Skip to main content
SpringerLink
Log in

Nestling rearing is antioxidant demanding in female barn swallows (Hirundo rustica)

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Beaulieu M, Thierry AM, González-Acuña D, Polito MJ (2013) Integrating oxidative ecology into conservation physiology. Conser Physiol 1:cot004

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Losdat S, Helfenstein F, Gaude B, Richner H (2011) Reproductive effort transiently reduces antioxidant capacity in a wild bird. Behav Ecol 22:1218–1226

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rands SA, Cuthill IC, Houston AI (2006) Explaining individual variation in patterns of mass loss in breeding birds. Theor Biol Med Modell 3:20

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Saino N, Calza S, Ninni P, Møller AP (1999) Barn swallows trade survival against offspring condition and immunocompetence. J Anim Ecol 68:999–1009

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Salmon AD, Marx DB, Harshman LG (2001) A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution 55:1600–1608

    Article  CAS  PubMed  Google Scholar 

  • Speakman JR, Garratt M (2014) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. Bioessays 36:93–106

    Article  PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Williams GC (1966) Natural selection, the cost of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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

  1. Department of Biology, University of Antwerp, Universiteitsplein 1, 2610, Wilrijk, Belgium

    David Costantini

  2. Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, G12 8QQ, UK

    David Costantini

  3. Department of Biological Sciences, University of South Carolina, 715 Sumter Street, 29208, Columbia, SC, USA

    Andrea Bonisoli-Alquati

  4. Dipartimento di Bioscienze, Università degli Studi di Milano, Milan, Italy

    Diego Rubolini, Manuela Caprioli, Maria Romano & Nicola Saino

  5. Dipartimento di Biotecnologie e Bioscienze, Università degli Studi di Milano-Bicocca, Milan, Italy

    Roberto Ambrosini

Authors
  1. David Costantini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Bonisoli-Alquati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diego Rubolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuela Caprioli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberto Ambrosini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nicola Saino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David Costantini.

Additional information

Communicated by: Alexandre Roulin

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-014-1190-2

Keywords

Search

Navigation