Hostname: page-component-7c8c6479df-nwzlb Total loading time: 0 Render date: 2024-03-28T14:28:54.969Z Has data issue: false hasContentIssue false

Tick-borne Great Island Virus: (I) Identification of seabird host and evidence for co-feeding and viraemic transmission

Published online by Cambridge University Press:  11 October 2005

M. A. NUNN
Affiliation:
NERC Centre for Ecology and Hydrology, Mansfield Road, Oxford OX1 3SR
T. R. BARTON
Affiliation:
NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory, Kincardineshire, AB31 4BW Present address: University of Aberdeen, Lighthouse Field Station, George Street, Cromarty, Ross-Shire, IV11 8YJ
S. WANLESS
Affiliation:
NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory, Kincardineshire, AB31 4BW
R. S. HAILS
Affiliation:
NERC Centre for Ecology and Hydrology, Mansfield Road, Oxford OX1 3SR
M. P. HARRIS
Affiliation:
NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory, Kincardineshire, AB31 4BW
P. A. NUTTALL
Affiliation:
NERC Centre for Ecology and Hydrology, Mansfield Road, Oxford OX1 3SR

Abstract

Great Island Virus (GIV) is an arbovirus present in the tick Ixodes uriae, a common ectoparasite of nesting seabirds. Common guillemot (Uria aalge) and black-legged kittiwake (Rissa tridactyla) are the preferred and most abundant hosts of I. uriae on the Isle of May, Scotland. As part of a study to understand the epidemiology of GIV, the ability of guillemot and kittiwake to support tick-borne transmission of GIV was examined. GIV was present in ticks feeding in isolated guillemot colonies and guillemots had virus-specific neutralizing antibodies demonstrating previous GIV infection. By contrast, only uninfected ticks were found in colonies inhabited solely by kittiwakes. GIV was isolated from kittiwake ticks in colonies which also contained breeding guillemots but no virus-specific neutralizing antibodies were present in blood samples of kittiwake on which infected ticks were feeding. Thus guillemots are the main vertebrate hosts of GIV on the Isle of May whereas kittiwakes do not appear to be susceptible to infection. Virus infection of adult ticks feeding on guillemots was highly efficient and may involve both viraemic transmission and transmission from infected to uninfected ticks feeding together on birds that do not develop a patent viraemia.

Type
Research Article
Copyright
2005 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 May, R. M. ( 1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press: East Kilbride, Scotland.
Barton, T. R., Harris, M. P., Wanless, S. and Elston, D. ( 1996). The activity periods and life-cycle of the tick Ixodes uriae (Acari: Ixodidae) in relation to host breeding strategies. Parasitology 112, 571580.CrossRefGoogle Scholar
Bucher-Osmond, C. ( 2003). The Universal Virus Database ICTVdB. Computing Science and Engineering 5, 1625.CrossRefGoogle Scholar
De Swart, R. L., Harder, T. C., Ross, P. S., Vos, H. W. and Osterhaus, A. D. ( 1995). Morbilliviruses and morbillivirus diseases of marine mammals. Infectious Agents and Disease 4, 125130.Google Scholar
Doherty, R. L., Carley, J. G., Murray, M. D., Main, A. J., Kay, B. H. and Domrow, R. ( 1975). Isolation of arboviruses (Kemerovo group, Sakhalin group) from Ixodes uriae collected at Macquarie Island, Southern Ocean. American Journal of Tropical Medicine and Hygiene 24, 521526.CrossRefGoogle Scholar
Eveleigh, E. S. and Threlfall, W. ( 1975). Bionomics of Ixodes (Ceratixodes) uriae White, 1852 on auks (Alcidae) from Newfoundland. Canadian Journal of Zoology 53, 8286.CrossRefGoogle Scholar
Grenfell, B. T. and Gulland, F. M. D. ( 1995). Ecological impact of parasitism on wildlife host populations. Parasitology 111 (Suppl.) S3S14.CrossRefGoogle Scholar
Grenfell, B. T., Amos, W., Arneberg, P., Bjornstad, O. N., Greenman, J. V., Harwood, J., Lanfranchi, P., McLean, A. R., Norman, R. A., Read, A. F. and Skorping, A. ( 2002). Visions for future research in wildlife epidemiology. In The Ecology of Wildlife Diseases ( ed. Hudson, P. J., Rizzoli, A. P., Grenfell, B. T., Heesterbeck, H. and Dobson, A. P.), pp. 151165. Oxford University Press, Oxford.
Harris, M. P., Halley, D. J. and Swann, R. L. ( 1994). Age of first breeding in common murres. The Auk 111, 207209.CrossRefGoogle Scholar
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 (Suppl.) S49S58.CrossRefGoogle Scholar
Jones, L. D., Davies, C. R., Steele, G. M. and Nuttall, P. A. ( 1987). A novel mode of arbovirus transmission involving a non-viraemic host. Science 237, 775777.CrossRefGoogle Scholar
Jones, L. D., Gaunt, M., Hails, R. S., Laurenson, K., Hudson, P. J., Henbest, P. and Gould, E. A. ( 1997). Transmission of louping ill virus between infected and uninfected ticks cofeeding on mountain hares. Medical and Veterinary Entomology 11, 172176.CrossRefGoogle Scholar
Labuda, M., Kozuch, O., Zuffova, E., Eleckova, E., Hails, R. S. and Nuttall, P. A. ( 1997). Tick-borne virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235, 138143.CrossRefGoogle Scholar
Lord, C. C. and Tabachnik, W. J. ( 2002). Influence of nonsystemic transmission on the epidemiology of insect-borne arboviruses: a case study of vesicular stomatitis epidemiology in the western United States. Journal of Medical Entomology 39, 417426.CrossRefGoogle Scholar
McCullagh, P. and Nelder, J. A. ( 1989). Generalised Linear Models, 2nd Edn. Chapman and Hall, London.
McCoy, K. D. and Tirard, C. ( 2002). Reproductive strategies of the seabird tick Ixodes uriae (Acari: Ixodidae). Journal of Parasitology 88, 813816.CrossRefGoogle Scholar
McCoy, K. D., Tirard, C. and Michalkis, Y. ( 2003). Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host. Heredity 91, 422429.CrossRefGoogle Scholar
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, 119134.CrossRefGoogle Scholar
Nunn, M. A., Barton, T. R., Wanless, S., Hails, R. S., Harris, M. P. and Nuttall, P. A. ( 2006). Tick-borne Great Island Virus: (II) Impact of age related acquired immunity on transmission in a natural seabird host. Parasitology 132 (in this issue).CrossRefGoogle Scholar
Nuttall, P. A., Carey, D., Reid, H. W. and Harrap, K. A. ( 1981). Orbiviruses and bunyaviruses from a seabird colony in Scotland. Journal of General Virology 57, 127137.CrossRefGoogle Scholar
Nuttall, P. A., Kelly, T. C., Carey, D., Moss, S. R. and Harrap, K. A. ( 1984 a). Mixed infections with tick-borne viruses in a seabird colony in Eire. Archives of Virology 79, 3544.Google Scholar
Nuttall, P. A., Moss, S. R., Jones, L. D. and Carey, D. ( 1984 b). Comparison of mice and cell cultures for isolation of tick-borne viruses. Journal of Virological Methods 9, 2733.Google Scholar
Nuttall, P. A. ( 1985). Tick-borne viruses in seabird colonies. Seabird 7, 3642.Google Scholar
Porter, J. M. and Coulson, J. C. ( 1987). Long term changes in recruitment to the breeding group, and quality of recruits at a kittiwake Rissa tridactyla colony. Journal of Animal Ecology 56, 675690.CrossRefGoogle Scholar
Randolph, S. E., Gern, L. and Nuttall, P. A. ( 1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472479.CrossRefGoogle Scholar
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, 177186.CrossRefGoogle Scholar
Rappole, J. H., Derrickson, S. R. and Hubalek, Z. ( 2000). Migratory birds and spread of West Nile virus in the Western Hemisphere. Emerging Infections and Diseases 6, 319328.CrossRefGoogle Scholar