Elsevier

Harmful Algae

Volume 60, December 2016, Pages 45-56
Harmful Algae

A new Gambierdiscus species (Dinophyceae) from Rarotonga, Cook Islands: Gambierdiscus cheloniae sp. nov

https://doi.org/10.1016/j.hal.2016.10.006Get rights and content

Abstract

Ciguatera fish poisoning (CFP) has been reported for many years in Rarotonga, Cook Islands, and has had the world’s highest reported incidence of this illness for the last 20 years. Following intensive sampling to understand the distribution of the causative organisms of CFP, an undescribed Gambierdiscus species was isolated from the Rarotongan lagoon. Gambierdiscus cheloniae sp. nov. has the common Gambierdiscus Kofoidian plate formula (except for a variability in the number of precingular plates in aberrant cells): Po, 3′, 6″ (7″), 6C?, 6 or 7S, 5′″, 1p and 2″″. The 2′ plate is hatchet shaped and the dorsal end of 1p is pointed and the relatively narrow 1p plate. Morphologically G. cheloniae is similar to the genetically closely related species G. pacificus, G. toxicus and G. belizeanus, although smaller (depth and length) than G. toxicus. The apical pore plate varies from those of G. belizeanus and G. pacificus, which are shorter and narrower, and from G. toxicus, which is larger. G. cheloniae also differs from G. pacificus in the shape of the 2′ plate. The description of this new species is supported by phylogenetic analyses using three different gene regions. G. cheloniae produced the putative maitotoxin-3 analogue, MTX-3, but neither maitotoxin or monitored ciguatoxin. Extracts of G. cheloniae were shown to be highly toxic to mice by intraperitoneal (i.p.) injection, although they were less toxic by gavage. It is possible that this species produces toxins other than putative MTX-3.

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,

References (36)

  • M.L. Richlen et al.

    Phylogeography, morphological variation and taxonomy of the toxic dinoflagellate Gambierdiscus toxicus (Dinophyceae)

    Harmful Algae

    (2008)
  • T. Rongo et al.

    Socioeconomic consequences of ciguatera poisoning in Rarotonga, southern Cook Islands

    Harmful Algae

    (2012)
  • Y. Xu et al.

    Distribution, abundance and diversity of Gambierdiscus spp. from a ciguatera-endemic area in Marakei Republic of Kiribati

    Harmful Algae

    (2014)
  • R. Adachi et al.

    The thecal structure of a marine toxic dinoflagellate Gambierdiscus toxicus gen. et sp. nov. collected in a ciguatera-endemic area

    Bull. Jpn. Soc. Sci. Fish.

    (1979)
  • E. Berdalet et al.

    Global Ecology and Oceanography of Harmful Algal Blooms, GEOHAB Core Research Project: HABs in Benthic Systems

    (2012)
  • M. Chinain et al.

    Morphology and molecular analyses of three toxic species of Gambierdiscus (Dinophyceae): G. pacificus, sp nov., G. australes, sp. nov., and G. polynesiensis, sp. nov

    J. Phycol.

    (1999)
  • M.A. Faust

    Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species

    J. Phycol.

    (1995)
  • L. Fritz et al.

    A rapid simple technique utilizing calcofluor white M2R for the visualization of dinoflagellate thecal plates

    J. Phycol.

    (1985)
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