Antarctic climate change: Extreme events disrupt plastic phenotypic response in Adélie penguins

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Lescroël, Amélie ^a,b   Ballard, Grant ^c   Grémillet, David ^b,d   Authier, Matthieu ^b   Ainley, David G ^e  

^a UNIVERSITÉ DE RENNES 1   (France)

^b CNRS   (France)

^c PRBO CONSERVATION SCIENCE   (United States)

^d UNIVERSITY OF CAPE TOWN   (South Africa)

^e H T HARVEY AND ASSOCIATES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADELIE PENGUIN; ANTARCTICA; ARTICLE; CLIMATE CHANGE; FORAGING BEHAVIOR; ICEBERG; NONHUMAN; PENGUIN; PHENOTYPE; PHENOTYPIC PLASTICITY; SEA ICE;

ANIMAL MIGRATION; ANIMALS; ANTARCTIC REGIONS; CLIMATE CHANGE; FEMALE; ICE COVER; MALE; MODELS, STATISTICAL; OCEANS AND SEAS; POPULATION DYNAMICS; REPRODUCTION; SPHENISCIDAE;

EID: 84900448180     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085291     Document Type: Article

References (93)

1. Katz RW, Brown BG (1992) Extreme events in a changing climate: variability is more important than averages. Clim Change 21: 289-302.
2. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, et al. (2000) Climate extremes: observations, modeling, and impacts. Science 289: 2068-2074.
3. IPCC (2012) Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation: Special Report of the Intergovernmental Panel on Climate Change. Cambridge University Press. Field, C.B., V. Barros, T.F. Stocker, D. Qin, D.J. Dokken, K.L. Ebi, M.D. Mastrandrea, K.J. Mach, G.-K. Plattner, S.K. Allen, M. Tignor, and P.M. Midgley. 582 p.
4. Hansen J, Sato M, Ruedy R (2012) Perception of climate change. Proc Natl Acad Sci 109: E2415-E2423.
5. Parmesan C, Root TL, Willig MR (2000) Impacts of Extreme Weather and Climate on Terrestrial Biota. Bull Am Meteorol Soc 81: 443-450. doi:10.1175/1520-0477(2000)081〈0443:IOEWAC〉2.3.CO;2.
6. Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci 95: 14839-14842. (Pubitemid 29003717)
7. Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18: 648-656. (Pubitemid 37399486)
8. Gutschick VP, BassiriRad H (2003) Extreme events as shaping physiology, ecology, and evolution of plants: toward a unified definition and evaluation of their consequences. New Phytol 160: 21-42.
9. Thompson RM, Beardall J, Beringer J, Grace M, Sardina P (2013) Means and extremes: building variability into community-level climate change experiments. Ecol Lett. Available: http://onlinelibrary.wiley.com/doi/10.1111/ele.12095/full.
10. Ameca y Juárez EI, Mace GM, Cowlishaw G, Pettorelli N (2012) Natural population die-offs: causes and consequences for terrestrial mammals. Trends Ecol Evol 27: 272-277. doi:10.1016/j.tree.2011.11.005.
11. Dugger KM, Ainley DG, Lyver PO, 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 107: 12375-12380.
12. Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proc R Soc B Biol Sci 280. Available: http://rspb.royalsocietypublishing.org/content/280/1754/20122829.short.
13. Smith MD (2011) The ecological role of climate extremes: current understanding and future prospects. J Ecol 99: 651-655.
14. Chambert T, Rotella JJ, Garrott RA (2012) Environmental extremes versus ecological extremes: impact of a massive iceberg on the population dynamics of a high-level Antarctic marine predator. Proc R Soc B Biol Sci 279: 4532-4541.
15. Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, et al. (2007) Regional Climate Projections. The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, NY, USA.
16. Gille ST (2008) Decadal-scale temperature trends in the Southern Hemisphere ocean. J Clim 21: 4749-4765.
17. Madhusoodanan MS, Thompson B (2011) Decadal variability of the Arctic Ocean thermal structure. Ocean Dyn 61: 873-880.
18. Pritchard HD, Arthern RJ, Vaughan DG, Edwards LA (2009) Extensive dynamic thinning on the margins of the Greenland and Antarctic ice sheets. Nature 461: 971-975.
