Dynamics of ciguatoxins from Gambierdiscus polynesiensis in the benthic herbivore Mugil cephalus: Trophic transfer implications

This study investigates ciguatoxin dynamics in mullet after controlled feeding of Gambierdiscus polynesiensis cells as a model to characterize the absorption, distribution, retention and accumulation of ciguatoxins into the second trophic level of southwestern Pacific coral reef ecosystems. Mullet (Mugil cephalus) were fed once every other day over a period of 16 days for nine toxic feedings, and ciguatoxin activity was assessed over time in blood and seven tissues using the Neuro2a assay. Within 3 h of feeding on G. polynesiensis cells, ciguatoxins attained maximal blood concentrations, indicating rapid absorption of toxins into the systemic circulation. The time course for distribution of the estimated total tissue burden of ciguatoxin closely followed the time course for blood toxin levels, indicating a rapid distribution of the ciguatoxins throughout the fish body. The large majority (95%) of the ciguatoxin ingested dose was eliminated from the examined fish tissues 24 h after a single toxic meal, indicating little retention potential for ciguatoxin. We found no evidence for ciguatoxin accumulation after nine repeated feedings spaced two days apart, indicating that mullet did not accumulate ciguatoxin. These results provide the first experimental evidence supporting the central tenet of Randall's food chain hypothesis that ciguatoxins enter the food chain by transfer from unicellular algae to herbivorous and detritus-feeding fish. We propose that a time-dependent transformation of oxopene ciguatoxins may be necessary for the concentration of ciguatoxin through higher trophic levels.