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Variability in the intensity of nematode larvae from gastrointestinal tissues of a natural herbivore

Published online by Cambridge University Press:  25 January 2013

ANDREW T. VAN KUREN ,
BRIAN BOAG ,
EMILIE HRUBAN  and
ISABELLA M. CATTADORI
ANDREW T. VAN KUREN
Affiliation:
Center for Infectious Disease Dynamics and Department of Biology, The Pennsylvania State University, University Park PA 16802, USA
BRIAN BOAG
Affiliation:
The James Hutton Institute, Invergowrie DD2 5DA, UK
EMILIE HRUBAN
Affiliation:
Center for Infectious Disease Dynamics and Department of Biology, The Pennsylvania State University, University Park PA 16802, USA
ISABELLA M. CATTADORI*
Affiliation:
Center for Infectious Disease Dynamics and Department of Biology, The Pennsylvania State University, University Park PA 16802, USA
*
*Corresponding author: Center for Infectious Disease Dynamics, Department of Biology, 128W Millennium Science Complex, The Pennsylvania State University, University Park, PA 16802USA. Tel: ++ 814 8659694. Fax: ++ 814 8659131. E-mail: imc3@psu.edu
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Summary

The migration of infective nematode larvae into the tissues of their hosts has been proposed as a mechanism of reducing larval mortality and increase parasite lifetime reproductive success. Given that individual hosts differ in the level of exposure, strength of immune response and physiological conditions we may expect the number of larvae in tissue to vary both between and within hosts. We used 2 gastrointestinal nematode species common in the European rabbit (Oryctolagus cuniculus) and examined how the number of larvae in the tissue changed with the immune response, parasite intensity-dependent constraints in the lumen and seasonal weather factors, in rabbits of different age, sex and breeding status. For both nematode species, larvae from the gastrointestinal tissue exhibited strong seasonal and host age-related patterns with fewer larvae recovered in summer compared to winter and more in adults than in juveniles. The number of larvae of the 2 nematodes was positively associated with intensity of parasite infection in the lumen and antibody responses while it was negatively related with air temperature and rainfall. Host sex, reproductive status and co-infection with the second parasite species contributed to increase variability between hosts. We concluded that heterogeneities in host conditions are a significant cause of variability of larval abundance in the gastrointestinal tissues. These findings can have important consequences for the dynamics of nematode infections and how parasite's life-history strategies adjust to host changes.

Keywords

infective larvaegastrointestinal tissueseasonalityantibodiesGraphidium strigosumTrichostrongylus retortaeformisEuropean rabbit
Type
Research Article
Information
Parasitology , Volume 140 , Issue 5 , April 2013 , pp. 632 - 640
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Anderson, R. C. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission. CABI Publishing, Wallingford, Oxon, UK.Google Scholar
Armour, J. and Duncan, M. (1987). Arrested larval development in cattle nematodes. Parasitology Today 3, 171–176.CrossRefGoogle ScholarPubMed
Ashworth, S. T. and Kennedy, C. R. (1999). Density-dependent effects on Anguillicola crassus (Nematoda) within its European eel definitive host. Parasitology 118, 289–296.Google Scholar
Audebert, F. J., Cassone, J. H., Hoste, H. and Durette-Desset, M. C. (2000). Morphogenesis and distribution of Trichostrongylus retortaeformis in the intestine of the rabbit. Journal of Helminthology 74, 95–107.Google Scholar
Audebert, F. and Durette-Desset, M. C. (2007). Do lagomorphs play a relay role in the evolution of the Trichostrongylina nematodes? Parasite 14, 183–197.CrossRefGoogle ScholarPubMed
Audebert, F., Hoste, H. and Durette-Desset, M. C. (2002). Life cycle of Trichostrongylus retortaeformis in its natural host, the rabbit (Oryctolagus cuniculus). Journal of Helminthology 76, 189–192.Google Scholar
Audebert, F., Vuong, P. N. and Durette-Desset, M. C. (2003). Intestinal migrations of Trichostrongylus retortaeformis (Trichostrongylina, Trichostrongylidae) in the rabbit. Veterinary Research 112, 131–146.Google Scholar
Boag, B. (1985). The incidence of helminth parasites from the wild rabbit Oryctolagus cuniculus (L.) in Eastern Scotland. Journal of Helminthology 59, 61–69.Google Scholar
Borgsteede, F. H. M. and Eysker, M. (1987). Strains of cattle parasites in the Netherlands with different propensities for inhibited development. Veterinary Parasitology 24, 93–101.Google Scholar
Cattadori, I. M., Boag, B., Bjornstad, O. N., Cornell, S. J. and Hudson, P. J. (2005). Peak shift and epidemiology in a seasonal host-nematode system. Proceeding of The Royal Society of London, B 272, 1163–1169.Google Scholar
Cattadori, I. M., Boag, B. and Hudson, P. J. (2008). Parasite co-infection and interaction as drives of host heterogeneity. International Journal for Parasitology 38, 371–380.Google Scholar
Ciordia, H., Vegors, H. H. and Bizzell, W. E. (1957). Freezing procedures for greater flexibility in application of the digestive method for post-mortem recovery of cattle nematodes. Journal of Parasitology 43, 532–534.CrossRefGoogle ScholarPubMed
Connan, R. M. (1969). Studies on the inhibition of development of Ostertagia spp. in lambs. Journal of Helminthology 43, 287–292.Google Scholar
Chubb, J. C., Ball, M. A. and Parker, G. A. (2010). Living in intermediate hosts: evolutionary adaptations in larval helminths. Trends in Parasitology 26, 93–102.Google Scholar
Dunsmore, J. D. (1961). Effect of whole body irradiation and cortisone on the development of Ostertagia species in sheep. Nature, London 192, 139–140.Google Scholar
Eysker, M. (1978). Inhibition of the development of Trichostrongylus spp. as third stage larvae in sheep. Veterinary Parasitology 4, 29–33.CrossRefGoogle Scholar
Herd, R. P. and McNaught, D. J. (1975). Arrested development and the histotropic phase of Ascaridia galli in the chicken. International Journal for Parasitology 5, 401–406.Google Scholar
Herlich, H. (1956). A digestion method for post-mortem recovery of nematodes from ruminants. Proceedings of the Helminthological Society of Washington 23, 102–103.Google Scholar
Hewitson, J. P., Grainger, G. R. and Maizels, R. M. (2009). Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 1–11.Google Scholar
Hutchinson, G. W., Lee, E. H. and Fernando, M. A. (1972). Effects of variations in temperature on infective larvae and their relationship to inhibited development of Obeliscoides cuniculi in rabbits. Parasitology 65, 333–342.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.) Journal of Parasitology 68, 131–133.CrossRefGoogle Scholar
Martin, W. B., Thomas, B. A. C. and Urquhart, G. M. (1957). Chronic diarrhoea in housed cattle due to atypical parasitic gastritis. Veterinary Records 69, 736–739.Google Scholar
Massoni, J., Cassone, J., Durette-Dusset, M. C. and Audebert, F. (2011). Development of Graphidium strigosum (Nematoda, Haemonchidae) in its natural host, the rabbit (Oryctolagus cuniculus) and comparison with several Haemonchidae parasities of ruminants. Parasitological Research 109, 25–36.Google Scholar
McKenna, P. B. (1973). The effect of storage on the infectivity and parasitic development of third-stage Haemonchus contortus larvae in sheep. Research in Veterinary Science 14, 312–316.Google Scholar
Michel, J. F. (1952). Inhibition of development of Trichostrongylus retortaeformis . Nature, London 169, 933–934.Google Scholar
Michel, J. F. (1974). Arrested development of nematodes and some related phenomena. Advances in Parasitology 12, 274–366.Google Scholar
Michel, J. F. (1978). Topical themes in the study of arrested development. In Facts and Reflections III, Arrested Development of Nematodes in Sheep and Cattle (ed. Borgsteede, F. H. M., Armour, J. and Jansen, J.), pp. 7–24. Central Veterinary Institute, Lelystad, The Netherlands.Google Scholar
Mulcahy, G., O'Neill, S., Fanning, J., McCarthy, E. and Sekiya, M. (2005). Tissue migration by parasitic helminths – an immunoevasive strategy? Trends in Parasitology 21, 273–277.Google Scholar
Murphy, L., Nalpas, N., Stear, M. and Cattadori, I. M. (2011). Explaining patterns of infection in free-living populations using laboratory immune experiments. Parasite Immunology 33, 287–302.Google Scholar
Parker, G. A., Ball, M. A. and Chubb, J. C. (2009). Why do larval helminths avoid the gut of intermediate hosts? Journal of Theoretical Biology 260, 460–473.CrossRefGoogle ScholarPubMed
Pathak, A. K., Pelenski, C., Boag, B. and Cattadori, I. M. (2012). Immuno-epidemiology of chronic bacteria-helminth co-infections: observations from the field and evidences from the laboratory. Interntional Journal for Parasitology 42, 647–655.CrossRefGoogle Scholar
Read, A. F. and Skorping, A. (1995). The evolution of tissue migration by parasitic nematode larvae. Parasitology 111, 359–371.Google Scholar
Smith, W. D., Jackson, F., Jackson, E. and Williams, J. (1983). Local immunity and Ostertagia circumcincta: changes in the gastric lymph of immune sheep after a challenge infection. Journal Comparative Pathology 93, 479–488.CrossRefGoogle ScholarPubMed
Sommerville, R. I. and Davey, K. G. (2002). Diapause in parasitic nematodes: a review. Canadian Journal of Zoology 80, 1817–1840.Google Scholar
Thakar, J., Pathak, A. K., Murphy, L., Albert, R. and Cattadori, I. M. (2012). Network model of immune responses reveals key effectors to single and co-infection kinetics by a respiratory bacterium and a gastrointestinal helminth. PLoS Computational Biology 8, e1002345.Google Scholar
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