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Behavioural defense against parasites: interaction with parasite invasiveness

Published online by Cambridge University Press:  16 March 2011

B. L. Hart
B. L. Hart
Affiliation:
Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California, Davis, USA
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Summary

Behavioural patterns involved in avoiding, repelling, or removing parasites allow mammalian hosts to defend themselves from an array of parasites that threaten the host's fitness in the natural world. Some examples of behavioural defenses and the presumed target parasites are: grooming to remove ticks, grouping to reduce attack rate of biting flies, fly repelling movements to reduce parasitic flies, and selective grazing to reduce intake of faecal-borne parasites. These behavioural defenses are discussed with regard to effectiveness in controlling the target parasites. Parasites have sometimes evolved behavioural strategies of evading, penetrating or disabling these behavioural defenses. These parasite behavioural strategies, though less studied, are discussed. Also discussed is the possibility that host behavioural patterns that may defend against one parasite may be exploited by a different type of parasite to facilitate its own transmission. The interplay between host defensive strategies, the cost versus the effectiveness of such strategies, and a parasite's evasion or exploitation of such strategies, may be useful in understanding some aspects of host-parasite dynamics in nature.

Keywords

Parasite defensegroomingfly repellinggroupingforaging.
Type
Research Article
Information
Parasitology , Volume 109 , supplement S1: Parasites and behaviour , 1994 , pp. S139 - S151
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Austen, E. E. (1939). Gad flies. Appendix B. In British Blood Sucking Flies (eds. Edwards, F. W.; Oldroyd, H.; Smart, J.) pp. 149–152 British Museum, London.Google Scholar
Bell, J. F., Clifford, C. M., Moore, G. J. & Raymond, G. (1966). Effects of limb disability on lousiness in mice. III. Gross aspects of acquired resistance. Experimental Parasitology 18, 49–60.CrossRefGoogle Scholar
Bennett, G. F. (1969). Boophilus microplus (Acarina: Ixodidae): Experimental infestations on cattle restrained from grooming. Experimental Parasitology 26, 323–8.CrossRefGoogle ScholarPubMed
Bergerud, A. T. (1974). The role of the environment in the aggregation, movement and disturbance behaviour of caribou. In The Behaviour of Ungulates and its Relation to Management, (ed. Geist, V. & Walther, F.) pp. 552–584. Iucn Publications new series 24, Morges, Switzerland.Google Scholar
Bolles, R. C. (1960). Grooming behavior in the rat. Journal of Comparative Physiological Psychology 53, 306–10.Google Scholar
Breev, K. A. (1954). The behaviour of blood-sucking Diptera and bot-flies when attacking reindeer. Review of Applied Entomology 42, 67–8 (translation of Parasit. Sborn 12; p. 167–198, in Russian).Google Scholar
Brown, C. R. & Brown, W. B. (1986). Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67, 1206–18.Google Scholar
Christie, M. G. (1963). The disintegration of sheep dung and the pre-parasitic stages of trichonstrongylids. Journal of Comparative Pathology 73, 416–23.CrossRefGoogle Scholar
Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex, Vol. 1, Murray, London.Google Scholar
Day, F. & Edman, J. D. (1983). Malaria renders mice susceptible to mosquito feeding when gametocytes are most infective. Journal of Parasitology 69, 163–70.CrossRefGoogle ScholarPubMed
Decastro, J. J. & Newson, R. M. (1993). Host resistance in cattle tick control. Parasitology Today 9, 13–17.CrossRefGoogle Scholar
Downes, C. M., Theberge, J. B. & Smith, S. M. (1986). The influence of insects on the distribution, microhabitat choice, and behavior of the Burwash caribou herd. Canadian Journal of Zoology 64, 622—9.Google Scholar
Duncan, P. & Vigne, N. (1979). The effect of group size in horses on the rate of attacks by blood-sucking flies. Animal Behaviour 27, 623—5.Google Scholar
Durie, P. H. (1961). Parasitic gastro-enteritis of cattle: The distribution and survival of infective strongyle larvae on pasture. Australian Journal of Agricultural Research 12, 1200–11.CrossRefGoogle Scholar
Edman, J. D. & II,Kale, H. W. (1971). Host behavior: Its influence on the feeding success of mosquitoes. Annals of Entomology Society of America 64, 513–16.Google Scholar
Elgar, M. A. (1989). Predator vigilance and group size in mammals and birds: A critical review of the empirical evidence. Biological Review 64, 13–33.CrossRefGoogle ScholarPubMed
English, A. W. (1979). The epidemiology of equine strongylosis in southern Queensland. Australian Veterinary Journal 55, 299–305.Google Scholar
Espmark, Y. (1967). Observations of defence reactions to oestrid flies by semidomestic forest reindeer (Rangifer tarandus L.) in Swedish Lapland. Zoologische Beitrage 14, 155–67.Google Scholar
Eysker, M. (1991). Direct measurement of dispersal of Dictyocaulus viviparous in sporangia of Pilobolus species. Research in Veterinary Science 50, 29—32.Google Scholar
Fitzgibbons, C. D. (1989). A cost to individuals with reduced vigilance in groups of Thomson's gazelles hunted by cheetahs. Animal Behaviour 37, 508–10.CrossRefGoogle Scholar
Garcia, R. (1962). Carbon dioxide as an attractant for certain ticks (Acarina, Argasidae and Ixodidae). Annals of the Entomological Society of America 14, 605–6.Google Scholar
Hamilton, W. D. (1971). Geometry for the selfish herd. Journal of Theoretical Biology 31, 295–311.Google Scholar
Harris, J. A., Hillerton, J. E. & Morant, S. V. (1987). Effect on milk production of controlling muscid flies, and reducing fly-avoidance behaviour, by use of Fenvalerate ear tags during the dry period. Journal of Dairy Research 54, 165–71.CrossRefGoogle ScholarPubMed
Hart, B. L. (1990). Behavioral adaptations to pathogens and parasites: Five strategies. Neuroscience and Biobehavioral Reviews 14, 273–94.CrossRefGoogle ScholarPubMed
Hart, B. L. & Hart, L. A. (1994). Fly switching in Asian elephants: Tool use to control parasites. Animal Behaviour 48, 35–45.CrossRefGoogle Scholar
Hart, B. L., Hart, L. A. & Mooring, M. S. (1990). Differential foraging of oxpeckers on impala in comparison with sympatric antelope species. African Journal of Ecology 28, 240–9.Google Scholar
Hart, B. L., Hart, L. A., Mooring, M. S. & Olubayo, R. (1992). Biological basis of grooming behaviour in antelope; the body-size, vigilance and habitat principles. Animal Behaviour 44, 615–31.CrossRefGoogle Scholar
Harvey, P. H. & Greenwood, P. J. (1978). Anti-predator defence strategies: some evolutionary problems. In Behavioural Ecology: An Evolutionary Approach (ed. Krebs, J. R. & Davies, N. B.) pp. 129–151, Blackwell, Oxford.Google Scholar
Harvey, T. L. & Launchbaugh, J. L. (1982). Effect of horn flies on behavior of cattle. Journal of Economic Entomology 75, 25–7.Google Scholar
Helle, T. & Aspi, J. (1983). Does herd formation reduce insect harassment among reindeer ? A field experiment with animal traps. Ada Zoologica Fennica 175, 129–31.Google Scholar
Hieber, C. S. & Uetz, G. W. (1990). Colony size and parasitoid load in two species of colonial Meteperia spiders from Mexico (Araneae, Araneidae). Oecologia 82, 145–50.Google Scholar
Hillerton, J. E., Morant, S. V. & Harris, J. A. (1986). Control of Muscidae on cattle by flucythrinate eartags, the behaviour of these flies on cattle and the effect on fly-dislodging behaviour. Entomology and Experimental Applications 41, 213–18.Google Scholar
Hoagland, J. L. (1979). Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp.) coloniality. Behaviour LXIX, 1–35.CrossRefGoogle Scholar
Hoagland, J. L. & Sherman, P. W. (1976). Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecological Monographs 46, 33–58.Google Scholar
Howell, C. J., Walker, J. B. & Nevill, E. M. (1978). Ticks, mites and insects infesting domestic animals in South Africa. Part 1. Descriptions and biology. Science Bulletin Department of Agricultural Technical Services Republic of South Africa 393, 1–69.Google Scholar
