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. 2016 Oct 9;43(19):10366–10376. doi: 10.1002/2016GL070023

An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions

Ryan M McCabe 1,✉, Barbara M Hickey 2, Raphael M Kudela 3, Kathi A Lefebvre 4, Nicolaus G Adams 4, Brian D Bill 4, Frances M D Gulland 5, Richard E Thomson 6, William P Cochlan 7, Vera L Trainer 4
PMCID: PMC5129552  PMID: 27917011

Abstract

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.

Keywords: harmful algal bloom, Pseudo‐nitzschia australis, domoic acid, upwelling, warm anomaly, toxin

Key Points

  • The 2015 U.S. West Coast wide toxic Pseudo‐nitzschia australis bloom was facilitated by anomalous ocean conditions

  • The seasonal transition to upwelling provided nutrients for the bloom, and spring storms delivered toxic cells to the nearshore environment

  • West Coast toxic Pseudo‐nitzschia events are triggered by warm anomalies associated with El Niño and the Pacific Decadal Oscillation

1. An Unprecedented Coastwide Toxic Algal Bloom

Record‐breaking concentrations of the marine neurotoxin, domoic acid (DA) in 2015 caused unprecedented widespread closures of commercial and recreational shellfish and finfish fisheries and contributed to the stranding of numerous marine mammals along the U.S. West Coast (Figure 1). Several species of the marine diatom, Pseudo‐nitzschia, many of which produce DA, have been responsible for toxic blooms around the world [Lelong et al., 2012; Trainer et al., 2012]. The toxin is transferred through marine food webs by ingestion of live, dying, or dead Pseudo‐nitzschia cells by pelagic and benthic organisms and sickens or kills marine mammals and sea birds, as well as humans who ingest contaminated fish, shellfish, or crustaceans [Lefebvre et al., 2002]. Seafood contaminated with DA cause symptoms in humans ranging from mild gastrointestinal distress to seizures, coma, permanent short‐term memory loss, and death [Perl et al., 1990].

Figure 1.

Figure 1

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Impacts of domoic acid (DA) on fisheries and marine mammals in 2015. Shaded areas with shellfish symbols on land denote shellfish closures. Fish symbols indicate northern anchovy closures at designated landing sites. Shaded or hatched areas offshore (Dungeness crab and rock crab) correspond to the closures listed on the left. Stranded marine mammals with detectable DA (orange) and California sea lions diagnosed with DA poisoning (red) are pictured with the number of individuals indicated. DA poisoning is defined as the presentation of at least two of the following: neurologic signs (seizures, head weaving, ataxia), detectable DA, histopathologic lesions, and/or blood chemistry changes.

Seasonal blooms of Pseudo‐nitzschia are common along the U.S. West Coast. Past toxic events have been attributed to a number of different species of this genus [Trainer et al., 2012]. Analyses of DA outbreaks over the last two decades have identified regional initiation “hotspots” where blooms either develop or become concentrated. These source zones tend to coincide with retentive flow patterns, such as those associated with seasonal eddies [Trainer et al., 2002], over submarine banks [Hickey et al., 2013], or in the lee of coastal capes [Graham et al., 1992; Trainer et al., 2000]. Toxic blooms off central and southern California are generally due to P. australis [Scholin et al., 2000; Sekula‐Wood et al., 2011] whereas toxic spring blooms off Washington and Oregon are rarely caused by P. australis and, instead, are attributed to several different species [Trainer and Suddleson, 2005; Trainer et al., 2009]. Here we show that the highly toxic species, P. australis, bloomed simultaneously along the west coast of the U.S. and Canada in spring 2015. This extensive bloom was a consequence of three sequential factors: the onset of seasonal upwelling, followed by a series of late spring storms and the northward transport of the toxin‐producing P. australis at a time of anomalously high surface temperatures throughout the northeast Pacific. Refer to the supporting information for a description of data analysis methods used herein.

2. The North Pacific Ocean Warm Anomaly

A ~500 km wide and ~100 m deep body of anomalously warm, relatively fresh, and nutrient‐poor water (hereafter referred to as the warm anomaly) developed in fall 2013 in the northeast Pacific Ocean and persisted throughout 2014 and 2015 [Freeland and Whitney, 2014; Bond et al., 2015; Whitney, 2015a, 2015b; Peña and Nemcek, 2016; Di Lorenzo and Mantua, 2016] (Figure 2). Water in this region was more than 2.5°C warmer at the sea surface than the long‐term mean temperature. The anomaly was caused by an expansion of the North Pacific atmospheric high‐pressure cell to the north, which led to reduced ocean cooling and enhanced northward surface ocean transport by anomalous easterly winds [Freeland and Whitney, 2014; Bond et al., 2015; Peterson et al., 2015a].

Figure 2.

Figure 2

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Anomalously warm surface water in the North Pacific Ocean. Sea surface temperature anomalies (°C) from the NCEP/NCAR Reanalysis for the 3 month period of (a) January, February, March (JFM) 2015 and (b) April, May, June (AMJ) 2015, relative to the 1981–2010 composite average. Blue arrows indicate (Figure 2a) downwelling and (Figure 2b) upwelling. (c–e) Multiyear near‐surface temperature records from three National Data Buoy Center (NDBC) buoys off the U.S. West Coast (numbered locations shown in left panels). Temperature records from 2014 and 2015 are colored cyan and magenta, respectively, whereas data from all other years are colored gray.

