Harmful Algal Events Research Articles

Perceived global increase in algal blooms is attributable to intensified monitoring and emerging bloom impacts

Global trends in the occurrence, toxicity and risk posed by harmful algal blooms to natural systems, human health and coastal economies are poorly constrained, but are widely thought to be increasing due to climate change and nutrient pollution. Here, we conduct a statistical analysis on a global dataset extracted from the Harmful Algae Event Database and Ocean Biodiversity Information System for the period 1985–2018 to investigate temporal trends in the frequency and distribution of marine harmful algal blooms. We find no uniform global trend in the number of harmful algal events and their distribution over time, once data were adjusted for regional variations in monitoring effort. Varying and contrasting regional trends were driven by differences in bloom species, type and emergent impacts. Our findings suggest that intensified monitoring efforts associated with increased aquaculture production are responsible for the perceived increase in harmful algae events and that there is no empirical support for broad statements regarding increasing global trends. Instead, trends need to be considered regionally and at the species level.

Diversity and regional distribution of harmful algal events along the Atlantic margin of Europe

The IOC-ICES-PICES Harmful Algal Event Database (HAEDAT) was used to describe the diversity and spatiotemporal distribution of harmful algal events along the Atlantic margin of Europe from 1987 - 2018. The majority of events recorded are caused by Diarrhetic Shellfish Toxins (DSTs). These events are recorded annually over a wide geographic area from southern Spain to northern Scotland and Iceland, and are responsible for annual closures of many shellfish harvesting areas. The dominant causative dinoflagellates, members of the morphospecies ‘Dinophysis acuminata complex’ and D. acuta, are common in the waters of the majority of countries affected. There are regional differences in the causative species associated with PST events; the coasts of Spain and Portugal with the dinoflagellates Alexandrium minutum and Gymnodinium catenatum, north west France/south west England/south Ireland with A. minutum, and Scotland/Faroe Islands/Iceland with A. catenella. This can influence the duration and spatial scale of PST events as well as the toxicity of shellfish. The diatom Pseudo-nitzschia australis is the most widespread Domoic Acid (DA) producer, with records coming from Spain, Portugal, France, Ireland and the UK. Amnesic Shellfish Toxins (ASTs) have caused prolonged closures for the scallop fishing industry due to the slow depuration rate of DA. Amendments to EU shellfish hygiene regulations introduced between 2002 and 2005 facilitated end-product testing and sale of adductor muscle. This reduced the impact of ASTs on the scallop fishing industry and thus the number of recorded HAEDAT events. Azaspiracids (AZAs) are the most recent toxin group responsible for events to be characterised in the ICES area. Events associated with AZAs have a discrete distribution with the majority recorded along the west coast of Ireland. Ciguatera Poisoning (CP) has been an emerging issue in the Canary Islands and Madeira since 2004. The majority of aquaculture and wild fish mortality events are associated with blooms of the dinoflagellate Karenia mikimotoi and raphidophyte Heterosigma akashiwo. Such fish killing events occur infrequently yet can cause significant mortalities. Interannual variability was observed in the annual number of HAEDAT areas with events associated with individual shellfish toxin groups. HABs represent a continued risk for the aquaculture industry along the Atlantic margin of Europe and should be accounted for when considering expansion of the industry or operational shifts to offshore areas.

Three decades of Canadian marine harmful algal events: Phytoplankton and phycotoxins of concern to human and ecosystem health

Spatial and temporal trends of marine harmful algal events in Canada over the last three decades were examined using data from the Harmful Algal Event Database (HAEDAT). This database contains the most complete record of algal blooms, phycotoxins and shellfish harvesting area closures in Canada since 1987. This 30-year review of 593 Canadian HAEDAT records from 1988 to 2017, together with other Canadian data and publications, shows that recurring harmful algal events have been widespread throughout both the Atlantic and Pacific coastal regions. The 367 paralytic shellfish toxin (PST) reports revealed annual and frequent recurrence throughout both the Atlantic and Pacific regions, including multi-year PST events in the Bay of Fundy, the Estuary and Gulf of St. Lawrence and the Strait of Georgia. The 70 amnesic shellfish toxin (AST) records revealed no recognizable trend, as these events were usually area specific and did not recur annually. The increasing frequency of diarrhetic shellfish toxin (DST) events over the period of this review, in total 59 records, can be at least partially explained by increased sampling effort. Marine species mortalities caused by harmful algae (including diatoms, dictyochophytes, dinoflagellates, and raphidophytes), were a common occurrence in the Pacific region (87 reports), but have been reported much less frequently in the Atlantic region (10 reports). Notable Canadian records contained in HAEDAT include the first detection worldwide of amnesic shellfish poisoning (ASP), attributed to the production of domoic acid (an AST) by a diatom (Pseudo-nitzschia multiseries) in Prince Edward Island in 1987. The first proven case of diarrhetic shellfish poisoning (DSP) in Canada and North America was recorded in 1990, and the first closures of shellfish harvesting due to DST (associated with the presence of Dinophysis norvegica) occurred in Nova Scotia in 1992, followed by closures in Newfoundland and Labrador in 1993. In 2008, mass mortalities of fishes, birds and mammals in the St. Lawrence Estuary were caused by Alexandrium catenella and high levels of PST. During 2015, the Pacific coast experienced a large algal bloom that extended from California to Alaska. It resulted in the closure of several shellfish harvesting areas in British Columbia due to AST, produced by Pseudo-nitzschia australis. Data from the Canadian Arctic coast is not included in HAEDAT. However, because of the emerging importance of climate change and increased vessel traffic in the Arctic, information on the occurrence of harmful algal species (pelagic and sympagic = sea ice-associated) in that region was compiled from relevant literature and data. The results suggest that these taxa may be more widespread than previously thought in the Canadian Arctic. Information in HAEDAT was not always robust or complete enough to provide conclusions about temporal trends. Compilation of spatial and temporal information from HAEDAT and other records is nevertheless important for evaluating the potential role of harmful algae as a stressor on Canadian marine ecosystems, and will support the next step: developing a knowledge gap analysis that will establish research priorities for determining their consequences on human and ecosystem health.

Overview of Australian and New Zealand harmful algal species occurrences and their societal impacts in the period 1985 to 2018, including a compilation of historic records

Similarities and differences between Australia and New Zealand in Harmful Algal species occurrences and Harmful Algal Events impacting on human society (HAEDAT) are reported and factors that explain their differences explored. Weekly monitoring of harmful phytoplankton and biotoxins commenced in Australia in 1986 and in New Zealand in 1993. Anecdotal historic HAB records in both countries are also catalogued. In Australia, unprecedented highly toxic Paralytic Shellfish Toxin (PST)-producing blooms of Alexandrium catenella have impacted the seafood industry along the 200 km east coast of Tasmania from 2012 to present. Toxic blooms in 1986-1993 by Gymnodinium catenatum in Tasmania were effectively mitigated by closing the affected area for shellfish farming, while a bloom by this same species in 2000 in New Zealand caused significant economic damage from restrictions on the movement of greenshell mussel spat. The biggest biotoxin event in New Zealand was an unexpected outbreak of Neurotoxic Shellfish Poisoning (NSP) in 1993 in Hauraki Gulf (putatively due to Karenia cf. mikimotoi) with 180 reported cases of human poisonings as well as reports of respiratory irritation north of Auckland. Strikingly, NSP never recurred in New Zealand since and no NSP events have ever been reported in Australia. In New Zealand, Paralytic Shellfish Poisoning (PSP) was the predominant seafood toxin syndrome, while in Australia Ciguatera Fish Poisoning (CFP) was the major reported seafood toxin syndrome, while no CFP has been recorded from consumption of New Zealand fish. In Australia, Diarrhetic Shellfish Poisoning (DSP) illnesses were recorded from two related outbreaks in 1997/98 following consumption of beach harvested clams (pipis) from a previously non-monitored area, whereas in New Zealand limited DSP illnesses are known. No human illnesses from Amnesic Shellfish Poisoning (ASP) have been reported in either Australia or New Zealand. Selected examples of HABs appearing and disappearing (NSP in New Zealand, Alexandrium catenella in Tasmania), species expanding their ranges (Noctiluca, Gambierdiscus), and reputed ballast water introductions (Gymnodinium catenatum) are discussed. Eutrophication has rarely been invoked as a cause except for confined estuaries and fish ponds and estuarine cyanobacterial blooms. No trend in the number of HAEDAT events from 1985 to 2018 was discernible.

