Origin of Ciguateric Fish: Quantitative Modelling of the Flow of Ciguatoxin through a Marine Food Chain

Abstract

To begin to understand the impact of food chain dynamics on ciguatera risk, we used published data to model the transfer of ciguatoxins across four trophic levels of a marine food chain in Platypus Bay, Australia. The data to support this first attempt to conceptualize the scale of each trophic transfer step was limited, resulting in broad estimates. The hypothetical scenario we explored generated a low-toxicity 10 kg Spanish mackerel (Scomberomorus commerson) with a flesh concentration of 0.1 µg/kg of Pacific-ciguatoxin-1 (P-CTX-1, also known as CTX1B) from 19.5–78.1 µg of P-CTX-1 equivalents (eq.) that enter the marine food chain from a population of 12–49 million benthic dinoflagellates (Gambierdiscus sp.) producing 1.6 × 10−12 g/cell of the P-CTX-1 precursor, P-CTX-4B. This number of Gambierdiscus could be epiphytic on 22–88 kg of the benthic macroalgae (Cladophora) that carpets the bottom of much of Platypus Bay, with the toxin transferred to an estimated 40,000–160,000 alpheid shrimps in the second trophic level. This large number of shrimps appears unrealistic, but toxic shrimps would likely be consumed by a school of small, blotched javelin fish (Pomadasys maculatus) at the third trophic level, reducing the number of shrimps consumed by each fish. The Spanish mackerel would accumulate a flesh concentration of 0.1 µg/kg P-CTX-1 eq. by preying upon the school of blotched javelin and consuming 3.6–14.4 µg of P-CTX-1 eq. However, published data indicate this burden of toxin could be accumulated by a 10 kg Spanish mackerel from as few as one to three blotched javelin fish, suggesting that much greater amounts of toxin than modelled here must at certain times be produced and transferred through Platypus Bay food chains. This modelling highlights the need for better quantitative estimates of ciguatoxin production, biotransformation, and depuration through marine food chains to improve our understanding and management of ciguatera risk.

Model of the Origin of a Ciguatoxic Grouper (Plectropomus leopardus)

“…We modelled the hypothetical transfer of ciguatoxins from Gambierdiscus epiphytic on a turf algae layer at surface (plan view) densities of ≤10, 100, and 1000 cells/cm 2 to span the globally reported cell densities from surfaces (mostly screens). We based our model on these cells producing 1.6 pg of P-CTX-4B/cell, which was the same theoretical toxin concentration used for our recent modelling of the contamination of pelagic Spanish mackerel ( Scomberomorus commerson (Lacépède 1800)) by Gambierdiscus from Platypus Bay on the east coast of Queensland (a non-coral reef habitat south of the GBR) [ 64 ]. This CTX concentration is 2.7-fold greater than the maximum known combined cellular concentrations of P-CTX-4A and -4B of 0.6 pg/cell produced by cultured G. polynesiensis [ 33 ].…”

“…This flesh concentration of CTX would likely produce mild symptoms in 2 out of 10 people [ 85 ]. We calculated a total CTX burden for a 1.6 kg common coral trout by using the method of Holmes and Lewis [ 64 ], based upon a flesh (fillet) recovery weight of 50% total fish weight [ 86 , 87 ] and a toxin assimilation efficiency of 43% across each trophic level, with flesh contributing 10–40% of the total CTX burden [ 64 , 88 ]. On this basis, a 1.6 kg common coral trout would accumulate between 0.2 and 0.8 µg P-CTX-1 equivalents (eq.).…”

“…Our estimate for the population of ciguatoxic Gambierdiscus that is required to produce a mildly toxic coral trout on the GBR is <10-times our estimate to produce a mildly toxic Spanish mackerel ( Scomberomorus commerson ) from Platypus Bay, a small bay to the south of the GBR [ 64 ]. This difference arises because groupers are typically much smaller than Spanish mackerel and probably need to ingest less toxin to produce the same level of muscle contamination, and our assumption that toxin is transferred across three trophic levels on the GBR, but across four trophic levels in Platypus Bay [ 64 ].…”

“…Our estimate for the population of ciguatoxic Gambierdiscus that is required to produce a mildly toxic coral trout on the GBR is <10-times our estimate to produce a mildly toxic Spanish mackerel ( Scomberomorus commerson ) from Platypus Bay, a small bay to the south of the GBR [ 64 ]. This difference arises because groupers are typically much smaller than Spanish mackerel and probably need to ingest less toxin to produce the same level of muscle contamination, and our assumption that toxin is transferred across three trophic levels on the GBR, but across four trophic levels in Platypus Bay [ 64 ]. If Gambierdiscus population density were the main determining factor for the production of ciguateric higher trophic-level fish along the east coast of Australia, then it would be reasonable to assume that the chance of producing a ciguateric grouper should be greater than the production of ciguateric Spanish mackerel (all other factors being equal).…”

“…We use C. striatus as our model for the transfer of ciguatoxins by surgeonfishes to common coral trout but, where possible, include comparisons with A. nigrofuscus as an alternate vector. This contribution builds upon previous modelling for the production of ciguateric pelagic fish (Spanish mackerel) from the east coast of Australia [ 64 ] and conceptual models for ciguateric food chains on the GBR, as well as models for the reduction in CTX concentrations in fishes through growth and depuration [ 13 ]. Our model synthesizes research on ciguatera, fisheries, and coral reef ecology to produce quantitative estimates for the flow of CTX through food chains.…”