The Arctic ecosystem: A canary in the coal mine for global multiple stressors

The Arctic was previously considered a last frontier for ecosystems unimpacted by human activity. However, scientific evidence has increasingly demonstrated that the Arctic is at risk from various anthropogenic stressors, including environmental pollution. Environmental pollutants were identified in the Arctic several decades ago, and are still of concern for Arctic wildlife and indigenous peoples even though they have been subject to first national and then international regulation (Arctic Monitoring and Assessment Programme 2018). In addition, new chemicals and substitutes for banned chemicals continue to enter use in society, and a number of these have been identified as chemicals of emerging Arctic concern (CEAC; Arctic Monitoring and Assessment Programme 2017). Most persistent organic environmental pollutants and CEACs reach the Arctic via long-range transport (Arctic Monitoring and Assessment Programme 2018), although some have local sources (Arctic Monitoring and Assessment Programme 2017). Recently, more than 1000 time-series of contaminants from the Arctic were summarized (Rigét et al. 2019). For many legacy contaminants that have been subject to regulation (such as polychlorinated biphenyls, whose main route to the Arctic is long-range transport), the temporal trends are generally decreasing. The temporal trends of CEACs and of contaminants with some local sources (such as long-chain perfluoroalkyl carboxylic acids and hexabromocyclododecane) are generally increasing. Thus, the Arctic not only accumulates globally transported environmental contaminants, it also responds to regional and international measures to ban or control contaminants. Good examples are polybrominated diphenyl ethers and perfluorooctanesulfonic acid, whose levels increased until the early 2000s followed by a rapid decline (Rigét et al. 2019). In fact, data on environmental pollutants from the Arctic are used for monitoring the effectiveness of regional and global regulatory actions, such as the Global Monitoring Plan under the Stockholm Convention on Persistent Organic Pollutants (POPs; 2001). Also, when inclusion under the Stockholm Convention is considered, the presence of new contaminants in the Arctic with no local sources is used as an indication of high persistence and the potential for long-range transport, as specified in the Convention's screening criteria in Annex D. However, despite declining levels of legacy POPs, hundreds to thousands of chemicals are in commerce globally that are predicted to have long-range transport and persistence properties similar to some of the legacy POPs, and effects of contaminants in Arctic wildlife are documented at multiple levels of biological organization, with top predators being at particular risk due to biomagnification (Arctic Monitoring and Assessment Programme 2018). The negative effects in apex predators are often associated with highly persistent chemicals that will continue to pollute the Arctic and other parts of our planet for decades to come (even though some of them are regulated). Ecosystems at high latitudes such as the Arctic have adapted to the strong seasonality by using lipids as an energy buffer. Consequently, lipid-soluble contaminants are prone to accumulate, distribute, and transfer among animals, across trophic levels, generations, and ecosystems, together with the transfer of energy (lipids). Even near the base of the marine food web, Arctic copepods have been shown to accumulate organic pollutants, with negative impacts including reduced feeding, winter survival, and lipid mobilization (Toxværd et al. 2018). Documenting effects in wildlife due to specific contaminants is challenging, and it is not always possible to identify the “smoking gun”; in addition to exposure to a cocktail of pollutants, wildlife is increasingly subjected to other stressors to the ecosystems, some of which may also affect the potency of the pollutants on the ecosystem. Other stressors to the Arctic ecosystem include climate change and ocean acidification, risk of disturbance due to increased traffic and tourism, litter and microplastics, fishing and hunting pressure, petroleum exploration, food availability, oxygen depletion, and habitat destruction. Most studies targeting environmental pollution in combination with other stressors usually address climate change parameters, for example, temperature increase or drought. Climate change is occurring most rapidly in Polar Regions, and the magnitude of change is greater than currently experienced in other parts of the world. The Arctic thus functions as a “canary in the coal mine” with respect to direct and indirect responses induced by climate change. Climate change has resulted in “borealization” of the Arctic, with increasing warming and influx of Atlantic water (Fossheim et al. 2015). Not only does borealization affect physical conditions (such as sea temperature and sea ice distribution, age and, thickness), it also alters food-web structures and function, as southern species expand their northward boundaries. The overall effect of climate change on Arctic ecosystem responses to pollution occurrence, food-web accumulation, and effects is unknown, and the direct and indirect responses induced by climate change can moderate or intensify effects of environmental pollution and other Arctic stressors, both abiotic (such as ocean acidification) and biological (such as decreased food availability or increased predation). As an example, polar bears (Ursus maritimus) show increased stress due to deceasing sea ice as a consequence of climate change (Arctic Monitoring and Assessment Programme 2018). Sea ice is the main hunting area for polar bears, and this loss of habitat is thus linked to decrease in food availability. Stress responses in the polar bears under these conditions are reinforced by dietary exposure to pollutants, many of which biomagnify in the food webs with polar bears as the apex predator (Figure 1). As another example of response to multiple stressors, a recent modeling study of the Arctic-breeding common eider duck (Somateria mollissima) showed that for pollution to be a significant stressor alone, the exposures need to be unrealistically high (Bårdsen et al. 2018). However, when pollution occurs in concert with other stressors (climate change and predation in this example), adverse effects and population declines were predicted at low pollutant levels, and also at slightly lower temperatures compared with the present-day situation. If these data are extrapolated to other species, severe population declines could be expected for Arctic wildlife at realistic levels of pollution in combination with temperature increase, even at a temperature rise lower than the 1.5 °C global increase threshold predicted by the Intergovernmental Panel on Climate Change (2018). Studies including other stressors in combination with environmental pollution, such as risk of predation, can show surprising responses and potencies of stressors (Lode et al. 2018). Based on our current knowledgebase, and with the increasing footprints from human activity (such as petroleum exploration, fishing, shipping, and tourism), the Arctic provides an excellent platform for future studies on these stressors in concert with climate change and environmental pollution. It is now time for increased efforts to expand our research with the aim of including other stressors, to ensure a more realistic understanding of nature's responses to multiple stressors and to reduce our impact in the Anthropocene. The present study is part of the University of Oslo, Department of Bioscience project Life History under Multiple Stressors, and The Research Council of Norway projects 276730 Nansen Legacy and 280843 Effects of Climate Change in a Multiple Stress Multispecies Perspective. Many thanks to D. Muir and S. Wilson for valuable comments, and to D. Hitchcock for proofreading.