Abstract
Mercury emissions have increased over the past decades affecting even remote areas such as Antarctica. As gentoo penguins (Pygoscelis papua) breed on many of the islands surrounding Antarctica, foraging close to their colonies, their mercury load should reflect concentrations in the region. We therefore evaluated mercury concentrations in adult gentoo penguin feathers at Bird Island, South Georgia. We found no significant differences in mercury levels between 2009 and 2010 (mean ± SD 0.97 ± 0.67 mg kg−1, mean ± SD 1.13 ± 0.62 mg kg−1, respectively). Stable nitrogen isotope values in feathers indicated that feeding habits had a stronger influence on male mercury concentrations, whereas stable carbon isotope values indicated that foraging habitat had a stronger influence on females. Though no temporal variation in levels of mercury in gentoo penguin feathers was observed, spatial differences were evident when compared with previous studies. Our results could have implications for other animals higher in the food web that prey upon gentoo penguins, with potential consequential effects on their reproduction and development.
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Ancora S, Volpi V, Olmastroni S et al (2002) Assumption and elimination of trace elements in Adélie penguins from Antarctica: a preliminary study. Mar Environ Res 54:341–344
Anderson O, Phillips R, McDonald R et al (2009) Influence of trophic position and foraging range on mercury levels within a seabird community. Mar Ecol Prog Ser 375:277–288. doi:10.3354/meps07784
Bargagli R (2008) Environmental contamination in Antarctic ecosystems. Sci Total Environ 400:212–226. doi:10.1016/j.scitotenv.2008.06.062
Bearhop S, Phillips R, McGill R et al (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164. doi:10.3354/meps311157
Becker PH, González-solís J, Behrends B, Croxall J (2002) Feather mercury levels in seabirds at South Georgia: influence of trophic position, sex and age. Mar Ecol Prog Ser 243:261–269
Berrow SD, Taylor RI, Murray AW (1999) Influence of sampling protocol on diet determination of gentoo penguins Pygoscelis papua and Antarctic fur seals Arctocephalus gazella. Polar Biol 22:156–163. doi:10.1007/s003000050405
Blévin P, Carravieri A, Jaeger A et al (2013) Wide range of mercury contamination in chicks of southern ocean seabirds. PLoS One. doi:10.1371/journal.pone.0054508
Bocher P, Caurant F, Miramand P et al (2003) Influence of the diet on the bioaccumulation of heavy metals in zooplankton-eating petrels at Kerguelen archipelago, Southern Indian Ocean. Polar Biol 26:759–767. doi:10.1007/s00300-003-0552-6
Bond AL, Diamond AW (2009) Mercury concentrations in seabird tissues from Machias Seal Island, New Brunswick, Canada. Sci Total Environ 407:4340–4347. doi:10.1016/j.scitotenv.2009.04.018
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 Pollut Bull 75:244–249. doi:10.1016/j.marpolbul.2013.08.003
Brasso RL, Abel S, Polito MJ (2012) Pattern of mercury allocation into egg components is independent of dietary exposure in Gentoo penguins. Arch Environ Contam Toxicol 62:494–501. doi:10.1007/s00244-011-9714-7
Brasso RL, Drummond BE, Borrett SR et al (2013) Unique pattern of molt leads to low intraindividual variation in feather mercury concentrations in penguins. Environ Toxicol Chem 32:2331–2334. doi:10.1002/etc.2303
Brasso RL, Polito MJ, Emslie SD (2014) Multi-tissue analyses reveal limited inter-annual and seasonal variation in mercury exposure in an Antarctic penguin community. Ecotoxicology 23:1494–1504. doi:10.1007/s10646-014-1291-x
Braune BM, Mallory ML, Gilchrist HG (2006) Elevated mercury levels in a declining population of ivory gulls in the Canadian Arctic. Mar Pollut Bull 52:978–982. doi:10.1016/j.marpolbul.2006.04.013
Braune B, Chételat J, Amyot M et al (2015) Mercury in the marine environment of the Canadian Arctic: review of recent findings. Sci Total Environ 509–510:67–90. doi:10.1016/j.scitotenv.2014.05.133
Burnham KP, Anderson DR (2002) Chapter 2. Information and likelihood theory : a basis for model selection and inference. In: Burnham KP, Anderson DR (eds) Model sel. multimodel inference. Springer, New York, pp 49–57
Bustamante P, Bocher P, Chérel Y et al (2003) Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands. Sci Total Environ 313:25–39. doi:10.1016/S0048-9697(03)00265-1
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 454–455:141–148. doi:10.1016/j.scitotenv.2013.02.060
