Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus)

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

  1. Allen PC (1997) Production of free radical species during Eimeria maxima infections in chickens. Poult Sci 76:814–821

    PubMed  CAS  Google Scholar 

  2. 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

    Article  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90:7915–7922

    PubMed  Article  CAS  Google Scholar 

  5. Armitage P, Berry G (1996) Statistical methods in medical research (Italian edition). McGraw-Hill, Milano and New York

    Google Scholar 

  6. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581

    PubMed  CAS  Google Scholar 

  7. 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

    Article  Google Scholar 

  8. 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

    Article  CAS  Google Scholar 

  9. 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

    Article  CAS  Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. 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

    Article  PubMed  CAS  Google Scholar 

  13. 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)

  14. Chiarotti F (2004) Detecting assumption violations in mixed-model analysis of variance. Ann Ist Super Sanità 40:165–171

    PubMed  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  CAS  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  Google Scholar 

  20. 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

    Article  CAS  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Google Scholar 

  23. Fernie KJ, Bird DM (2001) Evidence of oxidative stress in American kestrels exposed to electromagnetic fields. Environ Res 86:198–207

    Article  PubMed  CAS  Google Scholar 

  24. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    Article  PubMed  CAS  Google Scholar 

  25. Fridolfsson A-K, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121

    Article  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. Goodwin TW (1984) The biochemistry of carotenoids. Animals, volume II. Chapman and Hall, London

  28. 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

    Google Scholar 

  29. 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

    Article  CAS  Google Scholar 

  30. Halliwell BH, Gutteridge JMC (1989) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  31. Halliwell B, Gutteridge MC (1990) The antioxidants of human extracellular fluids. Archs Biochem Biophys 280:1–8

    Article  CAS  Google Scholar 

  32. Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  33. Hayes JP, Shonkwiler JS (1996) Analyzing mass-independent data. Physiol Zool 69:974–980

    Google Scholar 

  34. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  35. Iorio EL (2004) The d-ROMs test and the evaluation of oxidative stress (in Italian). Diacron International, Pistoia

    Google Scholar 

  36. Krinsky NI, Yeum K-J (2003) Carotenoid–radical interactions. Biochem Biophys Res Commun 305:754–760

    Article  PubMed  CAS  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Leffler JE (1993) An introduction to free radicals. Wiley, New York

    Google Scholar 

  39. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  40. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  41. 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

    Article  Google Scholar 

  42. Masoro EJ (2002) Caloric restriction: a key to understanding and modulating aging. Elsevier, Amsterdam

    Google Scholar 

  43. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  44. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  45. 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

    Google Scholar 

  46. 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

    Article  PubMed  CAS  Google Scholar 

  47. 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

    Article  Google Scholar 

  48. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  Google Scholar 

  49. Palozza P, Krinsky NI (1992a) Antioxidant effects of carotenoids in vivo and in vitro: an overview. Methods Enzymol 213:403–419

    CAS  Article  Google Scholar 

  50. Palozza P, Krinsky NI (1992b) β-Carotene and α-tocopherol are synergistic antioxidants. Arch Biochem Biophys 297:184–187

    Article  CAS  Google Scholar 

  51. 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

    Article  PubMed  CAS  Google Scholar 

  52. 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

    Google Scholar 

  53. Robles R, Palomino N, Robles A (2001) Oxidative stress in the neonate. Early Human Dev 65:S75–S81

    Article  CAS  Google Scholar 

  54. 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

    Article  Google Scholar 

  55. Simmons RE (2002) Siblicide provides food benefits for raptor chicks: re-evaluating brood manipulation studies. Anim Behav 64:F19–F24

    Article  Google Scholar 

  56. Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63

    PubMed  Article  CAS  Google Scholar 

  57. 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

    Article  PubMed  CAS  Google Scholar 

  58. Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651

    Article  CAS  Google Scholar 

  59. 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

    PubMed  CAS  Google Scholar 

  60. 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

    Article  Google Scholar 

  61. 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

    Article  CAS  Google Scholar 

  62. 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

    Google Scholar 

  63. Weindruch R, Walford RL (1988) The retardation of aging and disease by dietary restriction. C.C. Thomas, Springfield

  64. 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

    Article  PubMed  CAS  Google Scholar 

  65. 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

    Article  CAS  Google Scholar 

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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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Correspondence to David Costantini.

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Communicated by G. Heldmaier

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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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Keywords

  • Oxidative stress
  • Free radicals
  • Antioxidant power
  • Carotenoids
  • Falco tinnunculus