Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-24T02:33:56.613Z Has data issue: false hasContentIssue false
  • English
  • Français

Tick-borne Great Island Virus: (II) Impact of age-related acquired immunity on transmission in a natural seabird host

Published online by Cambridge University Press:  03 October 2005

M. A. NUNN ,
T. R. BARTON ,
S. WANLESS ,
R. S. HAILS ,
M. P. HARRIS  and
P. A. NUTTALL
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
Get access Rights & Permissions [Opens in a new window]

Abstract

Tick-borne pathogen transmission is dependent upon tick number per host and the physical and temporal distribution of each feeding stage. Age-related acquired immunity to tick and pathogen may also be important but has received less attention. In this study we evaluate which of these parameters has the greatest impact on Great Island Virus (GIV) transmission between Ixodes uriae ticks and common guillemots (Uria aalge). The study system is well suited to investigate age-related effects because the guillemot population is naturally divided into 2 groups, older breeding and younger pre-breeding adult birds. The physical distribution and timing of adult and nymphal tick feeding was similar for both guillemot age groups. However, breeding birds were parasitized by significantly more ticks (mainly nymphs). Calculations based on tick number predict virus prevalence should be higher in ticks that have fed on breeding rather than pre-breeding birds. However, empirical evidence indicates the reverse. Protective acquired immunity to GIV infection may be the reason why GIV prevalence is actually significantly lower in ticks that have fed on breeders. Far more breeding (74%) than pre-breeding (12%) guillemots had antibodies that neutralized 1 or more GIV strains. Estimates of the force of infection support the view that pre-breeding birds experience higher rates of virus infection than breeding birds. The results indicate age-related acquired immunity is a key factor in GIV transmission and highlight the need to consider age-related effects and host immunity when undertaking quantitative studies of tick-borne pathogen transmission.

Keywords

age-related immunityarbovirusUria aalgevirus transmissiontickIxodes uriae
Type
Research Article
Information
Parasitology , Volume 132 , Issue 2 , February 2006 , pp. 241 - 253
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.
Anderson, R. M. and Trewhella, W. ( 1985). Population dynamics of the badger (Meles meles) and the epidemiology of bovine tuberculosis (Mycobacterium bovis). Philosophical Transactions of the Royal Society London B310, 327–381.CrossRefGoogle Scholar
Barton, T. R. ( 1995). A modified technique for extracting live ticks from small soil and litter samples. Experimental and Applied Acarology 19, 357–360.CrossRefGoogle Scholar
Barton, T. R., Harris, M. P. and Wanless, S. ( 1995). Natural attachment duration of nymphs of the tick Ixodes uriae (Acari: Ixodidae) on kittiwake Rissa tridactyla nestlings. Experimental and Applied Acarology 19, 61–68.CrossRefGoogle Scholar
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, 571–580.CrossRefGoogle Scholar
Danchin, E. ( 1992). The incidence of the tick parasite Ixodes uriae in kittiwake Rissa tridactyla colonies in relation to the age of the colony, and mechanism of infecting new colonies. Ibis 134, 134–141.CrossRefGoogle Scholar
Du Toit, J. S., Fourie, L. J. and Horak, I. G. ( 1994). Sequential feeding of Ixodes rubicundus on its natural host, Elephantulus myurus: effects on tick mass and on engorgement and moulting success. Onderstepoort Journal of Veterinary Research 61, 143–147.Google Scholar
Dye, C. and Williams, B. G. ( 1995). Non-linearities in the dynamics of indirectly transmitted infections (or does having a vector make a difference?). In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. and Dobson, A. P.) pp. 260–279. Cambridge, Cambridge University Press.CrossRef
Elliott, J. M. ( 1983). Some Methods for the Statistical Analysis of Benthic Invertebrates. Freshwater Biological Association, Scientific Publication No. 25.
Eveleigh, E. S. and Threlfall, W. ( 1974). The biology of Ixodes (ceratixodes) uriae (White, 1852) in Newfoundland. Acarologia 16, 621–635.Google Scholar
Finney, S. K., Wanless, S. and Elston, D. A. ( 1999). Natural attachment duration of adult female ticks Ixodes uriae (Acari: Ixodidae) in free-living adult black-legged kittiwakes Rissa tridactyla. Experimental and Applied Acarology 23, 1–5.Google Scholar
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 Scholar
Gilbert, L., Jones, L. D., Laurenson, M. K., Gould, E. A., Reid, H. W. and Hudson, P. ( 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 (Suppl.) S202–S205.CrossRefGoogle Scholar
Grenfell, B. T. and Anderson, R. M. ( 1985). The estimation of age-related rates of infection from case notifications and serological data. The Journal of Hygiene 95, 419–436.CrossRefGoogle Scholar
Gupta, S., Ferguson, N. and Anderson, R. M. ( 1998). Chaos, persistence and the evolution of strain structure in populations of antigenically variable infectious agents. Science 240, 912–915.CrossRefGoogle Scholar
Halley, D. J. and Harris, M. P. ( 1994). Age related changes in the agonistic behaviour of immature common guillemots Uria aalge. Seabird 16, 8–14.Google Scholar
Halley, D. J., Harris, M. P. and Wanless, S. ( 1995). Colony attendance patterns and recruitment in immature common murres. The Auk 112, 947–957.Google Scholar
Harris, M. P. and Birkhead, T. R. ( 1985). Breeding ecology of the Atlantic Alcidae. In The Atlantic Alcidae ( ed. Nettleship, D. N. and Birkhead, T. R.), pp. 155–204. Academic Press, London.
Harris, M. P., Halley, D. J. and Swann, R. L. ( 1994). Age of first breeding in common murres. The Auk 111, 207–209.CrossRefGoogle Scholar
Harris, M. P. and Wanless, S. ( 1995). Survival and non-breeding of adult common guillemots Uria aalge. Ibis 137, 192–197.CrossRefGoogle Scholar
Harris, M. P., Wanless, S., Barton, T. R. and Elston, D. A. ( 1997). Nest site characteristics, duration of use and breeding success in the guillemot Uria aalge. Ibis 139, 468–476.CrossRefGoogle Scholar
Hart, B. L. ( 1997). Behavioural defence. In Host-Parasite Evolution: General Principles and Avian Models ( ed. D. H. Clayton and J. Moore), pp. 59–77. Oxford University Press, Oxford.
Jones, L. D. and Nuttall, P. A. ( 1989). The effect of virus-immune hosts on Thogoto virus infection of the tick Rhipicephalus appendiculatus. Virus Research 14, 129–140.CrossRefGoogle Scholar
Jones, L. D., Gaunt, M., Hails, R. S., Laurenson, K., Hudson, P. J., Henbest and Gould, E. A. ( 1997). Transmission of louping ill virus between infected and uninfected ticks cofeeding on mountain hares. Medical and Veterinary Entomology 11, 172–176.CrossRefGoogle Scholar
