Response of diatoms and silicoflagellates to climate change and warming in the California Current during the past 250 years and the recent rise of the toxic diatom Pseudo-nitzschia australis

Quaternary International 310 (2013) 140e154

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Response of diatoms and silicoflagellates to climate change and warming in the California Current during the past 250 years and the recent rise of the toxic diatom Pseudo-nitzschia australis John A. Barron a, *, David Bukry a, David B. Field b, Bruce Finney c, d a

Volcano Science Center, U.S. Geological Survey, 345 Middlefield Road, MS 910, Menlo Park, CA 94025, USA Department of Natural and Computational Sciences, Hawaii Pacific University, Kaneohe, HI 96744, USA Department of Geosciences, Idaho State University, Pocatello, ID 83209-8007, USA d Department of Biological Sciences, Idaho State University, Pocatello, ID 83209-8007, USA b c

a r t i c l e i n f o

a b s t r a c t

Article history: Available online 11 July 2012

Diatoms and silicoflagellate assemblages were examined in two year-increments of varved samples spanning the interval from 1748 through 2007 in Santa Barbara Basin (SBB) box core SBBC0806 to determine the timing and impact of possible 20th century warming on several different components of the plankton. Diatoms (Thalassionema nitzschioides ¼ TN) and silicoflagellates (Distephanus speculum s.l. ¼ DS) indicative of cooler waters and a shallow thermocline begin to decline in the 1920s and persistently compose a lower percentage of the assemblage in the SBB by about 1940. Prior to 1940, TN constituted on average w30% of the Chaetoceros-free diatom sediment assemblage and DS on average w36% of the silicoflagellate assemblage. Between 1940 and 1996, these relative abundances were w20% (TN) and w8% (DS). These results are consistent with results from planktonic foraminifera and radiolarians that indicate an influence of 20th century warming on marine ecosystems before most scientific observations began. Cooling of surface waters coincident with the one of the strongest La Niña events of the 20th century (and a return to negative PDO conditions) in late 1998 brought about a return to pre-1940 values of these cool water taxa (TN w31%, DS w25%). However, this recent regional cooling appears to have been accompanied by profound changes in the diatom assemblage. Pseudo-nitzschia australis, and Pseudo-nitzschia multiseries, diatom species associated with domoic acid, a neurotoxin that causes shellfish poisoning and marine mammal deaths, rapidly became dominant in the SBB sediment record at the time of the regional cooling (1999) and increased substantially in numbers as a bloomforming taxon (relative to Chaetoceros spores) in 2003. Prior to 2003, diatom blooms recorded in the SBB sediment record consisted predominantly of Chaetoceros spores and less commonly of Rhizosoleniarelated species (Neocalyptrella robusta and Rhizosolenia setigera). Fecal pellets dominated by valves of P. australis, however, were particularly abundant in both the 2003 and 2006 samples, coincident with recorded incidents of domoic acid increase and widespread shellfish poisoning in the SBB. Ó 2012 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction Understanding the nature of natural variability in climate and ecosystems is a critical aspect of understanding the response of ocean ecosystems to recent warming and anthropogenic activities. In the North Pacific, many studies relate variations in populations of plankton and fish over the last several decades to basin-scale

* Corresponding author. E-mail addresses: [email protected] (J.A. Barron), [email protected] (D. Bukry), dfi[email protected] (D.B. Field), fi[email protected] (B. Finney). 1040-6182/$ e see front matter Ó 2012 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2012.07.002

fluctuations in climate that are characterized by the Pacific Decadal Oscillation (PDO; Mantua et al., 1997; De Bernardi et al., 2008; Grelaud et al., 2009). Such variability makes it difficult to separate the effects of the secular warming trend from changes associated with the PDO. However, much longer time series of radiolarians, foraminifera, diatoms, and silicoflagellates from Santa Barbara Basin (SBB) sediments indicate that a 20th century warming trend began influencing marine populations of the California Current (CC) before most time series of fish catch and plankton sampling began (Weinheimer et al., 1999; Field et al., 2006a). Because different taxa have different responses to ocean conditions, it is important to determine when the warming trend

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began affecting different taxa, and how well downcore changes in any given taxa reflect variations throughout the ecosystem. Recent work found that both diatoms and silicoflagellates showed an influence of the warming trend but was unable to determine when the warming influence began (Barron et al., 2010). Assemblages were quantified from two-year increments of box core SBBC2902 spanning the years 1940 through 2001 and compared with those recovered from Ocean Drilling Program (ODP) Hole 893A between w220 BC and AD 1880 (warm-water diatoms (Fragilariopsis doliolus and Nitzschia interrupeteseriata)) and silicoflagellates (mainly Dictyocha stapedia) were much more common in the younger box core than in the uppermost samples of ODP 893A, suggesting that considerable warming of surface waters occurred between w1880 and 1940. Since the relative abundance of these warm-water diatoms and silicoflagellates tracked sea surface temperature (SST) during the past 60 years in the SBB, it was concluded that the response of diatoms and silicoflagellates to 20th century warming was anomalous relative to the last two millennia of change. While late 20th century warming is clearly linked to anthropogenic activities (Levitus et al., 2000), it is unclear whether early 20th century warming is linked to anthropogenic activities or not. Modeling studies suggest that an influence, albeit small, is quite possible, particularly in the North Pacific (Barnett et al., 2005). One reason that early 20th century warming may appear anomalous in many Northern Hemisphere records is that several pulses of cooling associated with volcanic activity resulted in anomalous cooling in the late 19th and early 20th century (Crowley, 2000). A decrease in solar radiation could also have played a role in northern hemisphere cooling prior to the 20th century (Crowley, 2000). Therefore, early 20th century warming might merely be a consequence of ascent out of the Little Ice Age (LIA) into warmer ocean surface conditions. Complicating the issue of whether early 20th century warming in the California Current might be due in part to anthropogenic activities is evidence that the eastern North Pacific climate may differ from the general Northern Hemisphere reconstructions. There are conflicting records indicating that the California Current and central tropical Pacific may have been cooler during the LIA (Fisler and Hendy, 2008), while others indicate a warming (Graham et al., 2007). These differences may be due to the use of different proxies that reflect different water mass conditions. Examination of diatoms and silicoflagellate assemblages over the last 2000 years suggested the interval of the Medieval Climate Anomaly (MCA) between wAD 880 and 1350 was generally cooler than that of the LIA (wAD 1400e1800) in the California Current. Other evidence also suggests that the eastern Pacific was anomalously warm during the LIA (Graham et al., 2007). Therefore, understanding the nature of the early 20th century warming in the California Current is of particular interest. The present study uses two-year sampling intervals to better resolve the multiannual variability of the last w250 years and the nature of 20th century warming on different taxa of diatoms and silicoflagellates. 2. Background 2.1. Regional setting The varved sediments of the Santa Barbara Basin (Fig. 1) have been the focus of numerous high-resolution climate and paleoclimate studies over timescales ranging from subannual resolution to millennia across the past w140,000 years (e.g. Schimmelmann et al., 2006; Kennett et al., 2007; Grelaud et al., 2009). The regular occurrence of anoxic bottom waters inhibits bioturbation and results in good preservation of many fossils. Moreover, high

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a

b Fig. 1. Location map of the Santa Barbara Basin showing the box core studied, bathymetry in meters, and general surface circulation. B e Seasonal circulation of the California Current (CC) modified from P.T. Strub, written comm., 2007; SBB ¼ Santa Barbara Basin; WWD ¼ West Wind Drift; SCC ¼ Southern California Countercurrent; PtC ¼ Pt. Conception; DC ¼ Davidson Current.

sedimentation rates and seasonal differences in particle flux result in annual varves that can be counted to develop a chronology more accurate than radiocarbon or 210Pb dating permit. Nonetheless, many periods of the sediment record have unclear varve sequences that challenge development of an accurate chronology. The location of the SBB, southeast of Point Conception and shoreward of the southeasterly-flowing, cool-water California Current (CC), results in complex, seasonally changing oceanographic conditions (Fig. 1). Strong northwesterly winds associated with the offshore high-pressure cell over the California Current induce coastal upwelling during most of the year. These winds are most intense in spring, resulting in the lowest sea surface temperatures (SSTs). During other seasons of the year, the combination of upwelling favorable wind events and the advection of warmer surface waters from the south via the Southern California Countercurrent (SCC) result in cyclonic circulation over the basin (Harms and Winant, 1998). The influence of the SCC on the surface waters of the SBB is especially strong during the summer and early fall when SSTs are typically the highest. During the late fall and winter, the Davidson Current, a northward-flowing, coastal countercurrent that extends northward to w40 N (Hendershott and Winnant, 1996; Di Lorenzo, 2003), is especially active. Average SSTs in the SBB range from about 13  C in the spring to 18  C in the late summer, although higher (lower) SSTs can occur seasonally during El Niño (La Niña) events (California Cooperative Oceanic Fisheries {CalCOFI} Investigations database http://www.calcofi.org/ newhome/data/database/database.htm).

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2.2. Sea surface temperature variability around the Santa Barbara Basin The major interannual, decadal, and secular variations observed in SST and zooplankton abundance in or near the SBB follow the same patterns of variability observed coherently throughout the California Current (McGowran et al., 1998; Field et al., 2006b). The SBB lies within a region of predominantly cyclonic circulation, whereby warmer water from the southern California bight is advected northward via the countercurrent, while recently upwelled water off Point Conception can be advected eastward over the basin. The relative amount of upwelling is accentuated by a strong high pressure offshore, causing anomalously cool SSTs and advection of species more strongly associated with the California Current and/or upwelling environments. During anomalous warming in the California Current, an increase in the countercurrent transports warmer water and a greater portion of tropical and subtropical species from farther south in the bight (Venrick et al., 2006). Thus regional and basin-scale oceanographic processes can accentuate large-scale forcing of changing SST and plankton, even though upwelling events add an additional component of variability (Venrick et al., 2006; Field et al., 2006b). Various studies on planktonic foraminifers, calcareous nannoplankton, diatoms, radiolarians, and silicoflagellates have clearly demonstrated response of SBB assemblages to the major El NiñoSouthern Oscillation (ENSO) events of the late 20th Century (e.g., Lange et al., 2000; Black et al., 2001; De Bernardi et al., 2008). However, it is also clear that different taxa have different responses and timescales of response to oceanographic conditions. Moreover, SST is often just a surrogate variable of the important processes of change. Due to the different responses of different taxa, it is becoming increasingly apparent that multiple proxies are necessary to have confidence in paleoceanographic records. El Niño-Southern Oscillation and the Pacific Decadal Oscillation (PDO) as well as a long term, secular warming trend affect modern surface water conditions in the SBB. The ENSO events begin in the tropical Pacific with warm/cold phases varying every 2 to 7e8 years (Grelaud et al., 2009). The largest temperature anomaly associated with El Niño is within the thermocline, which results in a deepened and thickened thermocline and nutricline. In contrast, decadalscale changes associated with the PDO primarily result in a change in surface stratification, with little change in the depth of the thermocline and nutricline. The PDO is defined as the leading principal component of Pacific Ocean SSTs north of 20 N with the trend removed and primarily captures a dipole of anomalous SSTs between the central and the eastern North Pacific (Mantua et al., 1997). This dipole is the dominant pattern of variability in SST in the North Pacific, although there are several different processes that can result in this pattern (Schneider and Cornuelle, 2005). While the PDO pattern accounts for much of the variability in SST, the influence of the warming trend is becoming increasingly important to SST change and ecosystems (Field et al., 2006b). 3. SST variability of the past w300 years A fundamental aspect of understanding the potential effect of the 20th century warming trend is the need to determine the relative role of long-term variability. Instrumental SST records in the SBB compiled by CalCOFI extend back to the 1950s, while those at Scripps Pier and Pacific Grove extend respectively back to 1916 and 1919. Field et al. (2006b) compared these SST records with reconstructed SST records from the North Pacific between 1900 and 2006. They noted that 18e48% of the variability seen in annually averaged SST anomalies is associated with the PDO on interannual and decadal timescales, which ranges from about 1.5 to 4  C in

different regions. In addition, they noted that the secular increase in SST of 0.6e1.0  C over the past 100 years in different regions of the North Pacific, particularly the California Current, is approaching (although still less than) the range of variability in SST that is associated with the PDO and may have a persistent impact on populations of some organisms. Finally, Field et al. (2006b) noted that records from Pacific Grove, the International Comprehensive Ocean-Atmosphere Data Set (ICOADS) and planktonic foraminifera from the Santa Barbara Basin all suggested very strong negative SST anomalies in the early 20th century, whereas the more well known Scripps pier record does not indicate such a cool early 20th century. However, the lack of reliable SST records in the early 20th century points to the importance of having good paleo records spanning this time period. The SST trend of the California Current is slightly larger than the linear trend in global mean SST over the 1900e2005 period of approximately 0.6  0.2  C (Smith and Reynolds, 2004). Di Lorenzo et al. (2005) found that warming off southern California since the mid-1970s could only be explained by large scale atmospheric heating, while analyses of broader oceanic regions conclude that the ocean’s heat content has increased by a magnitude that could only be explained by greenhouse gas forcing (Levitus et al., 2000). Therefore, Field et al. (2006a, 2006b) argued that highly anomalous increases in the abundance of tropical and subtropical foraminifera were a clear response to anthropogenically forced global warming. A number of other high-resolution studies have attempted to expand these proxy studies back through the past 300 years or more to address both natural variability and SST. Some of these studies aim to reconstruct the dipole of SST anomalies associated with the PDO through analyses of tree ring thickness, which reflect temperature and precipitation. Other studies aim to reconstruct SST, or the response to SST by marine organisms from varved sediments of the SBB. In investigations of marine organisms from the SBB, there are several studies indicating an influence of 20th century warming. Weinheimer and Cayan (1997) and Weinheimer et al. (1999) examined variations in radiolarian assemblages in SBB sediments since the early 1900s and suggested that warming of surface waters has been occurring throughout the 20th century. The radiolarian assemblages also indicate that reduced upwelling of nutrient-rich surface waters occurred at multiple times during the 20th century and was well established by the 1960s: however, their study included only the 20th century. Field et al. (2006a) used a longer box core record spanning over 250 years to examine the influence of the warming trend on zooplankton and place 20th century variability into a longer-term perspective. An increase in abundance of primarily tropical and subtropical species along with a decrease in the abundance of the sinistral form of Neoglooquadrina pachyderma that has a subpolar to polar affinity was captured by the first principal component (PC1) of the abundances. This increase in subtropical species was highly anomalous compared with all species for the last few centuries, and analysis of several species indicated that 20th century warming was anomalous relative to assemblage changes occurring over the last 1400 years. Their second principal component PC2 was made up primarily of species with temperate to polar affinities and reflected a dramatic reduction in these species in the late 20th century. Field et al. (2006a) showed that their PC1 reflected SST variability during the last 100 years and that a strong divergence of PC1 from PC2 in the late 20th century reflected an ecosystem response to highly anomalous ocean warming. De Bernardi et al. (2008) completed a high-resolution study of calcareous nannofossils in a SBB box core covering the interval from a shorter time period, 1940 through 1996. They noted that

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Gephyrocapsa oceanica production increased during El Niño years in response to higher SSTs, whereas the flux of Helicospaera carteri increased during La Niña conditions and lower SSTs. They also reported that increased abundances of Florisphaera profunda and Umilicosphaera sibogae after 1970 reflected a warming trend and increased stratification of the water column associated with the warm phase of PDO. During the previous cold phase of the PDO, De Bernardi et al. (2008) noted increased abundances of Coccolithus pelagicus and Calcidiscus leptoporus. Work in progress from longer cores indicates that increases of F. profunda and U. sibogae of the 20th century are also anomalous and support conclusions from foraminifera and radiolarians (De Bernardi et al., personal communication 2010). A study using automated counts of coccolithophorids found different results than the microscope quantification by De Bernardi et al. (2008). Grelaud et al.’s (2009) automated counts of coccolithophores span from 1917 to 2004 and focus on six species that represent at least 96% of the total assemblage. They argue that G. oceanica, H. carteri, and F. profunda are proxies for the strength of the northward-flowing, warm-water California Counter Current, whereas Gephyrocapsa ericsonii and Gephyrocapsa mullerae are characteristic of the colder California Current. They suggest that increased relative abundances of G. oceanica and H. carteri are associated with warm ENSO events, whereas G. mullerae increases during warm PDO events and G. ericsonii abundance increases during cold PDO events. Grelaud et al. (2009) did not feel that their coccolithophore assemblage changes showed any evidence of the 20th Century warming reported by others, arguing that seasonal differences in SST within the SBB are much greater than the 1.5  C regional warming that has been reported by Roemmich and McGowan (1995). However, they did observe a >33% increase in the mean weight of coccoliths of the Order Isochrysidales that are associated with the California Counter Current between 1917 and 2004. Nevertheless, the validity of automated counts remains to be established. Records from geochemical techniques and biomarkers often match some interannual variations in temperature, but they do not consistently indicate a clear 20th century warming, nor do they suggest a warming since prior centuries. Zhao et al. (2000) published a high-resolution alkenone (UK0 37) SST record for the period of 1440e1940 in the SBB. They argued that positive SST anomalies were generally between 0.0 and þ0.5  C from 1650 to 1850 with an exception of a cooler period (0 to 0.5  C) recorded between 1750 and 1770. However, Zhao et al. (2000) observed that individual increases in alkenone SST did not correlate well with historical ENSO records, which questions the reliability of alkenones as indicators of SST in the SBB. In a study of sediment trap samples, Hardee and Thunell (2006) found that the alkenone temperature index reflects temperatures within the chlorophyll maximum, as one might expect. The chlorophyll maximum is deeper over the SBB when stratification and SST increase, therefore the alkenone-derived temperature is likely to reflect a greater portion of thermocline waters rather than mixed-layer waters. Mollenhauer and Eglinton (2007) highlighted other fundamental problems with SST-indicating biomarkers in SBB. They concluded that some of the biomarkers are pre-aged (resuspended from elsewhere) and mixed with new biomarkers, therefore resulting in questionable SST records. Huguet et al. (2007) investigated the TEX86 temperature proxy based on marine crenarchaeotal membrane lipids in a two-yearlong sediment trap study and applied the technique to a highresolution sediment record from 1850 to 1987. After comparison with instrumental SST records, they concluded that TEX86 records reflect subsurface temperatures in the SBB but do not reflect interannual variability in temperature due to changes in habitat production of the Crenarchaeotal.

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The purpose of this study is to extend the diatom and silicoflagellate paleoclimate data in the SBB from the recent back to the middle part of the 18th century at a two-year resolution in order to compare natural climate variability with potential 20th century anthropogenic change. In particular, the aim is to further test the hypothesis that the 20th century warming was anomalous relative to natural variability and had a large and notable effect on various members of pelagic ecosystems. 4. Material and methods 4.1. Samples and chronology Box core SBBC0806 was collected at 3413.30 N, 120 01.70 W in the deepest portion of the SBB in June 2008 with a Soutar box corer. The presence of bacterial mats at the surface indicated that the sediment surface was recovered for box core. The site for this core was chosen based on the excellent laminae structure observed in core SBBC 3001-1001. SBBC0806 was subsampled with a 14  14 cm acrylic liner that was inserted into the core on board ship. The core bottom was frozen with dry ice to prevent sediment slumping upon opening. The core was then opened and the frozen sediments surrounding the liner washed away until the acrylic liner could be sealed at the bottom. The cores was stored at w5  C and allowed to drain. Long vertical sections of the core were sliced into slabs along the vertical axis of the core. The slab used for analyses was Xradiographed from three different perspectives by centering the Xray beam vertically over the top and bottom of the slab to obtain the best focus of the laminae structure. A detailed chronology was developed based on visual cross correlation of individual varves from the X-radiographs of this core compared with a master chronology developed from different slabs of six different cores (Supplementary Fig. S1; Tables S1 and S2). Since sedimentary sequences vary across the basin, examination of slabs from several cores reveals different perspectives of the laminae structure. Gray layers were considered as instantaneous deposits (Hülsemann and Emery, 1961) for the chronology developed. This chronology is anchored by the well-established varve count from several box cores extending to 1880 that has been verified by 210Pb dating (Soutar and Crill, 1977). As shown in Supplementary Fig. S1, comparison of Field et al.’s (2006a) varve chronology with that of Schimmelmann et al. (2006) is straightforward down to the varve identified as 1900 (varve #102 of Field). However, the chronologies diverge below 1900 (Supplementary Fig. S1). There is a clear correlation of a distinctive varve lying above a homogeneous layer, which Schimmelmann et al. (2006) determine to be 1862 with varve #143, estimated to be the year 1859 (suggesting a negative three-year offset in chronology with theirs). On the other hand, a distinctive varve lying immediately above the homogenous Macoma layer (varve #168) is dated at 1834, whereas Schimmelmann et al. (2006) place the age of the same varve at 1841; thereby, suggesting a negative seven-year offset in chronology further downcore. An age of 1886 is assigned to the first of three distinctively light colored varves (varve #116), which appears to be dated as 1890 by Schimmelmann et al. (2006) (or a negative four-year offset in the chronology). The difference between the chronologies likely arises from the higher quality X-radiographs available to Field et al. (2006b) and differences in varve interpretation between groups. 4.2. Processing and slide preparation Samples from SBBC0806 were placed in a glass vial and covered by a volume of 7e10 times more distilled water than that occupied by the sample. A disposable wooden stick was then used to

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disaggregate the samples in the vials by stirring the suspension. To prepare slides, the vial was shaken and a drop of the suspension was taken after 5e10 s of settling from near the top of the vial, transferred to a 30  22 mm cover slip and allowed to dry on a warming tray overnight. Slides were then mounted in Naphrax (index of refraction ¼ 1.74). 4.3. Diatoms At least 300 individual diatoms were counted per sample by making random traverses of the slide under the light microscope at 1250 using the counting techniques of Schrader and Gersonde (1978). Following Sancetta (1992) and Barron et al. (2003), Chaetoceros resting spores, which dominate in nearshore coastal upwelling environments (Lopes et al., 2006), were not counted in order to better resolve differences in offshore oceanic conditions. Chaetoceros spores are resistant to dissolution, so that their relative numbers may be enhanced in recycled sediments. Relative diatom abundances were estimated by recording the number of diatom valves encountered while making vertical traverses of the slide (length of traverse ¼ 22 mm) at 1250 (total area covered per traverse ¼ 4.114 mm2) under the light microscope. Random traverses were made until >300 diatom valves were counted. The taxonomy of Barron et al. (2003) was followed.

4.4. Silicoflagellates One to three slides were systematically scanned to obtain a representative count of 50e100 silicoflagellate specimens per sample. Light microscope counts typically were made at 250 magnification, with 500 used for checking questionable specimens. Taxonomy follows that used by Barron et al. (2004, 2005) and Barron and Bukry (2007). Intraspecific variants of silicoflagellate taxa were tabulated in an effort to determine environmental preferences.

4.5. Biogenic opal Samples were freeze-dried and acid-washed to remove carbonates via treatment in 1 N HCl overnight, followed by three rinses in deionized water. Samples were subsequently freeze-dried, homogenized and measured for biogenic silica (opal) following a wet-alkali extraction method modified from Mortlock and Froelich (1989). Values are reported as 10% hydrated opal (SiO2 $ 0.4 H2O) using a multiplier of 2.4 times the weight percent of biogenic silica content. An estimated error of <4.6% (calculated as the coefficient of variation) is based on replicate measurements of two internal sediment standards.

5. Results and discussion The downcore patterns of diatoms and silicoflagellates of the present study are presented in Figs. 2 and 3. Census data are show in Supplementary Tables S1 and S2. First, an overview is given of the taxonomical groupings and the general downcore patterns. Then, select data of the 20th century are compared with SST records to determine the linkage with climate. Having established some links with ocean climate, the multiannual to decadal variations prior to the 20th century are discussed, followed by an examination of the influence of 20th century warming on the assemblages. Finally, the anomalous diatom fluxes of the 21st century are discussed.

5.1. Diatoms 5.1.1. Assemblage data The relative abundance of the dominant diatom taxa in box core SBBC0806 below the 2001 varve is presented in Fig. 2. Below the 1994 varve, the diatom assemblage represents a composite of two years’ deposition and data are plotted at the age of the older varve. Above 1994, analyses were done on annual intervals. The great majority of diatom taxa that dominate in the surface plankton are not preserved in the sediments (Venrick et al., 2006). This is especially true of Chaetoceros, a bloom-forming diatom, associated with spring upwelling events. Chaetoceros is commonly only represented by resting spores in the sediment. When present in the sediment, it is difficult to determine whether the resting spores of Chaetoceros were part of the year’s deposition or whether there have been reworked from previous years. Consequently, in the same manner as Barron et al. (2010), diatom relative abundances are tabulated as percent of the Chaetoceros spore-free assemblage. Thalassionema nitzschioides, a cosmopolitan species that is indicative of a shallow thermocline and presumably the cooler surface waters associated with spring, is plotted on the left side of Fig. 2 along with Rhizosolenia-related spp., bloom-forming diatoms in the SBB that consists mostly of Neocalyptrella robusta and Rhizosolenia setigera. Dense groupings of Rhizosolenia-related valves, presumably deposited in fecal pellets were observed in SBB samples characterized by high relative abundances of Rhizosoleniarelated spp. (Table S1). Warm-water diatom taxa are plotted in the middle of Fig. 2 with F. doliolus and Nitzschia interrupteseriata, the warm-water diatoms used by Barron et al. (2010) compiled separately from more sparsely-occurring warm-water taxa including Azpeitia nodulifera, Azpeitia africana, Azpeitia tabularis, Hemidiscus cuneiformis, Roperia tesselata, and Thalassiosira oestrupii. These species show many multiannual to decadal variations throughout the downcore record, but with a tendency towards increasing proportions during the 20th century. Benthic diatoms and other transported diatoms, including freshwater and reworked taxa as well as the tychopelagic or shelfassociated taxa such as Actinoptychus spp., Paralia sulcata, and Stephanopyxis spp. are plotted to the right. These species are not likely to have a clear link with climate change, but their abundance may be affected indirectly through variations in freshwater transport, mixing, or other processes affecting sediment transport. Two unusual trends in diatom relative abundances are apparent in the more recent part of the SBBC0806 diatom record. T. nitzschioides, which is indicative of a shallow thermocline, declines after 1940, suggesting a warming of SBB surface waters and/or increased stratification of surface waters in agreement with the planktonic foraminiferal interpretations of Field et al. (2006a) and with analysis of instrumental records by Field et al. (2006b). Perhaps, more surprising, however, is the recent rise in dominance of Pseudo-nitzschia plotted on the left side of Fig. 2. Prior to 1999, bloom-forming diatoms other than Chaetoceros spores consist of Rhizosolenia-related spp. (N. robusta and R. setigera). Beginning in 1999, the abundance of Pseudo-nitzschia species (P. multiseries and P. australis, a neurotoxin-secreting diatom) increases markedly in the sediments. 5.2. Silicoflagellates Unlike diatoms, silicoflagellate assemblages are not reported to be different between the plankton and those preserved in the sediments. However, they are much less abundant than diatoms in SBB sediment samples, and it can be time consuming to count large numbers of specimens.

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Fig. 2. Relative abundance of the main diatom taxa in core SBBC0806 as a percent of the Chaetoceros-free assemblage. Fd þ Ni ¼ Fragilariopsis doliolus þ Nitzschia interrupteseriata.

5.2.1. Assemblage data The relative abundance of selected silicoflagellate taxa in box core SBBC0806 are presented in Fig. 3. Dictyocha aculeata, a taxon that is associated with deeper thermocline conditions in waters spanning the tropical Pacific to the Gulf of Alaska, is plotted on the left side of Fig. 3. Its wide geographic distribution suggests that this species may be less sensitive to climate change. Distephanus speculum s.l., a silicoflagellate typical of a shallow thermocline or upwelling conditions and its even cooler water variant, D. speculum minutus, are plotted to the right. These species are likely to indicate increases in transport of cold water from the California Current or upwelling. Silicoflagellates characteristic of warmer surface waters include Dictyocha perlaevis, D. stapedia aspinosa, and D. stapedia. These warm-water Dictyocha taxa are grouped together and plotted in the center of Fig. 3, with D. perlaevis plotted separately. The vast majority of the other warm-water silicoflagellates consist of D. stapedia and its varieties. Octactis pulchra, a silicoflagellate associated with upwelling in tropical waters, and Distephanus octangulatus, a subarctic form, are plotted to the right. The silicoflagellate assemblages also show many interannual to decadal variations throughout the last several centuries, along with an increase (decrease) in tropical and subtropical (temperate and

subpolar) species during the 20th century. Beginning at about 1940, D. speculum s.l., declines sharply in relative abundance from values that had been averaging w40% of the silicoflagellate assemblage prior to 1900 to values <20%, suggesting a deepening of the thermocline in the SBB, similar to what is implied by diatoms and planktonic foraminifers. Octactis, a tropical upwelling form, fluctuates at low percentages throughout the SBBC0806 record, although it appears to increase during the 20th century. D. octangulatus, a subarctic form, occurs sporadically in consecutive sampling intervals during the following intervals: 1756e1766, 1857e1863, and 1923e1925 (Fig. 3). D. octangulatus also occurs occasionally in single sampling intervals. The period of absence of D. octangulatus from 1925 to 2006 is the longest in the record (although it was also absent from 1863 to 1923). 5.3. Comparison of assemblages with anomaly SST The downcore records are compared with instrumental records to determine how well the percentage of a given species may reflect changes in ocean conditions over the last 100 years. Fig. 4A compares the relative abundance of warm-water diatoms for the

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Fig. 3. Relative abundance of the main silicoflagellate taxa in core SBBC0806.

interval of 1900 through 2003 with the Kaplan reconstructed SST anomalies for the 5  5 grid centered at 32.5 N, 122.5 W (Kaplan et al., 1998). The Kaplan SST index is chosen because it represents a larger area off of California and therefore may represent more of the large-scale changes in the California Current, although it is highly correlated with other indices (Field et al., 2006b). In general, the temporal pattern of the relative abundance of warm-water diatoms and anomaly SST are similar. While there is a significant correlation between diatoms with SST (R2 value ¼ 0.12; p < 0.001) when compared for the same yearly increments, the amount of variability explained is low. Multiple reasons may explain why the relationship between diatoms with SST anomalies is not higher. First, there could be slight misalignment between the sediment sampling and the chronology determined by X-radiography, or one to two year offsets between the varve chronology and calendar years (due to difficulty in distinguishing varves from intraseasonal changes in sediment). For

example, the observation that warm-water diatoms sometime lag changes in SST by one sampling interval in the early 20th century could be due to such errors. However, such offsets would not be expected to be consistent throughout the record. Second, the period of the early 1950s has a large portion of warm-water diatoms but anomalously low SSTs. This same time period also shows low oxygen isotope values in several species of planktonic foraminifera, which is also suggestive of warmer waters, even though CalCOFI records clearly indicate some of the lower SSTs on record (Field, 2004). The cause of anomalous signals in several proxies during the 1950s remains unknown. Finally, the timescales of change that affect diatoms are much shorter than the SST annual averages. The diatom assemblage present in two-year composite samples is likely to be strongly biased by blooms that are related to brief periods of preferred conditions. Fig. 4B and C, respectively, compare the relative abundance of warm-water silicoflagellates of the genus Dictyocha and the

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Fig. 4. Comparison of various climate sensitive species groupings with SST anomalies: warm-water diatoms (A); warm Dictyocha (silicoflagellates) (B); Distephanus speculum (silicoflagellates) (C); Principal Component 1 of planktonic foraminifera (representing tropical and subtropical species) (D). SST is the Kaplan reconstructed SST anomaly for the 5  5 grid centered at 122.5 W, 32.5 N (Kaplan et al., 1998).

cool-water proxy D. speculum with SST anomalies. The relative abundance of warm-water Dictyocha displays a moderately good (for paleoceanographic indices) correlation with SST anomalies (R2 value of 0.30; p < 0.001) when values are compared for the same temporal intervals. The temporal changes, in particular the longterm trend, of the reconstructed anomaly SST and the relative abundance of warm-water Dictyocha are remarkably similar. However, like the diatoms, some downcore variations in silicoflagellates may precede or follow variations in SST anomalies by one sampling interval, perhaps due to an offset in the varve sampling. The relative abundances of D. speculum, on the other

hand, display a negative (R2 value of 0.26; p < 0.001) relationship with SST anomalies. One notable deviation in the relationship occurs during the time period from approximately 1945e1975, a time of lower SST anomalies in the 20th century (but not necessarily anomalously low in the longer term perspective). In order to put the results of the present study into the context of previous work, Fig. 4D compares PC 1 (Principal Component 1) of planktonic foraminifera (from Field et al., 2006a), which represents tropical and subtropical species, with the SST anomalies for the interval of 1901 through 2001, as described in detail in Field et al. (2006a, 2006b). PC1 displays a moderately good correlation with

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SST (R2 value of 0.31), similar to the relationship found with silicoflagellates. However, PC1 appears to be persistently higher than SST in the late 20th century relative to the early 20th century. There is no reason to expect linear relationships between the indices with SST as changes in planktonic foraminiferal might be partly due to a biogeographic shift in populations (or other non-linear factors), whereas the interannual changes are more likely to be related to changes in regional upper ocean conditions. While the indices from each different taxa (diatoms, silicoflagellates, and foraminifera) do not have strong relationships with SST, strong relationships are not necessarily expected from sedimentary records due to the numerous processes (biological, oceanographic, and sedimentological) that affect paleoceanographic proxies (e.g. Field, 2004). However, each different taxon has different ecological niches and often deviates from SST in different portions of the record. Application of three different taxa provides a multi-proxy approach to determining major climate signals on plankton, by noting where at least two or more indices are in agreement. By the same reasoning, it is of interest that no index showed a relationship with the PDO. Mantua et al.’s (1997, updated http://jisao.washington.edu/pdo/ ) index for the PDO for 1900 through 2010 was also compared with the assemblage data. However, the various diatom, silicoflagellate, or foraminiferal indices all have weaker relationships with the PDO than with SST, with R2 values (data combined for comparable intervals) only being significant for warm-water Dictyocha (R2 ¼ 0.09; p < 0.05) and non-significant for all the other indices. The lack of a relationship with the PDO does not mean that basin-scale processes do not affect these organisms. Rather, the lack of a relationship is likely a consequence of the fact that the PDO has the warming trend removed and the assemblage data all suggest a strong influence of the warming trend across the last century. 5.4. Microfossil proxy SST data for interval w1750e1900 The comparison of downcore variations with SST makes it apparent that each of the taxa reflects variations in upper ocean conditions to some extent, although different taxa have different responses to the SST anomalies over the past century. Thus, downcore anomalies present in at least two of the proxy records are considered to be meaningful. The multiple proxies developed here are compared to examine multiannual to decadal variations prior to the 20th century. Fig. 5 compares the high-resolution records of planktonic foraminifera (A.), diatom (C.), and silicoflagellate (D.) SST proxies and % opal data (B.) (Table S3) in SBB0806 between 1750 and 1900. Although the planktonic foraminifera data were taken from box core SBBC3001-1001 (Field et al., 2006a) and the diatom and silicoflagellate data are from box core SBBC0806, correlation of individual varves has been done by X-radiographs (see Supplementary Fig. S1). Average values of PC 1 from planktonic foraminifera and warm-water diatoms between 1750 and 1900, as well their 1-sigma standard deviation, are plotted as dashed lines on the figure. Intervals containing more than one successive proxy SST value exceeding one standard deviation above or below the long-term average are highlighted in pink (above) and blue (below). For silicoflagellates, the warm Dictyocha proxy (red curve) is combined with the total percent of D. speculum, a cool-water indicator, (dashed blue curve), as they display a very strong (R2 ¼ 0.61) negative correlation with one another (as expected since they make up a large portion of the assemblage). The reconstructed PDO records of Biondi et al. (2001) and MacDonald and Case (2005) are added for comparison (Fig. 5E). It is assumed that cooler predicted SST should coincide with more negative predicted PDO, whereas conversely more positive PDO should mark intervals of warmer SST.

It should be remembered, however, that precise chronological matching of these various chronologies is difficult to confirm, so that curve matching is somewhat arbitrary. In general, there are very few intervals that show a strong agreement between all the different proxy records, although some intervals indicate cooling or warming from two or three of the proxies. Most of these intervals showing agreement between multiple proxies occur on a multiannual timescale, generally 2e3 sampling intervals (or 4e6 years). One interval of widespread agreement is the cooler interval indicated by the percent opal, diatoms and silicoflagellates between w1752 and 1758 (Fig. 5). This interval correlates well with a period of negative PDO recorded between about 1752 and 1756 by the two tree ring indices (event C1). Both diatoms and silicoflagellates suggest warmer SST conditions between w1770 and 1774. The PDO index of MacDonald and Case (2005) indicates strong positive PDO conditions during this time, whereas the index of Biondi et al. (2001) suggests only moderately positive PDO conditions the other microfossil proxies reasonable. The two silicoflagellate indices also indicate brief intervals of cooler SST between w1786e1788, 1806e1808, 1824e1829, 1860e1862, and 1890e1892 (blue shading in Fig. 5D) that compare reasonably well with intervals of negative PDO identified by both Biondi et al. (2001) and MacDonald and Case (2005) (blue shading in Fig. 5E). On the other hand, brief intervals of warmer SST suggested at w1810e1812, 1820e1822, 1865e1867, 1869e1871, 1875e1877, and 1883e1885 (pink shading in Fig. 5D) do not appear to correlate that well with intervals where positive PDO conditions are suggested. There are fewer periods of agreement between planktonic foraminifera and diatoms with other proxies. However, Fig. 5 shows that planktonic foraminifers and diatoms suggest an interval of warmer SSTs between 1838 and 1846. Although this warm event is not supported by silicoflagellates (Fig. 5), the PDO index of MacDonald and Case (2005) indicates fairly strong positive PDO values during this 1838e1842 interval, while Biondi et al.’s (2001) proxy PDO values are only moderately positive (Fig. 5E). 5.4.1. The Macoma event The Macoma shell layer is a massive, non-laminated layer containing shells of the pelecypod Macoma leptonoidea that is universally found near the top of the SBB varve sediment record (Soutar and Crill, 1977; Schimmelmann et al., 1992). Schimmelmann et al. (1992) propose that this interval reflects a brief period during which oxygen levels rose enough in SBB bottom waters to support benthic macrofauna. They argue that the Macoma shell layer is overlain by varved sediment that marks a return of low oxygen conditions to SBB bottom waters and suffocation of the Macoma, an event the Schimmelmann et al. (1992) date to 1840  2 years, about six to seven years younger than the date (AD 1834) that is suggested by the varve chronology (Fig. S1). However, when examining the Macoma layer from multiple cores, it is apparent that the thickness of the event varies between cores, even if the same varve structure is present above and below the layer. These stratigraphic changes suggest that the Macoma layer is an instantaneous deposit in time. Regardless of the origin of the Macoma event, the study by Schimmelmann et al. (1992) provides an opportunity to compare downcore changes documented by different studies. Schimmelmann et al. (1992) argue that decreased surface water productivity in the years immediately prior to deposition of the Macoma layer resulted in increased oxygen content of waters spilling over the sill of the SBB. The increased bottom water oxygen content allowed for the temporary colonization of the pelecypod on the floor of the SBB. Their study of multiple proxies indicated

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Fig. 5. Comparison of SST proxies and percent opal for the Santa Barbara basin for the interval of AD 1750 through 1900. Average values for PC1 of planktonic foraminifers (A), % opal (B), diatoms (C), and silicoflagellates (D) and their 1-sigma standard deviations are shown by dashed lines. For silicoflagellates, the warm SST proxy (red) is plotted along with the proxy for upwelling (cool SST conditions) (blue). Proxies are plotted so that warmer SSTs trend upward and cooler SSTs trend downward. Blue and pink shaded intervals indicate where two successive proxy data values exceed 1-sigma standard deviations for cool (blue) and warm (pink) events. The reconstructed Pacific Decadal Oscillation (PDO) records of Biondi et al. (2001) and MacDonald and Case (2005) are added for comparison (E). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

a warming prior to the Macoma event followed by a cooling and return to anoxia. Contrary to the findings of Schimmelmann et al. (1992), planktonic foraminiferal, diatom, and silicoflagellate SST proxies suggest that the interval immediately preceding the Macoma event was marked by cool to moderately cool SSTs (Fig. 5) that are not consistent with reduced productivity. Percent opal values were slightly lower than average during this pre-Macoma interval, but they were not any lower than background levels recorded for the w50 year long interval preceding the Macoma event. Immediately following the Macoma event layer percent opal

increases slightly (1e2%); however, the SST proxies for planktonic foraminifers, diatoms, and silicoflagellates all suggest surface water warming. Benthic and transported diatoms decline from relative abundances that are consistently >24% during the w50 years preceding the Macoma event to <16% across the Macoma event (Fig. 2). The reduction of benthic diatoms could indicate reduced downslope transport of shelf material into the SBB beginning with the Macoma event. Alternatively, if the Macoma layer is an instantaneous deposit from upslope, the upslope sediments may have accumulated less

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benthic diatoms (due to being located on the slope). Thus the true nature of the Macoma layer is not resolved here. 5.4.2. The storm of 1862 The California storm of January 1862 is considered the greatest storm in the written history of California (Engstrom, 1996). Beginning on Christmas Eve of 1861 and lasting for 45 days, a series of middle-latitude cyclones struck the coast. Widespread flooding occurred in both southern and northern California with lakes forming in the Mojave Desert and Los Angeles Basin and extensive arroyo cutting throughout southern California. Whereas two other large late 19th century floods in December 1867 and February 1891 were associated, respectively with a moderate and very strong El Niño, the storm of January 1862 coincided with colder than normal temperatures and an absence of El Niño conditions. Engstrom (1996) cites evidence from strong meridional circulation, with a large amplitude jet stream meander that gave rise to a deep upper level trough in the extreme eastern Pacific. He notes that a failure to identify the 1862 storm event in the SBB varve record was attributed by Soutar and Crill (1977) to the “basin’s (sediment record) inability . to respond (consistently) to specific high-rainfall years”. The varve chronology suggests that varve number 140 corresponds with the year 1862 (Fig. S1), although uncertainty in assignment of the year increases downcore. Planktonic foraminiferal, diatom, and silicoflagellate SST proxies all identify cooler than normal SST at or immediately preceding this varve (Fig. 5). The subarctic silicoflagellate, D. octangulatus, increased to relatively high abundances >5% during the four varves immediately preceding varve number 140 (Fig. 5, Table S2), suggesting anomalously cold conditions. It is possible that the relatively low amount of opal near and after this interval reflects dilution by terrigenous material rather than reduced productivity. 5.5. 20th century warming of the water column In order to illustrate the temporal patterns of 20th century warming that occur in the different proxies of the present study, downcore variations in each proxy are shown for the post-1900 period (Fig. 6). The average values and their standard deviations for planktonic foraminifers, diatoms, silicoflagellates, and percent opal between 1750 and 1900 are plotted as dashed lines on Fig. 6. Pink shading indicates intervals where these SST indices exceed more than one standard deviation above their 1750e1900 average values. Similarly, pink shading also indicates intervals where percent opal values are less than one standard deviation below their average 1750e1900 values. It is assumed that reduced diatom productivity associated with warmer SST would result in lower percent opal values. Perhaps the most notable aspect of this early 20th century warming is that it occurs in each of the individual proxies examined, whereas previous multiannual to decadal variations were usually inconsistent between proxies. Unlike the pre-20th century variations, the long-term (1750e1900) relative abundances of diatoms (Fig. 2) and silicoflagellates (Fig. 3) as well as % opal show additional evidence of early 20th century surface water warming observed in instrumental records and planktonic foraminiferal assemblages (Field et al., 2006a, b). Each of the proxies displayed in Fig. 6 shows evidence of early 20th century warming (e.g. before 1950), although the timing of the warming varies in each individual proxy. PC1 for planktonic foraminifera increases above the long-term average by the mid 1920s, with more persistently high values occurring by the late 1930s (Field, 2004). Percent opal values slowly decline from values near the long-term average in the early 1920s to anomalously low biosiliceous values in the late 1930’s. Both the diatom and

silicoflagellate indices show some warming in the late 1920s, but indicate persistent warming around 1940. Taken together, the proxy records consistently show that increases in SST that occurred from the mid 1920s to the late 1930s had a notable effect on marine ecosystems that exceeded the range of typical preceding variations. While the proxies all indicate anomalous 20th century warming from at least 1940 on, there are many multiannual to decadal variations superimposed upon the warming trend, including multiple returns to the long-term average. In particular, the warm Dictyocha (silicoflagellate) proxy returns to around or below the long-term average between the intervals of 1944e1954 and again from 1960 to 1977. These periods coincide with periods of a negative PDO and low instrumental SSTs. However, from the perspective of the proxy records, these decades show values typical of the longterm average. In contrast, from the perspective of the PDO or any record that does not extend the length of the 20th century or longer, these decades could be considered anomalously cool (and highly productive). Diatoms (T. nitzschioides) and silicoflagellates (D. speculum s.l.), indicative of cooler waters and a shallow thermocline, decline markedly in relative numbers in the SBB beginning at about 1940 (Figs. 2 and 3). Prior to that time, T. nitzschioides constituted on average w31% of the Chaetoceros-free diatom sediment assemblage, whereas D. speculum s.l. made up on average w36% of the silicoflagellate assemblage. Between 1940 and 1996 these relative abundances dropped to w20% (T. nitzschioides) and w8% (D. speculum s.l.). After the decline of D. speculum s.l. at w1940, silicoflagellate assemblages are dominated by D. aculeata, a species preferring of a deeper thermocline, and other taxa of the genus Dictyocha, which are indicative of warmer SSTs (Figs. 3 and 4). These two silicoflagellates display a strong negative relationship after 1940 (R2 ¼ 0.45), suggesting that with the reduced influence of the spring upwelling signal of D. speculum, SBB waters vary between dominance of a deep thermocline species, presumably winter conditions (D. aculeata), and warmer surface waters, presumably a summer-fall signal of warm Dictyocha species. Martínez López et al. (2007) completed a high-resolution study of diatom and silicoflagellate flux in SBB varves between 1909 and 1991. They noted that prior to the 1940’s diatom assemblages were characterized by gradual increasing fluxes of Chaetoceros spores and T. nitzschioides. After the 1940s, these taxa declined and were replaced by increased flux of large-sized diatoms of Coscinodiscus and Rhizosolenia. Martínez López et al. (2007) suggested that these changes were due to a reduction in the expression of the spring upwelling signal and an increase in the expression of the fallwinter signal that they attributed to global warming. Taken together, the combination of the present study, Barron et al. (2010), and that of Martínez López et al. (2007) suggest that the changes from the 1940s on are anomalous with respect to at least the last two thousand years. Cooling of surface waters coincident with the onset of negative PDO conditions, or a shift to a different regime (Bond et al., 2003) in the North Pacific in 1999 brought about a return to pre-1940 values of these cool water taxa (T. nitzschioides w31%, D. speculum s.l. w25%). Between 1941 and 1962, warm-water diatoms showed a steady increase in relative abundance from values <20% of the Chaetoceros-free diatom assemblage to values >30% (Fig. 7). Beginning in the 1964e1965 sample and continuing through the 1990e1991 sample, Rhizosolenia spp. displayed marked but sporadic fluctuations in relative abundance ranging as high as 57% and as low as 3% (Table S1). Where abundant, apical horns of N. robusta and R. setigera are concentrated in packages that appear to be fecal pellets, presumably recording bloom events. The results indicate a fundamental difference in the response to the negative

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Fig. 6. Comparison of SST proxies for the Santa Barbara basin for wAD 1900 through 2007. Average values of PC1 for planktonic foraminifers, % opal, diatoms and silicoflagellates with 1-sigma standard deviations for the years AD 1750-1900 shown by dashed lines. For silicoflagellates, the warm SST proxy (red) is plotted along with the proxy for upwelling (blue). Pink shaded regions indicate where SST proxy values exceed 1-sigma standard deviation for the mean of AD 1750e1900. Reconstructed Kaplan anomaly SST for the 5  5 grid centered at 12.5 E, 32.5 N and the monthly average PDO index (Mantua et al., 1997, updated) are compared at the bottom of the figure. Interruptions in the post 1940 trend of anomalously warm conditions (non pink intervals) tend to coincide with -PDO and cooler anomaly SST (gray shading). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

PDO values of recent years as compared with those from 1945 to 1975, which is particularly noteworthy with respect to Pseudonitzschia species. 5.5.1. The rise of Pseudo-nitzschia species Beginning in the 1986e1987 sample Pseudo-nitzschia multiseries (Psm) increased from very low relative abundances (consistently 1% during the entire high-resolution SBB0806 diatom record extending back through 1748) to >3% (Table S1, Fig. 2). The relative

abundance of Psm rose to 12% in the 1990e1991 sample and subsequently declined until the 1999 sample, where it increased to 26% (Table S1), an event documented by Barron et al. (2010) as a 5% relative abundance of Pseudo-nitzschia australis. Sibel Bargu Ates of Louisiana State University (written comm. 2010), however, recently confirmed by transmission electron microscope study, that the form that Barron et al. (2010) referred to as P. australis is, in fact, P. multiseries (Hasle). Dr. Bargu Ates also confirmed that a second Pseudo-nitzschia form that first occurs in the 1999 sample and

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Fig. 7. Light microscope photographs of and the record of Pseudo-nitzschia species in Santa Barbara Basin core SBBC0806 expressed as relative abundance of the Chaetoceros-free diatom assemblage (blue and red curves) and as a ratio to Chaetoceros spores (orange bars). X ¼ years of recorded shellfish poisoning and marine mammals deaths. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

increases to >26% of the Chaetoceros-free diatom assemblage in the 2002 sample is the more delicate form, P. australis (Fig. 7). In discussing the rise of Pseudo-nitzschia in the SBBC2902 Barron et al. (2010) noted that Fritz et al. (1992) were the first to show that an outbreak of domoic acid poisoning in seabirds in Monterey Bay, California, in 1991 coincided with a bloom of P. australis. Barron et al. (2010) suggested that the increase in Pseudo-nitzschia in their 1990e1991 sample might have been a consequence of that bloom, which would have extended to other regions of the coastline. Fryxell et al. (1997) reviewed the occurrence of Pseudo-nitzschia on the West Coast between 1920 and 1996, noting that it produces domoic acid, which when concentrated by organisms higher in the food chains, can lead to sickness and mortality in sea mammals, seabirds, and humans. Schnetzer et al. (2007) determined the abundances of Pseudo-nitzschia spp. in phytoplankton off the coasts of Los Angeles and Orange counties during the spring and summer of 2003 and 2004. They noted that Pseudo-nitzschia abundances correlated with lower values of salinity such as are found in regions of river plumes and not chlorophyll a concentrations. Schnetzer et al. (2007) related these abundances to concentrations of domoic acid in particulate organic matter and to recorded toxic events for higher organisms. These authors cited laboratory studies

demonstrating that silica and phosphate stress caused increased domoic acid production by cells of Pseudo-nitzschia. The first recorded large-scale toxigenic P. australis bloom in the SBB occurred in June 1998 as part of more widespread blooms and shellfish poisoning along the central California coast (Trainer et al., 2000). Although high numbers (or blooms) of P. australis were reported in plankton studies off the Scripps Pier in La Jolla during the 1930’s, 1967, and 1983, blooms of P. australis associated with toxic domoic acid levels were first reported in 1991 in Monterey Bay (Lange et al., 1994). Sekula-Wood et al. (2011) analyzed a 15-year time series (1993e2008) of sediment trap samples collected from the SBB at 540 m for concentrations and fluxes of Pseudo-nitzschia and domoic acid. They observed an abrupt increase in the frequency and magnitude of Pseudo-nitzschia blooms and toxic domoic acid events after the year 2000 and made comparisons with various environmental indices, including Ventura River discharge, ENSO, PDO, the Pacific Fisheries Environmental Laboratory’s upwelling index, and the North Pacific Gyre Oscillation (NPGO). The NPGO is a climate pattern that emerges as the “2nd dominant mode of sea surface height variability in the Northeast Pacific” and is “significantly correlated with fluctuations of salinity, nutrients and chlorophylla measured in long-term observations in the California Current and Gulf of Alaska” (Di Lorenzo et al., 2008). Sekula-Wood et al. (2011) concluded that the recent increase in Pseudo-nitzschia blooms best correlated with a 1999 shift in the NPGO, which modulates basin scale upwelling and nutrient availability. If such an association were truly related, the evidence would suggest that the recent shift in the NPGO is atypical of natural variability. In contrast, another yet unidentified factor may be important. The recent Pseudo-nitzschia blooms off the California coast occurred during periods of lowered sea surface temperatures and higher salinity that are typical of coastal upwelling events (Trainer et al., 2000; Anderson et al., 2009), but it is unclear whether increased nutrient levels from river runoff have been a factor in the recent increase of the blooms (Schnetzer et al., 2007). Laboratory studies have demonstrated that toxin production in some species of Pseudo-nitzschia may increase under silicic acid or phosphate limitation (Schnetzer et al., 2007; Silver et al., 2010). Mengelt and Prézelin (2005) and others have suggested Pseudo-nitzschia is less susceptible to growth inhibition by Ultraviolet A (320e400 nm) radiation than other planktonic diatoms and therefore can remain in near surface waters for longer periods of time. Whatever the cause, the 253 year-long diatom sediment record suggests that the recent increase of Pseudo-nitzschia blooms has occurred at the expense of Chaetoceros and Rhizosolenia-related species, the natural bloom-forming diatoms in the Santa Barbara Basin. 6. Conclusions Diatoms and silicoflagellate assemblages were studied in two year-increments of varved samples spanning the interval from w1750 through 2007 in Santa Barbara Basin box core SBBC0806. The relative abundance of several key indices are moderately to weakly correlated with Kaplan reconstructed anomaly SST for the 5  5 grid centered at 122.5 W, 32.5 N for the interval from 1900 through 2003, suggesting their utility for proxy SST reconstruction. As each taxon may have different responses to oceanographic conditions, emphasis is placed on the major downcore variations shared between the different indices. When compared with each other for years 1750e1900, the planktonic foraminiferal, diatom, and silicoflagellate SST proxies and % opal data suggest intervals of cooling/increased biosilica productivity coincide reasonably well with intervals of negative PDO conditions according to the tree-ring derived indices of

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Biondi et al. (2001) and MacDonald and Case (2005), most convincingly at w1752e58 but also at w1786e1788, 1806e1808, 1824e1829, 1860e1862, 1890e1892. Agreement of warmer/less productive conditions between the proxies is less pronounced and limited to the intervals of w1768e1774 and w1838e1846, both of which correspond with strong positive PDO conditions according to the tree-ring derived index of MacDonald and Case (2005), but with less distinctive PDO conditions according to the index of Biondi et al. (2001). The most clearly shared signal between diatom and silicoflagellate assemblages is that a warming of SBB surface waters occurred after 1940. While Di Lorenzo et al. (2005) and Field et al. (2006b) emphasized a clear warming for the California margin since the mid-1970s, the combined records indicate that warming began decades sooner. In 1999 cooling of surface waters coincident with the onset of a PDO or other regime shift in the North Pacific brought about a return to pre-1940 values of these cool water taxa (T. nitzschioides increased to w31%, D. speculum s.l. increased to w25%). However, this recent regional cooling appears to have been accompanied by profound changes to surface water productivity events in the SBB of a unique nature relative to this w250-year record. P. australis, a diatom associated with domoic acid, a neurotoxin that causes shellfish poisoning and marine mammal deaths, appeared suddenly in the SBB sediment record in 1999 and increased significantly in numbers as a bloom-forming taxon (relatively to Chaetoceros spores) in 2003. Prior to 2003 diatom blooms represented in the SBB sediment record consisted predominantly of Chaetoceros spores and less commonly of Rhizosolenia-related spp. (N. robusta and R. setigera). Fecal pellets dominated by valves of P. australis, however, were abundant in both the 2003 and 2006 samples, coincident with recorded incidents of domoic acid increase and widespread shellfish poisoning in the SBB. Documented Pseudo-nitzschia blooms along the California margin appear to correspond with lowered SST and increased salinity, but it is unclear whether increased nutrients levels from river runoff have been a factor in the recent increase of the blooms. Other researchers have suggested that Pseudo-nitzschia is less susceptible to growth inhibition by Ultraviolet A than other diatom taxa, allowing it to remain in surface waters for longer periods of time ready to respond quickly as blooms under favorable upwelling conditions. Whatever the cause for the post 2002 increase in Pseudo-nitzschia blooms in the SBB, they seem to a consequence of anomalous surface water conditions in the SBB that became apparent after w1940. These changes may reflect a new circulation pattern or the PDO change may be superimposed on the secular warming trend, resulting in unique changes in water column properties. Acknowledgements We thank Scott Starratt for both his very thorough initial and final reviews. This manuscript also benefitted greatly from the comments of two anonymous reviewers for Quaternary International. Appreciation is due to Dr. Sibel Bargu Ates of Louisiana State University for her identification of Pseudo-nitzschia species in SBBC0806 sample that was sent to her. Holly Olson is thanked for processing the samples. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.quaint.2012.07. 002.

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