Uptake and Depuration Kinetics of Pacific Ciguatoxins in Orange-Spotted Grouper (Epinephelus coioides)

Abstract

Ciguatoxins (CTXs), produced by toxic benthic dinoflagellates, can bioaccumulate in marine organisms at higher trophic levels. The current study evaluated the uptake and depuration kinetics of some of the most potent CTXs, Pacific CTX-1, -2, and -3 (P-CTX-1, -2, and -3), in orange-spotted grouper (Epinephelus coioides) exposed to 1 ng P-CTXs g −1 fish daily. Over a 30 d exposure, P-CTX-1, -2, and -3 were consistently detected in various tissues of exposed fish, and the concentrations of the total P-CTXs in tissues generally ranked following the order of liver, intestine, gill, skin, brain, and muscle. Relatively higher uptake rates of P-CTX-1 in the groupers were observed compared with those of P-CTX-2 and -3. The depuration rate constants of P-CTX-1, -2, and -3 in different tissues were (0.996−16.5) × 10 −2 , (1.51−16.1) × 10 −2 , and (0.557−10.6) × 10 −2 d −1 , respectively. The accumulation efficiencies of P-CTX-1, -2, and -3 in whole groupers were 6.13%, 2.61%, and 1.15%, respectively. The increasing proportion of P-CTX-1 and the decreasing proportion of P-CTX-2 and -3 over the exposure phase suggest a likely biotransformation of P-CTX-2 and -3 to P-CTX-1, leading to higher levels of P-CTX-1 in fish and possibly a higher risk of CTXs in long-term exposed fish.

Characteristic Distribution of Ciguatoxins in the Edible Parts of a Grouper, Variola louti

“…Although high in concentration, the eyes alone cannot account for the legends of higher toxicity of the head. According to Li et al [29], CTXs were consistently detected in various tissues of grouper Epinephelus coioides over 30 days of exposure. CTX levels ranked from high to low in the following order: liver, intestine, gill, skin, brain, and muscle.…”

“…Thus, avoiding the consumption of the viscera and the head is recommended [4,27]. The presence of high levels of CTXs in the liver of ciguateric fish is well documented [26,[28][29][30], providing the basis for the use of the livers as the source of toxin isolation [31,32]. Conversely, toxicity data on the CTX levels in head samples are scarce [29].…”

Ciguatera Mini Review: 21st Century Environmental Challenges and the Interdisciplinary Research Efforts Rising to Meet Them

“…After ingestion, CTXs are metabolized in different ways, subject to the animal’s individual biochemical/biological/physiological processes. Generally, CTXs are taken up and first detected in the gastrointestinal tract and liver, then eventually transferred to the muscle tissue and throughout the body and skin [ 134 , 135 , 136 , 137 ]. Studies examining the behavior of fish administered CTXs found both behavioral abnormalities and the absence of impacts [ 135 , 137 ].…”

“…The application of next-generation sequencing in fish ecotoxicogenomics could help bridge the link between exposure and effects, a benefit for environmental assessments for CTXs as well as assessing risks to fish health [ 138 , 139 ]. Available data regarding the absorption efficiency of CTXs from fish feed was approximately 1–6%, where depuration half-life rates were tissue-related, from several days for the liver to several months in the skin [ 134 ]. Within the fish reside many useful biological data points for gaining insight into CTX accumulation, including age (through otolith analysis), dietary shifts due to prey availability or ontogeny (stable isotopic analysis to determine trophic feeding level, location, or habitat utilization type), fish prey information (analysis of gut contents) [ 140 ], fish size (by standard morphometrics), fecundity by egg production/weight (impact of CTXs on fish reproduction), and the liver/viscera/brain for bioaccumulation and metabolism data.…”

Experimental Evidence of Ciguatoxin Accumulation and Depuration in Carnivorous Lionfish

“…Ciguatoxins found in the brain, liver, and muscles of stranded Monachus schauinslandi monk seals [ 26 ] suggest that marine mammals may also suffer from CTX exposure, and that these compounds persist within the complex marine food webs. However, marine species experimentally fed with CTX ( Naso brevirostris [ 27 ] and Epinephelus coioides [ 28 ]) did not seem sensitive to the effects of CTX. The fish resistance mechanism to CTX is still unknown.…”