Higher stress protein levels are associated with lower humoral and cell-mediated immune responses in Pied Flycatcher females

Functional Ecology

Volumn 20, Issue 4, 2006, Pages 647-655

  Morales, J ^a,b   Moreno, J ^a   Lobato, E ^a   Merino, S ^a   Tomas G ^a   Martinez De La Puente J ^a   Martinez J ^c  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b UNIVERSITY OF ALCALÁ   (Spain)

^c NONE

Author keywords

Birds; Blood parasites; HSPs; Immunocompetence; Life history trade offs

Indexed keywords

IMMUNE RESPONSE; PASSERINE; PROTEIN; STRESS;

FICEDULA HYPOLEUCA; HAEMOPROTEUS;

EID: 33745837068     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2006.01139.x     Document Type: Article

References (79)

1. Apanius, V. (1998) Stress and immune defence. Advances in the Study of Behavior 27, 133-153.
2. Ardia, D.R. (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. Journal of Animal Ecology 74, 517-524.
3. Berczi, I. (1998) The stress concept and neuroimmunoregulation in modern biology. Annals of the New York Academy of Sciences 851, 1-12.
4. Bettencourt, B.R., Feder, M.E. & Cavicchi, S. (1999) Experimental evolution of HSP70 expression and thermotolerance in Drosophila melanogaster. Evolution 53, 484-492.
5. Cichoñ, M., Dubiec, A. & Chadzinska, M. (2001) The effect of elevated reproductive effort on humoral immune function in collared flycatcher females. Acta Oecologica - International Journal of Ecology 22, 71-76.
6. Dohms, J.E. & Metz, A. (1991) Stress-mechanisms of immunosuppression. Veterinary Immunology and Immunopathology 30, 89-109.
7. Eeva, T., Tanhuanpaa, S., Rabergh, C., Airaksinen, S., Nikinmaa, M. & Lehikoinen, E. (2000) Biomarkers and fluctuating asymmetry as indicators of pollution-induced stress in two hole-nesting passerines. Functional Ecology 14, 235-243.
8. El-Lethey, H., Huber-Eicher, B. & Jungi, T.W. (2003) Exploration of stress-induced immunosupression in chickens reveals both stress-resistant and stress-susceptible antigen responses. Veterinary Immunology and Immunopathology 95, 91-101.
9. Fargallo, J.A., Laaksonen, T., Poyri, V. & Korpimaki, E. (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecology Letters 5, 95-101.
10. Feder, M.E. & Hofmann, G.E. (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243-282.
11. Folstad, I. & Karter, A.J. (1992) Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603-622.
12. Garamszegi, L.Z., Merino, S., Török, J., Eens, M. & Martínez, J. (2006) Indicators of physiological stress and the elaboration of sexual traits in the collared flycatcher. Behavioural Ecology 17, 399-404.
13. Glaser, R., Kiecolt-Glaser, J.K., Malarkey, W.B. & Sheridan, J.F. (1998) The influence of psychological stress on the immune response to vaccines. Annals of the New York Academy of Sciences 840, 649-655.
14. Gonzalez, G., Sorci, G., Møller, A.P., Ninni, P., Haussy, C. & De Lope, F. (1999) Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). Journal of Animal Ecology 68, 1225-1234.
15. Hall, T.J. (1994) Role of hsp70 in citokine production. Experientia 11/12, 1048-1053.
16. Hamdoun, A.M., Cheney, D.P. & Cherr, G.N. (2003) Phenotypic plasticity of HSP70 and HSP70 gene expression in the Pacific oyster (Crassostrea gigas): implications for thermal limits and induction of thermal tolerance. Biology Bulletin 205, 160-169.
17. Ilmonen, P., Taarna, T. & Hasselquist, D. (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proceedings of the Royal Society of London Series B 267, 665-670.
18. Ilmonen, P., Hasselquist, D., Langefors, A. & Wiehn, J. (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136, 148-154.
19. Jenkins, R.R. (1993) Exercise, oxidative stress, and antioxidants: a review. International Journal of Sport Nutrition 3, 356-375.
20. Kaufmann, S.H.E. (1990) Heat-shock proteins and the immune response. Immunology Today 11, 129-135.
21. Kilpimaa, J., Alatalo, R.V. & Siitari, H. (2004) Trade-offs between sexual advertisement and immune function in the pied flycatcher (Ficedula hypoleuca). Proceedings of the Royal Society of London Series B 271, 245-250.
22. Klasing, K.C. & Leshchinsky, T.V. (1999) Functions, costs, and benefits of the immune system during development. Proceedings of the 22nd International Ornithological Congress (eds N.J. Adams & R.H. Slotow). BirdLife South Africa, Johannesburg, South Africa.
23. Lifjeld, J.T., Dunn, P.O. & Whittingham, L.A. (2002) Short-term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130, 185-190.
24. Lindquist, S. (1986) The heat-shock response. Annual Review of Biochemistry 55, 1151-1191.
25. Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98.
26. Lundberg, A. & Alatalo, R.V. (1992) The Pied Flycatcher. Poyser, London.
27. Martin, L.B., 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 270, 153-158.
28. Martínez, J., Pérez-Serrano, J., Bernadina, W.E. & Rodríguez-Caabeiro, F. (1999a) Influence of parasitization by Trichinella spiralis on the levels of heat shock proteins in rat liver and muscle. Parasitology 118, 201-209.
29. Martínez, J., Pérez-Serrano, J., Bernadina, W.E. & Rodríguez-Caabeiro, F. (1999b) Shock response induced in rat brain and spleen during primary infection with Trichinella spiralis larvae. Parasitology 118, 201-209.
30. Martínez, J., Pérez-Serrano, J., Bernardina, W.E. & Rodríguez-Caabeiro, F. (1999c) In vitro stress response to elevated temperature, hydrogen peroxide and mebendazole in Trichinella spiralis muscle larvae. International Journal of Parasitology 29, 1457-1464.
31. Martínez, J., Merino, S. & Rodríguez-Caabeiro, F. (2004) Physiological responses to Trichinella spiralis infection in Wistar rats: is immune response costly? Helminthologia 41, 67-71.
32. Martínez-Padilla, J., Martínez, J., Dávila, J.A., Merino, S., Moreno, J. & Millán, J. (2004) Within-brood size differences, sex and parasites determine blood stress protein levels in Eurasian Kestrel nestlings. Functional Ecology 18, 426-434.
33. Merino, S. & Potti, J. (1995) High prevalence of hematozoa in nestlings of a passerine species, the pied flycatcher (Ficedula hypoleuca). Auk 112, 1041-1043.
34. Merino, S., Potti, J. & Fargallo, J.A. (1997) Blood parasites of passerine birds from central Spain. Journal of Wildlife Diseases 33, 638-641.
35. Merino, S., Martínez, J., Barbosa, A., Møller, A.P., De Lope, F., Pérez, J. & Rodríguez-Caabeiro, F. (1998) Increase in a heat-shock protein from blood cells in response of nestling house martins (Delichon urbica) to parasitism: an experimental approach. Oecologia 116, 343-347.
36. Merino, S., Moreno, J. Sanz, J.J. & Arriero, E. (2000a) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London Series B 267, 2507-2510.
37. Merino, S., Møller, A.P. & de Lope, F. (2000b) Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: a parasite-mediated effect? Oikos 90, 327-332.
38. Merino, S., Martinez, J., Møller, A.P., Barbosa, A., de Lope, F. & Rodríguez-Caabeiro, F. (2001) Physiological and haematological consequences of a novel parasite on the red-rumped swallow Hirundo daurica. International Journal of Parasitology 31, 1187-1193.
39. Merino, S., Martínez, J., Møller, A.P., Barbosa, A., de Lope, F. & Rodríguez-Caabeiro, F. (2002) Blood stress protein levels in relation to sex and parasitism of barn swallows (Hirundo rustica). Ecoscience 9, 300-305.
40. Møller, A.P. (1997) Parasites and the evolution of host life history. Host-Parasite Evolution: General Principles and Avian Models (eds D. Clayton & J. Moore), pp. 105-127. Oxford University Press, Oxford.
41. Møller, A.P. & Saino, N. (1998) The avian immune system: a jack-of-all-trades. Proceedings of the 22nd International Ornithological Congress (eds N.J. Adams & R.H. Slotow). BirdLife South Africa, Johannesburg, South Africa.
42. Morales, J., Moreno, J., Merino, S., Tomás, G., Martínez, J. & Garamszegi, L.Z. (2004) Associations between immune parameters, parasitism, and stress in breeding pled flycatcher (Ficedula hypoleuca) females. Canadian Journal of Zoology 82, 1484-1492.
43. Moreno, J., Cowie, R.J., Sanz, J.J. & Williams, R.S.R. (1995) Differential response by males and females to brood manipulations in the pied flycatcher, energy expenditure and nestling diet. Journal of Animal Ecology 64, 721-732.
44. Moreno, J., Sanz, J.J. & Arriero, E. (1999) Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proceedings of the Royal Society of London Series B 266, 1105-1109.
45. Moreno, J., Sanz, J.J., Merino, S. & Arriero, E. (2001) Daily energy expenditure and cell-mediated immunity in pied flycatchers while feeding nestlings: interaction with moult. Oecologia 129, 492-497.
46. Moreno, J., Merino, S., Martínez, J., Sanz, J.J. & Arriero, E. (2002) Heterophil/lymphocyte ratios and heat-shock protein levels are related to growth in nestling birds. Ecoscience 9, 434-439.
47. Moreno, J., Morales, J., Lobato, E., Merino, S., Tomás, G. & Martínez-de la Puente, J. (2005) Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca. Behavioral Ecology 16, 931-937.
48. Navarro, C., Marzal, A., de Lope, F. & Møller, A.P. (2003) Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101, 291-298.
49. Nordling, D., Andersson, M., Zohari, S. & Gustafsson, L. (1998) Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London Series B 265, 1291-1298.
50. Norris, K. & Evans, M.R. (2000) Ecological immunology: life history trade-offs and immune defence in birds. Behavioural Ecology 11, 19-26.
51. Pap, P.L. & Márkus, R. (2003) Cost of reproduction, T-lymphocyte mediated immunocompetence and health status in female and nestling barn swallows Hirundo rustica. Journal of Avian Biology 34, 428-434.
52. Parsell, D.A. & Lindquist, S. (1994) Heat shock proteins and stress tolerance. The Biology of Heat Shock Proteins and Molecular Chaperones (eds R.I. Morimoto, A. Tissieres & C. Georgopoulos), pp. 457-494. Cold Spring Harbor Laboratory Press, Plainview, NY.
53. Parsons, P.A. (1996) Stress, resources, energy balances and evolutionary change. Evolutionary Biology 29, 39-71.
54. Pedersen, B.K. & Hoffman-Goetz, L. (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiological Reviews 80, 1055-1081.
55. Pedersen, B.K. & Steensberg, A. (2002) Exercise and hypoxia: effects on leukocytes and interleukin-6 - shared mechanisms? Medicine and Science in Sports and Exercise 34, 2004-2012.
56. Pockley, A.G. (2003) Heat shock proteins as regulators of the immune response. Lancet 362, 469-476.
57. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. (1998) On the adaptive significance of stress-induced immunosupression. Proceedings of the Royal Society of London Series B 265, 1637-1641.
58. Råberg, L., Nilsson, J.-A., Ilmonen, P., Stjernman, M. & Hasselquist, D. (2000) The cost of an immune response: vaccination reduces parental effort. Ecology Letters 3, 382-386.
59. Roitt, I., Brostoff, J. & Male, D. (2001) Immunology. Mosby-Harcourt Publishers Ltd, London.
60. Saino, N., Incagli, M., Martinelli, R. & Møller, A.P. (2002) Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behavioral Ecology 13, 169-174.
61. Sanz, J.J., Moreno, J., Arriero, E. & Merino, S. (2002) Reproductive effort and blood parasites of breeding pied flycatchers: the need to control for interannual variation and initial health state. Oikos 96, 299-306.
62. Sanz, J.J., Potti, J., Moreno, J., Merino, S. & Frías, O. (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Global Change Biology 9, 461-472.
63. Sapolsky, R.M. (1992) Neuroendocrinology of the stress response. Behavioural Endocrinology (eds J.B. Becker, S.M. Breedlove & D. Crews), pp. 287-324. MIT Press, Cambridge, MA.
64. Schmid-Hempel, P. (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B 270, 357-366.
65. Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317-321.
66. Sheridan, J.F., Dobbs, C., Jung, J., Chu, X., Konstantinos, A., Padgett, D. & Glaser, D. (1998) Stress-induced neuroendocrine modulation of viral pathogenesis and immunity. Annals of the New York Academy of Sciences 840, 803-808.
67. Sørensen, J.G., Dahlgaard, J. & Loeschcke, V. (2001) Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of HSP70 expression and variation in heat stress resistance traits. Functional Ecology 15, 289-296.
68. Sørensen, J.G., Kristensen, T.N. & Loeschcke, V. (2003) The evolutionary and ecological role of heat shock proteins. Ecology Letters 6, 1025-1037.
69. Sørensen, J.G., Nielsen, M.M., Kruhøffer, M., Justensen, J. & Loeschcke, V. (2005) Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress and Chaperones 10, 312-328.
70. Svensson, L. (1984) Identification Guide to European Passerines. Ugga, Stockholm.
71. Svensson, E., Råberg, L., Koch, C. & Hasselquist, D. (1998) Energetic stress, immunosuppression and the costs of an antibody response. Functional Ecology 12, 912-919.
72. Tomás, G., Merino, S., Martínez, J., Moreno, J. & Sanz, J.J. (2005) Stress protein levels and blood parasite infection in blue tits (Parus caeruleus): a medication field experiment. Annales Zoologici Fennici 42, 45-56.
73. Valkiûnas, G. (2005) Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL.
74. Voellmy, R. (1996) Sensing stress and responding to stress. Stress-inducible Cellular Responses (eds U. Feige, R.I. Morimoto, I. Yahara & B.S. Polla), pp. 121-137. Birkhäuser Verlag, Basel, Switzerland.
75. Von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. & Wittzell, H. (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proceedings of the Royal Society of London Series B 266, 1-12.
76. Wakelin, D. (1994) Immunoparasitology. Introduction to Animal Parasitology (ed. J.D. Smyth). Cambridge University Press, Cambridge.
77. Wakelin, D. (1997) Parasites and the immune system, conflict or compromise? Bioscience 47, 32-40.
78. Westneat, D.F., Hasselquist, D. & Wingfield, J.C. (2003) Tests of association between the humoral immune response of red-winged blackbirds (Agelaius phoeniccus) and male plumage, testosterone, or reproductive success. Behavioural Ecology and Sociobiology 53, 315-323.
79. Zuk, M. & Stoehr, A.M. (2002) Immune defense and host life history. American Naturalist 160, S9-S22.