Abstract
The fitness of an organism can be affected by conditions experienced during early development. In light of the impact that oxidative stress can have on the health and ageing of a bird species, this study evaluated factors accounting for the variation in oxidative stress levels in nestlings of the Eurasian kestrel (Falco tinnunculus) by measuring the serum concentration of reactive oxygen metabolites and the serum antioxidant barrier against hypochlorite-induced oxidation. The ratio between these two variables was considered as an index of oxidative stress, with higher values meaning higher oxidative damage. Six-chick broods showed the highest level of oxidative stress, while no effect of sex was found. Age showed an inverse relationship with the oxidants and the levels of oxidative stress, with younger birds having higher levels. Hatching date, body condition, body mass and carotenoid concentration did not show any relationship with oxidants, antioxidants or degree of oxidative stress. These findings suggest that intrabrood sibling competition could play a role in determining oxidative stress, and that in carnivorous birds other antioxidant molecules could be more important than carotenoids to reduce oxidative stress.




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References
Allen PC (1997) Production of free radical species during Eimeria maxima infections in chickens. Poult Sci 76:814–821
Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004a) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659
Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004b) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7:363–368
Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90:7915–7922
Armitage P, Berry G (1996) Statistical methods in medical research (Italian edition). McGraw-Hill, Milano and New York
Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581
Blount JD, Surai PF, Houston DC, Møller AP (2002a) Patterns of yolk enrichment with dietary carotenoids in gulls: the roles of pigment acquisition and utilization. Funct Ecol 16:445–453
Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002b) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36
Blount JD, Metcalfe NB, Arnold KE, Surai PF, Devevey GL, Monaghan P (2003) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finches. Proc R Soc Lond B 270:1691–1696
Bortolotti GR, Tella JL, Forero MG, Dawson RD, Negro JJ (2000) Genetics, local environment and health as factors influencing plasma carotenoids in wild American kestrels (Falco sparverius). Proc R Soc Lond B 267:1433–1438
Brambilla G, Fiori M, Archetti LI (2001) Evaluation of the oxidative stress in growing pigs by microplate assay. J Veter Med A 48:33–38
Brambilla G, Civitareale C, Ballerini A, Fiori M, Amadori M, Archetti LI, Regini M, Betti M (2002) Response to oxidative stress as a welfare parameter in swine. Redox Report 7:159–163
Casagrande S, Csermely D, Pini E, Bertacche V, Tagliavini J (2006) Skin carotenoid concentration correlates with male hunting skill and territory quality in the kestrel (Falco tinnunculus). J Avian Biol (in press)
Chiarotti F (2004) Detecting assumption violations in mixed-model analysis of variance. Ann Ist Super Sanità 40:165–171
Chin EH, Love OP, Clark AM, Williams TD (2005) Brood size and environmental conditions sex-specifically affect nestling immune response in the European starling Sturnus vulgaris. J Avian Biol 36:549–554
Costantini D, Casagrande S, Di Lieto G, Fanfani A, Dell’Omo G (2005a) Consistent differences in feeding habits between neighbouring breeding kestrels. Behaviour 142:1409–1421
Costantini D, Dell’Omo G, Casagrande S, Fabiani A, Carosi M, Bertacche V, Marquez C, Snell H, Snell H, Tapia W, Gentile G (2005b) Inter-population variation of carotenoids in Galápagos land iguanas (Conolophus subcristatus). Comp Biochem Physiol B 142:239–244
Dawson RD, Bortolotti GR (1997) Variation in hematocrit and total plasma proteins of nestling American kestrels (Falco sparverius) in the wild. Comp Biochem Physiol A 117:383–390
Dijkstra C, Bult A, Bijlsma S, Daan S, Meijer T, Zijlstra M (1990) Brood size manipulations in the kestrel Falco tinnunculus: effects on offspring and parent survival. J Anim Ecol 59:269–286
Dotan Y, Lichtenberg D, Pinchuck I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Progr Lip Res 43:200–227
Fargallo JA, Laaksonen T, Pöyri V, Korpimäki E (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecol Lett 5:95–101
Fargallo JA, Laaksonen T, Korpimäki E, Pöyri V, Griffith SC, Valkama J (2003) Size-mediated dominance and begging behaviour in Eurasian kestrel broods. Evol Ecol Res 5:549–558
Fernie KJ, Bird DM (2001) Evidence of oxidative stress in American kestrels exposed to electromagnetic fields. Environ Res 86:198–207
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247
Fridolfsson A-K, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121
Garcia-Berthou E (2001) On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. J Anim Ecol 70:708–711
Goodwin TW (1984) The biochemistry of carotenoids. Animals, volume II. Chapman and Hall, London
Gredilla R, Sanz A, Lopez-Torres M, Barja G (2001) Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J 14:1589–1591
Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322
Halliwell BH, Gutteridge JMC (1989) Free radicals in biology and medicine. Oxford University Press, Oxford
Halliwell B, Gutteridge MC (1990) The antioxidants of human extracellular fluids. Archs Biochem Biophys 280:1–8
Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354
Hayes JP, Shonkwiler JS (1996) Analyzing mass-independent data. Physiol Zool 69:974–980
Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211
Iorio EL (2004) The d-ROMs test and the evaluation of oxidative stress (in Italian). Diacron International, Pistoia
Krinsky NI, Yeum K-J (2003) Carotenoid–radical interactions. Biochem Biophys Res Commun 305:754–760
Laaksonen T, Fargallo JA, Korpimäki E, Lyytinen S, Valkama J, Pöyri V (2004) Year- and sex-dependent effects of experimental brood sex ratio manipulation on fledging condition of Eurasian kestrels. J Anim Ecol 73:342–352
Leffler JE (1993) An introduction to free radicals. Wiley, New York
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348
Martínez-Padilla J, Martínez J, Dávila JA, Merino S, Moreno J, Millán J (2004) Within-brood size differences, sex and parasites determine blood stress protein levels in Eurasian Kestrel nestlings. Funct Ecol 18:426–434
Masoro EJ (2002) Caloric restriction: a key to understanding and modulating aging. Elsevier, Amsterdam
Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260
Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford
Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159
Negro JJ, Tella JL, Blanco G, Forero MG, Garrido-Fernández J (2000) Diet explains interpopulation variation in plasma carotenoids and skin pigmentation in nestling white storks. Physiol Biochem Zool 73:97–101
Neuenschwander S, Brinkhof MWG, Kölliker M, Richner H (2003) Brood size, sibling competition, and the cost of begging in great tits (Parus major). Behav Ecol 14:457–462
Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514
Palozza P, Krinsky NI (1992a) Antioxidant effects of carotenoids in vivo and in vitro: an overview. Methods Enzymol 213:403–419
Palozza P, Krinsky NI (1992b) β-Carotene and α-tocopherol are synergistic antioxidants. Arch Biochem Biophys 297:184–187
Perez-Campo R, López-Torres M, Cadenas S, Rojas C, Barja G (1998) The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B 168:149–158
Price T (1996) Maternal and paternal effects in birds. Effects on offspring fitness. In: Timothy AM, Charles W (eds) Maternal effects as adaptation. Oxford University Press, Oxford, pp 202–226
Robles R, Palomino N, Robles A (2001) Oxidative stress in the neonate. Early Human Dev 65:S75–S81
von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266:1–12
Simmons RE (2002) Siblicide provides food benefits for raptor chicks: re-evaluating brood manipulation studies. Anim Behav 64:F19–F24
Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63
Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H (1994) Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction. Mech Ageing Dev 74:121–133
Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651
Surai PF, Noble RC, Speake BK (1996) Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochim Biophys Acta 1304:1–10
Tanganelli I, Ciccoli L, Tansi R, Borgogni P, Rossi V, Gistri M, Pettinari O, Signorini C, Marisi M (2000) Markers of oxidative stress in diabetic patients. Diab Res Clin Prac 50:S1
Tella JL, Bortolotti GR, Dawson RD, Forero MG (2000) The T-cell-mediated immune response and return rate of fledgling American kestrels are positively correlated with parental clutch size. Proc R Soc Lond B 267:891–895
Vleck CM, Bucher TL (1998) Energy metabolism, gas exchange, and ventilation. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial–precocial spectrum. Oxford University Press, Oxford, pp 89–116
Weindruch R, Walford RL (1988) The retardation of aging and disease by dietary restriction. C.C. Thomas, Springfield
Wienburg CL, Shore RF (2004) Factors influencing liver PCB concentrations in sparrowhawks (Accipiter nisus), kestrels (Falco tinnunculus) and herons (Ardea cinerea) in Britain. Environ Pollut 132:41–50
Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond B (Biol Lett) 271:360–363
Acknowledgements
We are grateful to G. Di Lieto for helping with the data collection and to A. Sorace for ringing the birds. TERNA and ACEA allowed the monitoring of nest boxes on their utility lines. In particular, we are grateful to G. Cavallari, N. Landini and A. Olivieri from ENEL, and to G. La Catena, G. Noia and C. Puliti from ACEA. Ornis italica sponsored part of the fieldwork. Three reviewers improved the manuscript with their valuable comments. P. W. Christie for improving the English. D. Costantini was supported by a PhD fellowship from the University of Rome La Sapienza. G. Dell’Omo was supported by the Swiss National Science Foundation and the NCCR “Neural Plasticity and Repair”.
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Costantini, D., Casagrande, S., De Filippis, S. et al. Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176, 329–337 (2006). https://doi.org/10.1007/s00360-005-0055-6
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DOI: https://doi.org/10.1007/s00360-005-0055-6
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