, Volume 23, Issue 8, pp 1494–1504 | Cite as

Multi-tissue analyses reveal limited inter-annual and seasonal variation in mercury exposure in an Antarctic penguin community

  • Rebecka L. BrassoEmail author
  • Michael J. Polito
  • Steven D. Emslie


Inter-annual variation in tissue mercury concentrations in birds can result from annual changes in the bioavailability of mercury or shifts in dietary composition and/or trophic level. We investigated potential annual variability in mercury dynamics in the Antarctic marine food web using Pygoscelis penguins as biomonitors. Eggshell membrane, chick down, and adult feathers were collected from three species of sympatrically breeding Pygoscelis penguins during the austral summers of 2006/2007–2010/2011. To evaluate the hypothesis that mercury concentrations in penguins exhibit significant inter-annual variation and to determine the potential source of such variation (dietary or environmental), we compared tissue mercury concentrations with trophic levels as indicated by δ15N values from all species and tissues. Overall, no inter-annual variation in mercury was observed in adult feathers suggesting that mercury exposure, on an annual scale, was consistent for Pygoscelis penguins. However, when examining tissues that reflected more discrete time periods (chick down and eggshell membrane) relative to adult feathers, we found some evidence of inter-annual variation in mercury exposure during penguins’ pre-breeding and chick rearing periods. Evidence of inter-annual variation in penguin trophic level was also limited suggesting that foraging ecology and environmental factors related to the bioavailability of mercury may provide more explanatory power for mercury exposure compared to trophic level alone. Even so, the variable strength of relationships observed between trophic level and tissue mercury concentrations across and within Pygoscelis penguin species suggest that caution is required when selecting appropriate species and tissue combinations for environmental biomonitoring studies in Antarctica.


Mercury Pygoscelis penguins Antarctica Stable isotopes Trophic level 



Funding for this research was provided by a United States National Science Foundation Office of Polar Programs grant (Grant No. ANT0739575) to S. Emslie, M. Polito, and W. Patterson. For their assistance with sample collection we thank the US Antarctic Marine Living Resources program researchers at the Admiralty Bay field camps including W. Trivelpiece, and S. Trivelpiece. We thank Raytheon Polar Services and Lockheed Martin for logistical support. D. Besic, B. Drummond, K. Durenberger, E. Guber, A. Hydrusko, T. Prokopiuk, C. Tobias and E. Unger provided helpful assistance with sample preparation and stable isotope analysis. This study was conducted under approved animal use protocols from the Institutional Animal Care and Use Committees at the University of California San Diego (S05480) and the University of North Carolina Wilmington (A0910-020) and in accordance to Antarctic Conservation Act permits provided by NSF OPP to S. Emslie (2006-001), R. Holt (2008-008) and G. Watters (2011-05).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ackerman JT, Eagles-Smith CA (2009) Integrating toxicity risk in bird eggs and chicks: using chick down feathers to estimate mercury concentrations in eggs. Environ Sci Technol 43:2166–2172CrossRefGoogle Scholar
  2. Ainley DG (2002) The Adélie penguin: bellwether of climate change. Columbia University Press, New YorkGoogle Scholar
  3. Akearok JA, Hebert CE, Braune BM, Mallory ML (2010) Inter- and intraclutch variation in egg mercury levels in marine birds species from the Canadian Arctic. Sci Total Environ 408:836–840CrossRefGoogle Scholar
  4. Anderson ORJ, Phillips RA, McDonald RA, Shore RF, McGill RAR, Bearhop S (2009) Influence of trophic position and foraging range on mercury levels within a seabird community. Mar Ecol Prog Ser 375:277–288CrossRefGoogle Scholar
  5. Barrera-Oro E (2002) The role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula. Antarct Sci 14:293CrossRefGoogle Scholar
  6. Bearhop S, Ruxton RD, Furness RW (2000) Dynamics of mercury in blood and feathers of great skuas. Eviron Toxicol Chem 19:1638–1643CrossRefGoogle Scholar
  7. Blévin P, Carravieri A, Jaeger A, Chastel O, Bustamante P, Cherel Y (2013) Wide range of mercury contamination in chicks of southern ocean seabirds. PLoS ONE 8:e54508. doi: 10.1371/journal.pone.0054508 CrossRefGoogle Scholar
  8. Blum JD, Popp BN, Drazen JC, Choy CA, Johnson MW (2013) Methylmercury production below the mixed layer in the North Pacific Ocean. Nat Geosci 6:879–884CrossRefGoogle Scholar
  9. Bond AL, Diamond AW (2008) High within-individual variation in total mercury concentration in seabird feathers. Environ Toxicol Chem 27:2375–2377CrossRefGoogle Scholar
  10. Bond AL, Diamond AW (2009) Total and methyl mercury concentrations in seabird feathers and eggs. Arch Environ Toxicol Chem 56:286–291CrossRefGoogle Scholar
  11. Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of trees wallows (Tachycineta bicolor). Ecotoxicology 17:133–141CrossRefGoogle Scholar
  12. Brasso RL, Polito MJ (2013) Trophic calculations reveal the mechanism of population-level variation in mercury concentrations between marine ecosystems: case studies of two polar seabirds. Mar Poll Bull 75:244–249CrossRefGoogle Scholar
  13. Brasso RL, Polito MJ, Lynch HJ, Naveen R, Emslie S (2012a) Penguin egg shell membranes reflect homogeneity of mercury in the marine food web surrounding the Antarctic Peninsula. Sci Total Environ 439:165–171CrossRefGoogle Scholar
  14. Brasso RL, Abel S, Polito MJ (2012b) Pattern of mercury allocation into egg components is independent of dietary exposure in Gentoo penguins. Arch Environ Contam Toxicol 62:494–501CrossRefGoogle Scholar
  15. Brasso RL, Drummond BE, Borrett SR, Chiaradia A, Polito MJ, Raya Rey A (2013) Unique pattern of molt leads to low intraindividual variation in feather mercury concentrations in penguins. Environ Toxicol Chem 32:2331–2334CrossRefGoogle Scholar
  16. Brasso RL, Lang J, Jones CD, Polito MJ (2014) Ontogenetic niche expansion influences mercury exposure in the Antarctic silverfish Pleuragramma antarcticum. Mar Ecol Prog Ser 504:253–263CrossRefGoogle Scholar
  17. Burger J, Gochfeld M (2000) Metal levels in feathers of 12 species of seabirds from Midway A toll in the northern Pacific Ocean. Sci Total Environ 257:37–52CrossRefGoogle Scholar
  18. Carravieri A, Bustamante P, Chulard 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 454–455:141–148CrossRefGoogle Scholar
  19. Choy CA, Popp BN, Kaneko J, Drazen JC (2009) The influence of depth of mercury levels in pelagic fishes and their prey. Proc Natl Acad Sci 106:13865–13869CrossRefGoogle Scholar
  20. Cossa D, Heimbürger LE, Lannuzel D, Rintoul SR, Butler ECV, Bowie AR, Averty B, Watson RJ, Remenyi T (2011) Mercury in the Southern Ocean. Geochim Cosmochim Acta 75:4037–4052CrossRefGoogle Scholar
  21. Croxall JP, Reid K, Prince PA (1999) Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Mar Ecol Prog Ser 177:115–131CrossRefGoogle Scholar
  22. Davis LS, Renner M (2003) Penguins. Yale University Press, New HavenGoogle Scholar
  23. Deniro MJ, Epstein S (1981) Influence of diet on the distribution of stable isotopes of nitrogen in animals. Geochim Cosmochim Ac 45:341–351CrossRefGoogle Scholar
  24. Evers DC, Taylor KM, Major A, Taylor RJ, Poppenga RH, Scheuhammer AM (2003) Common loon eggs as indicators of methylmercury availability in North America. Ecotoxicology 12:69–81CrossRefGoogle Scholar
  25. Evers D, Savoy L, DeSorbo C, Yates D, Hanson W, Taylor K, Siegel L, Cooley J, Bank M, Major A, Munney K, Mower B, Vogel H, Schoch N, Pokras M, Goodale W, Fair J (2008) Adverse effects from environmental mercury loads on breeding Common Loons. Ecotoxicology 17:69–81CrossRefGoogle Scholar
  26. Ferriss BE, Essington TE (2011) Regional patterns in mercury and selenium concentrations of yellowfin tuna (Thunnusalbacares) and bigeye tuna (Thunnusobesus) in the Pacific Ocean. Can J Fish Aquat Sci 68:2046–2056CrossRefGoogle Scholar
  27. Frederick PC, Spalding MG, Dusek R (2002) Wading birds as bioindicators of mercury contamination in Florida, USA: annual and geographic variation. Environ Toxicol Chem 21:163–167CrossRefGoogle Scholar
  28. Furness RW (1993) Birds as monitors of pollutants. In: Furness RW, Greenwood JJD (eds) Birds as monitors of environmental change. Chapman and Hall, London, pp 86–143CrossRefGoogle Scholar
  29. Gariboldi JC, Brian AL, Jagoe CH (2000) Annual and regional variation in mercury concentrations in wood stork nestlings. Environ Toxicol Chem 20:1551–1556CrossRefGoogle Scholar
  30. Hallinger KK, Cristol DA (2011) The role of weather in mediating the effect of mercury exposure on reproductive success in tree swallows. Ecotoxicology 20:1368–1377CrossRefGoogle Scholar
  31. Hartman CA, Ackerman JT, Herring G, Isanhart J, Herzog M (2013) Marsh wrens as bioindicators of mercury in wetlands of Great Salt Lake: do blood and feathers reflect site-specific exposure risk to bird reproduction? Environ Sci Technol 47:6597–6605Google Scholar
  32. Hobson KA, Bond AL (2012) Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses. Mar Ecol Prog Ser 461:233–243CrossRefGoogle Scholar
  33. Karnovsky NJ (1997) The fish component of Pygoscelis penguin diets. MS thesis, Montana State University, BozemanGoogle Scholar
  34. Laws RM (1985) The ecology of the Southern ocean. Am Sci 73:26–40Google Scholar
  35. Le Faucher S, Campbell PGC, Fortin C, Slaveykova VI (2013) Interactions between mercury and phytoplankton: speciation, bioavailability, and internal handling. Environ Toxicol Chem 33:1211–1224CrossRefGoogle Scholar
  36. Lynnes AS, Reid K, Croxall JP, Trathan PN (2002) Conflict or co-existence? Foraging distribution and competition for prey between Adélie and Chinstrap penguins. Mar Biol 141:1165–1174CrossRefGoogle Scholar
  37. Mason RP, Choi AL, Fitzgerald WF, Hammerschmidt CF, Lamborg CH, Soerensen AL, Sunderland EM (2012) Mercury biogeochemical cycling in the ocean and policy implications. Environ Res 119:101–117CrossRefGoogle Scholar
  38. 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 154:201–208CrossRefGoogle Scholar
  39. Miller AK, Karnovsky NJ, Trivelpiece WZ (2009) Flexible foraging strategies of gentoo penguins Pygoscelis papua over 5 years in the South Shetland Islands, Antarctica. Mar Biol 156:2527–2537CrossRefGoogle Scholar
  40. Miller AK, Kappes MA, Trivelpiece SG, Trivelpiece WZ (2010) Foraging-niche separation of breeding Gentoo and Chinstrap penguins, South Shetland Islands, Antarctica. Condor 112:683–695Google Scholar
  41. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140CrossRefGoogle Scholar
  42. Moline MA, Prézelin BB (1996) Long-term monitoring and analyses of physical factors regulating variability in coastal Antarctic phytoplankton biomass, in situ productivity and taxonomic composition over subseasonal, seasonal and interannual time scales. Mar Ecol Prog Ser 145:143–160CrossRefGoogle Scholar
  43. Montiero LR, Furness RW (1997) Accelerated increase in mercury contamination in north Atlantic mesopelagic food chains as indicated by time series of seabird feathers. Environ Toxicol Chem 16:2489–2493CrossRefGoogle Scholar
  44. Montiero LR, Costa V, Furness RW, Santos RS (1996) Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Mar Ecol Prog Ser 141:21–25CrossRefGoogle Scholar
  45. Morera M, Sanpera C, Crespo S, Jover L, Ruiz X (1997) Inter- and intraclutch variability in heavy metals and selenium levels in Audoin’s gull eggs from the Ebro Delta, Spain. Arch Environ Contam Toxicol 33:71–75CrossRefGoogle Scholar
  46. Polito MJ, Fisher S, Tobias CR, Emslie SD (2009) Tissue specific isotopic discrimination factors in Gentoo penguin (Pygoscelis papua) egg components: implications for dietary reconstruction using stable isotopes. J Exp Mar Biol Ecol 372:106–112CrossRefGoogle Scholar
  47. Polito MJ, Lynch HJ, Naveen R, Emslie SD (2011) Stable isotopes reveal regional heterogeneity in the pre-breeding distribution and diets of sympatrically breeding Pygoscelis spp. penguins. Mar Ecol Prog Ser 421:265–277CrossRefGoogle Scholar
  48. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  49. Rigét F, Braune B, Bignert A, Wilson S, Aars J, Born E, Dam M, Dietz R, Evans M, Evans T, Gamberg M, Gantner N, Green N, Gunnlaugsdóttir H, Kannan K, Letcher R, Muir D, Roach P, Sonne C, Stern G, Wiig Ø (2011) Temporal trends of Hg in Arctic biota, an update. Sci Total Environ 409:3520–3526CrossRefGoogle Scholar
  50. Scheifler R, Gauthier-Clerc M, Le Bohec C, Crini N, Cœurdassier M, Badot PM, Giraudoux P, Le Maho Y (2005) Mercury concentrations in king penguin (Aptenodytespatagonicus) feathers at Crozet Islands (sub-Antarctic): temporal trend between 1966–1974 and 2000–2001. Environ Toxicol Chem 24:125–128CrossRefGoogle Scholar
  51. Siegel V (2005) Distribution and population dynamics of Euphausia superba: a summary of recent findings. Polar Biol 29:1–22CrossRefGoogle Scholar
  52. Søreide JE, Tamelander T, Hop H, Hobson KA, Johansen I (2006) Sample preparation effects on stable C and N isotope values: a comparison of methods in Arctic marine food web studies. Mar Ecol Prog Ser 328:17–28CrossRefGoogle Scholar
  53. Stonehouse B (1967) The general biology and thermal balances of penguins. Adv Ecol Res 4:131–196CrossRefGoogle Scholar
  54. Stowasser G, Atkinson A, McGill RAR, Phillips RA, Collins MA, Pond DW (2012) Food web dynamics in the Scotia Sea in summer: a stable isotope study. Deep Sea Res II 59–60:208–221CrossRefGoogle Scholar
  55. Szczebak JT, Taylor DL (2011) Ontogenetic patterns in bluefish (Pomatomus saltatrix) feeding ecology and the effect on mercury biomagnification. Environ Toxicol Chem 30:1447–1458CrossRefGoogle Scholar
  56. Taylor JRE (1985) Ontogeny of thermoregulation and energy metabolism in pygoscelid penguin chicks. J Comp Physiol B 155:615–627CrossRefGoogle Scholar
  57. Thompson DR, Furness RW, Lewis SA (1993) Temporal and spatial variation in mercury concentrations in some albatrosses and petrels from the sub-Antarctic. Polar Biol 13:239–244CrossRefGoogle Scholar
  58. Trivelpiece WZ, Trivelpiece SG (1990) Courtship period of Adélie, gentoo and chinstrap penguins. In: Davis LS, Darby JT (eds) Penguin biology. Academic Press Inc., San Diego, pp 113–126CrossRefGoogle Scholar
  59. 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
  60. Vo AE, Bank MS, Shine JP, Edwards SV (2011) Temporal increase in organic mercury in an endangered pelagic seabird assessed by century-old museum specimens. Proc Natl Acad Sci 108:7466–7471CrossRefGoogle Scholar
  61. Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Rebecka L. Brasso
    • 1
    Email author
  • Michael J. Polito
    • 2
  • Steven D. Emslie
    • 1
  1. 1.Department of Biology and Marine BiologyUniversity of North Carolina WilmingtonWilmingtonUSA
  2. 2.Woods Hole Oceanographic InstitutionWoods HoleMA

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