Abstract
Reproduction is a demanding activity, since organisms must produce and, in some cases, protect and provision their progeny. Hence, a central tenet of life-history theory predicts that parents have to trade parental care against body maintenance. One physiological cost thought to be particularly important as a modulator of such trade-offs is oxidative stress. However, evidence in favour of the hypothesis of an oxidative cost of reproduction is contradictory. In this study, we manipulated the brood size of wild barn swallows Hirundo rustica soon after hatching of their nestlings to test whether an increase in nestling rearing effort translates into an increased oxidative damage and a decreased antioxidant protection at the end of the nestling rearing period. We found that, while plasma oxidative damage was unaffected by brood size enlargement, females rearing enlarged broods showed a decrease in plasma non-enzymatic antioxidants during the nestling rearing period. This was not the case among females rearing reduced broods and among males assigned to either treatment. Moreover, individuals with higher plasma oxidative damage soon after the brood size manipulation had lower plasma non-enzymatic antioxidants at the end of the nestling rearing period, suggesting that non-enzymatic antioxidants were depleted to buffer the negative effects of high oxidative damage. Our findings point to antioxidant depletion as a potential mechanism mediating the cost of reproduction among female birds.
Similar content being viewed by others
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
Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol 25:577–585
Beaulieu M, Thierry AM, González-Acuña D, Polito MJ (2013) Integrating oxidative ecology into conservation physiology. Conser Physiol 1:cot004
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57:289–300
Bergeron P, Careau V, Humphries M, Réale D, Speakman J, Garant D (2011) The energetic and oxidative costs of reproduction in a free-ranging rodent. Funct Ecol 25:1063–1071
Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584
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
Boonekamp JJ, Salomons M, Bouwhuis S, Dijkstra C, Verhulst S (2014) Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol Lett, in press
Casagrande S, Dell’Omo G, Costantini D, Tagliavini J, Groothuis T (2011) Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study. Comp Biochem Physiol A 160:16–26
Christie P, Glaizot O, Strepparava N, Devevey G, Fumagalli L (2012) Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress. Proc R Soc Lond B 279:1142–1149
Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251
Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23:506–509
Costantini D, Metcalfe NB, Monaghan P (2010) Ecological processes in a hormetic framework. Ecol Lett 13:1435–1447
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
Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, Hurst JL (2011) Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc R Soc Lond B 278:1098–1106
Halliwell BH, Gutteridge JMC (2007) Free radicals in biology and medicine 4th edn. Oxford University Press, Oxford
Heiss R, Schoech SJ (2012) Oxidative cost of reproduction is sex specific and correlated with reproductive effort in a cooperatively breeding bird, the Florida scrub jay. Physiol Biochem Zool 85:499–503
Helfenstein F, Losdat S, Møller AP, Blount JD, Richner H (2010) Sperm of colourful males are better protected against oxidative stress. Ecol Lett 13:213–222
Kim S-Y, Velando A, Sorci G, Alonso-Alvarez C (2010) Genetic correlation between resistance to oxidative stress and reproductive lifespan in a bird species. Evolution 64:852–857
Losdat S, Helfenstein F, Gaude B, Richner H (2011) Reproductive effort transiently reduces antioxidant capacity in a wild bird. Behav Ecol 22:1218–1226
Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996
Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, Oxford
Nussey DH, Pemberton JM, Pilkington JG, Blount JD (2009) Life history correlates of oxidative damage in a free-living mammal population. Funct Ecol 23:809–817
Pike T, Blount JD, Bjerken B, Lindström J, Metcalfe NB (2007) Carotenoids, oxidative stress and female mating preference for longer lived males. Proc R Soc Lond B 274:1591–1596
Rands SA, Cuthill IC, Houston AI (2006) Explaining individual variation in patterns of mass loss in breeding birds. Theor Biol Med Modell 3:20
Rubolini D, Colombo G, Ambrosini R, Caprioli M, Clerici M, Colombo R, Dalle-Donne I, Milzani A, Romano A, Romano M, Saino N (2012) Sex-related effects of reproduction on biomarkers of oxidative damage in free-living barn swallows (Hirundo rustica). PLoS One 7:e48955
Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows (Hirundo rustica) in relation to brood size and parental effort. J Anim Ecol 66:827–836
Saino N, Calza S, Ninni P, Møller AP (1999) Barn swallows trade survival against offspring condition and immunocompetence. J Anim Ecol 68:999–1009
Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, Ambrosini R, Bonisoli-Alquati A, Romano A (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS One 6:e19593
Salmon AD, Marx DB, Harshman LG (2001) A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution 55:1600–1608
Speakman JR, Garratt M (2014) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. Bioessays 36:93–106
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stier A, Reichert S, Massemin S, Bize P, Criscuolo F (2012) Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Front Zool 9:37
Travers M, Clinchy M, Zanette L, Boonstra R, Williams TD (2010) Indirect predator effects on clutch size and the cost of egg production. Ecol Lett 13:980–988
van de Crommenacker J (2011) Hard times in paradise? Oxidative status, physiology and fitness in the tropical Seychelles warbler. PhD Thesis, University of Groningen
Wang Y, Salmon AB, Harshman LG (2001) A cost of reproduction: oxidative stress susceptibility is associated with increased egg production in Drosophila melanogaster. Exp Geront 36:1349–1359
Weinert BT, Timiras PS (2003) Invited review: Theories of aging. J Appl Physiol 95:1706–1716
Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond B 270:S360–S363
Williams GC (1966) Natural selection, the cost of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690
Yang D-B, Xu Y-C, Wang D-H, Speakman JR (2013) Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent. J Exp Biol 216:4242–4250
Acknowledgments
We thankfully acknowledge P. Bize and an anonymous reviewer for providing comments that helped us to improve the presentation of the article. We thank C. Girardo, R. Grossi, T. Noyere, D. Patelli, V. Pignataro, and M. Prinzivalli for help during fieldwork, the International Observatory for Oxidative Stress (Salerno, Italy) for advice and support, G. Brambilla and E. Vignolo for technical and logistical support at the ISS, Rome. ABA was funded by a MIUR PhD grant.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Alexandre Roulin
Rights and permissions
About this article
Cite this article
Costantini, D., Bonisoli-Alquati, A., Rubolini, D. et al. Nestling rearing is antioxidant demanding in female barn swallows (Hirundo rustica). Naturwissenschaften 101, 541–548 (2014). https://doi.org/10.1007/s00114-014-1190-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-014-1190-2