# Arctic climate change and pollution impact little auk foraging and fitness across a decade

Françoise Amélineau, David Grémillet, Ann Harding, Wojciech Walkusz,

Rémi Choquet, Jérôme Fort

► To cite this version:

Françoise Amélineau, David Grémillet, Ann Harding, Wojciech Walkusz, Rémi Choquet, et al., Arctic climate change and pollution impact little auk foraging and fitness across a decade. Scientific Reports, 2019, 9, 10.1038/s41598-018-38042-z. http://dx.doi.org/10.1038/s41598-018-38042-z

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# Arctic climate change and pollution impact little auk foraging and fitness across a decade

Received: 13 June 2018

Accepted: 10 December 2018

Published online: 31 January 2019

Françoise Amélineau ID<fnref n="1" />,², David Grémillet ID<fnref n="1" />,⁶, Ann M. A. Harding³, Wojciech Walkusz⁴,⁵, Rémi Choquet<fnref n="1" /> & Jérôme Fort ID²

Ongoing global changes apply drastic environmental forcing onto Arctic marine ecosystems, particularly through ocean warming, sea-ice shrinkage and enhanced pollution. To test impacts on arctic marine ecological functioning, we used a 12-year integrative study of little auks (Alle alle), the most abundant seabird in the Atlantic Arctic. We monitored the foraging ecology, reproduction, survival and body condition of breeding birds, and we tested linkages between these biological variables and a set of environmental parameters including sea-ice concentration (SIC) and mercury contamination. Little auks showed substantial plasticity in response to SIC, with deeper and longer dives but less time spent underwater and more time flying when SIC decreased. Their diet also contained less lipid-rich ice-associated prey when SIC decreased. Further, in contrast to former studies conducted at the annual scale, little auk fitness proxies were impacted by environmental changes: Adult body condition and chick growth rate were negatively linked to SIC and mercury contamination. However, no trend was found for adult survival despite high inter-annual variability. Our results suggest that potential benefits of milder climatic conditions in East Greenland may be offset by increasing pollution in the Arctic. Overall, our study stresses the importance of long-term studies integrating ecology and ecotoxicology.

Arctic biotas are facing rapid environmental modifications. The Arctic is warming twice as fast as any other place on earth, with visible negative impacts on sea-ice distribution, significantly changing wind regimes and precipitation levels<fnref n="1" />,². The concurrent emergence of competitors³, parasites⁴ or pollutants⁵,⁶ poses additional new threats for Arctic wildlife⁷. In this context, there is an urgent need for long-term monitoring programs to investigate Arctic species and ecosystem reactions to multiple environmental modifications⁸⁻¹². This is especially true in the North as arctic biomes are poorly studied compared to the rest of the world⁷. In this region, coastal ecosystems deserve particular attention¹¹; they host endemic seabirds which have been identified as powerful ecological indicators, and are emblematic for Arctic peoples⁸. Seabirds are subjected to a fair number of long-term monitoring programs in polar regions⁸,¹³⁻¹⁸. Yet most of these studies focus on the sub-Antarctic and the Antarctic, and integrative, long-term studies of the impacts of environmental changes on the foraging ecology and fitness proxies of arctic seabirds are rare (e.g.⁸,¹⁵,¹⁷,¹⁹). Those are however needed to fully apprehend the incidence of ecosystem modifications on these vulnerable species.

In this study, we focused on little auks (Alle alle), the most abundant seabird breeding in the Arctic (estimated 40 to 80 million individuals²⁰). Little auks are ecologically important in regional food webs²¹ and could be negatively impacted by ongoing environmental change²²⁻²⁴. Notably, little auks are zooplanktivorous, and the distribution of their main prey, Calanoid copepods, is changing along with the warming of the North Atlantic. As a result, the range of the smallest and less energy-rich species, Calanus finmarchicus, of Atlantic origin, is extending northwards²⁵. It may result in replacement of the two larger and energetically favoured Arctic species, C. glacialis and C. hyperboreus, that are preferred by little auks²⁶,²⁷. Such a change could prevent birds from covering their energetic needs²²,²⁸. Although previous studies highlighted that little auks from different colonies

<footnote n="1">¹Centre d'Ecologie Fonctionnelle et Evolutive (CEFE) UMR 5175, CNRS - Université de Montpellier - Université Paul-Valéry Montpellier - EPHE, Montpellier, France. ²Littoral Environnement et Sociétés (LIENSs), UMR 7266 CNRS - Université de La Rochelle, La Rochelle, France. ³Environmental Science Department, Alaska Pacific University, Anchorage, AK, USA. ⁴Freshwater Institute, Fisheries and Oceans Canada, 501 University Crescent, Winnipeg, MB, Canada. ⁵Institute of Oceanology, Polish Academy of Sciences, Sopot, Poland. ⁶Percy FitzPatrick Institute and DST/NRF Excellence Centre at the University of Cape Town, Rondebosch, South Africa. Correspondence and requests for materials should be addressed to F.A. (email: francoise.amelineau@gmail.com)</footnote>
<table><caption>**Table 1.** Sample sizes for each biological parameter.</caption><thead><tr><th></th><th>2004</th><th>2005</th><th>2006</th><th>2007</th><th>2008</th><th>2009</th><th>2010</th><th>2011</th><th>2012</th><th>2013</th><th>2014</th><th>2015</th></tr></thead><tbody><tr><td>Foraging behaviour</td><td>4</td><td>—</td><td>—</td><td>6</td><td>10</td><td>—</td><td>—</td><td>—</td><td>8</td><td>8</td><td>11</td><td>20</td></tr><tr><td>Chick diet</td><td>35</td><td>35</td><td>48</td><td>39</td><td>—</td><td>21</td><td>20</td><td>20</td><td>20</td><td>20</td><td>20</td><td>20</td></tr><tr><td>Chick growth</td><td>—</td><td>30</td><td>38</td><td>29</td><td>—</td><td>—</td><td>12</td><td>33</td><td>21</td><td>29</td><td>28</td><td>32</td></tr><tr><td>Adult body condition</td><td>89</td><td>502</td><td>174</td><td>308</td><td>85</td><td>145</td><td>169</td><td>143</td><td>85</td><td>86</td><td>129</td><td>76</td></tr><tr><td>Birds ringed in survival plot</td><td>—</td><td>191</td><td>—</td><td>—</td><td>—</td><td>17</td><td>45</td><td>30</td><td>—</td><td>—</td><td>50</td><td>—</td></tr><tr><td>Hg Winter</td><td>—</td><td>—</td><td>—</td><td>20</td><td>20</td><td>20</td><td>40</td><td>25</td><td>20</td><td>20</td><td>20</td><td>20</td></tr><tr><td>Hg Summer</td><td>—</td><td>—</td><td>10</td><td>12</td><td>9</td><td>18</td><td>8</td><td>10</td><td>20</td><td>—</td><td>—</td><td>10</td></tr><tr><td>Stable isotopes (blood)</td><td>—</td><td>15</td><td>—</td><td>15</td><td>15</td><td>15</td><td>15</td><td>15</td><td>15</td><td>15</td><td>15</td><td>32</td></tr></tbody></table>

can demonstrate strong behavioural plasticity to foraging conditions and prey availability, these studies were performed at the scale of one or a few breeding seasons<sup>29,30</sup> and longer term impacts are unknown. Furthermore, the largest little auk populations rely on sea-ice and polynya<sup>31</sup>, which are likely to disappear soon from their summer foraging grounds according to IPCC predictions<sup>1</sup>, and this could further modify bird foraging behaviour and reproduction<sup>32</sup>. Similarly, changes in wind regimes could directly affect little auk energetics<sup>33</sup> and their capacity to respond to the aforementioned changes. At a broader spatial scale, the North Atlantic Oscillation (NAO) index reflects climatic conditions and is commonly used to test for the effects of climate on seabirds (e.g.<sup>34,35</sup>). The NAO index seems to be particularly well suited to studying the population dynamics of migrants that rely on climatic clues<sup>36</sup>. As an example, survival of little auks breeding in Spitsbergen was linked to winter NAO with a time lag of 2 years, with negative effects on the birds being possibly mediated through varying intakes of little auk prey<sup>23</sup>.

In addition to these climatic and resource modifications, little auks could face large changes in the contamination of their environment. For instance, mercury (Hg) concentrations measured in little auks from East Greenland and reflecting the contamination of their environment have increased by 3.4% per year over the last decade<sup>37</sup>. Mercury is a powerful neurotoxin as well as an endocrine disruptor<sup>38</sup> which could therefore have significant impacts on the reproduction of this arctic seabird species<sup>39,40</sup>. High mercury concentrations could also act as an additional stress factor for adult birds and, in combination with other aforementioned environmental changes, indirectly impact their body condition or foraging performances<sup>41</sup>.

In this context, we propose to examine the multiannual behavioural plasticity of this species in response to environmental change and to investigate impacts on bird fitness. More specifically, and based on recent findings for little auks and their prey, we tested the following hypotheses: (1) the proportion of ice-associated prey in little auk chick diet is decreasing with decreasing sea-ice extent, and the proportion of *Calanus finmarchicus* is increasing<sup>25</sup>. (2) Adult little auks modify their foraging behaviour to cope with a changing environment during summer, to maintain their body condition and the provisioning of their chicks, thereby also maintaining chick growth rates<sup>29,42</sup>. (3) Increasing Hg contamination of little auk environments directly impacts their breeding performances (hatching date, chick growth rate)<sup>39,40</sup> and acts as an additional stress factor for adults, affecting their body condition<sup>41</sup>. (4) Little auk inter-annual survival is impacted by environmental conditions, both during the breeding and the inter-breeding seasons<sup>23,43</sup>.

To test these hypotheses, we used the longest integrative time-series currently available with respect to little auk ecology and ecotoxicology, which we collected at the breeding colony of Ukaleqarteq (East Greenland, Supplementary Fig. S1) during 12 consecutive summers (2004–2015). We investigated adult foraging behaviour, adult and chick diet, adult winter survival, chick growth, hatching date, and tested the incidence of environmental conditions (sea-surface temperature, sea-ice concentration (SIC), wind force, North Atlantic Oscillation and Hg concentrations inferred from levels measured in bird feathers).

## Results

A summary of sample sizes and biological parameters monitored annually is presented in Table 1. Despite a 12-year long dataset, we were limited by gaps in some of our biological measures and environmental variables (Table 1). This prevented the use of a global approach with causal inference, such as path analysis<sup>44</sup>, as well as the use of principal component analysis to reduce the number of environmental covariables<sup>45</sup>. For this reason, we decided to apply a hypothesis-based approach to target specific questions. We therefore built independent regression models for each biological parameter studied, to test the effects of one or two environmental covariates at a time, to avoid overfitting<sup>45</sup>. A summary of the results is presented in Table 2.

**Environmental variables.** Over the period 2004–2015, mean summer SIC varied between 1.8 and 19.8% within the foraging range of little auks (Fig. 1), allowing us to study the links between ice conditions and little auk ecology. SIC was negatively related to sea-surface temperature (SST, n = 12, R<sup>2</sup> = 0.74, p < 0.001, y = -6.1x + 13.6) and to wind speed (n = 8, R<sup>2</sup> = 0.57, p = 0.03, y = -1.3x + 42.9, Fig. 1). No temporal trend was found for summer SIC during the study period, however, a decrease in SIC was found in the same area for the period 1979–2014<sup>26</sup>. In addition, the range of SIC encountered in our study period was lower than the range of SIC for the period 1979–2000 (10 to 40%<sup>26</sup>). Summer Hg contamination of little auk environment (derived from body feathers, BF, see methods for details) did not vary with SIC (p > 0.1).

**Variations in chick and adult diet.** We found an inter-annual variability in chick diet (Figs 2 and 3, n = 298). Changes in the proportions of *Calanus finmarchicus*, *C. glacialis* and other prey were best explained by
<table><caption>**Table 2.** Summary of the interactions found between biological and environmental parameters. Results are presented in the direction of expected environmental changes, with a decrease in sea-ice concentration (SIC) and an increase in mercury (Hg). ✓: increase, \: decrease, NS: non significant, —: not tested according to our hypotheses. (*p* = 0.052).</caption><thead><tr><th rowspan="3"></th><th rowspan="3"></th><th rowspan="3"></th><th colspan="7">Environmental parameters</th></tr><tr><th colspan="2">summer</th><th colspan="5">Winter</th></tr><tr><th>SIC</th><th>Hg</th><th>SST</th><th>Wind</th><th>Hg</th><th>NAO</th><th>Time</th></tr></thead><tbody><tr><td rowspan="12">Biological parameters</td><td rowspan="4">Diet</td><td rowspan="3">Chick diet</td><td>Apherusa glacialis</td><td>\</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Calanus hyperboreus</td><td>NS</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Calanus glacialis</td><td>✓</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Calanus finmarchicus</td><td>\</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td rowspan="2">Adult diet</td><td>δ<sup>15</sup>N</td><td>NS</td><td>—</td><td>—</td><td>—</td><td>—</td><td>✓</td></tr><tr><td>δ<sup>13</sup>C</td><td>NS</td><td>—</td><td>—</td><td>—</td><td>—</td><td>✓</td></tr><tr><td rowspan="4">Foraging behaviour</td><td>Maximum depth</td><td>✓</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Dive duration</td><td>✓</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Number of dives/day</td><td>\</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Time spent underwater</td><td>\</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td rowspan="5">Fitness proxies</td><td>Foraging trip duration</td><td>NS</td><td>—</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Adult body condition</td><td>✓</td><td>\</td><td>—</td><td>—</td><td>—</td><td>—</td></tr><tr><td>Chick growth rate</td><td>✓</td><td>\</td><td>—</td><td>—</td><td>—</td><td>\*</td></tr><tr><td>Hatching date</td><td>\</td><td>—</td><td>—</td><td>—</td><td>NS</td><td>✓</td></tr><tr><td>Survival probability</td><td>NS</td><td>NS</td><td>NS</td><td>NS</td><td>NS</td><td>NS</td></tr></tbody></table>

<figure><img src="image_3.png" /><figcaption>**Figure 1.** Environmental parameters during the breeding season: (a) Sea-ice concentration (SIC, solid line), (b) Sea surface temperature (SST, dotted line) and (c) wind speed (dashed line) during summer in the vicinity of the studied colony, from remote sensing data. (d) Mean mercury concentration of body feathers representing summer contamination (solid line and black dots). SIC was negatively linked with both SST (n = 12, R² = 0.74, p < 0.001, y = -6.1x + 13.6) and wind speed (n = 8, R² = 0.57, p = 0.03, y = -1.3x + 42.9) but was not linked with summer Hg contamination (n = 8, p > 0.1).</figcaption></figure>

GAMs (Fig. 3a-c) while proportions of *Apherusa glacialis* and *C. hyperboreus* were best explained by linear models (Fig. 3d,e). The proportion of *Calanus finmarchicus* increased at higher SIC (N = 298, p = 0.001, R² = 0.05, Fig. 3a). The proportion of *Calanus glacialis* was lower when SIC was >10% (N = 298, p < 0.0001, R² = 0.13, Fig. 3b). The proportion of *Apherusa glacialis* increased with SIC (N = 298, p = 0.01, R² = 0.04, y = 0.035x - 2.1, Fig. 3d). The proportion of *C. hyperboreus* did not vary with SIC (N = 298, p = 0.25, R² = 0.005, Fig. 3e). The proportion of other prey was higher when SIC was <5% (N = 298, p < 0.0001, R² = 0.28, Fig. 3c).

Adult diet, as reflected by δ¹⁵N isotopic values, did not change along with SIC (n = 167, p > 0.1). However, adult foraging ecology changed over time (Fig. 4, trophic status δ¹³N: n = 167, R² = 0.32, p < 0.001, y = -138 + 0.07x, feeding habitat δ¹³C: n = 167, R² = 0.36, p < 0.001, y = 96.4 - 0.06x).

**Foraging behaviour.** Analysis of dive depths for all dives across the study period showed a bimodal pattern with two distinct peaks: one with dives <7 m and one with dives between 10 and 40 m (Fig. 5). Further
<figure><img src="image_4.png" /><figcaption>**Figure 2.** Relative chick diet composition of main prey, classified by increasing sea-ice concentration.</figcaption></figure>

<figure><img src="image_5.png" /><figcaption>**Figure 3.** Changes in chick diet with sea-ice concentration (SIC; N = 298). (a) *Calanus finmarchicus*, GAM, p = 0.001, R² = 0.05; (b) *C. glacialis*, GAM, p < 0.0001, R² = 0.13; (c) other prey species, GAM, p < 0.0001, R² = 0.28; (d) *Apherusa glacialis*, linear model, p = 0.01, R² = 0.04, y = 0.035x - 2.1; and (e) *C. hyperboreus*, linear model, p = 0.25, R² = 0.005. Logit (p + a) represents the logit transformation applied to the proportion of prey (p) and a constant a (see Material and Methods for details).</figcaption></figure>

investigations showed a link between diving behaviour and SIC (Fig. 6). Dives were deeper and the proportion of shallow dives (<7 m) decreased when there was less ice (Fig. 6a,b; Maximum depth: n = 67, R² = 0.26, p < 0.001, y = -0.40x + 21.7, Proportion of shallow dives: n = 67, R² = 0.40, p < 0.001, y = 1.68x + 5.74). Dives were also longer and birds performed fewer dives per day when SIC decreased (Fig. 6c,d; Dive duration: n = 67, R² = 0.38, p < 0.001, y = -0.91x + 63.0, Number of dives per 24 h: n = 61, R² = 0.26, p < 0.001, y = 9.6x + 226.8). Birds spent slightly less time underwater and more time flying when SIC was low (Fig. 6e,f; Time underwater: n = 61, R² = 0.09, p = 0.02, y = 0.31x + 17.0, Time spent flying: n = 53, R² = 0.12, p = 0.01, y = -0.62x + 38.0). There was no link between foraging trip duration and SIC (n = 53, R² = 0.004, p > 0.1).
<figure><img src="image_6.png" /><figcaption>**Figure 4.** Temporal variation of adult δ¹⁵N and δ¹³C values (‰) over the study period. (a) δ¹⁵N, linear model, n = 167, R² = 0.32, p < 0.001, y = -138 + 0.07x. (b) δ¹³C, linear model, n = 167, R² = 0.36, p < 0.001, y = 96.4 - 0.06x.</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>**Figure 5.** Distribution of maximum dive depths for all recorded dives over the study period. N = 75,173 dives from 67 individuals.</figcaption></figure>

**Adult body condition, chick growth and hatching date.** Hatching date was delayed when SIC increased (n = 303, R² = 0.08, p < 0.001, y = 16.7 + 0.15x, Fig. 7a) but was not linked to female exposure to Hg during winter (n = 225, p > 0.1). Chicks hatched later over time (n = 303, R² = 0.11, p < 0.001, y = -660 + 0.34x).

A decrease in chick growth rate (mass gained per day) was observed when SIC increased (n = 252, R² = 0.03, p = 0.007, y = -0.037x + 6.79, Fig. 7b). Chick growth rate decreased when summer Hg increased (n = 165, R² = 0.03, p = 0.02, y = -0.66x + 7.2, Fig. 7c) and chick growth rate tended to decrease over time (n = 252, R² = 0.02, p = 0.052, y = 103 - 0.05x).

Adult body condition worsened with increasing summer Hg and increasing SIC (n = 1051, R² = 0.04, p(Hg) < 0.001, p(SIC) < 0.001, y = 9.9 - 0.030x₁ - 4.2x₂ - 0.18x₃, with x₁ = day of year, x₂ = Hg, x₃ = SIC, Fig. 8), but there was no difference between years (n = 1787, p > 0.1).

**Survival.** Results of the goodness-of-fit tests are detailed in the methods and in Table 3. A summary of the selection model process is presented in Table 4. We constructed a model with capture heterogeneity due to the physical structure of the colony where some burrow entrances were harder to monitor⁴⁶. Survival probabilities for the best model (φ(t), p(het + t)) is presented in Fig. 9. No direct relationship was found between survival and environmental parameters (tested one by one: North-Atlantic Oscillation (current year, previous year and two years before²³), SST in their wintering area (current and previous year) and in their breeding area, SIC, wind conditions, summer and winter Hg). Survival probability was lower for two years: 2006–2007 and 2012–2013 (Fig. 9).

**Discussion**

Using a unique dataset of biological parameters from a 12-year long-term monitoring program in East Greenland, we found that little auks are impacted by current environmental changes occurring in the Arctic. (1) As expected, the proportion of ice-associated species in chick diet was related to SIC, but the proportion of *C. finmarchicus* (copepod of Atlantic origin) did not decrease with increasing SIC. (2) Despite substantial plasticity in foraging behaviour and diet, adult body condition and chick growth rates decreased when SIC increased. (3) Adult body
<figure><img src="image_8.png" /><figcaption>**Figure 6.** Dive characteristics in relation to sea-ice concentration. (a) Maximum depth (n = 67, R² = 0.26, p < 0.001, y = -0.40x + 21.7). (b) Proportion of shallow dives (n = 67, R² = 0.40, p < 0.001, y = 1.68x + 5.74). (c) Dive duration (n = 67, R² = 0.38, p < 0.001, y = -0.91x + 63.0). (d) Number of dives per 24 h (n = 61, R² = 0.26, p < 0.001, y = 9.6x + 226.8). (e) Time underwater (n = 61, R² = 0.09, p = 0.02, y = 0.31x + 17.0). (f) Time spent flying (n = 53, R² = 0.12, p = 0.01, y = -0.62x + 38.0).</figcaption></figure>

condition and chick growth rate were negatively related to summer levels of mercury. (4) Despite these changes, adult survival was not linked to environmental variables.

**Methodological caveats.** Overall, we detected strong environmental impacts on little auks, but our work entails methodological limitations. Indeed, organism answer to overall forcing is the integration of all
<figure><img src="image_9.png" /><figcaption>**Figure 7.** (a) Linear relationship between hatching date and SIC (n = 303, R² = 0.08, p < 0.001, y = 16.7 + 0.15x), (b) Linear relationship between chick growth rate and SIC (n = 252, R² = 0.03, p = 0.007, y = -0.037x + 6.79), (c) Linear relationship between chick growth rate and summer mercury contamination (n = 165, R² = 0.03, p = 0.02, y = -0.66x + 7.2).</figcaption></figure>

environmental parameters, and disentangling the relative importance of each factor as well as their interactions requires advanced statistical methods that we could not apply due to temporal gaps in our datasets (Table 1). Consequently, as we used only one or two environmental independent variables at a time to explain one biological parameter with a hypothesis-based approach, the percentage of covariance explained by our significant relationships was low. It is therefore crucial to continue long-term monitoring programs to increase sample sizes. In addition, we possibly missed important additional environmental factors. For instance, we know that the timing of breeding in little auks is linked to the timing of snow melt in spring, which determines nest accessibility⁴⁷. Spring snow melt can be approximated by spring temperature, but we did not have access to this information at our study site. Also, other pollutants could, in addition to Hg, impact little auk reproduction and survival (e.g.⁴⁸,⁴⁹) but were not considered in the present study. Concerning survival data, we could not take oil spills into account⁵⁰, although it is known that little auks can be highly impacted during winter, with for instance an estimated 22,000 guillemots and little auks killed by hydrocarbon contamination in 2011–2012 off Newfoundland⁵¹.

**Foraging plasticity as a buffer to climate change.** Among all biological parameters investigated, foraging behaviour was the most variable. While little auks foraged in the same areas at the shelf break with or without sea-ice²⁶, we found that diving behaviour changed with SIC: Birds performed shallower and shorter dives when SIC was the highest (Fig. 6). Thereby, dives <7 m (Fig. 5, Supplementary Fig. S2) probably reflected foraging directly underneath the sea ice, to feed on sympagic species such as *Aферуса glacialis*, and indeed the proportion of this species in chick diet increased along with SIC (Fig. 3d). This was also supported by preliminary results concerning birds for which diving behaviour and diet were collected simultaneously (n = 15, Amélineau *et al.* unpublished).
<figure><img src="image_10.png" /><figcaption>**Figure 8.** Predicted effects of summer mercury (Hg) contamination and SIC on adult body condition (residual body mass). Predictions were calculated from the model $y = -0.030x_1 - 4.2x_2 - 0.18x_3 + 9.9$, with $x_1$ = day of year, $x_2$ = Hg, $x_3$ = SIC.</figcaption></figure>

<table><caption>**Table 3.** Goodness of fit of the CJS (Cormack Jolly Seber) model by U-CARE. The CJS model is rejected.</caption><thead><tr><td>Test</td><td>df</td><td>χ<sup>2</sup></td><td>P</td></tr></thead><tbody><tr><td>3.SR</td><td>5</td><td>9.45</td><td>0.092</td></tr><tr><td>3.SM</td><td>4</td><td>5.36</td><td>0.252</td></tr><tr><td>2.CT</td><td>8</td><td>77.71</td><td>&lt;0.001</td></tr><tr><td>2.CL</td><td>5</td><td>5.10</td><td>0.404</td></tr><tr><td>Sum</td><td>22</td><td>97.6</td><td>&lt;0.001</td></tr></tbody></table>

Little auks seem capable of switching from pelagic to below-ice feeding, and therefore to cope with a wide range of foraging conditions. Their energy expenditure as determined using the doubly-labelled water (DLW) technique thereby seemed to remain unchanged<sup>29</sup>, yet additional studies combining 3D acceleration recordings of their actual foraging movements, and DLW are needed to fully test the impact of foraging plasticity on energy balance<sup>52–54</sup>.

Changes in little auk diet reflect their preferences, as well as prey availability in the environment. Recent studies suggest that little auks favour larger and fattier species<sup>26,27</sup> and, therefore, observed changes in prey proportions are likely to reflect the availability of larger prey species in the foraging range of birds. In the North Atlantic Arctic, it is predicted that smaller *C. finmarchicus* should be present during “warm” conditions (high SST, low SIC), and larger *C. glacialis* and *C. hyperboreus* in “cold” conditions (low SST, high SIC)<sup>25,55,56</sup>. However, proportions of little auk main prey, the three species of *Calanus*, did not vary as expected: the proportion of *C. finmarchicus* slightly increased at higher SIC, and the proportion of *C. glacialis* decreased at higher SIC. Underlying mechanisms driving zooplankton abundance at a given place are complex and do not depend solely on local summer SIC/SST, but might also vary with, for instance salinity and depth<sup>57</sup> which were not included in this study. However, little auks have access to distant foraging areas spread over dozens of kilometers where depth and salinity and thus prey availability might vary substantially<sup>27</sup>. In addition, it should be noted that although slightly increasing with SIC, the proportion of *C. finmarchicus* in chick diet remained low in comparison to other *Calanus* species, whatever the SIC (Fig. 2). Interestingly, despite no clear pattern in chick diet, adult diet shifted to a higher trophic level (higher δ<sup>15</sup>N values) and to more offshore feeding habitats (lower δ<sup>13</sup>C values) during the study period (Fig. 4). Such stable isotope analyses are particularly integrative and could therefore reflect fine changes occurring in the longer term among the zooplankton community. Moreover, it is still unclear whether adults and chicks feed on the exact same prey because the compositions of their diets have never been measured concomitantly. While stomach contents of adults are comparable to gular pouch samples<sup>58,59</sup>, stable isotope studies suggest that there could be a difference<sup>60,61</sup>, as do our observations. More generally, little auks seem able to cope with different prey assemblages in their environment<sup>27,30,62–64</sup>.

**Do little auk living conditions improve in the absence of sea-ice?** Little auks have a non-obligate affinity to sea-ice which varies according to location or timing of the year. During the breeding season, they can forage at the marginal ice zone in Spitsbergen<sup>32,65</sup> but can also thrive in the absence of sea-ice<sup>26,66</sup>. After the breeding season, birds from different colonies migrate towards higher latitudes and the MIZ to moult<sup>67,68</sup>, before
<table><caption>**Table 4.** Model selection for the survival analysis. Φ: survival probability. p: resighting probability. Np: number of identifiable parameters. ΔQAICc: difference between the current model AIC and the smallest AIC. QAICc W: QAIC weight. het: heterogeneity of capture (seen with a high probability/seen with a low probability/not seen). NAO: North Atlantic Oscillation winter index. SST or NAO n-1 = the winter of year n-1. δ<sup>13</sup>C and δ<sup>15</sup>N: summer isotopes from blood. The best model is in bold.</caption><thead><tr><th>Φ</th><th>p</th><th>Np</th><th>ΔQAICc</th><th>QAICc W</th><th>Deviance</th></tr></thead><tbody><tr><td colspan="6"><strong>STEP 1: models with time and capture heterogeneity</strong></td></tr><tr><td>time</td><td>het x time</td><td>30</td><td>13.26</td><td>0.00</td><td>1367.80</td></tr><tr><td><strong>time</strong></td><td><strong>het + time</strong></td><td><strong>22</strong></td><td><strong>0.00</strong></td><td><strong>0.87</strong></td><td><strong>1371.41</strong></td></tr><tr><td>time</td><td>het</td><td>13</td><td>7.35</td><td>0.02</td><td>1397.42</td></tr><tr><td>1</td><td>het + time</td><td>13</td><td>26.84</td><td>0.00</td><td>1416.91</td></tr><tr><td>time</td><td>time</td><td>19</td><td>105.13</td><td>0.00</td><td>1482.80</td></tr><tr><td>time</td><td>1</td><td>11</td><td>128.21</td><td>0.00</td><td>1522.38</td></tr><tr><td colspan="6"><strong>STEP 2: models with environmental data</strong></td></tr><tr><td>summer wind</td><td>het + time</td><td>15</td><td>4.61</td><td>0.09</td><td>1390.56</td></tr><tr><td>winter wind</td><td>het + time</td><td>15</td><td>8.27</td><td>0.01</td><td>1394.22</td></tr><tr><td>winter Hg + winter SST</td><td>het + time</td><td>15</td><td>16.85</td><td>0.00</td><td>1402.81</td></tr><tr><td>winter SST n-1</td><td>het + time</td><td>14</td><td>18.04</td><td>0.00</td><td>1406.05</td></tr><tr><td>summer Hg + SIC</td><td>het + time</td><td>15</td><td>18.48</td><td>0.00</td><td>1404.43</td></tr><tr><td>prop. of winter wind > 40 km/h</td><td>het + time</td><td>15</td><td>20.08</td><td>0.00</td><td>1406.03</td></tr><tr><td>SIC</td><td>het + time</td><td>14</td><td>21.28</td><td>0.00</td><td>1409.29</td></tr><tr><td>prop. of winter wind > 30 km/h</td><td>het + time</td><td>15</td><td>23.04</td><td>0.00</td><td>1408.99</td></tr><tr><td>NAO n-1 + winter SST</td><td>het + time</td><td>14</td><td>26.50</td><td>0.00</td><td>1414.51</td></tr><tr><td>NAO n-1</td><td>het + time</td><td>14</td><td>27.25</td><td>0.00</td><td>1415.26</td></tr><tr><td>NAO n-1 + NAO n-2</td><td>het + time</td><td>14</td><td>27.70</td><td>0.00</td><td>1415.72</td></tr><tr><td>NAO n-2</td><td>het + time</td><td>14</td><td>28.26</td><td>0.00</td><td>1416.27</td></tr><tr><td>NAO</td><td>het + time</td><td>14</td><td>28.40</td><td>0.00</td><td>1416.41</td></tr><tr><td>winter SST</td><td>het + time</td><td>14</td><td>28.53</td><td>0.00</td><td>1416.55</td></tr><tr><td>time x summer body condition</td><td>het + time</td><td>14</td><td>28.68</td><td>0.00</td><td>1416.70</td></tr><tr><td>NAO + SST n-1</td><td>het + time</td><td>14</td><td>28.81</td><td>0.00</td><td>1416.83</td></tr><tr><td>winter SST + NAO</td><td>het + time</td><td>14</td><td>28.82</td><td>0.00</td><td>1416.83</td></tr><tr><td>summer Hg + winter Hg</td><td>het + time</td><td>15</td><td>29.60</td><td>0.00</td><td>1415.55</td></tr><tr><td>SST n-1 + NAO n-1</td><td>het + time</td><td>14</td><td>29.91</td><td>0.00</td><td>1417.92</td></tr><tr><td>summer Hg</td><td>het + time</td><td>15</td><td>31.55</td><td>0.00</td><td>1417.50</td></tr><tr><td>winter Hg</td><td>het + time</td><td>15</td><td>33.03</td><td>0.00</td><td>1418.98</td></tr><tr><td>NAO + NAO n-1</td><td>het + time</td><td>14</td><td>33.74</td><td>0.00</td><td>1421.76</td></tr><tr><td>winter SST + winter SST n-1</td><td>het + time</td><td>14</td><td>33.81</td><td>0.00</td><td>1421.82</td></tr><tr><td>summer δ<sup>15</sup>N</td><td>het + time</td><td>13</td><td>363.62</td><td>0.00</td><td>1753.68</td></tr><tr><td>summer δ<sup>13</sup>C</td><td>het + time</td><td>13</td><td>366.85</td><td>0.00</td><td>1756.91</td></tr><tr><td>summer δ<sup>15</sup>N + summer δ<sup>13</sup>C</td><td>het + time</td><td>13</td><td>366.98</td><td>0.00</td><td>1757.05</td></tr><tr><td>summer SST</td><td>het + time</td><td>13</td><td>367.76</td><td>0.00</td><td>1757.83</td></tr></tbody></table>

reaching their wintering grounds. At our study site, contrasting SIC from year to year allowed to study impacts on little auk foraging and fitness proxies.

Interestingly, adult body condition and chick growth rates were higher when SIC was low, meaning that less sea-ice and higher SSTs provided better environmental conditions for breeding little auks in East Greenland. The link between environmental conditions and fitness proxies could be direct, as higher temperatures reduce energy requirements for thermoregulation³³, and energy gained could then be reallocated to body maintenance or chick rearing. Linkages could also be indirect, via trophic interactions and bottom-up effects: lower SIC during summer reflects an earlier sea-ice breakup and a shorter lag between ice-algae bloom and pelagic phytoplankton bloom⁶⁹. Our results suggest that prey quality and/or availability would be better when sea-ice breakup occurs earlier. However, this is not in accordance with previous findings from Spitsbergen, where earlier sea-ice breakup lead to a mismatch between algal blooms and copepod *C. glacialis* phenology, and ultimately to a lower chick survival in little auks and Brünnich's guillemots⁷⁰,⁷¹. Changes in the trophic interactions occurring in the Western Greenland Sea are probably more complex and reflects high variability of local conditions throughout the Arctic¹². Lastly, SIC encountered during the study period (2004–2015, 9.1 ± 6.8%) were already lower than SIC encountered during the period 1979–2003 (20.0 ± 10.4%)²⁶ and may already feature suboptimal conditions for little auks.

Regarding SSTs, previous studies suggested that the most profitable foraging areas for little auks are located in the cold waters encountered in the Sørkapp Current (SW Spitsbergen) and in the East Greenland Current that contain bigger *Calanus* species²⁷,⁷². Our results contrast with those from previous studies performed in Spitsbergen where higher SSTs were associated with a higher proportion of *C. finmarchicus* in the environment and in chick
<figure><img src="image_11.png" /><figcaption>**Figure 9.** Survival probability of adult little auks over the study period. Year represent the recapture year (e.g. 2015 for the 2014-2015 survival rate). Dashed lines represent 95% CI.</figcaption></figure>

diet, and led to a lower chick survival or probability to fledge<sup>22,72</sup>, and to a lower adult survival<sup>23</sup>. SSTs are higher in Western Spitsbergen than in East Greenland, and these contrasting findings suggest that little auk fitness could follow a quadratic relationship with SST, peaking at intermediate SST. An increase in SST could then be beneficial at low SSTs (East Greenland, mean SST of 0.67 °C) but detrimental at high SSTs (Spitsbergen, mean SST of 1.81 °C at Hornsund and 4.51 °C at Kongsfjorden). However, little auks did not seem impacted by observed changes in SST around Bjørnøya, where they foraged in warm waters (median SST of 6.6 °C) during the period 2005–2012<sup>66</sup>.

Among pagophilic seabird species, reactions to variations in SIC are diverse and depend on species-specific sea-ice affinity. High SIC during the breeding season can reduce access to prey and lead to lower breeding success for moderately pagophilic seabirds<sup>15,16,73</sup>. Species that are more dependent on sea-ice, on the contrary, have lower breeding success and survival when SIC is reduced, and have to travel over longer distances to reach the MIZ<sup>74,75</sup>. At the larger temporal and spatial scales, changes in SIC likely lead to changes in species range to the detriment of pagophilic species<sup>9,76</sup>.

**Pollutants offset observed benefits from lower SIC.** Hg concentrations during summer increased in adult little auks, likely linked to an increase in prey Hg concentrations over time<sup>37</sup>, but also to changes in diet towards prey that are higher in the food chain (biomagnifications)<sup>77</sup>, as reflected by the increase in δ<sup>15</sup>N in adult blood (Fig. 4a). Although measured Hg concentrations were below toxicity thresholds<sup>38,78</sup>, they were negatively related to adult body condition and chick growth rate. These observed effects suggest that Hg might act as a cumulative stressor which, in combination with other environmental constraints like the quality of their habitat or resource availability<sup>41</sup>, could impact the condition of marine predators beyond its single effects. In addition, one should also bear in mind that little auks are exposed not only to Hg, but to a variety of pollutants reaching the Arctic from northern mid-latitude industrial regions, some of them emerging but already of high concern in this sensitive region<sup>79</sup>. We specifically focused on Hg, which is known to bioaccumulate in polar regions and severely impact marine top predators<sup>38,78</sup>, but these other pollutants may as well impact little auk metabolism and ultimately their body condition and growth rate, such as organochlorine pesticides or PFASs<sup>80</sup>. In addition, Hg disrupts breeding behavior in black-legged kittiwakes and snow petrels<sup>40,81</sup> and this mechanism could also explain reduced chick growth when Hg concentrations are high in our study. However, no link was found between Hg and adult survival in our study, as well as in other seabird species<sup>48,82-84</sup>.

Hg levels in the Arctic are modified by ongoing environmental changes<sup>85</sup>. In particular, increasing Hg trends are expected with permafrost thawing, the warming of ocean water masses and increasing human activities in the Arctic<sup>85-87</sup>. According to our results, negative effects of increasing Hg could offset observed positive effects of climate warming in East Greenland. This stresses again the complexity of biological answers to environmental changes and the need for integrative approaches.

## Conclusion

Understanding how animals will cope with environmental changes is a topical challenge in ecology. Since the Arctic is warming twice as fast as the rest of the world it can be seen as a natural laboratory to anticipate changes occurring at a more global scale. Unfortunately, logistical constraints, including year round access, limit fieldwork studies in this part of the world. In addition, biological responses are complex and integrate environmental constraints which may be logistically difficult to evaluate at remote locations. Our results highlight the importance of pursuing long term monitoring programs in the Arctic to improve dataset length and quality, and gain power to elaborate more complex models<sup>88</sup>.

## Methods

**General fieldwork context.** All field work in East Greenland was conducted in accordance with guidelines for the use of animals<sup>89</sup>. Experiments were approved by the Danish Polar Center and the Government of Greenland, Ministry of Environment and Nature and Department of Fisheries, Hunting and Agriculture (No. 512-240 (2005), No. 512-258 (2006), No. 07-501 (2007), No. 66.24/23 (2008), No. 66.01.13 (2009 and 2010), No. 2011-047447 (2011), No. 2012-065815 (2012), No. 2013-083634 (2013), No. 2014-098814 (2014) No. 2015-115290 (2015).
Little auks from Ukaleqarteq (Kap Höegh, East Greenland, 70°44′N, 21°35′W, Supplementary Fig. S1a) were studied during the breeding season (mid-July/mid-August) from 2004 to 2015. Birds breed under rocks in steep boulder fields, where they raise a single offspring. Adult birds fly out to sea where they forage on zooplankton, which they bring back to their chick in a sublingual pouch. During the inter-breeding period (Sept-May), birds migrate to wintering areas in the North Atlantic, notably off Newfoundland⁹⁰. Each summer, a set of biological parameters detailed below were monitored, and sample sizes are presented in Table 1. Adult birds were caught either in their nest or on the surrounding rocks using a lasso or noose carpets. Breeding status was assessed by the presence of a chick, a full sublingual pouch or a brood patch. Handling time was <10 min. For all sampling except for the survival study (see below), each year different individuals were studied. Therefore, our investigations were mainly conducted at the population – and not at the individual – level.

**Chick and adult diet.** Breeding adults were captured on arrival at the colony and the content of their sub-lingual pouch (chick diet) was removed and stored either in 4% borax-buffered formaldehyde solution (2005 to 2007) or in 70% ethanol (2008 and beyond). Samples were identified to the lowest possible taxonomical level under a stereomicroscope following groups presented in Harding *et al.*²⁸. Adult diet was estimated from stable isotope analyses (δ¹⁵N and δ¹³C) performed on total blood samples⁶¹. δ¹⁵N isotopic values reflect the relative trophic posi-tion of birds and are considered an indicator of their diet a couple of weeks before the sampling⁹¹. δ¹³C was also considered as an indicator of bird foraging habitats with higher values representing more coastal habitats⁹¹. Blood samples (0.3 ml) were collected from bird brachial vein, stored in 70% ethanol and kept frozen at -20 °C. Prior to analyses, blood samples were freeze-dried for 48 h and homogenized. Stable isotope analyses were then performed on ~0.5 mg subsamples of homogenized, non-lipid extracted whole blood loaded into tin cups, and using an ele-mental analyzer (Flash EA 1112, Thermo Fisher) coupled in continuous flow mode to an isotope ratio mass spec-trometer (Delta V Advantage, Thermo Fisher, Bremen, Germany). Stable isotope abundances were expressed in δ notation as the deviation from standards in parts per thousand (‰) according to the equation: δX = [(Rsample/ Rstandard) - 1] × 1000 where X is ¹³C or ¹⁵N and R is the corresponding ratio ¹³C/¹²C or ¹⁵N/¹⁴N. Standard values were Vienna Pee Dee Belemnite (VPDB) for C and atmospheric N₂ (air) for N. Replicate measurements of internal laboratory standards (acetanilide) indicated that the measurement error was <0.2% for both δ¹⁵N and δ¹³C values.

**Foraging behaviour.** Numbers of equipped birds are presented in Table 1. Breeding adults were equipped with temperature-depth recorders (TDRs) attached ventrally, recording at 0.2, 0.5 or 1 Hz for 2–5 d during the chick-rearing period. Details on TDR types and attachment methods are presented in Supplementary Methods and Supplementary Table S1. Data were analyzed with MultiTrace™ to extract maximum dive depth, dive and pause duration for each dive. Depth was corrected for Star Oddi devices because they showed a slight underes-timation of depth according to a calibration made in Amélineau *et al.*²⁶. We also measured time spent flying and foraging trip duration following Welcker *et al.*⁹², and calculated the time spent underwater, and the number of dives per day. For each parameter, a mean value per individual was calculated and used for statistical analyses.

**Hatching date and chick growth.** Nests were controlled for hatching date and chicks were weighed every second day. For each chick, we calculated the chick growth rate (g d⁻¹) as the slope of the linear growth period²⁶ (4–14 days). Due to logistical constraints usually preventing measurements after August 10, we could not control all nests until fledging to measure fledging success (range of fledging age = 21–31 days⁹³).

**Adult body condition and mercury contamination.** Each handled adult was weighed (g), and wing and head-bill lengths were measured (mm). We constructed a body condition index, correcting adult body mass by wing length and head-bill length to take bird size into account. The body condition index was calculated as the residual body mass from a regression of body mass on wing length and head-bill length⁴³.

Total Hg was measured on one complete back cover feather (abbreviated BF hereafter) or one complete throat feather (abbreviated HF hereafter) using an advanced Hg analyzer spectrophotometer (Altec AMA 254) as described in Bustamante *et al.*⁹⁴. Hg in little auk BF reflect the amount of Hg accumulated by birds during the previous breeding season spent in East Greenland (year preceding the sample), while Hg in HF reflect the amount of Hg accumulated during the previous winter (see Fort *et al.*³⁷). Hence, BF collected from 2007 to 2016 were analyzed for comparison with the biological time-series. Previous studies showed that >90% of Hg in seabird feathers is methyl-Hg (Me-Hg), the most toxic form of Hg⁹⁵. Total Hg measured in feathers is thus considered as an indicator of bird exposure to Me-Hg. Hg concentrations measured in bird feathers are also an indicator of the contamination level of the food chain on which birds feed during both seasons³⁷. Analyses were repeated two or three times (two or three feathers) for each bird and feather type until the relative standard deviation for two samples was <10%; samples not meeting this criterion were excluded from the analysis. The mean Hg concentra-tions for those two or three measurements were then considered for statistical analyses. To ensure the accuracy of measurements, a certified reference material (CRM) was used [Lobster Hepatopancreas Tort-2; NRC, Canada; Hg concentration of 0.27 ± 0.06 µg.g⁻¹ of dry weight (dw)]. The CRM was measured every 10 samples and the average measured value was 0.26 ± 0.01 µg.g⁻¹ dw (n = 113). Additionally, blanks were run at the beginning of each sample set. The detection limit of the method was 0.005 µg.g⁻¹ dw.

**Survival analysis.** One plot of the colony was dedicated to a capture-mark-recapture experiment. Birds (n = 333) were marked with a unique code composed of 3 colour rings and one metal ring. Each season, recap-ture sessions lasted 6 d with 7 h of continuous observation per day. Data were analyzed using a capture-recapture model⁹⁶ with E-SURGE. We first built a structural model without any external covariate. To define the structural model, we first did single state goodness-of-fit tests (GOF, Table 3) using U-CARE⁹⁷. Only the 2.CT test was
significant, indicating a difference in the probability of being recaptured at $i + 1$ for birds seen and not seen at occasion i. In order to take into account recapture heterogeneity among marked birds, we used a model with two classes of capture⁹⁸ and defined three states: individuals with a high recapture probability, individuals with a low recapture probability and dead individuals. Changes of state between high and low recapture probability were not permitted. Such a structure explained our data better than a model including trap-dependence or allowing changes of recapture probability through time (if, for example, this was linked to breeding status). Biologically, recapture heterogeneity was due to the structure of the colony, where some birds nest in areas where it is more difficult to see them enter and leave their burrows. Such a model with recapture heterogeneity was used for least auklets (*Aethia pusilla*) that also breed in burrows like little auks⁴⁶. The model selection was conducted with E-SURGE⁹⁹. The general starting model was ($\varphi(t), p(\text{het}.t)$), where “het” denotes the heterogeneous effect on capture with two levels (seen with a high or low probability), $t$ denotes the time effect. Models were selected based on Akaike¹⁰⁰ Information Criterion (AIC) corrected for sample sizes and overdispersion (QAICc). During first step, we selected the best model with only time and state as explanatory variables. In step two, we included environmental variables (one or two at a time⁴⁵, the absence of correlation was verified when two environmental variables were included simultaneously) to the model with the best structure in the first step (Table 4).

**Environmental data.** For the summer period, environmental data were dealt with within a 160 × 200 km plot surrounding the colony, which also included little auk at-sea habitats as determined through GPS tracking²⁶ (Supplementary Fig. S1b). Monthly SST came from the Multi-scale Ultra-high resolution (MUR) SST analysis from the NASA (v4.1, global 0.01° resolution, monthly) and were acquired from http://coastwatch.pfeg.noaa.gov/erddap/index.html. Monthly wind data came from the Metop/ASCAT data set (0.25° resolution, monthly, starting in 2007) from CERSAT and were acquired from http://cersat.ifremer.fr/. Daily sea-ice concentration (SIC, percentage of sea surface covered by ice in a given area) came from the Eumetsat OSI SAF and were acquired from http://osisaf.met.no/, using the Global Sea Ice Concentration reprocessing dataset (0.25° resolution, daily). For wind and SST data, we used monthly values for July and we calculated the mean annual value for the foraging area defined above. For SIC, we calculated a mean annual value from the daily SIC concentration in the area between 15th July and 15th August.

Overwintering locations of birds from Ukaleqarteq were known from birds equipped with geolocators⁹⁰, and we defined the core wintering area of birds as the 50% kernel area of positions between 1st November to 28th February obtained for 94 little auks equipped between 2009 and 2015¹⁰¹. Yearly winter environmental conditions (wind speed, SST) were calculated as a mean value within the core wintering area from November to February from monthly values of the datasets mentioned above. In addition, we calculated the proportion of days with high winds (mean daily wind speed > 40 km/h) during the same period, using daily wind speeds from the Metop/ASCAT data set (0.25° resolution). Data for the North Atlantic Oscillation (NAO) came from the UCAR and were acquired from https://climatedataguide.ucar.edu/climate-data. Herein we used the winter NAO index²³. Winter environmental parameters were used for the survival analyses only.

**Statistical analyses.** All analyses were performed with the R software (v. 3.4.2; R core team 2017). We adopted a hypothesis-based approach to study the link between environmental variables and biological parameters, i.e. we tested specific linear models with one or two explanatory variables at a time that are meaningful in a biological context, instead of testing all possible combinations of factors. This ensured to reduce type 1 errors, and to avoid overfitting, as well as issues regarding autocorrelation among environmental variables⁴⁵. In particular, summer SIC, summer SST and summer wind were highly related (Fig. 1). Among these environmental variables, SIC was selected as the main environmental parameter to test, due to its strong and direct influence on the foraging behaviour of little auks at our study site. Mean yearly Hg concentrations in head or body feathers were considered as environmental variables reflecting Hg found in the environment in winter and in the previous summer, respectively³⁷. Hg was either tested independently when a direct influence is expected (chick growth rate and hatching date), or tested concomitantly with SIC when it is expected to be an additional stress factor (adult body condition). We also investigated temporal variations of biological parameters. "Day of year" was included in the models with adult body condition as a response variable as body mass is slightly decreasing along the breeding season.

For adult diet, foraging behaviour, adult body condition and chick growth rate, we performed linear regressions to model the relationship between biological variables and environmental variables, when the assumptions were met. We did not use mixed-effects models because each bird was only sampled one time. Results of the tests were considered significant when p-value was <0.05. For changes in prey proportion in chick diet in relation to SIC, we first used Generalized Additive Models (GAMs) as no linear curve was expected. We performed a logit transformation of the proportions ($p$: log((p + a)/(1 – (p + a))), and where $a$ is a constant ($a = 0.1$) in order to get a logit for all proportions including null values. Each GAM was then compared with a linear model and the model with the lower AIC was retained (all differences in AIC were greater than 2).

**Data Availability**

All data are available on request from the CEFE CNRS database accessible here: http://www.cefe.cnrs.fr/fr/resources/base-de-donnees/1114-puechdb-station-experimentale-de-puechabon-tour-a-flux-sp-23356.

**References**

1. IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. [Stocker, T. F., D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P. M. Midgley (eds)] Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 1535 pp. (2013).

2. AMAP. Snow, water, ice and permafrost. Summary for policy-makers. (Arctic Monitoring and Assessment Programme (AMAP) Oslo, 2017).
3. Gilg, O. et al. Climate change and the ecology and evolution of Arctic vertebrates. *Ann. N. Y. Acad. Sci.* **1249**, 166–190 (2012).

4. Kutz, S. J., Hoberg, E. P., Polley, L. & Jenkins, E. J. Global warming is changing the dynamics of Arctic host–parasite systems. *Proc. R. Soc. Lond. B Biol. Sci.* **272**, 2571–2576 (2005).

5. Amélineau, F. et al. Microplastic pollution in the Greenland Sea: Background levels and selective contamination of planktivorous diving seabirds. *Environ. Pollut.* **219**, 1131–1139 (2016).

6. Vorkamp, K. et al. Novel brominated flame retardants and dechlorane plus in Greenland air and biota. *Environ. Pollut.* **196**, 284–291 (2015).

7. Meltofte, H. et al. Arctic Biodiversity Assessment. Synthesis. (Conservation of Arctic Flora and Fauna (CAFF), 2013).

8. Descamps, S. et al. Climate change impacts on wildlife in a High Arctic archipelago–Svalbard, Norway. *Glob. Change Biol.* **23**, 490–502 (2017).

9. Eamer, J. et al. Life linked to ice. A guide to sea-ice associated biodiversity in this time of rapid change. Conservation of Arctic Flora and Fauna (CAFF). *Akureyri, Iceland*. (Conservation of Arctic Flora and Fauna (CAFF), 2013).

10. Høye, T. T., Post, E., Meltofte, H., Schmidt, N. M. & Forchhammer, M. C. Rapid advancement of spring in the High Arctic. *Curr. Biol.* **17**, R449–R451 (2007).

11. Post, E. et al. Ecological consequences of sea-ice decline. *Science* **341**, 519–524 (2013).

12. Wassmann, P., Duarte, C. M., Agustí, S. & Sejr, M. K. Footprints of climate change in the Arctic marine ecosystem. *Glob. Change Biol.* **17**, 1235–1249 (2011).

13. Bost, C. A. et al. Large-scale climatic anomalies affect marine predator foraging behaviour and demography. *Nat. Commun.* **6**, 8220 (2015).

14. Croxall, J. P., Trathan, P. N. & Murphy, E. J. Environmental change and Antarctic seabird populations. *Science* **297**, 1510–1514 (2002).

15. Gaston, A. J., Gilchrist, H. G. & Hipfner, J. M. Climate change, ice conditions and reproduction in an Arctic nesting marine bird: Brunnich's guillemot (*Uria lomvia L.). *J. Anim. Ecol.* **74**, 832–841 (2005).

16. Lescroël, A., Ballard, G., Grémillet, D., Authier, M. & Ainley, D. G. Antarctic climate change: extreme events disrupt plastic phenotypic response in Adélie penguins. *PloS One* **9**, e85291 (2014).

17. Vihtakari, M. et al. Black-legged kittiwakes as messengers of Atlantification in the Arctic. *Sci. Rep.* **8**, 1178 (2018).

18. Weimerskirch, H., Louzao, M., de Grissac, S. & Delord, K. Changes in wind pattern alter albatross distribution and life-history traits. *Science* **335**, 211–214 (2012).

19. Divoky, G. J., Lukacs, P. M. & Druckenmiller, M. L. Effects of recent decreases in arctic sea ice on an ice-associated marine bird. *Prog. Oceanogr.* **136**, 151–161 (2015).

20. Egevang, C., Boertmann, D., Mosbech, A. & Tamstorf, M. P. Estimating colony area and population size of little auks *Alle alle* at Northumberland Island using aerial images. *Polar Biol.* **26**, 8–13 (2003).

21. Karnovsky, N. J. & Hunt, G. L. Estimation of carbon flux to dovekies (*Alle alle*) in the North Water. Deep-Sea Res. Part I-Top. Stud. Oceanogr.* **49**, 5117–5130 (2002).

22. Kidawa, D. et al. Parental efforts of an Arctic seabird, the little auk *Alle alle*, under variable foraging conditions. *Mar. Biol. Res.* **11**, 349–360 (2015).

23. Hovinen, J. E. H. et al. Climate warming decreases the survival of the little auk (*Alle alle*), a high Arctic avian predator. *Ecol. Evol.* **4**, 3127–3138 (2014).

24. Jakubas, D., Wojczulanis-Jakubas, K., Iliiszko, L. M., Strøm, H. & Stempniewicz, L. Habitat foraging niche of a High Arctic zooplanktivorous seabird in a changing environment. *Sci. Rep.* **7**, 16203 (2017).

25. Reygondeau, G. & Beaugrand, G. Future climate-driven shifts in distribution of *Calanus finmarchicus*. *Glob. Change Biol.* **17**, 756–766 (2011).

26. Amélineau, F., Grémillet, D., Bonnet, D., Bot, T. L. & Fort, J. Where to forage in the absence of sea ice? Bathymetry as a key factor for an Arctic seabird. *PLOS ONE* **11**, e0157764 (2016).

27. Karnovsky, N. et al. Foraging distributions of little auks *Alle alle* across the Greenland Sea: implications of present and future Arctic climate change. *Mar. Ecol. Prog. Ser.* **415**, 283–293 (2010).

28. Harding, A. M. A. et al. Estimating prey capture rates of a planktivorous seabird, the little auk (*Alle alle*), using diet, diving behaviour, and energy consumption. *Polar Biol.* **32**, 785–796 (2009).

29. Grémillet, D. et al. Little auks buffer the impact of current Arctic climate change. *Mar Ecol Prog Ser* **454**, 197–206 (2012).

30. Karnovsky, N. J. et al. Inter-colony comparison of diving behavior of an Arctic top predator: implications for warming in the Greenland Sea. *Mar Ecol Prog Ser* **440**, 229–240 (2011).

31. Mosbech, A. et al. On the crucial importance of a small bird: The ecosystem services of the little auk (*Alle alle*) population in Northwest Greenland in a long-term perspective. *Ambio* **47**, 226–243 (2018).

32. Jakubas, D. et al. Foraging closer to the colony leads to faster growth in little auks. *Mar. Ecol. Prog. Ser.* **489**, 263–278 (2013).

33. Fort, J., Porter, W. P. & Grémillet, D. Thermodynamic modelling predicts energetic bottleneck for seabirds wintering in the northwest Atlantic. *J. Exp. Biol.* **212**, 2483–2490 (2009).

34. Sandvik, H., Erikstad, K. E., Barrett, R. T. & Yoccoz, N. G. The effect of climate on adult survival in five species of North Atlantic seabirds. *J. Anim. Ecol.* **74**, 817–831 (2005).

35. Sandvik, H., Erikstad, K. E. & S\a ether, B.-E. Climate affects seabird population dynamics both via reproduction and adult survival. *Mar. Ecol. Prog. Ser.* **454**, 273–284 (2012).

36. Frederiksen, M., Harris, M. P., Daunt, F., Rothery, P. & Wanless, S. Scale-dependent climate signals drive breeding phenology of three seabird species. *Glob. Change Biol.* **10**, 1214–1221 (2004).

37. Fort, J., Grémillet, D., Traisnel, G., Amélineau, F. & Bustamante, P. Does temporal variation of mercury levels in Arctic seabirds reflect changes in global environmental contamination, or a modification of Arctic marine food web functioning? *Environ. Pollut.* **211**, 382–388 (2016).

38. Wolfe, M. F., Schwarzbach, S. & Sulaiman, R. A. Effects of mercury on wildlife: a comprehensive review. *Environ. Toxicol. Chem.* **17**, 146–160 (1998).

39. Tartu, S. et al. To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird. *Biol. Lett.* **9**, 20130317 (2013).

40. Tartu, S. et al. Mercury exposure, stress and prolactin secretion in an Arctic seabird: an experimental study. *Funct. Ecol.* **30**, 596–604 (2016).

41. van Straalen, N. M. Ecotoxicology becomes stress ecology. (ACS Publications, 2003).

42. Jakubas, D. et al. Intra-seasonal variation in zooplankton availability, chick diet and breeding performance of a high Arctic planktivorous seabird. *Polar Biol.* **1**–15, https://doi.org/10.1007/s00300-015-1880-z (2016).

43. Harding, A. M. et al. Adverse foraging conditions may impact body mass and survival of a high Arctic seabird. *Oecologia* **167**, 49–59 (2011).

44. Shipley, B. Cause and correlation in biology: a user's guide to path analysis, structural equations and causal inference with R. (Cambridge University Press, 2016).

45. Grosbois, V. et al. Assessing the impact of climate variation on survival in vertebrate populations. *Biol. Rev.* **83**, 357–399 (2008).

46. Jones, I. L., Hunter, F. M. & Robertson, G. J. Annual adult survival of Least Auklets (Aves, Alcidae) varies with large-scale climatic conditions of the North Pacific Ocean. *Oecologia* **133**, 38–44 (2002).
47. Moe, B. *et al.* Climate change and phenological responses of two seabird species breeding in the high-Arctic. *Mar. Ecol. Prog. Ser.* **393**, 235–246 (2009).

48. Goutte, A. *et al.* Survival rate and breeding outputs in a high Arctic seabird exposed to legacy persistent organic pollutants and mercury. *Environ. Pollut.* **200**, 1–9 (2015).

49. Tartu, S. *et al.* Increased adrenal responsiveness and delayed hatching date in relation to polychlorinated biphenyl exposure in Arctic-breeding black-legged kittiwakes (*Rissa tridactyla*). *Gen. Comp. Endocrinol.* **219**, 165–172 (2015).

50. Votier, S. C. *et al.* Oil pollution and climate have wide-scale impacts on seabird demographics. *Ecol. Lett.* **8**, 1157–1164 (2005).

51. Robertson, G. J., Wiese, F. K., Ryan, P. C. & Wilhelm, S. I. Updated numbers of murrets and dovekies oiled in Newfoundland waters by chronic ship-source oil pollution. In *Proceedings of the 37th AMOP Technical Seminar on Environmental Contamination and Response* 265–275 (Environment Canada Ottawa, ON, 2014).

52. Woo, K. J., Elliott, K. H., Davidson, M., Gaston, A. J. & Davoren, G. K. Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. *J. Anim. Ecol.* **77**, 1082–1091 (2008).

53. Fort, J., Porter, W. P. & Grémillet, D. Energetic modelling: A comparison of the different approaches used in seabirds. *Comp. Biochem. Physiol. A. Mol. Integr. Physiol.* **158**, 358–365 (2011).

54. Watanabe, Y. Y. & Takahashi, A. Linking animal-borne video to accelerometers reveals prey capture variability. *Proc. Natl. Acad. Sci.* **110**, 2199–2204 (2013).

55. Beaugrand, G., Luczak, C. & Edwards, M. Rapid biogeographical plankton shifts in the North Atlantic Ocean. *Glob. Change Biol.* **15**, 1790–1803 (2009).

56. Kjellerup, S. *et al.* Effects of a future warmer ocean on the coexisting copepods *Calanus finmarchicus* and *C. glacialis* in Disko Bay, western Greenland. *Mar. Ecol. Prog. Ser.* **447**, 87–108 (2012).

57. Carstensen, J., Weydmann, A., Olszewska, A. & Kwaśniewski, S. Effects of environmental conditions on the biomass of *Calanus spp.* in the Nordic Seas. *J. Plankton Res.* **34**, 951–966 (2012).

58. Lønne, O. J. & Gabrielsen, G. W. Summer diet of seabirds feeding in sea-ice-covered waters near Svalbard. *Polar Biol.* **12**, 685–692 (1992).

59. Mehlum, F. & Gabrielsen, G. W. The diet of high-arctic seabirds in coastal and ice-covered, pelagic areas near the Svalbard archipelago. *Polar Res.* **12**, 1–20 (1993).

60. Harding, A. M. *et al.* Can stable isotope (δ13C and δ15N) measurements of little auk (*Alle alle*) adults and chicks be used to track changes in high-Arctic marine foodwebs? *Polar Biol.* **31**, 725–733 (2008).

61. Fort, J. *et al.* Geographic and seasonal variability in the isotopic niche of little auks. *Mar. Ecol. Prog. Ser.* **414**, 293–302 (2010).

62. Pedersen, C. E. & Falk, K. Chick diet of dovekies *Alle alle* in Northwest Greenland. *Polar Biol.* **24**, 53–58 (2001).

63. Rosing-Asvid, A., Hedeholm, R., Arendt, K. E., Fort, J. & Robertson, G. J. Winter diet of the little auk (*Alle alle*) in the Northwest Atlantic. *Polar Biol.* **36**, 1601–1608 (2013).

64. Kwasniewski, S. *et al.* The impact of different hydrographic conditions and zooplankton communities on provisioning Little Auks along the West coast of Spitsbergen. *Prog. Oceanogr.* **87**, 72–82 (2010).

65. Jakubas, D., Iliszko, L., Wojczulanis-Jakubas, K. & Stempniewicz, L. Foraging by little auks in the distant marginal sea ice zone during the chick-rearing period. *Polar Biol.* **35**, 73–81 (2012).

66. Jakubas, D. *et al.* Foraging behavior of a high-Arctic zooplanktivorous alcid, the little auk, at the southern edge of its breeding range. *J. Exp. Mar. Biol. Ecol.* **475**, 89–99 (2016).

67. Bradstreet, M. S. W. Pelagic feeding ecology of dovekies, *Alle alle*, in Lancaster Sound and Western Baffin Bay. *Arctic* **35**, 126–140 (1982).

68. Fort, 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.* **19**, 1322–1332 (2013).

69. Ji, R., Jin, M. & Varpe, Ø. Sea ice phenology and timing of primary production pulses in the Arctic Ocean. *Glob. Change Biol.* **19**, 734–741 (2013).

70. Søreide, J. E., Leu, E., Berge, J., Graeve, M. & Falk-Petersen, S. Timing of blooms, algal food quality and *Calanus glacialis* reproduction and growth in a changing Arctic. *Glob. Change Biol.* **16**, 3154–3163 (2010).

71. Ramírez, F. *et al.* Sea ice phenology and primary productivity pulses shape breeding success in Arctic seabirds. *Sci. Rep.* **7** (2017).

72. Hovinen, J. E. H. *et al.* Fledging success of little auks in the high Arctic: do provisioning rates and the quality of foraging grounds matter? *Polar Biol.* **37**, 665–674 (2014).

73. Ropert-Coudert, Y. *et al.* A complete breeding failure in an Adélie penguin colony correlates with unusual and extreme environmental events. *Ecography* **38**, 111–113 (2015).

74. Jenouvrier, S., Péron, C. & Weimerskirch, H. Extreme climate events and individual heterogeneity shape life-history traits and population dynamics. *Ecol. Monogr.* **85**, 605–624 (2015).

75. Gilg, O. *et al.* Living on the edge of a shrinking habitat: the ivory gull, *Pagophila eburnea*, an endangered sea-ice specialist. *Biol. Lett.* **12**, 20160277 (2016).

76. Gilg, O., Boertmann, D., Merkel, F., Aebischer, A. & Sabard, B. Status of the endangered ivory gull, *Pagophila eburnea*, in Greenland. *Polar Biol.* **32**, 1275–1286 (2009).

77. Dietz, R., Outridge, P. M. & Hobson, K. A. Anthropogenic contributions to mercury levels in present-day Arctic animals—a review. *Sci. Total Environ.* **407**, 6120–6131 (2009).

78. Dietz, R. *et al.* What are the toxicological effects of mercury in Arctic biota? *Sci. Total Environ.* **443**, 775–790 (2013).

79. AMAP. AMAP Assessment 2016: Chemicals of Emerging Arctic Concern. xvi + 353pp (Arctic Monitoring and Assessment Programme (AMAP), 2017).

80. Blévin, P. *et al.* Contaminants and energy expenditure in an Arctic seabird: Organochlorine pesticides and perfluoroalkyl substances are associated with metabolic rate in a contrasted manner. *Environ. Res.* **157**, 118–126 (2017).

81. Tartu, S. *et al.* Corticosterone, prolactin and egg neglect behavior in relation to mercury and legacy POPs in a long-lived Antarctic bird. *Sci. Total Environ.* **505**, 180–188 (2015).

82. Thompson, D. R., Hamer, K. C. & Furness, R. W. Mercury accumulation in Great Skuas *Catharacta skua* of known age and sex, and its effects upon breeding and survival. *J. Appl. Ecol.* **28**, 672–684 (1991).

83. Goutte, A. *et al.* Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross. *Proc. R. Soc. Lond. B Biol. Sci.* **281**, 20133313 (2014).

84. Goutte, A. *et al.* Demographic responses to mercury exposure in two closely related Antarctic top predators. *Ecology* **95**, 1075–1086 (2014).

85. Stern, G. A. *et al.* How does climate change influence arctic mercury? *Sci. Total Environ.* **414**, 22–42 (2012).

86. Rydberg, J., Klaminder, J., Rosén, P. & Bindler, R. Climate driven release of carbon and mercury from permafrost mires increases mercury loading to sub-arctic lakes. *Sci. Total Environ.* **408**, 4778–4783 (2010).

87. Cossa, D. Marine biogeochemistry: methylmercury manufacture. *Nat. Geosci.* **6**, 810 (2013).

88. Rigét, F. *et al.* Twenty years of monitoring of persistent organic pollutants in Greenland biota. A review. *Environ. Pollut.* **217**, 114–123 (2016).

89. Buchanan, K. *et al.* Guidelines for the treatment of animals in behavioural research and teaching. *Anim. Behav.* **83**, 301–309 (2012).

90. Fort, J., Beaugrand, G., Grémillet, D. & Phillips, R. A. Biologging, remotely-sensed oceanography and the Continuous Plankton Recorder reveal the environmental determinants of a seabird wintering hotspot. *PLoS ONE* **7**, e41194 (2012).
91. Kelly, J. F. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. *Can. J. Zool.* **78**, 1-27 (2000).

92. Welcker, J. *et al*. Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk *Alle alle*. *J. Avian Biol.* **40**, 388–399 (2009).

93. Wojczulanis-Jakubas, K. & Jakubas, D. When and why does my mother leave me? The question of brood desertion in the dovekie (*Alle alle*). *The Auk* **129**, 632–637 (2012).

94. Bustamante, P., Lahaye, V., Durnez, C., Churlaud, C. & Caurant, F. Total and organic Hg concentrations in cephalopods from the North Eastern Atlantic waters: influence of geographical origin and feeding ecology. *Sci. Total Environ.* **368**, 585–596 (2006).

95. Renedo, M. *et al*. Assessment of mercury speciation in feathers using species-specific isotope dilution analysis. *Talanta* **174**, 100–110 (2017).

96. Lebreton, J.-D., Burnham, K. P., Clobert, J. & Anderson, D. R. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. *Ecol. Monogr.* **62**, 67–118 (1992).

97. Choquet, R., Lebreton, J.-D., Gimenez, O., Reboulet, A.-M. & Pradel, R. U-CARE: Utilities for performing goodness of fit tests and manipulating CApture-REcapture data. *Ecography* **32**, 1071–1074 (2009).

98. Pledger, S., Pollock, K. H. & Norris, J. L. Open capture-recapture models with heterogeneity: I. Cormack-Jolly-Seber model. *Biometrics* **59**, 786–794 (2003).

99. Choquet, R., Rouan, L. & Pradel, R. Program E-SURGE: a software application for fitting multievent models. in Modeling demographic processes in marked populations 845–865 (Springer, 2009).

100. Akaike, H. Factor analysis and AIC. *Psychometrika* **52**, 317–332 (1987).

101. Amélineau, F. *et al*. Energyscapes and prey fields shape a North Atlantic seabird wintering hotspot under climate change. *R. Soc. Open Sci.* **5**, 171883 (2018).

## Acknowledgements

This study and long-term monitoring program on little auks have been funded by the French Polar Institute (grant 388 to DG and JF), the National Science Foundation (NSF Grant 0612504 to Nina Karnovsky & AMAH), the National Geographic Society (GEFNE 41–12 grant to JF), the Belmont Forum (TAMANI project to DG), the European Commission (Marie Curie IEF and Marie Curie CIG to JF, Projects 273061 and 631203), the French Arctic Initiative – CNRS (PARCS project) and the Mission pour l’Interdisciplinarité – CNRS (Changements en Sibérie project). We thank all the field assistants for their great work, Delphine Bonnet and Rumsais Blatrix for their help/technical assistance for the zooplankton identification, Francis Crenner who kindly provided 4 LULs and Jean-Yves Barnagaud for inspiring discussions on the methods. We also thank the platforms ‘Spectrométrie Isotopique’ and ‘Analyses Elémentaires’ at LIENSs, as well as G. Guillou and M. Brault-Favrou for their help with stable isotope and Hg analyses.

## Author Contributions

Conceived and designed the experiments: D.G., A.M.A.H., J.F. Performed the experiments: D.G., A.M.A.H., J.F., F.A. Analyzed the data: F.A., W.W., R.C. Wrote the paper: F.A., J.F., D.G. All authors reviewed the manuscript.

## Additional Information

Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-018-38042-z.

**Competing Interests:** The authors declare no competing interests.

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