Okadaic acid accumulation in macrofilter feeders subjected to natural blooms of Dinophysis acuminata

doi:10.1016/j.hal.2007.08.001

Harmful Algae

Volume 7, Issue 2, February 2008, Pages 228-234

https://doi.org/10.1016/j.hal.2007.08.001 Get rights and content

Abstract

Thermaikos Gulf is a eutrophic area located in the Northwestern part of the Aegean Sea in the Eastern Mediterranean. Interspecific differences among various filter feeders in their ability to accumulate okadaic acid, were observed during natural blooms of Dinophysis acuminata in the gulf. Okadaic acid analyses by high performance liquid chromatography (HPLC) were performed on benthic specimens and D. acuminata cell densities and cell toxin content were estimated in water samples. Seven filter feeding species were collected in the gulf during two DSP outbreaks in May 2003 and March 2004. The various species showed a different potential to accumulate okadaic acid in their tissues. The highest concentrations were found in the mussel populations (Mytilus galloprovincialis and Modiolus barbatus), while among the non-bivalve filter feeders, ascidians were the main accumulators of okadaic acid. The rest of shellfish populations (Flexopecten proteus, Chlamys varia and Venus verrucosa) were found to contain toxins only during 2004, when D. acuminata densities were found above 10000 cells l⁻¹. M. galloprovincialis was proved to be the most appropriate indicator for a safe warning of okadaic acid contamination in Thermaikos Gulf.

Introduction

Harmful algal blooms cause severe economical losses to aquaculture and adversely impact human health. Diarrhetic Shellfish Poison (DSP) in humans causes mainly gastrointestinal symptoms as a result of eating shellfish contaminated with okadaic acid (OA) group of toxins. OA and its derivatives are powerful cytotoxins that can block dephosphorylation of proteins in mammals and plants, but very little is known regarding the effect of these compounds on marine organisms (Bauder et al., 2001). The most important DSP toxin producers belong to the genus Dinophysis, which produce toxins consisting mostly of OA and its derivatives.

Thermaikos Gulf (N. Aegean Sea, Eastern Mediterranean) is enclosed and eutrophic, with reduced water flux, receiving high nutrient inputs from rivers, urban and industrial runoff (Gotsis-Skretas and Friligos, 1990, Balopoulos and Friligos, 1993, Moncheva et al., 2001). The shellfish farming activity in this area represents about 85% of the total production in Greece (€10 million annually; Zanou and Anagnostou, 2001), with 70–80% of the product exported (Karageorgis et al., 2005). Mussel rafts increase water stability and water residence time, and create microhabitats favouring dinoflagellate growth (Granéli et al., 1998). Many sources of nutrients such as sewage and animal wastes, agricultural and fertilizer runoff, as well as the growing aquaculture industry in coastal areas, can also contribute to stimulate harmful algal blooms (Anderson et al., 2002).

In Thermaikos Gulf since 2000, DSP outbreaks have been confirmed and the causative organism has been identified as Dinophysis acuminata. The most serious HAB event was recorded during the winter of 2000, when D. acuminata reached 8.5 × 10⁴ cells l⁻¹ at the end of January (Koukaras and Nikolaidis, 2004). During each bloom period (usually early spring), mussel cultures remain closed to harvest, resulting in a substantial socio-economic impact in the area (economic losses of ∼€3 million annually) (Karageorgis et al., 2005).

As filter feeder animals gather food by filtering the water, contamination with DSP toxins occurs after their feeding on toxic Dinophysis cells. The filtering capacity of the filter feeding communities may play an important role on the control of phytoplankton blooms (Granéli et al., 1998, Cloern, 2001). The accumulation of OA, which D. acuminata mainly produces (Vale et al., 1998), has been until now studied in shellfish populations, while for other benthic groups (ascidians and polychaetes), to our knowledge there is no available information in the published literature.

Two successive annual DSP toxin outbreaks in Thermaikos Gulf presented an opportunity to (1) assess, determine and compare the amounts of free okadaic acid in different filter feeding species naturally contaminated by D. acuminata; and (2) identify the most appropriate species to be used as an indicator of DSP contamination in the Gulf, as a tool in the shellfish stocks management in DSP-affected areas, such as Thermaikos Gulf.

Section snippets

Description of the study area

The investigation area, Thermaikos Gulf, is located in the nortwestern part of the Aegean Sea (Fig. 1). Five major and several minor rivers flow into the gulf, introducing significant amounts of particulate matter and nutrient loads (Lykousis and Chronis, 1989, Friligos et al., 1997, Karageorgis et al., 2005). The city of Thessaloniki, with its partly untreated domestic sewage effluents and adjacent industrial zone, contributes to the eutrophication of the Gulf (Anagnostou et al., 1997). The

Results

Fig. 2 illustrates the spatial and vertical distribution of D. acuminata cell densities and their cellular toxin content during the blooms of May 2003 and March 2004.

In May 2003, D. acuminata cell densities varied from 500 cells l⁻¹ in stations DA3 and TP7 to 2200 cells l⁻¹ at station TP2 and the average OA intracelullar concentrations in D. acuminata varied from 3.7 to 8.6 pg cell⁻¹ (Fig. 2).

The highest D. acuminata cell densities were recorded during March 2004. Cell densities ranged from 600 cells l

Discussion

The intense toxic bloom of March 2004 in Thermaikos Gulf was associated with an increased OA accumulation in animal tissues and also a higher number of filter feeding species found to be contaminated, in comparison to the toxic bloom of 2003. During both toxic blooms, D. acuminata cell densities in the mussel culture area (st. DA3) were generally comparable, indicating that mussels are effective filter feeders and their dense populations, are able to reduce/or control Dinophysis cell densities.

Acknowledgements

We thank I. Varkintzi, A. Gremmenas and S. Mitsoudi for their help during the field surveys in Thermaikos Gulf. Financial support was provided by the European Commission through the FATE project “Transfer and Fate of Harmful Algal Bloom (HAB) Toxins in European Marine Waters” (contract EVK3-CT01-00055) as part of the EC-EUROHAB cluster.[SS]

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Okadaic acid accumulation in macrofilter feeders subjected to natural blooms of Dinophysis acuminata

Abstract

Introduction

Section snippets

Description of the study area

Results

Discussion

Acknowledgements

Mar. Geol.

Toxicon

Estuar. Coast. Shelf Sci.

Aquat. Toxicol.

Aquat. Toxicol.

Toxicon

Harmful Algae

Toxicon

Toxicon

Harmful Algae

Mar. Pollut. Bull.

Environmental impact on the surface sediments of the bay and the gulf of Thessaloniki according to the Geoaccumulation Index classification

Harmful algal blooms and eutrophication: nutrient sources, composition and consequences

Estuaries

Water circulation and eutrophication in the North-West Aegean Sea: Thermaikos Gulf

J. Environ. Sci. Health A

Uptake and fate of diarrhetic shellfish poisoning toxins from the dinoflagellate Prorocentrum lima in the bay scallop Argopecten irradians

Mar. Ecol. Prog. Ser.