Marine Biology

, 164:99 | Cite as

Incubation increases oxidative imbalance compared to chick rearing in a seabird, the Magellanic penguin (Spheniscus magellanicus)

  • Roger Colominas-CiuróEmail author
  • Marcelo Bertellotti
  • Eliana Carabajal
  • Verónica L. D’Amico
  • Andrés Barbosa
Original Paper


It is expected that activities which require a high use of energy could generate higher oxidative stress. In the present study, we have compared two breeding periods (incubation and chick rearing) with different energetic demands in the Magellanic penguin, predicting a higher oxidative unbalance during chick rearing since involves higher demanding activities such as chick feeding and greater nest protection than during incubation. Specifically, we predicted higher oxidative damage and lower antioxidant defences during chick rearing than during incubation. Fieldwork was conducted in a Magellanic penguin colony located in Estancia San Lorenzo (42°05′S, 63°49′W), Peninsula Valdes, Argentina, during the breeding season of 2014–2015. Surprisingly, our results did not support our initial prediction. Incubating adults had their oxidative status unbalanced showing significantly lower antioxidant levels than those rearing chicks. Moreover, oxidative damage did not show any significant variation between both breeding periods. Further, we did not find differences in oxidative status between sexes. Our results suggest that incubation is a highly demanding activity compared to chick rearing in terms of oxidative balance since the lower presence of antioxidants can be explained as they have probably depleted to limit oxidative damage by ROS. Differential foraging effort could explain such results as Magellanic penguins adjust their foraging location to prey availability performing longer foraging trips during incubation than during chick rearing which increases the energy costs and therefore imbalance penguins oxidative status. Our results show the importance of examining physiological markers such as oxidative stress to assess differences during the breeding cycle and how the behaviour at sea could explain such differences in seabirds.


Breeding Period Reactive Oxygen Metabolite Magellanic Penguin Chick Rear Total Plasma Antioxidant Capacity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Export and import permits for biological samples were acquired from government authorities in both Argentina and Spain. We thank D. A. Saban and A. Medina Vanina for field assistance and laboratory advice, respectively, Dominic L. Cram for helpful comments on an early version of the paper and finally, our thanks to E. Serrano-Davies for her help drawing the maps. Deborah Fuldauer corrected the English language usage. This study was funded by the Spanish Ministry of Economy and Competitiveness (CTM2011-24427) and Multiannual Research Projects-CONICET (PIP 112-20110100680). RCC received financial aid from an FPI and a mobility grant from the Spanish Ministry of Economy and Competitiveness (BES2012-059299 and EEBB-I-14-078877), and EC has a CONICET doctoral fellowship. This study is a contribution to the PINGUCLIM project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All animal handling and experimental procedures were approved by the Office of Tourism and Protected Areas of Chubut Province and Fauna and Flora Department, Argentina.


  1. 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. doi: 10.1111/j.1461-0248.2004.00594.x CrossRefGoogle Scholar
  2. Astheimer LB, Grau CR (1985) The timing and energetic consequences of egg formation in the Adélie penguin. Condor 87:256–268. doi: 10.2307/1366891 CrossRefGoogle Scholar
  3. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483–495. doi: 10.1016/j.cell.2005.02.001 CrossRefGoogle Scholar
  4. Barbosa A, Palacios MJ, Negro JJ, Cuervo JJ (2013) Plasma carotenoid depletion during fasting in moulting penguins. J Ornithol 154:559–562. doi: 10.1007/s10336-012-0918-z CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  6. Beaulieu M, Ropert-Coudert Y, Le Maho Y, Ancel A, Criscuolo F (2010) Foraging in an oxidative environment: relationship between delta C-13 values and oxidative status in Adelie penguins. Proc R Soc B Biol Sci 277:1087–1092. doi: 10.1098/rspb.2009.1881 CrossRefGoogle Scholar
  7. 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. doi: 10.1111/j.1365-2435.2010.01825.x CrossRefGoogle Scholar
  8. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581Google Scholar
  9. Bertellotti M (2013) Magellanic penguin. Patagonian Ambassador. Vazquez Mazzini Editores, Ciudad Autónoma de Buenos AiresGoogle Scholar
  10. Bertellotti M, Tella JL, Godoy JA, Blanco G, Forero MG, Donázar JA, Ceballos O (2002) Determining sex of Magellanic penguins using molecular procedures and discriminant functions. Waterbirds 25:479–484. doi: 10.1675/1524-4695(2002)025[0479:DSOMPU]2.0.CO;2 CrossRefGoogle Scholar
  11. Butler MW, Lutz TJ, Fokidis HB, Stahlschmidt ZR (2016) Eating increases oxidative damage in a reptile. J Exp Biol. doi: 10.1242/jeb.138875 Google Scholar
  12. Catoni C, Peters A, Martin Schaefer H (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Anim Behav 76:1107–1119. doi: 10.1016/j.anbehav.2008.05.027 CrossRefGoogle Scholar
  13. 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 B Biol Sci 279:1142–1149. doi: 10.1098/rspb.2011.1546 CrossRefGoogle Scholar
  14. Cohen AA, McGraw KJ, Robinson WD (2009) Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecol 161:673–683. doi: 10.1007/s00442-009-1423-9 CrossRefGoogle Scholar
  15. Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251. doi: 10.1111/j.1461-0248.2008.01246.x Google Scholar
  16. Costantini D (2010) Effects of diet quality on serum oxidative status and body mass in male and female pigeons during reproduction. Comp Biochem Physiol A Mol Integr Physiol 156:294–299. doi: 10.1016/j.cbpa.2010.02.021 CrossRefGoogle Scholar
  17. Costantini D (2014) Oxidative stress and hormesis in evolutionary ecology and physiology. A marriage between mechanistic and evolutionary approaches. Springer, BerlinGoogle Scholar
  18. Costantini D, Dell’ariccia G, Lipp HP (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211:377–381. doi: 10.1242/jeb.012856 CrossRefGoogle Scholar
  19. 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 101:541–548. doi: 10.1007/s00114-014-1190-2 CrossRefGoogle Scholar
  20. Costantini D, Casasole G, Eens M (2014b) Does reproduction protect against oxidative stress? J Exp Biol 217:4237–4243. doi: 10.1242/jeb.114116 CrossRefGoogle Scholar
  21. Croxall JP (1982) Energy costs of incubation and moult in petrels and penguins. J Anim Ecol 51:177–194. doi: 10.2307/4318 CrossRefGoogle Scholar
  22. Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology. Wiley-Blackwell, ChicesterGoogle Scholar
  23. Davis RW, Croxall JP, O’Connell MJ (1989) The reproductive energetics of gentoo (Pygoscelis papua) and macaroni (Eudyptes chrysolophus) penguins at South Georgia. J Anim Ecol 58:59–74. doi: 10.2307/4986 CrossRefGoogle Scholar
  24. Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B Biol Sci 276:1737–1745. doi: 10.1098/rspb.2008.1791 CrossRefGoogle Scholar
  25. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247CrossRefGoogle Scholar
  26. Gaál T, Ribiczeyné-Szabó P, Stadler K, Jakus J, Reiczigel J, Kövér P, Mézes M, Sümeghy L (2006) Free radicals, lipid peroxidation and the antioxidant system in the blood of cows and newborn calves around calving. Comp Biochem Physiol B Biochem Mol Biol 143:391–396. doi: 10.1016/j.cbpb.2005.12.014 CrossRefGoogle Scholar
  27. Gales R, Green B (1990) The annual energetics cycle of Little penguins (Eudyptula minor). Ecol 71:2297–2312. doi: 10.2307/1938641 CrossRefGoogle Scholar
  28. Goodwin TW (1984) The biochemistry of the carotenoids. Volume II. Animals. Chapman and Hall, New YorkCrossRefGoogle Scholar
  29. Green JA, Boyd IL, Woakes AJ, Warren NL, Butler PJ (2009) Evaluating the prudence of parents: daily energy expenditure throughout the annual cycle of a free-ranging bird, the macaroni penguin Eudyptes chrysolophus. J Avian Biol 40:529–538. doi: 10.1111/j.1600-048X.2009.04639.x CrossRefGoogle Scholar
  30. Halliwell BH, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  31. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11(3):298–300CrossRefGoogle Scholar
  32. Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86. doi: 10.1016/j.tree.2006.10.008 CrossRefGoogle Scholar
  33. Heaney V, Monaghan P (1996) Optimal allocation of effort between reproductive phases: the trade-off between incubation costs and subsequent brood rearing capacity. Proc R Soc B Biol Sci 263:1719–1724. doi: 10.1098/rspb.1996.0251 CrossRefGoogle Scholar
  34. Hulbert AJ (2005) On the importance of fatty acid composition of membranes for aging. J Theor Biol 234:277–288. doi: 10.1016/j.jtbi.2004.11.024 CrossRefGoogle Scholar
  35. Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997. doi: 10.2307/2533558 CrossRefGoogle Scholar
  36. Kuznetsova A, Brockhoff PB, Christensen RHB (2014) lmerTest: test for random and fixed effects for linear mixed effect models. R package version 2.0-20.
  37. López-Arrabé J, Cantarero A, Pérez-Rodríguez L, Palma A, Moreno J (2014) Plumage ornaments and reproductive investment in relation to oxidative status in the Iberian Pied Flycatcher (Ficedula hypoleuca iberiae). Can J Zool 92:1019–1027. doi: 10.1139/cjz-2014-0199 CrossRefGoogle Scholar
  38. Losdat S, Helfenstein F, Gaude B, Richner H (2011) Reproductive effort transiently reduces antioxidant capacity in a wild bird. Behav Ecol 22:1218–1226. doi: 10.1093/beheco/arr116 CrossRefGoogle Scholar
  39. 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. doi: 10.1111/j.1365-2435.2010.01750.x CrossRefGoogle Scholar
  40. Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28:347–350. doi: 10.1016/j.tree.2013.01.015 CrossRefGoogle Scholar
  41. Monaghan P, Nager RG (1997) Why don’t birds lay more eggs? Trends Ecol Evol 12:270–274. doi: 10.1016/S0169-5347(97)01094-X CrossRefGoogle Scholar
  42. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92. doi: 10.1111/j.1461-0248.2008.01258.x CrossRefGoogle Scholar
  43. Moreno J, Carlson A (1989) Clutch size and the costs of incubation in the pied flycatcher Ficedula hypoleuca. Ornis Scand 20:123–128. doi: 10.2307/3676879 CrossRefGoogle Scholar
  44. Moreno J, Sanz JJ (1996) Field metabolic rates of breeding Chinstrap penguins (Pygoscelis antarctica) in the South Shetlands. Physiol Zool 69:586–598CrossRefGoogle Scholar
  45. Ołdakowski Ł, Piotrowska Ż, Chrząścik KM, Sadowska ET, Koteja P, Taylor JRE (2012) Is reproduction costly? No increase of oxidative damage in breeding bank voles. J Exp Biol 215:1799–1805. doi: 10.1242/jeb.068452 CrossRefGoogle Scholar
  46. Pájaro M, Leonarduzzi E, Hansen JE, Macchi GJ (2011) Analysis of the reproductive potential of two stocks of Engraulis anchoita in the Argentine Sea. Cienc Mar 37:603–618Google Scholar
  47. Pamplona R, Barja G (2007) Highly resistant macromolecular components and low rate of generation of endogenous damage: two key traits of longevity. Ageing Res Rev 6:189–210. doi: 10.1016/j.arr.2007.06.002 CrossRefGoogle Scholar
  48. Pastous Madureira LS, Castello JP, Prentice-Hernández C, Queiroz MI, Espírito Santo ML, Ruiz WA, Raggi Abdallah P, Hansen J, Bertolotti MI, Manca E, Yeannes MI, Avdalov N, Fernandez Amorín S (2009) Current and potential alternative food uses of the Argentine anchoita (Engraulis anchoita) in Argentina, Uruguay and Brazil. In: Hasan MR, Halwart M (eds) Fish as feed inputs for aquaculture: practices, sustainability and implications. FAO fisheries and aquaculture technical paper no 518, Rome, FAO, pp 269–287Google Scholar
  49. R Core Team (2014) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  50. Reid JM, Monaghan P, Ruxton GD (2000) Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation. Proc Biol Sci 267:37–41CrossRefGoogle Scholar
  51. Rey AR, Pütz K, Scioscia G, Lüthi B, Schiavini A (2012) Sexual differences in the foraging behaviour of Magellanic penguins related to stage of breeding. Emu 112:90–96. doi: 10.1071/MU11065 CrossRefGoogle Scholar
  52. Roff DA (1992) Evolution of life histories: theory and analysis. Chapman & Hall, LondonGoogle Scholar
  53. Sala JE, Wilson RP, Frere E, Quintana F (2012a) Foraging effort in Magellanic penguins in coastal Patagonia, Argentina. Mar Ecol Prog Ser 464:273–287. doi: 10.3354/meps09887 CrossRefGoogle Scholar
  54. Sala JE, Wilson RP, Quintana F (2012b) How much is too much? Assessment of prey consumption by Magellanic penguins in patagonian colonies. PLoS ONE. doi: 10.1371/journal.pone.0051487 Google Scholar
  55. Sala JE, Wilson RP, Frere E, Quintana F (2014) Flexible foraging for finding fish: variable diving patterns in Magellanic penguins Spheniscus magellanicus from different colonies. J Ornithol 155:801–817. doi: 10.1007/s10336-014-1065-5 CrossRefGoogle Scholar
  56. Salin K, Auer SK, Rudolf AM, Anderson GJ, Cairns AG, Mullen W, Hartley RC, Selman C, Metcalfe NB (2015) Individuals with higher metabolic rates have lower levels of reactive oxygen species in vivo. Biol Lett. doi: 10.1098/rsbl.2015.0538 Google Scholar
  57. Schull Q, Viblanc VA, Stier A, Saadaoui H, Lefol E, Criscuolo F, Bize P, Robin J-P (2016) The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins. J Exp Biol. doi: 10.1242/jeb.145250 Google Scholar
  58. Scioscia G, Rey AR, Samaniego RAS, Florentin O, Schiavini A (2014) Intra- and interannual variation in the diet of the Magellanic penguin (Spheniscus magellanicus) at Martillo Island, Beagle Channel. Polar Biol 37:1421–1433. doi: 10.1007/s00300-014-1532-8 CrossRefGoogle Scholar
  59. Selman C, Blount JD, Nussey DH, Speakman JR (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27:570–577. doi: 10.1016/j.tree.2012.06.006 CrossRefGoogle Scholar
  60. Sies H (2007) Total antioxidant capacity: appraisal of a concept. J Nutr 137:1493–1495Google Scholar
  61. Speakman JR, Garratt M (2014) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays 36:93–106. doi: 10.1002/bies.201300108 CrossRefGoogle Scholar
  62. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268. doi: 10.2307/2389364 CrossRefGoogle Scholar
  63. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  64. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nothingham University Press, NothinghamGoogle Scholar
  65. Sylvie G, Marion K, le Yvon M, Jean-Patrice R, Criscuolo F (2012) Of the importance of metabolic phases in the understanding of oxidative stress in prolonged fasting and refeeding. Physiol Biochem Zool 85:415–420. doi: 10.1086/666364 CrossRefGoogle Scholar
  66. Visser ME, Lessells CM (2001) The costs of egg production and incubation in great tits (Parus major). Proc R Soc B Biol Sci 268:1271–1277. doi: 10.1098/rspb.2001.1661 CrossRefGoogle Scholar
  67. Walker BG, Boersma PD (2003) Diving behavior of Magellanic penguins (Spheniscus magellanicus) at Punta Tombo, Argentina. Can J Zool 81:1471–1483. doi: 10.1139/z03-142 CrossRefGoogle Scholar
  68. Wegmann M, Voegeli B, Richner H (2015) Physiological responses to increased brood size and ectoparasite infestation: adult great tits favour self-maintenance. Physiol Behav 141:127–134. doi: 10.1016/j.physbeh.2015.01.017 CrossRefGoogle Scholar
  69. Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc R Soc B Biol Sci 271:S360–S363CrossRefGoogle Scholar
  70. Williams TD (1995) The penguins. Oxford University Press Inc., New YorkGoogle Scholar
  71. Wilson RP, Scolaro JA, Gremillet D, Kierspel MAM, Laurenti S, Upton J, Gallelli H, Quintana F, Frere E, Muller G, Straten MT, Zimmer I (2005) How do Magellanic Penguins cope with variability in their access to prey? Ecol Monogr 75:379–401. doi: 10.1890/04-1238 CrossRefGoogle Scholar
  72. Xu Y-C, Yang D-B, Speakman JR, Wang D-H (2014) Oxidative stress in response to natural and experimentally elevated reproductive effort is tissue dependent. Funct Ecol 28:402–410. doi: 10.1111/1365-2435.12168 CrossRefGoogle Scholar
  73. Ziomkiewicz A, Sancilio A, Galbarczyk A, Klimek M, Jasienska G, Bribiescas RG (2016) Evidence for the cost of reproduction in humans: high lifetime reproductive effort is associated with greater oxidative stress in post-menopausal women. PLoS ONE 11:e0145753. doi: 10.1371/journal.pone.0145753 CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Dpto. Ecología EvolutivaMuseo Nacional de Ciencias Naturales (CSIC)MadridSpain
  2. 2.Centro para el Estudio de Sistemas Marinos-Centro Nacional Patagónico (CONICET)Puerto MadrynArgentina

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