Skip to main content
SpringerLink
Log in

Effects of parasites on fish behaviour: a review and evolutionary perspective

  • Published:
Reviews in Fish Biology and Fisheries Aims and scope Submit manuscript

Abstract

Fish serve as hosts to a range of parasites that are taxonomically diverse and that exhibit a wide variety of life cycle strategies. Whereas many of these parasites are passed directly between ultimate hosts, others need to navigate through a series of intermediate hosts before reaching a host in (or on) which they can attain sexual maturity. The realisation that parasites need not have evolved to minimise their impact on hosts to be successful, and in many cases may even have a requirement for their hosts to be eaten by specific predators to ensure transmission, has renewed interest in the evolutionary basis of infection-associated host behaviour. Fishes have proved popular models for the experimental examination of such hypotheses, and parasitic infections have been demonstrated to have consequences for almost every aspect of fish behaviour. Despite a scarcity of knowledge regarding the mechanistic basis of such behaviour changes in most cases, and an even lower understanding of their ecological consequences, there can be little doubt that infection-associated behaviour changes have the potential to impact severely on the ecology of infected fishes. Changes in foraging efficiency, time budget, habitat selection, competitive ability, predator-prey relationships, swimming performance and sexual behaviour and mate choice have all been associated with – and in some cases been shown to be a result of – parasite infections, and are reviewed here in some detail. Since the behavioural consequences of infections are exposed to evolutionary selection pressures in the same way as are other phenotypic traits, few behavioural changes will be evolutionarily neutral and host behaviour changes that facilitate transmission should be expected. Despite this expectation, we have found little conclusive evidence for the Parasite Increased Trophic Transmission (PITT) hypothesis in fishes, though recent studies suggest it is likely to be an important mechanism. Additionally, since the fitness consequences of the many behavioural changes described have rarely been quantified, their evolutionary and ecological significance is effectively unknown.

Potential hosts may also change their behaviour in the presence of infective parasite stages, if they adopt tactics to reduce exposure risk. Such `behavioural resistance', which may take the form of habitat avoidance, prey selectivity or avoidance of infected individuals, can be viewed as behavioural change associated with the threat of being parasitised, and so is included here. Actually harbouring infections may also stimulate fishes to perform certain types of simple or complex behaviours aimed at removing parasites, such as substrate scraping or the visitation of cleaning stations, although the efficacy of the latter as a parasite removal strategy is currently subject to a good deal of debate.

The effects parasites have on shoaling behaviour of host fish have attracted a good deal of attention from researchers, and we have provided a case study to summarise the current state of knowledge. Parasites have been shown to affect most of the antipredator effects of shoaling (such as vigilance, co-ordinated evasion and predator confusion) and can also impair an individual's foraging ability. It therefore seems unsurprising that, in a number of species avoidance of parasitised individuals has evolved which may explain the occurrence of parasite-assorted shoals in the field. Parasitised fish are found more often in peripheral shoal positions and show a reduced tendency for shoaling in some fish species. Given the array of host behaviours that may be changed, the fitness consequences of shoal membership for parasitised hosts and their parasites are not always easy to predict, yet an understanding of these is important before we can make predictions regarding the ecological impact of infections on host fish populations.

Clearly, there remain many gaps in our knowledge regarding the effects of parasites on the behaviour of host fish. We believe that a much greater understanding of the importance of infection-associated behaviour changes in fish could be gained from high quality research in comparatively few areas. We have completed our review by highlighting the key research topics that we believe should attract new research in this field.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ackman R.G. and Gjelstad R.T. (1975) Gas-chromatographic resolution of isomeric pentanols and pentanones in the identification of volatile alcohols and ketones in the codworm Terranova decipiens (Krabbe, 1878). Anal. Biochem. 67, 684–687.

    Google Scholar 

  • Adams C.E., Brown D.W. and Keay L. (1994) Elevated predation pressure associated with inshore migrations of fish in a large lake, Loch Lomond, Scotland. Hydrobiologia 290, 135–138.

    Google Scholar 

  • Alexander R.D. (1974) The evolution of social behaviour. Ann. Rev. Ecol. Syst. 5, 325–383.

    Google Scholar 

  • Anderson R.M. (1994) Epidemiology. In: Cox F.E.G. (ed.), Modern Parasitology, 3rd Edition. Blackwell Scientific Publications, Oxford, pp. 75–116.

    Google Scholar 

  • Andersson M. (1994) Sexual Selection. Princeton University Press, Princeton, New Jersey, 599 pp.

    Google Scholar 

  • Arme C. (1968) Effects of the plerocercoid larvae of a pseudophyllidean cestode, Ligula intestinalis, on the pituitary gland and gonads of its host. Biol. Bull. 134, 15–25.

    Google Scholar 

  • Arme C. and Owen R.W. (1967) Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus with special reference to pathological effects. Parasitology 57, 301–304.

    Google Scholar 

  • Arme C. and Owen R.W. (1968) Occurrence and pathology of Ligula intestinalis infections in British fishes. J Parasitol. 54, 272–280.

    Google Scholar 

  • Ashworth J.H. and Bannerman J.C.W. (1927) On a tetracotyle (T. phoxini) in the brain of the minnow. Trans. Roy. Soc. Edin. 55, 159–171

    Google Scholar 

  • Baldwin N.L., Millemann R.E. and Knapp S.E. (1967) “Salmon poisoning” disease. III. Effect of experimental Nanophyetus salmonicola infection on the fish host. J. Parasitol. 53, 556–564.

    Google Scholar 

  • Balling T.E. and Pfeiffer W. (1997) Location-dependent infection of fish parasites in Lake Constance. J. Fish Biol. 51, 1025–1032.

    Google Scholar 

  • Barber I. (1997) A non-invasive morphometric technique to estimate the cestode plerocercoid load of small freshwater fishes. J. Fish Biol. 51, 654–658.

    Google Scholar 

  • Barber I. and Crompton D.W.T. (1997) The distribution of Diplostomum phoxini metacercariae (Trematoda) in the brain of minnows (Phoxinus phoxinus) Fol. Parasitol. 44, 19–25.

    Google Scholar 

  • Barber I. and Huntingford F.A. (1995) The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132, 1223–1240.

    Google Scholar 

  • Barber I. and Huntingford F.A. (1996) Parasite infection impairs schooling behaviour: spatial deviance of helminth-infected minnows in conspecific groups. Proc. R. Soc. Lond. Ser. B. 263, 1095–1102.

    Google Scholar 

  • Barber I. and Ruxton G.D. (1998) Temporal prey distribution affects the competitive ability of parasitised sticklebacks. Anim. Behav. 58, 1477–1483.

    Google Scholar 

  • Barber I. Huntingford F.A. and Crompton D.W.T. (1995) The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish. J. Fish Biol. 47, 524–536.

    Google Scholar 

  • Barber I., Downey L.C. and Braithwaite V.A. (1998) Parasitism, oddity and the mechanism of shoal choice. J. Fish Biol. 52, 1365–1368.

    Google Scholar 

  • Barnard C.J. (1990) Parasitic Relationships. In: Barnard C.J. and Behnke J.M. (eds.), Parasitism and Host Behaviour. Taylor and Francis, London, UK, pp. 1–33.

    Google Scholar 

  • Bean C.W. and Winfield I.J. (1989) Biological and ecological effects of a Ligula intestinalis (L.) infestation of the gudgeon, Gobio gobio (L.), in Lough Neagh, Northern Ireland. J. Fish Biol. 34, 135–147.

    Google Scholar 

  • Bean C.W. and Winfield I.J. (1992) Influences of the tapeworm Ligula intestinalis (L.) on the spatial distributions of juvenile roach Rutilus rutilus (L.) and Gudgeon Gobio gobio (L.) in Lough Neagh, Northern Ireland. Neth. Jnl. Zool. 42, 416–423.

    Google Scholar 

  • Beaver P.C. (1939) The morphology and life history of Psilostomum ondatrae Price, 1931 (Trematoda: Psilostomidae) J. Parasitol. 25, 383.

    Google Scholar 

  • Begon M., Harper J.L. and Townsend C.R. (1990) Ecology: Individuals, Populations and Communities, 2nd edition. Blackwell Scientific Publications, Boston, MA, 945 pp.

    Google Scholar 

  • Blake M.A. and Hart P.J.B. (1995) The vulnerability of juvenile signal crayfish to perch and eel predation. Freshwater Biol. 33, 233–244.

    Google Scholar 

  • Blake R.W. (1983) Fish Locomotion. Cambridge University Press, Cambridge, 208 pp.

    Google Scholar 

  • Bleckmann H. (1993) Role of the lateral line in fish behaviour. In: Pitcher T.J. ed. Behaviour of Teleost Fishes. Chapman and Hall, London, pp. 201–246.

    Google Scholar 

  • Bone Q., Marshall N.B. and Blaxter J.H.S. (1995) Biology of Fishes, 2nd edition. Chapman and Hall, London, 332 pp.

    Google Scholar 

  • Brassard P., Rau M.E. and Curtis M.A. (1982) Parasite-induced susceptibility to predation in diplostomoiasis. Parasitology 85, 495–501.

    Google Scholar 

  • Brønseth T. and Folstad I. (1997) The effect of parasites on courtship dance in threespine sticklebacks: more than meets the eye? Can. J. Zool. 75, 589–594

    Google Scholar 

  • Brown C.R. and Brown M.B. (1986) Ectoparasitism as a cause of natal dispersal in cliff swallows. Ecology 67, 1206–1218.

    Google Scholar 

  • Brown J.A. and Colgan P.W. (1986) Individual and species recognition in centrarchid fishes: evidence and hypotheses. Behav. Ecol. Sociobiol. 19, 373–379.

    Google Scholar 

  • Brown G.E. and Smith R.J.F. (1994) Fathead minnows use chemical cues to discriminate natural shoalmates from unfamiliar conspecifics. J. Chem. Ecol. 20, 3051–3061.

    Google Scholar 

  • Butler J.A. and Millemann R.E. (1971) Effect of the "salmon poisoning" trematode, Nanophyetus salmonicola, on the swimming ability of juvenile salmonid fishes. J. Parasitol. 57, 860–865.

    Google Scholar 

  • Chappell L.H., Hardie L.J. and Secombes C.J. (1994) Diplostomiasis: the disease and host-parasite interactions. In: Pike A.W. and Lewis J.W. eds. Parasitic Diseases of Fish. Samara Publishing, Dyfed, Wales, pp. 59–86.

  • Christiansen R., Glette J., Lie Ø., Torrissen O.J. and Waagbø R. (1995) Antioxidant status and immunity in Atlantic salmon, Salmo salar L., fed semi-purified diets with and without astaxanthin supplementation. J. Fish Dis. 18, 317–328.

    Google Scholar 

  • Coble D.W. (1970) Vulnerability of fathead minnows infected with yellow grub to largemouth bass predation. J. Parasitol. 56, 395–396.

    Google Scholar 

  • Coleman F.C. (1993) Morphological and physiological consequences of parasites encysted in the bulbus arteriosus of an estuarine fish, the sheepshead minnow, Cyprinodon variegatus. J. Parasitol. 79, 247–254.

    Google Scholar 

  • Combes C. (1991) Ethological aspects of parasite transmission. Am. Nat. 138, 866–880.

    Google Scholar 

  • Combes C. (1996) Parasites, biodiversity and ecosystem stability. Biodiv. Cons. 5, 953–962.

    Google Scholar 

  • Costello M.J. (1996) Development and future of cleaner-fish technology and other biological control techniques in fish farming. In: Sayer, M.D.J. Treasurer, J.W. and Costello, M.J. (eds.), Wrasse Biology and Use in Aquaculture. Fishing News Books, Oxford, pp. 171–184.

    Google Scholar 

  • Cote I.M. and Gross M.R. (1993) Reduced disease in offspring - a benefit of coloniality in sunfish. Behav. Ecol. Sociobiol. 33, 269–274.

    Google Scholar 

  • Cote I.M. and Poulin R. (1995) Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. Sociobiol. 95, 159–165.

    Google Scholar 

  • Cowell L.E., Watanabe W.O., Head W.D., Grover J.J. and Sheaker J.M. (1993) Use of tropical cleanerfish to control the ectoparasite Neobenedenia melleni (Monogenea, Capsalidae) on seawatercultured Florida red tilapia. Aquaculture 113, 189–200.

    Google Scholar 

  • Cox F.E.G. (1994) Immunology. In: Cox, F.E.G. (ed.), Modern Parasitology, 3rd Edition. Blackwell Scientific Publications, Oxford, pp. 193–218.

    Google Scholar 

  • Crowden A.E. (1976) Diplostomum spathaceum in the Thames; occurrence and effects on fish behaviour. Parasitology 73, vii.

    Google Scholar 

  • Crowden A.E. and Broom D.M. (1980) Effects of the eyefluke, Dipostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus) Anim. Behav. 28, 287–294.

    Google Scholar 

  • Cunningham E.J. Tierney J.F. and Huntingford F.A. (1994) Effects of the cestode Schistocephalus solidus on food intake and foraging decisions in the three-spined stickleback Gasterosteus aculeatus. Ethology 79, 65–75.

    Google Scholar 

  • Cusack R. and Cone D.H. (1986) Gyrodactylus salmonis (Yin and Sproston, 1948) parasitising fry of Salvelinus fontinalis (Mitchill) J. Wildlife Disease 22, 209–213.

    Google Scholar 

  • Dawkins R. (1982) The Extended Phenotype. Oxford University Press, Oxford.

    Google Scholar 

  • Dawkins R. and Krebs J.R. (1979) Arms races between and within species. Proc. Roy. Soc. Lond. B. 205, 489–511.

    Google Scholar 

  • Dence W.A. (1958) Studies on Ligula-infected common shiners (Notropis cornutus frontinalis Agassiz) in the Adirondacks. J. Parasitol. 44, 334–338.

    Google Scholar 

  • Dobson A.P. (1988) The population biology of parasite-induced changes in host behaviour. Quart. Rev. Biol. 63, 139–165.

    Google Scholar 

  • Dugatkin L.A. FitzGerald G.J. and Lavoie J. (1994) Juvenile threespined sticklebacks avoid parasitised conspecifics. Env. Biol. Fishes 39, 215–218.

    Google Scholar 

  • Fitzgerald G.J. and Morissette J. (1992) Kin recognition and choice of shoalmates by threespine sticklebacks. Ethol. Ecol. Evol. 4, 273–283.

    Google Scholar 

  • Folstad I. and Karter A.J. (1992) Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603–622.

    Google Scholar 

  • Forbes M.R.L. (1993) Parasitism and host reproductive effort. Oikos 67, 444–450.

    Google Scholar 

  • Freeland W.J. (1977) Blood sucking flies and primate polyspecific associations. Nature 269, 801–802.

    Google Scholar 

  • Gaten E. (1987) Aggregation of the eyefluke Diplostomum spathaceum (Digenea: Diplostomatidae) in the lenses of various species of fish. J. Fish Diseases 10, 69–74.

    Google Scholar 

  • Gilbertson L.G. (1979) Variation and natural selection in an Alaskan population of the threespine stickleback (Gasterosteus aculeatus L.) PhD thesis, University of Washington, Seattle.

    Google Scholar 

  • Giles N. (1983) Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 31, 1192–1194.

    Google Scholar 

  • Giles N. (1987a) A comparison of the behavioural responses of parasitised and non-parasitised three-spined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia. J. Fish Biol. 30, 631–638.

    Google Scholar 

  • Giles N. (1987b) Predation risk and reduced foraging activity in fish: experiments with parasitised and non-parasitised three-spined sticklebacks, Gasterosteus aculeatus. J. Fish Biol. 31, 37–44.

    Google Scholar 

  • Godin J.-G.J. and Sproul C.D. (1988) Risk taking in parasitised sticklebacks under threat of predation: effects of energetic need and food availability. Can. J. Zool. 66, 2360–2367.

    Google Scholar 

  • Gorlick D.L., Atkins P.D. and Losey G.S. (1978) Cleaning stations as water holes, garbage dumps, and sites for the evolution of reciprocal altruism? Am. Nat. 112, 341–353.

    Google Scholar 

  • Gray J.A.B. and Denton E.J. (1991) Fast pressure pulses and communication between fish. J.M.B.A. 71, 83–106.

    Google Scholar 

  • Grutter A.S. (1996) Experimental demonstration of no effect by the cleaner wrasse Labroides dimidiatus (Cuvier and Valenciennes) on the host fish Pomacentrus moluccensis (Bleeker) J. Exp. Mar. Biol. Ecol. 196, 285–298.

    Google Scholar 

  • Guthrie D.M. and Muntz W.R.A. (1993) Role of vision in fish behaviour. In: Pitcher T.J. (ed.), Behaviour of Teleost Fishes. Chapman and Hall, London, pp. 89–128.

    Google Scholar 

  • Guthrie J.F. and Kroger R.L. (1974) Schooling habits of injured and parasitised menhaden. Ecology 55, 208–210.

    Google Scholar 

  • Gwinner H., Oltrogge M., Trost L. and Nienaber U. (2000) Green plants in starling nests: effects on nestlings. Anim. Behav. 59, 301–309.

    Google Scholar 

  • Hakkarainen H., Ilmonen P., Koivunen V. and Korpimaki E. (1998) Blood parasites and nest defense behaviour of Tengmalm's owls. Oecologia 114, 574–577.

    Google Scholar 

  • Hamilton W.D. (1971) Geometry for the selfish herd. J. Theor. Biol. 31, 295–311.

    Google Scholar 

  • Hamilton W.D. and Zuk M. (1982) Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.

