Elsevier

Harmful Algae

Volume 10, Issue 6, September 2011, Pages 567-575
Harmful Algae

Pseudo-nitzschia and domoic acid fluxes in Santa Barbara Basin (CA) from 1993 to 2008

https://doi.org/10.1016/j.hal.2011.04.009Get rights and content

Abstract

Blooms of domoic acid (DA) producing Pseudo-nitzschia, regularly occur off the coast of California. Although it has been hypothesized that these blooms are increasing in frequency, the lack of historical records limits our understanding of potential causal mechanisms. In this study, an 15-year time-series (1993–2008) of sediment trap samples collected from the Santa Barbara Basin (SBB) at 540 m were analyzed for Pseudo-nitzschia (n = 196, microscopy and SEM) and DA (n = 206, LC–MS/MS) concentrations and fluxes. Results suggest that there was an abrupt shift towards greater frequency and higher magnitude Pseudo-nitzschia blooms and toxic DA flux events in the SBB after the year 2000. SEM analysis of sediment trap material indicates that these events were mainly blooms of P. australis, with cell fluxes increasing by an order of magnitude from a maximum of 4.5 × 106 cells m−2 d−1 pre-2000, to as high as 3.2 × 108 cells m−2 d−1 thereafter. Similarly, sediment trap DA fluxes increased by an average of 13.4 μg m−2 d−1, with only one large event (>5 μg m−2 d−1) from 1993 to 1999 versus 16 large DA events from 2000 to 2008. While the causes of this abrupt shift remain ambiguous, we suggest that this shift may be related to natural climate variability associated with a change in phase of the North Pacific Gyre Oscillation (NPGO) and its potential influence on the composition and magnitude of waters that are upwelled into the SBB.

Highlights

► Blooms of domoic acid producing Pseudo-nitzschia have been occurring in the Santa Barbara Basin since 1994. ► There is an abrupt increase in Pseudo-nitzschia bloom abundance and domoic acid toxicity in 1998–2000, with only one large event (>5 μg m−2 d−1) from 1993 to 1999 versus 16 large DA events from 2000 to 2008. ► This abrupt shift in Pseudo-nitzschia bloom intensity and toxicity may be related to natural shifts in climate associated with the North Pacific Gyre Oscillation.

Introduction

Toxic Pseudo-nitzschia were first recorded in the Santa Barbara Basin (SBB) in 1998 during a wide-spread bloom that affected the central California coastline (Trainer et al., 2000). The species responsible was identified as Pseudo-nitzschia australis and its production of the neurotoxin domoic acid (DA) resulted in the mass mortality of over 400 California sea lions (Scholin et al., 2000). Since then, toxic Pseudo-nitzschia blooms have occurred regularly in SBB, prompting regulatory monitoring of shellfish DA concentrations in SBB shellfish by the California Department of Public Health beginning in 2002 (Langlois, Biotoxin Monthly Reports).

The environmental drivers of toxic Pseudo-nitzschia blooms remain enigmatic. Several studies off central and southern California suggest that toxic Pseudo-nitzschia blooms are associated with the upwelling of colder, high-nutrient waters (Anderson et al., 2006, Kudela et al., 2004), whereas others report blooms after periods of high-nutrient river runoff (Bates et al., 1998, Dortch et al., 1997, Fisher et al., 2003, Lane et al., 2009, Pan et al., 2001, Trainer et al., 2000, Van Dolah et al., 2003, Wells et al., 2005), or due to resuspension of seeding populations into the euphotic zone during upwelling and storms (Garrison, 1981, Trainer et al., 2000). These studies are further complicated by the fact that peaks in Pseudo-nitzschia cell abundance and DA concentrations may be loosely coupled in time. For example, increases in toxin production may be a function of silicic acid or phosphate stress (Bates et al., 1991, Fehling et al., 2004, Pan et al., 1996a, Pan et al., 1996b), as well as iron and copper limitation that may occur prior to and after Pseudo-nitzschia abundance maxima (Maldonado et al., 2002, Rue and Bruland, 2001, Wells et al., 2005).

Coastal eutrophication is often cited as driving the observed increase in HAB frequency worldwide (see reviews by Anderson et al., 2002, Glibert et al., 2005, Hallegraeff, 1993), but this may also be due to enhanced awareness and monitoring. In the case of Pseudo-nitzschia, for example, a number of the species now recognized to be toxic were previously identified as “Nitzschia seriata (Cleve) Peragallo”, a composite taxon that may contain both toxic and non-toxic species (e.g. Bates, 2000). Off the coast of California, a recent examination of SBB sediment cores suggests that a rise in the relative abundance of Pseudo-nitzschia in SBB is a modern phenomenon with significant increases beginning in 2000–2001 (Barron et al., 2010).

Sediment trap studies in SBB and San Pedro Basin (SPB), also located off the coast of southern California, have demonstrated that sediment traps are effective tools for documenting both Pseudo-nitzschia and DA fluxes to deep waters in coastal regions (Schnetzer et al., 2007, Sekula-Wood et al., 2009). These studies indicate that high concentrations of surface water Pseudo-nitzschia and DA are temporally coupled to those measured in sinking particles collected in sediment traps located as deep as 800 m, providing a pathway for toxin exposure in deep water and benthic ecosystems. As such, the transport of DA to depth is theorized to be particle-mediated: (i) retained intracellularly within Pseudo-nitzschia frustules, (ii) incorporated into the biomass and fecal pellets of biota (e.g. zooplankton and planktivorous fish) which have fed on toxic Pseudo-nitzschia blooms, and/or (iii) adsorbed onto particles (Burns and Ferry, 2007, Lail et al., 2007). Aggregation of particles and fast sinking rates may decrease exposure of DA to photodegradation in surface waters and potentially increase the retention of this toxin for transport to deep water ecosystems.

Building upon previous sediment trap work in SBB, a major goal of this study was to investigate long-term changes in Pseudo-nitzschia and DA fluxes at ∼550 m from 1993 to 2008. Bottom sediments were also obtained to contrast Pseudo-nitzschia and DA water column fluxes, as well as investigate variability of DA retention in surface sediments at varying depths within the basin. Furthermore, as the advent of using sediment trap samples for DA detection is recent, we more closely describe one method for DA determination in sediment trap samples which focuses on quantifying DA in both the particulate and dissolved phases of the collected trap material.

Section snippets

Sample collection

The SBB sediment trap mooring has been stationed near the center of the basin (34°14′N, 120°2′W) since August 1993 (Thunell, 1998) (Fig. 1). Over the course of the trapping program, the deep-moored Mark VI sediment trap has been positioned between 490 and 540 m water depth (total water depth ≈590 m). Deployments last ∼6 months, such that each of the 13 trap cups continuously collect material for ∼2 weeks. Cups are prepared with filtered seawater amended with preservatives and buffers to a final

Pseudo-nitzschia in sinking particles and bottom sediments

Light microscopy of sediment trap material revealed that Pseudo-nitzschia was present as broken fragments and whole frustules, and in some cases as intact chains of two to four frustules in length. Other diatom genera commonly present included Skeletonema, Ditylum, Coscinodiscus, Chaetoceros, Thalassionema, Navicula. Other plankton frequently observed were foraminifera and coccolithophores (intact or as individual coccoliths). Closer inspection of Pseudo-nitzschia within the trap cups using

Quantifying DA in sediment trap samples

In previous studies measuring DA in sediment trap samples, DA was determined by either: (1) methanol extraction of a wet split of the sediment trap sample which collectively accounts for toxin in the particulate and dissolved phases (Schnetzer et al., 2007, Sekula-Wood et al., 2009) or (2) separate analyses of trap particulates and aliquots of trap cup solution (Sekula-Wood et al., 2009) which were then summed (given mass and volume corrections). Both approaches are reasonable for determining

Conclusions

Long time-series measurements of sediment trap material collected at ∼500 m water depth suggests that toxic blooms of Pseudo-nitzschia have occurred annually in SBB since at least 1994 and have increased in magnitude beginning in 2000. These Pseudo-nitzschia blooms are dominated by P. australis, one of the most toxic Pseudo-nitzschia spp. in the California region. The vertical transport of DA-laden particles represents a significant sink of the toxin to deeper waters and a source of toxin for

Acknowledgements

We thank Eric Tappa for his outstanding contributions to the success of the SBB sediment trapping program and the crew of the R/V Yellowfin for their efforts in both sediment trap deployments and recovery. We also wish to thank Steven Bograd for his advice on the NPGO. Two anonymous reviewers helped to significantly improve the manuscript. This work was supported in part by the National Science Foundation Chemical Oceanography Program, Grant #OCE0850425.

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