CH-8600, Dübendorf, Switzerland
*
*Corresponding author: Current address: Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306Plön, Germany. Tel: +49 45227 63258. Fax: +49 45227 63310. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Trophically-transmitted parasites frequently alter multiple aspects of their host's phenotype. Correlations between modified characteristics may suggest how different traits are mechanistically related, but these potential relationships remain unexplored. We recorded 5 traits from individual isopods infected with an acanthocephalan (Acanthocephalus lucii): hiding, activity, substrate colour preference, body (pereon) coloration, and abdominal (pleon) coloration. Infected isopods hid less and had darker abdominal coloration than uninfected isopods. However, in 3 different experiments measuring hiding behaviour (time-scales of observation: 1 h, 8 h, 8 weeks), these two modified traits were not correlated, suggesting they may arise via independent mechanisms. For the shorter experiments (1 h and 8 h), confidence in this null correlation was undermined by low experimental repeatability, i.e. individuals did not behave similarly in repeated trials of the experiment. However, in the 8-week experiment, hiding behaviour was relatively consistent within individuals, so the null correlation at this scale indicates, less equivocally, that hiding and coloration are unrelated. Furthermore, the difference between the hiding behaviour of infected and uninfected isopods varied over 8 weeks, suggesting that the effect of A. lucii infection on host behaviour changes over time. We emphasize the importance of carefully designed protocols for investigating multidimensionality in host manipulation.

Keywords

altered host phenotypeplastic/flexible behaviourrepeatabilityAsellus aquaticusAcanthocephalaintermediate hostisopod
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 5 , May 2008 , pp. 617 - 626
Copyright
Copyright © Cambridge University Press 2008

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

Andryuk, L. V. (1979). Developmental cycle of the thorny-headed worm, Acanthocephalus lucii (Echinorhynchidae). Parazitologiia 13, 530–539 (in Russian).Google Scholar
Amin, O. M., Burns, L. A. and Redlin, M. J. (1980). The ecology of Acanthocephalus parksidei (Acanthocephala: Echinorhynchidae) in its isopod intermediate host. Proceedings of the Helminthological Society of Washington 47, 37–46.Google Scholar
Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.CrossRefGoogle Scholar
Benesh, D. P. and Valtonen, E. T. (2007). Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies. Journal of Parasitology 93, 735–741.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
Brattey, J. (1986). Life history and population biology of larval Acanthocephalus lucii (Acanthocephala: Echinorhynchidae) in the isopod Asellus aquaticus. Journal of Parasitology 72, 633–645.CrossRefGoogle ScholarPubMed
Brown, S. P. (1999). Cooperation and conflict in host-manipulating parasites. Proceedings of the Royal Society of London, B 266, 1899–1904.CrossRefGoogle Scholar
Camp, J. W. and Huizinga, H. W. (1979). Altered color, behavior, and predation susceptibility of the isopod Asellus intermedius infected with Acanthocephalus dirus. Journal of Parasitology 65, 667–669.CrossRefGoogle Scholar
Cézilly, F. and Perrot-Minnot, M.-J. (2005). Studying adaptive changes in the behaviour of infected hosts: a long and winding road. Behavioural Processes 68, 223–228.CrossRefGoogle ScholarPubMed
Davies, S. J. and McKerrow, J. H. (2003). Developmental plasticity in schistosomes and other helminths. International Journal for Parasitology 33, 1277–1284.CrossRefGoogle ScholarPubMed
Dohm, M. R. (2002). Repeatability estimates do not always set an upper limit to heritability. Functional Ecology 16, 273–280.Google Scholar
Graca, M. A. S., Maltby, L. and Calow, P. (1993). Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus I: feeding strategies. Oecologia 96, 139–144.CrossRefGoogle Scholar
Hargeby, A., Johansson, J. and Ahnesjö, J. (2004). Habitat-specific pigmentation in a freshwater isopod: adaptive evolution over a small spatiotemporal scale. Evolution 58, 81–94.Google Scholar
Hargeby, A., Stoltz, J. and Johansson, J. (2005). Locally differentiated cryptic pigmentation in the freshwater isopod Asellus aquaticus. Journal of Evolutionary Biology 18, 713–721.CrossRefGoogle ScholarPubMed
Hasu, T., Holmes, J. C. and Valtonen, E. T. (2007). Isopod size and Acanthocephalus lucii infection. Journal of Parasitology 93, 450–457.CrossRefGoogle Scholar
Hetchtel, L. J., Johnson, C. L. and Juliano, S. A. (1993). Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus. Ecology 74, 710–713.CrossRefGoogle Scholar
Hindsbo, O. (1972). Effects of Polymorphus (Acanthocephala) on colour and behaviour of Gammarus lacustris. Nature, London 238, 333.CrossRefGoogle Scholar
Kuris, A. (1997). Host behavior modification: an evolutionary perspective. In Parasites and Pathogens, Effects on Host Hormones and Behavior (ed. Beckage, N. E.), pp. 231–245. Chapman and Hall, New York.Google Scholar
Lagrue, C. and Poulin, R. (2007). Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 1189–1195.CrossRefGoogle ScholarPubMed
Liang, K.-Y. and Zeger, S. L. (1986). Longitudinal data analysis using generalized linear models. Biometrika 73, 13–22.CrossRefGoogle Scholar
Lyndon, A. R. (1996). The role of acanthocephalan parasites in the predation of freshwater isopods by fish. In Aquatic Predators and their Prey (ed. Greenstreet, S. P. R. and Tasker, M. L.), pp. 26–32. Blackwell Scientific, Oxford.Google Scholar
Medoc, 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
Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000–1015.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, New York.CrossRefGoogle Scholar
Müller, R. and Büttner, P. (1994). A critical discussion of intraclass correlation coefficients. Statistics in Medicine 13, 2465–2476.CrossRefGoogle ScholarPubMed
Muzzall, P. M. and Rabalais, F. C. (1975). Studies on Acanthocephalus jacksoni Bullock, 1962 (Acanthocephala: Echinorhynchidae). III. The altered behavior of Lirceus lineatus (Say) infected with cystacanths of Acanthocephalus jacksoni. Proceedings of the Helminthological Society of Washington 42, 116–118.Google Scholar
Oetinger, D. F. and Nickol, B. B. (1981). Effects of acanthocephalans on pigmentation of freshwater isopods. Journal of Parasitology 67, 672–684.CrossRefGoogle Scholar
Piersma, T. and Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends in Ecology and Evolution 18, 228–233.CrossRefGoogle Scholar
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.CrossRefGoogle ScholarPubMed
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 2899–2903.Google Scholar
Poulin, R., Nichol, K. and Latham, A. D. M. (2003). Host sharing and host manipulation by larval helminthes in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425–433.CrossRefGoogle ScholarPubMed
Seidenberg, A. J. (1973). Ecology of the acanthocephalan, Acanthocephalus dirus (Van Cleave, 1931) in its intermediate host, Asellus intermedius Forbes (Crustacea: Isopoda). Journal of Parasitology 59, 957–962.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.CrossRefGoogle 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 London, B 273, 3039–3045.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
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387–390.CrossRefGoogle ScholarPubMed
Vizoso, D. B. and Ebert, D. (2005). Phenotypic plasticity of host-parasite interactions in response to the route of infection. Journal of Evolutionary Biology 18, 911–921.CrossRefGoogle Scholar
Wilson, K. and Grenfell, B. T. (1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle ScholarPubMed