Skip to main content

Host–parasite biology in the real world: the field voles of Kielder

  • A. K. TURNER (a1), P. M. BELDOMENICO (a1) (a2) (a3), K. BOWN (a1) (a4), S. J. BURTHE (a1) (a2) (a5), J. A. JACKSON (a1) (a6), X. LAMBIN (a7) and M. BEGON (a1)...

Research on the interactions between the field voles (Microtus agrestis) of Kielder Forest and their natural parasites dates back to the 1930s. These early studies were primarily concerned with understanding how parasites shape the characteristic cyclic population dynamics of their hosts. However, since the early 2000s, research on the Kielder field voles has expanded considerably and the system has now been utilized for the study of host–parasite biology across many levels, including genetics, evolutionary ecology, immunology and epidemiology. The Kielder field voles therefore represent one of the most intensely and broadly studied natural host–parasite systems, bridging theoretical and empirical approaches to better understand the biology of infectious disease in the real world. This article synthesizes the body of work published on this system and summarizes some important insights and general messages provided by the integrated and multidisciplinary study of host–parasite interactions in the natural environment.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Host–parasite biology in the real world: the field voles of Kielder
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Host–parasite biology in the real world: the field voles of Kielder
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Host–parasite biology in the real world: the field voles of Kielder
      Available formats
The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution licence
Corresponding author
* Corresponding author. Institute of Integrative Biology, University of Liverpool, Crown Street, Liverpool L69 7ZB, UK. E-mail:
Hide All
Acevedo-Whitehouse, K. and Cunningham, A. A. (2006). Is MHC enough for understanding wildlife immunogenetics? Trends in Ecology and Evolution 21, 433438. doi: 10.1016/j.tree.2006.05.010.
Albright, J. W. and Albright, J. F. (1991). Rodent trypanosomes: their conflict with the immune system of the host. Parasitology Today 7, 137140.
Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: part I. Nature 280, 361367. doi: 10.1038/280361a0.
Arthur, D. R. (1963). British Ticks. Butterworths, London, UK.
Ayres, J. S. and Schneider, D. S. (2012). Tolerance of infections. Annual Review of Immunology 30, 271294. doi: 10.1146/annurev-immunol-020711-075030.
Baxby, D. and Bennett, M. (1999). Cowpox virus (Poxviridae). In Encyclopedia of Virology (ed. Webster, R. G. and Granhoff, A.), pp. 298304. Academic Press, London, UK.
Baxby, D., Bennett, M. and Getty, B. (1994). Human cowpox 1969–93: a review based on 54 cases. British Journal of Dermatology 131, 598607.
Begon, M. (2003). Disease: health effects on humans, population effects on rodents. In Rats, Mice and People: Rodent Biology and Management (ed. Singleton, G. R., Hinds, L. A., Krebs, C. J. and Spratt, D. M.), pp. 1319. Australian Centre for International Agricultural Research, Canberra, Australia.
Begon, M. (2008). Effects of host diversity on disease dynamics. In Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems (ed. Ostfeld, R. S., Keesing, F. and Eviner, V. T.), pp. 1229. Princeton University Press, Princeton, NJ, USA.
Begon, M. and Bowers, R. G. (1994). Host–host–pathogen models and microbial pest control: the effect of host self regulation. Journal of Theoretical Biology 169, 275287.
Begon, M., Sait, S. M. and Thompson, D. J. (1996). Predator–prey cycles with period shifts between two-and three-species systems. Nature 381, 311315. doi: 10.1038/381311a0.
Begon, M., Feore, S. M., Bown, K., Chantrey, J., Jones, T. and Bennett, M. (1998). Population and transmission dynamics of cowpox in bank voles: testing fundamental assumptions. Ecology Letters 1, 8286.
Begon, M., Hazel, S. M., Baxby, D., Bown, K., Cavanagh, R., Chantrey, J., Jones, T. and Bennett, M. (1999). Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proceedings of the Royal Society B: Biological Sciences 266, 19391945.
Begon, M., Hazel, S. M., Telfer, S., Bown, K., Carslake, D., Cavanagh, R., Chantrey, J., Jones, T. and Bennett, M. (2003). Rodents, cowpox virus and islands: densities, numbers and thresholds. Journal of Animal Ecology 72, 343355. doi: 10.1046/j.1365-2656.2003.00705.x.
Begon, M., Telfer, S., Burthe, S., Lambin, X., Smith, M. J. and Paterson, S. (2009 a). Effects of abundance on infection in natural populations: field voles and cowpox virus. Epidemics 1, 3546. doi: 10.1016/j.epidem.2008.10.001.
Begon, M., Telfer, S., Smith, M. J., Burthe, S., Paterson, S. and Lambin, X. (2009 b). Seasonal host dynamics drive the timing of recurrent epidemics in a wildlife population. Proceedings of the Royal Society B: Biological Sciences 276, 16031610. doi: 10.1098/rspb.2008.1732.
Beldomenico, P. M. and Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25, 2127. doi: 10.1016/j.tree.2009.06.015.
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008 a). Poor condition and infection: a vicious circle in natural populations. Proceedings of the Royal Society of London B: Biological Sciences 275, 17531759. doi: 10.1098/rspb.2008.0147.
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008 b). The dynamics of health in wild field vole populations: a haematological perspective. Journal of Animal Ecology 77, 984997. doi: 10.1111/j.1365-2656.2008.01413.x.
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008 c). Azurocytes in wild field voles: factors associated with their occurrence. EcoHealth 5, 317327. doi: 10.1007/s10393-008-0186-9.
Beldomenico, P. M., Telfer, S., Lukomski, L., Gebert, S. and Bennett, M. (2009 a). Host condition and individual risk of cowpox virus infection in natural animal populations: cause or effect? Epidemiology and Infection 137, 12951301. doi: 10.1017/S0950268808001866.Host.
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2009 b). The vicious circle and infection intensity: the case of Trypanosoma microti in field vole populations. Epidemics 1, 162167. doi: 10.1016/j.epidem.2009.05.002.
Bierman, S. M., Fairbairn, J. P., Petty, S. J., Elston, D. A., Tidhar, D. and Lambin, X. (2006). Changes over time in the spatiotemporal dynamics of cyclic populations of field voles (Microtus agrestis L.). American Naturalist 167, 583590. doi: 10.1086/501076.
Birtles, R. J. (2005). Bartonellosis. In Arthropod-borne Infectious Diseases of the Dog and Cat (ed. Shaw, S. E. and Day, M. J.), pp. 110119. CRC Press, London, UK.
Birtles, R. J., Harrison, T. G. and Molyneux, D. H. (1994). Grahamella in small woodland mammals in the U.K.: isolation, prevalence and host specificity. Annals of Tropical Medicine and Parasitology 88, 317327.
Birtles, R. J., Hazel, S. M., Bennett, M., Bown, K., Raoult, D. and Begon, M. (2001). Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126, 323329.
Blanchet, S., Méjean, L., Bourque, J.-F., Lek, S., Thomas, F., Marcogliese, D. J., Dodson, J. J. and Loot, G. (2009). Why do parasitized hosts look different? Resolving the “chicken-egg” dilemma. Oecologia 160, 3747. doi: 10.1007/s00442-008-1272-y.
Boonstra, R. and Krebs, C. (1979). Viability of large- and small-sized adults in fluctuating vole populations. Ecology 60, 567573.
Bown, K. J., Begon, M., Bennett, M., Woldehiwet, Z. and Ogden, N. H. (2003). Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases 9, 6370. doi: 10.3201/eid0901.020169.
Bown, K. J., Begon, M., Bennett, M., Birtles, R. J., Burthe, S., Lambin, X., Telfer, S., Woldehiwet, Z. and Ogden, N. H. (2006). Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector Borne and Zoonotic Diseases 6, 404410. doi: 10.1089/vbz.2006.6.404.
Bown, K. J., Lambin, X., Telford, G. R., Ogden, N. H., Telfer, S., Woldehiwet, Z. and Birtles, R. J. (2008). Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Applied and Environmental Microbiology 74, 71187125. doi: 10.1128/AEM.00625-08.
Bown, K. J., Lambin, X., Ogden, N. H., Begon, M., Telford, G., Woldehiwet, Z. and Birtles, R. J. (2009). Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerging Infectious Diseases 15, 1948–1954. doi: 10.3201/eid1512.090178.
Bown, K. J., Lambin, X., Telford, G., Heyder-Bruckner, D., Ogden, N. H. and Birtles, R. J. (2011). The common shrew (Sorex araneus): a neglected host of tick-borne infections? Vector Borne and Zoonotic Diseases 11, 947953. doi: 10.1089/vbz.2010.0185.
