Hostname: page-component-77f85d65b8-5ngxj Total loading time: 0 Render date: 2026-03-28T13:22:35.943Z Has data issue: false hasContentIssue false
  • English
  • Français

Assessment of trophic segregation amongst gentoo penguin (Pygoscelis papua) individuals in Antarctica using a non-invasive methodology

Published online by Cambridge University Press:  15 March 2024

Lucía Rabinovich-Larrechea Open the ORCID record for Lucía Rabinovich-Larrechea [Opens in a new window] ,
Daniel E. Naya ,
Mariana Cosse ,
Nadia Bou  and
Valentina Franco-Trecu
Lucía Rabinovich-Larrechea*
Affiliation:
Department of Ecology and Evolution, Faculty of Sciences, University of the Republic, Montevideo, Uruguay
Daniel E. Naya
Affiliation:
Department of Ecology and Evolution, Faculty of Sciences, University of the Republic, Montevideo, Uruguay Museum of Vertebrate Zoology, University of California, Berkeley, CA, USA
Mariana Cosse
Affiliation:
Department of Biodiversity and Genetics, Clemente Estable Biological Research Institute (IIBCE-MEC), Montevideo, Uruguay
Nadia Bou
Affiliation:
Department of Biodiversity and Genetics, Clemente Estable Biological Research Institute (IIBCE-MEC), Montevideo, Uruguay
Valentina Franco-Trecu
Affiliation:
Department of Ecology and Evolution, Faculty of Sciences, University of the Republic, Montevideo, Uruguay
*
lrabinovich@fcien.edu.uy
Get access Rights & Permissions [Opens in a new window]

Abstract

Individual trophic specialization (ITS) refers to the trophic diversification amongst individuals within a population. The gentoo penguin (Pygoscelis papua) is considered a trophic generalist at the population level, but little is known about its individual trophic differentiation. We assessed the degree of ITS at one of its main breeding colonies: Ardley Island, South Shetland Islands. We used skin from 19 dead individuals to determine species and sex by molecular methods and a nail for stable isotope analysis of δ15N and δ13C. Isotopic niche metrics and ITS were estimated for the population and for each sex. We found a moderately high degree of ITS associated with the trophic position of the resources consumed (δ15N) for the population and both sexes, as well as a moderate degree of ITS in the foraging habitat (δ13C) for the population and females. Females showed a higher exclusive niche area, suggesting that they use resources and foraging areas that males do not, probably related to reproductive energy demands. Given the high population density of this species, ITS could function as a mechanism to decrease intraspecific competition. This combination of genetic and isotopic tools allowed us to provide relevant information on the trophic ecology of the gentoo penguin without manipulating animals or using invasive methods.

Keywords

intrapopulation variationpenguinsstable isotope analysistrophic ecology

Information

Type
Biological Sciences
Information
Antarctic Science , Volume 36 , Issue 1 , February 2024 , pp. 10 - 19
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Antarctic Science Ltd

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.)

Article purchase

Temporarily unavailable

References

Ainley, D.G., Ballard, G., Barton, K.J., Karl, B.J., Rau, G.H., Ribic, C.A. & Wilson, P.R. 2003. Spatial and temporal variation of diet within a presumed metapopulation of Adélie penguins. The Condor, 105, 10.1093/condor/105.1.95.CrossRefGoogle Scholar
Araújo, M.S., Bolnick, D.I. & Layman, C.A. 2011. The ecological causes of individual specialisation. Ecology Letters, 14, 10.1111/j.1461-0248.2011.01662.x.CrossRefGoogle ScholarPubMed
ASPA. 2009. No. 150 Ardley Island, King George Island: Management Plan. Retrieved from https://www.env.go.jp/nature/nankyoku/kankyohogo/database/jyouyaku/aspa/aspa_pdf_en/150.pdfGoogle Scholar
Black, C.E. 2016. A comprehensive review of the phenology of Pygoscelis penguins. Polar Biology, 39, 10.1007/s00300-015-1807-8.CrossRefGoogle Scholar
Bolnick, D.I., Svanbäck, R., Araújo, M.S. & Persson, L. 2007. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proceedings of the National Academy of Sciences of the United States of America, 104, 10.1073/pnas.0703743104.Google ScholarPubMed
Bolnick, D.I., Yang, L.H., Fordyce, J.A., Davis, J.M. & Svanbäck, R. 2002. Measuring individual-level resource specialization. Ecology, 83, 10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2.CrossRefGoogle Scholar
Bolnick, D.I., Svanbäck, R., Fordyce, J.A., Yang, L.H., Davis, J.M., Hulsey, C.D. & Forister, M.L. 2003. The ecology of individuals: incidence and implications of individual specialization. American Naturalist, 161, 10.1086/343878.CrossRefGoogle ScholarPubMed
Brault, E.K., Koch, P.L., McMahon, K.W., Broach, K.H., Rosenfield, A.P., Sauthoff, W., et al. 2018. Carbon and nitrogen zooplankton isoscapes in West Antarctica reflect oceanographic transitions. Marine Ecology Progress Series, 593, 10.3354/meps12524.CrossRefGoogle Scholar
Cherel, Y., Hobson, K.A., Guinet, C. & Vanpe, 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, 10.1111/j.1365-2656.2007.01238.x.CrossRefGoogle Scholar
Clucas, G. V., Dunn, M.J., Dyke, G., Emslie, S.D., Naveen, R., Polito, M.J., et al. 2014. A reversal of fortunes: climate change ‘winners’ and ‘losers’ in Antarctic Peninsula penguins. Scientific Reports, 4, 10.1038/srep05024.CrossRefGoogle ScholarPubMed
Costa-Pereira, R. & Araújo, M.S. 2022. Individual specialization. Encyclopedia of Biodiversity, 6, 10.1016/b978-0-12-822562-2.00068-2.Google Scholar
Costa-Pereira, R., Rudolf, V.H.W., Souza, F.L. & Araújo, M.S. 2018. Drivers of individual niche variation in coexisting species. Journal of Animal Ecology, 87, 10.1111/1365-2656.12879.CrossRefGoogle ScholarPubMed
Dall, S.R.X., Bell, A.M., Bolnick, D.I. & Ratnieks, F.L.W. 2012. An evolutionary ecology of individual differences. Ecology Letters, 15, 10.1111/j.1461-0248.2012.01846.x.CrossRefGoogle ScholarPubMed
DE Lima, R.C., Franco-Trecu, V., Carrasco, T.S., Inchausti, P., Secchi, E.R. & Botta, S. 2022. Segregation of diets by sex and individual in South American fur seals. Aquatic Ecology, 56, 10.1007/s10452-021-09915-9.CrossRefGoogle Scholar
Firla, M., Mustafa, O., Pfeifer, C., Senf, M. & Hese, S. 2019. Intraseasonal variability of guano stains in a remotely sensed penguin colony using UAV and satellite. ISPRS Annals of the Photogrammetry, Remote Sensing and Spatial Information Sciences, 4, 10.5194/isprs-annals-IV-2-W5-111-2019.Google Scholar
France, R.L. 1995. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnology and Oceanography, 40, 10.4319/lo.1995.40.7.1310.CrossRefGoogle Scholar
González, S., Cosse, M., Del Rosario Franco, M., Emmons, L., Vynne, C., Duarte, J.M.B., et al. 2015. Population structure of mtDNA variation due to Pleistocene fluctuations in the South American maned wolf (Chrysocyon brachyurus, Illiger, 1815): management units for conservation. Journal of Heredity, 106, 10.1093/jhered/esv043.CrossRefGoogle ScholarPubMed
Gorman, K.B. 2015. Integrative studies of Southern Ocean food- webs and Pygoscelis penguin demography: mechanisms of population response to environmental change. Doctor of Philosophy thesis. Burnaby, BC: Simon Fraser University, 311 pp.Google Scholar
Griffiths, R., Double, M.C., Orr, K. & Dawson, R.J.G. 1998. A DNA test to sex most birds. Molecular Ecology, 7, 10.1046/j.1365-294x.1998.00389.x.CrossRefGoogle ScholarPubMed
Hadfield, J.D. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software, 33, 10.18637/jss.v033.i02.CrossRefGoogle Scholar
Handley, J.M., Connan, M., Baylis, A.M.M., Brickle, P. & Pistorius, P. 2017. Jack of all prey, master of some: influence of habitat on the feeding ecology of a diving marine predator. Marine Biology, 164, 10.1007/s00227-017-3113-1.CrossRefGoogle Scholar
Herman, R.W. 2016. Investigating species and population level foraging variation and individual specialization in Pygoscelis penguins using stable isotope analysis. Thesis. Baton Rouge, LA: Louisiana State University, 73 pp.Google Scholar
Hinke, J.T., Polito, M.J., Reiss, C.S., Trivelpiece, S.G. & Trivelpiece, W.Z. 2012. Flexible reproductive timing can buffer reproductive success of Pygoscelis spp. penguins in the Antarctic Peninsula region. Marine Ecology Progress Series, 454, 10.3354/meps09633.Google Scholar
Ingram, T., Costa-Pereira, R. & Araújo, M.S. 2018. The dimensionality of individual niche variation. Ecology, 99, 10.1002/ecy.2129.CrossRefGoogle ScholarPubMed
Jackson, A.L., Inger, R., Parnell, A.C. & Bearhop, S. 2011. Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology, 80, 10.1111/j.1365-2656.2011.01806.x.CrossRefGoogle ScholarPubMed
Jaeger, A., Blanchard, P., Richard, P. & Cherel, Y. 2009. Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Marine Biology, 156, 10.1007/s00227-009-1165-6.CrossRefGoogle Scholar
Karnovsky, N.J. 1997. The fish component of Pygoscelis penguin diets. Master of Science in Biological Sciences thesis. Bozeman, MT: Montana State University, 76 pp.Google Scholar
Kokubun, N., Takahashi, A., Mori, Y., Watanabe, S. & Shin, H.C. 2010. Comparison of diving behavior and foraging habitat use between chinstrap and gentoo penguins breeding in the South Shetland Islands, Antarctica. Marine Biology, 157, 10.1007/s00227-009-1364-1.CrossRefGoogle Scholar
Layman, C.A., Arrington, D.A., Montaña, C.G. & Post, D.M. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology, 88, 10.1890/08-0167.1.CrossRefGoogle ScholarPubMed
Lescroël, A., Dugger, K.M., Ballard, G. & Ainley, D.G. 2009. Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. Journal of Animal Ecology, 78, 10.1111/j.1365-2656.2009.01542.x.CrossRefGoogle ScholarPubMed
Lescroël, A., Ballard, G., Grémillet, D., Authier, M. & Ainley, D.G. 2014. Antarctic climate change: extreme events disrupt plastic phenotypic response in Adélie penguins. PLoS ONE, 9, 10.1371/journal.pone.0085291.CrossRefGoogle ScholarPubMed
Lescroël, A., Lyver, P.O., Jongsomjit, D., Veloz, S., Dugger, K.M., Kappes, P., et al. 2020. Inter-individual differences in the foraging behavior of breeding Adélie penguins are driven by individual quality and sex. Marine Ecology Progress Series, 636, 10.3354/meps13208.CrossRefGoogle Scholar
Marschoff, E.R., Barrera-Oro, E.R., Alescio, N.S. & Ainley, D.G. 2012. Slow recovery of previously depleted demersal fish at the South Shetland Islands, 1983–2010. Fisheries Research, 125–126, 10.1016/j.fishres.2012.02.017.Google Scholar
Massaro, M., Ainley, D.G., Santora, J.A., Quillfeldt, P., Lescroël, A., Whitehead, A., et al. 2020. Diet segregation in Adélie penguins: some individuals attempt to overcome colony-induced and annual foraging challenges. Marine Ecology Progress Series, 645, 10.3354/meps13370.CrossRefGoogle Scholar
McMahon, K.W., Hamady, L.L. & Thorrold, S.R. 2013. A review of ecogeochemistry approaches to estimating movements of marine animals. Limnology and Oceanography, 58, 10.4319/lo.2013.58.2.0697.CrossRefGoogle Scholar
McMahon, K.W., Michelson, C.I., Hart, T., McCarthy, M.D., Patterson, W.P. & Polito, M.J. 2019. Divergent trophic responses of sympatric penguin species to historic anthropogenic exploitation and recent climate change. Proceedings of the National Academy of Sciences of the United States of America, 116, 10.1073/pnas.1913093116.Google ScholarPubMed
Naya, D.E. & Franco-Trecu, V. 2019. An unbiased method to estimate individual specialisation from multi-tissue isotopic data. Freshwater Biology, 64, 10.1111/fwb.13316.CrossRefGoogle Scholar