Hudson, R. & Distel, H. (1982). The pattern of behaviour of rabbit pups in the nest. Behaviour 79, 255–71.Google Scholar
Inman, A. J. & Krebs, J. (1987). Predation and group living. Trends in Ecological Evolution 2, 31–2.Google Scholar
Kaiser, M. N., Sutherst, R. W. & Bourne, A. S. (1991). Tick (Acarina: Ixodidae) infestations on zebu cattle in northern Uganda. Bulletin on Entomology Research 81, 257–62.Google Scholar
Ladewig, J. & Matthews, L. R. (1992). The importance of physiological measurements in farm animal stress research. Proceedings of the New Zealand Society of Animal Production, 52, 77–9.Google Scholar
Lehmann, T. (1993). Ectoparasites: Direct impact on host fitness. Parasitology Today 9, 8–13.Google Scholar
Lewis, L. F., Christenson, D. M. & Eddy, G. W. (1967). Rearing the long-nosed cattle louse and cattle biting louse on host animals in Oregon. Journal of Economic Entomology 60, 755—7.Google Scholar
Main, A. J., Sprange, H. E., Klotter, K. O. & Brown, S. E. (1981). Ixodes daminini (Acari: Ixodidae) on whitetailed deer Odocoileus virginianus in Connecticut, USA. Journal of Medical Entomology 18, 487–92.Google Scholar
Mckenzie, A. A. (1990). The ruminant dental grooming apparatus. Zoological Journal of the Linnean Society 99, 117–28.CrossRefGoogle Scholar
Mckenzie, A. A. & Weber, A. (1993). Loose front teeth: radiological and histological correlation with grooming functioning in the impala Aepyceros melampus. Journal of Zoology, London 231, 167–74.Google Scholar
Michel, J. F. (1955). Parasitological significance of bovine grazing behaviour. Nature 175, 1088–9.Google Scholar
Mooring, M. S. (1995). The effect of tick challenge on grooming rate by impala. Animal Behaviour, in press.Google Scholar
Mooring, M. S. & Hart, B. L. (1993). Animal grouping for protection from parasites: Selfish herd and encounter/dilution effects. Behaviour 123, 173–93.Google Scholar
Mooring, M. S. & Hart, B. L. (1994). Differential grooming rate and tick load of territorial male and female impala. Behavioral Ecology, in press.Google Scholar
Murray, M. D. (1961). The ecology of the louse Polyplax serrata (Berm.) on the mouse Mus musculus L. Australian Journal of Zoology 9, 1–13.Google Scholar
Murray, M. D. (1987). Effects of host grooming on louse populations. Parasitology Today 3, 276–8.CrossRefGoogle ScholarPubMed
Nelson, W. A., Keirans, J. E., Bell, J. F. & Clifford, C. M. (1975). Host-ectoparasite relationships. Journal of Medical Entomology 12, 143–66.Google Scholar
Norval, R. A. I., Sutherst, R. W., Kurki, J., Gibson, J. D. & Kerr, J. D. (1988). The effect of the brown ear-tick Rhipicephalus appendiculatus on the growth of sanga and European bred cattle. Veterinary Parasitology 30, 149–64.CrossRefGoogle Scholar
Ödberg, F. O. & Francis-Smith, K. (1977). Studies on the formation of ungrazed eliminative areas in fields used by horses. Applied Animal Ethology 3, 27–44.Google Scholar
Okumura, T. (1977). The relationship of attacking fly abundance to behavioral responses of grazing cattle. Japanese Journal of Applied Entomology & Zoology 21, 119–22.Google Scholar
Olubayo, R., Jono, J., Orinda, G., Groothenhuis, J. G. & Hart, B. L. (1993). Comparative differences in density of adult ticks as a function of body size in some East African antelope. African Journal of Ecology 31, 26–34.Google Scholar
Pain, B. F., Leaver, J. D. & Broom, D. M. (1974). Effects of cow slurry on herbage intake by cattle and grazing behaviour. Journal of the British Grassland Society 29, 85–91.Google Scholar
Poulin, R. F. (1991). Group-living and infestation by ectoparasites in passerines. Condor 93, 418—23.CrossRefGoogle Scholar
Poulin, R. & Fitzgerald, G. J. (1989). Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.). Behavioral Ecological Sociobiology 24, 251–5.CrossRefGoogle Scholar
Pulliam, H. R. (1973). On the advantages of flocking. Journal of Theoretical Biology 38, 419–22.CrossRefGoogle ScholarPubMed
