Context

1Several populations living in remote areas of the Americas depend upon small-scale fishing activities for meeting their protein needs. These populations comprise for example subsistence fishers from First Nations communities of the Canadian boreal forest and the Canadian Arctic, sports fishers frequently using the fish resource of lakes and rivers not far from their homes, and riparian communities settled on the shores of large watercourses in the Amazon. For these people, fish and/or marine mammals constitute irreplaceable components of daily meals, either in response to traditional values, limited availability of other protein sources and/or economic dependency. Many of these populations enjoy simple life styles, in harmony with the relatively pristine environments in which they evolve, far from direct industrial contamination point sources. Despite this fact, several scientific evidences prove that the health of these communities might be threatened by high levels of methylmercury (MeHg) in fish and marine mammal tissues.

2Fish eating communities are often not aware of the dangers related to MeHg, or even of its existence in their milieus. The sole concept of “contaminant” is frequently missing from First Nations regional languages and dialects. Moreover, the presence of mercury (Hg) in the global ecosystems is ubiquitous, following its emission to the atmosphere—mainly from coal combustion, waste incineration, ore refining or from natural sources such as volcanoes or wind erosion—its transport and diffuse deposition on lands and water plans, its transformation into MeHg occurring in wetlands and aquatic systems, and its accumulation throughout the aquatic food chain (ICMGP, 2006; Gbor et al., 2007, Munthe et al., 2007). In this context, it is difficult to properly inform and arm inhabitants from isolated communities about the Hg threat, especially since these people are usually not responsible for the pollution.

3The environmental and health impacts in remote ecosystems of global Hg cycling constitute a concrete example of environmental injustice and have focused the international attention on the following questions:

1. Does Hg accumulation in remote North American ecosystems have an impact on human health?

2. Can the extensive gold mining activities in remote tropical regions of South America constitute a potential time bomb, threatening the health of numerous riparian populations, far away downstream from gold extraction sites?

3. How could these situations evolve and what could be done to protect the health of fish eating populations?

4As a result, scientific efforts have provided a general picture of Hg pathways from the Brazilian tropics to the Canadian Arctic. This paper synthesizes the main pathways undertaken by Hg in its journey from skies to fishes through specific regional case studies and presents pieces of answers toward lessening exposure to MeHg through fish consumption endured by remote populations relying on local fish resources. These examples clearly demonstrate that, for a given ecosystem, the Hg loading is often not strictly correlated with the local/regional contamination of the biota by MeHg. In fact, the environmental characteristics and human uses of aquatic ecosystem, often dictate its overall response (or sensitivity) to various levels of Hg loadings. In turn, mercury contamination of the ecosystems, monitored by the accumulation of mercury in top predator fish species, can lead to health deteriorations. Related impacts on human health depend on the economic/social/traditional dependency of communities to the fish resource, on exposure to other persistent bio-accumulative contaminants and on metabolic ability to handle xenobiotics (defined here as the human vulnerability to Hg). These multiple parameters provide partial answers on how exposure to MeHg can be lessen in remote populations relying on local fish resources.

Exposure to methylmercury and human health

5The formal identification of the clinical symptoms induced by MeHg poisoning was made at the end of the 1950s, following an episode of wide scale environmental contamination that occurred in the city of Minamata, Kyūshū district, Japan. For more than 30 years, the Chisso Corporation, a chemical factory located in the middle of the city, dumped its untreated wastewaters in the Minamata Bay, including several tons of Hg, which was used as a catalyst for the production of acetaldehyde. The symptoms of MeHg intoxication include ataxia, numbness in the hands and feet, muscle weakness, narrowing of vision, loss of cognitive functions and coordination of movements (NRC 2000). Extreme exposure to MeHg in Minamata also provoked numerous cases of insanity, paralysis, coma and the death of more than 900 community members.

6With the exception of major disasters or spills, Hg usually does not produce dramatic immediate health effects, but slow insidious changes in biological functions, reflecting diminishing well-being and affecting the quality of life (Clarkson, 1990; NRC, 2000; Grandjean, 2007). Evidence of physiological changes associated with exposure to low dose of MeHg were reported by extensive studies carried out in the Brazilian Amazon (Lebel et al., 1996 and 1998, Mergler, 2002) and among children from the Faroe Islands (Grandjean et al., 1997; Murata et al., 1999; Sørensen et al., 1999, Weihe et al., 2003; Debes et al., 2006). These early health deteriorations include partial narrowing of the visual field, loss of manual dexterity, loss of sensitivity in hands and feet, partial loss of color perception, alteration of cognitive functions and learning deficiency at childhood (NRC 2000). Early health alterations constitute not only a warning for increased risk of eventual illness, but, more important, reflect diminished well-being and functional capacities. This can have dramatic effects in situation of self-sustained economy, particularly when coupled to poverty, malnutrition, poor living conditions, inadequate health care and schooling.

7Human exposure to MeHg in remote populations of the Americas derives primarily from the consumption of freshwater and marine fishes, or marine mammals, all important sources of many essential elements for these people and an integral part of their culture and economy (Wheatley and Paradis, 1996, Van Oostdam et al., 1999, Muckle et al., 2001; Mergler et al., 2007). In all cases, the extent of exposure to Hg greatly depends on the specific fish species and marine mammal consumption patterns. The fish species, size and consumption frequency are key parameters when it comes to determining the acceptable limits for steady-state exposure (ALSSE) to MeHg (e.g. 0.1 to 0.5 ug.kg^-1bw.day^-1). This is an important issue in aboriginal gill-net based fisheries, as well as in recreational—or economy-related fisheries which tend to target the larger specimens of piscivorous species, those usually bearing the highest Hg levels, for regular consumption. ALSSE can be exceeded by eating only two meal per month of northern pike (typical Hg level of 0,7 to 1,0 ppm) caught in Northern Québec, or by eating one single meal of beluga muscle (1,0 to 1,5 ppm Hg)—greatly praised by the Inuit communities. Let’s now look at the main pathways leading Hg, from atmospheric sources to fish and marine mammal tissues.

Mercury sources and cycling in Northern ecosystems

8It is widely admitted that, with the exception of specific geological features or local contaminant point sources, the most important source of Hg to Northern environments is the global atmospheric pool. Even though the atmospheric Hg loading is diffuse and occurs at low rates in these regions, numerous boreal and Arctic ecosystems can be described as Hg-sensitive environments because they efficiently: (1) transform the Hg atmospheric load into bioassimilable MeHg; and (2) biomagnify MeHg along food webs, yielding contaminant levels in top fish predator species and/ or marine mammals unsafe for regular human consumption. It is possible to distinguish between two major processes that drive the Hg burden from the atmosphere down to aquatic ecosystems. While airborne chemical reactions seem to dominate Hg deposition patterns in the Arctic (figure 1), land processes appear to be of greater importance in the boreal ecozone (figure 2).

Arctic environments: The Mercury Depletion Events

9The chemical speciation of Hg in the atmosphere is rather complex. One can distinguish between two main categories according to the oxidation state of the Hg molecules: Hg0 (or Gaseous Elemental Mercury—GEM) and HgII (or Reactive Gaseous Mercury—RGM) species. Several recent observations, made in the Arctic and sub-Arctic atmosphere, point to a cyclic depletion of GEM levels that corresponds with enrichment in RGM, which then also rapidly vanishes from the atmosphere. The most plausible explanation for this phenomenon, known as Mercury Depletion Events (MDE), is as follow:

10The periodic appearance of polar sunrise provokes the evaporation of bromine species from saltwater. Bromine then reacts with atmospheric ozone to form bromine oxide (BrO), which can transform GEM species into RGM, readily stripped from the atmosphere (Boudris et al., 2000; Ebinghaus et al., 2002, Skov et al., 2004; Lindberg et al., 2002):

11This process is thought to deposit between 90 to 450 tons Hg per year on Arctic and sub-Arctic environments (Poissant et al., 2008).

