Changes in mercury content in oysters in relation to sediment and seston content in the Colombian Caribbean lagoons

doi:10.21203/rs.3.rs-4725392/v1

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Changes in mercury content in oysters in relation to sediment and seston content in the Colombian Caribbean lagoons

https://doi.org/10.21203/rs.3.rs-4725392/v1

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Total mercury was evaluated in the mangrove oyster Crassostrea rhizophorae, in sediments and seston from the Ciénaga Grande de Santa Marta (CGSM) and Cispatá Bay (BhC) in two climatic seasons (rainy and dry). Composite samples of sediments, seston and oysters in juvenile and adult sizes were collected at six stations (three in each ecosystem) and Hg was quantified by atomic absorption spectrophotometry (EPA method 7473 PLTX-017). BhC had the highest Hg concentrations in sediment, seston and oysters compared to CGSM, with values close to the tolerable threshold for the ecosystem and associated biota (TEL) of 0.13 µg/g Hg and with a low risk of Hg contamination in the mangrove oyster. Although at CGSM Hg was below the TEL in sediment and was considered safe in the oyster, significant bioaccumulation was evident with the metal content in the seston, indicating a potential risk to the ecosystem and humans. The variables organic matter and temperature influenced metal availability in the sediment and seston, respectively; in contrast, they had no significant relationship in the oyster. In CGSM, higher [Hg] was recorded in adult sizes, while in BhC the highest accumulation occurred in juveniles, especially during the dry season. These results emphasize the need for continuous monitoring of Hg contamination in both ecosystems. In addition, they highlight the importance of considering the size of oysters when assessing Hg contamination, as they may vary according to specific ecosystem and climatic conditions.

Mercury

Crassostrea rhizophorae

bioconcentration factor

pollution index

sizes

Mercury contamination is a global environmental challenge due to its capacity for bioaccumulation and biomagnification in food webs, and its potentially devastating effects on ecosystems [1, 2]. Throughout history, catastrophic events linked to metal contamination have been recorded, with the Minamata disaster in Japan being the iconic example for Hg intoxication. This incident, generated by the release of Hg in toxic forms such as methylmercury (CH₃Hg) into Minamata Bay, left catastrophic after-effects on both the human population and local marine life [3]. This grim historical episode strongly underscores the dangers of Hg to human health and the environment.

Hg contamination represents a significant threat to coastal marine ecosystems. The ability of this element to bioaccumulate and biomagnify in the tissues of organisms means that it can reach dangerous concentrations as it progresses through the food web [4]. Hg in toxic forms such as CH₃Hg affects the reproduction of aquatic organisms, with negative effects on the formation and growth of eggs and larvae. It also has serious neurological impacts, altering behaviors such as feeding and predator avoidance [5]. Bivalves, such as oysters, are vulnerable at the cellular level to Hg, affecting their reproduction, growth and quality of edible tissues for humans [6]. This phenomenon has generated global concern, prompting the use of indicator organisms, such as bivalves, to assess their presence in marine-coastal ecosystems [7].

Despite the decrease in Hg levels in bivalves due to stricter regulations, concerns persist worldwide. Colombia, unfortunately, does not escape from this problem, as it is among the countries with the highest per capita Hg contamination in the world, largely due to illegal mining and gold mining [8].

In Colombia, despite the growing interest in the problem generated by Hg contamination due to illegal mining and gold mining, research on the presence of this metal in bivalves is recent. Studies conducted in areas near Cartagena Bay, such as Brujas Island and Barú Island in Cartagena, as well as in the Marina and Taganga in Santa Marta, have revealed variations in Hg concentrations in the oyster Crassostrea rhizophorae, depending on the climatic season [9]. In addition, it has been observed that climatic conditions in tropical regions, such as the Colombian Caribbean, as well as changes in physicochemical variables in the water column such as temperature, salinity, pH and dissolved oxygen [10], and the organic matter content in fine sediments and reducing condictions [11] can influence the availability of Hg in the environment.

The response of bivalves to environmental variables during their life cycle [12] complicates the understanding of Hg accumulation. In turn, the differences in Hg concentrations between sites highlight [9, 10] the need to further understand the factors that influence Hg concentrations in marine and coastal organisms such as the oyster C. rhizophorae, determine the specific sources of contamination, and assess the impacts on local ecosystems in Colombia.

This study evaluated Hg contamination in the oyster C. rhizophorae and determined whether environmental variables and oyster size can facilitate Hg bioaccumulation. The research contributes to understanding the dynamics of contamination by this metal in tropical marine and coastal systems.

2.1 Study area

The Colombian Caribbean region is characterized by a bimodal climatic regime with a rainy and dry season influenced by the Intertropical Convergence Zone (ITCZ) that generates periodic patterns [13]. Trade winds predominate from December to April (dry season), changing direction to the southeast between April and November (rainy season) [14].

