Ann. N.Y. Acad. Sci. ISSN 0077-8923

ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue: The Year in Ecology and Conservation Biology

Climate change and the ecology and evolution of Arctic vertebrates

Olivier Gilg,1,2,3 Kit M. Kovacs,4 Jon Aars,4 Jer´ omeˆ Fort,5 Gilles Gauthier,6 David Gremillet,´ 7 Rolf A. Ims,8 Hans Meltofte,5 Jer´ omeˆ Moreau,1 Eric Post,9 Niels Martin Schmidt,5 Glenn Yannic,3,6 and Lo¨ıc Bollache1 1Universite´ de Bourgogne, Laboratoire Biogeosciences,´ UMR CNRS 5561, Equipe Ecologie Evolutive, Dijon, France. 2Division of Population Biology, Department of Biological and Environmental Sciences, University of Helsinki, Finland. 3Groupe de Recherche en Ecologie Arctique (GREA), Francheville, France. 4Norwegian Polar Institute, FRAM Centre, Tromsø, Norway. 5Department of Bioscience, Aarhus University, Roskilde, Denmark. 6Departement´ de Biology and Centre d’Etudes´ Nordiques, Universite´ Laval, Quebec,´ Quebec,´ G1V 0A6, Canada. 7FRAM Centre d’Ecologie Fonctionnelle et Evolutive, UMR CNRS 5175, Montpellier, France. 8Department of Arctic and Marine Biology, University of Tromsø, Tromsø, Norway. 9Department of Biology, Penn State University, University Park, Pennsylvania

Address for correspondence: Olivier Gilg, Laboratoire Biogeosciences,´ UMR CNRS 5561, Equipe Ecologie Evolutive, 6 Boulevard Gabriel, 21000 Dijon, France. [email protected]

Climate change is taking place more rapidly and severely in the Arctic than anywhere on the globe, exposing Arctic vertebrates to a host of impacts. Changes in the cryosphere dominate the physical changes that already affect these animals, but increasing air temperatures, changes in precipitation, and ocean acidification will also affect Arctic ecosystems in the future. Adaptation via natural selection is problematic in such a rapidly changing environment. Adjustment via phenotypic plasticity is therefore likely to dominate Arctic vertebrate responses in the short term, and many such adjustments have already been documented. Changes in phenology and range will occur for most species but will only partly mitigate climate change impacts, which are particularly difficult to forecast due to the many interactions within and between trophic levels. Even though Arctic species richness is increasing via immigration from the South, many Arctic vertebrates are expected to become increasingly threatened during this century.

Keywords: impacts; phenological changes; plasticity; range shifts; adaptations; threat; trophic interactions; mis- matches; sea ice; tundra; parasites; geese; shorebirds; rodents; lemmings; large herbivores; seabirds; marine mammals; polar bear

ing: in Africa, water stress is expected to become the Introduction main constraint in the future, with arid and semi- Several studies have already reviewed the ongoing arid land projected to increase; in eastern South and forecasted impacts of climate change on the America, drought and increasing temperatures will ecology and evolution of vertebrates on Earth.1,2 induce a gradual replacement of tropical forests by Overall, changes in phenologies, in distributional savanna; in boreal regions, increasing rainfall and range, in evolutionary adaptations—on the long temperature will in many places allow the forest term—and, in the structure and the dynamics of to expand in altitude and latitude, replacing the communities, are forecast to be the main biological Arctic and Alpine tundras; and in many coastal consequences of climate change. However, due to lowlands, the elevation of sea level will replace ter- regional differences in climate change and in biotic restrial ecosystems by marine ones. In the Arctic, characteristics, climate-induced impacts on species physical changes will be dominated by changes in the will differ in their nature and magnitude between re- cryosphere (glaciers, permafrost, sea ice, and snow gionsandecosystems.3 Examples include the follow- layers), primarily due to increasing temperatures.

doi: 10.1111/j.1749-6632.2011.06412.x 166 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates

To understand how Arctic vertebrates will respond type in the Arctic. If these trends continue as pre- to these changes, we have to consider their particu- dicted by models, the Arctic Ocean should become lar history, the extreme physical environment they ice free in summer well before the end of this cen- currently inhabit, and the relatively simple structure tury,7 and this would be a first for Arctic marine and composition of the communities to which they systems during the last 5+ million years.8 belong. Arctic vertebrates possess many adaptations that Of course, changes in climate are not entirely new, have enabled their persistence in Arctic environ- and Arctic vertebrates have already lived through ments. These traits include behavioral (e.g., day tor- several periods of “historical climate changes”— por, seasonal migration), physiological (e.g., sea- although the speed and the extent of the current sonal metabolic adjustments, fasting ability), and changes are probably unprecedented. However, un- morphological (e.g., white coats, short extremities, less we enter the realm of paleoecology, we know extensive blubber layers, thick fur, lack of dorsal little about ecological responses of vertebrates to fins among ice whales) mechanisms. But despite past changes in climate. Vibe’s seminal study4 is their extreme and varied adaptations to coping with one notable exception. He clearly showed, nearly the harsh and highly variable Arctic climate, these 50 years ago, the importance of climate, and more species are considered to be particularly vulnera- precisely the availability of specific ice types, in de- ble to ongoing climate changes. Their peculiar life- termining the distribution of marine mammals on history strategies have served them well in a low- the west coast of Greenland. More recent analyses competition situation but leave them vulnerable to of decadal patterns of sea ice and their influences on competitive stress from temperate species that are marine mammals can also be used to predict that already invading their ranges. Arctic endemics have changes in recent years are likely to impact resident little potential for northward retraction to avoid marine mammal populations at both regional and such overlap. In addition, they may have limited hemispheric scales.5 capacity to deal with exposure to disease because The Arctic biome is already changing, and this of their limited exposure in the past. Furthermore, change is rapid and severe compared to other re- the heavy lipid-based dietary dependence of some gions of the globe. It is expected that the changes that Arctic species leaves them disproportionately vul- will take place in the Arctic in the coming decades nerable to the effects of lipophilic contaminants. will surpass what many Arctic vertebrates have ex- Arctic vertebrates can adjust to cope with climate- perienced in the past, despite the extreme variabil- related changes (i.e., through their phenotypic plas- ity that is normal in the climate of the Arctic. In- ticity) or adapt (via the differential selection of some deed, while the global mean surface temperature has genotypes) in many different ways. The aim of our warmed by 0.6–0.8◦ Cduringthe20thcentury,ithas paper is to review these different responses and, increased ca. twice as much in the Arctic during the whenever possible, to present examples of the im- same period.3 Theconsequencesofthiswarmingin- pacts of climate change at the community level, clude decreases in snow, ice, and frozen ground lay- explicitly taking into account interspecific interac- ers, while precipitation has increased overall in the tions. Given the wide range of possible interactions, Northern hemisphere.3 The strong environmental predictionsmadeatthislevelusuallyremainspecu- constraints that prevail in the Arctic—including the lative. On the other hand, predictions that overlook harsh climate, strong seasonality, low productivity, interaction processes would lack realism. To avoid and numerous ecological barriers—are likely to ex- these pitfalls, the examples supporting our text are acerbate the impacts that are expected due to direct primarily chosen from the few biological models influences of climate change.6 that have already been studied comprehensively in Documented declines in Arctic sea ice are symp- the Arctic in recent years—that is, rodents and their tomatic of these ongoing changes. Its overall extent, predators, geese and shorebirds, large herbivores, thickness, seasonal duration, and the proportion of seabirds, and marine mammals and their prey. multiyear ice have all declined. Multiyear sea ice Our paper is structured in nine sections and has disappeared three times faster during the past follows a process orientation, rather than the tra- decade than during the previous three decades, and ditional species by species approach. In the first seasonal ice is thus becoming the dominant sea ice section, we present a general outline of how

