Investigation of the Toxicokinetics of Dietary Pacific Ciguatoxins (P-CTXs) in Orange-Spotted Grouper and the Trophodynamics of Marine Lipophilic Phycotoxins in a Food Web in the South China Sea


Student thesis: Doctoral Thesis

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Award date24 May 2021


The occurrence of harmful algal blooms has increased worldwide over the past few decades because of global warming and various anthropogenic factors. Marine phycotoxins produced by harmful and toxic algae are readily released into the marine environment and can be bio-accumulated and bio-transformed in various marine organisms. There has been an increasing trend of fast-rising phycotoxin levels in the marine environment and phycotoxin-related food-poisoning events. To date, more than 300 phycotoxins have been identified in various marine species, over 90% of which are lipophilic, which are more easily bioaccumulated than hydrophilic phycotoxins, raising even more public concern. Typical marine lipophilic phycotoxins (MLPs), such as azaspiracids (AZAs), brevetoxins (BTXs), ciguatoxins (CTXs), okadaic acid (OA), dinophysistoxins (DTXs), pectenotoxins (PTXs), gymnodimine (GYM), spirolides (SPXs), and yessotoxins (YTXs), are frequently involved in phycotoxin-related poisoning cases. However, the sources, fate, and uptake and depuration mechanisms of these toxins in marine organisms are still largely unknown. Therefore, the objectives of the present study are to: (1) investigate the uptake and depuration kinetics of MLPs in marine organisms; (2) investigate the multi-phase occurrence and the influence of environmental factors, of MLPs in marine environment; and (3) assess the bioaccumulation and biomagnification potential of MLPs in a food web, comprising species of different trophic levels.

The food chain hypothesis of CTXs (which are the most toxic MLPs) has been proposed that the precursors of CTX4A/4B produced by Gambierdiscus spp. can be oxidized into the more toxic and polar CTXs (such as Pacific-CTX-1, -2, and -3), leading to the biomagnification along the food chains and higher risks for the organisms at relatively higher trophic levels. In this study, I evaluated the uptake and depuration kinetics of P-CTX-1, -2, and -3 in carnivorous orange-spotted grouper (Epinephelus coioides) exposed to 1 ng P-CTXs g−1 fish daily. Over a 30-d exposure period, P-CTX-1, -2, and -3 were consistently detected in various tissues of exposed fish, with concentrations of total P-CTXs in tissue generally ranked in the following order: liver, intestine, gill, skin, brain, and muscle. A relatively higher uptake rate of P-CTX-1 in the grouper was observed than for P-CTX-2 and -3. The depuration rate constants of P-CTX-1, -2, and -3 in whole grouper were 3.23×10−2, 3.23×10−2, and 1.83×10−2 d−1, respectively. The accumulation efficiencies of P-CTX-1, -2, and -3 in whole fish 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 during the exposure phase suggested the 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.

Moreover, the information on the multi-phase distribution and influence of environmental factor of MLPs in the Pearl River Estuary (PRE), which is an important fishery zone and largely impacted by the various human associated activities in South China, is limited. Surface and bottom seawater suspended particulate matter (SPM), and surface sediment were collected in the PRE in July 2020, to investigate the occurrence and spatial distribution of the 17 MLPs as well as the influence of environmental factors. Nine MLPs, including OA, DTXs1−2, PTX2, homoYTX, GYM, and AZAs1−3, were detected, with the total MLP concentrations ranging from 545−12,600 pg L−1 and 619−8,800 pg L−1 in surface and bottom seawater, respectively, <76.3 to 3,540 pg L−1 and 89.6−4,440 pg L−1 in surface and bottom SPM, respectively, and 3.9−982 pg g−1 dry weight in surface sediment. PTX2 was predominant across samples. Lower MLP levels in seawater were found closer to the PRE coast and gradually increased with distance offshore, which may be explained by the influence of environmental variables that the MLP levels exhibited positive correlations with temperature, salinity, and dissolved oxygen while were negatively correlated with turbidity and chlorophyll.

Furthermore, I conducted a comprehensive food web study to investigate the bioaccumulation and trophic transfer of MLPs in a food web in Hong Kong waters, South China. A total of 17 species of mollusks, crustaceans, and fishes were analyzed for the typical 17 MLPs. Twelve MLPs, including OA, DTXs1−2, PTX2, YTX and its derivate homoYTX, GYM, SPX1, AZAs1−3, and BTX3, were detected with the total MLP concentrations ranging from 316 to 20,300 pg g−1 wet weight (ww). The means of total MLP concentrations generally followed the rank of mollusks (8,540 pg g−1, ww) > crustaceans (1,380 pg g−1, ww) > fishes (914 pg g−1, ww). OA, DTXs, and YTXs were predominant phycotoxin groups accumulated in mollusks, crustaceans, and fishes. The differences in specific MLP bioaccumulation analog profiles between invertebrates and fishes may result from the variable of multi-sources of exposure as well as the metabolisms of MLPs. Trophic dilution was observed for the total MLPs with the trophic magnification factor of 0.109. The studied MLPs might not pose health risks to residents who may consume contaminated seafood; however, their potential risks posed to the marine ecosystem can be a cause for concern.

In summary, I provided the insight toxicokinetics data of selected-MLPs in a carnivorous fish via laboratory feeding experiment and important information of representative 17 MLPs in the marine abiotic environment and in a food web via field works, which are of interest for future risk assessment and fisheries management for controlling different kinds of MLP-related poisoning. This was the first study to investigate the toxicokinetics of P-CTXs in carnivorous fish through repeated, long-term dietary exposure. In addition, the multi-phase occurrence of MLPs in the PRE of the South China Sea was firstly studied and I demonstrated that the distribution of MLPs can be affected by various the environmental factors. Last but not the least, a food web study of MLPs in the South China Sea revealed their trophic dilution potential.