The phytoplankton bloom response to wind events and upwelled nutrients during the CoOP WEST study

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Deep-Sea Research II 53 (2006) 3023–3048 www.elsevier.com/locate/dsr2

The phytoplankton bloom response to wind events and upwelled nutrients during the CoOP WEST study Frances P. Wilkerson, Adria M. Lassiter, Richard C. Dugdale, Albert Marchi, Victoria E. Hogue Romberg Tiburon Center, San Francisco State University, 3152 Paradise Drive, Tiburon, CA 94920, USA Received 5 November 2004; accepted 13 July 2006 Available online 20 November 2006

Abstract In the coastal waters off northern California, seasonal wind-driven upwelling supplies abundant nutrients to be processed by phytoplankton productivity. As part of the Coastal Ocean Processes: Wind Events and Shelf Transport (CoOP WEST) study, nutrients, CO2, size-fractionated chlorophyll, and phytoplankton community structure were measured in the upwelling region off Bodega Bay, CA, during May–June 2000, 2001 and 2002. The ability of this ecosystem to assimilate nitrate (NO3) and silicic acid/silicate (Si(OH)4) and accumulate particulate material (i.e. phytoplankton) was realized in all 3 years, following short events of upwelling-favorable winds, followed by periods of relaxed winds. This was observed as phytoplankton blooms, dominated by chlorophyll in cells greater than 5 mm in diameter, that reduced the ambient nutrients to zero. These communities were located over the near-shore shelf (o100 m depth) and were dominated by diatoms. An optimal window of 3–7 days of relaxed winds, following an upwelling pulse, was required for chlorophyll accumulation. The large-celled phytoplankton that result are likely important players in coastal new production and carbon cycling. r 2006 Published by Elsevier Ltd. Keywords: Phytoplankton; Diatom; Upwelling; Nutrients; California; Bodega Bay

1. Introduction Although contemporary research has focused on the flux of biogenic elements between the upper and deep ocean or ocean and atmosphere with an emphasis on open-ocean systems (e.g., JGOFS studies, Murray, 1995; Smith, 1999; Smith and Anderson, 2000), it has become apparent that the ocean margins play an important role in global Corresponding author. Tel.: +415 338 3519/435 7142; fax: +415 435 7120. E-mail address: [email protected] (F.P. Wilkerson).

0967-0645/$ - see front matter r 2006 Published by Elsevier Ltd. doi:10.1016/j.dsr2.2006.07.007

ocean flux. A significant proportion of the global production occurs in the coastal ocean (Walsh, 1991; Chavez and Smith, 1995) where the biological pump exports carbon to deep water and lowers the pCO2 in surface waters (Volk and Hoffert, 1985). The pump’s efficiency depends on the fraction of carbon fixation that escapes recycling within the mixed layer (Berger et al., 1988)—i.e. new production (Dugdale and Goering, 1967), which is supported by nutrient influx (e.g., nitrate, NO3 or silicate, Si(OH)4) to the euphotic zone. Wind-driven coastal upwelling can provide the nutrient enrichment for high rates of new production in eastern

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boundary ocean margins (e.g., MacIsaac et al., 1985; Dugdale, 1985; Dugdale and Wilkerson, 1989). The composition and size structure of the phytoplankton assemblage in the coastal upwelling ecosystems are major determinants of the quantity of new production (Hutchings et al., 1995). The larger net and nanoplankton size fractions of the phytoplankton community are more effective than the smaller size classes of the microbial web at using recently upwelled ‘‘new’’ nutrients (Probyn, 1985, 1992; Brink et al., 1995; Varela et al., 1991; Wilkerson et al., 2000). In Monterey Bay, CA, the dominant role larger phytoplankton (45 mm in diameter) play in nutrient depletion and chlorophyll increase was demonstrated by Wilkerson et al. (2000). These phytoplankton were most likely diatoms, as indicated by a 1:1 rato of Si:N uptake (White and Dugdale, 1997; Brzezinski et al., 1997). Diatoms are typically the dominant species when external ‘‘new’’ nitrogen enters the euphotic zone (Malone, 1980; Bode et al., 1997). Upwelling areas are characterized by chain-forming and colonial diatoms that have individual cell diameters of typically 5–30 mm (Estrada and Blasco, 1985; Hutchings et al., 1995). The diatoms have fast division rates (Furnas, 1991) and a favorable respiration to photosynthesis ratio (Harris, 1978). Diatom physiology seems well adapted to exploit periods of increased nutrient availability (Hutchings et al., 1995) as occur in wind-driven upwelling. There is likely to be an optimal frequency of wind events (upwelling, relaxation and stratification) to promote the dominance of large-celled phytoplankton. Legendre and Le Fe`vre (1989) described an optimal environment window for diatoms. During this window, upwelled phytoplankton must be able to ‘‘shift-up’’ physiological rate processes (Kudela and Dugdale, 2000; Hutchings et al., 1995) in response, to maximize nutrient uptake and growth processes. The response of the phytoplankton to upwelling and stratification residence time has been described as a series of increased physiological rates (Bode et al., 1997) occurring along a conveyor (MacIsaac et al., 1985; Wilkerson and Dugdale, 1987; Dugdale et al., 1990), that have been modeled as such (Zimmerman et al., 1987; Botsford et al., 2003; Dugdale et al., 1997). At the beginning of the conveyor, seed stocks of algal cells are upwelled; chlorophyll concentrations are low and concentrations of nutrients are high, with phytoplankton rate

processes minimal (Slawyk et al., 1997). Then, as the water is advected downstream (or offshore), with relaxed wind conditions, the algae respond with elapsed time to the high light and nutrients by turning on nutrient-uptake mechanisms and starting to photosynthesize. Balanced growth is reached when C:N uptake equals Redfield ratios (Kudela et al., 1997); there are now high chlorophyll concentrations and low nutrients that have been drawn down biologically, due to high phytoplankton uptake rates. Further downstream (or later) the larger phytoplankton run out of nutrients and rate processes slow down with a switch to dominance by the microbial loop and smaller phytoplankton that use regenerated nutrients (e.g., NH4) (Wilkerson et al., 2000; Kudela et al., 1997; Painting et al., 1993; Chang et al., 1992, 1995). Zooplankton concentrations and grazing increase at this region (the upwelling frontal area) (e.g., Smith and Whitledge, 1977). Biological particles (both algal cells and feces produced by grazers) likely carry carbon to below the euphotic zone (export production). This cycle from upwelling to nutrient depletion may take about 5–7 days (MacIsaac et al., 1985 in Peru; Dugdale and Wilkerson, 1989 in Point Conception, CA). Modeling and experiments show that regardless of how much nutrient is upwelled during the upwelling phase, if a suitable period of relaxation follows, all is taken up within 72 h ¼ 3 days (Zimmerman et al., 1987; Dugdale et al., 1990). This sets the minimum relaxation period for full utilization of upwelled nutrients: a conceptual framework for understanding the phytoplankton response in upwelling regions. These temporal changes during an upwelling event are translated into spatial changes as newly upwelled water is advected offshore, such that near-shore physical conditions are conducive to diatom growth (Hutchings et al., 1995). The greatest bloom development and spatial extent occur after upwelling ceases and there follows an optimal period of water-column stability due to relaxation of the winds. Although models show this period of phytoplankton response to be on the order of 3 days, and field data obtained using drogue studies, to be 5–7 days, it is unclear what the optimal period is in upwelling ecosystems with different upwelling conditions. The Coastal Ocean Processes: Wind Events and Shelf Transport (CoOP WEST) program provided an interdisciplinary field experiment at an ideal eastern boundary upwelling location off Bodega Bay, CA, to measure both the temporal and spatial