    Google Scholar 

  • Hamilton W.J. and Poulin R. (1995) Parasites, aggression and dominance in male upland bullies. J. Fish Biol. 47, 302–307.

    Google Scholar 

  • Hamilton W.J. and Poulin R. (1997) The Hamilton and Zuk hypothesis revisited: a meta-analytical approach. Behaviour 134, 299–320.

    Google Scholar 

  • Harris M.T. and Wheeler A. (1974) Ligula infestation of bleak Alburnus alburnus (L.) in the tidal Thames. J. Fish Biol. 6, 181–188.

    Google Scholar 

  • Hart B. (1990) Behavioural adaptations to pathogens and parasites: five strategies. Neuro. Biobehav. Rev. 14, 273–294.

    Google Scholar 

  • Hart B. (1994) Behavioural defense against parasites: interaction with parasite invasiveness. Parasitol. 109, S139–S151.

    Google Scholar 

  • Hasson, O. (1990) The role of amplifiers in sexual selection - an integration of the amplifying and the Fisherian mechanism. Evol. Ecol. 4, 277–289.

    Google Scholar 

  • Hawkins A.D. (1993) Underwater sound and fish behaviour. In: Pitcher T.J. (ed.), Behaviour of Teleost Fishes. Chapman and Hall, London, pp. 129–169.

    Google Scholar 

  • Helluy S.M. and Holmes J.C. (1990) Serotonin, octopamine and the clinging behaviour induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea) Can. J. Zool. 68, 1214–1220.

    Google Scholar 

  • Herting G.E. and Witt A. (1967) The role of physical fitness of forage fishes in relation to their vulnerability to predation by bowfin (Amia calva) Trans. Am. Fish. Soc. 96, 427–430.

    Google Scholar 

  • Hillgarth N. (1996) Ectoparasite transfer during mating in ringnecked pheasants Phasianus colchicus. J. Avian. Biol. 27, 260–262.

    Google Scholar 

  • Hoare D.J., Ruxton G.D., Godin J-.G.J. and Krause J. (2000) The social organization of free-ranging fish shoals. Oikos 89, 546–554.

    Google Scholar 

  • Holmes J.C. and Bethel W.M. (1972) Modification of intermediate host behaviour by parasites. In: Canning E.U. and Wright C.A. (eds.), Behavioural Aspects of Parasite Transmission. Academic Press, London, U.K., pp. 123–149.

    Google Scholar 

  • Holmes J.C. and Zohar S. (1990) Pathology and host behaviour. In: Barnard C.J. and Behnke J.M. (eds.), Parasitism and Host Behaviour. Taylor and Francis, London, U.K., pp. 193–229.

    Google Scholar 

  • Hoogenboom I. and Dijkstra C. (1987) Sarcocystis cernae: A parasite increasing the risk of predation of its intermediate host, Microtus arvalis. Oecologia 74, 86–92.

    Google Scholar 

  • Hoogland J.L. (1979) Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys sp.) coloniality. Behav. 69, 1–35.

    Google Scholar 

  • Hoogland R., Morris D. and Tinbergen N. (1957) The spines of sticklebacks (Gasterosteus and Pygosteus) as a means of defence against predators (Perca and Esox) Behaviour 10, 205–236.

    Google Scholar 

  • Jakobsen P.J. Johnsen G.H. and Larsson P. (1988) Effects of predation risk and parasitism on the feeding ecology, habitat use, and abundance of lacustrine threespine stickleback (Gasterosteus aculeatus) Can. J. Fish. Aq. Sci. 45, 426–431.

    Google Scholar 

  • Jönsson E., Johnsson J.I. and Thrandur Bjornsson B. (1996) Growth hormone increases predation exposure of rainbow trout. Proc. R. Soc. Lond. B. 263, 647–651.

    Google Scholar 

  • Jönsson E., Johnsson J.I. and Thrandur Bjornsson B. (1998) Growth hormone increases risk-taking in foraging rainbow trout. Ann. New York Acad. Sci. 839, 636–638.

    Google Scholar 

  • Kearn G.C. (1986) The eggs of monogeneans. Adv. Parasitol. 25, 175–273.

    Google Scholar 

  • Kennedy C.E.J., Endler J.A., Poynton S.L. and McMinn H. (1987) Parasite load predicts mate choice in guppies. Behav. Ecol. Sociobiol. 21, 291–295.

    Google Scholar 

  • Kennedy C.R. (1974) A checklist of British and Irish freshwater fish parasites with notes on their distribution. J. Fish Biol. 6, 613–644.

    Google Scholar 

  • Keymer A.D. and Read A.F. (1991) Behavioural ecology: the impact of parasitism. In: Toft C.A., Aeschliman A. and Bolis L. (eds.), Parasite-Host Associations: Coexistance or Conflict? Oxford University Press, Oxford, pp. 37–61.

    Google Scholar 

  • Klein W.D. Olsen O.W. and Bowden D.C. (1969) Effects of intestinal fluke, Crepidostomum farionis, on rainbow trout, Salmo gairdnerii. Trans. Am. Fish. Soc. 98, 1–6.

    Google Scholar 

  • Kramer D.L., Manley D. and Bourgeois R. (1983) The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes. Can. J. Zool. 61, 653–665.

    Google Scholar 

  • Krause J. (1993) The relationship between foraging and shoal position in a mixed shoal of roach (Rutilus rutilus) and chub (Leuciscus cephalus): a field study. Oecologia 93, 356–359.

    Google Scholar 

  • Krause J. (1994a) Differential fitness returns in relation to spatial position within groups. Biol. Rev. 69, 187–206.

    Google Scholar 

  • Krause J. (1994b) The influence of food competition and predation risk on size-assortative shoaling in juvenile chub (Leuciscus cephalus). Ethology 96, 105–116.

    Google Scholar 

  • Krause J. and Godin J.-G.J. (1994a) Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanus. Can. J. Zool. 72, 1775–1779.

