, Volume 177, Issue 4, pp 1211–1220 | Cite as

Relationships between isotopic values and oxidative status: insights from populations of gentoo penguins

  • Michaël Beaulieu
  • Daniel González-Acuña
  • Anne-Mathilde Thierry
  • Michael J. Polito
Physiological ecology - Original research


Feeding strategies can affect the balance between the production of reactive oxygen species and antioxidant defences (i.e. oxidative status). This is ecologically relevant, as variation in oxidative status can in turn strongly affect fitness. However, how animals regulate their oxidative status through their feeding behaviour under natural conditions remains poorly understood. Thus, relating the isotopic values of free-ranging animals to their oxidative status may prove useful. Here, we considered three colonies of gentoo penguins (Pygoscelis papua) in which we measured (1) δ13C and δ15N values, and (2) antioxidant defences and oxidative damage. We found that colonies with the highest δ13C and δ15N values also had the highest levels of antioxidant defences and oxidative damage, resulting in positive relationships between isotopic values and markers of oxidative status. As a result, colony segregation in terms of isotopic values was reflected by segregation in terms of oxidative markers (although more markedly for oxidative damage than for antioxidant defences). Interestingly, variation in the estimated contribution of krill in the diet of penguins followed an opposite pattern to that observed for markers of oxidative status, providing evidence that inter-population differences in terms of foraging strategies can result in inter-population differences in terms of oxidative status. More studies examining simultaneously oxidative status, isotopic signature, foraging behaviour and food allocation between parents and young are, however, needed to understand better the interplay between the foraging strategies adopted by animals in their natural habitat and their oxidative status.


Antarctica Diet Oxidative stress Penguins SIAR 



This work was supported by the Antarctic Science Bursary. It receives supplementary support from the Instituto Antártico Chileno (INACH), American Ornithologist Union, and Sigma Xi. We thank the US Antarctic Marine Living Resources program, Raytheon Polar Services, G. Watters, and W. Trivelpiece for providing logistical support. Animal use was conducted under approved protocols from INACH (Project T-27-10), the University of North Carolina Wilmington (A0910-20), and a US National Science Foundation Antarctic Conservation Act permit provided to G. Watters (2011-005).

Conflict of interest

The authors declare no conflict of interest.


  1. Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103. doi: 10.1038/nature02950.1 CrossRefPubMedGoogle Scholar
  2. 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
  3. Barquete V, Strauss V, Ryan PG (2013) Stable isotope turnover in blood and claws: a case study in captive African penguins. J Exp Mar Bio Ecol 448:121–127. doi: 10.1016/j.jembe.2013.06.021 CrossRefGoogle Scholar
  4. Beaulieu M, Costantini D (2014) Biomarkers of oxidative status: missing tools in conservation physiology. Conserv Physiol 2: cou14. doi: 10.1093/conphys/cou014
  5. Beaulieu M, Reichert S, Le Maho Y et al (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
  6. Beaulieu M, Ropert-Coudert Y, Le Maho Y et al (2010) Foraging in an oxidative environment: relationship between δ13C values and oxidative status in Adélie penguins. Proc R Soc Lond B 277:1087–1092. doi: 10.1098/rspb.2009.1881 CrossRefGoogle Scholar
  7. Beaulieu M, Schaefer HM (2013) Rethinking the role of dietary antioxidants through the lens of self-medication. Anim Behav 86:17–24. doi: 10.1016/j.anbehav.2013.05.022 CrossRefGoogle Scholar
  8. Beaulieu M, Sockman KW (2014) Comparison of optimal foraging versus life-history decisions during nestling care in Lincoln’s sparrows Melospiza lincolnii through stable isotope analysis. Ibis 156:424–432CrossRefGoogle Scholar
  9. Beaulieu M, Thierry A-M, González-Acuña D, Polito MJ (2013) Integrating oxidative ecology into conservation physiology. Conserv Physiol. doi: 10.1093/conphys/cot004 Google Scholar
  10. Benito MM, González-Solís J, Becker PH (2011) Carotenoid supplementation and sex-specific trade-offs between colouration and condition in common tern chicks. J Comp Physiol B 181:539–549. doi: 10.1007/s00360-010-0537-z PubMedGoogle Scholar
  11. Bize PB, Devevey G, Monaghan P et al (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89:2584–2593CrossRefPubMedGoogle Scholar
  12. Carravieri A, Bustamante P, Churlaud C, Cherel Y (2013) Penguins as bioindicators of mercury contamination in the Southern Ocean: birds from the Kerguelen Islands as a case study. Sci Total Environ 455:141–148CrossRefGoogle Scholar
  13. 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. doi: 10.1016/j.anbehav.2008.05.027 CrossRefGoogle Scholar
  14. Celis J, Jara S, González-Acuña D et al (2012) A preliminary study of trace metals and porphyrins in excreta of Gentoo penguins (Pygoscelis papua) at two locations of the Antarctic Peninsula. Arch Med Vet 44:311–316CrossRefGoogle Scholar
  15. Cherel Y (2008) Isotopic niches of emperor and Adélie penguins in Adélie Land, Antarctica. Mar Biol 154:813–821. doi: 10.1007/s00227-008-0974-3 CrossRefGoogle Scholar
  16. Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888CrossRefGoogle Scholar
  17. 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 PubMedGoogle Scholar
  18. Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370. doi: 10.1111/j.1365-2435.2007.01366.x CrossRefGoogle Scholar
  19. Costantini D, Dell’Ariccia G, Lipp H-P (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 4:377–381. doi: 10.1242/jeb.012856 CrossRefGoogle Scholar
  20. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  21. Freeman-Gallant CR, Amidon J, Berdy B et al (2011) Oxidative damage to DNA related to survivorship and carotenoid-based sexual ornamentation in the common yellow throat. Biol Lett 7:429–432. doi: 10.1098/rsbl.2010.1186 CrossRefPubMedCentralPubMedGoogle Scholar
  22. García-Tarrasón M, Sanpera C, Jover L, Costantini D (2014) Levels of antioxidants in breeding female Audouin’s gulls and their deposition in eggs across different environments. J Exp Mar Biol Ecol 453:116–122. doi: 10.1016/j.jembe.2014.01.012 CrossRefGoogle Scholar
  23. Geiger S, Le Maho Y, Kaufmann M et al (2012) Of the importance of metabolic phases in the understanding of oxidative stress in prolonged fasting and refeeding. Physiol Biochem Zool 85:1–8. doi: 10.1086/666364 CrossRefGoogle Scholar
  24. Gilmour M (2011) Physiological ecology and reproductive effort in a migratory seabird. Master’s thesis, Bucknell University, LewisburgGoogle Scholar
  25. Helfenstein F, Losdat S, Møller AP et al (2010) Sperm of colourful males are better protected against oxidative stress. Ecol Lett 13:213–222. doi: 10.1111/j.1461-0248.2009.01419.x CrossRefPubMedGoogle Scholar
  26. Hipfner JM, Dale J, McGraw KJ (2010) Yolk carotenoids and stable isotopes reveal links among environment, foraging behavior and seabird breeding success. Oecologia 163:351–360. doi: 10.1007/s00442-010-1618-0 CrossRefPubMedGoogle Scholar
  27. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602. doi: 10.1111/j.1365-2656.2011.01806.x CrossRefPubMedGoogle Scholar
  28. Jerez S, Motas M, José M et al (2011) Concentration of trace elements in feathers of three Antarctic penguins: geographical and interspecific differences. Environ Pollut 159:2412–2419. doi: 10.1016/j.envpol.2011.06.036 CrossRefPubMedGoogle Scholar
  29. Koivula MJ, Eeva T (2010) Metal-related oxidative stress in birds. Environ Pollut 158:2359–2370. doi: 10.1016/j.envpol.2010.03.013 CrossRefPubMedGoogle Scholar
  30. Lescroël A, Bost C (2005) Foraging under contrasting oceanographic conditions: the gentoo penguin at Kerguelen Archipelago. Mar Ecol Prog Ser 302:245–261CrossRefGoogle Scholar
  31. Losdat S, Helfenstein F, Blount JD et al (2013) Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird. Biol Lett 9:20120888. doi: 10.1098/rsbl.2012.0888 CrossRefPubMedCentralPubMedGoogle Scholar
  32. Miller AK, Trivelpiece WZ (2008) Chinstrap penguins alter foraging and diving behavior in response to the size of their principle prey, Antarctic krill. Mar Biol 154:201–208. doi: 10.1007/s00227-008-0909-z CrossRefGoogle Scholar
  33. Miller AK, Kappes Ma, Trivelpiece SG, Trivelpiece WZ (2010) Foraging-niche separation of breeding gentoo and chinstrap penguins, South Shetland Islands, Antarctica. Condor 112:683–695. doi: 10.1525/cond.2010.090221 CrossRefGoogle Scholar
  34. 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 CrossRefPubMedGoogle Scholar
  35. Munshi-South AJ, Wilkinson GS (2006) Diet influences life span in parrots (Psittaciformes). Auk 123:108–118CrossRefGoogle Scholar
  36. Noguera JC, Kim S-Y, Velando A (2012) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett 8:61–63. doi: 10.1098/rsbl.2011.0756 CrossRefPubMedCentralPubMedGoogle Scholar
  37. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672. doi: 10.1371/journal.pone.0009672 CrossRefPubMedCentralPubMedGoogle Scholar
  38. Polito MJ, Abel S, Tobias CR, Emslie SD (2011a) Dietary isotopic discrimination in gentoo penguin (Pygoscelis papua) feathers. Polar Biol 34:1057–1063. doi: 10.1007/s00300-011-0966-5 CrossRefGoogle Scholar
  39. Polito MJ, Trivelpiece WZ, Karnovsky NJ et al (2011b) Integrating stomach content and stable isotope analyses to quantify the diets of Pygoscelid penguins. PLoS One 6:e26642. doi: 10.1371/journal.pone.0026642 CrossRefPubMedCentralPubMedGoogle Scholar
  40. Polito MJ, Clucas GV, Hart TOM, Trivelpiece WZ (2012) A simplified method of determining the sex of Pygoscelis penguins using bill measurements. Mar Ornithol 94:89–94Google Scholar
  41. Post DM, Layman CA, Arrington DA et al (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. doi: 10.1007/s00442-006-0630-x CrossRefPubMedGoogle Scholar
  42. Quillfeldt P, McGill R, Furness R (2005) Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson’s storm-petrel. Mar Ecol Prog Ser 295:295–304. doi: 10.3354/meps295295 CrossRefGoogle Scholar
  43. Rau GH, Takahashi T, Des Marais DJ (1989) Latitudinal variations in plankton δ13C: implications for CO2 and productivity in past oceans. Nature 341:516–518CrossRefPubMedGoogle Scholar
  44. Ropert-Coudert Y, Kato A, Bost CA et al (2002) Do Adélie penguins modify their foraging behaviour in pursuit of different prey? Mar Biol 140:647–652. doi: 10.1007/s00227-001-0719-z CrossRefGoogle Scholar
  45. Saino N, Bertacche V, Bonisoli-Alquati A et al (2008) Phenotypic correlates of yolk and plasma carotenoid concentration in yellow-legged gull chicks. Physiol Biochem Zool 81:211–225. doi: 10.1086/527454 CrossRefPubMedGoogle Scholar
  46. Saino N, Caprioli M, Romano M et al (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS ONE 6:e19593. doi: 10.1371/journal.pone.0019593 CrossRefPubMedCentralPubMedGoogle Scholar
  47. Shchepinov MS (2007a) Do “‘heavy’” eaters live longer? BioEssays 29:1247–1256. doi: 10.1002/bies.20681 CrossRefPubMedGoogle Scholar
  48. Shchepinov MS (2007b) Reactive oxygen species, isotope effect, essential nutrients, and enhanced longevity. Rejuvenation Res 10:47–59. doi: 10.1089/rej.2006.0506 CrossRefPubMedGoogle Scholar
  49. Strickland ME, Polito M, Emslie SD (2008) Spatial and seasonal variation in Adélie penguin diet as inferred from stable isotope analysis of eggshell. J North Carolina Acad Sci 124:65–71Google Scholar
  50. Tou JC, Jaczynski J, Chen Y (2007) Krill for human consumption: nutritional value and potential health benefits. Nutr Rev 65:63–77. doi: 10.1301/nr.2007.feb.63 CrossRefPubMedGoogle Scholar
  51. Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1987) Ecological segregation of Adélie, gentoo, and chinstrap penguins at King George Island, Antarctica. Ecology 68:351–361CrossRefGoogle Scholar
  52. Wasser DE, Sherman PW (2010) Avian longevities and their interpretation under evolutionary theories of senescence. J Zool 280:103–155. doi: 10.1111/j.1469-7998.2009.00671.x CrossRefGoogle Scholar
  53. Wilson RP (2009) Resource partitioning and niche hyper-volume overlap in free-living Pygoscelid penguins. Funct Ecol. doi: 10.1111/j.1365-2435.2009.01654.x Google Scholar
  54. Woshner V, Knott K, Wells R et al (2008) Mercury and selenium in blood and epidermis of bottlenose dolphins (Tursiops truncatus) from Sarasota Bay, FL: interaction and relevance to life history and hematologic parameters. EcoHealth 5:360–370. doi: 10.1007/s10393-008-0164-2 CrossRefPubMedGoogle Scholar
  55. Yin X, Xia L, Sun L et al (2008) Animal excrement: a potential biomonitor of heavy metal contamination in the marine environment. Sci Total Environ 399:179–185. doi: 10.1016/j.scitotenv.2008.03.005 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Michaël Beaulieu
    • 1
  • Daniel González-Acuña
    • 2
  • Anne-Mathilde Thierry
    • 3
    • 4
  • Michael J. Polito
    • 5
  1. 1.Zoological Institute and MuseumUniversity of GreifswaldGreifswaldGermany
  2. 2.Facultad de Ciencias VeterinariasUniversidad de ConcepciónChillánChile
  3. 3.Norwegian Institute for Nature ResearchTrondheimNorway
  4. 4.Département de Biologie et Centre d’Etudes NordiquesUniversité du Québec à RimouskiRimouskiCanada
  5. 5.Department of Oceanography and Coastal SciencesLouisiana State UniversityBaton RougeUSA

Personalised recommendations