19. Pritchard HD, Ligtenberg SRM, Fricker HA, Vaughan DG, Van den Broeke MR, et al. (2012) Antarctic ice-sheet loss driven by basal melting of ice shelves. Nature 484: 502-505.
20. Barnes DK, Souster T (2011) Reduced survival of Antarctic benthos linked to climate-induced iceberg scouring. Nat Clim Change 1: 365-368.
21. Lescroël A, Ballard G, Toniolo V, Barton KJ, Wilson PR, et al. (2010) Working less to gain more: when breeding quality relates to foraging efficiency. Ecology 91: 2044-2055.
22. Arrigo KR, van Dijken GL, Ainley DG, Fahnestock MA, Markus T (2002) Ecological impact of a large Antarctic iceberg. Geophys Res Lett 29: 8-1.
23. Thrush SF, Cummings VJ (2011) Massive icebergs, alteration in primary food resources and change in benthic communities at Cape Evans, Antarctica. Mar Ecol 32: 289-299.
24. Thompson DW, Solomon S (2002) Interpretation of recent Southern Hemisphere climate change. Science 296: 895-899. (Pubitemid 34464892)
25. Holland PR, Kwok R (2012) Wind-driven trends in Antarctic sea-ice drift. Nat Geosci. doi:10.1038/NGEO1627.
26. Ainley D, Russell J, Jenouvrier S, Woehler E, Lyver PO, et al. (2010) Antarctic penguin response to habitat change as Earth's troposphere reaches 2°C above preindustrial levels. Ecol Monogr 80: 49-66.
27. Mulvaney R, Abram NJ, Hindmarsh RC, Arrowsmith C, Fleet L, et al. (2012) Recent Antarctic Peninsula warming relative to Holocene climate and ice-shelf history. Nature 489: 141-144.
28. Nettles M, Ekström G (2010) Glacial earthquakes in Greenland and Antarctica. Annu Rev Earth Planet Sci 38: 467-491.
29. Croxall JP, Trathan PN, Murphy EJ (2002) Environmental change and Antarctic seabird populations. Science 297: 1510-1514. (Pubitemid 34970990)
30. Forcada J, Trathan PN, Murphy EJ (2008) Life history buffering in Antarctic mammals and birds against changing patterns of climate and environmental variation. Glob Change Biol 14: 2473-2488.
31. Jenouvrier S (2013) Impacts of climate change on avian populations. Glob Change Biol 19: 2036-2057. doi:10.1111/gcb.12195.
32. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294: 321-326.
33. Donnelly A, Caffarra A, Kelleher CT, O'Neill BF, Diskin E, et al. (2012) Surviving in a warmer world: environmental and genetic responses. Clim Res 53: 245-262. doi:10.3354/cr01102.
34. Ainley DG (2002) The Adélie penguin: bellwether of climate change. New York: Columbia University Press. 310 p.
35. Ballard G, Toniolo V, Ainley DG, Parkinson CL, Arrigo KR, et al. (2010) Responding to climate change: Adélie penguins confront astronomical and ocean boundaries. Ecology 91: 2056-2069.
36. Watanabe YY, Takahashi A (2013) Linking animal-borne video to accelerometers reveals prey capture variability. Proc Natl Acad Sci 110: 2199-2204.
37. Ainley DG, Ballard G (2012) Non-consumptive factors affecting foraging patterns in Antarctic penguins: a review and synthesis. Polar Biol 35: 1-13.
38. Pitman RL, Durban JW (2010) Killer whale predation on penguins in Antarctica. Polar Biol 33: 1589-1594.
39. Clarke J, Kerry K, Fowler C, Lawless R, Eberhard S, et al. (2003) Post-fledging and winter migration of Adélie penguins Pygoscelis adeliae in the Mawson region of East Antarctica. Mar Ecol Prog Ser 248: 267-278.
40. Dunn MJ, Silk JRD, Trathan PN (2011) Post-breeding dispersal of Adélie penguins (Pygoscelis adeliae) nesting at Signy Island, South Orkney Islands. Polar Biol 34: 205-214.
41. Clarke J, Kerry K, Irvine L, Phillips B (2002) Chick provisioning and breeding success of Adélie penguins at Béchervaise Island over eight successive seasons. Polar Biol 25: 21-30. (Pubitemid 36058960)
42. Emmerson L, Southwell C (2008) Sea ice cover and its influence on Adélie penguin reproductive performance. Ecology 89: 2096-2102.
43. Emslie SD, Berkman PA, Ainley DG, Coats L, Polito M (2003) Late-Holocene initiation of ice-free ecosystems in the southern Ross Sea, Antarctica. Mar Ecol Prog Ser 262: 19-25. (Pubitemid 37496503)
44. 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.
45. 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.
46. Ballard G, Jongsomjit D, Veloz SD, Ainley DG (2012) Coexistence of mesopredators in an intact polar ocean ecosystem: the basis for defining a Ross Sea marine protected area. Biol Conserv 156: 72-82.
47. Ainley DG, Ballard G, Dugger KM (2006) Competition among penguins and cetaceans reveals trophic cascades in the western Ross Sea, Antarctica. Ecology 87: 2080-2093. (Pubitemid 44215733)
48. Kooyman GL, Ainley DG, Ballard G, Ponganis PJ (2007) Effects of giant icebergs on two emperor penguin colonies in the Ross Sea, Antarctica. Antarct Sci 19: 31-38. (Pubitemid 46662190)
49. Siniff DB, Garrott RA, Rotella JJ, Fraser WR, Ainley DG (2008) Opinion: Projecting the effects of environmental change on Antarctic seals. Antarct Sci 20: 425-435.
50. Lescroël A, Dugger KM, Ballard G, Ainley DG (2009) Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. J Anim Ecol 78: 798-806.
51. Shepherd LD, Millar CD, Ballard G, Ainley DG, Wilson PR, et al. (2005) Microevolution and mega-icebergs in the Antarctic. Proc Natl Acad Sci U S A 102: 16717-16722. (Pubitemid 41688843)
52. Ainley DG, Ribic CA, Ballard G, Heath S, Gaffney I, et al. (2004) Geographic structure of Adélie penguin populations: overlap in colony-specific foraging areas. Ecol Monogr 74: 159-178. (Pubitemid 41123459)
53. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates Incorporated. Available: http://www.cabdirect. org/abstracts/19980108896.html.
54. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21: 394-407. (Pubitemid 46802146)
55. Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B Biol Sci 275: 649-659.
56. Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8: e1000357.
57. Jacobs SS, MacAyeal DR, Ardai Jr JL (1986) The recent advance of the Ross Ice Shelf, Antarctica. J Glaciol 32: 464-474.
58. Lazzara MA, Jezek KC, Scambos TA, MacAyeal DR, Van der Veen CJ (1999) On the recent calving of icebergs from the Ross Ice Shelf 1. Polar Geogr 23: 201-212. (Pubitemid 32152450)
59. Ballard G, Ainley DG, Ribic CA, Barton KR (2001) Effect of instrument attachment and other factors on foraging trip duration and nesting success of Adélie penguins. The Condor 103: 481-490. (Pubitemid 32747961)
60. Dugger KM, Ballard G, Ainley DG, Barton KJ, Burger AE (2006) Effects of flipper bands on foraging behavior and survival of Adélie penguins (Pygoscelis adeliae). The Auk 123: 858-869. (Pubitemid 44106826)
61. Cavalieri D, Parkinson C, Gloersen P, Zwally H (1996) Sea Ice Concentrations from Nimbus-7 SMMR and DMSP SSM/I-SSMIS Passive Microwave Data, [Dec. 21 to Jan. 7, from 1997 to 2010].
62. Dingemanse NJ, Kazem AJ, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25: 81-89.
63. Reed TE, Warzybok P, Wilson AJ, Bradley RW, Wanless S, et al. (2009) Timing is everything: flexible phenology and shifting selection in a colonial seabird. J Anim Ecol 78: 376-387.
64. Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, et al. (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10: 212-217.
65. R Development Core Team (2012) R: A language and environment for statistical computing. R Found Stat Comput.
66. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (n.d.) nlme: Linear and Nonlinear Mixed Effects Models, 2012. R Package Version: 3-1.
67. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes (2011). R package version 0.999375-42.
68. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. New York: Springer Science+ Business Media.
69. Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-PLUS. New York: Springer Verlag.
70. Lindquist MA, Spicer J, Asllani I, Wager TD (2012) Estimating and testing variance components in a multi-level GLM. NeuroImage 59: 490-501.
71. Faraway JJ (2006) Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. London: Chapman & Hall/CRC.
72. O'Hara RB, Sillanpää MJ (2009) A review of Bayesian variable selection methods: what, how and which. Bayesian Anal 4: 85-117.
73. Vonesh EF, Chinchilli VM, Pu K (1996) Goodness-of-fit in generalized nonlinear mixed-effects models. Biometrics: 572-587. (Pubitemid 26187062)
74. Rockova V, Lesaffre E, Luime J, Löwenberg B (2012) Hierarchical Bayesian formulations for selecting variables in regression models. Stat Med 31: 1221-1237.
75. Huey RB, Kearney MR, Krockenberger A, Holtum JA, Jess M, et al. (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B Biol Sci 367: 1665-1679.
76. Canale CI, Henry PY (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim Res 43: 135-147.
77. Grémillet D, Charmantier A (2010) Shifts in phenotypic plasticity constrain the value of seabirds as ecological indicators of marine ecosystems. Ecol Appl 20: 1498-1503.
78. Westneat DF, Hatch MI, Wetzel DP, Ensminger AL (2011) Individual variation in parental care reaction norms: integration of personality and plasticity. Am Nat 178: 652-667.
79. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20: 831-844. (Pubitemid 46663106)
80. Clarke J, Manly B, Kerry K, Gardner H, Franchi E, et al. (1998) Sex differences in Adélie penguin foraging strategies. Polar Biol 20: 248-258. (Pubitemid 28456131)
81. Martin JG, Nussey DH, Wilson AJ, Réale D (2011) Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol 2: 362-374.
82. Smith WO, Ainley DG, Cattaneo-Vietti R (2007) Trophic interactions within the Ross Sea continental shelf ecosystem. Philos Trans R Soc B Biol Sci 362: 95-111. (Pubitemid 47055513)
83. Ainley DG, Clarke ED, Arrigo K, Fraser WR, Kato A, et al. (2005) 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. (Pubitemid 40849960)
84. Ainley DG, Wilson PR, Barton KJ, Ballard G, Nur N, et al. (1998) Diet and foraging effort of Adélie penguins in relation to pack-ice conditions in the southern Ross Sea. Polar Biol 20: 311-319. (Pubitemid 28490114)
85. Arrigo KR, van Dijken GL (2003) Phytoplankton dynamics within 37 Antarctic coastal polynya systems. J Geophys Res Oceans 1978-2012 108. Available: http://earth.agu.org/journals/jc/jc0308/2002JC001739/.
86. Clarke J, Emmerson LM, Otahal P (2006) Environmental conditions and life history constraints determine foraging range in breeding Adélie penguins. Mar Ecol Prog Ser 310: 247-261.
87. Kato A, Yoshioka A, Sato K (2009) Foraging behavior of Adélie penguins during incubation period in Lützow-Holm Bay. Polar Biol 32: 181-186.
88. Ujvari B, Shine R, Luiselli L, Madsen T (2011) Climate-induced reaction norms for life-history traits in pythons. Ecology 92: 1858-1864.
89. 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. (Pubitemid 46131808)
90. Keys HJ, Jacobs SS, Barnett D (1990) The calving and drift of iceberg B-9 in the Ross Sea, Antarctica. Antarct Sci 2: 243-257.
91. Martin S, Drucker R, Aster R, Davey F, Okal E, et al. (2010) Kinematic and Seismic Analysis of Giant Tabular Iceberg Breakup at Cape Adare. J Geophys Res 115: B06311. doi:10.1029/2009JB006700.
92. Chapman EW, Hofmann EE, Patterson DL, Fraser WR (2010) The effects of variability in Antarctic krill (Euphausia superba) spawning behavior and sex/maturity stage distribution on Adélie penguin (Pygoscelis adeliae) chick growth: A modeling study. Deep Sea Res Part II Top Stud Ocean 57: 543-558.
93. LaRue MA, Ainley DG, Swanson M, Dugger KM, Lyver PO, et al. (2013) Climate Change Winners: Receding Ice Fields Facilitate Colony Expansion and Altered Dynamics in an Adélie Penguin Metapopulation. PLoS ONE 8: e60568. doi:10.1371/journal.pone.0060568.