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 167 Climate change impacts on Arctic vertebrates Gilg et al. vertebrates will respond to changes in the The winter is a key period in the annual cycle cryosphere, because most species living in the Arctic of Arctic small mammals as some—for example, biome are exceedingly dependent on snow and ice the Arctic lemmings—live under the snow for up regimes for their reproduction and survival. Second, to nine months of the year at the most northerly we give a brief overview of some important eco- sites; they even reproduce under the snow. The in- physiological constraints that directly link climate crease phase of lemming population cycles is almost and species and can hence result in very rapid re- always driven by reproduction under the snow,11 sponses. In the third and fourth sections, we provide and thus events occurring under the snow have a an extensive review of the main responses of Arctic strong impact on their population dynamics. Lem- vertebratestoclimatechange:changesinphenology, mings clearly choose particular sites under the snow that is, the timing of seasonal activities (e.g., migra- for their winter activities. The distribution of their tion, calving, egg-laying), and range shifts, that is, winter nests show a strong association with deeper moving to track suitable habitat.1,2,9,10 The fifth sec- snow, and the greatest probability of occurrence is tion aims to present the need for considering inter- at snow depths from 60 to 120 cm.12,13 Adeep,dry actions, especially in relatively simple communities snow cover reduces thermal stress on small mam- such as those found in the Arctic, in order to under- mals that overwinter in subnivean spaces, most no- stand the complexity and diversity of the observed tably by dampening the daily temperature fluctu- responses. A particular case study involving para- ations that they experience.12,14 Many parts of the sites is presented in section six as an example. The Arctic receive less than 40 cm of snowfall during seventh section provides an evolutionary perspec- a winter, but this is often redistributed heavily by tive for the phenotypic and genotypic responses that wind, creating a mosaic of habitat patches differ- are likely to arise in Arctic vertebrates, highlighting ing substantially in snow depth, with snow being how molecular ecology can help us to infer the fate trapped by topography and vegetation. A recent of these species. In the eighth section, we list some manipulation experiment that altered snow cover principle knowledge gaps that currently prevent us showed that increasing the snow depth in marginal from having a better understanding or being able to winter habitat increased habitat use by small mam- forecast climate change responses well. Finally, we mals in these areas, as expected, but the impact on summarize the general trends that emerged from demography (reproductive rate or mortality due to our review in a concluding section. predation) was less clear.14 Nonetheless, it is likely that change in snow depth or snow quality (e.g., in- creased amount of wet snow, icing, or collapses in Coping with a changing cryosphere the subnivean spaces, which increase the energetic Ongoing changes in snow and sea ice conditions will costs incurred in getting access to food plants or have strong and wide impacts on Arctic vertebrates’ in severe instances totally obstruct access) caused habitats and food resources. These widespread and by climate warming will have a strong impact on long-lasting layers of frozen water are far from ho- small mammal population dynamics. Such find- mogenous. Dozens of different types of snow and ingshavebeenreportedrecentlyfromsomeparts ice can be distinguished according to their thickness, of Fennoscandia and Greenland (see section “Cas- age, density, temperature, chemical composition, cading changes”).15,16 physical structure, location (e.g., latitude, which ac- Among large mammals, variation and trends in counts for temporal differences in solar radiation), snow cover, especially during late winter, will likely history, etc. Depending on the quality and quantity also affect foraging ecology and population dynam- of snow or ice found in their habitats, Arctic verte- ics. Evidence from long-term monitoring at Zacken- brates will react differently in order to optimize their berg in northeast Greenland indicates, for example, fitness. Forecasted changes in the Arctic cryosphere that biomass production and spatial synchrony in will hence impact Arctic vertebrates in many differ- the growth of the main willow forage species for ent ways that will be presented in more details in the muskoxen Ovibos moschatus there, Salix arctica,are following sections, but let us just start here with a both negatively related to snow cover.17 Increasing few examples chosen from among some of the most snowfall in the High Arctic with continued warm- important vertebrate guilds found in the Arctic. ing could therefore translate into increased spatial

168 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates heterogeneity of willow growth, which might result than 200,000 years ago22—polar bears have become in increases in local density-dependent competition highly adapted to life on the sea ice. Their depen- for forage among muskoxen.17 In the High Arctic dency on sea ice is mainly via their extreme spe- Archipelago of Svalbard, population dynamics of cialization in feeding on ice-associated seals, partic- Svalbard reindeer Rangifer tarandus platyrhynchus ularly ringed seals Pusa hispida and bearded seals display a generally positive association with an in- Erignathus barbatus.23 In addition, sea ice is im- dex of winter ablation, or the energy available for portant because it is a solid substrate on which snowmelt, suggesting that continued warming may bears can move and rest. Coastal sea ice habitats are promote an increase in that population through re- particularly important to females with dependent duced winter starvation mortality.18 young.24 Some bears use sea ice in all seasons, while Most tundra breeding birds (shorebirds and other bears stay on land for much of the year, but passerines alike) are long-distance migrants, and most feed at least seasonally on ice-associated seals. many of them winter in rich intertidal flats in tem- However, it is noteworthy that ice linkage varies perate and tropical regions. By spending only some geographically for bears among the different popu- weeks in the Arctic, they avoid the harsh Arctic win- lations and also among individuals; different space- ter but still take advantage of the summer boom use strategies can be found even within polar bear of food on the tundra, particularly to raise their subpopulations.25 Theobservedlossofseaicein young.19 Indeed, many tundra birds rely heavily on recent decades has raised concerns about the future invertebrate food during the entire breeding sea- of polar bears in the Arctic.26–28 In areas where sea son. For the adults, invertebrate food is particu- ice is absent in summer, polar bears depend on fat larly important for the development of eggs and for reserves acquired in the peak feeding period to get building up body stores to be used during the in- them through long periods of fasting. Polar bears cubation period, while hatchlings either feed them- are unique among larger mammals in their ability selves (shorebirds) or are fed (passerines) with in- to survive many months without feeding. Repro- vertebrates during their growing period.20,21 Both ducing females may fast for up to eight months adult and juvenile shorebirds have to build up body and still nurse cubs. There is, however, a balance stores rapidly during the postbreeding period, based between fat reserves and survival/breeding capabil- on invertebrate food, for their long autumn migra- ities. In some areas where sea ice breaks up earlier tion, while passerines feed primarily on seeds that in spring and access to ringed seal pups has been re- ripen at this time of the year. The first weeks fol- duced, for example, in western Hudson Bay, survival lowing the shorebirds’ arrival on the tundra (i.e., of cubs, subadults, and even older bears is lower in when eggs are formed) are particularly critical, be- years with early ice breakup, and recent longer ice- cause snow melt and weather conditions in general free summers are concomitant with a reduction in vary a lot from year to year in most parts of the this subpopulation’s size.29 In the southern Beau- Arctic.21 Because global warming is expected to re- fort Sea, survival of adult females was considerably sult in earlier snow melt and more benign summer higher in 2001–2003, when the mean ice-free period weather, tundra birds may well benefit from more was 101 days, compared to 2004–2005, when it was favorable breeding conditions in most years.21 How- 135 days. Breeding rates and cub survival also de- ever, they might also suffer from more variable con- creased during the latter period.30 Another change ditions, because the amount of snow falling in win- in the Alaskan part of the southern Beaufort Sea ter is expected to increase in most Arctic regions, is a profound decline in the proportion of females a change that, in combination with cooler springs, denning in the multiyear sea ice: 62% in 1985–1994 could result in more chaotic—both in regularity and versus 37% in 1998–2004.31 However, in most ar- severity—breeding conditions (also see the follow- eas of the polar bear’s range, denning occurs only ing section). on land. In Svalbard, many female bears denned When moving to ice loss–related threats to Arc- on the isolated island Hopen decades ago. But in tic marine vertebrates, the polar bear Ursus mar- recent years, when sea ice has not extended south itimus is undoubtedly the first species people have to Hopen in the late autumn, almost no denning in mind. During their short evolutionary history— has been documented on this island.26 Reduction they diverged from brown bears Ursus arctos less of sea ice has also been proposed as a causal factor

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 169 Climate change impacts on Arctic vertebrates Gilg et al. behind increased intraspecific predation,32 drown- willaccompanyseaicelossescomparedtogener- ing of bears during storms,33 and extraordinary long alist feeders. In addition, widely distributed species swims that may lead to loss of cubs.34 In areas where will have greater chances of shifting to suitable re- polar bears have high levels of lipophilic pollutants, gions than species with restricted ranges. Ice breed- toxins and their metabolites are released into the ers that require long periods of stable ice late in the blood stream under periods of nutritional stress. spring season are also likely to be impacted more This is a concern given the longer fasting periods rapidly than late winter ice breeders that require being experienced by populations with reduced ice ice for shorter periods of time.42,43,52 Other risks conditions, although the exact effects this may have posed by climate change include the increased risk on survival and reproduction are not known.35 of disease in a warmer climate, the potential for Other marine mammals will also face important increased effects of pollution, increased competi- environmental changes in the Arctic that will al- tion from temperate marine mammal species that ter the communities in which they live,36–38 par- are expanding northward, and stronger impacts of ticularly pagophilic (“ice-loving”) species.5,6,39–45 A shipping and development in the north—in par- summertime ice-free Arctic Ocean will have major ticular from the petroleum industry—in previously implications for ocean circulation and our global inaccessible areas.41 In combination, these various climate system3,46,47 and will also have impacts changes are likely to result in substantial distribu- throughout marine food webs. Implications for the tional shifts and abundance reductions for many organisms that are residents of the unique Arctic endemic Arctic marine mammal species. sea ice habitat have been described as “transforma- Although Arctic seabirds are highly adapted to ex- tive.”48 For its mammalian residents, Arctic sea ice treme environmental conditions, their energy bal- has been a spatially extensive, virtually disease-free ance is nonetheless affected by harsh environments. habitat that is to a large extent sheltered from open- Heat losses in cold air, water, or in stormy condi- water predators (i.e., killer whales Orcinus orca)and tions can be extremely high despite the waterproof human impacts (e.g., oil development, shipping). and well insulated plumage of adults.53 Some species It has been a low-competition environment that such as guillemots and little auks Alle alle can be has provided a spatially predictable, seasonally rich found dead by the thousands in coastal areas fol- food supply, particularly in the marginal ice-edge lowing severe winter storms.54 Because the inten- zone and at predictable polynyas.49,50 It is further- sity and frequency of winter storms are forecast to more sheltered from storm action for the mam- increase with climate warming,6,55 important im- mals that have succeeded in dealing with the pre- pacts are expected on seabird energetics and winter vailing cold temperatures, risk of ice entrapment, survival. The relative sensitivity of seabirds to cli- dramatic seasonality, and other aspects of an ice- mate changes is also obvious during the breeding associated lifestyle.41 Seven seal species and three season for their chicks, whose downy plumage is whale species have evolved within the Arctic sea ice much less waterproof and a poorer insulator than environment, or joined it, over the millions of years that of the adults. Chicks are highly vulnerable to of its existence.51 Loss of sea ice represents a reduc- changes in wind speed and precipitation. Indeed, tion in available habitat for pagophilic mammals, harsher wind conditions as well as more frequent and this is already affecting the distribution, body heavy or freezing rain will most likely impact their condition, survival rates, and reproductive output energetics and result in higher mortality. Even for of some species.41 In the longer term, it is expected the extremely well-adapted High Arctic ivory gull that foraging success, fertility rates, mortality rates, Pagophila eburnea, a single day of rain accompanied and other population parameters will be impacted by strong winds can destroy all clutches and broods for additional populations and species. Northward in some colonies in some years (Gilg and Aebischer, range contractions are possible only within a lim- personal communication 2011). ited scale before deep Arctic Ocean conditions re- Ecophysiological constraints place the productive shelf habitats upon which most Arctic marine mammals depend. Generally speak- The most direct link between climate and the ing, specialist feeders are likely to be more heav- ecology of most species is probably the physio- ily impacted by changes in Arctic food webs that logical interplay between environmental and body

170 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates temperatures. Each organism lives within a given benefit—increase in abundance and distribution— range of temperature (i.e., “thermal window”).56 more from climate change than others.60 To minimize maintenance costs, thermal windows Changes in hormonal responses are also expected are thought to evolve to be as narrow as is possi- in Arctic vertebrates as a result of climate change, ble around normal environmental temperature(s), with potentially very important outcomes on indi- which results in different temperature tolerance vidualfitness.Thestressaxisinparticularisbelieved ranges between species, subspecies, or even popu- to play a central role in the adaptation of birds and lations of a given species living in different regions. mammals to a changing environment. For many When environmental temperatures shift closer to of them, breeding is only possible below a given one edge of the individual’s thermal window—for stress response. An increasingly stressful environ- example, climate warming driving the temperature ment, whether due to direct abiotic changes (e.g., higher—the individual’s physiological performance temperature, snow, or ice cover) or to indirect bi- (e.g., growth, reproduction, foraging, immune com- otic changes (e.g., new competitors, changing pre- petence, competitiveness) will be negatively im- dation pressure), could negatively impact the fitness pacted.56 This is contrary to the layman’s belief that of Arctic vertebrates.61 Expected range shifts will an increase in environmental temperature will im- help some Arctic vertebrates maintain their stress prove the “welfare” of Arctic vertebrates. Climate levels within acceptable ranges, but changes in food change is forecasted to have a stronger negative resources and availability, which also impact the impact on species that have narrow thermal win- stress axis, also need to be taken into account to dows, long generation times, and limited genetic predict their overall responses. Finally, hormonal diversity.56 Conversely and at a larger geographic responses and immune status are also modulated to scale, some vertebrate species currently living at the some extent by pollutants.61,62 The future impact southern border of the Arctic region will benefit of contaminants will likely be correlated to the in- from climate warming and will be able to expand tensity of climate change;63 pollutants make it even northward, because their thermal windows will soon more difficult to untangle causes and consequences match the new environmental temperatures found of climate-induced impacts on the ecophysiology of in the Arctic (see also section “Advanced phenolo- Arctic vertebrates. gies”). Because aquatic habitats have more stable Advanced phenologies and trophic temperatures than terrestrial ones, most aquatic in- match/mismatch vertebratesandfishhavenarrowerthermalwindows than warm-blooded vertebrates and are probably Because ongoing climate changes are relatively rapid more sensitive to changes in environmental tem- while most Arctic vertebrates are long-lived animals peratures (see examples for sockeye, Pacific salmon, with slow population growth rates and long genera- Atlantic cod, and zooplankton).57–59 tion times, selection for the most adapted genotypes Because the energy budget of an individual inte- to new environmental conditions will likely be too grates both biotic and abiotic constraints, a bioen- slow to guarantee the survival of these species in the ergetic approach can be used to assess the impacts short term (see section “Evolutionary responses”). of climate change. For instance, seabirds wintering Instead, phenotypic plasticity is likely to be the prin- in the North Atlantic experience an energetic bottle- ciple response mechanism that will permit Arc- neck in November and December due to low tem- tic vertebrates to respond to the rapid, ongoing peratures and strong winds.53 A milder climate in changes.64 If individuals can adjust rapidly to new this region would hence likely increase their winter environmental conditions by changing the timing survival and allow other less cold-adapted species of their migration or the initiation of their annual to use these areas in winter. One of the main infer- breeding events, then, in some cases at least, their ences from bioenergetic studies to date is that the populations could be little impacted by the climate- impacts of climate change in the Arctic are likely induced changes described earlier. Advanced phe- to stem from the immigration of new colonizing nologies are a widespread response of plants and species as much if not more than from the disap- animals to changes in climate. They have already pearance of current Arctic species. And some par- been described in recent decades for organisms liv- ticular species, like hibernating mammals, should ing in a wide variety of areas around the world,

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 171 Climate change impacts on Arctic vertebrates Gilg et al. including the Arctic where they have been most portant forage for caribou. In this case, despite an pronounced (up to 20 day shifts during the past advance in the onset of spring plant growth, the decade for some plants and invertebrates).2,6,65,66 timing of calving by caribou has not advanced to Unfortunately, phenologies are not plastic for all the same extent, with the result that calving is not traits, nor among all species. For some vertebrates, well synchronized with the onset of the plant grow- the timing of migration or breeding is regulated by ing season in the warmest years, when calf produc- a rigid endogenous clock or by fixed environmen- tion is lowest.69 There is also a spatial component to tal clues (e.g., photoperiod) and cannot therefore trophic mismatch, in this case because during warm be adjusted to other environmental conditions that springs, the timing of plant growth is more highly may be changing.67 For such species, shifting their synchronized across the landscape on the caribou distribution range in order to track their optimal calving grounds, reducing the advantage that spa- environmental conditions—abiotic but also biotic tial heterogeneity in plant phenology otherwise af- if interacting species also shift their range—might fordshighlymobileherbivoressuchascaribou.73 be a more relevant response. If they are not able to These observations suggest that warming may, in adjust the timing of their life cycle events (e.g., mi- populations of caribou inhabiting regions with typ- gration, breeding, molting, fattening) to temporal ically short plant growing seasons, adversely affect changes in the quality of their habitat and espe- offspring production and survival if the timing of cially to their food resources, then they will face calving is inflexible and, thereby, unable to keep mismatches and will be left with no other choice pace with advances in the timing of spring plant than moving to different habitats, using different growth on calving grounds. Indeed, recent work in- food resources (both responses allowing them to dicates that caribou lack an internal circadian clock “rematch”), or their populations will decline.68 due to selection for a circ-annual clock and thus Mismatches have both trophic and dynamic im- may display a physiologically “hard-wired” timing plications. If temporal relationships are disrupted of parturition.74 or altered, fitness will be affected,69 leading to de- In the Arctic, most mismatches are likely going clines in population abundance.70 Different trophic to be related to the advancement of the spring.66 levels—plants, herbivores, predators—may respond Among Arctic shorebirds for example, initiation in differently to warming, which may lead to mis- egg laying is governed by a combination of spring matches in the timing of events between trophic cues, including snow cover and food availability dur- levels. For instance, gosling growth in herbivorous ing the egg-laying period, and it occurs in early June geese is dependent upon good synchrony between in most areas. If the snow melts early, invertebrate hatching and the seasonal change in plant nutritive emergence could be affected. This is the strongest quality, especially protein, an essential nutrient for factor governing chick success, and shorebirds can growth.71 In snow geese Anser caerulescens breed- adjust their laying date to these local conditions by ing in the High Arctic, there is evidence that in up to four weeks.75 In years with late snow melt, the years with early and warm spring, gosling growth is birds have to wait for the snow to disappear, which reduced,72 probably because they hatch too late to might result in a mismatch between invertebrate benefit from high-quality plants. This has a negative availability and chick growth later in the season. impact on the recruitment of young because their However, in some regions, climate change could ac- survival during the autumn migration is dependent tually improve the match between the annual cycle on their mass at the end of the summer. Climate of shorebirds and the phenology of their prey. There warming will increase this mismatch and may result are indications that Arctic shorebirds may suffer in a reduction of recruitment in some populations. from trophic mismatch on the High Arctic Siberian Large terrestrial herbivores may also be suscepti- breeding grounds,76 while they might benefit from a ble to trophic mismatch derived from an advance in better temporal fit between their reproductive cycle spring phenology associated with warming. In West and the availability of their food in other places—for Greenland, for instance, long time series of observa- example, in High Arctic Greenland.21,77 The reason tional data indicate that April warming is associated for this difference is that the duration of the peak with an advance in the emergence date and rate of in invertebrates on the High Arctic Siberian tundra emergence of species of plants that comprise im- is rather short, while invertebrates are plentiful for

