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Modelling macroparasite aggregation using a nematode-sheep system: the Weibull distribution as an alternative to the Negative Binomial distribution?

Published online by Cambridge University Press:  25 April 2005

S. GABA
Affiliation:
INRA-Unité de Biométrie (UR 546), Domaine Saint Paul – Site Agroparc, 84814 Avignon cedex 9, France INRA-Unité BioAgresseurs, Santé et Environnement (UR 86), Equipe d'Ecologie et Génétique des Parasites, 37380 Nouzilly, France
V. GINOT
Affiliation:
INRA-Unité de Biométrie (UR 546), Domaine Saint Paul – Site Agroparc, 84814 Avignon cedex 9, France
J. CABARET
Affiliation:
INRA-Unité BioAgresseurs, Santé et Environnement (UR 86), Equipe d'Ecologie et Génétique des Parasites, 37380 Nouzilly, France

Abstract

Macroparasites are almost always aggregated across their host populations, hence the Negative Binomial Distribution (NBD) with its exponent parameter k is widely used for modelling, quantifying or analysing parasite distributions. However, many studies have pointed out some drawbacks in the use of the NBD, with respect to the sensitivity of k to the mean number of parasites per host or the under-representation of the heavily infected hosts in the estimate of k. In this study, we compare the fit of the NBD with 4 other widely used distributions on observed parasitic gastrointestinal nematode distributions in their sheep host populations (11 datasets). Distributions were fitted to observed data using maximum likelihood estimator and the best fits were selected using the Akaike's Information Criterion (AIC). A simulation study was also conducted in order to assess the possible bias in parameter estimations especially in the case of small sample sizes. We found that the NBD is seldom the best fit for gastrointestinal nematode distributions. The Weibull distribution was clearly more appropriate over a very wide range of degrees of aggregation, mainly because it was more flexible in fitting the heavily infected hosts. Moreover, the Weibull distribution estimates are less sensitive to sample size. Thus, when possible, we suggest to carefully check on observed data if the NBD is appropriate before conducting any further analysis on parasite distributions.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

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.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1982). Population dynamics of human helminth infections: control by chemotherapy. Nature, London 297, 557563.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1985). Age related changes in the rate of disease transmission: implications for the design of vaccination programmes. Journal of Hygiene 94, 365436.CrossRefGoogle Scholar
Barger, I. A. ( 1985). The statistical distribution of Trichostrongylid nematodes in grazing lambs. International Journal for Parasitology 15, 645649.CrossRefGoogle Scholar
Brown, S. P., Loot, G., Teriokhin, A., Brunel, A., Brunel, C. and Guegan, J. F. ( 2002). Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation? International Journal for Parasitology 32, 817824.Google Scholar
Burnham, K. P. and Anderson, D. R. ( 2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer-Verlag, New York.
Clark, J. S. ( 1998). Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. American Naturalist 152, 204224.CrossRefGoogle Scholar
Cornell, S. J., Isham, V. S., Smith, G. and Grenfell, B. T. ( 2003). Spatial parasite transmission, drug resistance and the spread of rare genes. Proceedings of the National Academy of Science, USA 100, 74017405.CrossRefGoogle Scholar
Denham, D. A. ( 1969). The development of Ostertagia circumcincta in lambs. Journal of Helminthology 43, 299310.CrossRefGoogle Scholar
Ebert, D., Lipsitch, M. and Mangin, K. ( 2000). The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. The American Naturalist 156, 459477.CrossRefGoogle Scholar
Elliot, J. M. ( 1977). Statistical Analysis of Samples of Benthic Invertebrates. Freshwater Biological Association, Ambleside, UK.
Githigia, S. M., Thamsborg, S. M. and Larsen, M. ( 2001). Effectiveness of grazing management in controlling gastrointestinal nematodes in weaner lambs on pasture in Denmark. Veterinary Parasitology 99, 115121.CrossRefGoogle Scholar
Gregory, R. D. and Woolhouse, M. E. J. ( 1993). Quantification of parasite aggregation – a simulation study. Acta Tropica 54, 131139.CrossRefGoogle Scholar
Gruner, L., Mandonnet, N., Bouix, J., Vu Tien Khang, J., Cabaret, J., Hoste, H., Kerboeuf, D. and Barnouin, J. ( 1994). Worm population characteristics and pathological changes in lambs after a single or trickle infection with Teladorsagia circumcincta. International Journal for Parasitology 24, 347356.CrossRefGoogle Scholar
Gruner, L., Bouix, J., Khang, J. V. T., Mandonnet, N., Eychenne, F., Cortet, J., Sauve, C. and Limouzin, C. ( 2004). A short-term divergent selection for resistance to Teladorsagia circumcincta in Romanov sheep using natural or experimental challenge. Genetics Selection Evolution 36, 217242.CrossRefGoogle Scholar
Hoste, H., Chartier, C. and Le Frileux, Y. ( 2002). Control of gastrointestinal parasitism with nematodes in dairy goats by treating the host category at risk. Veterinary Research 33, 531545.CrossRefGoogle Scholar
Keymer, A. E. and Anderson, R. M. ( 1979). The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: influence of infective-stage density and spatial distribution. Parasitology 79, 195207.CrossRefGoogle Scholar
Kotz, S., Johnson, N. L. and Read, R. C. B. ( 1982). Encyclopaedia of Statistical Sciences, in 9 volumes, pp 583587. Wiley New York, USA.
Leignel, V. ( 2000). Diversité génétique et résistance aux anthelminthiques chez Teladorsagia circumcincta (nematoda, Trichostrongyloidea) parasite de petits ruminants. Ph.D. thesis. University of Montpellier.
Pacala, S. W. and Dobson, A. P. ( 1988). The relation between the number of parasites host and host age per host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197210.CrossRefGoogle Scholar
Poulin, R. ( 1993). The disparity between observed and uniform distributions – a new look at parasite aggregation. International Journal for Parasitology 23, 937944.CrossRefGoogle Scholar
Poulin, R. ( 1998). Evolutionary Ecology of Parasites: From Individuals to Communities. Chapman and Hall, London.
Scott, M. E. ( 1987). Temporal changes in aggregation: a laboratory study. Parasitology 94, 583595.CrossRefGoogle Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597610.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. ( 1995). Patterns of macroparasites abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111 (Suppl.), S111S133.CrossRefGoogle Scholar
Smith, G. ( 1984). Density-dependent mechanisms in the regulation of Fasciola hepatica populations in sheep. Parasitology 88, 449461.CrossRefGoogle Scholar
Southwood, T. R. E. ( 1978). Ecological Methods with Particular Reference to the Study of Insect Populations, 2nd Edn. Chapman and Hall, London and New York.
Steel, J. W., Symons, L. E. A. and Jones, W. O. ( 1980). Effects of level of larval intake on the productivity and physiological and metabolic responses of lambs infected with Trichostrongylus colubriformis. Australian Journal of Agricultural Research 31, 821838.CrossRefGoogle Scholar
Taylor, L. R., Woiwood, I. P. and Perry, J. N. ( 1979). The negative binomial as a dynamic ecological model and the density dependence of k. Journal of Animal Ecology 47, 383406.CrossRefGoogle Scholar
Tufto, J., Engen, S. and Hindar, K. ( 1997). Stochastic dispersal processes in plant populations. Theoretical Population Biology 52, 1626.CrossRefGoogle Scholar
Wilson, K. and Grenfell, B. T. ( 1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 3338.CrossRefGoogle Scholar
Wilson, K., Bjornstad, O. N., Dobson, A. P., Merler, S., Poglaven, G., Randolph, S. E., Read, A. F. and Skorping, A. ( 2002). Heterogeneities in macroparasites infections: patterns and processes. In Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P.), pp. 644. Cambridge University Press, Cambridge.
Woolhouse, M. J. E., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J, Watts, C. H., Chandiwana, S. K. and Anderson, R. M. ( 1997). Heterogeneities in transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338342.CrossRefGoogle Scholar
Xiao, C. L., Subbarao, K. V. and Zeng, S. M. ( 1996). Incorporating an asymptotic parameter into the Weibull model to describe plant disease progress. Journal of Phytopathology 1144, 375382.CrossRefGoogle Scholar