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Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits

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Abstract

Oxidative stress has been suggested as a mechanism underlying the costs of reproduction and life history trade-offs. Reproductive activities may lead to high production of pro-oxidants, whose activity can generate oxidative damage when not countered by adequate antioxidant defenses. Because inter-individual differences in the efficiency of the antioxidant system are influenced by an individual’s diet, food availability experienced during reproduction may affect the females’ antioxidant status and, in birds, their ability to transfer antioxidants into their eggs. Moreover, a female’s ability to cope with oxidative stress has been suggested to influence pigment deposition in the eggshell, suggesting a possible signaling function of eggshell maculation. Here we performed a food supplementation experiment in a natural population of great tits (Parus major) in order to investigate how nutritional conditions experienced during the egg laying period affect the female’s oxidative status and egg investment and how maternal oxidative status and egg antioxidant protection relate to eggshell pigmentation. We show that food-supplemented females had lower oxidative damage levels (ROMs) than non-food-supplemented females. Furthermore, a female’s ROMs levels were negatively associated with the levels of yolk antioxidant protection in her eggs, but this negative association was only significant in non-food-supplemented females. This suggests that oxidative stress experienced during reproduction influences the allocation of antioxidants into the eggs. Moreover, we observed a positive relationship between eggshell pigment distribution and maternal and yolk antioxidant protection, suggesting that eggshell pigmentation is a cue of female (and offspring) quality.

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References

  • Afonso S, Vanore G, Batlle A (1999) Protoporphyrin IX and oxidative stress. Free Radic Res 31:161–170

    Article  CAS  PubMed  Google Scholar 

  • Alan RR, McWilliams SR (2013) Oxidative stress, circulating antioxidants, and dietary preferences in songbirds. Comp Biochem Physiol B 164:185–193

    Article  CAS  PubMed  Google Scholar 

  • Alberti A, Bolognini L, Macciantelli D, Caratelli M (2000) The radical cation of N, N-diethyl-para-paraphenylendiamine: a possible indicator of oxidative stress in biological samples. Res Chem Intermed 26:253–267

    Article  CAS  Google Scholar 

  • 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 

  • Arthur JR (2000) The glutathione peroxidases. Cell Mol Life Sci 57:1825–1835

    Article  CAS  PubMed  Google Scholar 

  • Berthouly A, Helfenstein F, Richner H (2007) Cellular immune response, stress resistance and competitiveness in nestling great tits in relation to maternally transmitted carotenoids. Funct Ecol 21:335–343

    Article  Google Scholar 

  • Bindoli A, Fukuto JM, Forman HJ (2008) Thiol chemistry in peroxidase catalysis and redox signaling. Antioxid Redox Signal 10:1549–1564

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002) 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

    Article  CAS  Google Scholar 

  • Bryant DM (1997) Energy expenditure in wild birds. Proc Nutr Soc 56:1025–1039

    Article  CAS  PubMed  Google Scholar 

  • Catoni C, Peters A, Schaefer HM (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Anim Behav 76:1107–1119

    Article  Google Scholar 

  • 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 279:1142–1149

    Article  CAS  Google Scholar 

  • Cohen AA, McGraw KJ, Robinson WD (2009) Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia 161:673–683

    Article  PubMed  Google Scholar 

  • Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251

    PubMed  Google Scholar 

  • Costantini D (2010) 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

    Article  CAS  PubMed  Google Scholar 

  • Costantini D, Monaghan P, Metcalfe NB (2011) Biochemical integration of blood redox state in captive zebra finches (Taeniopygia guttata). J Exp Biol 214:1148–1152

    Article  CAS  PubMed  Google Scholar 

  • Costantini D, Meillere A, Carravieri A et al (2014) Oxidative stress in relation to reproduction, contaminants, gender and age in a long-lived seabird. Oecologia 175:1107–1116

    Article  PubMed  Google Scholar 

  • De Coster G, De Neve L, Lens L (2013) Intra-clutch variation in avian eggshell pigmentation covaries with female quality. J Ornithol 154:1057–1065

    Article  Google Scholar 

  • de Heij ME, van der Graaf AJ, Hafner D, Tinbergen JM (2007) Metabolic rate of nocturnal incubation in female great tits, Parus major, in relation to clutch size measured in a natural environment. J Exp Biol 210:2006–2012

    Article  PubMed  Google Scholar 

  • Fechner A, Bohme CC, Gromer S, Funk M, Schirmer RH, Becker K (2001) Antioxidant status and nitric oxide in the malnutrition syndrome kwashiorkor. Pediatr Res 49:237–243

    Article  CAS  PubMed  Google Scholar 

  • Feoli AM, Siqueira IR, Almeida L, Tramontina AC, Vanzella C, Sbaraini S, Schweigert ID, Netto CA, Perry MLS, Goncalves CA (2006) Effects of protein malnutrition on oxidative status in rat brain. Nutrition 22:160–165

    Article  CAS  PubMed  Google Scholar 

  • Gibb J (1957) Food requirements and other observations on captive tits. Bird Study 4:207–215

    Article  Google Scholar 

  • Giordano M, Groothuis TGG, Tschirren B (2014) Interactions between prenatal maternal effects and posthatching conditions in a wild bird population. Behav Ecol 25:1459–1466

    Article  Google Scholar 

  • Giordano M, Costantini D, Tschirren B (2015) Sex-specific effects of prenatal and postnatal nutritional conditions on the oxidative status of great tit nestlings. Oecologia 177:123–131

    Article  CAS  PubMed  Google Scholar 

  • Gosler AG, Barnett PR, Reynolds SJ (2000) Inheritance and variation in eggshell patterning in the great tit Parus major. Proc R Soc Lond B 267:2469–2473

    Article  CAS  Google Scholar 

  • Gosler AG, Higham JP, Reynolds SJ (2005) Why are birds’ eggs speckled? Ecol Lett 8:1105–1113

    Article  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford

    Google Scholar 

  • Hanley D, Heiber G, Dearborn DC (2008) Testing an assumption of the sexual-signaling hypothesis: does blue-green egg reflect maternal antioxidant capacity? Condor 110:767–771

    Article  Google Scholar 

  • Hansen M, Flatt T, Aguilaniu H (2013) Reproduction, fat metabolism, and life span: what is the connection? Cell Metab 17:10–19

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86

    Article  PubMed  Google Scholar 

  • Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213

    Article  CAS  PubMed  Google Scholar 

  • Isaksson C, Johansson A, Andersson S (2008) Egg yolk carotenoids in relation to habitat and reproductive investment in the great tit Parus major. Physiol Biochem Zool 81:112–118

    Article  CAS  PubMed  Google Scholar 

  • Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, Motterlini R (2003) Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 543:113–119

    Article  CAS  PubMed  Google Scholar 

  • Kennedy GY, Vevers HG (1976) Survey of avian eggshell pigments. Comp Biochem Physiol B 55:117–123

    CAS  PubMed  Google Scholar 

  • Li J, Wang H, Stoner GD, Bray TM (2002) Dietary supplementation with cysteine prodrugs selectively restores tissue glutathione levels and redox status in protein-malnourished mice. J Nutr Biochem 13:625–633

    Article  PubMed  Google Scholar 

  • Marques de Sá JP (2007) Applied statistics. Springer, Berlin

    Google Scholar 

  • Marri V, Richner H (2014) Yolk carotenoids increase fledging success in great tit nestlings. Oecologia 176:371–377

    Article  PubMed  Google Scholar 

  • Martínez-de la Puente J, Merino S, Moreno J, Tomás G, Morales J, Lobato E, García-Fraile S, Martínez J (2007) Are eggshell spottiness and colour indicators of health and condition in blue tits Cyanistes caeruleus? J Avian Biol 38:377–384

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  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

    Article  Google Scholar 

  • Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28:347–350

    Article  PubMed  Google Scholar 

  • Morales J, Velando A, Moreno J (2008) Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behav Ecol Sociobiol 63:227–233

    Article  Google Scholar 

  • Moreno J, Osorno JL (2003) Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol Lett 6:803–806

    Article  Google Scholar 

  • Moreno J, Sanz JJ (1994) The relationship between energy-expenditure during incubation and clutch size in the pied flycatcher Ficedula hypoleuca. J Avian Biol 25:125–130

    Article  Google Scholar 

  • Nikolaidis MG, Mougios V (2004) Effects of exercise on the fatty-acid composition of blood and tissue lipids. Sports Med 34:1051–1076

    Article  PubMed  Google Scholar 

  • Nilsson JA, Råberg L (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128:187–192

    Article  Google Scholar 

  • Nord A, Sandell MI, Nilsson JA (2010) Female zebra finches compromise clutch temperature in energetically demanding incubation conditions. Funct Ecol 24:1031–1036

    Article  Google Scholar 

  • Olsson M, Healey M, Perrin C, Wilson M, Tobler M (2012) Sex-specific SOD levels and DNA damage in painted dragon lizards (Ctenophorus pictus). Oecologia 170:917–924

    Article  PubMed  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  PubMed  Google Scholar 

  • Perrins CM (1996) Eggs, egg formation and the timing of breeding. Ibis 138:2–15

    Article  Google Scholar 

  • Porter NA, Caldwell SE, Mills KA (1995) Mechanisms of free-radical oxidation of unsaturated lipids. Lipids 30:277–290

    Article  CAS  PubMed  Google Scholar 

  • Postma E, Siitari H, Schwabl H, Richner H, Tschirren B (2014) The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models. Oecologia 174:631–638

    Article  PubMed  Google Scholar 

  • Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Remeš V, Matysiokova B, Klejdus B (2011) Egg yolk antioxidant deposition as a function of parental ornamentation, age, and environment in great tits Parus major. J Avian Biol 42:387–396

    Article  Google Scholar 

  • Reynolds SJ, Martin GR, Cassey P (2009) Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Anim Behav 78:209–215

    Article  Google Scholar 

  • Rindler PM, Plafker SM, Szweda LI, Kinter M (2013) High dietary fat selectively increases catalase expression within cardiac mitochondria. J Biol Chem 288:1979–1990

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sanz JJ, García-Navas V (2009) Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. J Anim Ecol 78:31–41

    Article  PubMed  Google Scholar 

  • SAS Institute (1989–2007) JMP, Version 10. Cary, NC

  • Sies H (1991) The role of reactive oxygen species in biological processes. Klin Wochenschr 69:965–968

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham

    Google Scholar 

  • Surai PF, Noble RC, Speake BK (1996) Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochim Biophys Acta 1304:1–10

    Article  CAS  PubMed  Google Scholar 

  • Török J, Hargitai R, Hegyi G, Matus Z, Michl G, Peczely P, Rosivall B, Toth G (2007) Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order. Behav Ecol Sociobiol 61:541–550

    Article  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 

  • Tschirren B, Richner H, Schwabl H (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc Lond B 271:1371–1375

    Article  CAS  Google Scholar 

  • van de Crommenacker J, Horrocks NPC, Versteegh MA, Komdeur J, Tieleman BI, Matson KD (2010) Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: implications for ecologists. J Exp Biol 213:3527–3535

    Article  PubMed  Google Scholar 

  • Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond B 271:S360–S363

    Article  CAS  Google Scholar 

  • Williams TD (2005) Mechanisms underlying the costs of egg production. Bioscience 55:39–48

    Article  Google Scholar 

  • Wilson HR (1997) Effects of maternal nutrition on hatchability. Poult Sci 76:134–143

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Martina Keller, Kathrin Näpflin and Jamal Hanafi for field assistance and help in the lab and three anonymous reviewers for comments on the manuscript. This research was financially supported by the Swiss National Science Foundation (grant PP00P3_128386 to BT).

Ethical standards

All procedures were conducted under license from the Veterinary Office of the Canton of Zurich, Switzerland (195/2010) and the Federal Office for the Environment, Switzerland (324).

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Marta Giordano, Joel L. Pick & Barbara Tschirren

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

    David Costantini

  3. Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Graham Kerr Building, Glasgow, G12 8QQ, UK

    David Costantini

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  1. Marta Giordano
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  2. David Costantini
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  3. Joel L. Pick
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  4. Barbara Tschirren
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Correspondence to Marta Giordano.

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Communicated by K. McGraw

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Giordano, M., Costantini, D., Pick, J.L. et al. Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits. Behav Ecol Sociobiol 69, 777–785 (2015). https://doi.org/10.1007/s00265-015-1893-1

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