Mercury in tropical and subtropical coastal...

Environmental Research 119 (2012) 88–100

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Mercury in tropical and subtropical coastal environments

Monica F. Costa a,n, William M. Landing b, Helena A. Kehrig c, Mario Barletta a, Christopher D. Holmes d,Paulo R.G. Barrocas e, David C. Evers f, David G. Buck f, Ana Claudia Vasconcellos e, Sandra S. Hacon e,Josino C. Moreira e, Olaf Malm c

a Departamento de Oceanografia. Universidade Federal de Pernambuco. Recife, Pernambuco, Brazilb Department of Earth, Ocean, and Atmospheric Science, Florida State University, Tallahassee, FL, USAc Laboratorio de Radioisotopos Eduardo Penna Franca (IBCCF / CCS), Universidade Federal do Rio de Janeiro. Rio de Janeiro, Rio de Janeiro, Brazild University of California at Irvine. Department of Earth System Science, Irvine, CA, USAe Escola Nacional de Saude Publica. Fundac- ~ao Oswaldo Cruz. Rio de Janeiro, Rio de Janeiro, Brazilf BioDiversity Institute, Gorham, ME, USA

a r t i c l e i n f o

Available online 14 August 2012

Keywords:

Mercury land-based sources

Atmospheric transport

Tropical estuaries

Bacterial methylation

Trophic transfer

Human health

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esponding author. Fax: þ1 5502 1812 1268 2

ail address: [email protected] (M.F. Costa).

a b s t r a c t

Anthropogenic activities influence the biogeochemical cycles of mercury, both qualitatively and

quantitatively, on a global scale from sources to sinks. Anthropogenic processes that alter the temporal

and spatial patterns of sources and cycling processes are changing the impacts of mercury contamina-

tion on aquatic biota and humans. Human exposure to mercury is dominated by the consumption of

fish and products from aquaculture operations. The risk to society and to ecosystems from mercury

contamination is growing, and it is important to monitor these expanding risks. However, the extent

and manner to which anthropogenic activities will alter mercury sources and biogeochemical cycling in

tropical and sub-tropical coastal environments is poorly understood. Factors as (1) lack of reliable local/

regional data; (2) rapidly changing environmental conditions; (3) governmental priorities and;

(4) technical actions from supra-national institutions, are some of the obstacles to overcome in

mercury cycling research and policy formulation. In the tropics and sub-tropics, research on mercury in

the environment is moving from an exploratory ‘‘inventory’’ phase towards more process-oriented

studies. Addressing biodiversity conservation and human health issues related to mercury contamina-

tion of river basins and tropical coastal environments are an integral part of paragraph 221 of the

United Nations document ‘‘The Future We Want’’ issued in Rio de Janeiro in June 2012.

& 2012 Elsevier Inc. All rights reserved.

1. Introduction

1.1. The atmospheric and riverine sources of mercury to tropical

coastal environments

The oceans play a central role in the biogeochemical cycles ofessential and non-essential elements through a series of abioticprocesses (chemical speciation, inorganic scavenging, sedimenta-tion) and biological processes (bio-alteration, bio-accumulation,and bio-magnification). In the last few centuries (and especiallysince World War II), anthropogenic perturbations to the globalmercury cycle have in many cases overwhelmed the naturalprocesses of mercury cycling (Mason et al., 1994, 2012). For along time human influence on mercury cycling was detectableonly at the local scale, but it is now clear that these influences areglobal. From land-based sources, natural and anthropogenic

ll rights reserved.

25.

mercury releases reach coastal areas and from there gain accessto the ocean and its trophic webs. Although changes in Hgconcentrations in seawater through direct measurements arenot yet fully documented in the tropics, inventories of localsources (e.g., Marins et al., 2004), the increase of mercury levelsin the biota (Evers et al., 2008a), temporal trends in geochemicalrecords (Xu et al., 2011) and mercury cycling models, all pointtowards the existence of a global problem (Doney, 2010), of whichtropical coasts are only part.

The tropical and subtropical belt includes countries of everysocio-economic level, including very poor countries to some of theten largest global economies (Fig. 1). It is associated with some ofthe largest coastal population densities (e.g., India, Bangladesh,China, South-East Asia, Caribbean Islands and Nigeria), and someof the World’s megacities are on the margins of estuaries intropical regions (e.g., Hong Kong, Rio de Janeiro, Bombay). Globalmercury emission patterns (Pacyna et al., 2010) place most of themercury atmospheric sources in densely populated coastal areas.However, nations in the tropical region are mainly emergingand developing economies, struggling with issues of population

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mailto:[email protected]


Tropic of Cancer 23.5°N

1 6

Equator

Tropic of Capricorn 23.5°S4

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Source: Food and Agriculture Organizationof the United Nations (2008) FAOSTAT

5

2

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Fig. 1. More than 150 countries are in the tropical and subtropical zones, the large majority are small island states. Only a few countries have vast extensions of coastline

in the tropics and sub-tropics (ex. Brazil, Australia, India, China, Mexico, USA, Chile, Peru, Angola). Seafood consumption varies widely among these nations, depending on

size and capacity of fishing fleets and cultural values. Coastal pollution by mercury and other pollutants might have a role to play in this scenario at the local scale. Studies

with Trichiurus lepturus (1) Shrestha et al., 1988—Venezuela; (2) Mol et al., 2001—Suriname; (3) Costa et al., 2009; Barbosa-Cintra et al., 2011—NE Brazil; (4) Kehrig et al.,

2004; Cardoso et al., 2009; Kehrig et al., 2009c,, 2010,, 2011; Carvalho et al., 2008; Di Beneditto et al., 2012; Muto et al., 2011; Bisi et al., 2012; Seixas et al., 2012a, b; Seixas

et al., 2012—SE Brazil; (5) Saei-Dehkordi et al., 2010—Persian Gulf; (6) Prudente et al., 1997—Philippines.

M.F. Costa et al. / Environmental Research 119 (2012) 88–100 89

welfare, environmental protection and economic growth. In thesecases, health and environment policies vary, and (mercury) pollu-tion-oriented policies are not always in place. Therefore, coastalpopulations and environments are at risk in terms of direct andindirect exposure to mercury (e.g., thorough atmospheric trans-port-deposition, river discharge and seafood contamination).

Despite efforts to improve the situation, the linkages betweenriver basin and coastal environmental management plans arepoorly developed in countries of the tropical and subtropical belts(Barletta et al., 2010). The consequences of poorly integratedbasin and estuarine management regarding water quality, andmercury pollution in particular, are transferred to (and amplified)in coastal waters (Costa et al., 2009; Evers et al., 2008a).

Each country has mercury emission characteristics related totheir own socio-economic status, but some common features exist.The three major sources of mercury are related to energy generation(industrial and domestic) through coal burning, the sum of small-and large-scale gold mining, production of non-ferrous metals andcement production. Deforestation may be another source of mercuryto aquatic and coastal environments (Almeida et al., 2005). In somecountries, such as China, mercury mining can also be a contributorto coastal contamination (Li et al., 2009)

Mercury and gold mining remain as major sources of environ-mental mercury contamination in tropical regions, putting nearly9 million people at risk at approximately 280 of the 2100 identi-fied contaminated sites all around the world (www.unep.org).Chlor-alkali plants, while historically responsible for significantlocal and regional mercury contamination, are no longer a majormercury source for the environment since mercury electrodesare being replaced by the membrane-based production processand, where it has not yet been done, effluent treatment is usuallyin place.

The accumulation of mercury from non-point sources inremote ecosystems, where aquatic resources are extensively usedby local populations, is a serious conservation and human healthconcern in coastal areas (Canuel et al., 2009), as for example inrelatively isolated Pacific Islands (Denton et al., 2009; Chouvelonet al., 2009).

Tropical coasts harbour a variety of biomes, ecosystems, andhabitats that are home to sand beaches, wetlands and floodedmangrove forests surrounding estuaries which support a richbiodiversity. Coastal reefs and seagrass meadows complete theecoclines, leading to platform environments. Some of thesecontinuums might disappear, or decline in areal extent. Habitatloss and changes in biological community structure may altermercury cycling in these regions before we have a chance to fullyunderstand the important mercury cycling processes. The con-sequences for the remaining elements of the coastal mercurycycle are unpredictable. Simplification of coastal tropical foodwebs, and consequent loss of biodiversity, may result in newpatterns for mercury cycling and contamination in tropicalcoastal regions. Therefore, we are likely to face new and challen-ging human health and conservation issues in the near future.

In the absence of significant point sources for mercury con-tamination, aquatic biota in tropical regions are exposed tomercury contamination derived ultimately from highly seasonalatmospheric deposition (Costa et al., 2009; Barletta et al., 2012).The tropical climate is characterized not only by high air(418 1C) and water (425 1C) temperatures, but also by intense,well-defined rainy seasons (type ‘‘A’’ climates, from the Koppen–Geiger classification). Triggered by enhanced nutrient supply toestuaries and coastal waters, eutrophication and concomitantbiological dilution tends to reduce mercury bioavailability toconsumers, namely vertebrates who prey on estuarine and coastal

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M.F. Costa et al. / Environmental Research 119 (2012) 88–10090

organisms. On the other hand, mercury bioavailability canincrease during the dry season, such that animals towards thetop of the food web tend to show higher mercury concentrations(Costa et al., 2009; Barletta et al., 2012).

Mason et al. (1994; 2012) have shown that, in the last fivecenturies, anthropogenic impacts on mercury biogeochemicalcycles have significantly changed both the nature of the processesand the fluxes of mercury on a global scale. Those impacts ontropical coastal ecosystems and habitats are no exception to thatpattern. This paper discusses the possible nature and patterns ofsuch changes in the tropics, focusing on coastal food webs fromtheir base (bacteria and plankton), through filter feeders andother consumers, to apex predators (large fish, reptiles, birds andmammals) and finally to humans.

2. Mercury atmospheric sources to tropical and sub-tropicalcoasts

In tropical coastal regions, rivers and direct discharges fromindustrial facilities and sewage can be the dominant sources ofmercury to seawater, biota and sediments. Although this is quite

Fig. 2. Annual mercury deposition (wet plus dry, including Hg(0); mg m�2 yr�1) over th

over tropical latitudes (241N to 241S).

Fig. 3. The seasonal variability in total mercury deposition (wet plus dry includ

often the situation, direct atmospheric deposition can also be veryimportant. Atmospheric sources of mercury might be of a moreglobal nature (coal burning, volcanoes etc.), but others can bequite unexpectedly local, as for instance medical incinerators(Denton et al., 2011) and mishandling of e-wastes (Robinson,2009). The mercury burden delivered to coastal environments byatmospheric transport and deposition interacts with local ecolo-gical and social patterns (Jardine and Bunn, 2010). So, it isnecessary to take this atmospheric contribution into considera-tion, especially when inventories suggest higher levels of mercuryin coastal environmental compartments than the most obvious,waterborne mercury sources, can possibly explain.

The GEOS-Chem model (Holmes et al., 2010) was used toestimate wet and dry deposition of oxidized Hg(II), particulateHgP, and gaseous elemental Hg(0) to the tropical oceans on aseasonal and annual basis as a function of longitude. For thissimulation of atmospheric mercury deposition in the tropics, weused the Streets et al. (2009) global anthropogenic inventory for2006 partitioned into 17 regions; emissions within each regionfollow the GEIA 2000 distribution (Pacyna et al., 2006). Inaddition, we included Hg(0) emissions from artisanal gold mining(total 450 Mg a�1; Hylander and Meili, 2005). Anthropogenic

e tropical oceans simulated using GEOS-Chem. Deposition shown here is averaged

ing Hg(0); mg m�2 month�1) across latitude simulated using GEOS-Chem.


emissions total 2050 Mg a�1. Biomass burning emits 300 Mg a�1

following the distribution of CO from biomass burning. Themodel calculates soil, vegetation, snow, and ocean emissions(1200 Mg a�1, 260 Mg a�1, 210 Mg a�1, and 2000 Mg a�1, res-pectively) with coupled surface reservoir sub-models. Globalmercury emissions are 8300 Mg a�1 if we include gross oceanHg(0) emissions or 6300 Mg a�1 if we include only net oceanemission. These emission totals for anthropogenic and naturalsources are within 15% of recent UNEP estimates for 2005 (Pacynaet al., 2010; Pirrone et al., 2010), but uncertainties for individualsource types are estimated to be 25–50% (Pacyna et al., 2010).

On an annual basis (Fig. 2), Hg deposition is highest in thewestern Pacific (14 mg m�2 yr�1) and lowest in the eastern Pacific(9 mg m�2 yr�1). The high deposition rates in June–October inthe western Pacific (Fig. 3) are due to elevated wet deposition,while wet and dry deposition are roughly equivalent the rest ofthe time. Dry deposition of elemental Hg generally accounts forabout 10–20% of the total deposition.

Very few wet or dry mercury deposition measurements existin the tropics (Mason et al., 1992; Lamborg et al., 1999), withnone published in the scientific literature in the last decade.Atmospheric concentration measurements in the tropics comemainly from transient ship cruises, with very few long-termmonitoring sites (Sheu et al., 2010; Muller et al., 2012). Observa-tions in this region are essential for evaluating and improving ourunderstanding of mercury inputs to tropical terrestrial andmarine ecosystems. In addition, global modelling efforts wouldbenefit from research on the rate and mechanisms of the oxida-tion and reduction reactions for atmospheric mercury species,rate coefficients for gas-aerosol partitioning, mechanistic controlsfor natural land emissions, and field observations in remoteregions, especially the southern hemisphere.

3. Mercury inputs to tropical coastal food webs

In many cases, mercury reaches coastal habitats through riverdischarge into estuaries. From there, a number of abiotic pro-cesses influence mercury cycling in tropical coastal waters (Costaand Liss, 1999, 2000; Paraquetti et al., 2007; Muresan et al.,2008a). Mercury methylation and uptake by the biota is also aconcern since the average mercury levels in biota increased (Everset al., 2008a), following expected biogeochemical trends (Masonet al., 1994,, 2012).

Both primary producers and higher plants are seldom usedin mercury research in tropical coastal environments, butoccasionally appear in the literature in combination with otherenvironmental compartments (water, sediments, primary con-sumers) (Stavros et al., 2008). A few studies used mercurymeasurements on mangrove tree leaves to assess the impor-tance of the mangrove detritus food web on local and regionalmercury cycles. Although these are frequent food items forcharismatic organisms such as marine turtles (Guebert-Bartholo et al., 2011a) and the manatee (Stavros et al., 2008),studies on other multicellular tissues such as macroalgae andseagrass are rare.

Mercury (Hg) is an environmental pollutant that accumulatesin aquatic ecosystems, generating health concerns for consumersof contaminated organisms (wildlife and humans). The mostcommon organic form of Hg, methylmercury (MeHg), is ofparticular concern because it is a potent neurotoxin and bio-magnifies in aquatic food webs. Thus, it becomes concentratedin the tissues of higher trophic level organisms (Wolfe et al.,1998). From a toxicological point of view, the key process thatfacilitates mercury entrance in coastal food webs is mercurymethylation.

3.1. Bacteria and mercury transformations in tropical coastal

environments

The microbial community plays a critical role in the biogeo-chemical cycling of mercury, influencing its chemical speciation,reactivity, and bioavailability through mediation of processessuch as methylation, demethylation, oxidation, and reduction.For some of these processes, the relevant bacterial groups, theimportant environmental factors, the biochemical pathways, andeven the genes involved have been described in the literature(e.g., mercury demethylation and reduction). However, forother reactions (e.g., mercury methylation) our knowledge isstill incomplete, despite the number of studies that have beenconducted (Benoit et al., 2001; Barkay et al., 2003; Merrit,Amirbahman (2009); Barrocas et al., 2010).

The key process that drives mercury bioaccumulation ismercury methylation. Most of the research concerning thisprocess has been conducted in freshwater ecosystems, both intemperate and tropical areas. Huguet et al. (2010) found high Hgmethylation potential in planktonic microorganisms in the anoxicwater column and downstream waters of a reservoir in FrenchGuiana, supporting the hypothesis that Hg methylation occursunder moderately anoxic conditions. Such conditions can occur inbottom waters and sediments where mixing and oxygenation arerestricted, but also in microenvironments (i.e., biofilms) within anotherwise oxic water column. Coelho-Souza et al. (2006) reportedthe contribution of cyanobacteria (e.g., Microcystis aeruginosa andSineccocystis sp.) and bacteria associated with its mucilage to Hgmethylation in an oligohaline tropical coastal lagoon in Brazil.Also, mercury methylation rates measured in periphyton asso-ciated with the roots of aquatic macrophyte in tropical freshwatersystems (e.g., Amazonian lakes and rivers) were higher than ratesmeasured elsewhere, demonstrating the relevance of these micro-environments (Mauro et al., 2002; Acha et al., 2011). Whencomparing Hg methylation rates in periphyton associated withaquatic macrophytes from a tropical and a temperate system,Guimar~aes et al. (2006) attributed the higher rates in the tropicalecosystem to higher bacterial production rates. Other studiesreported higher methylation potential in tropical aquatic systemsdue to relatively high Hg(II) levels in the water column combinedwith elevated sulphate-reducing bacteria (SRB) activity, whichwas promoted by high temperature and organic substrate con-centration and consequently low dissolved oxygen (Muresanet al., 2008b).

Despite the importance coastal zones play in the globalmercury cycle, very little process-oriented Hg research has beendone in coastal ecosystems, especially in the tropics (Whalinet al., 2007). New research to improve our understanding of thebiogeochemical cycling of Hg in aquatic systems must take intoaccount the prominent role played by the microbial community.

3.2. Estuarine, coastal and marine plankton: The base of the food

web

The trophic transfer of mercury along marine food webs hasbeen recognized as an important process, influencing bioaccumu-lation and the geochemical cycling of mercury (Fisher andReinfelder, 1995). The trophic transfer factors along the foodweb are a useful tool to assess the biomagnification of mercuryfrom one trophic link to another. However, bioavailability andchemical speciation (especially free ions) influences mercurytoxicity and its bioaccumulation by organisms in the marineenvironment (Wang and Rainbow, 2005).

Primary producers can represent an important exposure routefor mercury (Watras et al., 1998) to primary consumers, suchas zooplankton and filter-feeding bivalves (Okay et al., 2000;


Anandraj et al., 2008). Autotrophic and heterotrophic organismsin the microbial loop play key roles in the transfer of mercury intomarine food webs (Fenchel, 2008), influencing the biogeochem-ical cycling of the aquatic ecosystem, as well as being majorcontributors to elemental cycling and vertical fluxes (Fisher et al.,2000). Dissolved MeHg, which is the most biologically availableorganic form of mercury, is bioaccumulated up to a million timesin microscopic particles, including phytoplankton and bacteria,via adsorption to cell surfaces in the water column (Mason et al.,1996; Miles et al., 2001). These MeHg-enriched particles are thenconsumed by zooplankton, which in turn are a primary foodsource for larval, juvenile, and some adult fish (Hall et al., 1997).

The microbial loop is expected to be an especially importantfeature in the ecology of tropical waters, due to the warmtemperatures, high dissolved organic carbon (DOC) concentra-tions, and year-round high solar insolation. One important impactof the microbial loop on mercury cycling (Fig. 4) in the watercolumn is the acceleration of organic matter mineralization andthe regeneration of nutrients to fuel primary production (Fenchel,2008). The accumulation of methyl mercury in prokaryotes(bacterio-plankton) will impact the transfer of mercury into foodwebs, due to the fact that bacterio-plankton can serve as food forzooplankton and small fish (Fenchel, 2008). The nature of metalbinding in microplankton may significantly affect trophic transfer(Ng et al., 2005).

Due to their short life cycles, plankton respond quickly toenvironmental changes in the water column and phytoplanktoncommunity structure can reflect increased eutrophication andchanges in water quality in aquatic systems (Linton and Warner,2003). In tropical Brazilian aquatic ecosystems, cyanobacteria, asignificant component of the marine nitrogen cycle and animportant primary producer in many areas of the ocean, areassociated with MeHg production; however showing low methy-lation potentials (Coelho-Souza et al., 2006).

Coastal eutrophication can affect the cycling of carbon, nitro-gen and phosphorus, increasing primary production and plank-tonic biomass, and changing the biogeochemical cycling ofmercury. Thus, coastal eutrophication can affect metal uptake,

protozooplankton

demersal fish

zooplankton

Kehrig, H.A., 2011

juvenile &planktivorous fish

Me-Hg fluxes through food

Primary production uptakeExcreta

Fig. 4. Microbial loop and trophic transfer of methylmercury (MeH

toxicity and trophic transfer in aquatic food webs (Wang et al.,2001). Under bloom dilution, as the algal biomass increases, theconcentration of MeHg per cell decreases, resulting in a lowerdietary input to the grazer community (zooplankton) and actuallyreducing bioaccumulation in algal-rich eutrophic systems(Pickhardt et al., 2002; Chen and Folt, 2005).