The Ciénaga Grande de Santa Marta (CGSM) has an area of 450 km² [15] and was declared a Ramsar Wetland and Biosphere Reserve [16]. Its body of water is made up of several interconnected lagoons and a sand bar to the northeast of the Ciénaga that separates it from the Caribbean Sea [17] (Fig. 1). The exchange of fresh and brackish water is conducive to the development of the red mangrove Rhizophora mangle, which is essential for the mangrove oyster because it (the mangrove root) provides a substrate for the oysters [18]. It stands out as one of the most productive tropical ecosystems in the Caribbean, with significant catches of commercial fish, crustaceans and mollusks [19].

The bay of Cispatá (BhC) was transformed into an estuary as part of the lagoon system of the Sinú River delta. This mangrove-estuarine ecosystem has fine and very fine sediments, largely influenced by the Sinú River [20]. The estuary covers an area of 130 km² covered predominantly by mangroves [21] (Fig. 1), has an average monthly rainfall of 66 mm and an average sediment discharge of 3.1 kg/day. The rainy season from May to November records an average monthly rainfall of 150 mm and a sediment discharge of 11.5 kg/day [22]. Salinity is influenced by the hydrological dynamics of the ecosystem, fluctuating between rainy seasons, drought and a mixture of fresh and brackish water [23].

2.2 Field phase

Samples were collected at three stations in CGSM and three in BhC trying to cover sites with gradients of water inflow from the sea and freshwater bodies that may carry contaminants. Sampling was conducted in the rainy season (November 2021) and in the dry season (March 2022). In situ measurements of temperature, salinity, pH and dissolved oxygen were made at a depth of 0.5 m using WTW 3110 and YSI Pro1030 multiparameter probes.

Oyster individuals were collected at each of the stations and grouped into juveniles (22.0–32.0 mm) and adults (35.0-56.5 mm) [24, 25]. Several specimens of the same category were stored in previously labeled airtight polyethylene bags and transferred preserved in cold (~ 4°C).

For the determination of mercury in seston, at each station three replicates of water were collected in 2.8 L amber flasks and stored cold (~ 4°C). After homogenization, they were filtered through two Whatman GF/C glass fiber filters of 47 mm diameter per sample with a manual vacuum pump. They were stored in hermetically sealed polyethylene bags previously labeled, dried in an oven at 45°C for 24 h and weighed on an analytical balance [11].

At each station, three replicates of sediment were collected with a van Veen dredge. From each unified sample per station, 600 g of sediments were separated to determine mercury, 75 g for organic matter and 75 g for redox potential. Samples were stored in airtight polyethylene bags with silicone scoop avoiding touching the edges of the dredge and kept cold (~ 4°C) [11].

2.3 Laboratory phase

For the determination of organic matter, 5 g of dry sediment were placed in porcelain crucibles (previously weighed), subjected to calcination in a muffle at 550°C for 5 h and kept in the desiccator for 2 h. The determination of organic matter was based on the difference in dry and calcined weight [26].

For redox potential quantification, the sediment sample was dried at 40°C for 24 h. 25 g of sediment were taken and homogenized in 50 mL of deionized water using a VELP Scientifica magnetic stirrer for 30 min. Measurement was performed with a YSI Pro1030 multiparameter probe through the oxidation-reduction potential electrode, previously calibrated at a standard temperature of 25°C [27].

For the chemical analyses, all the material used was previously purged with 5% nitric acid (HNO₃) and deionized water for 24 h. With the precaution of not contaminating the samples, gloves and glass and plastic elements were used. The samples were transferred cold preserved (~ 4°C) to the Toxicology and Environmental Management laboratory of the University of Cordoba for Hg quantification.

The collected oysters were cleaned to remove any particles adhering to the valves. The anteroposterior length APL (mm) was measured on the inner side of the ventral valve to the mark of the edge of the mantle with a Vernier caliper (precision of 0.05 mm). The soft tissue was then weighed using an analytical balance (0.1 mg accuracy). In each sample composed of organisms of similar size, all soft tissue was removed and deposited in 30 mL glass vials previously washed, labeled and weighed. The soft material was weighed by subtracting the weight of the vial and the samples were lyophilized.

From each seston, sediment, and oyster tissue sample, 20 to 40 mg were weighed and subjected to calcination at 450°C with a ramp of 50°C for 8 h. Then, 1 mL of concentrated HNO₃ was added and volatized on a heating plate. Finally, the sample was subjected to microwave-assisted acid digestion at 180°C for 20 min with a volume of 25 mL of distilled water.

The fraction less than or equal to 65 µm of sediments and seston was digested with 5% nitric acid (HNO₃) for subsequent determination of total Hg concentration by atomic absorption spectrometry [28]. Hg analysis was performed by EPA method 7473 PLTX-017, which consists of direct analysis by thermal decomposition, amalgamation, and atomic absorption spectrometry [29].

For the analytical control in sediments, seston and oysters, a triplicate analysis of a solution of Hg at different concentrations (0.02, 0.05 and 0.5 µg of Hg) was used, complying with the acceptance criteria of the Association of Official Analytical Chemists (AOAC), with determination coefficients greater than 0.995 for the calibration curve and error percentages of less than 15%. TORT-1 (lobster hepatopancreas) from the National Research Council of Canada (NRCC) was used as reference material. Recovery percentages were 100 ± 1.4% in sediments (limit of detection, LOD, = 0.00073 µg/g Hg), 100 ± 5.4% in seston (LOD = 0.000015 µg/g Hg) and 100 ± 1.4% in oysters (LOD = 0.00073 µg/g Hg) [12].

2.4 Cabinet phase

The bioconcentration factor (BCF) was calculated as the ratio of Hg concentration in oyster tissue to its presence in sediment (sd) and seston (st), expressed in parts per million (ppm, µg/g) in dry weight (d.w.). This calculation was based on Mountouris et al. [1] and Romero-Murillo et al. [12].

$$\:{BCF}_{sd}=\frac{{\left[Metal\right]}_{organism}}{{\left[Metal\right]}_{sedimento}},\:{BCF}_{st}=\frac{{\left[Metal\right]}_{organism}}{{\left[Metal\right]}_{seston}}$$

BCF was used to evaluate the efficiency of Hg accumulation in oyster soft tissue. According to Mountouris et al. [1], BCF < 1 suggests no metal accumulation, BCF ≥ 1 and < 10 indicates accumulation and BCF ≥ 10 indicates hyperaccumulation of metal.

Permutation analysis of variance (PERMANOVA) was applied to compare Hg concentration in oyster tissue and its BCF between the two ecosystems (k = 2), the two climatic seasons (k = 2), the six stations (k = 6) and the two categorized size classes (k = 2). 9 999 permutations were performed using Euclidean distance and type III sum of squares. The p-values was computed using Monte Carlo (MC) permutation testing only when unique permutations were less than 100 [30].

The relationship of Hg concentration between sediment and seston was examined using Pearson's (data fitted to the normal distribution) and Spearman's (data not fitted to the normal distribution) correlation analyses. These analyses were conducted to identify potential relationships between physicochemical variables on Hg availability in sediments and seston [31]

The influence of environmental predictor variables on the oyster Hg concentration and Hg BCF in relation to seston was evaluated using a distance-based linear model (DistLM) with adjusted R² criterion and 9999 permutations [30].

To evaluate mercury contamination in bivalves, the Nemerow integral contamination index -P_c- was used [32]. The calculation of P_c is based on the average value of the individual pollution index (P_avg), the maximum value (P_max) and the minimum value (P_min). The individual index values were calculated using the following formula:

$$\:{P}_{avg}=\frac{{C}_{avg}}{S},\:{\:\:\:\:\:\:P}_{max}=\frac{{C}_{max}}{S},\:{\:\:\:\:\:\:P}_{min}=\frac{{C}_{min}}{S}\:\:\:\:\:\:\:\:\:\:\:\left[1\right]$$

C _avg is the average concentration value recorded in the data set evaluated, C_max and C_min are the maximum and minimum concentration values from the same data set, and S is the maximum concentration allowed in marine organisms (mollusks) with Hg (0.5 µg/g) [33].

Once the historical values of P_avg, P_max and P_min were obtained for each country by year, the calculation of P_c was performed establishing (i) P_c ≤ 0.7 considered no risk, (ii) 0.7 < P_c ≤ 1 low risk, (iii) 1 < P_c ≤ 2 medium risk, (iv) 2 < P_c ≤ 3 high risk and (v) P_c > 3 very high risk of contamination [29]. It was calculated using the following equation:

$$\:\frac{\sum\:{P}_{c}}{n}=\sqrt{\frac{{P}_{avg}^{2}+{P}_{max}^{2}+{P}_{min}^{2}}{3}}\:\:\:\:\:\:\:\:\:\:\:\:\:\:\left[2\right]$$

ΣP_c is the sum of all P_c values divided by "n", the total number of years evaluated per country published in its historical record. This ensures that the values of P_max and P_min do not overestimate or underestimate the calculation of the contamination index for each metal evaluated, respectively.

The similarities and differences of the sites were assessed with a hierarchical clustering analysis, a multivariate technique applied to construct distance dendrograms from the classification of each site according to the level of metal contamination. The analysis was applied through the use of the squared Euclidean distance with Ward's linkage, minimizing variability and producing uniformly sized clusters [34, 35].

3.1 Environmental conditions in both coastal lagoons

The average water temperature in CGSM and BhC reached its highest value during the rainy season. In CGSM, the temperature during the rainy season was 31.17 ± 0.48°C (n = 3), while in dry season it was 30.53 ± 0.84°C (n = 3). In BhC, with slightly lower temperatures compared to CGSM, the temperature during the rainy season was 28.97 ± 0.43°C (n = 3), and in dry season it was 29.75 ± 0.03°C (n = 3) (Fig. 2A, Supplementary Table S1).

Regarding pH, during the rainy season, CGSM had a higher pH value (8.77 ± 0.12, n = 3) compared to BhC (7.84 ± 0.09, n = 3), while during the dry season, were a decrease in pH in CGSM (8.44 ± 0.16, n = 3) and an increase in BhC (8.19 ± 0.003, n = 3). The values were similar in both study areas (Fig. 2A, Supplementary Table S1).

