Introduction

Seafood consumption by humans contributes significantly to the intake of eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids, vitamin D, and other micronutrients that are essential to keep a healthy life1,2. Despite knowing the origin of these micronutrients, consumers usually show no preference for certain seafood products, certification, or where the seafood was captured3, and some of these organisms could contain toxic substances above maximum residue levels (MRLs) that might risk people's health4. Food safety is essential to prevent these health risks regarding toxic pollutants in seafood caused by anthropogenic activities5. Among the most toxic anthropogenic pollutants are organochlorine pesticides (OCPs) and trace metals that are environmentally persistent, become bioaccumulated and biomagnified due to their low water solubility and slow chemical decomposition6. The OCPs and trace metal residues are transported to the marine ecosystems by environmental factors such as effluents, wind, and rain, becoming bioavailable from marine sediments or water columns for the marine organisms7,8.

The persistence of trace metals and OCPs in the environment allows them to be found as residues in areas far away from the original sites of their application9. Trace metals, such as Pb and Cd, are elements that interfere in biochemical metabolic processes10. Other trace metals such as Fe, Zn, and Cu, when they are above MRLs, might cause health problems inhibiting nutrient absorption11.

The persistence of these toxic pollutants makes their study crucial to determine their health impact as a human health concern12.

The present study was performed in the Navachiste complex coastal lagoon (NAV), which is constantly impacted by the inputs of the wastewaters of the adjacent agricultural Guasave Valley, low-density tourism, urban and aquaculture activities. The NAV lagoon complex encompasses three coastal lagoons that geologically include coastal plains (55%), with dunes and salt flats (4.3%), deltaic depositional facies (21%), marshes and salt flats (17%), beach and sand bars (2%), and low mountains of steep slopes with dunes (0.5%)13 (Fig. 1). The field data was converted to grid data, and spatial analysis was performed with the ARCGIS DESKTOP® Ver. 10.8.2 with the authorization number ESU 125678848 using the georeferenced shapefiles from the ARCGIS®14 and CONABIO, Mexico15 databases (Supplementary table 1). Previous studies in the area have reported the presence of the OCPs and trace metals in edible tissues of inhabiting seafood species16,17,18,19,20. Among the polluted seafood species reported in the NAV are those of the Tetraodontidae family, like the pufferfish Sphoeroides spp.21, a euryhaline fish that inhabits coastal lagoons and estuaries22, and its feeding habits include zoo benthivores and omnivores, including bivalves, gastropods, and macrophytes23,24,25. The commercial value of the pufferfish Sphoeroides spp. is sizable and its catch reached, in Sinaloa in 2020, more than 708 tons with a value of more than 3 million USD, and its capture has been increasing in the last decade26,27. However, due to the constant pollution with OCPs and trace metal residues of the NAV, the risk of being subjected to carcinogenic or non-carcinogenic effects by the consumption of Sphoeroides spp. is evident. In this sense, the aim of the present study was to evaluate the carcinogenic and non-carcinogenic risk of the Sphoeroides spp. from the NAV.

Figure 1
figure 1

Navachiste coastal lagoon complex location and sampling collection sites (black stars) of fillet of Sphoeroides spp. for analysis of their trace metal content. Map was constructed using the ARCGIS DESKTOP® Ver. 10.8.2 with the authorization number ESU 125678848 using the georeferenced shapefiles the ARCGIS®14 and CONABIO, Mexico15 databases, field data converted to grid data.

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Methods

Eighty-six fillet of the pufferfish Sphoeroides spp. were obtained from the local fishers with a fishery permit in the NAV, located in the southern part of the Gulf of California in Mexico between 25.4° and 25.7° N and 108.85°–108.55° W28,29. None of the specimens were taken alive to perform the following laboratory experiments that were performed in accordance to national or international agreements guidelines and regulations.

Pufferfishes were obtained once every quarter of a year between summer (July 2016) and autumn (October 2017). Sampling points were selected among frequent fishing areas identified by local fishers. Frozen pufferfishes were dissected to remove the fillet that was divided into two parts, one part was kept in aluminum foil for posterior OCP content analysis, and the other part was kept in Ziploc® bags for trace metal content analysis. All samples were kept frozen in an ice acid-based cooler and transported for storage in a freezer in the Pollution laboratory located in the CIIDIR-SINALOA, Mexico. During each sampling period, pH, temperature (°C), salinity (‰), and dissolved oxygen (DO) were registered with a multiparameter HANNA® HI-9828 (HANNA Instruments, Woonsocket, RI, USA).

Trace metal analysis

Acid digestion with nitric acid according to Méndez et al.30 was the procedure used for the trace metals extraction from muscle, and determined by atomic absorption spectroscopy. Each collected Sphoeroides spp. sample was dehydrated until constant weight. Five grams of dehydrated sample was digested in Erlenmeyer flasks with a concentrated HNO3 and HCL acids (1:5) mixture. Samples in the digestion procedure were boiled on a heating plate until dissolved. Cooled samples were mixed in 24 mL of deionized water and 1 mL of HCl, and taken to 50 mL with deionized water, and stored at room temperature for later analysis. The trace metals were determined by atomic absorption spectrophotometry (AVANTA GBC ®, US) with an air/acetylene flame burner and hollow cathode lamps. Trace metal standards of 0.125, 0.25, 0.5, 1, 2, and 4 ppm were prepared to verify the accuracy of the instrument. The quality control of the procedure was achieved using PACS and MESS reference materials (Supplementary table 2) in blank samples which were analyzed after each 10 of digested samples.

Organochlorine pesticides analysis

The extraction, purification, analysis and quantification of OCP in the fillet samples were performed following the modified EPA-8081b31. Was macerated 10 g of sample with 5 g of Na2SO4 (Sigma Aldrich, St. Louis, MO, US) and 30 mL of hexane (chromatographic grade). The recovered hexane was purified with a clean-up column (fiberglass wool, alumina, florisil, silica gel, and anhydrous sodium sulfate, at a proportion of 2:1:1:1:3, respectively). The extracts were concentrated and completely dried in a hood, and then dissolved in 2 mL of isooctane.

The gas chromatograph (Perkin Elmer® XL, Auto System®, Perkin Elmer, Inc., Waltham, MA, US) is coupled to a 63Ni-ECD detector, TotalChrom Navigator® software, and DB-5 column (Agilent®). A six-point calibration curve was constructed (0.001–0.05 µL mL−1). The chromatography conditions were: oven heating ramp to 120 °C (for 1 min) until 240 °C increasing at a rate of 4 °C min−1; EDC at 300 °C; injector at 260 °C; 2 µL of sample injection; split-split less on; attenuation of 16; nitrogen as a carrier gas at 8.7 psi at 30 mL min−1. Pesticide mix standards (EPA 8081®) and pesticide subrogate mix (SUPELCO® Cat. CRM46845 and CRM48460, respectively), and linearity, detection limit, and recovery range (Supplementary table 3) were calculated to ensure the accuracy of the results.

A database was constructed with Microsoft Excel®, and data were statistically analyzed with Minitab17® software. A Kolmogorov Smirnoff normality test, ANOVA, and posthoc Tukey test were performed to determine significant differences.

Human health risk assessment

Estimated daily intakes (EDI) for trace metals (TM) and OCP in the Sphoeroides spp. fillet from the NAV were calculated8,32,33 (Eqs. 1, 2):

$${EDI}_{TM}= \frac{{TM}_{C }\times {VIR}_{d}\times ED\times EF}{BW \times AT}$$
(1)
$${EDI}_{OCP}= \frac{{VIR}_{d}\times {OCP}_{C}}{BW}$$
(2)

where, TMC or OCPC = average TM (μg g−1) or OCP (mg kg−1) concentration in fish tissue (dry weight); VIRd = average daily fish consumed in Mexico (32.88 g day−1), ED = exposure duration (26 years), EF = exposure frequency (365 days year−1), BW = Mexican adult average human weight (74.3 kg), and AT = average time (365 days year−1 per 26 years).

