Volume 49, No. 1

Volumes > 38 (2010-->) Volumes 28-37 (2000-09) Volumes 18-27 (1990-99) Volumes 5-17 (1978-89)
a.k.a. Cormorant

Quick Search by author or article title:

Stable isotope analysis of multiple tissues from chick carcasses of three pygoscelid penguins in Antarctica



1University of North Carolina Wilmington, Department of Biology and Marine Biology, 601 S. College Rd., Wilmington, NC 28403, USA *(emslies@uncw.edu)
2Departamento de Biología de Predadores Tope, Coordinación de Ciencias de la Vida, Instituto Antártico Argentino, 25 de Mayo 1143, San Martín, Buenos Aires B1650CSP, Argentina
3Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Rivadavia 1917, Buenos Aires C1033AAJ, Argentina
4Laboratorios Anexos, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Calle 64 N8 3, La Plata, Buenos Aires B1904AMA, Argentina

Received 07 July 2020, accepted 08 August 2020

Date Published: 2021/04/15
Date Online: 2021/02/02

Download PDF


CIRIANI, Y.A., JUÁRES, M.A., SANTOS, M.M. & EMSLIE, S.D. 2021. Stable isotope analysis of multiple tissues from chick carcasses of three pygoscelid penguins in Antarctica. Marine Ornithology 49: 9-17.

Key words: 25 de Mayo/King George Island, δ15N, δ13C, Pygoscelis penguins, dietary shifts, opportunistic sampling


Many types of animal tissues are increasingly being used for stable isotope analysis, with their application dependent on the time frame they reflect and their availability for collection. Here, we investigated the isotopic values (δ13C and δ15N) of four tissues (feather, skin, toenail, and bone) collected from fledgling-period chick carcasses of three species of pygoscelid penguins to compare the variability and accuracy of the data among tissues. Samples were collected at 25 de Mayo/King George Island during the 2017/18 austral summer. Chick carcasses are commonly found at active penguin colonies, and “opportunistic sampling” can easily be performed without disturbing nesting penguins. A total of 25-36 carcasses per species were sampled at active colonies of Adélie Pygoscelis adeliae, Gentoo P. papua, and Chinstrap P. antarcticus penguins. A linear mixed model showed that δ13C values varied significantly between tissues, presumably due to tissue-specific isotopic discrimination. In contrast, the only tissue with significantly different δ15N values was toenail. Stable isotope data revealed dietary differences among species, with Gentoo Penguins having higher average isotopic values in tissues compared to Adélie and Chinstrap penguins. In addition, Chinstrap Penguins showed a consistent, but not statistically significant, trend in having higher δ13C values compared to Adélie Penguins. Gentoo Penguins displayed the highest isotopic variability of any species for all tissues. Isotopic composition was most variable in skin in all three species making skin the least reliable tissue for isotope analysis, whereas isotopic values were least variable in toenails. Comparison of isotopic values between two bones (tibiotarsus and coracoid) showed no significant differences in isotopic values, indicating that when the same bone is not available for sampling from carcasses, sampling of any major skeletal element is likely to provide a meaningful comparison. These results allow for more informed opportunistic sampling to accurately estimate and compare penguin diet among species and between ancient and active colonies.


AGNEW, D. J. 1997. Review: the CCAMLR Ecosystem Monitoring Programme. Antarctic Science 9: 235-242. doi:10.1017/S095410209700031X

AINLEY, D. G., BALLARD, G., BARTON, K. J. ET AL. 2003. Spatial and temporal variation of diet within a presumed metapopulation of Adélie Penguins. The Condor 105: 95-106. doi:10.1093/condor/105.1.95

AINLEY, D. G. & BLIGHT, L. K. 2009. Ecological repercussions of historical fish extraction from the southern ocean. Fish and Fisheries 10: 13-38.

BALLANCE, L., PITMAN, R., HEWITT, R. P., SINIFF, D. B., TRIVELPIECE, W. Z., CLAPHAM, P. J. & BROWNELL, R. L. 2006. The removal of large whales from the Southern Ocean: evidence for long-term ecosystem effects? In: ESTES, J. A., DEMASTER, D. P., DOAK, D. F., WILLIAMS, T. E., BROWNELL, R. L. (Eds.) Whales, Whaling and Ocean Ecosystems. Berkeley, USA: University of California Press, pp 215-230.

BARQUETE, V., STRAUSS, V. & RYAN, P. G. 2013. Stable isotope turnover in blood and claws: A case study in captive African Penguins. Journal of Experimental Marine Biology and Ecology 448: 121-127. doi:10.1016/j.jembe.2013.06.021

BARRETT, R. T., CAMPHUYSEN, C. J., ANKER-NILSSEN, T. ET AL. 2007. Diet studies of seabirds: a review and recommendations. ICES Journal of Marine Science 64: 1675-1691. doi:10.1093/icesjms/fsm152

BARRERA-ORO, E., MARSCHOFF, E. & AINLEY, D. 2017. Changing status of three notothenioid fish at the South Shetland Islands (1983-2016) after impacts of the 1970-80s commercial fishery. Polar Biology 40: 2047-2054. doi:10.1007/s00300-017-2125-0

BATES, D., MAECHLER, M., BOLKER, B. & WALKER, S. 2015.  Fitting Linear Mixed Effects Models Using lme4. Journal of Statistical Software 67:1-48. doi:10.18637/jss.v067.i01

BEARHOP, S., FURNESS, R. W., HILTON, G. M., VOTIER, S. C. & WALDRON, S. 2003. A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Functional Ecology 17: 270-275. doi:10.1046/j.1365-2435.2003.00725.x

BRANCH, T. A. 2011. Humpback whale abundance south of 60°S from three complete circumpolar sets of surveys. Journal of Cetacean Research and Management (Special Issue) 3: 53-69.

CAMPRASSE, E. C. M., CHEREL, Y., BUSTAMANTE, P., ARNOULD, J. P. & BOST, C. 2017. Intra- and inter-individual variation in the foraging ecology of a generalist subantarctic seabird, the gentoo penguin. Marine Ecology Progress Series 568: 227-242. doi:10.3354/meps12151

CARLINI, A. R., CORIA, N. R., SANTOS, M. M. NEGRETE, J., JUÁRES, M. A. & DANERI, G. A. 2009. Responses of Pygoscelis adeliae and P. papua populations to environmental changes at Isla 25 de Mayo (King George Island). Polar Biology 32: 1427-1433. doi:10.1007/s00300-009-0637-y

CCAMLR. 2016. Report on the monitoring program of chinstrap and gentoo penguins at Narębski Point (ASPA No. 171), King George Island, since 2006. WG-EMM-16/62. Tasmania, Australia: Commission for the Conservation of Antarctic Marine Living Resources. 

CHEREL Y., HOBSON, K. A., BAILLEUL, F. & GROSCOLAS, R. 2005. Nutrition, physiology, and stable isotopes: New information from fasting and molting penguins. Ecology 86: 2881-2888.

CHEREL Y. & HOBSON, K. A. 2007. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology Progress Series 329: 281-287. doi:10.3354/meps329281

COX, M. J., CANDY, S., DE LA MARE, W. K., NICOL, S., KAWAGUCHI, S. & GALES, N. 2018. No evidence for a decline in the density of Antarctic krill Euphausia superba Dana, 1850, in the Southwest Atlantic sector between 1976 and 2016. Journal of Crustacean Biology 38: 656-661. doi:10.1093/jcbiol/ruy072.

DALERUM, F. & ANGERBJÖRN, A. 2005. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144: 647-658. doi:10.1007/s00442-005-0118-0

DIMITRIJEVIĆ, D., PAIVA, V. H., RAMOS, J. A., ET AL. 2018. Isotopic niches of sympatric Gentoo and Chinstrap Penguins: evidence of competition for Antarctic krill? Polar Biology 41: 1655-1669. doi:10.1007/s00300-018-2306-5

DUCKLOW, H. W., BAKER, K., MARTINSON, D. G. ET AL. 2006. Marine pelagic ecosystems: the West Antarctic Peninsula. Philosophical Transactions of the Royal Society B: Biological Sciences 362: 67-94. doi:10.1098/rstb.2006.1955

EMSLIE, S. D. & PATTERSON, W.  2007. Abrupt recent shift in 13C and 15N values in Adélie penguin eggshell in Antarctica. Proceedings of the National Academy of Sciences 104: 11666-11669.

EMSLIE, S. D., POLITO, M. J., BRASSO, R., PATTERSON, W. P. & SUN, L. 2014 Ornithogenic soils and the paleoecology of pygoscelid penguins in Antarctica. Quaternary International 352: 4-15. doi:10.1016/j.quaint.2014.07.031

EMSLIE, S. D., ROMERO, M., JUÁRES, M. A. & ARGOTA, M. R. 2020. Holocene occupation history of pygoscelid penguins at Stranger Point, King George (25 de Mayo) Island, northern Antarctic Peninsula. The Holocene. 30: 190-196. doi:10.1177/0959683619875814

FLORES, H., ATKINSON, A., KAWAGUCHI S. ET AL. 2012. Impact of climate change on Antarctic krill. Marine Ecology Progress Series 458: 1-19.

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

GIRAUDOUX, P. 2018. pgirmess: Spatial Analysis and Data Mining for Field Ecologists. R package version 1.6.9. R Foundation for Statistical Computing, Vienna, Austria.  https://CRAN.R-project.org/package=pgirmess

GORMAN, K. B., WILLIAMS, T. D. & FRASER, W. R. 2014. Ecological sexual dimorphism and environmental variability within a community of Antarctic penguins (genus Pygoscelis). PLoS One 9: e90081. doi:10.1371/journal.pone.0090081

HERMAN, R. W., VALLS, F. C. L., HART, T., PETRY, M. V., TRIVELPIECE, W. Z. & POLITO, M. J. 2017. Seasonal consistency and individual variation in foraging strategies differ among and within Pygoscelis penguin species in the Antarctic Peninsula region. Marine Biology 164: 115.

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

HOTHORN, T., BRETZ, F. & WESTFALL, P. 2008. Simultaneous inference in general parametric models. Biometrical Journal 50: 346-363. doi:10.1002/bimj.200810425

JUÁRES, M. A. 2013. Biología reproductiva y ecología trófica de dos especies simpátricas del género Pygoscelis en las islas Shetland del Sur, Antártida. Phd thesis. La Plata, Argentina: Universidad Nacional de La Plata.

JUÁRES, M. A., SANTOS, M. M., NEGRETE, J. ET AL. 2013. Better late than never? Interannual and seasonal variability in breeding chronology of gentoo penguins at Stranger Point, Antarctica. Polar Research 32: 18448. doi:10.3402/polar.v32i0.18448

JUÁRES, M. A., SANTOS, M. M., NEGRETE, J. ET AL. 2015. Adélie penguin population changes at Stranger Point: 19 years of monitoring. Antarctic Science 27: 455-461. doi:10.1017/S0954102015000152

JUÁRES, M. A, CASAUX, R., CORBALAN, A. ET AL. 2018. Diet of Adélie penguins (Pygoscelis adeliae) at Stranger Point (25 de Mayo/King George Island, Antarctica) over a 13-year period (2003-2015). Polar Biology 41: 303-311. doi:10.1007/s00300-017-2191-3

JUÁRES, M. A., CASAUX, R., NEGRETE, J. ET AL. 2020. Update of the population size and breeding performance of gentoo penguins (Pygoscelis papua) at Stranger Point/Cabo Funes, South Shetland Islands. Polar Biology 43: 123-129. doi:10.1007/s00300-019-02614-0

KARNOVSKY, N. J., HOBSON, K. A. & IVERSON, S. J. 2012. From lavage to lipids: estimating diets of seabirds. Marine Ecology Progress Series 451: 263-284. doi:10.3354/meps09713

KEENAN, S. W. & DEBRUYN, J. M. 2019. Changes to vertebrate tissue stable isotope (δ15N) composition during decomposition. Scientific reports 9: 9929. doi:10.1038/s41598-019-46368-5

KELLY, J. F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78: 1-27. doi:10.1139/z99-165

KOKUBUN, N., TAKAHASHI, A., MORI, Y., WATANABE, S. & SHIN, H. 2010. Comparison of diving behavior and foraging habitat use between chinstrap and gentoo penguins breeding in the South Shetland Islands, Antarctica. Marine Biology 157: 811-825. doi:10.1007/s00227-009-1364-1

KRISTAN, A. K., EMSLIE, S. D. & PATTERSON, W. P. 2019. Stable isotope analyses of ancient and modern Adélie Penguin (Pygoscelis adeliae) mummies from the Ross Sea Region, Antarctica. Polar Biology 42: 1183-1192. doi:10.1007/s00300-019-02513-4

KUZNETSOVA, A., BROCKHOFF, P. B. & CHRISTENSEN, R. H. B. 2017. lmerTest Package: Tests in Linear Mixed Effects Models. Journal of Statistical Software 82: 1-26. doi:10.18637/jss.v082.i13

LA MESA, M., RIGINELLA, E., MAZZOLDI, C. & ASHFORD, J. 2015. Reproductive resilience of ice-dependent Antarctic silverfish in a rapidly changing system along the Western Antarctic Peninsula. Marine Ecology 36: 235-245.

LIDEN, K., TAKAHASHI, C. & NELSON, D. E. 1995. The Effects of Lipids in Stable Carbon Isotope Analysis and the Effects of NaOH Treatment on the Composition of Extracted Bone Collagen. Journal of Archaeological Science 22: 321-326. doi:10.1006/jasc.1995.0034

LOURENÇO, P. M., GRANADEIRO, J. P., GUILHERME, J. L. & CATRY, T. 2015. Turnover rates of stable isotopes in avian blood and toenails: implications for dietary and migration studies. Journal of Experimental Marine Biology and Ecology 472: 89-96. doi:10.1016/j.jembe.2015.07.006

MILLER, A. K., KAPPES, M. A., TRIVELPIECE, S. G. & TRIVELPIECE, W. Z. 2010. Foraging-niche separation of breeding gentoo and chinstrap penguins, South Shetland Islands, Antarctica. The Condor 112: 683-695. doi:10.1525/cond.2010.090221

POLITO, M. J., FISHER, S., TOBIAS, C. R. & EMSLIE, S. D. 2009. Tissue-specific isotopic discrimination factors in gentoo penguin (Pygoscelis papua) egg components: Implications for dietary reconstruction using stable isotopes. Journal of Experimental Marine Biology and Ecology 372: 106-112. doi:10.1016/j.jembe.2009.02.014

POLITO M. J., TRIVELPIECE, W. Z., KARNOSVSKY, N. J., NG, E., PATTERSON, W. P. & EMSLIE S. D. 2011. Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins. PLoS One 6: e26642. doi:10.1371/journal.pone.0026642

POLITO, M. J., TRIVELPIECE, W. Z., PATTERSON, W. P., KARNOVSKY, N. J., REISS, C. S. & EMSLIE, S. D. 2015. Contrasting specialist and generalist patterns facilitate foraging niche partitioning in sympatric populations of Pygoscelis penguins. Marine Ecology Progress Series 519: 221-237. doi: 10.3354/meps11095

R DEVELOPMENT CORE TEAM (2019). R: A language and environment for statistical computing. Vienna, Austria: The R Foundation for Statistical Computing. 

ROMBOLÁ, E. F., MARSCHOFF, E. & CORIA, N. 2010. Inter-annual variability in Chinstrap penguin diet at South Shetland and South Orkneys Islands. Polar Biology 33: 799-806. doi:10.1007/s00300-009-0757-4

SANTORA, J. A., LARUE, M. A. & AINLEY, D. G. 2020. Geographic structuring of Antarctic penguin populations. Global Ecology and Biogeography 29: 1716-1728. doi:10.1111/geb.13144

SEALY, J., JOHNSON, M., RICHARDS, M. & NEHLICH, O. 2014. Comparison of two methods of extracting bone collagen for stable carbon and nitrogen isotope analysis: comparing whole bone demineralization with gelatinization and ultrafiltration. Journal of Archaeological Science 47: 64-69. doi:10.1016/j.jas.2014.04.011

SWEETING, C. J., POLUNIN, N. V. C. & JENNINGS, S. 2006. Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Communications in Mass Spectrometry 20: 595-601. doi:10.1002/rcm.2347

TRIVELPIECE W. Z., TRIVELPIECE, S. G. & VOLKMAN, N. J. 1987. Ecological segregation of Adélie, gentoo, and chinstrap penguins at King George Island, Antarctica. Ecology 68: 351-361. doi:10.2307/1939266

VASIL, C.A., POLITO, M. J., PATTERSON, W. P. & Emslie, S. D. 2012. Wanted: dead or alive? Isotopic analysis (δ13C and δ15N) of Pygoscelis penguin chick tissues supports opportunistic sampling. Rapid Communication in Mass Spectrometry 26: 487-493.

VAUGHAN, D. G., MARSHALL, G. J., CONNOLLEY, W. M. ET AL. 2003. Recent rapid regional climate warming on the Antarctic Peninsula. Climatic Change 60: 243-274. doi: 10.1023/A:1026021217991

WICKHAM, H. 2016. ggplot2: Elegant Graphics for Data Analysis. New York, USA: Springer-Verlag.

WILLIAMS, T. D. 1995. The Penguins. Oxford, UK: Oxford University Press. 

© Marine Ornithology 2022