Seasonal changes in immune response and parasite impact on hosts

American Naturalist

Volumn 161, Issue 4, 2003, Pages 657-671

  Møller, Anders Pape ^a   Erritzøe, Johannes ^a   Saino, Nicola ^a  

^a NONE

Author keywords

Birds; Parasite host interactions; Phytohemagglutinin; Spleen; T cell mediated immune response

Indexed keywords

ECTOPARASITE; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; SEASONAL VARIATION;

ANIMALIA; AVES;

EID: 0242432557     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/367879     Document Type: Article

References (82)

1. Abbas, A. K., A. H. Lichtman, and J. S. Pober. 1994. Cellular and molecular immunology. Saunders, Philadelphia.
2. Alberts, B., J. Lewis, M. Ratt, K. Roberts, and J. D. Watson, eds. 1983. Molecular biology of the cell. Garland, New York.
3. Allander, K., and J. Sundberg. 1997. Temporal variation and reliability of blood parasite levels in captive yellow-hammer males Emberiza citrinella. Journal of Avian Biology 28:325-330.
4. Alonso-Alvarez, C., and J. L. Tella. 2001. Effects of experimental food restriction and body-mass changes on avian T-cell mediated immune response. Canadian Journal of Zoology 79:101-105.
5. Anderson, R. M., and R. M. May. 1982. Coevolution of hosts and parasites. Parasitology 8:411-426.
6. Apanius, V. 1998. Stress and immune response. Pages 133-154 in A. P. Møller, M. Milinski, and P. J. B. Slater, eds. Stress and behavior. Academic Press, New York.
7. Applegate, J. E., and R. L. Beaudoin. 1970. Mechanism of spring relapse in avian malaria: effect of gonadotropin and corticosterone. Journal of Wildlife Diseases 6:443-447.
8. Arvy, L. 1965. Splénologie. Gauthiers-Villars, Paris.
9. Birkhead, T. R., F. Fletcher, and E. J. Pellatt. 1998. Sexual selection in the zebra finch Taeniopygia guttata: condition, sex traits and immune capacity. Behavioral Ecology and Sociobiology 44:179-191.
10. Brinkhof, M. W. G., P. Heeb, M. Kølliker, and H. Richner. 1999. Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proceedings of the Royal Society of London B, Biological Sciences 266:2315-2322.
11. Bull, J. J. 1994. Virulence. Evolution 48:1423-1437.
12. Casto, J. M., V. Nolan, Jr., and E. D. Ketterson. 2001. Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). American Naturalist 157:408-420.
13. Chandra, R. K., and P. M. Newberne. 1977. Nutrition, immunity, and infection. Plenum, New York.
14. Chernin, E. 1952. The relapse phenomenon in Leucocytozoon infections of the domestic duck. American Journal of Hygiene 56:101-118.
15. Christe, P., A. P. Møller, and F. de Lope. 1998. Immunocompetence and nestling survival in the house martin: "the tasty chick hypothesis." Oikos 83:175-179.
16. Christe, P., R. Arlettaz, and P. Vogel. 2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3:207-212.
17. Christe, P., F. de Lope, G. Gonzalez, N. Saino, and A. P. Møller. 2001. The influence of weather conditions and ectoparasites on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia (Berlin) 126:333-338.
18. Deerenberg, C., V. Apanius, S. Daan, and N. Bos. 1997. Reproductive effort decreases antibody responsiveness. Proceedings of the Royal Society of London B, Biological Sciences 264:1021-1029.
19. de Lope, F., and A. P. Møller. 1993. Effects of ectoparasites on reproduction of their swallows hosts: a cost of being multi-brooded. Oikos 67:557-562.
20. de Lope, F., G. González, J. J. Pérez, andA. P. Møller. 1993. Increased detrimental effects of ectoparasites on their bird hosts during adverse environmental conditions. Oecologia (Berlin) 95:234-240.
21. Dietert, R. R., K. A. Golemboski, H. Kwak, R. Ha, and T. E. Miller. 1996. Environment-immunity interactions. Pages 343-356 in T. F. Davison, T. R. Morris, and L. N. Payne, eds. Poultry immunology. Carfax, Abingdon.
22. Ewald, P. W. 1983. Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14:465-485.
23. Folstad, I., and A. J. Karter. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist 139:603-622.
24. Foster, M. S. 1969. Synchronized life cycles in the orange-crowned warbler and its mallophagan parasites. Ecology 50:315-323.
25. Frank, S. A. 1996. Models of parasite virulence. Quarterly Review of Biology 71:37-78.
26. Gershwin, M. E., R. S. Beach, and L. S. Hurley. 1985. Nutrition and immunity. Academic Press, Orlando, Fla.
27. González, G., G. Sorci, and F. de Lope. 1999. Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus). Behavioral Ecology and Sociobiology 46:117-122.
28. Goto, N., H. Kodama, K. Okada, and Y. Fujimoto. 1978. Suppression of phytohaemagglutinin skin response in thymectomized chickens. Poultry Science 57:246-250.
29. Hochberg, M. E., and M. van Baalen. 1999. Antagonistic coevolution along environmental gradients. American Naturalist 152:629-634.
30. Hörak, P., L. Tegelmann, I. Ots, and A. P. Møller. 1999. Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia (Berlin) 121:316-322.
31. Hughes, C. S., R. M. Gaskall, R. C. Jones, J. M. Bradbury, and F. T. W. Jordon. 1989. Effects of certain stress factors on the re-excretion of infectious laryngotracheitis virus from latently infected carrier birds. Research in Veterinary Science 46:274-276.
32. Isogai, H., E. Isogai, T. Masuzawa, Y. Yanagihara, M. Matsubara, M. Shimanuki, T. Seta, K. Fukai, N. Kurosawa, and M. Enokidani. 1992. Seroepidemiological survey for antibody to Borrelia burgdorferi in cows. Microbiology and Immunology 36:1029-1039.
33. John, J. 1994. The avian spleen: a neglected organ. Quarterly Review of Biology 69:327-351.
34. Keymer, I. F. 1982. Parasitic diseases. Pages 535-598 in M. L. Petrak, ed. Diseases in cage and aviary birds. Lea & Febiger, Philadelphia.
35. Krause, R. 1922. Die Milz. Pages 313-314 in Mikroskopische Anatomie der Wirbeltiere, Vögel und Reptilien. Vol. 2. de Gruyter, Berlin.
36. Lack, D. 1954. The natural regulation of animal numbers. Clarendon, Oxford.
37. Lochmiller, R. L., and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
38. Lochmiller, R. L., M. R. Vestey, and J. C. Boren. 1993. Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503-510.
39. Lochmiller, R. L., M. R. Vestey, and S. T. McMurry. 1994. Temporal variation in humoral and cell-mediated immune response in a Sigmodon hispidus population. Ecology 75:236-245.
40. Marshall, A. G. 1981. The ecology of ectoparasitic insects. Academic Press, London.
41. Martin, T. E., A. P. Møller, S. Merino, and J. Clobert. 2001. Does clutch size evolve in response to parasites and immunocompetence? Proceedings of the National Academy of Sciences of the USA 98:2071-2076.
42. McCorkle, F., Jr., I. Olah, and B. Glick. 1980. The morphology of the phytohemagglutinin-induced cell response in the chicken's wattle. Poultry Science 59:616-623.
43. Merino, S., A. P. Møller, and F. de Lope. 2000. Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: a parasite-mediated effect? Oikos 90:327-332.
44. Møller, A. P. 1993. Parasites increase the cost of reproduction in their hosts. Journal of Animal Ecology 62:309-322.
45. Møller, A. P., and T. R. Birkhead. 1992. A pairwise comparative method as illustrated by copulation frequency in birds. American Naturalist 139:644-656.
46. Møller, A. P., and J. Erritzøe. 1996. Parasite virulence and host immune defense: host immune response is related to nest re-use in birds. Evolution 50:2066-2072.
47. _. 1998. Host immune defence and migration in birds. Evolutionary Ecology 12:945-953.
48. _. 2000. Predation against birds with low immunocompetence. Oecologia (Berlin) 122:500-504.
49. _. 2001. Dispersal, vaccination and regression of immune defence organs. Ecology Letters 4:484-490.
50. _. 2002. Coevolution of host immune defence and parasite-induced mortality: relative spleen size and mortality in altricial birds. Oikos 99:95-100.
51. Møller, A. P., P. Christe, J. Erritzøe, and J. Mavarez. 1998. Condition, disease and immune defence. Oikos 83:301-306.
52. Møller, A. P., P. Christe, and E. Lux. 1999. Parasitism, host immune function and sexual selection: a meta-analysis of parasite-mediated sexual selection. Quarterly Review of Biology 74:3-20.
53. Møller, A. P., C. Biard, J. D. Blount, D. C. Houston, P. Ninni, N. Saino, and P. F. Surai. 2000. Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Poultry and Avian Biology Reviews 11:137-159.
54. Møller, A. P., S. Merino, C. R. Brown, and R. J. Robertson. 2001. Immune defense and host sociality: a comparative study of swallows and martins. American Naturalist 158:136-145.
55. Molyneux, D. H., J. E. Cooper, and W. J. Smith. 1983. Studies on the pathology of an avian trypanosome (T. bouffardi) infection in experimentally infected canaries. Parasitology 87:49-54.
56. Morand, S., and R. Poulin. 2000. Nematode parasite species richness and the evolution of spleen size in birds. Canadian Journal of Zoology 78:1356-1360.
57. Moreno, J., J. J. Sanz, and E. Arriero. 1999. Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proceedings of the Royal Society of London B, Biological Sciences 266:1105-1109.
58. Navarro, C., A. Marzal, F. de Lope, and A. P. Møller. 2003. Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos (in press).
59. Nelson, R. J., and G. E. Demas. 1996. Seasonal changes in immune function. Quarterly Review of Biology 71:511-548.
60. Nordling, D., M. Andersson, S. Zohari, and L. Gustafsson. 1998. Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London B, Biological Sciences 265:1291-1298.
61. Oakesson, B. B. 1953. Cyclic changes in liver and spleen weights in migratory white-crowned sparrows. Condor 55:3-16.
62. _. 1956. Liver and spleen weight cycles in non-migratory white-crowned sparrows. Condor 58:45-50.
63. Parmentier, H. K., J. W. Scharma, F. Meijer, and M. G. B. Nieuwland. 1993. Cutaneous hypersensitivity responses in chickens divergently selected for antibody responses to sheep red blood cells. Poultry Science 72:1679-1692.
64. Parmentier, H. K., G. de Vries Reilingh, and M. G. B. Nieuwland. 1998. Kinetic immunohistochemical characteristic of mitogen-induced cutaneous hypersensitivity responses in chickens divergently selected for antibody responsiveness. Veterinary Immunology and Immunopathology 66:367-376.
65. Råberg, L., M. Grahn, D. Hasselquist, and E. Svensson. 1998. On the adaptive significance of stress-induced immunosuppression. Proceedings of the Royal Society of London B, Biological Sciences 265:1637-1641.
66. Riddle, O. 1928. Sex and seasonal differences in weight of liver and spleens. Proceedings of the Society for Experimental Biology and Medicine 25:474-476.
67. Rose, M. E. 1981. Lymphatic system. Pages 341-384 in A. S. King and J. McLelland, eds. Form and function in birds. Vol. 2. Academic Press, London.
68. Saino, N., S. Calza, and A. P. Møller. 1997. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. Journal of Animal Ecology 66:827-836.
69. Saino, N., M. Incagli, R. Martinelli, and A. P. Møller. 2002. Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behavioral Ecology 13:169-174.
70. Shutler, D., R. T. Alisauskas, and J. D. McLaughlin. 1999. Mass dynamics of the spleen and other organs in geese: measures of immune relationships to helminths? Canadian Journal of Zoology 77:351-359.
71. Sibley, C. G., and J. E. Ahlquist. 1990. Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven, Conn.
72. Silverin, B. 1981. Reproductive effort, as expressed in body and organ weights, in the pied flycatcher. Ornis Scandinavica 12:133-139.
73. Silverin, B., R. Fänge, P.-A. Viebke, and J. Westin. 1999. Seasonal changes in mass and histology of the spleen in willow tits Parus montanus. Journal of Avian Biology 30:255-262.
74. Soler, M., M. Martín-Vivaldi, J. M. Marín, and A. P. Møller. 1999. Weight lifting and health status in the black wheat-ear. Behavioral Ecology 10:281-286.
75. Svensson, L. 1995. Identification guide to European passerines. Svensson, Stockholm.
76. Tella, J. L. 2002. The evolutionary transition to coloniality promotes higher blood parasitism in birds. Journal of Evolutionary Biology 15:32-41.
77. Toivanen, P., and A. Toivanen, eds. 1987. Avian immunology. CRC, Boca Raton, Fla.
78. van Baalen, M. 1997. Coevolution of recovery ability and virulence. Proceedings of the Royal Society of London B, Biological Sciences 265:317-325.
79. Vindervogel, H., H. Debruyne, and P. P. Pastoret. 1985. Observation of pigeon herpesvirus 1 re-excretion during the reproduction period in conventionally reared homing pigeons. Journal of Comparative Pathology 95:105-112.
80. von Schantz, T., S. Bensch, M. Grahn, D. Hasselquist, and H. Wittzell. 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proceedings of the Royal Society of London B, Biological Sciences 266:1-12.
81. Wingfield, J. C., and G. J. Kenagy. 1991. Natural regulation of reproductive cycles. Pages 181-241 in M. Schreibman and R. E. Jones, eds. Vertebrate endocrinology. Academic Press, New York.
82. Zuk, M., and T. S. Johnsen. 1998. Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proceedings of the Royal Society of London B, Biological Sciences 265:1631-1635.