Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T10:45:56.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Simple epidemiological model predicts the relationships between prevalence and abundance in ixodid ticks

Published online by Cambridge University Press:  11 October 2006

M. STANKO ,
B. R. KRASNOV ,
D. MIKLISOVA  and
S. MORAND
M. STANKO
Affiliation:
Institute of Zoology, Slovak Academy of Sciences, Lofflerova 10, SK-04001 Kosice, Slovakia
B. R. KRASNOV
Affiliation:
Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel Ramon Science Center, P.O. Box 194, Mizpe Ramon 80600, Israel
D. MIKLISOVA
Affiliation:
Institute of Zoology, Slovak Academy of Sciences, Lofflerova 10, SK-04001 Kosice, Slovakia
S. MORAND
Affiliation:
Center for Biology and Management of Populations, Campus International de Baillarguet, CS 30016 34988 Montferrier-sur-Lez cedex, France
Get access Rights & Permissions [Opens in a new window]

Abstract

We tested whether the prevalence of ticks can be predicted reliably from a simple epidemiological model that takes into account only mean abundance and its variance. We used data on the abundance and distribution of larvae and nymphs of 2 ixodid ticks parasitic on small mammals (Apodemus agrarius, Apodemus flavicollis, Apodemus uralensis, Clethrionomys glareolus and Microtus arvalis) in central Europe. Ixodes trianguliceps is active all year round, occurs in the study area in the mountain and sub-mountain habitats only and inhabits mainly host burrows and nests, whereas Ixodes ricinus occurs mainly during the warmer seasons, occupies a large variety of habitats and quests for hosts outside their shelters. In I. ricinus, the models with k values calculated from Taylor's power law overestimated prevalences. However, if moment estimates of k corrected for host number were used instead, expected prevalences of both larvae and nymphs I. ricinus in either host did not differ significantly from observed prevalences. In contrast, prevalences of larvae and nymphs of I. trianguliceps predicted by models using parameters of Taylor's power law did not differ significantly from observed prevalences, whereas the models with moment estimates of k corrected for host number in some cases under-estimated relatively lower larval prevalences and over-estimated relatively higher larval prevalences, but predicted nymphal prevalences well.

Keywords

abundanceepidemiological modelmammalsprevalenceticks
Type
Research Article
Information
Parasitology , Volume 134 , Issue 1 , January 2007 , pp. 59 - 68
Copyright
© 2006 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

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 mortality. Parasitology 85, 373–398.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
Anderson, R. M. and May, R. M. ( 1985). Helminth infection of humans: mathematical models, population dynamics and control. Advances in Parasitology 24, 1–101.CrossRefGoogle Scholar
Brown, J. H. ( 1984). On the relationship between abundance and distribution of species. American Naturalist 124, 255–279.CrossRefGoogle Scholar
Černý, V. ( 1972). The tick fauna of the Czechoslovakia. Folia Parasitologica 19, 87–92 (in Czech).Google Scholar
Elliot, J. M. ( 1977). Some Methods for Statistical Analysis of Samples of Benthic Invertebrates, 2nd Edn. Freshwater Biological Association Sceintific Publications, No. 25, Titus Wilson and Son, Ambleside, UK.
Estrada-Peña, A. ( 2001). Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in Northern Spain. Journal of Medical Entomology 38, 361–370.CrossRefGoogle Scholar
Estrada-Peña, A., Osacar, J. J., Gortazar, C., Calvete, C. and Lucientes, J. ( 1992). An account of the ticks of the northeastern of Spain (Acarina, Ixodidae). Annales de Parasitologie Humaine et Comparée 67, 42–49.CrossRefGoogle Scholar
Estrada-Peña, A., Guglielmone, A. A. and Mangold, A. J. ( 2004). The distribution and ecological “preferences” of the tick Amblyomma cajennense (Acari: Ixodidae), an ectoparasite of humans and other mammals in the Americas. Annals of Tropical Medicine and Parasitology 98, 283–292.CrossRefGoogle Scholar
Filippova, N. A. ( 1977). Ixodid Ticks of Subfamily Ixodinae. Fauna USSR. Arachnids, Vol 4. Nauka, Leningrad, USSR (in Russian).
Folstad, I. and Karter, A. J. ( 1992). Parasites, bright males and the immunocompetence handicap hypothesis. American Naturalist 139, 603–622.CrossRefGoogle Scholar
Gaston, K. J. ( 2003). The Structure and Dynamics of Geographic Ranges. Oxford University Press, Oxford.
Gaston, K. J., Blackburn, T. M. and Lawton, J. H. ( 1997). Interspecific abundance-range size relationships: an appraisal of mechanisms. Journal of Animal Ecology 66, 579–601.CrossRefGoogle Scholar
Gregory, R. D. and Woolhouse, M. E. ( 1993). Quantification of parasite aggregation: a simulation study. Acta Tropica 54, 131–139.CrossRefGoogle Scholar
Grafen, A. and Woolhouse, M. E. ( 1993). Does the negative binomial distribution add up? Parasitology Today 9, 475–477.Google Scholar
Hanski, I., Kouki, J. and Halkka, A. ( 1993). Three explanations of the positive relationship between distribution and abundance of species. In Species Diversity in Ecological Communities. Historical and Geographical Perspectives ( ed. Ricklefs, R. E. and Schluter, D.), pp. 108–116. University of Chicago Press, Chicago.
Honzáková, E., Olejníček, J., Černý, V., Daniel, M. and Dusbábek, F. ( 1975). Relationships between number of eggs deposited and body of engorged Ixodes ricinus female. Folia Parasitologica 22, 37–43.Google Scholar
Hudson, P. J., Norman, R., Laurenson, M. K., Newborn, D., Gaunt, M., Jones, L., Reid, H., Gould, E., Bowers, R. and Dobson, A. P. ( 1995). Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations. Parasitology 111, S49–S58.CrossRefGoogle Scholar
Hughes, V. L. and Randolph, S. E. ( 2001 a). Testosterone increases the transmission potential of tick-borne parasites. Parasitology 123, 365–371.Google Scholar
Hughes, V. L. and Randolph, S. E. ( 2001 b). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. Journal of Parasitology 87, 49–54.Google Scholar
Klein, S. L. ( 2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.CrossRefGoogle Scholar
Krasnov, B. R., Khokhlova, I. S. and Shenbrot, G. I. ( 2002). The effect of host density on ectoparasite distribution: an example with a desert rodent parasitized by fleas. Ecology 83, 164–175.CrossRefGoogle Scholar
Krasnov, B. R., Stanko, M., Miklisova, D. and Morand, S. ( 2005 a). Distribution of fleas (Siphonaptera) among small mammals: mean abundance predicts prevalence via simple epidemiological model. International Journal for Parasitology 35, 1097–1101.Google Scholar
Krasnov, B. R., Morand, S., Khokhlova, I. S., Shenbrot, G. I. and Hawlena, H. ( 2005 b). Abundance and distribution of fleas on desert rodents: linking Taylor's power law to ecological specialization and epidemiology. Parasitology 131, 825–837.Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. ( 2006 a). Age-dependent flea (Siphonaptera) parasitism in rodents: a host's life history matters. Journal of Parasitology 92, 242–248.Google Scholar
Krasnov, B. R., Stanko, M., Miklisova, D. and Morand, S. ( 2006 b). Host specificity, parasite community size and the relation between abundance and its variance. Evolutionary Ecology 20, 75–91.Google Scholar
