The Epiphytic Genus Gambierdiscus (Dinophyceae) in the Kermadec
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marine drugs Article The Epiphytic Genus Gambierdiscus (Dinophyceae) in the Kermadec Islands and Zealandia Regions of the Southwestern Pacific and the Associated Risk of Ciguatera Fish Poisoning Lesley L. Rhodes 1,*, Kirsty F. Smith 1, Sam Murray 1, D. Tim Harwood 1, Tom Trnski 2 and Rex Munday 3 1 Cawthron Institute, Private Bag 2, Nelson 7042, New Zealand; [email protected] (K.F.S.); [email protected] (S.M.); [email protected] (D.T.H.) 2 Auckland War Memorial Museum, Private Bag 92018, Victoria Street West, Auckland 1010, New Zealand; [email protected] 3 AgResearch, Ruakura Research Centre, 10 Bisley Road, Private Bag 3240, Hamilton 3214, New Zealand; [email protected] * Correspondence: [email protected]; Tel.: +64-(3)548-2319 Received: 17 May 2017; Accepted: 5 July 2017; Published: 11 July 2017 Abstract: Species in the genus Gambierdiscus produce ciguatoxins (CTXs) and/or maitotoxins (MTXs), which may cause ciguatera fish poisoning (CFP) in humans if contaminated fish are consumed. Species of Gambierdiscus have previously been isolated from macroalgae at Rangitahua (Raoul Island and North Meyer Islands, northern Kermadec Islands), and the opportunity was taken to sample for Gambierdiscus at the more southerly Macauley Island during an expedition in 2016. Gambierdiscus cells were isolated, cultured, and DNA extracted and sequenced to determine the species present. Bulk cultures were tested for CTXs and MTXs by liquid chromatography-mass spectrometry (LC-MS/MS). The species isolated were G. australes, which produced MTX-1 (ranging from 3 to 36 pg/cell), and G. polynesiensis, which produced neither MTX-1 nor, unusually, any known CTXs. Isolates of both species produced putative MTX-3. The risk of fish, particularly herbivorous fish, causing CFP in the Zealandia and Kermadec Islands region is real, although in mainland New Zealand the risk is currently low. Both Gambierdiscus and Fukuyoa have been recorded in the sub-tropical northern region of New Zealand, and so the risk may increase with warming seas and shift in the distribution of Gambierdiscus species. Keywords: Gambierdiscus; ciguatera fish poisoning; ciguatoxins; maitotoxin; Kermadec Islands, New Zealand 1. Introduction Gambierdiscus Adachi and Fukuyo is an epiphytic dinoflagellate genus found attached to macroalgae, dead corals and volcanic sands throughout the world’s tropical regions [1,2]. In the Pacific region, Gambierdiscus is found on macroalgae, particularly filamentous red macroalgae, coralline turfs, and the calcareous green genus, Halimeda, and on the volcanic debris that is common in the active zones. Species in the Gambierdiscus genus are the causative organisms of ciguatera fish poisoning (CFP) [2]. The toxins produced by some Gambierdiscus species include ciguatoxins (CTXs), maitotoxin (MTX) and its analogues, gambieric acids, gambieroxide, gambierol and gambierone [3]. CTXs are considered the main cause of CFP, the economic impacts of which on Pacific Island communities are just beginning to be recognized. The illness is widely under-reported and may include gastrointestinal and neurological Mar. Drugs 2017, 15, 219; doi:10.3390/md15070219 www.mdpi.com/journal/marinedrugs Mar. Drugs 20172017,, 1515,, 219219 2 of 10 gastrointestinal and neurological effects, and deaths have occurred [4,5]. Folk remedies based on the effects,local floras and are deaths used have in many occurred Pacific [4,5 ].Islands, Folk remedies and intravenous based on mannitol the local has floras been are suggested used in many as a Pacificpossible Islands, treatment and [6], intravenous although mannitol the efficacy has beenof this suggested substance as has a possible been disputed treatment [7]. [6 ],Currently, although thetreatment efficacy is of largely this substance supportive has beenand disputedsymptom-dr [7].iven, Currently, as a proven treatment antidote is largely has supportive not yet been and symptom-driven,developed for CFP as [5]. a proven antidote has not yet been developed for CFP [5]. The numbernumber ofof newnew GambierdiscusGambierdiscus speciesspecies beingbeing describeddescribed annuallyannually hashas increased.increased. At thethe beginning of 2017, fifteenfifteen species of GambierdiscusGambierdiscus had been described globally with three of these being describeddescribed in in 2016, 2016, an an increase increase of nearly of near 30%ly in30% that in one that year one [8 ].year One [8]. species, One G.species, honu, described G. honu, indescribed 2017, was in isolated 2017, was from isolated Rangitahua/North from Rangitah Meyerua/North Island, KermadecMeyer Island, Islands Kermadec [9]. Currently, Islands twelve [9]. GambierdiscusCurrently, twelvespecies Gambierdiscus