A General Food Chain Model for Bioaccumulation of Ciguatoxin into Herbivorous Fish in the Pacific Ocean Suggests Few Gambierdiscus Species Can Produce Poisonous Herbivores, and Even Fewer Can Produce Poisonous Higher Trophic Level Fish

We adapt previous conceptual and numerical models of ciguateric food chains for the bioaccumulation of Pacific-ciguatoxin-1 (P-CTX-1) to a general model for bioaccumulation of P-CTX3C by parrotfish (<i>Scarus frenatus</i>, <i>S. niger</i>, and <i>S. psittacus</i>) that feed by scraping turf algae, and surgeonfish (<i>Naso unicornis</i>) that mostly feed on macroalgae. We also include the Indian Ocean parrotfish <i>Chlorurus sordidus</i> as a model for an excavator feeding parrotfish and include comparisons with the detritivorous surgeonfish <i>Ctenochaetus striatus</i> that brush-feeds on turf algae. Our food chain model suggests that, of the <i>Gambierdiscus</i> and <i>Fukuyoa</i> species so far analysed for ciguatoxin (CTX) production from the Pacific, only <i>G. polynesiensis</i> produces sufficient P-CTX3C to consistently produce parrotfish or <i>N. unicornis</i> with poisonous flesh. Our model suggests that insufficient CTX would accumulate into the flesh of parrotfish or <i>N. unicornis</i> to become poisonous from ingesting benthic dinoflagellates producing ≤0.03 pg P-CTX3C eq./cell, except from extended feeding times on high-density blooms and in the absence of significant depuration of CTX. Apart from <i>G. polynesiensis</i>, only <i>G. belizeanus</i> and possibly <i>G. silvae</i> and <i>G. australes</i> are thought to produce >0.03 pg P-CTX3C eq./cell in the Pacific. However, with relatively low maximum concentrations of ≤0.1 pg P-CTX3C eq./cell it is likely that their contribution is minimal. Our model also suggests that the differences between the area of turf algae grazed by parrotfish and similar sized <i>C. striatus</i> results in greater accumulation of CTX by this surgeonfish. This makes <i>C. striatus</i> a higher ciguatera risk than similar sized parrotfish, either directly for human consumption or as prey for higher trophic level fishes, consistent with poisoning data from Polynesia. It also suggests the possibility that <i>C. striatus</i> could bioaccumulate sufficient CTX to become mildly poisonous from feeding on lower toxicity <i>Gambierdiscus</i> or <i>Fukuyoa</i> species known to produce ≥0.02 P-CTX3C eq./cell. This indicates the potential for at least two food chain pathways to produce ciguateric herbivorous fishes, depending on the CTX concentrations produced by resident <i>Gambierdiscus</i> or <i>Fukuyoa</i> on a reef and the grazing capacity of herbivorous fish. However, only <i>G. polynesiensis</i> appears to produce sufficient P-CTX3C to consistently accumulate in food chains to produce higher trophic level fishes that cause ciguatera in the Pacific. We incorporate CTX depuration into our model to explore scenarios where mildly poisonous parrotfish or <i>N. unicornis</i> ingest CTX at a rate that is balanced by depuration to estimate the <i>Gambierdiscus</i>/<i>Fukuyoa</i> densities and CTX concentrations required for these fish to remain poisonous on a reef.