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When noise becomes the signal: Chemical contamination of aquatic ecosystems under a changing climate
Marine Pollution Bulletin 60 (2010) 1633–1635
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Editorial
When noise becomes the signal: Chemical contamination of aquatic ecosystems under a changing climate
Two major phenomena mark the Anthropocene: chemical contamination of air, water, soil and the biosphere, and global climate change (Crutzen, 2002). An enormous scientific effort has reached the consensus that a significant component of climate variability and change can be attributed to storing greenhouse gases in the atmosphere (IPCC, 2007) and ocean (Doney et al., 2009). But, until recently, almost no attention has been paid to the collateral effect of climate change on chemical contaminants stored in or entering the environment (Macdonald et al., 2005; Outridge et al., 2008). Evidence is now emerging that climate change alters storage, transformation, transport pathways, eco-dynamics and bio-uptake of contaminants (Outridge et al., 2007; Loseto et al., 2008; Becker et al., 2009; Gaden et al., 2009; Carrie et al., 2010). Here, we propose a new paradigm that during a rapidly changing climate, emission control of some contaminants may be followed by long delays, on the order of decades or longer, before ensuing reduction is seen in food-web contaminant levels. Delayed response would occur particularly for those chemicals that are prone to biomagnification in food webs and are archived in large quantities in reservoirs with long residence times, such as global soils and oceans. This response lag makes it all the more urgent to reduce or halt any further loading of certain types of chemicals into these key environmental reservoirs. Regulators must also accept that benefits from emission reductions will not been seen immediately at the ecosystem level. Although our remarks are focused explicitly on aquatic systems, much of our discussion is applicable also to terrestrial ecosystems. There is no doubt that human activities have dispersed chemical contaminants, some of which have natural cycles (e.g., mercury (Hg)) while others do not occur naturally (e.g., polychlorinated biphenyls (PCBs) and dichlorodiphenyltrichloroethane (DDT)). Following the addition of a bioaccumulating contaminant, a rapid increase has frequently been observed in biological tissue concentrations in laboratory, mesocosm, or whole-ecosystem studies (e.g., Harris et al., 2007). Exponential increases have been observed for some chemicals even in locations remote from sources, such as the Arctic (e.g., Ikonomou et al., 2002; Dietz et al., 2009). A rapid dose-response during the loading phase of a chemical offers hope that a similarly rapid response would follow emission control and, indeed, after wide-spread control on production of some chemicals such as PCBs in the 1970s, rapid reductions were initially observed in many species of aquatic biota (Braune et al., 2005). We propose here that as emissions are increasingly placed under control, the global cycle of a contaminant, particularly those 0025-326X/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2010.05.018
few that biomagnify, passes a turning point beyond which biogeochemical processes emerge as the major driver for bioaccumulation: from that point onwards, variations in biotic contaminant levels cease to reflect variations in emissions. A classic example is shown by PCBs: after the initial rapid decline in top marine predators, PCBs have stubbornly remained at high levels (Hickie et al., 2007). Signs of a shift from emission-driven trends to biogeochemical process-driven variability for persistent organic pollutants (POPs) and Hg are perhaps most profound in the Arctic, where melting of ice and thawing of permafrost have resulted in dramatic changes in biogeochemical cycling and ecosystem structure and function (Macdonald et al., 2005; McKinney et al., 2009; Post et al., 2009). Mercury provides a particularly pertinent example. Tropospheric Hg concentrations in the Arctic have been constant or declining since the 1970s (Temme et al., 2007; Fain et al., 2009; Li et al., 2009). Meanwhile, Hg concentrations in Arctic predators have exhibited a remarkable degree of spatial and temporal variation: Hg has decreased in female beluga muscle tissue from western Hudson Bay (Gaden and Stern, 2010), increased in an Arctic freshwater fish in the Mackenzie basin (Carrie et al., 2010) and in the majority of marine mammals species from the west Greenland Arctic (AMAP, 2005), and fluctuated greatly without a persistent trend in beluga muscle and liver tissues from Beaufort Sea (Lockhart et al., 2005). Much of the time tissue concentrations of Hg in these species have exceeded human consumption guidelines. These biological patterns can in no way be explained by emission histories or atmospheric loadings. The single most important parameter determining how emission control will be reflected in biotic burdens is residence time of a chemical in large environmental reservoirs. Residence time is a function of the size of the