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MERCURY EXPOSURE AND ECOSYSTEM HEALTH IN THE AMAZON: BUILDING SOLUTIONS WITH THE COMMUNITY. Donna Mergler1, Jean Rémy Guimarães2, Marc Lucotte1, Ana Amélia Boischio3, Robert Davidson1,4, Johanne Saint-Charles5, Nicolina Farella1, Elizete Gaspar1, Carlos José Passos1, Delaine Sampaio1, Hugo Poirier1, Silmara Morais1, Frédéric Mertens1 1

Institut des sciences de l’environnement, Université du Québec à Montréal, Canada Laboratório de Radioisótopos, Universidade Federal do Rio de Janeiro, Brazil 3 Universidade Estadual Feira de Santana, Bahia, and Brazilian Research Council, Brazil 4 Biodôme de Montréal, Montréal, Québec, Canada 5 Département des communications, Université du Québec à Montréal, Canada 2

This article is dedicated the memory of Dr. Fernando Branches, a Santarém physician, who was an active researcher throughout this project Abstract This paper summarises the results and achievements of an 8-year participatory research project (Caruso Project) carried out in the Tapajós Basin, representing the joint efforts of Brazilian and Canadian researchers in the study of the environmental dynamics of mercury, as well as the health effects on the fish-eating communities. It coupled scientific investigation and community action to improve human health and ecosystem management. Based on an ecosystem approach, this project provided a new understanding regarding the environmental dynamics and the health effects of mercury for local communities. Results showed that deforestation and not gold-mining is probably the major source of mercury contamination in this region. Furthermore, dose related neurological and cytogenetic deficits are evident below thresholds previously considered for adverse health effects. The studies also allowed us to initiate actions to reduce human exposure and improve well being. They were conducted in two stages (Caruso I and II) and involved a number of communities in a successful participatory intervention based on the choice of the least contaminated fish species for consumption, which allowed a significant reduction of exposure with consequent human health improvements, while maintaining fish consumption.

1. Introduction Mercury (Hg) contamination of the Amazonian basin has been extensively studied over the last decades. The concerns on the presence of Hg in the environment and potential human exposure begun in the 1970’s, due to the great gold rush. During the 1970’s and 1980’s, approximately 1 million people were involved in rudimentary gold extraction in the river sediments based on the amalgamation technique with mercury (Cleary, 1990). It has been estimated that 130 metric tons of mercury have been spilled annually into the Brazilian Amazon, attaining various compartments of the ecosystem (Martinelli et al.,

2 1988; Malm et al., 1990; Lacerda & Salomons, 1991; Pfeiffer et al., 1991). Large-scale destruction of the ecosystems and mercury contamination have become the focal points of today's environmental concerns in Amazonia. Rise in mercury contamination of the waterways increases the methylmercury content of fish, a dietary mainstay of Amazonian riparian populations. When mercury is released into aquatic environments, it is methylated by bacteria, present in river sediments, to its organic form: methylmercury. In this form, it then becomes bioavailable to the ichthyofauna, where it can be biomagnified through every step of the food chain up to humans (WHO, 1989). Previous studies on the mercury content of fish in the Amazonian river system have shown that levels often surpass 0.5 µg/g fresh weight (Pfeiffer et al., 1991; Lacerda and Salomons, 1991; Barbosa et al., 1995; Boischio et al., 1995; Malm et al., 1995a, Lebel et al, 1997, Dolbec et al, 2001), a value that is considered in many countries as a standard not to be exceeded for safe consumption, when the total fish consumption does not exceed 400 grams per week. Hair mercury concentration is considered a good biomarker of methylmercury absorption by humans. In the Brazilian Amazon, hair mercury concentrations range from a few µg/g up to 300 µg/g, with median exposure values in the order of 2 µg/g up to 20 µg/g (Akagi et al., 1995; Malm et al., 1995b; Barbosa et al., 1995; Boischio et al., 1995, 1996; Grandjean et al., 1993; Nakanishi, 1992). From a public health point of view, numerous studies indicate that the nervous system is a prime target for methylmercury, thereby placing the exposed populations at a disadvantage with respect to adequate development of intellectual and physical capacities due to nervous system deficits (Ratcliffe et al, 1996). The purpose of this article is to present the major research findings and achievements of the Caruso Project, which has been conducted since 1994.

