Investigation of a Mass Stranding Event Reveals a Novel Pattern of Cascading Comorbidities in Northern Fulmars (Fulmarus glacialis).

During 2018, a seabird mortality event occurred in central California, US, that affected Northern Fulmars (Fulmarus glacialis), Common Murres (Uria aalge), and Cassin's Auklets (Ptychoramphus aleuticus). An increase in beachcast birds were reported on standardized surveys in conjunction with an increased number of live-stranded birds admitted to rehabilitation centers. Neurologic symptoms were noted during intake examination for some birds. Coincident with the mortality event, increased levels of the harmful algal bloom toxins domoic acid and saxitoxin were recorded in Monterey Bay and Morro Bay. Birds that died in care and beachcast carcasses were submitted to the California Department of Fish and Wildlife-Marine Wildlife Veterinary Care and Research Center for postmortem examination (n=24). All examined birds were emaciated. Examined Common Murres and Cassin's Auklets had no gross evidence of preexisting disease; however, all examined Northern Fulmars exhibited severe pyogranulomatous inflammation of the urogenital system at gross postmortem exam. Tissues from nine Northern Fulmars were examined by histopathology, and samples from two Northern Fulmars were tested for the presence of domoic acid and saxitoxin. Histopathology revealed moderate to severe kidney infection by Eimeria sp. and gram-negative bacteria, intratubular urate stasis, ureter rupture, and emaciation. Additionally, domoic acid and saxitoxin were detected simultaneously in tissues of some tested birds. This communication highlights a novel pattern of cascading comorbidities in native seabirds from a mass stranding event.

What happens in the shadows - Influence of seasonal and non-seasonal dynamics on domoic acid monitoring in the Monterey Bay upwelling shadow.

Domoic acid produced by toxigenic Pseudo-nitzschia species is the main toxin threat from harmful algal blooms in Monterey Bay and the larger California Current region on the West Coast of the United States. Toxin monitoring in Monterey Bay includes a long-running time series of weekly measurements of domoic acid from water samples, sentinel mussels, and solid phase adsorption toxin tracking (SPATT) at the Santa Cruz Municipal Wharf (SCW). The SCW sampling site is unusual because of its position in the Monterey Bay upwelling shadow in the north bay. The upwelling shadow circulation pattern has been previously characterized as a bloom incubator for dinoflagellates, but it has not yet been analyzed in the context of long-term monitoring methods. In data collected from the SCW from 2012 - 2020, domoic acid from water samples and sentinel mussels had a different temporal distribution than domoic acid from SPATT. Here we explore the discrepancy through a seasonal and non-seasonal analysis including physical oceanography of the region. Results show that domoic acid from water samples and sentinel mussels are related to seasonal upwelling and Pseudo-nitzschia blooms. Domoic acid monitored by SPATT, on the other hand, is correlated to anomalous upwelling and warmer than usual temperatures during the relaxation season. This work builds on previous analyses of the SCW time series and contributes to understanding of the circulation of dissolved toxin in the environment. Results lend rationale for the continuation of rigorous domoic acid monitoring in Monterey Bay and encourage stakeholders to consider local physical dynamics when interpreting toxin monitoring data.

Molecular Forecasting of Domoic Acid during a Pervasive Toxic Diatom Bloom.

