MERCURY EXPOSURE AND ECOSYSTEM HEALTH IN THE

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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
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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.
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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
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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
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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;
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•
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
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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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