Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore Lagodon rhomboides: Implications for Trophic Transfer and Ciguatera Risk.

Clayton T Bennett,Alison Robertson

doi:10.3390/toxins13110774

Abstract

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.

Highlights

Benthic dinoflagellates have the capacity to produce a diverse suite of bioactive secondary metabolites that have been linked with seafood safety and human health concerns globally
Two dual-phase experimental trials were conducted to assess the depuration of Caribbean CTX-1 (C-CTX-1) that had bioaccumulated in Lagodon rhomboides fed a control or low-dose CTX diet through time and were sampled according to Table 1
In this study we report that C-CTX-1 was bioaccumulated in L. rhomboides from low environmentally relevant doses (0.02 ng Ciguatoxin 3C (CTX3C) eq g−1 day−1), and present that total ciguatoxicity was retained for at least 3.3 months and depuration was mostly a function of fish growth, a pseudo-elimination factor

Summary

Introduction

Benthic dinoflagellates have the capacity to produce a diverse suite of bioactive secondary metabolites that have been linked with seafood safety and human health concerns globally One such group includes the neurotoxic ciguatoxins (CTXs) that have been linked to ciguatera poisoning and have been associated with some species and strains of epibenthic dinoflagellates from the genus Gambierdiscus and Fukuyoa [1–5]. It has been proposed that CTX environmental pulses are linked to the presence of highly toxic Gambierdiscus strains rather than high overall algal biomass [5,6,9,10] potentially reducing the effectiveness of genus-level monitoring for these benthic HABs in terms of risk reduction This presents some questions on the subsequent CTX load and CTX pulses that may occur in other demersal marine biota feeding on potentially toxicogenic epiphytic algae, aquatic invertebrates (e.g., amphipods), and other small grazers

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