At the end of the upwelling season in September 2014, the warm anomaly expanded to waters adjacent to the continental margin, as was apparent from the exceedingly warm surface temperatures measured at continental shelf buoys (Figures 2c–2e). Coincident with this encroachment of warm water into the coastal zone, the copepod community off central Oregon transitioned from a “cold water” to a “warm water” assemblage that included southern species, such as Rhincalanus nasutus and Clausocalanus furcatus, not seen since the 1998 El Niño [Peterson et al., 2015a]. Numerous observations of other southern species well north of their typical habitats have been linked to the warm anomaly [Bond et al., 2015; Peterson et al., 2015a, 2015b]. In early 2015, the warm anomaly extended along the entire west coasts of the U.S. and Canada (Figure 2a). On 10 March 2015, DA was detected in preserved zooplankton net tow samples collected in the warm water off Trinidad, California (41°N). Similar samples collected 1 month later off Newport, Oregon (44.6°N), also contained DA. Both samples confirm the presence of a toxic species of Pseudo‐nitzschia within the anomalously warm water prior to spring 2015.

In spring 2015, the warm anomaly moved well offshore (Figure 2b) and by summer had diminished in size and strength and remained isolated from the coast (with the exception of southern California). The summertime offshore movement of the warm anomaly was controlled by the alongshore, southward winds, which move surface water to the right of the wind vector as a result of Earth's rotation. Onshore movement of the water mass was critical to whether any associated biotoxin‐producing species were able to reach the coast where they could then be fueled by nutrients from coastal upwelling. As long as the anomalously warm water remained separated from the coast, it would have lacked sufficient macronutrients to fuel a significant phytoplankton bloom.

3. Springtime Shelf Conditions and Nutrient Supply

Northward winds over the continental shelf during storms cause onshore flow in the upper water column and downwelling and mixing at the coast. The switch to prevailing southward winds along the coast in late spring and summer leads to offshore transport of near‐surface waters and to upwelling of deep nutrient‐rich water within a few tens of kilometers of the coast (Figure 2). This seasonal change, termed the “spring transition” [Huyer et al., 1975], occurs almost simultaneously along the entire coast [Strub et al., 1987; Strub and James, 1988] and provides the macronutrients that drive the rich biological ecosystem characteristic of North American west coast waters.

Nutrient‐depleted water does not generally support a dense phytoplankton bloom. Indeed, no evidence of enhanced chlorophyll a (a proxy for phytoplankton biomass) was observed in the winter or early spring satellite images in the central North Pacific (Figure 3e), although brief upwelling favorable winds did result in a few short‐lived phytoplankton blooms very near the coast. However, with the return to seasonal upwelling favorable conditions in mid April 2015 (the mean transition period observed in this region for the past two decades [Thomson et al., 2014]), satellite‐derived chlorophyll a increased along the continental margin of the western U.S. (Figure 3f). Off Washington, winds switched to a predominantly southward direction (Figure 3a), with the upwelling response clearly captured by a moored chain of thermistors as a rapid cooling and increased stratification beginning in mid April (Figure 3b). Near‐surface currents at a site on the southern British Columbia continental slope changed from weak (and often northward) prior to the transition, to strongly southward following the mid April switch to upwelling (Figure 3c). After the spring transition, surface waters all along the continental margin cooled as the anomalously warm water was advected offshore (Figures 2b–2e).

Figure 3.

Figure 3

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Relationship between physical environmental conditions and the toxic spring Pseudo‐nitzschia bloom. (a) North‐south wind stress off Washington (site NDBC). (b) Water column temperature at five depths at a site on the 42 m isobath off Teahwhit Head, Washington (site TH). (c) Along‐slope near‐surface currents off the southern British Columbia‐northern Washington continental slope (site A1). (d) Total Pseudo‐nitzschia abundance (black line with green shading) and pDA (magenta line) off Long Beach, Washington (site LB). Site locations are shown in the inset. Satellite chlorophyll a estimates are averaged over the periods of (e) 27–31 March 2015, and (f) 06–08 May 2015.

4. The Phytoplankton Bloom and Its Toxin

With the transition to upwelling of cold, nutrient‐rich water to the euphotic zone, spring blooms of phytoplankton are observed annually over the continental shelf of the northeast Pacific [Thomas and Strub, 1989; Landry et al., 1989; Lynn et al., 2003; Jackson et al., 2015]. Such blooms contain many phytoplankton species but are primarily composed of centric diatoms, which are not toxic.

Details of the timing between coastal winds and currents, the spring transition, the rise of total Pseudo‐nitzschia abundance, and toxin concentration in seawater are shown in Figure 3 for Long Beach, Washington. Results for this station are representative of other U.S. West Coast locations north of central California (Figure 4). The spring transition to upwelling began with weak southward winds on 7 April, culminating in strong upwelling winds on 16 April (Figure 3a). Phytoplankton near the coast began to increase in abundance (i.e., bloom) when nutrients from depth were supplied to the euphotic zone on the inner shelf. Once the upwelled water mixed with the overlying and adjacent waters of the warm anomaly, phytoplankton, including P. australis, bloomed (Figures 3 and 4) and moved seaward in the offshore flowing surface layers. Scanning electron microscope analysis of a zooplankton net tow sample (integrated 0–100 m, 202 µm mesh) collected ~9 km offshore of Newport, Oregon, on 7 April reveal an assemblage of Pseudo‐nitzschia chains containing 65% P. pungens and 35% P. australis (Figure 4e). On 15 April, a phytoplankton net tow (20 µm mesh) off Kalaloch, Washington, documented a similar assemblage (56% P. pungens, 22% P. australis, and 22% P. cf. heimii; Figure 4c). By 22 April Pseudo‐nitzschia abundance estimates were 104 cells L−1 at Washington beaches, and on 26 April cell densities had increased by an order of magnitude immediately following the first of a series of spring storms that moved toxic cells shoreward. Two additional storms occurred in early May, transporting the surface bloom back toward shore while mixing near‐surface and middepth water with recently upwelled water. As Pseudo‐nitzschia abundances peaked in early May (Figure 3d), P. australis emerged as the dominant species from central California to southern British Columbia (Figure 4). In late May, upwelling was more persistent and P. australis abundance decreased dramatically as newly upwelled water likely transported more regionally typical species from deeper depths. By June 2015, the more endemic and less toxic diatom P. fraudulenta had replaced P. australis in the northern waters off Washington and Oregon (Figure 4).