The average dissolved oxygen content was higher in CGSM during both climatic seasons, with values of 7.83 ± 0.66 mg/L (n = 3) in rainy season and 7.39 ± 2.4 mg/L (n = 3) during dry season. In BhC, the contents were 4.32 ± 0.5 mg/L (n = 3) in rainy season and 5.52 ± 1.28 mg/L (n = 3) along the dry season (Fig. 2A, Supplementary Table S1).

Regarding salinity and organic matter, CGSM showed variations in these variables, with salinity values from 2.47 ± 1.01 (n = 3) in rainy season to 18.53 ± 6.33 (n = 3) in dry season, and organic matter content during the rainy season of 11.67 ± 3.27% (n = 3), doubling the observed values on the dry season (5.97 ± 2.4%, n = 3). In contrast, in BhC, the average salinity values (from 24.9 ± 1.01, n = 3 to 30.83 ± 0.56, n = 3) and organic matter (from 5.6 ± 0.5%, n = 3 to 6.06 ± 1.28%, n = 3) varied the less between those two climatic seasons (Fig. 2A, Supplementary Table S1).

In sediments the redox potential, both in CGSM and BhC, reducing conditions were recorded with a range of values from 28 to 77 mV between both study areas. Increases in redox potential were observed in BhC (52 ± 3, n = 3 to 65 ± 4, n = 3), and decreases in CGSM (50 ± 11, n = 3 to 35 ± 4, n = 3) from rainy season to dry season (Fig. 2A, Supplementary Table S1).

3.2 Concentration of Hg in sediments, seston and Crassostrea rhizophorae

Hg concentration in sediments and seston varied markedly between the two ecosystems. In BhC, in both sediments and seston, Hg concentrations are consistently higher than in CGSM in both climatic seasons (Fig. 2B, Supplementary Table S2).

In the rainy season, the highest concentration of Hg in sediments was found in CIS-1 (BhC) with 0.128 µg/g Hg dry weight (d.w.) which is double the highest content detected in CGSM (0.059 µg/g Hg _d.w. in CGS-1). Hg content in sediments at BhC was slightly lower in the dry season but remained above 0.08 µg/g Hg _d.w. indicating a possible constant source of Hg contamination. In CGSM, during the dry season, lower Hg was observed in CGS-1 and higher in CGS-2 (Fig. 2B, Supplementary Table S2).

Table 1

PERMANOVA analysis on Hg concentration and bioconcentration factor (BCF-Hg) vs. sizes (juveniles and adults), stations, ecosystem, and climatic season in the oyster *Crassostrea rhizophorae*. Ecosytem (EC), climatic season (CS), station (ST), size (SZ), degrees of freedom (df), sum of squares (SS), and mean square (MS). For more information, see Supplementary Table S4
Hg (µg/g d.w.)
Factor	df	SS	MS	Pseudo-F	Únique	p-value
EC	1	8.8 × 10^− 2	8.8 × 10^− 2	47.31	9 836	1 × 10^− 4
CS	1	4.6 × 10^− 5	4.6 × 10^− 5	0.03	9 837	0.876
ST (EC)	4	2.5 × 10^− 2	6.2 × 10^− 3	3.31	9 948	1.6 × 10^− 2
EC × CS	1	5.3 × 10^− 3	5.3 × 10^− 3	2.85	9 843	0.098
SZ (ST (EC))	6	4.6 × 10^− 2	7.7 × 10^− 3	4.11	9 954	1.8 × 10^− 3
CS × ST (EC)	4	2.9 × 10^− 2	7.4 × 10^− 3	3.94	9 949	7 × 10^− 3
CS × SZ (ST (EC))	6	2.5 × 10^− 2	4.2 × 10^− 3	2.27	9 939	0.049
Residual	47	8.8 × 10^− 2	1.87 × 10^− 3
Total	70	3.07 × 10^− 1
BCF-Hg
Factor	df	SS	MS	Pseudo-F	Únique	p-value
EC	1	747.7	747.7	72.14	9 841	1 × 10^− 4
CS	1	594.8	594.8	57.39	9 864	1 × 10^− 4
ST (EC)	4	62.78	15.7	1.514	9 954	0.219
EC × CS	1	152.9	152.9	14.76	9 837	4 × 10^− 4
SZ (ST (EC))	6	200.8	33.5	3.23	9 949	0.011
CS × ST (EC)	4	84.1	21.03	2.03	9 951	0.107
CS × SZ (ST (EC))	6	322.4	53.7	5.18	9 931	4 × 10^− 4
Res	47	487.1	10.3
Total	70	2 720

* p-value < 0.05 indicates significant differences among the analyzed factors. In red the significant ones.

The Hg available in the seston presented similar values in the stations of each ecosystem and in the two climatic seasons. However, as in sediments, a lower concentration was detected in the dry season. In BhC, the concentration went from 0.032 ± 0.005 µg/g Hg _d.w. in the rainy season to 0.022 ± 0.001 µg/g Hg _d.w. in the dry season. Lower concentrations were found in CGSM, with values ranging from 0.01 ± 0.001 µg/g Hg _d.w. in the rainy season to 0.004 ± 0.001 µg/g Hg _d.w. in the dry season (Fig. 2B, Supplementary Table S2).

In BhC the highest Hg content in seston was positively and significantly related to temperature (Pearson, r = 0.93, p-value < 0.001) and in sediments Hg was significantly related to organic matter (Pearson, r = 0.84, p-value = 0.04) (Fig. 2, Supplementary Table S3).

Hg concentrations in oyster tissue show distinct accumulation patterns in CGSM and BhC, varying as a function of climatic seasons. However, a pattern similar to that of sediment and seston was maintained, with a higher Hg content in oyster soft tissue in BhC (Fig. 2B). In the rainy season, Hg in the oyster was 0.083 ± 0.007 µg/g _d.w. (n = 17) in CGSM and of 0.135 ± 0.015 µg/g _d.w. (n = 18) in BhC showing significant differences between the two ecosystems (Permanova, p-value < 0.01). In dry season, these differences were maintained, given the decrease in oyster Hg content in CGSM (0.066 ± 0.007 µg/g Hg _d.w., n = 18) and increased in BhC (0.154 ± 0.019 µg/g Hg _d.w., n = 18) (Table 1, Fig. 3A, Supplementary Table S4).

With respect to Hg BCF, both in sediments and seston, both ecosystems presented accumulation to hyperaccumulation of Hg in the oyster tissue, with the highest values in the dry season. In this same climatic season, at CGSM, the oyster presented an accumulation of Hg with the sediment (BCF ≥ 1) and a hyperaccumulation of the metal with the seston (BCF ≥ 10), as opposed to the accumulation condition in both matrices during the rainy season. In BhC, the oyster maintained the accumulation condition in both matrices (BCF ≥ 1) as in rainy season (Table 1). These results notably emphasize the capacity of the oyster to accumulate Hg in its tissues, especially in CGSM through the seston in the dry season. Significant differences in BCF were determined between CGSM and BhC ecosystems, with higher concentrations in BhC (Permanova, p-value < 0.05). However, no significant differences in concentrations were observed between climatic seasons, since the values measured at two of three stations in both CGSM (CGS-2 and CGS-3) and BhC (CIS-1 and CIS-3) were similar in both climatic seasons (Table 1, Fig. 3B, Supplementary Table S4).

In the two ecoystems evaluated, there were significant differences in the Hg contents between stations (Permanova, p-value < 0.05; Table 1). In the rainy season at CGSM the differences occurred between stations CGS-1 and CGS-2 and at BhC between CIS-2 and CIS-3. In the dry season, significant differences were found between CIS-1 and CIS-2 in BhC, with the lowest concentrations in CIS-1 (Fig. 2B, Supplementary Table S4 and S5).

There were significant differences in the length of juveniles and adults (Permanova, p-value < 0.05) between stations (Table 1). In CGSM in the dry season, concentrations were higher in adult sizes at station CGS-3 (0.121 ± 0.016 µg/g Hg _d.w.) with respect to juveniles (0.039 ± 0.009 µg/g Hg _d.w.). In BhC, in both rainy and dry seasons, the highest concentration of juvenile lengths was at station CIS-2 (Fig. 3A, Supplementary Table S4 and S5).

3.2.1 Importance of seston in the bioconcentration of Hg

High Hg bioconcentration factor values reflected a significant correlation with seston content (Pearson, r = 0.72, p-value < 0.01), with conditions of accumulation (BCF ≥ 1) in BhC and hyperaccumulation in CGSM (BCF ≥ 10; Supplementary Table S4).

Differences in Hg bioconcentration between CGSM and BhC were determined (Permanova, p-value < 0.05; Table 1). These differences were also observed as a function of climatic seasons, with an increase during the dry season in each CGSM season, and significant in the CIS-2 season in BhC compared to the rainy season. When the factors ecosystem and climatic season were combined, significant differences were still present, with higher values of Hg bioconcentration in CGSM in both climatic seasons compared to BhC (Fig. 3B, Supplementary Table S4 and S5). These results indicate that the oyster in CGSM is accumulating higher concentrations of Hg in its tissues compared to the BhC oyster, although the accumulation is also considerably higher in the BhC oyster.

Significant differences between juvenile and adult sizes were determined with the BCF-Hg, which was maintained when considering the climatic season (Table 1). In BhC, the highest values of BCF-Hg were observed in juvenile sizes in both climatic seasons. In CGSM, the highest BCF occurred in adult sizes during the dry season, while they were similar in both sizes during the rainy season (Spearman, r = 0.25, p-value > 0.05; Fig. 3B, Supplementary Table S4).

