Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T18:11:10.821Z Has data issue: false hasContentIssue false
  • English
  • Français

Low-level parasitic worm burdens may reduce body condition in free-ranging red deer (Cervus elaphus)

Published online by Cambridge University Press:  04 July 2006

R. J. IRVINE ,
H. CORBISHLEY ,
J. G. PILKINGTON  and
S. D. ALBON
R. J. IRVINE
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY
H. CORBISHLEY
Affiliation:
Chamber Height Farm, Water, Rosserdale, Lancashire BB4 9NQ
J. G. PILKINGTON
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY
S. D. ALBON
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY
Get access Rights & Permissions [Opens in a new window]

Abstract

Regulation of ungulate populations by parasites relies on establishing a density-dependent relationship between infection and vital demographic rates which may act through the effect of parasites on body condition. We examine evidence for parasite impacts in 285 red deer (Cervus elaphus) harvested during 1991 and 1992 on the Isle of Rum. In the abomasa, prevalence of nematodes was 100% and the most abundant genus observed were Ostertagia species, however, mean intensity of infection was low (less than 1000) relative to other studies. Additional species, also present in low numbers, included Nematodirus spp., Capillaria spp., Cooperia spp., Monieza expanza, Oesophagostomum venulosum and Trichuris ovis. Lungworm (Dictyocaulus spp.) and tissue worm (Elaphostronygylus cervi) larvae were also observed in faecal samples. There was no evidence for acquired immunity to abomasal nematodes. Despite low levels of infection, both adult male and female deer showed significant negative correlation between indices of condition (kidney fat index, dressed carcass weight and larder weight) and intensity of Ostertagia spp. infection. However, there was no evidence that pregnancy rate in females was related to intensity of infection. For calves, there was no relationship between body condition and intensity of infection. The apparent subclinical effects of low-level parasite infection on red deer performance could alternatively be due to animals in poorer nutritional state being more susceptible to infection. Either way the results suggest that further studies of wild populations are justified, in particular where high local host densities exist or alternative ungulate hosts are present, and, where experimental treatments are tractable.

Keywords

nematode parasitesred deercost of parasitismbody massbody conditionpregnancy
Type
Research Article
Information
Parasitology , Volume 133 , Issue 4 , October 2006 , pp. 465 - 475
Copyright
© 2006 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