Koumbati, M., Mangana, O., Nomikou, K., Mellor, P. S. and Papadopoulos, O. ( 1998). Duration of bluetongue viraemia and serological responses in experimentally infected European breeds of sheep and goats. Veterinary Microbiology 64, 277–285.Google Scholar
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 spirochaete transmission to Ixodes ricinus (Acari: Ixodidae). Infection and Immunity 62, 5344–5352.Google Scholar
Kurtenbach, K., Kampen, H., Dizij, A., Arndt, S., Seitz, S., Schaible, U. E. and Simon, M. M. ( 1995). Infestation of rodents with larval Ixodes ricinus (Acari: Ixodidae) is an important factor in the transmission cycle of Borrelia burgdorferi s.l. in German woodlands. Journal of Medical and Veterinary Entomology 32, 807–817.CrossRefGoogle Scholar
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 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, 138–143.CrossRefGoogle Scholar
Levin, M. L. and Fish, D. ( 2000). Immunity reduces reservoir competence of Peromyscus leucopus for Ehrlichia phagocytophila. Infection and Immunity 68, 1514–1518.CrossRefGoogle Scholar
MacLachlan, N. J., Barratt-Boyes, S. M., Brewer, A. W. and Stott, J. L. ( 1992). Bluetongue virus infection of cattle. In Bluetongue and Related Orbiviruses pp. 725–734. A. R. Liss: New York.Google Scholar
McCoy, K. D. and Tirard, C. ( 2002). Reproductive strategies of the seabird tick Ixodes uriae (Acari: Ixodidae). Journal of Parasitology 88, 813–816.CrossRefGoogle Scholar
McCullagh, P. and Nelder, J. A. ( 1989). Generalised Linear Models, 2nd Edn. Chapman and Hall, London.
Nielsen, M. A., Staalsoe, T., Kurtzhals, J. A. L., Goka, B. Q., Dodoo, D., Alifrangis, M., Theander, T. G., Akanmori, B. D. and Hviid, L. ( 2002). Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and non-severe malaria and is modified by acquired immunity. Journal of Immunology 168, 3444–3450.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 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, 119–134.CrossRefGoogle Scholar
Nunamaker, R. A., Sieburth, P. J., Dean, V. C., Wigington, J. G., Nunamaker, C. E. and Mecham, J. O. ( 1990). Absence of transovarial transmission of bluetongue virus in Culicoides variipennis: immunogold labelling of bluetongue virus antigen in developing oocytes from Culicoides variipennis (Coquillett). Comparative Biochemistry and Physiology A 96, 19–31.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: (I) Identification of seabird host and evidence for co-feeding and viraemic transmission. Parasitology (in this issue).CrossRef
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, 127–137.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, 35–44.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, 27–33.Google Scholar
O'Callaghan, C. J., Medley, G. F., Peter, T. F. and Perry, B. D. ( 1998). Investigating the epidemiology of heartwater (Cowdria ruminantium infection) by means of a transmission dynamics model. Parasitology 117, 49–61.CrossRefGoogle Scholar
Ogden, N. H., Kurtenbach, K. and Nuttall, P. A. ( 1998). Interstadial and infestation level dependent variation in the transmission efficiency of Borrelia burgdorferi from mice to Ixodes ricinus ticks. Experimental and Applied Acarology 22, 367–372.CrossRefGoogle Scholar
Quist, C. F., Howerth, E. W., Stalknecht, D. E., Brown, J., Pisel, T. and Nettles, V. F. ( 1997). Host defence responses associated with experimental hemorrhagic disease in white-tailed deer. Journal of Wildlife Diseases 33, 584–599.CrossRefGoogle Scholar
Randolph, S. E. ( 1994). Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti. Parasitology 108, 413–419.CrossRefGoogle Scholar
Randolph, S. E. ( 1998). Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186–192.CrossRefGoogle Scholar
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 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, 177–186.CrossRefGoogle Scholar
Roy, P., Urakawa, T., Van-Dijk, A. A. and Erasmus, B. J. ( 1990). Recombinant virus vaccine for bluetongue disease in sheep. Journal of Virology 64, 1998–2003.Google Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle Scholar
Stone-Marscaht, M. A., Moss, S. R., Burage, T. G., Barber, M. L., Roy, P. and Laegrid, W. ( 1996). Immunization with VP2 is sufficient for protection against lethal challenge with African horsesickness virus type 4. Virology 220, 219–222.CrossRefGoogle Scholar
Toft, C. A., Aeschilman, A. and Bolis, L. ( 1991). Parasite-Host Associations: Coexistence or Conflict? Oxford University Press, Redwood Books, Wiltshire.
Wikel, S. K. ( 1996). Host immunity to ticks. Annual Reviews of Entomology 41, 1–22.CrossRefGoogle Scholar
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnel, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. ( 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 Scholar