In 2015, the largest recorded harmful algal bloom (HAB) occurred in the Northeast Pacific, causing nearly 100 million dollars in damages to fisheries and killing many protected marine mammals. Dominated by the toxic diatom Pseudo-nitzschia australis , this bloom produced high levels of the neurotoxin domoic acid (DA). Through molecular and transcriptional characterization of 52 near-weekly phytoplankton net-tow samples collected at a bloom hotspot in Monterey Bay, California, we identified active transcription of known DA biosynthesis ( dab ) genes from the three identified toxigenic species, including P. australis as the primary origin of toxicity. Elevated expression of silicon transporters ( sit1 ) during the bloom supports the previously hypothesized role of dissolved silica (Si) exhaustion in contributing to bloom physiology and toxicity. We find that co-expression of the dabA and sit1 genes serves as a robust predictor of DA one week in advance, potentially enabling the forecasting of DA-producing HABs. We additionally present evidence that low levels of iron could have co-limited the diatom population along with low Si. Iron limitation represents a previously unrecognized driver of both toxin production and ecological success of the low iron adapted Pseudo-nitzschia genus during the 2015 bloom, and increasing pervasiveness of iron limitation may fuel the escalating magnitude and frequency of toxic Pseudo-nitzschia blooms globally. Our results advance understanding of bloom physiology underlying toxin production, bloom prediction, and the impact of global change on toxic blooms. Significance: Pseudo-nitzschia diatoms form oceanic harmful algal blooms that threaten human health through production of the neurotoxin domoic acid (DA). DA biosynthetic gene expression is hypothesized to control DA production in the environment, yet what regulates expression of these genes is yet to be discovered. In this study, we uncovered expression of DA biosynthesis genes by multiple toxigenic Pseudo-nitzschia species during an economically impactful bloom along the North American West Coast, and identified genes that predict DA in advance of its production. We discovered that iron and silica co-limitation restrained the bloom and likely promoted toxin production. This work suggests that increasing iron limitation due to global change may play a previously unrecognized role in driving bloom frequency and toxicity.

A cross-regional examination of patterns and environmental drivers of Pseudo-nitzschia harmful algal blooms along the California coast.

Pseudo-nitzschia species with the ability to produce the neurotoxin domoic acid (DA) are the main cause of harmful algal blooms (HABs) along the U.S. West Coast, with major impacts on ecosystems, fisheries, and human health. While most Pseudo-nitzschia (PN) HAB studies to date have focused on their characteristics at specific sites, few cross-regional comparisons exist, and mechanistic understanding of large-scale HAB drivers remains incomplete. To close these gaps, we compiled a nearly 20-year time series of in situ particulate DA and environmental observations to characterize similarities and differences in PN HAB drivers along the California coast. We focus on three DA hotspots with the greatest data density: Monterey Bay, the Santa Barbara Channel, and the San Pedro Channel. Coastwise, DA outbreaks are strongly correlated with upwelling, chlorophyll-a, and silicic acid limitation relative to other nutrients. Clear differences also exist across the three regions, with contrasting responses to climate regimes across a north to south gradient. In Monterey Bay, PN HAB frequency and intensity increase under relatively nutrient-poor conditions during anomalously low upwelling intensities. In contrast, in the Santa Barbara and San Pedro Channels, PN HABs are favored under cold, nitrogen-rich conditions during more intense upwelling. These emerging patterns provide insights on ecological drivers of PN HABs that are consistent across regions and support the development of predictive capabilities for DA outbreaks along the California coast and beyond.

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).

Development, calibration, and evaluation of a model of Pseudo-nitzschia and domoic acid production for regional ocean modeling studies.

Pseudo-nitzschia species are one of the leading causes of harmful algal blooms (HABs) along the western coast of the United States. Approximately half of known Pseudo-nitzschia strains can produce domoic acid (DA), a neurotoxin that can negatively impact wildlife and fisheries and put human life at risk through amnesic shellfish poisoning. Production and accumulation of DA, a secondary metabolite synthesized during periods of low primary metabolism, is triggered by environmental stressors such as nutrient limitation. To quantify and estimate the feedbacks between DA production and environmental conditions, we designed a simple mechanistic model of Pseudo-nitzschia and domoic acid dynamics, which we validate against batch and chemostat experiments. Our results suggest that, as nutrients other than nitrogen (i.e., silicon, phosphorus, and potentially iron) become limiting, DA production increases. Under Si limitation, we found an approximate doubling in DA production relative to N limitation. Additionally, our model indicates a positive relationship between light and DA production. These results support the idea that the relationship with nutrient limitation and light is based on direct impacts on Pseudo-nitzschia biosynthesis and biomass accumulation. Because it can easily be embedded within existing coupled physical-ecosystem models, our model represents a step forward toward modeling the occurrence of Pseudo-nitzschia HABs and DA across the U.S. West Coast.

Hepatotoxic shellfish poisoning: Accumulation of microcystins in Eastern oysters (Crassostrea virginica) and Asian clams (Corbicula fluminea) exposed to wild and cultured populations of the harmful cyanobacteria, Microcystis.

The Asian clam (Corbicula fluminea) and eastern oyster (Crassostrea virginica) are important resource bivalves found in and downstream of waterways afflicted with cyanobacterial harmful algae blooms (CHABs), respectively. This study examined the potential for C. fluminea and C. virginica to become vectors of the hepatotoxin, microcystin, from the CHAB Microcystis. Laboratory experiments were performed to quantify clearance rates, particle selection, and accumulation of the hepatotoxin, microcystin, using a microcystin-producing Microcystis culture isolated from Lake Erie (strain LE-3) and field experiments were performed with water from Microcystis blooms in Lake Agawam, NY, USA. Clearance rates of Microcystis were faster (p<0.05) than those of Raphidocelis for C. fluminea, while C. virginica cleared Microcystis and Tisochrysis at similar rates. For both bivalves, clearance rates of bloom water were slower than cultures and clams displayed significantly greater electivity for green algae compared to wild populations of cyanobacteria in field experiments while oysters did not. In experiments with cultured Microcystis comprised of single and double cells, both bivalves accumulated >3 µg microcystins g - 1 (wet weight) in 24 - 72 h, several orders of magnitude beyond California guidance value (10 ng g - 1) but accumulated only up to 2 ng microcystins g - 1 when fed bloom water dominated by large Microcystis colonies for four days. For Asian clams, clearance rates and tissue microcystin content decreased when exposed to toxic Microcystis for 3 - 4 days. In contrast, eastern oysters did not depurate microcystin over 3 - 4-day exposures and accumulated an order of magnitude more microcystin than clams. This contrast suggests Asian clams are likely to accumulate minor amounts of microcystin by reducing clearance rates during blooms of Microcystis, selectively feeding on green algae, and depurating microcystin whereas oysters are more likely to accumulate microcystins and thus are more likely to be a vector for hepatotoxic shellfish poisoning in estuaries downstream of Microcystis blooms.

Modeling hyperspectral normalized water-leaving radiance in a dynamic coastal ecosystem.

Next-generation satellite sensors such as the Ocean Color Instrument (OCI) aboard the NASA Plankton, Aerosols, Cloud and ocean Ecosystem (PACE) satellite and the proposed Surface Biology and Geology (SBG) sensor will provide hyperspectral measurements of water-leaving radiances. However, acquiring sufficiently accurate in situ validation data in coastal ecosystems remains challenging. Here we modeled hyperspectral normalized water-leaving radiance ([LW(λ)]N) in a dynamic coastal ecosystem using in situ inherent optical properties (IOPs) as inputs to the Hydrolight radiative transfer model. By reducing uncertainty of modeled hyperspectral [LW(λ)]N (%RMSE ≤ 21%) relative to [LW(λ)]N derived from in situ radiometric measurements (%RMSE ≤ 33%), we introduce modeling as an alternative or complementary method to in-water radiometric profilers for validating satellite-derived hyperspectral data from coastal ecosystems.

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.

The tide turns: Episodic and localized cross-contamination of a California coastline with cyanotoxins.

The contamination of coastal ecosystems from a variety of toxins of marine algal origin is a common and well-documented situation along the coasts of the United States and globally. The occurrence of toxins originating from cyanobacteria along marine coastlines is much less studied, and little information exists on whether toxins from marine and freshwater sources co-occur regularly. The current study focused on the discharge of cyanotoxins from a coastal lagoon (Santa Clara River Estuary) as a consequence of an extreme tide event (King Tides; December 3-5, 2017) resulting in a breach of the berm separating the lagoon from the ocean. Monthly monitoring in the lagoon throughout 2017 documented more than a dozen co-occurring cyanobacterial genera, as well as multiple algal and cyanobacterial toxins. Biotoxin monitoring before and following the King Tide event using Solid Phase Adsorption Toxin Tracking (SPATT) in the lagoon and along the coast revealed the co-occurrence of microcystins, anatoxin, domoic acid, and other toxins on multiple dates and locations. Domoic acid was ubiquitously present in SPATT deployed in the lagoon and along the coast. Microcystins were also commonly detected in both locations, although the beach berm retained the lagoonal water for much of the year. Mussels collected along the coast contained microcystins in approximately half the samples, particularly following the King Tide event. Anatoxin was observed in SPATT only in late December, following the breach of the berm. Our findings indicate both episodic and persistent occurrence of both cyanotoxins and marine toxins may commonly contaminate coastlines in proximity to cyanobacteria-laden creeks and lagoons.

Domoic acid and saxitoxin in seabirds in the United States between 2007 and 2018.

As harmful algal blooms (HABs) increase in magnitude and duration worldwide, they are becoming an expanding threat to marine wildlife. Over the past decade, blooms of algae that produce the neurotoxins domoic acid (DA) and saxitoxin (STX) and documented concurrent seabird mortality events have increased bicoastally in the United States. We conducted a retrospective analysis of HAB related mortality events in California, Washington, and Rhode Island between 2007 and 2018 involving 12 species of seabirds, to document the levels, ranges, and patterns of DA and STX in eight sample types (kidney, liver, stomach, intestinal, cloacal, cecal contents, bile, blood) collected from birds during these events. Samples (n = 182) from 83 birds were examined for DA (n = 135) or STX (n = 17) or both toxins simultaneously (n = 30), using ELISA or LCMS at the National Oceanographic and Atmospheric Administration, National Marine Fisheries Service (NOAA-NMFS) Wildlife Algal-toxin Research and Response Network (WARRN-West) or the University of California, Santa Cruz (UCSC). DA or STX was detected in seven of the sample types with STX below the minimum detection limit in blood for the three samples tested. DA was found in 70% and STX was found in 23% of all tested samples. The ranges of detectable levels of DA and STX in all samples were 0.65-681,190.00 ng g-1 and 2.00-20.95 ng g-1, respectively. Cloacal contents from a Pacific loon (Gavia pacifica) collected in 2017 from Ventura County, California, had the highest maximum level of DA for all samples and species tested in this study. The highest level of STX for all samples and species was detected in the bile of a northern fulmar (Fulmarus glacialis) collected in 2018 from San Luis Obispo County, California. DA detections were consistently found in gastrointestinal samples, liver, bile, and kidney, whereas STX detections were most frequently seen in liver and bile samples. Co-occurring HAB toxins (DA and STX) were detected in white-winged scoters (Melanitta deglandi) in 2009, a Brandt's cormorant (Phalacrocorax penicillatus) in 2015, and a northern fulmar and common murre (Uria aalge) in 2018. This article provides DA and STX tissue concentrations and patterns in avian samples and shows the utility of various sample types for the detection of HAB toxins. Future research to understand the pharmacodynamics of these toxins in avian species and to establish lethal doses in various bird species would be beneficial.

Large-scale shift in the structure of a kelp forest ecosystem co-occurs with an epizootic and marine heatwave.

Climate change is responsible for increased frequency, intensity, and duration of extreme events, such as marine heatwaves (MHWs). Within eastern boundary current systems, MHWs have profound impacts on temperature-nutrient dynamics that drive primary productivity. Bull kelp (Nereocystis luetkeana) forests, a vital nearshore habitat, experienced unprecedented losses along 350 km of coastline in northern California beginning in 2014 and continuing through 2019. These losses have had devastating consequences to northern California communities, economies, and fisheries. Using a suite of in situ and satellite-derived data, we demonstrate that the abrupt ecosystem shift initiated by a multi-year MHW was preceded by declines in keystone predator population densities. We show strong evidence that northern California kelp forests, while temporally dynamic, were historically resilient to fluctuating environmental conditions, even in the absence of key top predators, but that a series of coupled environmental and biological shifts between 2014 and 2016 resulted in the formation of a persistent, altered ecosystem state with low primary productivity. Based on our findings, we recommend the implementation of ecosystem-based and adaptive management strategies, such as (1) monitoring the status of key ecosystem attributes: kelp distribution and abundance, and densities of sea urchins and their predators, (2) developing management responses to threshold levels of these attributes, and (3) creating quantitative restoration suitability indices for informing kelp restoration efforts.

Exposure to domoic acid is an ecological driver of cardiac disease in southern sea otters✰.

Harmful algal blooms produce toxins that bioaccumulate in the food web and adversely affect humans, animals, and entire marine ecosystems. Blooms of the diatom Pseudo-nitzschia can produce domoic acid (DA), a toxin that most commonly causes neurological disease in endothermic animals, with cardiovascular effects that were first recognized in southern sea otters. Over the last 20 years, DA toxicosis has caused significant morbidity and mortality in marine mammals and seabirds along the west coast of the USA. Identifying DA exposure has been limited to toxin detection in biological fluids using biochemical assays, yet measurement of systemic toxin levels is an unreliable indicator of exposure dose or timing. Furthermore, there is little information regarding repeated DA exposure in marine wildlife. Here, the association between long-term environmental DA exposure and fatal cardiac disease was investigated in a longitudinal study of 186 free-ranging sea otters in California from 2001 - 2017, highlighting the chronic health effects of a marine toxin. A novel Bayesian spatiotemporal approach was used to characterize environmental DA exposure by combining several DA surveillance datasets and integrating this with life history data from radio-tagged otters in a time-dependent survival model. In this study, a sea otter with high DA exposure had a 1.7-fold increased hazard of fatal cardiomyopathy compared to an otter with low exposure. Otters that consumed a high proportion of crab and clam had a 2.5- and 1.2-times greater hazard of death due to cardiomyopathy than otters that consumed low proportions. Increasing age is a well-established predictor of cardiac disease, but this study is the first to identify that DA exposure affects the risk of cardiomyopathy more substantially in prime-age adults than aged adults. A 4-year-old otter with high DA exposure had 2.3 times greater risk of fatal cardiomyopathy than an otter with low exposure, while a 10-year old otter with high DA exposure had just 1.2 times greater risk. High Toxoplasma gondii titers also increased the hazard of death due to heart disease 2.4-fold. Domoic acid exposure was most detrimental for prime-age adults, whose survival and reproduction are vital for population growth, suggesting that persistent DA exposure will likely impact long-term viability of this threatened species. These results offer insight into the pervasiveness of DA in the food web and raise awareness of under-recognized chronic health effects of DA for wildlife at a time when toxic blooms are on the rise.

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.

Chlorophyll absorption and phytoplankton size information inferred from hyperspectral particulate beam attenuation.

Electromagnetic theory predicts spectral dependencies in extinction efficiency near a narrow absorption band for a particle with an index of refraction close to that of the medium in which it is immersed. These absorption band effects are anticipated in oceanographic beam-attenuation (beam-c) spectra, primarily due to the narrow red peak in absorption produced by the phytoplankton photopigment, chlorophyll a (Chl a). Here we present a method to obtain Chl a absorption and size information by analyzing an eigendecomposition of hyperspectral beam-c residuals measured in marine surface waters by an automatic underway system. We find that three principal modes capture more than 99% of the variance in beam-c residuals at wavelengths near the Chl a red absorption peak. The spectral shapes of the eigenvectors resemble extinction efficiency residuals attributed to the absorption band effects. Projection of the eigenvectors onto the beam-c residuals produces a time series of amplitude functions with absolute values that are strongly correlated to concurrent Chl a absorption line height (aLH) measurements (r values of 0.59 to 0.83) and hence provide a method to estimate Chl a absorption. Multiple linear regression of aLH on the amplitude functions enables an independent estimate of aLH, with RMSE of 3.19⋅10-3m-1 (3.3%) or log10-RMSE of 18.6%, and a raw-scale R2 value of 0.90 based on the Tara Oceans Expedition data. Relationships between the amplitude functions and the beam-c exponential slopes are in agreement with theory relating beam-c to the particle size distribution. Compared to multispectral analysis of beam-c slope, hyperspectral analysis of absorption band effects is anticipated to be relatively insensitive to the addition of nonpigmented particles and to monodispersion.

Unexpected presence of the nitrogen-fixing symbiotic cyanobacterium UCYN-A in Monterey Bay, California.

In the last decade, the known biogeography of nitrogen fixation in the ocean has been expanded to colder and nitrogen-rich coastal environments. The symbiotic nitrogen-fixing cyanobacteria group A (UCYN-A) has been revealed as one of the most abundant and widespread nitrogen-fixers, and includes several sublineages that live associated with genetically distinct but closely related prymnesiophyte hosts. The UCYN-A1 sublineage is associated with an open ocean picoplanktonic prymnesiophyte, whereas UCYN-A2 is associated with the coastal nanoplanktonic coccolithophore Braarudosphaera bigelowii, suggesting that different sublineages may be adapted to different environments. Here, we study the diversity of nifH genes present at the Santa Cruz Municipal Wharf in the Monterey Bay (MB), California, and report for the first time the presence of multiple UCYN-A sublineages, unexpectedly dominated by the UCYN-A2 sublineage. Sequence and quantitative PCR data over an 8-year time-series (2011-2018) showed a shift toward increasing UCYN-A2 abundances after 2013, and a marked seasonality for this sublineage which was present during summer-fall months, coinciding with the upwelling-relaxation period in the MB. Increased abundances corresponded to positive temperature anomalies in MB, and we discuss the possibility of a benthic life stage of the associated coccolithophore host to explain the seasonal pattern. The dominance of UCYN-A2 in coastal waters of the MB underscores the need to further explore the habitat preference of the different sublineages in order to provide additional support for the hypothesis that UCYN-A1 and UCYN-A2 sublineages are different ecotypes.

Is San Francisco Bay resistant to Pseudo-nitzschia and domoic acid?

San Francisco Bay (SFB), California, USA is the largest estuary in the western United States and is home to more than 7 million people in nine counties and 101 cities. It is highly nutrient enriched and is directly connected to the Gulf of the Farallones and coastal Pacific ocean through the Golden Gate strait. The Gulf of the Farallones is one of several "hotspots" for the neurotoxin domoic acid, produced by members of the genus Pseudo-nitzschia. Despite the close proximity, SFB has few reports of harmful algal blooms and low concentrations of domoic acid, suggesting that SFB is somehow resistant to toxic blooms. Here we evaluate the potential growth and toxicity of the dominant toxigenic species in California coastal waters, P. australis and P. multiseries, to directly test the hypothesis that SFB waters confer resistance to blooms. We specifically evaluate the effect of varying temperature, salinity, and to a lesser extent, nutrients on growth and toxin production. Results show equivalent growth in SFB water (maximum growth rates of 0.71 and 1.35 d-1 for P. multiseries and P. australis) compared to open-coast water, and comparable or greater toxicity (0 to >100 pg DA cell-1). The historical resistance to blooms in SFB is hypothesized to be caused by a combination of insufficient acclimation time for advected Pseudo-nitzschia populations to become established and suppression of toxin production in warm waters.

Pelagic harmful algal blooms and climate change: Lessons from nature's experiments with extremes.

Time series now have sufficient duration to determine harmful algal bloom (HAB) responses to changing climate conditions, including warming, stratification intensity, freshwater inputs and natural patterns of climate variability, such as the El Niño Southern Oscillation and Pacific Decadal Oscillation. Against the context of time series, such as those available from phytoplankton monitoring, dinoflagellate cyst records, the Continuous Plankton Recorder surveys, and shellfish toxin records, it is possible to identify extreme events that are significant departures from long-term means. Extreme weather events can mimic future climate conditions and provide a "dress rehearsal" for understanding future frequency, intensity and geographic extent of HABs. Three case studies of extreme HAB events are described in detail to explore the drivers and impacts of these oceanic outliers that may become more common in the future. One example is the chain-forming diatom of the genus Pseudo-nitzschia in the U.S. Pacific Northwest and its response to the 2014-16 northeast Pacific marine heat wave. The other two case studies are pelagic flagellates. Highly potent Alexandrium catenella group 1 dinoflagellate blooms (up to 150 mg/kg PST in mussels; 4 human poisonings) during 2012-17 created havoc for the seafood industry in Tasmania, south-eastern Australia, in a poorly monitored area where such problems were previously unknown. Early evidence suggests that changes in water column stratification during the cold winter-spring season are driving new blooms caused by a previously cryptic species. An expansion of Pseudochattonella cf. verruculosa to the south and A. catenella to the north over the past several years resulted in the convergence of both species to cause the most catastrophic event in the history of the Chilean aquaculture in the austral summer of 2016. Together, these two massive blooms were colloquially known as the "Godzilla-Red tide event", resulting in the largest fish farm mortality ever recorded worldwide, equivalent to an export loss of USD$800 million which when combined with shellfish toxicity, resulted in major social unrest and rioting. Both blooms were linked to the strong El Niño event and the positive phase of the Southern Annular Mode, the latter an indicator of anthropogenic climate change in the southeastern Pacific region. For each of these three examples, representing recent catastrophic events in geographically distinct regions, additional targeted monitoring was employed to improve the understanding of the climate drivers and mechanisms that gave rise to the event and to document the societal response. Scientists must be poised to study future extreme HAB events as these natural experiments provide unique opportunities to define and test multifactorial drivers of blooms.

Trends in Dinophysis abundance and diarrhetic shellfish toxin levels in California mussels (Mytilus californianus) from Monterey Bay, California.

Diarrhetic shellfish toxins (DSTs) are produced by the marine dinoflagellate, Dinophysis, as well as select species of benthic Prorocentrum. The DSTs can bioaccumulate in shellfish and cause gastrointestinal illness when humans consume high levels of this toxin. Although not routinely monitored throughout the U.S., recent studies in Washington, Texas, and New York suggest DSTs may be widespread throughout U.S. coastal waters. This study describes a four-year time series (2013-2016) of Dinophysis concentration and DST level in California mussels (Mytilus californianus) from Santa Cruz Municipal Wharf (SCMW) in Monterey Bay, California. Results show a maximum Dinophysis concentration of 9404 cells/L during this study and suggest Dinophysis persists as a member of the background phytoplankton community throughout the year. In California mussels, DSTs were found at persistent low levels throughout the course of this study, and exceeded the FDA guidance level of 160 ng/g 19 out of 192 weeks sampled. Concentrations of Dinophysis alone are a positive but weak predictor of DST level in California mussels, and basic environmental variables (temperature, salinity, and nutrients) do not sufficiently explain variation in Dinophysis concentration at SCMW. This study demonstrates that Dinophysis in Monterey Bay are producing DSTs that accumulate in local shellfish throughout the year, occasionally reaching levels of concern.