    Google Scholar 

  • Krause J. and Godin J.-G.J. (1994b) Shoal choice in the banded killi-fish (Fundulus diaphanous, Teleostei, Cyprinodontidae): effects of predation risk, fish size, species composition, and size of shoals. Ethology 98, 128–136.

    Google Scholar 

  • Krause J. and Godin J.-G.J. (1996) Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanous, Teleostei, Cyprinodontidae). Ethology 102, 40–49.

    Google Scholar 

  • Krause J., Godin J.-G.J. and Brown D. (1996) Phenotypic variability within and between fish shoals. Ecology 77, 1586–1591.

    Google Scholar 

  • Krause J., Godin J.-G.J. and Brown D. (1998) Body size variation among multi-species fish shoals: the effects of shoal size and number of species. Oecologia 114, 67–72.

    Google Scholar 

  • Krause J., Ruxton G.D. and Godin J.-G.J. (1999) Parasite load and prevalence in fish shoals: is there evidence for parasiteassortative shoaling behaviour? J. Anim.Ecol. 68, 27–33.

    Google Scholar 

  • Kreirer J.P. and Baker J.R. (1987) Parasitic Protozoa. Allen and Unwin, Boston, 241 pp.

    Google Scholar 

  • Lafferty K.D. (1992) Foraging on prey that are modified by parasites. Am. Nat. 140, 854–867.

    Google Scholar 

  • Lafferty K.D. (1999) The evolution of trophic transmission. Parasitol. Today 15, 111–115.

    Google Scholar 

  • Lafferty K.D. and Morris A.K. (1996) Altered behaviour of parasitised killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.

    Google Scholar 

  • Landeau L. and Terborgh J. (1986) Oddity and the 'confusion effect' in predation. Anim. Behav. 34, 1372–1380.

    Google Scholar 

  • Lemly A.D. and Esch G.W. (1984) Effects of the trematode Uvulifer ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. J. Parasitol. 70, 475–492.

    Google Scholar 

  • Lester R.J.G. (1971) The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behavior of the fish. Can. J. Zool. 49, 361–366.

    Google Scholar 

  • Lester R.S.G. and Adams J.R. (1974) Gyrodactylus alexanderi: reproduction, mortality, and effect on its host Gasterosteus aculeatus. Can J. Zool. 52, 827–833.

    Google Scholar 

  • LoBue C.P. and Bell M.A. (1993) Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the threespine stickleback. Am. Nat. 142, 725–735.

    Google Scholar 

  • Lozano G.A. (1991) Optimal foraging theory: a possible role for parasites. Oikos 60, 391–395.

    Google Scholar 

  • MacKenzie K. and Longshaw M. (1995) Parasites of the hakes Merluccius australis and Merluccius hubbsi in the waters around the Falkland Islands, Southern Chile, and Argentina, with an assessment of their potential value as biological tags. Can. J. Fish. Aq. Sci. 52, 213–224.

    Google Scholar 

  • MacKenzie K., Williams H.H., Williams B., McVicar A.H. and Siddall R (1995) Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv. Parasitol. 35, 85–144.

    Google Scholar 

  • Magurran A.E. (1990) The adaptive significance of schooling as an anti-predator defence in fish. Ann. Zool. Fenn. 27, 51–66.

    Google Scholar 

  • Magurran A.E., Oulton W. and Pitcher T.J. (1985) Vigilant behaviour and shoal size in minnows. Z. Tierpsychol. 67, 167–178.

    Google Scholar 

  • Magurran A.E., Seghers B.H., Shaw P.W. and Carvalho G.R. (1994) Schooling preferences for familiar fish in the guppy, Poecilia reticulata. J. Fish Biol. 45, 401–406.

    Google Scholar 

  • Margolis L., Esch G.W., Holmes J.C., Kuris A.M. and Schad G.A. (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists) J. Parasitol. 68, 131–133.

    Google Scholar 

  • Markiw M.E. (1992) Salmonid whirling disease. US Fisheries and Wildlife Service Leaflet 17. Washington, DC.

  • Mathis A. and Smith R.J.F. (1993) Chemical labelling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas). J. Chem. Ecol. 19, 1967–1979.

    Google Scholar 

  • May R.M. and Anderson R.M. (1979) Population biology of infectious disease. Nature 280, 455–461.

    Google Scholar 

  • Maynard B.J., deMartini L. and Wright W.G. (1996) Gammarus lacustris harboring Polymorphus paradoxus show altered patterns of serotonin-like immunoreactivity. J. Parasitol. 82, 663–666.

    Google Scholar 

  • McClelland G. (1995) Experimental infection of fish with larval sealworm, Pseudoterranova decipiens (Nematoda, Aniskinae), transmitted by amphipods. Can. J. Fish. Aquat. Sci. 52, 140–155.

    Google Scholar 

  • McPhail J.D. and Peacock S.D. (1983) Some effects of the cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus): evolutionary aspects of a host-parasite interaction. Can. J. Zool. 61, 901–908.

    Google Scholar 

  • Meakins R.H. and Walkey M. (1975) The effects of parasitism by the plerocercoid of Schistocephalus solidus Muller, 1776 (Pseudophyllidea) on the respiration of the three-spined stickleback, Gasterosteus aculeatus. J. Fish Biol. 7, 817–824.

    Google Scholar 

  • Metcalfe N.B. and Thomson B.C. (1995) Fish recognize and prefer to shoal with poor competitors. Proc. Roy. Soc. Lond., Ser. B 259, 207–210.

    Google Scholar 

  • Milinski M. (1982) Optimal foraging: the influence of intraspecific competition on diet selection. Behav. Ecol. Sociobiol. 11, 109–115.

    Google Scholar 

  • Milinski M. (1984) Parasites determine a predator's optimal feeding strategy. Behav. Ecol. Sociobiol. 15, 35–370.

    Google Scholar 

  • Milinski M. (1985) Risk of predation of parasitised sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93, 203–216.