of the fifteen species described of the are fifteen known described in the Pacificare known region, in althoughthe Pacific the region, CTX producer,although theG. polynesiensisCTX producer,, has G. beenpolynesiensis isolated, has much been less isolated frequently much from less samplesfrequently than from the samples MTX-1 producer,than the MTX-1G. australes producer,[8] (Figure G. australes1). [8] (Figure 1). CFP was recently recently identified identified as as a apotential potential risk risk in inthe the temperate temperate southwest southwest Pacific Pacific based based on the on theemergence emergence of G. of carpenteriG. carpenteri bloomsblooms in inthe the temperate temperate waters waters of of New New South South Wales, Wales, Australia Australia [10]. [10]. G.G. carpenteri has previously been found only in the tropicaltropical waterswaters ofof northernnorthern AustraliaAustralia and,and, whilewhile G.G. carpenteri is notnot aa CTXCTX producer,producer, otherother CTXCTX producingproducing speciesspecies may also move into this region in time. The genus Gambierdiscus and the closely related genusgenus FukuyoaFukuyoa (previously(previously transferredtransferred fromfrom the genusgenus GambierdiscusGambierdiscus) have alsoalso beenbeen reportedreported fromfrom NewNew Zealand’sZealand’s northern,northern, mainlandmainland coastalcoastal waterswaters [[11,12]11,12] andand thethe samesame potentialpotential riskrisk scenarioscenario applies.applies. Figure 1. Map of the Pacific region showing the geographic distribution of Gambierdiscus species (as Figure 1. Map of the Pacific region showing the geographic distribution of Gambierdiscus species (as of of April 2017; updated from Rhodes et al., 2017a,b [8,9]). April 2017; updated from Rhodes et al., 2017a,b [8,9]). The expected effects of climate change include changing currents and warming seas [13,14]. The risk Theof CFP expected is expected effects to of increase climate as change Gambierdiscus include changingis delivered currents to more and temperate warming regions seas [13 [10],,14]. Thewhere risk cells of CFP may is become expected adapted to increase to cooler as Gambierdiscus conditions. isAnother delivered likely to morescenario temperate is that regionscells will [10 be], wheretransported cells mayto previously become adapted temperate to cooler habitats conditions. which Anotherhave become likely scenariotropicalized is that [15]. cells A will more be transportedhaphazard way to previously that the biogeographic temperate habitats occurrence which haveof Gambierdiscus become tropicalized may expand, [15]. Aand more therefore haphazard CFP wayrisk thatoccur the in biogeographic new areas, is occurrence via rafting of pumice,Gambierdiscus followingmay expand,submerged and thereforevolcanic activity CFP risk [16]. occur For in newexample, areas, pumice is via raftingfrom the pumice, Havre following seamount submerged eruption in volcanic the Kermadec activity Islands [16]. For (2012) example, was pumicetracked Mar. Drugs 2017, 15, 219 3 of 10 from the Havre seamount eruption in the Kermadec Islands (2012) was tracked over thousands of kilometersMar. Drugs of 2017 the, 15 Pacific, 219 Ocean [17]. These rafts are not uncommon in the southwestern Pacific3 of and 10 the pumiceover isthousands often fouled of kilometers with mixed of populationsthe Pacific Ocean of flora [17]. and These fauna rafts [17]. are not uncommon in the southwesternMainland New Pacific Zealand and the ispumice situated is often on whatfouled is with now mixed considered, populations albeit of flora controversially, and fauna [17]. to be a submergedMainland geological New Zealand continent, is situated Zealandia on what [18]. Zealandiais now considered, reaches albeit (and controversially, includes) New to Caledonia be a to thesubmerged northwest, geological where continent, CFP has Zealandia been well [18]. Ze documentedalandia reaches [19 ](and and incl whereudes) NewG. toxicus Caledoniahas to been reportedthe northwest, [20,21]. where There CFP has has been been speculation well documented that CTX-like[19] and where compounds G. toxicus found has been in reported giant clams (Tridacna[20,21].spp.) There in has New been Caledonia speculation were that due CTX-like to cyanobacteria compounds [22 found], but in this giant remains clams ( hypothetical.Tridacna spp.) in Clams mayNew take Caledonia up Gambierdiscus were dueand to cyanobacteria accumulate CTX [22], [ 23but] andthis storageremains of hypothetical. toxins produced Clams by may dinoflagellates take up (forGambierdiscus example, saxitoxins) and accumulate in clam siphonsCTX [23] for extendedand storage periods of toxins of time produced is well documentedby dinoflagellates [24]. (forRangitahua example, saxitoxins) (Kermadec in Islands) clam siphons