Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-28T14:52:34.743Z Has data issue: false hasContentIssue false
  • English
  • Français

The importance of the aggregation of ticks on small mammal hosts for the establishment and persistence of tick-borne pathogens: an investigation using the R0 model

Published online by Cambridge University Press:  19 July 2012

ALAN HARRISON  and
NIGEL C. BENNETT
ALAN HARRISON*
Affiliation:
Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa
NIGEL C. BENNETT
Affiliation:
Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa Department of Zoology, King Saud University, Riyadh, Kingdom of Saudi Arabia
*
*Corresponding author: Department of Zoology and Entomology, University of Pretoria, Private Bag X20, Hatfield, 0028, Pretoria, South Africa. Tel: +27(0)713815103. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Aggregation of parasites amongst hosts is important for the epidemiology of vector-borne diseases because hosts that support the majority of the vector population are responsible for the majority of pathogen transmission. Ixodes ricinus ticks transmit numerous pathogens of medical importance including Borrelia burgdorferi s.l. and tick-borne encephalitis virus. One transmission route involved is ‘co-feeding transmission’, where larvae become infected via feeding alongside infected nymphs. The aggregation of ticks on hosts leads to an increase in the number of larvae feeding alongside nymphs, increasing the transmission potential via this route. The basic reproduction number, R0, can be used to identify whether a pathogen will become established if introduced. In the current study we use previously published tick, and pathogen, specific data to parameterize an R0 model to investigate how the degree of aggregation of ticks on hosts affects pathogen persistence. The coincident aggregated distribution permitted the establishment of tick-borne encephalitis virus but did not influence whether B. burgdorferi s.l. became established. The relationship between the k-exponent of the negative binomial distribution and R0 was also defined. Therefore, the degree of aggregation of ticks on small mammal hosts has important implications for the risk to human health in a given area.

Keywords

vector-borne diseasesaggregationtransmissionIxodes ricinusBorrelia burgdorferi s.l.epidemiology
Type
Research Article
Information
Parasitology , Volume 139 , Issue 12 , October 2012 , pp. 1605 - 1613
Copyright
Copyright © Cambridge University Press 2012

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 May, R. M. (1990). Modern vaccines: Immunisation and herd immunity. Lancet 335, 641–645.CrossRefGoogle Scholar
Bouchard, C., Beauchamp, G., Trudel, L., Milford, F., Lindsay, L. R., Belanger, D. and Ogden, N. H. (2011). Associations between Ixodes scapularis ticks and small mammal hosts in a newly endemic zone in southeastern Canada: Implications for Borrelia burgdorferi transmission. Ticks and Tick-borne Diseases 2, 183–190.CrossRefGoogle Scholar
Boyer, N., Réale, D., Marmet, J., Pisanu, B. and Chapuis, J. L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. Journal of Animal Ecology 79, 538–547.CrossRefGoogle Scholar
Caraco, T., Glavankov, S., Chen, G., Flaherty, J. E., Ohsumi, T. K. and Szymanksi, B. K. (2002). Stage-structured infection transmission and a spatial epidemic: a model for Lyme disease. American Naturalist 160, 348–359.CrossRefGoogle Scholar
Crofton, H. (1971). A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
Daniels, T. J. and Fish, D. (1990). Spatial distribution and dispersal of unfed larval Ixodes dammini (Acari: Ixodidae) in southern New York. Environmental Entomology 19, 1029–1033.CrossRefGoogle Scholar
Diekmann, O., Heesterbeek, J. A. P. and Metz, J. A. J. (1990). On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. Journal of Mathematical Biology 28, 365–382.CrossRefGoogle ScholarPubMed
Dobson, A. P. and Merenlender, A. (1991). Coevolution of macroparasites and their hosts. In Parasite-host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), pp. 83–101. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88–94.CrossRefGoogle Scholar
Gallivan, G. and Horak, I. (1997). Body size and habitat as determinants of tick infestations of wild ungulates in South Africa. South African Journal of Wildlife Research 27, 63–70.Google Scholar
Gatewood, A. G., Liebman, K. A., Vourc'h, G., Bunikis, J., Hamer, S. A., Cortinas, R., Melton, F., Cislo, P., Kitron, U. and Tsao, J. (2009). Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Applied and Environmental Microbiology 75, 2476–2483.CrossRefGoogle ScholarPubMed
Gern, L. and Rais, O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189–192.CrossRefGoogle ScholarPubMed
Ghosh, M. and Pugliese, A. (2004). Seasonal population dynamics of ticks, and its influence on infection transmission: a semi-discrete approach. Bulletin of Mathematical Biology 66, 1659–1684.CrossRefGoogle ScholarPubMed
Goodman, J. L., Dennis, D. T. and Sonenshine, D. E. (2005). Tick-borne diseases of humans. 1st Edn.American Society for Microbiology, Washington.CrossRefGoogle Scholar
Gray, J. S. (2002). Biology of Ixodes species ticks in relation to tick-borne zoonoses. Wiener klinische Wochenschrift 114, 473–478.Google ScholarPubMed
Harrison, A., Montgomery, W. I. and Bown, K. J. (2011). Investigating the persistence of tick-borne pathogens via the R0 model. Parasitology 138, 896–905.CrossRefGoogle ScholarPubMed
Harrison, A., Scantlebury, M. and Montgomery, W. I. (2010). Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 9999.Google Scholar
Hartemink, N. A., Randolph, S. E., Davis, S. A. and Heesterbeek, J. A. P. (2008). The basic reproduction number for complex disease systems: Defining R0 for tick-borne infections. The American Naturalist 171, 743–754.CrossRefGoogle ScholarPubMed
Hubálek, Z. and Halouzka, J. (1998). Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167–172.Google ScholarPubMed
Hudson, P. J., Norman, R., Laurenson, M. K., Newborn, D., Gaunt, M., Jones, L., Reid, H., Gould, E., Bowers, R., and Dobson, A. (1995). Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations. Parasitology 111, S49–S58.CrossRefGoogle ScholarPubMed
Hughes, V. L. and Randolph, S. E. (2001). 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.CrossRefGoogle ScholarPubMed
Humair, P. F., Rais, O. and Gern, L. (1999). Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 118, 33–42.CrossRefGoogle ScholarPubMed
Jongejan, F. and Uilenberg, G. (2004). The global importance of ticks. Parasitology 129, 3–14.CrossRefGoogle ScholarPubMed
Koch, R. (1999). 80/20 Principle: The Secret to Success by Achieving More with Less. 1st Edn.Currency, New York, USA.Google Scholar
Kurtenbach, K., Hanincová, K., Tsao, J. I., Margos, G., Fish, D. and Ogden, N. H. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660–669.CrossRefGoogle ScholarPubMed
Kurtenbach, K., Dizij, A., Seitz, H. M., Margos, G., Moter, S. E., Kramer, M. D., Wallich, R., Schaible, U. E. and Simon, M. M. (1994). Differential immune responses to Borrelia burgdorferi in European wild rodent species influence spirochete transmission to Ixodes ricinus L. (Acari: Ixodidae). Infection and Immunity 62, 5344–5352.CrossRefGoogle ScholarPubMed
Labuda, M., Jones, L. D., Williams, T., Danielova, V. and Nuttall, P. A. (1993). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. Journal of Medical Entomology 30, 295–299.CrossRefGoogle ScholarPubMed
Labuda, M., Kozuch, O. and Lys, J. (1997). Tickborne encephalitis virus natural foci in Slovakia: ticks, rodents, and… goats. In 4th International Potsdam Symposium on Tick-borne Diseases: Tick-borne Encephalitis and Lyme borreliosis (ed. Suss, J. and Kahl, O.), pp. 21–22. Pabst Science Publishers, Lengerich, Germany.Google Scholar
Mannelli, A., Bertolotti, L., Gern, L. and Gray, J. (2012). Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiology Reviews (in the Press).CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Norman, R., Ross, D., Laurenson, M. K., and Hudson, P. J. (2004). The role of non-viraemic transmission on the persistence and dynamics of a tick borne virus-Louping ill in red grouse (Lagopus Lagopus scoticus) and mountain hares (Lepus timidus). Journal of Mathematical Biology 48, 119–134.CrossRefGoogle ScholarPubMed
Ostfeld, R. S. and Keesing, F. (2000). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722–728.CrossRefGoogle Scholar
Pal, U., De Silva, A. M., Montgomery, R. R., Fish, D., Anguita, J., Anderson, J. F., Lobet, Y. and Fikrig, E. (2000). Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. Journal of Clinical Investigation 106, 561–569.CrossRefGoogle ScholarPubMed
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909–917.CrossRefGoogle ScholarPubMed
Randolph, S. E. (1977). Changing spatial relationships in a population of Apodemus sylvaticus with the onset of breeding. The Journal of Animal Ecology 46, 653–676.CrossRefGoogle Scholar
Randolph, S. (1998). Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186–192.CrossRefGoogle Scholar
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, 37–65.CrossRefGoogle ScholarPubMed
Randolph, S. E. and Craine, N. G. (1995). General framework for comparative quantitative studies on transmission of tick-borne diseases using Lyme borreliosis in Europe as an example. Journal of Medical Entomology 32, 765–777.CrossRefGoogle ScholarPubMed
Randolph, S. E., Gern, L. and Nuttall, P. A. (1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472–479.CrossRefGoogle ScholarPubMed
Randolph, S. E., Miklisova, D., Lysy, J., Rogers, D. J. and Labuda, M. (1999). Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177–186.CrossRefGoogle ScholarPubMed
Randolph, S. E. and Rogers, D. J. (2000). Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. Proceedings of the Royal Society of London, B 267, 1741–1744.CrossRefGoogle ScholarPubMed
Randolph, S. E. and Steele, G. M. (1985). An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.)(Acari: Ixodidae). II. The dynamics of the tick-host interaction. Bulletin of Entomological Research 75, 501–518.Google Scholar
Rosá, R. and Pugliese, R. (2007). Effects of tick population dynamics and host densities on the persistence of tick-borne infections. Mathematical Biosciences 208, 216–240.CrossRefGoogle ScholarPubMed
Rosá, R., Pugliese, R., 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 ScholarPubMed
Schmidt, K. A. and Ostfeld, R. S. (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.CrossRefGoogle Scholar
Shaw, D. and Dobson, A. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, 111–133.CrossRefGoogle ScholarPubMed
Telford, S. R. III, Cunningham, J. A., Waltari, E. and Hu, L. (2011). Nest box-deployed bait for delivering oral vaccines to white-footed mice. Ticks and Tick-borne Diseases 2, 151–155.CrossRefGoogle ScholarPubMed
Tsao, J. I., Wootton, J. T., Bunikis, J., Luna, M. G., Fish, D. and Barbour, A. G. (2004). An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences, USA 101, 18159–18164.CrossRefGoogle ScholarPubMed
Wilson, K., Bjørnstad, O., Dobson, A., Merler, S., Poglayen, G., Randolph, S., Read, A., Skorping, A., Hudson, P. and Rizzoli, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. P. J., Hudson, Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J., Garnett, G., Hagan, P., Hii, J., Ndhlovu, P. and Quinnell, R. (1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338–342.CrossRefGoogle ScholarPubMed
Supplementary material: File

Harrison and Bennett supllementary material

Supplementary data

Download Harrison and Bennett supllementary material(File)
File 17.8 KB