Integrative monitoring strategy for marine and freshwater harmful algal blooms and toxins across the freshwater-to-marine continuum.

Many coastal states throughout the USA have observed negative effects in marine and estuarine environments caused by cyanotoxins produced in inland waterbodies that were transported downstream or produced in the estuaries. Estuaries and other downstream receiving waters now face the dual risk of impacts from harmful algal blooms (HABs) that occur in the coastal ocean as well as those originating in inland watersheds. Despite this risk, most HAB monitoring efforts do not account for hydrological connections in their monitoring strategies and designs. Monitoring efforts in California have revealed the persistent detection of cyanotoxins across the freshwater-to-marine continuum. These studies underscore the importance of inland waters as conduits for the transfer of cyanotoxins to the marine environment and highlight the importance of approaches that can monitor across hydrologically connected waterbodies. A HAB monitoring strategy is presented for the freshwater-to-marine continuum to inform HAB management and mitigation efforts and address the physical and hydrologic challenges encountered when monitoring in these systems. Three main recommendations are presented based on published studies, new datasets, and existing monitoring programs. First, HAB monitoring would benefit from coordinated and cohesive efforts across hydrologically interconnected waterbodies and across organizational and political boundaries and jurisdictions. Second, a combination of sampling modalities would provide the most effective monitoring for HAB toxin dynamics and transport across hydrologically connected waterbodies, from headwater sources to downstream receiving waterbodies. Third, routine monitoring is needed for toxin mixtures at the land-sea interface including algal toxins of marine origins as well as cyanotoxins that are sourced from inland freshwater or produced in estuaries. Case studies from California are presented to illustrate the implementation of these recommendations, but these recommendations can also be applied to inland states or regions where the downstream receiving waterbody is a freshwater lake, reservoir, or river. Integr Environ Assess Manag 2023;19:586-604. © 2022 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).

Persistent domoic acid in marine sediments and benthic infauna along the coast of Southern California.

Blooms of the diatom genus Pseudo-nitzschia occur annually in the Southern California Bight (SCB), and domoic acid (DA) associated with these events can contaminate fisheries, presenting both human and wildlife health risks. Recent studies have suggested that marine sediments may act as a reservoir for DA, extending the risk of food web contamination long after water column blooms have ended. In this study, we conducted a regional assessment of the extent and magnitude of DA in the benthic environment, and monthly observations of sediments and benthic infauna at multiple stations over a 16-month period. DA was widespread in continental shelf sediments of the SCB. The toxin was detected in 54% of all shelf habitats sampled. Detectable concentrations ranged from 0.11 ng/g to 1.36 ng/g. DA was consistently detected in benthic infauna tissues over the monthly timeseries, while the DA concentrations in sediments during the same period were commonly below detection or at low concentrations. The presence of DA in the benthic environment did not always have an apparent water column source, raising the possibility of lateral transport, retention/preservation in sediments or undetected blooms in subsurface waters. In most cases, DA was detected in tissues but not in the co-located surface sediments. Coarse taxonomic sorting of the infauna revealed that the accumulation of DA varied among taxa. We observed that DA was widespread among lower trophic level organisms in this study, potentially acting as a persistent source of DA to higher trophic levels in the benthos.

Synthesis of ecotoxicological studies on cyanotoxins in freshwater habitats - Evaluating the basis for developing thresholds protective of aquatic life in the United States.

In recent decades, cyanobacteria harmful algal blooms (cyanoHABs) have increased in magnitude, frequency, and duration in freshwater ecosystems. CyanoHABs can impact water quality by the production of potent toxins known as cyanotoxins. Environmental exposure to cyanotoxins has been associated with severe illnesses in humans, domestic animals, and wildlife. However, the effects of sustained exposure to cyanotoxins on aquatic life are poorly understood. In this study, over 150 peer-reviewed articles were critically evaluated to better understand the ecotoxicity of 5 cyanotoxin classes (microcystins, cylindrospermopsin, anatoxin-a, saxitoxins, nodularin) on fish, amphibians, aquatic invertebrates, and birds exclusively feeding in freshwater habitats. The systemic review demonstrated that microcystins, and more specifically microcystin-LR, were the most studied cyanotoxins. Ecotoxicological investigations were typically conducted using a fish or aquatic invertebrate model, with mortality, bioaccumulation, and biochemical responses as the most frequently measured endpoints. After excluding the studies that did not meet our acceptability criteria, remaining studies were examined to identify the no-observed and lowest observed effect concentrations (NOEC and LOEC) for microcystins; the limited amount of data for other cyanotoxins did not allow for analysis. The published ecotoxicity data suggests that the U.S. EPA recreational water quality criteria for microcystin (8 µg/L) may be protective of acute toxicity in aquatic organisms but does not appear to protect against chronic toxicity. Individual U.S. states have developed more stringent recreational health-based thresholds, such as 0.8 µg/L in California. Comparisons of this threshold to the chronic NOEC and LOEC data indicate that more restrictive microcystins thresholds may be required to be protective of aquatic life. Additional research is needed to evaluate the sublethal effects of a wider array of microcystin congeners and other cyanotoxins on organisms relevant to U.S. watersheds to better support nationwide thresholds protective of aquatic life.

Multiple co-occurring and persistently detected cyanotoxins and associated cyanobacteria in adjacent California lakes.

The global proliferation of toxin producing cyanobacterial blooms has been attributed to a wide variety of environmental factors with nutrient pollution, increased temperatures, and drought being three of the most significant. The current study is the first formal assessment of cyanotoxins in two impaired lakes, Canyon Lake and Lake Elsinore, in southern California that have a history of cyanobacterial blooms producing high biomass as measured by chl-a. Cyanotoxins in Lake Elsinore were detected at concentrations that persistently exceeded California recreational health thresholds, whereas Canyon Lake experienced persistent concentrations that only occasionally exceeded health thresholds. The study results are the highest recorded concentrations of microcystins, anatoxin-a, and cylindrospermopsin detected in southern California lakes. Concentrations exceeded health thresholds that caused both lakes to be closed for recreational activities. Cyanobacterial identifications indicated a high risk for the presence of potentially toxic genera and agreed with the cyanotoxin results that indicated frequent detection of multiple cyanotoxins simultaneously. A statistically significant correlation was observed between chlorophyll-a (chl-a) and microcystin concentrations for Lake Elsinore but not Canyon Lake, and chl-a was not a good indicator of cylindrospermopsin, anatoxin-a, or nodularin. Therefore, chl-a was not a viable screening indicator of cyanotoxin risk in these lakes. The study results indicate potential acute and chronic risk of exposure to cyanotoxins in these lakes and supports the need for future monitoring efforts to help minimize human and domestic pet exposure and to better understand potential effects to wildlife. The frequent co-occurrence of complex cyanotoxin mixtures further complicates the risk assessment process for these lakes given uncertainty in the toxicology of mixtures.

A decade and a half of Pseudo-nitzschia spp. and domoic acid along the coast of southern California.

Blooms of the marine diatom genus Pseudo-nitzschia that produce the neurotoxin domoic acid have been documented with regularity along the coast of southern California since 2003, with the occurrence of the toxin in shellfish tissue predating information on domoic acid in the particulate fraction in this region. Domoic acid concentrations in the phytoplankton inhabiting waters off southern California during 2003, 2006, 2007, 2011 and 2017 were comparable to some of the highest values that have been recorded in the literature. Blooms of Pseudo-nitzschia have exhibited strong seasonality, with toxin appearing predominantly in the spring. Year-to-year variability of particulate toxin has been considerable, and observations during 2003, 2006, 2007, 2011 and again in 2017 linked domoic acid in the diets of marine mammals and seabirds to mass mortality events among these animals. This work reviews information collected during the past 15 years documenting the phenology and magnitude of Pseudo-nitzschia abundances and domoic acid within the Southern California Bight. The general oceanographic factors leading to blooms of Pseudo-nitzschia and outbreaks of domoic acid in this region are clear, but subtle factors controlling spatial and interannual variability in bloom magnitude and toxin production remain elusive.

Microcystin Prevalence throughout Lentic Waterbodies in Coastal Southern California.

Toxin producing cyanobacterial blooms have increased globally in recent decades in both frequency and intensity. Despite the recognition of this growing risk, the extent and magnitude of cyanobacterial blooms and cyanotoxin prevalence is poorly characterized in the heavily populated region of southern California. Recent assessments of lentic waterbodies (depressional wetlands, lakes, reservoirs and coastal lagoons) determined the prevalence of microcystins and, in some cases, additional cyanotoxins. Microcystins were present in all waterbody types surveyed although toxin concentrations were generally low across most habitats, as only a small number of sites exceeded California's recreational health thresholds for acute toxicity. Results from passive samplers (Solid Phase Adsorption Toxin Tracking (SPATT)) indicated microcystins were prevalent throughout lentic waterbodies and that traditional discrete samples underestimated the presence of microcystins. Multiple cyanotoxins were detected simultaneously in some systems, indicating multiple stressors, the risk of which is uncertain since health thresholds are based on exposures to single toxins. Anatoxin-a was detected for the first time from lakes in southern California. The persistence of detectable microcystins across years and seasons indicates a low-level, chronic risk through both direct and indirect exposure. The influence of toxic cyanobacterial blooms is a more complex stressor than presently recognized and should be included in water quality monitoring programs.

Multiple Stressors at the Land-Sea Interface: Cyanotoxins at the Land-Sea Interface in the Southern California Bight.

Blooms of toxic cyanobacteria in freshwater ecosystems have received considerable attention in recent years, but their occurrence and potential importance at the land-sea interface has not been widely recognized. Here we present the results of a survey of discrete samples conducted in more than fifty brackish water sites along the coastline of southern California. Our objectives were to characterize cyanobacterial community composition and determine if specific groups of cyanotoxins (anatoxins, cylindrospermopsins, microcystins, nodularins, and saxitoxins) were present. We report the identification of numerous potentially harmful taxa and the co-occurrence of multiple toxins, previously undocumented, at several locations. Our findings reveal a potential health concern based on the range of organisms present and the widespread prevalence of recognized toxic compounds. Our results raise concerns for recreation, harvesting of finfish and shellfish, and wildlife and desalination operations, highlighting the need for assessments and implementation of monitoring programs. Such programs appear to be particularly necessary in regions susceptible to urban influence.

Are harmful algal blooms becoming the greatest inland water quality threat to public health and aquatic ecosystems?

In this Focus article, the authors ask a seemingly simple question: Are harmful algal blooms (HABs) becoming the greatest inland water quality threat to public health and aquatic ecosystems? When HAB events require restrictions on fisheries, recreation, and drinking water uses of inland water bodies significant economic consequences result. Unfortunately, the magnitude, frequency, and duration of HABs in inland waters are poorly understood across spatiotemporal scales and differentially engaged among states, tribes, and territories. Harmful algal bloom impacts are not as predictable as those from conventional chemical contaminants, for which water quality assessment and management programs were primarily developed, because interactions among multiple natural and anthropogenic factors determine the likelihood and severity to which a HAB will occur in a specific water body. These forcing factors can also affect toxin production. Beyond site-specific water quality degradation caused directly by HABs, the presence of HAB toxins can negatively influence routine surface water quality monitoring, assessment, and management practices. Harmful algal blooms present significant challenges for achieving water quality protection and restoration goals when these toxins confound interpretation of monitoring results and environmental quality standards implementation efforts for other chemicals and stressors. Whether HABs presently represent the greatest threat to inland water quality is debatable, though in inland waters of developed countries they typically cause more severe acute impacts to environmental quality than conventional chemical contamination events. The authors identify several timely research needs. Environmental toxicology, environmental chemistry, and risk-assessment expertise must interface with ecologists, engineers, and public health practitioners to engage the complexities of HAB assessment and management, to address the forcing factors for HAB formation, and to reduce the threats posed to inland surface water quality.

Development, comparison, and validation using ELISAs for the determination of domoic acid in California sea lion body fluids.

Mortalities of California sea lions (Zalophus californianus) attributed to the neurotoxin domoic acid (DA) produced by the diatom Pseudo-nitzschia have occurred repeatedly along the U.S. west coast since the late 1990s. Quantifying the amount of DA in these animals and correlating this information with the presence of DA in phytoplankton and the local food web has become a research focus for many scientists. However, differences in materials, equipment, technical capability, budgets, and objectives of the various groups and/or agencies involved in this work have influenced the DA quantification platforms used. The goal of the present study was to compare the performance of two commercially available ELISAs for the determination of DA in a spectrum of California sea lion body fluids and to compare the results with LC/MS of the same samples. The results indicated differences among these approaches, presumably owing to matrix effects (particularly urine) and antibody reactivities. This information implies that care should be taken in attempting to compare datasets generated using different analytical platforms and interpreting the results of published studies.

Seasonal and annual dynamics of harmful algae and algal toxins revealed through weekly monitoring at two coastal ocean sites off southern California, USA.

Reports of toxic harmful algal blooms (HABs) attributed to the diatom Pseudo-nitzschia spp. have been increasing in California during the last several decades. Whether this increase can be attributed to enhanced awareness and monitoring or to a dramatic upswing in the development of HAB events remains unresolved. Given these uncertainties, the ability to accurately and rapidly identify an emerging HAB event is of high importance. Monitoring of HAB species and other pertinent chemical/physical parameters at two piers in southern California, Newport and Redondo Beach, was used to investigate the development of a site-specific bloom definition for identifying emerging domoic acid (DA) events. Emphasis was given to abundances of the Pseudo-nitzschia seriata size category of Pseudo-nitzschia due to the prevalence of this size class in the region. P. seriata bloom thresholds were established for each location based on deviations from their respective long-term mean abundances, allowing the identification of major and minor blooms. Sixty-five percent of blooms identified at Newport Beach coincided with measurable DA concentrations, while 36 % of blooms at Redondo Beach coincided with measurable DA. Bloom definitions allowed for increased specificity in multiple regression analysis of environmental forcing factors significant to the presence of DA and P. seriata. The strongest relationship identified was between P. seriata abundances 2 weeks following upwelling events at Newport Beach.

QUANTITATIVE REAL-TIME POLYMERASE CHAIN REACTION FOR COCHLODINIUM FULVESCENS (DINOPHYCEAE), A HARMFUL DINOFLAGELLATE FROM CALIFORNIA COASTAL WATERS(1).

Harmful blooms formed by species of the dinoflagellate Cochlodinium have caused massive fish kills and substantial economic losses in the Pacific Ocean. Recently, prominent blooms of Cochlodinium have occurred in central and southern California (2004-2008), and Cochlodinium cells are now routinely observed in microscopical analysis of algal assemblages from Californian coastal waters. The first documented economic loss due to a Cochlodinium bloom in California occurred in Monterey Bay and resulted in the mortality of commercially farmed abalone. Increasing occurrences of Cochlodinium blooms, the fact that these cells preserve poorly using standard techniques, and the difficulty of identifying preserved specimens using morphological criteria make Cochlodinium species prime candidates for the development of a quantitative real-time polymerase chain reaction (qPCR) approach. The 18S rDNA gene sequenced from Cochlodinium cells obtained from California coastal waters, as well as GenBank sequences of Cochlodinium, were used to design and test a Molecular Beacon(®) approach. The qPCR method developed in this study is species specific, sensitive for the detection of C. fulvescens that has given rise to the recent blooms in the eastern Pacific Ocean, and spans a dynamic abundance range of seven orders of magnitude. Initial application of the method to archived field samples collected during blooms in Monterey Bay revealed no statistically significant correlations between gene copy number and environmental parameters. However, the onset of Cochlodinium blooms in central California was consistent with previously reported findings of correlations to decreased surface temperature and increased inputs of nitrogenous nutrients.

Harmful algae and their potential impacts on desalination operations off southern California.

Seawater desalination by reverse osmosis (RO) is a reliable method for augmenting drinking water supplies. In recent years, the number and size of these water projects have increased dramatically. As freshwater resources become limited due to global climate change, rising demand, and exhausted local water supplies, seawater desalination will play an important role in the world's future water supply, reaching far beyond its deep roots in the Middle East. Emerging contaminants have been widely discussed with respect to wastewater and freshwater sources, but also must be considered for seawater desalination facilities to ensure the long-term safety and suitability of this emerging water supply. Harmful algal blooms, frequently referred to as 'red tides' due to their vibrant colors, are a concern for desalination plants due to the high biomass of microalgae present in ocean waters during these events, and a variety of substances that some of these algae produce. These compounds range from noxious substances to powerful neurotoxins that constitute significant public health risks if they are not effectively and completely removed by the RO membranes. Algal blooms can cause significant operational issues that result in increased chemical consumption, increased membrane fouling rates, and in extreme cases, a plant to be taken off-line. Early algal bloom detection by desalination facilities is essential so that operational adjustments can be made to ensure that production capacity remains unaffected. This review identifies the toxic substances, their known producers, and our present state of knowledge regarding the causes of toxic episodes, with a special focus on the Southern California Bight.

Phylogenetic relationships of yessotoxin-producing dinoflagellates, based on the large subunit and internal transcribed spacer ribosomal DNA domains.

Yessotoxin (YTX) is a globally distributed marine toxin produced by some isolates of the dinoflagellate species Protoceratium reticulatum, Lingulodinium polyedrum, and Gonyaulax spinifera within the order Gonyaulacales. The process of isolating cells and testing each isolate individually for YTX production during toxic blooms are labor intensive, and this impedes our ability to respond quickly to toxic blooms. In this study, we used molecular sequences from the large subunit and internal transcribed spacer genomic regions in the ribosomal operon of known YTX-producing dinoflagellates to determine if genetic differences exist among geographically distinct populations or between toxic and nontoxic isolates within species. In all analyses, all three YTX-producing species fell within the Gonyaulacales order in agreement with morphological taxonomy. Phylogenetic analyses of available rRNA gene sequences indicate that the capacity for YTX production appears to be confined to the order Gonyaulacales. These findings indicate that Gonyaulacoloid dinoflagellate species are the most likely to produce YTX and thus should be prioritized for YTX screening during events. Dinoflagellate species that fall outside of the Gonyaulacales order are unlikely to produce YTX. Although the rRNA operon offers multiple sequence domains to resolve species level diversification within this dinoflagellate order, these domains are not sufficiently variable to provide robust markers for YTX toxicity.