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.

Dinoflagellate vertical migration fuels an intense red tide.

Harmful algal blooms (HABs) are increasing globally, causing economic, human health, and ecosystem harm. In spite of the frequent occurrence of HABs, the mechanisms responsible for their exceptionally high biomass remain imperfectly understood. A 50-y-old hypothesis posits that some dense blooms derive from dinoflagellate motility: organisms swim upward during the day to photosynthesize and downward at night to access deep nutrients. This allows dinoflagellates to outgrow their nonmotile competitors. We tested this hypothesis with in situ data from an autonomous, ocean-wave-powered vertical profiling system. We showed that the dinoflagellate Lingulodinium polyedra's vertical migration led to depletion of deep nitrate during a 2020 red tide HAB event. Downward migration began at dusk, with the maximum migration depth determined by local nitrate concentrations. Losses of nitrate at depth were balanced by proportional increases in phytoplankton chlorophyll concentrations and suspended particle load, conclusively linking vertical migration to the access and assimilation of deep nitrate in the ocean environment. Vertical migration during the red tide created anomalous biogeochemical conditions compared to 70 y of climatological data, demonstrating the capacity of these events to temporarily reshape the coastal ocean's ecosystem and biogeochemistry. Advances in the understanding of the physiological, behavioral, and metabolic dynamics of HAB-forming organisms from cutting-edge observational techniques will improve our ability to forecast HABs and mitigate their consequences in the future.

A marine protected area network does not confer community structure resilience to a marine heatwave across coastal ecosystems.

Marine protected areas (MPAs) have gained attention as a conservation tool for enhancing ecosystem resilience to climate change. However, empirical evidence explicitly linking MPAs to enhanced ecological resilience is limited and mixed. To better understand whether MPAs can buffer climate impacts, we tested the resistance and recovery of marine communities to the 2014-2016 Northeast Pacific heatwave in the largest scientifically designed MPA network in the world off the coast of California, United States. The network consists of 124 MPAs (48 no-take state marine reserves, and 76 partial-take or special regulation conservation areas) implemented at different times, with full implementation completed in 2012. We compared fish, benthic invertebrate, and macroalgal community structure inside and outside of 13 no-take MPAs across rocky intertidal, kelp forest, shallow reef, and deep reef nearshore habitats in California's Central Coast region from 2007 to 2020. We also explored whether MPA features, including age, size, depth, proportion rock, historic fishing pressure, habitat diversity and richness, connectivity, and fish biomass response ratios (proxy for ecological performance), conferred climate resilience for kelp forest and rocky intertidal habitats spanning 28 MPAs across the full network. Ecological communities dramatically shifted due to the marine heatwave across all four nearshore habitats, and MPAs did not facilitate habitat-wide resistance or recovery. Only in protected rocky intertidal habitats did community structure significantly resist marine heatwave impacts. Community shifts were associated with a pronounced decline in the relative proportion of cold water species and an increase in warm water species. MPA features did not explain resistance or recovery to the marine heatwave. Collectively, our findings suggest that MPAs have limited ability to mitigate the impacts of marine heatwaves on community structure. Given that mechanisms of resilience to climate perturbations are complex, there is a clear need to expand assessments of ecosystem-wide consequences resulting from acute climate-driven perturbations, and the potential role of regulatory protection in mitigating community structure changes.

Stable isotope analysis reveals differences in domoic acid accumulation and feeding strategies of key vectors in a California hotspot for outbreaks.

Given the effects of harmful algal blooms (HABs) on human and wildlife health, understanding how domoic acid (DA) is accumulated and transferred through food webs is critical for recognizing the most affected marine communities and predicting ecosystem effects. This study combines stable isotopes of carbon (δ13C) and nitrogen (δ15N) from bulk muscle tissue with DA measurements from viscera to identify the foraging strategies of important DA vectors and predators in Monterey Bay, CA. Tissue samples were collected from 27 species across three habitats in the summer of 2018 and 2019 (time periods without prominent HABs). Our results highlight an inshore-offshore variation in krill δ13C values and DA concentrations ([DA]; ppm) in anchovies indicating differences in coastal productivity and DA accumulation. The narrow overlapping isotopic niches between anchovies and sardines suggest similar diets and trophic positions, but striking differences in [DA] indicate a degree of specialization, thus, resource partitioning. In contrast, krill, market squid, and juvenile rockfish accumulated minimal DA and had comparatively broad isotopic niches, suggesting a lower capacity to serve as vectors because of potential differences in diet or feeding in isotopically distinct locations. Low [DA] in the liver of stranded sea lions and their generalist foraging tendencies limits our ability to use them as sentinels for DA outbreaks in a specific geographic area. Collectively, our results show that DA was produced a few kilometers from the coastline, and anchovies were the most powerful DA vector in coastal-pelagic zones (their DA loads exceeded the 20 ppm FDA regulatory limits for human consumption), while mussels did not contain detectable DA and only reflect in situ DA, δ13C, and δ15N values. Our study demonstrates the efficacy of combining multiple biogeochemical tracers to improve HAB monitoring efforts and identify the main routes of DA transfer across habitats and trophic levels.

A Time Series of Water Column Distributions and Sinking Particle Flux of Pseudo-Nitzschia and Domoic Acid in the Santa Barbara Basin, California.

Water column bulk Pseudo-nitzschia abundance and the dissolved and particulate domoic acid (DA) concentrations were measured in the Santa Barbara Basin (SBB), California from 2009⁻2013 and compared to bulk Pseudo-nitzschia cell abundance and DA concentrations and fluxes in sediment traps moored at 147 m and 509 m. Pseudo-nitzschia abundance throughout the study period was spatially and temporally heterogeneous (<200 cells L-1 to 3.8 × 106 cells L-1, avg. 2 × 105 ± 5 × 105 cells L-1) and did not correspond with upwelling conditions or the total DA (tDA) concentration, which was also spatially and temporally diverse (<1.3 ng L-1 to 2.2 × 105 ng L-1, avg. 7.8 × 10³ ± 2.2 × 104 ng L-1). We hypothesize that the toxicity is likely driven in part by specific Pseudo-nitzschia species as well as bloom stage. Dissolved (dDA) and particulate (pDA) DA were significantly and positively correlated (p < 0.01) and both comprised major components of the total DA pool (pDA = 57 ± 35%, and dDA = 42 ± 35%) with substantial water column concentrations (>1000 cells L-1 and tDA = 200 ng L-1) measured as deep as 150 m. Our results highlight that dDA should not be ignored when examining bloom toxicity. Although water column abundance and pDA concentrations were poorly correlated with sediment trap Pseudo-nitzschia abundance and fluxes, DA toxicity is likely associated with senescent blooms that rapidly sink to the seafloor, adding another potential source of DA to benthic organisms.

Initial skill assessment of the California Harmful Algae Risk Mapping (C-HARM) system.

Toxic algal events are an annual burden on aquaculture and coastal ecosystems of California. The threat of domoic acid (DA) toxicity to human and wildlife health is the dominant harmful algal bloom (HAB) concern for the region, leading to a strong focus on prediction and mitigation of these blooms and their toxic effects. This paper describes the initial development of the California Harmful Algae Risk Mapping (C-HARM) system that predicts the spatial likelihood of blooms and dangerous levels of DA using a unique blend of numerical models, ecological forecast models of the target group, Pseudo-nitzschia, and satellite ocean color imagery. Data interpolating empirical orthogonal functions (DINEOF) are applied to ocean color imagery to fill in missing data and then used in a multivariate mode with other modeled variables to forecast biogeochemical parameters. Daily predictions (nowcast and forecast maps) are run routinely at the Central and Northern California Ocean Observing System (CeNCOOS) and posted on its public website. Skill assessment of model output for the nowcast data is restricted to nearshore pixels that overlap with routine pier monitoring of HABs in California from 2014 to 2015. Model lead times are best correlated with DA measured with solid phase adsorption toxin tracking (SPATT) and marine mammal strandings from DA toxicosis, suggesting long-term benefits of the HAB predictions to decision-making. Over the next three years, the C-HARM application system will be incorporated into the NOAA operational HAB forecasting system and HAB Bulletin.