Carravieri A, Bustamante P, Churlaud C et al (2014a) Moulting patterns drive within-individual variations of stable isotopes and mercury in seabird body feathers: implications for monitoring of the marine environment. Mar Biol 161:963–968. doi:10.1007/s00227-014-2394-x
Carravieri A, Cherel Y, Blévin P et al (2014b) Mercury exposure in a large subantarctic avian community. Environ Pollut 190:51–57. doi:10.1016/j.envpol.2014.03.017
CCAMLR (2014) Ecosystem monitoring program: standard methods. Commission for the Conservation of Antarctic Marine Living Resources, Tasmania, pp 1–233
Cherel Y, Hobson K (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287
Cherel Y, Jaeger A, Alderman R et al (2013) A comprehensive isotopic investigation of habitat preferences in nonbreeding albatrosses from the Southern Ocean. Ecography 36:277–286. doi:10.1111/j.1600-0587.2012.07466.x
Condon A, Cristol D (2009) Feather growth influences blood mercury level of young songbirds. Environ Toxicol Chem 28:395–401. doi:10.1897/08-094.1
Cossa D, Heimbu L, Lannuzel D et al (2011) Mercury in the Southern Ocean. Geochim Cosmochim Acta 75:4037–4052. doi:10.1016/j.gca.2011.05.001
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 177:115–131. doi:10.3354/meps177115
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
Dietz R, Outridge PM, Hobson KA (2009) Anthropogenic contributions to mercury levels in present-day Arctic animals-A review. Sci Total Environ 407:6120–6131. doi:10.1016/j.scitotenv.2009.08.036
Fitzgerald WF, Lamborg CH, Hammerschmidt CR (2007) Marine biogeochemical cycling of mercury. Chem Rev 107:641–662. doi:10.1021/cr050353m
Frias JE, Gil MN, Esteves JL et al (2012) Mercury levels in feathers of Magellanic penguins. Mar Pollut Bull 64:1265–1269. doi:10.1016/j.marpolbul.2012.02.024
Goutte A, Barbraud C, Meillère A et al (2014a) Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross. Proc R Soc B. doi:10.1098/rspb.2013.3313
Goutte A, Bustamante P, Barbraud C et al (2014b) Demographic responses to mercury exposure in two closely related antarctic top predators. Ecology 95:1075–1086. doi:10.1890/13-1229.1
Grecian WJ, McGill RAR, Phillips RA et al (2015) Quantifying variation in δ13C and δ15N isotopes within and between feathers and individuals: is one sample enough? Mar Biol 162:733–741. doi:10.1007/s00227-015-2618-8
Griffiths R, Double MC, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075. doi:10.1046/j.1365-294x.1998.00389.x
Hallanger IG, Warner NA, Ruus A et al (2011) Seasonality in contaminant accumulation in Arctic marine pelagic food webs using trophic magnification factor as a measure of bioaccumulation. Environ Toxicol Chem 30:1026–1035. doi:10.1002/etc.488
Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461. doi:10.1111/j.1474-919X.2008.00839.x
Jouventin P (1982) Visual and vocal signals in penguins, their evolution and adaptive characters. Verlag Paul Parey, Berlin
Kojadinovic J, Bustamante P, Churlaud C et al (2007) Mercury in seabird feathers: insight on dietary habits and evidence for exposure levels in the western Indian Ocean. Sci Total Environ 384:194–204. doi:10.1016/j.scitotenv.2007.05.018
Lescroël A, Bost CA (2005) Foraging under contrasting oceanographic conditions: the gentoo penguin at Kerguelen Archipelago. Mar Ecol Prog Ser 302:245–261. doi:10.3354/meps302245
Lescroël A, Ridoux V, Bost CA (2004) Spatial and temporal variation in the diet of the gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol 27:206–216. doi:10.1007/s00300-003-0571-3
Lescroël A, Bajzak C, Bost CA (2009) Breeding ecology of the gentoo penguin Pygoscelis papua at Kerguelen Archipelago. Polar Biol 32:1495–1505. doi:10.1007/s00300-009-0647-9
Mão de Ferro A, Mota AM, Canário J (2014) Pathways and speciation of mercury in the environmental compartments of Deception Island, Antarctica. Chemosphere 95:227–233. doi:10.1016/j.chemosphere.2013.08.081
Metcheva R, Yurukova L, Teodorova S, Nikolova E (2006) The penguin feathers as bioindicator of Antarctica environmental state. Sci Total Environ 362:259–265. doi:10.1016/j.scitotenv.2005.05.008
Metcheva R, Yurukova L, Teodorova SE (2011) Biogenic and toxic elements in feathers, eggs, and excreta of Gentoo penguin (Pygoscelis papua ellsworthii) in the Antarctic. Environ Monit Assess 182:571–585. doi:10.1007/s10661-011-1898-9
Monteiro LR, Furness RW (1995) Seabirds as monitors of mercury in the marine environment. Water Air Soil Pollut 54:851–870
Nygård T, Lie E, Røv N, Steinnes E (2001) Metal dynamics in an Antarctic food chain. Mar Pollut Bull 42:598–602
Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Mar Biol 158:2199–2208. doi:10.1007/s00227-011-1725-4
Pinheiro J, Bates D, DebRoy S, et al (2013) nlme: linear and nonlinear mixed effects models. R Packag. version 3, pp 1-113. http://cran.r-project.org/web/packages/nlme/index.html. Accessed 15 Nov 2014
Polito MJ, Trivelpiece WZ, Karnovsky NJ et al (2011) Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins. PLoS One. doi:10.1371/journal.pone.0026642
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical computing. http://web.mit.edu/r/r_v3.0.1/fullrefman.pdf. Accessed 3 Dec 2013
Ramos R, González-Solís J (2012) Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10:258–266. doi:10.1890/110140
Ratcliffe N, Trathan P (2011) A review of the diet and at-sea distribution of penguins breeding within the CAMLR convention area. CCAMLR Sci 18:75–114
Robinson SA, Lajeunesse MJ, Forbes MR (2012) Sex differences in mercury contamination of birds: testing multiple hypotheses with meta-analysis. Environ Sci Technol 46:7094–7101. doi:10.1021/es204032m
Santos I, Silva-filho E, Schaefer C et al (2006) Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ Pollut 140:304–311. doi:10.1016/j.envpol.2005.07.007
Scheuhammer A, Braune B, Chan HM et al (2015) Recent progress on our understanding of the biological effects of mercury in fish and wildlife in the Canadian Arctic. Sci Total Environ 509–510:91–103. doi:10.1016/j.scitotenv.2014.05.142
Stewart F, Phillips R, Bartle J et al (1999) Influence of phylogeny, diet, moult schedule and sex on heavy metal concentrations in New Zealand Procellariiformes. Mar Ecol Prog Ser 178:295–305
Streets D, Zhang Q, Wu Y (2009) Projections of global mercury emissions in 2050. Environ Sci Technol 43:2983–2988
Tanton JL, Reid K, Croxall JP, Trathan PN (2004) Winter distribution and behaviour of gentoo penguins Pygoscelis papua at South Georgia. Polar Biol 27:299–303. doi:10.1007/s00300-004-0592-6
Tavares S, Xavier JC, Phillips RA et al (2013) Influence of age, sex and breeding status on mercury accumulation patterns in the wandering albatross Diomedea exulans. Environ Pollut 181:315–320. doi:10.1016/j.envpol.2013.06.032
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 13:239–244
Trathan PN, García-Borboroglu P, Boersma D et al (2014) Pollution, habitat loss, fishing, and climate change as critical threats to penguins. Conserv Biol 29:31–41. doi:10.1111/cobi.12349
UNEP (2013) Global Mercury Assessment 2013: sources, emissions, releases and environmental transport. UNEP Chemicals Branch, Geneva
Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for {PCR}—based typing from forensic material. Biotechniques 10:506–513. doi:10.2144/000113897
Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J Field Ornithol 55:109–111. doi:10.2307/4512864
Winder VL, Michaelis AK, Emslie SD (2012) Understanding associations between nitrogen and carbon isotopes and mercury in three Ammodramus sparrows. Sci Total Environ 419:54–59. doi:10.1016/j.scitotenv.2012.01.003
Xavier JC, Croxall JP, Reid K (2003) Interannual variation in the diets of two albatross species breeding at South Georgia: implications for breeding performance. Ibis 145:593–610. doi:10.1046/j.1474-919X.2003.00196.x
Zuur A, Ieno E, Smith G (2007) Analysing ecological data. doi:10.1007/978-0-387-45972-1
Acknowledgments
This work contributes to the BAS Ecosystems programme. The work was sponsored by the Foundation for Science and Technology (FCT; Portugal) under the project POLAR, within the Portuguese Polar Program PROPOLAR, and a postdoctoral grant to Filipe R. Ceia (SFRH/BPD/95372/2013), and part of the international programs ICED (Integrating climate and ecosystem dynamics of the Southern Ocean) and SCAR-AnT-ERA (Antarctic Thresholds, ecosystem resilience and adaptation of the Scientific committee for Antarctic Research) and of the SCAR EGBAMM (expert group on Birds and Antarctic marine mammals of SCAR).
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Pedro, S., Xavier, J.C., Tavares, S. et al. Mercury accumulation in gentoo penguins Pygoscelis papua: spatial, temporal and sexual intraspecific variations. Polar Biol 38, 1335–1343 (2015). https://doi.org/10.1007/s00300-015-1697-9
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DOI: https://doi.org/10.1007/s00300-015-1697-9