2. The Caruso phase I project 2.1. A new source of mercury contamination: soil erosion Concerned about the Hg environmental contamination and human exposure of riverside populations, Brazilian and Canadian researchers teamed up in 1994 to explore the problem in the Tapajós region, where thousands of gold miners had panned for gold over the last 30 years, with its peak production during the 1980s and subsequent major decline. On a first phase of the project, (Caruso I, 1994-1997), our research team collected and analyzed water, river sediments and soil at intervals along the Tapajós river, starting at gold mining sites and ending hundreds of kilometers away. Results showed that Hg concentrations were relatively constant along the Tapajós River, suggesting the presence of a major source of mercury other than mining. Following such results, analyses of riverbed sediments showed that the most recent layers contained 1.5 to 3 times more mercury than layers deposited 40 years ago, even 400 kilometers downstream of the gold-mining sites. Sampling and analyses of nearby soils revealed high mercury concentrations throughout entire soil profiles down to 1-m depth. These findings led to the conclusion that

3 deforestation has allowed rain to erode soils of the river watershed, transferring high Hg loads into the aquatic ecosystems, where it is then methylated by bacteria and contaminates the aquatic food web (Farella et al, 2001; Roulet et al, 1998a, 1998b, 1999, 2000a, 2000b, 2001a, 2001b; Roulet and Grimaldi, 2001). Furthermore, other studies suggest that the climatic conditions and aquatic vegetation in many of the Amazonian ecosystems are optimal for mercury methylation speeding up the process of the incorporation of mercury into the trophic chain (Guimarães et al, 2000a, 2000b; Guimarães, 2001). Large mats of floating macrophytes are key sites of this transformation into methylmercury, leading to its absorption by aquatic fauna, which increases in concentration as it moves up the food chain and then to humans. The new understanding of mercury contamination dynamics that emerges from these results can be summarised as follows: Mercury pollution is far more widespread than originally thought since soil erosion and lixiviation subsequent to deforestation ‘slash and burn’ agricultural practices adds to the already known sources from gold mining activities. Policies of massive colonization are not only reducing the existing forest cover, but also increasing the mercury contamination of the Amazon.

2.2. Methylmercury health effects at low-dose chronic exposure Since people living along the Tapajós depend on fish for a major part of their diet, our research team studied the fish-eating habits in relation to mercury exposure in a number of communities of the Tapajós (Ponta de Pedras, Cameta, Brasília Legal). Our studies demonstrated that biodiversity of fish stocks is complex and that mercury exposure of human populations is intimately linked to their diet. Longitudinal studies revealed that hair mercury levels vary sinusoically over time, paralleling seasonal variations in fish species consumption during the rainy and dry seasons. This probably reflects fish bioavailability due to differences in the lifecycle characteristics of the various species (Lebel et al, 1997; Dolbec et al, 2001). Mercury exposure was assessed through the analysis of hair, blood and urine samples. In addition, we conducted neurobehavioral testing to determine the health impacts of exposure. The results showed a strong relationship between fish consumption and mercury exposure, as well as significant declines in motor coordination, certain visual functions as well as cytogenetic properties, at mercury levels well below accepted international safety standards (Lebel et al, 1996, 1998; Amorim et al, 2000; Dolbec et al, 2000). The findings of this first stage demonstrated mercury related diminished well-being and warned that more serious neurological and cytogenetic problems could develop within these populations. particularly among the more vulnerable individuals. These results allow us to conclude that dose related neurological and cytogenetic deficits are evident below thresholds previously considered for adverse health effects.