    Google Scholar 

  • Milinski M. (1990) Parasites and host decision-making. In: Barnard C.J. and Behnke J.M. (eds.), Parasitism and Host Behaviour. Taylor and Francis, London, pp. 95–116.

    Google Scholar 

  • Milinski M. and Bakker T.C.M. (1990) Female sticklebacks use male colouration in mate choice and hence avoid parasitised males. Nature, Lond. 344, 330–333.

    Google Scholar 

  • Milinski M., Kulling D. and Kettler R. (1990) Tit for tat: sticklebacks trusting a cooperating partner. Behav. Ecol. 1, 7–11.

    Google Scholar 

  • Minchella D.J. (1985) Host life-history variation in response to parasitism. Parasitology 90, 205–216.

    Google Scholar 

  • Moles A. and Heifetz J. (1998) Effects of the brain parasite Myxobolus arcticus on sockeye salmon. J. Fish Biol. 52(1), 146–151.

    Google Scholar 

  • Møller A.P. (1994) Parasite infestation and parental care in the barn swallow Hirundo rustica - a test of the resource-provisioning model of parasite-mediated sexual selection. Ethology 97, 215–225.

    Google Scholar 

  • Moody J. and Gaten E. (1982) The population dynamics of eyeflukes Diplostomum spathaceum and Tylodelphys clavata (Digenea: Diplostomatidae) in rainbow and brown trout in Rutland Water: 1974-1978. Hydrobiologia 88, 207–209.

    Google Scholar 

  • Moore J. (1983) Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000–1015.

    Google Scholar 

  • Moore J. (1995) The behaviour of parasitized animals. BioScience 45, 89–96.

    Google Scholar 

  • Moore J. and Gotelli N.J. (1990) A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In: Barnard C.J. and Behnke J.M. (eds.), Parasitism and Host Behaviour. Taylor and Francis, London, U.K., pp. 193–229.

    Google Scholar 

  • Moore J., Simberloff D. and Freehling M. (1988) Relationships between bobwhite quail social-group size and intestinal helminth parasitism. Am. Nat. 131, 22–32.

    Google Scholar 

  • Mooring M.S. and Hart B.L. (1992) Animal grouping for protection from parasites: selfish herd and encounter dilution effects. Behaviour 123, 173–193.

    Google Scholar 

  • Nelson W.A., Keirans J.E., Bell J.F. and Clifford C.M. (1975) Hostectoparasite relationships.J. Med. Entomol. 12, 143–166.

    Google Scholar 

  • Ness J.H. and Foster S.A. (1999) Parasite-associated phenotype modifications in threespine stickleback. Oikos 85, 127–134.

    Google Scholar 

  • Olson V.A. and Owens I.P.F. (1998) Costly sexual signals: are carotenoids rare, risky or required? TREE 13, 510–514.

    Google Scholar 

  • Orr T.S.C. and Hopkins C.A. (1969) Maintenance of Schistocephalus solidus in the laboratory with observation on the rate of growth of, and proglottid formation in, the plerocercoid. J. Fish. Res. Bd. Can. 26, 741–752.

    Google Scholar 

  • Owen S.F. Barber I. and Hart P.J.B. (1993) Low level infection by eyefluke, Diplostomum spp. affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J. Fish Biol. 42, 803–806.

    Google Scholar 

  • Partridge B.L. and Pitcher T.J. (1980) The sensory basis of fish schools: relative roles of lateral line and vision. J. comp. Physiol. 135A, 315–325.

    Google Scholar 

  • Pascoe D and Mattey D. (1977) Dietary stress in parasitised and non-parasitised Gasterosteus aculeatus L. Z. Parasitkd. 51, 179–186.

    Google Scholar 

  • Pasternak A.F., Huntingford F.A. and Compton D.W.T. (1995) Changes in metabolism and behaviour of the fresh-water copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110, 395–399.

    Google Scholar 

  • Pitcher T.J. and Parrish J.K. (1993) Functions of shoaling behaviour in teleosts. In: Pitcher T.J. (ed.), Behaviour of Teleost Fishes. Chapman and Hall, London, pp. 363–439.

    Google Scholar 

  • Poulin R. (1991a) Group-living and the richness of the parasite fauna in Canadian freshwater fishes. Oecologia 86, 390–394.

    Google Scholar 

  • Poulin R. (1991b) Group-living and infestation by ectoparasites in passerines. Condor 93, 418–423.

    Google Scholar 

  • Poulin R. (1992) Toxic pollution and parasitism in freshwater fish. Parasitol. Today 8, 58–61.

    Google Scholar 

  • Poulin R. (1993a) Age-dependent effects of parasites on antipredator responses in two New Zealand freshwater fish. Oecologia 96, 431–438.

    Google Scholar 

  • Poulin R. (1993b) A cleaner perspective on cleaning symbiosis. Rev. Fish Biol. Fish. 3, 75–79.

    Google Scholar 

  • Poulin R. (1994a) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.

    Google Scholar 

  • Poulin R. (1994b) Mate choice decisions by parasitized female upland bullies, Gobiomorphus breviceps. Proc. Roy. Soc. Lond. B. 256, 183–187.

    Google Scholar 

  • Poulin R. (1995) 'Adaptive' changes in the behaviour of parasitised animals: a critical review. Int. J. Parasitol. 25, 1371–1383.

    Google Scholar 

  • Poulin R. (1998) Evolutionary Ecology of Parasites: from Individuals to Communities. Chapman and Hall, London, 212 pp.

    Google Scholar 

  • Poulin R. and FitzGerald G.J. (1987) The potential of parasitism in the structuring of a salt marsh stickleback community. Can. J. Zool. 65, 2793–2798.

    Google Scholar 

  • Poulin R. and FitzGerald G.J. (1988) Water temperature, vertical distribution, and risk of ectoparasitism in juvenile sticklebacks. Can. J. Zool. 66, 2002–2005.

    Google Scholar 

  • Poulin R. and FitzGerald G.J. (1989a) Shoaling as an antiectoparasitic mechanism in juvenile sticklebacks (Gasterosteus spp.). Behav. Ecol. Sociobiol. 24, 251–255.

    Google Scholar 

  • Poulin R. and FitzGerald G.J. (1989b) A possible explanation for the aggregated distribution of Argulus Canadensis Wilson, 1916 (Crustacea: Branchiura) on juvenile sticklebacks (Gasterosteidae). J. Parasitol. 75, 58–60.

    Google Scholar 

  • Poulin R. and FitzGerald G.J. (1989c) Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can. J. Zool. 67, 14–18.

    Google Scholar 

  • Poulin R. and Grutter A.S. (1996) Cleaning symbioses: Proximate and adaptive explanations. Bioscience 46, 512–517.

    Google Scholar 

  • Poulin R. and Vickery W.L. (1996) Parasite mediated sexual selection: Just how choosy are parasitized females? Behav. Ecol. Sociobiol. 38, 43–49.

    Google Scholar 

  • Poulin R., Brodeur J. and Moore J. (1994) Parasite manipulation of host behaviour - should hosts always lose? Oikos 70, 479–484.

    Google Scholar 

  • Radabaugh D.C. (1980) Changes in minnow, Pimephales promelas Rafinesque, schooling behaviour associated with infections of brain-encysted larvae of the fluke, Ornithodiplostomum ptychocheilus. J. Fish Biol. 16, 621–628.

    Google Scholar 

  • Ranta E. (1992) Gregariousness versus solitude: another look at parasite faunal richness in Canadian freshwater fishes. Oecologia 89, 150–152.

    Google Scholar 

  • Ranta E. (1995) Schistocephalus infestation improves prey-size selection by three-spined sticklebacks, Gasterosteus aculeatus. J. Fish Biol. 46, 156–158.

    Google Scholar 

  • Ranta E., Lindstrom K. and Peukuri N. (1992) Size matters when 3-spined sticklebacks go to school. Anim. Behav. 43, 160–162.

    Google Scholar 

  • Ranta E., Rita H. and Lindstrom K. (1993) Competition versus cooperation: success of individuals foraging alone and in groups. Am Nat. 142, 42–58.

    Google Scholar 

  • Ratanarat-Brockelman C. (1974) Migration of Diplostomum spathaceum (Trematoda) in the fish intermediate host. Z. Parasitenkunde 43, 123–134.

    Google Scholar 

  • Rau M.E. and Caron F.R. (1979) Parasite-induced susceptibility of moose to hunting. Can. J. Zool. 57, 2466–2468.

    Google Scholar 

  • Read A.F. (1990) Parasites and the evolution of host sexual behaviour. In: Barnard C.J. and Behnke J.M. (eds.), Parasitism and Host Behaviour. Taylor and Francis, London, pp. 95–116.

    Google Scholar 

  • Reebs S.G. and Saulnier N. (1997) The effect of hunger on shoal choice in golden shiners (Pisces: Cyprinidae, Notemigonus crysoleucas). Ethology 103, 642–652.

    Google Scholar 

  • Rees G. (1955) The adult and Diplostomulum stage (Diplostomulum phoxini (Faust)) of Diplostomum pelmatoides Dubois and an experimental demonstration of part of the life cycle. Parasitology 45, 295–311.

    Google Scholar 

  • Reimchen T.E. (1982) Incidence and intensity of Cyathocephalus truncates and Schistocephalus solidus infection in Gasterosteus aculeatus. Can. J. Zool. 60, 1091–1095.

    Google Scholar 

  • Reimchen T.E. (1988) Inefficient predators and injuries in a population of giant stickleback. Can. J. Zool. 66, 2036–2044.

    Google Scholar 

  • Renaud F., Clayton D. and deMeeus T. (1996) Biodiversity and evolution in host-parasite associations. Biodiv. Cons. 5, 963–974.

    Google Scholar 

  • Ridley M. (1993) The Red Queen: Sex and the Evolution of Human Nature. Penguin, London.

    Google Scholar 

  • Rodewald A.D. and Foster S.A. (1998) Effects of gravidity on habitat use and anti-predator behaviour in three-spined sticklebacks. J. Fish Biol. 52, 973–984.

    Google Scholar 

  • Rohde K. (1993) Ecology of Marine Parasites, 2nd ed. CAB International, Wallingford.

    Google Scholar 

  • Rosenqvist G. and Johansson K. (1995) Male avoidance of parasitized females explained by direct benefits in a pipefish. Anim. Behav. 49, 1039–1045.

    Google Scholar 

  • Rowland W.J. (1994) Proximate determinants of stickleback behaviour: an evolutionary perspective. In: Bell M.A. and Foster S.A. (eds.), The Evolutionary Biology of the Threespine Stickleback. Oxford University Press, Oxford.

    Google Scholar 

  • Rubenstein D. and Hohmann M.E. (1989) Parasites and social behaviour of feral horses. Oikos 55, 312–320.

    Google Scholar 

  • Russell L.R. (1980) Effects of Truttaedacnitis truttae (Nematoda: Cucullanidae) on growth and swimming of rainbow trout, Salmo gairdneri. Can. J. Zool. 58, 1220–1226.

    Google Scholar 

  • Scott M.E. (1985) Experimental epidemiology of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata): shortand long-term studies. In: Rollinson D. and Anderson R.M. (eds.), Ecology and Genetics of Host-Parasite Interactions. Academic Press, London, pp. 21–38.

    Google Scholar 

  • Skarstein F. and Folstad I. (1996) Sexual dichromatism and the immunocompetence handicap: An observational approach using Arctic charr. Oikos 76, 359–367.

    Google Scholar 

  • Smith H.D. (1973) Observations on the cestode Eubothrium salvelini in juvenile sockeye salmon (Oncorhynchus nerka) at Babine Lake, British Columbia. J. Fish. Res. Bd. Can. 30, 947–964.

    Google Scholar 

  • Smith R.S. and Kramer D.C. (1987) Effects of a cestode (Schistocephalus sp.) on the response of ninespine sticklebacks (Pungitius pungitius) to aquatic hypoxia. Can. J. Zool. 65, 1862–1865.

    Google Scholar 

  • Smith H.D. and Margolis L. (1970) Some effects of Eubothrium salvelini (Schrank, 1790) on sockeye salmon, Oncorhynchus nerka (Walbaum), in Babine Lake, British Columbia. J. Parasitol. 56(II), 321–322.

    Google Scholar 

  • Smith Trail D.R. (1980) Behavioural interactions between parasites and hosts: host suicide and the evolution of complex life cycles. Am. Nat. 116, 77–91.

    Google Scholar 

  • Smyth J.D. (1985) An Introduction to Animal Parasitology. Hodder and Stoughton, London.

    Google Scholar 

  • Sprengel G. and Lüchtenberg H. (1991) Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. Dis. Aq. Org. 11, 31–35.

    Google Scholar 

  • Sproston N.G. and Hartely P.H.T. (1941) The ecology of some parasitic copepods of gadoids and other fishes. J. Mar. Biol. Assn. UK 25, 361–392.

    Google Scholar 

  • Stephens D.W. and Krebs J.R. (1986) Foraging Theory. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Stott M.K. and Poulin R. (1996) Parasites and parental care in male upland bullies (Eleotridae). J. Fish. Biol. 48, 283–291.

    Google Scholar 

  • Svensson P.A., Barber I. and Forsgren E. (2000) Shoaling behaviour of the two spotted goby. J. Fish. Biol. 56, 1477–1487.

    Google Scholar 

  • Sweeting R.A. (1976) Studies on Ligula intestinalis (L.) effects on a roach population in a gravel pit. J. Fish Biol. 9, 515–522.

    Google Scholar 

  • Sweeting R.A. (1977) Studies on Ligula intestinalis: some aspects of the pathology in the second intermediate host. J. Fish Biol. 10, 43–50.

    Google Scholar 

  • Szidat L. (1969) Structure, development and behaviour of new strigeatoid metacercariae from subtropical fishes of South America. J. Fish. Res. Bd. Can. 26, 753–786.

    Google Scholar 

  • Theodorakis C.W. (1989) Size segregation and the effects of oddity on predation risk in minnow schools.Anim. Behav. 38, 496–502.

    Google Scholar 

  • Thompson S.N. and Kavaliers M. (1994) Physiological bases for parasite-induced alterations of host behaviour. Parasitol. 109, S119–S138.

    Google Scholar 

  • Tierney J.F. (1994) Effects of Schistocephalus solidus (Cestoda) on the food intake and diet of the three-spined stickleback, Gasterosteus aculeatus. J. Fish Biol. 44, 731–735.

    Google Scholar 

  • Tierney J.F. and Crompton D.W.T. (1992) Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. J. Parasitol. 78, 1049–1054.

    Google Scholar 

  • Tierney J.F., Huntingford F.A. and 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. Anim. Behav. 46, 603–605.

    Google Scholar 

  • Tinsley R.C. (1990) Host behaviour and opportunism in parasite life cycles. In: Barnard C.J. and Behnke J.M. (eds.), Parasitism and Host Behaviour. Taylor and Francis, London, U.K., pp. 95–116.

    Google Scholar 

  • Urawa S. (1992) Trichodina truttae Mueller 1937 (Ciliophora, Peritrichida) on juvenile chum salmon (Oncorhynchus keta) - pathogenicity and host-parasite interactions. Fish Pathol. 27, 29–37.

    Google Scholar 

  • Urdal K., Tierney J.F. and Jakobsen P.J. (1995) The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. J. Parasitol. 81, 330–333.

    Google Scholar 

  • Uspenskaya A.V. 1957. The ecology and spreading of the pathogen of trout whirling disease - Myxosoma cerebralis (Hofer, 1903, Plehn, 1905) in the fish ponds of the Soviet Union. In: Izvestiya Vsesoyuznogo naucho-issledovatel'skogo instituta ozernogo i rechnogo rybnogo khozyaistva, Vol. XLII.

  • van Dobben W.H. (1952) The food of the cormorant in the Netherlands. Ardea 40, 1–63.

    Google Scholar 

  • van Havre N. and FitzGerald G.J. (1988) Shoaling and kin recognition in the threespine stickleback (Gasterosteus aculeatus L.). Biol. Behav. 13, 190–201.

    Google Scholar 

  • Vaughan G.E. (1979) Comparative vulnerability of bluegills with and without lymphocystis disease to predation by largemouth bass. Prog. Fish. Cult. 41, 163–164.

    Google Scholar 

  • Vaughan G.E. and Coble D.W. (1975) Sublethal effects of three ectoparasites on fish. J. Fish Biol. 7, 283–294.

    Google Scholar 

  • Vickery and Poulin (1998) Parasitised non-choosy females do slow down the process: a reply to J. Rolff. Behav. Ecol. Sociobiol. 44, 75–76.

    Google Scholar 

  • Videler J.J. (1993) Fish Swimming. Chapman and Hall, London, 260 pp.

    Google Scholar 

  • Walkey M. and Meakins R.H. (1970) An attempt to balance the energy budget of a host-parasite system. J. Fish Biol. 2, 361–372.

    Google Scholar 

  • 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.

    Google Scholar 

  • Wootton R.J. (1990) Ecology of Teleost Fishes. Chapman and Hall, London, 404 pp.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fish Biology Group, Institute of Biomedical and Life Sciences, University of Glasgow, Scotland, UK;

    Iain Barber

  2. Institute of Biological Sciences, University of Wales Aberystwyth, Wales, UK;

    Iain Barber

  3. School of Biology, University of Leeds, UK

    Danie Hoare & Jens Krause

Authors
  1. Iain Barber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danie Hoare
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jens Krause
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iain Barber.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barber, I., Hoare, D. & Krause, J. Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165 (2000). https://doi.org/10.1023/A:1016658224470

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016658224470

Search

Navigation