Non-carcinogenic risk

For TM the target hazard quotient (THQ) (Eq. 3) and the hazard index (HI) (Eq. 4)32,34,35 were used to calculate the non-carcinogenic risk.

$${THQ}_{noncancer}= \left(\frac{EF\times ED \times {VIR}_{d} \times {TM}_{C}}{RfD+ BW+ {AT}_{noncancer}}\right) \times {10}^{-3}$$
(3)
$$HI= \sum_{n}^{i}{THQ}_{n}$$
(4)

If THQ or HQ is below 1 represents non-carcinogenic risk; if it is above 1 non-carcinogenic risk can occur.

For OCP, the non-carcinogenic risk was assessed by the hazard quotient (HQ) (Eq. 5) and the total hazard quotient (THQ)36,37 (Eq. 6):

$$\text{HQ }= \text{ } \frac{EDI}{{RfD}_{OCPx}}\times 100$$
(5)
$$THQ= \sum_{i=1}^{n}{HQ}_{i}$$
(6)

where, RfDOCPx = reference doses for “x” OCP.

HQ or THQ values lower than 100 represent a non-carcinogenic risk, but HQ or THQ above 100 means that non-carcinogenic symptoms can occur.

Carcinogenic risk

For the TM the risk of cancer for each TM was calculated by the incremental lifetime cancer risk (ILCR)38 (Eq. 7):

$$ILCR={EDI}_{TMx}\times {CSf}_{TMx}$$
(7)

CSf = Cancer slope factor of carcinogenic TM estimated39.

For OCP the carcinogenic risk (CRlim) was calculated40 (Eq. 8):

$${\text{CR}}_{{{\text{lim}}}} { =}\frac{{{{{\text ARL}~ \times ~{\text BW}}}}}{{\mathop \sum \nolimits_{{m = 1}}^{x} C_{m} ~ \times ~CSF_{{OCPx}} }}$$
(8)

where CRlim is the maximum allowable consumption rate for an aquatic product (kg day−1); ARL is the maximum acceptable individual lifetime risk level, which is dimensionless and a value of 10–5 was used in this study41,42; CSFOCPx is the cancer slope factor of OCPx for a carcinogenic risk (mg kg−1 day−1).

Results

Morphometric data and TM and OCP concentrations in fish edible fillet

In this study, 20 OCP and seven trace metals (TM) were detected in the Sphoeroides spp. fillets from NAV. Some TM concentrations were detected above MRLs and showed a carcinogenic and non-carcinogenic risk for human consumption. A not normal distribution was found with the Kolmorov-Smirnoff (KW) test (α = 0.05), concentration of trace metals (KS = 0.117, p < 0.01), size (KS = 0.141, p = 0.010), weight (KS = 0.211, p < 0.010), and OCPs concentration (KS = 0.43, p < 0.01) (Table 1). The average length and weight of specimens (24.028 cm and 334.28 g, respectively), were similar to specimens of the same genus from shallow brackish water areas43. A correlation was found between weight (Pearson, α = 0.05, p = 0.001) and height (Pearson, α = 0.05 p = 0.0005) and with the concentration of trace metals (Pearson, α = 0.05 p = 0.179).

Table 1 Frequency percentage, mean concentration, standard deviation (± SD) of trace metals and OCPs in the fillet of Sphoeroides spp. from NAV, Mexico.
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TM concentration in Sphoeroides spp.

The TM concentrations in Sphoeroides spp. presented the following trend: Zn > Fe > Pb > Ni > Mn > Cu > Cd, from which, Cd, Cu, Fe, Mn, Pb, and Zn were above MRLs established by some countries´ Environmental Protection Agencies44,43,44,45,46,47,48,51, or were higher than in other marine fish52,51,52,55. Cd was detected in just one specimen.

In this study, the average concentrations of Cd (1.45 mg kg−1 dw) was above the MRLs (3 × 10–5–2 × 10–3 mg kg−1 dw). Cu average concentration (1.45 mg kg−1 dry wt) showed values above MRL (0.03–0.12 mg kg−1 dw). Zn was detected in 100% of samples, with an average concentration (189.55 mg kg−1 dw) higher than the recommended MRLs (0.03–0.12 mg kg−1 dw). The average concentration of Fe detected in this study (80.52 mg kg−1 dry wt) was below the MRL (0.7–0.8 mg kg−1 dw). The Pb concentration was the third highest in the samples analyzed, and the average concentration for Pb (18.42 mg kg−1 dw) exceeded the recommended MRL (0.0003–0.004 mg kg−1 dw). Ni was detected in a third of the samples (32.56%) with an average concentration (8.06 mg kg−1 dw) below the MRLs (0.0005–0.14 mg kg−1 dw). The average concentration of Mn (6.13 mg kg−1 dw) detected in 38.37% of the samples was above the MRLs (1 mg kg−1 dw) (Table 1).

OCP concentrations in Sphoeroides spp.

Twenty-two OCPs were detected in the muscle of Sphoeroides spp., several of them already listed as prohibited by the member countries of the WTO56. γ‒Chlordane was the most frequent OCP, and the analytes with the highest average concentration were α‒HCH, followed by γ‒chlordane (Table 1). No relation was found between size and OCPs concentration (Kruskal–Wallis, α 0.05, p = 0.442), nor between weight and pesticide concentration (Kruskal–Wallis, α 0.05, p = 0.438). Others studies in fish, the concentration of OCPs in tissues follows the following order of magnitude: liver > intestine > skin > muscle57,58, but, in the present study, the presence of these contaminants was determined only in the muscle of Sphoeroides spp. to assess their risk due to consumption.

Among the OCPs determined in the muscle of Sphoeroides spp. were HCHs, such as α‒HCH (24.7 µg kg−1 ww), β‒HCH (3.52 µg kg−1 ww), γ‒HCH (5.33 µg kg−1 ww), and δ‒HCH (3.52E-03 mg kg−1 ww), none of these concentrations were above MRLs (Table 1).

The DDT was detected in only two samples below the detection limit, but isomers, p, p'‒DDE (0.12 µg kg−1 ww) and p, p'‒DDD (10.11 µg kg−1 ww) were detected with a frequency of 26.74 and 10.47%, respectively.

From the drin family, aldrin (0.8 µg kg−1 ww), dieldrin (0.13 µg kg−1 ww), and endrin (2.22 µg kg−1 ww) were detected, with a frequency of 3.49, 15.12 and 16.28%, respectively. None of these OCPs were detected above MRLs.

Chlordane for technical use consists of a mixture of the stereoisomers α‒chlordane, γ‒chlordane, heptachlor, and heptachlor epoxide, which present concentrations of 0.02, 22.94, 0.17, and 0.07 µg kg−1, and a frequency of 60.47, 3.49, 1.16 and 3.49%, respectively. In the present study, the detected concentrations of these OCPs were lower than the MRLs (Table 1).

The endosulfan technical product consists of 70% endosulfan I and 30% endosulfan II, whose concentrations (0.25 and 0.21 µg kg−1, respectively) were below the MLRs (Table 1). Methoxychlor at a mean concentration of 6.14 µg kg−1 ww, was detected in 18.6% of the samples, and the concentration detected is within the permissible limits in Mexico (Table 1).

Seasonal concentrations

The highest TM concentration was detected in the spring of 2017, when Zn and Fe were at the highest average concentration (425 and 81.96 mg kg−1). The spring and summer of 2016 showed the highest diversity of TM, whereas the autumn 2016 and spring 2017 had the lowest diversity. Most average TM concentrations among the seasons depicted values below 90 mg kg−1 (Fig. 2).

Figure 2
figure 2

Seasonal concentration of TM in the Sphoeroides spp. fillet from Navachiste coastal lagoon.

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The presence of OCPs in Sphoeroides spp. tissue was detected in the five collection periods. The spring and summer of 2016 were the seasons with the highest concentration of OCP, with the highest concentrations of methoxychlor, α‒HCH endosulfan sulfate, and γ‒chlordane (94.29, 56.95, 23.94, and 10.80 µg kg−1 dw, respectively), whereas, in the summer, the highest concentrations corresponded to β‒HCH and γ‒chlordane (99.18 and 19.48 µg kg−1 dw, respectively) (Fig. 3).

Figure 3
figure 3

Seasonal concentrations of OCP in the Sphoeroides spp. fillet from Navachiste coastal lagoon, Mexico.

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TM risk of Sphoeroides spp.

The EDI values for the consumption of Sphoeroides spp. and their TM content indicate that most of the TM analyzed, except for Pb, do not exceed the EDI values. Pb exceeded the maximum recommended daily limit by 28.8-times at a rate of 32 g day−1 of Sphoeroides spp. fillet, representing a potential risk of long-term non-carcinogenic effects due to its consumption (Table 2).

Table 2 Concentration, estimated daily intake (EDI), target hazard quotient (THQ), and hazard index (HI) for trace metals analyzed in the edible fillet of Sphoeroides spp. from Navachiste, Mexico.
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OCP risk in Sphoeroides spp.

The non-carcinogenic and carcinogenic risk values were obtained for each OCP, considering a probability of 5/100,000 individuals having symptoms during a lifetime (Table 4). The average concentration of each OCP did not exceed the RfD values. The calculated HQ values < 100 and THQ = 55.2 do not imply a risk of having symptoms of non-carcinogenic diseases in the mid- or long-term after consuming this species of the NAV.

Discussion

TM concentration in Sphoeroides spp.

The concentration of Cd (1.45 mg kg−1 dw) below other fish species could be related to Sphoeroides spp. feeding habits and its place in the trophic web (Table 3). The top predatory fish in the open sea are found in most cases in the upper levels of the food web59, depending on whether their feeding habit is filtering or detritivorous35,60, or demersal or pelagic61. These characteristics make these species suitable for larger biomagnifying and bioaccumulating of trace metals than Sphoeroides spp., which an omnivorous species located at the mid-level of the food web, its diet includes fish, crustaceans, and mollusks.

Even though Cu is an essential nutrient for the synthesis of proteins and functioning of enzymes, its consumption in excess presents adverse effects on human health10. In the present study, Cu showed higher concentrations (5.06 mg kg−1 dw) compared to other carnivorous fishes62,63 (Table 3); this could be attributed to the level of TM pollution in NAV caused by human activities13, and the position of carnivorous fishes in the food web due to biomagnification52,64.

Ni is not essential for human health, but it is toxic above 0.5 mg kg−1. The latest reports indicate that the presence of Ni in marine organisms is due to anthropogenic or natural sources, but that in areas with high oil industrial activity the values rise65, which may represent risks to human health. However, in NAV there is no oil industry like the one found in the Gulf of Mexico and, as in previous studies66, its presence could be due to a lithogenic origin. The Ni concentration (8.06 mg kg−1 dw) of the edible tissue of Sphoeroides spp. were higher to those reported in recent studies on other marine species of the region35,60,67,66,69 (Table 3). However, the concentration of Ni in predatory fishes has been reported to be slightly higher than those in herbivorous and omnivorous species66.

The highest concentration of Zn (189.55 mg kg−1 dw) could be a response to lithogenic or anthropogenic sources70, such as the increased number of boats due to tourism and artisanal fisheries activities13, the effluents from the thermal power plant71, and the chemical fertilizers wastes from the neighbored agricultural valley of Guasave. All together could increase the concentration, bioavailability and bioaccumulation of Zn in the environment72,73, increasing it in the tissues of aquatic organisms72,74; due to its essential micronutrient role as a component of enzymes and oxides, it is automatically adsorbed by the body75.

Iron is an important metal for life, essential as a component of proteins, such as hemoglobin, and of muscle tissue76. The origin of its high concentration in the analyzed fillet could be attributed to the presence and erosion of this element from the earth crust in the region, or by the untreated sewage discharges from municipal and rural populations to the lagoon35,60. This Fe concentration in the present study (80.52 mg kg−1 dw) was similar to that detected in Atherina hepsetus (78 mg kg−1)77, higher than in farmed snapper species (5.103–19.985 mg kg−1)78 (Table 3). These differences can be attributed to the detritivorous feeding habits from sediments rich in Fe and the metabolic differences among species.

In the case of Pb, its concentration (18.42 mg kg−1 dw) in Sphoeroides spp. was higher than in other species of carnivorous fishes62,63 (Table 3), and could be attributed to Pb in sediments and water due to agricultural residues74. The latter could reflect the impact of the economic development in the last decade and has been related to the increased amounts of vehicles and traffic and the use of leaded gasoline or diesel or to the mining residues that could be carried by rivers79,80.

Mn is considered a micronutrient, enzyme activator, and main component in mitochondrial enzymes such as superoxide dismutase and pyruvate carboxylase11, but, above certain concentrations, it generates damage at the genetic, enzymatic, or neurological level81,82. The Mn concentration detected in the Sphoeroides spp. (6.13 mg kg−1 dw) was above the MRL (0.140)44,83. In relation to other species, Mn showed a discrepancy with other marine fish species (Table 3). Due to the critical role of Mn in fish metabolism, it is immediately absorbed due to its involvement in gill metallothionein levels, oxidative protein damage in liver and muscle, and gill activity of superoxide dismutase; it is influenced by the trophic level and feeding habit of the species84.

Table 3 Trace metal concentrations (mg kg−1 dry wt) in marine fishes Sphoeroides spp. and other regions in the world.
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The bioavailability of TM depends mainly on the sediment's physicochemical characteristics, chemical fractions, and pH, most of them affect their bioavailability85. However, the chemical form in which they are found and the anthropogenic contributions increase their basal concentration in a specific site. In the case of NAV, it is adjacent to more than 150,000 ha of intensive agricultural activities (> 160,000 ha). The presence of Cd, Zn, and Cu coincides with the use of fertilizers and pesticides by this agricultural area86, shrimp culture, and domestic sludge, which influence the concentration in the seawater and sediments of the NAV region60. The concentrations of Cd, Cu, and Ni revealed the significant relationship previously reported with trophic levels. Benthic invertebrates have shown a species-specific accumulation of these TM in the food web rather than biomagnification52, and it has been reported that bioaccumulation of TM depends on fish feeding habits and the inhabited region54. The TM concentrations in Sphoeroides spp. are higher than those previously reported in marine fishes83,87,88. This higher concentration depends on various factors, the feeding habit of Sphoeroides spp. as carnivorous, the enrichment factor in the sediments, the continental crust contribution, and the grade and source of anthropogenic pollution13,28,35,89. Compared with recent reports on the concentration of TM in the muscle of other marine fish species, the concentrations of Cd, Ni, Zn, and Pb in the Sphoeroides spp. fillet were higher. Lower concentrations of Cu and Fe have been reported in Apocryptes bato, Harpadon nehereus, Polynemus paradiseus, and Otolothoides pama from coastal areas around the mouth of the Meghna River in Bangladesh; a lower concentration of Mn has been reported in Cepola macrophthalma in Karatas, Turkey90,91 (Table 3). The concentration of TM depends on the degree and sources of anthropogenic contamination present in the areas and the feeding habits of the species62. As explained above, Navachiste is constantly impacted by effluents from intensive irrigation residues from the neighboring agricultural valley, and Sphoerpoides spp. is a pelagic and benthic carnivorous species. Therefore, its location in the food web allows it to bioaccumulate biomagnified TM. The same occurs with the species reported for Bangladesh. Although the area where those species were caught are defined as marine species90, they possibly were captured from coastal areas impacted by human activities.

OCP concentrations in Sphoeroides spp.

The high ratios of p, p'‒ DDE (0.52) and p, p'‒DDD (0.48), and the absence of p, p'‒ DDT suggest that there have been no recent applications of p, p'‒DDT in the area. DDE is the most persistent metabolite of p, p'‒DDT in the environment that can last up to 10 years available in the environment92. The presence of non-detected p, p'‒DDT concentration in the edible tissue of Sphoeroides spp. suggests the persistence of residues from the 60's to the '90 s in the sediments of NAV. During that time, p, p'‒DDT was an insecticide used intensively to control insects in crops93. This persistence can be corroborated by the present detected low concentrations of p, p'‒ DDT in Sphoeroides spp. previously detected in fishes from the same study area17,18 Currently, in Mexico, technical p, p'‒ DDT is an OCP commercially banned but of restricted use exclusively by the Mexican Ministry of Health for the control of vectors of infectious diseases such as the mosquito that mainly transmits dengue.

The high aldrin and lower endrin and dieldrin concentrations could be due to the recent use of the three pesticides on agricultural crops45,94. In the present study, the higher ratios for dieldrin (0.43) and endrin (0.47) than for aldrin (0.1) indicate historical contamination. In this case, most of the dieldrin available in the environment could be originated from the oxidation of aldrin, as previously reported95; in Mexico, as stated above it is actually prohibited, but it was very popular in the past as an insecticide in agriculture93,96.

Technical grade HCH is a mixture of isomers of this molecule, α‒HCH (60–70%), β‒HCH (5–12%), γ‒HCH (10–15%), δ‒HCH (6- 10%), the commercial lindane product consists of 99% γ‒HCH, and the presence of all HCH isomers and the ratio of γ‒HCH to the rest indicates historical contamination from the use of lindane and technical HCH40,97,98.

Technical chlordane has a restricted use as a termiticide, and it is not prohibited in Mexico. The ratios of the isomers, α‒ chlordane (0.0007), γ‒chlordane (0.98), heptachlor (0.007), and heptachlor epoxide (0.003), and the low frequency of the last two in the samples imply a historical use and might be attributed to atmospheric transport or their runoff in the last decades from the neighboring agricultural area.

The degradation product of technical endosulfan to endosulfan sulfate, could result as a product of the metabolism of some fungi such as Trametes versicolor and Pleurotus ostreatus99; and which was detected with an average concentration of 4.93 µg kg−1 and a frequency of 11.63% of the samples. In this way, it is plausible that the residual products of endosulfan and its isomers from the neighboring agricultural valley indicate endosulfan's recent use due to its low persistence between 30 and 150 days100, resulting in the bioaccumulation by Sphoeroides spp.

Methoxychlor is used as a larvicide in crops and can persist in the environment for up to 6 months101, and the detection in the fillet of Sphoeroides spp. would imply a recent use in the agricultural area of the Valle de Guasave even its use is restricted to the exclusive use in seed treatment for sowing in crops of rice, oats, barley, peas, beans, corn, sorghum102.

The bioavailability of OCPs has been correlated with the yearly seasons, their concentrations have been reported to be higher in the seasons after the rainy season or in the dry season103,104. In this study, the same characteristics were found, the highest concentrations occurred in the spring after the intensive agricultural irrigation season in the zone35, and OCP become bioaccumulated by marine organisms105.

TM risk of Sphoeroides spp.

The THQ for each metal, except for Pb (THQ = 2.16), was less than 1. The Pb value indicates a high possibility of non-carcinogenic effects in the mid-term due to the consumption of Spheroides spp. from NAV at 32.88 g day−1. This result regarding the toxic implications of Pb in the edible tissues of marine fish have been previously reported61. However, if the consumption ratio of Sphoeroides spp. fillet increases to a rate of 120 g day−1 on average (equivalent to three "tacos"), the chances of presenting symptoms due to non-carcinogenic effects increase substantially for Pb (THQ = 7.89) and other TMs such as Cd (2.49) and Zn (1.08).

