Harmful Algal Blooms Toxins Research Articles

Dietary exposure to harmful algal bloom (HAB) toxins in the endangered manatee (Trichechus manatus latirostris) and green sea turtle (Chelonia mydas) in Florida, USA

Florida is a hotspot for cyano- and microalgal harmful algal blooms (HABs) with annual red-tide events off-shore and blooms of Lyngbya spp. commonly observed in both marine and freshwater environments. This region also provides extensive foraging habitat for large populations of herbivorous green turtles (Chelonia mydas) and manatees (Trichechus manatus latirostris). The exposure of aquatic organisms to HAB toxins is not well known and whilst acute exposures are better understood, the vulnerability of aquatic animals to chronic exposure from multiple HAB toxins over prolonged periods has rarely been addressed. This study aimed to identify the presence of toxic compounds produced by HAB species commonly found in Florida (brevetoxins, okadaic acid, saxitoxins and Lyngbya toxins) in tissues and gut samples from manatee and green sea turtles that stranded in Florida, USA. Muscle, liver and alimentary tract samples were opportunistically collected from 14 manatees and 13 green turtles that stranded on the Florida shoreline between December 2003 and February 2006. Samples from each animal were assessed for the presence of brevetoxin, okadaic acid, lyngbyatoxin-A and saxitoxin. Nine (64%) manatees and 11 (85%) turtles were found to have been exposed to one or more of the HAB toxins. Okadaic acid and saxitoxin were only found in alimentary tract samples, whereas brevetoxin was more widely distributed. No lyngbyatoxin-A was observed in any tissue samples. The majority of turtles (13) stranded on the Atlantic coast between St. Johns and Monroe counties, with one on the Gulf coast at Bay County, whereas nine manatees were stranded on the Gulf coast between Levy and Lee counties, with the remaining five between Volusia and Brevard counties on the Atlantic coast. This HAB toxin screen has identified that a large proportion of a random sample of turtles and manatees that stranded in Florida in 2003–2006 were exposed to HAB toxins. Most of the concentrations measured were low, and the toxins were directly linked to the death of only three of these animals. However, the presence of these compounds, and in some cases the presence of multiple HAB toxins in individual animals, indicates that turtles and manatees in Florida are exposed to deleterious compounds at sub-lethal levels in their environment, which could ultimately compromise their health.

Algal toxins and reverse osmosis desalination operations: Laboratory bench testing and field monitoring of domoic acid, saxitoxin, brevetoxin and okadaic acid

The occurrence and intensity of harmful algal blooms (HABs) have been increasing globally during the past few decades. The impact of these events on seawater desalination facilities has become an important topic in recent years due to enhanced societal interest and reliance on this technology for augmenting world water supplies. A variety of harmful bloom-forming species of microalgae occur in southern California, as well as many other locations throughout the world, and several of these species are known to produce potent neurotoxins. These algal toxins can cause a myriad of human health issues, including death, when ingested via contaminated seafood. This study was designed to investigate the impact that algal toxin presence may have on both the intake and reverse osmosis (RO) desalination process; most importantly, whether or not the naturally occurring algal toxins can pass through the RO membrane and into the desalination product. Bench-scale RO experiments were conducted to explore the potential of extracellular algal toxins contaminating the RO product. Concentrations exceeding maximal values previously reported during natural blooms were used in the laboratory experiments, with treatments comprised of 50 μg/L of domoic acid (DA), 2 μg/L of saxitoxin (STX) and 20 μg/L of brevetoxin (PbTx). None of the algal toxins used in the bench-scale experiments were detectable in the desalinated product water. Monitoring for intracellular and extracellular concentrations of DA, STX, PbTx and okadaic acid (OA) within the intake and desalinated water from a pilot RO desalination plant in El Segundo, CA, was conducted from 2005 to 2009. During the five-year monitoring period, DA and STX were detected sporadically in the intake waters but never in the desalinated water. PbTx and OA were not detected in either the intake or desalinated water. The results of this study demonstrate the potential for HAB toxins to be inducted into coastal RO intake facilities, and the ability of typical RO operations to effectively remove these toxins.

Forecasts Aid HABs Response

Large accumulations of algae, or harmful algal blooms (HABs), can release toxins and contribute to oxygen-depleted “dead zones” in waters, causing human health problems and disrupting food webs.1 Costs associated with closed fisheries and beaches caused by marine HABs total at least $82 million annually2; freshwater HABs can complicate water treatment and decrease recreational revenue, accounting for millions more in costs.3 Now consortia of researchers across the country are developing forecasts to help local public health officials better monitor and respond to HABs. Anthropogenic nutrient enrichment and a warming climate are contributing to increased frequencies, intensities, and distributions of freshwater cyanobacteria HABs worldwide.1,4,5 When cyanobacteria covered much of Lake Erie’s western basin in July 2011, levels of the cyanotoxin microcystin-LR reached 1,000 µg/L in near-record6 water temperatures averaging just above 77°F.7 An Ohio Department of Health representative reports nine probable cases of algal-caused illnesses in Ohio in 2011 (unpublished data); however, many cases of illness attributable to HABs, especially milder cases, are probably never reported. Although reports of marine HABs—which include blooms of the dinoflagellates Karenia brevis and Alexandrium spp. and the diatoms Pseudo-nitzschia spp.—appear to be increasing,1 researchers lack the long-term data sets needed to prove incidences really are on the rise,8 according to Barbara Kirkpatrick, a senior scientist at Mote Marine Laboratory in Sarasota, Florida. “The more we look for HABs, the more we find them,” she says. “The more we populate along our coastlines, the greater the impact of HABs on people.” The health effects resulting from exposure to HAB toxins can include gastric, respiratory, and neurologic impacts; acute exposure to some HAB toxins can cause death. Exposure can occur through consumption of fish, shellfish, or crustaceans that accumulate the toxins when feeding on algae. Commercial shellfish operations are now routinely monitored for HABs, but controlling recreational harvests is more difficult.1 “We only have toxic shellfish poisonings in Florida when a visitor wanders on the beach and collects clams or oysters from an area not open for harvesting,” says Andrew Reich, coordinator of the Florida Department of Health Aquatic Toxins Program. A Massachusetts sign warns of the historic A. fundyense outbreak that hit the New England coast in 2005. A multiagency con-sor-tium of re-searchers led by the National Ocean-ic and Atmospheric Admin-istration (NOAA) is working to improve prediction and monitoring of HABs.9 In 2004 NOAA initiated a forecasting system for K. brevis in the Gulf of Mexico that uses satellite imagery, field observations, and buoy data to provide information on HAB locations, extent, and potential for change in size or location. Woods Hole Ocean-ographic Institution (WHOI), supported by NOAA, led an effort to use computer models to successfully predict HABs of Alexandrium fundyense in the Gulf of Maine in 2008.10 NOAA is now operating a demonstration forecast project for cyanobacteria HABs in Lake Erie and is coordinating development of forecasts for HABs of the dinoflagellate Karlodinium veneficum in the Chesapeake Bay and of Pseudo-nitzschia on the Washington coast. Detecting HABs can be tricky. Not all blooms produce toxins, even though they may have unpleasant tastes and odors. “Visible blooms may be harmless, and harmful blooms may be almost invisible,” says Sherwood Hall, a marine toxin specialist at the Center for Food Safety and Applied Nutrition of the U.S. Food and Drug Administration. To further complicate management, conditions that cause algal blooms to produce toxins can vary dramatically among different organisms. Forecasting doesn’t eliminate the need for shellfish resource managers to test and monitor toxicity, but it can help them do so more effectively, says WHOI senior scientist Dennis McGillicuddy, a member of the team that developed HAB forecasting methods for the Gulf of Maine. It can also assist local public health departments in their responses to HABs. The NOAA forecasts are “wonderful for us in public health,” says Reich, who advises Florida’s 67 local health departments on HAB response. “Generally, if they find a HAB offshore, and there’s a circulation pattern or wind pattern blowing it onshore, we have two or three days’ warning, so we have time to gear up.”

