barbosa&2003

8/6/2019 Barbosa&2003

1/12

Mercury Biomagnification in a Tropical Black Water, Rio Negro, Brazil

A. C. Barbosa,1 J. de Souza,2 J. G. Dorea,3 W. F. Jardim,4 P. S. Fadini5

1 Instituto Brasileiro do Meio Ambiente (IBAMA), Bras lia, Brazil2 Instituto de Qumica, Universidade de Braslia, Braslia, Brazil3 Faculdade de Ciencias da Saude, Universidade de Braslia, C. P. 04322, 70919-970 Braslia, DF, Brazil4 Instituto de Qumica, Universidade de Campinas (UNICAMP), Campinas, Brazil5 PUC, Campinas, Brazil

Received: 10 September 2002/Accepted: 8 March 2003

Abstract. The population living along the riverbanks of the

Amazon basin depends heavily on fish for nutritional support.Mono-methyl-mercury (MMHg) concentrates in fish, which can

contaminate humans, the risk depending not only on fish MMHg

concentration but also on the amount of fish consumed. We

sampled nine locations of the Rio Negro basin, differing in water

pH, Hg concentrations, and dissolved organic carbon (DOC), and

determined total Hg from 951 fish samples of species representa-

tive of the food web: herbivorous, detritivorous, omnivorous, and

piscivorous. Mercury concentrations varied widely in all species

but showed a trend that depended on fish feeding strategies. The

highest mean concentration was found in the piscivorous species

(688.90 ng/g1), followed by omnivorous (190.30 ng/g1), detri-

tivorous (136.04 ng/g1), and herbivorous (70.39 ng/g1). Fish

Hg concentrations exceeding current safe limits (500 ng/g1) for

human consumption were found mainly in the piscivorous species(60%). Significant positive correlation between fish weight and

Hg concentration was seen for the piscivorous Serrasalmus spp.

(n 326; r 0.3977; p 0.0001), Cichla spp. (n 125; r

0.4600; p 0.0001), and Pimelodus spp. (n 12; r 0.8299;

p 0.0008), known locally as Piranha, Tucunare, and Mandi,

respectively. However, a negative correlation was seen for non-

piscivorous Potamorhina latior(n 30; r0.3763; p 0.0404)

and Leporinus spp. (n 44; r3987; p 0.0073), known as

Branquinha (detritivorous) and Aracu (omnivorous). Fish-Hg con-

centrations in the acidic waters (pH range, 4.096.31) of the Rio

Negro habitat, with its wide gradient of Hg concentrations (3.4

11.9 g/L1) and DOC (1.8515.3 mg/L1)but no history of

gold mining activityare comparable to other Amazonian rivers.

Opportunity fish catches in the Rio Negro habitat show highmuscle-Hg derived from natural sources, but no systematic asso-

ciation with site-dependent geochemistry.

Mercury (Hg) is widespread in the environment and is an impor-

tant food contaminant that, under special circumstances, can cause

neuromotor disturbances and neuropathies. It occurs naturally in

three oxidation states Hg0

, Hg1

, and Hg2

. A series of complexchemical transformations allows Hg to cycle in the environment,

but methylation is the most important step for Hg entry to the

aquatic food chain. Fish is the highest bioaccumulator of mono-

methyl-mercury (MMHg) and serves as an indicator of Hg con-

tamination of aquatic systems. Mercury concentration in fish de-

pends on species feeding strategies and, within a species, the age

and size of the fish as well as water parameters related to acidity

and Hg speciation. Therefore, contamination of fish-eating popu-

lations will depend not only on the quantity of fish consumed, but

also on the species of choice.

MMHg bioaccumulation in aquatic systems varies consider-

ably with food-chain structure and length. It can be simplified

with plankton at the base (zooplankton as the primary consum-

er), followed by small forage fishes (secondary consumers) andpiscivorous fishes (tertiary consumers) where higher MMHg

concentrations are expected (Nichols et al. 1999). However,

even within a food trophic category, fish species present a

variety of feeding strategies that influence MMHg acquisition.

In the Amazonian ecosystem, and the Rio Negro in particular,

fish feeding strategies may change on a seasonal basis (Goul-

ding et al. 1988). Fish physiology and environmental interac-

tions with regards to Hg bioaccumulation are not well under-

stood, and in the Amazonian ecosystem, little is known

regarding Hg trophic transport along the food chain.

Artisanal gold extraction from alluvial deposits in rivers of

the Amazonia is carried out without regulations and causes

great environmental damage, regardless of country. The meth-

ods used involve hydraulic dismount of river terraces and

dredging of watercourses. In terrace dismount, miners use

water jets to remove land strips, while pumps are used in water

courses. Mercury is used to improve gold recovery by amal-

gamation and all discarded material is put back into rivers,

causing turbidity and shoaling (Kligerman et al. 2001). In areas

of intensive gold-mining activity, a gradient of fish-Hg con-

centration was suggested (Uryu et al. 2001). Some have done

research, attempting to relate the direct impact of gold-mining

activities and fish-Hg concentration (Lima et al. 2000; Hy-

lander et al. 1994). Although the environmental damage due to

alluvial gold extraction is enormous, with disruption and de-Correspondence to: J. G. Dorea; email: [email protected]

Arch. Environ. Contam. Toxicol. 45, 235246 (2003)DOI: 10.1007/s00244-003-0207-1

A R C H I V E S O F

EnvironmentalContaminationa n d Toxicology 2003 Springer-Verlag New York Inc.

8/6/2019 Barbosa&2003

2/12

struction of aquatic ecosystems (Kligerman et al. 2001), the Hg

balance showed the metal discharged from gold-mining activ-

ities accounted for less than 1% of the total Hg (Fadini and

Jardim 2001). Furthermore, extensive deforestation and agri-

cultural developments (that also occurred in the 1970s and

1980s), were environmentally destructive and may have im-

pacted on the release of Hg from soil (Roulet et al. 1999).

Recent work is unveiling the dynamics of environmental Hgin the Amazonian ecosystem showing that Hg is released from

sediment and soil. Roulet et al. (2001) showed that Hg con-

centrations of the Amazon basin rivers (Arapiunas, Tapajos,

and Amazon) are governed by the concentrations of suspended

particles. They also found that the dominant stock of Hg in the

aquatic ecosystem is derived from soil erosion. Indeed, Ol-

iveira et al. (2001) showed that the upper horizon of the

Amazon soil receives an important contribution from anthro-

pogenic activity95% of the total. This includes fire defores-

tation, agriculture, and gold-mining activities. However, a

complex hydrological cycle in which some flooded plains can

be covered by 615 m of water for six or more months adds

confounding variables to the origin of Hg in the aquatic food

chain.Riverbank inhabitants of the Amazon are heavily dependent

on fish for their daily nutritional sustenance and therefore are

exposed to the easily absorbed MMHg consumed in contami-

nated fish. For these populations, fish is a culturally important

food resource occurring naturally and in abundance. A survey

of Rio Negro riparians showed that fish is eaten at least once a

day (7.1%), but that most of them (78.6%) consumed it at least

twice a day (Barbosa et al. 2001). Per capita fish intake has

been estimated as 200 g/day1 (Barbosa et al. 1995). These

populations benefit greatly from this excellent source of high-

quality protein, macronutrients, and micronutrients, especially

its unique source of highly unsaturated fatty acids.

To identify the sources and fate of environmental Hg, and toenrich the Hg ecotoxicological studies in Amazonia, a moni-

toring program was established in 1995 in the Rio Negro basin,

aimed at sampling soils, water, sediment, air, rainwater, fish,

and hair from riverine populations. Studies of hair-Hg specia-

tion of the riverbank population and environmental Hg mass-

balance have already been published (Barbosa et al. 2001;

Fadini and Jardim 2001). In order to understand fish-Hg bio-

accumulation we studied muscle-Hg concentrations in a large

number of fish representative of all stages of the trophic chain.

Materials and Methods

The Rio Negro basin has distinctive physicochemical characteristics

and does not have a recent history of gold-mining activities along its

tributaries (Figure 1). Its catchment spreads over an area of 690 103

km2, representing around 14% of the total area of the Brazilian

Amazon, and it has well-defined seasons of high and low waters, with

an average annual rainfall of 2000 mm. The Rio Negro joins the Rio

Solimoes to form the Rio Amazonas (Figure 1), with an average flow

of 29,000 m3/s1 at Manaus. As part of an ongoing monitoring project

for Hg contamination of the Amazon basin we surveyed the Rio Negro

from March of 1998 to August of 2001. We sampled fish at nine

specific locations (see map, Figure 1) and determined total Hg in fish

species. The fish sampled were representative of the feeding hierarchy:

herbivorous, detritivorous, omnivorous, and piscivorous. A previous

publication (Fadini and Jardim 2001) described the protocol for sam-

pling soils, sediments, water, and respective Hg concentrations. Per-

tinent data regarding water pH, Hg concentrations, and DOC are

summarized in Table 1.

The fish were caught by local professional fisherman, identified

(Ferreira et al. 1998), weighed, and measured for length. Approxi-

mately 20 g of muscle samples were immediately taken, frozen to be

transported, and analyzed in the laboratory at the University of Bra-

slia. The samples were digested with concentrated HNO3

. For 0.4 g of

sample, 4 mL of acid was added and then digested for 20 min in amicrowave system DGT-100 Provecto Sistemas Analticos, with

power between 0 and 800 W. After digestion, the sample is cooled

until the temperature reached 25C (room temperature), transferred to

a 25-mL volumetric flask. Then, 1.5 mL of a 6% KMnO4 solution and

0.8 mL of a 1% hydroxylamine solution were added to the volumetric

flask. All measurements were carried out by cold vapor atomic ab-

sorption spectroscopy (AAS-CV), using a Hg monitor of LDC Ana-

lytical, Model 1255. All glassware used in the analytical protocol was

washed clean, rinsed with both KOH and double-distilled water, and

left to rest in 50% HNO3

for 24 h. It was then rinsed again in

double-distilled water, and dried at 100C for 12 h.

Precision and accuracy of Hg determinations were assured by the

use of internal standards prepared in our laboratory and used in

intercalibration exercises among Brazilian laboratories. Our laboratory

is also a participant in the Mercury Quality Assurance Program forFish (Department of Fisheries and Oceans, Central and Artic Region,

Fresh Water Institute, Winnipeg, Canada), that began in 1992. Our

performance was considered acceptable with 94% 2 s.d. (n 16)

for fish.

Summarized data (mean, s.d., and ranges), Pearson correlation be-

tween variables, and analysis of variance, were performed using a SAS

(SAS Institute, Cary, NC, USA). We also summarized and compared

data of total fish-Hg concentration from other water bodies in Ama-

zonia and Central Brazil.

Results

Results of fish-Hg concentrations and respective range of fish

weight are organized according to feeding strategies in Table 2.

Fish weight and Hg concentrations in this habitat show a wide

variation. However, the species at the top of the food chain had

the highest concentrations of muscle-Hg. Median Hg concen-

trations were higher in predatory and lowest in herbivores

species. In the piscivorous category, Tucunares (Cichla spp.),

Piranhas (Serrasalmus spp.), and Peixe Cachorro (Hydrolycus

scomberoids) comprised 70% of the catch and showed the

highest mean Hg concentrations.

Bioaccumulation of Hg is further illustrated by its distribu-

tion according to fish trophic level presented in Figure 2. Most

of the fish (75%) in the herbivorous group showed Hg concen-

trations below 100 ng/g1, while most of the samples (65%) inthe piscivorous group showed Hg concentrations above 400

ng/g1.

A summary of physicochemical characteristics of the sam-

pled aquatic habitat is integrated with fish-Hg concentrations in

Figure 3. Abiotic parameters that influence fish-Hg concentra-

tions showed variability among sites with regards to pH (4.09

6.31), DOC (1.8515.3 mg/L1), and water-Hg concentration

(3.411.9 g/L1). Sorting fish-Hg by feeding strategy did not

show a consistent trend as a function of these water parameters,

except for the piscivorous category. Collectively, predatory

species showed a tendency to increase muscle-Hg with wa-

ter-Hg concentrations and dissolved organic carbon (DOC). In

236 A. C. Barbosa et al.

8/6/2019 Barbosa&2003

3/12

spite of a three-fold increase in water-Hg concentration and aeight-fold increase in DOC, there was no apparent impact of

muscle-Hg concentrations of nonpredatory species.

The correlation data between fish weight and Hg concentra-

tion by species is presented in Table 3. Significant correlations

were seen for the piscivorous Serrasalmus spp. (n 326; r

0.3977; p 0.0001), Cichla spp. (n 125; r 0.4600; p

0.0001), and Pimelodus spp. (n 12; r 0.8299; p 0.0008).

