SciELO - Scientific Electronic Library Online

 
vol.49 issue1Effect of Bacillus firmus C101 on the growth of Litopenaeus vannamei Boone (White Shrimp) post-larvae, and Brachionus plicatilis s.s. Müller (Rotifer)Long-term coral colonization by an excavating Caribbean sponge author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Boletín de Investigaciones Marinas y Costeras - INVEMAR

Print version ISSN 0122-9761

Bol. Invest. Mar. Cost. vol.49 no.1 Santa Marta Jan./June 2020

https://doi.org/10.25268/bimc.invemar.2020.49.1.775 

Research Articles

Estimation of the ecological and human health risk of mercury in a mangrove area of the La Puntilla estuary, El Oro province, southern Ecuador

Patricio Colón Velásquez-López1  2 

Ivonne Yadira López-Sánchez3 

María Fernanda Rivera-Velásquez3  4  * 

1 Universidad Técnica de Machala, Unidad de Ciencias Agropecuarias, Ecuador.

2 Canadian International Resource and Development Institute, The University of British Columbia, Vancouver, Canadá.

3 Escuela Superior Politécnica de Chimborazo, Grupo de investigación Ciencias de Datos, Facultad de Ciencias, Riobamba, Ecuador.

4 Universidad Nacional de Chimborazo, Facultad de Ingeniería, Riobamba, Ecuador.


ABSTRACT

Present study focused on the evaluation of total mercury concentration and the estimation of ecological risk (Er), the ecological risk index (IR); and the toxic risk or hazard quotient (HQ) for human health in a mangrove area that borders the mouths of the Chaguana and Siete rivers, in La Puntilla estuary in the south of Ecuador. For the determination of the Er, RI, and HQ, we identified three indicators of mercury contamination: sediments, mangrove root, and soft tissue of the bivalve mollusk Anadara tuberculosa. In the mangrove area that borders the mouth of the Chaguana river, the mercury concentration fluctuated between 0,11-0,06 mg/kg in sediments, 0.06-0,01mg/kg in mangrove root, with a more consistence presence of A. tuberculosa, but one bivalve sample reported a level of 0,034 mg/kg of mercury. In contrast to the mangrove area adjacent to the mouth of the Siete river, whose concentrations ranged from 0,77-0,42 in sediments, and 0,15-0,12 in mangrove root, we found the highest mercury contamination, being imperceptible to the presence of A. tuberculosa. Results of the risk analysis indicated that, at the mouth of the Chaguana river, the Er and the RI index were placed in the "low" category. In contrast, at the mouth of the Siete river, the Er was "high," and RI was "moderate." Potential risk to human health was low, consistent with the value of HQ < 1 that considers the consumption of A. tuberculosa and dermal contact through sediments; however, the low presence of the bivalve at the mouth of the Siete river is of concern.

KEYWORDS: ecological risk index; mercury; Anadara tuberculosa; mangrove ecosystem

RESUMEN

El presente estudio se centra en la evaluación de los niveles de concentración de mercurio total y la estimación del riesgo ecológico (Er), el índice de riesgo ecológico (RI) y el coeficiente de riesgo tóxico o peligro (HQ) para la salud humana en un área de manglar junto a las desembocaduras de los ríos Chaguana y Siete, en el estuario de La Puntilla en el sur de Ecuador. Para la determinación de Er, RI y HQ, identificamos tres indicadores de contaminación por mercurio: sedimentos, raíz de mangle y tejido blando del bivalvo Anadara tuberculosa. En el área de manglar que bordea la desembocadura del río Chaguana, las concentraciones de mercurio fluctuaron entre 0,11±0,06 mg/kg en sedimentos, 0,06±0,01mg/kg en raíz de mangle, con una consistente presencia de A. tuberculosa, pero solo una muestra del bivalvo registró un nivel de 0,034 mg/kg de mercurio. En contraste, en el área de manglar adyacente a la desembocadura del río Siete, las concentraciones de mercurio oscilaron entre 0,77±0,42 mg/kg en sedimentos y 0,15±0,12 mg/kg en la raíz de manglar, siendo imperceptible la presencia de A. tuberculosa. Los resultados del análisis de riesgo indicaron que en la desembocadura del río Chaguana, el Er y el índice de RI se colocaron en la categoría "baja". En contraste, en la desembocadura del río Siete, el Er resultó "alto" y RI resultó "moderado". El riesgo potencial para la salud humana fue bajo, en consistencia con el valor de HQ < 1 que considera el consumo de A. tuberculosa y el contacto dérmico a través de sedimentos; sin embargo, la escasa presencia del bivalvo en la desembocadura del río Siete es de preocupación.

PALABRAS CLAVE: índice de riesgo ecológico; mercurio; Anadara tuberculosa; ecosistema de manglar

INTRODUCTION

Pollution processes generated by natural and anthropic activities in the vicinity of water bodies are an increasingly common problem facing aquatic ecosystems. In tropical regions, heavy metal contamination can reach mangrove areas, the habitat of important marine species for the sustenance of coastal communities (Silva et al., 2003). For approximately 25 years, miners in the southern region of Ecuador have used mercury for gold recovery, considering it one of the main causes of contamination in rivers and streams, in some cases exceeding the permissible levels established according to international regulations for river and sediments (Velásquez-López et al., 2011). It is estimated that in 2010 artisanal and small-scale gold mining activity was responsible for 29 % of mercury released into the atmosphere in Latin America and the Caribbean (Santana et al., 2014). The waste resulting from extractive and mineral processing activities eventually reaches the riverbed causing the accumulation of mercury-enriched sediments (Appleton et al., 2001; Carling et al., 2013). For example, mercury released from mining activities was found 250 km downstream in the Puyango river in southern Ecuador (Schudel et al., 2019). Once mercury reaches aquatic ecosystems can precipitate to the bottom (Marchand et al., 2006; Bazzi, 2014), remaining for long periods, or can be bioaccumulated and biomagnified in the food chain (Morel et al., 1998; Chen et al., 2009; Le et al., 2017). Within the trophic chain, bivalve molluscs for their filtering capacity are recognized as sentinel organisms for biomonitoring of mercury in aquatic systems (Maanan, 2008). In terms of risk to human health, the consumption of bivalve molluscs may be the main route of exposure to mercury (World Health Organization, 1996); however, another form of exposure is dermal contact through contaminated sediments (US Environmental Protection Agency, 2001). Admitting the danger posed by mercury contamination, many of the countries in the region have taken emerging measures. Consequently, in October 2013, Ecuador signed its adhesion to the Minamata Agreement. Since then, actions are executed to identify critical points of contamination, thereby, increasing the technical capacities for mercury monitoring in different environmental matrices, for a useful application of the commitments acquired within the international agreement.

In southern Ecuador, 25 km away from the coastal zone for around 25 years, artisanal and small-scale miners use mercury for gold extraction. Previous studies have reported that mercury can reach mangrove areas, but the information about the concentratin levels and posible risks in these maritime areas is limited. Mangroves represent ecological niches that embrace various species of birds, fish, and reptiles (Medina et al., 2007; Cardoso et al., 2009). Despite the ecological, social, and economic importance of the mangrove ecosystem in southern Ecuador and the evident contamination by heavy metals in its proximity, the risks associated with the presence of metals in these fragile environments have been scarcely studied. In developing countries such as Ecuador, mangroves benefit the practice of artisanal fishing and recreation activities, and due to potential polluting sources, there is interest in understanding the environmental state of these regions for the formulation of management and protection measures. The objective of the present study was to determine the concentration of mercury in sediments, mangrove root and in the bivalve mollusc Anadara tuberculosa at two sites in the La Puntilla estuary and to estimate the Ecological Risk Index (RI); and the Toxic Hazard or Hazard Quotient (HQ) for human health. The research scenario considered in situ samplings in mangrove areas of the estuary adjacent to the mouths of the Chaguana and Siete rivers for a comparative analysis of 1) Ecological Risk Index (RI), and 2) Toxic Risk or Hazard Quotient (HQ) for human health.

The environmental health risk analysis is known as the evaluation of toxicological damage caused by an effect of a contaminating that reach to a potential receptor through various migration and exposure pathways (US Environmental Protection Agency, 1989). On the other hand, an ecological risk estimation is a tool used to perform a quantitative diagnosis of environmental sensitivity based on the analysis of concentrations of pollutants (mercury) at the study site and its impact on the environment in which it is present (Hakanson, 1980). Although the current study only offers essential information about mercury contamination and risks in a mangrove area, it is a significant contribution to knowledge about what is undoubtedly an area of significant academic interest regarding heavy metal contamination in mangrove areas. The study benefits international organizations and organizations that work in ecological preservation and offers information to those in charge of formulating measures for the protection and management of coastal resources.

METHODS

The present study was conducted in the mangrove biome located at the mouths of the Chaguana and Siete rivers, in the La Puntilla estuary, El Oro province, Ecuador. The study area adjoins the Guayas province to the north and the Azuay province to the northwest. The La Puntilla estuary originates in the western foothills of the Andes Mountains in the Ponce-Enriquez (Azuay Province) and El Guabo (El Oro Province), having the Chaguana and Siete rivers as the main tributaries. The flow of water in both rivers varies considerably. The Siete river has an average of 0.2-0.3 m3/s, while in times of high rain intensity, water flow increases to 2.5-7 m3/s (National Secretariat of Planning and Development, 2009). The Chaguana river is connected to the Pagua and Bonito rivers, which currently provide a flow of around 4 m3/s, constituting a more significant body of water than the Siete river.

In February and August of 2018, four sampling campaigns were carried out in the mangrove ecosystem of the La Puntilla estuary next to the mouths of the Chaguana and Siete rivers (Figure 1). Two sampling sites were located, one next to the mouth of the Chaguana river, and another next to the mouth of the Siete river. The estuary daily features two high tides and two low tides. The samplings were carried out at low tide when it is possible to access the mangrove land since it is not flooded by water. The samples were taken in the mangrove biome mudflat, habitat of bivalves, and crustaceans. For the sampling, it was essential to consider local artisanal fishers' knowledge with whom access was planned according to the intertidal state and in the function of the movement of one fisherman per day (between 4-6 hours) during his daily journey. With the accompaniment of artisanal fishers, we sampled the Anadara tuberculosa and obtained the mangrove root of the Rhizophora mangle sp species at each site. The samples were taken separately to avoid risks of cross-contamination. Sediment and mangrove root samples were collected at each station, accumulated in separate and clean containers. In the case of A. tuberculosa, the organisms were placed in baskets after superficial cleaning, ruling out the presence of sediment and mud in the external valves. On each sampling day, the materials and utensils were washed and rinsed with 5 % nitric acid.