reservoir and the loading or removal rates of the chemical. When the accumulated mass of the contaminant in the reservoir becomes large enough relative to the emission-driven loading rate, the internal biogeochemical processes that control the permanent removal (e.g., degradation and burial) or the recycling of the contaminant into the biosphere increasingly become the determining steps in bioaccumulation. Biogeochemical processes operating on the chemicals contained in these large reservoirs affect contaminant bioaccumulation in at least four major ways including: (1) contaminant transport by, or exchange among, various reservoirs (e.g., cryosphere, water, sediment, soil, and rhizosphere); (2) transformation of the contaminant among different chemical forms with various degrees of bioavailability and toxicity (e.g., methylation of Hg); (3) degradation (e.g., photolysis, metabo-
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Editorial / Marine Pollution Bulletin 60 (2010) 1633–1635
lization); and (4) structure and dynamics of food webs (e.g., number of trophic levels and foraging strategy). All of these pathways are inherently sensitive to climate variability and change. Prior to the Anthropocene, the cycling of chemical contaminants was relatively low (e.g., Hg) or completely absent (e.g., DDT), and likewise the concentration in the biosphere (‘‘baseline phase” in Fig. 1). Although bioaccumulation would have operated just as it does now, variation in biota would have been produced entirely by variation in the internal biogeochemical processes (shown in Fig. 1 as sine-wave ‘‘noise”). Examples of such baseline behaviour can be found in archived biological tissues (Dietz et al., 2009). At the onset of the Anthropocene, the ‘‘pristine” environment responded to emissions from human activities (‘‘source-driven phase” in Fig. 1). Rapid response in remote areas would indicate atmospheric-transport, which readily disseminates semi-volatile chemicals, while ocean transport would exhibit a delay of perhaps decades. Tissue concentrations would increase rapidly due to increasing exposure and uptake of these chemicals from a small but growing environmental reservoir. With time, variation or changes in internal biogeochemical processes would become more important than during the baseline phase, but their effect on contaminant bioaccumulation would remain secondary to rapidly increasing emissions and loadings of global reservoirs. This source-driven phase has operated since the beginning of the Anthropocene for Hg, and since the 1930s for many POPs up until controls for some of the latter were instituted commencing in the 1970s (Dietz et al., 2009). For Hg, controls have been initiated in Europe and North America, but coal-fired power plants in many countries contribute increasing amounts of Hg to the atmosphere (Streets et al., 2009). Once system reservoirs have accumulated sufficient chemical, say at a critical influx (Fc), additional increases in influx become secondary to the recycling of the chemical from the large ‘‘inertia” of the environmental reservoir created by years of loading. Bioaccumulation then draws predominantly on the stored chemical reservoir, which is operated on by the internal biogeochemical processes (i.e., the ‘‘process-driven phase” in Fig. 1). Throughout all three phases, biogeochemical cycling determines the speciation, bioavailability, and uptake of the contaminant, but it is in the latter phase that these processes emerge to create a variability that is large enough to obscure down-turning trends, at least at the decadal scale if not longer (Fig. 1). We find ourselves in this process-driven phase presently for chemicals like Hg and PCBs. In the case of Hg, noise from the processes operating on reservoirs has become the main signal in the ‘‘trend” data for Hg in Arctic marine animals during the past 30 years (AMAP, 2005; Lockhart et al., 2005; Gaden et al., 2009). A similar circumstance may emerge in the coming decade for DDT in the eastern Arctic (Stemmler and Lammel, 2009). The critical influx (Fc in Fig. 1) varies among chemicals depending on physicochemical properties, persistence, reservoir residence time, and potential for biomagnification. For instance, anthropogenic activities have contributed both lead (Pb) and Hg to Arctic marine ecosystems. Declines in Pb have been termed a success story (Macdonald et al., 2000), but Hg remains stubbornly at levels of concern. There are crucial differences between these trace metals (volatility, residence time in water, chemical forms, methylation, toxicity and potential to biomagnify) that set them apart during the process-driven phase. In the perspective presented here, Hg has a smaller Fc than Pb. What makes Hg particularly sensitive are the methylation and biomagnification processes: any change in the production of methylmercury (e.g., by changes in temperature or organic carbon influx) or the route of uptake (e.g., by changes in the food-web structure) results in major changes in tissue levels in aquatic predators.
Fig. 1. Change of the paradigms in driving bioaccumulation of chemicals in the environment. Fc: critical influx.
Furthermore, Fc also depends on ecosystem characteristics including environmental conditions, contaminant residence time within the local environment, and complexity of food webs. In the case of polar and alpine environments, an archive from former times has been stored in the ‘‘freezer” (i.e., permanent snow and ice), and this archive is now poised to be set again in motion with warming (Macdonald et al., 2005; Gieisz et al., 2008). We propose that a shift from source-driven to process-driven bioaccumulation in remote areas like the Arctic may be a bellwether of changes to come at lower latitudes. Even though the immediate benefit of downward trends in top predators, including humans, may not be realized for biomagnifying contaminants that have accrued large inventories in environmental reservoirs, the view put forward here underscores the importance of controlling sources for precisely these chemicals as early as possible. Acknowledgement This Viewpoint article is based on extensive field and laboratory studies that were funded primarily by the ArcticNet, the Circumpolar Flaw Lead (CFL) System Studies (an International Polar Year project), the Natural Science and Engineering Research Council (NSERC) of Canada, and the Northern Contaminants Program (NCP) of Canada. References AMAP, 2005. AMAP Assessment 2002: Heavy Metals in the Arctic. Arctic Monitoring and Assessment Programme, Oslo. Becker, S., Halsall, C.J., Tych, W., Kallenborn, R., Schlabach, M., Manø, S., 2009. Changing sources and environmental factors reduce the rates of decline of organochlorine pesticides in the Arctic atmosphere. Atmospheric Chemistry and Physics Discussions 9, 515–540. Braune, B.M., Outridge, P.M., Fisk, A.T., Muir, D.C.G., Helm, P.A., Hobbs, K., Hoekstra, P.F., Kuzyk, Z.A., Kwan, M., Letcher, R.J., Lockhart, W.L., Norstrom, R.J., Stern, G.A., Stirling, I., 2005. Persistent organic pollutants and mercury in marine biota of the Canadian Arctic: an overview of spatial and temporal trends. Science of the Total Environment 351, 4–56. Carrie, J., Wang, F., Sanei, H., Macdonald, R.W., Outridge, P.M., Stern, G., 2010. Increasing contaminant burdens in an Arctic fish, burbot (Lota lota), in a warming climate. Environmental Science and Technology 44, 316–322. Crutzen, P.J., 2002. Geology of mankind. Nature 415, 23. Dietz, R., Outridge, P.M., Hobson, K.A., 2009. Anthropogenic contributions to mercury levels in present-day Arctic animals – a review. Science of the Total Environment 407, 6120–6131. Doney, S.C., Fabry, V.J., Feely, R.A., Kleypas, J.A., 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169–192. Fain, X., Ferrari, C.P., Dommergue, A., Albert, M.R., Battle, M., Severinghaus, J., Arnaud, L., Barnola, J.M., Cairns, W., Barbante, C., Boutron, C., 2009. Polar firn air reveals large-scale impact of anthropogenic mercury emissions during the 1970s. Proceedings of the National Academy of Sciences of the USA 106, 16114– 16119.
Editorial / Marine Pollution Bulletin 60 (2010) 1633–1635 Gaden, A., Stern, G.A., 2010. Temporal trends in beluga, narwhal and walrus mercury levels. Links to climate change. In: Ferguson, S.H., Loseto, L.L., Mallory, M.L. (Eds.), A Little Less Arctic: Top Predators in the World’s Largest Northern Inland Sea, Hudson Bay. Springer, pp. 197–216. Gaden, A., Ferguson, S.H., Harwood, L., Melling, H., Stern, G.A., 2009. Mercury trends in ringed seals (Phoca hispida) from the western Canadian Arctic since 1973: associations with length of ice-free season. Environmental Science and Technology 43, 3646–3651. Gieisz, H.N., Dickhut, R.M., Chochran, M.A., Fraser, W.R., Ducklow, H.W., 2008. Melting glaciers: a probable source of DDT to the Antarctic marine ecosystem. Environmental Science and Technology 42, 3958–3962. Harris, R.C., Rudd, J.W.M., Amyot, M., Babiarz, C.L., Beaty, K.G., Blanchfield, P.J., Bodaly, R.A., Branfireun, B.A., Gilmour, C.C., Graydon, J.A., Heyes, A., Hintelmann, H., Hurley, J.P., Kelly, C.A., Krabbenhoft, D.P., Lindberg, S.E., Mason, R.P., Paterson, M.J., Podemski, C.L., Robinson, A., Sandilands, K.A., Southworth, G.R., Louis, V.L.S., Tate, M.T., 2007. Whole-ecosystem study shows rapid fish-mercury response to changes in mercury deposition. Proceedings of the National Academy of Sciences of the USA 104, 16586–16591. Hickie, B.E., Ross, P.S., Macdonald, R.W., Ford, J.K.B., 2007. Killer whales (Orcinus orca) face protracted health risks associated with lifetime exposure to PCBs. Environmental Science and Technology 41, 6613–6619. Ikonomou, M.G., Rayne, S., Addison, R.F., 2002. Exponential increases of the brominated flame retardants, polybrominated diphenyl ethers, in the Canadian arctic from 1981 to 2000. Environmental Science and Technology 36, 1886–1892. IPCC, 2007. Climate Change 2007 – The Physical Science Basis. Cambridge University Press. Li, C., Cornett, J., Willie, S., Lam, J., 2009. Mercury in Arctic air: the long-term trend. Science of the Total Environment 407, 2756–2759. Lockhart, W.L., Stern, G.A., Wagemann, R., Hunt, R.V., Metner, D.A., DeLaronde, J., Dunn, B., Stewart, R.E.A., Hyatt, C.K., Harwood, L., Mount, K., 2005. Concentrations of mercury in tissues of beluga whales (Delphinapterus leucas) from several communities in the Canadian Arctic from 1981 to 2002. Science of the Total Environment 351/352, 391–412. Loseto, L.L., Stern, G.A., Ferguson, S.H., 2008. Size and biomagnification: how habitat selection explains beluga mercury levels. Environmental Science and Technology 42, 3982–3988. Macdonald, R.W., Barrie, L.A., Bidleman, T.F., Diamond, M.L., Gregor, D.J., Semkin, R.G., Strachan, W.M.J., Li, Y.F., Wania, F., Alaee, M., Alexeeva, L.B., Backus, S.M., Bailey, R., Bewers, J.M., Gobeil, C., Halsall, C.J., Harner, T., Hoff, J.T., Jantunen, L.M.M., Lockhart, W.L., Mackay, D., Muir, D.C.G., Pudykiewicz, J., Reimer, K.J., Smith, J.N., Stern, G.A., Schroeder, W.H., Wagemann, R., Yunker, M.B., 2000. Contaminants in the Canadian Arctic: 5 years of progress in understanding sources, occurrence and pathways. Science of the Total Environment 254, 93– 234. Macdonald, R.W., Harner, T., Fyfe, J., 2005. Recent climate change in the Arctic and its impact on contaminant pathways and interpretation of temporal trend data. Science of the Total Environment 342, 5–86. McKinney, M.A., Peacock, E., Letcher, R.J., 2009. Sea ice-associated diet change increases the levels of chlorinated and brominated contaminants in polar bears. Environmental Science and Technology 43, 4334–4339. Outridge, P.M., Sanei, H., Stern, G.A., Hamilton, P.B., Goodarzi, F., 2007. Evidence for control of mercury accumulation rates in Canadian high arctic lake sediments by variations in aquatic primary productivity. Environmental Science and Technology 41, 5259–5265. Outridge, P.M., Macdonald, R.W., Wang, F., Stern, G.A., Dastoor, A.P., 2008. A mass balance inventory of mercury in the Arctic Ocean. Environmental Chemistry 5, 89–111. Post, E., Forchhammer, M.C., Bret-Harte, M.S., Callaghan, T.V., Christensen, T.R., Elberling, B., Fox, A.D., Gilg, O., Hik, D.S., Hoye, T.T., Ims, R.A., Jeppesen, E., Klein, D.R., Madsen, J., McGuire, A.D., Rysgaard, S., Schindler, D.E., Stirling, I., Tamstorf, M.P., Tyler, N.J.C., van der Wal, R., Welker, J., Wookey, P.A., Schmidt, N.M.,
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Aastrup, 2009. Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358. Stemmler, I., Lammel, G., 2009. Cycling of DDT in the global environment 1950– 2002: World Ocean returns the pollutant. Geophysics Research Letters 36, L24602. Streets, D.G., Zhang, Q., Wu, Y., 2009. Projections of global mercury emissions in 2050. Environmental Science and Technology 43, 2983–2988. Temme, C., Blanchard, P., Steffen, A., Banic, C., Beauchamp, S., Poissant, L., Tordon, R., Wiens, B., 2007. Trend, seasonal and multivariate analysis study of total gaseous mercury data from the Canadian atmospheric mercury measurement network (CAMNet). Atmospheric Environment 41, 5423–5441.
Feiyue Wang Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Department of Chemistry, University of Manitoba, Winnipeg, MB, Canada R3T 2N2. Tel.: +1 204 474 6250 E-mail address: [email protected] Robie W. Macdonald Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Institute of Ocean Sciences, Department of Fisheries and Oceans, P.O. Box 6000, Sidney, BC, Canada V8L 4B2 Gary A. Stern Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Freshwater Institute, Department of Fisheries and Oceans, 501 University Crescent, Winnipeg, MB, Canada R3T 2N6 Peter M. Outridge Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Geological Survey of Canada, 601 Booth Street, Ottawa, ON, Canada K1A 0E8
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Editorial
When noise becomes the signal: Chemical contamination of aquatic ecosystems under a changing climate
Two major phenomena mark the Anthropocene: chemical contamination of air, water, soil and the biosphere, and global climate change (Crutzen, 2002). An enormous scientific effort has reached the consensus that a significant component of climate variability and change can be attributed to storing greenhouse gases in the atmosphere (IPCC, 2007) and ocean (Doney et al., 2009). But, until recently, almost no attention has been paid to the collateral effect of climate change on chemical contaminants stored in or entering the environment (Macdonald et al., 2005; Outridge et al., 2008). Evidence is now emerging that climate change alters storage, transformation, transport pathways, eco-dynamics and bio-uptake of contaminants (Outridge et al., 2007; Loseto et al., 2008; Becker et al., 2009; Gaden et al., 2009; Carrie et al., 2010). Here, we propose a new paradigm that during a rapidly changing climate, emission control of some contaminants may be followed by long delays, on the order of decades or longer, before ensuing reduction is seen in food-web contaminant levels. Delayed response would occur particularly for those chemicals that are prone to biomagnification in food webs and are archived in large quantities in reservoirs with long residence times, such as global soils and oceans. This response lag makes it all the more urgent to reduce or halt any further loading of certain types of chemicals into these key environmental reservoirs. Regulators must also accept that benefits from emission reductions will not been seen immediately at the ecosystem level. Although our remarks are focused explicitly on aquatic systems, much of our discussion is applicable also to terrestrial ecosystems. There is no doubt that human activities have dispersed chemical contaminants, some of which have natural cycles (e.g., mercury (Hg)) while others do not occur naturally (e.g., polychlorinated biphenyls (PCBs) and dichlorodiphenyltrichloroethane (DDT)). Following the addition of a bioaccumulating contaminant, a rapid increase has frequently been observed in biological tissue concentrations in laboratory, mesocosm, or whole-ecosystem studies (e.g., Harris et al., 2007). Exponential increases have been observed for some chemicals even in locations remote from sources, such as the Arctic (e.g., Ikonomou et al., 2002; Dietz et al., 2009). A rapid dose-response during the loading phase of a chemical offers hope that a similarly rapid response would follow emission control and, indeed, after wide-spread control on production of some chemicals such as PCBs in the 1970s, rapid reductions were initially observed in many species of aquatic biota (Braune et al., 2005). We propose here that as emissions are increasingly placed under control, the global cycle of a contaminant, particularly those 0025-326X/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2010.05.018
few that biomagnify, passes a turning point beyond which biogeochemical processes emerge as the major driver for bioaccumulation: from that point onwards, variations in biotic contaminant levels cease to reflect variations in emissions. A classic example is shown by PCBs: after the initial rapid decline in top marine predators, PCBs have stubbornly remained at high levels (Hickie et al., 2007). Signs of a shift from emission-driven trends to biogeochemical process-driven variability for persistent organic pollutants (POPs) and Hg are perhaps most profound in the Arctic, where melting of ice and thawing of permafrost have resulted in dramatic changes in biogeochemical cycling and ecosystem structure and function (Macdonald et al., 2005; McKinney et al., 2009; Post et al., 2009). Mercury provides a particularly pertinent example. Tropospheric Hg concentrations in the Arctic have been constant or declining since the 1970s (Temme et al., 2007; Fain et al., 2009; Li et al., 2009). Meanwhile, Hg concentrations in Arctic predators have exhibited a remarkable degree of spatial and temporal variation: Hg has decreased in female beluga muscle tissue from western Hudson Bay (Gaden and Stern, 2010), increased in an Arctic freshwater fish in the Mackenzie basin (Carrie et al., 2010) and in the majority of marine mammals species from the west Greenland Arctic (AMAP, 2005), and fluctuated greatly without a persistent trend in beluga muscle and liver tissues from Beaufort Sea (Lockhart et al., 2005). Much of the time tissue concentrations of Hg in these species have exceeded human consumption guidelines. These biological patterns can in no way be explained by emission histories or atmospheric loadings. The single most important parameter determining how emission control will be reflected in biotic burdens is residence time of a chemical in large environmental reservoirs. Residence time is a function of the size of the reservoir and the loading or removal rates of the chemical. When the accumulated mass of the contaminant in the reservoir becomes large enough relative to the emission-driven loading rate, the internal biogeochemical processes that control the permanent removal (e.g., degradation and burial) or the recycling of the contaminant into the biosphere increasingly become the determining steps in bioaccumulation. Biogeochemical processes operating on the chemicals contained in these large reservoirs affect contaminant bioaccumulation in at least four major ways including: (1) contaminant transport by, or exchange among, various reservoirs (e.g., cryosphere, water, sediment, soil, and rhizosphere); (2) transformation of the contaminant among different chemical forms with various degrees of bioavailability and toxicity (e.g., methylation of Hg); (3) degradation (e.g., photolysis, metabo-
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Editorial / Marine Pollution Bulletin 60 (2010) 1633–1635
lization); and (4) structure and dynamics of food webs (e.g., number of trophic levels and foraging strategy). All of these pathways are inherently sensitive to climate variability and change. Prior to the Anthropocene, the cycling of chemical contaminants was relatively low (e.g., Hg) or completely absent (e.g., DDT), and likewise the concentration in the biosphere (‘‘baseline phase” in Fig. 1). Although bioaccumulation would have operated just as it does now, variation in biota would have been produced entirely by variation in the internal biogeochemical processes (shown in Fig. 1 as sine-wave ‘‘noise”). Examples of such baseline behaviour can be found in archived biological tissues (Dietz et al., 2009). At the onset of the Anthropocene, the ‘‘pristine” environment responded to emissions from human activities (‘‘source-driven phase” in Fig. 1). Rapid response in remote areas would indicate atmospheric-transport, which readily disseminates semi-volatile chemicals, while ocean transport would exhibit a delay of perhaps decades. Tissue concentrations would increase rapidly due to increasing exposure and uptake of these chemicals from a small but growing environmental reservoir. With time, variation or changes in internal biogeochemical processes would become more important than during the baseline phase, but their effect on contaminant bioaccumulation would remain secondary to rapidly increasing emissions and loadings of global reservoirs. This source-driven phase has operated since the beginning of the Anthropocene for Hg, and since the 1930s for many POPs up until controls for some of the latter were instituted commencing in the 1970s (Dietz et al., 2009). For Hg, controls have been initiated in Europe and North America, but coal-fired power plants in many countries contribute increasing amounts of Hg to the atmosphere (Streets et al., 2009). Once system reservoirs have accumulated sufficient chemical, say at a critical influx (Fc), additional increases in influx become secondary to the recycling of the chemical from the large ‘‘inertia” of the environmental reservoir created by years of loading. Bioaccumulation then draws predominantly on the stored chemical reservoir, which is operated on by the internal biogeochemical processes (i.e., the ‘‘process-driven phase” in Fig. 1). Throughout all three phases, biogeochemical cycling determines the speciation, bioavailability, and uptake of the contaminant, but it is in the latter phase that these processes emerge to create a variability that is large enough to obscure down-turning trends, at least at the decadal scale if not longer (Fig. 1). We find ourselves in this process-driven phase presently for chemicals like Hg and PCBs. In the case of Hg, noise from the processes operating on reservoirs has become the main signal in the ‘‘trend” data for Hg in Arctic marine animals during the past 30 years (AMAP, 2005; Lockhart et al., 2005; Gaden et al., 2009). A similar circumstance may emerge in the coming decade for DDT in the eastern Arctic (Stemmler and Lammel, 2009). The critical influx (Fc in Fig. 1) varies among chemicals depending on physicochemical properties, persistence, reservoir residence time, and potential for biomagnification. For instance, anthropogenic activities have contributed both lead (Pb) and Hg to Arctic marine ecosystems. Declines in Pb have been termed a success story (Macdonald et al., 2000), but Hg remains stubbornly at levels of concern. There are crucial differences between these trace metals (volatility, residence time in water, chemical forms, methylation, toxicity and potential to biomagnify) that set them apart during the process-driven phase. In the perspective presented here, Hg has a smaller Fc than Pb. What makes Hg particularly sensitive are the methylation and biomagnification processes: any change in the production of methylmercury (e.g., by changes in temperature or organic carbon influx) or the route of uptake (e.g., by changes in the food-web structure) results in major changes in tissue levels in aquatic predators.
Fig. 1. Change of the paradigms in driving bioaccumulation of chemicals in the environment. Fc: critical influx.
Furthermore, Fc also depends on ecosystem characteristics including environmental conditions, contaminant residence time within the local environment, and complexity of food webs. In the case of polar and alpine environments, an archive from former times has been stored in the ‘‘freezer” (i.e., permanent snow and ice), and this archive is now poised to be set again in motion with warming (Macdonald et al., 2005; Gieisz et al., 2008). We propose that a shift from source-driven to process-driven bioaccumulation in remote areas like the Arctic may be a bellwether of changes to come at lower latitudes. Even though the immediate benefit of downward trends in top predators, including humans, may not be realized for biomagnifying contaminants that have accrued large inventories in environmental reservoirs, the view put forward here underscores the importance of controlling sources for precisely these chemicals as early as possible. Acknowledgement This Viewpoint article is based on extensive field and laboratory studies that were funded primarily by the ArcticNet, the Circumpolar Flaw Lead (CFL) System Studies (an International Polar Year project), the Natural Science and Engineering Research Council (NSERC) of Canada, and the Northern Contaminants Program (NCP) of Canada. References AMAP, 2005. AMAP Assessment 2002: Heavy Metals in the Arctic. Arctic Monitoring and Assessment Programme, Oslo. Becker, S., Halsall, C.J., Tych, W., Kallenborn, R., Schlabach, M., Manø, S., 2009. Changing sources and environmental factors reduce the rates of decline of organochlorine pesticides in the Arctic atmosphere. Atmospheric Chemistry and Physics Discussions 9, 515–540. Braune, B.M., Outridge, P.M., Fisk, A.T., Muir, D.C.G., Helm, P.A., Hobbs, K., Hoekstra, P.F., Kuzyk, Z.A., Kwan, M., Letcher, R.J., Lockhart, W.L., Norstrom, R.J., Stern, G.A., Stirling, I., 2005. Persistent organic pollutants and mercury in marine biota of the Canadian Arctic: an overview of spatial and temporal trends. Science of the Total Environment 351, 4–56. Carrie, J., Wang, F., Sanei, H., Macdonald, R.W., Outridge, P.M., Stern, G., 2010. Increasing contaminant burdens in an Arctic fish, burbot (Lota lota), in a warming climate. Environmental Science and Technology 44, 316–322. Crutzen, P.J., 2002. Geology of mankind. Nature 415, 23. Dietz, R., Outridge, P.M., Hobson, K.A., 2009. Anthropogenic contributions to mercury levels in present-day Arctic animals – a review. Science of the Total Environment 407, 6120–6131. Doney, S.C., Fabry, V.J., Feely, R.A., Kleypas, J.A., 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169–192. Fain, X., Ferrari, C.P., Dommergue, A., Albert, M.R., Battle, M., Severinghaus, J., Arnaud, L., Barnola, J.M., Cairns, W., Barbante, C., Boutron, C., 2009. Polar firn air reveals large-scale impact of anthropogenic mercury emissions during the 1970s. Proceedings of the National Academy of Sciences of the USA 106, 16114– 16119.
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Feiyue Wang Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Department of Chemistry, University of Manitoba, Winnipeg, MB, Canada R3T 2N2. Tel.: +1 204 474 6250 E-mail address: [email protected] Robie W. Macdonald Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Institute of Ocean Sciences, Department of Fisheries and Oceans, P.O. Box 6000, Sidney, BC, Canada V8L 4B2 Gary A. Stern Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Freshwater Institute, Department of Fisheries and Oceans, 501 University Crescent, Winnipeg, MB, Canada R3T 2N6 Peter M. Outridge Centre for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Geological Survey of Canada, 601 Booth Street, Ottawa, ON, Canada K1A 0E8