Abstract
Organisms face resource trade-offs to support their parental effort and survival. The life-history oxidative stress hypothesis predicts that an individual’s redox state modulates the trade-off between current and residual fitness, but this has seldom been tested experimentally in non-captive organisms. In this study, we manipulated the brood size in breeding pairs of barn swallows (Hirundo rustica) and found that females tending enlarged broods had increased levels of plasma oxidative damage (malondialdehyde concentration). This effect, however, was not accompanied by either a depletion, or defensive upregulation in antioxidants (glutathione, total antioxidant capacity, and uric acid) that may explain the increase in oxidative damage. Brood size manipulation and the level of plasma oxidative damage during brood rearing are not translated into decreased annual return rate, which does not support the oxidative stress hypothesis of life-history trade-offs. On the contrary, we found that female’s oxidative damage and total glutathione levels, an important intracellular non-enzymatic antioxidant measured at hatching decreased and correlated positively, respectively with annual return rate, suggesting that oxidative condition at hatching might be a more important contributor to fitness than the oxidative physiology measured during chick rearing. We also show that individual traits and ecological factors, such as the timing of breeding and the abundance of blood-sucking nest mites, correlated with the redox state of males and females during brood care.
Significance statement
Oxidative stress is one of the most important physiological costs of reproduction and thus a key modulator of life-history trade-offs. In this study, we manipulated reproductive effort in breeding pairs of barn swallows and found that females tending enlarged broods had increased levels of plasma oxidative damage. This effect, however, was not accompanied by either a depletion or upregulation in antioxidants that may explain the increase in oxidative damage. We found that female’s oxidative damage and total glutathione levels measured at hatching decreased and correlated positively, respectively with annual return rate, suggesting that oxidative condition at hatching might be an important contributor to fitness. Brood size manipulation and the increased levels of plasma oxidative damage are not translated into decreased annual return rate; thus, our results support the hypothesis that reproductive effort has a transient effect on oxidative physiology.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aloise King ED, Garratt M, Brooks R (2013) Manipulating reproductive effort leads to changes in female reproductive scheduling but not oxidative stress. Ecol Evol 3(12):4161–4171. https://doi.org/10.1002/ece3.786
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(5):363–368. https://doi.org/10.1111/j.1461-0248.2004.00594.x
Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1:1–7 https://github.com/lme4/lme4/ http://lme4.r-forge.r-project.org/
Beaulieu M, Geiger RE, Reim E, Zielke L, Fischer K (2015) Reproduction alters oxidative status when it is traded-off against longevity. Evolution 69(7):1786–1796. https://doi.org/10.1111/evo.12697
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(9):2584–2593. https://doi.org/10.1890/07-1135.1
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24(3):127–135. https://doi.org/10.1016/j.tree.2008.10.008
Blount JD, Vitikainen EIK, Stott I, Cant MA (2016) Oxidative shielding and the cost of reproduction. Biol Rev 91(2):483–497. https://doi.org/10.1111/brv.12179
Bókony V, Lendvai ÁZ, Vágási CI et al (2014) Necessity or capacity? Physiological state predicts problem-solving performance in house sparrows. Behav Ecol 25(1):124–135. https://doi.org/10.1093/beheco/art094
Bucolo G, David H (1973) Quantitative determination of serum triglycerides by the use of enzymes. Clin Chem 19(5):476–482
Christe 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(1731):1142–1149. https://doi.org/10.1098/rspb.2011.1546
Cohen A, Klasing K, Ricklefs R (2007) Measuring circulating antioxidants in wild birds. Comp Biochem Physiol B 147(1):110–121. https://doi.org/10.1016/j.cbpb.2006.12.015
Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11(11):1238–1251. https://doi.org/10.1111/j.1461-0248.2008.01246.x
Costantini D (2014) Oxidative stress and hormesis in evolutionary ecology and physiology. A marriage between mechanistic and evolutionary approaches. Springer, Berlin
Costantini D, Bonisoli-Alquati A, Rubolini D, Caprioli M, Ambrosini R, Romano M, Saino N (2014a) Nestling rearing is antioxidant demanding in female barn swallows (Hirundo rustica). Naturwissenschaften 101(7):541–548. https://doi.org/10.1007/s00114-014-1190-2
Costantini D, Casasole G, Eens M (2014b) Does reproduction protect against oxidative stress? J Exp Biol 217(23):4237–4243. https://doi.org/10.1242/jeb.114116
Costantini D, Casasole G, AbdElgawad H, Asard H, Eens M (2016) Experimental evidence that oxidative stress influences reproductive decisions. Funct Ecol 30(7):1169–1174. https://doi.org/10.1111/1365-2435.12608
Costantini D, Dell’Omo G (2015) Oxidative stress predicts long-term resight probability and reproductive success in Scopoli’s shearwater (Calonectris diomedea). Conserv Physiol 3:cov024
Costantini D, Møller AP (2009) Does immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Physiol A 153(3):339–344. https://doi.org/10.1016/j.cbpa.2009.03.010
Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23(3):506–509. https://doi.org/10.1111/j.1365-2435.2009.01546.x
Cram DL, Blount JD, Young AJ (2015) The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder. Proc R Soc B 282(1819):20152031. https://doi.org/10.1098/rspb.2015.2031
Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic melocule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15(4):316–328. https://doi.org/10.1016/j.numecd.2005.05.003
Emaresi G, Henry I, Gonzalez E, Roulin A, Bize P (2016) Sex- and melanic-specific variations in the oxidative status of adult tawny owls in response to manipulated reproductive effort. J Exp Biol 219(1):73–79. https://doi.org/10.1242/jeb.128959
Erel O (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37(4):277–285. https://doi.org/10.1016/j.clinbiochem.2003.11.015
Fletcher QE, Selman C, Boutin S, McAdam AG, Woods SB, Seo AY, Leeuwenburgh C, Speakman JR, Humphries MM (2012) Oxidative damage increases with reproductive energy expenditure and is reduced by food-supplementation. Evolution 67:1527–1536
Fossati P, Prencipe L (1982) Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin Chem 28(10):2077–2080
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks, CA
Freeman-Gallant CR, Amidon J, Berdy B, Wein S, Taff CC, Haussmann MF (2011) Oxidative damage to DNA related to survivorship and carotenoid-based sexual ornamentation in the common yellowthroat. Biol Lett 11:429–432
Fülöp A, Vágási CI, Pap PL (2017) Cohabitation with farm animals rather than breeding effort increases the infection with feather-associated bacteria in the barn swallow Hirundo rustica. J Avian Biol 48(7):1005–1014. https://doi.org/10.1111/jav.01262
Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS One 3(10):e3335. https://doi.org/10.1371/journal.pone.0003335
Garratt M, Pichaud N, Aloise King ED, Brooks RC (2013) Physiological adaptations to reproduction. I. Experimentally increasing litter size enhances aspects of antioxidant defence but does not cause oxidative damage in mice. J Exp Biol 216(15):2879–2888. https://doi.org/10.1242/jeb.082669
Halliwell B, Gutteridge J (2007) Free radicals in biology and medicine. Oxford University Press, Oxford
Hõrak P, Sild E, Soomets U, Sepp T, Kilk K (2010) Oxidative stress and information content of black and yellow plumage coloration: an experiment with greenfinches. J Exp Biol 213(13):2225–2233. https://doi.org/10.1242/jeb.042085
Isaksson C (2013) Opposing effects on glutathione and reactive oxygen metabolites of sex, habitat, and spring date, but no effect of increased breeding density in great tits (Parus major). Ecol Evol 3(8):2730–2738. https://doi.org/10.1002/ece3.663
Jenni-Eiermann S, Jenni L, Kvist A, Lindström Å, Piersma T, Visser GH (2002) Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205(Pt 16):2453–2460
Jenni-Eiermann S, Jenni L, Smith S, Costantini D (2014) Oxidative stress in endurance flight: an unconsidered factor in bird migration. PLoS One 9(5):e97650. https://doi.org/10.1371/journal.pone.0097650
Klasing KC, Austic RE (1984) Changes in plasma tissue and urinary nitrogen metabolites due to an inflammatory challenge. Proc Soc Exp Biol Med 176(3):276–284. https://doi.org/10.3181/00379727-176-41871
Lendvai AZ, Akçay Ç, Ouyang JQ, Dakin R, Domalik AD, St John PS, Stanback M, Moore IT, Bonier F (2015) Analysis of the optimal duration of behavioral observations based on an automated continuous monitoring system in tree swallows (Tachycineta bicolor): is one hour good enough? PLoS One 10(11):e0141194. https://doi.org/10.1371/journal.pone.0141194
López-Arrabé J, Cantarero A, Pérez-Rodríguez L, Palma A, Alonso-Alvarez C, González-Braojos S, Moreno J (2015) Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment. Oecologia 179(1):29–41. https://doi.org/10.1007/s00442-015-3321-7
Losdat S, Helfenstein F, Gaude B, Richner H (2011) Reproductive effort transiently reduces antioxidant capacity in a wild bird. Behav Ecol 22(6):1218–1226. https://doi.org/10.1093/beheco/arr116
Markó G, Costantini D, Michl G, Török J (2011) Oxidative damage and plasma antioxidant capacity in relation to body size, age, male sexual traits and female reproductive performance in the collared flycatcher (Ficedula albicollis). J Comp Physiol B 181(1):73–81. https://doi.org/10.1007/s00360-010-0502-x
Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28(6):347–350. https://doi.org/10.1016/j.tree.2013.01.015
Møller AP (1990) Effects of parasitism by the haematophagous mite Ornithonyssus bursa on reproduction in the barn swallow Hirundo rustica. Ecology 71(6):2345–2357. https://doi.org/10.2307/1938645
Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, Oxford
Møller AP, de Lope F (1999) Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. J Anim Ecol 68(1):163–171. https://doi.org/10.1046/j.1365-2656.1999.00274.x
Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12(1):75–92. https://doi.org/10.1111/j.1461-0248.2008.01258.x
Ninni P, de Lope F, Saino N, Haussy C, Møller AP (2004) Antioxidants and condition-dependence of arrival date in a migratory passerine. Oikos 105(1):55–64. https://doi.org/10.1111/j.0030-1299.2004.12516.x
Noguera JC, Kim S-Y, Velando A (2012) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett 8(1):61–63. https://doi.org/10.1098/rsbl.2011.0756
Pap PL, Pătraș L, Osváth G, Buehler DM, Versteegh MA, Sesarman A, Banciu M, Vágási CI (2015) Seasonal patterns and relationships among coccidian infestations, measures of oxidative physiology, and immune function in free-living house sparrows over an annual cycle. Physiol Biochem Zool 88(4):395–405. https://doi.org/10.1086/681243
Pap PL, Tökölyi J, Szép T (2005) Frequency and consequences of feather holes in barn swallows Hirundo rustica. Ibis 146:169–175
Partadiredja G, Worrall S, Bedi KS (2009) Early life undernutrition alters the level of reduced glutathione but not the activity levels of reactive oxygen species enzymes or lipid peroxidation in the mouse forebrain. Brain Res 1285:22–29. https://doi.org/10.1016/j.brainres.2009.06.010
Pérez-Rodríguez L, Romero-Haro AA, Sternalski A, Muriel J, Mougeot F, Gil D, Alonso-Alvarez C (2015) Measuring oxidative stress: the confounding effect of lipid concentration in measures of lipid peroxidation. Physiol Biochem Zool 88(3):345–351. https://doi.org/10.1086/680688
R Core Team (2016) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org
Rey B, Pélisson PF, Bel-Venner MC, Voituron Y, Venner S (2015) Revisiting the link between breeding effort and oxidative balance through field evaluation of two sympatric sibling insect species. Evolution 69(3):815–822. https://doi.org/10.1111/evo.12586
Romero-Haro AA, Alonso-Alvarez A (2015) The level of an intracellular antioxidant during development determines the adult phenotype in a bird species: a potential organizer role for glutathione. Am Nat 185(3):390–405. https://doi.org/10.1086/679613
Rothman KJ (1990) No adjustments are needed for multiple comparisons. Epidemiology 1(1):43–46. https://doi.org/10.1097/00001648-199001000-00010
Rothman KJ (2014) Six persistent research misconceptions. J Gen Int Med 29(7):1060–1064. https://doi.org/10.1007/s11606-013-2755-z
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(5):e19593. https://doi.org/10.1371/journal.pone.0019593
Saino N, Romano M, Ambrosini R, Ferrari RP, Møller AP (2004) Timing of reproduction and egg quality covary with temperature in the insectivorous barn swallow, Hirundo rustica. Funct Ecol 18(1):50–57. https://doi.org/10.1046/j.0269-8463.2004.00808.x
Schaub M, von Hirschheydt J (2009) Effect of current reproduction on apparent survival, breeding dispersal, and future reproduction in barn swallows assessed by multistate capture–recapture models. J Anim Ecol 78(3):625–635. https://doi.org/10.1111/j.1365-2656.2008.01508.x
Selman C, Blount JD, Nussey DH, Speakman JR (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27(10):570–577. https://doi.org/10.1016/j.tree.2012.06.006
Senn SS (2008) Baselines and covariate information. In: Senn SS (2008) statistical issues in drug development, 2nd edn. John Wiley & Sons Ltd, Chichester, pp 95–112
Sepp T, Karu U, Blount JD, Sild E, Männiste M, Hõrak P (2012) Coccidian infection causes oxidative damage in greenfinches. PLoS One 7(5):e36495. https://doi.org/10.1371/journal.pone.0036495
Sepp T, Sild E, Hõrak P (2010) Hematological condition indexes in greenfinches: effects of captivity and diurnal variation. Physiol Biochem Zool 83(2):276–282. https://doi.org/10.1086/648580
Sorci G, Faivre B (2009) Inflammation and oxidative stress in vertebrate host–parasite systems. Philos T Roy Soc B 364(1513):71–83. https://doi.org/10.1098/rstb.2008.0151
Speakman JR, Blount JD, Bronikowski AM, Buffenstein R, Isaksson C, Kirkwood TBL, Monaghan P, Ozanne SE, Beaulieu M, Briga M, Carr SK, Christensen LL, Cochemé HM, Cram DL, Dantzer B, Harper JM, Jurk D, King A, Noguera JC, Salin K, Sild E, Simons MJP, Smith S, Stier A, Tobler M, Vitikainen E, Peaker M, Selman C (2015) Oxidative stress and life histories: unresolved issues and current needs. Ecol Evol 5(24):5745–5757. https://doi.org/10.1002/ece3.1790
Speakman JR, Garratt M (2014) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays 36(1):93–106. https://doi.org/10.1002/bies.201300108
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3(3):259–268. https://doi.org/10.2307/2389364
Stier A, Reichert S, Criscuolo F, Bize P (2015) Red blood cells open promising avenues for longitudinal studies of ageing in laboratory, non-model and wild animals. Exp Gerontol 71:118–134. https://doi.org/10.1016/j.exger.2015.09.001
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(1):37. https://doi.org/10.1186/1742-9994-9-37
Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham
van de Crommenacker J, Richardson DS, Koltz AM, Hutchings K, Komdeur J (2012) Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler. Proc R Soc Lond B 279(1733):1466–1476. https://doi.org/10.1098/rspb.2011.1865
Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond B 271(Suppl_5):S360–S363. https://doi.org/10.1098/rsbl.2004.0171
Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134(3):489–492
Yang DB, Xu YC, Wang DH, 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(22):4242–4250. https://doi.org/10.1242/jeb.092049
Acknowledgments
We thank Jácint Nagy for his help in data collection, Manuela Banciu and Alina Sesarman for their help with the biochemical assays, and Gareth Dyke for English editing. We are grateful to Antoine Stier, Pierre Bize, and two anonymous reviewers for their constructive comments on an earlier version of the manuscript.
Funding
This study was founded by a bilateral collaboration grant between Romanian and Hungarian research groups (RO–HU 679/2010), by a research grant of the Romanian Ministry of Education and Research (#PN-III-P4-ID-PCE-2016-0404), and by the Hungarian National Research, Development and Innovation Office (OTKA grant K11308 to Ádám Z. Lendvai). PLP was financed by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences (HAS), and OV was supported by the Hungarian Eötvös Scholarship (MÁEÖ2017_16/156845) awarded by the Tempus Public Foundation and by the Ginko Investments Ltd. AF was supported through the ÚNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities of Hungary, and also by two scholarships of the Campus Hungary Program (grants B2/1SZ/11551 and B2/1R/19362), and by a grant from the Hungarian National Research, Development and Innovation Office (OTKA grant no. K112527). CIV was financed by the János Bolyai Research Scholarship of the HAS and a post-doctoral grant of the Hungarian National Research, Development and Innovation Office (PD 121166).
Author information
Authors and Affiliations
Contributions
PLP and CIV conceived and designed the study. PLP, OV, AF, OSB, LP, and CIV performed the study. OV and PLP analyzed the data. PLP, CIV, OV, and AF wrote the manuscript. All authors commented, read, and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
Birds were handled in strict accordance with good animal welfare and ethical prescriptions.
The authors declare that this publication complies with the current laws of the country in which the experiment was performed (Romania).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by K. McGraw
Electronic supplementary material
ESM 1
(DOCX 17 kb).
Rights and permissions
About this article
Cite this article
Pap, P.L., Vincze, O., Fülöp, A. et al. Oxidative physiology of reproduction in a passerine bird: a field experiment. Behav Ecol Sociobiol 72, 18 (2018). https://doi.org/10.1007/s00265-017-2434-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-017-2434-x