172 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates a more extended period in High Arctic Greenland. riod, which can result in widespread failure of goose Hence, shorebird chicks in High Arctic Greenland nests in the earliest ice breakup years. In this case, may benefit from earlier appearance of sufficient the increased match between bears and geese is ben- amounts of invertebrates, while some of their later eficial to the predator but highly detrimental to the arriving Siberian counterparts—due to often later prey. In Svalbard, increased presence of polar bears snow melt than in Greenland—may not be able to at barnacle goose Branta bernicla colonies in recent hatch in time for the peak. years has contributed to a decline in goose numbers in some coastal areas.85 Marine environments Beyond sea ice extent, the increase in sea surface Phenological adjustments also occur in marine temperatures also affects the breeding phenology of ecosystems. The reduction of sea ice extent in the seabirds.86 Despite the possibility for certain seabird Arctic will allow earlier access to benthic feeding species to adjust their breeding time in response to a grounds and create new areas of open water earlier in change in their physical environment, most of them the season for foraging, which could lead to changes might face climate change–related modifications of in seabird breeding times. Falk and Møller78 showed the spatial and temporal distribution of their prey— that the phenology of northern fulmars Fulmarus that is, trophic mismatch between predators and glacialis breeding in northeast Greenland was cor- resources.68 For instance, an earlier melting of sea- related to the sea ice dynamics of a nearby polynya. sonal sea ice in the Arctic will advance the timing Similarly, Canadian northern fulmars as well as and modify the rate of nutrient supply in upper sur- thick-billed murre Uria lomvia in West Greenland face layers, therefore affecting the timing and species have been shown to respond to sea ice conditions by composition of the phytoplankton spring bloom. adjusting their timing of arrival at their colony, ar- This change will in turn affect the zooplankton and riving later when the sea ice was more extensive.79,80 fish communities81 and modify their availability for A decrease of seasonal ice distribution should be predatory seabirds during their respective breeding beneficial to many Arctic seabird populations, as seasons. To cope with these changes, seabirds have this may advance the start of their breeding season to breed earlier to follow the timing of prey avail- and therefore allow more time to raise their chicks, ability. However, while this seems to be possible for provided these species are not indirectly affected some species—described earlier—it might not be by other mismatches—for example, between plank- the case for all of them. For example, seabird species ton bloom or fish prey availability and the chick nesting in crevices or burrows—little auks, auklets, rearing period.81 But sea ice declines will also be puffins, etc.—can only access their nest when snow detrimental to some of the most typical High Arctic has melted and might therefore be limited in their species, such as the ivory gull and several species of response, as future climate changes are also expected marine mammals (described later), that are sea ice to be associated with an increase in precipitation in- specialists.41,82 These contrasting effects are some- cluding snow fall. times even found between populations of the same Many ice-associated marine mammals use tradi- species. Thick-billed murres breeding in the Cana- tional breeding sites where these broadly dispersed dian Arctic experience a beneficial effect of a reduced populations congregate at very specific times—for sea ice season at the northern limit of the breeding example, harp seals Phoca groenlandica. These ren- range due a lengthening of the breeding season but dezvous match availability of their ice habitat, but a detrimental effect at its southern limit, because it also match food availability at the time of weaning leads to mismatches between the timing of fish prey of the young. As the sea ice season contracts, it is availability around the colony and the chick rearing easy to envisage mismatches occurring between the period.83 timing of independence of the young and the lower Along western Hudson Bay there has been a trophic prey upon which they depend. Many tem- climate-driven increase in the overlap between nest- perate whale species migrate into the Arctic to feed ing geese and polar bears.84 Late ice formation in fall in the marginal ice-edge zone, taking advantage of and early break-up has extended the terrestrial pe- the spatially and temporally predictable late spring riod for the bears. This means that the bears now and early summer high productivity. In the future, forage on energy-rich goose eggs for a longer pe- it is likely that the Arctic marine ecosystem will be

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 173 Climate change impacts on Arctic vertebrates Gilg et al. more productive in an overall sense, but it is also the southern (or lowest) and northern (or high- likely that prey will be more dispersed and hence est) borders of distribution ranges are constrained more energetically costly to acquire. by climate and can hence move as a consequence As illustrated by the few examples described ear- of climate change. There are situations, however, lier, it will often be difficult or even sometimes totally when only one of these borders is constrained by impossible for Arctic vertebrates to adjust their phe- climate—the other being constrained by geograph- nologies in order to avoid mismatches. Responses ical barriers, competitors, etc. In these cases, climate to such challenges will be particularly difficult for warming can either induce a decrease in distribu- species that use different habitats or food resources tion range—if the southern border is constrained during their annual life cycles—for example, migra- by climate—or an increase. Several predictive mod- tory species wintering outside the Arctic or species els based on habitat utilization by feeding or nest- like salmonids using both oceanic and continen- ing geese follow this rationale.94,95 Jensen et al.96 tal ecosystems; see also the section on “Cascading recently attempted to predict the future distribu- changes.”87 Indeed, the various mismatches these tion of pink-footed geese Anser brachyrhynchus in species will face in these different habitats through- Svalbard, considering that warm temperatures will out the year will be different in speed, intensity, and create a longer summer season, thereby increasing nature, and must therefore be solved by different— the probability that geese will be able to complete and sometimes antinomic—responses. their breeding cycle, and also experience increased food availability. According to their model, a 2oC Poleward changes in habitat and species increase in summer temperature should lead to an distributions: a large-scale paradox of expansion in goose distribution and ultimately an enrichment enhanced population growth (but also see contrast- Due to various underlying processes already pre- ing results based on seasonal changes in food quality sented in other sections of this review (e.g., physio- in the previous section). logical constraints, specialization for some habitats Another peculiarity of range shifts in the Arctic and prey, limited phenological plasticity, interspe- is related to the geophysics of the Earth. Any pole- cific interactions, biogeographical history, etc.), ev- ward shift in species distributions will mechanisti- ery species uses a given geographical area (delimited cally lead to a decline in the size of these ranges—a by its distribution range) characterized by a specific “polar squeeze”—the surface of latitudinal belts de- climate (sometime used to define species’ “climatic creasing northward (e.g., a 1◦ Lat. by 1◦ Long. area envelopes”).88 As seen in the previous section, many covers ca. 6200 km2 at 60◦ Lat. but only 4200 km2 at species try to adjust to their changing environment 70◦ Lat. and 2100 km2 at 80◦ Lat.). The most severe (e.g., by changing the timing of their annual cy- losses should therefore concern habitats that already cle) in order to stay in their current distribution reach the highest possible (90◦ Lat.) or potential (see range, but the phenotypic plasticity of individuals is later) latitudes, because surface lost in the South of finite and such adjustments are therefore limited.89 their range cannot be fully compensated by the col- Hence, shifting the latitude or altitude in which they onization of new areas in the North. live in order to track their optimal environment Sea ice is probably the best example of a habitat appears to be a better strategy in the long term, that can only decline under current climate change especially for Arctic vertebrates that are extremely scenarios, because it already occupies the northern- well adapted to their harsh environment but that most seas on Earth. Poleward shifts will be impossi- have limited evolutionary capabilities on short time ble for species already distributed in these extreme scales (see section “Evolutionary responses”). regions. In addition, retractions of sea ice that oc- Poleward shifts have been documented for many cur to the degree that the remaining ice is no longer species in recent decades, even for animals that live over productive shelf seas, but instead over the deep, only within the Arctic region.90–93 As for phenolog- unproductive Arctic Ocean, are likely to have ex- ical changes, given the intensity of climate change treme impacts and may induce tipping points. The in the Arctic, range shifts are expected to be more well-documented polar bear case has already been pronounced here than in other biomes. In a strict presented, but this will also be the case for less sense, range shifts describe situations when both well-known species such as the ivory gull and the

174 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates ice-dependent seals that require sea ice on a year- (e.g., kittiwakes Rissa tridactyla and common eiders round basis.41,82,97 In the long term, the disappear- Somateria mollissima) and for the establishment ance of summer sea ice in most of the Polar Basin of new breeding species—like black-backed gulls may restrict ice-dependent species to the north Larus marinus and Larus fuscus.101–104 The kittiwake coasts of Greenland and Ellesmere Island (Canada), nicely illustrates the ongoing changes in range shifts where multiyear ice is predicted to last longest or for widespread species: its populations are increas- even drive some of these species to total extinction. ing and its distribution range is expanding in the Some terrestrial habitats like the High Arctic po- Arctic, while they are simultaneously declining in lar deserts are similarly threatened because there is Europe at the southern border of its range.102,103,105 virtually no new area to colonize for the inhabi- The first records of gray seals Halichoerus grypus tants of these areas, including the vertebrate species in southern Greenland, harbor porpoise Phocoena they host—for example, the Peary caribou Rangifer phocoena in Svalbard and well-documented shifts tarandus Pearyi. This “dead end” problem can be a in gray whale Eschrichtius robustus distribution sug- concern even in low-Arctic regions. Here, narrow gest that range shifts are also occurring quite broadly belts of open tundra are currently colonized at their among marine mammals that are resulting in tradi- southern borders by shrub communities, while the tionally more southerly species spending more time typical open tundra is prevented from extending in the Arctic as well as regular Arctic migrants stay- northward due to bordering seas (e.g., in north- ing for longer periods.41 ern Alaska and on the continental part of northern Another consequence of the reduction of sea ice is Russia). that many islands currently connected to the main- Species and subspecies that already have small dis- land by ice bridges for most of the year will become tribution ranges, small population sizes, or that are ice free for a longer period. This loss of connectivity to some extent dependant on typical Arctic habi- will prevent access for predator species like the Arc- tats like sea ice (e.g., polar bear, walrus Odobenus tic fox Vulpes lagopus to some bird colonies during rosmarus, narwhal Monodon monoceros,bowhead the breeding period and will strongly benefit birds whale Balaena mysticetus, ivory gull, and a few oth- nesting on these islands, as already seen for common ers) or High Arctic tundra (e.g., several wildfowl eiders in Canada.106 On a larger spatial and tempo- and shorebird species, muskox, several reindeer sub- ral scale, it is also likely that the small Arctic fox populations, etc.) will hence face a growing risk of populations historically found on Jan Mayen and extinction during the coming decades.21,98,99 Bjørnøya (Norway)—two oceanic islands holding Despite this dark picture for endemic Arctic important seabird colonies in summer but no alter- species, many “meridional” species are colonizing native food resources to sustain fox populations dur- the Arctic and their marginal Arctic populations ing the winter period—declined and eventually be- are increasing. Due to their ability to cross-oceanic came extinct in recent decades due to the loss of sea barriers, many of these species are fish, seabirds, ice connectivity, making regular immigration from seals, and cetaceans, with the highly visible colo- large nearby populations—that is, northeast Green- nial seabird being the best documented group. Cli- land and Spitzbergen—difficult.107,108 Although ex- mate change is expected to induce northward shifts tensive sea ice periods have promoted population in the distribution of most seabirds and some ma- exchanges among Arctic fox, reindeer, and other rine mammals in response to the appearance of new terrestrial mammal populations, they have actu- suitable habitats and to the modification of their ally limited population exchange within marine prey distribution. In northeast Greenland, for ex- mammals and conversely, of course, periods with ample, the coastal waters between 72 and 80◦Lat. little sea ice have promoted population linkages North were until recently covered year round by and genetic exchange for marine mammals.109 Less multiyear drift ice transported from the Polar Basin sea ice in the future is almost certain to pro- by the East Greenland Current. Historically, this mote more extensive and regular population ex- coast only hosted a few, small breeding seabird change among various marine mammal species, colonies.100 Recent changes in sea ice regimes (both particularly among those cetaceans that have ex- in extent and duration) are providing opportunities tensive migrations as a normal part of their annual for this region to host larger seabird populations cycles.110

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 175 Climate change impacts on Arctic vertebrates Gilg et al.

Simultaneously, the warming of the oceans has their populations decline and in some cases even go also led to important changes in zooplankton and extinct. fish communities, and several studies predict these Cascading changes and feedbacks: from modifications will continue.111 The overall trend population dynamics to ecosystem is a northward movement of species along with functioning a replacement of Arctic species by more temper- ate ones with different energetic values—for exam- Arctic ecosystems are hypothesized to have little ple, the replacement of the cold adapted, lipid-rich functional redundancy. Changes in the phenology, copepods Calanus hyperboreus and C. glacialis by distribution, or behavior of species—as already de- southern, low-lipid C. finmarchicus being a particu- scribed in previous sections—may therefore have larly well-studied example.81 These sorts of changes disproportional impacts on the abundance and dy- will indirectly impact breeding seabirds and marine namics of species, and in turn on the structure and mammals through bottom–up control processes.112 functioning of their communities and ecosystems. Because these Arctic marine top predators are often Therefore, the impacts of climate change cannot be specialized, their fate will depend on their ability to inferred or predicted using either single-species ap- modify their diet according to new prey conditions, proaches or simple empirical relationships between a plasticity that has already been shown in several processes and driving variables. Tounderstand these Arctic species but within given limits.113,114 changes and predict their consequences, one must For the long-distance migratory Arctic shore- instead explore them in a multitrophic and multi- birds, climate change effects on their staging and species perspective, particularly in the Arctic.119–121 wintering areas may be just as—or even more— Climate change has already been shown to af- important than conditions in the Arctic.21 This is fect life-history traits like survival and reproductive because most of them stop over and winter along success of many Arctic vertebrates.122–124 Climate- marine coasts, on a small number of exceedingly im- driven impacts on dynamics are, however, often portant intertidal areas, where sea level rise or other more difficult to understand because impacts also climate-related changes may modify their current vary in direction and strength depending on how feeding grounds (e.g., in the West European Wad- trophic interactions are disrupted.125 Small rodents den Sea, Banc de Arguin in West Africa, the Yellew in general and lemmings in particular provide good Sea in East Asia, and Copper River Delta in southern examples of such interspecific interactions across Alaska).115 several trophic levels. Lemmings are central to the For all these reasons, overall distribution ranges of multitrophic interactions in the Arctic tundra and most Arctic vertebrates are predicted to shift north- play a key role in shaping the structure and dy- ward, and population sizes of many of them are namics of these ecosystems. They impact repro- likely to decline as a consequence of the reduction duction and abundance of many terrestrial Arctic of their habitats and immigration of new competi- predators,126,127 whichinturncreatesfeedbackson tors. However, in the Arctic, gains and losses will not lemming cyclic dynamics as well as on the dynam- be similar to other biomes,116 because only a few icsofothervertebrateprey.128,129 In Greenland and vertebrate taxa are likely to disappear while many in Scandinavia, lemming cycles have recently been “new” ones will colonize from the South. The para- fading out.15,16,130 This situation is not particularly dox here is that species richness in the Arctic will surprising given the evidence from both paleo- and undoubtedly increase in the future—more species current records showing that rodent population dy- colonizing than species disappearing—but Arctic namics are highly influenced by climate variables biodiversity, that is, its contribution to the biolog- in the Arctic, in particular by snow characteris- ical diversity on a worldwide scale as defined by tics.11,12,15,16,129,131,132 Not only does snow provide its original sense,117,118 can only decline. Indeed, insulation from the harsh Arctic weather, but a thick the many taxa colonizing from the South will often snow cover also prevents most predator access to the just expand or shift their ranges northward (see the subnivean rodents.133 For lemmings in particular, kittiwake example described earlier), while the few sufficient snow cover is important for winter breed- Arctic ones, only present in this biome and that have ing.11,12 The ongoing and future changes in temper- no alternate region to colonize to the North, will see ature and snow conditions are therefore expected

176 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates to have important implications for the population Bylot Island provides another interesting exam- dynamics of lemmings, in terms of both increased ple of altered community function. Reproduction length of the lemming cycle and reduced peak densi- of snow geese is strongly affected by weather con- ties.16,129 Such changes in rodent dynamics will have ditions prevailing in spring at this location. When immediate effects on the predator community, not the spring is early and warm, the probability of lay- only in terms of reduced abundance and productiv- ing eggs increases, that is, the nest density is higher, ity,16 but also in terms of more indirect effects on the laying is early, and individuals lay larger clutches, predation pressure on alternative prey species, such resulting in a higher reproductive effort at the pop- as ground-nesting birds.134–138 Ultimately, this may ulation level.72,150,151 But climate also drives pri- even affect the geographical distribution of shore- mary production. In wetlands used by geese, pro- birds and other species sensitive to predation.139 The duction has increased by 85% during the period of fading out of the small mammal population cycles 1990–2009, most likely as a direct consequence of will have far-reaching, cascading effects, ultimately the warming temperatures. The cumulative num- impacting the structure and functioning of the en- ber of thawing degree-days during the summer tire terrestrial Arctic ecosystem.130,140 As lemmings is an important determinant of plant biomass at are key grazer and browsers of Arctic plants, loss the end of the summer.152 Although this suggests of cyclic lemming outbreaks will also feedback on that snow geese should benefit from climate warm- important structural components of the vegetation ing, other factors such as increasing mismatch be- like tall shrubs.141 Consequently, negative effects of tween the timing of breeding and plant phenol- climate warming on lemmings may create a positive ogy (see section earlier) could mitigate these effects. feedback on the ongoing greening of the Arctic ow- Moreover, in recent decades, goose population in- ing to shrubs encroaching on tundra plant commu- creases have largely been driven by events occur- nities.142 Finally, shrub encroachment is predicted ring during winter—mostly food subsidy provided to provide a positive feedback on the climate system by feeding in agricultural lands—and this has had itself through more absorption of sunlight that is negative impacts with snow geese overgrazing their converted to heat.143 Arctic breeding habitat in several localities.153,154 Changes in distribution ranges—see the previous Thus, climatic effects cannot be fully understood section—can also impact the population dynamics without considering all factors affecting the dynam- of competing species and deeply modify the struc- ics of a population. ture of communities. In Scandinavia, there is now The well-known influences of large, mammalian extensive empirical evidence that the larger red fox herbivores on primary production and plant com- Vulpes vulpes can expel its smaller congener, the arc- munity composition may play a role in ecosystem tic fox, from food resources in winter144 and from responses to climate change in areas with increasing breeding territories145 and dens146 in summer. Dur- or stable populations of large herbivores. Experi- ing the last century, the red fox has extended its mental evidence indicates, for example, that graz- range northwards into the tundra zone at the ex- ing by caribou and muskoxen in West Greenland pense of the Arctic fox, which has retracted its south- suppresses the positive response of woody, decid- ern distribution limits.147,148 Although it has been uous shrubs to warming, maintaining the plant suggested that the range expansion of the red fox community in a graminoid-dominated state.155 Be- is related to climate warming and concomitant in- cause woody shrubs have a much greater carbon creased primary productivity of the tundra,147 the uptake potential than do graminoids, this suggests link to increased secondary productivity and hence mammalian herbivores may have the potential in food for carnivores has yet to be demonstrated.149 In some parts of the Arctic to constrain carbon up- this context, it is important to keep in mind that the take by ecosystems in response to warming. Indeed, Arctic is changing not only due to climate change, experimental warming resulted in a threefold in- but also for other reasons owing to local anthro- crease in ecosystem carbon uptake in West Green- pogenic activities—e.g., intensified land use, infras- land, but only where caribou and muskoxen had tructure, settlements—which may pave the way for been excluded; in sites where these herbivores grazed highly adaptive generalist predators like the red fox warmed plots, there was no net increase in carbon and corvids.144 uptake in response to warming.156

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 177 Climate change impacts on Arctic vertebrates Gilg et al.

As seen earlier, climate change will impact the fluence individual fitness and in turn population dynamics of Arctic multitrophic systems whether dynamics.166–170 they are bottom-up or top-down controlled. Other Several climate-driven changes in host–parasite important clues to understanding these impacts are interactions are already obvious in the Arctic, and space and time. Even a significant impact of climate several reviews have recently been devoted to the ef- on breeding success can take several years to show fects of climate change on parasite infections and the effects in many species. For instance, it takes the ecological and evolutionary consequences for Arc- young several years to reach sexual maturity and re- tic vertebrates.162,171–173 Overall, these studies sug- turn to the breeding sites in many seabird or marine gest that climate warming can increase pathogen mammal species.157 In addition, one needs to ac- development and survival rates, disease transmis- count for regional climate change variation, partic- sion, and host susceptibility through at least three ularly for animals that use areas experiencing differ- main mechanisms. ent degrees of change during their annual cycles, in First, global warming could change the abun- order to comprehensively assess changes in popula- dance as well as spatial and temporal distribution tion dynamics. Arctic terns Sterna paradisaea winter of existing parasites. Indeed, the life cycles of nu- in sub-Antarctic waters while little auks remain in merous parasites are more efficient in warmer con- Arctic waters, despite the fact that both breed in the ditions, and global warming is hence expected to High Arctic. These two species will of course be dif- increase the success of infective stages. One of the ferently exposed and differently impacted by climate best examples of this phenomenon is the infection change.112,158 Even the lemming predator commu- of muskoxen by the nematode Umingmakstrongy- nity described in the previous example is indirectly lus pallikuukensis.163 Empirical field and laboratory linked to pelagic intertropical climates, via two skua data have demonstrated that the life cycle of this species that are highly specialized on lemming prey parasite has become shorter due to temperature spending the summer in the Arctic but the rest of increases, resulting in an increased parasite bur- the year in the south.159,160 But despite the recent dens for their host.163 Increases in pathogen in- development of year-round tracking devices, our fections linked to warmer temperature have also knowledge is still mostly restricted to the summer been documented for other parasites in muskox,174 season for many Arctic migrants, while spatial dis- reindeer,175 marine mammals,176 and seabirds.170 tribution or foraging behavior are still poorly known Second, global warming might also induce north- during the nonbreeding season, which is of course ward range shifts of parasites due to the relaxation an essential period in these animals’ life cycles.53 of the environmental constraints that affect their survival and developmental rates. For example, in The cryptic parasites Canada, the northern limit of the moose winter tick The overall health of an individual is the result of Dermacentor albipictus has already significantly ex- many interactions between its immune status, body panded.173 Finally, temperature increase will facili- condition, pathogens, exposure to pollutants, and tate the arrival and establishment of new pathogen other environmental conditions that influence these species previously unknown in the North and for factors.161 Because climate is one of the main factors which Arctic hosts have no previous exposure and driving the diversity, distribution, and abundance hence no immunity.177 A number of studies have of pathogens, understanding how climate changes shown that new parasites are currently emerging in might affect host–pathogen interactions is a ma- northern ungulates due to climate change, modified jor, though often overlooked, challenge.162 As the movements of animals, and population density.178 Arctic climate becomes warmer and wetter, pro- Direct impacts of new parasites on naive host pop- found changes are expected in host–parasite inter- ulation could lead to epidemic disease outbreaks actions; many pathogens are sensitive to tempera- (e.g., Elaphostrongylus rangiferi within caribou in ture, rainfall, and humidity. The transmission rates Newfoundland).179 of pathogens and their period of transmission will There is no doubt that climate change is al- become longer in warmer conditions.163–165 This ready altering the dynamics of host–parasite inter- change could have profound consequences on Arc- actions in the Arctic. Such changes will have pro- tic vertebrates, because parasites are known to in- found impacts on population dynamics of hosts and

178 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates for the ecology and evolution of Arctic vertebrates, four subarctic marine mammal species. According although the consequences of these changes have to their sensitivity index, the hooded seal Cystophora not yet been properly evaluated. cristata, the polar bear, and the narwhal appear to be the three most sensitive Arctic marine mam- Evolutionary responses mal species, primarily due to reliance on sea ice Most studies to date that have attempted to fore- and specialized feeding. The least sensitive species cast the impact of climate change on species and were the ringed seal and bearded seal, primarily communities have used phenomenological models due to large circumpolar distributions, currently based on species niche, largely ignoring the species’ large population sizes, and flexible habitat require- adaptive potential and biotic interactions.180 Many ments. Although, the very specific breeding require- examples have already been given throughout this ments of ringed seals (for snow availability on sea review to emphasize the importance of biotic inter- ice that must last for a period of months) proba- actions, but evolutionary responses are likely also bly warrants their inclusion in the most sensitive 41 important to consider because evolution is a perma- category. nent and sometimes rapid process that can mitigate There are limits to plastic responses, and they are the effects of climate change.181,182 unlikely to provide long-term solutions for the chal- lenges currently facing populations of Arctic ver- Change in phenology: adjust where you live tebrates, especially for specialized species that are Phenology is a key aspect of the adaptation of Arctic experiencing continued directional environmental vertebrates. The short growing season in the Arc- change.185,186 Microevolutionary changes—that is, tic represents a challenge for most animals, and changes in gene frequencies between generations— life-history strategies of successful Arctic vertebrates allow populations to cope with longer-term envi- have evolved to enable individuals to fulfill their life ronmental changes through permanent modifica- cycles under time constraints and high environmen- tions of phenotypes and will reflect selection on tal unpredictability.6,183 In such a highly seasonal phenotypic traits.187 As climate warming continues, environment, offspring production is timed to coin- shifting optima for phenological traits—for exam- cide with the annual peak of resource availability— ple, the timing of development, reproduction, mi- see section “Advanced phenology.” The mechanisms gration, or fall dormancy—will at some point exceed that allow organisms to cope with climate-induced the limits of individual plasticity and selection for phenological changes are likely to be of two basic genetic change in populations will occur. Indeed, kinds. when faced with long-term directional changes in Phenotypic plasticity—changes within indivi- environmental conditions, evolutionary adaptation duals—allows organisms to rapidly cope with short- becomes essential for the long-term persistence of term changes in the environment without a change populations. in genotypes. Some individuals in a population Evolutionary response to selection will depend on can accommodate large amounts of environmen- the presence of heritable variation—that is, stand- tal variation while other individuals can tolerate ing genetic variation within populations and addi- only a narrow range of environmental variation.184 tional variation generated by mutation and immi- Across the circumpolar Arctic, species are region- gration.188–190 However, there is growing evidence ally exposed to varying sets of environmental con- that populations of Arctic species have relatively ditions in different parts of their range and thus low genetic diversity, a pattern observed for such may demonstrate considerable plasticity.66 But plas- diverse species as polar bears,22 muskoxen,191 col- ticity will also depend on species–specific sensitiv- lared lemmings Dicrostonyx groenlandicus,132 and ity to climate change that may vary according to the wolf Canis lupus.192 Most studies suggest that population size, geographic range, habitat speci- the Last Glacial Maximum (25.0–18.0 cal. kyr BP), ficity, diet diversity, migration, site fidelity, sensi- which was strongly associated with a cold and dry tivity to changes in sea ice, sensitivity to changes in climate, had strong effects on the genetic variation the trophic web, and maximum population growth of Arctic vertebrates. High Arctic shorebird species potential. This series of factors allowed Laidre et have probably been through similar genetic bot- al.43 to quantify the sensitivity of seven Arctic and tlenecks since the last interglacial, in contrast with

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 179 Climate change impacts on Arctic vertebrates Gilg et al. low-Arctic and sub-Arctic species that show exten- tation of the distribution range of Arctic vertebrates, sive polymorphism.21 This likely indicates that High eventually below the critical level of metapopula- Arctic shorebirds have been repeatedly exposed to tion persistence.196,197 Future decreases of sea ice “Arctic squeeze”—that is, their southern limit of extent will lead to a loss of connectivity between distribution being pushed northwards, while they Arctic regions, preventing or impeding dispersal of could not move farther North due to the Arctic pagophilic species in summer. Even for some terres- Ocean barrier (see also section “Poleward shifts”). trial mammals like the Arctic fox, sea ice is necessary Although one may therefore expect a constant for long-distance dispersal.198,199 Genetic structure decrease of genetic diversity for current Arctic pop- of fox populations is therefore likely to change dra- ulations and low evolutionary potential, it should matically in the future, both at the circumpolar scale be mentioned that most studies done to date have and within populations, as a consequence of the on- used neutral markers (e.g., mitochondrial DNA) to going sea ice declines (see also section “Poleward evaluate the level of genetic variation within and shifts”).108,200,201 between populations. Hence, they may have little To improve our knowledge of the evolutionary bearing on real measures of genetic variation in mor- consequences of climate change, we can also learn phology and life-history traits, which are directly ex- from the past. The Quaternary period (the past posed to selection. Few Arctic vertebrates have been 2.6 Myr) was marked by glacial–interglacial phases studied using a quantitative genetic approach that and can be used as a model system to infer how Arc- addresses the potential for rapid adaptation to cli- tic species have responded to past climatic variation. matic change. Using such a quantitative genetic ap- In order to track their preferred habitats, species proach, Reale´ et al.193 showed that northern boreal should increase their distribution ranges during pe- red squirrels Tamiasciurus hudsonicus were able to riods of suitable climate and conversely contract respond to increased temperatures both plastically them when climate conditions become unsuitable. and genetically within a decade. Pedigree analysis The lesson we have learned from the past is that for showed that about 13% of the 18-day advance in temperate species, warming periods are often in- mean parturition date was genetic and that 62% of dicative of range expansions, while for Arctic species the change in breeding dates was a result of phe- (e.g., muskox), populations are seen to increase notypic plasticity. This study emphasizes the need during global climatic cooling and decline during for extensive, long-term ecological and quantitative the warmer and climatically unstable interglacial genetic data for estimating the relative roles of evo- period.191 lution and plasticity on response to climate change. Finally, a different approach to study past de- Given that species with short generation times tend mographic changes is to use ancient DNA, which to have higher rates of molecular evolution,194 we allows the study of dynamic genetic variation over can expect that long-generation-time species such time. Thanks to well-preserved samples buried in as bowheads or the monodont whales should have permafrost, this approach has been used in sev- less evolutionary potential to respond to new selec- eral Arctic species—e.g., muskoxen,191 collared lem- tive pressures than shorter generation–time species ming,132 and Arctic fox.202 The results show that such as shorebirds or rodents.183 for the Arctic fox, populations in middle Europe became extinct at the end of the Pleistocene—ca. Range shifts: tracking suitable habitats 18 Kyr ago—and did not track its habitat when it Global warming over the past 40 years has shifted shifted to the north. These results suggest that some the ecological niche of many species spatially—that populations, despite high specific dispersal capa- , is, towards the poles or higher altitudes (see sec- bilities,198 199 might be unable to track their habi- tion “Poleward shifts”). An ability to track shifting tats.202 For collared lemming, results also showed habitat is critically influenced by individual disper- that previous climate events have strongly influ- sal, which is key to the dynamics of genetic diver- enced genetic diversity and population size.132 Due sity in time and space and has profound effects on to its already reduced genetic diversity, a further de- the ecological structure and dynamics of popula- crease would strongly impede the evolutionary po- tions.180,195 In the meantime, however, global warm- tential of this species. Local extinctions of collared ing might cause an overall contraction and fragmen- lemmings would in turn have severe effects on the

180 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates entire terrestrial ecosystem, and perhaps even be- “exploitative competition.”205 In the High Arctic, yond it into the marine environment (see section the breeding success of some waders and wildfowl “Cascading changes”).16,126,152 is sometimes assumed to mirror changes in lem- ming densities mediated by shared predators—that Missing pieces is, “apparent competition.”136,137,139,206 Due to low species richness, relatively simple func- Precipitation can also lead to unforeseen changes 207 tioning, and high exposure to climate changes, Arc- in interspecific interactions. Lecomte et al. tic ecosystems are already being strongly impacted recently showed that water availability—and by climate-driven changes and are among the best rainfall—affects the interaction between snow geese candidates to study ecological impacts of this phe- and the Arctic fox. Egg predation is reduced in nomenon.6,123,140 Arctic ecologists often advertise years of high rainfall because incubating females their studies for their inferential potential—that is, walk shorter distances from their nest to drink and for the overall knowledge that can be gained from feed and therefore have a better chance to defend their study to understand and possibly mitigate the their nests from predators. Because climate change 3,6 impact of climate change in other ecosystems that should affect precipitation regimes in the Arctic, are not yet, or not so strongly, impacted. Even if this may impact nesting success of geese by changing we agree with these statements in general, we also water availability for incubating females. However, call for great caution when discussing the results of the direction of the effect is difficult to predict be- such studies on larger taxonomic or geographical cause although total precipitation should increase, it scales. For the time being, most studies claiming to may be concentrated in fewer, more intense rainfall show impacts of climate change—in the Arctic and events. elsewhere—are species oriented and only present Even though they are strong enough to shape correlative evidence. They are therefore specula- entire vertebrate communities, such indirect inter- tive because they only consider a small fraction of actions are often difficult to discern without long- the interacting species and have a limited predictive term, large-scale, and multispecies time series. Such value since they often do not explicitly study the data sets are rare for Arctic systems. An additional factors driving these population dynamics. Meta- challenge is to untangle climate-driven changes analyses, experiments, and modeling studies can from other anthropogenic impacts. In Canada, for partly address these problems, but they also have example, the predation of large gulls Larus argen- weaknesses—for example, low predictive power at tatus and Larus marinus on kittiwake is sometimes the species level,90 narrow scope for the second be- linked to the availability of capelin Mallotus villo- cause only a few parameters can be tested simul- sus, and when capelin are scarce, kittiwakes suf- taneously, and too many nontestable assumptions. fer higher predation from large gulls. But capelin Below, we address a few of these missing pieces. availability is driven both by climate and fishing pressure.208 Cryptic indirect interactions As seen in the previous sections, interspecific in- The winter gap teractions strongly influence how climate change Until recently, and with the exception of a few affects organisms—for example, competition, par- species, our ecological knowledge of most Arctic asitism, and predation can impact behavior, indi- vertebrates has been extremely limited for the win- vidual fitness, geographic range, and ultimately the ter period. Yet this time, season is very important to structure and dynamics of the community—but are the understanding of the dynamics of species. Ex- too often overlooked.120 Predators, for example, are changes of resources across ecosystem boundaries both impacting and in turn impacted by their prey— are known to impact food webs, especially in low- see section “Cascading changes.” But interspecific productive Arctic systems.152 Because most Arctic interactions also often produce indirect and unpre- vertebrates are to some extent migratory and make dictable impacts.203,204 In Scandinavia, for instance, use of different ecosystems during their annual cy- the impact of increasing red fox populations on the cles, they contribute to such exchanges. In recent regionally endangered Arctic fox is thought to be years, satellite tracking has allowed major progress mediated by their shared microtine prey—that is, in our knowledge of nonbreeding distribution and

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 181 Climate change impacts on Arctic vertebrates Gilg et al. migration flyways of many large Arctic vertebrates, But such abilities are limited, and “points of no and geolocators are currently filling the gaps for return” might be reached when conditions change small, site fidel birds species. Thanks to these ad- sufficiently. Complex systems in particular are of- vances, we recently learned that several of the ter- ten characterized by nonlinear responses to changes restrial predators that reproduce in the Arctic tundra and can have thresholds that once passed lead to in summer make extensive use of the sea ice ecosys- abrupt and irreversible changes.213 Such thresholds, tem during the winter period.199,209,210 This unex- or “tipping points,” are highly unpredictable in bi- pected behavior—at least for the snowy owl and ological systems, because they can be the result of the gyrfalcon—undoubtedly impacts the fitness of a number of changes in the population dynamics these individuals and their subsequent impact on of several interacting species. Any taxon that dis- terrestrial prey in the tundra ecosystem during the appears from an assemblage or even just declines breeding season. Consequently, the current changes due to climate change will alter ecosystem function- in sea ice regimes may also increase the vulnerabil- ing. This can lead to sudden, steep, and irreversible ity of these predators to climate warming.152 Further changes in Arctic ecosystems where vertebrates have technological innovations will hopefully allow us to low functional redundancy (see also section “Cas- gain more knowledge regarding the winter ecology cading changes”). of many others species in the near future. When tipping points result from a single domi- nant driving force, their consequences can be easier “Subsidies” to foresee. For example, thermal windows have given Anthropogenic food resources and animal carcasses limits (see section “Ecophysiological constraints”). have often been an overlooked resource in the past— The dynamics of a species can remain relatively sta- except for typical scavenging species—when assess- ble as long as the climate fluctuates within these ing energy flows and population dynamics of Arctic limits, but might suddenly and rapidly decline once vertebrate communities. Yet these alternate food re- these limits are crossed. In addition, species can only sources are currently increasing in the Arctic, both adjust their phenologies to a changing environment as a consequence of climate change—for exam- within given limits—for example, long-distance mi- ple, herbivores suffer higher mortality due to ic- grants need a minimum period of time to build up ing events140—and increasing human activities— fat reserves on their wintering and staging grounds for example, reindeer management149 and fishing and then to travel all the way to their breeding waste.211 Increasing numbers of ungulate carcasses, grounds. Hence, their arrival in the Arctic cannot for example, are assumed to benefit red foxes in be brought forward indefinitely. Similarly, plastic- Scandinavia, which can in turn negatively impact ity of diets has limits, which once crossed—that is, the regionally endangered Arctic fox.149,212 Simi- when the more profitable food items become too larly, it is assumed that spatio-temporal differences “expensive” to get—will rapidly impact fitness. Fi- in muskox mortality impacts the population dy- nally, some biotic tipping points can just mechanis- namics of Arctic foxes and stoats Mustela erminea tically mirror abiotic tipping point. The reduction in northeast Greenland, which could in turn ex- of sea ice, for instance, is believed to have geophys- plain regional differences in the amplitude and cycle ical tipping points according to some climate mod- length of lemming fluctuations.16 Because the avail- els,214 which would induce correlated tipping points ability of such alternate food is likely to increase for pagophilic species. in the future or at least change in abundance and distribution, it is important to consider them in fu- Where are the Arctic vertebrates heading? ture studies aiming to assess population dynamics Due to the large variance in climate models, in- of Arctic vertebrates. herent complexity of natural systems, and the diffi- Tipping points culties of implementing large-scale, long-term, and Ecosystems do not always respond in smooth, linear, multi-trophic studies in the Arctic, predictions of and reversible ways to pressures. As seen in previ- climate-induced ecological impacts are difficult and ous sections, many Arctic species will first be able to remain highly speculative.119,215 Even though pre- buffer the effects of climate change to some extent— dictions might be easier in the Arctic than elsewhere, for example, thanks to their behavioral plasticity. the Arctic is nonetheless a complex system where

