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Blooms and Biotoxins

• Reviews
• Environmental Change
• Environmental/Ecological Impacts
• Bloom Events
• Biotoxins: Human Health
• Biotoxins: Detection and Identification
• Bloom Management and Control

Reviews

• Lopes, V.R. and Vasconcelos, V.M.  Planktonic and benthic cyanobacteria of European brackish waters: a perspective on estuaries and brackish seas.  European Journal of Phycology 46(3): 292-304, 2011.  
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  Cyanobacteria are photosynthetic organisms found in aquatic and terrestrial biotopes and ecosystems throughout the world. Marine and freshwater cyanobacteria have been extensively studied due to the toxic hazards that some of them create and biotechnological interest. In contrast, the cyanobacteria of brackish waters have been less studied despite being able to form toxic blooms like their freshwater and marine counterparts. We review the occurrence, diversity and toxicity of cyanobacteria species in the brackish waters of Europe, mainly estuaries and brackish environments of the Atlantic Ocean and the Mediterranean and Baltic Seas. The dominant cyanobacteria belong mainly to the planktonic genera Nodularia, Aphanizomenon, Microcystis and Anabaena, but also the benthic forms of Anabaena and Phormidium. Most genera from brackish waters are reported to be hepatotoxin producers (microcystin and nodularin). However, anatoxin-a and other bioactive compounds (e.g. apoptogens) can also be found and are produced exclusively by benthic forms. Nodularin is the best-characterized brackish-water cyanotoxin, being primarily produced by N. spumigena. Data are presented on cyanotoxin production, accumulation, and potential food chain transfer, with a particular focus on nodularin, which induces multiple effects on food-chain dynamics. Microcystins and anatoxin-a are also considered. Potential risks to animals and humans from cyanotoxin exposure are discussed, although reports of animal poisoning by brackish-water toxic cyanobacteria are scarce and no cases of human intoxication are yet known.

Environmental Change

• Walsh, J.J., Tomas, C.R., Steidinger, K.A., Lenes, J.M., Chen, F.R., Weisberg, R.H., Zheng, L., Landsberg, J.H., Vargo, G.A., and Heil, C.A.  Imprudent fishing harvests and consequent trophic cascades on the West Florida shelf over the last half century: A harbinger of increased human deaths from paralytic shellfish poisoning along the southeastern United States, in response to oligotrophication?  Continental Shelf Research 31(9): 891-911, 2011.  
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  Within the context of ubiquitous overfishing of piscivores, recent consequent increments of jellyfish and clupeids have occurred at the zooplanktivore trophic level in the eastern Gulf of Mexico (GOM), after overfishing of one of their predators, i.e. red snapper. Initiation of a local trophic cascade thence led to declines of herbivore stocks, documented here on the West Florida shelf. These exacerbating world-wide trophic cascades have resulted in larger harmful algal blooms (HABs), already present at the base of most coastal food webs. Impacts on human health have thus far been minimal within nutrient-rich coastal regions. To provide a setting for past morbidities, consideration is given to chronologies of other trophic cascades within eutrophic, cold water marine ecosystems of the Scotian Sea, in the Gulf of Alaska, off Southwest Africa, within the Barents, White, and Black Seas, in the Gulf of Maine, and finally in the North Sea. Next, comparison is now made here of recent ten-fold increments within Florida waters of both relatively benign and saxitoxic HABs, some of which are fatal to humans. These events are placed in a perspective of other warm shelf systems of the South China and Caribbean Seas to assess prior and possible future poison toxicities of oligotrophic coastal habitats. Past wide-spread kills of fishes and sea urchins over the Caribbean Sea and the downstream GOM are examined in relation to the potential transmission of dinoflagellate saxitoxin and other epizootic poison vectors by western boundary currents over larger "commons" than local embayments. Furthermore, since some HABs produce more potent saxitoxins upon nutrient depletion, recent decisions to ban seasonal fertilizer applications to Florida lawns may have unintended consequences. In the future, human-killing phytoplankton, rather than relatively benign fish-killing HABs of the past, may be dispersed along the southeastern United States seaboard.

• Gobler, C.J., et al.  Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics.  Proceedings of the National Academy of Sciences [USA] 108(11): 4352-4357, 2011.
  Open Access >>
  Read Abstract >>

  Harmful algal blooms (HABs) cause significant economic and ecological damage worldwide. Despite considerable efforts, a comprehensive understanding of the factors that promote these blooms has been lacking, because the biochemical pathways that facilitate their dominance relative to other phytoplankton within specific environments have not been identified. Here, biogeochemical measurements showed that the harmful alga Aureococcus anophagefferens outcompeted co-occurring phytoplankton in estuaries with elevated levels of dissolved organic matter and turbidity and low levels of dissolved inorganic nitrogen. We subsequently sequenced the genome of A. anophagefferens and compared its gene complement with those of six competing phytoplankton species identified through metaproteomics. Using an ecogenomic approach, we specifically focused on gene sets that may facilitate dominance within the environmental conditions present during blooms. A. anophagefferens possesses a larger genome (56 Mbp) and has more genes involved in light harvesting, organic carbon and nitrogen use, and encoding selenium-and metal-requiring enzymes than competing phytoplankton. Genes for the synthesis of microbial deterrents likely permit the proliferation of this species, with reduced mortality losses during blooms. Collectively, these findings suggest that anthropogenic activities resulting in elevated levels of turbidity, organic matter, and metals have opened a niche within coastal ecosystems that ideally suits the unique genetic capacity of A. anophagefferens  and thus, has facilitated the proliferation of this and potentially other HABs.

• Van de Waal, D.B., Verspagen, J.M.H., Finke, J.F., Vournazou, V., Immers, A.K., Kardinaal, W.E.A., Tonk, L., Becker, S., Van Donk, E., Visser, P.M., and Huisman, J.  Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO₂.  ISME Journal 5(9): 1438-1450, 2011.
  Open Access >>   
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  Climate change scenarios predict a doubling of the atmospheric CO₂ concentration by the end of this century. Yet, how rising CO₂ will affect the species composition of aquatic microbial communities is still largely an open question. In this study, we develop a resource competition model to investigate competition for dissolved inorganic carbon in dense algal blooms. The model predicts how dynamic changes in carbon chemistry, pH and light conditions during bloom development feed back on competing phytoplankton species. We test the model predictions in chemostat experiments with monocultures and mixtures of a toxic and non-toxic strain of the freshwater cyanobacterium Microcystis aeruginosa. The toxic strain was able to reduce dissolved CO₂ to lower concentrations than the non-toxic strain, and became dominant in competition at low CO₂ levels. Conversely, the non-toxic strain could grow at lower light levels, and became dominant in competition at high CO₂ levels but low light availability. The model captured the observed reversal in competitive dominance, and was quantitatively in good agreement with the results of the competition experiments. To assess whether microcystins might have a role in this reversal of competitive dominance, we performed further competition experiments with the wild-type strain M. aeruginosa PCC 7806 and its mcyB mutant impaired in microcystin production. The microcystin-producing wild type had a strong selective advantage at low CO₂ levels but not at high CO₂ levels. Our results thus demonstrate both in theory and experiment that rising CO₂ levels can alter the community composition and toxicity of harmful algal blooms.

• Keesing, J.K., Liu, D., Fearns, P., and Garcia, R.  Inter- and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007-2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China.  Marine Pollution Bulletin 62(6): 1169-1182, 2011.
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  The large green-tide events that occurred in the Yellow Sea in 2008 (3489 km²) and 2009 (4994 km²) are shown to be novel events preceded only once by a much smaller event in 2007 (82 km²). The blooms originated in the coastal area of Jiangsu province and spread north-east towards the Shandong Peninsula. The blooms grew at different rates and mesoscale variability in surface winds explained the differences in the spatial and temporal patterns of blooms in 2008 and 2009. The 2009 bloom was tracked to its origin immediately offshore of extensive intertidal flats between Yancheng and Nantong where recent rapid expansion of Porphyra aquaculture has occurred. We review published hypotheses which have been advanced to explain the occurrence of blooms and in light of our findings, we conclude that the accumulation and disposal of waste Ulva prolifera from Porphyra aquaculture rafts is the most likely cause of the blooms.

• Moore, S.K., Mantua, N.J., and Salathé, E.P.  Past trends and future scenarios for environmental conditions favoring the accumulation of paralytic shellfish toxins in Puget Sound shellfish.  Harmful Algae 10(5): 521-529, 2011.
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  The risk of harmful algal blooms (HABs) of the dinoflagellate Alexandrium catenella in Puget Sound, Washington State, can be assessed by identifying and predicting climate and environmental conditions that are favorable for bloom development and the accumulation of paralytic shellfish toxins (PSTs) in shellfish. When these favorable conditions occur in combination, a harmful algal bloom window of opportunity (HAB-WOO) exists for A. catenella. The original HAB-WOO was identified by Moore et al. (2009) for the time period 1993-2007. In general, it showed that warm air and water temperatures, low streamflow, low winds, and small tidal variability precede PST events. Here, we use the HAB-WOO model to examine (i) changes in the annual HAB-WOO duration over the period from 1967 to 2006, and (ii) the potential effect of future climate change on HAB risk through the late 21st century. The annual HAB-WOO duration increased between 1978 and 2006, as did the frequency and geographic extent of PST events. Two step-like changes occurred in 1978 and 1992 with higher annual values attained by the HAB-WOO compared to previous years. The 1978 step change may be related to the 1977 reversal of the Pacific Decadal Oscillation from cool to warm phase. Climate change projections from global climate models and regionally downscaled climate models for the Pacific Northwest are used to evaluate scenarios for the future HAB-WOO. Under a moderate greenhouse gas emissions scenario (i.e., A1B), the annual HAB-WOO for A. catenella in Puget Sound is projected to increase by an average of 13 days by the end of the 21st century. Furthermore, the annual HAB-WOO may begin up to 2 months earlier in the year and persist for up to 1 month later in the year compared to the present day. This research provides managers, health authorities, and shellfish growers in Washington State with critical information for anticipating climate impacts on toxic HABs in the Pacific Northwest now and in a future warmer climate.

• Ye, N., Zhang, X., Mao, Y., Liang, C., Xu, D., Zou, J., Zhuang, Z., and Wang, Q.  'Green tides' are overwhelming the coastline of our blue planet: taking the world's largest example.  Ecological Research 26(3): 477-485, 2011.
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  A broad spectrum of events that come under the category of green tide are recognized world-wide as a response to elevated levels of seawater nutrients in coastal areas. Green tides involve a wide diversity of sites, macroalgal species, consequences, and possible causes. Here we review the effect of natural and man-induced environmental fluctuations on the frequency and apparent spread of green tides. This article highlights the need for interdisciplinary research aimed at shedding light on the basic mechanisms governing the occurrence and succession of green algae in coastal seas. This will result in more effective management and mitigation of the effects of green tides, thus safeguarding the intrinsic and commercial value of coastal marine ecosystems.

Environmental/Ecological Impacts

• Bottein, M.-Y.D., Kashinsky, L., Wang, Z., Littnan, C., and Ramsdell, J.S.  Identification of ciguatoxins in Hawaiian monk seals Monachus schauinslandi from the Northwestern and Main Hawaiian Islands.  Environmental Science and Technology 45(12): 5403-5409, 2011.  
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  Ciguatoxins are potent algal neurotoxins that concentrate in fish preyed upon by the critically endangered Hawaiian monk seal (Monachus schauinslandi). The only report for Hawaiian monk seal exposure to ciguatoxins occurred during a 1978 mortality event when two seal liver extracts tested positive by mouse bioassay. Ciguatoxins were thus proposed as a potential threat to the Hawaiian monk seal population. To reinvestigate monk seal exposure to ciguatoxins we utilized more selective detection methods, the Neuro-2A cytotoxicity assay, to quantify ciguatoxin activity and an analytical method LC-MS/MS to confirm the molecular structure. Tissue analysis from dead stranded animals revealed ciguatoxin activity in brain, liver, and muscle, whereas analysis of blood samples from 55 free-ranging animals revealed detectable levels of ciguatoxin activity (0.43 to 5.49 pg/mL P-CTX-1 equiv) in 19% of the animals. Bioassay-guided LC fractionation of two monk seal liver extracts identified several ciguatoxin-like peaks of activity including a peak corresponding to the P-CTX-3C which was confirmed present by LC-MS/MS. In conclusion, this work provides first confirmation that Hawaiian monk seals are exposed to significant levels of ciguatoxins and first evidence of transfer of ciguatoxin to marine mammals. This threat could pose management challenges for this endangered marine mammal  species.

• Fire, S.E., Wang, Z.H., Byrd, M., Whitehead, H.R., Paternoster, J., and Morton, S.L.  Co-occurrence of multiple classes of harmful algal toxins in bottlenose dolphins (Tursiops truncatus) stranding during an unusual mortality event in Texas, USA.  Harmful Algae 10(3): 330-336, 2011.
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  During February-April 2008, an unusual mortality event occurred in Texas coastal waters that resulted in over 100 bottlenose dolphin (Tursiops truncatus) deaths. This mortality event overlapped spatially and temporally with a harmful algal bloom (HAB) composed of the toxin-producing genera Dinophysis spp. and Prorocentrum spp., and was associated with shellfish bed closures due to HAB toxins. A bloom of the toxin-producing diatom Pseudo-nitzschia pungens was also detected in Texas coastal waters in early April, towards the end of the dolphin mortality event. Analysis of dolphin gastrointestinal contents collected during this event demonstrated the presence of the HAB toxins domoic acid and okadaic acid in association with these blooms, as well as evidence of brevetoxin exposure in the absence of an associated K. brevis bloom. Historical dolphin stranding data for Texas waters indicate seasonal stranding peaks similar to the present study, indicating a need for investigating potential HAB involvement in mass strandings in previous years and in future events. This study marks the first reported occurrence of okadaic acid in marine mammals, and documents a unique co-occurrence of multiple HAB toxins associated with an unusual mortality event. Texas waters harbor a high diversity of HAB events relative to other coastal regions, and this study highlights the importance of efforts to understand the impacts of such HAB events on the health of Texas marine wildlife.

• Sopanen, S., Setälä, O., Piiparinen, J., Erler, K., and Kremp, A.  The toxic dinoflagellate Alexandrium ostenfeldii promotes incapacitation of the calanoid copepods Eurytemora affinis and Acartia bifilosa from the northern Baltic Sea.  Journal of Plankton Research 33(10): 1564-1573, 2011.   
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  Dense localized blooms of the toxic dinoflagellate Alexandrium ostenfeldii are a recent phenomenon in the low salinity waters of the Baltic Sea. This study reports results from laboratory experiments investigating the interaction between PSP toxin producing strains of A. ostenfeldii and two copepod species, Eurytemora affinis and Acartia bifilosa, from the northern Baltic Sea. Copepod grazing rates were studied by incubating the copepods with mixed cultures of A. ostenfeldii isolated from a bloom area. The effect of A. ostenfeldii on copepod condition and behavior was studied by exposing copepods to the mixed cultures and cell-free filtrates. Grazing on A. ostenfeldii cells was negligible for both copepod species. The 24 h incapacitation incubations indicated that the condition of both copepod species was negatively affected by the presence of A. ostenfeldii. The behavioral changes observed took place during the first hours of exposure to A. ostenfeldii cells, and little or no change was observed in the condition of the copepods after 6 h compared to 24 h. Similar observations were made for E. affinis incubated in cell-free filtrates of A. ostenfeldii, while the response of A. bifilosa was less pronounced. Our study shows that the copepods do not graze on A. ostenfeldii due to rapid behavioral disturbance and incapacitation by the algal cells and their exudates. This represents the first observation of a negative effect of the A. ostenfeldii on co-occurring biota in the northern Baltic Sea.

Bloom Events

• Álvarez, G., Uribe, E., Díaz, Rosario, Braun, M., Mariño, C., and Blanco, J.  Bloom of the yessotoxin producing dinoflagellate Protoceratium reticulatum (Dinophyceae) in Northern Chile.  Journal of Sea Research 65(4): 427-434, 2011.  
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  In summer 2007, a dinoflagellate preliminarily identified as Protoceratium reticulatum bloomed in Bahía Mejillones, northern Chile. Phytoplankton samples were analyzed in detail by light and scanning electron microscopy revealing the presence of resting cyst and motile cells of P. reticulatum. Oceanographic and phytoplankton data suggest that the bloom was initiated offshore by motile cells and germinated cysts during an upwelling pulse. These cells were advected into the bay when upwelling relaxed and grew without any relevant competitor. Phytoplankton net samples were found to contain yessotoxin as the only toxin in an estimated proportion of 0.2 and 0.4 pg cell^-1, thus confirming that P. reticulatum is a source of yessotoxin in northern Chilean waters and consequently that it poses a risk for human health and mollusk exploitation in the area.

• Accoroni, S. et al.  Ostreopsis cf. ovata bloom in the northern Adriatic Sea during summer 2009: Ecology, molecular characterization and toxin profile.  Marine Pollution Bulletin 62(11): 2512-2519, 2011.
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  Intense blooms of the benthic dinoflagellate Ostreopsis cf. ovata have occurred in the northern Adriatic Sea since 2006. These blooms are associated with noxious effects on human health and with the mortality of benthic organisms because of the production of palytoxin-like compounds. The O. cf. ovata bloom and its relationships with nutrient concentrations at two stations on the Conero Riviera (northern Adriatic Sea) were investigated in the summer of 2009. O. cf. ovata developed from August to November, with the highest abundances in September (1.3 × 10⁶ cells g-1 fw corresponding to 63.8 × 10³ cells cm^-2). The presence of the single O. cf. ovata genotype was confirmed by a PCR assay. Bloom developed when the seawater temperature was decreasing. Nutrient concentrations did not seem to affect bloom dynamics. Toxin analysis performed by high resolution liquid chromatography–mass spectrometry revealed a high total toxin content (up to 75 pg cell^-1), including putative palytoxin and all the ovatoxins known so far.

• Maric, D., Ljubešic, Z., Godrijan, J., Vilicic, D., Ujevic, I., and Precali, R.  Blooms of the potentially toxic diatom Pseudo-nitzschia calliantha Lundholm, Moestrup & Hasle in coastal waters of the northern Adriatic Sea (Croatia).  Estuarine, Coastal and Shelf Science 92(3): 323-331, 2011.  
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  The genus Pseudo-nitzschia contains more than 30 species, though most of them are discernible only on the basis of ultrastructural or genetic differences. We present a taxonomic study of Pseudo-nitzschia calliantha Lundhum, Hasle & Moestrup in the coastal waters of the northern Adriatic Sea together with domoic acid (DA) measurements on natural and breeding populations of shellfish. Sampling carried out monthly at 13 stations during 2007 showed Pseudo-nitzschia species to be present with high abundances during the entire year, forming blooms in coastal waters (reaching abundances of up to 1.2 × 10⁶ cells L^-1) during the late summer/early autumn, when they contributed up to 70% of the whole phytoplankton community. Ultrastructural examination provided evidence that the observed blooms were formed by the potentially toxic species P. calliantha. After the P. calliantha bloom, DA was detected at 3 stations along the north-eastern Adriatic coast with concentrations ranging from 0.11 to 1.32 μg g^-1 in shellfish tissue. The distribution patterns of the species were analyzed statistically in order to explain the relationships between environmental variables and population dynamics. We here report on a mass appearance of the potentially toxic P. calliantha in the coastal waters of the northern Adriatic.

Biotoxins: Human Health

• Paredes, I., Rietjens, I.M.C.M., Vieites, J.M., and Cabado, A.G.  Update of risk assessments of main marine biotoxins in the European Union.  Toxicon 58(4): 336-354, 2011.
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  This review is an up-to-date compilation of the available literature, including scientific papers, reviews, and EFSA's opinions, on toxicity and risk assessment data on the main marine biotoxins of importance in the European Union, including the legislated ones and the ones of recent appearance which are not legislated. Information about the hazard identification and hazard characterisation of okadaic acid, dynophysistoxins, pectenotoxins, yessotoxins, azaspiracids, domoic acid, saxitoxins, tetrodotoxins, brevetoxins, ciguatoxins, cyclic imines and palytoxins is reviewed and presented in the form of a collection of risk assessments. It is concluded that the importance of having an appropriate exposure assessment reiterates the urgency of establishing a database with representative and comparable data on exposure to food items possiby containing marine biotoxins. It is also concluded that a revision of the present regulation of marine biotoxins in the EU legislation could be considered, as some regulated toxins have been shown not to pose a risk for EU's population (as yessotoxin) and some non regulated toxins have been shown to be harmful and/or to occur in the EU (as tetrodotoxin, palytoxin, and some cyclic imines) while they are not regulated.

• Hinder, S.L., Hays, G.C., Brooks, C.J., Davies, A.P., Edwards, M., Walne, A.W., and Gravenor, M.B.  Toxic marine microalgae and shellfish poisoning in the British isles: history, review of epidemiology, and future implications.  Environmental Health 10: art. 54, 2011.
  Open Access >>   
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  The relationship between toxic marine microalgae species and climate change has become a high profile and well discussed topic in recent years, with research focusing on the possible future impacts of changing hydrological conditions on Harmful Algal Bloom (HAB) species around the world. However, there is very little literature concerning the epidemiology of these species on marine organisms and human health. Here, we examine the current state of toxic microalgae species around the UK, in two ways: first we describe the key toxic syndromes and gather together the disparate reported data on their epidemiology from UK records and monitoring procedures. Secondly, using NHS hospital admissions and GP records from Wales, we attempt to quantify the incidence of shellfish poisoning from an independent source. We show that within the UK, outbreaks of shellfish poisoning are rare but occurring on a yearly basis in different regions and affecting a diverse range of molluscan shellfish and other marine organisms. We also show that the abundance of a species does not necessarily correlate to the rate of toxic events. Based on routine hospital records, the numbers of shellfish poisonings in the UK are very low, but the identification of the toxin involved, or even a confirmation of a poisoning event is extremely difficult to diagnose. An effective shellfish monitoring system, which shuts down aquaculture sites when toxins exceed regularity limits, has clearly prevented serious impact to human health, and remains the only viable means of monitoring the potential threat to human health. However, the closure of these sites has an adverse economic impact, and the monitoring system does not include all toxic plankton. The possible geographic spreading of toxic microalgae species is therefore a concern, as warmer waters in the Atlantic could suit several species with southern biogeographical affinities enabling them to occupy the coastal regions of the UK, but which are not yet monitored or considered to be detrimental.

• Picot, C., Nguyen, T.A., Roudot, A.C., and Parent-Massin, D.  A preliminary risk assessment of human exposure to phycotoxins in shellfish: A review.  Human and Ecological Risk Assessment 17(2): 328-366, 2011.
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  Over the past few decades, phycotoxins, secondary metabolites produced by toxic phytoplankton, have seen an increase in their frequency, concentrations, and geographic distribution. As shellfish accumulate phycotoxins making them unfit for human consumption, they are considered as an important food safety issue. Thus, a consumer exposure assessment on phycotoxins is necessary. Exposure assessment requires two types of information: contamination and consumption data. Shellfish contamination data on major toxins encountered by at-risk populations (Domoic Acid group, Okadaic Acid group, and Saxitoxin group) have been reviewed. Consumption data have been reviewed for both general and potential high-consumer populations. Then, we undertook acute and chronic exposure assessments, combining available French contamination data and our own consumption data. Studies including exposure assessment were then reviewed. Lastly, risk characterization was undertaken. It can be concluded that both acute and chronic exposure to phycotoxins via shellfish consumption is a matter of concern, mainly for high consumers identified in this review (specific populations and shellfish harvesters). However, the results for risk characterization must be improved. There is a need for (i) toxicological data to establish a Tolerable Daily Intake; (ii) an assessment of consumption and contamination data, undertaken at the same time, so as to assess exposure.

• Rongo, T. and van Woesik, R.  Ciguatera poisoning in Rarotonga, southern Cook Islands.  Harmful Algae 10(4): 345-355, 2011.
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  The central Pacific Ocean has arguably more ciguatera poisoning than any other place on earth. Here we tested two competing hypotheses that outline the primary causes of ciguatera outbreaks: (1) the 'new surface hypothesis' and (2) the 'climate oscillation hypothesis'. Our findings indicated that in Rarotonga, from 1994 to 2010, the annual incidence of ciguatera poisoning ranged from 204 to 1,058 per 10,000 population per year. We found that the widest reefs of Rarotonga elicited the most cases of ciguatera poisoning, but found no relationship between ciguatera outbreaks and reef exposure. We also found strong correlations between cases of ciguatera poisoning and (i) the positive phase of the Pacific Decadal Oscillation, (ii) El Niño years, and (iii) periods with frequent disturbances. Yet, most disturbances occurred during the above-mentioned climate phases. This study links the two supposedly, mutually exclusive hypotheses. Moreover, as predicted by the 'climate oscillation hypothesis', the Pacific Ocean is now, in 2010, experiencing a negative phase of the Pacific Decadal Oscillation, and Rarotonga is reporting few cases of ciguatera poisoning.

• Noguchi, T., Miyazawa, K., Daigo, K., and Arakawa, O.  Paralytic shellfish poisoning (PSP) toxin- and/or tetrodotoxin-contaminated crabs and food poisoning by them.  Toxin Reviews 30(4): 91-102, 2011.
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  Outbreaks of human intoxication by toxic crabs have been reported in various parts of the world. Sporadic outbreaks of intoxication in humans and domestic animals due to ingestion of the toxic crab have especially occurred in the Ryukyu Islands, Japan. Using a screening test for toxic crabs, 1000 specimens of 72 species in the family Xanthidae were tested for toxicity and Zosimus aeneus, Atergatis floridus and Platypodia granulosa were found to be toxic. The toxin was confirmed to be identical to saxitoxin (STX). It was later confirmed that there are great individual and regional variations in toxicity and the toxin varies with exposure of the toxic crab to Paralytic Shellfish Poisoning (PSP) toxin and/or tetrodotoxin (TTX). Edible crabs "Togekurigani" (Telmessus acutidens) and "Ishigani" (Charybdis japonica) were contaminated with PSP for a short time in 2003, in Japan. The mechanism of PSP intoxication was shown to be the food chain by feeding PSP-contaminated bivalves. However, in the case of toxic xanthid crabs, which are not plankton feeders, the conclusions were uncertain. This review describes the occurrence, causative agents and intoxication mechanisms for food poisoning by toxic crabs containing PSP or TTX or other marine toxins, either alone or mixed.

Biotoxins: Detection and Identification

• Honsell, G., De Bortoli, M., Boscolo, S., Dell-Aversano, C., Battocchi, C., Fontanive, G., Penna, A., Berti, F., Sosa, S., Yasumoto, T., Ciminiello, P., Poli, M., and Tubaro, A.  Harmful dinoflagellate Ostreopsis cf. ovata Fukuyo: Detection of ovatoxins in field samples and cell immunolocalization using antipalytoxin antibodies.  Environmental Science and Technology 45(16): 7051-7059, 2011.  
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  Ostreopsis cf. ovata, a benthic dinoflagellate often blooming along the Mediterranean coasts, has been associated with toxic events ranging from dyspnea to mild dermatitis. In late September 2009, an Ostreopsis cf. ovata bloom occurred in the Gulf of Trieste (Northern Adriatic Sea; Italy), causing pruritus and mild dermatitis in beachgoers. An integrated study was initiated to characterize Ostreopsis cells by light and confocal microscopy, PCR techniques, immunocytochemistry, and high resolution liquid chromatography-mass spectrometry (HR LC-MS). The presence of Ostreopsis cf. ovata of the Atlantic/Mediterranean clade was unambiguously established by morphological and genetic analyses in field samples. Several palytoxin-like compounds (ovatoxin-a,-b,-c,-d,-e) were identified by HR LC-MS, ovatoxin-a being the most abundant (45-64 pg/cell). Surprisingly, no palytoxin was detected. For the first time, monoclonal and polyclonal antipalytoxin antibodies revealed the intracellular cytoplasmic localization of ovatoxins, suggesting their cross-reactivity with these antibodies. Since harmful dinoflagellates do not always produce toxins, the immunocytochemical localization of ovatoxins, although qualitative, can provide an early warning for toxic Ostreopsis cells before their massive diffusion and/or concentration in seafood.

• Schock, T.B., Huncik, K., Beauchesne, K.R., Villareal, T.A., and Moeller, P.D.R.  Identification of trichotoxin, a novel chlorinated compound associated with the bloom forming cyanobacterium, Trichodesmium thiebautii.  Environmental Science and Technology 45(17): 7503-7509, 2011.
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  Trichodesmium is a suspected toxin-producing nonheterocystous cyanobacteria ubiquitous in tropical, subtropical, and temperate seas. The genus is known for its ability to fix nitrogen and form massive blooms. In oligotrophic seas, it can dominate the biomass and be a major component of oceanic primary production and global nitrogen cycling. Numerous reports suggest Trichodesmium-derived toxins are a cause of death of fish, crabs, and bivalves. Laboratory studies have demonstrated neurotoxic effects in T. thiebautii cell extracts and field reports suggest respiratory distress and contact dermatitis of humans at collection sites. However, Trichodesmium toxins have not been identified and characterized. Here, we report the extraction of a lipophilic toxin from field-collected T. thiebautii using a purification method of several chromatographic techniques, nuclear magnetic resonance (NMR), mass spectroscopy (MS), and Fourier transformed-infrared spectroscopy (FT-IR). Trichotoxin has a molecular formula of C₂₀H₂₇ClO and a mass of 318 m/z and possesses cytotoxic activity against GH₄C₁ rat pituitary and Neuro-2a mouse neuroblastoma cells. A detection method using liquid chromatography/mass spectrometry (LC/MS) was developed. This compound is the first reported cytotoxic natural product isolated and fully characterized from a Trichodesmium species.

• Salas, R., Tillmann, U., John, U., Kilcoyne, J., Burson, A., Cantwell, C., Hess, P., Jauffrais, T., and Silke, J.  The role of Azadinium spinosum (Dinophyceae) in the production of azaspiracid shellfish poisoning in mussels.  Harmful Algae 10(6): 774-783, 2011.   
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  Azaspiracids (AZAs) are a group of lipophilic polyether compounds first detected in Ireland which have been implicated in shellfish poisoning incidents around Europe. These toxins regularly effect shellfish mariculture operations including protracted closures of shellfish harvesting areas for human consumption. The armoured dinoflagellate Azadinium spinosum Elbrächter et Tillmann gen. et sp. nov. (Dinophyceae) has been described as the de novo azaspiracid toxin producer; nonetheless the link between this organism and AZA toxin accumulation in shellfish has not yet been established. In August 2009, shellfish samples of blue mussel (Mytilus edulis) from the Southwest of Ireland were analysed using liquid chromatography–tandem-mass spectrometry (LC–MS/MS) and were found to be above the regulatory limit (0.16 μg g-1 AZA-equiv.) for AZAs. Water samples from this area were collected and one algal isolate was identified as A. spinosum and was shown to produce azaspiracid toxins. This is the first strain of A. spinosum isolated from Irish waters. The Irish A. spinosum is identical with the other two available A. spinosum strains from Scotland (3D9) and from Denmark (UTHE2) in its sequence of the D1–D2 regions of the LSU rDNA. A 24 h feeding trial of blue mussels (M. edulis) using an algal suspension of the Irish A. spinosum culture at different cell densities demonstrated that A. spinosum is filtered, consumed and digested directly by mussels. Also, LC–MS/MS analysis had shown that AZAs were accumulating in the shellfish hepatopancreas. The toxins AZA1 and -2 were detected in the shellfish together with the AZA analogues AZA3, AZA6, AZA17 and -19 suggesting that AZA1 and -2 are metabolised in the shellfish within the first 24 h after ingestion of the algae. The levels of AZA17 detected in the shellfish hepatopancreas (HP) were equivalent to the levels of AZA1 but in the remainder tissues the levels of AZA17 were four to five times higher than that of AZA1, only small quantities of AZA3 and -19 were present with negligible amounts of AZA6 detected after the 24 h period. This could have implications in the future monitoring of these toxins given that at present according to EU legislation only AZA1–AZA3 is regulated for. This is the first report of blue mussels' (M. edulis) feeding on the azaspiracid producing algae A. spinosum from Irish waters.

Bloom Management and Control

• Brookes, J.D. and Carey, C.C.  Resilience to blooms.  Science 334(6052): 46-47, 2011.  
• Paerl, H.W., Hall, N.S., and Calandrino, E.S.  Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change.  The Science of the Total Environment 409(10): 1739-1745, 2011.
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  Harmful (toxic, food web altering, hypoxia generating) cyanobacterial algal blooms (CyanoHABs) are proliferating world-wide due to anthropogenic nutrient enrichment, and they represent a serious threat to the use and sustainability of our freshwater resources. Traditionally, phosphorus (P) input reductions have been prescribed to control CyanoHABs, because P limitation is widespread and some CyanoHABs can fix atmospheric nitrogen (N₂) to satisfy their nitrogen (N) requirements. However, eutrophying systems are increasingly plagued with non N₂ fixing CyanoHABs that are N and P co-limited or even N limited. In many of these systems N loads are increasing faster than P loads. Therefore N and P input constraints are likely needed for long-term CyanoHAB control in such systems. Climatic changes, specifically warming, increased vertical stratification, salinization, and intensification of storms and droughts play additional, interactive roles in modulating CyanoHAB frequency, intensity, geographic distribution and duration. In addition to having to consider reductions in N and P inputs, water quality managers are in dire need of effective tools to break the synergy between nutrient loading and hydrologic regimes made more favorable for CyanoHABs by climate change. The more promising of these tools make affected waters less hospitable for CyanoHABs by 1) altering the hydrology to enhance vertical mixing and/or flushing and 2) decreasing nutrient fluxes from organic rich sediments by physically removing the sediments or capping sediments with clay. Effective future CyanoHAB management approaches must incorporate both N and P loading dynamics within the context of altered thermal and hydrologic regimes associated with climate change.

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