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relaxed winds, (2) that surface nutrients would be depleted as a result, and (3) the chlorophyll biomass would be dominated by large cell-sized phytoplankton, most likely diatoms.

development of phytoplankton response to winddriven upwelling. The site is situated in a region of maximal northwesterly upwelling-favorable winds (Parrish et al., 1981). During the upwelling season, the duration of upwelling-favorable winds may be as short an event scale as 1 day (of similar duration to phytoplankton generation times; Estrada and Blasco, 1985) but can be as long as weeks at a time (Dorman and Winant, 1995). These periods are interspersed with relaxation events of decreased or no winds (Wing et al., 1995a, b) and at times a reversal in the winds, resulting in downwelling. The importance of these relaxation events in dispersal and settlement of benthic invertebrates in this region was described (Wing et al., 1995a, b), although their role in phytoplankton productivity has not been studied previously. The goal of our study was to investigate how phytoplankton adapt to optimal conditions on wind event time scales, by measuring their response to increased nutrient availability during upwelling-favorable conditions at the CoOP WEST site during the summer months of 2000–2002. Our hypotheses, based upon modeling and fieldwork in other upwelling areas, were that; (1) phytoplankton would increase in biomass following an upwelling nutrient pulse only if there was a subsequent 3–7-day period of reversed or

2. Materials and methods 2.1. General The study site (Fig. 1) was located in northern California, just off Bodega Bay, California between Points Reyes and Arena. Data described here were collected aboard the R.V. Point Sur during 4-week summer cruises in 2000 (CoOP WEST 2000, 1–30 June), 2001 (CoOP WEST 2001, 15 May–15 June), 2002 (CoOP WEST 2002, 29 May–28 June). Nearsurface water (5 m, or depth equivalent to the 50% light penetration depth), the data reported here, were collected at fixed stations making up a largescale survey grid of three offshore transect lines (A, D and F, south to north) that included the original CODE (Coastal Ocean Dynamics Experiment) (Kosro and Huyer, 1986) line C (equivalent to WEST line F). A time series station, station D2 was sampled at least daily, and sometimes more often. D2 was located at the location of the CoOP WEST D090 central mooring location, 381 28.30 N, 1231

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16.00 W (Dever et al., 2006; Largier et al., 2006) on the shelf (Fig. 1). Wind speed data were obtained from the National Data Buoy Center (NDBC) Buoy 46013 (located between D2 and D3) at 381 13.370 N, 1231 19.480 W. Wind speeds of o 5 m s1 were categorized as upwelling winds and those 45 m s1 as relaxed or reversed winds. Seawater was collected with acid-cleaned 10-L PVC Nisken bottles equipped with Teflon-coated springs and fittings and silicone tubing mounted on an instrumented rosette sampler. Hydrographic data (temperature and salinity) were recorded from a Seabird SBE-19 Plus CTD. Depths in the euphotic zone for sampling were selected (depths corresponding to 100%, 50%, 30%, 15%, 5% and 1% of surface irradiance) using either a vertical profile of photosynthetically active radiation (PAR) using a submersible PAR sensor and/or a Secchi disk. Data from either the depth where 50% of surface irradiance occured or 5-m depth are reported here. 2.2. Nutrients, chlorophyll-a, phytoplankton enumeration Water samples for nitrate and silicate analyses were collected in 20-ml polypropylene bottles, held in the refrigerator until analysis (within 12–24 h) with a Bran and Luebbe AutoAnalyzer II (NO3 according to Whitledge et al. (1981), Si(OH)4 using Bran and Luebbe Method G-177-96 (Bran Luebbe, 1999)). Some samples were frozen for up to a month. These were subsequently thawed 24 h prior to analysis to avoid polymerization effects on Si(OH)4 measurements (MacDonald et al., 1986). For ammonium (NH4) analyses, water was sampled into 60-ml polycarbonate centrifuge tubes and treated with phenol reagent (Solorzano, 1969) on shipboard and held at 4 1C until analysis using a Hewlett Packard Model 8452A diode array spectrophotometer equipped with a 10-cm cuvette. pCO2 was measured with a nondispersive infrared analyzer (LI-COR 6252) equipped with a shower-head equilibrator (Friederich et al., 1995). Chlorophyll-a concentrations were determined by in vitro fluorometry using the extraction protocol of Arar and Collins (1992) with a Turner Designs Model 10 fluorometer, calibrated with commercial chlorophyll-a (Turner Designs), and chlorophyll-a concentrations calculated according to Holm-Hansen et al. (1965). Water samples were collected in 280-ml polycarbonate bottles. These were then filtered onto either a Whatman 25-mm glass microfiber filter

(GF/F, 0.7 mm nominal pore-size) to provide ‘‘total chlorophyll’’, or a 25-mm 5-mm pore-sized polycarbonate filter to estimate chlorophyll contribution by cells 45 mm in diameter, ‘‘fractionated chlorophyll’’. Phytoplankton identification and enumeration was carried out using light microscopy on water sampled into 250-ml amber glass bottles and preserved with 2 ml of Lugol’s solution. Subsamples (25 or 50 ml volume depending on chlorophyll concentration) were concentrated by the Utermo¨hl (1958) technique and counted at 400  using a Nikon Type 180 phase contrast inverted microscope. Cells were identified to species when possible (see Lassiter, 2003; Lassiter et al., 2006) and then divided into three groups: diatoms, flagellates and the small o2-mm cells (not reported here).

3. Results After describing the wind events for each cruise (2000–2002) the spatial and temporal changes and patterns in phytoplankton response to these wind events are reported. First the spatial patterns of temperature, nutrients and phytoplankton measured during the large-scale spatial surveys are described. Then the results will focus in more detail on the time scale of response of the phytoplankton at the shelf location D2.

3.1. 2000 cruise (1– 30 June 2000) 3.1.1. Wind data at NODC 46013 The wind data from the NODC Buoy 46013 near D3 (Fig. 2) show that winds had been blowing from the northwest at 5–10 m s1 for at least 14 consecutive days, with stronger consistent upwelling winds (up to 15 m s1) for 4 days immediately before the shipboard field sampling began. Then there was a period (1–8 June) of weak equatorward winds with three brief and small relaxation events with winds of o5 m s1. Then the upwelling-favorable winds returned from the northwest (7–8 m s1) and continued to increase to 13 m s1 by 14 June. Another relaxation event began on 14 June, lasting until 22 June, followed by 2 days (22–24 June) of upwelling-favorable winds that blew at a maximum of 12 m s1. From this time to the end of the cruise, wind speed, and direction were variable, and the northwesterly upwelling winds were weak and relaxed.