Regarding the carcinogenicity risk, the ILCR values were greater than 1 × 10–6 (lifetime cancer risk probability), and the risk is not significant if the ILCR value is lower than 1 × 10–6. In the present study, all ILCR values of the analyzed TM were above 1 × 10–6, indicating a high risk for cancer development in the long-term (Table 2)106. Nevertheless, the cooking procedures could reduce the bioaccessibility and concentrations of the TM in the edible tissue of marine fish107,108.

It has been previously reported how pollutant residues inputs are deposited in the sediments of the coastal lagoons close to agricultural drains80, such as TM residues, which have been reported in edible tissues of the marine species and sediments inhabiting those ecosystems17,18,20,35,69,109. The discrepancies in the levels of heavy metals among the different studies could be due to the difference in fish metabolism, metal bioactivity, species of fishes, and trophic levels55,59, type of contaminants, geographical location110, capture season, fish size, fish age52,55, and the detainment period of metals in water111,112.

OCP risk in Sphoeroides spp.

Regarding the carcinogenic risk (CRLim), only aldrin, p, p′‒ DDD, p, p′‒ DDE, dieldrin, endosulfan, heptachlor, heptachlor epoxide, α‒HCH, β‒HCH, and γ‒HCH CRLim showed values that represent a high probability for developing cancer in the long-term (Table 4). These values were higher than those reported in edible muscle in fishwhich CRLim could allow eating higher portions of them before reaching a potential health risk40,113. In the present study, the CRLim of some OCPs was remarkably lower than the meal size analyzed here (32.88 g), implying that the consumption of the edible fillet of Sphoeroides spp. over a long time could be a potential cause of cancer at this meal portion. Nevertheless, the amount of OCP considered here was in raw fish tissue, and factors such as the bioavailability of pesticides in the tissue, the possibility that the ingested OCPs are totally or partially excreted, or the amount lost during the cooking process of the fillet may alter the concentration of OCP40. As reported, the cooking process used (microwaving, roasting. and boiling) will reduce the concentrations of OCP in the edible tissue of marine fish114.

Table 4 OCP concentration (mg kg−1), oral slope factor (OSF), reference dose (RfD), estimated daily intake (EDI), target hazard quotient (THQ), hazard quotient (HQ), and cancer risk limit (CRLim) in Sphoeroides spp. of the Navachiste Lagoon System.
Full size table

Conclusions

The health risk posed by the TM and OCPs concentration in the edible tissue of Sphoeroides spp from the NAV in the southwestern part of the Gulf of California was evaluated. The results of non-carcinogenic and carcinogenic risks revealed that the Pb value pose a high possibility of inducing non-carcinogenic effects in the mid-term. However, if the consumption ratio increases up to 120 g day−1 of edible tissue (equivalent to three “tacos” per day), the non-carcinogenic effects symptoms increase substantially for Pb and become potential for Cd and Zn. The evaluated OCP carcinogenic risks highlight that the ILCR values were more significant for a lifetime cancer risk probability, and the TM analyzed here were above minimum ILCR (> 1 × 10–6), indicating a high-risk potential for the development of cancer in the long-term. OCP´s did not exceed the RfD values, and the HQ values did not imply a risk to present non-carcinogenic diseases in the mid- or long-term. The CRLim of aldrin, p, p'‒ DDD, p, p'‒ DDE, dieldrin, endosulfan, heptachlor, heptachlor epoxide, α‒HCH, β‒HCH, and γ‒HCH CRLim had values that represent a high probability for developing cancer in the long-term. It is evident that if local communities consume the fillet of the Sphoeroides spp. in portions above 120 g day−1 it could represent a carcinogenic and non-carcinogenic risks in the mid and long term. Nevertheless, if the fillet is cooked, mainly boiling, frying or steaming, it could reduce the bioaccessible OCP and TM fractions. Intensive anthropogenic activities constantly dispose of their residues, after irrigation or water exchange, directly into the NAV through discharge channels, which is evidenced by the pesticides and chemical residues pollution recorded in the NAV sediments.