Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-05T16:29:21.421Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal host-parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.) as revealed by stable isotope analyses

Published online by Cambridge University Press:  25 April 2005

R. NEILSON ,
B. BOAG  and
G. HARTLEY
R. NEILSON
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA
B. BOAG
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA
G. HARTLEY
Affiliation:
Scottish Agricultural Science Agency, 82 Craigs Road, East Craigs, Edinburgh EH12 8NJ
Get access Rights & Permissions [Opens in a new window]

Abstract

Natural abundances of the stable isotopes, 15N/14N (δ15N) and 13C/12C (δ13C), were used to study temporal host-parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.). During the 12-month sampling period, temporal isotopic shifts in δ15N were noted for dietary vegetation, host rabbit faeces and fur, but not for muscle or stomach contents. δ15N varied temporally for the parasitic cestode species, Mosgovoyia pectinata but not for Cittotaenia denticulata. Similarly, intestinal parasitic nematodes had apparent species-specific δ15N patterns. Only rabbit fur and intestinal parasitic nematodes did not exhibit temporal shifts in δ13C. Overall, host faeces and stomach contents were isotopically indistinct as a likely consequence of coprophagy. Relative to their host, parasitic nematodes were 15N-enriched, consistent with an increase in trophic level status. Conversely, cestodes were 15N-depleted. Isotopically, each parasite reflected a species-specific relationship with their rabbit host. This technique could be utilized to integrate parasites into food-web studies.

Keywords

host-parasite interactionsrabbitstable isotopestrophic interactions
Type
Research Article
Information
Parasitology , Volume 131 , Issue 2 , August 2005 , pp. 279 - 285
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

AMES, A. L., VAN VLEET, E. S. & SACKETT, W. M. ( 1996). The use of stable carbon isotope analysis for determining the dietary habits of the Florida manatee, Trichechus manatus latirostris. Marine Mammal Science 12, 555–563.CrossRefGoogle Scholar
BARKER, I. K. & FORD, G. E. ( 1975). Development and distribution of atrophic enteritis in the small intestine of rabbits infected with Trichostrongylus retortaeformis. Journal of Comparative Pathology 85, 427–435.CrossRefGoogle Scholar
BARRETT, J. ( 1981). Biochemistry of Parasitic Helminths. Macmillan, London.CrossRef
BEN-DAVID, M., FLYNN, R. W. & SCHELL, D. M. ( 1997). Annual and seasonal changes in diets of martens: evidence from stable isotope analysis. Oecologia 111, 280–291.CrossRefGoogle Scholar
BJÖRNHAG, G. ( 1994). Adaptations in the large intestine allowing small animals to eat fibrous food. In The Digestive System in Mammals (ed. Chivers, D. J & Langer, P.), Cambridge University Press, Cambridge.CrossRef
BOAG, B. ( 1972). Helminth parasites of the wild rabbit Oryctolagus cuniculus (L.) in North East England. Journal of Helminthology 46, 73–79.Google Scholar
BOAG, B. ( 1988). Population dynamics of parasites of the wild rabbit (Oryctolagus cuniculus L.). In Mammals as Pests. ( ed. Putman, R. J.), pp. 186–195. Chapman and Hall, London.
BOAG, B., NEILSON, R., ROBINSON, D., SCRIMGEOUR, C. M. & HANDLEY, L. L. ( 1998). Wild rabbit host and some parasites show trophic-level relationships for δ13C and δ15N: a first report. Isotopes in Environmental and Health Studies 34, 81–85.CrossRefGoogle Scholar
CHAMBERLAIN, P. J., BULL, I. D., BLACK, H. I. J., INESON, P. & EVERSHED, R. P. ( 2004). Lipid content and carbon assimilation in Collembola: implications for the use of compound-specific carbon isotope analysis in animal dietary studies. Oecologia 139, 325–335.CrossRefGoogle Scholar
CHANG, S. X. & HANDLEY, L. L. ( 2000). Site history affects soil and plant 15N natural abundances (δ15N) in forests of northern Vancouver Island, British Columbia. Functional Ecology 14, 273–280.CrossRefGoogle Scholar
COWAN, D. P. ( 1991). Lagomorphs: Order Lagomorpha. In The Handbook of British Mammals (ed. Corbet, G. B. & Harris, S.), pp. 146–175. Blackwell Scientific Publications, Oxford.
DENIRO, M. J. & EPSTEIN, S. ( 1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
DENIRO, M. J. & EPSTEIN, S. ( 1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.CrossRefGoogle Scholar
DEUDERO, S., PINNEGAR, J. K. & POLUNIN, N. V. C. ( 2002). Insights into fish host-parasite trophic relationships revealed by stable isotope analysis. Diseases of Aquatic Organisms 52, 77–86.CrossRefGoogle Scholar
DOUCETT, R. R., GIBERSON, D. J. & POWER, G. ( 1999). Parasitic association of Nanocladius (Diptera: Chironomidae) and Pteronarcys biloba (Plecoptera: Pteronarcyidae): insights from stable-isotope analysis. Journal of the North American Benthological Society 18, 514–523.CrossRefGoogle Scholar
EVANS, C. J., EVERSHED, R. P., BLACK, H. I. J. & INESON, P. ( 2003). Compound-specific stable isotope analysis of soil mesofauna using thermally assisted hydrolysis and methylation for ecological investigations. Analytical Chemistry 75, 6056–6062.CrossRefGoogle Scholar
FARQUHAR, G. D. & RICHARDS, R. A. ( 1984). Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 10, 205–226.CrossRefGoogle Scholar
FOCKEN, U. & BECKER, K. ( 1998). Metabolic fractionation of stable carbon isotopes: implications of different proximate compositions for studies of aquatic food webs using δ13C data. Oecologia 115, 337–343.CrossRefGoogle Scholar
FRAYHA, G. J. & SMYTH, J. D. ( 1983). Lipid metabolism in parasitic helminths. Advances in Parasitology 22, 309–387.CrossRefGoogle Scholar
GODLEY, B. J., THOMPSON, D. R., WALDRON, S. & FURNESS, R. W. ( 1998). The trophic status of marine turtles as determined by stable isotope analysis. Marine Ecology Progress Series 166, 277–284.CrossRefGoogle Scholar
HANDLEY, L. L. & SCRIMGEOUR, C. M. ( 1997). Terrestrial plant ecology and 15N natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish Old Field. Advances in Ecological Research 27, 133–212.CrossRefGoogle Scholar
HARE, P. E., FOGEL, M. L., STAFFORD, J. T. W., MITCHELL, A. D. & HOERING, T. C. ( 1991). The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. Journal of Archaeological Science 18, 277–292.CrossRefGoogle Scholar
HILDERBRAND, G. V., FARLEY, S. D., ROBBINS, C. T., HANLEY, T. A., TITUS, K. & SERVHEEN, C. ( 1996). Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology 74, 2080–2088.CrossRefGoogle Scholar
HIRAKAWA, H. ( 2001). Coprophagy in leporids and other mammalian herbovires. Mammal Review 31, 61–80.CrossRefGoogle Scholar
HOBSON, K. A. ( 1993). Trophic relationships among high Arctic seabirds: insights from tissue-dependent stable-isotope models. Marine Ecology Progress Series 95, 7–18.CrossRefGoogle Scholar
HOBSON, K. A., ALISAUKAS, R. T. & CLARK, R. G. ( 1993). Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95, 388–394.CrossRefGoogle Scholar
HOBSON, K. A. & CLARK, R. G. ( 1992). Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94, 181–188.CrossRefGoogle Scholar
HOBSON, K. A., DREVER, M. C. & KAISER, G. W. ( 1999). Norway rats as predators of burrow-nesting seabirds: insights from stable isotope analyses. Journal of Wildlife Management 63, 14–25.CrossRefGoogle Scholar
HOBSON, K. A. & SEALY, S. G. ( 1991). Marine protein contributions to the diet of northern saw-whet owls on the Queen Charlotte Islands: a stable isotope approach. Auk 108, 114–132.Google Scholar