Figure 1 Study area: La Puntilla estuary, belonging to Bajo Alto, El Guabo canton, El Oro province, Ecuador. 

Sediment sampling

At each point following the artisanal fisherman's sequence and using a 6-inch diameter PVC tube, approximately 3000 g of sediment were randomly taken at various locations at a depth of about 20 centimeters. A composite sample of around 500 g was formed from the discrete sediment samples, which was packed in plastic covers with hermetic closure and placed in a container specially prepared for the sediments. Subsequently, the samples were subjected to drying, grinding, and sieving (75 μm, 150 μm, 300 μm, and 850 μm) and hermetically packed for subsequent transport to the analytical laboratory.

Root sampling of Rhizophora sp.

At the two sampling sites previously described, and following the trajectory of the artisanal fisherman, samples of the mangrove root were obtained. Mangrove root samples were taken by cutting off the soft tissue at the suspended plant root. In general, the mangrove root contains suspended particles and microorganisms. The root samples were stored with all their content. A sample consisted of several mangrove root fragments to complete approximately 250 g, which was placed in plastic bags with a hermetic seal and placed in a cold container.

Sampling of Anadara tuberculosa

The capture of bivalves was carried out with particular attention to obtaining the black shellfish A. tuberculosa, which was carried out with the help of the fisherman, who was the only one who extracted the bivalve from the mud of the mangrove habitat at a depth of around 20 cm. Another person received the shellfishes with clean hands for handling rinsing them in seawater to remove excess sediment, packaging, and storage in the collecting container. In the laboratory and under thorough aseptic conditions, the bivalves were dissected, extracting the soft tissue. A sample weight of around 100 g was required for analytical purposes at the laboratory. From the total number of individuals captured in the four sampling campaigns, 22 samples were obtained and analyzed. Each sample consisted of between 20 to 30 specimens of A. tuberculosa. The size and weight of the captured individuals were recorded, measured utilizing a scale and a digital scale with sensitivity to 0.1 g, respectively. The storage of samples of sediments, mangrove root and A. tuberculosa was carried out separately, using thermal containers for preservation at low temperatures and keeping sample conservation and transport criteria in mind (Instituto de Investigaciones Marinas y Costeras, 2013).

Mercury analysis

The concentrations of total mercury in the samples of sediment, mangrove root and the bivalve A. tuberculosa were analyzed in the laboratory of the Undersecretary of Quality and Safety, of the Ministry of Aquaculture and Fisheries of Ecuador with accreditation for the determination of mercury in biological samples. The analysis was performed by using the cold vapor technique using the Atomic Absorption Spectrophotometer (reference method P1-MP1 VARIAN AA 60), and according to intrinsic analytical procedures of the laboratory. The detection limit reported by the laboratory was 0.09 mg/kg Hg, and the reported values correspond to the dry weight of the samples. The mercury concentration results were analyzed using a one-way analysis of variance (ANOVA) to determine if there is a significant difference between the averages determined for each component in the two points of the La Puntilla estuary.

Ecological risk calculation

To calculate the ecological risk, we used the method described by Hakanson (1980), which aims to identify the concentration of heavy metals on the sample to assess the pollution factor , ecological risk potential (Eri), ecological risk potential index (RI). The pollution factor identifies how polluting, mercury can be in the study site, and was calculated as follows:

Where,

is the concentration of mercury in the sample

corresponds to the reference mercury values whose value proposed by Hakanson is 0.25

The potential ecological risk factor helps to know the ecological risk (Eri) that mercury can have based on the relationship between the pollution factor and the toxic response values. They are interpreted as follows:

Where,

Tri corresponds to the toxic response factor of the substance, with a value of 40 for mercury.

represents the pollution factor.

The ecological risk index (RI) integrates the ecological risk potential factors of mercury and allows establishing whether the concentrations in the study sample have ecological risk. The RI category was calculated with the following equation.

The interpretation of the potential ecological risk pollution factor and ecological risk index is summarized in Table 1, where the values and their respective categories are presented.

Table 1 Interpretation categories of the potential ecological risk pollution factor and ecological risk index. 

Environmental health risk analysis

The environmental health risk calculation was carried out, taking into consideration active exposure routes such as ingestion (Eq. 4) and Dermal Contact (Eq. 5). We consider that the study site is a habitat where small family groups settle that take advantage of the mangrove for artisanal fishing by both subsist on this resource. On the other hand, the risk produced by the ingestion of mercury through the consumption of shells of the genus A. tuberculosa (Eq. 6) was calculated considering that this bivalve is distributed and consumed in various parts of the region. Table 2 shows a description of the variables, values, and units used.

Table 2 Values used to calculate risk. 

The HQ is a hazard index that quantitatively identifies whether exposure to mercury exceeds the tolerable or reference dose RfD (reference dose) [mg/kg d]. The RfD estimates the average daily exposure that does not produce measurable adverse effects on the human organism during its life. The total hazard coefficient is considered as the sum of the individual factors. For the determination of the total HQ, the following summation was performed, taking into account the route of exposure.

The standards for personal protection defined by various international organizations provide the following acceptability criteria: for non-carcinogenic risk (exposure to one or more substances) HQ, HQ < 1.0 (Environmental Protection Agency, 1997).

RESULTS

Mercury concentration in sediments, mangrove root, and bivalve Anadara tuberculosa

Figure 2 shows the results of mercury (Hg) concentration levels in sediments, the soft tissue of Anadara tuberculosa and mangrove root detected in the La Puntilla estuary along the mangrove bed that adjoins the mouths of the Siete and Chaguana rivers.

Figure 2 Mercury concentration in sediments, Anadara tuberculosa, and mangrove root. The vertical axis shows the levels of mercury concerning sediment, mangrove root, and the bivalve A. tuberculosa, and the horizontal axis shows the components analyzed in the mangrove area adjacent to the mouths of the Chaguana and Siete rivers, in the La Puntilla estuary, El Oro province, southern Ecuador. 

In the mangrove sector adjacent to the Chaguana river's mouth, 29 sediment samples were taken with mercury concentration levels of 0.12-0.06 mg/kg. The determined value represents five samples (18.5 %) of the total samples obtained, in such a way that 24 samples (81.5 %) reported concentrations below the detection limit. This means that the presence of mercury is inconsistent in the mangrove area near the mouth of the Chaguana river. On the other hand, when heading towards the mangrove sector that adjoins the Siete river, entry to the site was difficult at sea due to the excessive sedimentation that exists in the estuary bed, forming a barrier that blocks access to the river. In the mud of the mangrove bed next to the Siete river's mouth, five sediment samples were taken, identifying in all the samples the presence of mercury whose concentrations fluctuated around 0.77-0.42 mg/kg. The analysis of variance shows that the mercury concentration in sediments of the mangrove zone adjacent to the Siete river was significantly different from the level registered for the mangrove zone adjacent to the Chaguana river (p > 0.05). Additionally, unlike what was determined for the mouth of the Chaguana river, a homogeneous distribution was established in the sediments of the mangrove area adjacent to the Siete river, registering the highest concentration with 1.09 mg/kg of mercury.

Regarding the concentration of mercury in mangrove root in the Chaguana river, out of a total of 23 samples, five samples (21 %) reported a mercury concentration of 0.06-0.01 mg/kg. In comparison, 18 (79 %) samples reported levels below the detection limit. In contrast, in the Siete river of five mangrove root samples obtained, reported a concentration of 0.151-0.121 mg/kg. The analysis of variance shows that the level of mercury in mangrove root in the area adjacent to the mouth of the Chaguana river was not significantly different from the concentration registered near the Siete river (p> 0.05).

Concerning A. tuberculosa, 60 % of the captured individuals had a size between 3-4 cm, 31% between 4-5 cm, and 9 % fluctuated between 5-5.5 cm. Similarly, the registered individuals' valve weights were 15.5 g, 44.2 g, and 78.7 g, respectively, according to their size. The mass of the muscle tissue represented approximately 30 % of its total weight; that is, it varied between 4.46 to 23.60 g of wet weight per individual. The composition of a sample was achieved by gathering between 20 to 30 specimens according to the individual's size. In the mangrove bed towards the mouth of the Chaguana river, 450 individuals were collected, completing a total of 15 samples. Of these, 14 samples reported concentrations below the detection limit and only one with a level of 0.034 mg/kg of mercury. In contrast, in the mangrove bed towards the mouth of the Siete river, the scarce presence of A. tuberculosa made it impossible to complete a sample at the required weight for the analysis, coinciding with the presence of some dead specimens in the habitat.

Ecological risk and environmental health risk analysis

Table 3 shows the values of the ecological risk indices for scenarios A and B. The results demonstrated that in the Siete river the Cf is in the "considerable" category, the Er is "high" while the RI it is at a "moderate" level. In contrast, the Factors Cf, Er, and the RI index were located in the "low" category at the mouth of the Chaguana river.

Table 3 Calculation of ecological risk indices. 

This study defines a model that considers sediments as the route of exposure by dermal contact, and the soft tissue of A. tuberculosa as the route of exposure by ingestion. Dermal contact is associated with the manipulation of sediment and mercury-contaminated bivalve. That is percutaneous absorption of the element that can enter the human body when a person is in touch with the contaminant. The receivers considered correspond to adults and children who live in the sector or make fishing lines in the mangrove forest (Figure 3).

Figure 3 Conceptual model of the exposure scenario in the Bajo Alto area. 

The environmental health risk analysis was carried out designating values to the parameters shown in Equations 4-7, considering the factors and levels shown in Table 4. The data of mercury concentration in sediments for the Chaguana river and the Siete river corresponds to 0.225 mg/kg and 1.086 mg/kg, respectively, estimated using the UCL criteria of the EPA (US Environmental Protection Agency, 2002). The risk calculation values for scenario A corresponds to the mangrove habitat adjacent to the mouth of the Siete river for adults, and children were 2.00 x 10-02 and 1.74 x 10-01, respectively. On the other hand, for scenario B corresponding to the mangrove habitat adjacent to the Chaguana river, the values for adults and children are 1.83 x 10-02 and 1.02 x 10-01, respectively.

Table 4 Values obtained from the calculation of the Hazard Quotient for adults and children for scenarios 1 and 2. 

From the results obtained, estimating the total risk for adults and children, it is observed that the tolerance limits of HQ = 1, were not exceeded in the two sites. However, the values recorded in the Chaguana river are significantly lower than those determined in the Siete river.

DISCUSSION

The present work analyzed mercury concentrations in three components of the mangrove habitat in the La Puntilla estuary in southern Ecuador. We estimated the ecological and environmental health risk of mercury at two sites. It is essential to highlight that the samples were taken in the mangrove habitat and not precisely in the riverbed. Hence, the sediment samples represent the mud that characterizes the mangrove biome adjacent to the Chaguana river's mouths.

According to the results obtained, it is observed that the transport and diffusion mechanisms of mercury towards the La Puntilla estuary are carried out by river drainage from the upper part where waste and mining tailings are discharged reaching the coastal zone. Previous studies on the concentration of mercury in sediments of the riverbed Siete reported mercury concentrations of 2.0 mg/kg (Tarras-Wahlberg et al., 2000), 13 mg/kg (Appleton et al., 2001) and 1.4 mg/kg (Carling et al., 2013). In the estuary of the Tumbes river, Schudel et al., (2018) determined levels of 0.13 mg/kg of mercury in sediments and through isotopic analysis confirm that the element is associated with discharges of waste material from mining activities upstream of the river Puyango-Tumbes. High variability in mercury concentrations was observed in the three components of the Chaguana river, with 80 % of samples under the detection limit. This may be due to multiple factors such as water mixing and dilution in the estuary zone, as well as the dynamics that characterize the coastal area (Tam and Wong, 1995). Approximately 20 km from our study area, concentrations of 3.97 ± 0.73 mg/kg of mercury have been reported in sediments (Marin et al., 2016). Lacerda et al. (1993), when investigating mangroves in a coastal zone of Brazil, found higher concentration of metals in sediments from the estuary bed than in mangroves mudflats. Similarly, Silva et al. (2003) determined mercury concentrations between 0.022-0.060 mg/kg of mercury and corroborates that mercury accumulates mostly in sediments from the estuary bed compared to deposits from the mangrove forest. When mercury enters aquatic environments, it precipitates due to its high density and is incorporated into the bottom, which acts as a sink that adheres to the finest particles (Andren and Harriss, 1975; Vane et al., 2009). Based on what was examined in this study, more specific studies are required to understand the mechanisms that govern mercury's mobility in the mangrove biome of the Siete river and its surroundings.

The mercury concentrations found in the mangrove mud show superiority to the Canadian standard limits for the protection of aquatic life, which is 0.49 mg/kg. Additionally, the mercury concentrations detected in the present study exceed the remediation levels (Soil Cleanup Target Levels) established by the Department of Environment and Toxicology of the University of Florida (Center for Environmental & Human Toxicology, 2005). This criterion is based on Leachability Based on Marine Surface Water Criteria, which establishes a limit of 0.03 mg/kg. Ecuadorian legislation does not establish sediment remediation criteria for mangrove environments. The mangrove forest habitat characterizes approximately 75 % of Ecuador's coastline, representing a critical ecoregion for the growth and reproduction of some marine species of fish, mollusks, and crustaceans. In the present study, the mangrove root sample contained particulate material, microalgae, and invertebrates, which supposes possible contamination of marine fish that at low tide or high tide graze the mangrove to feed. In the Chaguana river, the concentration of mercury in sediments was approximately two times higher than the mercury level in mangrove roots. In the Siete river, the difference was eight times higher. This suggests higher absorption of mercury in sediments, while lower mercury distribution in the mangrove root system (Silva et al., 2003; Alongi, 2005). Although research on mercury in mangrove root is limited, Huang et al. (2020) discusses mercury absorption processes in mangrove root and indicates that the transport mechanisms may be subject to intertidal variations. The mercury attached to the mangrove aerial roots may undergo a volatilization process due to the effect of solar radiation on the moment of exposure to the atmosphere at low tide (Huang et al., 2020).

Concerning mercury contamination in bivalves, it is known that the concentration in the same place differs between different species and individuals (Elder and Collins, 1991), and the age of the organisms can influence the accumulation of mercury (Otchere et al., 2003). Studies in mangroves in India determined a low correlation between the concentration of mercury in sediments and that established in the gastropod Pirinella cingulata. Research on mercury in bivalves in the past 50 years has been reviewed by Otchere (2019), who reports an extensive list of bivalve molluscs from various locations and diverse environments whose average concentrations fluctuate around 0.92 ± 1.67 mg/kg, with a minimum value of 0.03 mg/kg and a maximum of 7.5 mg/kg. The values recorded in the present study in the samples of the black shellfish A. tuberculosa obtained in the mangrove mudflats next to the Chaguana river are close to the minimum values reported in other studies. These levels are not considered high about the permissible limits of the Food and Agriculture Organization (FAO) and the World Health Organization (WHO), which presents a reference value of 0.5 mg/kg (World Health Organization, 2008). It is essential to consider that a sample consisted of 20 to 30 individuals, which implies variability in the concentration of mercury between the specimens that form one sample size corresponding to the same species in the same locality. Consequently, a single specimen could report mercury levels between 0.68 to 1.02 mg/kg, which are similar to the range stated by Otchere (2019).

It has been reported that mercury can cause a cellular alteration in blood cells of bivalve molluscs, and an absolute concentration can have a lethal effect in aquatic organisms (Jakimska et al., 2011; Denil et al., 2017). Other researchers deduce the presence of protection mechanisms against metals through vesicles that facilitate cell excretion (Dallinger, 1993; Claisse et al., 2001), or defense throughout their shells as protective biofilms (Scardino et al., 2013). In the same order, other studies affirm that the outer shell can absorb metal from water or sediment, reaching concentrations higher than those of the internal tissues (Zuykov et al., 2011, 2012). Additionally, biological factors such as species, age, size, sex, genotype, phenotype, feeding activity, and reproductive status influence the accumulation of metals and their toxicity (Riget et al., 1996; Kehrig et al., 2006; Sevillano-Morales et al., 2015), aspects that require more attention in the study area.

La Puntilla estuary is a dynamic area influenced by tides that come from the ocean and by the drainage of freshwater from rivers. In southern Ecuador the estuary dynamics is associated to an intensive coastal aquaculture. In the Siete river, a fluvial body of low flow was observed; therefore, a more severe effect is presumed in the configuration of the channel (Figure 3a). In contrast, in the Chaguana river (Figure 3b), a healthier body of water was observed, where the aquatic and wildlife of some species are found, including the presence of birds, bivalves and crustaceans. The perception of artisanal fishers regarding the situation observed in the estuary is negative and critical. It indicates their concern about the river's low flow and the waste from the upstream mining activity. Likewise, they generally associate habitat problems with wastewater discharges from shrimp farms. With special precaution to the Siete river, the fishermen do not approach the place, indicating that A. tuberculosa and other bio-aquatic species such as the red crab are invisible in that area.

Figure 3 Images of the study area where the samples were taken a) Siete river b) Chaguana river. 

From the results obtained, mercury contamination in the mangrove swamp of the La Puntilla estuary defines two risk scenarios, referred to as scenario A at the mouth of the Siete river and Scenario B at the mouth of the Chaguana river. For none of the cases was the HQ exceeded, presenting values less than one. However, it is crucial to consider that the HQ is nothing more than a conservative estimate of the potential effects on human health. The risk factors and ecological risk indices associated with the Siete river are approximately four times higher than in the Chaguana river. The scarce presence of A.tuberculosa at the mouth of the Siete river evidences a severe ecological effect on this stream. It causes local uncertainty, which is why it is necessary to deepen the research at this site. Other metals reported in the Siete river watershed that could add toxic effects to aquatic organisms were not a reason for analysis in this study. It is substantial to execute a comprehensive research program in mangrove areas considering the analysis of other metals and abiotic parameters in the ecosystem.

ACKNOWLEDGEMENTS

This work was developed through the cooperation agreement between the Technical University of Machala-Ecuador and the Canadian International Resource and Development Institute (CIRDI) for the execution of the "TransMAPE" and "Heavy metal pollution" projects. Special recognition is left to the artisanal fishermen of the Tendales parish, especially to the Guerrero-García family for their support and accompaniment in-field tasks, and interest demonstrated in the ecological situation of their place of living and work

BIBLIOGRAFÍA/LITERATURE CITED

Alongi, D.M. 2013. Mangrove-microbe-soil relations. Interactions between macro- and microorganisms in marine sediments: 85-103. https://doi.org/10.1029/CE060p0085. [ Links ]

Andren, A.W. and R.C. Harriss. 1975. Observations on the association between mercury and organic matter dissolved in natural waters. Geochim. Cosmochim. Acta, 39: 1253-1258. https://doi.org/10.1016/0016-7037(75)90132-5. [ Links ]

Appleton, J.D., T.M. Williams, H. Orbea and M. Carrasco. 2001. Fluvial contamination associated with artisanal gold mining in the Ponce Enriquez, Portovelo-Zaruma and Nambija areas, Ecuador. Water Air Soil Poll., 131(1-4): 19-39. [ Links ]

Bazzi, A. 2014. Heavy metals in seawater, sediments and marine organisms in the Gulf of Chabahar, Oman Sea. J. Oceanogr. Mar. Sci., 5(3): 20-29. https://doi.org/10.5897/JOMS2014.0110. [ Links ]

Cardoso, P.G., A.I. Lillebe, E. Pereira, A.C. Duarte and M.A. Pardal. 2009. Different mercury bioaccumulation kinetics by two macrobenthic species: the bivalve Scrobicularia plana and the polychaete Hediste diversicolor. Mar. Environ. Res., 68(1): 12-18. https://doi.org/10.1016/j.marenvres.2009.03.006. [ Links ]

Carling, G.T., X. Diaz, M. Ponce, L. Perez, L. Nasimba, E. Pazmino and W.P. Johnson. 2013. Particulate and dissolved trace element concentrations in three southern Ecuador rivers impacted by artisanal gold mining. Water Air Soil Poll., 224(2): 1415. [ Links ]

Center for Environmental & Human Toxicology. 2005. Final technical report: Development of Cleanup Target Levels (CTLs). Division of Waste Management FDEP. [ Links ]

Chen, C.Y., M. Dionne, B.M. Mayes, D.M. Ward, S. Sturup and B.P. Jackson. 2009. Mercury bioavailability and bioaccumulation in estuarine food webs in the Gulf of Maine. Environ. Sci. Technol., 43(6): 1804-10. https://doi.org/10.1021/es8017122. [ Links ]

Claisse, D., D. Cossa, J. Bretaudeau-Sanjuan, G. Touchard and B. Bombled. 2001. Methylmercury in molluscs along the French coast. Mar. Pollut. Bull., 42(4): 329-332. https://doi.org/10.1016/S0025-326X(01)00036-4. [ Links ]

Dallinger, R. 1993. Strategies of metal detoxification in terrestrial invertebrates: 245-289. In Ecotoxicology of metals in invertebrates. Lewis Publishers, London. [ Links ]

Denil, D.J., F.F. Ching and J. Ransangan. 2017. Health risk assessment due to heavy metals exposure via consumption of bivalves harvested from Marudu Bay, Malaysia. Open J. Mar. Sci., 7: 494-510. https://doi.org/10.4236/ojms.2017.74035. [ Links ]

Elder, J.F. and J.J. Collins. 1991. Freshwater molluscs as indicators of bioavailability and toxicity of metals in surface-water systems. Rev. Environ. Contam. Toxicol., 122: 37-79. https://doi.org/10.1007/978-1-4612-3198-1_2. [ Links ]

Environmental Protection Agency. 1997. Analysis of risk for environmental pollutants application of deterministic and probabilistic methods for a school scenario. [ Links ]

Hakanson, L. 1980. An ecological risk index for aquatic pollution control. A sedimentological approach. Water Res., 14(8): 975-1001. https://doi.org/10.1016/0043-1354(80)90143-8. [ Links ]

Huang, S., R. Jiang, Q. Song, Y. Zhang, Q. Huang, B. Su, ... and H. Lin. 2020. Study of mercury transport and transformation in mangrove forests using stable mercury isotopes. Sci. Total Environ., 704, 135928. [ Links ]

Institute of Marine and Coastal Research. 2013. Manual of analytical techniques for the determination of isicochemical parameters and marine pollutants (water, sediments and organisms). Inst. Coast. Mar. Res., Santa Marta. https://doi.org/10.1017/CBO9781107415324.004. [ Links ]

Jakimska, A., P. Konieczka, K. Skóra and J. Namiesnik. 2011. Bioaccumulation of metals in tissues of marine animals, Part I: the role and impact of heavy metals on organisms. Pol. J. Environ. Stud., 20(5): 1117-1125. [ Links ]

Kehrig, H. A., M. Costa, I. Moreira and O. Malm. 2006. Total and methyl mercury in different species of molluscs from two estuaries in Río de Janeiro state. J. Braz. Chem. Soc., 17(7): 1409-1418. [ Links ]

Lacerda, L.D., C.E. Carvalho, K. Tanizaki, A. Ovalle and C. Rezende. 1993. The biogeochemistry and trace metals distribution of mangrove rhizospheres. Biotropica, 252-257. [ Links ]

Le, D.Q., K. Tanaka, L.V. Dung, Y.F. Siau, L. Lachs, S.T. Kadir, ... and K. Shirai. 2017. Biomagnification of total mercury in the mangrove lagoon foodweb in east coast of Peninsula, Malaysia. Reg. Stud. Mar. Sci., 16, 49-55. https://doi.org/10.1016/j.rsma.2017.08.006. [ Links ]

Maanan, M. 2008. Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environ. Poll., 153(1): 176-183. https://doi. org/10.1016/j.envpol.2007.07.024. [ Links ]

Marchand, C., E. Lallier-Vergès, F. Baltzer, P. Albéric, D. Cossa and P. Baillif. 2006. Heavy metals distribution in mangrove sediments along the mobile coastline of French Guiana. Mar. Chem., 98(1): 1-17. https://doi.org/10.1016/j.marchem.2005.06.001. [ Links ]

Marín, A., V.H. González, B. Lapo, E. Molina y M. Lemus. 2016. Niveles de mercurio en sedimentos de la zona costera de El Oro, Ecuador. Gayana, 80(2): 147-153. http://dx.doi.org/10.4067/S0717-65382016000200147Links ]

Medina, M.H., J. Correa and C. Barata. 2007. Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere, 67(11): 2105-2114. https://doi.org/10.1016/j.chemosphere.2006.12.024. [ Links ]

Morel, F.M., A. Kraepiel and M. Amyot. 1998. The chemical cycle and bioaccumulation of mercury. Annu. Rev. Ecol. Syst., 29(1): 543-66. https://doi.org/10.1146/annurev.ecolsys.29.1.543. [ Links ]

Otchere, F.A. 2019. A 50-year review on heavy metal pollution in the environment: Bivalves as bio-monitors. Afr. J. Environ. Sci. Tech., 13(6): 220-227. [ Links ]

Otchere, F.A., C.R. Joiris and L. Holsbeek. 2003. Mercury in the bivalves Anadara (Senilia) senilis, Perna perna and Crassostrea tulipa from Ghana. Sci. Total Environ., 304: 369-375. https://doi.org/10.1016/S0048-9697(02)00582-X. [ Links ]

Riget, F., P. Johansen and G. Asmund. 1996. Influence of length on element concentrations in blue mussels (Mytilus edulis). Mar. Pollut. Bull., 32(10): 74551. doi:10.1016/0025-326X(96)00067-7. [ Links ]

Santana, V., G. Medina y A. Torre. 2014. El convenio de Minamata sobre el mercurio y su implementación en la región de América Latina y el Caribe. http://www.mercuryconvention.org/Portals/11/documents/publications/informe_Minamata_LAC_ES_FINAL.pdf. [ Links ]

Scardino, A., R. De Nys, O. Ison, W. O'Connor and P. Steinberg. 2003. Microtopography and antifouling properties of the shell surface of the bivalve molluscs Mytilus galloprovincialis and Pinctada imbricata. Biofouling, 19: 221-230. doi: 10.1080/0892701021000057882. [ Links ]

Schudel, G., R.A. Miserendino, M.M. Veiga, P.C. Velásquez-López, P.S.J. Lees, S. Winland-Gaetz, J.R. Guimarães and B.A. Bergquist. 2018. An investigation of mercury sources in the Puyango-Tumbes River: using stable Hg isotopes to characterize transboundary Hg pollution. Chemosphere, 202: 777-787. https://doi.org/10.1016/j.chemosphere.2018.03.081. [ Links ]

Schudel, G ., R. Kaplan, R.A. Miserendino , M.M. Veiga , P.C. Velásquez-López , J.R. Davée Guimarães and B.A. Bergquist . 2019. Mercury isotopic signatures of tailings from artisanal and small-scale gold mining (ASGM) in southwestern Ecuador. Sci. Total Environ., 686: 301-10. https://doi.org/10.1016/j.scitotenv.2019.06.004. [ Links ]

Secretaria Nacional de Planificación y Desarrollo. 2009. Evaluación social y técnica de los recursos hídricos de las subcuencas de los ríos Jagua, Balao, Gala, Tengel y Siete, en la provincia de Azuay. https://es.scribd.com/doc/29929927/INVENTARIO-R-HIDRICOS-JAGUA-TENGUELGALA-SIETE. [ Links ]

Sevillano, J.S., M. Cejudo-Gómez, A.M. Ramírez-Ojeda, F. Cámara-Martos and R. Moreno-Rojas. 2015. Risk profile of methylmercury in seafood. Curr. Opin. Food. Sci., 6: 53-60. https://doi.org/10.1016j.cofs.2016.01.003. [ Links ]

Silva, F.S., W. Machado, F. Lisboa and D. Lacerda. 2003. Mercury accumulation in sediments of a mangrove ecosystem in SE Brazil. Water Air Soil Poll., 145: 67-77. https://doi.org/10.1023/A. [ Links ]

Tam, N. e Y. Wong. 1995. Spatial and temporal variations of heavy metal contamination in sediments of a mangrove swamp in Hong Kong. Mar. Pollut. Bull., 31(4-12): 254-261. https://doi.org/10.1016/0025-326X(95)00141-9. [ Links ]

Tarras-Wahlberg, N.H., A. Flachier, G. Fredriksson and S. Lane. 2000. Environmental impact of small-scale and artisanal gold mining in southern Ecuador. AMBIO, 29(8): 484-491. doi: 10.1579/0044-7447-29.8.484. [ Links ]

U.S. Environmental Protection Agency. 1989. Risk assessment guidance for superfund. Vol. I Human Health Evaluation Manual (Part A). https://doi.org/EPA/540/1-89/002. [ Links ]

U.S. Environmental Protection Agency. 2001. Water quality criterion for the protection of human health: methylmercury. Methylmercury water quality criterion. EPA-823-R-. https://doi.org/EPA-823-F-01-001. [ Links ]

U.S. Environmental Protection Agency. 2002. Calculating upper confidence limits for exposure point concentrations at hazardous waste sites. Washington. [ Links ]

Vane, C.H., I. Harrison, A.W. Kim, V. Moss-Hayes, B.P. Vickers and K. Hong. 2009. Organic and Metal contamination in surface mangrove sediments of south China. Mar. Pollut. Bull., 58: 134-144. https://doi.org/10.1016j.marpolbul.2008.09.024. [ Links ]

Velásquez López, P.C., M.M. Veiga , B. Klein, J.A. Shandro and K. Hall. 2011. Cyanidation of mercury-rich tailings in artisanal and small-scale gold mining: identifying strategies to manage environmental risks in southern Ecuador. J. Clean. Prod., 19(9-10): 1125-1133. https://doi.org/10.1016/j.jclepro.2010.09.008. [ Links ]

World Health Organization. 1996. Guidelines for drinking water quality. Vol. 2. Geneva: WHO library. [ Links ]

World Health Organization. 2008. Guidance for identifying populations at risk from mercury exposure. Geneva. https://doi.org/10.1289/ehp.7856. [ Links ]

Zuykov, M., E. Pelletier, C. Belzile and S. Demers. 2011. Alteration of shell nacre micromorphology in blue mussel Mytilus edulis after exposure to free-ionic silver and silver nanoparticles. Chemosphere, 84: 701-706. doi: 10.1016/j.chemosphere.2011.03.021. [ Links ]

Zuykov, M ., E. Pelletier , R. St-Louis, A. Checa and S. Demers . 2012. Biosorption of thorium on the external shell surface of bivalve mollusks: The role of shell surface microtopography. Chemosphere, 86: 680-683. https://doi.org/10.1016/j.chemosphere.2011.11.023. [ Links ]

Received: August 24, 2019; Accepted: April 20, 2020

maríaf.rivera@espoch.edu.ec * Autora para correspondencia

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License