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Chapter Twenty-one - Processes generating heterogeneities in infection and transmission in a parasite–rabbit system

from Part III - Understanding wildlife disease ecology at the community and landscape level

Published online by Cambridge University Press:  28 October 2019

By
Isabella M. Cattadori ,
Ashutosh Pathak  and
Brian Boag
Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
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Summary

Infection severity and persistence in a host population is affected by variation in host susceptibility. External disturbance can exacerbate/reduce individual variation by affecting the interactions between the host and its parasites and the dynamics of infection and transmission. We investigated the impact of three sources of disturbance (climate change, the presence of a second parasite species and anthelmintic treatment) on the dynamics of infection and shedding of three common parasites of the rabbit. Data were collected from long-term field studies and laboratory experiments and analysed using mathematical modelling and analytical tools. Our studies show that they all affect host–parasite interactions by altering the intensity of infection and/or the degree of parasite shedding. They also generate patterns of infections that could not have been predicted in the absence of these disturbances or from performing analyses at a different temporal scale. Modelling simulations confirmed the complexity of the processes involved and identified the critical interactions shaping the patterns observed.

Keywords

host heterogeneityhost immunityhost ageenvironmental disturbanceclimate warmingseasonalityanthelminthic treatmenthost–parasite interactionparasite–parasite interactionscoinfectionsgastrointestinal helminthsrespiratory bacteriumEuropean rabbit
Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 598 - 622
Publisher: Cambridge University Press
Print publication year: 2019

