Fast climate changes in the western Antarctic Peninsula are reducing krill density, which along with increased fishing activities in recent decades, may have had synergistic effects on penguin populations. We tested that assumption by crossing data on fishing activities and Southern Annular Mode (an indicator of climate change in Antarctica) with penguin population data. Increases in fishing catch during the non-breeding period were likely to result in impacts on both chinstrap (Pygoscelis antarcticus) and gentoo (P. papua) populations. Catches and climate change together elevated the probability of negative population growth rates: very high fishing catch on years with warm winters and low sea ice (associated with negative Southern Annular Mode values) implied a decrease in population size in the following year. The current management of krill fishery in the Southern Ocean takes into account an arbitrary and fixed catch limit that does not reflect the variability of the krill population under effects of climate change, therefore affecting penguin populations when the environmental conditions were not favorable.
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Atkinson, A., V. Siegel, E.A. Pakhomov, M.J. Jessopp, and V. Loeb. 2009. A re-appraisal of the total biomass and annual production of Antarctic krill. Deep-Sea Research Part I: Oceanographic Research Papers 56: 727–740. https://doi.org/10.1016/j.dsr.2008.12.007.
Atkinson, A., S.L. Hill, E.A. Pakhomov, V. Siegel, C.S. Reiss, V.J. Loeb, D.K. Steinberg, K. Schmidt, et al. 2019. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nature Climate Change 9: 142–147. https://doi.org/10.1038/s41558-018-0370-z.
Ballerini, T., E.E. Hofmann, D.G. Ainley, K. Daly, M. Marrari, C.A. Ribic, W.O. Smith, and J.H. Steele. 2014. Productivity and linkages of the food web of the southern region of the western Antarctic Peninsula continental shelf. Progress in Oceanography 122: 10–29. https://doi.org/10.1016/j.pocean.2013.11.007.
Brooks, C.M., L.B. Crowder, L.M. Curran, R.B. Dunbar, D.G. Ainley, K.J. Dodds, K.M. Gjerde, and U.R. Sumaila. 2016. Science-based management in decline in the Southern Ocean. Science 354: 185–187. https://doi.org/10.1126/science.aah4119.
Casanovas, P., R. Naveen, S. Forrest, J. Poncet, and H.J. Lynch. 2015. A comprehensive coastal seabird survey maps out the front lines of ecological change on the western Antarctic Peninsula. Polar Biology.. https://doi.org/10.1007/s00300-015-1651-x.
CCAMLR. 2018. Krill Fishery Report. Commission for the Conservation of Antarctic Marine Living Resources. Hobart: CCAMLR.
CCAMLR. 2019. Report of the Thirty-Eighth Meeting of the Scientific Committee. Hobart: CCAMLR.
Che-Castaldo, C., S. Jenouvrier, C. Youngflesh, K.T. Shoemaker, G. Humphries, P. McDowall, L. Landrum, M.M. Holland, et al. 2017. Pan-Antarctic analysis aggregating spatial estimates of Adélie penguin abundance reveals robust dynamics despite stochastic noise. Nature Communications 8: 832. https://doi.org/10.1038/s41467-017-00890-0.
Chirico, A.A.D., T.R. McClanahan, and J.S. Eklöf. 2017. Community- and government-managed marine protected areas increase fish size, biomass and potential value. PLoS ONE 12: e0182342. https://doi.org/10.1371/journal.pone.0182342.
Clem, K.R., J.A. Renwick, J. McGregor, and R.L. Fogt. 2016. The relative influence of ENSO and SAM on Antarctic Peninsula climate. Journal of Geophysical Research 121: 9324–9341. https://doi.org/10.1002/2016JD025305.
Coetzee, B.W.T., P. Convey, and S.L. Chown. 2017. Expanding the Protected Area Network in Antarctica is urgent and readily achievable. Conservation Letters 10: 670–680. https://doi.org/10.1111/conl.12342.
Constable, A.J. 2011. Lessons from CCAMLR on the implementation of the ecosystem approach to managing fisheries. Fish and Fisheries 12: 138–151. https://doi.org/10.1111/j.1467-2979.2011.00410.x.
Constable, A.J., and S. Nicol. 2002. Defining smaller-scale management units to further develop the ecosystem approach in managing large-scale pelagic krill fisheries in Antarctica. CCAMLR Science 9: 117–131.
Cook, A.J., P.R. Holland, M.P. Meredith, T. Murray, A. Luckman, and D.G. Vaughan. 2016. Ocean forcing of glacier retreat in the western Antarctic Peninsula. Science 353: 283–286. https://doi.org/10.1126/science.aae0017.
Dahood, A., G.M. Watters, and K. de Mutsert. 2019. Using sea-ice to calibrate a dynamic trophic model for the Western Antarctic Peninsula. PLoS ONE 14: 1–28. https://doi.org/10.1371/journal.pone.0214814.
Doddridge, E.W., and J. Marshall. 2017. Modulation of the seasonal cycle of Antarctic Sea ice extent related to the southern annular mode. Geophysical Research Letters 44: 9761–9768. https://doi.org/10.1002/2017GL074319.
Duffy, J.E., J.S. Lefcheck, R.D. Stuart-Smith, S.A. Navarrete, and G.J. Edgar. 2016. Biodiversity enhances reef fish biomass and resistance to climate change. Proceedings of the National Academy of Sciences of USA 113: 6230–6235. https://doi.org/10.1073/pnas.1524465113.
Eveleth, R., N. Cassar, S.C. Doney, D.R. Munro, and C. Sweeney. 2017a. Biological and physical controls on O2/Ar, Ar and pCO2 variability at the Western Antarctic Peninsula and in the Drake Passage. Deep-Sea Research Part II: Topical Studies in Oceanography 139: 77–88. https://doi.org/10.1016/j.dsr2.2016.05.002.
Eveleth, R., N. Cassar, R.M. Sherrell, H. Ducklow, M.P. Meredith, H.J. Venables, Y. Lin, and Z. Li. 2017b. Ice melt influence on summertime net community production along the Western Antarctic Peninsula. Deep-Sea Research Part II: Topical Studies in Oceanography 139: 89–102. https://doi.org/10.1016/j.dsr2.2016.07.016.
Flores, H., A. Atkinson, S. Kawaguchi, B.A. Krafft, G. Milinevsky, S. Nicol, C. Reiss, G.A. Tarling, et al. 2012. Impact of climate change on Antarctic krill. Marine Ecology Progress Series 458: 1–19. https://doi.org/10.3354/meps09831.
Forcada, J., P.N. Trathan, K. Reid, E.J. Murphy, and J.P. Croxall. 2006. Contrasting population changes in sympatric penguin species in association with climate warming. Global Change Biology 12: 411–423. https://doi.org/10.1111/j.1365-2486.2006.01108.x.
Fraser, W.R., W.Z. Trivelpiece, D.G. Ainley, and S.G. Trivelpiece. 1992. Increases in Antarctic penguin populations: Reduced competition with whales or a loss of sea ice due to environmental warming? Polar Biology 11: 525–531. https://doi.org/10.1007/BF00237945.
Gong, D., and S. Wang. 1999. Definition of Antarctic oscillation index. Geophysical Research Letters 26: 459–462. https://doi.org/10.1029/1999GL900003.
Hijmans, M.R.J. 2013. Geographic data analysis and modeling. The Comprehensive R Archive Network CRAN. https://cran.r-project.org/web/packages/raster/raster.pdf.
Hill, S.L., A. Atkinson, C. Darby, S. Fielding, B.A. Krafft, O.R. Godø, G. Skaret, P.N. Trathan, et al. 2016. Is current management of the Antarctic krill fishery in the Atlantic sector of the Southern Ocean precautionary? CCAMLR Science 23: 31–51.
Hinke, J.T., K. Salwicka, S.G. Trivelpiece, G.M. Watters, and W.Z. Trivelpiece. 2007. Divergent responses of Pygoscelis penguins reveal a common environmental driver. Oecologia 153: 845–855. https://doi.org/10.1007/s00442-007-0781-4.
Hinke, J.T., M.J. Polito, M.E. Goebel, S. Jarvis, C.S. Reiss, S.R. Thorrold, W.Z. Trivelpiece, and G.M. Watters. 2015. Spatial and isotopic niche partitioning during winter in chinstrap and Adélie penguins from the South Shetland Islands. Ecosphere 6: art125. https://doi.org/10.1890/es14-00287.1.
Hinke, J.T., A.M. Cossio, M.E. Goebel, C.S. Reiss, W.Z. Trivelpiece, and G.M. Watters. 2017. Identifying Risk: Concurrent overlap of the Antarctic krill fishery with krill-dependent predators in the scotia sea. PLoS ONE 12: e0170132. https://doi.org/10.1371/journal.pone.0170132.
Hofmann, E.E., P.H. Wiebe, D.P. Costa, and J.J. Torres. 2011. Introduction to understanding the linkages between Antarctic food webs and the environment: A synthesis of Southern Ocean GLOBEC studies. Deep-Sea Research Part II: Topical Studies in Oceanography 58: 1505–1507. https://doi.org/10.1016/j.dsr2.2011.02.001.
Humphries, G.R.W., R. Naveen, M. Schwaller, C. Che-Castaldo, P. McDowall, M. Schrimpf, and H.J. Lynch. 2017. Mapping Application for Penguin Populations and Projected Dynamics (MAPPPD): Data and tools for dynamic management and decision support. Polar Record 53: 160–166. https://doi.org/10.1017/S0032247417000055.
Klein, E.S., and G.M. Watters. 2020. What’s the catch? Profiling the benefits and costs associated with marine protected areas and displaced fishing in the Scotia Sea. PLoS ONE 15: e0237425. https://doi.org/10.1371/journal.pone.0237425.
Krüger, L. 2019. Spatio-temporal trends of the Krill fisheries in the Western Antarctic Peninsula and Southern Scotia Arc. Fisheries Management and Ecology 26: 327–333. https://doi.org/10.1111/fme.12363.
Kuznetsova, A., P. B. Brockhoff, and R. H. B. Christensen. 2018. lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software 8:2. https://doi.org/10.18637/jss.v082.i1310.18637/jss.v082.i13.
Kwok, R., and J.C. Comiso. 2002. Southern Ocean climate and sea ice anomalies associated with the Southern Oscillation. Journal of Climate 15: 487–501. https://doi.org/10.1175/1520-0442(2002)015<0487:SOCASI>2.0.CO;2.
Lima, M., and S.A. Estay. 2013. Warming effects in the western Antarctic Peninsula ecosystem: The role of population dynamic models for explaining and predicting penguin trends. Population Ecology 55: 557–565. https://doi.org/10.1007/s10144-013-0386-1.
Lüdecke, D., A. Bartel, C. Schwemmer, C. Powell, and A. Djalowski. 2019. Data visualization for statistics in Social Science. The Comprehensive R Archive Network CRAN. https://cran.r-project.org/web/packages/sjPlot/sjPlot.pdf.
Lynch, H.J., W.F. Fagan, R. Naveen, S.G. Trivelpiece, and W.Z. Trivelpiece. 2012. Differential advancement of breeding phenology in response to climate may alter staggered breeding among sympatric pygoscelid penguins. Marine Ecology Progress Series 454: 135–145. https://doi.org/10.3354/meps09252.
Lynham, J., A. Nikolaev, J. Raynor, T. Vilela, and J.C. Villaseñor-Derbez. 2020. Impact of two of the world’s largest protected areas on longline fishery catch rates. Nature Communications 11: 979. https://doi.org/10.1038/s41467-020-14588-3.
Marshall, G.J., and T.J. Bracegirdle. 2014. An examination of the relationship between the Southern Annular Mode and Antarctic surface air temperatures in the CMIP5 historical runs. Climate Dynamics 45: 1513–1535. https://doi.org/10.1007/s00382-014-2406-z.
Meyer, B. 2012. The overwintering of Antarctic krill, Euphausia superba, from an ecophysiological perspective. Polar Biology 35: 15–37. https://doi.org/10.1007/s00300-011-1120-0.
Moffat, C., and M. Meredith. 2018. Shelf-ocean exchange and hydrography west of the Antarctic Peninsula: A review. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 376: 20170164. https://doi.org/10.1098/rsta.2017.0164.
Nicol, S., and J. Foster. 2016. The fishery for Antarctic Krill: Its current status and management regime. In Biology and ecology of Antarctic Krill, Advances in polar ecology, ed. V. Siegel, vol 1, 387–421. Cham: Springer. https://doi.org/10.1007/978-3-319-29279-3.
Nicol, S., J. Foster, and S. Kawaguchi. 2012. The fishery for Antarctic krill—Recent developments. Fish and Fisheries 13: 30–40. https://doi.org/10.1111/j.1467-2979.2011.00406.x.
Parkinson, C.L. 2019. A 40-y record reveals gradual Antarctic sea ice increases followed by decreases at rates far exceeding the rates seen in the Arctic. Proceedings of the National Academy of Sciences of the United States of America 116: 14414–14423. https://doi.org/10.1073/pnas.1906556116.
Perry, F.A., A. Atkinson, S.F. Sailley, G.A. Tarling, S.L. Hill, C.H. Lucas, and D.J. Mayor. 2019. Habitat partitioning in Antarctic krill: Spawning hotspots and nursery areas. PLoS ONE 14: e0219325. https://doi.org/10.1371/journal.pone.0219325.
Petry, M.V., F.C.L. Valls, and E. de S. Petersen, L. Krüger, R. da C. Piuco, and C. R. dos Santos. 2016. Breeding sites and population of seabirds on Admiralty Bay, King George Island, Antarctica. Polar Biology 39: 1343–1349. https://doi.org/10.1007/s00300-015-1846-1.
Petry, M.V., F.C.L. Valls, E.S. Petersen, J.V.G. Finger, and L. Krüger. 2018. Population trends of seabirds at Stinker Point, Elephant Island, Maritime Antarctica. Antarctic Science 30: 220–226. https://doi.org/10.1017/S0954102018000135.
Piñones, A., and A.V. Fedorov. 2016. Projected changes of Antarctic krill habitat by the end of the 21st century. Geophysical Research Letters 43: 8580–8589. https://doi.org/10.1002/2016GL069656.
R Development Core Team. 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
Reiss, C.S., A.M. Cossio, V. Loeb, and D.A. Demer. 2008. Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland Islands, 1996–2006. ICES Journal of Marine Science 65: 497–508. https://doi.org/10.1093/icesjms/fsn033.
Ryabov, A.B., A.M. de Roos, B. Meyer, S. Kawaguchi, and B. Blasius. 2017. Competition-induced starvation drives large-scale population cycles in Antarctic krill. Nature Ecology and Evolution 1: 0177. https://doi.org/10.1038/s41559-017-0177.
Sala, E., and S. Giakoumi. 2018. No-take marine reserves are the most effective protected areas in the ocean. ICES Journal of Marine Science 75: 1166–1168. https://doi.org/10.1093/icesjms/fsx059.
Santa Cruz, F., B. Ernst, J.A. Arata, and C. Parada. 2018. Spatial and temporal dynamics of the Antarctic krill fishery in fishing hotspots in the Bransfield Strait and South Shetland Islands. Fisheries Research 208: 157–166. https://doi.org/10.1016/j.fishres.2018.07.020.
Stammerjohn, S. E., D. G. Martinson, R. C. Smith, X. Yuan, and D. Rind. 2008. Trends in Antarctic annual sea ice retreat and advance and their relation to El Niño—Southern Oscillation and Southern Annular Mode variability. Journal of Geophysical Research 113: C03S90. https://doi.org/10.1029/2007JC004269.
Stoffer, D. 2008. Applied statistical time series analysis. CRAN. https://doi.org/10.1007/978-3-319-52452-8.
Surma, S., E.A. Pakhomov, and T.J. Pitcher. 2014. Effects of whaling on the structure of the Southern Ocean food web: Insights on the “krill surplus” from ecosystem modelling. PLoS ONE 9: e114978. https://doi.org/10.1371/journal.pone.0114978.
Tarling, G.A., S. Hill, H. Peat, S. Fielding, C. Reiss, and A. Atkinson. 2016. Growth and shrinkage in Antarctic krill Euphausia superba is sex-dependent. Marine Ecology Progress Series 547: 61–78. https://doi.org/10.3354/meps11634.
Thiebot, J.-B., A. Lescroël, D. Pinaud, P.N. Trathan, and C.-A. Bost. 2011. Larger foraging range but similar habitat selection in non-breeding versus breeding sub-Antarctic penguins. Antarctic Science 23: 117–126. https://doi.org/10.1017/S0954102010000957.
Thorpe, S.E., G.A. Tarling, and E.J. Murphy. 2019. Circumpolar patterns in Antarctic krill larval recruitment: An environmentally driven model. Marine Ecology Progress Series 613: 77–96. https://doi.org/10.3354/meps1288.
Trathan, P.N., and K. Reid. 2009. Exploitation of the marine ecosystem in the sub-Antarctic: Historical impacts and current consequences. Papers and Proceedings of the Royal Society of Tasmania 143: 9–14.
Trathan, P.N., V. Warwick-Evans, J.T. Hinke, E.F. Young, E.J. Murphy, A.P.B. Carneiro, M.P. Dias, K.M. Kovacs, et al. 2018. Managing fishery development in sensitive ecosystems: Identifying penguin habitat use to direct management in Antarctica. Ecosphere. https://doi.org/10.1002/ecs2.2392.
Trivelpiece, W.Z., S. Buckelew, C. Reiss, and S.G. Trivelpiece. 2007. The winter distribution of chinstrap penguins from two breeding sites in the South Shetland Islands of Antarctica. Polar Biology 30: 1231–1237. https://doi.org/10.1007/s00300-007-0283-1.
Trivelpiece, W.Z., J.T. Hinke, A.K. Miller, C.S. Reiss, S.G. Trivelpiece, and G.M. Watters. 2011. Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proceedings of the National Academy of Sciences of the United States of America 108: 7625–7628. https://doi.org/10.1073/pnas.1016560108.
Walsh, J., C. Reiss, and G. Watters. 2020. Flexibility in Antarctic krill Euphausia superba decouples diet and recruitment from overwinter sea-ice conditions in the northern Antarctic Peninsula. Marine Ecology Progress Series 642: 1–19. https://doi.org/10.3354/meps13325.
Warwick-Evans, V., N. Ratcliffe, A.D. Lowther, F. Manco, L. Ireland, H.L. Clewlow, and P.N. Trathan. 2018. Using habitat models for chinstrap penguins Pygoscelis antarctica to advise krill fisheries management during the penguin breeding season. Diversity and Distributions 24: 1756–1771. https://doi.org/10.1111/ddi.12817.
Watters, G.M., J.T. Hinke, and C.S. Reiss. 2020. Long-term observations from Antarctica demonstrate that mismatched scales of fisheries management and predator–prey interaction lead to erroneous conclusions about precaution. Scientific Reports 10: 2314. https://doi.org/10.1038/s41598-020-59223-9.
Wickham, H. 2020. Tools for splitting, applying and combining data. The Comprehensive R Archive Network CRAN. https://cran.r-project.org/web/packages/plyr/plyr.pdf.
Wickham, H., and W. Chang. 2015. Package ‘ggplot2.’ The Comprehensive R Archive Network CRAN. https://cran.r-project.org/web/packages/ggplot2/ggplot2.pdf.
Wilson, R.P., B. Alvarrez, L. Latorre, D. Adelung, B. Culik, and R. Bannasch. 1998. The movements of gentoo penguins Pygoscelis papua from Ardley Island, Antarctica. Polar Biology 19: 407–413. https://doi.org/10.1007/s003000050266.
The authors would like to thank the CCAMLR Secretariat and co-originators/owners for providing data access on krill fishery. The authors acknowledge the important contribution of the MAPPPD resources towards the increasing knowledge of penguin species ecology. This study benefited from the “Marine Protected Areas program” of the Instituto Antártico Chileno.
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Krüger, L., Huerta, M.F., Santa Cruz, F. et al. Antarctic krill fishery effects over penguin populations under adverse climate conditions: Implications for the management of fishing practices. Ambio 50, 560–571 (2021). https://doi.org/10.1007/s13280-020-01386-w
- Antarctic Peninsula
- Chinstrap penguin
- Gentoo penguin
- Population growth rate
- Southern annular mode