Individual variation in migratory movements of chinstrap penguins leads to widespread occupancy of ice-free winter habitats over the continental shelf and deep ocean basins of the Southern Ocean

Autoři: Jefferson T. Hinke aff001;  Maria M. Santos aff002;  Malgorzata Korczak-Abshire aff004;  Gennadi Milinevsky aff005;  George M. Watters aff001
Působiště autorů: Antarctic Ecosystem Research Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, California, United States of America aff001;  Departamento Biología de Predadores Tope, Instituto Antártico Argentino, San Martín, Argentina aff002;  Laboratorios Anexos, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina aff003;  Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, Poland aff004;  National Antarctic Scientific Center of Ukraine, Kyiv, Ukraine aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


A goal of tracking migratory animals is to characterize the habitats they use and to interpret population processes with respect to conditions experienced en route to, and within, overwintering areas. For migratory seabirds with broad breeding ranges, inferring population-level effects of environmental conditions that are experienced during migratory periods would benefit by directly comparing how birds from different breeding aggregations disperse, characterizing the physical conditions of areas they use, and determining whether they occupy shared foraging areas. We therefore tracked 41 adult and juvenile chinstrap penguins (Pygoscelis antarctica) from three breeding locations in the northern Antarctic Peninsula region during the austral winter of 2017. The satellite tracking data revealed overlap of individuals over continental shelf areas during autumn months (Mar-May), shared outbound corridors that track the southern Antarctic circumpolar current front, followed by occupancy of progressively colder, deeper, and ice-free waters that spanned the entire western hemisphere south of the Polar Front. Despite broadly similar physical environments used by individuals from different colonies, the proportion of birds from each colony that remained within 500km of their colony was positively correlated with their local population trends. This suggests that local migration strategies near the Antarctic Peninsula may benefit breeding populations. However, the magnitude of inter-colony and intra-colony overlap was generally low given the broad scale of habitats occupied. High individual variation in winter movements suggests that habitat selection among chinstrap penguins is more opportunistic, without clear colony-specific preference for fine-scale foraging hotspots. Mixing of individuals from multiple colonies across broad regions of the Southern Ocean would expose chinstrap penguins from the Antarctic Peninsula to a shared environmental experience that helps explain the regional decline in their abundance.

Klíčová slova:

Animal migration – Animal sexual behavior – Animal sociality – Antarctica – Birds – Foraging – Sea ice – Penguins


1. Wilson PR, Ainley DG, Nur N, Jacobs SS, Barton KJ, Ballard G, et al. Adélie penguin population change in the Pacific Sector of Antarctica: relation to sea-ice extent and the Antarctic Circumpolar Current. Mar Ecol Prog Ser. 2001; 213:301–309.

2. Perryman WL, Donahue MA, Perkins PC, Reilly SB. Gray whale calf production 1994–2000: are observed fluctuations related to changes in seasonal ice cover? Mar Mamm Sci. 2006; 18:121–144.

3. Robbins CS, Sauer JR, Greenberg RS, Droege S. Population declines in North American birds that migrate to the neotropics. Proc Natl Acad Sci USA. 1989; 86:7658–7662. doi: 10.1073/pnas.86.19.7658 2798430

4. Costa DP, Breed GA, Robinson PW. New insights into pelagic migrations: implications for ecology and conservation. Annu Rev Ecol Evol Syst. 2012; 43:73–96.

5. Fort J, Moe B, Strøm H, Gremillet D, Welcker J, Schultner J, et al. Multicolony tracking reveals potential threats to little auks wintering in the North Atlantic from marine pollution and shrinking sea ice cover. Divers Distrib. 2013; 19:1322–1332.

6. Péron C, Grémillet D. Tracking through life stages: adult, immature and juvenile autumn migration in a long-lived seabird. PLoS ONE 2013; 8(8): e72713. doi: 10.1371/journal.pone.0072713 23977344

7. BirdLife International [Internet]. Pygoscelis antarcticus. The IUCN Red List of Threatened Species 2018. e.T22697761A132601557. [cited 2019 Mar 7]

8. Lynch HJ, Naveen R, Trathan PN, Fagan WF. Spatially integrated assessments reveal wide-spread changes in penguin populations on the Antarctic Peninsula. Ecology. 2012; 93:1367–1377. doi: 10.1890/11-1588.1 22834377

9. Fraser W, Trivelpiece WZ, Ainley DG, Trivelpiece SG. Increases in Antarctic penguin populations: reduced competition with whales or a loss of sea ice due to environmental warming? Polar Biol. 1992; 11:525–531.

10. Hinke JT, Salwicka K, Trivelpiece SG, Watters GM, Trivelpiece WZ. Divergent responses of Pygoscelis penguins reveal a common environmental driver. Oecologia. 2007; 153:845–855. doi: 10.1007/s00442-007-0781-4 17566778

11. Wilson RP, Culik BM, Kosiorek P, Adelung D. The over-winter movements of a chinstrap penguin (Pygoscelis antarctica). Polar Rec. 1998; 34:107–112.

12. Trivelpiece WZ, Buckelew S, Reiss CS, Trivelpiece SG. The overwinter distribution of chinstrap penguins from two breeding sites in the South Shetland Islands of Antarctica. Polar Biol. 2007; 30:1231–1237.

13. Biuw M, Lydersen C, Nico de Bruyn PJ, Arriola A, Hofmeyr GGJ, Kritzinger P, et al. Long-range migration of a chinstrap penguin from Bouvetøya to Montagu Island, South Sandwich Islands. Antarct Sci. 2009; 22:157–162.

14. Hinke JT, Polito MJ, Goebel ME, Jarvis S, Reiss CS, Thorrold SR, et al. Spatial and isotopic niche partitioning during winter in chinstrap and Adélie penguins from the South Shetland Islands. Ecosphere. 2015; 6(7):125. doi: 10.1890/ES14-00287.1

15. Hinke JT, Cossio AM, Goebel ME, Reiss CS, Trivelpiece WZ, Watters GM. Identifying risk: concurrent overlap of the Antarctic krill fishery with krill-dependent predators in the Scotia Sea. PLoS ONE. 2017; 12(1): e0170132. doi: 10.1371/journal.pone.0170132 28085943

16. Polito MJ, Hinke JT, Hart T, Santos M, Houghton LA, Thorrold SR. Stable isotope analyses of feather amino acids identify penguin migration strategies at ocean basin scales. Biol Lett. 2017; 13:20170241. doi: 10.1098/rsbl.2017.0241 28794274

17. Shillinger GL, Bailey H, Bograd SJ, Hazen E, Hamann M, Gaspar P, et al. Tagging through the stages: technical and ecological challenges in observing life histories through biologging. Mar Ecol Prog Ser. 2012; 457:165–170.

18. Thiebot J-B, Cherel Y, Crawford RJM, Makhado AB, Trathan PN, Pinaud D, et al. A space oddity: geographic and specific modulation of migration in Eudyptes penguins. PLoS ONE. 2013; 8(8):e71429. doi: 10.1371/journal.pone.0071429 23936507

19. Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM. Variability in krill biomass links harvesting and climate warming to penguin populations in Antarctica. Proc Natl Acad Sci USA. 2011; 108:7625–7628. doi: 10.1073/pnas.1016560108 21482793

20. Korczak-Abshire M, Zmarz A, Rodzewicz M, Kycko M, Karsznia I, Chwedorzewska KJ. Study of fauna population changes on Penguin Island and Turret Point Oasis (King George Island, Antarctica) using Unmanned Aerial Vehicle. Polar Biol. 2019; 42:217–224. doi: 10.1007/s00300-018-2379-1

21. González-Zevallos D, Santos MM, Rombolá EF, Juáres MA, Coria NR. Abundance and breeding distribution of seabirds in the northern part of the Danco Coast, Antarctic Peninsula. Polar Res. 2013; 32:11133. doi: 10.3402/polar.v32i0.11133

22. Ainley DG, Ribic CA, Fraser WR. Ecological structure among migrant and resident seabirds of the Scotia-Weddell confluence region. J Anim Ecol. 1994; 63:347–364.

23. Orsi AH, Whitworth T III, Nowlin WD Jr.. On the meridional extent and fronts of the Antarctic Circumpolar Current. Deep-Sea Res I, 1995; 42:641–673.

24. Bost CA, Cotté C, Bailleul F, Cherel Y, Charrassin JB, Guinet C, et al. The importance of oceanographic fronts to marine birds and mammals of the southern oceans. J Mar Syst. 2009; 78:363–376.

25. Miller AK, Trivelpiece WZ. Chinstrap penguins alter foraging and diving behavior in response to the size of their principle prey, Antarctic krill. Mar Biol. 2008; 154:201–208.

26. Johnson D, London J, Lea M-A, Durban J. Continuous-time correlated random walk model for animal telemetry data. Ecology. 2008; 89:1208–1215. doi: 10.1890/07-1032.1 18543615

27. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018.

28. Johnson DS London JM (2018). crawl: an R package for fitting continuous-time correlated random walk models to animal movement data. Zenodo.

29. London J. 2016. crawlr: utilities and visualization functions in support of crawl. R package version 0.1.0.

30. Amante C, Eakins BW. ETOPO1 1 Arc-Minute Global Relief Model: Procedures, Data Sources and Analysis. NOAA Technical Memorandum NESDIS NGDC-24. National Geophysical Data Center, NOAA. 2009. [cited 2018 Nov 20].

31. Bonjean F, Lagerloef GSE. Diagnostic model and analysis of the surface currents in the tropical Pacific Ocean. J Phys Oceanogr. 2002; 32:2938–2954.

32. Earth Space Research. OSCAR third degree resolution ocean surface currents. Ver. 1. PO.DAAC, CA, USA. 2009. [cited 2018 Nov 20].

33. Werdell PJ, Franz BA, Bailey SW, Feldman GC, Boss E, Brando VE, et al. Generalized ocean color inversion model for retrieving marine inherent optical properties. Appl Opt. 2013; 52:2019–2037. doi: 10.1364/AO.52.002019 23545956

34. Ocean Biology Processing Group. MODIS Aqua Level 3 SST Thermal IR Monthly 9km Daytime v2014.0. Ver. 2014.0. PO.DAAC, CA, USA. 2015. [cited 2018 Nov 20].

35. Peng G, Meier WN, Scott D, Savoie M. A long-term and reproducible passive microwave sea ice concentration data record for climate studies and monitoring. Earth Syst Sci Data. 2013; 5:311–318. doi: 10.5194/essd-5-311-2013

36. Meier WN, Fetterer F, Savoie M, Mallory S, Duerr R, Stroeve J. NOAA/NSIDC Climate Data Record of Passive Microwave Sea Ice Concentration, Version 3. Boulder, Colorado USA. NSIDC: National Snow and Ice Data Center. 2017.

37. Hijmans RJ. raster: Geographic Data Analysis and Modeling. R package version 2.6–7. 2017.

38. Chin TM, Vazquez-Cuervo J, Armstrong EM. A multi-scale high-resolution analysis of global sea surface temperature. Remote Sens Environ. 2017; 200:154–169.

39. Bivand RS, Pebesma E, Gomez-Rubio V. Applied spatial data analysis with R, 2nd ed. New York: Springer; 2013.

40. Bivand R, Rundel C. rgeos: Interface to geometry engine—open source ('GEOS'). R package version 0.3–28. 2018.

41. Wessel P, Smith WHF. A global self-consistent, hierarchical, high-resolutions shoreline database, J. Geophys. Res. 1996; 101:8741–8743.

42. Pinheiro J, Bates D, DebRoy S, Sarkar D. nlme: Linear and Nonlinear Mixed Effects Models, R package version 3.1–141.

43. Lynch HJ, White R, Naveen R, Black A, Meixler MS, Fagan WF. In stark contrast to widespread declines along the Scotia Arc, a survey of the South Sandwich Islands finds a robust seabird community. Polar Biol. 2016; 39:1615–1625.

44. Stammerjohn SE, Martinson DG, Smith RC, Yuan X, Rind D. Trends in Antarctic sea ice retreat and advance and their relation to El Niño—Southern Oscillation and Southern Annular Mode variability. J Geophys Res. 2008; 113:C03S90. doi: 10.1029/2007JC004269

45. Reiss CS, Cossio A, Santora JA, Dietrich KS, Murray A, Mitchell BG, et al. Overwinter habitat selection by Antarctic krill under varying sea-ice conditions: implications for top predators and fishery management. Mar Ecol Prog Ser. 2017; 568:1–16.

46. Humphries G, Naveen R, Schwaller M, Che-Castaldo C, McDowell P, Schrimpf M, et al. Mapping Application for Penguin Populations and Projected Dynamics (MAPPPD): data and tools for dynamic management and decision support. Polar Rec. 2017; 53:60–166. doi: 10.1017/S0032247417000055

47. Gutowsky SE, Leonard ML, Conners MG, Shaffer SA, Jonsen ID. Individual-level variation and higher-level interpretations of space use in wide-ranging species: an albatross case study of sampling effects. Frontiers in Marine Science. 2015; 2:93. doi: 10.3389/fmars.2015.00093

48. Yuan X. ENSO-related impacts on Antarctic sea ice: a synthesis of phenomenon and mechanisms. Antarct Sci.16; 415–425. doi: 10.1017/S0954102004002238

49. Lowther AD, Trathan P, Tarroux A, Lyderson C, Kovacs KM. The relationship between coastal weather and foraging behavior of chinstrap penguins, Pygoscelis antarctica. ICES J Mar Sci. 2018; 75:1940–1948.

50. Oliver MJ, Kohut J, Bernard K, Fraser W, Winsor P, Statscewich H, et al. Central place foragers select ocean surface convergent features despite differing foraging strategies. Sci Rep. 2019; 9:157. doi: 10.1038/s41598-018-35901-7 30655549

51. McFarlane Tranquilla LA, Montevecchi WA, Hedd A, Fifield DA, Burke CM, Smith PA, et al. Multiple-colony winter habitat use by murres Uria spp. in the Northwest Atlantic Ocean: implications for marine risk assessment. Mar Ecol Prog Ser. 2013; 472:287–303.

52. Green JA, Boyd IL, Woakes AJ, Warren NL, Butler PJ. Behavioral flexibility during year-round foraging in macaroni penguins. Mar Ecol Prog Ser. 2005; 296:183–196.

53. Takahashi A, Ito M, Nagai K, Thiebot J-B, Mitamura H, Noda T, et al. Migratory movements and winter diving activity of Adélie penguins in East Antarctica. Mar Ecol Prog Ser. 2018; 589:227–239.

54. Trathan PN, Warwick-Evans V, Hinke JT, Young EF, Murphy EJ, Carneiro APB, et al. Managing fishery development in sensitive ecosystems: identifying penguin habitat use to direct management in Antarctica. Ecosphere. 2018; 9(8):e02392. doi: 10.1002/ecs2.2392

55. Dias MP, Carneiro APB, Warwick-Evans V, Harris C, Lorenz K, Lascelles B, et al. Identification of marine Important Bird and Biodiversity Areas for penguins around the South Shetland and South Orkney Islands. Ecol Evol. 2018; 8:10520–10529. doi: 10.1002/ece3.4519 30464824

56. Oppel S, Bolton M, Carneiro APB, Dias MP, Green JA, Masello JF, et al. Spatial scales of marine conservation management for breeding seabirds. Mar Policy. 2018; 98:37–46.

57. Hayes GC, Bailey H, Bograd SJ, Bowen WD, Campagna C, Carmichael RH, et al. Translating marine animal tracking data into conservation policy and management. TREE. 34; 459–473. doi: 10.1016/j.tree.2019.01.009 30879872

58. Commission for the Conservation of Antarctic Marine Living Resources. Report of the thirty-sixth meeting of the Scientific Committee. Hobart, 2017.

59. Schofield O, Ducklow HW, Martinson DG, Meredith MP, Moline MA, Fraser WR. How do polar marine ecosystems respond to rapid climate change? Science. 2010; 328:1520–1523. doi: 10.1126/science.1185779 20558708

60. Casanovas P, Naveen R, Forrest S, Poncet J, Lynch HJ. A comprehensive coastal seabird survey maps out the front lines of ecological change on the western Antarctic Peninsula. Polar Biol. 2015; 38:927–940.

61. Meredith MP, King JC. 2005. Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett. 2005; 32:L19604. doi: 10.1029/2005GL024042

62. Nicol S, Foster J, Kawaguchi S. The fishery for Antarctic krill—recent developments. Fish Fish 2012; 13:30–40.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden