Abstract
Birds exhibit exceptional longevity and are thus regarded as a convenient model to study the intrinsic mechanisms of aging. The oxidative stress theory of aging suggests that individuals age because molecules, cells, tissues, organs, and, ultimately, animals accumulate oxidative damage over time. Accumulation of damage progressively reduces the level of antioxidant defences that are expected to decline with age. To test this theory, we measured the resistance of red blood cells to free radical attack in a captive population of greater flamingo (Phoenicopterus ruber roseus) of known age ranging from 0.3 to 45 years. We observed a convex relationship with young adults (12–20 years old) having greater resistance to oxidative stress than immature flamingos (5 months old) and old flamingos (30–45 years old). Our results suggest that the antioxidant detoxifying system must go through a maturation process before being completely functional. It then declines in older adults, supporting the oxidative theory of aging. Oxidative stress could hence play a significant role in shaping the pattern of senescence in a very long-lived bird species.
References
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. Ecol Lett 7:363–368
Alonso-Alvarez C et al (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60:1913–1924
Andziak B, O’Connor TP, Buffenstein R (2005) Antioxidants do not explain the disparate longevity between mice and the longest-living rodent, the naked mole-rat. Mech Ageing Dev 126:1206–1212
Andziak B et al (2006) High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell 5:463–471
Apanius V (1998) The Immune System. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, New York
Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581
Bize P, Devevey G, Monaghan P, Doligez B, Christe P (2008) Fecundity and survival in relation to resistance to oxidative stress in a free living bird. Ecology 89:2584–2593
Blount JD, Metcalfe NB, Arnold KE, Surai PF, Devevey G, Monaghan P (2003) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc Roy Soc B 270:1691–1696
Brunet-Rossinni AK (2004) Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mech Ageing Dev 125:11–20
Cézilly F, Viallefont A, Boy V, Johnson AR (1996) Annual variation in survival and breeding probability in greater flamingos. Ecology 77:1143–1150
Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247
Hagen TM (2003) Oxidative stress, redox imbalance, and the aging process. Antioxid Redox Signal 5:503–506
Harman D (1956) Ageing: a theory based on free radical and radiation chemistry. J Gerontol 2:298–300
Harmann GE, Mattick LR (1976) Association of lipid oxidation with seed ageing and death. Nature 260:323–324
Haussmann MF et al (2005) Cell-mediated immunosenescence in birds. Oecologia 145:270–275
Holmes DJ, Ottinger MA (2003) Birds as long-lived animal models for the study of aging. Exp Gerontol 38:1365–1375
Holmes DJ, Fluckiger R, Austad SN (2001) Comparative biology of aging in birds: an update. Exp Gerontol 36:869–883
Kapahi P, Boulton ME, Kirkwood TBL (1999) Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med 26:495–500
Kim H–S et al (1996) Age-related changes of alpha-tocopherol transfer protein expression in rat liver. J Nutr Sci Vitaminol 42:11–18
Kirkwood TBL (2005) Understanding the odd science of aging. Cell 120:437–447
Kirkwood TBL, Austad SN (2000) Why do we age? Nature 408:233–238
Kregel KC, Zhang HJ (2007) An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol Regul Integr Comp Physiol 292:18–36
Ku HH, Brunk UT, Sohal RS (1993) Relationship between mitochondrial superoxide and hydrogen-peroxide production and longevity of mammalian-species. Free Radic Biol Med 15:621–627
Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118
Medvedev ZA (1990) An attempt at a rational classification of theories of ageing. Biol Rev Camb Philos Soc 65:375–398
Monaghan P, Charmantier A, Nussey DH, Ricklefs RE (2008) The evolutionary ecology of senescence. Funct Ecol 22:371–378
Ricklefs RE, Scheuerlein A (2001) Comparison of aging-related mortality among birds and mammals. Exp Gerontol 36:845–857
Scheuerlein A, Ricklefs RE (2006) The evolution of senescence in birds: evidence from animals in zoos. J Ornithol 147:246
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Vleck CM, Haussmann MF, Vleck D (2006) Senescence in birds I: mechanisms. J Ornithol 147:S67
Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc Roy Soc B 271:S360–S363 (Supplement Biology Letters)
Zann RA (1996) The zebra finch. Oxford University Press, Oxford
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The experiments described herein comply with the current laws of Switzerland. This research was supported by grant 3100AO-104118 from the Swiss National Science Foundation.
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Communicated by C. G. Guglielmo.
G. Devevey and N. Bruyndonckx contributed equally to the work.
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Devevey, G., Bruyndonckx, N., von Houwald, F. et al. Age-specific variation of resistance to oxidative stress in the greater flamingo (Phoenicopterus ruber roseus). J Ornithol 151, 251–254 (2010). https://doi.org/10.1007/s10336-009-0456-5
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DOI: https://doi.org/10.1007/s10336-009-0456-5