HOBSON, K. A. & WELCH, H. E. ( 1992). Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84, 9–18.CrossRefGoogle Scholar
IKEN, K., BREY, T., WAND, U., VOIGHT, J. & JUNGHANS, P. ( 2001). Food web structure of the benthic community at Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Progress in Oceanography 50, 383–405.CrossRefGoogle Scholar
JACOBSEN, N. S. & FAIRBURN, D. ( 1967). Lipid metabolism in helminth parasites. III. Biosynthesis and interconversion of fatty acids by Hymenolepis diminuta (Cestoda). Journal of Parasitology 53, 355–361.Google Scholar
KÖHLER, P. & VOIGHT, W. P. ( 1988). Nutrition and metabolism. In Parasitology in Focus: Facts and Trends. ( ed. Mehlhorn, H.), pp. 412–453. Springer-Verlag, Berlin.CrossRef
LEVER, C. ( 1977). The Naturalised Animals of the British Isles. Hutchinson, London.
MACKO, S., FOGEL, M. L., HARE, P. E. & HOERING, T. C. ( 1987). Isotopic fractionation of nitrogen and carbon in the synthesis of amino acids by microorganisms. Chemical Geology 65, 79–92.CrossRefGoogle Scholar
MADSEN, H. ( 1939). Does the rabbit chew the cud? Nature, London 143, 981–982.Google Scholar
MARCOGLIESE, D. J. & CONE, D. K. ( 1997). Food webs: a plea for parasites. Trends in Ecology and Evolution 12, 320–325.CrossRefGoogle Scholar
MILLS, S. ( 1986). Rabbits breed a growing controversy. New Scientist 109, 50–54.Google Scholar
MINAGAWA, M. & WADA, E. ( 1984). Stepwise enrichment of 15N along food chains, further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.CrossRefGoogle Scholar
MIZUTANI, H., HASEGAWA, H. & WADA, E. ( 1986). High nitrogen isotope ratio for soils of seabird rookeries. Biogeochemistry 2, 221–247.CrossRefGoogle Scholar
NEILSON, R., BOAG, B. & SMITH, M. ( 2000). Earthworm δ13C and δ15N analyses suggest that putative functional classifications of earthworms are site-specific and may also indicate habitat diversity. Soil Biology and Biochemistry 32, 1053–1061.CrossRefGoogle Scholar
NEILSON, R. & BROWN, D. J. F. ( 1999). Feeding on different host plants alters the natural abundances of δ13C and δ15N in Longidoridae (Nemata). Journal of Nematology 31, 20–26.Google Scholar
NEILSON, R. & BROWN, D. J. F. ( 2000). Natural abundances of 15N and 13C indicating physiological responses in Petunia hybrida to infection by longidorid nematodes and nepoviruses. Nematology 1, 315–320.Google Scholar
NEILSON, R., HAMILTON, D., WISHART, J., MARRIOTT, C. A., BOAG, B., HANDLEY, L. L., SCRIMGEOUR, C. M., MCNICOL, J. W. & ROBINSON, D. ( 1998). Stable isotope natural abundances of soil, plants and soil invertebrates in an upland pasture. Soil Biology and Biochemistry 30, 1773–1782.CrossRefGoogle Scholar
NEILSON, R., ROBINSON, D., MARRIOTT, C. A., SCRIMGEOUR, C. M., HAMILTON, D., WISHART, J., BOAG, B. & HANDLEY, L. L. ( 2002). Above-ground grazing affects floristic composition and modifies soil trophic interactions. Soil Biology and Biochemistry 34, 1507–1512.CrossRefGoogle Scholar
PETERSON, B. J. & FRY, B. ( 1987). Stable isotopes in ecosystem studies. Annual Review of Ecology Evolution and Systematics 18, 293–320.CrossRefGoogle Scholar
PINNEGAR, J. K. & POLUNIN, N. V. C. ( 1999). Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.CrossRefGoogle Scholar
PINNEGAR, J. K., CAMPBELL, N. & POLUNIN, N. V. C. ( 2001). Unusual stable isotope, fractionation patterns observed for fish host-parasite trophic relationships. Journal of Fish Biology 59, 494–503.Google Scholar
POLLARD, E., HOOPER, M. D. & MOORE, N. W. ( 1974). Hedges. Collins, London.
RAMSAY, M. A. & HOBSON, K. A. ( 1991). Polar bears make little use of terrestrial food webs: evidence from stable-carbon isotope analysis. Oecologia 86, 598–600.CrossRefGoogle Scholar
ROBINSON, D. ( 2001). δ15N as an integrator of the nitrogen cycle. Trends in Ecology and Evolution 16, 153–162.CrossRefGoogle Scholar
SCRIMGEOUR, C. M., GORDON, S. C., HANDLEY, L. L. & WOODFORD, J. A. T. ( 1995). Trophic levels and anomalous δ15N of insects on raspberry (Rubus idaeus L.). Isotopes in Environmental and Health Studies 31, 107–115.CrossRefGoogle Scholar
SMYTH, J. D. ( 1994). Physiology of cestodes. In Introduction to Animal Parasitology, pp. 349–367. Cambridge University Press, Cambridge.
STENHOUSE, M. J. & BAXTER, M. S. ( 1979). The uptake of bomb 14C in humans. In Radiocarbon Dating (ed. Berger, R. & Suess, H.), pp. 324–341. University of California Press, Berkeley.
STEWART, G. R., TURNBULL, M. H., SCHMIDT, S. & ERSKINE, P. D. ( 1995). 13C natural abundance in plant communities along a rainfall gradient: a biological integrator of water availability. Australian Journal of Plant Physiology 22, 51–55.CrossRefGoogle Scholar
TAYLOR, E. L. ( 1939). Does the rabbit chew the cud? Nature, London 143, 982–983.Google Scholar
THOMPSON, H. V. & KING, C. M. ( 1994). The European Rabbit: the History and Biology of a Successful Coloniser. Oxford University Press, Oxford.
TIESZEN, L. L., BOUTTON, T. W., TESDAHL, K. G. & SLADE, N. A. ( 1983). Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.CrossRefGoogle Scholar
TIESZEN, L. L., HEIN, D., QVORTRUP, S. A., TROUGHTON, J. H. & IMBAMBA, S. K. ( 1979). Use of δ13C values to determine vegetation selectivity in East African herbivores. Oecologia 37, 351–359.CrossRefGoogle Scholar
WADA, E., KABAYA, Y. & KURIHARA, Y. ( 1993). Stable isotope structure of aquatic ecosystems. Journal of Biosciences 18, 483–499.CrossRefGoogle Scholar