Infection dynamics of endemic malaria in a wild bird population: Parasite species-dependent drivers of spatial and temporal variation in transmission rates

Journal of Animal Ecology

Volumn 80, Issue 6, 2011, Pages 1207-1216

  Lachish, Shelly ^a   Knowles, Sarah C L ^a,b   Alves, Ricardo ^a   Wood, Matthew J ^a,c   Sheldon, Ben C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF GLOUCESTERSHIRE   (United Kingdom)

Author keywords

Avian malaria; Blue tits; Cyanistes caeruleus; Disease incidence rate; Environmental heterogeneity; Host age; Host sex; Multievent mark recapture models; Plasmodium; Transition rates

Indexed keywords

AGE; BIOTIC FACTOR; BIRD; DISEASE INCIDENCE; DISEASE TRANSMISSION; DISEASE VECTOR; DIVERGENCE; ENDEMIC SPECIES; EPIDEMIOLOGY; HEMOPARASITE; HETEROGENEITY; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; INFECTIVITY; MALARIA; MARK-RECAPTURE METHOD; PROTIST; SEX DETERMINATION; SONGBIRD; SPATIAL VARIATION; TEMPORAL VARIATION; WILD POPULATION;

ANIMAL; ARTICLE; AVIAN MALARIA; BIOLOGICAL MODEL; DISEASE TRANSMISSION; HOST PARASITE INTERACTION; INCIDENCE; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM; POPULATION DYNAMICS; PREVALENCE; SONGBIRD; SPECIES DIFFERENCE; UNITED KINGDOM;

ANIMALS; ENGLAND; HOST-PARASITE INTERACTIONS; INCIDENCE; MALARIA, AVIAN; MODELS, BIOLOGICAL; PLASMODIUM; POPULATION DYNAMICS; PREVALENCE; SONGBIRDS; SPECIES SPECIFICITY;

AVES; CYANISTES CAERULEUS; PLASMODIUM PARASITES; PLASMODIUM RELICTUM;

EID: 80053636950     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2011.01893.x     Document Type: Article

References (57)

1. Anderson, R.M. & May, R.M. (1979) Population biology of infectious diseases: Part 1. Nature, 280, 361-367.
2. Anderson, R.M. & May, R.M. (1986) The invasion, persistence and spread of infectious diseases within animal and plant communities. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 314, 533-570.
3. Arriero, E. & Moller, A.P. (2008) Host ecology and life-history traits associated with blood parasite species richness in birds. Journal of Evolutionary Biology, 21, 1504-1513.
4. Atkinson, C.T. & LaPointe, D.A. (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery, 23, 53-63.
5. Atkinson, C.T. & Samuel, M.D. (2010) Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on 'apapane Himatione sanguinea. Journal of Avian Biology, 41, 357-366.
6. Atkinson, C.T., Lease, J.K., Dusek, R.J. & Samuel, M.D. (2005) Prevalence of pox-like lesions and malaria in forest bird communities on leeward Mauna Loa Volcano, Hawaii. Condor, 107, 537-546.
7. Balls, M.J., Bodker, R., Thomas, C.J., Kisinza, W., Msangeni, H.A. & Lindsay, S.W. (2004) Effect of topography on the risk of malaria infection in the Usambara Mountains, Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 98, 400-408.
8. Beldomenico, P.M., Telfer, S., Lukomski, L., Gebert, S., Bennett, M. & Begon, M. (2009) Host condition and individual risk of cowpox virus infection in natural animal populations: cause or effect? Epidemiology and Infection, 137, 1295-1301.
9. Bensch, S., Perez-Tris, J., Walling, C.A. & Hellgren, O. (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution, 58, 1617-1621.
10. Bolzoni, L., Real, L. & De Leo, G. (2007) Transmission heterogeneity and control strategies for infectious disease emergence. PLoS ONE, 2, e747.
11. Borer, E.T., Seabloom, E.W., Mitchell, C.E. & Power, A.G. (2010) Local context drives infection of grasses by vector-borne generalist viruses. Ecology Letters, 13, 810-818.
12. Byers, J.E., Blakeslee, A.M.H., Linder, E., Cooper, A.B. & Maguire, T.J. (2008) Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology, 89, 439-451.
13. Caley, P. & Hone, J. (2004) Disease transmission between and within species, and the implications for disease control. Journal of Applied Ecology, 41, 94-104.
14. Choquet, R. (2009) Program E-SUREGE: a software application for fitting multievent models. Modelling Demographic Processes in Marked Populations (eds D.L. Thomspon, E.G. Cooch & M.J. Conroy). pp. 845-866, Springer, New York.
15. Conn, P.B. & Cooch, E.G. (2009) Multistate capture-recapture analysis under imperfect state observation: an application to disease models. Journal of Applied Ecology, 46, 486-492.
16. Cosgrove, C.L., Wood, M.J., Day, K.P. & Sheldon, B.C. (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology, 77, 540-548.
17. Cranston, P.S., Ramsdale, C.D., Snow, K.R. & White, G.B. (1987) Adults, larvae and pupae of british mosquitoes (Culicidae). Scientific Publication, 48, 1-152.
18. Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica, 78, 103-116.
19. Dybdahl, M.F. & Storfer, A. (2003) Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology & Evolution, 18, 523-530.
20. Faustino, C.R., Jennelle, C.S., Connolly, V., Davis, A.K., Swarthout, E.C., Dhondt, A.A. & Cooch, E.G. (2004) Mycoplasma gallisepticum infection dynamics in a house finch population: seasonal variation in survival, encounter and transmission rate. Journal of Animal Ecology, 73, 651-669.
21. Foley, D.H., Torres, E.P., Mueller, I., Bryan, J.H. & Bell, V. (2003) Host-dependent Anopheles flavirostris larval distribution reinforces the risk of malaria near water. Transactions of the Royal Society of Tropical Medicine and Hygiene, 97, 283-287.
22. Freed, L.A., Cann, R.L., Goff, M.L., Kuntz, W.A. & Bodner, G.R. (2005) Increase in avian malaria at upper elevation in Hawai'i. The Condor, 107, 753-764.
23. Garant, D., Kruuk, L.E.B., Wilkin, T.A., McCleery, R.H. & Sheldon, B.C. (2005) Evolution driven by differential dispersal within a wild bird population. Nature, 433, 60-65.
24. Harvell, D., Altizer, S., Cattadori, I.M., Harrington, L. & Weil, E. (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology, 90, 912-920.
25. Heisey, D.M., Joly, D.O. & Messier, F. (2006) The fitting of general force-of-infection models to wildlife disease prevalence data. Ecology, 87, 2356-2365.
26. Hestbeck, J.B., Nichols, J.D. & Malecki, R.A. (1991) Estimates of movement and site fidelity using mark resight data of wintering canada geese. Ecology, 72, 523-533.
27. Hudson, P.J., Rizzoli, A.P., Grenfell, B.T., Heesterbeek, H. & Dobson, A. (2002) Ecology of Wildlife Diseases. Oxford University Press, New York.
28. Jennelle, C.S., Cooch, E.G., Conroy, M.J. & Senar, J.C. (2007) State-specific detection probabilities and disease prevalence. Ecological Applications, 17, 154-167.
29. Kaltz, O. & Shykoff, J.A. (1998) Local adaptation in host-parasite systems. Heredity, 81, 361-370.
30. Knowles, S.C.L., Nakagawa, S. & Sheldon, B.C. (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Functional Ecology, 23, 405-415.
31. Knowles, S.C.L., Wood, M.J., Alves, R., Wilson, G.J., Bensch, S. & Sheldon, B.C. (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology, 20, 1062-1076.
32. Korpimäki, E., Hakkarainen, H. & Bennett, G.F. (1993) Blood parasites and reproductive success of Tengmalm's Owls: detrimental effects on females but not on males? Functional Ecology, 7, 420-426.
33. Lachish, S., Knowles, S.C.L., Alves, R., Wood, M.J. & Sheldon, B.C. (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. Journal of Animal Ecology, 80. DOI:.
34. Lafferty, K.D. & Kuris, A.M. (1999) How environmental stress affects the impacts of parasites. Limnology and Oceanography, 44, 925-931.
35. Lipsitch, M., Cohen, T., Cooper, B., Robins, J.M., Ma, S., James, L., Gopalakrishna, G., Chew, S.K., Tan, C.C., Samore, M.H., Fisman, D. & Murray, M. (2003) Transmission dynamics and control of severe acute respiratory syndrome. Science, 300, 1966-1970.
36. Loiseau, C., Iezhova, T., Valkiūnas, G., Chasar, A., Hutchinson, A., Buermann, W., Smith, T.B. & Sehgal, R.N.M. (2010) Spatial variation of Haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology, 96, 21-29.
37. Marzal, A., Bensch, S., Reviriego, M., Balbontin, J. & de Lope, F. (2008) Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology, 21, 979-987.
38. McCallum, H., Barlow, N. & Hone, J. (2001) How should pathogen transmission be modelled? Trends in Ecology & Evolution, 16, 295-300.
39. McClintock, B.T., Nichols, J.D., Bailey, L.L., MacKenzie, D.I., Kendall, W.L. & Franklin, A.B. (2010) Seeking a second opinion: uncertainty in disease ecology. Ecology Letters, 13, 659-674.
40. O'Connor, J.A., Dudaniec, R.Y. & Kleindorfer, S. (2010) Parasite infestation and predation in Darwin's small ground finch: contrasting two elevational habitats between islands. Journal of Tropical Ecology, 26, 285-292.
41. van Oers, K., Richardson, D.S., Saether, S.A. & Komdeur, J. (2010) Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection? Journal of Ornithology, 151, 69-77.
42. Osnas, E.E., Heisey, D.M., Rolley, R.E. & Samuel, M.D. (2009) Spatial and temporal patterns of chronic wasting disease: fine-scale mapping of a wildlife epidemic in Wisconsin. Ecological Applications, 19, 1311-1322.
43. Ozgul, A., Oli, M.K., Bolker, B.M. & Perez-Heydrich, C. (2009) Upper respiratory tract disease, force of infection, and effects on survival of gopher tortoises. Ecological Applications, 19, 786-798.
44. Palinauskas, V., Kosarev, V.V., Shapoval, A.P., Bensch, S. & Valkiūnas, G. (2007) Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa, 1626, 39-50.
45. Perez-Tris, J. & Bensch, S. (2005) Dispersal increases local transmission of avian malarial parasites. Ecology Letters, 8, 838-845.
46. Pope, K., Masuoka, P., Rejmankova, E., Grieco, J., Johnson, S. & Roberts, D. (2005) Mosquito habitats, land use, and malaria risk in Belize from satellite imagery. Ecological Applications, 15, 1223-1232.
47. Pradel, R. (2005) Multievent: an extension of multistate capture-recapture models to uncertain states. Biometrics, 61, 442-447.
48. Randolph, S.E. (2001) The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 356, 1045-1056.
49. Ricklefs, R.E., Fallon, S.M. & Bermingham, E. (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology, 53, 111-119.
50. Schwarz, C.J., Schweigert, J.F. & Arnason, A.N. (1993) Estimating migration rates using tag-recovery data. Biometrics, 49, 177-193.
51. Sinski, E., Pawelczyk, A., Bajer, A. & Behnke, J.M. (2006) Abundance of wild rodents, ticks and environmental risk of Lyme borreliosis: a longitudinal study in an area of Mazury Lakes district of Poland. Annals of Agricultural and Environmental Medicine, 13, 295-300.
52. Slater, L.B. (2005) Malarial birds: modeling infectious human disease in animals. Bulletin of the History of Medicine, 79, 261-294.
53. Valkiūnas, G.N. (2005) Avian Malaria Parasites and Other Haemosporidia, CRC Press, Boca Raton, FL.
54. Waldenström, J., Bensch, S., Hasselquist, D. & Ostman, O. (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology, 90, 191-194.
55. Williams, B.K., Conroy, M.J. & Nichols, J.D. (2001) Analysis and Management of Animal Populations. Academic Press, San Diego.
56. Wolinska, J. & King, K.C. (2009) Environment can alter selection in host-parasite interactions. Trends in Parasitology, 25, 236-244.
57. Wood, M.J., Cosgrove, C.L., Wilkin, T.A., Knowles, S.C.L., Day, K.P. & Sheldon, B.C. (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, 16, 3263-3273.