Hostname: page-component-6766d58669-rxg44 Total loading time: 0 Render date: 2026-05-17T21:44:06.320Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  03 September 2012

R. PORTER ,
R. A. NORMAN  and
L. GILBERT
R. PORTER
Affiliation:
The James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen AB15 8QH, UK Computing Science and Mathematics, University of Stirling, Stirling FK9 4LA, UK
R. A. NORMAN
Affiliation:
Computing Science and Mathematics, University of Stirling, Stirling FK9 4LA, UK
L. GILBERT*
Affiliation:
The James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen AB15 8QH, UK
*
*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
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

acaricideapparent competitioncullingdeergrouselouping illmanagementmathematical modelling

Information

Type
Research Article
Information
Parasitology , Volume 140 , Issue 2 , February 2013 , pp. 247 - 257
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.)

Article purchase

Temporarily unavailable

References

REFERENCES

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, 451–524.Google Scholar
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, 423–430.CrossRefGoogle ScholarPubMed
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, 407–416.CrossRefGoogle ScholarPubMed
Clutton-Brock, T., and Albon, S. (1989). Red Deer in the Highlands. BSP Professional Books.Google Scholar
Gaunt, M. W. (1997). The epidemiology of louping ill virus and lavivirus evolution. Ph.D. thesis, University of Oxford, Oxford, UK.Google Scholar
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, 277–282.CrossRefGoogle ScholarPubMed
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, 1053–1061.CrossRefGoogle Scholar
Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249–258.CrossRefGoogle 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. American Naturalist 171, 743–754.CrossRefGoogle ScholarPubMed
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, 431–438.CrossRefGoogle ScholarPubMed
Holt, R. D. (1977). Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 12, 197–229.CrossRefGoogle ScholarPubMed
Hudson, P. J. (1992). Grouse in Space and Time. Game Conservancy Trust, Fordingbridge, UK.Google Scholar
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, 172–176.CrossRefGoogle ScholarPubMed
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, 67–70.CrossRefGoogle ScholarPubMed
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, 722–725.CrossRefGoogle ScholarPubMed
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, 79–94.CrossRefGoogle ScholarPubMed
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, 177–185.CrossRefGoogle Scholar
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, 63–69.CrossRefGoogle ScholarPubMed
Porter, R., Norman, R. and Gilbert, L. (2011). Controlling tick-borne diseases through domestic animal management: a theoretical approach. Theoretical Ecology 4, 321–339.CrossRefGoogle Scholar
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.Google Scholar
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, 439–448.CrossRefGoogle ScholarPubMed
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, 588–594.CrossRefGoogle Scholar
Randolph, S. E. (2004). Evidence that climate change has caused 'emergence’ of tick-borne diseases in Europe? International Journal of Medical Microbiology 293 S37, 5–15.Google ScholarPubMed
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, 223–229.CrossRefGoogle Scholar
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, 1013–1020.CrossRefGoogle ScholarPubMed
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, 1–18.CrossRefGoogle Scholar
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, 59–63.CrossRefGoogle ScholarPubMed
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, 117–134.Google ScholarPubMed
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, 149–154.CrossRefGoogle ScholarPubMed
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, 642–652.CrossRefGoogle ScholarPubMed
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, 371–379.CrossRefGoogle Scholar
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, 529–533.CrossRefGoogle ScholarPubMed
Supplementary material: File

Porter Supplementary Material

Supplementary Material.doc

Download Porter Supplementary Material(File)
File 102.9 KB