Skip to main content Accessibility help
×
Home

An alternative to killing? Treatment of reservoir hosts to control a vector and pathogen in a susceptible species

  • R. PORTER (a1) (a2), R. A. NORMAN (a2) and L. GILBERT (a1)

Summary

Parasite-mediated apparent competition occurs when one species affects another through the action of a shared parasite. One way of controlling the parasite in the more susceptible host is to manage the reservoir host. Culling can cause issues in terms of ethics and biodiversity impacts, therefore we ask: can treating, as compared to culling, a wildlife host protect a target species from the shared parasite? We used Susceptible Infected Recovered (SIR) models parameterized for the tick-borne louping ill virus (LIV) system. Deer are the key hosts of the vector (Ixodes ricinus) that transmits LIV to red grouse Lagopus lagopus scoticus, causing high mortality. The model was run under scenarios of varying acaricide efficacy and deer densities. The model predicted that treating deer can increase grouse density through controlling ticks and LIV, if acaricide efficacies are high and deer densities low. Comparing deer treated with 70% acaricide efficacy with a 70% cull rate suggested that treatment may be more effective than culling if initial deer densities are high. Our results will help inform tick control policies, optimize the targeting of control methods and identify conditions where host management is most likely to succeed. Our approach is applicable to other host-vector-pathogen systems.

Copyright

Corresponding author

*Corresponding author: The James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen AB15 8QH, UK. Tel: +44 (0)1224 395187. Fax: +44 (0) 844 928 5429. Lucy.Gilbert@hutton.ac.uk

References

Hide All
Anderson, R. M. and May, R. M. (1981). The population-dynamics of micro-parasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London, B 291, 451524.
Brei, B., Brownstein, J. S., George, J. E., Pound, J. M., Miller, J. A., Daniels, T. J., Falco, R. C., Stafford, K. C., Schulze, T. L., Mather, T. N., Carroll, J. F. and Fish, D. (2009). Evaluation of the United States Department of Agriculture Northeast Area-Wide Tick Control Project by meta-analysis. Vector-Borne and Zoonotic Diseases 9, 423430.
Carroll, J. F., Hill, D. E., Allen, P. C., Young, K. W., Miramontes, E., Kramer, M., Pound, J. M., Miller, J. A., and George, J. E. (2009). The impact of ‘4-poster’ deer self-treatment devices at three locations in Maryland. Vector-Borne and Zoonotic Diseases 9, 407416.
Clutton-Brock, T., and Albon, S. (1989). Red Deer in the Highlands. BSP Professional Books.
Gaunt, M. W. (1997). The epidemiology of louping ill virus and lavivirus evolution. Ph.D. thesis, University of Oxford, Oxford, UK.
Gilbert, L., Jones, L. D., Hudson, P. J., Gould, E. A. and Reid, H. W. (2000). Role of small mammals in the persistence of Louping-ill virus: field survey and tick co-feeding studies. Medical and Veterinary Entomology 14, 277282.
Gilbert, L., Norman, R., Laurenson, M. K., Reid, H. W. and Hudson, P. J. (2001). Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale, wild populations. Journal of Animal Ecology 70, 10531061.
Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249258.
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. American Naturalist 171, 743754.
Hoen, A. G., Rollend, L. G., Papero, M. A., Carroll, J. F., Daniels, T. J., Mather, T. N., Schulze, T. L., Stafford, K. C. III and Fish, D. (2009). Effects of tick control of acaricide self-treatment of white-tailed deer onhost-seeking tick infection prevalence and entomologic risk for Ixodes scapularis-borne pathogens. Vector-Borne and Zoonotic Diseases 9, 431438.
Holt, R. D. (1977). Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 12, 197229.
Hudson, P. J. (1992). Grouse in Space and Time. Game Conservancy Trust, Fordingbridge, UK.
Jones, L. D., Gaunt, M., Hailes, R. S., Laurenson, K., Hudson, P. J., Reid, H., Henbest, P. and Gould, E. A. (1997). Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Medical and Veterinary Entomology 11, 172176.
Kirby, A. D., Smith, A. A., Benton, T. G. and Hudson, P. J. (2004). Rising burden of immature sheep ticks Ixodes ricinus on red grouse Lagopus lagopus scoticus chicks in the Scottish uplands. Medical and Veterinary Entomology 18, 6770.
Kulasekera, V. L., Kramer, L., Nasci, R. S., Mostashari, F., Cherry, B., Trock, S. C., Glaser, C. and Miller, J. R. (2001). West Nile virus infection in mosquitoes, birds, horses, and humans, Staten Island, New York, 2000. Emerging Infectious Diseases 7, 722725.
Kiffner, C., Lödige, C., Alings, M., Vor, T. and Rühe, F. (2011). Attachment site selection of ticks on roe deer, Capreolus capreolus. Experimental and Applied Acarology 53, 7994.
Laurenson, M. K., Norman, R. A., Gilbert, L., Reid, H. W. and Hudson, P. J. (2003). Identifying disease reservoirs in complex systems: mountain hares as reservoirs of ticks and louping-ill virus, pathogens of red grouse. Journal of Animal Ecology 72, 177185.
Newborn, D. and Baines, D. (2012). Enhanced control of sheep ticks in upland sheep flocks: repercussions for red grouse co-hosts. Medical and Veterinary Entomology 26, 6369.
Porter, R., Norman, R. and Gilbert, L. (2011). Controlling tick-borne diseases through domestic animal management: a theoretical approach. Theoretical Ecology 4, 321339.
Porter, R. (2011). Mathematical models of a tick borne disease in a British gamebird with potential management strategies. Ph.D. thesis, University of Stirling, Scotland, UK.
Pound, J. M., Miller, J. A., George, J. E., Fish, D., Carroll, J. F., Schulze, T. L., Daniels, T. J., Falco, R. C., Stafford, K. C. III and Mather, T. N. (2009). The United States Department of Agriculture's Northeast Area-Wide Tick Control Project: summary and conclusions. Vector-Borne and Zoonotic Diseases 9, 439448.
Pound, J. M., Miller, J. A., George, J. E. and Lemeilleur, C. A. (2000). The “4-Poster” passive topical treatment device to apply acaricide for controlling ticks feeding on white-tailed deer. Journal of Medical Entomology 37, 588594.
Randolph, S. E. (2004). Evidence that climate change has caused 'emergence’ of tick-borne diseases in Europe? International Journal of Medical Microbiology 293 S37, 515.
Reid, H. W. (1975). Experimental infection of red grouse with Louping-Ill virus flavivirus group. 1 Viremia and antibody-response. Journal of Comparative Pathology 85, 223229.
Ruiz-Fons, F. and Gilbert, L. (2010). The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. International Journal for Parasitology 40, 10131020.
Rushton, S. P., Lurz, P. W. W. and Gurnell, J. (2000). Modelling the spatial dynamics of parapoxvirus disease in red and grey squirrels: a possible cause of the decline in the red squirrel in the United Kingdom? Journal of Applied Ecology 37, 118.
Schmidtmann, E. T., Carroll, J. F. and Watson, D. W. (1998). Attachment-site patterns of adult black-legged ticks on white-tailed deer and horses. Journal of Medical Entomology 35, 5963.
Solberg, V. B., Miller, J. A., Hadfield, T., Burge, R., Schech, J. M. and Pound, J. M. (2003). Control of Ixodes scapularis Acari: Ixodidae. with topical self-application of permethrin by white-tailed deer inhabiting NASA, Beltsville, Maryland. Journal of Vector Ecology 28, 117134.
Sonenshine, D., Allen, S. A., Noval, R. A. and Burridge, M. J. (1996). A self-medicating applicator for control of ticks on deer. Medical and Veterinary Entomology 10, 149154.
Stafford, K. C. 3rd, Denicola, A. J. and Kilpatrick, H. J. (2003). Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with reduction of white-tailed deer. Journal of Medical Entomology 40, 642652.
Stafford, K. C. III, Denicola, A. J., Pound, J. M., Miller, J. A. and George, J. E. (2009). Topical treatment of white-tailed deer with an acaricide for the control of Ixodes scapularis Acari: Ixodidae. in a Connecticut Lyme Borreliosis hyperendemic community. Vector-Borne and Zoonotic Diseases 9, 371379.
Tompkins, D., Sainsbury, A. W., Nettleton, P., Buxton, D. and Gurnell, J. (2002). Parapoxvirus causes a deleterious disease of red squirrels associated with UK population declines. Proceedings of the Royal Society of London, B 269, 529533.

Keywords

Type Description Title
WORD
Supplementary materials

Porter Supplementary Material
Supplementary Material.doc

 Word (103 KB)
103 KB

An alternative to killing? Treatment of reservoir hosts to control a vector and pathogen in a susceptible species

  • R. PORTER (a1) (a2), R. A. NORMAN (a2) and L. GILBERT (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed