Abstract
Environmental variability drives Adélie penguin (Pygoscelis adeliae) population dynamics through its effects on vital rates (e.g., survival, dispersal, or breeding success) resulted in penguin abundance changes with time delays. The lagged effects of environmental changes on penguin abundance are still not well defined. We divided the Ross Sea region into six areas to investigate the effects of environmental changes on penguin abundance from 1982 to 2013. Time lagged analysis of 1–6 years between penguin abundance and environmental factors were conducted in our study. We found that penguin abundance was significantly correlated with environmental factors at different lag times (p < 0.05). The relationship between penguin abundance and environmental factors might differ among regions. Generalized additive model results showed that sea surface temperature negatively affected penguin abundance in most regions of the Ross Sea. In mid-Victoria Land, the relationship between sea-ice concentration and penguin abundance was quadratic. Penguin abundance peaked when sea-ice concentration was approximately 40%. Optimal ranges of environmental factors for Adélie penguin population might exist. Our study highlighted the lagged response of penguin abundance to environmental factors to further understand the effects of climate changes on the Antarctic biosphere.
Similar content being viewed by others
References
Ainley D (2002) The Adélie Penguin: Bellwether of climate change. Columbia University Press, New York
Ainley DG, Ballard G, Dugger KM (2006) Competiton among penguins and cetaceans reveals trophic cascades in the western Ross Sea, Antarctica. Ecology 87:2080–2093
Ainley DG, Ballard G, Jones RM, Jongsomjit D, Pierce SD, Smith WO Jr, Veloz S (2015) Trophic cascades in the western Ross Sea, Antarctica: revisited. Mar Ecol Prog Ser 534:1–16
Ainley DG, Clarke ED, Arrigo K, Fraser WR, Kato A, Barton KJ, Wilson PR (1990s) Decadal-scale changes in the climate and biota of the Pacific sector of the Southern Ocean, 1950s to the 1990s. Antarct Sci 17:171–182
Ainley DG et al (2017) How overfishing a large piscine mesopredator explains growth in Ross Sea penguin populations: a framework to better understand impacts of a controversial fishery. Ecol Model 349:69–75
Ainley DG et al (2018) Post-fledging survival of Adélie penguins at multiple colonies: chicks raised on fish do well. Mar Ecol Prog Ser 601:239–251
Ainley DG, Fraser WR, Smith WO, Hopkins TL, Torres JJ (1991) The structure of upper level pelagic food webs in the Antarctic: effect of phytoplankton distribution. J Mar Syst 2:111–122. https://doi.org/10.1016/0924-7963(91)90017-O
Ainley DG, Russell JL, Jenouvrier S, Woehler EJ, Lyver POB, Fraser WR, Kooyman GL (2010) Antarctic penguin response to habitat change as Earth’s troposphere reaches 2°C above preindustrial levels. Ecol Monogr 80:49–66
Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100. https://doi.org/10.1038/nature02996
Ballard G, Dugger KM, Nur N, Ainley DG (2010) Foraging strategies of Adélie penguins: adjusting body condition to cope with environmental variability. Mar Ecol Prog Ser 405:287–302. https://doi.org/10.3354/meps08514
Barbraud C, Delord K, Weimerskirch H (2015) Extreme ecological response of a seabird community to unprecedented sea ice cover. R Soc Open Sci 2:140456. https://doi.org/10.1098/rsos.140456
Black CE (2016) A comprehensive review of the phenology of Pygoscelis penguins. Polar Biol 39:405–432. https://doi.org/10.1007/s00300-015-1807-8
CCAMLR (2004) CCAMLR ecosystem monitoring program—standard methods. Commission for the Conservation of Antarctic Marine Living Resources, Hobart
Che-Castaldo C et al (2017) Pan-Antarctic analysis aggregating spatial estimates of Adélie penguin abundance reveals robust dynamics despite stochastic noise. Nat Commun 8:832. https://doi.org/10.1038/s41467-017-00890-0
Cimino MA, Fraser WR, Irwin AJ, Oliver MJ (2013) Satellite data identify decadal trends in the quality of Pygoscelis penguin chick-rearing habitat. Glob Change Biol 19:136–148. https://doi.org/10.1111/gcb.12016
Cimino MA, Lynch HJ, Saba VS, Oliver MJ (2016) Projected asymmetric response of Adélie penguins to Antarctic climate change. Sci Rep 6:28785
Coetzee BWT, Chown SL (2016) A meta-analysis of human disturbance impacts on Antarctic wildlife. Biol Rev 91:578–596. https://doi.org/10.1111/brv.12184
Croxall JP, Trathan PN, Murphy EJ (2002) Environmental change and Antarctic seabird populations. Science 297:1510–1514
Davis LB, Hofmann EE, Klinck JM, Piñones A, Dinniman MS (2017) Distributions of krill and Antarctic silverfish and correlations with environmental variables in the western Ross Sea, Antarctica. Mar Ecol Prog Ser 584:45–65
Dugger KM, Ainley DG, Lyver POB, Barton K, Ballard G (2010) Survival differences and the effect of environmental instability on breeding dispersal in an Adélie penguin meta-population. Proc Natl Acad Sci USA 107:12375–12380. https://doi.org/10.1073/pnas.1000623107
Dugger KM, Ballard G, Ainley DG, Lyver POB, Schine C (2014) Adélie penguins coping with environmental change: results from a natural experiment at the edge of their breeding range. Front Ecol Evol. https://doi.org/10.3389/fevo.2014.00068
Emslie SD, Coats L, Licht K (2007) A 45,000 yr record of Adélie penguins and climate change in the Ross Sea, Antarctica. Geology 35:61–64. https://doi.org/10.1130/g23011a.1
