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Population biology of multispecies helminth infection: interspecific interactions and parasite distribution

  • C. BOTTOMLEY (a1), V. ISHAM (a2) and M.-G. BASÁÑEZ (a3)

Abstract

Despite evidence for the existence of interspecific interactions between helminth species, there has been no theoretical exploration of their effect on the distribution of the parasite species in a host population. We use a deterministic model for the accumulation and loss of adult worms of 2 interacting helminth species to motivate an individual-based stochastic model. The mean worm burden and variance[ratio ]mean ratio (VMR) of each species, and the correlation between the two species are used to describe the distribution within different host age classes. We find that interspecific interactions can produce convex age-intensity profiles and will impact the level of aggregation (as measured by the VMR). In the absence of correlated exposure, the correlation in older age classes may be close to zero when either intra- or interspecific synergistic effects are strong. We therefore suggest examining the correlation between species in young hosts as a possible means of identifying interspecific interaction. The presence of correlation between the rates of exposure makes the interpretation of correlations between species more difficult. Finally we show that in the absence of interaction, strong positive correlations are generated by averaging across most age classes.

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Centre for Mathematics and Physics in the Life Sciences and Experimental Biology (CoMPLEX), Wolfson House, 4 Stephenson Way, London NW1 2HE. Tel: +44 (0)20 7679 5063. E-mail: h.bottomley@ucl.ac.uk

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REFERENCES

Anderson, R. M. and Gordon, D. M. ( 1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373398.
Anderson, R. M. and May, R. M. ( 1985 a). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1101.
Anderson, R. M. and May, R. M. ( 1985 b). Herd immunity to helminth infection and implications for parasite control. Nature 315, 493496.
Anderson, R. M. and May, R. M. ( 1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.
Behnke, J. M., Bajer, A., Sinski, E. and Wakelin, D. ( 2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122 (Suppl.), S39S49.
Behnke, J. M., Gilbert, F., Abu-Madi, M. and Lewis, J. ( 2005). Do helminth parasites of wood mice interact? Journal of Animal Ecology (in the Press).
Booth, M., Vennervald, B. J., Butterworth, A. E., Kariuki, H. C., Amaganga, C., Kimani, G., Mwatha, J. K., Otedo, A., Ouma, J. H. and Dunne, D. W. ( 2004 a). Exposure to malaria affects the regression of hepatosplenomegaly after treatment for Schistosoma mansoni infection in Kenyan children. BMC Medicine 2, 36.
Booth, M., Vennervald, B. J., Kenty, L., Butterworth, A. E., Kariuki, H. C., Kadzo, H., Ireri, E., Amaganga, C., Kimani, G., Mwatha, J. K., Otedo, A., Ouma, J. H., Muchiri, E. and Dunne, D. W. ( 2004 b). Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children. BMC Infectious Diseases 4, 13.
Bundy, D., Sher, A. and Michael, E. ( 2000). Good worms or bad worms: do worm infections affect the epidemiological patterns of other diseases? Parasitology Today 16, 273274.
Bush, A. O. and Holmes, J. C. ( 1986). Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132141.
Byrne, C. J., Holland, C. V., Kennedy, C. R. and Poole, W. R. ( 2003). Interspecific interactions between acanthocephala in the intestine of brown trout: are they more frequent in Ireland? Parasitology 127, 399409.
Christensen, N. O., Nansen, P., Fagbemi, B. O. and Monrad, J. ( 1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.
Cox, F. E. G. ( 2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.), S23S38.
Dobson, A. P. ( 1985). The population dynamics of competition between parasites. Parasitology 91, 317347.
Duerr, H. P., Dietz, K. and Eichner, M. ( 2003). On the interpretation of age-intensity profiles and dispersion patterns in parasitological surveys. Parasitology 126, 87101.
Esch, G. and Fernandez, J. ( 1993). A Functional Biology of Parasitism: Ecological and Evolutionary Implications. Chapman and Hall, London.
Faulkner, H., Turner, J., Behnke, J., Kamgno, J., Rowlinson, M.-C., Bradley, J. and Boussinesq, M. ( 2005). Associations between filarial and gastrointestinal nematodes. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 301312.
Fenwick, A., Savioli, L., Engels, D., Bergquist, N. R. and Todd, M. H. ( 2003). Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Trends in Parasitology 19, 509515.
Fulford, A. J., Butterworth, A. E., Sturrock, R. F. and Ouma, J. H. ( 1992). On the use of age-intensity data to detect immunity to parasitic infections, with special reference of Schistosoma mansoni in Kenya. Parasitology 105, 219227.
Gatto, M. and De Leo, G. A. ( 1998). Interspecific competition among macroparasites in a density-dependent host population. Journal of Mathematical Biology 37, 467490.
Geiger, S., Hoffmann, W., Rapp, J., Schulz-Key, H. and Eisenbeiss, W. ( 1996). Filariidae: cross-protection in filarial infections. Experimental Parasitology 83, 352356.
Gems, D. ( 2000). Longevity and ageing in parasitic and free-living nematodes. Biogerontology 1, 289307.
Hall, A. and Holland, C. ( 2000). Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitology Today 16, 540544.
Harms, G. and Feldmeier, H. ( 2002). HIV infection and tropical diseases-deleterious interactions in both directions? Tropical Medicine and International Health 7, 479488.
Haukisalmi, V. and Henttonen, H. ( 1998). Analyzing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia 116, 565574.
Hayward, C. J., Perera, K. M. and Rohde, K. ( 1998). Assemblages of ectoparasites of a pelagic fish, slimy mackerel (Scomber australasicus), from south-eastern Australia. International Journal for Parasitology 28, 263273.
Herbert, J. and Isham, V. ( 2000). Stochastic host-parasite interaction models. Journal of Mathematical Biology 40, 343371.
Isham, V. ( 1995). Stochastic models of host-macroparasite interaction. The Annals of Applied Probability 5, 720740.
Jackson, J. A., Tinsley, R. C. and Hinkel, H. H. ( 1998). Mutual exclusion of congeneric monogenean species in a space-limited habitat. Parasitology 117, 563569.
Kennedy, C. ( 1975). Ecological Animal Parasitology. Blackwell Scientific Publications, Oxford.
Kleinbaum, D. G., Kupper, L. L., Muller, K. E. and Nizam, A. ( 1998). Applied Regression Analysis and other Multivariable Methods, 3rd Edn. Duxbury Press, Pacific Grove, USA.
Kuris, A. M. and Lafferty, K. D. ( 1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189217.
Leathwick, D., Miller, C., Brown, A. and Sutherland, I. ( 1999). The establishment rate of Ostertagia circumcincta and Trichostrongylus colubriformis in lactating Romney ewes. International Journal for Parasitology 29, 315320.
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. ( 2004). Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840844.
Lotz, J. M. and Font, W. F. ( 1994). Excess positive associations in communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398413.
Mariotti, S. P., Pararajasegaram, R. and Resnikoff, S. ( 2003). Trachoma: looking forward to global elimination of trachoma by 2020 (GET 2020). American Journal of Tropical Medicine and Hygiene 69, 3335.
Molyneux, D. H. and Zagaria, N. ( 2002). Lymphatic filariasis elimination: progress in global programme development. Annals of Tropical Medicine and Parasitology 96 (Suppl. 2), S15S40.
Moore, J. and Simberloff, D. ( 1990). Gastrointestinal helminth communities of bobwhite quail. Ecology 71, 344359.
Nacher, M. ( 2001). Malaria vaccine trials in a wormy world. Trends in Parasitology 17, 563565.
Nacher, M., Gay, F., Singhasivanon, P., Krudsood, S., Treeprasertsuk, S., Mazier, D., Vouldoukis, I. and Looareesuwan, S. ( 2000). Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunology 22, 107113.
Pacala, S. W. and Dobson, A. P. ( 1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197210.
Petney, T. N. and Ross, A. H. ( 1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377393.
Plaisier, A. P., van Oortmarssen, G. J., Remme, J. and Habbema, J. D. ( 1991). The reproductive lifespan of Onchocerca volvulus in West African savanna. Acta Tropica 48, 271284.
Poulin, R. ( 1998). Evolutionary Ecology of Parasites. Chapman and Hall, London.
Price, P. W. ( 1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton.
Quinnell, R. J. ( 2003). Genetics of susceptibility to human helminth infection. International Journal of Parasitology 33, 12191231.
Remme, J. H. F., Binka, F. and Nabarro, D. ( 2001). Toward a framework and indicators for monitoring roll back malaria. American Journal of Tropical Medicine and Hygiene 64, 7684.
Roberts, M. G. and Dobson, A. P. ( 1995). The population dynamics of communities of parasitic helminths. Mathematical Biosciences 126, 191214.
Sékétéli, A., Adeoye, G., Eyamba, A., Nnoruka, E., Drameh, P., Amazigo, U. V., Noma, M., Agboton, F., Aholou, Y., Kale, O. O. and Dadzie, K. Y. ( 2002). The achievements and challenges of the African Programme for Onchocerciasis Control (APOC). Annals of Tropical Medicine and Parasitology 96 (Suppl. 1), S15S28.
Sharma, D. K., Chauhan, P. P. and Agrawal, R. D. ( 2000). Interaction between Trypanosoma evansi and Haemonchus contortus infection in goats. Veterinary Parasitology 92, 261267.
Simberloff, D. ( 1990). Free-living communities and alimentary tract helminths: hypotheses and pattern analyses. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 289319. Chapman and Hall, London.
Tallis, G. M. and Leyton, M. ( 1966). A stochastic approach to the study of parasite populations. Journal of Theoretical Biology 13, 251260.
Tallis, G. M. and Leyton, M. ( 1969). Stochastic models of populations of helminthic parasites in the definitive host. I. Mathematical Biosciences 4, 3948.
Tchuem Tchuenté, L. A., Behnke, J. M., Gilbert, F. S., Southgate, V. R. and Vercruysse, J. ( 2003). Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine and International Health 8, 975986.
Thomas, J. D. ( 1964). Studies on populations of helminth parasites in brown trout (Salmo trutta L.). Journal of Animal Ecology 33, 8395.
Wahl, G., Enyong, P., Ngosso, A., Schibel, J. M., Moyou, R., Tubbesing, H., Ekale, D. and Renz, A. ( 1998). Onchocerca ochengi: epidemiological evidence of cross-protection against Onchocerca volvulus in man. Parasitology 116, 349362.
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. ( 2002). Heterogeneities in macroparasite infections: patterns and processes. In Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), chapter 2. Oxford University Press, Oxford.
Wong, M. S., Bundy, D. A. and Golden, M. H. ( 1988). Quantitative assessment of geophagus behaviour as a potential source of exposure to geohelminth infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 621625.
Woolhouse, M. E. J. ( 1992 a). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563578.
Woolhouse, M. E. J. ( 1992 b). Immunoepidemiology of intestinal helminths: pattern and process. Parasitology Today 8, 111.
Woolhouse, M. E. J., Ndamba, J. and Bradley, D. ( 1994). The interpretation of intensity and aggregation data for infections of Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 520526.

Keywords

Population biology of multispecies helminth infection: interspecific interactions and parasite distribution

  • C. BOTTOMLEY (a1), V. ISHAM (a2) and M.-G. BASÁÑEZ (a3)

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