Cellular immune response, stress resistance and competitiveness in nestling great tits in relation to maternally transmitted carotenoids

Functional Ecology

Volumn 21, Issue 2, 2007, Pages 335-343

  Berthouly, Anne ^a   Helfenstein, Fabrice ^a   Richner, Heinz ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Ectoparasite resistance; Maternal effects; Nestling competition; Stress; Yolk carotenoids

Indexed keywords

CAROTENOID; ECTOPARASITE; EGG PRODUCTION; FLEA; IMMUNE RESPONSE; IMMUNOCOMPETENCE; MATERNAL EFFECT; NESTING; NESTLING; PARASITE RESISTANCE; PASSERINE; RESOURCE ALLOCATION; STRESS RESISTANCE; TRADE-OFF;

AVES; CERATOPHYLLUS GALLINAE; PARUS MAJOR; SIPHONAPTERA (FLEAS);

EID: 33947245550     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2006.01236.x     Document Type: Article

References (55)

1. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Gaillard, M., Prost, J., Faivre, B. & Sorci, G. (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. American Naturalist 164, 651-659.
2. Andersson, S., Uller, T., Lohmus, M. & Sundstrom, F. (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. Journal of Evolutionary Biology 17, 501-505.
3. Anisman, H., Zaharia, M.D., Meaney, M.J. & Merali, Z. (1998) Do early-life events permanently alter behavioral and hormonal responses to stressors? International Journal of Developmental Neuroscience 16, 149-164.
4. Biard, C., Surai, P.F. & Møller, A.P. (2005) Effects of carotenoid availability during laying on reproduction in the blue tit. Oecologia 144, 32-44.
5. Blount, J.D., Surai, P.F., Houston, D.C. & Møller, A.P. (2002a) Patterns of yolk enrichment with dietary carotenoids in gulls: the roles of pigment acquisition and utilization. Functional Ecology 16, 445-453.
6. Blount, J.D. Surai, P.F. Nager, R.G. Houston, D.C. Møller, A.P. Trewby, M.L. & Kennedy, M.W. (2002b) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proceedings of the Royal Society of London, B 269, 29-36.
7. Blount, J.D., Metcalfe, N.B., Birkhead, T.R. & Surai, P.F. (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300, 125-127.
8. Bortolotti, G.R., Negro, J.J., Surai, P.F. & Prieto, P. (2003) Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiological and Biochemical Zoology 76, 367-374.
9. Brinkhof, M.W.G. 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, B 266, 2315-2322.
10. Buechler, K., Fitze, P.S., Gottstein, B., Jacot, A. & Richner, H. (2002) Parasite-induced maternal response in a natural bird population. Journal of Animal Ecology 71, 247-252.
11. Desai, M., Crowther, N.J., Ozanne, S.E., Lucas, A. & Hales, C.N. (1995) Adult glucose and lipid-metabolism may be programmed during fetal life. Biochemical Society Transactions 23, 331-335.
12. El-Lethey, H., Huber-Eicher, B. & Jungi, T.W. (2003) Exploration of stress-induced immunosuppression in chickens reveals both stress-resistant and stress-susceptible antigen responses. Veterinary Immunology and Immunopathology 95, 91-101.
13. Gasparini, J., McCoy, K.D., Tveraa, T. & Boulinier, T. (2002) Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecology Letters 5, 519-524.
14. Gonzalez, G., Sorci, G., Møller, A.P., Ninni, P., Haussy, C. & De Lope, F. (1999) Immunocompetence and conditiondependent sexual advertisement in male house sparrows (Passer domesticus). Journal of Animal Ecology 68, 1225-1234.
15. Griffiths, R., Double, M.C., Orr, K. & Dawson, R.J.G. (1998) A DNA test to sex most birds. Molecular Ecology 7, 1071-1075.
16. Grindstaff, J.L. Brodie, E.D. & Ketterson, E.D. (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proceedings of the Royal Society of London, B 270, 2309-2319.
17. Heeb, P., Werner, I., Richner, H. & Kölliker, M. (1996) Horizontal transmission and reproductive rates of hen fleas in great tit nests. Journal of Animal Ecology 65, 474-484.
18. Heeb, P., Werner, I., Kolliker, M. & Richner, H. (1998) Benefits of induced host responses against an ectoparasite. Proceedings of The Royal Society of London B 265, 51-56.
19. Karadas, F., Pappas, A.C., Surai, P.F. & Speake, B.K. (2005) Embryonic development within carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken. Comparative Biochemistry and Physiology B 141, 244-251.
20. Kitaysky, A.S., Kitaiskaia, E.V., Wingfield, J.C. & Piatt, J.F. (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. Journal of Comparative Physiology B 171, 701-709.
21. Koutsos, E.A., Clifford, A.J., Calvert, C.C. & Klasing, K.C. (2003) Maternal carotenoid status modifies the incorporation of dietary carotenoids into immune tissues of growing chickens (Gallus gallus domesticus). Journal of Nutrition 133, 1132-1138.
22. Koutsos, E.A., Lopez, J.C.G. & Klasing, K.C. (2006) Carotenoids from in ovo or dietary sources blunt systemic indices of the inflammatory response in growing chicks (Gallus gallus domesticus). Journal of Nutrition 136, 1027-1031.
23. Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98.
24. de Lope, F., Møller, A.P. & de la Cruz, C. (1998) Parasitism, immune response and reproductive success in the house martin Delichon urbica. Oecologia 114, 188-193.
25. Love, O.P., Chin, E.H., Wynne-Edwards, K.E. & Williams, T.D. (2005) Stress hormones: a link between maternal condition and sex-biased reproductive investment. American Naturalist, 166, 751-766.
26. Maindonald, J. & Braun, J. (2003) Data Analysis and Graphics Using R - An Example-based Approach. Cambridge University Press.
27. McGraw, K.J. & Ardia, D.R. (2004) Immunoregulatory activity of different dietary carotenoids in male zebra finches. Chemoecology 14, 25-29.
28. McGraw, K.J., Adkins-Regan, E. & Parker, R.S. (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92, 375-380.
29. Møller, A.P., Biard, C., Blount, J.D., Houston, D.C., Ninni, P., Saino, N. & Surai, P.F. (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian and Poultry Biology Reviews 11, 137-159.
30. Naef-Daenzer, B., Widmer, F. & Nuber, M. (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. Journal of Animal Ecology 70, 730-738.
31. Nilsson, J.A. (2003) Ectoparasitism in marsh tits: costs and functional explanations. Behavioral Ecology 14, 175-181.
32. Olson, V.A. & Owens, I.P.F. (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends in Ecology and Evolution 13, 510-514.
33. Partali, V., Liaaenjensen, S., Slagsvold, T. & Lifjeld, J.T. (1987) Carotenoids in food-chain studies. 2. The food-chain of Parus spp. monitored by carotenoid analysis. Comparative Biochemistry and Physiology B 87, 885-888.
34. Pilz, K.M., Smith, H.G., Sandell, M.I. & Schwabl, H. (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Animal Behaviour 65, 841-850.
35. R Development Core Team (2006) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
36. Richner, H., Oppliger, A. & Christe, P. (1993) Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology 62, 703-710.
37. Romero, L.M. (2004) Physiological stress in ecology: lessons from biomedical research. Trends in Ecology and Evolution 19, 249-255.
38. Royle, N.J., Surai, P.F., McCartney, R.J. & Speake, B.K. (1999) Parental investment and egg yolk lipid composition in gulls. Functional Ecology 13, 298-306.
39. Rutkowska, J., Cichon, M., Puerta, M. & Gil, D. (2005) Negative effects of elevated testosterone on female fecundity in zebra finches. Hormones and Behavior 47, 585-591.
40. Saino, N., Ambrosini, R., Martinelli, R. & Møller, A.P. (2002a) Mate fidelity, senescence in breeding performance and reproductive trade-offs in the barn swallow. Journal of Animal Ecology 71, 309-319.
41. Saino, N. Bertacche, V. Ferrari, R.P. Martinelli, R. Møller, A.P. & Stradi, R. (2002b) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proceedings of the Royal Society of London, Series B 269, 1729-1733.
42. Saino, N. Ferrari, R. Romano, M. Martinelli, R. & Møller, A.P. (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proceedings of the Royal Society of London, B 270, 2485-2489.
43. Saino, N., Romano, M., Ambrosini, R., Ferrari, R.P. & Møller, A.P. (2004) Timing of reproduction and egg quality covary with temperature in the insectivorous Barn Swallow, Hirundo rustica. Functional Ecology 18, 50-57.
44. SAS® (2003) SAS User's Guide. SAS Institute Inc., Cary, NC, USA.
45. Schwabl, H. (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comparative Biochemistry and Physiology A 114, 271-276.
46. Simon, A., Thomas, D., Blondel, J., Perret, P. & Lambrechts, M.M. (2004) Physiological ecology of Mediterranean blue tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings. Physiological and Biochemical Zoology 77, 492-501.
47. Smits, J.E., Bortolotti, G.R. & Tella, J.L. (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Functional Ecology 13, 567-572.
48. Surai, P.F. & Speake, B.K. (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. Journal of Nutritional Biochemistry 9, 645-651.
49. Tripet, F. & Richner, H. (1999) Dynamics of hen flea Ceratophyllus gallinae subpopulations in blue tit nests. Journal of Insect Behavior 12, 159-174.
50. Tschirren, B., Fitze, P.S. & Richner, H. (2003a) Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.). Journal of Evolutionary Biology 16, 91-100.
51. Tschirren, B., Fitze, P.S. & Richner, H. (2003b) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology 72, 839-845.
52. Tschirren, B. Richner, H. & Schwabl, H. (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proceedings of the Royal Society of London, B 271, 1371-1375.
53. Verboven, N., Evans, N.P., D'Alba, L., Nager, R.G., Blount, J.D., Surai, P.F. & Monaghan, P. (2005) Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behavioral Ecology and Sociobiology 57, 357-365.
54. Wayland, M., Gilchrist, H.G., Marchant, T., Keating, J. & Smits, J.E. (2002) Immune function, stress response, and body condition in arctic-breeding common eiders in relation to cadmium, mercury, and selenium concentrations. Environmental Research 90, 47-60.
55. Westneat, D.F., Weiskittle, J., Edenfield, R., Kinnard, T.B. & Poston, J.P. (2004) Correlates of cell-mediated immunity in nestling house sparrows. Oecologia 141, 17-23.