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Spatial and seasonal mercurydistribution in the Ayapel Marsh,Mojana region, ColombiaJosé Marrugo-Negrete a , Luís Norberto Benítez b , Jesús Olivero-Verbel c , Edineldo Lans a & Felipe Vazquez Gutierrez da Grupo de Aguas, Química Aplicada y Ambiental, University ofCórdoba , Montería, Colombiab Department of Chemistry , Universidad del Valle , Cali,Colombiac Environmental and Computational Chemistry Group, Universityof Cartagena , Cartagena, Colombiad Laboratorio de Fisicoquimica Marina, Instituto de Ciencias delMar y Limnologia, Universidad Nacional Autonoma de Mexico ,MexicoPublished online: 14 Dec 2010.

To cite this article: José Marrugo-Negrete , Luís Norberto Benítez , Jesús Olivero-Verbel , EdineldoLans & Felipe Vazquez Gutierrez (2010) Spatial and seasonal mercury distribution in the AyapelMarsh, Mojana region, Colombia, International Journal of Environmental Health Research, 20:6,451-459, DOI: 10.1080/09603123.2010.499451

To link to this article: http://dx.doi.org/10.1080/09603123.2010.499451

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Spatial and seasonal mercury distribution in the Ayapel Marsh, Mojana

region, Colombia

Jose Marrugo-Negretea*, Luıs Norberto Benıtezb, Jesus Olivero-Verbelc,Edineldo Lansa and Felipe Vazquez Gutierrezd

aGrupo de Aguas, Quımica Aplicada y Ambiental, University of Cordoba, Monterıa, Colombia;bDepartment of Chemistry, Universidad del Valle, Cali, Colombia; cEnvironmental andComputational Chemistry Group, University of Cartagena, Cartagena, Colombia; dLaboratoriode Fisicoquimica Marina, Instituto de Ciencias del Mar y Limnologia, Universidad NacionalAutonoma de Mexico, Mexico

(Received 9 December 2009; final version received 6 May 2010)

Geographical and temporal changes of total mercury (T-Hg) concentrations insediments, macrophytes and fish were evaluated in the Ayapel Marsh, Mojana,Colombia. Sampling was conducted during 2006–2007, including both rainy anddry seasons, and T-Hg was measured using atomic absorption spectroscopy.Distribution of T-Hg in sediments and the macrophyte Eichhornia crassipesshowed that higher concentrations were found along the flooding pathway of theCauca River. Hg has also polluted the food chain. Highest T-Hg concentrationsin fish were detected for the carnivorous Pseudoplatystoma fasciatun(0.432 + 0.107 mg/g, fresh weight [fw]), and lowest in the non-carnivorousProchilodus magdalenae (0.143 + 0.053 mg/g, fw), with differences betweentrophic levels. T-Hg for fish samples (0.298 + 0.148 mg/g, fw) did not exceedthe limit consumption level (0.50 mg/g, fw). It is concluded that mercury-pollutedsediments from the Cauca River, contribute to Hg deposition into the AyapelMarsh. Accordingly, interventions must be conducted to decrease Hg accumula-tion in fish.

Keywords: Ayapel; Mojana; mercury; fish; sediments; macrophyte; flooding;Colombia

Introduction

Mercury (Hg) is one of the metals with highest impact on aquatic ecosystems due tothe biotic exposure to methylmercury (MeHgþ), a highly toxic ionic compoundderived from biomethylation of Hg that bioaccumulates and biomagnifies in thefood chain (WHO 1989; Uryu et al. 2001; Ullrich et al. 2001; Wiener and Suchanek2008). It has been established that for tropical ecosystems, MeHgþ is the main formof Hg in aquatic biota; in particular in benthic macro invertebrates and fish (Lacerdaet al. 1994; Morel et al. 1998), consequently, the major source of human exposure toHg is fish consumption (Kehrig et al. 1998; WHO 1990). Hg can also be present inplants. In fact, in tropical freshwater marshes with abundant aquatic macrophytes,

*Corresponding author. Email: jlmarrugon@yahoo.com

International Journal of Environmental Health Research

Vol. 20, No. 6, December 2010, 451–459

ISSN 0960-3123 print/ISSN 1369-1619 online

� 2010 Taylor & Francis

DOI: 10.1080/09603123.2010.499451

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these can also be important for Hg methylation (Guimaraes et al. 1998, 2000; Mauroet al. 2001), and can be used to monitor heavy metal pollution (Pfeiffer et al. 1986).

In Latin America, particularly in countries such as Colombia, gold mining is themayor contributor to Hg pollution. It has been estimated that from 1987–1997,approximately 30 tons per year were released in this country as a result of thisactivity (Malm 1998). Despite the magnitude of the problem, only few studies havebeen reported on mercury distribution around different Colombian environments(Olivero et al. 1997; Olivero-Verbel et al. 2002, Marrugo-Negrete et al. 2008).

Among the most important freshwater fishing resources in Colombia is theAyapel Marsh in the Mojana region. During rainy seasons with heavy rainfall,flooding events occur and the streams from the Cauca River, a body of water thatreceives Hg from a large number of gold mines (Marrugo-Negrete 2007), reaches themarsh and discharges Hg-polluted sediments into it. The aim of this paper was totest the hypothesis that Hg distribution in the marsh varies geographically dependingon the sediment input from the Cauca River, and also that this pollution has beenincorporated into the food chain.

Materials and methods

Study area

The Ayapel Marsh has an area of approximately 180 km2. It is located in northwestColombia (88170788240 N and 75840775890 W), at 25 m above sea level andapproximately 50 km from the largest gold production area in the country (southernBolivar and northeast Antioquia). The mean annual precipitation and temperatureare 2260 mm and of 278C, respectively. In addition, around this site (15 km from thesoutheast side), the basin floodplains interchange water with the Cauca River thatcarries gold mining residues. The maximum water level has been observed from Julyto November and the lowest in March. The dry season occurs from January untilApril, and the rainy season from May to December.

Sample collection and analysis

Sampling was conducted at 11 sampling stations (Figure 1) from September 2006 toMarch 2007, covering both rainy and dry seasons. Superficial sediment samples wereobtained lowering a Van Veen grab from a boat. At each station four samples werecollected at all cardinal points within a 3 m radius from a reference point, and thenmixed together to generate a composite sample per station. Samples were placed inplastic bags, labeled and packed in ice, transported to the laboratory, and dried in anoven at 408C for 48 h (Canario et al. 2007).

Samples of the macrophyte Eichhornia crassipes were manually collected atstations 2 and 6 (S2 and S6), washed with water from the marsh and cleaned withdistilled water before being packed in plastic bags, refrigerated and transported tothe lab, where samples were washed again with distilled water and dried on papertowels at room temperature. Fish species belonging to different trophic levels werecollected during fishing campaigns with local fishermen. Those species were selectedbased on their economical importance and abundance in the marsh. After measuringlength, fish were eviscerated, placed individually into a plastic bag, labeled andtransported on ice to the lab. Samples for analyses were obtained from the dorsalmuscle dissected with a plastic knife and analyzed fresh (Olivero and Solano 1998).

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Mercury analysis

Total mercury (T-Hg) concentrations were determined following US EnvironmentalProtection Agency (US EPA 1994) recommendations. First, sediment samples weredigested with mercury-free H2SO4-HNO3 7:3 v/v and 5% w/v KMnO4 at 1008C for1 h, whereas fish and plants were treated with 2:1 v/v H2SO4-HNO3 at 100–1108Cfor 3 h (Sadiq et al. 1991). T-Hg analysis was performed by cold-vapor atomic-absorption spectroscopy using a Thermo Elemental Solaar S4. Detection limits,calculated as three times the standard deviation (three sigma) of 10 measurements ofthe blank divided by the slope of the calibration curve (Long and Winefordner 1983),were 0.026 mg/g dry weight (dw), and 0.013 mg/g fresh weight (fw), for sediments andbiological samples, respectively. Quality control was performed using certifiedmaterials and spiked samples. The T-Hg concentration for the biological material(DORM-2, dogfish muscle, National Research Council Canada) was4.46 + 0.25 mg/g, dw (certified value 4.64 + 0.26 mg/g, dw), and for sediments

Figure 1. Total mercury (T-Hg) distribution in sediments from the Ayapel Marsh, Mojanaregion, Colombia.

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(CRM008-050, Resource Technology Corporation) was 0.74 + 0.02 mg/g, dwt(certified value 0.72 + 0.03 mg/g, dw). Sediment and biological samples (250–500 mg) were spiked with Hg to obtain approximately 30, 350 and 600 ng/g,covering almost the entire calibration curve. Hg recovery percentages from spikedsamples were 98.0 + 4.2% and 95.2 + 4.3% (n ¼ 6) for sediments and biologicalmaterial, respectively. In both methods the relative standard deviation (RSD) for sixreplicates was 510%. Organic matter (OM) content in sediments was determined asreported by Coquery and Welbourn (1995), measuring weight loss on ignition(4508C, 4 h). pH was measured in the sediment slurry using a pH-meter (HannaInstruments, Italy) calibrated with its respective solutions before every analysis.

Statistical analysis

Values for T-Hg concentrations are shown as the mean + the standard deviation(SD) of duplicated determinations. Data normality was assessed using Kolmogorov–Smirnov, and t-test or ANOVA were used to compare means between two or moregroups, respectively. When data did not follow a normal distribution, non-parametric methods were used. Spearman correlation analysis was used to establishrelationships between two variables. Statistical analysis was done using SPSS 10.5program. For all purposes, significance was set at p 5 0.05.

Results

T-Hg concentrations in sediments are presented in Figure 1. Mean values rangedfrom 0.160–0.301 mg/g (0.243 + 0.062 mg/g, dw). pH values did not varyconsiderably between stations (6.3–7.1), whereas OM concentrations showedmoderate variability (7.1–11%) (Table 1). The T-Hg concentrations in themacrophyte E. crassipes collected in the northeast (S2) and the southern (S6) partsof the marsh are presented in Table 2. Hg concentrations in this plant were alwaysgreater in roots than in stems, and for most cases, highest values were found in thenortheast area.

T-Hg levels found in fish from the Ayapel Marsh are presented in Table 3.Overall, T-Hg concentration in fish muscle was 0.298 + 0.148 mg/g, fw (n ¼ 172).

Table 1. Organic matter and pH in sediments from the Ayapel Marsh, Mojana region,Colombia.

Station (S) Organic matter (%) pH

S1 9.32 + 0.30 6.32 + 0.41S2 9.96 + 0.17 7.00 + 0.27S3 7.13 + 1.09 7.09 + 0.31S4 10.02 + 0.62 7.06 + 0.14S5 10.22 + 1.04 6.66 + 0.36S6 9.58 + 0.22 6.55 + 0.18S7 9.55 + 0.22 6.79 + 0.24S8 11.04 + 0.36 6.39 + 0.05S9 10.33 + 0.31 6.53 + 0.27S10 9.00 + 0.55 6.28 + 0.27S11 10.12 + 0.29 6.85 + 0.36

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Pooled data for carnivorous and non-carnivorous fish species showed that therewere significant statistical differences (p 5 0.001) in T-Hg mean concentrations inmuscle for these two groups, with values of 0.358 + 0.139 mg/g, fw, and 0.195 +0.096 mg/g fw, respectively. Lowest mean concentration was observed in Prochilodusmagdalenae, a non-carnivorous species (0.143 + 0.053 mg/g, fw), whereas themaximum was found in Pseudoplatystoma fasciatun (Bagre pintado) (0.432 +0.107 mg/g, fw). However, when T-Hg were compared for species belonging to thesame trophic group, no statistical differences were found (p 4 0.05).

Correlations between fish length and T-Hg in muscle are presented in Table 4.Correlations had the tendency to increase their significance when species wereanalyzed within seasons. However, for all species, a positive and significantcorrelation between these two variables was found (R ¼ 0.32, P 5 0.001).

Discussion and conclusion

T-Hg levels found in sediments from the Ayapel Marsh were similar to thoseobtained from the Mina Santa Cruz Marsh (gold mining site), south of Bolivar,Colombia (0.140–0.355 mg/g, dw; Olivero and Solano 1998), but greater than thosereported by Olivero-Verbel et al. (2004) in marshes located 35 km north of our studyarea (Village of Caimito, San Jorge River basin: 0.155 + 0.016 mg/g, dw).

Table 2. T-Hg concentrations (mg/g, dw) in roots and stems of Eichhornia crassipes collectedat two different sampling stations from the Ayapel Marsh.

Samples

T-Hg (m + SD) northeast zone(S2)

T-Hg (m + SD) southern zone(S6)

n Stems Roots n Stems Roots

September 2006 4 0.473 + 0.033 0.717 + 0.071 3 0.375 + 0.053 0.625 + 0.031(0.437–0.502) (0.655–0.819) (0.316–0.420) (0.595–0.657)

December 2006 4 0.370 + 0.046 0.529 + 0.092 4 0.242 + 0.066 0.447 + 0.141(0.330–0.428) (0.450–0.628) (0.159–0.318) (0.289–0.620)

March 2007 3 0.504 + 0.034 0.956 + 0.031 3 0.368 + 0.042 0.706 + 0.028(0.469–0.536) (0.922–0.982) (0.325–0.410) (0.680–0.735)

T-Hg, total mercury; m, mean, SD: standard deviation, n: sample number. Range values are shown inparenthesis.

Table 3. T-Hg concentrations (mg/g, fw) in fish species from the Ayapel Marsh.

Common name Scientific nameFoodhabits

T-Hg

nMean + SD range

Bagre pintado Pseudoplatystoma fasciatun C* 0.432 + 0.107 0.225–0.603 24Mojarra Caquetaia kraussi C 0.403 + 0.113 0.231–0.586 22Moncholo Hoplias malabaricus C 0.328 + 0.113 0.136–0.545 33Pacora Plagioscion surinamensis C 0.317 + 0.171 0.110–0.951 33Subtotal 0.358 + 0.139 0.110–0.951 112Bocachico Prochilodos magdalenae NC** 0.143 + 0.053 0.054–0.241 33Liseta Leporinus muyscoruma NC 0.263 + 0.097 0.112–0.465 27Subtotal 0.195 + 0.096 0.054–0.465 60Total (C þ NC) 0.298 + 0.148 0.054–0.951 172

*C, Carnivorous. **NC, Non-carnivorous.

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T-Hg concentrations in sediments varied according to geographical position. Ingeneral, stations located in the northeast area of the Ayapel Marsh had greater Hglevels, probably as a result of a direct impact of the flooding path of the Cauca River.This pollution process has also been documented for other gold mining areas(Appleton et al. 2001, 2006). Average T-Hg concentrations measured in sedimentscollected at the site the Cauca River enters the Ayapel Marsh during the samplingperiod has been reported to be 0.833 + 0.021 mg/g (Marrugo-Negrete 2007), a value3.4-fold greater than the average observed for all stations at the Ayapel Marsh. Itshould be pointed out that flooding itself could represent a factor for removingdeposited Hg from the sediments. Moreover, due to the proximity to the gold miningareas, atmospheric deposition could also be a source of Hg for this ecosystem(Mirlean et al. 2005).

There was a significant correlation between the contents of OM and T-Hg insediments (R ¼ 0.65, P ¼ 0.03, n ¼ 11). This relationship, pH levels ranging between6.0 and 7.15, as well as high temperatures, have been linked to increasing mercurymethylation rates by sulfate reducing bacteria (Morel et al. 1998; Ullrich et al. 2001).Therefore, physico-chemical conditions of water and sediments reported here arelikely to favor methylation process and incorporation of Hg in the food chain.

Eichhornia crassipes (water hyacinth) is an emergent aquatic macrophyteabundant in tropical ecosystems. It is well known for its high heavy metalaccumulation capacity (Pfeiffer et al. 1986; Jana 1988). T-Hg values found in thisplant are up to 2.3 times greater than those reported for roots of the same species inthe Mina Santa Cruz Marsh, in the south of Bolivar (0.114–0.432 mg/g, dw; Oliveroand Solano 1998). On average, T-Hg concentrations in plants collected from thenortheast zone (S2) were greater than those found in the southern zone (S6), a trendsimilar to that found for sediments. On the other hand, for most macrophytesamples, greater T-Hg values were observed during the dry season. This could beexplained considering that during the dry season, water level is lower and roots arecloser to the sediments. It has been reported that aquatic macrophytes accumulatemetals directly from sediments, showing higher metal concentrations than sediments(Coquery and Welbourn 1995; Mauro et al. 2001; Cardwell et al. 2002). Moreover,high temperatures during the dry season may increase methylation activity,increasing Hg bioavailability in this ecosystem (Ullrich et al. 2001). Despite thefact that there was a moderate but no significant relationship between T-Hg

Table 4. Spearman correlation coefficients (R) for relationships between T-Hg levels (mg/g,fw) and length (cm) for fish species in the Ayapel Marsh.

Species

Rainy season Dry season Both seasons

R P n R P n R P

Bagre pintado 0.45 0.120 13 0.75 0.140 11 0.54 0.020Mojarra 0.64 0.040 15 0.79 0.036 7 0.13 0.620Moncholo 0.21 0.400 20 0.38 0.150 13 0.04 0.800Pacora 0.54 0.015 18 0.86 50.001 15 0.74 50.001Bocachico 0.38 0.060 20 0.12 0.650 13 0.29 0.074Liseta 0.47 0.060 15 0.41 0.180 12 0.03 0.890Total 0.42 0.041 101 0.39 0.021 71 0.32 50.001

P, significance level; n ¼ number of data.

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concentrations in roots of E. crassipes and sediments (R ¼ 0.52, P ¼ 0.08), T-Hglevels found in sediments and plants reflect differential Hg pollution along the marsh.

Some authors have reported that for E. crassipes found in tropical ecosystems,methylation percentages could be up to 30 times greater than that measured atsuperficial sediments (Guimaraes et al. 2000; Mauro et al. 2001). This is due to thefact that the roots of these floating macrophytes are densely populated by differentgroups of bacteria (Acha et al. 2005), and therefore these plants could constitute anessential pathway for methylmercury uptake into tropical aquatic food chains.

Mean T-Hg concentrations in the muscle of carnivorous (0.358 + 0.139 mg/g,dw) and non-carnivorous fish species (0.195 + 0.096 mg/g, dw) resulted in a 2:1 ratiobetween these two trophic levels. The highest T-Hg concentrations were foundduring the dry season, probably due to more primary production leading to anincrease in Hg bioavailability in the food chain, an increase in gold mining,decreasing water volumes and changing habitats, among other factors (Zapata 1994;Hylander et al. 2000).

Correlation analysis revealed that relationships between size and T-Hg dependon the species and season. However, overall T-Hg tends to increase with size. It hasbeen shown that usually older individuals have greater Hg concentrations thanyounger ones as a consequence of a longer exposure time (Dixon and Jones 1994;Mauk and Brown 2001).

Although the overall mean T-Hg concentration was found to be below 0.50 mg/g,fw, the maximum T-Hg concentration that should be present in fish for humanconsumption according to the World Health Organization (WHO 1990), 24 fishsamples, representing 13% of the total collected, presented values above this limit.To protect vulnerable people, in particular pregnant women, those under 15 years ofage, and frequent fish consumers, the WHO has recommended a lower guideline of0.20 mg/g for those groups (WHO 1990). T-Hg concentrations found in allcarnivorous and some non-carnivorous (Liseta) species were greater than 0.2 mg/kg. These values are similar to those measured in other zones subjected to mercurypollution in Colombia (Olivero and Solano 1998; Olivero-Verbel et al. 2004), butlower than those reported for gold mining sites in Brazil (Porvari 1995; Malm et al.1997; Barbosa et al. 2003). Olivero-Verbel et al. (2002) reported that T-Hgconcentrations in hair for people from Caimito, a municipality close to the AyapelMarsh, are linked to fish consumption, being the T-Hg concentrations in fish for thisplace similar to those found in this study. This fact should encourage moreextensively and intensively ecological and environmental health studies in the area bylocal government. Although fish are considered the main source of MeHgþ exposure,they are also the most important source of protein for many populations in thisregion.

Taken together, the results presented in this report show that T-Hg concentra-tions in sediments and macrophytes of the Ayapel Marsh, Mojana region, Colombia,follow a geographical pattern linked to the flooding pathway of the Cauca River, acurrent that carries Hg from nearby gold mining areas. Hg presence in sediments hascontaminated food chains to such an extent that human fish consumption representsa potential health risk. A governmental intervention in several aspects, such asapplying law regulations to develop environmental friendly gold mining practices,educational programs about mercury pollution, programs for forest protection inriver basins and reforestation, among others, are pivotal actions to protect this foodsource from mercury contamination.

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