Ramachondra, R. N. & Wikel, S. K. (1992). Modulation of host-immune responses by ticks (Acari: Ixodidae): Effects of salivary gland extracts on host macrophages and lymphocyte cytokine production. Journal of Medical Entomology 29, 818–26.Google Scholar
Rechal, Y., Clarke, F. C., Els, D. A. & Dauth, J. (1991). Development of resistance in laboratory animals to adults of the tick Rhiphicephalis evertsi evertsi. Medical and Veterinary Entomology 5, 29–34.Google Scholar
Ribeiro, J. M. C. (1989). Role of saliva in tick/host interactions. Experimental and Applied Acarology 7, 15–20.Google Scholar
Ritter, R. C. & Epstein, A. N. (1974). Saliva lost by grooming: A major item in the rat's water economy. Behavioral Biology 11, 581–5.Google Scholar
Robinson, J. (1962). Pilobolus spp. and the translation of infective larvae of Dictyocaulus viviparus from faeces to pastures. Nature 193, 353–4.Google Scholar
Rothschild, M. (1965). The rabbit flea and hormones. Endeavour 24, 162–8.Google ScholarPubMed
Rothschild, M. & Ford, B. (1966). Hormones of the vertebrate host controlling ovarian regression and copulation in the rabbit flea. Nature, London 211, 261–6.Google Scholar
Rothschild, M. & Ford, R. (1973). Factors influencing the breeding of the rabbit flea (Spilopsyllus cuniculi): A spring-time accelerator and a kairomone in nestling rabbit urine (with notes on Cediopsylla simplex, another “hormone bound” species). Journal of Zoology 170, 87–137.Google Scholar
Rubenstein, D. I. & Hohmann, M. E. (1989). Parasites and social behavior of island feral horses. Oikos 55, 312–20.Google Scholar
Rutberg, A. T. (1987). Horse fly harassment and the social behavior of feral ponies. Ethology 75, 145–54.Google Scholar
Schmidt, G. D. & Roberts, L. S. (1985). Foundations of Parasitology. Times Mirror/Mosby College Publication, St. Louis.Google Scholar
Schmidtmann, E. T. & Valla, M. E. (1982). Face-fly pest intensity, fly-avoidance behavior (bunching) and grazing time in Holstein heifers. Applied Animal Ethology 8, 429–38.Google Scholar
Snowball, G. J. (1956). The effect of self licking by cattle on infestation of cattle tick Boophilus microplus (Canestrini). Australian Journal of Agricultural Research 1, 227–32.CrossRefGoogle Scholar
Soulsby, E. J. L. (1982). Helminths, Arthropods and Protozoa of Domesticated Animals (Seventh ed). Lea & Febiger, Philadelphia.Google Scholar
Sutherst, R. W., Floyd, R. B., Bourne, A. S. & Daltwitz, M. J. (1986). Cattle grazing behavior regulates tick populations. Experientia 42, 194—6.Google Scholar
Steullet, P. & Guerin, P. M. (1992 a). Perception of breath components by the tropical bout tick, Amblyomma variegatum Fabricius (Ixodidae). I. CO2-excited and CO2-inhibited receptors. Journal of Comparative Physiology A 170, 665–76.Google Scholar
Steullet, P. & Guerin, P. M. (1992 b). Perception of breath components by the tropical bout tick, Amblyomma variegatum Fabricicus (Ixodidae). II. Sulfide-receptors. Journal of Comparative Physiology A 170, 677–85.Google Scholar
Tashiro, H. & Schwardt, H. H. (1953). Biological studies of horse flies in New York. Journal of Economic Entomology 46, 813–22.Google Scholar
Turner, G. F. & Pitcher, T. J. (1986). Attack abatement: A model for group protection by combined avoidance and dilution. American Naturalist 128, 225—40.Google Scholar
Wakelin, D. (1984). Immunity to Parasites. Arnold, London.Google Scholar
Wikel, S. K. (1984). Immunomodulation of host responses to ectoparasite infestation - an overview. Veterinary Parasitology 321–39.CrossRefGoogle Scholar
Willadsen, P. (1980). Immunity to ticks. Advances in Parasitology 18, 293–313.Google Scholar
Wiesbroth, S. H., Friedman, S. & Powell, M. (1974). The parasitic ecology of the rodent mite Myobia mulculi. I. Grooming factors. Laboratory Animal Science 26, 725–35.Google Scholar
Yunker, C. E., Peter, T., Norval, R. A. I., Sonenshine, D. E., Burridge, M. J. & Butler, J. F. (1992). Olfactory responses of adult Amblyomma hebraeum and A. variegatum (Acari: Ixodidae) to attractal chemicals in laboratory tests. Experimental and Applied Acarology 13, 295–301.Google Scholar