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References

Allen, J.E. & Maizels, R.M. (2011) Diversity and dialogue in immunity to helminths. Nature Reviews Immunology, 11, 375–388.Google Scholar
Allen, J.E. & Sutherland, T.E. (2014) Host protective roles of type 2 immunity: parasite killing and tissue repair, flip sides of the same coin, Seminars in Immunology, 26, 329–340.Google Scholar
Allotey, P. & Gyapong, M. (2008) Gender in tuberculosis research. International Journal of Tuberculosis and Lung Disease, 12, 831–836.Google Scholar
Anderson, R.M. & Gordon, D.M. (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology, 85, 373–398.Google Scholar
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions I: regulatory processes. Journal of Animal Ecology, 47, 219–247.CrossRefGoogle Scholar
Anthony, R.M., Rutitzky, L.I., Urban, J.F., Stadecker, M.J. & Gause, W.C. (2007) Protective immune mechanisms in helminth infection. Nature Reviews Immunology, 7, 975–987.CrossRefGoogle ScholarPubMed
Audebert, F., Cassone, J., Hoste, H. & 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. & 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., Vuong, P.N. & Durette-Desset, M.C. (2003) Intestinal migrations of Trichostrongylus retortaeformis (Trichostrongylina, Trichostrongylidae) in the rabbit. Veterinary Parasitology, 112, 131–146.Google Scholar
Blackwell, A.D., Gurven, M.D., Sugiyama, L.S., et al. (2011) Evidence for a peak shift in a humoral response to helminths: age profiles of IgE in the Shuar of Ecuador, the Tsimane of Bolivia, and the US NHANES. PLoS Neglected Tropical Diseases, 5, e1218.CrossRefGoogle Scholar
Blackwell, A.D., Martin, M., Kaplan, H. & Gurven, M. (2013) Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proceedings of the Royal Society of London B, 280, 20131671.Google Scholar
Bleay, C., Wilkes, C.P., Paterson, S. & Viney, M.E. (2007) Density-dependent immune responses against the gastrointestinal nematode Strongyloides ratti. International Journal for Parasitology, 37, 1501–1509.Google Scholar
Bowers, R.G. (1999) A baseline model for the apparent competition between many host strains: the evolution of host resistance. Journal of Theoretical Biology, 200, 65–75.Google Scholar
Bourke, C.D., Maizels, R.M. & Mutapi, F. (2011) Acquired immune heterogeneity and its sources in human helminth infection. Parasitology, 138, 139–159.Google Scholar
Brady, M.T., O’Neill, S.M., Dalton, J.P. & Mills, K.H. (1999) Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infection and Immunity, 67, 5372–5378.Google Scholar
Brogden, K.A., Lehmkuhl, H.D. & Cutlip, R.C. (1998) Pasteurella haemolytica complicated respiratory infections in sheep and goats. Veterinary Research, 29, 233–254.Google ScholarPubMed
Brooker, S., Akhwale, W., Pullan, R., et al. (2007) Epidemiology of Plasmodium–helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. The American Journal of Tropical Medicine and Hygiene, 77(S6), 88–98.Google Scholar
Cattadori, I.M., Boag, B., Bjørnstad, O.N., Cornell, S. & Hudson, P.J. (2005) Immuno-epidemiology and peak shift in a seasonal host-nematode system. Proceedings of the Royal Society of London B, 272, 1163–1169.Google Scholar
Cattadori, I.M., Boag, B. & Hudson, P.J. (2008) Parasite co-infection and interaction as drivers of host heterogeneity. International Journal for Parasitology, 38, 371–380.CrossRefGoogle ScholarPubMed
Cattadori, I.M., Pathak, A.K. & Ferrari, M.J. (2019) Changes in helminth–host interactions under external disturbances: dynamics of infection, parasite traits and host immune responses. Under review.Google Scholar
Cattadori, I.M., Wagner, B.R., Wodzinski, L.A., et al. (2014) Infections do not predict shedding in co-infections with two helminths from a natural system. Ecology, 95, 1684–1692.Google Scholar
Chase-Topping, M., Gally, D., Low, C., Matthews, L. & Woolhouse, M. (2008) Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nature Reviews Microbiology, 6, 904–912.Google Scholar
Cizauskas, C.A., Turner, W.C., Pitts, N. & Getz, W.M. (2015) Seasonal patterns of hormones, macroparasites, and microparasites in wild African ungulates: the interplay among stress, reproduction, and disease. PLoS ONE, 10, 0120800.Google Scholar
Cornell, S., Bjørnstad, O.N., Cattadori, I.M., Boag, B. & Hudson, P.J. (2008) Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system. Proceedings of the Royal Society of London B, 275, 473–591.Google Scholar
Curtale, F., Wahab Hassanein, Y.A., Barduagni, P., et al. (2007) Human fascioliasis infection: gender differences within school-age children from endemic areas of the Nile Delta, Egypt. Transactions of the Royal Society of Tropical Medicine and Hygiene, 101, 155–160.Google Scholar
Duerr, H.P., Dietz, K. & Eichner, M. (2003) On the interpretation of age–intensity profiles and dispersion patterns in parasitological surveys. Parasitology, 126, 87–101.Google Scholar
Elias, D., Akuffo, H. & Britton, S. (2006) Helminths could influence the outcome of vaccines against TB in the tropics. Parasite Immunology, 28, 507–513.CrossRefGoogle ScholarPubMed
Gao, L., Zhou, F., Li, X. & Jin, Q. (2010) HIV/TB co-infection in mainland China: a meta-analysis. PLoS ONE, 5, e10736.Google Scholar
Garske, T. & Rhodes, C.J. (2008) The effect of superspreading on epidemic outbreak size distributions. Journal of Theoretical Biology, 253, 228–237.Google Scholar
Geerts, S. & Gryseels, S. (2000) Drug resistance in human helminths: current situation and lessons from livestock. Clinical Microbiology Reviews, 13, 207–222.Google Scholar
Ghosh, S., Ferrari, M.J., Pathak, A.K. & Cattadori, I.M. (2018). Changes in parasite traits, rather than intensity, affect the dynamics of infection under external perturbation. PLoS Computational Biology, 14(6), e1006167.Google Scholar
Girgis, N.M., Gundra, U.M. & Loke, P. (2013) immune regulation during helminth infections. PLoS Pathogens, 9, e1003250.Google Scholar
Graham, A., Cattadori, I.M., Lloyd-Smith, J., Ferrari, M. & Bjornstad, O.N. (2007) Transmission consequences of co-infection: cytokines writ large? Trends in Parasitology, 6, 284–291.Google Scholar
Grenfell, B. T. & Anderson, R. M. (1989) Pertussis in England and Wales: an investigation of transmission dynamics and control by mass vaccination. Proceedings of the Royal Society of London B, 236, 213–252.Google Scholar
Harvell, D., Altizer, S., Cattadori, I.M., Harrington, L. & Weil, E. (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology, 90, 912–920.Google Scholar
Hayes, K.S., Bancroft, A.J., Goldrick, M., et al. (2010) Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science, 328, 1391–1394.Google Scholar
Hernandez, A.D., Poole, A. & Cattadori, I.M. (2013) Climate changes influence free-living stages of soil-transmitted parasites of European rabbits. Global Change Biology, 19, 1028–1042.Google Scholar
Hoffman, R.S. & Smith, A.T. (2005) “Order Lagomorpha”. In: Wilson, D.E. & Reeder, D.M. (eds.), Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Baltimore, MD: Johns Hopkins University Press.Google Scholar
Hudson, P.J. & Dobson, A.P. (1989) Population biology of Trichostrongylus tenuis, a parasite of economic importance for red grouse management. Parasitology Today, 5, 283–291.CrossRefGoogle ScholarPubMed
Hudson, P.J., Perkins, S.E. & Cattadori, I.M. (2008) The emergence of wildlife disease and the application of ecology. In: Ostfeld, R. (ed.), Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems, (1st edn, pp. 347–367). Princeton, NJ: Princeton University Press.Google Scholar
Izhar, R. & Ben‐Ami, F. (2015) Host age modulates parasite infectivity, virulence and reproduction. Journal of Animal Ecology, 84, 1018–1028.Google Scholar
Jackson, D.W. & Rohani, P. (2014) Perplexities of pertussis: recent global epidemiological trends and their potential causes. Epidemiology and Infection, 142, 672–684.CrossRefGoogle ScholarPubMed
Jackson, J.A., Friberg, I.M., Little, S. & Bradley, J.E. (2009) Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology, 126, 18–27.Google Scholar
James, C.E., Hudson, A.L. & Davey, M.W. (2009) Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology, 25, 328–335.Google Scholar
Jia, T.W., Melville, S., Utzinger, J., King, C.H. & Zhou, X.N. (2012) Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases, 6, e1621.Google Scholar
Kao, R.R., Gravenor, M.B., Charleston, B., et al. (2007) Mycobacterium bovis shedding patterns from experimentally infected calves and the effect of concurrent infection with bovine viral diarrhoea virus. Journal of The Royal Society Interface, 4, 545–551.Google Scholar
Keiser, J. & Utzinger, J. (2008) Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. Journal of the American Medical Association, 299, 1937–1948.Google Scholar
Keymer, A. (1982) Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology, 84, 573–587.Google Scholar
Lass, S., Hudson, P.J., Thakar, J., et al. (2013) Generating super-shedders: co-infection increases bacterial load and egg production of a gastrointestinal helminth. Journal of the Royal Society Interface, 10, 20120588.Google Scholar
Lloyd-Smith, J.O., Schreiber, S.J., Kopp, P.E. & Getz, W.M. (2005) Superspreading and the effect of individual variation on disease emergence. Nature, 438, 355–359.Google Scholar
Luong, L.T., Vigliotti, B.A. & Hudson, P.J. (2011) Strong density-dependent competition and acquired immunity constrain parasite establishment: implications for parasite aggregation. International Journal for Parasitology, 41, 505–511.Google Scholar
Maizels, R.M. (2009) Parasite immunomodulation and polymorphisms of the immune system. Journal of Biology, 8, 62.Google Scholar
Massoni, J., Cassone, J., Durette-Desset, M.C. & Audebert, F. (2011) Development of Graphidium strigosum (Nematoda, Haemonchidae) in its natural host, the rabbit (Oryctolagus cuniculus) and comparison with several Haemonchidae parasites of ruminants. Parasitology Research, 109, 25–36.Google Scholar
McRae, K.M., Stear, M.J., Good, B. & Keane, O.M. (2015) The host immune response to gastrointestinal nematode infection in sheep. Parasite Immunology, 37, 605–613.Google Scholar
Mignatti, A., Boag, B. & Cattadori, I.M. (2016) Host immunity shapes the impact of climate changes on the dynamics of parasite infections. Proceedings of the National Academy of Sciences of the United States of America, 113, 2970–2975.Google Scholar
Miller, M. R., White, A. & Boots, M. (2005) The evolution of host resistance: tolerance and control as distinct strategies. Journal of Theoretical Biology, 236, 198–207.Google Scholar
Molnár, P.K., Kutz, S.J., Hoar, B.M. & Dobson, A.P. (2013) Metabolic approaches to understanding climate change impacts on seasonal host–macroparasite dynamics. Ecology Letters, 16, 9–21.Google Scholar
Murphy, L., Nalpas, N., Stear, M. & Cattadori, I.M. (2011) The role of immunity on the dynamics of chronic gastrointestinal nematode infections of rabbits. Parasite Immunology, 33, 287–302.Google Scholar
Murphy, L., Pathak, A.K. & Cattadori, I.M. (2013) A co-infection with two gastrointestinal nematodes alters host immune responses and only partially parasite dynamics. Parasite Immunology, 35, 421–432.Google Scholar
Pathak, A.K., Boag, B., Poss, M., Harvill, E. & Cattadori, I.M. (2011) Seasonal incidence of Bordetella bronchiseptica in an age-structured free-living rabbit population. Epidemiology and Infection, 14, 1–10.Google Scholar
Pathak, A.K., Creppage, K.E., Werner, J.R. & Cattadori, I.M. (2010) Immune regulation of a chronic bacteria infection and consequences for pathogen transmission. BMC Microbiology, 10, 226.Google Scholar
Pathak, A.K., Pelensky, C., Boag, B. & Cattadori, I.M. (2012) Immuno-epidemiology of chronic bacterial and helminth co-infections: observations from the field and evidence from the laboratory. International Journal for Parasitology, 42, 647–655.Google Scholar
Paull, S.H. & Johnson, P.T.J. (2014) Experimental warming drives a seasonal shift in the timing of host–parasite dynamics with consequences for disease risk. Ecology Letters, 4, 445–453.Google Scholar
Pedersen, A.B. & Antonovics, J. (2013) Anthelmintic treatment alters the parasite community in a wild mouse host. Biology Letters, 9, 20130205.Google Scholar
Poulin, R. (2007) Evolutionary Ecology of Parasites (2nd edn). Princeton, NJ: Princeton University Press.Google Scholar
Quinnell, R.J., Medley, G.F. & Keymer, A.E. (1990) The regulation of gastrointestinal helminth populations. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 330, 191–201.Google Scholar
Raberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812–814.Google Scholar
Raffel, T.R., Romansic, J.M., Halstead, N.T., et al. (2013) Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change, 3, 146–151.Google Scholar
Redpath, S.A., Fonseca, N.M. & Perona-Wright, G. (2014) Protection and pathology during parasite infection: IL-10 strikes the balance. Parasite Immunology, 36, 233–252.Google Scholar
Restif, O. & Koella, J.C. (2004) Concurrent evolution of resistance and tolerance to pathogens. The American Naturalist, 164, 90–102.Google Scholar
Reynolds, A., Lindström, J., Johnson, P.C. & Mable, B.K. (2016) Evolution of drug-tolerant nematode populations in response to density reduction. Evolutionary Applications, 9, 726–738.Google Scholar
Roy, B.A. & Kirchner, J.W. (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution, 54, 51–63.Google Scholar
Sabatelli, L., Ghani, A.C., Rodrigues, L.C., Hotez, P.J. & Brooker, S. (2008) Modelling heterogeneity and the impact of chemotherapy and vaccination against human hookworm parasite. Journal of the Royal Society Interface, 5, 1329–1341.Google Scholar
Stear, M.J. & Bishop, S.C. (1999) The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. International Journal for Parasitology, 29, 777–780.Google Scholar
Stear, M.J., Boag, B., Cattadori, I.M. & Murphy, L. (2009) Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification. Parasite Immunology, 31, 274–282.Google Scholar
Stear, M.J., Strain, S. & Bishop, S.C. (1999) Mechanisms underlying resistance to nematode infection. International Journal for Parasitology, 29, 51–56.Google Scholar
Thakar, J., Pathak, A.K., Murphy, L., Albert, R. & 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
Thompson, H.V. & King, C.M. (1994) The European Rabbit. Oxford: Oxford University Press.Google Scholar
Tompkins, D.M. & Hudson, P.J. (1999) Regulation of nematode fecundity in the ring-necked pheasant (Phasianus colchicus): not just density dependence. Parasitology, 118, 417–423.Google Scholar
Van Kuren, A., Boag, B., Hrubar, E. & Cattadori, I.M. (2013) Variability in the intensity of nematode larvae from gastrointestinal tissues of a natural herbivore. Parasitology, 140, 632–640.Google Scholar
Woolhouse, M.E.J. (1992) A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology, 14, 563–578.Google Scholar
Woolhouse, M.E. (1998) Patterns in parasite epidemiology: the peak shift. Parasitology Today, 14, 428–434.Google Scholar
Yazdanbakhsh, M. & Sacks, D.L. (2010) Why does immunity to parasites take so long to develop? Nature Reviews Immunology, 10, 80–81.Google Scholar

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