A coastwide bloom of the toxigenic diatom Pseudo‐nitzschia in spring 2015 resulted in the largest recorded outbreak of the neurotoxin, domoic acid, along the North American west coast. Elevated toxins were measured in numerous stranded marine mammals and resulted in geographically extensive and prolonged closures of razor clam, rock crab, and Dungeness crab fisheries. We demonstrate that this outbreak was initiated by anomalously warm ocean conditions. Pseudo‐nitzschia australis thrived north of its typical range in the warm, nutrient‐poor water that spanned the northeast Pacific in early 2015. The seasonal transition to upwelling provided the nutrients necessary for a large‐scale bloom; a series of spring storms delivered the bloom to the coast. Laboratory and field experiments confirming maximum growth rates with elevated temperatures and enhanced toxin production with nutrient enrichment, together with a retrospective analysis of toxic events, demonstrate the potential for similarly devastating ecological and economic disruptions in the future.
A high degree of pseudo-cryptic diversity was reported in the well-studied diatom genus Pseudo-nitzschia. Studies off the coast of Washington State revealed the presence of hitherto undescribed diversity of Pseudo-nitzschia. Forty-one clonal strains, representing six different taxa of the P. pseudodelicatissima complex, were studied morphologically using LM and EM, and genetically using genes from three different cellular compartments: the nucleus (D1-D3 of the LSU of rDNA and internal transcribed spacers [ITSs] of rDNA), the mitochondria (cytochrome c oxidase 1), and the plastids (LSU of RUBISCO). Strains in culture at the same time were used in mating studies to study reproductive isolation of species, and selected strains were examined for the production of the neurotoxin domoic acid (DA). Two new species, P. hasleana sp. nov. and P. fryxelliana sp. nov., are described based on morphological and molecular data. In all phylogenetic analyses, P. hasleana appeared as sister taxa to a clade comprising P. calliantha and P. mannii, whereas the position of P. fryxelliana was more uncertain. In the phylogenies of ITS, P. fryxelliana appeared to be most closely related to P. cf. turgidula. Morphologically, P. hasleana differed from most other species of the complex because of a lower density of fibulae, whereas P. fryxelliana had fewer sectors in the poroids and a higher poroid density than most of the other species. P. hasleana did not produce detectable levels of DA; P. fryxelliana was unfortunately not tested. In P. cuspidata, production of DA in offspring cultures varied from higher than the parent cultures to undetectable.
Sea lion mortalities in central California during May and June 1998 were traced to their ingestion of sardines and anchovies that had accumulated the neurotoxin domoic acid. The detection of toxin in urine, feces, and stomach contents of several sea lions represents the first proven occurrence of domoic acid transfer through the food chain to a marine mammal. The pennate diatoms, Pseudo-nitzschia multiseries and P. australis, were the dominant, toxinproducing phytoplankton constituting algal blooms near Monterey Bay, Half Moon Bay, and Oceano Dunes, areas where sea lions with neurological symptoms stranded. Toxic Pseudo-nitzschia were also found near Morro Bay, Point Conception, Point Arguello, and Santa Barbara, demonstrating that these species were widespread along the central California coast in June 1998. Measurements of domoic acid during three cruises in early June showed the highest cellular toxin levels in P. multiseries near Point Año Nuevo at 6 pg cell Ϫ1 and in P. australis from Morro Bay at 78 pg cell Ϫ1 . Maximum cellular domoic acid levels were observed within 20 km of the coast between 0 and 5 m depth, although toxin was also measured to depths of 40 m. Hydrographic data indicated that the highest toxin levels and greatest numbers of toxic cells were positioned in water masses associated with upwelling zones near coastal headlands. Nutrient levels at these sites were less than those typically measured during periods of active upwelling, due to the 1998 El Niño event. The flow of cells and/or nutrients from coastal headlands into embayments where cells can multiply in a stratified environment is a possible mechanism of bloom development along the central California coast. This coupling of toxic Pseudo-nitzschia growth near upwelling zones with physical processes involved in cell transport will be understood only when long-term measurements are made at several key coastal locations, aiding in our capability to predict domoic-acid producing algal blooms.In May and June 1998, at least 70 California sea lions (Zalophus californianus) and one northern fur seal (Callorhinus ursinus) were found stranded along the central California coast. This stranding event occurred between 15 May 1 Corresponding author (Vera.L.Trainer@noaa.gov). AcknowledgmentsWe thank the captain and the crew of the RV Ballena, RV Shana Rae, and PB Bluefin for their help during these cruises, at times under strenuous conditions. We acknowledge the following people for their help in providing useful information that directed the locations of the cruises:
The illness of three people in 2011 after their ingestion of mussels collected from Sequim Bay State Park, Washington State, USA, demonstrated the need to monitor diarrhetic shellfish toxins (DSTs) in Washington State for the protection of human health. Following these cases of diarrhetic shellfish poisoning, monitoring for DSTs in Washington State became formalized in 2012, guided by routine monitoring of Dinophysis species by the SoundToxins program in Puget Sound and the Olympic Region Harmful Algal Bloom (ORHAB) partnership on the outer Washington State coast. Here we show that the DSTs at concentrations above the guidance level of 16 μg okadaic acid (OA) + dinophysistoxins (DTXs)/100 g shellfish tissue were widespread in sentinel mussels throughout Puget Sound in summer 2012 and included harvest closures of California mussel, varnish clam, manila clam and Pacific oyster. Concentrations of toxins in Pacific oyster and manila clam were often at least half those measured in blue mussels at the same site. The primary toxin isomer in shellfish and plankton samples was dinophysistoxin-1 (DTX-1) with D. acuminata as the primary Dinophysis species. Other lipophilic toxins in shellfish were pectenotoxin-2 (PTX-2) and yessotoxin (YTX) with azaspiracid-2 (AZA-2) also measured in phytoplankton samples. Okadaic acid, azaspiracid-1 (AZA-1) and azaspiracid-3 (AZA-3) were all below the levels of detection by liquid chromatography tandem mass spectrometry (LC-MS/MS). A shellfish closure at Ruby Beach, Washington, was the first ever noted on the Washington State Pacific coast due to DSTs. The greater than average Fraser River flow during the summers of 2011 and 2012 may have provided an environment conducive to dinoflagellates and played a role in the prevalence of toxigenic Dinophysis in Puget Sound.
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Oceanic high-nitrate, low-chlorophyll environments have been highlighted for potential large-scale iron fertilizations to help mitigate global climate change. Controversy surrounds these initiatives, both in the degree of carbon removal and magnitude of ecosystem impacts. Previous open ocean enrichment experiments have shown that iron additions stimulate growth of the toxigenic diatom genus Pseudonitzschia . Most Pseudonitzschia species in coastal waters produce the neurotoxin domoic acid (DA), with their blooms causing detrimental marine ecosystem impacts, but oceanic Pseudonitzschia species are considered nontoxic. Here we demonstrate that the sparse oceanic Pseudonitzschia community at the high-nitrate, low-chlorophyll Ocean Station PAPA (50° N, 145° W) produces approximately 200 pg DA L −1 in response to iron addition, that DA alters phytoplankton community structure to benefit Pseudonitzschia , and that oceanic cell isolates are toxic. Given the negative effects of DA in coastal food webs, these findings raise serious concern over the net benefit and sustainability of large-scale iron fertilizations.
Plankton samples from three inland embayments and several outer coastal sites of Washington State were collected from 1997 through 1999 and were examined for the presence of diatoms of the genus Pseudo-nitzschia and levels of the toxin, domoic acid (DA). Seven species were observed, including Pseudonitzschia pungens (Grunow ex Cleve) Hasle, P. multiseries (Hasle) Hasle, P. australis Frenguelli, P. fraudulenta (Cleve) Hasle, P. cf. heimii Manguim, P. pseudodelicatissima (Hasle) Hasle, and P. delicatissima (Cleve) Heiden. The coastal Pseudo-nitzschia species assemblages differed significantly from those observed within embayments. The dominant species observed at coastal sites were P. pseudodelicatissima and P. cf.heimii. Pseudo-nitzschia assemblages found in embayments included one or more of the following species: P. pungens , P. multiseries , P. australis , P. pseudodelicatissima , and P. fraudulenta. The nuclear large subunit rRNA gene was sequenced for six of the seven species identified. This sequence revealed that P. multiseries , P. pungens , P. australis , and P. heimii were genetically similar to those found in California, whereas P. delicatissima and P. pseudodelicatissima were distinct from the California isolates. Although the concentrations of DA in razor clams along Washington State coasts have exceeded regulatory limits several times since 1991, levels of DA in shellfish from Washington State embayments have not yet exceeded regulatory limits. The widespread presence of toxin-producing Pseudonitzschia species suggests, however, that toxic blooms are likely to occur within embayments in the future. In conjunction with the monitoring of environmental conditions conducive to toxic bloom formation, the development of species-specific probes for rapid and accurate detection of potentially toxic Pseudo-nitzschia species in this region would enable the forecasting of a toxic event before DA accumulates in shellfish, thereby reducing the impacts to coastal communities.
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