Jenouvrier S (2013) Impacts of climate change on avian populations. Glob Change Biol 19:2036–2057. https://doi.org/10.1111/gcb.12195
Jenouvrier S, Barbraud C, Weimerskirch H (2006) Sea ice affects the population dynamics of Adélie penguins in Terre Adélie. Polar Biol 29:413–423
Larue MA, Ainley DG, Swanson M, Dugger KM, Lyver PO, Barton K, Ballard G (2013) Climate change winners: receding ice fields facilitate colony expansion and altered dynamics in an Adélie penguin metapopulation. PLoS One 8:e60568
Le Guen C et al (2018) Reproductive performance and diving behaviour share a common sea-ice concentration optimum in Adélie penguins (Pygoscelis adeliae). Glob Change Biol 24:5304–5317
Lescroël A, Ballard G, Grémillet D, Authier M, Ainley DG (2014) Antarctic climate change: extreme events disrupt plastic phenotypic response in Adélie penguins. PLoS One 9:e85291
Lescroël A, Ballard G, Toniolo V, Barton KJ, Wilson PR, Lyver POB, Ainley DG (2010) Working less to gain more: when breeding quality relates to foraging efficiency. Ecology 91:2044–2055. https://doi.org/10.1890/09-0766.1
Lynch HJ, Larue MA (2014) First global census of the Adélie penguin. Auk 131:457–466
Lynch HJ, Naveen R, Trathan PN, Fagan WF (2012) Spatially integrated assessment reveals widespread changes in penguin populations on the Antarctic Peninsula. Ecology 93:1367–1377
Lynch HJ, Schwaller MR (2014) Mapping the abundance and distribution of Adélie penguins using Landsat-7: first steps towards an integrated multi-sensor pipeline for tracking populations at the continental scale. PLoS One 9:e113301
Lyver POB et al (2014) Trends in the breeding population of Adélie penguins in the Ross Sea, 1981–2012: a coincidence of climate and resource extraction effects. PLoS One 9:e91188
Humphries GRW, Naveen R, Schwaller M, Che-Castaldo C, McDowall P, Schrimpf M, Lynch HJ (2017) Mapping Application for Penguin Populations and Projected Dynamics (MAPPPD): data and tools for dynamic management and decision support. Polar Rec 53:160–166. https://doi.org/10.1017/S0032247417000055
Nicol S (2006) Krill, currents, and sea ice: Euphausia superba and its changing environment. Bioscience 56:111–120
Piñones A, Fedorov AV (2016) Projected changes of Antarctic krill habitat by the end of the 21st century. Geophys Res Lett 43:8580–8589. https://doi.org/10.1002/2016gl069656
Pinkerton MH, Lyver POB, Stevens DW, Forman J, Eisert R, Mormede S (2016) Increases in Adélie penguins in the Ross Sea: could the fishery for Antarctic toothfish be responsible? Ecol Model 337:262–271. https://doi.org/10.1016/j.ecolmodel.2016.07.007
Quetin LB, Ross RM (1984) Depth distribution of developing Euphausia superba embryos, predicted from sinking rates. Mar Biol 79:47–53. https://doi.org/10.1007/BF00404984
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Revelle W (2018) psych: Procedures for psychological, psychometric, and personality research. Northwestern University, Evanston
Rob JH, Yeasmin K (2008) Automatic time series forecasting: the forecast package for R. J Stat Softw 26:1–22
Robinson NJ, Williams MJM (2012) Iceberg-induced changes to polynya operation and regional oceanography in the southern Ross Sea, Antarctica, from in situ observations. Antarct Sci 24:514–526. https://doi.org/10.1017/S0954102012000296
Southwell C et al (2015) Spatially extensive standardized surveys reveal widespread, multi-decadal increase in East Antarctic Adélie penguin populations. PLoS One 10:e0139877
Taylor RH, Wilson PR (1990) Recent increase and southern expansion of Adélie penguin populations in the Ross Sea, Antarctica, related to climatic warming. N Z J Ecol 14:25–29
Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci USA 108:7625–7628
Warwick-Evans V, Downie R, Santos M, Trathan PN (2019) Habitat preferences of Adélie Pygoscelis adeliae and Chinstrap Penguins Pygoscelis antarctica during pre-moult in the Weddell Sea (Southern Ocean). Polar Biol 42:703–714. https://doi.org/10.1007/s00300-019-02465-9
Wilson PR, Ainley DG, Nur N, Jacobs S, Barton K, Ballard G, Comiso J (2001) Adélie penguin population change in the Pacific Sector of Antarctica: relation to sea-ice extent and the Antarctic Circumpolar Current. Mar Ecol Prog Ser 213:301–309. https://doi.org/10.3354/meps213301
Wood SN (2004) Stable and efficient multiple smoothing parameter estimation for generalized additive models. J Am Stat Assoc 99:673–686
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc. Ser B: Stat Methodol 73:3–36
Wood SN (2017) Generalized additive models: an introduction with R, 2nd edn. Chapman and Hall/CRC, New York. https://doi.org/10.1201/9781315370279
Youngflesh C et al (2017) Circumpolar analysis of the Adélie penguin reveals the importance of environmental variability in phenological mismatch. Ecology 98:940
Funding
Funding was provided by National Key Research and Development Program of China (Grant No. 2018YFC1406906), National Natural Science Foundation of China (Grant No. 41205104) and Fundamental Research Funds for the Central Universities.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, X., Cheng, X., Zhang, B. et al. Lagged response of Adélie penguin (Pygoscelis adeliae) abundance to environmental variability in the Ross Sea, Antarctica. Polar Biol 43, 1769–1781 (2020). https://doi.org/10.1007/s00300-020-02743-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-020-02743-x