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Ciguatoxic dinoflagellate densities and the effects of algal biomass and species composition in a Pacific coral reef, Amy Briggs [et al.]

Ciguatoxic dinoflagellate densities and the effects of algal biomass and species composition in a Pacific coral reef, Amy Briggs [et al.]

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Distribution and diversity of Gambierdiscus

spp. and associated levels of ciguatoxins in

herbivorous fish from a ciguatera-endemic

area in the Cook Islands

Kirsty Smith ∗ 1 , Lesley Rhodes 1 , Arjun Verma 2 , Belinda Curley 3 ,

Gurjeet Kohli 4 , Anna Liza Kretzschmar 2 , Tim Harwood 1 , Sam Murray

1

, Teina Rongo 5 , Taiana Darius 6 , J´erˆome Viallon 6 , Mireille Chinain 6 ,

Shauna Murray 2

1



Cawthron Institute (Cawthron) – 98 Halifax St East, Private Bag 2, Nelson, New Zealand

Climate Change Cluster, University of Technology Sydney – PO Box 123, Broadway, New South

Wales 2007, Australia

3

Fisheries Research, Department of Primary Industries – Locked Bag 1, Nelson Bay NSW 2315,

Australia

4

Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University – 60

Nanyang Dr, Singapore

5

Climate Change Cook Islands, Office of the Prime Minister – Private Bag, Avarua, Rarotonga,, Cook

Islands

6

Institut Louis Malard´e (ILM) – BP30, 98713, Papeete Tahiti, French Polynesia

2



Rarotonga (southern Cook Islands) has had the highest reported incidences of ciguatera fish

poisoning (CFP) globally over the last four decades, although in recent years there has been

a sharp decline in reported cases according to hospital records. Reasons for this decrease are

unknown but international research has linked CFP with decadal climate oscillations, cyclone

frequency and salinity levels. Additionally, small-island nations experiencing extensive CFP may

undergo dietary shifts away from reef fish, consequently lowering the number of poisoning events

albeit with associated health, economic, and cultural impacts. Alternatively, cases of CFP often

go unreported to health professionals. Accurate identification of Gambierdiscus species and

knowledge of their associated toxicity in food sources is essential for determining the current

risk of CFP in Rarotonga. The aim of this study was to determine the taxonomy and toxicity

of Gambierdiscus spp. and the associated levels of CTXs in the next direct trophic level –

herbivorous fish. Dinoflagellates were collected from six sites and species were identified via

high-throughput sequencing (metabarcoding). Gambierdiscus cells were isolated and cultures

established to determine the toxicity of different strains. At each site territorial herbivorous fish

(Ctenochaetus striatus) were collected and analysed for CTXs using both a cell-based assay and

liquid chromatography mass spectrometry. A range of fish species were also collected from the

southern side of the island for toxin analyses. Multiple Gambierdiscus species were present at all

sites, including two previously undescribed species (G. cheloniae and G. honu) and the known

CTX producer, G. polynesiensis. Samples with the highest number of sequence reads identified

as G. polynesiensis were from the south east side of the island. More than 90% of the C. striatus





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486



samples contained the dinoflagellate CTX analogue CTX-3b and the highest concentrations were

found in fish from the southern side of Rarotonga. Most of the other fish species collected also

contained CTXs. Despite the decrease in reported cases of CFP in Rarotonga in recent years,

Gambierdiscus species and fish contaminated with CTXs were ubiquitous at all sites around the

island. Currently, CTXs in food sources may still pose a health risk to residents of Rarotonga.



487



Distributions and toxin production of

Gambierdiscus and Fukuyoa spp. in the

Kingdom of Tonga

Phoebe Argyle ∗ 1,2 , Lesley Rhodes 1 , Tim Harwood 1 , Tuikolongahau

Halafihi 3 , Kirsty Smith 1 , Sam Murray 1 , Islay Marsden 2

1



Cawthron Institute (Cawthron) – 98 Halifax St East, Private Bag 2, Nelson, New Zealand

2

University of Canterbury – Private Bag 4800 Christchurch 8140, New Zealand

3

Ministry of Fisheries – Vuna Road Sopu Tongatapu, Tonga



Ciguatera poisoning, an illness caused by bioaccumulation of microalgae toxins, has been

observed for many decades in nations around the Pacific. This is the first study of the causative

genera, Gambierdiscus and Fukuyoa, in the Kingdom of Tonga. Ciguatera has been reported

in Tonga for many decades but no research has yet been done into the ecology of the causative

microalgae. Data were collected at multiple sites around Tongatapu, Ha’apai and Vava’u Island groups in collaboration with the Tongan Department of Fisheries. Ecological surveys were

conducted to characterise the different habitats within the site (seagrass, macrophyte, or coral

dominant).In addition, water quality measures were taken. To assess the diversity and distribution of Gambierdiscus and Fukuyoa, microalgae samples were collected from macroalgae and via

settlement on artificial substrates. Initial results show both Gambierdiscus and Fukuyoa were

detected at all sites around Tongatapu using DNA amplification and genus-specific qPCR methods. Further species-specific assays showed multiple Gambierdiscus and Fukuyoa species present

within sites. Toxin production of clonal cultures established from live isolates was assessed using LC-MS/MS, with 3 species represented. Consistent with prior research, the G. australes

isolate produced maitotoxin and maitotoxin-3, with the G. honu and G. pacificus isolates producing only maitotoxin-3. This research has shown these toxic algae to be more prevalent than

anticipated and provides a benchmark for further studies of benthic toxic microalgae in Tonga.







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488



Effects of ciguatoxins accumulation in fish

Mireille Chinain



∗† 1



, Cl´emence Gatti 1 , Marie-Yasmine Dechraoui

Bottein 2 , Taiana Darius 1



1



2



Institut Louis Malard´e (ILM) – BP30, 98713, Papeete Tahiti, French Polynesia

International Atomic Energy Agency (IAEA) – 4a quai Antoine 1er 98000 Monaco, Monaco



Ciguatera Fish Poisoning (CFP), the most common non-bacterial seafood intoxication globally, results from the consumption of fish contaminated by lipid soluble toxins known as ciguatoxins (CTXs).

Analysis conducted in the context of human intoxication incidents or field surveys from CFP

hotspots show that wild fish can accumulate very high concentrations levels of CTXs (> 10

ng P-CTX-3C equiv. g-1 of flesh). In French Polynesia, four families of reef fish are primarily

implicated in CFP poisoning cases, namely the Scaridae, Acanthuridae, Serranidae, and Lutjanidae, which account for 50% of the 3,618 poisoning cases reported in 2007-2017. However,

the existence of spatial differences in fish toxicity within a given species combined with the fact

that fish size is not a reliable proxy for toxicity, explain the slow progress currently achieved

towards a more reliable management and prevention of CFP risk.

It is well established that algal CTXs undergo biotransformation in fish organisms (oxidative

metabolism) as they pass through the marine food chain, leading to more oxidized (and more

toxic) forms of CTXs. Still, a popular notion about ciguatera is that ciguatoxic fish in the field

do not appear to be harmed by CTXs accumulated (even at high doses) in their tissue, nor can

be identified by appearance or behavior. In this presentation, we will review past and recent

published data providing evidence that CTXs do have detrimental effects on fish, such as behavioral abnormalities, skin color variation, histological alterations, developmental toxicity, etc.,

some of which have given rise to folk tests largely used among many Pacific island communities

to detect toxic fish.

Such observations open promising research prospects aiming at the identification of potential

ciguatera disease markers (transcriptomic signatures) in fish following experimental exposure

to ecologically relevant doses of CTXs. Practical examples of this research will be presented

further in this session.









Speaker

Corresponding author: mchinain@ilm.pf



489



Experimental evidence of ciguatoxin

continued bioaccumulation in an

herbivorous coral reef fish

Rachel Clausing 1 , Barbara Losen 1 , Fran¸cois Oberhaensli 2 , Taiana

Darius 3 , Manoella Sibat 4 , Philipp Hess 5 , Mireille Chinain 3 ,

Marie-Yasmine Dechraoui Bottein ∗ 1

1



Environment Laboratories (IAEA) – 4a Quai Antoine Ier 98000 Monaco, Monaco

Radioecology Laboratory - International Atomic Energy Agency (REL - IAEA) – 4a, Quai Antoine

1er - Principality Of Monaco, Monaco

3

Institut Louis Malard´e (ILM) – BP30, 98713, Papeete Tahiti, French Polynesia

4

Laboratoire Phycotoxines (PHYC) – Institut Fran¸cais de Recherche pour l’Exploitation de la MER IFREMER, Institut Fran¸cais de Recherche pour l’Exploitation de la Mer (IFREMER) – Rue de l’Ile

d’Yeu - BP 21105 - 44311 Nantes Cedex 03, France

5

´

Institut Fran¸cais de Recherche pour lExploitation

de la Mer - Nantes (IFREMER Nantes) – Universit´e

´ - BP 21105 - 44311 Nantes Cedex 03, France

de Nantes, Universit´e de Nantes – Rue de l´Ile dYeu

2



Ciguatoxins (CTXs) produced by dinoflagellates of the genera Gambierdiscus and Fukuyoa,

are potent lipophyllic neurotoxins responsible of ciguatera poisoning in human. To study CTX

trophic transfer we developed an ecologically relevant experimental model of dietary exposure

in fish to highly toxic Gambierdiscus polynesiensis. Naso fish were fed a gel-food preparation

embedded with the CTX producing cells five days per week for 16 weeks. Measurement of

CTX levels in muscle tissue of the exposed fish showed accumulation of CTXs over time and

although tissue concentrations appeared to stabilize after 8 weeks, total tissue burden continued

to increase linearly as the fish grew. The apparent saturation in concentrations of accumulated

toxin in muscle is explained by a pronounced somatic growth dilution (fish biomass increased

by roughly 400% in 16 weeks). Toxin consumption caused no obvious intoxication over the 16

weeks period.

The observed toxin concentrations, rate of accumulation, and absence of behavioral signs of

intoxication are consistent with findings on herbivorous fish in the wild and indicate this laboratory dietary exposure accurately reflects field conditions and may be useful to develop predictive

models of tissue-specific CTX accumulation for human risk assessment.







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Ciguatoxic dinoflagellate densities and the effects of algal biomass and species composition in a Pacific coral reef, Amy Briggs [et al.]

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