Table 2

Analysis of DistLM in the relationship between Hg concentration and its bioconcentration in *Crassostrea rhizophorae* with physicochemical variables (predictors). Stepwise model and selection criterion of adjusted R² were used (9999 permutations). SS: sum of squares.
Juvenile size
Variable	SS	Pseudo-F	p-value	Proportion of variation explained
Temperature	11.2	0.41	0.54	0.039
Salinity	28.1	1.09	0.33	0.098
pH	27.8	1.07	0.33	0.097
Dissolved oxygen	22.1	0.84	0.38	0.077
Organic matter	0.61	0.02	0.89	0.021
Adult size
Variable	SS	Pseudo-F	p-value	Proportion of variation explained
Temperature	1.2	0.03	0.88	0.026
Salinity	4.5	0.09	0.77	0.098
pH	39.9	0.95	0.36	0.087
Dissolved oxygen	106.7	3.01	0.11	0.231
Organic matter	0.1	0.03	0.96	0.026

*p-values < 0.05 express that the variable significantly explains the variations in Hg content and its bioconcentration in Crassostrea rhizophorae. In red is the greatest variation explained.

3.3 Relationship between environmental variables and Hg bioconcentration in oysters

Between the Hg concentration in the mangrove oyster tissue and its BCF by size in relation to the metal content in the seston, it was not possible to find a positive or negative relationship with the environmental variables analyzed. The relationship between physicochemical variables and size with Hg concentration and BCF in the mangrove oyster were not significant (DistLM; p-value > 0.05; Table 2). This suggests that environmental variables and size did not play a determining role in the differences in oyster Hg content and bioconcentration at CGSM and BhC (Fig. 3). Other factors, such as Hg content in the seston and local transport and sedimentation processes, may be playing a more influential role in Hg accumulation.

3.4 Hg contamination status of bivalves in a global context during the last decade

Considering Hg contamination levels in global monitoring during the last 12 years in different bivalve species, both ecosystems are part of Clade 1, CGSM presents no risk of Hg contamination in oyster consumption (similar to Taganga), while BhC is close to a low risk of Hg contamination along with Isla Cayo el Pigeon (Nicaragua). However, these values exceed those reported in other areas such as China, Italy and Montenegro, which presented the lowest risk of Hg consumption by bivalves. This makes it relevant to consider the potential risk of Hg contamination in the Colombian Caribbean, which presented the highest risk of contamination by Hg in the world with bivalves during the last decade (Fig. 4).

The higher concentrations of Hg, in all of them sediment, seston and oyster, in BhC compared to CGSM (Fig. 2B, Supplementary Table S1) raise concerns about environmental quality and ecosystem health in the region. Hg contamination in BhC is linked to the connection of the Sinú River through the Sicará stream, suggesting contamination associated with water and sediment flows from surrounding agricultural areas [36], as well as the use of fungicides containing phenylmercury (C₆H₅Hg) and extensive spraying of rice fields with mercury agrochemicals [37]. Other sources identified include regional gold mining, wastewater discharge, use of Hg in ship paints as an anti-corrosion compound, and air pollution [38, 39].

In CGSM, the sources of Hg contamination are less clear; the entry of this metal into the swamp is associated with atmospheric deposits and anthropogenic activities [40], gold mining and industrial activities [41, 42] mainly from the Magdalena River [43].

Although the levels of Hg in sediments in BhC and CGSM are lower than those reported in other regions, such as in Cartagena Bay, Colombia (0.094–10.293 µg/g Hg _d.w.) [40] and in San Vicente Bay, Chile (0.37 to 0.95 µg/g Hg _d.w.) [44], and considering that the Hg content was below the tolerable threshold for the ecosystem and associated biota (TEL) of 0.13 µg/g [45], the risk of Hg contamination is higher in BhC compared to CGSM. In previous assessments conducted by Feria et al. [46], Campos et al. [36] and Marrugo-Negrete et al. [37], Hg concentrations exceeding the TEL threshold have been reported in sediments along the Sinú riverbed and at the mouth of the BhC. In contrast, in CGSM, Hg concentrations reported in sediments have been less than 0.11 µg/g Hg _d.w., being similar to what was found in this study (Fig. 2B).

The slight increase in Hg content in sediment and seston during the rainy season compared to the dry season (Fig. 2B) could be attributed to metal flushing from land-based sources, influenced by increased sediment and freshwater input [47, 48]. These factors are especially relevant in the CGSM with significant contributions from the Magdalena River in the CGSM [40] and the Sinú River in BhC [37]. Although these variations between climatic seasons were not significant for Hg content in the mangrove oyster (Table 2, Fig. 3A), the importance of sediment-seston interaction and the influence of local conditions in the coastal areas of the Colombian Caribbean on Hg availability in the oyster is highlighted [9].

Variables such as temperature and organic matter may be playing an important role in the Hg content of sediments and seston. In BhC, the highest Hg contents in the seston during the rainy season were significantly correlated with the highest temperature values (Fig. 2), this being a variable that can affect the rate of chemical reactions, including its methylation [49]. In turn, higher Hg values in sediments were related to higher organic matter content in the rainy season, underlining the fundamental role of organic matter in the retention of metals in sediments, together with fine sediments and a sulfate-reducing environment [11], as in CGSM [43] and BhC (Fig. 2A).