4 3. The Caruso phase II project Based on the results of Caruso I, our research group pursued a second stage of the project. Here, we sought to merge our scientific findings with community knowledge in order to carry out and evaluate viable and sustainable solutions for reducing mercury contamination and ensuring ecosystem health. Several communities in the Tapajós participated in the studies. The community of Brasilia Legal, with whom we had maintained relations since 1994 when we initiated the research, has a well-established infrastructure. The village leaders are active in local and regional issues; there is a health post, with experienced community agents who are very aware of the issues surrounding mercury and fish consumption. Since this village is accessible, being on the route of the transport boats, it has been the site of several studies (Akagi et al., 1995; Grandjean et al., 1993; Malm et al., 1995b. Grandjean et al, 1999), which have confirmed the presence of low level exposure to mercury and demonstrated neurotoxic effects on the adults (Lebel et al., 1996; 1998) and in children (Grandjean et al, 1999). We have extensive data on mercury levels in different environmental compartments in the area surrounding this village, and, in particular, for fish in the areas where the villagers harvest. The communities of Pereira, Araipá and Cupú also participated in the Caruso II studies. These are agricultural communities situated around 3 fluvial lakes on the other side of the Tapajós from Brasilia Legal. This area was chosen in order to study the influence of agricultural practices and deforestation on mercury in the aquatic ecosystem and to organise pilot intervention projects. In addition to pursuing the environmental studies on Hg, we initiated a number of intervention projects with the communities in order to reduce Hg exposure while maintaining fish consumption. We worked in close collaboration with these communities to implement such solutions (short and long-term intervention projects) and evaluated the impact of these interventions on human health and exposure. To attain these goals, a series of workshops were organised (involving a general meeting of the villagers) in order to inform villagers of the scientific results of the study and discuss with them further work towards solutions. It should be noted that contact with the villagers was not limited to these meetings and members of the research group worked with the villagers on different aspects of the study at several occasions each year throughout the project.

I. First workshop: Caruso II was initiated with a workshop organised in January 1999 in the village of Brasilia Legal. The intervention projects, which were subsequently carried out, were planned at this workshop. II. Second workshop: In April 2000, a meeting was held with the villagers of Brasilia Legal to discuss the results obtained to that point and organise the field study. III. Third workshop: Held in September 2001, under the banner: ‘Congratulations Brasilia Legal’, this workshop was held to inform the villagers of the success of the their efforts to reduce mercury

5 exposure and maintain fish consumption and inform them of the results of the study on dietary habits (see results below). IV. Fourth workshop: On February 2002, a workshop was carried out with the Cupú, Pereira, and Araipá communities. The general objective of the meetings was to discuss with the villagers on the agricultural alternatives in the region that can orient the elaboration of a pilot project limiting soil erosion.

3.1. Major research findings of Caruso II 3.1.1. Mercury dynamics in the Tapajós ecosystems We studied the total mercury (Hg) concentrations, bioamplification and bioaccumulation in the ictyofauna of three lakes in the Brasília Legal region. In addition, special attention was given to possible seasonal and spatial variations in the Hg levels. Two sampling campaigns corresponding to the rainy (April – May 2000) and dry seasons (January 2001) were carried out. The bioamplification of Hg through the trophic chains of the three lakes was identified over these seasons. During the rainy season, 31% of piscivorous fish presented concentrations higher than the critical value of 500 ng/g, whereas in the rising water period, only 28% presented higher values. We rarely observed linear or curve-linear positive correlations between Hg concentrations of muscular tissue and the total length of fish. Various species of commercial importance did not present any variation in Hg concentrations with increasing length of fish. Other linear-negative and non-linear positive or negative correlations with Hg throughout fish’s development were likewise identified. Our data suggest that the Hg concentrations may vary seasonally. On the other hand, over the two seasons, no spatial variation in Hg concentrations was observed for most of the species studied. According to the present study, it is important to consider spatio-temporal variations of Hg levels in fish, as well as different mechanisms of accumulation of the metal, at the moment of implementing measures aiming to inform the populations at risk of Hg exposure. These results allow us to conclude that the complexity of the Amazonian trophic web associated to the changes of environmental variables imposes a fish’s adaptability and may be translated in differentiated patterns of Hg contamination (Lucotte et al, 2001; Sampaio et al, 2001). 3.1.2. Diet A 12-month prospective dietary survey was carried out with 26 adult women, using a daily food frequency diary and examined with respect to total monthly hair Hg levels, determined through sequential analyses. This study allowed the identification of a wide range of foods available in the community, whose availability varies seasonally (Passos et al, 2003a). In addition, results showed that the strong relation between fish consumption and Hg exposure was significantly modified by fruit consumption. For the same number of fish meals, those who ate more tropical fruits had lower hair mercury levels, suggesting that fruit consumption modulates the relation between fish consumption and mercury exposure. A number of phytochemicals and nutritional fibers present in fruits might be interacting with Hg in several points of the body: absorption and excretion, transport, binding to target proteins, metabolism and sequestration (Passos et al, 2003b). More studies are required on larger populations to further elucidate the extent and

