Effects of parental effort on blood stress protein HSP60 and immunoglobulins in female blue tits: A brood size manipulation experiment

Journal of Animal Ecology

Volumn 75, Issue 5, 2006, Pages 1147-1153

  Merino, Santiago ^a   Moreno, Juan ^a   Tomás, Gustavo ^a   Martínez, Javier ^b   Morales, Judith ^a   Martínez De La Puente, Josué ^a   Osorno, José Luis ^c  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b UNIVERSITY OF ALCALÁ   (Spain)

^c INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

Haemoproteus; Heat shock proteins; Parasites; Parental investment; Reproductive stress

Indexed keywords

CHAPERONIN; IMMUNOGLOBULIN;

BLOOD; BROOD SIZE; ENVIRONMENTAL STRESS; EXPERIMENTAL STUDY; MATERNAL EFFECT; NESTLING; PARENTAL CARE; PASSERINE; PHYSIOLOGICAL RESPONSE; POPULATION STRUCTURE; PROTEIN;

ANIMAL; ANIMAL DISEASE; ARTICLE; BLOOD; CLUTCH SIZE; COCCIDIA; COMPARATIVE STUDY; FEMALE; GENE EXPRESSION; IMMUNOLOGY; ISOLATION AND PURIFICATION; NESTING; PARASITOLOGY; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SONGBIRD; STRESS;

ANIMALS; CHAPERONIN 60; CLUTCH SIZE; FEMALE; GENE EXPRESSION; HAEMOSPORIDA; IMMUNOGLOBULINS; NESTING BEHAVIOR; PASSERIFORMES; STRESS;

ANIMALIA; CYANISTES CAERULEUS;

EID: 33746808093     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2006.01135.x     Document Type: Article

References (63)

1. Alatalo, R.V., Lundberg, A. & Stahlbrandt, K. (1982) Why do pied flycatcher females mate with already mated males? Animal Behaviour, 30, 585-593.
2. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B. & Sorci, G. (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecology Letters, 7, 363-368.
3. Apanius, V. & Nisbet, I.C.T. (2006) Serum immunoglobulin G levels are positively related to reproductive performance in a long-lived seabird, the common tern (Sterna hirundo). Oecologia, 147, 12-23.
4. Atkinson, C.T. & Van Riper,C. III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Bird-Parasite Interactions. Ecology, Evolution and Behaviour (eds J.E. Loye & M. Zuk), pp. 19-48. Oxford University Press, Oxford.
5. Christe, P., de Lope, F., González, G., Saino, N. & Møller, A.P. (2001) The influence of environmental conditions on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia, 126, 333-338.
6. Deerenberg, C., Pen, I., Dijkstra, C., Arkies, B.J., Visser, G.H. & Daan, S. (1995) Parental energy expenditure in relation to manipulated brood size in the European kestrel Falco tinnunculus. Zoology, 99, 39-48.
7. Deerenberg, C., de Kogel, C.H. & Overkamp, G.J.F. (1996) Cost of reproduction in the Zebra Finch Taenopygia guttata: manipulation of brood size in the laboratory. Journal of Avian Biology, 27, 321-326.
8. Deerenberg, C., Apanius, V., Daan, S. & Bos, N. (1997) Reproductive effort decreases antibody responsiveness. Proceedings of the Royal Society of London B, 264, 1021-1029.
9. Eguchi, K. (1993) Temporal changes in food resources, parental feeding and breeding success of Heron Island silvereyes, Zosterops lateralis chlorocephala. Ecological Research, 8, 319-327.
10. Forbes, L.S. (1993) Avian brood reduction and parent-offspring 'conflict'. American Naturalist, 142, 82-117.
11. Godfrey, R.D., Fedynich, A.M. & Pence, D.B. (1987) Quantification of hematozoa in blood smears. Journal of Wildlife Diseases, 23, 558-565.
12. Gustafsson, L. & Sutherland, W.J. (1988) The costs of reproduction in the collared flycatcher (Ficedula albicollis). Nature, 335, 813-815.
13. Haas, I.G. (1994) BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia, 11/12, 1012-1020.
14. Hanssen, S.A., Hasselquist, D., Folstad, I. & Erikstad, K.E. (2004) Cost of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society of London B, 271, 925-930.
15. Hartman, D. & Gething, M.J. (1996) Normal protein folding machinery. Stress-Inducible Cellular Responses (eds U. Feige, R.I. Morimoto & B.S. Yahara), pp. 3 -24. Birkhäuser-Verlag, Switzerland.
16. Hasselquist, D., Wasson, M.F. & Winkler, D.W. (2001) Humoral immunocompetence correlates with date of egg-laying and reflects work load in female tree swallows. Behavioral Ecology, 12, 93-97.
17. Hõrak, P. (1995) Brood reduction facilitates female but not offspring survival in the great tit. Oecologia, 102, 515-519.
18. Hõrak, P., Ots, I. & Murumägi, A. (1998) Haematological health state indices of reproducing great tits: a response to brood size manipulation. Functional Ecology, 12, 750-756.
19. Ilmonen, P., Hasselquist, D., Langerfors, A. & Wiehn, J. (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia, 136, 148-154.
20. Isobe, T. & Suzuki, K. (1987) Immunoglobulin M and G immune response to Leucocytozoon caulleryi in chickens. Japanese Journal of Veterinary Science, 49, 333-339.
21. Kaufmann, S.H.E. (1990) Heat shock proteins and the immune response. Immunology Today, 11, 129-135.
22. Lindén, M. & Møller, A.P. (1989) Costs of reproduction and covariation of life history traits in birds. Trends in Ecology and Evolution, 4, 367-370.
23. Martínez, J., Tomás, G., Merino, S., Arriero, E. & Moreno, J. (2003) Detection of serum immunoglobulins in wild birds by direct ELISA: a methodological study to validate the technique in different species using antichicken antibodies. Functional Ecology, 17, 700-706.
24. 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.
25. Merino, S., Potti, J. & Fargallo, J.A. (1997) Blood parasites of some passerine birds from central Spain. Journal of Wildlife Diseases, 33, 638-641.
26. Merino, S., Martínez, J., Barbosa, A., Møller, A.P., de Lope, F., Pérez, J. & Rodríguez-Caabeiro, F. (1998a) Increase in a heat shock protein from blood cells in response to parasitism of nestling house martins (Delichon urbica): An experimental approach. Oecologia, 116, 343-347.
27. Merino, S., Moreno, J., Potti, J., de León, A. & Rodríguez, R. (1998b) Nest ectoparasites and maternal effort in pied flycatchers. Biologia E Conservazione Della Fauna, 102, 200-205.
28. Merino, S., Moreno, J., Sanz, J.J. & Arriero, E. (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits. Proceedings of the Royal Society of London B, 267, 2507-2510.
29. 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.
30. Merino, S., Blázquez, M.C., Martínez, J. & Rodríguez-Estrella, R. (2004) Stress protein expression is related to tail loss in two species of iguanid lizards. Canadian Journal of Zoology, 82, 436-441.
31. Møller, A.P. (1997) Parasitism and the evolution of host life history. Host-Parasite Evolution (eds D.H. Clayton & J. Moore), pp. 105-127. Oxford University Press, Oxford.
32. Morales, J., Moreno, J., Merino, S., Tomás, G., Martínez, J. & Garamszegi, L.Z. (2004) Associations between immune parameters, parasitism and stress in breeding pied flycatcher females Ficedula hypoleuca. Canadian Journal Zoology, 82, 1484-1492.
33. Moreno, J. (1993) Physiological mechanisms underlaying reproductive trade-offs. Etología, 3, 41-56.
34. Moreno, J. (2002) La evolución de las estrategias vitales. Evolución, la Base de la Biología (ed. M. Soler), pp. 159-176. Proyecto Sur de Ediciones, Granada, Spain.
35. 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.
36. Moreno, J., Merino, S., Potti, J., de León, A. & Rodríguez, R. (1999a) Maternal effort does not change with flight cost or food availability in the pied flycatcher: cost and benefits for nestlings. Behavioral Ecology Sociobiology, 46, 244-251.
37. Moreno, J., Sanz, J.J. & Arriero, E. (1999b) Reproductive effort and T lymphocyte cell mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proceedings of the Royal Society of London B, 266, 1105-1109.
38. Morimoto, R.I. (1991) Heat shock: the role of transient inducible responses in cell damage, transformation, and differentiation. Cancer Cells, 3, 295-301.
39. 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 B, 265, 1291-1298.
40. Nur, N. (1984) The consequences of brood size for breeding blue tits I. Adult survival, weight change and the cost of reproduction. Journal of Animal Ecology, 53, 479-496.
41. Ots, I. & Hõrak, P. (1998) Health impact of blood parasites in breeding great tits. Oecologia, 116, 441-448.
42. Pedersen, B.K. & Hoffman-Goetz, L. (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiological Review, 80, 1055-1081.
43. Peterson, C.C., Nagy, K.A. & Diamond, J. (1990) Sustained metabolic scope. Proceedings of the National Academy of Sciences, USA, 87, 2324-2328.
44. Ploger, B.J. (1997) Does brood reduction provide nestlings survivors with a food bonus? Animal Behaviour, 54, 1063-1076.
45. Potti, J., Moreno, J. & Merino, S. (1999) Repeatability of parental effort in male and female pied flycatchers as measured with doubly-labelled water. Canadian Journal of Zoology, 77, 174-179.
46. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. (1998) On the adaptative significance of stress induced immunosuppression. Proceedings of the Royal Society of London B, 265, 1637-1641.
47. Roff, D.A. (1992) The Evolution of Life Histories. Chapman & Hall, New York.
48. 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.
49. 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.
50. Smith, H.G., Källander, H., Fontell, K. & Ljungström, M. (1988) Feeding frequency and parental division of labour in the double-brooded great tit Parus major. Behavioural Ecology Sociobiology, 22, 447-453.
51. Smith, H.G., Källander, H. & Nilsson, J.A. (1989) The trade-off between offspring number and quality in the great tit Parus major. Journal of Animal Ecology, 58, 383-402.
52. Sørensen, J.G., Kristensen, T.N. & Loeschcke, V. (2003) The evolutionary and ecological role of heat shock proteins. Ecology Letters, 6, 1025-1037.
53. Stearns, S. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.
54. Svensson, E., Råberg, L., Koch, C. & Hasselquist, D. (1998) Energetic stress, immunosuppression and the costs of an antibody response. Functional Ecology, 12, 912-919.
55. Tinbergen, J.M. & Boerlijst, M.C. (1990) Nestling weight and survival in individual great tits (Parus major). Journal of Animal Ecology, 59, 1113-1127.
56. Tomás, G., Martínez, J. & Merino, S. (2004) Collection and analysis of blood samples to detect stress proteins in wild birds. Journal of Field Ornithology, 75, 281-287.
57. 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.
58. Tuomi, J. (1990) On clutch size and parental survival. Oikos, 58, 387-389.
59. 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. 121-138. Birkhauser-Verlag, Basel, Switzerland.
60. Wakelin, D. & Apanius, V. (1997) Immune defence: genetic control. Host-Parasite Evolution (eds D.H. Clayton & J. Moore), pp. 30-58. Oxford University Press, Oxford.
61. Welch, W.J. (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiological Review, 72, 1063-1081.
62. Wiersma, P., Selman, C., Speakman, J.R. & Verhulst, S. (2004) Birds sacrifice oxidative protection for reproduction. Proceedings of the Royal Society of London B Supplement, 271, S360-S363.
63. Yang, X.D. & Feige, U. (1992) Heat shock proteins in autoimmune disease: from causative antigen to specific therapy? Experientia, 48, 650-656.