Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T07:57:32.188Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of host movement on viral transmission dynamics in a vector-borne disease system

Published online by Cambridge University Press:  27 July 2009

E. J. WATTS ,
S. C. F. PALMER ,
A. S. BOWMAN ,
R. J. IRVINE ,
A. SMITH  and
J. M. J. TRAVIS
E. J. WATTS
Affiliation:
Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory AB31 4BW, UK
S. C. F. PALMER*
Affiliation:
Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
A. S. BOWMAN
Affiliation:
Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
R. J. IRVINE
Affiliation:
Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
A. SMITH
Affiliation:
Game and Wildlife Conservation Trust, Drumochter Lodge, Dalwhinnie PH19 1AF, UK
J. M. J. TRAVIS
Affiliation:
Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
*
*Corresponding author: Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK. Tel: +44 (0) 1224 272693. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Many vector-borne pathogens whose primary vectors are generalists, such as Ixodid ticks, can infect a wide range of host species and are often zoonotic. Understanding their transmission dynamics is important for the development of disease management programmes. Models exist to describe the transmission dynamics of such diseases, but are necessarily simplistic and generally limited by knowledge of vector population dynamics. They are typically deterministic SIR-type models, which predict disease dynamics in a single, non-spatial, closed patch. Here we explore the limitations of such a model of louping-ill virus dynamics by challenging it with novel field data. The model was only partially successful in predicting Ixodes ricinus density and louping-ill virus prevalence at 6 Scottish sites. We extend the existing multi-host model by forming a two-patch model, incorporating the impact of roaming hosts. This demonstrates that host movement may account for some of the discrepancies between the original model and empirical data. We conclude that insights into the dynamics of multi-host vector-borne pathogens can be gained by using a simple two-patch model. Potential improvements to the model, incorporating aspects of spatial and temporal heterogeneity, are outlined.

Keywords

host movementIxodes ricinusLagopus lagopus scoticuslouping-ill virusmathematical modelspatial heterogeneitytick
Type
Research Article
Information
Parasitology , Volume 136 , Issue 10 , September 2009 , pp. 1221 - 1234
Copyright
Copyright © Cambridge University Press 2009

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

Brisson, D., Dykhuizen, D. E. and Ostfeld, R. S. (2008). Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proceedings of the Royal Society, B 275, 227–235.CrossRefGoogle ScholarPubMed
Brownstein, J. S., Holford, T. R. and Fish, D. (2003). A climate-based model predicts the spatial distribution of the Lyme disease vector lxodes scapularis in the United States. Environmental Health Perspectives 111, 1152–1157.CrossRefGoogle Scholar
Cope, D. R., Iason, G. R. and Gordon, I. J. (2004). Disease reservoirs in complex systems: a comment on recent work by Laurenson et al. Journal of Animal Ecology 73, 807–810.CrossRefGoogle Scholar
Daniel, M., Kolar, J. and Zeman, K. (2004). GIS tools for tick and tick-borne disease occurrence. Parasitology 129, S329–S352.CrossRefGoogle ScholarPubMed
Dobson, A. P. and Hudson, P. J. (1992). Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. II. Population models. Journal of Animal Ecology 61, 487–498.CrossRefGoogle Scholar
Elston, D. A. (1992). Sensitivity analysis in the presence of correlated parameter estimates. Ecological Modelling 64, 11–22.CrossRefGoogle Scholar
Foley, J. E., Queen, E. V., Sacks, B. and Foley, P. (2005). GIS-facilitated spatial epidemiology of tick-borne diseases in coyotes (Canis latrans) in northern and coastal California. Comparative Immunology Microbiology and Infectious Diseases 28, 197–212.CrossRefGoogle ScholarPubMed
Gaunt, M. W., Jones, L. D., Laurenson, K., Hudson, P. J., Reid, H. W. and Gould, E. A. (1997). Definitive identification of louping-ill virus by RT-PCR and sequencing in field populations of Ixodes ricinus on the Lochindorb Estate. Archives of Virology 142, 1181–1191.CrossRefGoogle ScholarPubMed
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., Jones, L. D., Laurenson, M. K., Gould, E. A., Reid, H. W. and Hudson, P. J. (2004). Ticks need not bite their red grouse hosts to infect them with louping ill virus. Proceedings of the Royal Society of London, B 271, S202–S205.CrossRefGoogle Scholar
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. and Lohan, G. (1982). The development of a sampling method for the tick Ixodes ricinus and its use in a redwater fever area. Annals of Applied Biology 101, 421–427.CrossRefGoogle Scholar
Guerra, M., Walker, E., Jones, C., Paskewitz, S., Cortinas, M. R., Stancil, A., Beck, L., Bobo, M. and Kitron, U. (2002). Predicting the risk of Lyme disease: Habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8, 289–297.CrossRefGoogle ScholarPubMed
Hancock, P. A. and Godfray, H. C. J. (2007). Application of the lumped age-class technique to studying the dynamics of malaria-mosquito-human interactions. Malaria Journal 6, 98–110.CrossRefGoogle ScholarPubMed
Hester, A. J. and Baillie, G. J. (1998). Spatial and temporal patterns of heather use by sheep and red deer within natural heather/grass mosaics. Journal of Applied Ecology 35, 772–784.CrossRefGoogle Scholar
Hewson, R. (1976). Grazing by mountain hares Lepus timidus L., red deer Cervus elaphus L. and red grouse Lagopus l. scoticus on heather moorland in north-east Scotland. Journal of Applied Ecology 13, 657–666.CrossRefGoogle Scholar
Hewson, R. and Hinge, M. D. C. (1990). Characteristics of the home range of mountain hares Lepus timidus. Journal of Applied Ecology 27, 651–666.CrossRefGoogle Scholar
Hubalek, Z., Pow, I., Reid, H. W. and Hussain, M. H. (1995). Antigenic similarity of Central European encephalitis and louping-ill viruses. Acta Virologica 39, 251–256.Google ScholarPubMed
Hudson, P. J. (1992). Grouse in Space and Time. The Game Conservancy, Fordingbridge, Hampshire, UK.Google Scholar
Hudson, P. J., Gould, E. A., Laurenson, M. K., Gaunt, M., Reid, H. W., Jones, J. D., Norman, R., MacGuire, K. and Newborn, D. (1997). The epidemiology of louping-ill, a tick-borne infection of red grouse (Lagopus lagopus scoticus). Parassitologia 39, 319–323.Google ScholarPubMed
Hudson, P. J., Newborn, D. and Dobson, A. P. (1992). Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. Journal of Animal Ecology 61, 477–486.CrossRefGoogle Scholar
Jenkins, D., Watson, A. and Miller, G. R. (1963). Population studies on red grouse,Lagopus lagopus scoticus (Lath.) in north-east Scotland. Journal of Animal Ecology 32, 317–376.CrossRefGoogle Scholar
Jones, L. D., Gaunt, M., Hails, 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
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
Laurenson, M. K., Norman, R. A., Gilbert, L., Reid, H. W. and Hudson, P. J. (2004). Mountain hares, louping-ill, red grouse and harvesting: complex interactions but few data. Journal of Animal Ecology 73, 811–813.CrossRefGoogle Scholar
Laurenson, M. K., Norman, R., Reid, H. W., Pow, I., Newborn, D. and Hudson, P. J. (2000). The role of lambs in louping-ill virus amplification. Parasitology 120, 97–104.CrossRefGoogle ScholarPubMed
Law, R. A., Murrell, D. J. and Dieckmann, U. (2003). Population growth in space and time: spatial logistic equations. Ecology 84, 252–262.CrossRefGoogle Scholar
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. (2003). The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567–571.CrossRefGoogle ScholarPubMed
McGuire, K., Holmes, E. C., Gao, G. F., Reid, H. W. and Gould, E. A. (1998). Tracing the origins of louping-ill virus by molecular phylogenetic analysis. Journal of General Virology 79, 981–988.CrossRefGoogle ScholarPubMed
MacLeod, J. (1939). The seasonal and annual incidence of the sheep tick, Ixodes ricinus, in Britain. Bulletin of Entomological Research 30, 103–118.CrossRefGoogle Scholar
Matthiopoulos, J., Moss, R. and Lambin, X. (1998). Models of red grouse cycles. A family affair? Oikos 82, 574–590.CrossRefGoogle Scholar
Morgan, E. R., Medley, G. F., Torgerson, P. R., Shaikenov, B. S. and Milner-Gulland, E. J. (2007). Parasite transmission in a migratory multiple host system. Ecological Modelling 200, 511–520.CrossRefGoogle Scholar
Moss, R. and Watson, A. (1991). Population cycles and kin selection in Red Grouse. Ibis 133, 113–120.CrossRefGoogle Scholar
Muetzelfeldt, R. I. and Massheder, J. (2003). The Simile visual modelling environment. European Journal of Agronomy 18, 345–358.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 ScholarPubMed
Ostfeld, R. S. and Keesing, F. (2000). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722–728.CrossRefGoogle Scholar
Palmer, S. C. F. and Bacon, P. J. (2001). The utilisation of heather moorland by territorial Red Grouse Lagopus lagopus scoticus. Ibis 143, 222–232.CrossRefGoogle Scholar
Palmer, S. C. F., Hester, A. J., Elston, D. A., Gordon, I. J. and Hartley, S. E. (2003). The perils of having tasty neighbors: grazing impacts of large herbivores at vegetation boundaries. Ecology 84, 2877–2890.CrossRefGoogle Scholar
Peterson, A. T., Martinez-Campos, C., Nakazawa, Y. and Martinez-Meyer, E. (2005). Time-specific ecological niche modeling predicts spatial dynamics of vector insects and human dengue cases. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 647–655.CrossRefGoogle ScholarPubMed
Pugliese, A. and Rosà, R. (2008). Effect of host populations on the intensity of ticks and the prevalence of tick-borne pathogens: how to interpret the results of deer exclosure experiments. Parasitology 135, 1531–1544.CrossRefGoogle ScholarPubMed
Pulliam, H. R. (1988). Sources, sinks and population regulation. American Naturalist 132, 652–661.CrossRefGoogle Scholar
Randolph, S. E. (2000). Ticks and tick-borne disease systems in space and from space. Advances In Parasitology 47, 217–243.CrossRefGoogle ScholarPubMed
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, S37–S65.CrossRefGoogle ScholarPubMed
Reid, H. W. (1978). The epidemiology of louping-ill. In Tick-Borne Diseases and their Vectors (ed. Wild, J. K. H.), pp. 501–507. Edinburgh University Press, Edingburgh.Google Scholar
Ruxton, G. D. (1996). The effects of stochasticity and seasonality on model dynamics: bovine tuberculosis in badgers. Journal of Animal Ecology 65, 495–500.CrossRefGoogle Scholar
Theophilides, C. N., Ahearn, S. C., Grady, S. and Merlino, M. (2003). Identifying West Nile virus risk areas: The dynamic continuous-area space-time system. American Journal of Epidemiology 157, 843–854.CrossRefGoogle ScholarPubMed
Watson, A., Moss, R., Parr, R., Mountford, M. D. and Rothery, P. (1994). Kin landownership, differential aggression between kin and non-kin, and population fluctuations in red grouse. Journal of Animal Ecology 63, 277–285.CrossRefGoogle Scholar