Organisms at the base of food web have been subject of severalstudies of the biological effects of contamination on planktonin coastal ecosystems worldwide (Barwick and Maher, 2003;Stewart et al., 2008; Telesh, 2004; Thompson et al., 2007). Theliterature includes studies in tropical marine ecosystem (Knauerand Martin 1972; Hirota et al., 1979, 1983; Zindge and Desai,1981; Thongra-ar and Parkpian, 2002; Al-Majed and Preston,2000; Al-Reasi et al., 2007; Kehrig et al., 2009a, b; 2010; 2011).

Zooplankton have the ability to accumulate both inorganic andorganic forms of mercury from ingested food and/or directly fromthe dissolved phase (Wang and Fisher, 1998). Copepods have beenshown to assimilate MeHg about twice as efficiently as inorganicmercury (Hginorg) (Lawson and Mason, 1998). Kainz andMazumder (2005) demonstrated that variations in zooplanktonMeHg concentrations can be better predicted assuming a bacterialdiet rather than a phytoplankton diet. Some variations in plank-ton community structure, mainly zooplankton, have been asso-ciated with variations in the concentrations of mercury in fishtissues (Chen and Folt, 2005). Thus, physical and biogeochemicalcharacteristics of the aquatic environment that affect growthdynamics of phytoplankton and the zooplankton communitiesthat depend on them may also affect uptake of mercury into thepelagic-based food web (Stewart et al., 2008).

In the Tropical Pacific Ocean, Hgtot in major zooplankton taxo-nomic groups was measured in order to obtain background ‘‘con-trol’’ data from unpolluted waters. The maximum value of Hgtot

(0.125 mg Hg g�1 dry wt) was found in ctenophore samples from Fijiand the minimum (0.019 mg Hg g�1 dry wt) in thaliaceans fromNortheastern Australia. However, neither a pronounced regionaldifference nor a characteristic difference in connection with thefood web was identified (Hirota et al., 1979). The Hgtot values inthe Hirota et al. (1979) study (average: 0.058 mg Hg g�1 dry wt)

bacteria

phytoplankton

P, Nnutrients

light

POM & DOM

Dissolved Hg+2

DissolvedMeHg

sediments

excreta

excreta

g) through a tropical estuarine food web. From Kehrig, 2011.


were lower than those found previously in zooplankton samples(0.081 to 0.448 mg Hg g�1 dry wt, average: 0.130 mg Hg g�1 drywt) collected between Hawaii and Monterey, California, USA(Knauer and Martin, 1972).

The concentrations of Hgtot in copepods from Minamata Baywere higher (over 0.4 mg Hg g�1 dry wt) than those in the otherregions investigated in a study of three inland seas in WesternJapan (Hirota et al., 1983), suggesting that Minamata Bay was stillpolluted by mercury. Copepods collected in Seto-Naikai had thelowest concentrations (0.08 mg Hg g�1 dry wt), indicating thatthis environment was not polluted by mercury.

Composite zooplankton samples, without any separationaccording to size classes or taxonomic groups, were collectedfrom the Inner Gulf of Thailand from 1976 to 1977. These sampleshad low values of Hgtot (0.0029570.0007 mg g�1 on wet wt),ranging from 0.002 to 0.0045 mg g�1 (Thongra-ar and Parkpian,2002).

Concentrations of Hgtot and MeHg were measured in zooplank-ton samples collected with a 250 mm mesh net in the Gulf of Oman.Total Hg in copepod samples ranged from 0.010 to 0.037 mg g�1

wet wt The mean concentrations were 0.02070.008 and0.02270.008 mg g�1 for the Matrah and A’Seeb sites, respectively.The MeHg fraction of the Hgtot ranged from 1 to 19% (Al-Reasiet al., 2007). The concentration range reported in the Al-Reasi et al.(2007) study was wider than the range determined by Al-Majedand Preston (2000) for samples from Kuwait Bay (0.003–0.010 mgHg g�1 wet wt). MeHg found in these samples accounted for 25%of Hgtot. However, these reported concentrations for Hgtot wellbelow those reported for polluted water bodies such as Bombayharbour (0.103–0.139 mg g�1) (Zindge and Desai, 1981).

In Guanabara Bay, in southeastern Brazil, Kehrig et al. (2009a,b, 2010, 2011) studied mercury cycling as it is influenced byplankton along an ecological gradient from the inner estuary tocoastal waters. The authors demonstrated a change in patternsof mercury cycling according to changes in the plankton commu-nity structure. MeHg and Hgtot were determined in three sizeclasses of autotrophic and heterotrophic microorganisms, 1.2–70 mm (seston, SPM), 70–290 mm (microplankton) and also theZ290 mm plankton components (mesoplankton). Higher MeHgand Hgtot concentrations were significantly correlated withincreasing size class. The increasing ratios of MeHg to Hgtot

(44% for seston, 60% for microplankton and 77% for mesozoo-plankton) reflects a transfer from the lowest trophic level,primary producers (cyanobacteria and diatoms), protist bacter-iophagous (tintinnids) to primary consumers (copepods, nauplii,cladocerans and fish larvae—mesozooplankton), suggesting thatbiomagnification is occurring throughout this food chain.

3.3. The filter feeders, another way up to the top

Mollusks, especially bivalves, are the archetypal sentinelorganisms. This group feeds by filtering particles from the watercolumn. Bivalves are often preyed upon by fishes and marinebirds. So, their participation in mercury transfer along trophicwebs in coastal waters includes a flux through the benthiccommunity, in addition to the pelagic pathway. Being a largetaxonomic group, their role in coastal trophic webs varies widely.In this way, they might either decrease or increase the number oftrophic steps as Hg moves from bacteria/plankton to the apex ofthe aquatic food web (and to humans). Their convenient indivi-dual size and ease of sampling have guaranteed bivalves aprivileged position in the study of mercury bioavailability. Theseanimals are also the main target of governmental and non-governmental monitoring programs, and are widely used inhuman health risk assessments, due to their frequent consump-tion by most socio-economic groups in coastal areas.

The North American National Oceanic and AtmosphericAdministration (NOAA) Mussel Watch program has been collect-ing and publishing information on mercury and other prioritycontaminants in mussels since 1986. The program also coverstropical coasts such as the Gulf of Mexico, Hawaii and Puerto Rico.The sample collection strategy includes species that feed ondifferent average particle sizes (e.g., Mytilidae, Oysters) whichallows a broader understanding of the mercury transport path-ways in coastal ecosystems. The concepts developed under theMussel Watch Program have been expanded to other countriesincluding France, Australia, and Japan (conf. Costa et al., 2000).Coordinated worldwide experiments remain difficult to conduct,but have been attempted in the past (e.g., Mussel WatchInternational—Latin America covered coastal areas from Mexicoto Patagonia). Although such an approach may or may not beadopted as a governmental priority in tropical countries, Hgtot andMeHg concentrations in bivalves are relatively well known, andother temporal series are starting to form, as in Brazil for instance(Costa et al., 2000; Kehrig et al., 2001, 2002, 2006). The specieschosen for these studies have responded to water quality andmercury levels changes in a proportional manner, as has beendemonstrated for Hgtot availability and accumulation duringtranslocation experiments (Fig. 5).

Many species of bivalves are being cultivated in aquaculturefarms. Microbiological and sanitary aspects are the main concernwith these animals and depuration in clean seawater for one totwo days is a common recommendation before consumption ofthese organisms. However, this time does not allow for mercury,or other contaminants to be depurated. This is a growing concern,since mollusks farming is part of governmental policies all overthe tropical world where they may offer animal protein whenfisheries yields are no longer sufficient. The cultivation of bivalvesinvolves less and cheaper technology than fish farming, and hasfaster results. Overall, mollusks aquaculture is more accessible formany coastal populations in tropical countries. Mercury levels incultivated bivalves is usually set by local health authorities, butnot necessarily are based on the WHO recommendations, and thatmight be in disagreement with local ecological conditions andsocial needs.

4. The consumers at risk

As the body size of aquatic organisms increases, the directuptake of dissolved MeHg becomes less important, and trophictransfer becomes the dominant route for uptake and accumula-tion of MeHg (Mason et al., 2000). In all ecosystems, includingtropical and subtropical regions, the biomagnification of methyl-mercury in the food web of consumers strongly dictates theirexposure level. In tropical vertebrates lower mercury concentra-tions are found in primary consumers such as the manatee(Trichechus spp.) (Stavros et al., 2008), low to moderate mercuryconcentrations in sea turtles (Day et al., 2010; Paez-Osuna et al.,2011) and many fish such as catfish species (Cathorops spixii;Azevedo et al., 2009; Barbosa-Cintra, 2010), and the highestmercury concentrations in upper trophic level species or apexpredators.

4.1. The apex predators

As long-lived apex predators, sharks are good indicators formeasuring spatial and temporal trends in MeHg availability fornear-shore tropical marine waters. They are not often protectedby law, and capture and consumption is part of the traditionaldiet of coastal human populations world-wide. Sharks are wellknown for their ability to biomagnify MeHg and contain levels

ng H

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Fig. 5. Total mercury (Hgtot) and methylmercury (MeHg) in Crassostrea rhizophorae (mangrove oyster) transplanted between two estuaries of the Brazilian Northeast. Top

panel: Mercury in suspended particulate matter (ng Hgtot L�1) at experimental sites. March (end dry season), May (early rainy season) and August (late rainy season) 2000.

High tide (H); Low tide (L). White bars contaminated estuary; gray bars non-contaminated estuary. Other panels: White symbols local oysters; Black symbols transplanted

oysters. (a) and (c) contaminated estuary; (b) and (d) non-contaminated estuary. M. F. Costa, N. Sant’Anna Jr. and H.A. Kehrig, unpublished data.


that are unsafe for frequent human consumption. Mercury con-centrations in shark muscle tissue regularly exceed the UnitedStates Environmental Protection Agency (USEPA) action level of0.30 mg Hg g�1 wet wt for many tropical and subtropical watersof the world, including Australia (Lyle, 1984), Belize (Evers et al.,2008b), Brazil (Pinho et al., 2002), and Florida (Adams andMcMichael 1999). Individual sharks that forage on prey relatedto the demersal fish community tend to have higher Hgtot

concentration than more pelagic species (Storelli et al., 2002). Incoastal waters of southern Belize, 101 sharks representing 10species were analyzed for muscle Hgtot levels (Evers et al., 2008b).The highest Hgtot was recorded in bull (Carcharhinus leucas),blacktip (Carcharhinus limbatus), hammerhead (Sphyrna spp.),and nurse sharks (Ginglymostoma cirratum). Over 88% of thesharks sampled exceeded USEPA human health consumptionstandards. Because muscle Hg can be positively correlated withsize for blacktip and nurse sharks (Evers et al., 2008b) and othershark species (Lyle, 1984; Hueter et al., 1995; Lacerda et al., 2000;Pinho et al., 2002), models for confidently predicting muscle Hglevels for species used for human consumption are promising.

Among tropical teleost fish, predatory species such as kingmackerel (Scomberomorus cavalla), and various species of cutlass-fish and grouper are apex predators that can contain elevatedHgtot levels of concern to human health and sustainability of theirpopulations. For example, the goliath grouper (Epinephelus itajara)is a long-lived species. In southern Belize, 40% of goliath grouperindividuals exceeded the USEPA action level of 0.30 mg Hg g�1

wet wt—including all individuals over 55 cm in total length(Evers et al., 2009). While regular consumption of this and other

grouper species by sensitive groups of people, such as pregnantwomen and young children, should be closely monitored thequestion of adverse impacts on this critically endangered speciesis also of concern, especially during complex social behavioursduring spawning aggregations. The Atlantic cutlassfish (Trichiurus

lepturus) has a pan-tropical distribution and has been widely usedas a bioindicator of mercury bioacumulation and biomagnifica-tion (Fig. 1) (Costa et al., 2009). Cutlassfish are highly valued atmarkets and widely consumed by communities living alongsidetropical and subtropical marine ecosystems. Larger individualsmay especially pose a health threat if consumed frequently or byvulnerable human groups (Barletta et al., 2012).

Crocodilians are also at risk to elevated mercury concentra-tions in tropical and subtropical ecosystems, although thresholdlevels of concern are undefined (Rainwater et al., 2007; Vieiraet al., 2011). Marine birds have also been a target for describingmercury exposure in the tropics (Kojadinovic et al., 2007; Catryet al., 2008). However, only a few species such as the white ibis(Eudocimus albus) and great egret (Ardea alba) have been use forlong-term monitoring and assessment efforts for mercury inFlorida (Sepulveda et al., 1999; Frederick et al., 2004, Jayasenaet al., 2011).

Many species of marine mammals inhabit tropical and sub-tropical coastal waters, especially porpoise and dolphins. Broadand wide-ranging prey sources likely dictate the great variabilityin mercury exposure documented (Seixas et al., 2007, 2008; Bisiet al., 2012; Moura et al., 2012). Although the live capture of mostmarine mammals is rare, studies on carcasses are becoming morefrequent along tropical coasts (e.g., Amazon River mouth), helping


to establish a broader ability to assess health and contaminationissues for marine mammals (Moura et al., 2011).

The feeding preferences of the costal dolphins Pontoporia

blainvillei and Sotalia guianensis in south-eastern Brazil wereassessed through the prey’s index of relative importance (IRI),Hgtot and isotopic signatures (d15N and d13C) to compare theirefficiency in the discrimination of prey contribution to thepredators’ diet. The IRI was found to be the best indicator of thedolphins’ prey preferences, while Hgtot and d15N seemed to be abetter indicator of trophic status when the diet was specific ormade up of prey of varying sizes. The d13C values were character-istic of a typical coastal food chain, confirming the preferredhabitat area of these species (Di Beneditto et al., 2011).

4.2. d13C and d15N in studies of mercury trophic transfers in tropical

coastal waters

Mercury levels in fish and marine mammals depend not onlyon the contamination of their environment but also on severalecological factors such as diet and trophic position (Das et al.,2000). Changes in ratios of stable isotopes of carbon (d13C)and nitrogen (d15N) help elucidate trophic relationships withinmarine food webs and to confirm the relationships betweencontaminant uptake and trophic position (Cabana and Rasmussen,1994).

Stable isotope ratios d15N and d13C help to identify organicmatter sources in the food web (Peterson and Fry, 1987), and havebeen used to asses trophic level and trophic transfer of Hgtot inaquatic food webs (Kidd et al., 1995; Al-Reasi et al., 2007; Ikemotoet al., 2008; Evers et al., 2009; Senn et al., 2010).

Several studies on mercury biomagnification and bioaccumu-lation using d13C and d15N in tropical marine food webs havebeen conducted. Al-Reasi et al. (2007) evaluated mercury bio-magnification in zooplankton and fish in the Gulf of Oman.Usinglinear regression modelling of d15N data to infer trophic position(slopes b1¼0.07 and 0.14; r2¼0.09 and 0.11) they reported thatbiomagnification of Hgtot and MeHg was lower than had beenobserved in the Arctic (b1¼0.2 ) (Atwell et al., 1998), or intemperate (b1¼0.29) (Jarman et al., 1996) marine and freshwater(b1¼0.17–0.48) (Kidd et al., 1995) ecosystems. The lower bio-magnification might be due to the fact that tropical marineecosystems generally have high species diversity and complexfood webs. However, the data sets on the relationships betweentrophic position determined by Hgtot and MeHg, and d15N areheterocedastic, preventing the use of some statistical analyses,even if the data are log-transformed. The safe use of Hgtot andMeHg biomagnification, d15N, biological and environmental datawithout mathematical manipulation requires a search for thebetter-fitted distributions, and only then the application of moreadequate statistical analysis becomes possible (Sonesten, 2003;Barletta et al., 2012).

Senn et al. (2010) combined N, C and Hg stable isotopesmeasurements to identify the factors influencing MeHg accumu-lation in fish from the northern Gulf of Mexico (USA), andconcluded that trophic position measured by d15N explainedmost of the variance in log[MeHg] (r2

�0.8). However, coastalspecies in the Mississippi River plume and migratory oceanicspecies derive their MeHg from multiple sources, and both foodwebs have different baseline d15N signatures and (possibly)isotopically distinct MeHg sources.

In the Mekong Delta (South Vietnam), a significant trophiclevel-dependent increase was detected in concentrations ofHg and others trace metals (Ikemoto et al., 2008). Based on thetrophic level assignments estimated from d15N analysis, theauthors suggest that differences in the biomagnification profilesbetween crustaceans and fish species might be due to differences

in metal accumulation and detoxification abilities such as posses-sion of metal-binding proteins (e.g., metallothioneins).

A tropical coastal lagoon located in Southeast Brazil thatreceives runoff from iron ore mining and processing activitieswas studied to assess the differences in trace element accumula-tion patterns in sediment and to investigate relationshipsbetween metal accumulation and trophic status of the organisms(Pereira et al., 2010). Trace element accumulation in biotadepended not only on the trophic position of the organisms butalso on the functional ecological guilds of the species involved.Gastropods (detritivores), showed higher trace element concen-trations than crustaceans and fishes. Although length co-varieswith the trophic position of fish species, it did not influence theconcentrations of trace elements. Moreover, omnivory in fisheswith fast growth may explain the general lack of correlationbetween d15N and trace elements. In the adjacent marine coastalecosystem, when species were grouped according their ecologicaland functional guilds. The values of Hgtot, d15N, and trophic levelincreased significantly from primary producer toward carnivores.

Evers et al. (2009) studied mercury concentrations in goliathgrouper Epinephelus itajara of Belize (Central America), andreported that the stable isotope analysis for d13C and d15Nindicates a broad prey base and a relatively high trophic level.This study also discusses ontogenetic dietary shifts and the Hgexposure in different size classes of grouper. Through biomagni-fication and bioaccumulation of MeHg, older specimens aretherefore at greatest risk of physiological impairment whenperforming complex and coordinated behaviours, such as thoseassociated with spawning aggregations.

In marine systems MeHg uptake and biomagnification in biotadepend not only on mercury input to the ecosystem but also onecological (e.g., ontogenetic phase, diet and trophic position), andenvironmental (e.g., rainfall, salinity, water temperature, sus-pended particulate matter) variables that affect MeHg sourcesand mobilization. If we assume that food availability in density(individuals.m�2) and biomass (g m�2) varies through space andtime (Barletta et al., 2005, 2008), thus influencing bioaccumula-tion and biomagnification, it is important to understand howseasonal fluctuations of the environmental variables influencefood availability at different trophic levels, and consequentlymercury accumulation and biomagnification fluctuations incoastal food webs.

5. Mercury and human health issues in tropical and sub-tropical coastal regions

On a global scale, the main pathway of Hg exposure to humans isthe ingestion of contaminated seafood (2.4 mg MeHg day�1 person�1,WHO), and this is most likely the major pathway of mercuryexposure for coastal populations in the tropics and sub-tropics. Localand regional impacts may differ considerably from global averagesdue to variations in the speciation of mercury emissions, pollutantdispersion, and dietary habits (Fig. 1). Understanding these differ-ences will require more detailed studies on local and regional scales.

This form of low-level exposure is probably more wide-spreadthan extreme cases of coastal pollution because it affects thehuman populations throughout their lives. Recent evidence onlow-level mercury exposure also shows mercury effects on end-points such as cardiovascular, immunologic, and birth outcomes(Karagas et al., 2012). But, with the exception of the Seychellesstudy, this issue has rarely been investigated by health authoritiesin human populations along tropical coasts. So, the delicatebalance between the benefits from fish eating and the risks dueto Hg exposure (Mergler et al., 2007; Oken et al., 2012) is difficultto establish.


Some of these native coastal populations have lived in relativeisolation for many decades. With the expansion of urban areas,the increased value of coastal tourism and the informationrevolution, these groups have emerged as active stakeholders.These populations are now the target of a number of sociologicalstudies (e.g., Diegues, 2008), but these rarely include healthassessments of mercury body burdens. Therefore, their realmercury contamination is unknown, but is suspected to besignificant, based on the parallels with their Amazonian counter-parts. They may have any number of nutritional deficits andendemic health problems (e.g., anaemia), aggravated by extremepoverty, malnutrition, inbreeding, intestinal parasites, and otheruntreated illnesses, including decompression sickness (Guebert-Bartholo et al., 2011b). In these communities there has often anearly complete dependency on aquatic resources, includingpractically all animal groups occurring in tropical coastal envir-onments. The intensification of contact with other groups canalter their dietary patterns and preferences (Sant’Anna et al.,2001), possibly due to access to other sources of animal proteinthat can be bought at markets (beef, pork and chicken), moreeasily and at better prices than fish or other seafood. These fooditems have become part of the culture, either by cultural coloni-zation or because high quality fish (apex predators) are no longeravailable. This dietary shift can ‘‘dilute’’ the mercury burden inthese populations and, at the same time, divert the seafood (andits associated mercury burden) to other markets where highly-valued seafood is sold.

Many marine fisheries are near collapse due to over-fishingand environmental degradation, and aquaculture (also referred toas mariculture and/or fish-farming) has become a significantalternative for the supply of protein to human and domesticanimal populations. However, as human population grows out ofcontrol, we will have to rely less on animal protein, especiallyseafood since most fisheries are already beyond sustainablelevels. Aquaculture will never be more than a minor source ofprotein. But the sustainability of these operations, and the safetyof the food thus produced, are nevertheless issues of concern. Forexample, mariculture operations may not be aware of the mer-cury burden in fish food, nor the impacts of this on the Hgconcentrations in the seafood that is being produced. With theexception of algae and filter feeders (e.g., Crassostrea spp., Mythi-lidae, Pekten), farmed species are generally omnivores that needsome amount of animal protein in their diets, and therefore havethe potential to biomagnify mercury from their feed to their finalhuman consumers.

Mercury use in amalgamation for gold ore mining has been amajor source of mercury pollution to terrestrial aquatic environ-ments. Occupational exposure of gold miners and their familieshas therefore received attention from health authorities acrosstropical regions such as the Amazon, for example (Hacon et al.,2008a, b). On the other hand, large-scale mining, chlor-alkali andother industrial plants, and coal burning, are the major sources ofmercury to coastal and marine environments, contributing Hgcontamination through river discharge and atmospheric deposi-tion. Regulation of industrial mercury emissions is contentiousbecause it should include the consideration of costs and benefits.The estimation of benefits is complex, partially because mercurycontamination is a global phenomenon and therefore benefitsneed to be assessed on a global scale. However, costs are usuallyassigned to someone, especially local governments. Abatementof mercury pollution can be cost-effective depending on themarginal costs which, in turn depend on available control techno-logies and specific local conditions. For example, in terms ofabsolute magnitude, the social costs due to IQ loss fromlow-level Hg exposure are low, but given the small amount ofmercury involved and the potential number of children affected,

the marginal cost is high when compared to other pollutants(Spadaro and Rabl, 2008).

Therefore, mercury environmental monitoring should includestudies of at-risk and control groups, since there are no consistentbackground values against which to compare mercury levels inthreatened human populations. It will be necessary to establishlocal/regional threshold or ‘‘background’’ mercury exposure levelsand mercury concentrations, in order to conclude whether apopulation is or is not statistically different from those withsimilar cultural, occupational and dietary habits. Proposals forintegrated projects with traditional populations of fishers intropical coastal areas should include objectives such as: (1) thecalculation of human exposure to mercury and other pollutantsthrough seafood consumption, especially for pregnant womenand children; (2) living resources and environmental servicesconservation to guarantee the survival of endangered species andsocioeconomically important seafood stocks; (3) assessment ofnutritional quality from traditional diets in order to suggest moreefficient and protective use of protein sources; (4) implementationof sustainable aquaculture projects; (5) educating local andregional ‘‘target’’ populations about the relative risks and benefitsfrom seafood consumption as a complimentary option to focusingsolely on reducing Hg releases to the environment (Spadaro andRabl, 2008).

6. Conclusions and recommendations

Tropical countries facing mercury pollution problems need tobe involved in research and monitoring of coastal environmentsfrom sources to sinks, and must recognize the risks it poses tohuman health and ecosystem preservation. Because of an histor-ical focus on mercury pollution in freshwater ecosystems, manymarine habitats in developing countries within the tropics remainunder-sampled with respect to mercury contamination. Moreprocess-oriented research is needed to answer questions suchas: (1) How are ecosystem functions and services affected bychanging mercury burdens through time and space, and how dothese factors affect the various biogeochemical Hg cycling pro-cesses? (2) To what extent have we already altered the mercurycycles and increased the mercury levels in coastal ecosystems ofthe tropical and subtropical belts by modifying river dischargeand increasing atmospheric transport and deposition?

Long term monitoring of mercury sources and cycling in theseenvironments has been limited (Evers et al., 2008a), and shouldbe established at ecosystem scales that also consider the impactsof human activities. Suitable locations for ecosystem-based stu-dies have been defined through international efforts to divide themajor marine habitats into ‘‘homogeneous areas’’ (e.g., LargeMarina Ecosystems – LME, Global International Water Assess-ment – GIWA and the Census of Marine Biodiversity) and studiesin these areas must consider the impacts from mercury pollution.New statistical approaches (e.g., long time series) are recom-mended for pre-existing and newly generated data, in order tofurther explore for information that might have a wider ecologicalsignificance. The inclusion of the most relevant environmentalvariables in monitoring programs (Barletta et al., 2012), distrib-uted across broad spatial and temporal scales, and the expandeduse of sentinel animal models is important (Evers et al., 2008a;Costa et al., 2009). Marine Conservation Units and fisheriesgrounds should be priority areas for such experiments andprograms. Before sampling and monitoring programs go out inthe field, the guarantee of quality data on mercury concentrationsand speciation, in the myriad of environmental, biologicaland human matrices must be assured by all candidate labora-tories that intend to participate in research and provide input to


policy-makers via participation in international intercalibrationexercises.

Some of the challenges to mercury biogeochemical research intropical coastal environments are the extreme climatic andenvironmental conditions in the tropics (e.g., high temperature;wide fluctuations of salinity and turbidity between rainy and dryseasons) and different socioeconomic conditions, even within thesame national territory. These conditions lead to high variabilityin many aspects of the mercury cycle. Biological turnover ratesare high throughout the year. Overfishing and over-pollution areserious threats to marine biodiversity in addition to invasivespecies, altered water temperature, ocean acidification, increasingfrequency of hypoxia events, expansion of aquaculture opera-tions, and maritime traffic. These are worldwide phenomena, andare threatening marine species of ecological and economicimportance. Direct and indirect anthropogenic mercury inputsin the tropics need reliable identification, quantification, andmonitoring. Climate change will inevitably alter rainfall regimesand river flow patterns. Deforestation and intense land use foreconomic development will also change the characteristics andecological services of river basins. In combination, these willprobably alter the cycling processes and bioavailability of mer-cury in coastal areas. Each of these areas have different sensitiv-ities to these various threats, however, water pollution is rankedhigh (3rd) in most cases. Understanding the synergistic andcumulative impacts of mercury and other pollutants within theframework of environmental change due to these multiple stres-sors is recognized as a challenge for the future.

Climate change can also increase the erosion of soils inmangrove areas, where large amounts of organic carbon, andpossibly mercury (Marchand et al., 2006), are presently stored.Connectivity between the terrestrial, coastal, and pelagic envir-onments and their biological communities will serve to transmitthe damages (Newton et al., 2012). Global climate change mayhave impacts on mercury cycling beyond those expressed directlyat the local and regional level, and we will not be able to predictthose impacts without a much better understanding of the ratesand mechanisms of biogeochemical mercury cycling. For example,biotic and photochemical reduction and re-emission of mercuryfrom the land and ocean are already significant terms in theglobal mercury budget. If global warming increases the reductionrates (and the subsequent re-emission rates), the mercury burdenmay be shifted by long-range atmospheric transport from morepolluted urbanized regions (such as North America and Europe) toless-polluted areas like tropical coastal environments. Accelera-tion of the reduction/emission/atmospheric oxidation/depositioncycle should lower the concentrations of bioavailable Hg(II) inaquatic systems (reducing fish mercury), while higher tempera-tures coupled with coastal eutrophication may enhance MeHgformation by expansion of suboxic and anoxic environments(increasing fish mercury). Changes in the chemical speciation ofHg(II) and MeHg due to ocean acidification will alter theirbioavailability in ways that we cannot reliably predict at present.Expansion of the tropics due to climate change (Seidel et al., 2008)will spread tropical coastal biological species, and their associatedmercury contamination issues, to higher latitudes in a matter of afew centuries.

High population densities and poverty result in poor land andwater resources use, including interference in trophic websthrough overfishing, for example. The rapidly increasing price ofland in urban centres and the economic development of somenations will set a trend towards the cremation of bodies, insteadof the conventional burial. This could increase the atmosphericdeposition of mercury near cremation facilities unless theiremissions are tightly controlled to prevent the release of reactiveoxidized gaseous mercury or aerosol mercury. Economic growth

and development also involves building more houses, roads andinfrastructure in general, which requires more metal and cementprocessing (resulting in more local and regional emissions ofmercury). Landfills, a known source of mercury to coastal envir-onments when poorly managed, will expand in numbers and in areaand volume. Tourism in coastal areas is increasing. The enhance-ment of tourism, especially eco-tourism, will encourage greater use,and impact upon, pristine areas, where development will inevitablyoccur. Such development inevitably leads to impacts on coastalenvironments, and steps must be taken to minimize the negativeimpacts of development. For example, the ecological services pro-vided by mangrove habitat will be at least partially impaired,especially with respect to sequestration of mercury in sediments.

The increase in coastal/maritime tourism and internationaltrade (shipping) due to the globalized economy will require morefrequent and deeper port maintenance. Dredging may become amore frequent activity due to poor conservation practices in theupland river basins. Many countries in the tropics have nocontrols or regulations on dredging activity or dredge spoildisposal, and this may increase the risk of mercury contamina-tion. Nations benefiting from these economic and social changesneed to cooperate on a global scale to evaluate the environmentalcosts from altered mercury cycling and to find appropriate waysto minimize or mitigate the negative impacts. Records frommuseum and biological specimen collections (Hill et al., 2010)and sediment cores (Xu et al., 2011) may contribute to theassessment of global and local conditions and their quantitativeand qualitative changes over time and space.

International collaboration can bring benefits that have a low-cost/high-impact effects on mercury research. Oceans and Seas

comprise an entire section of the United Nations report ‘‘Thefuture we want’’, and the participation of marine researchers iscalled upon in a number of other sections regarding the issuesdiscussed in this paper: coastal and marine pollution, oceans andhuman health, aquaculture, fisheries, food security, and capacitybuilding. In paragraph 221, mercury is specifically cited: ‘‘Wewelcome the on-going negotiating process on a global legallybinding instrument on mercury to address the risks to humanhealth and the environment and call for a successful outcome ofthe negotiations.’’ (UN, 2012). There is a need for research andmonitoring that can answer questions such as: are we changing,for better or for worse, the mercury cycling in coastal areas? Canglobal actions such as the Global International Water Assessment(GIWA) and the Agreement on Agriculture (AoA) take mercuryinto account, enhancing the collection of existing data, thegeneration of new knowledge, and the transformation of thisinformation to governments and other decision-makers?

Supra-national institutions (e.g., WHO, IAEA, UNEP, FAO) havean important role to play in the compilation of mercury emissionsand for supporting basic research on Hg cycling in countries of thetropical and subtropical belts. The goals of these institutions shouldbe focused on the transference/seeding of financial resourcesfor research and health care, and also on the identification andorganization of priority actions designed for each geographicalregion and for the various impacted human populations. In addi-tion, international aid to strengthen analytical and diagnosticcapabilities with respect to mercury pollution is welcome, espe-cially when a country may not have the funding, facilities, andhuman expertise to evaluate its own status concerning the impactsof mercury on their people and their environment. As theirmissions are re-defined and altered into the future, it will beimportant for these institutions to maintain an emphasis regardingmarine mercury research, seafood advisories, environmental mon-itoring and source control.

Many countries in the tropics and sub-tropics need assistancewith setting up appropriate seafood consumption advisories for


mercury (e.g., UNEP INC 1 to 5). Human exposure to mercury fromwild and farmed fish and shellfish are likely to be quite different,and establishing appropriate consumption standards for thegeneral population as well as at-risk populations should be partof every sustainable fisheries certification, since it is a matter offood security in many countries. Where they already exist,consumption standards for wild and farmed fish and shellfishshould be evaluated and revised when necessary. The establish-ment of such standards is an urgent action where they do notalready exist. Because of geographical variations in human cul-tures (dietary choices) and in climate and fauna (thus variationsin mercury cycling), it is important to recognize that consumptionstandards have to be determined at the appropriate national,regional, and perhaps even local scales.

We will have to constantly balance the desire to preserveecosystems and biological diversity against the needs of society(human health and food supply). Governments and NGOs mustcooperate to provide the funding that is needed to address thesecritical scientific and sociological research issues. The eradicationof Poliomyelitis through voluntary vaccination of children in mostcountries of the world is probably the best example where people,independent of culture, responded well to a serious health threatwhen correctly addressed by their governments. Improvements ininformation technology will continue to enhance the disseminationand availability of data (and other information) on mercury issuesthat will help to define the nature and scope of future ecosystemresearch programs as well as to translate the information tosociety. Scientists, governments, and non-governmental agenciesneed to cooperate to identify key research gaps, promote capacitybuilding, promote opportunities for experts to meet and exchangeknowledge, support low-cost, open access, publications targeted todecision makers as well as other scientists, develop new analyticaland pollution-abatement technologies and environmental manage-ment techniques, and support international collaboration at alllevels for all stakeholders (Costello et al., 2010).

Acknowledgments

MFC, MB, OM, JCM, SH are CNPq Fellows. This publication wasmade possible by NIH Grant Number P42 ES007373 from theNational Institute of Environmental Health Sciences. Its contentsare solely the responsibility of the authors and do not necessarilyrepresent the official views of NIH. Authors listed according totheir contribution to the work. Dr. Celia Y. Chen is thanked for hercritical reading during different phases along the preparation ofthe manuscript and careful work as guest editor of the C-Mercpapers at ER.

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