Toxic marine microalgae and noxious blooms in the Mediterranean Sea: A contribution to the Global HAB Status Report

We review the spatial distribution of toxic marine microalgal species and the impacts of all types of harmful algal events (Harmful Algal Blooms, HABs) in the Mediterranean Sea (MS), including the Black Sea, the Sea of Marmara, coastal lagoons and transitional waters, based on two databases compiled in the Ocean Biogeographic Information System (OBIS). Eighty-four potentially toxic species have been detected in the MS (2,350 records), of which 16 described from these waters between 1860 and 2014 and a few suspected to have been introduced. More than half of these species (46) produce toxins that may affect human health, the remainders ichthyotoxic substances (29) or other types of toxins (9). Nevertheless, toxicity-related events are not frequent in the MS (308 records in 31 years), and mainly consist of impacts on aquaculture, caused by the dinoflagellates Dinophysis and Alexandrium, along with a few actual shellfish poisoning cases. Pseudo-nitzschia blooms are widespread, but domoic acid in shellfish rarely exceeds regulatory levels. Fish kills are probably less sporadic than reported, representing a problem at a few places along the southern MS coasts and in the Ebro River Delta. Since the last decade of the 20th century, blooms of the benthic dinoflagellates Ostreopsis cf. ovata have regularly occurred all along rocky shores of the MS, at times with human health problems caused by toxic aerosol. New records of Gambierdiscus and Fukuyoa, until now reported for the westernmost and easternmost MS coasts, raise concerns about the risk of ciguatera, a syndrome so far known only for subtropical and tropical areas. Recent discoveries are the dinoflagellates Vulcanodinium rugosum, responsible for the presence of pinnatoxins in French lagoons’ shellfish, and the azaspiracid-producers Azadinium spp. Mucilages and discolorations have a major impact on tourism in summer. Reports of toxic species and HABs have apparently increased in the MS over the last half century, which is likely related to the increased awareness and monitoring operations rather than to an actual increase of these phenomena. Indeed, while the case of Ostreopsis appears as a sudden upsurge rather than a trend, no actual increase of toxic or noxious events has so far emerged in intensively studied areas, such as the French and Spanish coasts or the Adriatic Sea. Moreover, some cases of decrease are reported, e.g., for Alexandrium minutum blooms disappearing from the Harbour of Alexandria. Overall, main HAB risks derive from cases of massive development of microalgal biomass and consequent impacts of reduced coastal water quality on tourism, which represents the largest part of the marine economy along the MS coasts.

Neurotoxicology of Red Tide Poisoning

Red Tide poisoning is a result of toxins released from marine dinoflagellates (various algae) and received its name from the discolored (reddish) water created by an algal bloom. It appears this event has occurred for centuries in many locations even before the occurrence of pollution, agricultural run-off and current observations of global warming. There were reports of the Red Tide in Florida during the 1800’s [1, 2]. However, historical reports indicate that the Red Tide occurred throughout history with an observation noted as early as 1528 in the Gulf of Mexico; although, the first “verifiable” event was in 1648 [2, 3]. The Red Tide occurs throughout tropical waters of the world [4]. In the United States the predominant region is Florida, mostly in the Gulf of Mexico; but events have been noted in the Atlantic and Pacific Oceans. Periodically, there have also been occurrences off the Texas coast [2]. Other locations of notable interest where events occur include Scotland and the South Pacific (e.g. Australia), indicating harmful algal events can occur in northern locations and are likely experiencing an expanding geography due to global warming. There is an increasing frequency of Red Tide phenomena throughout the world with temperature and pollution being indicated as the contributing factors [2].

A review of the biophysical interactions relevant to the promotion of HABs in stratified systems: The case study of Ireland

The biophysical interactions involved in the promotion of harmful algal events are reviewed with specific reference to events that have occurred around Ireland. The direct and indirect effects of tides, solar heating and winds are considered over a range of length scales from ca. 105m down to <10m. For example the effects of tidal mixing across the continental shelf through to tidal flushing of embayments is discussed in relation to the distribution and timing of harmful algal events. The effects of winds in moderating coastal currents and also forcing exchanges between water in bays and that on the adjacent shelf are also described. Similarly, the consequences of the annual cycle of thermal stratification of the water column on the promotion of harmful algal events are illustrated over a range of temporal and spatial scales. These include the timing of a harmful event (seasonality) down to physical effects associated with sub-surface high-density thin layers of harmful species. The application of bulk models for predicting harmful events based on a thorough understanding of the physical promotion of the mechanisms involved is discussed.

An evaluation of the applicability of microarrays for monitoring toxic algae in Irish coastal waters

The applicability of microarrays to monitor harmful algae across a broad range of ecological niches and toxic species responsible for harmful algal events has been one of the key tasks in the EU Seventh Framework Programme (FP7)-funded Microarrays for the Detection of Toxic Algae project. The technique has a strong potential for improving speed and accuracy of the identification of harmful algae and their toxins to assist monitoring programmes. Water samples were collected from a number of coastal sites around Ireland, including several that are used in the Irish National Phytoplankton and Biotoxin Monitoring Programme. Ribosomal RNA was extracted from filtered field samples, labelled with a fluorescent dye, and hybridised to probes spotted in a microarray format on a glass slide. The fluorescent signal intensity of the hybridisation to >120 probes on the chip was analysed and compared with actual field counts. There was a general agreement between cell counts and microarray signal. Results are presented for field samples taken from a range of stations along the Irish coastline known for harmful algal events during the first field trial (July 2009-April 2010).

Remote sensing chlorophyll a of optically complex waters ( rias Baixas, NW Spain): Application of a regionally specific chlorophyll a algorithm for MERIS full resolution data during an upwelling cycle

This study takes advantage of a regionally specific algorithm and the characteristics of Medium Resolution Imaging Spectrometer (MERIS) in order to deliver more accurate, detailed chlorophyll a (chl a) maps of optically complex coastal waters during an upwelling cycle. MERIS full resolution chl a concentrations and in situ data were obtained on the Galician (NW Spain) shelf and in three adjacent rias (embayments), sites of extensive mussel culture that experience frequent harmful algal events. Regionally focused algorithms (Regional neural network for rias Baixas or NNRB) for the retrieval of chl a in the Galician rias optically complex waters were tested in comparison to sea-truth data. The one that showed the best performance was applied to a series of six MERIS (FR) images during a summer upwelling cycle to test its performance. The best performance parameters were given for the NN trained with high-quality data using the most abundant cluster found in the rias after the application of fuzzy c-mean clustering techniques (FCM). July 2008 was characterized by three periods of different meteorological and oceanographic states. The main changes in chl a concentration and distribution were clearly captured in the images. After a period of strong upwelling favorable winds a high biomass algal event was recorded in the study area. However, MERIS missed the high chlorophyll upwelled water that was detected below surface in the ria de Vigo by the chl a profiles, proving the necessity of in situ observations. Relatively high biomass “patches” were mapped in detail inside the rias. There was a significant variation in the timing and the extent of the maximum chl a areas. The maps confirmed that the complex spatial structure of the phytoplankton distribution in the rias Baixas is affected by the surface currents and winds on the adjacent continental shelf. This study showed that a regionally specific algorithm for an ocean color sensor with the characteristics of MERIS in combination with in situ data can be of great help in chl a monitoring, detection and study of high biomass algal events in an area affected by coastal upwelling such as the rias Baixas.

Neural network estimation of chlorophyll a from MERIS full resolution data for the coastal waters of Galician rias (NW Spain)

In typical Case 2 waters, accurate remote sensing retrieval of chlorophyll a (chl a) is still a challenging task. In this study, focusing on the Galician rias (ΝW Spain), algorithms based on neural network (NN) techniques were developed for the retrieval of chl a concentration in optically complex waters, using Medium Resolution Imaging Spectrometer (MERIS) data. There is considerable interest in the accurate estimation of chl a for the Galician rias, because of the economic and social importance of the extensive culture of mussels, and the high frequency of harmful algal events. Fifteen MERIS full resolution (FR) cloud-free images paired with in situ chl a data (for 2002–2004 and 2006–2008) were used for the development and validation of the NN. The scope of NN was established from the clusters obtained using fuzzy c-mean (FCM) clustering techniques applied to the satellite-derived data. Three different NNs were developed: one including the whole data set, and two others using only points belonging to one of the clusters. The input data for these latter two NNs was chosen depending on the quality level, defined on the basis of quality flags given to each data set. The fitting results were fairly good and proved the capability of the tool to predict chl a concentrations in the study area. The best prediction was given for the NN trained with high-quality data using the most abundant cluster data set. The performance parameters in the validation set of this NN were R 2 = 0.86, mean percentage error (MPE) = − 0.14, root mean square error (RMSE) = 0.75 mg m − 3 , and relative RMSE = 66%. The NN developed in this study detected accurately the peaks of chl a, in both training and validation sets. The performance of the Case-2-Regional (C2R) algorithm, routinely used for MERIS data, was also tested and compared with our best performing NN and the sea-truthing data. Results showed that this NN outperformed the C2R, giving much higher R 2 and lower RMSE values. This study showed that the combination of in situ data and NN technology improved the retrieval of chl a in Case 2 waters, and could be used to obtain more accurate chl a maps. A local-based algorithm for the chl a retrieval from an ocean colour sensor with the characteristics of MERIS would be a great support in the quantitative monitoring and study of harmful algal events in the coastal waters of the Rias Baixas. The limitations and possible improvements of the developed chl a algorithms are also discussed.

A simple short range model for the prediction of harmful algal events in the bays of southwestern Ireland

A simple model is described which predicts harmful algal events in the bays of southwestern Ireland. Fundamental to the model is the physical forcing of circulation in these bays in summer. The predominant hydrographic feature at this time is a wind-driven two-layer oscillatory flow acting in a thermally stratified water column. This mechanism exchanges substantial proportions of the bays' volumes, and harmful algal events arise with the associated transport of harmful populations into them. The model is therefore based on the criterion that wind-driven water exchanges result in exchanges of phytoplankton, which, if the time of year is correct, result in toxic events. Utilising Bantry Bay as an example, hindcasting showed that the model has a high degree of success using a wind index based on the sequence of winds that results in water exchange. The model was implemented by estimating indices from the five-day weather forecast, and trialled in 2005. Results were published on the web in real time, during which a predicted water exchange event in mid-June was accompanied by an influx of Dinophysis acuminata into Bantry Bay with an associated contamination of shellfish with Diarrheic Shellfish Poisoning toxins.

Dinoflagellate cysts from surface sediments of Syracuse Bay (Western Ionian Sea, Mediterranean)

The occurrence and abundance of dinoflagellate cysts were investigated for the first time at an Ionian locality along the south-eastern coast of Sicily, subject to spring–summer harmful algal events. Thirty-four cyst morphotypes were recognized belonging to 24 taxa identified at least at the genus level. Cyst abundance in surface sediments ranged from 43 to 828 cysts g−1 dry weight, with the highest numbers recorded at the most restricted station. Germination experiments allowed confirmation of species identification determined by cyst analysis and provided clonal cultures of Alexandrium minutum and Gymnodinium nolleri, two of the bloom-forming species in the area. This represents the first record of G. nolleri for the Mediterranean Sea.

The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA

Cultural eutrophication is frequently invoked as one factor in the global increase in harmful algal blooms, but is difficult to definitively prove due to the myriad of factors influencing coastal phytoplankton bloom development. To assess whether eutrophication could be a factor in the development of harmful algal blooms in California (USA), we review the ecophysiological potential for urea uptake by Pseudo-nitzschia australis (Bacillariophyceae), Heterosigma akashiwo (Raphidophyceae), and Lingulodinium polyedrum (Dinophyceae), all of which have been found at bloom concentrations and/or exhibited noxious effects in recent years in California coastal waters. We include new measurements from a large (Chlorophyll a > 500 mg m −3) red tide event dominated by Akashiwo sanguinea (Dinophyceae) in Monterey Bay, CA during September 2006. All of these phytoplankton are capable of using nitrate, ammonium, and urea, although their preference for these nitrogenous substrates varies. Using published data and recent coastal time series measurements conducted in Monterey Bay and San Francisco Bay, CA, we show that urea, presumably from coastal eutrophication, was present in California waters at measurable concentrations during past harmful algal bloom events. Based on these observations, we suggest that urea uptake could potentially sustain these harmful algae, and that urea, which is seldom measured as part of coastal monitoring programs, may be associated with these harmful algal events in California.

Effects of selenium, iron and cobalt addition to growth and yessotoxin production of the toxic marine dinoflagellate Protoceratium reticulatum in culture

The marine dinoflagellate Protoceratium reticulatum has been recently identified as a source for the disulfated polyether toxin, yessotoxin (YTX), and may pose a risk to human health, aquaculture development and coastal environments. The requirements of P. reticulatum for selenium, iron and cobalt were assessed in culture. P. reticulatum was grown in nutrient enriched seawater (1/10 GP medium) without selenium or with 0.003 and 0.0003 μM selenium added; without iron or with 0.076 and 0.0076 μM iron added; and without cobalt or with 0.008 μM cobalt added. Test flasks were monitored for growth rate, cell yield and YTX production. P. reticulatum was found to exhibit a strong requirement for both selenium and iron. Growth rate and cell yield in treatments without added selenium were significantly ( P<0.05) reduced to 60.2% ( μ=0.15 day −1) and 20.2% (4942 cell ml −1), respectively, of those with selenium added ( μ=0.23 day −1 and 24, 387 cell ml −1). YTX production was significantly increased by addition of selenium in two of three transfers tested. Cells of P. reticulatum subjected to medium without selenium added showed morphological changes observable at the light microscope level which included enlarged cell size. The diameter of cells in medium without selenium added were significantly ( P<0.05) enlarged to 36.7±0.90 μm compared to cells in the medium with selenium added, 27.5±1.25 μm. Growth rate and cell yield in treatments without added iron were also significantly reduced to 70.1% ( μ=0.16 day −1) and 34.2% (8003 cells ml −1), respectively, of those with iron added ( μ=0.23 day −1 and 23,416 cells ml −1). No significant effect on YTX production was measured. In contrast to selenium and iron, no limitation of growth or cell yield or differences in YTX production were observed for flasks without cobalt as compared to those with cobalt added. The possibility that harmful algal events of P. reticulatum may be influenced by selenium or iron in neritic waters is discussed.

Toxic Tides

Research ArticleOpen AccessToxic tides. J Tibbetts J Tibbetts Search for more papers by this author Published:1 July 1998https://doi.org/10.1289/ehp.98106a326Cited by:11AboutSectionsPDF ToolsDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InReddit FiguresReferencesRelatedDetailsCited by Morabito S, Silvestro S and Faggio C (2017) How the marine biotoxins affect human health, Natural Product Research, 10.1080/14786419.2017.1329734, 32:6, (621-631), Online publication date: 19-Mar-2018. Van Wagoner R, Satake M and Wright J (2014) Polyketide biosynthesis in dinoflagellates: what makes it different?, Natural Product Reports, 10.1039/C4NP00016A, 31:9, (1101) Dell’Aversano C (2011) Hydrophilic Interaction Liquid Chromatography–Mass Spectrometry (HILIC–MS) of Paralytic Shellfish Poisoning Toxins, Domoic Acid, and Assorted Cyanobacterial Toxins Hydrophilic Interaction Liquid Chromatography (HILIC) and Advanced Applications, 10.1201/b10609-7, (105-132), Online publication date: 17-Feb-2011. Ciminiello P, Dell'Aversano C, Fattorusso E, Forino M, Tartaglione L, Boschetti L, Rubini S, Cangini M, Pigozzi S and Poletti R (2010) Complex toxin profile of Mytilus galloprovincialis from the Adriatic sea revealed by LC–MS, Toxicon, 10.1016/j.toxicon.2009.07.037, 55:2-3, (280-288), Online publication date: 1-Feb-2010. Still K and Mohapatra A (2009) Biotoxins Information Resources in Toxicology, 10.1016/B978-0-12-373593-5.00010-0, (91-102), . Ciminiello P, Dell' Aversano C, Fattorusso E and Forino M (2009) Chapter 1 Recent Developments in Mediterranean Harmful Algal Events , 10.1016/S1872-0854(09)00001-0, (1-41), . Mao H, Thorne J, Pharr J and Gawley R (2006) Effect of crown ether ring size on binding and fluorescence response to saxitoxin in anthracylmethyl monoazacrown ether chemosensors, Canadian Journal of Chemistry, 10.1139/v06-093, 84:10, (1273-1279), Online publication date: 1-Oct-2006. Guy R (2005) Red Tide Encyclopedia of Toxicology, 10.1016/B0-12-369400-0/00835-8, (628-630), . Kirkpatrick B, Fleming L, Squicciarini D, Backer L, Clark R, Abraham W, Benson J, Cheng Y, Johnson D, Pierce R, Zaias J, Bossart G and Baden D (2004) Literature review of Florida red tide: implications for human health effects, Harmful Algae, 10.1016/j.hal.2003.08.005, 3:2, (99-115), Online publication date: 1-Apr-2004. Hales S, Weinstein P and Woodward A (1999) Ciguatera (Fish Poisoning), El Nino, and Pacific Sea Surface Temperatures, Ecosystem Health, 10.1046/j.1526-0992.1999.09903.x, 5:1, (20-25), Online publication date: 1-Mar-1999. Fleming L, Easom J, Baden D, Rowan A and Levfn B (2016) Review Article: Emerging Harmful Algal Blooms and Human Health: Pfiesteria and Related Organisms, Toxicologic Pathology, 10.1177/019262339902700511, 27:5, (573-581), Online publication date: 1-Sep-1999. Vol. 106, No. 7 July 1998Metrics About Article Metrics Publication History Originally published1 July 1998Published in print1 July 1998 Financial disclosuresPDF download License information EHP is an open-access journal published with support from the National Institute of Environmental Health Sciences, National Institutes of Health. All content is public domain unless otherwise noted. Note to readers with disabilities EHP strives to ensure that all journal content is accessible to all readers. However, some figures and Supplemental Material published in EHP articles may not conform to 508 standards due to the complexity of the information being presented. If you need assistance accessing journal content, please contact [email protected]. Our staff will work with you to assess and meet your accessibility needs within 3 working days.