Although no direct correlation was identified between pH and Hg concentrations in sediments and seston (Supplementary Table S3), slightly acidic or neutral pH conditions result in higher Hg precipitation in sediments [50], which could possibly explain why BhC, with lower pH values, had higher Hg contents in sediments compared to CGSM (Fig. 2).

Another aspect to take into account in the precipitation of Hg in sediments is the variations from sulfates to sulfides, which possibly increase the flux of reactive phosphate and ammonium at the sediment-water interface [51]. This process favors that Hg tends to precipitate in the sediments as insoluble hydroxides, oxides, carbonates or phosphates [52, 53]. The interaction of these processes could help to understand the variations of Hg content in sediments, taking into account the pH values in each climatic season. This pattern is particularly noticeable in BhC because of the differences in pH from rainy to dry season (Fig. 2).

With respect to the mangrove oyster, the influence of the environmental variables analyzed on the concentration and bioconcentration factor (BCF) of Hg was not significant (Tables 2, Fig. 3, Material Supplementary S4). This finding responds to what has been reported in other investigations, in which the influence of variables such as temperature, salinity and pH on the uptake and accumulation of Hg is not completely understood in bivalves [53], unlike what occurs in sediments and seston in which the processes of accumulation, uptake, toxicity and speciation of Hg are known [54, 55].

Although no significant relationship could be established between Hg BCF with environmental conditions in CGSM and BhC, it is important to consider that high concentrations of dissolved oxygen in CGSM, together with changes in the chemical composition of the sediments, may increase and/or alter the metabolic activity of bivalves [56, 57], which could affect the capacity for Hg uptake and excretion in bivalves such as the oyster [55].

The mangrove oyster is known for its ability to filter large volumes of water during feeding [17] and particulate matter from sediments [58]; therefore, Hg concentrations in the oyster were closely related to the metal content in its environment (Fig. 2B). Hg bioconcentration was significantly associated with seston, which was to be expected considering that collection of the organism was mainly on mangrove roots. As with seston, metal accumulation and hyperaccumulation were obtained with respect to Hg concentrations in the sediment (Table 1). In this regard, measurements of metals in sediments, such as with seston, provide crucial data on the availability and uptake of Hg by the bivalve, providing a comprehensive view of the interaction between these organisms and their contaminated environment.

The results in BhC are consistent with previous studies. Coimbra [59] in Sepetiba Bay in Brazil in Mytela guyanensis and Díaz et al. [44] in San Vicente Bay in Chile in Tagelus dombeii, reported inverse correlations between Hg content and species size. They suggested that there are metal assimilation rates similar to the excretion rate in larger individuals, which may be generated by decreased metabolism and less water pumping with bivalve growth [60].

During the growth of bivalves, several mechanisms are involved that regulate the accumulation of toxic metals such as Hg in their tissues. The formation of mineralized granules allows storage and possibly detoxification by Hg [61]. For its release, bivalves develop a homeostatic regulation system during their growth that includes several excretion mechanisms through urine and feces, which contribute to maintain adequate Hg concentrations [62].

Another aspect is the development of new gill systems; their formation plays a key role in the filtration of particles, including metals from the aquatic environment [48]. This progressive development of gill systems contributes to the efficiency of bivalves in capturing and regulating Hg in their tissues as they develop.

The emission of gametes during reproduction is another important strategy that bivalves deploy to mitigate the accumulation of toxic metals [60]. During the release of gametes from the mangrove oyster, an increase in Hg BCF could have been experienced during the rainy season, as it is associated with a decrease in organism biomass with spawning [63]. However, in both CGSM and BhC the highest values of BCF in oysters were obtained during the dry season (Table 1, Fig. 3B). During gamete release, which generally occurs during the rainy season and encompasses several breeding peaks in the Colombian Caribbean [17], mineralized granules stored in the lysosomes may be released along with the gametes. This process, called exocytosis, allows the contents of lysosomes, including metals such as Hg, to be released into the aquatic environment [61]. This possible release of mineralized Hg granules in lysosomes together with the expulsion of gametophytes could have contributed to the lower Hg BCF values during the rainy season.

As for CGSM, slightly higher concentrations and BCF in adult lengths were observed in dry season, similar to what was reported by Costa et al. [64] and De Gregori et al. [65], and being the inverse of what was found in BhC in both climatic seasons. This result highlights the complexity of the relationship between the various environmental and organismal factors that influence Hg bioconcentration.

4.1 Hg intake risk in C. rhizophorae at CGSM and BhC

Variability in contamination sources and Hg concentrations in CGSM and BhC stands out as a key factor influencing contamination risk. In particular, BhC shows values close to the permissible limit for Hg in bivalves for human consumption of 0.5 µg/g Hg _d.w. [33], raising concerns about the health of the ecosystem. This situation is similar to what has been reported on Cayo el Pigeon Island in Nicaragua and Santa Marta in Colombia by Aguirre-Rubí et al. [9] (Fig. 4). However, both ecosystems are far from what has been reported for this species in coastal areas of the Dominican Republic, where Sbriz et al. [66] recorded one of the highest Hg contents in the mangrove oyster (7.02 µg/g Hg _d.w.).

When comparing Hg concentrations in mangrove oysters with other bivalve species globally over the last decade, CGSM and BhC stand out as ecosystems that maintain low to no risk of Hg contamination. This contrasts with findings in coastal areas of China [67–69], Italy [70] and Montenegro [71], with a lower risk of Hg contamination in the world and serves as a reference for the potential risk of contamination in CGSM and BhC (Fig. 4).

The relevance of this study is intensified when considering the current situation of Hg contamination in Colombia. In the bay of Cartagena with C. rhizophorae its has reported the highest risk of Hg contamination in the last decade in the world [9] (Fig. 4, Supplementary Table S6 and S7). In a historical context, the Bay had a direct discharge of Hg from the Alcalis chlorine plant [40, 72]. Similar cases prior to 2010 have been reported in Tagelus dombeii (San Vicente Bay, Chile) [44], in Archivesica gigas (Gulf of California, United States) [73] and in Mytilus galloprovincialis (Adriatic Sea, Croatia) [74] with concentrations above 0.5 µg/g Hg _d.w. These findings underscore the need for continuous monitoring at CGSM and BhC to identify specific sources of contamination and generate appropriate preventive measures.

Cispatá Bay (BhC) had the highest concentrations of Hg in sediments, seston and oysters compared to Ciénaga Grande de Santa Marta (CGSM) in both climatic seasons. However, the oyster exhibited the highest values of bioconcentration factor (BCF) with the seston of the CGSM, with a higher risk of Hg contamination. Temperature in the water column and organic matter in sediments influenced Hg concentrations in seston and sediments but have a limited and insignificant impact with the other environmental variables on Hg bioconcentration by size in the oyster. Adult sizes accumulated more Hg in CGSM, while juvenile sizes accumulated more Hg in BhC. This highlights the importance of considering the size of the bivalve when assessing Hg contamination, taking into account the specific environmental conditions of each ecosystem. The CGSM exhibited contamination without risk for human consumption, similar to that reported in other areas in the Colombian Caribbean, while BhC presented near-low contamination due to its higher Hg content.

Founding sources

This study was done within the research program "Redes tróficas marinas del Caribe colombiano en la era del plástico y los contaminantes tóxicos” (code MINCIENCIAS 71475)”, funded by MINCIENCIAS and Universidad Jorge Tadeo Lozano, in partnership with Universidad Nacional de Colombia, sede Caribe. The funding for Hg analysis in oysters was provided of Colombia Biodiversa (I-2023) and Banco de la República with the Project 5.131 from the Foundation for the Promotion of Research and Technology (Fundación para la Promoción de la Investigación y la Tecnología). Translation funding was provided by internal grants from the Universidad Jorge Tadeo Lozano.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

CRediT authorship contribution statement

Anubis Vélez-Mendoza: Funding Acquisition, Conceptualization, Methodology, Data Curation, Formal Analysis, Visualitation, Writing & Original draft, Writing, Review & Editing. Jeimmy Paola Rico Mora: Funding Acquisition, Data Curation, Visualitation, Supervision, Writing, Review & Editing. Néstor Hernando Campos-Campos: Funding Acquisition, Data Curation, Visualitation, Supervision, Writing, Review & Editing. Margui Lorena Almario-García: Supervision, Writing, Review & Editing. Adolfo Sanjuan-Muñoz: Project Administration & Funding Acquisition, Supervision, Writing, Review & Editing.

Acknowledgement

We would like to especially thank the members of the team Diana Bustos-Montes, Paulo Tigreros-Benavides, Diana Rubio-Lancheros, María Camila Castellanos Jimenez, Ana M. Hernández-Chamorro, Nicólas Santos-Vásquez, Andrés Navarro-Martínez, Nelson Rafael Camargo Tibamoso, Laura Daniela García Meléndez and the students of the Marine Ecology and Biodiversity (ECOBIOMAR-UTADEO) research incubator, for their support in taking samples and laboratory analysis. Special thanks to CECIMAR of the Caribbean headquarters of the National University of Colombia for providing their spaces for sample processing. To INVEMAR for the support provided for the treatment of samples.

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Changes in mercury content in oysters in relation to sediment and seston content in the Colombian Caribbean lagoons

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Abstract

Figures

1. Introduction

2. Methods

2.1 Study area

2.2 Field phase

2.3 Laboratory phase

2.4 Cabinet phase

3 Results

3.1 Environmental conditions in both coastal lagoons

3.2 Concentration of Hg in sediments, seston and Crassostrea rhizophorae

3.2.1 Importance of seston in the bioconcentration of Hg

3.3 Relationship between environmental variables and Hg bioconcentration in oysters

3.4 Hg contamination status of bivalves in a global context during the last decade

4 Discussion

4.1 Hg intake risk in C. rhizophorae at CGSM and BhC

5 Conclusions

Declarations

Founding sources

Competing Interests

CRediT authorship contribution statement

Acknowledgement

References

Additional Declarations

Supplementary Files

Status:

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