Volume 48, No. 1

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Stable isotope and mercury analyses of the Galápagos Islands seabird community


1University of North Carolina, Department of Biology and Marine Biology, 601 S. College Rd., Wilmington, NC 28403, USA
2Universidad San Francisco de Quito USFQ, Colegio de Ciencias Biológicas y Ambientales COCIBA, Campus Cumbavá Av. Diego de Robles S/N e Interoceánica, Quito, Ecuador
3Galápagos Science Center GSC-USFQ, Av. Alsacio Northia, Isla San Cristóbal, Galápagos, Ecuador
4Weber State University, Department of Zoology, 1415 Edvalson St., Ogden, UT 84408, USA
5Texas Tech University, Department of Biological Sciences, Lubbock, TX 79409, USA


ZARN, A.M., VALLE, C.A., BRASSO, R., FETZNER, W. & EMSLIE, S.D. 2020. Stable isotope and mercury analyses of the Galápagos Islands seabird community. Marine Ornithology 48: 71 - 80

Received 07 March 2019, accepted 06 November 2019

Date Published: 2020/04/15
Date Online: 2019/03/30
Key words: foraging, δ15N, δ13C, mercury, ENSO events, tropical seabirds, dietary shifts


The Galápagos Islands seabird community is directly impacted by El Niño Southern Oscillation (ENSO) cycles, which makes understanding seabird foraging behavior in response to these events important for future conservation plans. In this study, we used stable isotope analysis (δ15N and δ13C) to investigate trophic status and foraging location in the seabird community before, during, and after the 2015-2016 El Niño event. Mercury (Hg) analysis was also performed to provide a more thorough understanding of the relationship between contaminant exposure and foraging behavior. We analyzed breast feathers collected across five years (2011, 2014-2017) from eight nesting seabird species (Sula sula, S. granti, S. nebouxii excisa, Fregata minor, F. magnificens, Oceanodroma tethys tethys, Creagrus furcatus, and Phaethon aethereus)for δ15N and δ13C isotopes and total Hg (ppm). These sampling periods occurred at different points in the ENSO cycle, which allowed shifts in foraging behavior to be monitored as environmental conditions changed. Our findings indicate that higher Hg contamination is positively correlated with La Niña. Additionally, as prey abundance decreased with the onset of El Niño in 2015, most species showed more negative δ13C values, which indicates a shift to more pelagic foraging. Furthermore, isotopic nitrogen values revealed that while foraging by most species decreased in trophic level during the 2015-2016 El Niño, some populations, mainly Sula species, increased in trophic level. Both responses indicate a change in diet, suggestive of flexible foraging behavior.


ALTABET, M.A., PILSKALN, C., THUNELL, R., PRIDE, C., SIGMAN, D., CHAVEZ, F. & FRANCOIS, R. 1999. The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific. Deep-Sea Research Part I-Oceanographic Research Papers 46: 655-679. doi:10.1016/s0967-0637(98)00084-3

ANCHUNDIA, D., HUYVAERT, K.P. & ANDERSON, D.J. 2014. Chronic lack of breeding by Galápagos Blue-Footed Boobies and associated population decline. Avian Conservation and Ecology 9: 6. doi:10.5751/ace-00650-090106

AWKERMAN, J.A., HOBSON, K.A. & ANDERSON, D.J. 2007. Isotopic (δ15N and δ13C) evidence for intersexual foraging differences and temporal variation in habitat use in Waved Albatrosses. Canadian Journal of Zoology-Revue Canadienne De Zoologie 85: 273-279. doi:10.1139/z06-202

BARGER, C.P. & KITAYSKY, A.S. 2012. Isotopic segregation between sympatric seabird species increases with nutritional stress. Biology Letters 8: 442-445. doi:10.1098/rsbl.2011.1020

BENJAMINI, Y. & HOCHBERG, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Statistical Methodology 57: 289-300. doi:10.1111/j.2517-6161.1995.tb02031.x

BOND, A.L. & JONES, I.L. 2009. A practical introduction to stable isotope analysis for seabird biologists: approaches, cautions and caveats. Marine Ornithology 37: 183-188. 

BOWERMAN, W.W., EVANS, E.D., GIESY, J.P. & POSTUPALSKY, S. 1994. Using feathers to assess risk of mercury and selenium to bald eagle reproduction in the Great Lakes region. Archives of Environmental Contamination and Toxicology 27: 294-298.

CHEREL, Y., LE CORRE, M., JAQUEMET, S., MENARD, F., RICHARD, P. & WEIMERSKIRCH, H. 2008. Resource partitioning within a tropical seabird community: new information from stable isotopes. Marine Ecology Progress Series 366: 281-291. doi:10.3354/meps07587

Cold and Warm Episodes by Season [Online]. College Park, USA: National Weather Service Climate Prediction Center. [Available online at: Accessed 24 October 2019].

DRAGO, M., FRANCO-TRECU, V., CARDONA, L., INCHAUSTI, P., TAPIA, W. & PÁEZ-ROSAS, D. 2016. Stable isotopes reveal long-term fidelity to foraging grounds in the Galápagos Sea Lion (Zalophus wollebaeki). PloS One 11: e0147857. doi:10.1371/journal.pone.0147857

ELLIOTT, J.E. 2005. Trace metals, stable isotope ratios, and trophic relations in seabirds from the North Pacific Ocean. Environmental Toxicology and Chemistry 24: 3099-3105. doi: 10.1897/04-474r.1

ENGLAND, M. 2000. A review of bird responses to El Niño-Southern Oscillation conditions in the Neotropics. Contiga 13: 83-88. 

EVERS, D. 2018. The effects of methylmercury on wildlife: a comprehensive review and approach for interpretation. In: DELLASALA D.A., GOLDSTEIN M.I. (Eds.) Encyclopedia of the Anthropocene, Book 5. Oxford, UK: Elsevier. 

FINKELSTEIN, M., KEITT, B.S., CROLL, D.A. ET AL. 2006. Albatross species demonstrate regional differences in North Pacific marine contamination. Ecological Applications 16: 678-686. doi:10.1890/1051-0761(2006)016[0678:asdrdi];2

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.

FRANCE, R.L. 1995. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnology and Oceanography 40: 1310-1313. doi:10.4319/lo.1995.40.7.1310

FRY, B. 2006. Stable Isotope Ecology. New York, USA: Springer.

FURNESS, R.W. & CAMPHUYSEN, C.J. 1997. Seabirds as monitors of the marine environment. Ices Journal of Marine Science 54: 726-737. doi:10.1006/jmsc.1997.0243

GRAJEWSKA, A., FALKOWSKA, L., SZUMILLO-PILARSKA, E. ET AL. 2015. Mercury in the eggs of aquatic birds from the Gulf of Gdansk and Wloclawek Dam (Poland). Environmental Science and Pollution Research 22: 9989-9898. doi:10.1007/s11356-015-4154-y

GWOREK, B., BEMOWSKA-KALABUN, O., KIJENSKA, M. & WRZOSEK-JAKUBOWSKA, J. 2016. Mercury in marine and oceanic waters—a review. Water Air and Soil Pollution 227. doi:10.1007/s11270-016-3060-3

HEINZ, G.H. 1979. Methylmercury: Reproductive and behavioral effects on three generations of Mallard ducks. Journal of Wildlife Management 43: 394-401.

HOBSON, K.A. & CLARK, R.G. 1992a. Assessing avian diets using stable isotopes I: Turnover of 13C in tissues. The Condor 94: 181-188. doi:10.2307/1368807

HOBSON, K.A. & CLARK, R.G. 1992b. Assessing avian diets using stable isotopes II: Factors influencing diet-tissue fractionation. The Condor 94: 189-197. doi:10.2307/5256

HOPKINS, W.A. & HOPKINS, L.B., UNRINE, J.M., SNODGRASS, J., ELLIOT, J.D. 2007. Mercury concentrations in tissues of osprey from the Carolinas, USA. Journal of Wildlife Management 71: 1819-1829. doi:10.2193/2006-016

HOWELL, S.N.G. 2003. Understanding Molt, Part I: The variety of molt strategies. Birding 35: 490-496.

HUTCHINSON, G.E. 1959. Homage to Santa-Rosalia or why are there so many kinds of animals? American Naturalist 93: 145-159.

JIMÉNEZ-UZCÁTEGUI, G., VACA, L., COTÍN, J., GARCÍA, C., COSTALES, A., SEVILLA, C. & PÁEZ-ROSAS, D. 2019. Using referential values of δ13C and δ15N to infer the foraging ecology of Galápagos seabirds. Marine Ornithology 47: 5-10. 

KOJADINOVIC, J., BUSTAMANTE, P., CHURLAUD, C., COSSON, R.P. & LE CORRE, M. 2007. Mercury in seabird feathers: Insight on dietary habits and evidence for exposure levels in the western Indian Ocean. Science of the Total Environment 384: 194-204. doi:10.1016/j.scitotenv.2007.05.018

MCPHADEN, M.J., ZEBIAK, S.E. & GLANTZ, M.H. 2006. ENSO as an integrating concept in Earth science. Science 314: 1740-1745. doi:10.1126/science.1132588

MENDEZ, L., COTTE, C., PRUDOR, A. & WEIMERSKIRCH, H. 2016. Variability in foraging behaviour of Red-Footed Boobies nesting on Europa Island. Acta Oecologica-International Journal of Ecology 72: 87-97. doi:10.1016/j.actao.2015.10.017

MONTEIRO, L.R. & FURNESS, R.W. 2001. Kinetics, dose-response, and excretion of methylmercury in free-living adult Cory's Shearwaters. Environmental Science & Technology 35: 739-746. doi:10.1021/es000114a

PALMA, C., LILLEBO, A.I., VALENCA, M., PEREIRA, E., ABREU, M.P. & DUARTE, A.C. 2009. Mercury in sediments of the Azores deep sea platform and on sea mounts south of the archipelago—Assessment of background concentrations. Marine Pollution Bulletin 58: 1583-1587. doi:10.1016/j.marpolbul.2009.07.012

RAU, G.H., TAKAHASHI, T. & MARAIS, D.J.D. 1989. Latitudinal variations in plankton δ13C—implications for CO2 and productivity in past oceans. Nature 341: 516-518. doi:10.1038/341516a0

ROBERTSON, B.A. 2004. Forging new links in bird migration. Birding 36:142-145. 

SCHREIBER, E.A. & BURGER, J. 2001. Biology of Marine Birds. Boca Raton, USA: CRC Press.

SIBLEY C.G. & MONROE, B.L. 1990. Distribution and taxonomy of birds of the world. New Haven, USA: Yale Univeristy Press. 

SIGMAN, D.M. & HAIN, M.P. 2012. The Biological Productivity of the Ocean. Nature Education 3: 1-16. 

STRAMMA, L., FISCHER, T., GRUNDLE, D.S., KRAHMANN, G., BANGE, H.W. & MARANDINO, C.A. 2016. Observed El Niño conditions in the eastern tropical Pacific in October 2015. Ocean Science 12: 861-873. doi:10.5194/os-12-861-2016

SZUMILO-PILARSKA, E., GRAJEWSKA, A., FALKOWSKA, L. ET AL. 2016. Species differences in total mercury concentration in gulls from the Gulf of Gdansk (Southern Baltic). Journal of Trace Elements in Medicine and Biology 33: 100-109. doi:10.1016/j.jtemb.2015.09.005

VALLE, C.A., CRUZ, F., CRUZ, J.B., MERLEN, G. & COULTER, M.C. 1987. The impact of the 1982-1983 El Niño Southern Oscillation on seabirds in the Galápagos Islands, Ecuador. Journal of Geophysical Research: Oceans 92: 14437-14444. doi:10.1029/JC092iC13p14437

WIENER, J.G. 2013. Mercury exposed: Advances in environmental analysis and ecotoxicology of a highly toxic metal. Environmental Toxicology and Chemistry 32: 2175-2178. doi:10.1002/etc.2333

WINDER, V.L., MICHAELIS, A.K. & EMSLIE, S.D. 2012. Understanding associations between nitrogen and carbon isotopes and mercury in three Ammodramus sparrows. Science of the Total Environment 419: 54-59. doi:10.1016/j.scitotenv.2012.01.003

YOUNG, H.S., MCCAULEY, D.J., DIRZO, R., DUNBAR, R.B. & SHAFFER, S.A. 2010b. Niche partitioning among and within sympatric tropical seabirds revealed by stable isotope analysis. Marine Ecology Progress Series 416: 285-294. doi:10.3354/meps08756

YOUNG, H.S., SHAFFER, S.A., MCCAULEY, D.J., FOLEY, D.G., DIRZO, R. & BLOCK, B.A. 2010a. Resource partitioning by species but not sex in sympatric Boobies in the central Pacific Ocean. Marine Ecology Progress Series 403: 291-301. doi:10.3354/meps08478

ZAVALAGA, C.B., EMSLIE, S.D., ESTELA, F.A., MULLER, M.S., DELL'OMO, G. & ANDERSON, D.J. 2012. Overnight foraging trips by chick-rearing Nazca Boobies Sula granti and the risk of attack by predatory fish. Ibis 154: 61-73. doi:10.1111/j.1474-919X.2011.01198.x

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