Reliability of flipper-banded penguins as indicators of climate change

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In 2007, the Intergovernmental Panel on Climate Change highlighted an urgent need to assess the responses of marine ecosystems to climate change1. Because they lie in a high-latitude region, the Southern Ocean ecosystems are expected to be strongly affected by global warming. Using top predators of this highly productive ocean2 (such as penguins) as integrative indicators may help us assess the impacts of climate change on marine ecosystems3, 4. Yet most available information on penguin population dynamics is based on the controversial use of flipper banding. Although some reports have found the effects of flipper bands to be deleterious5, 6, 7, 8, some short-term (one-year) studies have concluded otherwise9, 10, 11, resulting in the continuation of extensive banding schemes and the use of data sets thus collected to predict climate impact on natural populations12, 13. Here we show that banding of free-ranging king penguins (Aptenodytes patagonicus) impairs both survival and reproduction, ultimately affecting population growth rate. Over the course of a 10-year longitudinal study, banded birds produced 39% fewer chicks and had a survival rate 16% lower than non-banded birds, demonstrating a massive long-term impact of banding and thus refuting the assumption that birds will ultimately adapt to being banded6, 12. Indeed, banded birds still arrived later for breeding at the study site and had longer foraging trips even after 10years. One of our major findings is that responses of flipper-banded penguins to climate variability (that is, changes in sea surface temperature and in the Southern Oscillation index) differ from those of non-banded birds. We show that only long-term investigations may allow an evaluation of the impact of flipper bands and that every major life-history trait can be affected, calling into question the banding schemes still going on. In addition, our understanding of the effects of climate change on marine ecosystems based on flipper-band data should be reconsidered.

At a glance


  1. Survival of banded and non-banded king penguins during the 10-year study period.
    Figure 1: Survival of banded and non-banded king penguins during the 10-year study period.

    a, Cumulative survival was lower for banded birds (dashed line) than for non-banded birds (solid line) (Cox proportional hazard model, P = 0.04; assumption of proportional hazards verified, P = 0.83). b, Difference between the cumulative survivals of banded and non-banded penguins over time. There is a breakpoint at 54 months (4.5years) and the linear trend is indicated. Differences between banded and non-banded birds tended to disappear after the first 4.5years.

  2. Simulated population growth rates of banded and non-banded penguins as functions of SST.
    Figure 2: Simulated population growth rates of banded and non-banded penguins as functions of SST.

    a, Growth rates of both populations according to SST at the marginal ice zone (MIZ). Error bars, s.e.m. b, Difference between the two growth rates. A quadratic relation well approximated the difference (Growth rate(0.27±0.01)SST(0.09±0.00)SST2, P<0.001 for both SST and SST2).

  3. Potential mechanisms involved in negative impacts of flipper bands on life-history traits and population dynamics in king penguins.
    Figure 3: Potential mechanisms involved in negative impacts of flipper bands on life-history traits and population dynamics in king penguins.

    Flipper bands and climate interact to affect chick production negatively, mostly through delayed timing, survival and, ultimately, population growth rate.


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Author information


  1. Université de Strasbourg, Institut Pluridisciplinaire Hubert Curien, 23 rue Becquerel, 67087 Strasbourg, France

    • Claire Saraux,
    • Céline Le Bohec,
    • Vincent A. Viblanc,
    • David Beaune &
    • Yvon Le Maho
  2. CNRS, UMR7178, 67037 Strasbourg, France

    • Claire Saraux,
    • Céline Le Bohec,
    • Vincent A. Viblanc,
    • David Beaune &
    • Yvon Le Maho
  3. Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, PO Box 1066, Blindern, N-0316 Oslo, Norway

    • Claire Saraux,
    • Céline Le Bohec,
    • Joël M. Durant &
    • Nils C. Stenseth
  4. AgroParisTech, ENGREF, 19 avenue du Maine, F-75732 Paris, France

    • Claire Saraux
  5. Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France

    • Michel Gauthier-Clerc
  6. Département Milieux et Peuplements Aquatiques, USM 0402/LOCEAN, Muséum National d’Histoire Naturelle, 75231 Paris, France

    • Young-Hyang Park
  7. Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway

    • Nigel G. Yoccoz
  8. Institute of Marine Research, Flødevigen Marine Research Station, N-4817 His, Norway

    • Nils C. Stenseth


C.S. did the analyses and co-wrote the paper; C.L.B. helped in the analyses, the organization of the paper and the writing; Y.L.M. designed the study and co-wrote the paper; V.A.V. provided ideas on the analyses and co-wrote the paper; N.G.Y. proposed one of the analyses and helped with statistics; J.M.D. supplied ideas on the analyses and the organization of the paper; M.G.-C. and N.C.S. added some very useful comments and modifications to the manuscript; D.B. ran some pre-analyses; and Y.-H.P. provided climatic data.

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The authors declare no competing financial interests.

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    The file contains Supplementary Tables 1-3 and Supplementary Figures 1-4 with legends.


  1. Report this comment #17381

    Matt Chew said:

    It's good to see this phenomenon being taken seriously. All "mark and recapture" research programs need to find ways to evaluate the effects of their methods on the fitness of affected individuals, and continually seek ways to minimize observer effects on the organisms under study. "How it's always done" should never be a satisfactory standard.

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