Hostname: page-component-745bb68f8f-b6zl4 Total loading time: 0 Render date: 2025-01-11T04:42:04.334Z Has data issue: false hasContentIssue false
  • English
  • Français

Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience

Published online by Cambridge University Press:  06 October 2004

S. SHIRAKASHI  and
C. P. GOATER
S. SHIRAKASHI
Affiliation:
Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, Canada T1K 3M4 Present address: Fish Disease Laboratory, Department of Aquatic Organisms, University of Tokyo, Yayoe 1-1-1, Bunkyo, Tokyo, Japan 113-8657.
C. P. GOATER
Affiliation:
Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, Canada T1K 3M4
Get access Rights & Permissions [Opens in a new window]

Abstract

We monitored temporal changes in the magnitude of altered host behaviour in minnows (Pimephales promelas) experimentally infected with metacercariae of a brain-encysting trematode (Ornithodiplostomum ptychocheilus). This parasite develops and then encysts in a region of the brain that mediates the optomotor response (OMR), an innate behaviour that links visual stimuli with motor performance. The OMR of infected and uninfected minnows was evaluated between 0 and 10 weeks post-infection (p.i.), an interval spanning the development period of metacercariae to infectivity in birds. Trials involved monitoring the time an individual minnow spent following a spinning drum that had been painted with alternating black and white stripes. At 2 and 4 weeks p.i., infected minnows followed the drum 40% less often than controls. Differences between controls and infected fish declined thereafter, and were undetectable by 10 weeks p.i. Both control and infected fish habituated equally rapidly to the spinning drum. However, the difference in performance between controls and infected fish was 29% for experienced fish and 48% for fish that had never experienced the drum. Because maximum parasite-induced reduction in OMR coincided with the period of maximum parasite development, the behavioural effects are most likely due to unavoidable pathology in the brain associated with developing larvae.

Keywords

parasite-induced host behaviourfitnessrheotaxisoptomotorhost manipulation hypothesis
Type
Research Article
Information
Parasitology , Volume 130 , Issue 2 , February 2005 , pp. 177 - 183
Copyright
© 2005 Cambridge University Press