Figure 4.

Figure 4

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DA in mussels or razor clams (red line) and Pseudo‐nitzschia abundance at six locations along the North American west coast (see lower inset). (a) North‐south wind stress off Washington. Pseudo‐nitzschia species abundance (colored bars) quantified as (b–f) percentage or as (g) cells L−1. Text labels indicate sample type, including phytoplankton net (not labeled), Z = zooplankton net, W = whole water. The regulatory shellfish DA limit of 20 ppm is shown (horizontal gray band). Figures 4c and 4d include total Pseudo‐nitzschia abundance (black line). Figures 4c, 4d, and 4g include water column pDA (magenta line with open circles).

Concentrations of water column particulate DA (pDA) also peaked in late April and early May, coincident with peaks in P. australis abundance (Figures 3d and 4). DA concentrations in razor clams (Siliqua patula) and mussels (Mytilus spp.) began to rise in early May north of central California (Figure 4). As expected, the timing of maximum DA in razor clams lagged the periods of both maximum pDA and Pseudo‐nitzschia abundance [Hickey et al., 2013]. Laboratory analysis of DA concentrations in mussels (M. californianus) indicated that the regulatory limit of 20 ppm was first exceeded on 29 April off Santa Cruz, California. Following this, shellfish samples collected from beaches throughout Oregon, Washington, and British Columbia, exceeded the regulatory limit, resulting in the closures of tribal, commercial, and recreational shellfish harvests (Figure 1). In Washington, ~1950 kg of clams harvested 1 day prior to the closure were ordered to be discarded. Although mussels depurate DA relatively quickly (days to weeks), razor clams retain DA for months [Horner et al., 1993]. Razor clam DA concentrations began decreasing in late May off Washington and Oregon, but harvest closures continued at one Washington beach through June 2016.

Domoic acid outbreaks often continue to impact benthic organisms long after the toxin‐producing species have dissipated [Horner et al., 1993]. Following the 2015 spring bloom and the mussel and razor clam fishery closures, Washington closed the coastal Dungeness crab fishery on 5 June (Figure 1), ~4.5 months earlier than scheduled and were forced to delay the December reopening. In California, the commercial and recreational Dungeness and rock crab fisheries did not open as expected at the beginning of November and the Dungeness crab fishery was not reopened along the entire U.S. coast until May 2016. Given that Dungeness crab are the single most valuable fishery on the U.S. West Coast, with an estimated ex‐vessel value of ~$170 million [Pacific States Marine Fisheries Commission Dungeness Crab Report, 2014], it is not surprising that the State of California requested a federal fishery disaster declaration from the U.S. Department of Commerce.

A research cruise aboard the National Oceanic and Atmospheric Administration (NOAA) Ship Bell M. Shimada from 20 June to 7 September sampled phytoplankton abundance and pDA from southern California to northern British Columbia (Figure 5). Elevated concentrations of pDA and P. australis were measured at the majority of stations south of central Oregon, and the pDA concentrations at many of the California stations exceeded previously reported maximum values, reaching 19,978 ng mL−1. Pseudo‐nitzschia was the dominant phytoplankton genus at approximately half of the stations sampled off California (Figure 5b). At times, the densities of Pseudo‐nitzschia cells were so high that even zooplankton net tows were clogged with long chains (Figure 5c). Live samples collected near Point Conception, California, commonly included chains of 20–30 cells with large, bulging chloroplasts. The research vessel arrived off Oregon and Washington after the initial bloom and after the Pseudo‐nitzschia community shifted to P. fraudulenta in that region. Thus, pDA concentrations were low or undetectable in waters where either P. fraudulenta or P. pseudodelicatissima were prevalent (Figure 5).

Figure 5.

Figure 5

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(a) Particulate DA and (b) Pseudo‐nitzschia abundance in surface (3 m) seawater samples collected aboard the NOAA Ship Bell M. Shimada from June through September (months shown in shaded boxes, left side of both panels). Red “targets” in Figure 5b are locations where representative pDA and Pseudo‐nitzschia abundances are shown on select dates in adjacent boxes. Gray shading along the coast indicates regions where Pseudo‐nitzschia was the dominant phytoplankton. (c) A Bongo net tow sample off Point Conception on 24 June (concentrated sample, top panel; microscopic image of ~100X diluted sample at 200X magnification, bottom panel). ND = not detected.

5. Toxins and the Food Chain

The impact of this toxic diatom bloom propagated up the food chain to include many species of marine mammals. In 2015, DA was detected in whales, dolphins, porpoises, seals, and sea lions ranging from southern California to northern Washington between March and November (Figure 1). This was the largest geographic extent of DA detection in marine mammals ever recorded globally. DA was first recognized as a threat to marine mammal health in 1998 when hundreds of California sea lions (Zalophus californianus) stranded along beaches in central California exhibiting signs of neuroexcitotoxicity including seizures, head weaving, and ataxia [Scholin et al., 2000]. As sea lions are highly visible on public beaches and have been impacted every year in California since 1998 [Bejarano et al., 2008], the animals examined at veterinary research hospitals serve as relatively robust indicators of the severity of toxic blooms. From 2010 to 2013, the numbers of live sea lions stranding on the central California coastline with suspected DA toxicosis and admitted to The Marine Mammal Center in Sausalito, California, averaged 64 ± 21 animals per year. Beginning in 2014 and through 2015, the number of stranded sea lions from the same region diagnosed with suspected DA toxicosis rose to over 200 per year with 229 cases documented in 2015 (Figure 1). On 21 May 2015, DA‐related seizures and high levels of DA in feces (1014 ng g−1) were confirmed for a sea lion found on Long Beach, Washington, making this the first documented case of DA toxicosis in a sea lion this far north on the U.S. West Coast. Although DA was detected in several other stranded marine mammals in Washington and Oregon, DA‐associated lesions were not confirmed in those animals as they were not examined histologically. Sea lions commonly feed on planktivorous fish such as northern anchovies (Engraulis mordax) that can be found in schools as deep as 100 m and several meters thick. During the Shimada cruise, anchovies collected with net hauls to depths of ~30 m contained DA concentrations between 1–505 µg DA g−1 (whole fish) and 1–3239 µg DA g−1 (viscera). It is probable that stranded mammals with measurable DA in March 2015 acquired the toxin from these deep diving anchovies that fed on short‐lived blooms of toxic Pseudo‐nitzschia residing near the base of the nutrient‐depleted waters of the warm anomaly.

6. Prognosis

While DA reached unprecedented levels in water samples, planktivorous fish and marine mammals, field experiments suggest even greater toxicity had the bloom been provided with additional macronutrients [Kudela et al., 2008]. Nutrient manipulation experiments conducted in Monterey Bay during 2015 demonstrated that cellular toxicity increased up to fivefold in experiments of exponentially and stationary‐growing assemblages of P. australis (Figure 6e). Thus, the combination of warm ocean water and expected future increases in coastal nutrient loading from runoff (globally [Seitzinger et al., 2010; Lee et al., 2016] and locally [Bergamaschi et al., 2012]) could potentially lead to yet larger toxic events.

Figure 6.

Figure 6

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Variability of historical toxic events, biological response, and mechanisms. (a) The ONI (gold indicates El Niño, blue indicates La Niña, gray represents neutral conditions) and the PDO (black line). (b) Pseudo‐nitzschia growth rate anomaly estimated using the temperature‐growth relationship in Figure 6d. (c) Razor clam DA concentration at three beaches (sites in Figure 4). Periods of El Niño conditions (gray shading) and the 20 ppm regulatory DA limit (black line) are indicated. (d) Temperature‐growth rate results from laboratory cultures for three strains of P. australis isolated by H. Bowers from Monterey Bay during spring 2015. (e) Effects of nutrient enrichment on cell toxicity. Error bars in Figures 6d and 6e represent the standard error of the mean.

Although 2015 was unusual in the spatial extent and magnitude of the warm anomaly, the west coast of North America experiences regular warm periods in response to approximately decadal forcing from El Niño and the Pacific Decadal Oscillation (PDO; Figure 6a), with concomitant biological responses [Chavez et al., 2002; Mackas and Galbraith, 2002; Peterson and Schwing, 2003; Fisher et al., 2015]. Previous studies suggest that Pseudo‐nitzschia abundance in southern California is correlated with both the PDO and the North Pacific Gyre Oscillation [Sekula‐Wood et al., 2011]. Laboratory experiments conducted with P. australis strains isolated from Monterey Bay, California, in 2015 demonstrate that this toxic diatom reaches maximal growth rates at ~17–18°C with specific growth rates increasing by ~threefold from 5 to 17°C (Figure 6d). The resulting estimated growth rate anomalies (Figure 6b) exhibit a strong (r = 0.36, p < 0.001) correlation between P. australis growth potential and the PDO with 1 month lag and to the Oceanic Niño Index (ONI) with a 3 month lag (r = 0.34, p < 0.001). Toxin concentration in razor clams showed a strong relationship, with a 3 month lag to both growth potential (r = 0.14, p < 0.001) and the ONI (r = 0.20, p <<0.001), and with the PDO (r = 0.16, p <<0.001) at zero lag (Figure 6c). Moreover, the historical DA events in Figure 6c also track regional anomalies in southern zooplankton species [Fisher et al., 2015] (which, at times, peak in the year following an El Niño, similar to some DA events shown here; see their Figure 2), suggesting a relationship between toxic events and advectively driven ecosystem shifts [Bi et al., 2011]. Thus, west coast wide toxic bloom events are directly related to warm anomalies associated with both El Niño and PDO cycles, leading to faster growth (and northward expansion of P. australis habitat as seen in 2015), followed by increased toxin accumulation in razor clams.

This paper documents the first Pseudo‐nitzschia bloom to negatively impact both shellfish and fish harvest industries, as well as marine mammal health, along the entire U.S. and Canada west coasts. What led to such an unprecedented monospecific toxic bloom? Studies of P. australis isolated from coastal California waters show that this organism is well adapted to low‐nutrient conditions and is capable of responding rapidly to excess nutrients during upwelling, as well as to a variety of nitrogen sources, making the conditions during 2015 particularly amenable to blooms of this species [Cochlan et al., 2008; Kudela et al., 2010]. Laboratory and field experiments conducted in 2015 with P. australis confirm that it responds positively to both warm temperatures and enhanced nutrient loading. We suggest that the physiological capabilities of P. australis to acquire nitrate [Cochlan et al., 2008], to utilize a variety of nitrogen sources for growth [Howard et al., 2007], and to complex trace metals [Wells et al., 2005] selected for this genus over all other phytoplankton in the natural assemblage. The survival of P. australis in the anomalously warm and nutrient‐depleted waters, its unusual presence along the entire continental margin of the western U.S. prior to the upwelling season, and its rapid expansion following the injection of nutrients with the spring transition to upwelling conditions, resulted in the coastwide, high‐impact bloom. We may anticipate similarly severe toxic algal blooms along the North American west coast in future years with enhanced northward transport and relatively warm ocean conditions, including but not limited to El Niño periods. Given the large‐scale warming and potential increase in frequency of extreme events expected with climate change [Cai et al., 2014] coupled with documented links between increased temperature and increased Pseudo‐nitzschia abundance [Hinder et al., 2012], both the warm anomaly and the massive 2015 toxic algal bloom serve as instructive examples for what future decades may hold in store.

Supporting information

Supporting Information S1

Click here for additional data file. (129.8KB, docx)

Acknowledgments

We thank a number of people for the shellfish toxin data: Daniel L. Ayers, Zach Forster, and the Washington Department of Fish and Wildlife; Jerry Borchert and the Washington State Department of Health; Matthew V. Hunter and the Oregon Department of Fish and Wildlife; Gregg Langlois and the California Department of Public Health; and Lorraine McIntyre and the British Columbia Centre for Disease Control. The Olympic Region Harmful Algal Bloom Partnership provided Washington Pseudo‐nitzschia counts. We thank Liam Antrim, Kathy Hough, and others of the Olympic Coast National Marine Sanctuary for the moored temperature data, Bill Peterson for zooplankton net tow samples from the Newport Line off Oregon, Eric Bjorkstedt for net tow samples from the Trinidad Line off California, and Nicky Haigh for the Pseudo‐nitzschia sample from Barkley Sound, British Columbia. We also thank Anthony Odell, Madison Drescher, Jennifer Hagen, and Aaron Parker for sampling aboard the NOAA Ship Bell M. Shimada. We thank Bridget Hansen of the Romberg Tiburon Center, San Francisco State University, for performing the Pseudo‐nitzschia temperature‐growth experiments. Marine mammal samples were collected by the Wildlife Algal Toxin Research and Response Network Partners (http://www.nwfsc.noaa.gov/research/divisions/efs/warrnwest/). This work was supported by grants from the NOAA National Centers for Coastal Ocean Science Center for Sponsored Coastal Ocean Research to V.L.T., B.M.H., and R.M.M. (NA11NOS0120036); to B.M.H. and R.M.M. (NA14NOS0120149); to R.M.M., B.M.H., and V.L.T. (NA16NOS4780189); to R.M.K. (NA11NOS4780030 and NA04NOS4780239); and to the Joint Institute for the Study of the Atmosphere and Ocean (JISAO) under NOAA Cooperative Agreement NA10OAR4320148 (2010–2015) and NA15OAR4320063 (2015–2020). B.M.H. and R.M.M. acknowledge additional funding from the National Science Foundation (NSF; OCE‐1332753). K.A.L. acknowledges funding from NSF (OCE‐1314088) and the National Institutes of Health (NIH; RO1 ES021930). W.P.C. acknowledges undergraduate research funding from COAST that supported Pseudo‐nitzschia lab experiments conducted by Hansen. The authors declare no conflicts of interests. Primary environmental data will be summarized and delivered to a National Data Center's Environmental Data Management Committee (EDMC) within 6 months of the termination of funding or publication in the peer‐reviewed literature. This is NOAA Harmful Algal Bloom Event Response contribution 20, NOAA Ecology and Oceanography of Harmful Algal Bloom contribution 852, NOAA Monitoring and Event Response for Harmful Algal Bloom contribution 196, and JISAO contribution 2016‐01‐47. The statements, findings, conclusions, and recommendations are those of the authors and do not reflect the views of NSF, NIH, NOAA, or the Department of Commerce.

McCabe, R. M. , Hickey B. M., Kudela R. M., Lefebvre K. A., Adams N. G., Bill B. D., Gulland F. M. D., Thomson R. E., Cochlan W. P., and Trainer V. L. (2016), An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions, Geophys. Res. Lett., 43, 10366–10376, doi:10.1002/2016GL070023.

References

  1. Auro, M. E. , and Cochlan W. P. (2013), Nitrogen utilization and toxin production by two diatoms of the Pseudo‐nitzschia pseudodelicatissima complex: P. cuspidata and P. fryxelliana , J. Phycol., 49, 156–169, doi:10.1111/jpy.12033. [DOI] [PubMed] [Google Scholar]
  2. Beardsley, R. C. , Limeburner R., and Rosenfeld L. K. (1985), CODE‐2 moored array and large‐scale data report. Woods Hole Oceanographic Institution Tech. Rep. WHOI‐85‐35, 234 pp.
  3. Bejarano, A. C. , Gulland F. M., Goldstein T., Leger J. S., Hunter M., Schwacke L. H., VanDolah F. M., and Rowles T. K. (2008), Demographics and spatio‐temporal signature of the biotoxin domoic acid in California sea lion (Zalophus californianus) stranding records, Mar. Mammal Sci., 24, 899–912, doi:10.1111/j.1748-7692.2008.00224.x. [Google Scholar]
  4. Bergamaschi, B. A. , Smith R. A., Sauer M. J., and Shih J.‐S. (2012), Terrestrial fluxes of sediments and nutrients to Pacific coastal waters and their effects on coastal carbon storage rates, in Baseline and Projected Future Carbon Storage and Greenhouse‐Gas Fluxes in Ecosystems of the Western United States, U.S. Geol. Surv. Prof. Pap, vol. 1797, edited by Zhu Z. and Reed B. C., pp. 143–157, U.S. Geological Survey Science Network, Reston, Va: [Available at http://pubs.usgs.gov/pp/1797/.] [Google Scholar]
  5. Bi, H. , Peterson W. T., and Strub P. T. (2011), Transport and coastal zooplankton communities in the northern California Current system, Geophys. Res. Lett., 38, L12607, doi:10.1029/2011GL047927. [Google Scholar]
  6. Bill, B. D. , Moore S. K., Hay L. R., Anderson D. M., and Trainer V. L. (2016), Effects of temperature and salinity on the growth of Alexandrium (Dinophyceae) isolates from the Salish Sea, J. Phycol., 52, 230–238, doi:10.1111/jpy.12386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bond, N. A. , Cronin M. F., Freeland H., and Mantua N. (2015), Causes and impacts of the 2014 warm anomaly in the NE Pacific, Geophys. Res. Lett., 42, 3414–3420, doi:10.1002/2015GL063306. [Google Scholar]
  8. Cai, W. , et al. (2014), Increasing frequency of extreme El Niño events due to greenhouse warming, Nat. Clim. Change, 4, 111–116, doi:10.1038/nclimate2100. [Google Scholar]
  9. Chavez, F. P. , Pennington J. T., Castro C. G., Ryan J. P., Michisaki R. P., Schlining B., Walz P., Buck K. R., MacFadyen A., and Collins C. A. (2002), Biological and chemical consequences of the 1997–1998 El Niño in central California waters, Prog. Oceanogr., 54, 205–232, doi:10.1016/S0079-6611(02)00050-2. [Google Scholar]
  10. Cochlan, W. P. , Herndon J., and Kudela R. M. (2008), Inorganic and organic nitrogen uptake by the toxigenic diatom Pseudo‐nitzschia australis (Bacillariophyceae), Harmful Algae, 8, 111–118, doi:10.1016/j.hal.2008.08.008. [Google Scholar]
  11. Di Lorenzo, E. , and Mantua N. (2016), Multi‐year persistence of the 2014/15 North Pacific marine heatwave, Nat. Clim. Change, doi:10.1038/nclimate3082. [Google Scholar]
  12. Eberhart, B.‐T. L. , Bill B. D., and Trainer V. L. (2012), Strategies for remote sampling of harmful algal blooms: A case study on the Washington State coast, Harmful Algae, 19, 39–45, doi:10.1016/j.hal.2012.05.005. [Google Scholar]
  13. Fisher, J. L. , Peterson W. T., and Rykaczewski R. R. (2015), The impact of El Nino events on the pelagic food chain in the northern California Current, Global Change Biol., 21, 4401–4414, doi:10.1111/gcb.13054. [DOI] [PubMed] [Google Scholar]
  14. Freeland, H. , and Whitney F. (2014), Unusual warming in the Gulf of Alaska, North Pacific Marine Science Organization, PICES Press, 22, 51–52. [Google Scholar]
  15. Godin, G. (1972), The Analysis of Tides, pp. 264, Liverpool Univ. Press, Liverpool, U. K. [Google Scholar]
  16. Graham, W. M. , Field J. G., and Potts D. C. (1992), Persistent “upwelling shadows” and their influence on zooplankton distributions, Mar. Biol., 114, 561–570. [Google Scholar]
  17. Guillard, R. R. L. (1973), Division rates, in Handbook of Phycological Methods, edited by Stein J. R., pp. 290–311, Cambridge Univ. Press, Cambridge, U. K. [Google Scholar]
  18. Guillard, R. R. L. (1975), Culture of phytoplankton for feeding marine invertebrates, in Culture of Marine Invertebrate Animals, edited by Smith W. L. and Chanley M. H., pp. 26–60, Plenum Press, New York. [Google Scholar]
  19. Harrison, P. J. , Waters R. E., and Taylor F. J. R. (1980), A broad spectrum artificial seawater medium for coastal and open ocean phytoplankton, J. Phycol., 16, 28–35. [Google Scholar]
  20. Hickey, B. M. , Trainer V. L., Kosro P. M., Adams N. G., Connolly T. P., Kachel N. B., and Geier S. L. (2013), A springtime source of toxic Pseudo‐nitzschia cells on razor clam beaches in the Pacific Northwest, Harmful Algae, 25, 1–14, doi:10.1016/j.hal.2013.01.006. [Google Scholar]
  21. Hinder, S. L. , Hays G. C., Edwards M., Roberts E. C., Walne A. W., and Gravenor M. B. (2012), Changes in marine dinoflagellate and diatom abundance under climate change, Nat. Clim. Change, 2, 271–275, doi:10.1038/nclimate1388. [Google Scholar]
  22. Horner, R. A. , Kusske M. B., Moynihan B. P., Skinner R. N., and Wekell J. C. (1993), Retention of domoic acid by Pacific razor clams, Siliqua patula (Dixon, 1789): Preliminary study, J. Shellfish Res., 12, 451–456. [Google Scholar]
  23. Howard, M. D. A. , Cochlan W. P., Ladizinsky N., and Kudela R. M. (2007), Nitrogenous preference of toxigenic Pseudo‐nitzschia australis (Bacillariophyceae) from field and laboratory experiments, Harmful Algae, 6, 206–217, doi:10.1016/j.hal.2006.06.003. [Google Scholar]
  24. Huyer, A. , Sobey E. J. C., and Smith R. L. (1975), The spring transition in currents over the Oregon continental shelf, J. Geophys. Res., 84, 6995–7011, doi:10.1029/JC084iC11p06995. [Google Scholar]
  25. Jackson, J. M. , Thomson R. E., Brown L. N., Willis P. G., and Borstad G. A. (2015), Satellite chlorophyll off the British Columbia coast, 1997–2010, J. Geophys. Res. Oceans, 120, 4709–4728, doi:10.1002/2014JC010496. [Google Scholar]
  26. Kudela, R. M. , Lane J. Q., and Cochlan W. P. (2008), The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA, Harmful Algae, 8, 103–110, doi:10.1016/j.hal.2008.08.019. [Google Scholar]
  27. Kudela, R. M. , Seeyave S., and Cochlan W. P. (2010), The role of nutrients in regulation and promotion of harmful algal blooms in upwelling systems, Prog. Oceanogr., 85, 122–135, doi:10.1016/j.pocean.2010.02.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Landry, M. R. , Postel J. R., Peterson W. K., and Newman J. (1989), Broad‐Scale Distributional Patterns of Hydrographic Variables on the Washington/Oregon Shelf, Coastal Oceanography of Washington and Oregon, Elsevier Oceanogr. Ser, vol. 47, pp. 1–40, Elsevier Amsterdam, Netherlands. [Google Scholar]
  29. Large, W. G. , and Pond S. (1981), Open ocean momentum flux measurements in moderate to strong winds, J. Phys. Oceanogr., 11, 324–336. [Google Scholar]
  30. Lee, R. Y. , Seitzinger S., and Mayorga E. (2016), Land‐based nutrient loading to LMEs: A global watershed perspective on magnitudes and sources, Environ. Dev., 17, 220–229, doi:10.1016/j.envdev.2015.09.006. [Google Scholar]
  31. Lefebvre, K. A. , Bargu S., Kieckhefer T., and Silver M. W. (2002), From sanddabs to blue whales: The pervasiveness of domoic acid, Toxicon, 40, 971–977, doi:10.1016/S0041-0101(02)00093-4. [DOI] [PubMed] [Google Scholar]
  32. Lelong, A. , Hégaret H., Soudant P., and Bates S. S. (2012), Pseudo‐nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: Revisiting previous paradigms, Phycologia, 51, 168–216, doi:10.2216/11-37.1. [Google Scholar]
  33. Lynn, R. J. , Bograd S. J., Chereskin T. K., and Huyer A. (2003), Seasonal renewal of the California Current: The spring transition off California, J. Geophys. Res., 108(C8), 3279, doi:10.1029/2003JC001787. [Google Scholar]
  34. Mackas, D. L. , and Galbraith M. (2002), Zooplankton community composition along the inner portion of Line P during the 1997–1998 El Niño event, Prog. Oceanogr., 54, 423–437, doi:10.1016/S0079-6611(02)00062-9. [Google Scholar]
  35. Peña, A. , and Nemcek N. (2016), Phytoplankton in surface waters along Line P and off the west coast of Vancouver Island, in State of the Physical, Biological and Selected Fishery Resources of Pacific Canadian Marine Ecosystems in 2015, edited by Chandler P. C., King S. A., and Perry R. I., Can. Tech. Rep. Fish. Aquat. Sci. 3179, 57–60, Fisheries and Oceans Canada, Sydney, Canada. [Google Scholar]
  36. Perl, T. M. , Bédard L., Kosatsky T., Hockin J. C., Todd E. C. D., and Remis R. S. (1990), An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid, N. Engl. J. Med., 322, 1775–1780. [DOI] [PubMed] [Google Scholar]
  37. Peterson, W. T. , and Schwing F. B. (2003), A new climate regime in northeast Pacific ecosystems, Geophys. Res. Lett., 30(17), 1896, doi:10.1029/2003GL017528. [Google Scholar]
  38. Peterson, W. , Robert M., and Bond N. (2015a), The warm blob—Conditions in the northeastern Pacific Ocean, North Pacific Marine Science Organization, PICES Press, 23, 36–38. [Google Scholar]
  39. Peterson, W. , Robert M., and Bond N. (2015b), The warm Blob continues to dominate the ecosystem of the northern California Current, North Pacific Marine Science Organization, PICES Press, 23, 44–46. [Google Scholar]
  40. Pocklington, R. , Milley J. E., Bates S. S., Bird C. J., De Freitas A. S. W., and Quilliam M. A. (1990), Trace determination of domoic acid in sea water and phytoplankton by high‐performance liquid chromatography of the fluorenylmethoxycarbonyl (FMOC) derivative, Int. J. Environ. Anal. Chem., 38, 351–368. [Google Scholar]
  41. Pacific States Marine Fisheries Commission Dungeness Crab Report (2014), Pacific States Marine Fisheries Commission, California Department of Fish and Wildlife, California's Living Marine Resources: A Status Report, 5 pp. [Available at http://www.psmfc.org/crab/2014‐2015%20files/DUNGENESS%20CRAB%20REPORT2014.pdf.]
  42. Round, F. E. , Crawford R. M., and Mann D. G. (1990), The Diatoms: Biology and Morphology of the Genera, pp. 747, Cambridge Univ. Press, Cambridge, U. K. [Google Scholar]
  43. Scholin, C. A. , et al. (2000), Mortality of sea lions along the central California coast linked to a toxic diatom bloom, Nature, 403, 80–84, doi:10.1038/47481. [DOI] [PubMed] [Google Scholar]
  44. Seitzinger, S. P. , et al. (2010), Global river nutrient export: A scenario analysis of past and future trends, Global Biogeochem. Cycles, 24, GB0A08, doi:10.1029/2009GB003587. [Google Scholar]
  45. Sekula‐Wood, E. , Benitez‐Nelson C., Morton S., Anderson C., Burrell C., and Thunell R. (2011), Pseudo‐nitzschia and domoic acid fluxes in Santa Barbara Basin (CA) from 1993 to 2008, Harmful Algae, 10, 567–575, doi:10.1016/j.hal.2011.04.009. [Google Scholar]
  46. Seubert, E. L. , Howard M. D. A., Kudela R. M., Stewart T. N., Litaker R. W., Evans R., and Caron D. A. (2014), Development, comparison, and validation using ELISAs for the determination of domoic acid in California sea lion body fluids, J. AOAC Int., 97, 345–355, doi:10.5740/jaoacint.SGESeubert. [DOI] [PubMed] [Google Scholar]
  47. Strub, P. T. , and James C. (1988), Atmospheric conditions during the spring and fall transitions in the coastal ocean off western United States, J. Geophys. Res., 93, 15,561–15,584, doi:10.1029/JC093iC12p15561. [Google Scholar]
  48. Strub, P. T. , Allen J. S., Huyer A., and Smith R. L. (1987), Large‐scale structure of the spring transition in the coastal ocean off western North America, J. Geophys. Res., 92, 1527–1544, doi:10.1029/JC092iC02p01527. [Google Scholar]
  49. Thomas, A. C. , and Strub P. T. (1989), Interannual variability in phytoplankton pigment distribution during the spring transition along the west coast of North America, J. Geophys. Res., 94, 18,095–18,117, doi:10.1029/JC094iC12p18095. [Google Scholar]
  50. Thomson, R. E. , Hessemann M., Davis E. E., and Hourston R. A. S. (2014), Continental microseismic intensity delineates oceanic upwelling timing along the west coast of North America, Geophys. Res. Lett., 41, 6872–6880, doi:10.1002/2014GL061241. [Google Scholar]
  51. Trainer, V. L. , and Suddleson M. (2005), Monitoring approaches for early warning of domoic acid events in Washington State, Oceanography, 18, 228–237, doi:10.5670/oceanog.2005.56. [Google Scholar]
  52. Trainer, V. L. , Adams N. G., Bill B. D., Stehr C. M., Wekell J. C., Moeller P., Busman M., and Woodruff D. (2000), Domoic acid production near California upwelling zones, June 1998, Limnol. Oceanogr., 45, 1818–1833, doi:10.4319/lo.2000.45.8.1818. [Google Scholar]
  53. Trainer, V. L. , Hickey B. M., and Horner R. A. (2002), Biological and physical dynamics of domoic acid production off the Washington U.S.A. coast, Limnol. Oceanogr., 47, 1438–1446. [Google Scholar]
  54. Trainer, V. L. , Hickey B. M., Lessard E. J., Cochlan W. P., Trick C. G., Wells M. L., MacFadyen A., and Moore S. (2009), Variability of Pseudo‐nitzschia and domoic acid in the Juan de Fuca eddy region and its adjacent shelves, Limnol. Oceanogr., 54, 289–308, doi:10.4319/lo.2009.54.1.0289. [Google Scholar]
  55. Trainer, V. L. , Bates S. S., Lundholm N., Thessen A. E., Cochlan W. P., Adams N. G., and Trick C. G. (2012), Pseudo‐nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health, Harmful Algae, 14, 271–300, doi:10.1016/j.hal.2011.10.025. [Google Scholar]
  56. Wells, M. L. , Trick C. G., Cochlan W. P., Hughes M. P., and Trainer V. L. (2005), Domoic acid: The synergy of iron, copper, and the toxicity of diatoms, Limnol. Oceanogr., 50, 1908–1917, doi:10.4319/lo.2005.50.6.1908. [Google Scholar]
  57. Whitney, F. A. (2015a), Anomalous winter winds decrease 2014 transition zone productivity in the NE Pacific, Geophys. Res. Lett., 42, 428–431, doi:10.1002/2014GL062634. [Google Scholar]
  58. Whitney, F. A. (2015b), Impacts of the 2013–2014 warm anomaly on phytoplankton biomass in the NE Pacific, in State of the Physical, Biological and Selected Fishery Resources of Pacific Canadian Marine Ecosystems in 2014, edited by Chandler P. C., King S. A., and Perry R. I., Can. Tech. Rep. Fish. Aquat. Sci. 3131, 40–63, Fisheries and Oceans Canada, Sydney, Canada. [Google Scholar]

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