Negrete, P., Sallaberry, M., Barceló, G., Maldonado, K., Perona, F., McGill, R.A.R., et al. 2016. Temporal variation in isotopic composition of Pygoscelis penguins at Ardley Island, Antarctic: are foraging habits impacted by environmental change? Polar Biology, 40, 10.1007/s00300-016-2017-8.Google Scholar
Newsome, S.D., Tinker, M.T., Monson, D.H., Oftedal, O.T., Ralls, K., Staedler, M.M., et al. 2009. Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology, 90, 10.1890/07-1812.1.CrossRefGoogle ScholarPubMed
Patel, S., Waugh, J., Millar, C.D. & Lambert, D.M. 2010. Conserved primers for DNA barcoding historical and modern samples from New Zealand and Antarctic birds. Molecular Ecology Resources, 10, 10.1111/j.1755-0998.2009.02793.x.CrossRefGoogle ScholarPubMed
Pickett, E.P., Fraser, W.R., Patterson-Fraser, D.L., Cimino, M.A., Torres, L.G. & Friedlaender, A.S. 2018. Spatial niche partitioning may promote coexistence of Pygoscelis penguins as climate-induced sympatry occurs. Ecology and Evolution, 8, 10.1002/ece3.4445.CrossRefGoogle ScholarPubMed
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. 2021. nlme: linear and nonlinear mixed effects models. R package version 3.1-153 Retrieved from https://cran.r-project.org/package=nlmeGoogle Scholar
Polito, M.J., Lynch, H.J., Naveen, R. & Emslie, S.D. 2011. Stable isotopes reveal regional heterogeneity in the pre-breeding distribution and diets of sympatrically breeding Pygoscelis spp. penguins. Marine Ecology Progress Series, 421, 10.3354/meps08863.Google Scholar
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, 10.3354/meps11095.CrossRefGoogle Scholar
Post, D.M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83, 10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2.CrossRefGoogle Scholar
R Core Team. 2020. R: a language and environment for statistical computing Retrieved from https://www.r-project.org/Google Scholar
Roberts, S.J., Monien, P., Foster, L.C., Loftfield, J., Hocking, E.P., Schnetger, B., et al. 2017. Past penguin colony responses to explosive volcanism on the Antarctic Peninsula. Nature Communications, 8, 10.1038/ncomms14914.CrossRefGoogle ScholarPubMed
Roughgarden, J. 1972. Evolution of niche width. The American Naturalist, 106, 10.1086/282892.CrossRefGoogle Scholar
Roughgarden, J. 1974. Niche width: biogeographic patterns among Anolis lizard populations. The American Naturalist, 108, 429–442.CrossRefGoogle Scholar
Silva, L.A., Siles, L., Cardona, L., Tavares, M., Crespo, E. & Gandini, P. 2015. Diferencias estacionales en la dieta de individuos juveniles del Pingüino Patagónico (Spheniscus magellanicus) reveladas en base al análisis de isótopos estables en uñas. [Seasonal differences in the diet of juvenile Patagonian penguins (Spheniscus magellanicus) revealed by stable isotope analysis of nails]. Hornero, 30, 45–54.CrossRefGoogle Scholar
Trivelpiece, W.Z. & Trivelpiece, S.G. 1990. Courtship period of Adélie, gentoo, and chinstrap penguins. In Davis, L.S. & Darby, J.T., eds, Penguin biology. Cambridge, MA: Academic Press, 113–127.Google Scholar
Valenzuela-Guerra, P., Morales-Moraga, D., González-Acuña, D. & Vianna, J.A. 2013. Geographic morphological variation of gentoo penguin (Pygoscelis papua) and sex identification: using morphometric characters and molecular markers. Polar Biology, 36, 10.1007/s00300-013-1389-2.CrossRefGoogle Scholar
Vander Zanden, H.B., Bjorndal, K.A., Reich, K.J. & Bolten, A.B. 2010. Individual specialists in a generalist population: results from a long-term stable isotope series. Biology Letters, 6, 10.1098/rsbl.2010.0124.CrossRefGoogle Scholar
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 Communications in Mass Spectrometry, 26, 10.1002/rcm.5340.CrossRefGoogle ScholarPubMed
Werle, E., Schneider, C., Renner, M., Volker, M. & Fiehn, W. 1994. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22, 4354–4355.CrossRefGoogle ScholarPubMed
Zaccarelli, N., Bolnick, D.I. & Mancinelli, G. 2013. RInSp: an R package for the analysis of individual specialization in resource use. Methods in Ecology and Evolution, 4, 10.1111/2041-210X.12079.CrossRefGoogle Scholar