A new Gambierdiscus species (Dinophyceae) from Rarotonga, Cook Islands: Gambierdiscus cheloniae sp. nov
Introduction
The genus Gambierdiscus Adachi & Fukuyo is a marine benthic dinoflagellate that is widely distributed from tropical to warm-temperate environments, and is associated with a variety of habitats including sediments, macro-algae, seagrasses and coral (Parsons et al., 2012, Hoppenrath et al., 2014). Species of Gambierdiscus are known to produce the potent neurotoxins ciguatoxin (CTX), and maitotoxin (MTX), which have been implicated as the cause of ciguatera fish poisoning (CFP) (Kohli et al., 2015). CTXs, and potentially MTXs and MTX analogues (Kohli et al., 2014), accumulate through the food web via uptake by herbivorous fishes and transfer to carnivorous fishes (Parsons et al., 2012). CFP is associated with human illnesses and even deaths in the Pacific region (Berdalet et al., 2012) and in recent years, the world’s highest incidence of CFP has been reported from Rarotonga, in the southern Cook Islands (Rongo and van Woesik, 2012). In addition to human health impacts, CFP has significant social and economic impacts; for example, in the Cook Islands the economic consequences (e.g., monitoring and management costs; health-related costs) of CFP are approximately NZ$750,000 per year and costs associated with dietary shifts from reef to pelagic fishes are estimated to be NZ$1 million per year (Rongo and van Woesik, 2012).
CFP outbreaks present a huge challenge for public health monitoring, since outbreaks are both temporally and spatially variable and CFP can occur at extremely low toxin concentrations. Gambierdiscus species are difficult to identify, and outbreaks do not always correspond directly to Gambierdiscus cell densities. Differences in the toxicity of Gambierdiscus species and strains also influence the occurrence of CFP (Kohli et al., 2015). Accurate identification of species and their associated toxicity is therefore crucial. However, such assessments have been impeded by the fact that most Gambierdiscus species are difficult to distinguish morphologically using light microscopy (LM) (Litaker et al., 2009). The Gambierdiscus genus formerly contained species exhibiting either globular or anterior-posteriorly compressed morphologies, but globular species were recently transferred to a new genus Fukuyoa Gomez, Qiu, Lopes & Lin (Gómez et al., 2015). Differences in thecal plate morphology are used to distinguish the anterior-posteriorly compressed species (Chinain et al., 1999, Fraga et al., 2011, Fraga et al., 2016, Fraga and Rodríguez, 2014, Litaker et al., 2009, Nishimura et al., 2014) but these differences can be subtle and difficult to view without scanning electron microscopy. This makes monitoring for potential CFP outbreaks very difficult. For example, the Cook Island Ministry of Marine Resources carries out monthly monitoring by LM of potentially toxic dinoflagellates at several lagoon sites around Rarotonga, but Gambierdiscus cells can only be identified as Gambierdiscus spp. (Rongo and van Woesik, 2012) and so estimates of cell concentrations include both toxic and non-toxic species.
In recent years detailed taxonomic descriptions of Gambierdiscus isolates from Rarotonga, using morphological characteristics and phylogenetic analyses, have identified several toxic species. A strain of G. polynesiensis Chinain & Faust (CAWD212) was isolated from a single environmental sample in 2013 (Rhodes et al., 2014a) and this produced described CTXs and putative MTX-3. Several strains of G. australes Chinain & Faust and G. pacificus Chinain & Faust have also been isolated and both appear to be common species found epiphytically on macro-algae in Rarotongan lagoons. Isolates of G. australes have been found to produce MTX-1 and putative MTX-3 (Rhodes et al., 2010) and G. pacificus isolates have been shown to produce putative MTX-3 only (Rhodes et al., 2014a).
In November 2014, comprehensive sampling of benthic dinoflagellates from macro-algal substrates was carried out at six selected lagoon sites around Rarotonga to identify extant benthic dinoflagellate communities. The occurrence and potential toxicity of Gambierdiscus species was a key focus and, to achieve this, samples collected directly from macro-algae were used for single cell isolations. A new Gambierdiscus species, G. cheloniae sp. nov., is described from this study.
Section snippets
Sampling, isolation and growth
Sampling was carried out in November 2014 at six selected sample sites: Muri Lagoon, Titikaveka Beach, adjacent to the Queen’s Representative residence (near Turoa Beach), the Papua Passage, adjacent to the Highland Paradise Cultural Centre and Black Rock Beach (Fig. 1). Geographic co-ordinates for each site are presented in Table 1.
Dinoflagellate cells were shaken from macro-algae (Table 1) into sealable plastic containers containing local sea water (approx. 500 mL each). Sub-samples were
Description Gambierdiscus cheloniae sp. nov. Smith, Rhodes & Murray (Figs. 2–6)
The photosynthetic cells of G. cheloniae are anteroposteriorly compressed, with mean depth (ventral to dorsal distance) measuring 59.5 ± 12.2 μm, width (transdiameter) 62.9 ± 9.0 μm, and length (apical to antapical axis measured in either ventral or dorsal view) 32.6 ± 3.7 μm. The cells are rugose, although exceptions of individual smooth cells (possibly recently divided) were observed by SEM. The apical pore is almost centrally placed (not markedly displaced) and the 2′ plate is hatchet shaped and
Conclusions
The genus Gambierdiscus currently comprises 13 species, (G. toxicus, Adachi and Fukuyo, 1979; G. belizeanus, Faust, 1995; G. pacificus, G. australes, and G. polynesiensis, Chinain et al., 1999; G. caribaeus, G. carolinianus, and G. carpenteri, Litaker et al., 2009; G. excentricus, Fraga et al., 2011; G. scabrosus, Nishimura et al., 2014; G. silvae, Fraga and Rodríguez, 2014; G. balechii, Fraga et al., 2016) including the newly described toxic species, G. cheloniae, from this study. This new
Acknowledgements
Thanks to June Hosking for assisting with sampling, field work, and accommodation; Janet Adamson and Laura Biessy for technical support at Cawthron Institute; and Krystyna Ponikla for curation of the new Gambierdiscus species in the Cawthron Institute Culture Collection of Micro-algae. Thanks also to Niki Murray, Manawatu Microscopy and Imaging Centre, Massey University, Palmerston North, New Zealand, for SEMs. Funding from the New Zealand Ministry of Business, Innovation and Employment,
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2020, Harmful AlgaeCitation Excerpt :The anticipated temperatures over the next century are expected to become more favorable for a variety of Gambierdiscus species as well. In this context, it is important to note the location of New Zealand relative to the North Meyer and Kermadec Island (28 °S) and the Cook Islands (21 °S), where two new Gambierdiscus species were recently discovered: G. honu (Rhodes et al., 2017a), and G. cheloniae from Rarotonga (Cook Islands) (Smith et al., 2016). Twelve of the fifteen described species of Gambierdiscus occur on these and other island archipelagos in the region (Rhodes et al., 2017b).
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2019, ProtistCitation Excerpt :These Chinese strains may therefore represent a novel species. Gambierdiscus cheloniae has a strong foveate to reticulate-foveate ornamentation and a narrow 2′‴ plate like G. lewisii but showed a very variable tabulation (Smith et al. 2016). Gambierdiscus lapillus has the same type of ornamentation and tabulation with a narrow 2′‴ plate like G. lewisii and thus is morphologically similar, but is distinguished based on size (Kretzschmar et al. 2017; Fig. 4A).
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Current address: Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore.