Factors that influence trace element levels in blood and feathers of Pygoscelis penguins from South Shetland Islands, Antarctica

Padilha, J. A.; Carvalho, G. O.; Espejo, W.; Souza, J. S.; Pizzochero, A. C.; Cunha, L. S. T.; Costa, E. S.; Pessôa, A. R. L.; Almeida, A. P.; Torres, J. P. M.; Lepoint, Gilles; Michel, Loïc; Das, Krishna; Dorneles, P. R.

doi:10.1016/j.envpol.2021.117209

Article (Scientific journals)

Factors that influence trace element levels in blood and feathers of Pygoscelis penguins from South Shetland Islands, Antarctica

Padilha, J. A.; Carvalho, G. O.; Espejo, W. et al.

2021 • In Environmental Pollution, 284, p. 117209

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/260825

DOI
10.1016/j.envpol.2021.117209

PubMed
33932832

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

1-s2.0-S0269749121007910-main.pdf

Publisher postprint (2.09 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

stable isotopes; trace element; antarctica; penguin; pygoscelis; west antarctic peninsula

Abstract :

[en] Contaminant levels are lower in Antarctica than elsewhere in the world because of its low anthropogenic activities. However, the northern region of the Antarctic Peninsula, is close to South America and experiences the greatest anthropogenic pressure in Antarctica. Here, we investigated, in two Antarctic Peninsula islands, intra and interspecific factors that influence the concentrations of 17 trace elements (TEs) in blood and feathers of three penguin species breeding sympatrically in relation to their trophic ecology assessed via a stable isotopic approach (C, N and S). Geographical location, foraging zone (δ13C and δ34S) and diet influences the interspecific difference, and sex and maturity stage diet influence the intraspecific difference of Pygoscelis penguins. Penguins from Livingston showed higher values (mean, ng. g−1, dry weight - dw) of Zn (103), Mn (0.3), and Fe (95) than those from King George Island (Zn: 80, Mn: 1.9, and Fe: 11). Gender-related differences were observed, as males showed significantly higher values (mean, ng. g−1, dw) of Rb (3.4) and δ15N in blood of gentoo, and Ca (1344) in Adélie feathers. Chicks of gentoo and Adélie presented higher Zn, Mg, Ca, and Sr and lower 13C values in blood than adults. The highest concentrations (mean, ng. g−1, dw) of Cd (0.2) and Cu (26), and the lowest δ15N values were found in chinstrap. Geographical, intraspecific (i.e., ontogenetic and gender-related) and interspecific differences in feeding seemed to have influenced TE and stable isotope values in these animals. The TE bioaccumulation by penguins may have also been influenced by natural enrichment in environmental levels of these elements, which seems to be the case for Fe, Zn, and Mn. However, the high level of some of the TEs (Mn, Cd, and Cr) may reflect the increase of local and global human activities.

Research Center/Unit :

MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège

Disciplines :

Environmental sciences & ecology
Zoology
Aquatic sciences & oceanology

Author, co-author :

Padilha, J. A.

Carvalho, G. O.

Espejo, W.

Souza, J. S.

Pizzochero, A. C.

Cunha, L. S. T.

Costa, E. S.

Pessôa, A. R. L.

Almeida, A. P.

Torres, J. P. M.

More authors (4 more)

Language :

English

Title :

Factors that influence trace element levels in blood and feathers of Pygoscelis penguins from South Shetland Islands, Antarctica

Publication date :

01 September 2021

Journal title :

Environmental Pollution

ISSN :

0013-9327

Publisher :

Applied Science Publishers, United Kingdom

Volume :

284

Pages :

117209

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
WBI - Wallonie-Bruxelles International
CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico
CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior
FAPERJ - Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro

Available on ORBi :

since 09 June 2021

Statistics

Number of views

177 (14 by ULiège)

Number of downloads

173 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abrams, R.W., Energy and food requirements of pelagic aerial seabirds in different regions of the african sector of the Southern Ocean. Siegfried, W.R., Condy, P.R., Laws, R.M., (eds.) Antarctic Nutrient Cycles and Food Webs, 1985, Springer, Berlin, Heidelberg, 466–472, 10.1007/978-3-642-82275-9_65.
Almendros, J., et al. Array tracking of the volcanic tremor source at Deception Island, Antarctica. Geophys. Res. Lett. 24 (1997), 3069–3072.
Bargagli, R., Environmental contamination in Antarctic ecosystems. Sci. Total Environ. 400 (2008), 212–226, 10.1016/j.scitotenv.2008.06.062.
Bargagli, R., Nelli, L., Ancora, S., Focardi, S., Elevated cadmium accumulation in marine organisms from Terra Nova Bay (Antarctica). Polar Biol. 16 (1996), 513–520, 10.1007/BF02329071.
Bearhop, S., Phillips, R.A., McGill, R., Cherel, Y., Dawson, D.A., Croxall, J.P., Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar. Ecol. Prog. Ser. 311 (2006), 157–164, 10.3354/meps311157.
Bengtson Nash, S., Rintoul, S., Staniland, I., Van den Hoff, J., Tierney, M., Bossi, R., Perfluorinated compounds in the Antarctic region: ocean circulation provides prolonged protection from distant sources. Environ. Pollut. Barking Essex 1987:158 (2010), 2985–2991, 10.1016/j.envpol.2010.05.024.
Burger, J., Metals in avian feathers: bioindicators of environmental pollution. Rev Env. Toxicol 5 (1993), 203–311.
Burger, J., Gochfeld, M., Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci. Total Environ. 257 (2000), 37–52, 10.1016/S0048-9697(00)00496-4.
Campbell, Linda M., et al. Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci. Total Environ. 351-352 (2005), 247–263, 10.1016/j.scitotenv.2005.02.043.
Carravieri, A., Cherel, Y., Blévin, P., Brault-Favrou, M., Chastel, O., Bustamante, P., Mercury exposure in a large subantarctic avian community. Environ. Pollut. 190 (2014), 51–57, 10.1016/j.envpol.2014.03.017.
Celis, José, et al. A preliminary study of trace metals and porphyrins in excreta of Gentoo penguins (Pygoscelis papua) at two locations of the Antarctic Peninsula. Archivos de medicina veterinaria 44 (2012), 311–316, 10.4067/S0301-732X2012000300016.
Celis, José, et al. Trace element concentrations in biotic matrices of gentoo penguins (Pygoscelis papua) and coastal soils from different locations of the Antarctic Peninsula. Water, Air, Soil Pollut. 226 (2015), 1–12, 10.1007/s11270-014-2266-5.
Celis, J.E., Barra, R., Espejo, W., González-Acuña, D., Jara, S., Trace element concentrations in biotic matrices of gentoo penguins (Pygoscelis papua) and coastal soils from different locations of the antarctic peninsula. Water, Air, Soil Pollut., 226, 2014, 2266, 10.1007/s11270-014-2266-5.
Colominas-Ciuró, R., Santos, M., Coria, N., Barbosa, A., Sex-specific foraging strategies of Adélie penguins (Pygoscelis adeliae): females forage further and on more krill than males in the Antarctic Peninsula. Polar Biol. 41 (2018), 2635–2641, 10.1007/s00300-018-2395-1.
Connolly, R.M., Guest, M.A., Melville, A.J., Oakes, J.M., Sulfur stable isotopes separate producers in marine food-web analysis. Oecologia 138 (2004), 161–167.
Das, K., Malarvannan, G., Dirtu, A., Dulau, V., Dumont, M., Lepoint, G., Mongin, P., Covaci, A., Linking pollutant exposure of humpback whales breeding in the Indian Ocean to their feeding habits and feeding areas off Antarctica. Environ. Pollut. 220 (2017), 1090–1099, 10.1016/j.envpol.2016.11.032.
Data & Statistics - Iaato [WWW Document], n.d. URL https://iaato.org/information-resources/data-statistics/(accessed 3.2.21).
Davis, L.S., Darby, J.T., Penguin Biology. 2012, Elsevier.
Deheyn, D.D., Gendreau, P., Baldwin, R.J., Latz, M.I., Evidence for enhanced bioavailability of trace elements in the marine ecosystem of Deception Island, a volcano in Antarctica. Mar. Environ. Res. 60 (2005), 1–33, 10.1016/j.marenvres.2004.08.001.
Dobaradaran, S., Soleimani, F., Nabipour, I., Saeedi, R., Mohammadi, M.J., Heavy metal levels of ballast waters in commercial ships entering Bushehr port along the Persian Gulf. Mar. Pollut. Bull. 126 (2018), 74–76, 10.1016/j.marpolbul.2017.10.094.
Einoder, L.D., MacLeod, C.K., Coughanowr, C., Metal and isotope analysis of bird feathers in a contaminated estuary reveals bioaccumulation, biomagnification, and potential toxic effects. Arch. Environ. Contam. Toxicol. 75 (2018), 96–110, 10.1007/s00244-018-0532-z.
Espejo, W., Celis, J.E., GonzÃlez-Acuña, D., Banegas, A., Barra, R., Chiang, G., A global overview of exposure levels and biological effects of trace elements in penguins. Reviews of Environmental Contamination and Toxicology Volume 245, Reviews of Environmental Contamination and Toxicology, 2017, Springer, Cham, 1–64, 10.1007/398_2017_5.
Evers, David C., et al. Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17 (2008), 69–81, 10.1007/s10646-007-0168-7.
Fenstad, A.A., Bustnes, J.O., Lierhagen, S., Gabrielsen, K.M., Öst, M., Jaatinen, K., Hanssen, S.A., Moe, B., Jenssen, B.M., Krøkje, Å., Blood and feather concentrations of toxic elements in a Baltic and an Arctic seabird population. Mar. Pollut. Bull. 114 (2017), 1152–1158, 10.1016/j.marpolbul.2016.10.034.
Finger, Annett, et al. Metals and metalloids in Little Penguin (Eudyptula minor) prey, blood and faeces. Environ. Pollut. 223 (2017), 567–574, 10.1016/j.envpol.2017.01.059.
Fromant, A., Carravieri, A., Bustamante, P., Labadie, P., Budzinski, H., Peluhet, L., Churlaud, C., Chastel, O., Cherel, Y., Wide range of metallic and organic contaminants in various tissues of the Antarctic prion, a planktonophagous seabird from the Southern Ocean. Sci. Total Environ. 544 (2016), 754–764, 10.1016/j.scitotenv.2015.11.114.
Gorman, K.B., Williams, T.D., Fraser, W.R., Ecological sexual dimorphism and environmental variability within a community of antarctic penguins (genus Pygoscelis). PloS One, 9, 2014, e90081, 10.1371/journal.pone.0090081.
Griffiths, R., Double, M.C., Orr, K., Dawson, R.J.G., A DNA test to sex most birds. Mol. Ecol. 7 (1998), 1071–1075, 10.1046/j.1365-294x.1998.00389.x.
Herman, R.W., Valls, F.C.L., Hart, T., Petry, M.V., Trivelpiece, W.Z., Polito, M.J., Seasonal consistency and individual variation in foraging strategies differ among and within Pygoscelis penguin species in the Antarctic Peninsula region. Mar. Biol., 164, 2017, 115, 10.1007/s00227-017-3142-9.
Hong, S.-M., Lluberas, A., Lee, G.-W., Park, J.-K., Natural and anthropogenic heavy metal deposition to the snow in king George island, antarctic peninsula. Ocean Polar Res. 24 (2002), 279–287, 10.4217/OPR.2002.24.3.279.
Hur, S.D., Cunde, X., Hong, S., Barbante, C., Gabrielli, P., Lee, K., Boutron, C.F., Ming, Y., Seasonal patterns of heavy metal deposition to the snow on Lambert Glacier basin, East Antarctica. Atmos. Environ. 41 (2007), 8567–8578, 10.1016/j.atmosenv.2007.07.012.
Jackson, A.L., et al. Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol. 80 (2011), 595–602, 10.1111/j.1365-2656.2011.01806.x.
Janssens, Ellen, et al. Heavy metals and selenium in feathers of great tits (Parus major) along a pollution gradient. Environ. Toxicol. Chem.: Int. J., 2001, 2815–2820, 10.1002/etc.5620201221.
Jennings, S., Varsani, A., Dugger, K.M., Ballard, G., Ainley, D.G., Sex-based differences in adélie penguin (Pygoscelis adeliae) chick growth rates and diet. PloS One, 11, 2016, e0149090, 10.1371/journal.pone.0149090.
Jerez, S., Motas, M., Benzal, J., Diaz, J., Barbosa, A., Monitoring trace elements in antarctic penguin chicks from South Shetland islands, Antarctica. Mar. Pollut. Bull. 69 (2013), 67–75, 10.1016/j.marpolbul.2013.01.004.
Jerez, S., Motas, M., Benzal, J., Diaz, J., Vidal, V., D'Amico, V., Barbosa, A., Distribution of metals and trace elements in adult and juvenile penguins from the Antarctic Peninsula area. Environ. Sci. Pollut. Res. 20 (2013), 3300–3311, 10.1007/s11356-012-1235-z.
Jerez, S., Motas, M., Palacios, M.J., Valera, F., Cuervo, J.J., Barbosa, A., Concentration of trace elements in feathers of three Antarctic penguins: geographical and interspecific differences. Environ. Pollut., Nitrogen Deposition, Critical Loads and Biodiversity 159 (2011), 2412–2419, 10.1016/j.envpol.2011.06.036.
Jiankan, H., Zichu, X., Fengnian, D., Wanchang, Z., Volcanic eruptions recorded in an ice core from collins ice cap, king George island, Antarctica. Ann. Glaciol. 29 (1999), 121–125, 10.3189/172756499781821139.
Kakareka, S., Kukharchyk, T., Kurman, P., Study of trace elements in the surface snow for impact monitoring in Vecherny Oasis, East Antarctica. Environ. Monit. Assess., 192, 2020, 725, 10.1007/s10661-020-08682-8.
Kelly, Jeffrey F., Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 78 (2000), 1–27, 10.1139/z99-165.
Marques, R. C, et al. Maternal mercury exposure and neuro-motor development in breastfed infants from Porto Velho (Amazon), Brazil. Int. J. Hyg Environ. Health 210 (2007), 51–60, 10.1016/j.ijheh.2006.08.001.
Metcheva, R., Yurukova, L., Bezrukov, V., Beltcheva, M., Yankov, Y., Dimitrov, K., Trace and toxic elements accumulation in food chain representatives at Livingston Island (Antarctica). Int. J. Biol., 2, 2010, 155.
Metcheva, R., Yurukova, L., Teodorova, S., Nikolova, E., The penguin feathers as bioindicator of Antarctica environmental state. Sci. Total Environ. 362 (2006), 259–265, 10.1016/j.scitotenv.2005.05.008.
Miller, A.K., Kappes, M.A., Trivelpiece, S.G., Trivelpiece, W.Z., Foraging-Niche Separation of Breeding Gentoo and Chinstrap Penguins, South Shetland Islands, AntarcticaSeparación de Nicho de Forrajeo durante el Periodo de Cría en los Pingüinos Pygoscelis papua y P. Antarctica, en las Islas Shetland del Sur, Antártica. Condor 112 (2010), 683–695, 10.1525/cond.2010.090221.
Nash, S.B, Persistent organic pollutants in Antarctica: current and future research priorities. J. Environ. Monit, 2011, 497–504, 10.1039/C0EM00230E.
Newman, S.H., et al. Hematological and plasma biochemical reference ranges of Alaskan seabirds: their ecological significance and clinical importance. Colon. Waterbirds 20 (1997), 492–504, 10.2307/1521600.
Nordberg, G.F., Fowler, B.A., Nordberg, M., Handbook on the Toxicology of Metals. 2014, Academic Press.
Nygård, T., Lie, E., Røv, N., Steinnes, E., Metal dynamics in an antarctic food chain. Mar. Pollut. Bull. 42 (2001), 598–602, 10.1016/S0025-326X(00)00206-X.
Padilha, J.D.A., Da Cunha, L.S.T., De Castro, R.M., Malm, O., Dorneles, P.R., Exposure of magnificent frigatebird (Fregata magnificens) and Brown booby (Sula leucogaster) to metals and selenium in Rio de Janeiro state (Brazil) coastal waters. Orbital - Electron. J. Chem. 10 (2018), 254–261, 10.17807/orbital.v10i2.1050.
Pizzochero, A.C., et al. Use of multielement stable isotope ratios to investigate ontogenetic movements of Micropogonias furnieri in a tropical Brazilian estuary. Can. J. Fish. Aquat. Sci. 75 (2017), 977–986, 10.1139/cjfas-2017-0148.
Planchon, F.A.M., Boutron, C.F., Barbante, C., Cozzi, G., Gaspari, V., Wolff, E.W., Ferrari, C.P., Cescon, P., Changes in heavy metals in Antarctic snow from Coats Land since the mid-19th to the late-20th century. Earth Planet Sci. Lett. 200 (2002), 207–222, 10.1016/S0012-821X(02)00612-X.
Polito, M.J., Brasso, R.L., Trivelpiece, W.Z., Karnovsky, N., Patterson, W.P., Emslie, S.D., Differing foraging strategies influence mercury (Hg) exposure in an Antarctic penguin community. Environ. Pollut. 218 (2016), 196–206, 10.1016/j.envpol.2016.04.097.
Polito, M.J., Trivelpiece, W.Z., Patterson, W.P., Karnovsky, N.J., Reiss, C.S., Emslie, S.D., Contrasting specialist and generalist patterns facilitate foraging niche partitioning in sympatric populations of Pygoscelis penguins. Mar. Ecol. Prog. Ser. 519 (2015), 221–237, 10.3354/meps11095.
R Core Team, R: A Language and Environment for Statistical Computing. 2019, R Foundation for Statistical Computing.
Tierney, Megan, et al. Evaluating and using stable-isotope analysis to infer diet composition and foraging ecology of Adélie penguins Pygoscelis adeliae. Mar. Ecol.: Prog. Ser. 355 (2008), 297–307, 10.3354/meps07235.
Tin, T., Fleming, Z.L., Hughes, K.A., Ainley, D.G., Convey, P., Moreno, C.A., Pfeiffer, S., Scott, J., Snape, I., Impacts of local human activities on the Antarctic environment. Antarct. Sci. 21 (2009), 3–33, 10.1017/S0954102009001722.
Trivelpiece, W.Z., Trivelpiece, S.G., Volkman, N.J., Ecological segregation of adelie, gentoo, and chinstrap penguins at king George island, Antarctica. Ecology 68 (1987), 351–361, 10.2307/1939266.
Vanderklift, Mathew A., Ponsard, Sergine, Sources of variation in consumer-diet d15N enrichment: a meta-analysis. Oecologia 136 (2003), 169–182, 10.1007/s00442-003-1270-z.
Volkman, N.J., et al. Diets of pygoscelid penguins at King George Island, Antarctica. Condor, 1980, 373–378.
Walsh, P.M., The use of seabirds as monitors of heavy metals in the marine environment. Heavy Met. Mar. Environ. 10 (1990), 183–204.
Wang, W.-X., Chapter 4 - bioaccumulation and biomonitoring. Blasco, J., Chapman, P.M., Campana, O., Hampel, M., (eds.) Marine Ecotoxicology, 2016, Academic Press, 99–119, 10.1016/B978-0-12-803371-5.00004-7.
Xavier, J.C., Trathan, P.N., Ceia, F.R., Tarling, G.A., Adlard, S., Fox, D., Edwards, E.W.J., Vieira, R.P., Medeiros, R., Broyer, C.D., Cherel, Y., Sexual and individual foraging segregation in Gentoo penguins Pygoscelis papua from the Southern Ocean during an abnormal winter. PloS One, 12, 2017, e0174850, 10.1371/journal.pone.0174850.