Mercury and Selenium Trophic Transfer in the Mexican California Current Ecosystem Using a Top Predator as a Model

Abstract

Research on the trophic transfer of trace elements in food chains, particularly toxic elements like mercury (Hg) and essential elements like selenium (Se), is crucial for understanding their impact on human health. In this work, we assessed the transfer of Hg and Se in the blue shark (Prionace glauca), a top predator with economic importance. Muscle samples from sharks, as well as their main prey (squid, red shrimp, sardine, and mackerel), were analyzed for Hg and Se concentrations. The Hg levels of sharks were below the recommended legal limit for seafood consumption in Mexico (1 µg·g⁻¹ ww), while Se levels were significantly lower than previously reported for the species. Biomagnification was evaluated in this species by calculating biomagnification factors (BMF) for Hg and Se based on predator-prey element concentrations. Hg showed a BMF of 2.8, indicating biomagnification, while Se had a BMF of 0.2, suggesting biodilution. Trophic transfer factor models supported these findings, showing a positive correlation of Hg concentration with trophic level and a negative correlation with Se. However, while a hazard quotient under one does not pose a risk for consumption, a Se:Hg molar ratio under one estimated in the muscle tissue indicates that Hg levels along this food web should be approached with caution.

1. Introduction

The trophic transfer of essential and potentially toxic trace elements in marine food webs is an important environmental research area [1]. In particular, heavy metals such as mercury (Hg) are of great concern, since they may be transferred from the abiotic aquatic environment (water, sediments) to living organisms, with accumulation in diverse components of food chains and with a potentially toxic effect. While Hg is naturally emitted mainly from volcanoes, geothermal sources, and soils, it is continually recycled and re-emitted to the atmosphere and deposited on the sea surface [2]. However, over the past century, human activities have significantly increased the amount of Hg in the marine environment [3]. Methylmercury (MeHg) is the most toxic form of this element due to its capacity for absorption through cell membranes, producing several physiological changes, like oxidative stress and neurotoxicity, among others [4]. Understanding the global sources, speciation, and transport of Hg is crucial for comprehending its ultimate contribution to MeHg production in aquatic systems. This knowledge is essential for understanding the accumulation and transfer of MeHg among wildlife [5].

In aquatic systems, pH, dissolved organic matter, and oxygen play a significant role in the Hg cycle [6]. Hg methylation rates depend to some extent on the availability of electron acceptors (O, N, S, Fe) because they influence the metabolism of sulfate-reducing bacteria [7]. Thus, acidic waters and reducing conditions, associated with low dissolved oxygen (O₂), favor Hg methylation. Some processes connected with global climate change, such as the expansion of the minimum oxygen zones (MOZs) in the tropics, can modify and enhance the presence and abundance of Hg methylation microbiota [8], ultimately increasing MeHg availability. MeHg is incorporated into the marine food chain by producers (phytoplankton) and moves efficiently between inshore and offshore food webs through a ‘trophic transfer’ to finally sink into the higher trophic levels [9].

In contrast, selenium (Se) is an essential element for all organisms and is found worldwide in organic-rich sedimentary rocks. Most of its forms can be quickly transformed and incorporated into food webs [10]. Indeed, organic Se is the most bioavailable chemical form; thus, the primary route of exposure to Se in marine consumers is through the diet rather than the water [11]. However, this element is also supplied to aquatic systems as a by-product of several human activities, such as coal-fired energy plants, agriculture, crude oil refining, and coal mining, leading to elevated levels of Se. These elevated levels can result in the degradation of several ecosystems and have been linked to reproductive impairment in important fish species [12]. Se is also known to prevent Hg toxicity in the body through an interaction mechanism that occurs in the organism when both elements are present in the proper amount [13]. Hg has a strong affinity for Se, leading to the sequestration of Se by MeHg in the body. This prevents Se from carrying out its vital functions. Consequently, MeHg is demethylated to form inactive HgSe complexes, resulting in symptoms similar to Se deficiency in cases of Hg poisoning [14].

Seafood is one of the main routes of exposure to both elements (Hg, Se) in humans [15]. However, particularly long-lived top predatory fishes such as sharks, through processes like bioaccumulation and biomagnification, tend to have high concentrations of MeHg in their tissues, particularly in muscle (edible part), which may have serious implications for human health [16]. This is due to certain ecological features of this group, such as late maturity, large migratory movements, and opportunistic diet, which can lead to extended exposure to the contaminant [17]. Principally, feeding conditions, such as prey type and size, are potential indicators of Hg levels in top predators. Piscivorous fishes like the blue shark (Prionace glauca) have been shown to accumulate higher Hg concentrations in their tissues compared to other species that feed on lower-trophic-level prey [9]. In that sense, assessing the trophic level (TL) of commercial species is currently recognized as a powerful tool to assess disturbance in marine systems and is commonly used for fishery management [18]. However, variability in prey availability and ontogenetic changes may hinder the TL estimation within a complex food web, especially using Stomach Content Analyses (SCA). More recent techniques like Stable Isotopes Analysis (SIA) have provided a clearer approach to sharks’ feeding habits, suggesting that ontogenetic changes in habitat use and prey consumption between maturity stages may affect the TL [19]. Ultimately, the trophic status of the commercial species feeding along highly exploited marine food webs like the California Current Marine Large Ecosystem (CCLME) has a crucial role in determining Hg biomagnification, especially in medium-to high-trophic-level fishes consumed by humans.

Shark meat has raised concerns lately due to the growing demand worldwide. While, historically, markets like China and Japan have been the main fish consumers, nowadays shark muscle is considered a low-value protein source and sold in the form of fillets in several developing countries [20,21,22]. The blue shark is one of the most abundant global apex predators; therefore, it is one of the main species of shark caught by longline fisheries, both as a target and as a bycatch product [23]. Additionally, blue sharks are known to travel long distances in search of food and suitable breeding grounds. Their migratory behavior is influenced by factors like water temperature, prey availability, and reproductive cycles, enabling them to travel thousands of miles and making them one of the most widely distributed shark species. [24]. Organisms caught in the Mexican Pacific are supposed to move and feed along the CCLME [25]. While this species is not commonly traded in the U.S. due to the low quality of its meat [26], in Mexico, it is widely captured for human consumption locally and for exportation [27], with catches making up a significant portion of fishery landings (about 80%). Most of the catch (90%) is consumed domestically due to its availability and low cost [27]. However, due to its characteristics, it is known that it can accumulate high levels of toxic elements like Hg from different sources and potentially reach unacceptable levels for consumption [28]. In this study, we aimed to quantify the dietary contribution of the accumulation of Hg and Se in the muscle of blue sharks, considering the high potential of biomagnification of Hg and the possible biodilution of Se due to its antagonistic behavior, with the final purpose to assess the potential human health risks associated with consuming this shark meat.

2. Materials and Methods

2.1. Collection of Specimens

Twenty-two blue sharks were collected from fish surveys undertaken by the Mexican Institute for Research in Sustainable Fisheries and Aquaculture (IMIPAS) between 2019 and 2021 in the northwest Mexican Pacific (Figure 1). The sharks were captured by longline fisheries during the night. Specimens that did not survive the tagging process were retained for further study. Each shark’s weight, length, and sex were recorded. For trophic analysis purposes, we only kept those organisms cataloged as adults (total length < 180 cm) [29] to reduce ontogeny variation in Trophic Level (TL) estimation. Muscle tissue samples (20 g) from each of the 12 sharks selected were collected and stored at −4 °C. Additionally, samples of the blue shark’s main prey items in the study area were collected [30,31,32], including the red crab (Pleuroncodes planipes), the squid (Gonatus spp.), the anchovy (Engraulis mordax), and the mackerel (Scomber japonicus) (Figure 1). Five prey items of each species were collected with a trawl net.

2.2. Sampling Procedure

Blue shark muscle and complete prey organisms were freeze-dried (140 × 10⁻³ mBar; −49 °C) for 72 h using Labconco equipment (Marshall Scientific, Hampton NH, USA). Dry tissues were manually ground with an agate mortar. Homogenized powdered samples were digested with concentrated nitric acid (69%) (Trace Metal Grade) in stoppered vials for 3 h at 120 °C [33]. Concentrations of Se were measured by graphite furnace-atomic absorption spectrophotometry (GF-AAS) with Zeeman correction background using a model Analyst 800 instrument purchased from Perkin-Elmer (Waltham, MA, USA). Hg concentration was measured by cold vapor-atomic absorption spectrophotometry (CV-AAS) using a model 410 A instrument purchased from Buck Scientific (East Norwalk, CT, USA). The quality control of elemental analyses included blanks, duplicates, ultra-pure water (milli-Q, 18.2 MΩ cm), trace metal grade acids, and reference materials. The reference materials used were obtained from the National Research Council of Canada (Ottawa, ON, Canada), with dogfish muscle (DORM-3) for shark and fish samples, and lobster hepatopancreas (TORT-2) for squids and red crabs. The recovery percentage was 105 ± 7.4% (Se) and 101 ± 0.1% (Hg) in DORM-3 and 103 ± 0.06% (Se) and 100 ± 0.32% (Hg) in TORT-2. The limits of detection (three times the standard deviation of a blank) were 2.1 µg/L for Se and 0.11 µg/L for Hg. Conversions of concentration units from dry weight to wet weight were calculated considering the humidity percentage in muscle (for shark and fish tissue, 75%) and invertebrates (squids and crabs, 50%) [34]. Concentration units of Se and Hg are given as μg·g⁻¹ wet weight for comparison with the Hg consumption standards for seafood according to Mexican laws [35].

2.3. Data Analysis

The biomagnification factor (BMF) was calculated using Equation (1) [36]:

BMF = [element]_predator/[element]_prey.

(1)

BMF calculations were made based on the assumption that the concentrations of elements (Hg and Se) reached a steady state in the sampled tissues. BMF > 1 indicates biomagnification of the element [37].

The trophic transfer factor (TTF), assessing the biomagnification or biodilution of an element through the food chain, was analyzed by Equations (2) and (3) [38]:

Log10[element concentration] = a + b*TL

(2)

TMF = 10^b

(3)

where a is the intercept of the regression between log10[element concentration] and TL (trophic level), depending on the element background concentrations [39], and b is the slope of the regression line [40] representing the biomagnification or biodilution capacity of an element [41]. Finally, the antilog of slope b, which is the relationship between log10 transformed concentrations (µg·g⁻¹ ww) and TL, is used to calculate the TTF. Predator and prey TL were taken from bibliographic references [18]. Biomagnification causes a TTF > 1. So, a TTF above 1 implies a disequilibrium between organisms and the media (water) that increases with the TL. Slope b was weighted by linear regression for both elements.

Shark biological parameters and element concentrations in every species sampled were examined for normal distribution and homogeneity of variances using the Shapiro–Wilks test. Due to not meeting the normality assumption, a non-parametric Spearman’s test was performed to determine correlations between Se and Hg concentrations and shark length. The level of significance was designated at p < 0.05. Additionally, Se: Hg molar ratios were calculated by dividing the concentration in mg per kg by the molecular weight. For each specimen, we divided the Se concentration (mg·kg⁻¹) by 78.96 and the Hg concentration (mg·kg⁻¹) by 200.59, to finally assess the Se: Hg molar ratio means for each species. While, in prey, the Se: Hg molar ratio was estimated for the entire organism, it is worth mentioning that in sharks it was only calculated in muscle tissue. R Studio (version 2022.12.0) was used to display all the correlations, linear models, and graphs [42].

We calculated the hazard quotient (HQ) of Hg concentrations in the muscular tissues of the blue shark. The values of HQ were calculated using Equation (4) [43]:

HQ = E/RfD

(4)

where E is the exposure level or intake of total Hg and RfD is the reference dose for total Hg (0.5 μg/kg body weight/day) [44]. The exposure level (E) is calculated from Equation (5):

E = C × I/W

(5)

where C is the concentration of total Hg in the edible part of the fish in wet weight; I is the intake rate of shark meat expressed in grams per day per capita, determined as 17.38 g·day⁻¹ for the local population according to the Mexican Ministry of Environment and Natural Resources (SEMARNAT)[45]; W is the weight of an average adult in Mexico (70 Kg).

3. Results

3.1. Mercury and Selenium Assessment

Firstly, when comparing Hg levels in the blue shark prey, we found that they were consistently higher than previously reported values in the study area for three species (P. planipes, S. japonicus, and E. mordax). Previous studies in the area [22] reported Hg concentration values below 0.05 µg·g⁻¹ ww, while our results showed values above 0.2 µg·g⁻¹ ww in all reported prey (

Table 1. Mean and standard deviation concentrations of Hg and Se (µg·g⁻¹ ww) for the blue shark and its prey, with the BMF for each element and the Se:Hg molar ratio.

Specie	TL	Hg	BMF_Hg	Se	BMF_Se	Se:Hg
P. planipes	2.4	0.223 ± 0.003	2.82	0.353 ± 0.083	0.23	4.011 ± 0.903
Gonatus sp.	2.6	0.204 ± 0.007	3.07	0.359 ± 0.172	0.29	5.345 ± 2.193
S. japonicus	3.9	0.232 ± 0.006	2.70	0.319 ± 0.119	0.25	2.252 ± 0.436
E. mordax	3.9	0.239 ± 0.004	2.63	0.208 ± 0.056	0.38	3.500 ± 0.189
P. glauca	4.5	0.802 ± 0.360		0.086 ± 0.041		0.411 ± 0.292

). The Hg average concentration in the muscle of the shark P. glauca was below the recommended limit of 1 μg·g⁻¹ ww set by national and international standards [35,36] (Table 1). In contrast, Se levels were lower than those previously reported for some prey items [22], where authors reported values of 0.83 µg·g⁻¹ ww for S. japonicus and 0.90 µg·g⁻¹ ww for P. planipes, while the mean Se values in this study were below 0.35 µg·g⁻¹ ww (Table 1).

Molar ratios above one in all of the prey suggested there may be sufficient Se to potentially counteract Hg toxicity. In many fish and marine mammals, a ratio ≥1 is associated with protective effects through the demethylation of MeHg and the formation of inert HgSe complexes. While this interaction is well reported for bony fish, in invertebrate species, a gap remains [46]. In the shark, the Se: Hg molar ratio obtained for the muscle with a value under one indicates insufficient Se to detoxify the Hg burden fully. Thus, this imbalance suggests that not all Hg can be complexed, possibly leading to an elevated potential toxicological risk of consuming this part of the shark.

3.2. Trophic Transfer Models

Based on the significant linear relation between Hg and Se concentration with TL, we calculated the trophic transfer factor (TTF) for each element. This value reflects the ratio of an element concentration in predatory animals to concentration in prey organisms at a steady state. Results show that this ratio exceeded 1 for Hg (Figure 2a), suggesting that this toxic metal biomagnifies at every trophic step. The TTF value of <1 for Se (Figure 2b) suggests that this metalloid is not expected to be biomagnified along marine food chains.

3.3. Risk Assessment

The HQ estimated for each shark category was below 1, indicating no risk of consumption (

Table 2. HQ values in the muscle of blue sharks according to Hg concentrations and ingestion rate.

Category	N	HQ
Males	16	0.34
Females	6	0.24
Adults	12	0.41
Juveniles	10	0.10
All	22	0.16

). However, sensitive population sectors such as pregnant or breastfeeding women and children should always be mindful of the consumption amount for this species [47].

4. Discussion

4.1. Hg and Se Interaction Assessment in Shark Meat

Because of its widespread presence, toxicity, and ability to accumulate in organisms, Hg has been frequently used to study biomagnification in marine food webs [38]. Sharks, with their reproductive strategy (K), high trophic level, and economic significance, are commonly used as models to study the biomagnification process of this contaminant [48]. The dietary route plays a main role in determining toxic element burdens in marine organisms. Seafood is considered the major source of Hg intake in the human diet, but it also provides essential micronutrients like Se, which serve as enzymatic cofactors and offer other health benefits [49]. The final concentration of these elements in edible parts of exploited shark species will be the result of different processes known as bioaccumulation (increase of pollutant concentration with the size or age of the fish) and biomagnification (increase of pollutant concentration with the trophic level). It has been repeatedly reported that Hg concentration increases along the food chain, explaining the levels well above reference values in organisms living in the open sea [50]. This is mainly because long-lived, slow-growing, and highly migratory oceanic fishes such as sharks tend to accumulate high concentrations of Hg, especially in the muscle, which can often exceed recommended limits for human consumption [51].

After confirming the bioaccumulation of Hg in the muscle of the blue sharks captured in the southern part of the California Current Ecosystem, at the Gulf of California entrance, where adults showed a bigger concentration of Hg in muscle [52], we aim to assess the contribution of this element through the diet. Food serves as a vehicle for both toxic and beneficial elements, so apex predators, including humans, are exposed to high levels of these elements, potentially leading to organic dysfunctions [40]. While Se is essential within certain limits, excessive amounts can be harmful [41]. Most research on this topic agrees that Hg and Se should be assessed together due to their antagonistic relationship [18]. Se proteins are involved in Hg neutralization once they enter the body, to prevent its toxicity; thus, when an organism has high levels of Hg, it is likely to have low levels of available Se [42]. Therefore, it is crucial to monitor the concentration of both elements in marine products intended for human consumption. The final result of this interaction will depend on individual characteristics such as sex and age (size) but also on the specific function of the organ where the elements tend to be stored [53,54]. In bony fishes, while the liver is supposed to be the main organ sink for Se, Hg tends to accumulate in muscle [55]. Again, we could probe this statement with regard to our previous work with this species, where Se concentration was higher at hepatic tissue sampled in all sexes and ages [52]. While the blue shark liver can be consumed normally as an oil or a medicine supplement for high vitamin A content, in this work, we focus on the muscle as the most commonly consumed part and as the target organ for Hg accumulation, reaching human health risk implications [56].

Accordingly, our results show that the diet is a relevant source of Hg and Se in this top predator. While the Hg magnifies with the TL, Se tends to dissolve. We can attribute this phenomenon mainly to the Hg detoxification process, where most of the Se available in the muscle could be involved in the demethylation of MeHg to give place to inorganic Hg-Se compounds [57]. This compound (Hg-Se) reacts with selenoproteins, altering vital functions involved in oxidative stress [58]. However, the final protective function of Se to neutralize Hg toxicity in the organism will depend on tissue-specific distribution and physiological availability of this element. In that sense, analyzing the molar ratio between both elements only in one organ (i.e., muscle) can be tricky and lead to a misinterpretation or an overestimation of the antagonistic process. A molar ratio of less than one in the muscle of the blue shark indicates that the available Se can be insufficient to fully counteract Hg, potentially elevating toxicological risk.

4.2. Comparison with Similar Studies

Other authors who aimed to test the same biomagnification hypothesis in the blue shark captured along the northeastern Atlantic Ocean found that BMF remained always <1, suggesting that the biomagnification of Hg does not occur in this species [59]. In contrast, in the Mexican Pacific, previous studies reported that prey contains less Hg than predators but did not estimate the BMF, while also remarking that the main source of this toxic metal throughout the diet of the shark could be the pelagic red crab (P. planipes), due to the large amount that a predator needs to consume to compensate for the lack of energy that this small prey can offer [30]. The pelagic red crab is a common prey of several predators that move and feed along the CCLME, like the Yellowfin Tuna (Thunnus albacares); thus, this is a key species in the trophic web of the south of the California Current [58]. Due to the commercial importance of Tuna, Hg biomagnification through this prey was also addressed and confirmed by these authors, with a BMF > 1. Even with these study limitations, like a low number of organisms sampled, we were able to observe that the Hg values in pelagic red crabs obtained in this work were almost four times higher than previously reported [30,60]. It is worth mentioning that this species is also commercial, being caught and used for preparing animal feed for aquaculture, which ends up being consumed by humans. Regarding the Se:Hg molar ratio, studies in the same zone [30,60] also report values above one, indicating a molar excess of Se over Hg in prey items. While the blue shark diet components contribute to both elements, the final Se availability to avoid Hg toxicity in this predator is more complex to demonstrate.

4.3. Human Health Risk Assessment and Implications for the Fisheries Management

The shark fishery in the Mexican Pacific is a relevant food resource not only locally but globally since Mexico is one of the main producers and exporters of shark species [61,62]. IMIPAS, through various monitoring programs (such as the shark observer programs), and specifically the tagging of blue sharks on board oceanographic cruises, has revealed that catches of this species for human consumption have been increasing due to the growing demand for these products as a result of their low cost [63]. The results of this program after 15 years show that the blue shark population in the Mexican Northwest Pacific stays stable and is not overfished [64]. Therefore, it is important to consider the potential risks to human health that high levels of Hg accumulated in the edible parts of this shark can cause. One way to address this issue is the non-carcinogenic risk assessment method using the HQ established by the United States Environmental Protection Agency [65]. This approach assumes that there is a level of exposure to the toxic metal (the reference dose, RD) below which even the most sensitive sectors of the population are unlikely to experience adverse health effects [66].

Based on the results of our hazard quotient estimation, we could state that there is no risk for consumers of blue shark meat, since all values were less than one. However, taking into account that bioaccumulation and biomagnification of Hg occur in this species, it would be most prudent to recommend moderate consumption. In previous works with the same organisms sampled, we stipulated a daily consumption dose of this species that can be consumed without presenting risks of Hg poisoning; thus, under this calculation, an intake between 11.9 and 10.9 g per day can be recommended for an adult man or woman in Mexico [52]. These results are similar to those proposed for the Mediterranean, where the maximum consumption rate of blue sharks is 10 g per day [67]. In this sense, considering that shark meat is a great source of essential elements, but also the main Hg route of entry to humans, certain precautionary measures must be taken, especially when the specimens consumed are adults and the consumers belong to the more sensitive population sector (pregnant and breastfeeding woman and child) [68].

5. Conclusions

This study assessed the contribution of Hg and Se through diet in the top predator, the blue shark, feeding along the CCLME. The presence of heavy metal contamination in fish has significant implications for their management and conservation efforts, as it can impact their health, reproduction, and behavior, while also posing risks to human health [69]. Heavy metals found in fish tissues can lead to reduced fecundity, fertilization, and hatching rates as well as cause damage to vital organs [57]. These effects can ultimately decrease the biomass and recruitment of exploited fish populations, affecting their catch rates [70]. To address these challenges, it is crucial to implement effective management and conservation strategies, including pollution control, habitat protection, and regular monitoring of water and fish quality. Considering the results suggest a potential increase of Hg and a decrease of Se in the edible part of this species, we encourage its consumption with caution.