Occurrence and seasonal variations of algal toxins in water, phytoplankton and shellfish from North Stradbroke Island, Queensland, Australia

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Abstract

A number of marine microalgae are known to produce toxins that can accumulate in shellfish and when eaten, lead to toxic and potentially fatal reactions in humans. This paper reports on the occurrence and seasonal variations of algal toxins in the waters, phytoplankton and shellfish of Southeast Queensland, Australia. These algal toxins include okadaic acid (OA), domoic acid (DA), gymnodimine (GD), pectenotoxin-2 (PTX-2) and pectenotoxin-2-seco acid (PTX-2-SA), which were detected in the sampled shellfish and phytoplankton, via HPLC-MS/MS. Dissolved OA, PTX-2 and GD were also detected in the samples collected from the water column. This was the first occasion that DA and GD have been reported in shellfish, phytoplankton and the water column in Queensland waters. Phytoplankton tows contained both the toxic Dinophysis and Pseudo-nitzschia algae species, and are suspected of being the most likely producers of the OA, PTX-2s and DA found in shellfish of this area. The number of cells, however, did not correlate with the amount of toxins present in either shellfish or phytoplankton. This indicates that toxin production by algae varies with time and the species present and that number of cells alone cannot be used as an indicator for the presence of toxins. The presence of OA and PTX-2s were more frequently seen in the summer, while DA and GD were detected throughout the year and without any obvious seasonal patterns.

Introduction

Toxic shellfish poisonings occur when algal toxins are transferred through the food chain to higher trophic levels, including humans. Diarrhetic shellfish poisoning (DSP), named after the human symptom of gastroenteritis, is one such example (Yasumoto et al., 1987, Carmody, 1996, Fernandez et al., 2006). Within DSP, there are lipophilic group of toxins: okadaic acid (OA), dinophysis toxins (DTXs) and pectenotoxins (PTXs), which are produced by dinoflagellates (Yasumoto et al., 1987, Yasumoto and Murata, 1990, Draisci et al., 1996, James et al., 1999, Fernandez et al., 2006). These toxins are harmful to humans and pose a serious threat to aquaculture industries (Fernandez, 2000). The OA group is responsible for causing diarrhoea, inhibiting protein-phosphatase enzymes and has the potential to be a tumour promoter (Fujiki, 1990, Creppy et al., 2002). Although, PTXs do not cause such diarrhoea related illnesses, they were formally placed into this group since they are commonly found with the OA (Fernandez, 2000, Creppy et al., 2002, Miles et al., 2004). To date, no records of OA have been recorded in the waters around Southeast Queensland.

Domoic acid (DA) is a toxin produced by diatoms from the genus Pseudo-nitzschia, and is known to cause amnesic shellfish poisoning (ASP) (Van Dolah, 2000, Jeffery et al., 2004). Toxic reactions to DA in humans include abdominal cramps, vomiting, diarrhoea, disorientation, short term memory loss and even death (Perl et al., 1990). It has been documented to affect, not only humans, but marine organisms such as marine mammals and sea birds (Lefebvre et al., 1999, Gulland et al., 2002, Shumway et al., 2003). Although, DA has been detected in Australia, there has not been any reported incidences of ASP in Australia (Lapworth et al., 2000).

Gymnodimine (GD) was first detected in New Zealand in 1994 (Seki et al., 1995, Stirling, 2001). This toxin is a compound produced by dinoflagellates from the genus Karenia, with Karenia selliforme being associated with the toxin in New Zealand (Seki et al., 1995, Mackenzie and Beuzenberg, 2003). Although, this compound has low toxicity when introduced orally, it is a fast acting toxin when it is injected intraperitoneally (ip) into mice (Stirling, 2001). Due to its high potency when injected into mice, GD can cause Type I errors (false positive) during mouse bioassays designed to test for paralytic and neurotoxic shellfish poisoning (Seki et al., 1995).

This study assesses the occurrence and seasonal variations of marine algal toxins in shellfish and phytoplankton collected from waters around North Stradbroke Island, located in Moreton Bay, southeastern Queensland. The waters around the island yield a variety of shellfish, some of which are consumed by the locals and sold to the public by oyster lease owners. Although, there have been no reported incidences of algal toxin poisoning around the study sites, algal blooms have been observed around the island (Osborne et al., 2001). The work presented here provides information in qualifying and quantifying the potential hazard posed by endemic forms of marine algal toxin to the consumers of the shellfish caught in these waters. In this study, OA, DA, PTX-2s and GD were detected from the sampling sites, and their exposure to the consumers was estimated.

Section snippets

Sample collection

Sampling for this study was conducted monthly for 24 consecutive months from July 2003 to June 2005, in Moreton Bay, on the east-coast of Australia (27°15 S, 153°15E) (Fig. 1). Moreton Bay is a sub-tropical, shallow coastal embayment (1.5 × 103 km2) bordered by sand barrier islands to the east (Moreton Island and North and South Stradbroke Islands). A total of six sampling sites were selected for shellfish collection and phytoplankton tows, three within Moreton Bay and three along the exposed beach

Species identification

The occurrence of Dinophysis and Pseudo-nitzschia are plotted in Fig. 2a and b. These plots indicate that Dinophysis genus was present during the warmer months and was more prominent in the open beaches than in the bay. D. caudata was more abundant in November and January 2004, with the highest concentration of 15 cells l−1 recorded from the open beaches. D. acuminata was also present between November 2004 and January 2005, and only seen on the open beaches (data not shown).

Pseudo-nitzschia, was

Discussion

The Dinophysis detected around the North Stradbroke Island were most abundant during the warmer months and thereby, displayed similar trends to other members of this genus found in other geographical locations (Hallegraeff, 2002). In this study, D. acuminata was only detected in the second year of sampling, and they were only found in late spring and summer. Similar trends were seen in Portugal, where, the presence of D. acuminata are assumed to be related to organic nutrients (Vale and

Acknowledgements

National Research Centre for Environmental Studies is funded by State of Queensland – Queensland Health, Griffith University, The University of Queensland and Queensland University of Technology. We thank the staff at Centre for Microscopy and Microanalysis at UQ and Dr. Gustaaf Hallegraeff for the TEM analysis. The DNA probe analysis for Karenia selliformis were conducted by Cawthron Institute. We also thank Lincoln MacKenzie at Cawthron Institute for kindly providing the SPATT bags.

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    Present address: National Research Centre for Environmental Toxicology, 39 Kessels Road, Coopers Plains, QLD 4108, Australia.

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