182 Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. Gilg et al. Climate change impacts on Arctic vertebrates climate conditions, physical environments, or food access to alternative prey. High Arctic Canada and web structure can be markedly different. Different North Greenland are most likely the only regions species or even individuals within a species can re- where polar bear populations are likely to survive in act differently to similar environmental modifica- the future if summer sea ice continues to decline as tions according to their location and their current predicted by most sea ice models. life-history strategy. Predictions made for a spatially Although further work is needed before we can restricted area might not be applicable to other re- draw similarly precise predictive scenario for most gions and could lead to wrong interpretations, pre- other Arctic vertebrates, the current knowledge dictions, and management plans.216 summarized in this review nonetheless indicates The best example of an Arctic vertebrate for which that climate change driven impacts on Arctic ver- we have enough knowledge to reach this aim with tebrates follow some general trends. relatively high confidence is the iconic polar bear. Several studies have tried to predict what may hap- • Because the annual cycle of most Arctic verte- pen to polar bears and their habitat in the coming brates is tightly linked with the cryosphere (i.e., decades. Because the biology of polar bears in differ- snow cover for terrestrial species and sea ice for ent subpopulations around the Arctic varies consid- marine ones), they will have to adjust their phe- erably23 and vital demographic parameters vary in nologies to these new conditions on the short unpredictable ways with environmental change, the term, especially in order to avoid trophic mis- predicted outcomes must be considered cautiously. matches. But given the future predictions regarding sea ice • As vegetation belts and associated species move in most climate models, it is clear that the optimal northward, Arctic vertebrates will eventually habitat of polar bears will be severely reduced in have to follow these range shifts in order to the coming decades. This habitat where polar bears track their optimal living conditions. With a hunt and spend most of their time is mainly “not few exceptions, this will mechanistically lead too old sea ice over not too deep waters, not too far to the reduction of their distribution ranges, from land.”216 In addition, multiyear sea ice is an particularly among High Arctic species. important denning habitat north of Alaska, while in • For the most pronounced High Arctic species, other areas sufficient snow fall in autumn is neces- range shift may not be possible and selection for sary to form snow drifts where maternity dens will adaptive genotypes may be too slow, if possible not thaw or collapse. Sea ice around denning areas at all. These species will face the highest risk of must be in place in time for the autumn to per- extinction during the coming decades. mit access and also remain long enough to provide • The speed of these range shifts will for the hunting possibilities for ringed seals in the spring. A most part be species specific. Due to these model based on the expected changes of polar bear specific differences, the structure of the ver- habitat, in combination with demographic and en- tebrate communities will necessarily change in vironmental data, has predicted a strong decline in the future. It is expected that climate warming the number of polar bears, with total extirpation in will have stronger impacts on specialist feed- areas currently holding two thirds of the world pop- ers, which are less prone to respond to a rapid ulation by 2050.217 However, Amstrup et al.218 point change in prey availability, distribution, and out that slowing greenhouse gas emissions could re- quality. duce loss of polar bear habitat and stop their decline • Because many Arctic vertebrates have long gen- in large parts of the Arctic. The intimate connection eration times and sometimes highly variable between polar bear distribution and sea ice allows dynamics, a climate-induced reduction in in- us to predict where polar bears will likely survive dividual fitness may take significant periods of in the future. The decline in survival, reproduc- time to become perceptible in the population tion, and population size of the western Hudson dynamics of Arctic vertebrates. Bay population has given us some information on • New interspecific interactions will appear the maximum ice-free periods that polar bears can in Arctic communities—for example, be- tolerate, though the precise length of this period tween current competitors, predator–prey, will depend on the productivity in each area and or parasite–host arrangements of species—

Ann. N.Y. Acad. Sci. 1249 (2012) 166–190 c 2012 New York Academy of Sciences. 183 Climate change impacts on Arctic vertebrates Gilg et al.

with highly unpredictable cascading changes, is that they will undergo dramatic changes in the including feedbacks, in the dynamics of pop- coming years and decades. But any precise, spe- ulations and ultimately in the functioning cific prediction of their future state, even at the of these modified ecosystems. Due to these circumpolar scale, remains highly speculative given complex relations, even small changes in cli- our currently limited knowledge and the complex- mate can potentially lead to dramatic ecologi- ity of the processes involved. There is even some cal changes—for example, top-down regulated doubt about the widespread claim that Arctic species populations could well become bottom-up reg- are more sensitive to climate change impacts than ulated in some cases or vice versa. other species; some recent studies have suggested • Many of these ecological changes that are likely that they might actually be more resilient to climate to occur in the coming decades are nonlin- change, based on the fact that they have already un- ear, both in slope and intensity, and some can dergone more dramatic changes in the recent past reach tipping points. Small differences in envi- than species from other biomes.221 Given all the ronmental conditions can lead to very different doubts and major knowledge gaps, a conservative impacts between otherwise similar populations approach to mitigation policies is warranted at this or regions. time.218 • Our current knowledge of the impacts of cli- mate change on Arctic vertebrates is hampered Acknowledgments by major knowledge gaps in the ecology of We are grateful to the Conseil Regional´ de Bour- the species—for example, the winter period gogne and the French Polar Institute (IPEV) for or on the nonbreeding grounds for migratory its support to the project “1036-Interactions” (to species—and does not generally consider other OG, JM and LB) and to the latter for its support anthropogenic impacts—for example, see sec- to the project “388-Adaclim” (to JF and DG). Cli- tion “Subsidies.” mate change research in Norway has been funded largely by the Norwegian Research Council’s IPY How climate change will impact peoples through and NORKLIMA research programs. Some of the changes in the occurrence of Arctic vertebrates is researches reviewed herein have also been supported a question that we did not implicitly address in by the Norwegian Polar Institute. this review. However, from most of our exam- ples, one can ascertain that Arctic peoples depend- Conflicts of interest ing on traditional lifestyles will also be strongly The authors declare no conflicts of interest. impacted. Impacts on reindeer distribution, espe- cially in North America, will deeply impact the References economy and the culture of some Arctic and sub- Arctic peoples. Changes in fish, marine mammal, 1. Walther, G.-R. et al. 2002. Ecological responses to recent and seabird availability, central species in the econ- climate change. Nature, 416: 389–395. omy and culture of many Arctic peoples, will also 2. Parmesan, C. 2006. Ecological and evolutionary responses impact their societies and will force them to ad- to recent climate change. Ann. Rev. Ecol. Evol. Syst. 37: 637– 669. just their relationship with their environment and 3. IPCC. 2007. Climate Change 2007. Synthesis report. IPCC, perhaps adopt new environmental and manage- Valencia. ment policies.219,220 Most of the examples discussed 4. Vibe, C. 1967. Arctic animals in relation to climatic fluctu- in our review actually have cascading impacts on ations. Meddelelser om Grønland 170: 1–227. peoples. 5. Barber, D.G. & J. Iacozza. 2004. Historical analysis of sea ice conditions in M’Clintock Channel and the Gulf of Boothia, Despite the uncertainties associated to the many Nunavut: implications for ringed seal and polar bear habi- empirical and theoretical works available in the lit- tat. Arctic 57: 1–14. erature forecasting the fate of Arctic vertebrates, 6. ACIA. 2005. Arctic Climate Impact Assessment. Cambridge their future is at risk, especially the Arctic endemic University Press, Cambridge. species, which are highly adapted to survive in harsh 7. Overland, J.E. & M.Y.Wang. 2010. Large-scale atmospheric circulation changes are associated with the recent loss of Arctic environments that have been restrictive to Arctic sea ice. Tellus Series a-Dyn. Meteorol. Oceanogr. 62: other species. What can be taken for granted at least 1–9.

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