Bradley, J. E. and Jackson, J. A. (2008). Measuring immune system variation to help understand host–pathogen community dynamics. Parasitology 135, 807823. doi: 10.1017/S0031182008000322.
Buffet, J.-P., Kosoy, M. and Vayssier-Taussat, M. (2013). Natural history of Bartonella infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiology 8, 11171128. doi: 10.2217/fmb.13.77.
Burthe, S., Telfer, S., Lambin, X., Bennett, M., Carslake, D., Smith, A. and Begon, M. (2006). Cowpox virus infection in natural field vole Microtus agrestis populations: delayed density dependence and individual risk. Journal of Animal Ecology 75, 14161425. doi: 10.1111/j.1365-2656.2006.01166.x.
Burthe, S., Telfer, S., Begon, M., Bennett, M., Smith, A. and Lambin, X. (2008 a). Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival. Journal of Animal Ecology 77, 110119. doi: 10.1111/j.1365-2656.2007.01302.x.
Burthe, S., Bennett, M., Kipar, A., Lambin, X., Smith, A., Telfer, S. and Begon, M. (2008 b). Tuberculosis (Mycobacterium microti) in wild field vole populations. Parasitology 135, 309317. doi: 10.1017/S0031182007003940.
Burthe, S. J., Lambin, X., Telfer, S., Douglas, A., Beldomenico, P., Smith, A. and Begon, M. (2010). Individual growth rates in natural field vole, Microtus agrestis, populations exhibiting cyclic population dynamics. Oecologia 162, 653661. doi: 10.1007/s00442-009-1495-6.
Carslake, D., Bennett, M., Bown, K., Hazel, S., Telfer, S. and Begon, M. (2005). Space-time clustering of cowpox virus infection in wild rodent populations. Journal of Animal Ecology 74, 647655.
Carslake, D., Bennett, M., Hazel, S., Telfer, S. and Begon, M. (2006). Inference of cowpox virus transmission rates between wild rodent host classes using space-time interaction. Proceedings of the Royal Society B: Biological Sciences 273, 775782.
Cavanagh, R., Begon, M., Bennett, M., Ergon, T., Graham, I. M., de Haas, P., Hart, C., Koedam, M., Kremer, K., Lambin, X., Roholl, P. and van Soolingen, D. (2002). Mycobacterium microti infection (vole tuberculosis) in wild rodent populations. Journal of Clinical Microbiology 40, 32813285. doi: 10.1128/JCM.40.9.3281.
Cavanagh, R. D., Lambin, X., Ergon, T., Bennett, M., Graham, I. M., van Soolingen, D. and Begon, M. (2004). Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proceedings of the Royal Society B: Biological Sciences 271, 859867. doi: 10.1098/rspb.2003.2667.
Chantrey, J., Meyer, H., Baxby, D., Begon, M., Bown, K. J., Hazel, S. M., Jones, T., Montgomery, W. I. and Bennett, M. (1999). Cowpox: reservoir hosts and geographic range. Epidemiology and Infection 122, 455460.
Chen, S. M., Dumler, J. S., Bakken, J. S. and Walker, D. H. (1994). Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. Journal of Clinical Microbiology 32, 589595.
Chitty, D. (1952). Mortality among voles (Microtus agrestis) at Lake Vyrnwy, Montgomeryshire, in 1936–9. Philosophical Transactions of the Royal Society of London B: Biological Sciences 236, 505552.
Chitty, D. (1954). Tuberculosis among wild voles: with a discussion of other pathological conditions among certain mammals and birds. Ecology 35, 227237.
Chitty, D. (1996). Do Lemmings Commit Suicide? Beautiful Hypotheses and Ugly Facts. Oxford University Press, New York, NY, USA.
Clutton-Brock, T. H. and Pemberton, J. M. (eds.) (2004). Soay Sheep: Dynamics and Selection in an Island Population. Cambridge University Press, Cambridge, UK.
Coltman, D. W., Wilson, K., Pilkington, J. G., Stear, M. J. and Pemberton, J. M. (2001). A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep. Parasitology 122, 571582.
Crouch, A. C., Baxby, D., McCracken, C. M., Gaskell, R. M. and Bennett, M. (1995). Serological evidence for the reservoir hosts of cowpox virus in British wildlife. Epidemiology and Infection 115, 185191.
Davis, S., Begon, M., De Bruyn, L., Ageyev, V. S., Klassovskiy, N. L., Pole, S. B., Viljugrein, H., Stenseth, N. C. and Leirs, H. (2004). Predictive thresholds for plague in Kazakhstan. Science 304, 736738. doi: 10.1126/science.1095854.
Davis, S., Trapman, P., Leirs, H., Begon, M. and Heesterbeek, J. A. P. (2008). The abundance threshold for plague as a critical percolation phenomenon. Nature 454, 634637. doi: 10.1038/nature07053.
Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P. and French, S. S. (2011). Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. Journal of Animal Ecology 80, 710730. doi: 10.1111/j.1365-2656.2011.01813.x.
Dye, C. and Williams, B. G. (1995). Nonlinearities 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. 260279. Cambridge University Press, Cambridge, UK.
Elton, C. S. (1924). Periodic fluctuations in the numbers of animals: their causes and effects. Jorunal of Experimental Biology 2, 119163.
Elton, C. S. (1942). Voles, Mice and Lemmings. Clarendon Press, Oxford, UK.
Elton, C. S., Ford, E. B., Baker, J. R. and Gardner, A. D. (1931). The health and parasites of a wild mouse population. Proceedings of the Zoological Society of London 101, 657721.
Elton, C. S., Davis, D. H. S. and Findlay, G. M. (1935). An epidemic among voles (Microtus agrestis) on the Scottish Border in the spring of 1934. Journal of Animal Ecology 4, 277288.
Emmanuel, F. X., Seagar, A.-L., Doig, C., Rayner, A., Claxton, P. and Laurenson, I. (2007). Human and animal infections with Mycobacterium microti, Scotland. Emerging Infectious Diseases 13, 19241927.
Ergon, T., Lambin, X. and Stenseth, N. (2001 a). Life-history traits of voles in a fluctuating population respond to the immediate environment. Nature 411, 10431045.
Ergon, T., MacKinnon, J. L., Stenseth, N. C., Boonstra, R. and Lambin, X. (2001 b). Mechanisms for delayed density-dependent reproductive traits in field voles, Microtus agrestis: the importance of inherited environmental effects. Oikos 95, 185197.
Ergon, T., Ergon, R., Begon, M., Telfer, S. and Lambin, X. (2011). Delayed density-dependent onset of spring reproduction in a fluctuating population of field voles. Oikos 120, 934940. doi: 10.1111/j.1600-0706.2010.18983.x.
Ezenwa, V. O., Etienne, R. S., Luikart, G., Beja-Pereira, A. and Jolles, A. E. (2010). Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. American Naturalist 176, 613624. doi: 10.1086/656496.
Feldman, B. F., Zinkl, J. G. and Jain, N. C. (2000). Schalm's Veterinary Hematology. Lippincott Williams & Wilkins, Philadelphia, PA, USA.
Feore, S. M., Bennett, M., Chantrey, J., Jones, T., Baxby, D. and Begon, M. (1997). The effect of cowpox virus infection on fecundity in bank voles and wood mice. Proceedings of the Royal Society B: Biological Sciences 264, 14571461. doi: 10.1098/rspb.1997.0202.
Foggie, A. (1949). Studies on tick-borne fever in sheep. Journal of General Microbiology 3, vvi.
Graham, I. M. and Lambin, X. (2002). The impact of weasel predation on cyclic field-vole survival: the specialist predator hypothesis contradicted. Journal of Animal Ecology 71, 946956. doi: 10.1046/j.1365-2656.2002.00657.x.
Hazel, S. M., Bennett, M., Chantrey, J., Bown, K., Cavanagh, R., Jones, T. R., Baxby, D. and Begon, M. (2000). A longitudinal study of an endemic disease in its wildlife reservoir: cowpox and wild rodents. Epidemiology and Infection 124, 551562.
Hudson, J. R. (1950). The recognition off tick-borne fever as a disease of cattle. British Veterinary Journal 106, 317.
Huitu, O., Jokinen, I., Korpimäki, E., Koskela, E. and Mappes, T. (2007). Phase dependence in winter physiological condition of cyclic voles. Oikos 116, 565577. doi: 10.1111/j.2007.0030-1299.15488.x.
Jackson, J. A., Pleass, R. J., Cable, J., Bradley, J. E. and Tinsley, R. C. (2006). Heterogeneous interspecific interactions in a host–parasite system. International Journal for Parasitology 36, 13411349. doi: 10.1016/j.ijpara.2006.07.003.
Jackson, J. A., Friberg, I. M., Bolch, L., Lowe, A., Ralli, C., Harris, P. D., Behnke, J. M. and Bradley, J. E. (2009). Immunomodulatory parasites and Toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals. BMC Biology 7, 16. doi: 10.1186/1741-7007-7-16.
Jackson, J. A., Begon, M., Birtles, R., Paterson, S., Friberg, I. M., Hall, A., Lowe, A., Ralli, C., Turner, A., Zawadzka, M. and Bradley, J. E. (2011). The analysis of immunological profiles in wild animals: a case study on immunodynamics in the field vole, Microtus agrestis . Molecular Ecology 20, 893909. doi: 10.1111/j.1365-294X.2010.04907.x.
Kipar, A., Burthe, S. J., Hetzel, U., Rokia, M. A., Telfer, S., Lambin, X., Birtles, R. J., Begon, M. and Bennett, M. (2013). Mycobacterium microti tuberculosis in its maintenance host, the field vole (Microtus agrestis): characterization of the disease and possible routes of transmission. Veterinary Pathology [Epub ahead of print]. doi: 10.1177/0300985813513040.
Kosoy, M. Y., Regnery, R. L., Tzianabos, T., Marston, E. L., Jones, D. C., Green, D., Maupin, G. O., Olson, J. G. and Childs, J. E. (1997). Distribution, diversity, and host specificity of Bartonella in rodents from the Southeastern United States. American Journal of Tropical Medicine and Hygiene 57, 578588.
Lambin, X., Elston, D. A., Petty, S. J. and MacKinnon, J. L. (1998). Spatial asynchrony and periodic travelling waves in cyclic populations of field voles. Proceedings of the Royal Society B: Biological Sciences 265, 14911496. doi: 10.1098/rspb.1998.0462.
Lambin, X., Petty, S. J. and Mackinnon, J. L. (2000). Cyclic dynamics in field vole populations and generalist predation. Journal of Animal Ecology 69, 106119. doi: 10.1046/j.1365-2656.2000.00380.x.
Lochmiller, R. (1996). Immunocompetence and animal population regulation. Oikos 76, 594602.
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798. doi: 10.1034/j.1600-0706.2000.880110.x.
Mackinnon, J. L., Petty, S. J., Elston, D. A., Thomas, C. J., Sherratt, T. N. and Lambin, X. (2001). Scale invariant spatio-temporal patterns of field vole density. Journal of Animal Ecology 70, 101111. doi: 10.1111/j.1365-2656.2001.00479.x.
Martin, L. B., Hawley, D. M. and Ardia, D. R. (2011). An introduction to ecological immunology. Functional Ecology 25, 14. doi: 10.1111/j.1365-2435.2010.01820.x.
Massung, R. F., Priestley, R. A., Miller, N. J., Mather, T. N. and Levin, M. L. (2003). Inability of a variant strain of Anaplasma phagocytophilum to infect mice. Journal of Infectious Diseases 188, 17571763. doi: 10.1086/379725.
May, R. M. and Anderson, R. M. (1979). Population biology of infectious diseases: part II. Nature 280, 455461. doi: 10.1038/280455a0.
Medzhitov, R., Schneider, D. S. and Soares, M. P. (2012). Disease tolerance as a defense strategy. Science 335, 936941. doi: 10.1126/science.1214935.
Mihok, S. and Schwartz, B. (1991). Artificial induction of azurocytes in the meadow vole (Microtus pennsylvanicus). Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 99, 213218. doi: 10.1016/0742-8413(91)90102-Y.
Mihok, S., Descoteaux, J.-P., Lawton, T., Lobreau, A. and Schwartz, B. (1987). The azurocyte: a new kind of leukocyte from wild voles (Microtus). Canadian Journal of Zoology 65, 5462.
Morick, D., Krasnov, B. R., Khokhlova, I. S., Gutiérrez, R., Gottlieb, Y. and Harrus, S. (2013). Vertical nontransovarial transmission of Bartonella in fleas. Molecular Ecology 22, 47474752. doi: 10.1111/mec.12408.
Myllymaki, A., Paasikallio, A., Pankakoski, E. and Kanervo, V. (1971). Removal experiments on small quadrats as a means of rapid assessment of the abundance of small mammals. Annales Zoologici Fennici 8, 177185.
Niemann, S., Richter, E., Dalügge-Tamm, H., Schlesinger, H., Graupner, D., Königstein, B., Gurath, G., Greinert, U. and Rüsch-Gerdes, S. (2000). Two cases of Mycobacterium microti derived tuberculosis in HIV-negative immunocompetent patients. Emerging Infectious Diseases 6, 539542. doi: 10.3201/eid0605.000516.
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, 111118.
Noyes, H. A., Ambrose, P., Barker, F., Begon, M., Bennet, M., Bown, K. J. and Kemp, S. J. (2002). Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology 124, 185190.
Paun, A., Reinert, J. T., Jiang, Z., Medin, C., Balkhi, M. Y., Fitzgerald, K. A. and Pitha, P. M. (2008). Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response. Journal of Biological Chemistry 283, 1429514308. doi: 10.1074/jbc.M800501200.
Pedersen, A. B. and Babayan, S. A. (2011). Wild immunology. Molecular Ecology 20, 872880. doi: 10.1111/j.1365-294X.2010.04938.x.
Pedersen, A. B. and Greives, T. J. (2008). The interaction of parasites and resources cause crashes in a wild mouse population. Journal of Animal Ecology 77, 370377. doi: 10.1111/j.1365-2656.2007.01321.x.
Petty, S. J. (1992). Ecology of the tawny owl Strix aluco in the spruce forests of Northumberland and Argyll. PhD thesis. Open University, Milton Keynes.
Petty, S. J., Lambin, X., Sherratt, T. N., Thomas, C. J., Mackinnon, J. L., Coles, C. F., Davison, M. and Little, B. (2000). Spatial synchrony in field vole Microtus agrestis abundance in a coniferous forest in northern England: the role of vole-eating raptors. Journal of Applied Ecology 37, 136147. doi: 10.1046/j.1365-2664.2000.00473.x.
Piertney, S. B. and Oliver, M. K. (2006). The evolutionary ecology of the major histocompatibility complex. Heredity 96, 721. doi: 10.1038/sj.hdy.6800724.
Pusenius, J. and Viitala, J. (1993). Varying spacing behaviour of breeding field voles, Microtus agrestis . Annales Zoologici Fennici 30, 143152.
Randolph, S. E. (1975). Patterns of distribution of the tick Ixodes trianguliceps Birula on its hosts. Journal of Animal Ecology 44, 451474.
Randolph, S. E. (1991). The effect of Babesia microti on feeding and survival in its tick vector, Ixodes trianguliceps . Parasitology 102, 916.
Randolph, S. E. (1995). Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys glareolus). Parasitology 110, 287295.
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847863.
Reiner, S. L. (2007). Development in motion: helper T cells at work. Cell 129, 3336. doi: 10.1016/j.cell.2007.03.019.
Schmid-Hempel, P. (2011). Evolutionary Parasitology: the Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford University Press, Oxford, UK.
Schulenburg, H., Kurtz, J., Moret, Y. and Siva-Jothy, M. T. (2009). Introduction. Ecological immunology. Philosophical Transactions of the Royal Society of London B: Biological Sciences 364, 314. doi: 10.1098/rstb.2008.0249.
Seet, B. T., Johnston, J. B., Brunetti, C. R., Barrett, J. W., Everett, H., Cameron, C., Sypula, J., Nazarian, S. H., Lucas, A. and McFadden, G. (2003). Poxviruses and immune evasion. Annual Review of Immunology 21, 377423. doi: 10.1146/annurev.immunol.21.120601.141049.
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317321.
Sherlock, C., Xifara, T., Telfer, S. and Begon, M. (2013). A coupled hidden Markov model for disease interactions. Journal of the Royal Statistical Society: Series C (Applied Statistics) 62, 609627.
Sherratt, J. A. (2001). Periodic travelling waves in cyclic predator–prey systems. Ecology Letters 4, 3037. doi: 10.1046/j.1461-0248.2001.00193.x.
Smith, A., Telfer, S., Burthe, S., Bennett, M. and Begon, M. (2005). Trypanosomes, fleas and field voles: ecological dynamics of a host-vector–parasite interaction. Parasitology 131, 355. doi: 10.1017/S0031182005007766.
Smith, A., Telfer, S., Burthe, S., Bennett, M. and Begon, M. (2006). A role for vector-independent transmission in rodent trypanosome infection? International Journal for Parasitology 36, 13591366. doi: 10.1016/j.ijpara.2006.06.014.
Smith, M. J., White, A., Sherratt, J. A., Telfer, S., Begon, M. and Lambin, X. (2008). Disease effects on reproduction can cause population cycles in seasonal environments. Journal of Animal Ecology 77, 378389. doi: 10.1111/j.1365-2656.2007.01328.x.
Smith, M. J., Telfer, S., Kallio, E. R., Burthe, S., Cook, A. R., Lambin, X. and Begon, M. (2009). Host–pathogen time series data in wildlife support a transmission function between density and frequency dependence. Proceedings of the National Academy of Sciences USA 106, 79057909.
Snow, K. R. (1979). Identification of Larval Ticks Found on Small Mammals in Britain. The Mammal Society, Reading.
Spurgin, L. G. and Richardson, D. S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society B: Biological Sciences 277, 979988. doi: 10.1098/rspb.2009.2084.
Stockham, S. and Scott, M. (2002). Fundamentals of Veterinary Clinical Pathology. Iowa State Press, Ames, IA, USA.
Stone, L., Olinky, R. and Huppert, A. (2007). Seasonal dynamics of recurrent epidemics. Nature 446, 533536. doi: 10.1038/nature05638.
Telfer, S., Bennett, M., Bown, K., Cavanagh, R., Crespin, L., Hazel, S., Jones, T. and Begon, M. (2002). The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71, 558568.
Telfer, S., Bown, K., Sekules, R., Begon, M., Hayden, T. and Birtles, R. (2005 a). Disruption of a host–parasite system following the introduction of an exotic host species. Parasitology 130, 661668.
Telfer, S., Bennett, M., Bown, K., Carslake, D., Cavanagh, R. D., Hazel, S. M., Jones, T. and Begon, M. (2005 b). Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents. Oikos 109, 317322.
Telfer, S., Begon, M., Bennett, M., Bown, K. J., Burthe, S., Lambin, X., Telford, G. and Birtles, R. (2007 a). Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology 134, 413425. doi: 10.1017/S0031182006001624.
Telfer, S., Clough, H. E., Birtles, L. R. J., Bennett, M., Carslake, D., Helyar, S. and Begon, M. (2007 b). Ecological differences and coexistence in a guild of microparasites: Bartonella in wild rodents. Ecology 88, 18411849.
Telfer, S., Birtles, R., Bennett, M., Lambin, X., Paterson, S. and Begon, M. (2008). Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135, 767781. doi: 10.1017/S0031182008000395.
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243246. doi: 10.1126/science.1190333.
Tizard, I. R. (2004). Veterinary Immunology. An Introduction. Saunders, Philadelphia, PA, USA.
Turner, A. K. and Paterson, S. (2013). Wild rodents as a model to discover genes and pathways underlying natural variation in infectious disease susceptibility. Parasite Immunology 35, 386395.
Turner, A. K., Begon, M., Jackson, J. A., Bradley, J. E. and Paterson, S. (2011). Genetic diversity in cytokines associated with immune variation and resistance to multiple pathogens in a natural rodent population. PLOS Genetics 7, e1002343. doi: 10.1371/journal.pgen.1002343.
Turner, A. K., Begon, M., Jackson, J. and Paterson, S. (2012). Evidence for selection at cytokine loci in a natural population of field voles (Microtus agrestis). Molecular Ecology 21, 16321646.
Van Soolingen, D., van der Zanden, A. G., de Haas, P. E., Noordhoek, G. T., Kiers, A., Foudraine, N. A., Portaels, F., Kolk, A. H., Kremer, K. and van Embden, J. D. (1998). Diagnosis of Mycobacterium microti infections among humans by using novel genetic markers. Journal of Clinical Microbiology 36, 18401845.
Wells, A. Q. (1946). The Murine Type of Tubercle Bacillus: the Vole Acid-fast Bacillus. By A. Q. Wells. With notes on the morphology of infection by the vole acid-fast bacillus by A. H. T. Robb-Smith. Medical Research Council, London, UK.
Wiger, R. (1977). Some pathological effects of endoparasites on rodents with special reference to the population ecology of microtines. Oikos 29, 598606.
Woldehiwet, Z. (2010). The natural history of Anaplasma phagocytophilum . Veterinary Parasitology 167, 108122. doi: 10.1016/j.vetpar.2009.09.013.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 61
Total number of PDF views: 209 *
Loading metrics...

Abstract views

Total abstract views: 409 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd March 2018. This data will be updated every 24 hours.