Harmful phytoplankton ecology studies using an autonomous molecular analytical and ocean observing network

Using autonomous molecular analytical devices embedded within an ocean observatory, we studied harmful algal bloom (HAB) ecology in the dynamic coastal waters of Monterey Bay, California. During studies in 2007 and 2008, HAB species abundance and toxin concentrations were quantified periodically at two locations by Environmental Sample Processor (ESP) robotic biochemistry systems. Concurrently, environmental variability and processes were characterized by sensors co‐located with ESP network nodes, regional ocean moorings, autonomous underwater vehicle surveys, and satellite remote sensing. The two locations differed in their long‐term average physical and biological conditions and in their degree of exposure to episodic wind‐forced variability. While anomalously weak upwelling and strong stratification during the 2007 study favored toxigenic dinoflagellates (Alexandrium catenella), anomalously strong upwelling during the 2008 study favored toxigenic diatoms (Pseudo‐nitzschia spp.). During both studies, raphidophytes (Heterosigma akashiwo) were detected within a similar range of concentrations, and they reached higher abundances at the relatively sheltered, stratified site. During 2008, cellular domoic acid reached higher concentrations and was far more variable at the shallower ESP node, where phytoplankton populations were influenced by resuspended sediments. Episodic variability caused by wind forcing, lateral mixing, internal waves, and subsurface phytoplankton layers influenced ESP detection patterns. The results illustrate the importance of mobilizing HAB detection on autonomous platforms that can intelligently target sample acquisition as a function of environmental conditions and biological patch encounter.

Concurrent Exposure of Bottlenose Dolphins (Tursiops truncatus) to Multiple Algal Toxins in Sarasota Bay, Florida, USA

Sentinel species such as bottlenose dolphins (Tursiops truncatus) can be impacted by large-scale mortality events due to exposure to marine algal toxins. In the Sarasota Bay region (Gulf of Mexico, Florida, USA), the bottlenose dolphin population is frequently exposed to harmful algal blooms (HABs) of Karenia brevis and the neurotoxic brevetoxins (PbTx; BTX) produced by this dinoflagellate. Live dolphins sampled during capture-release health assessments performed in this region tested positive for two HAB toxins; brevetoxin and domoic acid (DA). Over a ten-year study period (2000–2009) we have determined that bottlenose dolphins are exposed to brevetoxin and/or DA on a nearly annual basis (i.e., DA: 2004, 2005, 2006, 2008, 2009; brevetoxin: 2000, 2004, 2005, 2008, 2009) with 36% of all animals testing positive for brevetoxin (n = 118) and 53% positive for DA (n = 83) with several individuals (14%) testing positive for both neurotoxins in at least one tissue/fluid. To date there have been no previously published reports of DA in southwestern Florida marine mammals, however the May 2008 health assessment coincided with a Pseudo-nitzschia pseudodelicatissima bloom that was the likely source of DA observed in seawater and live dolphin samples. Concurrently, both DA and brevetoxin were observed in common prey fish. Although no Pseudo-nitzschia bloom was identified the following year, DA was identified in seawater, fish, sediment, snails, and dolphins. DA concentrations in feces were positively correlated with hematologic parameters including an increase in total white blood cell (p = 0.001) and eosinophil (p<0.001) counts. Our findings demonstrate that dolphins within Sarasota Bay are commonly exposed to two algal toxins, and provide the impetus to further explore the potential long-term impacts on bottlenose dolphin health.

Co-occurrence of multiple classes of harmful algal toxins in bottlenose dolphins ( Tursiops truncatus) stranding during an unusual mortality event in Texas, USA

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.

Reporter Gene Assay for Detection of Shellfish Toxins

To explore the potential reporter gene assay for the detection of sodium channel-specific toxins in shellfish as an alternative for screening harmful algal bloom (HAB) toxins, considering the fact that the existing methods including HPLC and bioassay are inappropriate for identifying HAB toxins which poses a serious problem on human health and shellfish industry. A reporter plasmid pEGFP-c-fos containing c-fos promoter and EGFP was constructed and transfected into T24 cells using LipofectAMINE 2000. Positive transfectants were screened by G418 to produce a pEGFP-c-fos-T24 cell line. After addition of increasing neurotoxic shellfish poison (NSP) or GTX2,3, primary components of paralytic shellfish poison (PSP), changes in expression of EGFP in the cell line were observed under a laser scanning confocal microscope and quantified with Image-pro Plus software. Dose-dependent changes in the intensity of green fluorescence were observed for NSP in a range from 0 to 10 ng/mL and for GTX2,3 from 0 to 16 ng/mL. pEGFP-c-fos-T24 can be applied in detecting HAB toxins, and cell-based assay can be used as an alternative for screening sodium channel-specific HAB toxins.

Characterization of Intracellular and Extracellular Saxitoxin Levels in Both Field and Cultured Alexandrium spp. Samples from Sequim Bay, Washington

Traditionally, harmful algal bloom studies have primarily focused on quantifying toxin levels contained within the phytoplankton cells of interest. In the case of paralytic shellfish poisoning toxins (PSTs), intracellular toxin levels and the effects of dietary consumption of toxic cells by planktivores have been well documented. However, little information is available regarding the levels of extracellular PSTs that may leak or be released into seawater from toxic cells during blooms. In order to fully evaluate the risks of harmful algal bloom toxins in the marine food web, it is necessary to understand all potential routes of exposure. In the present study, extracellular and intracellular PST levels were measured in field seawater samples (collected weekly from June to October 2004- 2007) and in Alexandrium spp. culture samples isolated from Sequim Bay, Washington. Measurable levels of intra- and extra-cellular toxins were detected in both field and culture samples via receptor binding assay (RBA) and an enzyme-linked immunosorbent assay (ELISA). Characterization of the PST toxin profile in the Sequim Bay isolates by preMar. column oxidation and HPLC-fluorescence detection revealed that gonyautoxin 1 and 4 made up 65 ± 9.7 % of the total PSTs present. Collectively, these data confirm that extracellular PSTs are present during blooms of Alexandrium spp. in the Sequim Bay region.

Characterization of Intracellular and Extracellular Saxitoxin Levels in Both Field and Cultured Alexandrium spp. Samples from Sequim Bay, Washington

Traditionally, harmful algal bloom studies have primarily focused on quantifying toxin levels contained within the phytoplankton cells of interest. In the case of paralytic shellfish poisoning toxins (PSTs), intracellular toxin levels and the effects of dietary consumption of toxic cells by planktivores have been well documented. However, little information is available regarding the levels of extracellular PSTs that may leak or be released into seawater from toxic cells during blooms. In order to fully evaluate the risks of harmful algal bloom toxins in the marine food web, it is necessary to understand all potential routes of exposure. In the present study, extracellular and intracellular PST levels were measured in field seawater samples (collected weekly from June to October 2004–2007) and in Alexandrium spp. culture samples isolated from Sequim Bay, Washington. Measurable levels of intra- and extra-cellular toxins were detected in both field and culture samples via receptor binding assay (RBA) and an enzyme-linked immunosorbent assay (ELISA). Characterization of the PST toxin profile in the Sequim Bay isolates by pre-column oxidation and HPLC-fluorescence detection revealed that gonyautoxin 1 and 4 made up 65 ± 9.7 % of the total PSTs present. Collectively, these data confirm that extracellular PSTs are present during blooms of Alexandrium spp. in the Sequim Bay region.

BIOTOXINS FROM FRESHWATER AND MARINE HARMFUL ALGAL BLOOMS OCCURRING IN MEXICO

Mexican coasts and watersheds are among the places with the greatest marine toxin diversity worldwide. Toxins produced by harmful algal blooms (HAB) have severely affected the environment in Mexico, even causing several human casualties. HAB toxins chemically proven to date in Mexican waters include: amnesic shellfish poisoning (ASP), ciguatera fish poisoning (CFP), several cyanobacterial toxins (CTXs), diarrhetic shellfish poisoning (DSP), neurotoxic shellfish poisoning (NSP), and paralytic shellfish poisoning (PSP). Species producing other toxins (azaspiracids, gymnodimine, pectenotoxins, prorocentrolides, yessotoxins) have also been detected in Mexican waters. HAB-related poisoning is often lost from official statistics by designation as diarrhea with indeterminate origin.

Marine Biotechnology: Realizing the Potential

Marine biotechnology is an applied science, the goal of which is to develop goods and services from marine organisms and processes. The new wave of marine biotechnology research began in the early 1980s and includes some significant success stories. A new drug to manage pain is commercially available, and a new cancer drug has been recommended for approval, the first from a fish-eating snail and the second from a mangrove tunicate. Enzymes from hydrothermal vent microbes are routinely used in PCR reactions, and marine-derived molecular probes are helping understand the molecular basis of disease processes. Advances in aquaculture biotechnology have resulted in more efficient production of finfish and shellfish for human consumption, and polyunsaturated fatty acids from marine microalgae are used as nutritional supplements for adults and infants. Rapid diagnostic tools have been developed to monitor toxins in the environment and in seafood, and genetic fingerprinting techniques are helping to control illegal trade of threatened marine species. In the future, multidisciplinary programs in oceans and human health should focus not only on microbial pathogens and harmful algal bloom toxins but also on discovery of new chemicals to prevent or treat human diseases. And the development of biological and biochemical sensors to detect pathogens, contaminants, and toxins and to monitor human and environmental health indicators in the marine environment should be a very high priority in the establishment of U.S. coastal ocean observing systems.

Harmful algal bloom toxins alter c-Fos protein expression in the brain of killifish, Fundulus heteroclitus

The immediate early gene c-fos, and its protein product c-Fos, are known to be induced in neurons of mammals and fish as a result of neuronal stimulation. The purpose of this study was to quantitatively examine CNS alterations in killifish, Fundulus heteroclitus, in relation to harmful algal bloom (HAB) toxin exposure. c-Fos expression was visualized using immunocytochemistry in the brains of killifish exposed to the excitatory neurotoxins domoic acid (DA) and brevetoxin (PbTx-2), and a paralytic neurotoxin, saxitoxin (STX), released from HABs. In addition, a simulated transport stress experiment was conducted to investigate effects of physical stress on c-Fos induction. Groups of fish were exposed to the different stress agents, brain sections were processed for c-Fos staining, and expression was quantified by brain region. Fish exposed to DA, STX, and transport stress displayed significant alterations in neuronal c-Fos expression when compared to control fish ( p ≤ 0.05). DA, PbTx-2, and transport stress increased c-Fos expression in the optic tecta regions of the brain, whereas STX significantly decreased expression. This is the first study to quantify c-Fos protein expression in fish exposed to HAB toxins. General alterations in brain activity, as well as knowledge of specific regions within the brain activated in association with HABs or other stressors, provides valuable insights into the neural control of fish behavior as well as sublethal effects of specific stressors in the CNS.

Neurobehavioral effects of harmful algal bloom (HAB) toxins: A critical review

Human exposure to naturally occurring marine toxins has been associated with a range of neurobehavioral abnormalities. The toxins are produced by harmful algal blooms (HABs) and are typically contracted through seafood consumption. The primary target of many of the HAB toxins is the neurologic system, and the neurobehavioral symptoms associated with the HAB illnesses have influenced public health policy. The HAB-related illnesses most frequently linked to neuropsychological disturbance are Amnesic Shellfish Poisoning, Ciguatera Fish Poisoning, and Possible Estuarine Associated Syndrome, which is associated with exposure to the Pfiesteria piscicida organism. Although the neurophysiologic mechanisms underlying many of the HAB illnesses have been well delineated, the literature examining the neuropsychological impairments is unclear and needs to be defined. This review is intended to introduce an emerging area of study linking HAB illnesses with neuropsychological changes.

Shorebird foraging behavior, diet, and abundance vary with harmful algal bloom toxin concentrations in invertebrate prey

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 293:303-309 (2005) - doi:10.3354/meps293303 NOTEShorebird foraging behavior, diet, and abundance vary with harmful algal bloom toxin concentrations in invertebrate prey Rikk Kvitek, Carrie Bretz* California State University Monterey Bay, 100 Campus Center, Seaside, California 93955, USA *Corresponding author. Email: carrie_bretz@csumb.edu ABSTRACT: We demonstrate how harmful algal bloom (HAB) toxins can change the strength of consumer–prey interactions by altering the foraging behavior of avian predators on rocky and sandy shores. Changes in the foraging behavior and diet of 5 common northern California shorebirds (black oystercatchers, godwits, sanderlings, whimbrels, and willets) correlated with the predicted seasonal variation in paralytic shellfish poisoning toxin (PSPT) concentrations in their 2 major invertebrate prey species, sea mussels Mytilus californianus and sand crabs Emerita analoga, at 2 locations along the California coast. In rocky habitats, when mussel PSPT concentrations exceeded 150 µg saxitoxin (STX) eq · 100 g–1, oystercatchers increased their consumption of smaller, non-PSPT-accumulating prey (limpets, primarily Lottia spp.), as well as their discard rate of captured mussel tissue. In sandy habitats, when sand crab PSPT concentrations exceeded 150 to 200 µg STX eq · 100 g–1, shorebird abundance decreased, while their rejection rate of sand crab prey increased. These results confirm the prediction that shorebirds are able to detect and avoid consumption of lethal amounts of PSPT, and that the movement of HAB toxins through the marine food web can alter upper-level trophic interactions. KEY WORDS: Paralytic shellfish poisoning toxins · Harmful algal blooms · Saxitoxin · Shorebirds · Predation · Emerita analoga · Mytilus californianus Full text in pdf format PreviousExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 293. Online publication date: June 02, 2005 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2005 Inter-Research.

Altered brain activity in brevetoxin-exposed bluegill, Lepomis macrochirus, visualized using in vivo 14C 2-deoxyglucose labeling

This study investigated the neurological effects of sublethal brevetoxin (PbTx-2) exposure in bluegill ( Lepomis macrochirus) by measuring alterations in 2-deoxyglucose (2-DG) uptake in the brains of exposed fish. Changes in regional brain activity were quantified using digitized autoradiographs from exposed and control fish. Brains of brevetoxin-exposed fish had significantly higher labeling of 2-DG than brains of control fish. Regional increases in labeling were observed in the optic lobes, telencephalon, and cerebrum of PbTx-2 exposed fish. From these observations, we conclude that sublethal brevetoxin exposure in vivo in bluegill increases neurological stimulation, measured through quantification of [ 14C]2-DG uptake in the brain. Increases in the uptake of [ 14C]2-DG from this study may be indicative of differences in neural activity in the PbTx-exposed fish and are likely associated with the action of PbTx-2 on voltage-gated sodium channels (VGSC), as well as neurological alterations in calcium and neurotransmitter release downstream resulting from VGSC activation. These techniques quantify physiological alterations in fish brain activity resulting from exposure to brevetoxin and possibly other harmful algal bloom toxins.