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Experimental Evidence of Ciguatoxin Accumulation and Depuration in Carnivorous Lionfish.

ABSTRACT: Ciguatera poisoning is a food intoxication associated with the consumption of fish or shellfish contaminated, through trophic transfer, with ciguatoxins (CTXs). In this study, we developed an experimental model to assess the trophic transfer of CTXs from herbivorous parrotfish, Chlorurus microrhinos, to carnivorous lionfish, Pterois volitans. During a 6-week period, juvenile lionfish were fed naturally contaminated parrotfish fillets at a daily dose of 0.11 or 0.035 ng CTX3C equiv. g^-1, as measured by the radioligand-receptor binding assay (r-RBA) or neuroblastoma cell-based assay (CBA-N2a), respectively. During an additional 6-week depuration period, the remaining fish were fed a CTX-free diet. Using r-RBA, no CTXs were detectable in muscular tissues, whereas CTXs were measured in the livers of two out of nine fish sampled during exposure, and in four out of eight fish sampled during depuration. Timepoint pooled liver samples, as analyzed by CBA-N2a, confirmed the accumulation of CTXs in liver tissues, reaching 0.89 ng CTX3C equiv. g^-1 after 41 days of exposure, followed by slow toxin elimination, with 0.37 ng CTX3C equiv. g^-1 measured after the 6-week depuration. These preliminary results, which need to be pursued in adult lionfish, strengthen our knowledge on CTX transfer and kinetics along the food web.

SUBMITTER: Leite IDP

PROVIDER: S-EPMC8402466 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Modeling ciguatoxin (CTX) trophic transfer in marine food webs has significant implications for the management of ciguatera poisoning, a circumtropical disease caused by human consumption of CTX-contaminated seafood. Current models associated with CP risk rely on modeling abundance/presence of CTX-producing epi-benthic dinoflagellates, e.g., Gambierdiscus spp., and are based on studies showing that toxin production is site specific and occurs in pulses driven by environmental factors. However, food web models are not yet developed and require parameterizing the CTX exposure cascade in fish which has been traditionally approached through top-down assessment of CTX loads in wild-caught fish. The primary goal of this study was to provide critical knowledge on the kinetics of C-CTX-1 bioaccumulation and depuration in the marine omnivore Lagodon rhomboides. We performed a two-phase, 17 week CTX feeding trial in L. rhomboides where fish were given either a formulated C-CTX-1 (n = 40) or control feed (n = 37) for 20 days, and then switched to a non-toxic diet for up to 14 weeks. Fish were randomly sampled through time with whole muscle, liver, and other pooled viscera dissected for toxin analysis by a sodium channel-dependent MTT-based mouse neuroblastoma (N2a) assay. The CTX levels measured in all tissues increased with time during the exposure period (days 1 to 20), but a decrease in CTX-specific toxicity with depuration time only occurred in viscera extracts. By the end of the depuration, muscle, liver, and viscera samples had mean toxin concentrations of 189%, 128%, and 42%, respectively, compared to fish sampled at the start of the depuration phase. However, a one-compartment model analysis of combined tissues showed total concentration declined to 56%, resulting in an approximate half-life of 97 d (R2 = 0.43). Further, applying growth dilution correction models to the overall concentration found that growth was a major factor reducing C-CTX concentrations, and that the body burden was largely unchanged, causing pseudo-elimination and a half-life of 143-148 days (R2 = 0.36). These data have important implications for food web CTX models and management of ciguatera poisoning in endemic regions where the frequency of environmental algal toxin pulses may be greater than the growth-corrected half-life of C-CTX in intermediate-trophic-level fish with high site fidelity.

Project description:Freshwater cyanobacteria produce highly toxic secondary metabolites, which can be transported downstream by rivers and waterways into the sea. Estuarine and coastal aquaculture sites exposed to toxic cyanobacteria raise concerns that shellfish may accumulate and transfer cyanotoxins in the food web. This study aims to describe the competitive pattern of uptake and depuration of a wide range of microcystins (MC-LR, MC-LF, MC-LW, MC-LY, [Asp3]-MC-LR/[Dha7]-MC-LR, MC-HilR) and nodularins (NOD cyclic and linear) within the common blue mussel Mytilus edulis exposed to a combined culture of Microcystis aeruginosa and Nodularia spumigena into the coastal environment. Different distribution profiles of MCs/NODs in the experimental system were observed. The majority of MCs/NODs were present intracellularly which is representative of healthy cyanobacterial cultures, with MC-LR and NOD the most abundant analogues. Higher removal rate was observed for NOD (≈96%) compared to MCs (≈50%) from the water phase. Accumulation of toxins in M. edulis was fast, reaching up to 3.4 μg/g shellfish tissue four days after the end of the 3-days exposure period, with NOD (1.72 μg/g) and MC-LR (0.74 μg/g) as the dominant toxins, followed by MC-LF (0.35 μg/g) and MC-LW (0.31 μg/g). Following the end of the exposure period depuration was incomplete after 27 days (0.49 μg/g of MCs/NODs). MCs/NODs were also present in faecal material and extrapallial fluid after 24 h of exposure with MCs the main contributors to the total cyanotoxin load in faecal material and NOD in the extrapallial fluid. Maximum concentration of MCs/NODs accumulated in a typical portion of mussels (20 mussels, ≈4 g each) was beyond greater the acute, seasonal and lifetime tolerable daily intake. Even after 27 days of depuration, consuming mussels harvested during even short term harmful algae blooms in close proximity to shellfish beds might carry a high health risk, highlighting the need for testing.

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Experimental Evidence of Ciguatoxin Accumulation and Depuration in Carnivorous Lionfish.

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