Antioxidant protection, immune function and growth of nestling great tits Parus major in relation to within-brood hierarchy

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 157, Issue 3, 2010, Pages 288-293

  Kilgas, Priit ^a   Tilgar, Vallo ^a   Külavee, Rauno ^a   Saks, Lauri ^a,b   Hõrak, Peeter ^a   Mänd, Raivo ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b UNIVERSITY OF TARTU   (Estonia)

Author keywords

Antioxidant protection; Early development; Growth; Hatching asynchrony; Phytohaemagglutinin; Sibling competition; Trade off; Uric acid

Indexed keywords

PHYTOHEMAGGLUTININ; URIC ACID; ANTIOXIDANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIRD; BODY GROWTH; BODY MASS; COMPETITION; CONTROLLED STUDY; HATCHING; NESTLING; NONHUMAN; PARUS MAJOR; PLASMA; PRIORITY JOURNAL; SIBLING; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; SONGBIRD;

AVES; PARUS MAJOR;

ANIMALS; ANTIOXIDANTS; PASSERIFORMES; URIC ACID;

EID: 77956188140     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.07.002     Document Type: Article

References (57)

1. Alonso-Alvarez C., Ferrer M. A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol. Biochem. Zool. 2001, 74:703-713.
2. Alonso-Alvarez C., Bertrand S., Faivre B., Sorci G. Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Funct. Ecol. 2007, 21:873-879.
3. Banda E., Blanco G. Influence of hatching asynchrony and within-brood parental investment on size, condition, and immunocompetence in nestling red-billed choughs. Biol. J. Linn. Soc. 2008, 94:675-684.
4. Birkhead T.R., Fletcher F., Pellatt E.J. Nestling diet, secondary sexual traits and fitness in the zebra finch. Proc. R. Soc. B: Biol. Sci. 1999, 266:385-390.
5. Brommer J.E. Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc. R. Soc. B: Biol. Sci. (Suppl.) 2004, 271:S110-S113.
6. Carro M.D., Falkenstein E., Radke W.J., Klandorf H. Effects of allopurinol on uric acid concentrations, xanthine oxidoreductase activity and oxidative stress in broiler chickens. Comp. Biochem. Physiol. C 2010, 151:12-17.
7. Cohen A.A., McGraw K.J. No simple measures for antioxidant status in birds: complexity in inter- and intraspecific correlations among circulating antioxidant types. Funct. Ecol. 2009, 23:310-320.
8. Cohen A., Klasing K., Ricklefs R. Measuring circulating antioxidants in wild birds. Comp. Biochem. Physiol. B 2007, 147:110-121.
9. Costantini D. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 2008, 11:1238-1251.
10. Costantini D., Dell'Omo G. Effects of T-cell-mediated immune response on avian oxidative stress. Comp. Biochem. Physiol. A 2006, 145:137-142.
11. Costantini D., Møller A.P. Does immune response cause oxidative stress in birds? A meta-analysis. Comp. Biochem. Physiol. A 2009, 153:339-344.
12. Costantini D., Verhulst S. Does high antioxidant capacity indicate low oxidative stress?. Funct. Ecol. 2009, 23:506-509.
13. Cramp S., Perrins C.M. The Birds of the Western Palearctic 1993, Vol. VII. Oxford University Press, Oxford.
14. Criscuolo F., Monaghan P., Nasir L., Metcalfe N.B. Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood. Proc. R. Soc. B: Biol. Sci. 2008, 275:1565-1570.
15. De Block M., Stoks R. Compensatory growth and oxidative stress in a damselfly. Proc. R. Soc. B: Biol. Sci. 2008, 275:781-785.
16. Fair J.M., Hansen E.S., Ricklefs R.E. Growth, developmental stability and immune response in juvenile Japanese quails (Coturnix coturnix japonica). Proc. R. Soc. B: Biol. Sci. 1999, 266:1735-1742.
17. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
18. Fisher M.O., Nager R.G., Monaghan P. Compensatory growth impairs adult cognitive performance. Plos Biol. 2006, 4:1462-1466.
19. Hall M.E., Blount J.D., Forbes S., Royle N.J. Does oxidative stress mediate the trade-off between growth and self-maintenance in structured families?. Funct. Ecol. 2010, 24:365-373.
20. Hõrak P., Zilmer M., Saks L., Ots I., Karu U., Zilmer K. Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J. Exp. Biol. 2006, 209:4329-4338.
21. Hõrak P., Saks L., Zilmer M., Karu U., Zilmer K. Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches. Am. Nat. 2007, 170:625-635.
22. Hoyt D.F. Practical methods of estimating volume and fresh weight of bird eggs. Auk 1979, 96:73-77.
23. Kunz C., Ekman J. Genetic and environmental components of growth in nestling blue tits (Parus caeruleus). J. Evol. Biol. 2000, 13:199-212.
24. Lessells C.M., Boag P.T. Unrepeatable repeatabilities: a common mistake. Auk 1987, 104:116-121.
25. Lin H., Decuypere E., Buyse J. Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus). 1. Chronic exposure. Comp. Biochem. Physiol. B 2004, 139:737-744.
26. Lin H., Decuypere E., Buyse J. Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus). 2. Short-term effect. Comp. Biochem. Physiol. B 2004, 139:745-751.
27. Lindström J. Early development and fitness in birds and mammals. Trends Ecol. Evol. 1999, 14:343-348.
28. Mänd R., Tilgar V., Kilgas P., Mägi M. Manipulation of laying effort reveals habitat-specific variation in egg production constraints in Great Tits (Parus major). J. Ornithol. 2007, 148:91-97.
29. Martin L.B., Han P., Lewittes J., Kuhlman J.R., Klasing K.C., Wikelski M. Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct. Ecol. 2006, 20:290-299.
30. Martín-Vivaldi M., Ruiz-Rodríguez M., Méndez M., Soler J.J. Relative importance of factors affecting nestling immune response differs between junior and senior nestlings within broods of hoopoes Upupa epops. J. Avian Biol. 2006, 37:467-476.
31. Metcalfe N.B., Monaghan P. Compensation for a bad start: grow now, pay later?. Trends Ecol. Evol. 2001, 16:254-260.
32. Monaghan P. Early growth conditions, phenotypic development and environmental change. Phil. Trans. R. Soc. B 2008, 363:1635-1645.
33. Monaghan P., Metcalfe N.B., Torres R. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 2009, 12:75-92.
34. Newbrey J.L., Reed W.L., Foster S.P., Zander G.L. Laying-sequence variation in yolk carotenoid concentrations in eggs of yellow-headed blackbirds (Xanthocephalus xanthocephalus). Auk 2008, 125:124-130.
35. Nilsson J.-Å., Gårdmark A. Sibling competition affects individual growth strategies in marsh tit, Parus palustris, nestlings. Anim. Behav. 2001, 61:357-365.
36. Nilsson J.-Å̊., Svensson M. Fledging in altritial birds: parental manipulation or sibling competition?. Anim. Behav. 1993, 46:379-386.
37. Nilsson J.-Å., Svensson M. Sibling competition affects nestling growth strategies in marsh tits. J. Anim. Ecol. 1996, 65:825-836.
38. Oddie K.R. Size matters: competition between male and female great tit offspring. J. Anim. Ecol. 2000, 69:903-912.
39. Potti J., Moreno J., Merino S., Frías O., Rodríguez R. Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 1999, 120:1-8.
40. Roulin A., Brinkhof M.W.G., Bize P., Richner H., Jungi T.W., Bavoux C., Boileau N., Burneleau G. Which chick is tasty to parasites? The importance of host immunology vs. parasite life history. J. Anim. Ecol. 2003, 72:75-81.
41. Rubolini D., Romano M., Bonisoli Alquati A., Saino N. Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks. J. Evol. Biol. 2006, 19:1571-1584.
42. Saino N., Calza S., Møller A.P. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J. Anim. Ecol. 1997, 66:827-836.
43. Saino N., Incagli M., Martinelli R., Ambrosini R., Møller A.P. Immunity, growth and begging behaviour of nestling Barn Swallows Hirundo rustica in relation to hatching order. J. Avian Biol. 2001, 32:263-270.
44. Saino N., Dall'Ara P., Martinelli R., Møller A.P. Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J. Evol. Biol. 2002, 15:735-743.
45. Smits J.E., Bortolotti G.R., Tella J.L. Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct. Ecol. 1999, 13:567-572.
46. Sockman K.W., Sharp P.J., Schwabl H. Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol. Rev. 2006, 81:629-666.
47. Soler J.J., de Neve L., Pérez-Contreras T., Soler M., Sorci G. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc. R. Soc. B: Biol. Sci. 2003, 270:241-248.
48. Tella J.L., Schleuerlein A., Ricklefs R.E. Is cell-mediated immunity related to the evolution of life-history strategies in birds?. Proc. R. Soc. B: Biol. Sci. 2002, 269:1059-1066.
49. Tella J.L., Lemus J.A., Carrete M., Blanco G. The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS ONE 2008, 3(e3295):1-9.
50. Tilgar V., Mänd R. Sibling growth patterns in great tits: does increased selection on last-hatched chicks favour and asynchronous hatching strategy?. Evol. Ecol. 2006, 20:217-234.
51. Tobler M., Sandell M.I. Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch. J. Exp. Biol. 2009, 212:89-94.
52. Tsahar E., Arad Z., Izhaki I., Guglielmo C.G. The relationship between uric acid and its oxidative product allantoin: a potential indicator for the evaluation of oxidative stress in birds. J. Comp. Physiol. B 2006, 176:653-661.
53. Tschirren B., Fitze P., Richner H. Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J. Anim. Ecol. 2003, 72:839-845.
54. Tummeleht L., Mägi M., Kilgas P., Mänd R., Hõrak P. Antioxidant protection and plasma carotenoids of incubating great tits (Parus major L.) in relation to health state and breeding conditions. Comp. Biochem. Physiol. C 2006, 144:166-172.
55. Visser M.E., Lessels C.M. The costs of egg production and incubation in great tits (Parus major). Proc. R. Soc. B: Biol. Sci. 2001, 268:1271-1277.
56. von Schantz T., Bensch S., Grahn M., Hasselquist D., Wittzell H. Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. B: Biol. Sci. 1999, 266:1-12.
57. Williams T.D. Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol. Rev. 1994, 68:35-59.