Albon, S. D., Mitchell, B., Huby, J. B. and Brown, D. ( 1986). Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status. Journal of Zoology 209, 447–460.CrossRefGoogle Scholar
Albon, S. D., Mitchell, B. and Staines, B. W. ( 1983). Fertility and body-weight in female red deer – a density-dependent relationship. Journal of Animal Ecology 52, 969–980.CrossRefGoogle Scholar
Albon, S. D., Coulson, T. N., Brown, D., Guiness, F. E., Clutton-Brock, T. H. and Pemberton, J. M. ( 2000). Temporal changes in key factors and key age groups influencing the population dynamics of female red deer. Journal of Animal Ecology 69, 1099–1110.CrossRefGoogle Scholar
Albon, S. D., Stien, A., Irvine, R. J., Langvatn, R., Ropstad, E. and Halvorsen, O. ( 2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London, B 269, 1625–1632.CrossRefGoogle Scholar
Anderson, R. M. and Crombie, J. ( 1984). Experimental studies of age prevalence curves for Schistosoma mansoni infections in populations of Biomphalaria glabrata. Parasitology 89, 79–105.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1978). Regulation and stability of host parasite population interactions: Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Arneberg, P., Folstad, I. and Karter, A. J. ( 1996). Gastrointestinal nematodes depress food intake in naturally infected reindeer. Parasitology 112, 213–219.CrossRefGoogle Scholar
Bye, K. ( 1987). Abomasal nematodes from three Norwegian wild reindeer populations. Canadian Journal of Zoology 65, 677–680.CrossRefGoogle Scholar
Clutton-Brock, T. H. and Albon, S. D. ( 1989). Red Deer in the Highlands. BSP Professional Books, London, UK.
Clutton-Brock, T. H. and Ball, M. E. ( 1987). Rhum: The Natural History of an Island. Edinburgh University Press, Edinburgh.
Clutton-Brock, T. H., Coulson, T., Milner-Gulland, E. J., Thomson, D. and Armstrong, H. M. ( 2002). Sex differences in emigration and mortality affect optimal management of deer populations. Nature, London 415, 633–636.CrossRefGoogle Scholar
Clutton-Brock, T. H., Coulson, T. and Milner, J. M. ( 2004). Red deer stocks in the Highlands of Scotland. Nature,London 429, 261.CrossRefGoogle Scholar
Clutton-Brock, T. H., Guiness, F. and Albon, S. D. ( 1982). Red Deer. Behaviour and Ecology of two Sexes. Chicago University Press, Chicago, USA.
Clutton-Brock, T. H., Thomson, D. and Covey, C. ( 1997). Monitoring Red Deer Changes on Rum. Progress Report NCLS 024/97/UPB. Scottish National Heritage.
Coop, R. L. and Holmes, P. H. ( 1996). Nutrition and parasite interaction. International Journal for Parasitology 26, 951–962.CrossRefGoogle Scholar
Coop, R. L., Huntley, J. F. and Smith, W. D. ( 1995). Effect of dietary protein supplementation on the development of immunity to Ostertagia circumcincta in growing lambs. Research in Veterinary Science 59, 24–29.CrossRefGoogle Scholar
Coop, R. L. and Kyriazakis, I. ( 2001). Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325–330.CrossRefGoogle Scholar
Coulson, T., Catchpole, E. A., Albon, S. D., Morgan, B. J. T., Pemberton, J. M., Clutton-Brock, T. H., Crawley, M. J. and Grenfell, B. T. ( 2001). Age, sex, density, winter weather, and population crashes in Soay sheep. Science 292, 1528–1531.CrossRefGoogle Scholar
Coyne, M. J and Smith, G. ( 1994). Trichostrongylid parasites of domestic Ruminants. In Parasitic and Infectious Diseases: Epidemiology and Ecology ( ed. Scott, M. E. and Smith, G.), pp. 235–247. Academic Press, San Diego, CA.
Daszak, P., Cunningham, A. A. and Hyatt, A. D. ( 2000). Wildlife ecology – emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle Scholar
Flint, A. P. F., Albon, S. D. and Jafar, S. I. ( 1997 a). Blastocyst development and conceptus sex selection in red deer (Cervus elaphus): studies of a free-living population on the Isle of Rum. General and Comparative Endocrinology 106, 374–383.Google Scholar
Flint, A. P. F., Albon, S. D., Loudon, A. S. I. and Jabbour, H. N. ( 1997 b). Behavioral dominance and corpus luteum function in red deer (Cervus elaphus). Hormones and Behaviour 31, 296–304.Google Scholar
Folstad, I. and Karter, A. J. ( 1992). Parasites, bright males and the immunocompetance handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
Forbes, A. B., Huckle, C. A., Gibb, M. J., Rook, A. J. and Nuthall, R. ( 2000). Evaluation of the effects of nematode parasitism on grazing behaviour, herbage intake and growth in young grazing cattle. Veterinary Parasitology 90, 111–118.CrossRefGoogle Scholar
Fox, M. T. ( 1993). Pathophysiology of infection with Ostertagia ostertagi in cattle. Veterinary Parasitology 46, 143–158.CrossRefGoogle Scholar
Fox, M. T. ( 1997). Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Veterinary Parasitology 72, 285–308.CrossRefGoogle Scholar
Gaillard, J. M., Festa-Bianchet, M., Yoccoz, N. G., Loison, A. and Toigo, C. ( 2000). Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics 31, 367–393.CrossRefGoogle Scholar
Gershwin, M. E., Richard, B. S. and Hurley, L. S. ( 1985). Nutrition and Immunology. Academic Press, London.
Grenfell, B. T., Dietz, K. and Roberts, M. G. ( 1995 a). Modelling the immuno-epidemiology of macroparasites in naturally fluctuating host populations. In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. and Dobson, A. P.), pp. 362–383. Cambridge University Press, Cambridge.
Gulland, F. M. D. ( 1992). The role of nematode parasites in Soay sheep (Ovis aries. L) mortality during a population crash. Parasitology 105, 493–503.Google Scholar
Gulland, F. M. D. ( 1995). The impact of infectious diseases on wild animal populations: a review. In Ecology of Infectious Diseases in Natural Populations ( ed. Dobson, A. P. and Grenfell, B. T.), pp. 20–51. Cambridge University Press, Cambridge.CrossRef
Gunn, A. and Irvine, R. J. ( 2003) Sub-clinical parasitism and ruminant foraging strategies – a review. Wildlife Society Bulletin 31, 117–126.Google Scholar
Halvorsen, O. and Bye, K. ( 1986). Parasitter i Svalbardrein 1. Rundmark i løpen (in Norwegian). In Svalbardreinen og dens Livsgrunnlag ( ed N. A. Øritlaland), pp. 120–133. Universitetsforlaget, Oslo, Norway.
Halvorsen, O. and Bye, K. ( 1999). Parasites, biodiversity, and population dynamics in an ecosystem in the high arctic. Veterinary Parasitology 84, 205–227.CrossRefGoogle Scholar
Halvorsen, O., Stien, A., Irvine, J., Longratn, R. and Albon, S. D. ( 1999). Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter. International Journal for Parasitology 29, 567–579.CrossRefGoogle Scholar
Harvell, C. D., Kim, K., Burkholder, J. M., Colwell, R. R., Epstein, P. R., Grimes, D. J., Hofmann, E. E., Lipp, E. K., Osterhaus, A. D. M. E., Overstreet, R. M., Porter, J. W., Smith, G. W. and Vasta, G. R. ( 1999). Review: Marine ecology – emerging marine diseases – climate links and anthropogenic factors. Science 285, 1505–1510.CrossRefGoogle Scholar
Hendriksen, S. A. ( 1965). En forbedret teknik ved undersogelse for lungeormelarver i faeces. Nordic Veterinary Medicine 17, 446–454.Google Scholar
Hoberg, E. P., Kocan, A. A. and Richard, L. G. ( 2001). Gastrointestinal strongyles in wild ruminants. In Parasitic Diseases of Wild Mammals ( ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 193–227. Manson Publishing/Veterinary Press, London.CrossRef
Houdijk, J. G., Kyriazakis, I., Jackson, F. and Coop, R. L. ( 2001). The relationship between protein nutrition, reproductive effort and breakdown in immunity to Teladorsagia circumcincta in periparturient ewes. Animal Science 72, 595–606.CrossRefGoogle Scholar
Hudson, P. J. and Dobson, A. P. ( 1995). Macroparasites: observed patterns in naturally fluctuating animal populations. In Ecology of Infectious Diseases in Natural Populations ( ed. Dobson, A. P. and Grenfell, B. T.), pp. 144–169. Cambridge University Press, Cambridge.CrossRef
Hudson, P. J., Dobson, A. P. and Newborn, D. ( 1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle Scholar
Hutchings, M. R., Kyriazakis, I., Papachristou, T. G., Gordon, I. J. and Fackson, F. ( 2000). The herbivores' dilemma: trade-offs between nutrition and parasitism in foraging decisions. Oecologia 1245, 242–251.CrossRefGoogle Scholar
Irvine, R. J., Stien, A., Halvorsen, O., Langvatn, R. and Albon, S. D. ( 2000). Life history strategies and population dynamics of abomasal nematodes in Svalbard reindeer (Rangifer tarandus plathyrhynchus). Parasitology 120, 297–311.CrossRefGoogle Scholar
Lloyd, S. ( 1995). Environmental influences on host immunity. In Ecology of Infectious Diseases in Natural Populations ( ed. Dobson, A. P. and Grenfell, B. T.), pp. 144–176. Cambridge University Press.CrossRef
