Origin-related, environmental, sex, and age determinants of immunocompetence, susceptibility to ectoparasites, and disease symptoms in the barn owl

Biological Journal of the Linnean Society

Volumn 90, Issue 4, 2007, Pages 703-718

  Roulin, Alexandre ^a   Christe, Philippe ^a   Dijkstra, Cor ^b   Ducrest, Anne Lyse ^a   Jungi, Thomas W ^c  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

Carnus haemapterus; Cellular mediated immune system; Humoral immune system; Parasite; Pathogen; Tyto alba

Indexed keywords

ANTIPARASITE DEFENSE; BROOD SIZE; COEVOLUTION; ECTOPARASITE; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENCE; RAPTOR; SYMPTOM;

CARNUS; IXODES RICINUS; OVIS ARIES; STRIGIFORMES; TYTO ALBA; TYTONIDAE;

EID: 33947403925     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2007.00759.x     Document Type: Article

References (55)

1. Alonso-Alvarez C, Tella JL. 2001. Effects of experimental food restriction and body mass changes on the avian T-cell-mediated immune response. Canadian Journal of Zoology 7: 101-105.
2. Ardia DR, Schat KA, Winkler DW. 2003. Reproductive effort reduces long-term immune function in breeding tree swallows (Tachycineta bicolour). Proceedings of the Royal Society of London Series B, Biological Sciences 270: 1387-1392.
3. Bize P, Roulin A, Richner H. 2004. Parasitism, compensatory growth and bilateral asymmetry of wing feathers in Alpine swift (Apus melba) nestlings. Oikos 106: 317-323.
4. Bize P, Roulin A, Tella JL, Richner H. 2005. Female-biased mortality in experimentally parasitized Alpine swift (Apus melba). Functional Ecology 19: 405-513.
5. Bonneaud C, Mazuc J, González G, Haussy C, Chastel O, Faivre B, Sorci G. 2003. Assessing the cost of mounting an immune response. American Naturalist 161: 367-379.
6. Bos NA, Meeuwsen CG, Hooijkaas H, Benner R, Wostmann BS, Pleasants JR. 1987. Early development of Igsecreting cells in young of germ-free Balb/C mice fed a chemically defined ultrafiltered diet. Cellular Immunology 105: 235-245.
7. Brinkhof MWG, Heeb P, Kölliker M, Richner H. 1999. Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proceedings of the Royal Society of London Series B, Biological Sciences 266: 2315-2322.
8. Christe P, Arlettaz R, Vogel P. 2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat hosts (Myotis myotis). Ecology Letters 3: 207-212.
9. Christe P, de Lope F, González G, Saino N, Møller AP. 2001. The influence of environmental conditions on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia 126: 333-338.
10. Christe P, Giorgi MS, Vogel P, Arlettaz R. 2003. Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialization? Journal of Animal Ecology 72: 866-872.
11. Christe P, Møller AP, Saino N, de Lope F. 2000. Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity 85: 75-83.
12. Clayton DH, Moore J. 1997. Host-parasite evolution, General principles and avian models. Oxford: Oxford University Press.
13. Corrier DE, DeLoach JR. 1990. Interdigital skin test for evoluation of delayed hypersensitivity and cutaneous basophil hypersensitivity in young chickens. American Journal of Veterinary Research 51: 950-954.
14. Durant JM, Handrich Y. 1998. Growth and food requirement flexibility in captive nestlings of the European barn owl (Tyto alba). Journal of Zoology (London) 245: 137-145.
15. El-Leythey H, Huber-Eicher B, Jungi TW. 2003. Exploration of stress-induced immunosuppression in chickens reveals both stress-resistant and stress-susceptible antigen responses. Veterinary Immunology and Immunopathology 95: 91-101.
16. Fargallo JA, Laaksonen T, Pöyri V, Korpimäki E. 2002. Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecology Letters 5: 95-101.
17. Freitas AA, Viale AC, Sundblad A, Heusser AC, Coutinho A. 1991. Normal serum immunoglobulins participate in the selection of peripheral B-cell repertoires. Proceedings of the National Academy of Sciences of the United States of America 88: 5640-5644.
18. Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T. 2001. Induced maternal response to the Lyme disease spirochete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proceedings of the Royal Society of London Series B, Biologocal Sciences 268: 647-650.
19. Glick B. 1983. Bursa of Fabricius. In: Farner DS, King JR, Parkes KC, eds. Avian biology, Vol. 7. New York, NY: Academic Press, 443-500.
20. Hamilton WD, Zuk M. 1982. Heritable true fitness and bright birds: a role for parasites? Science 218: 384-387.
21. Hoffmann AA, Merilä J. 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends in Ecology and Evolution 14: 96-101.
22. Ilmonen P, Hasselquist D, Langefors Å, Wiehn J. 2003. Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136: 148-154.
23. John J. 1994. The avian spleen: a neglected organ. Quarterly Review Biology 69: 327-351.
24. Kilpimaa J, van de Casteele T, Jokinen I, Mappes J, Alatalo RV. 2005. Genetic and environmental variation in antibody and T-cell mediated responses in the great tit. Evolution 59: 2483-2489.
25. Kirkpatrick CE, Colvin BA. 1989. Ectoparasitic fly Carnus hemapterus (Diptera: Carnidae) in a nesting population of common barn-owls (Strigiformes: Tytonidae). Journal of Medical Entomology 26: 109-112.
26. Lifjeld JT, Dunn PO, Whittingham LA. 2002. Short-term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130: 185-190.
27. Martin LB, Scheuerlein A, Wikelski M. 2003. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proceedings of the Royal Society of London Series B, Biological Sciences B270: 153-158.
28. McCorkle FM, Olah I, Glick B. 1980. The morphology of phytohaemagglutinin-induced cell response in the chicken's wattle. Poultry Science 59: 616-623.
29. Merino S, Martínez J, Møller AP, Sanabria L, de Lope F, Pérez J, Rodríguez-Caabeiro F. 1999. Phytohaemagglutinin injection assay and physiological stress in nestling house martins. Animal Behaviour 58: 219-222.
30. Møller AP. 1990. Effects of a haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution 44: 771-784.
31. Møller AP, Erritzøe J, Saino N. 2003. Seasonal changes in immune response and parasite impact on hosts. American Naturalist 161: 657-671.
32. Moore SL, Wilson K. 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297: 2015-2017.
33. Mousseau TA, Roff DA. 1987. Natural selection and the heritability of fitness components. Heredity 59: 181-198.
34. Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H. 2005. Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proceedings of the Royal Society of London Series B, Biological Sciences 272: 1971-1977.
35. Price T, Schluter D. 1991. On the low heritability of life-history traits. Evolution 45: 853-861.
36. Råberg L, Grahn M, Hasselquist D, Svensson E. 1998. On the adaptive significance of stress-induced immunosuppression. Proceedings of the Royal Society of London Series B, Biological Sciences 265: 1637-1641.
37. Richner H, Oppliger A, Christe P. 1993. Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology 62: 703-710.
38. Roitt I, Brostoff J, Male D. 1996. Immunology. London: Mosby.
39. Roulin A. 1998. Cycle de reproduction et abondance du diptère parasite Canus hemapterus dans les nichées de chouettes effraies Tyto alba. Alauda 66: 265-272.
40. Roulin A. 2002. The barn owl. Update: Journal of the birds of Western Palearctic 4: 115-138.
41. Roulin A. 2004. The function of food stores in bird nests: observations and experiments in the barn owl Tyto alba. Ardea 92: 69-78.
42. Roulin A, Brinkhof MWG, Bize P, Richner H, Jungi TW, Bavoux C, Boileau N, Burneleau G. 2003. Which chick is tasty to parasites? The importance of host immunology versus parasite life history. Journal of Animal Ecology 72: 75-81.
43. Roulin A, Ducrest A-L, Dijkstra C. 1999. Effect of brood size manipulations on parents and offspring in the barn owl, Tyto alba. Ardea 87: 91-100.
44. Roulin A, Jungi TW, Pfister H, Dijkstra C. 2000. Female barn owls (Tyto alba) advertise good genes. Proceedings of the Royal Society of London Series B, Biological Sciences 267: 937-941.
45. Roulin A, Müller W, Sasvári L, Dijkstra C, Ducrest A-L, Riols C, Wink M, Lubjuhn T. 2004. Extra-pair paternity, testes size and testosterone level in relation to colour polymorphism in the barn owl Tyto alba. Journal of Avian Biology 35: 492-500.
46. Roulin A, Riols C, Dijkstra C, Ducrest A-L. 2001. Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behavioral Ecology 12: 103-110.
47. Saino N, Calza S, Møller AP. 1997. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. Journal of Animal Ecology 66: 827-836.
48. Sall J, Lehman A. 1996. JMP start statistics. A guide to statistical and data analysis using JMP and LMP in software. London: Duxbury Press, Wadsworth Publishing Co.
49. Schmid-Hempel P. 2003. Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B, Biological Sciences 270: 357-366.
50. Smits JE, Bortolotti GR, Tella JL. 1999. Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Functional Ecology 13: 567-572.
51. Soler JJ, de Neve L, Pérez-Contreras T, Soler M, Sorci G. 2002. Trade-off between immunocompetence and growth in magpies: an experimental study. Proceedings of the Royal Society of London Series B, Biological Sciences 270: 241-248.
52. Soler JJ, Moreno J, Potti J. 2003. Environmental, genetic and maternal components of immunocompetence of nestling pied flycatchers from a cross-fostering study. Evolutionary Ecology Research 5: 259-272.
53. Tella JL, Bortolotti GR, Dawson RD, Forero M. 2000. Environmental and genetic variation in T-cell-mediated immune response of fledgling American kestrels. Oecologia 123: 453-459.
54. Wehner R, Gehring W. 1990. Zoologie. Stuttgart: Georg Thieme.
55. Zuk M, McKean KA. 1996. Sex differences in parasite infections: patterns and processes. International Journal of Parasitology 26: 1009-1024.