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Fig. 2. Wind data from NOAA Buoy 46013 from 17 May to 3 July 2000. Yellow line is unfiltered wind speed, blue line is filtered wind speed. Lower red lines show periods of northwesterly upwelling-strength winds, upper red lines show reversal or relaxed periods. Aqua lines indicate wind speeds of zero and 45 m s1 used to define when upwelling winds occur.

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3.1.2. Large-scale survey (1– 3 June 2000) This survey was carried out between the end of the upwelling-favorable winds and the relaxation period of 2 June and reflected the upwelling conditions with a cold tongue stretching from Point Arena (F1) to D3 with cool saline water (8.7–9.8 1C, 33.8–33.98 psu, Fig. 3A and B) and following parallel to the coast, along the shelf, with warmer less saline water offshore (11–14 1C, 33–33.3 psu). Distributions of nutrients and pCO2 all showed similar patterns to temperature (Fig. 3C–E). The cold-water plume from F1 showed high, recently upwelled values (NO3 ¼ 32 mM, Si(OH)4 ¼ 46 mM) and CO2 above atmospheric (965 matm). There was another small cold high-salinity upwelling area at Point Reyes (A1), also accompanied by high levels of nutrients and pCO2. NH4 was near or at detection levels (Fig. 3F), except at A1 where it reached 0.6 mM. The chlorophyll concentrations were mostly low (o2 mg l1) except close to the coast, off Bodega and Point Reyes (D1 and A2), where there were 11 and 15 mg l1 total chlorophyll and 6.9 and 8.3 mg l1 for the 45-mm fraction, respectively (Fig. 4A and B). The community close to the coast (D2, D1, A4, A2, A1) was mostly made up of diatoms (Fig. 4C and D), contributing almost 100% to the total phytoplankton cell count. The rest of the area had low levels of both diatoms and flagellate cells, with flagellates dominating in the warmer offshore waters (Fig. 4E). 3.1.3. Time series data at D2 (1– 30 June 2000) Data from shelf station D2 shows how upwelled nutrients were drawn down and resulted in increased phytoplankton comprised mostly of diatoms (Fig. 5). Sea-surface temperature at the start (3 June) was 9.8 1C, then warmed to 11 1C during the slight relaxation event (5–6 June), and cooled again to 8.7 1C by 9 June with the next major wind event (Fig. 5A). Following the wind event (14 June), temperatures, increased to a maximum of 14.5 1C by 29 June (Fig. 5A) due to the 15–22 June relaxation event. The colder water had higher salinities and nutrient concentrations (Fig. 5A and B), with maximal concentrations of NO3 (31 mM) and Si(OH)4 (47.3 mM) on 3 June. Four days later nutrient concentrations had dropped to undetectable levels. Then, with the increase in upwelling strength winds (Fig. 2), they increased from 8 to 13 June, reaching 31.2 mM NO3 and 39.0 mM Si(OH)4. For the remainder of the cruise, with warmer and

less-saline water, nutrient concentrations were low (o10 mM; Fig. 5A and B). NH4 concentrations at D2 were much lower than those of NO3 and Si(OH)4, ranging from near-detection levels to 0.4 mM except for peaks of 1 mM on 9, 24 and 29 June (Fig. 5B). The cold, saline nutrient-replete water had low phytoplankton biomass; total chlorophyll on 3 June was 1 mg l1 with 0.35  106 phytoplankton cells l1 (Fig. 5D). By the next day, as nutrient concentrations started to decrease chlorophyll and phytoplankton counts increased (by 4 June there was 24.6 mg l1 and almost 20  106 phytoplankton cells l1) with diatoms contributing significantly (19  106 cells l1). This increase in biomass continued, reaching a maximum of 32.1 mg l1 on 7 June when nutrients were at zero. During this day chlorophyll ranged from 11.5 mg l1 at 01:00 to 32.14 mg l1 at 15:30, demonstrating the increase in chlorophyll accumulation as the cells converted the NO3 taken up into chlorophyll biomass. The fractionated chlorophyll data showed larger cells to dominate (485%; Fig. 5C). Unfortunately there was no phytoplankton sample taken to match the maximum chlorophyll data point (CTD 55), but a sample taken earlier that day (CTD 53) showed diatoms to make up 98% of the total phytoplankton cells counted (Fig. 5D). Chlorophyll and phytoplankton cell number decreased over the next few days to 2.5 mg l1 and 1.7  106 cells l1 by 10 June. With the second pulse of nutrients mid-June, relaxation of the winds, the nutrients declined (Fig. 5B) and a small increase in phytoplankton cells occurred, again dominated by diatoms (20 June). After this, with low ambient nutrient concentrations, flagellate numbers continued to increase, until they made up almost 100% of the cells in the community by 29 June. To illustrate more quantitatively the relationships between nutrients and chlorophyll, Si(OH)4 versus NO3 (surface D2 data), regressions show almost a 1:1 relationship (Fig. 6A and B) with a slight Si(OH)4 intercept (Si(OH)4 ¼ 1.13  NO3+1.7, n ¼ 27, r2 ¼ 0:93), indicating that NO3 was depleted first during the time series. The chlorophyll versus NO3 plot for the same data set shows low chlorophyll at high NO3 concentrations (upwelled water) and high levels as the NO3 is depleted and concentrations reduced. The regression is weak due the large range in chlorophyll data at zero NO3 concentrations (data collected on 7 June)—the result of sampling water in which phytoplankton

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Fig. 3. Large-scale survey (1–3 June 2000) showing distributions of near-surface (5 m depth) (A) temperature, 1C, (B) salinity, psu, (C) nitrate, mM, (D) silicate, mM, (E) pCO2, matm, (F) ammonium, mM.

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had depleted NO3 but had not yet converted it to biomass. 3.2. 2001 cruise (15 May– 15 June 2001) 3.2.1. Wind data at NODC 46013 Upwelling-favorable winds began from the northwest on 16 May reaching 15 ms1 by 18 May (Fig. 7). Then from 19 to 24 May there was a relaxation event as winds became southeasterly. By 24 May, the upwelling northwestly winds returned with an intensity of 11.5 m s1 and lasted for the remainder of the cruise, except for a short 1 day relaxation event from 31 May to 1 June.

3.2.2. Large-scale survey (19– 21 May 2001) This survey was conducted during the end of the first upwelling event of the 2001 cruise. Only lines D and F were sampled with one offshore station A8 from the southern part of the area (Fig. 1). As observed in 2000, accompanying the northwesterly winds was a cold saline upwelling tongue (9.5–10 1C, 33.8–34 psu) off Point Arena at F1 that extended along shelf to the D-line and spread out to D6 (Fig. 8A and B), with a similar pattern of nutrients and pCO2 (Fig. 8C–E). Maximal values occurred at F1; 28.5 mM NO3, 36.5 mM Si(OH)4) and 900 matm pCO2 (Fig. 8C–E). NH4 concentrations were higher than in 2000 with a maximum of 2 mM close to shore

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Silicate (µM)

3032 50

the population (making up 70–80% of the population, Fig. 9E).

40

3.2.3. Time series data at D2 (15 May– 5 June 2001) The time series shows the cold, saline, upwelled water that accompanied the northwesterly winds throughout most of the cruise, with surface temperature of 10.5 1C (salinity of 33.94 psu) on 19 May cooling to 9 1C (34.03 psu) by 13 June 2001 (Fig. 10A). A small relaxation event (20–24 May) was evident as warmer and less saline water at D2. Nutrient concentrations started high (NO3 of 22.7 mM, Si(OH)4 of 27 mM), and decreased rapidly during the relaxation event to near-detection levels by 25 May. Then, with the strong northwesterly winds and cool surface temperatures, nutrient concentrations remained high for the cruise, with maximal values of 31.51 mM NO3 and 42.8 mM Si(OH)4 in early June (Fig. 10B). During the relaxation event (19–24 May) NH4 concentrations paralleled the changes in salinity and nutrients, decreasing from 1.9 to 0.4 mM. Concentrations then increased to a maximum of 2.5 mM on 30 May and then gradually dropped to below 0.16 mM by 8 June. As in 2000, when the winds relaxed, nutrients decreased and chlorophyll increased (Fig. 10C), although the concentration reached was not as high as in 2000. Phytoplankton biomass started low on 19 May (0.54 mg l1chlorophyll and 0.88  106 phytoplankton cells l1 (Fig. 10C and D)) but by 21 May had increased to 1.9 mg l1 and 0.99  106 cells l1 (62% diatoms), with the relaxation in winds. By 23 May, chlorophyll was 4.6 mg-at l1 and cell numbers were 8.1  106 cells l1, with diatoms making up 75% of the sample (Fig. 10D). The peak was measured on 25 May with chlorophyll of 14.5 mg l1 (Fig. 10C) and high phytoplankton numbers (8.3  106 cells l1) still dominated by diatoms (78%). These were mostly Chaetoceros species (see Lassiter et al., 2006). Then, as strong upwelling-favorable winds returned, chlorophyll and cell numbers decreased and the ratio of diatoms to other phytoplankton cells began to shift, and flagellates and smaller cells increasingly made up the bulk of the population. By 8 June, chlorophyll was 2 mg l1, dominated by the o2-mm picoplankton cells (not shown) and flagellates (Fig. 10D) and few diatoms (only 3% of the total phytoplankton). Property–property plots of this surface dataset (Fig. 11A, B) show the same, almost 1:1 relationship as in 2000 for Si(OH)4 versus NO3, with a NO3 intercept (Si(OH)4 ¼ 1.48  NO35.23, n ¼ 17, r2 ¼ 0:99) indicating that Si(OH)4 was likely to be

30

20

10 Y = 1.13 * X + 1.71 n =27, r2 = 0.93 0 0

10

20

30

40

Nitrate (µM)

Chlorophyll (µg l-1)

30

20 Y =-0.43 * X +15.17 n = 23, r2 =0.36

10

0 0

10

20

30

40

Nitrate (µM)

Fig. 6. Regressions of (A) silicate, mM versus nitrate, mM and (B) total chlorophyll, mg l1 versus nitrate, mM, surface data from D2 2000 time series.

at D1/D2 (Fig. 8E). Surface chlorophyll values (both total and the45-mm fraction) were low, mostly o2 mg l1 except at D1 and D3 with almost 4 mg l1 (Fig. 9A and B) that had 2.3  106 phytoplankton cells l1, made up mostly (78%) by diatom cells (Fig. 9C and D). There was no area of higher chlorophyll along the coast as in 2000. Even so, the contribution by larger cells to the chlorophyll was relatively high close to shore (460%; Fig. 9B). Offshore and along the F line, where chlorophyll was low, flagellates dominated

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Buoy 13: May 2001 V along 320 10 5

m/s

0 -5 -10 -15 -20 1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16 CRUISE

MAY

STARTS Events: bottom red line = upwelling. top red line = relaxation

10 5

m/s

0 -5 -10 -15 -20 17

18

19

20

21

22

23

24

25

26

27

28

29

30

31

1 JUNE

day Buoy 13: June 2001 V along 320 10 5

m/s

0 -5 -10 -15 -20 1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16 CRUISE ENDS

JUNE

Fig. 7. Wind data from NOAA Buoy 46013 from 1 May to 17 June 2001. Colored lines as in Fig. 2.

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3034 38.7

38.7

(A)

(B)

38.5

38.5

38.3

38.3

38.1

38.1

37.9

37.9

37.7 -124

-123.8

-123.6

-123.4

-123.2

-123

-122.8

38.7

37.7 -124 38.7

(C) 38.5

38.5

38.3

38.3

38.1

38.1

37.9

37.9

37.7 -124 38.7

-123.8

-123.6

-123.4

-123.2

-123

-122.8

-123.6

-123.4

-123.2

-123

-122.8

-123.8

-123.6

-123.4

-123.2

-123

-122.8

-123.8

-123.6

-123.4

-123.2

-123

-122.8

(D)

37.7 -124 38.7

(E)

(F)

38.5

38.5

38.3

38.3

38.1

38.1

37.9

37.9

37.7 -124

-123.8

-123.8

-123.6

-123.4

-123.2

-123

-122.8

37.7 -124

Fig. 8. Large-scale survey (19–21May 2001) showing distributions of near-surface (5 m depth) (A) temperature, 1C, (B) salinity, psu, (C) nitrate, mM, (D) silicate, mM, (E) pCO2, matm, (F) ammonium, mM.

ARTICLE IN PRESS F.P. Wilkerson et al. / Deep-Sea Research II 53 (2006) 3023–3048 38.7

3035

38.7

(A)

(B)

Total chl, ug/L

38.5

38.5

38.3

38.3

38.1

38.1

37.9

37.9

37.7 -124

-123.8

-123.6

38.7

-123.4

-123.2

-123

-122.8

38.5

38.3

38.3

38.1

38.1

37.9

37.9

-123.8

-123.6

-123.4

-123.2

-123

-123.6

-123.4

-122.8

37.7 -124

38.7

-123.2

-123

-122.8

#diatom, x106/L

(D)

38.5

37.7 -124

-123.8

38.7

phytoplankton #, x106/L

(C)

37.7 -124

>5um chl, ug/L

-123.8

-123.6

-123.4

-123.2

-123

-122.8

flagellate #, x106/L

(E) 38.5

38.3

38.1

37.9

37.7 -124

-123.8

-123.6

-123.4

-123.2

-123

-122.8

Fig. 9. Large-scale survey (19–21 May 2001) showing distributions of near-surface (5 m depth) (A) total chlorophyll, mg l1, (B) fractionated, chlorophyll from cells 45 mm, mg l1, (C) total phytoplankton cells,  106 cells l1, (D) diatom cells,  106 cells l1, (E) flagellate cells,  106 cells l1.

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3036

(A) 12

(B) 50

34.04 Temperature Salinity

5

Nitrate Silicate Ammonium

40

4

30

3

20

2

33.88

10

1

33.84

0

34

33.92

Ammonium (µM)

10

Nitrate or Silicate (µM)

33.96

Salinity (psu)

Temperature (degC)

11

9

8 5/19/01 5/24/01 5/29/01

(C) 20

6/3/01

6/8/01

6/13/01

(D) 12

Total Chl Chlor > 5um

Phytoplankton (x106 cells l-1)

Chlorophyll (µgl-1)

15

10

5

0 5/19/01 5/24/01 5/29/01

6/3/01

6/8/01

6/13/01

Total phyto cells Diatoms Flagellates

9

6

3

0

0 5/19/01 5/24/01 5/29/01

6/3/01

6/8/01

6/13/01

5/19/01 5/24/01 5/29/01 6/3/01

6/8/01 6/13/01

Fig. 10. Time series data collected at D2 (19 May–13 June, 2001). Near surface (5 m) measurements of (A) temperature, 1C and salinity, psu, (B) nitrate, silicate, ammonium, mM, (C) total chlorophyll, mg l1 and fractionated chlorophyll from cells45 mm, mg l1, (D) total phytoplankton cells,  106 cells l1, including diatom cells,  106 cells l1, flagellate cells,  106 cells l1.

depleted first as chlorophyll accumulated. Chlorophyll versus NO3 had a similar relationship (Fig. 11B) as in the 2000 D2 time series with higher chlorophyll and lower NO3 concentrations and a slightly lower intercept (Chl ¼ 0.35  NO3+ 11.15, n ¼ 17, r2 ¼ 0:77). 3.3. 2002 cruise (31 May– 26 June 2002) 3.3.1. Wind data at NODC 46013 Upwelling favorable winds from the northwest blew almost continuously at or above 10 m s1 before and throughout the cruise (Fig. 12). There was one relaxation event that began on 11 June, when the direction shifted briefly to blow from the

southeast, and wind speed averaged 2.5 m s1, with a brief downwelling component (Fig. 12). 3.3.2. Large-scale survey (15– 17 June 2002) Unlike the other years, the surface survey described here was not sampled at the start of the cruise, as the entire area could not be sampled by ship at that time due to the intensity of the winds. The complete area was sampled mid cruise, 15–17 June after the short relaxation event but during upwelling conditions (Fig. 12). As in 2000 and 2001, a cold saline plume extended from F1 alongshore. However, values were colder and saltier than in 2000 and 2001; 8.4 1C and 34.06 psu at F1 (Fig. 13A and B). Nutrients were high (420 mM),

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cruise. This ‘‘peak’’ in chlorophyll was made up mostly of larger cells (65–83%) (Fig. 14B); that at D4 were mostly diatoms (3.6  106 diatom cells l1 making up 90% of the total phytoplankton cells) (Fig. 14C and D). Offshore, where chlorophyll values were low, phytoplankton cell numbers were relatively high (e.g., 1.3  106 cells l1) but this was almost entirely small flagellates, e.g., 96% at D6 and D7 (Fig. 14E).

50

Silicate (µM)

40

30

20

10 Y = 1.48* X - 5.23 n = 17, r2 = 0.99 0 0

10

20

30

40

Nitrate (µM) 16

12 Chlorophyll (µg l-1)

3037

Y = -0.35* X + 11.15 n = 17, r2 = 0.77 8

4

0 0

10

20

30

40

Nitrate (µM)

Fig. 11. Regressions of (a) silicate, mM versus nitrate, mM and (b) Total chlorophyll, mg l1 versus nitrate, mM, surface data from D2 2001 time series.

with elevated values in the cold swath (34 mM NO3 and 47 mM Si(OH)4 at F1) (Fig. 13C and D). Unfortunately pCO2 was not measured from F1 to F5, but values throughout the region were high, and were similar in pattern to the nutrients (Fig. 13E). As in 2000, NH4 was low or at detection limits except near Point Reyes, with 1.6 mM at A2 (Fig. 13F). Chlorophyll values were lower along the coast compared to other years, but concentrations of around 7 mg l1 were reached at D3–D4 (Fig. 14A), as a result of the short relaxation period that interrupted the strong upwelling winds in this

3.3.3. Time series data from D2 (31 May– 26 June 2002) Accompanying the consistent northwesterly winds, sea-surface temperatures were cold and saline throughout the cruise (mostly around 8.5 1C, 34 psu), and were never above 11 1C (Fig. 15A), compared to 2000 and 2001, when temperatures 411 1C were measured. At the start of the cruise and on 16 June following the short relaxation event (11–14 June), slightly warmer and less saline water occurred. Surface NO3 and Si(OH)4 concentrations tracked the salinity starting relatively low (8.7 mM NO3 and 11 mM Si(OH)4) (Fig. 15B), then increasing with the upwelling winds and decreasing temperatures (Fig. 15A) and reaching 34.2 and 48.8 mM by 9 June. Then, accompanying the short relaxation event, concentrations decreased to 23.8 mM NO3 and 32.3 mM Si(OH)4 by 16 June (Fig. 15B). With the onset of upwelling winds, they returned to high values (30.0 mM NO3 and 43 mM Si(OH)4) for the rest of the cruise (Fig. 15B). NH4 concentrations at D2 were o1.2 mM except a peak value of 2.6 mM on 5 June (Fig. 15B). Surface chlorophyll concentration and algal number started relatively high (12.2 mg l1 (Fig. 15C) and 5.48  106 cells l1 (Fig. 15D)) and was likely a consequence of the brief relaxation event on 26–30 May that occurred just prior to the cruise, This chlorophyll was composed mostly of large cells (78%, Fig. 15C), that were diatoms (73% of total phytoplankton, Fig. 15D). This diatom community, as in 2000 and 2001, was dominated by various Chaetoceros species (Lassiter et al., 2006). By the next time D2 was sampled, after the winds had increased again, on 3 June, the chlorophyll had dropped to 0.2 mg l1 (Fig. 15C), with 0.37  106 phytoplankton cells l1 composed almost entirely (90%) of o2 mm cells and flagellates (Fig. 15C and D). Chlorophyll and phytoplankton numbers remained low until just after the short relaxation event. By 16 June, nutrients had decreased and both chlorophyll and cell number increased to 6.5 mg l1,

ARTICLE IN PRESS 3038

F.P. Wilkerson et al. / Deep-Sea Research II 53 (2006) 3023–3048

Fig. 12. Wind data from NOAA Buoy 46013 from 17 May to 3 July 2002. Colored lines as in Fig. 2.

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38.7

Temperature, degC

(A)

38.5

38.3

38.3

38.1

38.1

37.9

37.9

37.7 -124 38.7

-123.8

-123.6

-123.4

-123.2

-123

-122.8

37.7 -124

-123.6

-123.4

-123.2

38.5

38.3

38.3

38.1

38.1

37.9

37.9

-123.8

-123.6

38.7

-123.4

-123.2

-123

-122.8

38.5

38.3

38.3

38.1

38.1

37.9

37.9

-123.6

-123.4

-123.2

-123.8

-123.6

-123.4

-123.2

-123

-122.8

Ammonium, uM

(F)

38.5

-123.8

-122.8

38.7

pCO2, uatm

(E)

37.7 -124

-123 Silicate, uM

(D)

Nitrate, uM

38.5

37.7 -124

-123.8

38.7

(C)

37.7 -124

Salinty, psu

(B)

38.5

3039

-123

-122.8

37.7 -124

-123.8

0 -123.6

-123.4

-123.2

-123

-122.8

Fig. 13. Large-scale survey (15–17 June 2002) showing distributions of near-surface (5 m depth) of (A) temperature, 1C, (B) salinity, psu, (C) nitrate, mM, (D) silicate, mM, (E) pCO2, matm, (F) ammonium, mM.

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3040 38.7

38.7

Total chl, ug/L

(A) 38.5

38.5

38.3

38.3

38.1

38.1

37.9

37.9

37.7 -124

-123.8

-123.6

38.7

-123.4

-123.2

-123

-122.8

37.7 -124

38.5

38.3

38.3

38.1

38.1

37.9

37.9

-123.8

-123.6

-123.4

-123.2

-123

-123.6

-123.4

-122.8

37.7 -124

-123.2

-123

-122.8

#diatom, x106/L

(D)

38.5

37.7 -124

-123.8

38.7

phytoplankton #, x106/L

(C)

> 5um chl, ug/L

(B)

-123.8

-123.6

-123.4

-123.2

-123

-122.8

38.7 #flagellates, x106/L

(E) 38.5

38.3

38.1

37.9

37.7 -124

-123.8

-123.6

-123.4

-123.2

-123

-122.8

Fig. 14. Large-scale survey (15–17 June 2002) showing distributions of near-surface (5 m depth) (A) total chlorophyll, mg l1, (B) fractionated chlorophyll from cells45 mm, mg l1, (C) total phytoplankton cells,  106 cells l1, (D) diatom cells,  106 cells l1, (E) flagellate cells,  106 cells l1.

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(A) 14

3041

34.08

(B) 50

5

34.04

40

4

30

3

10 33.96

20 Nitrate Silicate Ammonium

8

6

(C)

10

33.88

0

6/8/02 6/13/02 6/18/02 6/23/02 6/28/02

15

(D)

Chlorophyll (µgl-1)

12 Total Chl Chl > 5 um 9

6

3

1

0 6/8/02 6/13/02 6/18/02 6/23/02 6/28/02

6 Total phytocells Diatoms Flagellates 4

2

0

0 5/29/02 6/3/02

5/29/02 6/3/02

Phytoplankton (x 106 cells l-1)

5/29/02 6/3/02

33.92

2

Ammonium (µM)

34

Nitrate or Silicate (µM)

Temperature Salinity

Salinity (psu)

Temperature (degC)

12

6/8/02 6/13/02 6/18/02 6/23/02 6/28/02

5/29/02 6/3/02 6/8/02 6/13/02 6/18/02 6/23/02 6/28/02

Fig. 15. Time series data collected at D2 (30 May–25 June 2002). Near surface (5 m) measurements of (A) temperature, 1C and salinity, psu, (B) nitrate, silicate, ammonium, mM, (C) total chlorophyll, mg l1 and fractionated chlorophyll from cells 45 mm, mg l1, (D) total phytoplankton cells,  106 cells l1, including diatom cells,  106 cells l1, flagellate cells,  106 cells l1.

and 2.3  106 cells l1, with diatoms making up 75% of the sample (Fig. 15C and D). For the rest of the time-series, characterized by upwelling winds, chlorophyll concentrations and phytoplankton cell counts were low (1.2–3.3 mg l1, Fig. 15C and 0.62–1.11(106 cells l1, Fig. 15D). Si(OH)4 versus NO3 regressions resembled those from D2 in 2001 with a NO3 intercept (Si(OH)4 ¼ 1.44  NO31.7, n ¼ 12, r2 ¼ 0:99), although the data did not include as low values of NO3 as in 2001. Since most of this cruise had strong upwelling-favorable winds and few periods of relaxation, a plot of chlorophyll versus NO3 showed dominance by upwelled water, high in NO3 and low in chlorophyll. The regression slope (Chl ¼

0.47  NO3+16.4, n ¼ 12, r2 ¼ 0:92) was similar to the slopes measured in 2000 and 2001 (Fig. 16A and B; Table 1). 4. Discussion 4.1. Overview These data are the first nutrient and phytoplankton data to be collected at this northern California coastal upwelling ecosystem on this scale of time and space, and covering upwelling seasons over 3 years. They show the WEST site to be an eastern boundary system with predictable but variable upwelling that creates a highly productive region,

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3042 50 Y = 1.44 * X - 1.72 n = 12, r2 = 0.99

Silicate (µM)

40

30

20

10

0 0

10

20

30

40

Nitrate (µM) 16

response at the WEST site appears to be within the predicted 3–7 day window from other upwelling studies (MacIsaac et al., 1985; Dugdale and Wilkerson, 1989). Surface temperature, salinity, pCO2 and nutrient data collected during the summers of 2000–2002 indicate the upwelling center to be north of Bodega Bay, near Point Arena. In all three study periods, upwelling favorable winds from the north west resulted in a tongue of cold NO3 and Si(OH)4-rich water in May–June. Nutrients were then drawn down to near-detection levels in 2000 and 2001 (Figs. 6, 11 and 16) leading to phytoplankton blooms. NO3 and Si(OH)4 depletion tracked each other, with Si(OH)4 versus NO3 regressions showing almost 1:1 slopes (Table 1), indicative of Si(OH)4requiring diatoms. The size-fractionated chlorophyll data support this, with larger cells contributing significantly to the total chlorophyll concentrations when chlorophyll values were high. 4.2. Diatom success in upwelling

Chlorophyll (µg l-1)

12

8

4 Y = -0.47 * X + 16.42 n = 12, r2 = 0.92 0 0

10

20

30

40

Nitrate (µM)

Fig. 16. Regressions of (A) silicate, mM versus nitrate, mM and (B) total chlorophyll, mg l1 versus nitrate, mM, surface data from D2 2002 time series.

with surface chlorophyll concentrations reaching 32 mg l1 in this study (in 2000). In addition to the upwelling-favorable winds from the northwest providing nutrients to feed this new production cycle in these regions, an optimal window of relaxed or reduced winds for phytoplankton blooms is required (Hutchings et al., 1995). This wind relaxation ensures that the phytoplankton are kept in the euphotic zone, enabling biological nutrient drawdown and chlorophyll accumulation to occur. This window of non-upwelling winds with a chlorophyll

The larger phytoplankton cells dominating in early to mid phases of upwelling were primarily diatoms (Lassiter et al., 2006; Lassiter, 2003) as has been reported in other upwelling areas (Estrada and Blasco, 1985; Chavez et al., 1991). These cells accumulated downstream from the upwelling center, resulting in elevated chlorophyll along the coast, on the shelf in a similar manner to that described in other upwelling areas (e.g. Chang et al., 1995). The smaller flagellates dominated in late phases of upwelling (Figs. 5, 10 and 15) and were observed typically offshore as described in other upwelling regions (Fernandez and Bode, 1994; Botas et al., 1990). The diatom communities appear to do well in cold nutrient-rich upwelled water. They are capable of decreasing upwelled NO3 and Si(OH)4 concentrations from 30 and 40 mM to near detection levels in a matter of days with biomass accumulation to match this. Stolte et al. (1994) describe how larger phytoplankton cells can only become dominant when NO3 is the major nitrogen source available and NH4 is typically low or at detection levels, as in coastal upwelling ecosystems. Lomas and Glibert (1999a, 2000) describe how diatoms in colder water have higher NO3 uptake and storage capacity, and lower optimal temperatures for nitrate reduction enzymes than flagellates (Lomas and Glibert, 1999b). Diatoms have large vacuoles (Antia et al., 1963) capable of storing large amounts of NO3 that

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3043

Table 1 Regressions of property–property plots from the D2 time series surface data Property–property

D2 time series

Regression equation

r2

n

Si(OH)4 vs. NO3

WEST 2000 WEST 2001 WEST 2002

Si(OH)4 ¼ 1.13  NO3+1.71 Si(OH)4 ¼ 1.48  NO35.23 Si(OH)4 ¼ 1.44  NO31.72

0.93 0.99 0.99

27 17 12

Chlorophyll vs. NO3

WEST 2000 WEST 2001 WEST 2002

Chl ¼ 0.43  NO3+15.17 Chl ¼ 0.35  NO3+11.15 Chl ¼ 0.47  NO3+16.42

0.36 0.77 0.92

23 17 12

Table 2 Events (upwelling and relaxation pairs) observed during CoOP WEST: the duration of upwelling and the nitrate measured at D2 following each upwelling and the duration of relaxation and chlorophyll measured at D2 following relaxation. Year cruise dates

Event no.

Period of upwelling, d

Period of relaxation d

NO3 at end of upwelling, mM

Chl at end of relaxation, mg l1

2000 1–30 June

1

14 17–31 May 5 9–14 June 2 22–24 June

7 1–8 June 8 14–22 June 6 25–31 June

31.0 (1 June) 31.2 (13 June) 1.3 (20 June)

19.3 (8 June) 4.6 (20 June) 5.4 (29 June)

3 16–19 May 6 24–30 May 413

5 19–24 May 1 31 May–1 June

22.7 (19 May) 29.4 (30 May) 30.5 (13 Junea)

10.7 (24 May) 0.3 (4 June)

13 29 May–11 June 412

2 12–14 June

33.3 (10 June) 30.3 (25 Junea)

6.5 (16 June)

2 3 2001 15 May–15 June

1 2 3

2002 31 May–26 June

1 2

a

Last measurement of the cruise at D2.

is taken up. These vacuoles may take up to 90% of total cell volume in diatoms 45 mm in diameter (Smayda, 1970). The field studies of Bode et al. (1997) report that phytoplankton cells from upwelling situations have greater intracellular pools of NO3 than those from non-upwelling situations. 4.3. Optimal conditions for upwelled phytoplankton The optimal conditions for these larger phytoplankton and diatoms are pulsed wind events during which they take advantage of intermittent episodes of upwelled NO3, Si(OH)4 and CO2, while requiring relaxation events (Dugdale and Wilkerson, 1989). First there must be northwesterly upwelling-favorable winds of at least 12–15 m s1 (Figs. 2, 7 and 12),

followed by a reversal or relaxation in the winds. This lack of upwelling favorable winds must persist between 3 and 7 days for the upwelled nutrients to be drawn down and chlorophyll biomass to accumulate (MacIsaac et al., 1985; Dugdale and Wilkerson, 1989). Table 2 shows the D2 time series data split up into upwelling/relaxation pairs (events) based upon the wind data (Figs. 2, 7 and 12), with values of NO3 measured as close to possible to the end of the upwelling period and for chlorophyll that was observed as close to possible to the end of the relaxation period. A number of the events or upwelling/relaxation pairs showed this optimal scenario, with a period of 12–15 m s1 winds followed by a sufficient period of relaxation for chlorophyll to accumulate (Table 2; Figs. 5, 10 and

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15). In the first cruise of 2000, upwelling event 1 (Table 2) had strong upwelling that provided high levels of NO3 (31 mM), followed by a 7-day period of relaxation. Maximal chlorophyll values (32.1 mg l1) were reached earlier in the optimal window (after 6 days on 7 June), with a value of 19.3 mg l1 at the end of the relaxation period (8 June). The second event had upwelling-favorable winds for sufficient time for high NO3 concentrations to occur but the chlorophyll value was unavailable at the end of the following period of relaxation (22 June). The closest measurement was on 24 June, when chlorophyll had increased to 4.6 mg l1 from the low value of 1.7 mg l1 at the start of the relaxation period (13 June). The subsequent short and small upwelling (event 3) was not long enough for high surface NO3 to result, and the chlorophyll measured at the end of the subsequent relaxation period (5.4 mg l1) probably reflects phytoplankton biomass accumulation left over from the upwelling response of event 2. In 2001, upwelling event 1 (Table 2) also had strong upwelling followed by a 5-day relaxation event that fit the hypothetical 3–7 day window and chlorophyll accumulation resulted. The second event in 2001, only had relaxed winds for one day, insufficient for chlorophyll to be built up (0.3 mg l1 on 4 June). In 2002, the only chlorophyll bloom observed was in place when the study (cruise) began (i.e. 31 May 2002), but one could predict that 5 days before there was likely to have been a reversal in the winds, i.e. 26 May. The buoy record (Fig. 12) shows that this did occur, in support of a 3–7 day window. The rapid shift, just after a wind event, from low chlorophyll, low phytoplankton cell counts, and high nutrients to high chlorophyll, high cell numbers and low nutrients measured during WEST is a classic upwelling response (Barber and Smith, 1981; Huntsman and Barber, 1977; MacIsaac et al., 1985; Wilkerson and Dugdale, 1987). The WEST time scales of response compare favorably to other upwelling systems, for example drogue studies at 151S; Peru showed nutrient depletion within 2–3 days after the winds relaxed (MacIsaac et al., 1985), as observed in the WEST site (Figs. 5, 10 and 15). Drogue-following experiments initiated in recently upwelled water showed maxima in phytoplankton NO3 uptake capacity after 3–7 days (MacIsaac et al., 1985; Zimmerman et al., 1987 for 151S, Peru; Wilkerson and Dugdale, 1987; Dugdale and Wilkerson, 1989 for Point Conception, CA, Wilkerson unpubl. for Monterey Bay, CA). Estrada and

Blasco (1985) noted that the scale variability of upwelling wind events is important in most coastal upwelling systems. In other words wind fluctuations have to occur at time scales that are similar in duration to phytoplankton generation times. Zimmerman et al. (1987) and Dugdale et al. (1990) used simple models based upon the initial NO3 concentration in the upwelled water and the acceleration rate (a term used to describe the increased uptake rate of NO3 by upwelled phytoplankton that is directly related to the available NO3) to predict the time it would take for upwelled phytoplankton to respond and deplete the available nutrients. Zimmerman et al. (1987) indicated that the optimal condition (i.e. the shortest time for complete phytoplankton adaptation) to be with an initial NO3 concentration of at least 12.5 mM and a mixed-layer depth (MLD) of less than 25-m, with the effect of the mixed layer being small above 20-m. At the WEST site where the MLD is less than 25-m and NO3 concentrations are 430 mM, the time for complete physiological adaptation (i.e. maximum capacity for nutrient depletion) would be on the order of 4 days and the predicted time for complete NO3 utilization to be less than 8 days (Fig. 6 in Zimmerman et al., 1987). The natural phytoplankton in this study fit the time scales predicted by this model (Figs. 5, 10 and 15; Table 2). In 2001, the NH4 concentrations in the WEST study area were sufficiently high near the coast to delay the onset of rapid NO3 uptake by about 1 day following the beginning of relaxation (Dugdale et al., 2006). Neither the Zimmerman et al. (1987) model nor the shift-up model detailed in Dugdale et al. (1990) allowed for this effect (i.e. NH4 inhibition), which will need to be incorporated into future coastal upwelling productivity models designed to reproduce near-shore processes. 4.4. Interannual comparison Although the same trend of upwelled cold nutrient-rich water resulting in diatom-dominated phytoplankton accumulation occurred in all threesummer periods (2000–2003) the intensity and duration of the winds, the concentrations of upwelled nutrients, and the resultant chlorophyll accumulation was different between years (Figs. 6, 11 and 16). Lassiter (2003) reported mean surface temperatures at D2 during these cruises that showed a decrease from 2000 to 2001 to 2002, an increase in mean nutrients (NO3 and Si(OH)4), and

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a decrease in mean phytoplankton abundance either as chlorophyll or phytoplankton cell number. 2000 and 2001 were characterized by upwelling wind speeds of 12 m s1 or less, and significant relaxation periods of at least 5 days of relaxation (Table 2). The year 2002 had more intense upwelling winds of 12 m s1 and greater, with only one brief 2-day relaxation event, and had a high average Bakun index of 259 m3 s1 100-m coastline1 (N. Garfield, pers. commun.). The cooler nutrient-rich waters in 2002 may have been related to the anomalous highsalinity nutrient-rich waters reported for the upwelling area off Oregon studies (Huyer, 2003; Wheeler et al., 2003; Grantham et al., 2004). However, water mass analyses of the WEST site during the threesummer cruises (2000–2002) show no anomalously high salinity values in 2002 (N. Garfield, pers. commun.). The most optimal conditions for phytoplankton in the WEST site were in 2000, with the lowest Bakun index (77 m3 s1 100-m coastline1; N. Garfield, pers. commun.), and with more periods of sustained relaxation (Table 2). 4.5. Fate of the accumulated chlorophyll Surface chlorophyll data (i.e. Figs. 4,9 and 14) indicate that accumulation occurs downstream from the upwelling center and that the phytoplankton (dominated by the larger phytoplankton cells, likely diatoms) remain on the shelf and are propagated southward, rather than propagated offshore (Figs. 4, 9 and 14). Smaller cells (o2 mm picoplankton) may be carried offshore. In all threestudy years, the smaller flagellates were generally present in relatively consistent background numbers, with or without a diatom bloom (Lassiter, 2003). This pattern matches that reported by Brown and Hutchings (1985) in the Benguela Current region of South Africa, and likely occurred here because stations offshore of D4 were influenced by warmer water from the California Current, and not from coastal upwelled water. The fate of this along-shelf chlorophyll is unknown. It may be advected offshore, this seems unlikely (see Dever et al., 2006). It is most likely lost as sinking particles (export production) or is grazed and lost to upper trophic levels. It also may be recycled via the microbial web to fuel the background population of small-celled flagellates and picoplankton that most likely use ammonium as a N source. Probyn (1992) suggested that grazing on advected diatoms results in regenerated N that is

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released by grazers and taken up by the small-sized autotrophs (eukaryotic and prokaryotic), which have higher affinity for NH4 than diatoms, and so outcompete diatoms for regenerated nutrient (Probyn, 1992). These smaller non-sinking sizefractions conserve nutrients in the regenerative microbial loop (Chang et al., 1995) and thus are the likely biogenic agents carrying coastal new production offshore in the upper layer current system. It is likely that much of the chlorophyll reaches upper trophic levels. Typically diatoms dominate in short energy efficient foodwebs of coastal environments (e.g., Ryther, 1969). Following these blooms high biomasses of zooplankton (Dorman et al., 2005; Papastephanou et al., 2006) and zooplankton grazing (Slaughter et al., 2006) occurred. This region is just north of the Gulf of Farallones (for nutrients there, see Wilkerson et al., 2002) and it is likely that the productivity from this upwelling area is an important supply source for the rich breeding grounds of marine mammals (Allen et al., 1989), seabirds (Sydeman et al., 1998) and shark populations (Anderson and Goldman, 1996) in the Gulf. 5. Summary In summary, phytoplankton at the WEST site responded to optimal growth conditions on windevent time scales. As hypothesized, for this to occur persistent but pulsed upwelling favorable wind events of greater than three days, followed by a window of at least 3–7 days of reversed or relaxed winds were required. Typically the phytoplankton were capable of depleting surface nutrients and were a community made up mostly of large cell sizes, predominantly diatoms. These primary producers are likely important players in the carbon budgets of coastal upwelling regions through their influence on new production (Dugdale et al., 2006; Probyn, 1985) and export flux (Ragueneau et al., 2000). Acknowledgments We are grateful to Clive Dorman for providing the wind figures, to all the members of the Dugdale/ Wilkerson laboratory at RTC and the scientists involved with the CoOP WEST study for analytical help and useful discussions, and the assistance of the crew of the R.V. Point Sur. We thank two anonymous reviewers, and Misaki Takabayashi and Alex Parker for comments to the manuscript.

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We also thank N. Garfield for all the personal communications. This research was supported by the National Science Foundation (OCE-CoOP 99-10898).

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