Lichard, M. ( 1965). Notes on the occurrence and ecology of tick Ixodes trianguliceps Birula, 1895. Biologia (Bratislava) 20, 348–358 (in Slovak).Google Scholar
Morand, S. and Guégan, J.-F. ( 2000). Distribution and abundance of parasite nematodes: ecological specialization, phylogenetic constraints or simply epidemiology? Oikos 88, 563–573.Google Scholar
Nava, S., Mangold, A. J. and Guglielmone, A. A. ( 2006). The natural hosts of larvae and nymphs of Amblyomma tigrinum Kohh, 1844 (Acari: Ixodidae). Veterinary Parasitology 140, 124–132.CrossRefGoogle Scholar
Norman, R., Bowers, R. G., Begon, M. and Hudson, P. J. ( 1999). Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite mediated competition. Journal of Theoretical Biology 200, 111–118.CrossRefGoogle Scholar
Perret, J. L., Guigoz, E., Rais, O. and Gern, L. ( 2000). Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitology Research 86, 554–557.CrossRefGoogle Scholar
Perry, J. N. ( 1988). Some models for spatial variability of animal species. Oikos 51, 124–130.CrossRefGoogle Scholar
Perry, J. N. and Taylor, L. R. ( 1986). Stability of real interacting populations in space and time: implications, alternatives and negative binomial kc. Journal of Animal Ecology 55, 1053–1068.CrossRefGoogle Scholar
Pet'ko, B., Černý, V. and Jurášek, V. ( 1991). Parasite-host relationships of the tick Ixodes trianguliceps Bir. and coincidence of its ecological niches with those of Ixodes ricinus (L.). In Modern Acarology ( ed. Dusbábek, F. and Bukva, V.), pp. 455–460. Academia, Prague.
Randolph, S. E. ( 1975). Patterns of the distribution of the tick Ixodes trianguliceps Birula on its host. Journal of Animal Ecology 44, 451–474.CrossRefGoogle Scholar
Randolph, S. E. ( 1977). Changing spatial relationships in a population of Apodemus sylvaticus with the onset of breeding. Journal of Animal Ecology 46, 653–676.CrossRefGoogle Scholar
Randolph, S. E. and Steele, G. M. ( 1985). An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari, Ixodidae). 2. The dynamics of the tick-host interaction. Bulletin of Entomological Research 75, 501–518.Google Scholar
Randolph, S. E., Gern, L. and Nutall, P. A. ( 1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472–479.CrossRefGoogle Scholar
Randolph, S. E., Miklisova, D., Lysy, J., Rogers, D. J. and Labuda, M. ( 1999). Incidence from coincidence: patterns of tick infestation on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177–186.CrossRefGoogle Scholar
Rosà, R., Pugliese, A., Norman, R. and Hudson, P. J. ( 2003). Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. Journal of Theoretical Biology 224, 359–376.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations. A quantitative review. Parasitology 111, S111–S127.Google Scholar
Shluger, I. S. ( 1961). Some data on biology of Ixodes trianguliceps and Ixodes persulcatus in Krasnodarsk region. Meditzinskaya Parazitologiya [Medical Parasitology] 30, 425–433.Google Scholar
Simkova, A., Kadlec, D., Gelnar, M. and Morand, S. ( 2002). Abundance-prevalence relationship of gill congeneric ectoparasites: testing the core satellite hypothesis and ecological specialization. Parasitology Research 88, 682–686.Google Scholar
Southwood, T. R. E. ( 1966). Ecological Methods. Chapman and Hall, London.
Stanko, M. ( 1996). Ectoparasites of small mammals (Insectivora, Rodentia) of the Ondava downstream (East Slovakian Lowland). 3. Ticks (Ixodida). Natura Carpatica 37, 151–160 (in Slovak).Google Scholar
Stanko, M. ( 1998). Ectoparasites of small mammals (Insectivora, Rodentia) of the Natural nature reserve Latoricky luh (East Slovakian Lowland). 1. Fleas (Siphonaptera) and ticks (Ixodida). Natura Carpatica 39, 111–120 (in Slovak).Google Scholar
Stanko, M., Fričová, J., Miklisová, D. and Mošanský, L. ( 2006). Host-parasite relationships among parasitic arthropods and common vole (Microtus arvalis, Rodentia) in lowland ecosystems of Slovakia. In Arthropods: Epidemiological Importance ( ed. Buczek, A. and Blaszak, C.), pp. 89–97. Koliber, Lublin.
Taylor, L. R. ( 1961). Aggregation, variance and the mean. Nature, London 189, 732–735.CrossRefGoogle Scholar
Taylor, L. R., Woiwod, I. P. and Perry, J. N. ( 1979). The negative binomial as a dynamic ecological model and density-dependence of k. Journal of Animal Ecology 48, 289–304.CrossRefGoogle Scholar
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglaen, G., Randolph, S. E., Read, A. F. and Skorping, A. ( 2001). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases ( ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford.