Abstract
Anthropogenic activities generate increasing disturbance in wildlife especially in extreme environments where species have to cope with rapid environmental changes. In Antarctica, while studies on human disturbance have mostly focused on stress response through physiological and behavioral changes, local variability in population dynamics has been addressed more scarcely. In addition, the mechanisms by which breeding communities are affected around research stations remain unclear. Our study aims at pointing out the fine-scale impact of human infrastructures on the spatial variability in Adélie penguin (Pygoscelis adeliae) colonies dynamics. Taking 24 years of population monitoring, we modeled colony breeding success and growth rate in response to both anthropic and land-based environmental variables. Building density around colonies was the second most important variable explaining spatial variability in breeding success after distance from skua nests, the main predators of penguins on land. Building density was positively associated with penguins breeding success. We discuss how buildings may protect penguins from avian predation and environmental conditions. The drivers of colony growth rate included topographical variables and the distance to human infrastructures. A strong correlation between 1-year lagged growth rate and colony breeding success was coherent with the use of public information by penguins to select their initial breeding site. Overall, our study brings new insights about the relative contribution and ecological implications of human presence on the local population dynamics of a sentinel species in Antarctica.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Data supporting the results are available from the Figshare Digital Repository: http://doi.org/https://doi.org/10.6084/m9.figshare.22341229.
References
Acero JM, Aguirre CA (1994) A monitoring research plan for tourism in Antarctica. Ann Tour Res 21:295–302. https://doi.org/10.1016/0160-7383(94)90046-9
Ainley DG (2002) The Adélie penguin: bellwether of climate change. Columbia University Press, Columbia
Ainley DG, DeMaster DP (1980) Survival and mortality in a population of adelie penguins. Ecology 61:522–530. https://doi.org/10.2307/1937418
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
Barbraud C, Delord K, Bost CA et al (2020) Population trends of penguins in the French Southern Territories. Polar Biol 43:835–850. https://doi.org/10.1007/s00300-020-02691-6
Bejder L, Samuels A, Whitehead H et al (2009) Impact assessment research: use and misuse of habituation, sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli. Mar Ecol Prog Ser 395:177–185. https://doi.org/10.3354/meps07979
Bergström L, Kautsky L, Malm T et al (2014) Effects of offshore wind farms on marine wildlife—a generalized impact assessment. Environ Res Lett 9:034012. https://doi.org/10.1088/1748-9326/9/3/034012
Bivand R (2022) R packages for analyzing spatial data: a comparative case study with areal data. Geogr Anal 54(3):488–518. https://doi.org/10.1111/gean.12319
Brenning A (2008) Statistical geocomputing combining R and SAGA: the example of landslide susceptibility analysis with generalized additive models. In: Böhner J, Blaschke T, Montanarella L (eds) SAGA - seconds out (Hamburger Beiträge zur Physischen Geographie und Landschaftsökologie, 19). pp 23–32. ISSN: 1866-170X
Bricher PK, Lucieer A, Woehler EJ (2008) Population trends of Adélie penguin (Pygoscelis adeliae) breeding colonies: a spatial analysis of the effects of snow accumulation and human activities. Polar Biol 31:1397–1407. https://doi.org/10.1007/s00300-008-0479-z
Burnham KP, Anderson DR, Anderson DR (2010) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Caccavo JA, Raclot T, Poupart T et al (2021) Anthropogenic activities are associated with shorter telomeres in chicks of Adélie penguin (Pygoscelis adeliae). Polar Biol 44:1391–1399. https://doi.org/10.1007/s00300-021-02892-7
Carlini AR, Coria NR, Santos MM et al (2007) Breeding success and population trends in Adélie penguins in areas with low and high levels of human disturbance. Polar Biol 30:917–924. https://doi.org/10.1007/s00300-006-0251-1
Cavalieri DJ, Parkinson CL (2012) Arctic sea ice variability and trends, 1979–2010. Cryosphere 6:881–889. https://doi.org/10.5194/tc-6-881-2012
Ceballos G, Ehrlich PR, Barnosky AD et al (2015) Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci Adv 1:1–5. https://doi.org/10.1126/sciadv.1400253
Cimino MA, Lynch HJ, Saba VS, Oliver MJ (2016) Projected asymmetric response of Adélie penguins to Antarctic climate change. Sci Rep 6:1–9. https://doi.org/10.1038/srep28785
Cockrem JF (2007) Stress, corticosterone responses and avian personalities. J Ornithol 148:169–178. https://doi.org/10.1007/s10336-007-0175-8
Cockrem JF, Potter MA, Barrett DP, Candy EJ (2008) Corticosterone responses to capture and restraint in emperor and adelie penguins in Antarctica. Zoolog Sci 25:291–298. https://doi.org/10.2108/zsj.25.291
Coetzee BWT, Chown SL (2016) A meta-analysis of human disturbance impacts on Antarctic wildlife: human disturbance impacts on Antarctic wildlife. Biol Rev 91:578–596. https://doi.org/10.1111/brv.12184
Coetzee BWT, Convey P, Chown SL (2017) Expanding the protected area network in Antarctica is urgent and readily achievable: expanding Antarctica’s protected areas. Conserv Lett 10:670–680. https://doi.org/10.1111/conl.12342
Convey P, Peck LS (2019) Antarctic environmental change and biological responses. Sci Adv 5:1–16. https://doi.org/10.1126/sciadv.aaz0888
Culik B, Adelung D, Woakes AJ (1990) The effect of disturbance on the heart rate and behaviour of Adélie penguins (Pygoscelis adeliae) during the breeding season. Antarct Ecosyst. https://doi.org/10.1007/978-3-642-84074-6_18
Danchin E, Boulinier T, Massot M (1998) Conspecific reproductive success and breeding habitat selection: implications for the study of coloniality. Ecology 79:2415–2428. https://doi.org/10.1890/0012-9658(1998)079[2415:CRSABH]2.0.CO;2
De Neve L, Fargallo J, Polo V et al (2006) Subcolony characteristics and breeding performance in the chinstrap penguin Pygoscelis antarctica. Ardeola 53:19–29
Doligez B, Cadet C, Danchin E, Boulinier T (2003) When to use public information for breeding habitat selection? The role of environmental predictability and density dependence. Anim Behav 66:973–988. https://doi.org/10.1006/anbe.2002.2270
Donehower CE, Bird DM, Hall CS, Kress SW (2007) Effects of gull predation and predator control on tern nesting success at Eastern Egg Rock, Maine. Waterbirds Int J Waterbird Biol 30:29–39
Dorman M (2024) starsExtra: miscellaneous functions for working with ‘stars’ rasters. R package version 0.2.8. https://github.com/michaeldorman/starsExtra/, https://michaeldorman.github.io/starsExtra/
Eayrs C, Li X, Raphael MN, Holland DM (2021) Rapid decline in Antarctic sea ice in recent years hints at future change. Nat Geosci 14:460–464. https://doi.org/10.1038/s41561-021-00768-3
Emslie SD, Karnovsky N, Trivelpiece W (1995) Avian predation at penguin colonies on King George Island, Antarctica. Wilson Bull 107:317–327
Erbe C, Marley SA, Schoeman RP et al (2019) The effects of ship noise on marine mammals—a review. Front Mar Sci 6:1–41. https://doi.org/10.3389/fmars.2019.00606
Fraser W, Patterson-Fraser D, Ribic C et al (2013) A nonmarine source of variability in Adélie penguin demography. Oceanography 26:207–209. https://doi.org/10.5670/oceanog.2013.64
Gaw S, Thomas KV, Hutchinson TH (2014) Sources, impacts and trends of pharmaceuticals in the marine and coastal environment. Philos Trans R Soc B Biol Sci 369:1–11. https://doi.org/10.1098/rstb.2013.0572
Giese M (1996) Effects of human activity on adelie penguin Pygoscelis adeliae breeding success. Biol Conserv 75:157–164. https://doi.org/10.1016/0006-3207(95)00060-7
Gutt J, Isla E, Xavier JC et al (2021) Antarctic ecosystems in transition—life between stresses and opportunities. Biol Rev 96:798–821. https://doi.org/10.1111/brv.12679
Holmes ND, Giese M, Achurch H et al (2006) Behaviour and breeding success of gentoo penguins Pygoscelis papua in areas of low and high human activity. Polar Biol 29:399–412. https://doi.org/10.1007/s00300-005-0070-9
Horváth Z, Ptacnik R, Vad CF, Chase JM (2019) Habitat loss over six decades accelerates regional and local biodiversity loss via changing landscape connectance. Ecol Lett 22:1019–1027. https://doi.org/10.1111/ele.13260
Howat IM, Porter C, Smith BE et al (2019) The reference elevation model of Antarctica. Cryosphere 13:665–674. https://doi.org/10.5194/tc-13-665-2019
König-Langlo G, King JC, Pettré P (1998) Climatology of the three coastal Antarctic stations Dumont d’Urville, Neumayer, and Halley. J Geophys Res Atmospheres 103:10935–10946. https://doi.org/10.1029/97JD00527
Kwok KCS, Kim DH, Smedley DJ, Rohde HF (1992) Snowdrift around buildings for Antarctic environment. J Wind Eng Ind Aerodyn 44:2797–2808. https://doi.org/10.1016/0167-6105(92)90073-J
Lee JR, Raymond B, Bracegirdle TJ et al (2017a) Climate change drives expansion of Antarctic ice-free habitat. Nature 547:49–54. https://doi.org/10.1038/nature22996
Lee S, Volkov DL, Lopez H et al (2017b) Wind-driven ocean dynamics impact on the contrasting sea-ice trends around West Antarctica. J Geophys Res Oceans 122:4413–4430. https://doi.org/10.1002/2016JC012416
Marra G, Wood SN (2011) Practical variable selection for generalized additive models. Comput Stat Data Anal 55:2372–2387. https://doi.org/10.1016/j.csda.2011.02.004
McCarthy AH, Peck LS, Hughes KA, Aldridge DC (2019) Antarctica: the final frontier for marine biological invasions. Glob Change Biol 25:2221–2241. https://doi.org/10.1111/gcb.14600
Micol T, Jouventin P (2001) Long-term population trends in seven Antarctic seabirds at Pointe Géologie (Terre Adélie). Polar Biol 24:175–185
Morandini V, Dugger KM, Lescroël A et al (2021) Maintenance of nest quality in Adélie penguins Pygoscelis adeliae: an additional benefit to life in the center. Polar Biol 44:1553–1562. https://doi.org/10.1007/s00300-021-02894-5
Moret GJM, Huerta AD (2007) Correcting GIS-based slope aspect calculations for the Polar Regions. Antarct Sci 19:129–130. https://doi.org/10.1017/S0954102007000181
Naimi B, Hamm Na, Groen TA, Skidmore AK, Toxopeus AG (2014) Where is positional uncertainty a problem for species distribution modelling. Ecography 37:191–203. https://doi.org/10.1111/j.1600-0587.2013.00205.x
Nisbet IT (2000) Disturbance, habituation, and management of waterbird colonies. Waterbirds 2:312–332
Pacoureau N, Authier M, Delord K, Barbraud C (2019a) Population response of an apex Antarctic consumer to its prey and climate fluctuations. Oecologia 189:279–291. https://doi.org/10.1007/s00442-018-4249-5
Pacoureau N, Delord K, Jenouvrier S, Barbraud C (2019b) Demographic and population responses of an apex predator to climate and its prey: a long-term study of South Polar Skuas. Ecol Monogr 89:1–15. https://doi.org/10.1002/ecm.1388
Pebesma E (2018) Simple Features for R: Standardized Support for Spatial Vector Data. R J 10(1):439–446. https://doi.org/10.32614/RJ-2018-009
Pebesma E (2024) lwgeom: Bindings to Selected ‘liblwgeom’ functions for simple features. R package version 0.2-14. https://github.com/r-spatial/lwgeom, https://r-spatial.github.io/lwgeom/
Pertierra LR, Hughes KA, Vega GC, Olalla-Tárraga MÁ (2017) High resolution spatial mapping of human footprint across Antarctica and its implications for the strategic conservation of avifauna. PLoS ONE 12:1–20. https://doi.org/10.1371/journal.pone.0168280
Polar Geospatial Center, University of Minnesota Reference Elevation Model of Antarctica. https://data.pgc.umn.edu/elev/dem/setsm/REMA
Post E, Alley RB, Christensen TR et al (2019) The polar regions in a 2°C warmer world. Sci Adv 5:eaaw9883. https://doi.org/10.1126/sciadv.aaw9883
Purich A, Cai W, England MH, Cowan T (2016) Evidence for link between modelled trends in Antarctic sea ice and underestimated westerly wind changes. Nat Commun 7:1–9. https://doi.org/10.1038/ncomms10409
QGIS.org (2019) QGIS geographic information system. QGIS Association. http://www.qgis.org
R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Riensche DL, Kitting CL, Groff TC et al (2012) California gull predator management and reproductive success of endangered California least terns in the San Francisco Bay, California. Proc Vertebr Pest Conf. https://doi.org/10.5070/V425110504
Ropert-Coudert Y, Kato A, Meyer X et al (2015) A complete breeding failure in an Adélie penguin colony correlates with unusual and extreme environmental events. Ecography 38:111–113. https://doi.org/10.1111/ecog.01182
Ropert-Coudert Y, Kato A, Shiomi K et al (2018) Two recent massive breeding failures in an adélie penguin colony call for the creation of a marine protected area in D’Urville Sea/Mertz. Front Mar Sci 5:264. https://doi.org/10.3389/fmars.2018.00264
Roy P, Mohanty AK, Misra M (2022) Microplastics in ecosystems: their implications and mitigation pathways. Environ Sci Adv 1:9–29. https://doi.org/10.1039/D1VA00012H
Schmidt AE, Ballard G, Lescroël A et al (2021) The influence of subcolony-scale nesting habitat on the reproductive success of Adélie penguins. Sci Rep 11:1–15. https://doi.org/10.1038/s41598-021-94861-7
Taylor RH (2008) The Adélie penguin pygoscelis adeliae at Cape Royd. Ibis 104:176–204. https://doi.org/10.1111/j.1474-919X.1962.tb08644.x
Waters CN, Zalasiewicz J, Summerhayes C et al (2016) The anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351:1–10. https://doi.org/10.1126/science.aad2622
Wilson DJ, Lyver PO, Greene TC et al (2017) South Polar Skua breeding populations in the Ross Sea assessed from demonstrated relationship with Adélie penguin numbers. Polar Biol 40:577–592. https://doi.org/10.1007/s00300-016-1980-4
Winstral A, Elder K, Davis RE (2002) Spatial snow modeling of wind-redistributed snow using terrain-based parameters. J Hydrometeorol 3:524–538. https://doi.org/10.1175/1525-7541(2002)003%3c0524:SSMOWR%3e2.0.CO;2
Woehler EJ, Penney RL, Creet SM, Burton HR (1994) Impacts of human visitors on breeding success and long-term population trends in Adélie penguins at Casey, Antarctica. Polar Biol 14:269–274. https://doi.org/10.1007/BF00239175
Wood S (2017) Generalized additive models: an introduction with R, 2nd edn. Chapman and Hall/CRC. https://doi.org/10.1201/9781315370279
Wu Q, Brown A (2022) ‘whitebox’: ‘WhiteboxTools’ R Frontend. R package version 2.2.0. https://CRAN.R-project.org/package=whitebox
Acknowledgements
The authors thank the field workers involved in long-term demographic studies at the Pointe Géologie Archipelago. The authors thank David Pinaud and Jade Vacquié-Garcia for valuable comments on the methodology used in the study. The authors thank the IPEV AMMER program No. 1091 (resp. Akiko Kato and Thierry Raclot) for its collaboration.
Funding
The long-term demographic study at Dumont d’Urville station was supported by the French Polar Institute IPEV (OrnithoEco program No. 109, resp. Christophe Barbraud), and the Zone Atelier Antarctique (CNRS-Écologie & Environnement). The data were gathered as part of the « Suivi démographique des oiseaux marins et pinnipèdes en Terre Adélie» (CNRS-Écologie & Environnement long-term observatory, resp. Christophe Barbraud).
Author information
Authors and Affiliations
Contributions
YM, KD, TR, CAB, and CB contributed to the study conception and design. Data curation was performed by YM and KD with support from JV, JA, and VD. Data analysis was performed by YM with input from KD, ASBL, TR, CAB, and CB. The manuscript was written by YM, and all authors contributed to the revisions and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Ethics approval
The Ethics Committee of IPEV and Comite de l’Environnement Polaire approved the field procedures.
Additional information
Communicated by Thomas Koert Lameris.
Sizing the anthropic impact on Antarctic wildlife is a priority of managing committees. We report a long-term effect of infrastructures on a key species. This may help Antarctic conservation planning.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Méheust, Y., Delord, K., Bonnet-Lebrun, AS. et al. Human infrastructures correspond to higher Adélie penguin breeding success and growth rate. Oecologia 204, 675–688 (2024). https://doi.org/10.1007/s00442-024-05523-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-024-05523-0