Menu

Volume 46, No. 2

Search by author or title:

Persistent organic pollutants and stable isotopes in seabirds of the Rocas Atoll, Equatorial Atlantic, Brazil


Authors

PATRICK S. DIAS1, CAIO V. Z. CIPRO1, FERNANDA I. COLABUONO1, SATIE TANIGUCHI1 & ROSALINDA C. MONTONE1
1Laboratório de Química Orgânica Marinha, Instituto Oceanográfico, Universidade de São Paulo, 05508-120, São Paulo, SP, Brazil

Citation

DIAS, P.S., CIPRO, C.V.Z., COLABUONO, F.I., TANIGUCHI, S. & MONTONE, R.C. 2018. Persistent organic pollutants and stable isotopes in seabirds of the Rocas Atoll, Equatorial Atlantic, Brazil. Marine Ornithology 46: 139 - 148

Received 01 October 2017, accepted 13 June 2018

Date Published: 2018/10/15
Date Online: 2018/8/30
Key words: PCBs, organochlorine pesticides, trophic position, remote environments, long-range transport, stable isotopes, tropical seabirds

Abstract

Pollution is a key factor in efforts to conserve seabirds and their habitats. The Marine Biological Reserve of Rocas Atoll hosts the largest population of seabirds (~23 000 individuals) breeding in Brazilian waters. In the present study at Rocas Atoll, liver samples were collected from dead individuals of five species (adults and nestlings): Masked Booby Sula dactylatra, Brown Booby Sula leucogaster, Brown Noddy Anous stolidus, Black Noddy Anous minutus, and Sooty Tern Onychoprion fuscatus. They were analyzed for three persistent organic pollutants (POPs): polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), and polybrominated diphenyl ethers. Carbon and nitrogen stable isotopes (δ13C and δ15N) were also analyzed to assess feeding and foraging habits. PCBs (3.37-189 ng·g-1), OCPs (DDTs, 0.5-23.1 ng·g-1), and hexachlorobenzene (0.31-12.3 ng·g-1) were predominant overall, and results were generally consistent with previous studies. Despite the low levels of contaminants, intraspecific stratification was found with lower concentrations in nestlings compared to adults, as expected. Stable isotopes revealed that differences in POP levels and PCB profiles were associated with diet and foraging patterns. Low levels of POPs at Rocas Atoll were consistent with patterns observed in studies of other low-latitude and high-latitude seabirds.

References


ADELSBACH, T.L. & MAURER, T. 2007. Dioxin Toxic Equivalents, PCBs, and PBDEs in Eggs of Avian Wildlife of San Francisco Bay. Environmental Contaminants Program. Project ID#200110001.1. Sacramento, CA: US Fish and Wildlife Service.

BEARHOP, S., WALDRON, S., VOTIER, S.C. & FURNESS, R.W. 2002. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiological and Biochemical Zoology 75: 451-458.

BLIGHT, L.K., HOBSON, K.A., KYSER, T.K. & ARCESE, P. 2015. Changing gull diet in a changing world: A 150-year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America. Global Change Biology 21: 1497-1507.

BOSVELD, A.T.C., GRADENER, J., VAN DEN BERG, M. ET AL. 1995. Effects of PCDDs, PCDFs and PCBs in Common Tern (Sterna hirundo) breeding in estuarine and coastal colonies in the Netherlands and Belgium. Environmental Toxicology and Chemistry. 14: 99-115.

BOSVELD, A.T.C., NIEBOER, R., DE BONT, A. ET AL. 2000. Biochemical and developmental effects of dietary exposure to polychlorinated biphenyls 126 and 153 in Common Tern chicks (Sterna hirundo). Environmental Toxicology and Chemistry 19: 719-730.

BOURNE, W.R.P. 1976. Seabirds and pollution. In: JOHNSON, R. (Ed.) Marine Pollution. London, UK: Academic Press.

BOUWMAN, H., KYLIN, H., YIVE, N.S.C.K. ET AL. 2012. First report of chlorinated and brominated hydrocarbon pollutants in marine bird eggs from an oceanic Indian Ocean island. Environmental Research 118: 53-64.

BRAUNE, B.M., GASTON, A.J., LETCHER, R.J., GILCHRIST, H.G. & PROVENCHER, J.F. 2014. A geographical comparison of chlorinated, brominated and fluorinated compounds in seabirds breeding in the eastern Canadian Arctic. Environmental Research 134: 46-56.

BREIVIK, K., PACYNA, J.M. & MUNCH, J. 1999. Use of alpha-, beta- and gamma-hexachlorocyclohexane in Europe, 1970-1996. The Science of the Total Environment 239: 151-163.

BURGER, J. & GOCHFELD, M. 2001. Laridae, Sternidae and Rynchopidae. In: STEELE, J.H., THORPE, S.A. & TUREKIAN, K.K. (Eds.) Encyclopedia of Ocean Sciences, vol. 3. London, UK: Academic Press.

CARBONERAS, C. 1992. Family Sulidae (Gannets and Boobies). In: DELHOYO, J., ELLIOTT, A. & SARGATAL, J. (Eds.) Handbook of the Birds of the World, vol. 1. Ostrich to Ducks. Barcelona, Spain: Lynx Edicions.

CASEY, J.R., LOMAS, M.W., MANDECKI, J. & WALKER, D.E. 2007. Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum. Geophysical Research Letters 34: 1-5.

CIPRO, C.V.Z., BUSTAMANTE, P., TANIGUCHI, S. & MONTONE, R.C. 2012. Persistent organic pollutants and stable isotopes in pinnipeds from King George Island, Antarctica. Marine Pollution Bulletin 64: 2650-2655.

CIPRO, C.V.Z., COLABUONO, F.I., TANIGUCHI, S. & MONTONE, R.C. 2013. Persistent organic pollutants in bird, fish and invertebrate samples from King George Island, Antarctica. Antarctic Science 25: 545-552.

CIPRO, C.V.Z., MONTONE, R.C. & BUSTAMANTE, P. 2017. Mercury in the ecosystem of Admiralty Bay, King George Island, Antarctica: Occurrence and trophic distribution. Marine Pollution Bulletin 114: 564-570.

CHEREL, Y., HOBSON, K.A., GUINET, C. & VANPÉ, C. 2007. Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. Journal of Animal Ecology 76: 826-836.

CLARK, R.B. 2001. Marine Pollution, 5th Edition. Oxford, UK: Oxford University Press.

COLABUONO, F.I., BARQUETE, V., TANIGUCHI, S., RYAN, P.G. & MONTONE, R.C. 2014. Stable isotopes of carbon and nitrogen in the study of organochlorine contaminants in albatrosses and petrels. Marine Pollution Bulletin 83: 241-247.

CORBISIER, T.N., PETTI, M.A.V., SKOWRONSKI, R.S.P. & BRITO, T.A.S. 2004. Trophic relationships in the nearshore zone of Martel Inlet (King George Island, Antarctica): δ13C stable-isotope analysis. Polar Biology 27: 75-82. 

DENIRO, M.J. & EPSTEIN, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495-506. doi:10.1016/0016-7037(78)90199-0

DIAS, P.S., CIPRO, C.V.Z., TANIGUCHI, S. & MONTONE, R.C. 2013. Persistent organic pollutants in marine biota of São Pedro and São Paulo Archipelago, Brazil. Marine Pollution Bulletin 74: 435-440.

ELLIOTT, J.E. 2005. Chlorinated hydrocarbon contaminants and stable isotope ratios in pelagic seabirds from the North Pacific Ocean. Archives of Environmental Contamination and Toxicology 49: 89-96.

ELLIOTT, K.H., CESH, L.S., DOOLEY, J.A., LETCHER, R.J. & ELLIOTT, J.E. 2009. PCBs and DDE, but not PBDEs, increase with trophic level and marine input in nestling bald eagles. Science of the Total Environment 407: 3867-3875.

FISK, A.T., HOBSON, K.A. & NORSTROM, R.J. 2001. Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwater Polynya marine food web. Environmental Science & Technology 35: 732-738.

FORERO, M.G. & HOBSON, K.A. 2003. Using stable isotopes of nitrogen and carbon to study seabird ecology: Applications in the Mediterranean seabird community. Scientia Marina 67: 23-32.

FUOCO, R. & CECCARINI, A. 2001. Polychlorobiphenyls in Antarctic matrices. In: CAROLI, S., CESCON, P. & WALTON, D.W.H. (Eds.) Environmental Contamination in Antarctica: A Challenge to Analytical Chemistry. Oxford, UK: Elsevier B.V.