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

ANSTIS, S., HUTAHAJAN, P. & CAVANAGH, P. ( 1998). Optomotor test for wavelength sensitivity in guppyfish (Poecilia reticulata). Vision Research 38, 45–53.CrossRefGoogle Scholar
BARBER, I., HOARE, D. & KRAUSE, J. ( 2000). Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165.CrossRefGoogle Scholar
BETHEL, W. M. & HOLMES, J. C. ( 1974). Correlation of development of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host. Journal of Parasitology 60, 272–274.CrossRefGoogle Scholar
DE PEYSTER, A. & LONG, W. F. ( 1993). Fathead minnow optomotor response as a behavioral endpoint in aquatic toxicity testing. Bulletin of Environmental Contamination and Toxicology 51, 88–95.CrossRefGoogle Scholar
GUTHRIE, D. M. ( 1986). Role of vision in fish behaviour. In The Behaviour of Teleost Fishes ( ed. Pitcher, T. J.), pp. 111–121. Croom Helm, London.CrossRef
HENDRICKSON, G. L. ( 1979). Ornithodiplostomum ptychocheilus: migration to the brain of the fish intermediate host, Pimephales promelas. Experimental Parasitology 48, 245–258.CrossRefGoogle Scholar
KAVALIERS, M., COLWELL, D. D. & GALEA, L. A. M. ( 1995). Parasitic infection impairs spatial learning in mice. Animal Behaviour 50, 223–229.CrossRefGoogle Scholar
KORTRSCHAL, K., BRANDSTATTER, R., GOMAHR, A., JUNGER, K., PALZENBERGER, M. & ZAUNREITER, M. ( 1991). Brain and sensory systems. In Cyprinid Fishes: Systematics, Biology and Exploitation ( ed. Winfield, I. J. & Nelson, J. S.), pp. 284–331. Chapman and Hall, London.CrossRef
KVALSVIG, J. D. ( 1988). The effects of parasitic infection on cognitive performance. Parasitology Today 4, 206–208.CrossRefGoogle Scholar
LAFFERTY, K. D. & MORRIS, A. K. ( 1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.CrossRefGoogle Scholar
LEVRI, E. P. ( 1998). The influence of non-host predators on parasite-induced behavioural changes in a freshwater snail. Oikos 81, 531–537.CrossRefGoogle Scholar
LEVRI, E. P. & 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
MOORE, J. ( 2002). Parasites and the Behaviour of Animals. Oxford University Press, Oxford.
POULIN, R. ( 2000). Manipulation of host behaviour by parsasites: a weakening paradigm? Proceedings of the Royal Society, B 267, 787–792.Google Scholar
POULIN, R., BRODEUR, J. & MOORE, J. ( 1994). Parasite manipulation of host behaviour: should hosts always lose? Oikos 70, 479–484.Google Scholar
POULIN, R. & THOMAS, F. ( 1999). Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitology Today 15, 28–32.CrossRefGoogle Scholar
RADABAUGH, D. C. ( 1980). Encystment site selection in the brain inhabiting metacercariae of Ornithodiplostomum ptychocheilus (Trematoda: Strigeoidea). Journal of Parasitology 66, 183–184.CrossRefGoogle Scholar
ROBB, T. & REID, M. L. ( 1996). Parasite-induced changes in the behaviour of cestode-infected beetles: adaptation or simple pathology? Canadian Journal of Zoology 74, 1268–1274.Google Scholar
ROCK, I. & SMITH, D. ( 1986). The optomotor response and induced motion of the self. Perception 15, 497–502.CrossRefGoogle Scholar
ROCK, I., TAUBER, E. S. & HELLER, D. P. ( 1964). Perception of stroboscopic movement: evidence for its innate basis. Science 147, 1050–1052.Google Scholar
SANDLAND, G. J. & GOATER, C. P. ( 2000). Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows Pimephales promelas. Journal of Parasitology 86, 1056–1060.CrossRefGoogle Scholar
SANDLAND, G. J. & GOATER, C. P. ( 2001). Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows. Journal of Parasitology 87, 267–272.CrossRefGoogle Scholar
SANDLAND, G. J., GOATER, C. P. & DANYLCHUK, A. J. ( 2001). Population dynamics of Ornithodiplostumum ptychocheilus metacercariae in fathead minnows Pimephales promelas from 4 northern Alberta lakes. Journal of Parasitology 87, 744–748.CrossRefGoogle Scholar
SCHAERER, S. & NEUMEYER, C. ( 1996). Motion detection in goldfish investigated with the optomotor response is ‘color blind’. Vision Research 36, 4025–4034.CrossRefGoogle Scholar
SHAW, E. & TUCKER, A. ( 1965). The optomotor reaction of schooling carangid fishes. Animal Behaviour 13, 330–336.CrossRefGoogle Scholar
SHIRAKASHI, S. & GOATER, C. P. ( 2001). Brain-encysting parasites affect visually-mediated behaviours of fathead minnows. EcoScience 8, 289–293.CrossRefGoogle Scholar
SHIRAKASHI, S. & GOATER, C. P. ( 2002). Intensity-dependent alteration of minnow behaviour by a brain-encysting trematode. Journal of Parasitology 88, 1071–1074.CrossRefGoogle Scholar
SPRINGER, A. D., EASTER, S. S. & AGRANOFF, B. W. ( 1977). The role of the optic tectum in various visually mediated behaviors of goldfish. Brain Research 128, 393–404.CrossRefGoogle Scholar
TIERNEY, J. F., HUNTINGFORD, F. A. & CROMPTON, D. W. T. ( 1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 46, 603–605.CrossRefGoogle Scholar