Abstract
Parasites of all kinds affect the behaviour of their hosts, often making them more susceptible to predators. The associated loss in expected future reproductive success of infected hosts will vary among individuals, with younger ones having more lose than older ones. For this reason, young hosts would benefit more by opposing the effects of parasites than old ones. In a laboratory study, the effects of the trematode Telogaster opisthorchis on the anti-predator responses of the upland bully (Gobiomorphus breviceps) and of the common river galaxias (Galaxias vulgaris) were examined in relation to fish age. In a bully population where parasites were very abundant, the magnitude of the fish's anti-predator responses decreased as the number of parasites per fish increased, and this effect was significantly more pronounced in age 2 + and, to a lesser extent, age 3 + fish than in age 1 + fish. In another bully population where parasites were 10 times less abundant, similar effects were noticeable but not significant, whereas no effects of parasites on the responses of galaxiids to predators were apparent. Differences in the abundance of parasites and in their sites of infection in fish may explain the variability among host populations or species. However, in the bully population with high parasite abundance, parasitism has age-dependent effects on responses to predators, providing some support for the prediction that young fish with high expected future reproductive success invest more energy into opposing the effects of parasites than do older fish.
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References
Ballabeni P, Ward PI (1993) Local adaptation of the trematode Diplostomum phoxini to the European minnow Phoxinus phoxinus, its second intermediate host. Funct Ecol 7:84–90
Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34:171–182
Brassard P, Rau ME, Curtis MA (1982a) Infection dynamics of Diplostomum spathaceum cercariae and parasite-induced mortality of fish hosts. Parasitology 85:489–493
Brassard P, Rau ME, Curtis MA (1982b) Parasite-induced susceptibility to predation in diplostomiasis. Parasitology 85:495–501
Cadwallader PL (1978) Age, growth, and condition of the common river galaxias, Galaxias vulaaris Stokell, in the Glentui River, Canterbury, New Zealand. N Z Min Agric Fish Fish Res Bull 17:1–35
Coleman FC (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
Crowden AE, Broom DM (1980) Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav 28:287–294
Dill LM (1987) Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can J Zool 65:803–811
Dixon SM, Baker RL (1988) Effects of size on predation risk, behavioural response to fish, and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata). Oecologia 76:200–205
Dobson AP (1988) The population biology of parasite-induced changes in host behavior. Q Rev Biol 63:139–165
Endler JA (1986) Defense against predators. In: Feder ME, Lauder GV (eds) Predator-prey relationships: perspectives and approaches from the study of lower vertebrates. University of Chicago Press, Chicago, pp 109–134
Endler JA (1991) Interactions between predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell, Oxford, pp 169–196
Godin J-GJ, Sproul CD (1988) Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability. Can J Zool 66:2360–2367
Hechtel LJ, Johnson CL, Juliano SA (1993) Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus. Ecology 74:710–713
Helfman GS (1986) Behavioral responses of prey fishes during predator-prey interactions. In: Feder ME, Lauder GV (eds) Predator-prey relationships: perspectives and approaches from the study of lower vertebrates. University of Chicago Press, Chicago, pp 135–156
Hewitt GC, Hine PM (1972) Checklist of parasites of New Zealand fishes and of their hosts. N Z J Mar Freshwater Res 6:69–114
Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61:681–692
Keymer AE, Read AF (1991) Behavioural ecology: the impact of parasitism. In: Toft CA, Aeschlimann A, Bolis L (eds) Parasitehost associations: coexistence or conflict? Oxford University Press. Oxford, pp 37–61
Lemly AD, Esch GW (1984) Effects of the trematode Uvulifer ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. J Parasitol 70:475–492
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Macfarlane WV (1945) The life cycle of the heterophyoid trematode Telogaster opisthorchis n.g., n.sp. Trans R Soc N Z 75:218–230
Magnhagen C (1990) Reproduction under predation risk in the sand goby, Pomatoschistus minutus, and the black goby, Gobius niger: the effect of age and longevity. Behav Ecol Sociobiol 26:331–335
Magnhagen C (1992) Parental care and predation risk in fish. Ann Zool Fenn 29:227–232
McDowall RM (1990) New Zealand freshwater fishes: a natural history and guide. Heinemann Reed, Auckland
Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93:203–216
Milinski M (1990) Parasites and host decision-making. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor & Francis, London, pp 95–116
Milinski M, Heller R (1978) Influence of a predator on the optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus L.) Nature 275:642–644
Moore J (1983) Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64:1000–1015
Moore J, Gotelli NJ (1990) A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor & Francis, London, pp 193–233
Owen SF, Barber I, Hart PJB (1993) Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 42:803–806
Poulin R, Curtis MA, Rau ME (1992) Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105:265–271
Read AF (1990) Parasites and the evolution of host sexual behaviour. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor & Francis, London, pp 117–157
Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New York
Staples DJ (1975) Production biology of the upland bully Philypnodon breviceps Stokell in a small New Zealand lake. I. Life history, food, feeding and activity rhythms. J Fish Biol 7:1–24
Steedman RJ (1991) Occurrence and environmental correlates of black spot disease in stream fishes near Toronto, Ontario. Trans Am Fish Soc 120:494–499
Stein RA (1979) Behavioral response of prey to fish predators. In: Stroud RH, Clepper H (eds) Predator-prey systems in fisheries management. Sport Fishing Institute, Washington DC, pp 343–353
Vaughan GE, Coble DW (1975) Sublethal effects of three ectoparasites on fish. J Fish Biol 7:283–294
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Poulin, R. Age-dependent effects of parasites on anti-predator responses in two New Zealand freshwater fish. Oecologia 96, 431–438 (1993). https://doi.org/10.1007/BF00317516
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DOI: https://doi.org/10.1007/BF00317516