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

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-p...

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Autores principales:	Clayton T. Bennett, Alison Robertson
Formato:	article
Lenguaje:	EN
Publicado:	MDPI AG 2021
Materias:	<i>Lagodon rhomboides</i> pinfish bioaccumulation depuration ciguatoxin Caribbean ciguatoxin Medicine R
Acceso en línea:	https://doaj.org/article/d45b161a0ab041e4b19fcf0f59bed67e
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spelling	oai:doaj.org-article:d45b161a0ab041e4b19fcf0f59bed67e2021-11-25T19:08:43ZDepuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk10.3390/toxins131107742072-6651https://doaj.org/article/d45b161a0ab041e4b19fcf0f59bed67e2021-11-01T00:00:00Zhttps://www.mdpi.com/2072-6651/13/11/774https://doaj.org/toc/2072-6651Modeling 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., <i>Gambierdiscus</i> 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 <i>Lagodon rhomboides</i>. We performed a two-phase, 17 week CTX feeding trial in <i>L. rhomboides</i> where fish were given either a formulated C-CTX-1 (<i>n</i> = 40) or control feed (<i>n</i> = 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 (R<sup>2</sup> = 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 (R<sup>2</sup> = 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.Clayton T. BennettAlison RobertsonMDPI AGarticle<i>Lagodon rhomboides</i>pinfishbioaccumulationdepurationciguatoxinCaribbean ciguatoxinMedicineRENToxins, Vol 13, Iss 774, p 774 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	<i>Lagodon rhomboides</i> pinfish bioaccumulation depuration ciguatoxin Caribbean ciguatoxin Medicine R
spellingShingle	<i>Lagodon rhomboides</i> pinfish bioaccumulation depuration ciguatoxin Caribbean ciguatoxin Medicine R Clayton T. Bennett Alison Robertson Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk
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., <i>Gambierdiscus</i> 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 <i>Lagodon rhomboides</i>. We performed a two-phase, 17 week CTX feeding trial in <i>L. rhomboides</i> where fish were given either a formulated C-CTX-1 (<i>n</i> = 40) or control feed (<i>n</i> = 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 (R<sup>2</sup> = 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 (R<sup>2</sup> = 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.
format	article
author	Clayton T. Bennett Alison Robertson
author_facet	Clayton T. Bennett Alison Robertson
author_sort	Clayton T. Bennett
title	Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk
title_short	Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk
title_full	Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk
title_fullStr	Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk
title_full_unstemmed	Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk
title_sort	depuration kinetics and growth dilution of caribbean ciguatoxin in the omnivore <i>lagodon rhomboides:</i> implications for trophic transfer and ciguatera risk
publisher	MDPI AG
publishDate	2021
url	https://doaj.org/article/d45b161a0ab041e4b19fcf0f59bed67e
work_keys_str_mv	AT claytontbennett depurationkineticsandgrowthdilutionofcaribbeanciguatoxinintheomnivoreilagodonrhomboidesiimplicationsfortrophictransferandciguaterarisk AT alisonrobertson depurationkineticsandgrowthdilutionofcaribbeanciguatoxinintheomnivoreilagodonrhomboidesiimplicationsfortrophictransferandciguaterarisk
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Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore <i>Lagodon rhomboides:</i> Implications for Trophic Transfer and Ciguatera Risk

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