12The MDE have drawn much attention from the scientific community with over 200 papers published on the issue during the past decade (Poissant et al., 2008). Since the mechanisms behind the MDE were clearly identified, other studies demonstrated that the majority of the MDE- deposited Hg through MDE is evaporated back to the atmosphere under the form of GEM through the action of sunlight (Ariya et al., 2004; Skov et al., 2004; Lindberg et al., 2007; Poissant et al., 2008). The remaining deposited RGM burden appears to be available for assimilation by the freshwater biota, once carried to Arctic lakes by snowmelt and runoffs (Scott, 2001; Ariya et al., 2004). Mercury trapped in Arctic freshwater lakes following MDE and snowmelt, is thought to induce of Hg-related metabolic abnormalities such as lower testosterone levels and dysfunctions of reproductive capabilities observed among fathead minnows and northern pikes cohorts (Hammerschmidt et al., 2002, Drevnick and Sandheinrich, 2003).

13This picture somewhat differs for the Arctic saltwater environments. Outridge et al. (2008) reported that on a yearly basis, the total Hg flux entering the Arctic Ocean from all sources—MDE, wet Hg deposition, coastal erosion—is almost in balance with the total Hg mass removed from the ocean through evaporation, sedimentation and seawater exports, with a small yearly increase of 0,3% of the total Hg mass. This small net Hg gain by the Arctic Ocean may be enough to explain the progressive increase of the MeHg levels in the marine biota during the 20th century. However, this fragile balance will probably be modified by climate change which is likely to induce: (1) increased coastal erosion, river outflow and Hg transport; (2) changes in the ocean’s biological productivity which might affect Hg bioavailability and MeHg bioaccumulation. (Outridge et al., 2008; Poissant et al. 2008). The outstanding capacity of Hg to concentrate from one environmental compartment to the other is well known. This is particularly true in the case of complex saltwater food webs. For example, biomagnification factors as high as 380 were reported between ringed seal and its usual food source, zooplankton (Dehn et al., 2005).

14It is difficult to state on the origin of bulk atmospheric Hg brought to the Arctic but recent work suggests that about one third or more of the current Hg emissions to the atmosphere is from direct anthropogenic source (Lindberg et al., 2007). However, according to long term monitoring programs measuring atmospheric Hg levels in various locations of the Arctic, it is still difficult to identify a clear trend pointing to a recent decrease in the levels of total atmospheric Hg, despite the numerous efforts to diminish man-made Hg emissions by the industrialized countries of the World.

Boreal environments: Atmospheric deposition and land management

15Several fish communities of boreal lake ecosystems also exhibit Hg levels unsafe for frequent human consumption. However, the route between Hg atmospheric deposition processes and receptor lakes somewhat differs in boreal environments, compared to Arctic freshwater lakes. Here—and except for seepage lakes—almost 90% of the total Hg load to lake waters generally transit through the watershed before reaching the lakes. Thus, the link between the extent of Hg atmospheric deposition and its bioaccumulation along aquatic food webs—or the specific ecosystem’ sensitivity to Hg—rather depends on the following (see also Wiener et al., 2006; Munthe et al., 2007):

1. The characteristics of specific watersheds enabling an efficient transport of deposited Hg—through runoffs and erosion—from upland to methylation sites (riparian wetlands and peat lands, lake sediments).

2. The ability of specific ecosystems to efficiently transform this Hg burden into biologically available MeHg. Natural background MeHg levels do greatly vary, even within sub-regional scales. Environmental factors such as low pH, the presence of riparian wetlands, the extent of photochemical processes, high organic carbon and nutrients loadings, high biological activity, and elevated ratios of drainage basin to lake area, are favourable for MeHg production and therefore tend to yield fish with higher MeHg burdens (Wiener et al., 2006; Munthe et al., 2007).

3. The structure of aquatic food webs which also modulates MeHg bioaccumulation and biomagnification. Variation in invertebrate assemblages, food webs length and structure, and fish growth rates can alter the burdens of MeHg in prey and predator fish species (Parkman and Meili, 1993; Montgomery et al., 2000; Gorski et al., 2003; Kainz et al., 2003; Simoneau et al., 2005).

Tropical environments: gold mining and deforestation

18However, the Hg content of the top sediment samples retrieved along this gradient suggested that the recent sediments carried 1.5–3 times as much mercury as those deposited 40 years ago (Roulet et al., 2000 and 2001). This time frame correlates well with the massive colonization that the region had to face since the beginning of the 1960s following a series of initiatives from the Brazilian National Institute of Colonization and Agrarian Reform. The reform, intended to develop new agricultural regions in Brazil, had the consequence of moving tens of thousands of families from the poorer regions of northeastern Brazil to the Amazon basin. During the first 30 years of the reform, more than 350 000 families settled in these remote regions, gaining ground on the dense tropical forest through a slash and burn deforestation strategy, inducing a loss of forested soils that peaked to about 22 000 km² between the 1970-88 in the Amazon region (Hudson, 1998; Van de Steeg et al., 2006). These facts brought the authors to conclude that the loss of Hg from soils of the Tapajós shores, following deforestation and extensive erosion, was responsible for the high levels of Hg found in local fish species, making these environment sensitive to Hg loading and local population vulnerable to Hg exposure through their dependency toward the fish resource, which is needed to complete their diet. This hypothesis of extensive soil erosion was later supported by other studies describing the enhanced transfer of terrestrial organic carbon to the river, following extensive land use on the watershed of the Tapajós River (Farella et al., 2001 and 2007). Sustainable land use management strategies could again lead to an improvement of the Hg situation in this region.

Freshwater reservoirs: mercury hot spots throughout the Americas

19There are close to 10 000 large dams in North, Central and South America, build either to secure freshwater supply for domestic use and irrigation, or to produce electricity (WCD, 2000). These artificial lakes are attractive to populations, firstly because they often represent the only water plan available in the region, or because fish abundance and size is higher than those of surrounding lakes. Many of them are located on traditional hunting and fishing lands exploited by First Nations subsistence fisher communities.

20Most studies dealing with the environmental impacts of reservoirs converge on the fact that the flooding of terrestrial ecosystems consecutive to impoundments lead to significantly increased Hg levels in fish species living in the newly created water plan (Morrison et al., 1995; Rogers et al., 1995; Park and Curtis, 1997; Kehrig et al., 1998; Bermudez et al., 1999; Lucotte et al., 1999; Tuomola et al., 2008). In many cases, these increases translate in fish MeHg levels unsafe for regular human consumption (Lucotte et al., 1999; Nino et al., 2003). The creation of reservoirs favors the recycling of the Hg burden accumulated for years in soils prior to flooding. Reservoirs also act as efficient incubators for Hg methylation (Lucotte et al., 1999; Gray and Hines, 2008). Nutriments and particles leached from soils through the flooding process increase the biological productivity of these artificial aquatic ecosystems, including higher activities of bacterial consortiums involved in the transformation of Hg into bioavailable MeHg (Montgomery et al., 2000). Furthermore, draw down zones which did not suffer extensive erosion, periodically flooded and dried out, typically represent environments where efficient Hg methylation can occur. Increased Hg levels in fish tissues can be detected 15 to 40 years after the initial flooding episode, depending on the type of environment impacted by flooding and on the fish species considered (Schetagne and Verdon, 1999; Nino et al., 2003). Reservoirs must be regarded as sensitive environments of specific concerns for the Hg issue.

The Human component: health and perspectives

21Scientific literature does not rule out that pathogenic Hg levels in fish can also be solely the results of background (natural) Hg loading in certain lakes. Moreover, the worldwide geographic distribution of major anthropogenic Hg sources to the atmosphere has greatly evolved in the last part of the 20^th century. The reported stabilization (see Box A) of the measured atmospheric Hg levels—despite efforts to decrease the emission in the industrialized countries—could be consecutive to the emergence of important new foreign sources of atmospheric Hg. In 2000, Asian countries contributed for about 54% of the global Hg anthropogenic emissions and China alone was responsible for 28% of this pool (Pacyna et al., 2006). The needs of China for electricity, which is nowadays produced at over 75% through coal combustion, is expected to increase by roughly 75% by 2020, from the 2010 levels (Han et al., 2000; Compton and Wu, 2005; EIA, 2006) and the overall projections for Hg atmospheric loading are not reassuring. Furthermore, the industrialization of our societies has brought other contaminants—such as PCBs and other synthetic organics—to pristine environments, which enhance the risks to health consecutive to eating fish.

22In the mean time, remote communities will continue to rely on fish as a food source and they will need information to find the equilibrium between “exposure to Hg through fish consumption” vs. “land use changes in response to economic stress causing increased Hg transfer to aquatic ecosystems” vs. “health benefits related to a balanced diet, centered on fish consumption”. The challenge of identifying a safe level of fish consumption is not limited to the people of remote or aboriginal origins. But it is exacerbated by the need to elaborate solutions that respect traditions and are applicable to contexts where dietary alternatives are not available, or might even create other health deteriorations: For example in the Cree communities of Northern Québec, a drastic shift from a fish-based diet to less nutritive market food—in response to information campaigns on Hg fish contamination following the creation of hydroelectric reservoirs—led to the appearance of numerous cases of diabetes and other acquired diseases (Dannenbaum et al., 2008).

24Besides the development of sustainable land management strategies, other tools are proposed to remote communities to help them develop mitigation strategies and to lower their exposure level to this contaminant. For instance, it was demonstrated that proper fishing pressures imposed to boreal lakes might lead to lower Hg levels in the tissues of certain predator fish species. Lower competition for food following fish exploitation favors faster growing rates among the remaining fishes, and biodilution of their dietary Hg burden. Selective fish consumption strategies leading to a diversification of the fish size (“eat the smaller fish”) and species (“don’t eat the fish that eats fish”) consumed can also lead to decreased Hg intake. But these elements of solutions, in order to be effective and socially acceptable, must be developed, understood, desired and implemented by (and with) the communities, while in harmony with their traditions.

Conclusion

25Although there are no simple answers to the potential threats engendered by the presence of Hg in remote environments, it is clear that the comprehensive portrait of the subject as depicted is this paper, provides policy makers and community leaders with unique guidance on future ways to handle this important matter. Mercury accumulation in remote ecosystems do represent a significant and complex environmental issue, considering: (a) the high levels of Hg monitored in fish and marine mammals flesh; (b) the large-scale occurrence of such worrying Hg bioaccumulation patterns; (c) the extensive use of aquatic resources by numerous remote communities; (d) the fact that this issue shall persist at least on the mid-term, even if strong measures are taken to lessen Hg anthropogenic loadings to the global atmosphere. According to evidences presented here, actions should be envisioned at three levels:

1. Political interventions on: (a) the development and implementation of landscape management strategies that preserve forests and prevent extensive soils erosion toward aquatic ecosystems; (b) the continuing implementation and strengthening of actual legislation on Hg emission control, especially at the international level, guided by the precautionary principle. Despite the facts presented before, long-term improvement of the Hg situation might be expected following significant decreases in Hg atmospheric loadings. It is also worth noting that actual control technologies limiting atmospheric Hg releases solely target RGM, and should be improved to efficiently remove all Hg species and counteract processes such as the MDE.

2. Educational local/regional interventions directed to: (a) inform communities at risk of higher Hg exposure on the potential threat to their health and on the avenues offered to them to lessen these risks, while maximizing the nutritional benefits related to fish consumption; (b) empower populations towards a sustainable handling of their own environment.

3. Continuing scientific progress on key critical gaps of our collective knowledge of the Hg cycle in the environment, metabolic pathways in the human body and fine-scale toxicological effects. Such progress can only be achieved through multidisciplinary approaches applied at the ecosystem level.

Glossary

26AGM: Small-scale gold mining; ALSSE: acceptable limits for steady-state exposure; Br(dis): Dissolved Bromine; Br(gas): Gaseous Bromine; BrO: Bromine oxide; GEM (or Hg0): Gaseous elemental mercury; hv: Sunlight; Hg: Mercury; ICMGP: International Conference on Mercury as a Global Pollutant; MDE: Mercury depletion events; MeHg: methylmercury; O3: Ozone; PCBs: Polychlorinated biphenyls; ppm: Parts per millon; RGM (or HgII): Reactive gaseous mercury; ug.kg bw-1.day-1: Micrograms per kilogram of bodyweight per day