Lowe, V. P. W. ( 1969). Population dynamics of red deer (Cervus elaphus) on Rhum. Journal of Animal Ecology 38, 425–457.CrossRefGoogle Scholar
Lowe, V. P. W. ( 1967). Teeth as indicators of age with special reference to red deer (Cervus elaphus L.) of known age from Rhum. Journal of Zoology 152, 137–153.Google Scholar
Madhusudan, M. D. ( 2004). Recovery of wild large herbivores following livestock decline in a tropical Indian wildlife reserve. Journal of Applied Ecology 41, 858–869.CrossRefGoogle Scholar
MAFF/ADAS. ( 1986). Manual of Veterinary Parasitological Techniques. Reference Book 418 – HMSO, London.
May, R. M. and Anderson, R. M. ( 1978). Regulation and stability of host parasite population interactions: II. Destabilising processes. Journal of Animal Ecology 47, 249–267.CrossRefGoogle Scholar
Mitchell, B., McGowan, D. and Nicholson, I. A. ( 1976). Annual cycles of body weight and condition in Scottish red deer, Cervus elaphus. Journal of Zoology 180, 107–127.CrossRefGoogle Scholar
Moen, A. N. ( 1978). Seasonal changes in heart rates-activity, metabolism and forage intake of white tailed deer. Journal of Wildlife Management 42, 715–738.CrossRefGoogle Scholar
Moore, S. L. and Wilson, K. ( 2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015.CrossRefGoogle Scholar
Murray, D. L., Cary, J. R. and Keith, L. B. ( 1997). Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology 66, 250–264.CrossRefGoogle Scholar
Mysterud, A., Langvatn, R., Yoccoz, N. G., and Stenseth, N. C. ( 2002). Large-scale habitat variability, delayed density effects and red deer populations in Norway. Journal of Animal Ecology 71, 569–580.CrossRefGoogle Scholar
Newey, S., Shaw, D. J., Kirby, A., Montieth, P., Hudson, P. J. and Thirgood, S. J. ( 2005). Prevalence, intensity and aggregation of intestinal parasites in mountain hares and their potential impact on population dynamics. International Journal for Parasitology 35, 367–373.CrossRefGoogle Scholar
Newey, S. and Thirgood, S. ( 2004). Parasite-mediated reduction in fecundity of mountain hares. Proceedings of the Royal Society of London, B 271 (Suppl 6.) S413–S415.CrossRefGoogle Scholar
Pacala, S. W. and Dobson, A. D. ( 1988). The relation between the number of parasites/host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle Scholar
Parkins, J. J., Taylor, L. M., Holmes, P. H., Bairden, K., Salman, S. K. and Armour, J. ( 1990). Pathophysiological and and parasitological studis on concurrent infection of Ostertagia ostertagi and Cooperia oncophora in calves. Research in Veterinary Science 48, 201–208.Google Scholar
SAS v8.1, SAS Institute Inc., Cary, NC, USA.
Soulsby, E. J. L. ( 1982). Helminths, Arthropods and Protozoa of Domesticated Animals, 7th Edn. Baillière Tindall, London.
Stien, A., Irvine, R. J., Ropstad, E., Halvorsen, O., Langvatn, R. and Albon, S. D. ( 2002). The impact of gastrointestinal nematodes on wild reindeer: experimental and cross – sectional studies. Journal of Animal Ecology 71, 937–945.CrossRefGoogle Scholar
Suttie, M. J. ( 1983). The relationship between kidney fat index and marrow fat percentage as indicators of condition in Red deer stags (Cervus elaphus). Journal of Zoology 201, 563–565.Google Scholar
Tompkins, D. M., Draycott, R. A. H. and Hudson, P. J. ( 2000). Field evidence for apparent competition mediated via the shared parasites of two gamebird species. Ecology Letters 3, 10–14.CrossRefGoogle Scholar
Wilson, K. and Grenfell, B. T. ( 1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle Scholar
Wilson, K., Grenfell, B. T. and Shaw, D. J. ( 1996). Analysis of aggregated parasite distributions: A comparison of methods. Functional Ecology 10, 592–601.CrossRefGoogle Scholar
Wilson, K., Grenfell, B. T., Pilkington, J. G., Boyd, H. E. G. and Gulland, F. M. D. ( 2004). Parasites and their impact. In Soay Sheep: Dynamics and Selection in an Island Population ( ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 113–165. Cambridge University Press, Cambridge.
Xiao, L. and Gibbs, H. C. ( 1992). Nutritional and pathophysiological effects of clinically apparent and subclinical infections of Ostertagia ostertagi in calves. American Journal of Veterinary Research 53, 2013–2018.Google Scholar