FURNESS, R.W. & CAMPHUYSEN, C.J. 1997. Seabirds as monitors of the marine environment. ICES Journal of Marine Science 54: 726-737.

GUIOLI, S., NANDI, S., ZHAO, D., BURGESS-SHANNON, J., LOVELL-BADGE, R. & CLINTON, M. 2014. Gonadal asymmetry and sex determination in birds. Sexual Development 8: 227-242.

GUZZO, M.M., ECKBO, N.H., GABRIELSEN, G.W., FISK, A.T., HYLLAND, K. & BORGÅ, K. 2014. Persistent organic pollutant concentrations in fledglings of two arctic seabird species. Environmental Pollution 184: 414-418.

HARRISON, P. 1985. Seabirds: An Identification Guide, Revised Edition. Boston, MA: Houghton Mifflin Company.

HOBSON, K.A. & WELCH, H.E. 1992. Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84: 9-18.

HOFLICH, O. 1984. Climate of the South Atlantic Ocean. In: VAN LOON, H. (Ed.) Climates of the Oceans. Amsterdam: Elsevier Science.

JASPERS, V.L.B., SONNE, C., SOLER-RODRIGUEZ, F. ET AL. 2013. Persistent organic pollutants and methoxylatedpolybrominated diphenyl ethers in different tissues of white-tailed eagles (Haliaeetus albicilla) from West Greenland. Environmental Pollution 175: 137-146.

JENNINGS, S., PINNEGAR, J.K., POLUNIN, N.V.C. & BOON, T.W. 2001. Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. Journal of Animal Ecology 70: 934-944.

JONES, K.C. & DE VOOGT, P. 1999. Persistent organic pollutants (POPs): state of the science. Environmental Pollution 100: 209-221.

KIKUCHI, R.K.P. & LEÃO, Z.M.A.N. 1997. Rocas (Southwestern Equatorial Atlantic, Brazil): An atoll built primarily by coralline algae. Proceedings of the 8th International Coral Reef Symposium 1: 731-736.

KOCAGÖZ, R., ONMUS, O., ONAT, İ., ÇAǦDAŞ, B., SIKI, M. & ORHAN, H. 2014. Environmental and biological monitoring of persistent organic pollutants in waterbirds by non-invasive versus invasive sampling. Toxicology Letters 230: 208-217.

LUZARDO, O.P., RUIZ-SUÁREZ, N., HENRÍQUEZ-HERNÁNDEZ, L.A. ET AL. 2014. Assessment of the exposure to organochlorine pesticides, PCBs and PAHs in six species of predatory birds of the Canary Islands, Spain. Science of the Total Environment 472: 146-153.

MACLEOD, W.D., BROWN, D.W., FRIEDMAN, A.J. ET AL. 1985. Standard Analytical Procedures of the NOAA National Analytical Facility, 1985-1986: Extractable Toxic Organic Components, 2nd Edition. NOAA Technical Memorandum NMFS F/NWC-92. Seattle, WA: US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service.

MALLORY, M.L. & BRAUNE, B.M. 2012. Tracking contaminants in seabirds of Arctic Canada: Temporal and spatial insights. Marine Pollution Bulletin 64: 1475-1484.

MANCINI, P.L., HOBSON, K.A. & BUGONI, L. 2014. Role of body size in shaping the trophic structure of tropical seabird communities. Marine Ecology Progress Series 497: 243-257.

MANCINI, P.L., SERAFINI, P. & BUGONI, L. 2016. Breeding seabird populations in Brazilian oceanic islands: Historical review, update and a call for census standardization. Revista Brasileira de Ornitologia 24: 94-115

MARQUES, F.P., ROBALDO, R.B. & BUGONI, L. 2011. Identificação das áreas de invernagem do trinta-réis-das-rocas Onychoprion fuscatus no Oceano Atlântico, determinadas por isótopos estáveis. Trabalho de conclusão de curso, Universidade Federal de Pelotas.

MIZUKAWA, K., TAKADA, H., TAKEUCHI, I., IKEMOTO, T., OMORI, K. & TSUCHIYA, K. 2009. Bioconcentration and biomagnification of polybrominated diphenyl ethers (PBDEs) through lower-trophic-level coastal marine food web. Marine Pollution Bulletin 58: 1217-1224.

MOISEY, J., FISK, A.T., HOBSEN, K.A. & NORSTROM, R.J. 2001. Hexachlorocyclohexane (HCH) isomers and chiral signatures of α-HCH in the Arctic marine food web of the Northwater Polynya. Environmental Science & Technology 35: 1920-1927.

MURK, A.J., BOUDEWIJN, T.J., MEININGER, P.L. ET AL. 1996. Effects of polyhalogenated aromatic hydrocarbons and related contaminants on Common Tern reproduction: Integration of biological, biochemical, and chemical data. Archives of Environmental Contamination and Toxicology. 31: 128-140.

OHLENDORF, H.M., KLAAS, E.E. & KAISER, T.E. 1978. Organochlorine residues and eggshell thinning in wood storks and anhingas. The Wilson Bulletin 90: 608-618.

PANDIT, G.G., MOHAN RAO, A.M., JHA, S.K. ET AL. 2001. Monitoring of organochlorine pesticide residues in the Indian marine environment. Chemosphere 44: 301-305.

PEREIRA, N.S., MANSO, V.A.V., SILVA, A.M.C. & SILVA, M.B. 2010. Mapeamento geomorfológico e morfodinâmica do Atol das Rocas, Atlântico Sul. Revista da Gestão Costeira Integrada 10: 331-345.

POST, D.M., LAYMAN, C.A., ARRINGTON, D.A., TAKIMOTO, G., QUATTROCHI, J. & MONTAÑA, C.G. 2007. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179-189.

QUILLFELDT, P., MCGILL, R.A.R. & FURNESS, R.W. 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. Marine Ecology Progress Series 295: 295-304.

RICCA, M.A., MILES, A.K. & ANTHONY, R.G. 2008. Sources of organochlorine contaminants and mercury in seabirds from the Aleutian archipelago of Alaska: Inferences from spatial and trophic variation. Science of the Total Environment 406: 308-323.

SAADATI, N., ABDULLAH, M.P., ZAKARIA, Z., REZAYI, M. & HOSSEINIZARE, N. 2012. Distribution and fate of HCH isomers and DDT metabolites in a tropical environment-case study Cameron Highlands-Malaysia. Chemistry Central Journal 6: 130.

SAGERUP, K., HELGASON, L.B., POLDER, A. ET AL. 2009. Persistent organic pollutants and mercury in dead and dying glaucous gulls (Larus hyperboreus) at Bjørnøya (Svalbard). Science of the Total Environment 407: 6009-6016.

SCHULZ-NETO, A. 2004. Aves marinhas do Atol das Rocas, In: BRANCO, J.O. (Ed.) Aves marinhas e insulares brasileiras: biologia e conservação. Itajaí, SC, Brasil: Editorada Univali.

STEFANELLI, P., AUSILI, A., DI MUCCIO, A. ET AL. 2004. Organochlorine compounds in tissues of swordfish (Xiphias gladius) from Mediterranean Sea and Azores islands. Marine Pollution Bulletin 49: 938-950.

TANABE, S., SENTHILKUMAR, K., KANNAN, K. & SUBRAMANIAN, A.N. 1998. Accumulation features of polychlorinated biphenyls and organochlorine pesticides in resident and migratory birds from South India. Archives of Environmental Contamination and Toxicology 34: 387-397.

VAN DEN BRINK, N.W. 1997. Directed transport of volatile organochlorine pollutants to polar regions: The effect on the contamination pattern of Antarctic seabirds. Science of the Total Environment 198: 43-50.

VON WALDOW, H., MACLEOD, M., SCHERINGER, M. & HUNGERBÜHLER, K. 2010. Quantifying remoteness from emission sources of persistent organic pollutants on a global scale. Environmental Science & Technology 44: 2791-2796.

WADE, T.L. & CANTILLO, A.Y. 1994. Use of Standards and Reference Materials in the Measurement of Chlorinated Hydrocarbon Residues. Chemistry Workbook. NOAA Technical Memorandum NOS ORCA 77. Silver Spring, MD: US Department of Commerce.

WALKER, K., VALLERO, D.A. & LEWIS, R.G. 1999. Factors influencing the distribution of Lindane and other hexachlorocyclohexanes in the environment. Environmental Science & Technology 33: 4373-4378.

WEBER, R.R. 1983. ΣDDT and PCBs in equatorial Atlantic organisms. Marine Pollution Bulletin 14: 274-275.

Search by author or title:

Browse previous volumes: