Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>)
Published data were used to model the transfer of ciguatoxins (CTX) across three trophic levels of a marine food chain on the Great Barrier Reef (GBR), Australia, to produce a mildly toxic common coral trout (<i>Plectropomus leopardus</i>), one of the most targeted food fishes on the GBR...
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MDPI AG
2023-03-01
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| Series: | Toxins |
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| Online Access: | https://www.mdpi.com/2072-6651/15/3/230 |
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| author | Michael J. Holmes Richard J. Lewis |
| author_facet | Michael J. Holmes Richard J. Lewis |
| author_sort | Michael J. Holmes |
| collection | DOAJ |
| description | Published data were used to model the transfer of ciguatoxins (CTX) across three trophic levels of a marine food chain on the Great Barrier Reef (GBR), Australia, to produce a mildly toxic common coral trout (<i>Plectropomus leopardus</i>), one of the most targeted food fishes on the GBR. Our model generated a 1.6 kg grouper with a flesh concentration of 0.1 µg/kg of Pacific-ciguatoxin-1 (P-CTX-1 = CTX1B) from 1.1 to 4.3 µg of P-CTX-1 equivalents (eq.) entering the food chain from 0.7 to 2.7 million benthic dinoflagellates (<i>Gambierdiscus</i> sp.) producing 1.6 pg/cell of the P-CTX-1 precursor, P-CTX-4B (CTX4B). We simulated the food chain transfer of ciguatoxins via surgeonfishes by modelling <i>Ctenochaetus striatus</i> feeding on turf algae. A <i>C. striatus</i> feeding on ≥1000 <i>Gambierdiscus</i>/cm<sup>2</sup> of turf algae accumulates sufficient toxin in <2 days that when preyed on, produces a 1.6 kg common coral trout with a flesh concentration of 0.1 µg/kg P-CTX-1. Our model shows that even transient blooms of highly ciguatoxic <i>Gambierdiscus</i> can generate ciguateric fishes. In contrast, sparse cell densities of ≤10 <i>Gambierdiscus</i>/cm<sup>2</sup> are unlikely to pose a significant risk, at least in areas where the P-CTX-1 family of ciguatoxins predominate. The ciguatera risk from intermediate <i>Gambierdiscus</i> densities (~100 cells/cm<sup>2</sup>) is more difficult to assess, as it requires feeding times for surgeonfish (~4–14 days) that overlap with turnover rates of turf algae that are grazed by herbivorous fishes, at least in regions such as the GBR, where stocks of herbivorous fishes are not impacted by fishing. We use our model to explore how the duration of ciguatoxic <i>Gambierdiscus</i> blooms, the type of ciguatoxins they produce, and fish feeding behaviours can produce differences in relative toxicities between trophic levels. Our simple model indicates thresholds for the design of risk and mitigation strategies for ciguatera and the variables that can be manipulated to explore alternate scenarios for the accumulation and transfer of P-CTX-1 analogues through marine food chains and, potentially, for other ciguatoxins in other regions, as more data become available. |
| first_indexed | 2024-03-11T05:49:24Z |
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| id | doaj.art-8b8b3ce2ba3d4d529e328e13f5c79ec9 |
| institution | Directory Open Access Journal |
| issn | 2072-6651 |
| language | English |
| last_indexed | 2024-03-11T05:49:24Z |
| publishDate | 2023-03-01 |
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| spelling | doaj.art-8b8b3ce2ba3d4d529e328e13f5c79ec92023-11-17T14:14:41ZengMDPI AGToxins2072-66512023-03-0115323010.3390/toxins15030230Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>)Michael J. Holmes0Richard J. Lewis1Institute for Molecular Bioscience, The University of Queensland, Brisbane 4072, AustraliaInstitute for Molecular Bioscience, The University of Queensland, Brisbane 4072, AustraliaPublished data were used to model the transfer of ciguatoxins (CTX) across three trophic levels of a marine food chain on the Great Barrier Reef (GBR), Australia, to produce a mildly toxic common coral trout (<i>Plectropomus leopardus</i>), one of the most targeted food fishes on the GBR. Our model generated a 1.6 kg grouper with a flesh concentration of 0.1 µg/kg of Pacific-ciguatoxin-1 (P-CTX-1 = CTX1B) from 1.1 to 4.3 µg of P-CTX-1 equivalents (eq.) entering the food chain from 0.7 to 2.7 million benthic dinoflagellates (<i>Gambierdiscus</i> sp.) producing 1.6 pg/cell of the P-CTX-1 precursor, P-CTX-4B (CTX4B). We simulated the food chain transfer of ciguatoxins via surgeonfishes by modelling <i>Ctenochaetus striatus</i> feeding on turf algae. A <i>C. striatus</i> feeding on ≥1000 <i>Gambierdiscus</i>/cm<sup>2</sup> of turf algae accumulates sufficient toxin in <2 days that when preyed on, produces a 1.6 kg common coral trout with a flesh concentration of 0.1 µg/kg P-CTX-1. Our model shows that even transient blooms of highly ciguatoxic <i>Gambierdiscus</i> can generate ciguateric fishes. In contrast, sparse cell densities of ≤10 <i>Gambierdiscus</i>/cm<sup>2</sup> are unlikely to pose a significant risk, at least in areas where the P-CTX-1 family of ciguatoxins predominate. The ciguatera risk from intermediate <i>Gambierdiscus</i> densities (~100 cells/cm<sup>2</sup>) is more difficult to assess, as it requires feeding times for surgeonfish (~4–14 days) that overlap with turnover rates of turf algae that are grazed by herbivorous fishes, at least in regions such as the GBR, where stocks of herbivorous fishes are not impacted by fishing. We use our model to explore how the duration of ciguatoxic <i>Gambierdiscus</i> blooms, the type of ciguatoxins they produce, and fish feeding behaviours can produce differences in relative toxicities between trophic levels. Our simple model indicates thresholds for the design of risk and mitigation strategies for ciguatera and the variables that can be manipulated to explore alternate scenarios for the accumulation and transfer of P-CTX-1 analogues through marine food chains and, potentially, for other ciguatoxins in other regions, as more data become available.https://www.mdpi.com/2072-6651/15/3/230ciguateraciguatoxin<i>Gambierdiscus</i><i>Plectropomus</i><i>Ctenochaetus</i><i>Acanthurus</i> |
| spellingShingle | Michael J. Holmes Richard J. Lewis Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>) Toxins ciguatera ciguatoxin <i>Gambierdiscus</i> <i>Plectropomus</i> <i>Ctenochaetus</i> <i>Acanthurus</i> |
| title | Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>) |
| title_full | Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>) |
| title_fullStr | Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>) |
| title_full_unstemmed | Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>) |
| title_short | Model of the Origin of a Ciguatoxic Grouper (<i>Plectropomus leopardus</i>) |
| title_sort | model of the origin of a ciguatoxic grouper i plectropomus leopardus i |
| topic | ciguatera ciguatoxin <i>Gambierdiscus</i> <i>Plectropomus</i> <i>Ctenochaetus</i> <i>Acanthurus</i> |
| url | https://www.mdpi.com/2072-6651/15/3/230 |
| work_keys_str_mv | AT michaeljholmes modeloftheoriginofaciguatoxicgrouperiplectropomusleopardusi AT richardjlewis modeloftheoriginofaciguatoxicgrouperiplectropomusleopardusi |