6 public health implications of the use of fruits to counteract the toxic action of methylmercury. 3.1.3. The role of social networks on the diffusion of information and behavioural changes In 2001, we conducted a network analysis in order to determine the influence of interpersonal communication and social structure on individual behavioural changes in fish consumption, with the inhabitants of the Brasília Legal village (Mertens et al, 2002; Saint-Charles et al, 2003). Every household was visited and socio-demographic data, information about fish consumption and sociometric data on the communication network related to diet, health and mercury were collected for 85 women and 67 men. We were able to identify both male and female opinion leaders in the communication network. However, opinion leadership was associated with change in fish consumption only for women. Furthermore, results illustrate the influence of female opinion leaders at the community level and female spouses at the household level in promoting healthy changes in dietary habits to reduce mercury exposure. Preferential consumption of less-contaminated fish was associated with the presence of female communication partner – but not male – in the personal networks of both men and women. At the household level, men who considered their wife as a discussion partner were much more likely to change their behaviour than those who did not. These results illustrate the importance of interpersonal relationships and social structure of the community in the dissemination of information regarding the problem of mercury exposure, in the longterm involvement of villagers in participatory interventions, as well as in the adoption of new behaviours to decrease exposure. They show that men and women play different roles in the social network structured around the mercury problem and indicate that particular attention should be given to gender analysis in these network studies. They convinced us to incorporate social networks analysis in our methodological approach not only as an after-the-fact analytical method but as a way of developing a better understanding of social networks which in turn should facilitate the promotion of environmental awareness and actions. 3.2. Intervention Projects to Reduce Mercury Absorption and Restore Environmental Equilibrium Several projects, which sought to reduce mercury absorption, maintain and improve nutritional status using traditional foods and restore environmental equilibrium, were carried out with the villagers. Our main objectives were

to elaborate participative projects leading to the restoration of the environmental equilibrium of degraded areas;

to come forward with sound recommendations on fish consumption with respect to species and an implemented plan to properly inform and work with riparian populations;

to judge, on a preliminary basis, the efficiency and the impact of the different interventions made within riparian communities;


to evaluate mercury exposure among mothers, babies and breast milk, given the vulnerability of exposures during this period of life.

3.2.1. A gender-based approach A sociological component of the study allowed us to examine the social representations of environment, diet and health. This is a traditional population, with specific rules and particularities of social organisation; the actors – individuals, families, groups - are located in the context of their specific society with values, traditions, habits, representations, viewpoints, and strategies of production and reproduction, all factors that will influence reasoning and strategies to conduct any process of change. Intervention is feasible in a riverine community, exposed to Hg through fish consumption, if a number of persons in the village are capable of taking organized actions or stimulating appropriate measures towards intervention. In the social context of the community under study, three major recognised influential groups in the decision-making process were identified: women teachers, with strong influence in the community; women working in health, who have influence mostly on the health issues; women working in fishing, who despite their subtle representation, make certain decisions at the individual level, which have collective implications. For example, this latter group is responsible for choosing fish for household consumption as well as exchanging salty fish with farmers’ housewives for a variety of vegetables. As a consequence, these food exchanges influence modification of dietary habits in the community. At the beginnings of Caruso II (1999), thirty women of the village of Brasília Legal were selected to participate actively in different aspects of the study. First, a focus group was organised with the objective of understanding the role played by women in health, environmental issues and the issue of mercury contamination. The results of this aspect of the study, leading to the understanding of women’s ‘invisible power’, were essential for the implementation of mitigation strategies. 3.2.2. Fish and Fishing Fish is and most likely will continue to be the main dietary source of animal protein available and ingested by this riparian population. Moreover, fish is an excellent source of many nutrients and protective for several diseases. Therefore, the interventions aimed at decreasing Hg exposure need to take into account the nutritional value of fish, the availability of other protein sources, the economic status of the population, as well as the socio-cultural aspects of eating. We have worked in close collaboration with the villagers of Brasília Legal in order to better understand the social, economic and cultural factors playing a role on the fishing/fish eating practices. With a socio-anthropological approach, we have examined important links between the researchers of the various disciplines and the villagers of the community. The activities have focused on the commercial and subsistence aspects of fishing and their interconnections with the fish eating practices. In addition, the analyses of the community’s social structure have revealed important human relational dynamics, which play a role in fish-eating practices, including the gender issues and women’s role in community intervention studies. 3.2.3. Impact of the Interventions on Human Health and Exposure Using a participatory research approach, we initiated a pilot project based on dietary changes which sought to bring about solutions on the short term, in the Brasília Legal village. The study and resulting

8 understanding of the social organization in the community, which facilitated the identification of key individuals and groups in the community, has proven to be especially valuable for the success of the participatory intervention process. Meetings were held in the village and posters were distributed to every house with the levels of mercury in 42 different fish species (red fish: high levels; yellow fish: medium levels; green fish: low levels). A slogan was proposed: Eat more fish that don’t eat other fish. The message was positive ’eat fish’, but more non carnivorous than carnivorous. The participatory intervention based on dietary changes aimed at reducing mercury exposure from fish consumption has been hugely successful (Mergler et al, 2001; Morais et al, 2001). Comparison of diet and exposure of the same persons in 1995 and in 2000 showed that they continued to eat the same quantity of fish, but modified the relative proportions of carnivorous and non-carnivorous fish. This resulted in a decrease in hair mercury levels of approximately 35%. Thus, the slogan "Eat more fish that don’t eat other fish" was applied efficiently and the population was able to maintain the consumption of this healthy dietary component and reduce toxic exposure. Finally, given the vulnerability of mercury exposure during the reproductive stage of life, mercury analyses were conducted in maternal hair segments, babies hair and breast milk. Mercury results were consistent with those of other age groups, indicating the need of further investigation for this population group (Boischio et al., 2003). 3.3. Long term solutions: the development of sustainable agricultural systems models In addition, research has been developed in order to find ways of limiting soil erosion, based on a pilot project on the analysis of household agricultural practices and their influence on the soils. This particular study is aimed at evaluating the interconnections between the socio-economic context, including history of land use, and the quality of soils in the region of Brasilia Legal, in order to elaborate a pilot project whose most important objective is to reduce the erosion of soils and the transfer of terrestrial mercury into the aquatic ecosystems. Specifically, it is intended to describe the present practices of land use and relate them to the social, cultural, historical, and economic context. It is also planned to analyse the impact of different agricultural practices on the soils, establishing pedologic profiles of household properties according to the history of past and present land use, in order to identify the practices used for the least erosive lands in the soils of the study area. These investigations are now under way. Long-term research and intervention activities should address the issue of mercury contamination at the very sources of the problem, that is agricultural practices based on slash-and-burn. To do so, it is important to scale up research activities to the Regional level, directing agricultural practices towards a better land management in order to protect and restore highly significant ecosystems from the Amazon and to improve the quality of life of ever-poor farmers of this region. In this context, several members of our research team constituted a network made of Brazilian, Canadian and international institutions (interdisciplinary, intersectorial and international, namely the Montreal Biodome, CIAT, CIFOR, EMBRAPA, IBAMA, ICRAF, IEC, INCRA, MPEG, NAEA (UFPA), SECTAM, SUDAM, UFPA, UFRA, UFRJ and UQAM). All partners of this network agreed on a strong and unifying concept, based on an ecosystem approach that includes human aspects, environmental aspects and agricultural practices aspects. The networking was refined as the project was getting worked out, especially through the

9 inclusion of NGO’s to reflect communities’ interests. Apart from the modeling aspects themselves which will become a project as such, many research and intervention projects on varied issues related to agricultural are currently being defined, on such themes as soil erosion, social issues linked to the agricultural practices, integrated agricultural models that include the presence of trees, linkages between ecosystem health and human health, impact of colonization policies, riverbanks restoration and issues related to communities awareness. Capacity building of human resources will be an important aspect of this large-scale project.

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