Abstract
Despite the great deal of ecological research interest in modulators of offspring quality and consequences of reproduction on female status, we still know little about the relationships among diet quality, antioxidant capacity of egg components (yolk and albumen) and oxidative status of female birds. In this study, I compared the egg quality (egg size, albumen and yolk antioxidant capacity) and serum oxidative status (oxidative damage, total serum antioxidant capacity, and serum thiols) of female pigeons (Columba livia) fed with foods of different quality (standard quality and decreased quality). I also analysed the patterns of covariation among egg and female traits. The study focussed on the first clutch laid by the female in the breeding season and on the short-term effects of a decrease in diet quality. The treatment did not affect the egg volume, the lipophilic and hydrophilic components of antioxidant capacity (lipOXY and hydrOXY, respectively) or the antioxidant capacity of the albumen (albumOXY). However, females fed a higher quality diet were fatter and had marginally higher values of serum hydroperoxides (oxidative damage) than females fed a lower quality diet. Moreover, females that showed an increase in yolk hydrOXY and serum hydroperoxides also showed a decrease in yolk lipOXY, albumOXY and serum antioxidant capacity. These results show that the female’s oxidative status can be correlated with the antioxidant content of her eggs, but the nature of these correlations is complex, depending on the molecular component measured. The results also suggest that in the pigeon the deposition of hydrophilic and lipophilic antioxidants in the egg may trade off against each other.
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Bindoli A, Fukuto JM, Forman HJ (2008) Thiol chemistry in peroxidase catalysis and redox signaling. Antioxid Redox Signal 10:1549–1564
Birrenkott GP, Shoop MA, Cooper K, Wiggins M (1988) Ovarian follicular growth and maturation in the domestic pigeon and guinea fowl (Numidia meleagris). Poult Sci 67:1783–1786
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
Bortolotti GR, Negro JJ, Surai PF, Prieto P (2003) Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiol Biochem Zool 76:367–374
Carere C, Balthazart J (2007) Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol Metab 18:73–80
Carratelli M, Porcaro R, Rustica M, De Simone E, Bertelli AAE, Corsi MM (2001) Reactive oxygen metabolites (ROMs) and prooxidant status in children with Down Syndrome. Int J Clin Pharmacol Res 21:79–84
Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26
Cohen AA, McGraw KJ (2009) No simple measures for antioxidant status in birds: complexity in inter- and intraspecific correlations among circulating antioxidant types. Funct Ecol 23:310–320
Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251
Costantini D, Bonadonna F (2009) Patterns of variation of serum oxidative stress markers in two seabird species. Polar Res (in press)
Costantini D, Dell’Omo G (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol Part A 145:137–142
Costantini D, Lipp H-P (2010) Short restraint time does not influence markers of serum oxidative stress in homing pigeons (Columba livia). J Anim Physiol Anim Nutr 94:24–28
Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370
Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23:506–509
Costantini D, Casagrande S, De Filippis S, Brambilla G, Fanfani A, Tagliavini J, Dell’Omo G (2006) Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:329–337
Costantini D, Dell’Ariccia G, Lipp H-P (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211:377–381
Dickinson DA, Forman HJ (2002) Cellular glutathione and thiols metabolism. Biochem Pharmacol 64:1019–1026
Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Progr Lipid Res 43:200–227
Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc Lond B 276:1737–1745
Elman JL (1959) Tissue sulfhydryls groups. Arch Biochem Biophys 82:70–77
Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS One 3:e3335
Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128
Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil Trans R Soc B 363:1647–1661
Halliwell BH, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford
Hammer Ø et al (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
Hargitai R, Arnold KE, Herényi M, Prechl J, Török J (2009) Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol 63:869–882
Houston DC (1997) Nutritional constraints on egg production in birds. Proc Nutr Soc 56:1057–1065
Hoyt DF (1979) Practical measures of estimating volume and fresh weight of bird eggs. Auk 96:73–77
Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York
Lindström J (2001) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348
McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92:375–380
Metcalfe N, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260
Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans R Soc B 363:1635–1645
Monaghan P, Nager RG, Houston DC (1998) The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc R Soc Lond B 265:1731–1735
Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurement and interpretation. Ecol Lett 12:75–92
Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New York
Nager RG, Monaghan P, Houston DC (2000) Within-clutch trade-offs between the number and quality of eggs: experimental manipulations in gulls. Ecology 81:1339–1350
Navara KJ, Badyaev AV, Mendonça MT, Hill GE (2006) Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiol Biochem Zool 79:1098–1105
Oppliger A, Christie P, Richner H (1996) Clutch size and malaria resistance. Nature 381:565
Royle NJ, Surai PF, McCartney RJ, Speake BK (1999) Parental investment and egg yolk lipid composition in gulls. Funct Ecol 13:298–306
Royle NJ, Surai PF, Hartley IR (2003) The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Funct Ecol 17:472–481
Rubolini D, Romano M, Bonisoli Alquati A, Saino N (2006) Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks. J Evol Biol 19:1571–1584
Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733
Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450
Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham
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
Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59
Acknowledgments
I thank two anonymous reviewers for their comments, which helped me to improve the manuscript; Neil Metcalfe for kindly improving the English and for providing valuable comments that improved the manuscript; Claudio Carere and Pat Monaghan for valuable discussions on hormone deposition in the egg. I am also grateful to the International Observatory for Oxidative Stress (Salerno, Italy) and to Giacomo Dell’Omo for advice and support; to Gianfranco Brambilla and Edoardo Vignolo for technical and logistical support at the ISS, Rome.
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Communicated by G. Heldmaier.
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Costantini, D. Complex trade-offs in the pigeon (Columba livia): egg antioxidant capacity and female serum oxidative status in relation to diet quality. J Comp Physiol B 180, 731–739 (2010). https://doi.org/10.1007/s00360-010-0456-z
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DOI: https://doi.org/10.1007/s00360-010-0456-z