Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-12T21:03:57.148Z Has data issue: false hasContentIssue false
  • English
  • Français

Persistent organic pollutants and porphyrin levels in excreta of penguin colonies from the Antarctic Peninsula area

Published online by Cambridge University Press:  19 September 2016

Solange Jara-Carrasco ,
Ricardo Barra ,
Winfred Espejo ,
José E. Celis ,
Daniel González-Acuña ,
Gustavo Chiang  and
Juan Sánchez-Hernández
Solange Jara-Carrasco
Affiliation:
Department of Aquatic Systems, Faculty of Environmental Sciences and EULA-Chile Centre, Universidad de Concepción, Box 160C, Concepción, Chile.
Ricardo Barra
Affiliation:
Department of Aquatic Systems, Faculty of Environmental Sciences and EULA-Chile Centre, Universidad de Concepción, Box 160C, Concepción, Chile.
Winfred Espejo
Affiliation:
Department of Aquatic Systems, Faculty of Environmental Sciences and EULA-Chile Centre, Universidad de Concepción, Box 160C, Concepción, Chile.
José E. Celis
Affiliation:
Department of Animal Science, Faculty of Veterinary Sciences, Universidad de Concepción, Box 537, Chillán, Chile ([email protected])
Daniel González-Acuña
Affiliation:
Department of Animal Science, Faculty of Veterinary Sciences, Universidad de Concepción, Box 537, Chillán, Chile ([email protected])
Gustavo Chiang
Affiliation:
Melimoyu Ecosystem Research Institute, Lo Beltrán 2347 Vitacura, Santiago, Chile
Juan Sánchez-Hernández
Affiliation:
Ecotoxicology Laboratory, Faculty of Environmental Science and Biochemistry, Universidad de Castilla-La Mancha, Toledo, Spain
Get access Rights & Permissions [Opens in a new window]

Abstract

Persistent organic pollutants (POPs) and their effects on Antarctic seabirds by using excreta as a non-destructive biomonitoring tool have received little consideration. Here we determine the levels of polychlorinated biphenyls (PCBs) and some organochlorine pesticides such as dichlorodiphenyltrichloroethanes (DDTs), hexachlorobencene (HCB), heptachlor, and endrin aldehyde in penguin excreta. Animal exposure to these environmental contaminants was determined through porphyrins in penguin droppings. Stool samples of Adélie penguin (Pygoscelis adeliae), chinstrap penguin (Pygoscelis antarctica) and gentoo penguin (Pygoscelis papua) were collected on two locations of the Antarctic Peninsula area: Base O´Higgins (Antarctic Peninsula) and Ardley Island (King George Island). Despite POPs have been banned more than three decades ago, the levels (ng g−1 ww) of PCBs (1.45-2.35), DDTs (1.33-1.76), HCB (0.51-1.70), endrin (0.48-0.71) and heptachlor (0.97-2.40) showed that these pollutants are still present in Antarctica. Porphyrin levels in excreta (4.6-6.7 nmol g−1 dw) were significantly correlated to POPs, indicating certain chemical exposure on penguin colonies that inhabit the Antarctic Peninsula area. The levels of heptachlor found in penguin guano may be affecting some biota in terrestrial sites next to nesting places. Further studies and better understanding of POPs impact on animal performance in Antarctic biota are recommended.

Type
Research Article
Information
Polar Record , Volume 53 , Issue 1 , January 2017 , pp. 79 - 87
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anastassiades, M. S. Lehotay, D. Stajnbaher and one other. 2003. Fast and easy multiresidue method employing acetonitrile extraction/partitioning and dispersive solid-phase extraction for the determination of pesticide residues in produce. Journal of AOAC International 86: 412–431.CrossRefGoogle ScholarPubMed
Asensio-Ramos, M., Hernández-Borges, J., Ravelo-Pérez, L., and Rodríguez-Delgado, M.. 2010. Evaluation of a modified QuEChERS method for the extraction of pesticides from agricultural, ornamental and forestal soils. Analytical and Bioanalytical Chemistry 396: 2307–2319.Google Scholar
Barbosa, A., de Mas, E., Benzal, J., Diaz, J. and eight others. 2013. Pollution and physiological variability in Gentoo penguins at two rookeries with different levels of human visitation. Antarctic Science 25:329–338.Google Scholar
Bargagli, R. 2008. Environmental contamination in Antarctic ecosystems. Science of the Total Environment 400: 212–226.CrossRefGoogle ScholarPubMed
BAS (British Antarctic Survey). 2004. Antarctica: 1:10000000 scale map. BAS (Misc) 11. British Antarctic Survey, Cambridge URL: http://www.npolar.no/en/services/maps/printed/topographic-antarctica.html (accessed 11 December 2015).Google Scholar
Berón, M.P., Néstor, R., Coria, R. and one other. 2002. Monitoreo de la dieta post- reproductiva del pingüino papúa (Pygoscelis papua) en Isla Laurie (Orcadas del Sur, Antártida): periodo 1997–1999. Ornitología Neotropical 13: 413–422.Google Scholar
Bidleman, T., Walla, M., Roura, R. and two others. 1993. Organochlorine pesticides in the atmosphere of the Southern Ocean and Antarctica, January– March, 1990. Marine Pollution Bulletin 26: 258–262.Google Scholar
Bícego, M., Weber, R. and Ito, R.. 1996. Aromatic hydrocarbons on surface waters of Admiralty Bay, King George Island, Antarctica. Marine Pollution Bulletin 32: 549–553.Google Scholar
Boersma, P.D. 2008. Penguins as marine sentinels. Bioscience 58: 597–607.Google Scholar
Bright, D.A., Grundy, S.L., and Reimer, K.J.. 1995. Differential bioaccumulation of non-ortho-substituted and other PCB congeners in coastal Arctic invertebrates and fish. Environmental Science and Technology 29: 2504–2512.Google Scholar
Burton, G.A. 2002. Sediment quality criteria in use around the world. Limnology 3: 65–75.CrossRefGoogle Scholar
Bustnes, J.O., Moe, B., Herzke, D. and five others. 2010. Strongly increasing blood concentrations of lipid-soluble organochlorines in high Arctic common eiders during incubation fast. Chemosphere 79: 320–325.Google Scholar
Casini, S. 1997. Effects of hexachlorobenzene and poly-chlorinated biphenyls on porphyrin metabolism: a potential application in ecotoxicological studies. Pharmacological Research 35: 221–222.Google Scholar
Casini, S., Fossi, M.C., Gavilan, J.F. and four others. 2001. Porphyrin levels in excreta of sea birds of the Chilean coasts as nondestructive biomarker of exposure to environmental pollutants. Archives of Environmental Contamination and Toxicology 41: 65–72.Google Scholar
Casini, S., Fossi, M., Leonzio, C. and one other. 2003. Review: porphyrins as biomarkers for hazard assessment of bird populations: destructive and non-destructive use. Ecotoxicology 12: 297–305.Google Scholar
Celis, J., Jara, S., González-Acuña, D. and two others 2012. 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: 311–316.CrossRefGoogle Scholar
Celis, J., Espejo, W., González-Acuña, D. and two others. 2014. Assessment of trace metals and porphyrins in excreta of Humboldt penguins (Spheniscus humboldti) in different locations of the northern coast of Chile. Environmental Monitoring and Assessment 186: 1815–1824.CrossRefGoogle ScholarPubMed
Celis, J.E., Barra, R., Espejo, W. and two others. 2015. Trace element concentrations in biotic matrices of Gentoo penguins (Pygoscelis papua) and coastal soils from different locations of the Antarctic Peninsula. Water, Air and Soil Pollution 226: 2266, doi: 10.1007/s11270-014-2266-5.Google Scholar
Chapman, P.M. and Riddle, M.J.. 2005. Toxic effects of contaminants in polar marine environments. Environmental Science and Technology 39: 200A–206A.CrossRefGoogle ScholarPubMed
Cipro, C., Taniguchi, S. and Montone, R.. 2010. Occurrence of organochlorine compounds in Euphausia superba and unhatched eggs of Pygoscelis genus penguins from Admiralty Bay (King George Island, Antarctica) and estimation of biomagnification factors. Chemosphere 78: 767–771.Google Scholar
Cipro, C., Colabuono, F., Taniguchi, S. and one other. 2013. Persistent organic pollutants in bird, fish and invertebrate samples from King George Island, Antarctica. Antarctic Science 25: 545–552.CrossRefGoogle Scholar
Corsolini, S., Romeo, T., Ademollo, N. and two others. 2002. POPs in key species of marine Antarctic ecosystem. Microchemical Journal 73: 187–193.Google Scholar
Corsolini, S., Ademollo, N., Romeo, T. and two others. 2003. Persistent organic pollutants in some species of a Ross Sea pelagic trophic web. Antarctic Science 15: 95–104.Google Scholar
Corsolini, S. 2009. Industrial contaminants in Antarctic biota. Journal of Chromatography A 1216: 598–612.Google Scholar
Espejo, W., Celis, J., González-Acuña, D. and two others. 2014. Concentration of trace metals in excrements of two species of penguins from different locations of the Antarctic Peninsula. Polar Biology 37: 675–683.Google Scholar
Evenset, A., Christensen, G.N. and Kallenborn, R.. 2005. Selected chlorobornanes, polychlorinated naphthalenes and brominated flame retardants in Bjørnøya (Bear Island) freshwater biota. Environmental Pollution 136: 419–30.Google Scholar
Falkowska, L., Reindl, A.R., Szumilo, E. and five others. 2013. Mercury and chlorinated pesticides on the highest level of the food web as exemplified by herring from the Southern Baltic and African penguins from the Zoo. Water, Air and Soil Pollution 224: 1549.Google Scholar
Focardi, S., Corsolini, S. and Bargagli, R.. 1995. Isomer-specific analysis and toxic evaluation of polychlorinated biphenyls in Antarctic fish, seabirds and Weddell seal from Terra Nova Bay (Ross Sea). Antarctic Science 7: 31–35.Google Scholar
Fossi, M.C., Casini, S. and Marsili, L.. 1996. Porphyrins in excreta: a nondestructive biomarker for the hazard assessment of birds contaminated with PCBs. Chemosphere 33: 29–42.Google Scholar
Geisz, H., Dickhut, R., Cochran, M. and two others. 2008. Melting glaciers: A probable source of DDT to the Antarctic marine ecosystem. Environmental Science and Technology 42: 3958–3962.Google Scholar
Guertin, D., Harestad, A., Ben-David, M. and two others. 2010. Fecal genotyping and contaminant analyses reveal variation in individual river otter exposure to localized persistent contaminants. Environmental Toxicology and Chemistry 29: 275–284.CrossRefGoogle ScholarPubMed
Helander, B., Olsson, A., Bignert, A. and two others. 2002. The role of DDE, PCB, coplanar PCB and eggshell parameters for reproduction in the white-tailed sea eagle (Haliaeetus albicilla) in Sweden. Ambio 31: 386–403.Google Scholar
IAATO (International Association of Antarctic Tour Operators). 2010. 2009–2010 tourism summary. URL: http://www.iaato.org/tourism_stats.html (accessed 15 December 2015).Google Scholar
IUCN (International Union for the Conservation of Nature). 2012. Red list of threatened species.URL: http://www.iucnredlist.org/search (accessed 22 October 2014).Google Scholar
Jara-Carrasco, S., González, M., González-Acuña, D. and five others. 2015. Potential immunohematological effects of persistent organic pollutants on Chinstrap penguin. Antarctic Science 27: 373–381.CrossRefGoogle Scholar
Joshi, M., Bakre, P. and Bhatnagar. 2013. Avian guano: A non-destructive biomonitoring tool for organic pollutants in environment. Ecological Indicators 24: 284–286.Google Scholar
Letcher, R.J., Bustnes, J.O., Dietz, R. and six others. 2010. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Science of the Total Environment 408 : 2995–3043.CrossRefGoogle ScholarPubMed
Lim, C.K. 2002. Analysis of biosynthetic intermediates, 5-amino levulinic acid to heme. In: Smith, A.G., and Witty, M. (editors). Heme, chlorophylla and bilius : methods and protocols. Totowa: 95–109.Google Scholar
Llansola, M., Montoliu, C., Boix, J. and Felipo, V.. 2010. Polychlorinated biphenyls PCB 52, PCB 180, and PCB 138 impair the glutamate-nitric oxide-cGMP pathway in cerebellar neurons in culture by different mechanisms. Chemical Research in Toxicology 23: 813–820.Google Scholar
Lockwood, W.H., Poulus, V., Rossi, E. and one other. 1985. Rapid procedure for fecal porphyrin assay. Clinical Chemistry 31: 1163–1167.Google Scholar
Lynch, H. J., Crosbie, K., Fagan, W.F. and one other. 2010. Spatial patterns of tour ship traffic in the Antarctic Peninsula region. Antarctic Science 22: 123–130.CrossRefGoogle Scholar
Maervoet, J., Chu, S.G., Vos, D. and four others 2004. Accumulation and tissue distribution of selected polychlorinated biphenyl congeners in chickens. Chemosphere 57: 61–66.Google Scholar
Montone, R., Taniguchi, S. and Weber, R.. 2001. Polychlorinated biphenyls in marine sediments of Admiralty Bay, King George Island, Antarctica. Marine Pollution 42: 611–614.Google Scholar
Muir, D., Savinova, T., Savinov, V. and three others. 2003. Bioaccumulation of PCBs and chlorinated pesticides in seals, fishes and invertebrates from the White Sea, Russia. Science of the Total Environment 306: 111–131.Google Scholar
Norli, H., Christiansen, A. and Deribe, E.. 2011. Application of QuEChERS method for extraction of selected persistent organic pollutants in fish tissue and analysis by gas chromatography mass spectrometry. Journal of Chromatography A 1218: 7234–7241.Google Scholar
Norstrom, R.J., Simon, M., Muir, C.G. and one other. 1988. Organochlorine contaminants in Arctic marine food chains: identification, geographical distribution and temporal trends in polar bears. Environmental Science and Technology 22: 1063–1071.Google Scholar
Oliver, B.G. and Niimi, A.J.. 1988. Trophodynamic analysis of polychlorinated biphenyl congeners and other chlorinated hydrocarbons in the Lake Ontario ecosystem. Environmental Science and Technology 22: 388–397.CrossRefGoogle Scholar
Poland, J.S., Riddle, M.J. and Zeeb, B.A.. 2003. Contaminants in the Arctic and the Antarctic: a comparison of sources, impacts, and remediation options. Polar Record 39 (211): 369–383.Google Scholar
Roosens, L., van Den Brink, N., Riddle, M. and three others. 2007. Penguin colonies as secondary sources of contamination with persistent organic pollutants. Journal of Environmental Monitoring 9: 822–825.Google Scholar
Smit, M.D., Leonards, P.E.G., van Hattum, A.G.M. and one other. 1994. PCBs in European otter (Lutra lutra) populations. Amsterdam: Vrije Universiteit.Google Scholar
Subramanian, A., Tanabe, S., Fujise, Y. and one other. 1986. Bioaccumulation of organochlorines (PCBs and p,p'-DDE) in Antarctic Adélie penguins (Pygoscelis adeliae) collected during a breeding season. Environmental Pollution 40: 173–189.Google Scholar
Sun, L., Yin, X., Liu, X. and six others. 2006. Levels of hexachlorocyclohexanes and dichloro-dipheny-trichloroethanes in penguin droppings collected from Ardley Island, Maritime Antarctic. Human and Ecological Risk Assessment 12: 328–338.CrossRefGoogle Scholar
Taniguchi, S., Montone, R., Bícego, M. and three others. 2009. Chlorinated pesticides, polychlorinated biphenyls and polycyclic aromatic hydrocarbons in the fat tissue of seabirds from King George Island, Antarctica. Marine Pollution Bulletin 58: 129–133.Google Scholar
Tin, T., Fleming, Z.L., Hughes, K.A. and six others. 2009. Impacts of local human activities on the Antarctic environment. Antarctic Science 21: 3–33.Google Scholar
Van Birgelen, A., Fase, K., van Der Kolk, J. and four others. 1996. Synergistic effect of 2,2%,4,4%,5,5%-hexachlorobiphenyl and 2,3,7,8-tetrachlorodibenzo-p-dioxin on hepatic porphyrin levels in the rat. Environmental Health Perspectives 104: 550–557.Google Scholar
Williams, T.D. and Rothery, P.. 1990. Factors affecting variations in foraging and activity patterns of Gentoo penguins (Pygoscelis papua) during the breeding season at Bird Island, South Georgia. Journal of Applied Ecology 27: 1042–1054.CrossRefGoogle Scholar
Williams, T.D. 1990. Annual variation in breeding biology of gentoo penguin, Pygoscelis papua, at Bird Island, South Georgia. Journal of Zoology 222: 247–258.Google Scholar
Woehler, E.J. and Poncet, S.. 1993. The distribution and abundance of Antarctic and Subantarctic penguins. Cambridge: Scientific Committee on Antarctic Research.Google Scholar