Among other fish groups, significant correlations were seen

positively for Triportheus elongates (n 33; r 0.4588; p

0.0073), and negatively for Potamorhina latior (n 30; r

0.3763; p 0.0404).

To consolidate information on fish-Hg concentration in the

Amazon, a summary of reports is organized in Table 4 as afunction of water bodies (rivers, lakes, and reservoirs). No

salient feature in fish-Hg concentration can be distinguished

from rivers with intense gold-mining activities.

Discussion

The fish-Hg concentrations in the nonpolluted freshwater of the

Rio Negro habitat are in the upper range of values reported for

the Amazon rain forest and central wetlands with recent history

of gold mining (Table 4). A wide variation of fish-Hg bioac-

Fig. 1. Map of Rio Negro basin indicating sampling sites

Table 1. Location and physicochemical characteristics of the Rio Negro sampling sites

Local names Latitude S Longitude W

Water parameters

Hg

(ng/kg1)

DOC

(mg/L1) pH

(1) Rio Marauia 0.29910 65.20425 4.68 6.0 5.48

(2) Rio Padauar 0.13460 64.10531 4.25 9.5 4.09

(3) Rio Demini 0.44400 62.86000 3.4 6.0 4.93

(4) Foz do Rio Demini 0.77040 62.93433 3.4 3.8 4.93

(5) Barcelos 0.96676 62.90600 7.6 15.3 4.2

(6) Carvoeiro 1.33350 62.06350 9.5 10.7 4.8

(7) Vila da Cota 1.24862 61.88785 4.23 1.9 6.3

(8) Camanau 1.95500 61.20983 4.8 13.1 5.3

(9) Maependi 2.12905 61.03116 6.9 15.4 4.8

Site numbers correspond to Figure 1.

DOC is dissolved organic carbon.

Mercury Biomagnification in Rio Negro, Brazil 237

8/6/2019 Barbosa&2003

4/12

cumulation is expected because of the diversity in fish feeding

strategies involving mobility, foraging location, migratory

traits, as well as differences in Hg metabolism for each species.

In spite of a wide range of Hg bioconcentration between and

within fish trophic rank, this work clearly shows that the

dominant feature in Hg propagation is an increase in mus-

cle-Hg with increasing hierarchy of fish feeding strategy. Most

of the Hg found in fish is MMHg and in the Amazonian

ecosystem it represents 62100% of total Hg (Lacerda et al.

1994; Akagi et al. 1995; Malm et al. 1995b; Palheta and Taylor

1995; Guimaraes et al. 1999; Brabo et al. 2000).

Fish-Hg variation in rivers of the Amazon basin is wide and

a systematic comparison is difficult, not only because of habitatdiversity, but also because of incomplete information (Table 4).

Fish local names may change from region to region, and there

is also insufficient knowledge of fish feeding hierarchy, that is,

some fish may change food acquisition strategies during its life

cycle (Goulding et al. 1988). Coupled with that, most studies

do not report fish size (length or weight), nor age, important in

controlling the random nature of fish sampling. Such difficul-

ties limit comparison and causes confusion when drawing

conclusions on the diversity of the Amazonian ecosystem. The

complexity of inherent variability of fish-Hg bioaccumulation

is best illustrated by reports on Tucunares (Cichla spp.), a fish

commonly found and consumed throughout Amazonia (Table

4). With regards to sample size, while we analyzed 126 spec-

imens, others studied modest numbers such as four (Akagi et

al. 1995), six (Bidone et al. 1997a; Guimaraes et al. 1999), ten

(Santos et al. 2000a), 11 (Hacon et al. 1997), or 17 (Santos et

al. 2000b). Such small numbers compromise conclusions that

gold-mining activities impact on Hg concentrations for this

species (Guimaraes et al. 1999).

In tertiary-consumer fish, Hg is frequently reported to increase

as a function of age and size (length or weight). This association

was found in the freshwater Amazon ecosystems, although in a

seemingly inconsistent way. While no significant correlation was

reported for Tucunares in impacted and nonimpacted lakes of

north Amazon (Guimaraes et al. 1999) or in the Rio Madeira(Malm et al. 1997), some studies reported a positive correlation

for Tucunares (Castilhos et al. 2001), Trara, and Caratinga (Brabo

et al. 2000). Contrary to this, significant negative correlation

between fish-Hg concentration and fish weight, were reported by

Lima et al. (2000) in piscivorous species (Trara and Tucunare).

We also found a positive correlation between weight and Hg

concentration for Tucunares and Piranhas (Table 3) with a larger

number of samples (126 and 327, respectively), but not for Tra ra

(n 24). We found a negative correlation only for Branquinha

(Potamorhina latior), a detritivorous fish. Irrespective of trophic

level, fish-Hg concentration varies considerably, even when fish

age (size or weight) is considered. In this study, not all predator

Table 2. Fish weight and total mercury concentration in fish species according to feeding strategies

Common name Scientific name n

Weight (g)Hg range

(ng/g1)Min Max Median

Piscivorous

Agulha Potamorrhaphis spp. 16 68 420 1,065.5 254.81,408.0

Barba-chata Goslinia platynema 7 269 1,235 881.4 448.51,572.7

Bico-de-pato Sorubim lima 4 61 121 226.7 113.9388.6Jacunda Crenicichla reticulata 4 296 680 181.0 153.0606.8

Mandi Pimelodus spp. 12 17 745 125.2 60.42,024.0

Mandube Ageneiosus brevifilis 28 52 390 493.2 242.61,321.2

Peixe-cachorro Hydrolycus scomberoides 83 19 783 652.4 114.55,437.4

Pescada Plagioscion spp. 26 202 790 401.5 160.41,064.3

Piranha Serrasalmus spp. 327 18 1,653 320.0 15.01,713.7

Sorubim Pseudoplatystoma fasciatum 3 433 830 349.4 204.40436.0

Trara Hoplias malabaricus 24 124 2,020 301.7 120.11,592.1

Tucunare Cichla spp. 26 102 5,000 448.5 39.22,441.0

Omnivorous

Acara Acarichthys heckellii 15 102 560 132.0 69.0778.4

Acara preto Heros spp. 28 46 525 179.0 10.0506.6

Acaras Satanoperca spp. 20 65 469 180.0 47.8677.0

Aracu Leporinus spp. 44 40 682 95.9 10.0516.0

Cangat Parauchenipterus galeatus 10 143 217 93.1 40.4114.7Orana Hemiodus immaculatus 18 22 99 102.0 32.0170.0

Piaba Hemigrammus spp. 4 39 66 203.5 124.0368.0

Sardinha Triportheus elongatus 33 59 442 32.0 5.3476.5

Detritivorous

Acari-bodo Liposarcus pardalis 3 54 690 64.0 21.071.0

Arraia Potamotrygon scorbina 8 1,500 15,000 112.4 47.1189.1

Branquinha Potamorhina latior 30 41 334 85.9 23.0450.1

Jaraqui Semaprochilodus taeniurus 18 248 570 106.8 16.2207.3

Herbivorous

Cubiu-orana Anodus melanopogon 4 104 149.0 39.5 24.349.7

Pacu Mylossoma aureum 25 94.0 836.0 18.1 2.2186.0

Pacu branco Myleus torquatus 34 70.0 324.0 22.6 10.085.0


8/6/2019 Barbosa&2003

5/12

species showed a significant positive correlation between mus-

cle-Hg and fish weight (Table 3). This may be due to variability in

prey-Hg levels, the Hg chemical form in the water column and in

food material, or differences in fish physiology (Hg-depuration

rate). Rate constant of Hg loss in studied species is very low and

inversely correlated with fish size (Trudel and Rasmussen 1997).

Stafford and Haines (2001) discussed circumstances under which

fish-Hg bioconcentration and biodilution occur and recommended

that fish age should be included in contamination studies.

The origin of Hg in the Rio Negro waters does not include

industrial activities and there is no history of intensive gold-mining in upstream tributaries. The physicochemical charac-

teristics of the Rio Negro basin were discussed in a parent

publication indicating that 99.74% of its Hg would be of

natural sources (Fadini and Jardim 2001). Therefore, fish-Hg

contamination cannot be directly related to Hg released during

gold amalgamation. Instead, other anthropogenic activities re-

lated to deforestation by fire and agricultural practices may

play an important role in the release of natural Hg from soils.

As a consequence, abiotic parameters (pH, DOC, water-Hg

concentrations) are the most important determinants of Hg-

methylation and its acquisition and retention by fish. In the

Amazonian waters of Surinam, Mol et al. (2001) observed that

piscivorous species from freshwater habitats showed higher Hg

concentrations than those from estuarine and ocean habitats,while estuarine habitats showed the lowest Hg concentrations

for both piscivorous and nonpiscivorous species.

Natural Hg release and methylation potential are associated

with geochemistry and complex human activities, while Hg

acquisition, accumulation, and biomagnification by fish are

associated with the Hg chemical form in food material and fish

physiology. The Hg released during alluvial goldmining was

previously thought to contaminate the river biota, especially

fish, and ultimately the riverine population through their fish

consumption. Such studies used Hg concentration in fish mus-

cle and human hair as biomarkers of Hg pollution following

gold-mining activities in the Amazonian rivers. A gradient of

fish-Hg concentrations were proposed for the Rio Tapajos(Uryu et al. 2001)presently showing the most intense gold

mining activityto address Hg pollution that was assumed to

be caused by gold-mining activity. In the biochemical com-

plexity of a tropical rain forest like the Amazon, environmental

predictors of Hg acquisition by primary consumers, or biomag-

nification in tertiary consumers (predatory fish), are difficult to

trace to Hg released from gold-mining activity. Furthermore,

the rapid changes in land use coincided with the alluvial gold

rush. Table 4 shows that the ranges of mean fish-Hg concen-

trations in the Tapajos and other impacted rivers are not sys-

tematically higher. Mercury concentrations in freshwater fish

of the Rio Negro basin are comparable to those of other

Amazonian rivers (Table 4). Kehrig and Malm (1999) showed

that Hg concentrations in piscivorous species of the Balbinareservoir (also not impacted by gold mining, but in the Rio

Negro catchment) are among the highest in the Amazonia.

The interplay of Hg geochemistry among sampling sites

showed that gradients of pH, water-Hg, and DOC were not coin-

cident (Figure 3). Therefore fish-Hg (by food-chain rank) and

site-dependent, Hg geochemistry could be singled out. It is appar-

ent that preformed MMHg from animal sources is the primary

modulator of fish-Hg bioconcentration. The gradients of either Hg

(threefold) or DOC (eightfold) in the water column had no pro-

portional impact on nonpredatory species. Instead a tenfold in-

crease in fish-Hg concentration between extremes of feeding ranks

(herbivorous versus piscivorous) seemed to exist along all levels

Fig. 2. Percent distribution as a function of Hg concentrations in fish

samples organized by feeding strategies


8/6/2019 Barbosa&2003

6/12

Fig. 3. Hg concentrations in fish sam-

ples organized according to water pa-

rameters


8/6/2019 Barbosa&2003

7/12

of the water physicochemical parameters (pH, water-Hg, and

DOC). In this context, the constant challenge of water-Hg and

acidity is much less important than the preformed MMHg present

in the food material. Indeed, as already observed, Hg uptake for all

fish species occurs mainly from food, with biomagnification being

dominant in predatory species (Vigh et al. 1996). The retention of

Hg in muscle is operative in aquatic and terrestrial species, man

included. Reviewing the subject, Sweet and Zelikoff (2002)

showed that fish is more tolerant to Hg toxicity than humans and

coincidently shows a half-life of Hg in muscle one order of

magnitude higher than humans.Fish consumption advisories must take into consideration the

fundamental aspects of human ecology of the Amazonias riverine

population, which depends on fish for food security. As a constant

dietary item, fish is a good source of nutrients, high in protein and

available lysine, and with a good biological value (Batterham et

al. 1979) that balances the protein-poor starchy food consumed by

many (Araujo et al. 1975). With regards to other nutrients, small

fish are rich in available iodine (Toure et al. 2001) and other trace

elements (copper, zinc, iron, and manganese), as well as calcium

(Larsen et al. 2000), which compensates for the lack of dairy

products in riverines diet (Giugliano et al. 1984). Fish is also

known to enhance zinc (Garcia-Arias et al. 1993) and vegetable-

iron absorption (Larysse et al. 1968). Amazonian fish of higher

trophic level accumulate selenium (Dorea et al. 1998), whichcounteracts the toxic effect of Hg. According to Inhamuns and

Franco (2001), Amazonian fish are also a specific source of

omega-3 polyunsaturated fatty acids (PUFA; decosahexanoic [22:

6] acid and eicosapentaenoic [20:5] acid). As well as this, in the

human ecology of the Rio Negro ribeirinhos, fish have also

medicinal uses (Begossi et al. 2000).

As a result of legitimate concern over the extensive environ-

mentally-destructive alluvial gold mining and Hg release into the

Amazon rivers, there are fish consumption advisories aimed at

diminishing risk of MMHg intake. Work with the fish-eating

population of the Amazon has suggested that Hg contamination

could be reduced by changing the pattern of fish consumption

(Akagi et al. 1995; Boischio et al. 1995; Lebel et al. 1997).

Balancing the risks and benefits of fish consumption for indige-

nous populations was highlighted by Egeland et al. (1997). Clark-

son (1995) casts doubt on the application of advised safe upper-

limits of MMHg naturally bioaccumulated in fish. Indeed the

MMHg concentrations in aquatic mammals, such as the whale

(Clarkson 1995), are relatively higher than in most piscivorous

species reported in the Amazon basin (Table 4). The threat of

destruction of the fragile Amazonian ecosystem by gold-mining

activities is serious enough and raised world concern for curbing

additional release of Hg (Hylander 2001). Nevertheless, advisoriesof fish restriction for the ribeirinhos may prove disruptive for their

strategies of food security and maintenance of nutritional status

with unforeseen consequences. With regard to their current health

problems, changes of fish consumption for the Rio Negro ribeir-

inhos does not guarantee them better health.

Conclusions

The Rio Negro has no history of gold-mining activity. Never-

theless, its fish-Hg concentrations are among the highest in the

Amazon rain forest. Fish-Hg concentration is a consequence of

preformed MMHg in the natural material of the fish food chain.Although relatively high fish-Hg concentrations above 500

ng/g1 (wet weight) do occur in older (larger) predatory spe-

cies, Hg concentrations above 1,000 ng/g1 (wet weight) are

infrequently caught when subsistence fishing. Given the health

benefits of fish consumption to the Rio Negro ribeirinhos,

advisories for changes in food habits that curtail fish intake

may bring unforeseen consequences.

Acknowledgments. We thank the Rio Negro population for support

and participation in the study. We also thank Ms. Fatima Barretto of

Table 3. Summary of data correlating weight and mercury concentration in fish

Common name Scientific name

Feeding

strategy n r p

Agulha Potamorrhaphis spp. P 16 0.2514 0.3477

Cachorro Hydrolyeus scomberoides P 83 0.064 0.9536

Mand Pimelodus spp. P 12 0.8299 0.0008

Mandube Ageneiosus brevifilis P 28 0.3171 0.1002

Pescada Plagioscion spp. P 26 0.0129 0.9502Piranha Serrasalmus spp. P 326 0.3977 0.0001

Trara Hoplias malabaricus P 24 0.3629 0.0813

Tucunare Cichla spp. P 125 0.4600 0.0001

Acara Acarichthys heckellii O 15 0.4755 0.0733

Acaras Satanoperca spp. O 20 0.2448 0.2983

Acara-preto Heros spp. O 28 0.1644 0.4033

Aracu Leporinus spp. O 44 0.3987 0.0073

Orana Hemiodus immaculatus O 18 0.1038 0.6820

Sardinha Triportheus elongatus O 33 0.4588 0.0073

Braquinha Potamorhina latior D 30 0.3763 0.0404

Jaraqui Semaprochilodus taeniurus D 18 0.0413 0.8709

Pacu Mylossoma aureum H 25 0.1318 0.5301

Pacu branco Myleus torquartus H 34 0.2366 0.1780

P piscivorous; O omnivorous; D detritivorous; H herbivorous.


8/6/2019 Barbosa&2003

8/12

Table 4. Summary of Hg concentrations (ng/g1) in muscle of fish caught in the water bodies of the Amazonia and central wetlands (Pan-

tanal)

Sampling site

Feeding

strategy

Range of

mean Hg Local name Weight (kg)

Amapa Rivers

Guimaraes et al. 1999 P (342650) Tucunare (range) (0.311.05)

P (240269) Tucunare (range) (0.40.54)

P 197549 Trara, Piranha, Tucunare NG

Bidone et al. 1997b P 305742 Tucunare, Piranha, Pirarucu, Aruana, Itu, Jacunda, Jeju, Uena NG

O 351,225 Aracu, Cachorro de Pedra, Cara, Manduba, Matrinxa, Pacu

Branco, Taumata

NG

Andira River

Eve et al. 1996 P 5101,390 Tucunare, pescada NG

O 100 Acara

Balbina Reservoir

Kehrig et al. 1998 P 130700 Tucunare, Cachorro, Piranha NG

O 60 Acara-Tinga

Kehrig and Malm 1999 P 320 Tucunare, Cachorro, Piranha, Trara NG

O 60 Acara

Colombian Rivers

Olivero et al. 1997 P 5161 Surubim NG

N-P 48150 Sardinha NG

Olivero and Solano 1998 P 195322 Trara, Pescada NG

N-P 386 Sardinha NG

Olivero et al. 1998 P 501,130 Mandube, Trara, Surubim, Bico de Pato, Mandi, Pescada NG

French Guyana Rivers

Frery et al. 2001* P (1,4258,736) NK NG

O (256556) NK NG

D (116242) NK NG

H (8115) NK NG

Mol et al. 2001 P 1801,150 Piranha, Trara, Pescada, Tucunare NG

Richard et al. 2000 P 2201,113 Tucunare, Traira, Piranha, Mandube 0.0186

N-P 99230 Orana preta, Sardinha NG

Madeira Basin

Barbosa et al. 1995 (See details in Boischio et al. 2000)

Barbosa et al. 1997 (See details in Boischio et al. 2000)

Boischio and Henshel2000 P 2301340 Cara-Acu, Filhote, Piranha, Cachorro, Pescada, Jacundaa,Apapa, Surubim, Barba Chata, Tucunare, Bico de Pato,

Jeju, Piramitaba, Dourada, Jandira, Caparar , Trara,

Pirarucu

0.1826

D 110900 Tamoata, Cascudo, Jaraqu, Curimata, Bodo, Branquinha,

Ubarana, Mapara

0.070.53

O 1701440 Cubiu, Mandi, Cara, Cuiu-cuiu, Sardinha, Aruana, Pintadinho,

Pirarara, Aracu, Matrinxa

0.114.9

H ND360 Pacu, Bacu, Pirapitinga, Jatuarana, Tambaqui 0.318.3

Boischio et al. 1995 P 220740 Piranha, Barba-Chata, Dourada, Tucunare 0.235

O 1201,900 Aruana, Mandi, Sardinha, Aracu, Cara, 0.10.97

H 100360 Jatuarana, Pacu, Pirapitinga, Tambaqu, 1.1408.290

D 110240 Curimata, Jaraqu, Cascudo, Branquinha 0.070.56

Gali 1997 P 670 NG NG

Guimaraes et al. 1999 P 846 NG NG

Kehrig and Malm 1999 P 570 Tucunare, Cachorro, Piranha, Mapara, NGO 150 Pacu, Sardinha, Piau

D 180 Branquinha, NG

Lechler et al. 2000 280420 Matrinxa 3545 cm

Malm et al. 1990 P 702,700 Dourado, Filhote, Piranna, Tucunare, Pirarucu 0.4520

NP 80210 Curimata, Jatuarana 0.3430.520

Malm et al. 1995a P 700 NG NG

O 130 NG NG

Malm et al. 1997 P 846 NG NG

Maurice-Bougoin et al.

2000

P 491,522 Cachorro, Bagre, Dourado, Pintado, Surubim 0.1216.3

H 994 Jatara, Tambaqui, Pacu 0.74.5

Maurice-Bougoin et al.

1999

P 7121,819 Cachorro, Bagre, Dourado, Pintado, Surubim NG


8/6/2019 Barbosa&2003

9/12

Sampling site

Feeding

strategy

Range of

mean Hg Local name Weight (kg)

O 8129 Griso, Panete, Sabalo, Pacu Sabalo

D 55 Sabalo

Pfeifer et al. 1989 P 702,700 Dourado, Filhote, Pintado, Pirarucu NG

NP 210 Curimata, NG

Pfeifer et al. 1991 P 702,700 Dourado, Filhote, Pintado, Tucunare, Pirarucu NG

NP 80210 Curimata, Jatuarana NGReuther 1994 P 3401,330 Tucunare, Pintado, Piranha, Peixe-cachorro, Traira, Apapa,

Dourado, Filhote

NG

NP 120490 Acara, Mapara, Mandi, Curimata NG

Manu River

Gutleb et al. 1997 P 391,544 Surubim, Piranha NG

NP 51102 Mandi, Branquinha NG

Negro Basin

Kehrig and Malm 1999 P 610 Tucunare, Aruana, Cachorro, Piranha NG

D 90 Branquinha, Cara, Aracu

This study P 1811635 (See Table 2)

NP 18203 (See Table 2)

Tapajos Basin

Akagi et al. 1995 P 803,820 Dourada, Jau, Piraba, Mandube, Cachorro, Trara, Apapa,

Pescada, Tucunare, Filhote, Pirarucu

0.140

O 170280 Acara, Aruana 0.160.515H 100 Pacu 1.43

Bidone et al. 1997a P 100690 Tucunare, Piranha, Cachorro, Surubim, Jacunda, Mandi,

Pescada, Trara, Piracmuntaba

NG

O 52100 Acaratinga, Aracu, Matrinxa

H 3787 Pacu, Jaraqui

Brabo et al. 1999 (same as Brabo et al. 2000)

Brabo et al. 2000 P 174419 Tucunare, Trara, Barbado, Piranha, Surubim, Aruana, NG

O 95120 Caratinga, Jandia, Aracu, Mandia

H 42112 Jaraqu, Pacu,

Castilhos et al. 1998 P 60690 Apapa, Cachorro, Dourada, Filhote, Jacunda, Mandi, Pescada,

Piramutaba, Saranha, Piranha, Surubim, Trara, Tucunare

NG

O 16100 Acara-Acu, Acara-Tinga, Aracu, Curimata

D 36149 Jaraqui, Mapara, Matrinxa

H 1284 Pacu, Tambaqui

Castilhos et al. 2001 P NG Tucunare

Castilhos and Bidone

2001

P NG (See Castilhos et al. 2001)

Hacon et al. 1997 P 2802,750 Piraiba Jau, Pescada, Pintado, Dourada, Trara, Piranha,

Tucunare

NG

H 8080 Pacu, Curimata.

Hacon et al. 2000 P 3001000 Tucunare, Jau, Pintado 0.32.8

H 10170 Pacu, Matrinxa, Curimata 0.13.5

Kehrig and Malm 1999 P 140810 Tucunare, Trara NG

H 50 Aracu NG

Lebel et al. 1997 P 90800 Apapa, Barbado, Filhote, Mandi, Pescada, Piracatinga,

Piranha, Sarda, Surubim, Jiju, Tucunare, Jacunda, Dourada,

Cachorro, Trara, Pirarucu

NG

H 40110 Aracu, Caratinga, Pacu

O 130400 Caraucu, Mandube, Saranha, SardinhaLima et al. 2000 P 125306 Dourada, Cachorro, Pescada, Piranha, Sarda, Surubim,

Tucunare

0.311,420

H 3069 Pacu, Pirapitinga, Tambaqu, Aracu 0.2280.71

Malm et al. 1995b P 690 NG NG

Malm et al. 1997 P 482 NG NG

Martinelli and McGrath

1999

P (25776) Pirarucu 20

Moreton and Delves

1998

NG 92,575 NG NG

Palheta and Taylor 1995 P 110610 Tucunare, Trara NG

O 30210 Acara, Cachorrinho de Padre, Trara

H 40 190 Pacu, Piaba

Santos et al. 2000a P 529 NG NG


8/6/2019 Barbosa&2003

10/12

8/6/2019 Barbosa&2003

11/12

(2000) Mercury contamination of fish and exposures of an indig-

enous community in Para State, Brazil. Environ Res 84:197203

Castilhos ZC, Bidone ED, Lacerda LD (1998) Increase of the back-

ground human exposure to mercury through fish consumption due

to gold mining at the Tapajos River region, Para State, Amazon.

Bull Environ Contam Toxicol 61:202209

Castilhos ZC, Bidone ED (2001) Hg biomagnification in the ichthyo-

fauna of the Tapajos River Region, Amazonia, Brazil. Bull Envi-

ron Contam Toxicol 64:693700Castilhos ZC, Bidone ED, Hartz SM (2001) Bioaccumulation of

mercury by Tucunare (Cichla ocellaris) from Tapajos River re-

gion, Brazilian Amazon: A field dose-response approach. Bull

Environ Contam Toxicol 66:631637

Clarkson TW (1995) Environmental contaminants in the food chain.

Am J Clin Nutr 61:682S686S

Dorea JG, Moreira MB, East G, Barbosa AC (1998) Selenium and

mercury concentrations in some fish species of the Madeira River,

Amazon Basin, Brazil. Biol Trace Elem Res 65:211220

Egeland GM, Middaugh JP (1997) Balancing fish consumption bene-

fits with mercury exposure. Science 278:19041905

Eve E, Oliveira EF, Eve C (1996) The mercury problem and diets in

the Brazilian Amazon: Planning a solution. Environ Conserv

23:133139

Fadini PS, Jardim WF (2001) Is the Negro River Basin (Amazon)

impacted by naturally occurring mercury? Sci Total Environ 275:

7182

Ferreira EJG, Zuanon JAS, Santos GM (1998) Peixes Comerciais do

Medio Amazonas: Regiao de Santarem, Para. Edicoes IBAMA,

Brasilia (in Portugese)

Frery N, Maury-Brachet R, Maillot E, Deheeger M, de Merona B,

Boudou A (2001) Gold-mining activities and mercury contamina-

tion of native Amerindian communities in French Guiana: Key

role of fish in dietary uptake. Environ Health Perspect 109:449

456

Gali PA (1997) Contaminacao mercurial em peixes carnivoros dos

Rios Madeira, Jaci Parana e Jamari-Rondonia. B.Sc. Thesis. Fed-

eral University of Rondonia, Porto Velho, Brazil

Garcia-Arias MT, Castrillon AM, Navarro MP (1993) Bioavailabilityof zinc in rats fed on tuna as a protein source in the diet. J Trace

Elem Electrolytes Health Dis 7:2936

Giugliano R, Shrimpton R, Marinho HA, Giugliano LG (1984) Estu-

dos nutricionais das populacoes rurais da Amazonia. II. Rio Ne-

gro. Acta Amazonica 14:427449

Goulding M, Carvalho ML, Ferreira EG (1988) Rio Negro, rich life in

poor water. SPB Academic Publishing, The Hague

Guimaraes JRD, Fostier AH, Forti MC, Melfi JA, Kehrig H, Mauro

JBN, Malm O, Krug JF (1999) Mercury in human and environ-

mental samples from two lakes in Amapa, Brazilian Amazon.

Ambio 28:296301

Gutleb AC, Schenck C, Staib E (1997) Giant otter ( Pteronura brasil-

iensis) at risk? Total mercury and methylmercury levels in fish and

otter scats, Peru. Ambio 26:511514

Hacon S, Rochedo ER, Campos R, Lacerda LD (1997) Mercury

exposure through fish consumption in the urban area of Alta

Floresta in the Amazon Basin. J Geochem Explor 58:209216

Hacon S, Yokoo E, Valente J, Campos RC, da Silva VA, de Menezes

ACC (2000) Exposure to mercury in pregnant women from Alta

Floresta-Amazon Basin, Brazil. Environ Res 84:204210

Hylander LD, Silva EC, Oliveira LJ, Silva AS, Kuntze EK, Silva DX

(1994) Mercury levels in Alto-PantanalA screening study. Am-

bio 23:478484

Hylander LD, Pinto FN, Guimaraes JR, Meili M, Oliveira LJ, Castro

e Silva E (2000) Fish mercury concentration in the Alto Pantanal,

Brazil: Influence of season and water parameters. Sci Total Envi-

ron 261:920

Hylander LD (2001) Global mercury pollution and its expected de-

crease after a mercury trade ban. Water Air Soil Pollut 125:331

344

Inhamuns AJ, Franco MRB (2001) Composition of total, neutral and

phospholipids in mapara (Hypophtalmus sp.) from the Brazilian

Amazonian area. J Agric Food Chem 49: 48594863

Kehrig HA, Malm O, Moreira I (1998) Mercury in a widely consumed

fish Micropogonias furnieri (Demarest, 1823) from four main

Brazilian estuaries. Sci Total Environ 13:263 271

Kehrig HD, Malm O (1999) Methylmercury in fish as a tool forunderstanding the Amazon mercury contamination. Appl Orga-

nomet Chem 13:689696

Kehrig HD, Malm O, Akagi H, Guimaraes JRD, Torres JPM (1998)

Methylmercury in fish and hair samples from the Balbina reser-

voir, Brazilian Amazon. Environ Res 77:8490

Kligerman DC, La Rovere EL, Costa MA (2001) Management chal-

lenges on small-scale gold mining activities in Brazil Env Res

87:181198

Lacerda LD, Bidone ED, Guimaraes AF, Pfeiffer WC (1994) Mercury

concentrations in fish from the Itacaiunas-Parauapebas River sys-

tem, Carajas region, Amazon. An Acad Bras Cienc 66:373379

Lacerda LD, Pfeiffer WC, Marins RV, Sousa CMM, Rodrigues S,

Bastos WR (1991) Mercury dispersal in water, sediment, sand

aquatic biota of a gold mining tailing deposit in Pocone, Brazil.

Water Air Soil Pollut 55:238294Larsen T, Thilsted SH, Kongsbak K, Hansen M (2000) Whole small

fish as a rich calcium source. Br J Nutr 83:191196

Layrisse M, Martinez-Torres C, Roche M (1968) Effect of interaction

of various foods on iron absorption. Am J Clin Nutr 21:1175

1183

Lebel J, Roulet M, Mergler D, Lucotte M, Larribe F (1997) Fish diet

and mercury exposure in a riparian Amazonian population. Water

Air Soil Pollut 97:3144

Lechler PJ, Miller JR, Lacerda LD, Vinson D, Bonzongo JC, Lyons

WB, Warwick JJ (2000) Elevated mercury concentrations in soils,

sediments, water, and fish of the Madeira River basin, Brazilian

Amazon: A function of natural enrichments? Sci Total Environ

260:8796

Lima APD, Muller RCS, Sarkis JED, Alves CN, Bentes MHD, Brabo

E, Santos ED (2000) Mercury contamination in fish from San-

tarem, Para, Brazil, Environ Res 83:117122

Lodenius M, Malm O (1998) Mercury in the Amazon. Rev Environ

Contam Toxicol 157: 2552

Malm O, Castro MB, Bastos WR, Branches FJP, Guimaraes JRD,

Zuffo CE, Pfeiffer WC (1995a) An assessment of Hg pollution in

different goldmining areas, Amazon Brazil. Sci Total Environ

175:127140

Malm O, Branches FJ, Akagi H, Castro MB, Pfeiffer WC, Harada M,

et al. (1995b) Mercury and methylmercury in fish and human hair

from the Tapajos river basin, Brazil. Sci Total Environ 175:141

150

Malm O, Guimaraes JRD, Castro MB, Bastos WR, Viana JP, Branches

FJP, et al. (1997) Follow-up of mercury levels in fish, human hair

and urine in the Madeira and Tapajos basins, Amazon, Brazil.

Water Air Soil Pollut 97:4551

Malm O, Pfeiffer WC, Souza CMM, Reuther R (1990) Mercury

pollution due to gold mining in the Madeira River, Brazil. Ambio

19:1115

Martinelli MC, McGrath D (1999) Mercury accumulation in the pira-

rucu Arapaima gigas Cuvier (1918) in the Lower Amazonian

varzea. Bol Mus Par Emilio Goeldi-Zool 15:722

Maurice-Bourgoin L, Quiroga I, Guyot JL, Malm O (1999) Mercury

pollution in the Upper Beni River, Amazonian Basin: Bolivia.

Ambio 28:302306

Maurice-Bourgoin L, Quiroga I, Chincheros J, Courau P (2000) Mer-

cury distribution in waters and fishes of the upper Madeira rivers

and mercury exposure in riparian Amazonian populations. Sci

Total Environ 260:7386


8/6/2019 Barbosa&2003

12/12

Mol JH, Ramlal JS, Lietar C, Verloo M (2001) Mercury contamination

in freshwater, estuarine, and marine fishes in relation to small-

scale gold mining in Suriname, South America. Environ Res

86:183197

Moreton JA, Delves HT (1998) Simple direct method for the deter-

mination of total mercury levels in blood and urine and nitric acid

digests of fish by inductively coupled plasma mass spectrometry.

J Anal At Spect 13:659665

Moraes LAF, Lenzi E, Luchese EB (1997) Mercury in two fish speciesfrom the Parana River floodplain. Parana, Brazil. Environ Pollut

98:123127

Nico LG, Taphorn DC (1994) Mercury in fish from gold-mining

regions in the upper Cuyuni River system, Venezuela. Fresenius

Environ Bull 3:287292

Nichols J, Bradbury S, Swartout J (1999) Derivation of wildlife values

for mercury. J Toxicol Environ Health B Crit Rev 2:325355

Oliveira SMB, Melfi AJ, Fostier AH, Forti MC, Favaro DIT, Boulet R

(2001) Soils as an important sink for mercury in the Amazon.

Water Air Soil Pollut 126:321337

Olivero J, Navas V, Perez A, Solano B, Acosta I, Arguello E, Salas R

(1997) Mercury levels in muscle of some fish species from the

Dique Channel, Colombia. Bull Environ Contam Toxicol 58:865

870Olivero J, Solano B (1998) Mercury in environmental samples from a

waterbody contaminated by gold mining in Colombia, South

America. Sci Total Environ 217:8389

Olivero J, Solano B, Acosta I (1998) Total mercury in muscle of fish

from two marshes in goldfields, Colombia. Bull Environ Contam

Toxicol 61:182187

Palheta D, Taylor A (1995) Mercury in environmental and biological

samples from a gold mining area in the Amazon region of Brazil,

Sci Total Environ 168:6369

Pfeiffer WC, de Lacerda LD, Malm O, Souza CMM, da Silveira EG,

Bastos WR (1989) Mercury concentrations in inland waters of

gold-mining areas in Rondonia, Brazil. Sci Total Environ 87/88:

233240

Pfeiffer WC, Malm O, Souza CMM, de Lacerda LD, da Silveira EG,

Bastos WR (1991) Mercury in the Madeira River ecosystem,Rondonia, Brazil. Forest Ecol Manag 38:239 245

Porvari P (1995) Mercury levels of fish in Tucurui hydroelectric

reservoir and in River Moju in Amazonia, in the state of Para,

Brazil. Sci Total Environ 175:109117

Reuther R (1994) Mercury accumulation in sediments and fish from

rivers affected by alluvial gold mining in the Madeira River Basin,

Brazil. Environ Monit Assess 32:239 258

Richard S, Arnoux A, Cerdan P, Reynouard C, Horeau V (2000)

Mercury levels of soils, sediments and fish in French Guiana,

South America. Water Air Soil Pollut 124:221244

Roulet M, Lucotte M, Canuel R, Farella N, Goch YGD, Peleja JRP, etal. (2001) Spatio-temporal geochemistry of mercury in waters of

the Tapajos and Amazon rivers, Brazil. Limnol. Oceanogr 46:

11411157

Roulet M, Lucotte M, Farella N, Serique G, Coelho H, Passos CJS, et

al. (1999) Effects of recent human colonization on the presence of

mercury in Amazonian ecosystems. Water Air Soil Pollut 112:

297313

Santos EO, Jesus IM, Brabo ES, Loureiro EC, Mascarenhas AF,

Weirich J, et al. (2000a). Mercury exposures in riverside Amazon

communities in Para, Brazil. Environ Res 84:100107

Santos LS, Muller RC, de Sarkis JE, Alves CN, Brabo ES, Santos EO,

Bentes MH (2000b) Evaluation of total mercury concentrations in

fish consumed in the municipality of Itaituba, Tapajos River

Basin, Para, Brazil. Sci Total Environ 261:18

Stafford CP, Haines TA (2001) Mercury contamination and growthrate in two piscivore populations. Environ Toxicol Chem 20:

20992101

Sweet LI, Zelikoff JT (2002) Toxicology and immunotoxicology of

mercury: A comparative review in fish and humans. J Toxicol

Environ Health 4:161205

Trudel M, Rasmussen JB (1997) Modeling the elimination of mercury

by fish. Environ Sci Technol 31:17161722

Toure F, Stoecker BJ, Lucas E (2001) Fish and shrimp provided

bioavailable iodine for rats fed cassava/millet-based diets. FASEB

J 15:A635 (Abstract)

Uryu Y, Malm O, Thornton I, Payne I, Cleary D (2001) Mercury

contamination of fish and its implications for other wildlife of the

Tapajos Basin, Brazilian Amazon. Conserv Biol 15:438 446

Vigh P, Mastala Z, Balogh KV (1996) Comparisons of heavy metal

concentration of grass carp (Ctenopharyngodon idella Cuv. et

Val.) in a shallow eutrophic lake and a fish pond (possible effects

of food contamination). Chemosphere 32:691701


barbosa&2003

Documents