Variations in phytoplankton dynamics and primary production associated with ENSO cycle in the western and central equatorial Pacific during

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1 JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 116,, doi: /2010jc006845, 2011 Variations in phytoplankton dynamics and primary production associated with ENSO cycle in the western and central equatorial Pacific during Kazuhiko Matsumoto 1 and Ken Furuya 2 Received 29 November 2010; revised 4 September 2011; accepted 18 October 2011; published 29 December [1] We examined spatial and temporal variations in phytoplankton distribution and primary production on the equator between 143 E and 160 W during The study area extended from the nitrate-depleted western Pacific warm pool (WPWP) to the nitrate-replete upwelling region in the central equatorial Pacific. Whereas depth-integrated chlorophyll a concentrations did not differ greatly between the WPWP ( mg m 2 ) and upwelling region ( mg m 2 ), depth-integrated primary production in the upwelling region was approximately double ( mg C m 2 d 1 ) that in the WPWP region ( mg C m 2 d 1 ), owing to the presence of deep chlorophyll maximum in the former and higher nutrient availability in the latter. Marked differences in water column structure were observed in the WPWP region between El Niño and La Niña: eastward advection of the WPWP region with development of El Niño led to thermocline shoaling in the WPWP region, resulting in a significant nitracline uplift (P < 0.01). In this region, the isopleth of 1-mM nitrate in the nitracline was brought up from an average of 103 m during La Niña to 61 m during El Niño. When the uplift reached the lower part of the euphotic zone, primary production was enhanced. The enhancement occurred at 4% to 10% light depths relative to that at the surface. However, the magnitude of the enhancement was not large, and there was no substantial difference in depth-integrated primary production between El Niño and La Niña. Citation: Matsumoto, K., and K. Furuya (2011), Variations in phytoplankton dynamics and primary production associated with ENSO cycle in the western and central equatorial Pacific during , J. Geophys. Res., 116,, doi: / 2010JC Introduction [2] The equatorial Pacific is characterized by a distinct east west gradient of environmental conditions and primary productivity, with a nitrate-depleted western Pacific warm pool (WPWP) region and a cooler, nitrate-replete eastern upwelling region [Barber and Chavez, 1983; Picaut et al., 1996]. The WPWP region can be broadly characterized by high sea-surface temperatures (SSTs) (exceeding 29 C) and a reduction in the salinity of surface water as a result of heavy rainfall. Physically, the eastern edge of the WPWP region is distinguished by a sharp salinity front [Maes et al., 2006]. In contrast, the eastern upwelling region is generally characterized by a high-nutrient, low-chlorophyll (HNLC) regime [Minas et al., 1986]. The equatorial Pacific can be divided into three areas of varying nitrate concentrations in the surface mixed layer: the WPWP region (<0.1 mm), the HNLC upwelling region (>4 mm), and the intermediate 1 Research Institute for Global Change, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan. 2 Department of Aquatic Biosciences, University of Tokyo, Tokyo, Japan. Copyright 2011 by the American Geophysical Union /11/2010JC transition region [Matsumoto et al., 2004]. Horizontal heterogeneity of phytoplankton distribution has been reported in the surface mixed layer along the equator, and phytoplankton distribution is closely associated with nitrate availability [Matsumoto et al., 2004]. Whereas surface chlorophyll a (chl a) concentrations are much lower in the WPWP region than in the eastern upwelling region, as evident from ocean color satellite images [e.g., Ryan et al., 2006], the amount of depth-integrated chl a does not differ substantially between the two regions, because a deep chlorophyll maximum (DCM) develops around the thermocline in the WPWP region [Mackey et al., 1995]. [3] The DCM is caused by the suppression of upward nutrient flux from below the thermocline into the surface mixed layer as a result of density stratification. There is distinct halocline near the surface in the WPWP region, and it remains stable because of high precipitation levels, which exceed evaporation rates [Lukas and Lindstrom, 1991; Ando and McPhaden, 1997]. A thermocline is generally located beneath the halocline [Lukas and Lindstrom, 1991]. Thus, the salinity-derived pycnocline, which corresponds to the surface mixed layer, is often shallower than the temperaturederived pycnocline. The layer between the bottom of the surface mixed layer and the bottom of the isothermal layer, which corresponds to the top of the thermocline, is defined 1of16

2 Figure 1. Sampling locations during as the barrier layer [Lukas and Lindstrom, 1991]. The occurrence of a barrier layer indicates that there is a doublelayered structure in the vertical density profile. The presence of this barrier layer suppresses upward nutrient flux and consequently controls surface phytoplankton abundance in the WPWP region [Mackey et al., 1995; Radenac and Rodier, 1996]. [4] Despite the similar chl a amounts integrated through the water column, depth-integrated primary production is much lower in the WPWP region than in the upwelling region [Mackey et al., 1995]. This difference in primary production is attributable to a difference in the vertical distribution of chl a, the major portion of which is located in the lower part of the euphotic zone in the WPWP region. The vertical distribution of phytoplankton shows distinct eastwestward fluctuations along with an east-westward shift of the salinity front in association with the El Niño Southern Oscillation (ENSO) cycle [Matsumoto et al., 2004]. During El Niño, weakening of trade winds along the equator reduces equatorial upwelling in the central and eastern equatorial Pacific [McPhaden, 1999]. The weakened upwelling lowers nutrient availability for phytoplankton and consequently decreases primary production to below that of the climatological mean [Barber et al., 1996; Chavez et al., 1999; Strutton and Chavez, 2000]. Thus, El Niño events result in the progressive reduction of primary production in the central and eastern equatorial Pacific. The eastward advection of the WPWP water shoals the thermocline in the western part of the WPWP region [McPhaden, 1999]. In this area, the barrier layer thins or occasionally disappears; as a result, upward nutrient flux into the shallower depths is expected to increase, enhancing phytoplankton biomass and primary production [Mackey et al., 1997]. Thus, the El Niño event likely controls primary production through changes in nutrient availability in the equatorial Pacific. [5] Picophytoplankton such as Prochlorococcus, Synechococcus, and picoeukaryotes are dominant in the equatorial Pacific [Blanchot and Rodier, 1996; Matsumoto et al., 2004]. In the western and central equatorial Pacific, these groups have different distributional patterns from each other within the surface mixed layer, and the patterns are closely associated with ambient nitrate concentrations [Matsumoto et al., 2004]. This association is likely lead to regional differences in primary production on the equator. However, there have been few shipboard observations during the various ENSO states in these regions. Therefore, our understanding of the relationships between variations in the physicochemical properties associated with ENSO strength and biological responses is extremely limited. Our study aimed to clarify the interrelationships between phytoplankton dynamics and primary production in relation to nutrient fields in the three areas (WPWP, upwelling, and intermediate transition regions) during various ENSO states. 2. Methods 2.1. Sampling and Physicochemical Analyses [6] Oceanographic observations were conducted along the equator between 143 E and 160 W during 10 cruises of the research vessels Kaiyo or Mirai between 1994 and 2003 (Figure 1 and Table 1). Selected data obtained from these cruises are available at the data site of Japan Agency for Marine-Earth Science and Technology ( go.jp/cruisedata/e/index.html). Because SSTs in the WPWP Table 1. Cruise Information, Observation Periods, ENSO Status, and Methods of Analysis of chl a Cruise Name Ship Longitude Month and Year ENSO Status Chl a Analysis a K94-06 Kaiyo 147 E 165 W Nov Dec 1994 El Niño Spectrofluorometry K95-11 Kaiyo 147 E 165 W Dec 1995 Jan 1996 La Niña Spectrofluorometry K97-01 Kaiyo E W Jan 1997 La Niña Turner fluorometry (A) KY97-14 Kaiyo E 180 W Dec 1997 El Niño Spectrofluorometry MR98-01 Mirai 180 E W Feb 1998 El Niño Spectrofluorometry MR98-K02 Mirai 145 E W Jan 1999 La Niña Spectrofluorometry MR99-K07 Mirai 145 E W Nov Dec 1999 La Niña Spectrofluorometry MR00-K08 Mirai 145 E 160 W Jan 2001 La Niña Spectrofluorometry MR02-K01 Mirai 145 E 160 W Jan Feb 2002 Normal Spectrofluorometry MR02-K06 Mirai 145 E 160 W Dec 2002 Jan 2003 El Niño Turner fluorometry (NA) a Three methods were used for chl a analysis: spectrofluorometry without acidification, Turner fluorometry with acidification (A), and Turner fluorometry without acidification (NA). 2of16

3 region are the highest from December to April, and El Niño conditions are typically enhanced during this period [Wang and Fiedler, 2006], cruises were conducted once or twice during these months in most years. The status and strength of each ENSO event were indexed by using the multivariate ENSO index (MEI) [Wolter and Timlin, 1998]. [7] Water samples were collected from the upper 200 m. From 1994 to 1998, samples were collected in Niskin bottles on a Kevlar rope, the end of which was attached to a CTD profiler (SBE 19, Sea-Bird Electronics). From 1999 to 2003, sampling was conducted with Niskin bottles fitted on a rosette sampler system mounted on a CTD profiler (SBE 911 plus, Sea-Bird Electronics), which was connected to a wire cable. Each Niskin bottle was fitted with a silicon-rubber closure band and o-rings. Surface water samples were taken with a plastic bucket. The depth of the isothermal layer was defined as the depth at which the CTD profiler measured a net change of 0.5 C relative to the temperature just below the surface. The depth of the surface mixed layer was defined as that at which the profiler measured a net change of s q relative to the density just below the surface. The thermocline was defined as occurring at the depth with the steepest thermal gradient within the upper 200 m of the water column. The barrier layer thickness was estimated as the interval between the bottom of the surface mixed layer and the bottom of the isothermal layer [Lukas and Lindstrom, 1991]. Nitrate, phosphate, and silicate concentrations were analyzed on board by using standard methods and an Auto- Analyzer (TrAAcs 800 system; Bran+Luebbe). The detection limits were 0.05, 0.01, and 0.5 mm for nitrate, phosphate, and silicate, respectively Phytoplankton Abundance [8] Chlorophylla was quantified on board the ship by using fluorometry. A spectrofluorometer (RF-5000, Shimadzu), a Turner fluorometer (model 10-AU, Turner Designs), or both were used for non-acidification fluorometry [Welschmeyer, 1994] (Table 1). During cruise K97-01, only conventional acidification fluorometry [Holm-Hansen et al., 1965] was adopted, with the Turner fluorometer (Table 1). Systematic differences in fluorometry were noted among the methods: the values obtained with Turner acidification fluorometry were on average 11% lower than those obtained with (nonacidification) spectrofluorometry (P < 0.01, n = 508), whereas non-acidification Turner fluorometry gave estimates 11% higher than those with spectrofluorometry (P < 0.01, n = 517). In the present study, chl a determined by nonacidification spectrofluorometry were used except data obtained by acidification fluorometry during the K97-01 cruise and by non-acidification fluorometry during the MR98-K02 cruise. [9] Particles in 0.5-L water samples were filtered on a 0.4-mm polycarbonate filter (47 mm in diameter), and chl a was immediately extracted in N,N-dimethylformamide in darkness at 20 C for 24 h [Suzuki and Ishimaru, 1990]. Size-fractionated chl a was obtained by sequential filtration of 1-L water samples through 10-, 2-, and 0.4-mm pore size polycarbonate filters. The size-fractionated chl a was then quantified by using non-acidification spectrofluorometry. Total chl a and size-fractionated chl a were not quantified from the same aliquot. The fluorometers were calibrated against standard chl a (Sigma) to three significant digits. The highest chl a concentration we obtained was <0.8 mg L 1, and the detection limit was set at mg L 1. [10] For the four cruises of the study period spanning November 1999 January 2003, the abundance of three groups of picophytoplankton Prochlorococcus, Synechococcus, and picoeukaryotes was determined by flow cytometry. Water samples were prefiltered through a 10-mm meshand subsequently fixed with 1% (v/v final concentration) glutaraldehyde and stored at 4 C until analysis. Flow cytometry was conducted onboard the ship within 24 h of fixation by using a Bryte-HS flow cytometer (Bio-Rad Laboratories, Inc.). Details of the counting procedure are given by Matsumoto et al. [2004] Primary Production [11] Primary production was assessed by in situ 24-h or 3-h incubations. Seawater samples for 24-h incubation were collected just before dawn during cruises MR99-K07, MR00-K08, MR02-K01, and MR02-K06. Water samples (1 L) were placed into duplicated acid-cleaned transparent polycarbonate bottles after prefiltration through a 200-mm mesh, and NaH 13 CO 3 was added to each bottle for bicarbonate enrichment to 10% of ambient dissolved inorganic carbon (final concentration of NaH 13 CO 3, 0.2 mm). Subsequently, the bottles were placed at their original depths on a line that was attached to a drifting buoy or hung on the ship. Incubation was initiated immediately after sampling and conducted from dawn to the next dawn (24 h). During the incubation, downwelling photosynthetically available radiation (PAR) was measured at local noontime with an irradiance meter (MER-1010 system, Biospherical Instruments) or a SeaWiFS profiling multichannel radiometer (SPMR system, Satlantic). We defined the euphotic zone as the layer from the surface down to the depth at which the light intensity relative to that at the surface reached 1%. The bottles were recovered at about local sunset and kept in an on-deck bath cooled by running surface water with shading until just before next dawn. During cruises KY97-14 and MR98-01, incubation was conducted in situ at about local noontime for 3 h. After the incubation, water samples were filtered through a precombusted GF/F filter, and inorganic carbon was removed by HCl fume treatment. The 13 C content of the particulate fraction was measured with an automatic nitrogen and carbon analyzer (ANCA-SL) mass spectrometer (SerCon) [Hama et al., 1983]. [12] Size-fractionated analysis of primary production was conducted during cruise MR02-K06 after on-deck incubation. Seawater samples were collected from the surface, the DCM, and an intermediate depth at about local noon, introduced into acid-cleaned transparent polycarbonate bottles, and incubated in the on-deck bath for 24 h, until the next noon. The light intensity on each bottle was adjusted to that in situ by using neutral density screens corresponding to the light levels at specific sampling depths. After incubation, samples were divided into four fractions: (1) not prefiltered, (2) prefiltered through a 10-mm pore size filter, (3) prefiltered through a 3-mm pore size filter, and (4) prefiltered through a 1-mm pore size filter. All the fractions were subsequently filtered through a GF/F filter. 13 C was spiked and quantified in the same manner as described above. Thus, size-fractionated primary production 3of16

4 Figure 2. Time series of (a) the multivariate ENSO index (MEI), (b) surface salinity, and (c) surface nitrate along the equator between 143 E and 160 W during Positive and negative MEIs indicate El Niño and La Niña periods, respectively. Dots in Figures 2b and 2c denote sampling points. Areas without data for >10 of longitude are blacked out. was obtained for the <1 mm, 1- to 3-mm, 3- to 10-mm, and >10-mm fractions. 3. Results 3.1. Hydrological Variations [13] El Niño events, which are indicated by a positive MEI, occurred in , , and , corresponding to cruises K94-06, KY97-14, MR98-01, and MR02-K06 (Figure 2a). La Niña events, with negative MEI, occurred in , , , , and , corresponding to cruises K95-11, K97-01, MR98-K02, MR99-K07, and MR00-K08. During the MR02-K01 cruise in , the MEI was weakly negative, but the MEI values just before and just after the cruise were positive. Therefore, this period was regarded as normal and was excluded from the La Niña evaluations in our subsequent analysis. [14] On the basis of the definitions of Matsumoto et al. [2004], the study area was divided into three regions, i.e., the nitrate-depleted WPWP region, the HNLC upwelling region, and the intermediate transition region, to evaluate the relationships among nutrient availability, phytoplankton composition, and primary production. The 0.1-mM nitrate isopleth at the surface, which was used as the eastern boundary of the WPWP region, approximately coincided with the surface salinity front (Figures 2b and 2c). A nitratereplete upwelling region was found only during La Niña. The occurrence of El Niño events caused the WPWP region to extend eastward along the equator. During the El Niño, which is reportedly the strongest on record [McPhaden, 1999], the eastward expansion of the WPWP region extended beyond the study area. In comparison to the El Niño, the El Niño was moderate, with the WPWP region boundary being located just east of the dateline. During La Niña, the WPWP region was clearly confined to the west of the dateline, with the boundary being frequently located in the vicinity of 160 E. [15] We compiled vertical profiles of temperature, salinity, nutrients, and chl a for all the cruises (Figure 3). During the El Niño period, two cruises (KY97-14 and MR98-01) were conducted. The former covered an area between E and the dateline in December 1997, and the latter between the dateline and W in February Composite contour plots were prepared from the data for these two cruises. [16] High SSTs (exceeding 29 C) extended eastward with the development of El Niño conditions, and the least-saline water also shifted toward the east, as seen during (Figure 3). The deepest surface mixed layer appeared around the least-saline water (during cruise K94-06) or to the west of the least-saline water (during cruises MR02-K01 and MR02-K06). The surface mixed layer shoaled farther westward, as typically observed during cruise MR02-K06. The least-saline water shifted to the east during the strong El Niño, so that a shallower surface mixed layer was 4of16

5 Figure 3. Vertical cross-sections of temperature, salinity, nitrate, phosphate, silicate, and chl a. Dots indicate sampling depths. In the temperature and salinity plots, dashed lines represent the bottom of the surface mixed layer in the western Pacific warm pool region and dotted lines represent the isothermal layer in this region. Bold lines in the nutrient and chl a plots represent 1% light depth (note that data for this depth were not obtained during cruise MR98-01). Chl a was quantified by acidification Turner fluorometry during cruise K97-01, by non-acidification Turner fluorometry during cruise MR02-K06, and by nonacidification spectrofluorometry during all the other cruises. 5of16

6 Figure 3. present throughout the study area. To the west of the leastsaline water, the depth of the surface mixed layer tended to coincide with that of the isothermal layer. The barrier layer between the bottom of the surface mixed layer (dashed line) (continued) and the bottom of the isothermal layer (dotted line) became shallower and thinner (Figure 3), because the surface mixed layer and the isothermal layer tended to be shallow toward the west in the western part of the WPWP region. A thicker 6of16

7 Figure 3. (continued) barrier layer was generally observed in the eastern part of the WPWP region, although it was occasionally observed even in the western part of the least-saline water during El Niño. [17] Nitrate was almost depleted in the upper isothermal layer in the WPWP region during both El Niño and La Niña periods. During El Niño, the westward shoaling of the surface mixed layer and isothermal layer in the WPWP region was accompanied by shoaling of the 1-mM nitrate isopleth (Figure 3). The bottom of the isothermal layer (i.e., the top of the thermocline) did not coincide with the top of the 7of16

8 nitracline in the western part of the WPWP region, and nitrate depletion was observed even below the isothermal layer. This nitrate depletion below the isothermal layer in the western part of the WPWP region was not confirmed during La Niña periods, because the western part of the WPWP region was shifted far westward, beyond the study area. The vertical distributions of phosphate and silicate were similar to those of nitrate, but their concentrations within the surface mixed layer were greater during La Niña than during El Niño. During the strong El Niño, relatively high concentrations of nutrients were supplied to the bottom of the euphotic zone in the WPWP region (Figure 3). [18] A distinct DCM developed in the WPWP region at the bottom of the euphotic zone (Figure 3). The surface chl a concentration increased toward the east, causing the clear DCM to disappear. During La Niña, the DCM deepened and its chl a concentration decreased in the WPWP region. In contrast, during El Niño, with the eastward advection of the WPWP water, the DCM shoaled and its chl a concentrations increased. The maximum concentration of chl a was found during the strong El Niño in the shoaled DCM located at 60 m Vertical Profiles of Physicochemical Properties [19] The mean vertical profiles ( ) of physicochemical and biological properties, computed for 10 years from all the cruises, depicted a distinctive vertical structure in each region (Figure 4). Profiles for the WPWP region were subdivided into periods of El Niño and La Niña, because striking vertical differences were observed between the two periods (Figure 3). The transition and upwelling regions could not be subdivided into such periods, because limited observations were available in these regions during El Niño, owing to the eastward advection of the WPWP water beyond the study area. [20] The temperature profiles indicated that the bottom of the isothermal layer was located at 40 m in the WPWP region during El Niño (Figure 4a); during La Niña it was as deep as 70 m, with high temperatures (exceeding 29 C). The steep vertical gradient forming the thermocline thus appeared at a markedly shallower depth during El Niño than during La Niña. In the transition and upwelling regions, the bottom of the isothermal layer was located at 100 m. [21] The vertical gradient of the salinity profiles was steep from near the surface to 100 m during both El Niño and La Niña in the WPWP region. The water mass was stable in the upper 100 m water column, although it was less saline during El Niño (Figure 4b). In the transition region, a weak salinity increase with depth was apparent in the upper 100 m water column, but a uniform vertical profile was observed in the upwelling region. [22] The density profiles were relatively uniform above 120 m in both the transition and the upwelling region (Figure 4c), indicating that the water mass was well mixed. In the WPWP region, a vertical gradient was evident below the surface and above the deep, steeper gradient of the thermocline. This double-layered structure indicates the existence of a barrier layer. The steep gradient of the thermocline was deeper during La Niña, indicating that the barrier layer thickness was larger during La Niña. [23] Within the isothermal layer, nitrate was depleted in the WPWP region (Figure 4d), with levels increasing toward the eastern upwelling region. The vertical profiles of phosphate were similar to those of nitrate, but the concentrations of phosphate within the isothermal layer of the WPWP region were slightly higher during La Niña than during El Niño (Figure 4e). The steep nutrient gradient became shallower during El Niño, coinciding approximately with the shoaled thermocline in the WPWP region. During El Niño, high nitrate concentrations (exceeding 4 mm) were supplied into the lower part of the euphotic zone in the WPWP region, where the 1% light depth was located at 91 m on average (Table 2). The incident light intensity was significantly higher during La Niña than during El Niño in the WPWP region (P < 0.05, Table 2) Vertical Profiles of Biological Properties [24] In the WPWP region, the vertical profiles of chl a showed distinct DCMs that deepened slightly during La Niña (Figure 4f). The depth-integrated concentration of chl a from the surface to 200 m was significantly lower in the WPWP region than in the other regions (P < 0.01), but the difference was small (Table 2). Depth-integrated chl a concentration in the WPWP region did not differ between El Niño and La Niña, even though nitrate was less available in the euphotic zone during La Niña. [25] The <2-mm fraction was the most abundant throughout the water column in all regions (Figures 4g 4i and Table 2). Depth-integrated <2-mm chl a accounted for about 70% of the total, and >10-mm chl a accounted for about 10% or less, even in the upwelling region (Table 2). During La Niña, the DCM of the >10-mm fraction became less distinct, and an increased concentration of this fraction was observed sporadically in the surface layer. Microscopic analysis revealed the colony-forming diazotroph Trichodesmium spp. when high concentrations of >10-mm chl a were observed at the surface of the WPWP region (145 E) during La Niña (MR98-K02, data not shown). [26] Prochlorococcus showed a deep maximum in all regions, which was deeper in the WPWP region than in the other regions (Figure 4j). The surface abundance of Prochlorococcus increased toward the eastern upwelling region. However, the highest abundance of Prochlorococcus was recorded in the vicinity of the DCM in the WPWP region during La Niña. Synechococcus exhibited a weak deep maximum in the WPWP region; this maximum was shallower than that of Prochlorococcus (Figure 4k). In the WPWP region, the abundance of Synechococcus was higher during La Niña than during El Niño. The highest Synechococcus abundance was noted in the transition region. Figure 4. Vertical profiles of decadal mean (a) temperature, (b) salinity, (c) density, (d) nitrate, (e) phosphate, (f) total chl a (only those chl a data obtained by spectrofluorometry are plotted, owing to systematic errors among the different types of fluorometry (see section 2)), (g) <2-mm chl a, (h) 2- to 10-mm chl a, (i) >10-mm chl a, (j) Prochlorococcus, (k) Synechococcus, and (l) picoeukaryotes in the western Pacific warm pool (WPWP), transition, and upwelling regions during Data are shown separately for El Niño and La Niña periods in the WPWP region. Bars denote standard errors. Chl a was quantified by spectrofluorometry. 8of16

9 Figure 4 9of16

10 Figure 4. (continued) 10 of 16

11 Table 2. Total Chl a, Size-Fractionated Chl a, Primary Production, Daylight Surface PAR, and Euphotic Depth in Each Region During a WPWP El Niño t-test b La Niña Total Mean t-test c Transition t-test d Upwelling Total chl a (mg m 2 ) (31) NS (11) (50) P < (19) NS (7) <50 m 17% 21% 19% 38% 42% Size-fractionated chl a (%) <2 mm mm >10 mm Primary production (4) NS (3) (9) P < (6) P < (3) (mg C m 2 d 1 ) <50 m 72% 59% 62% 75% 69% PAR (mol quanta m 2 d 1 ) (29) P < (12) (43) P < (24) NS 54 5 (13) Euphotic depth (m) (36) NS (14) (58) P < (30) P < (13) a Data are depth-integrated means and standard deviations. For the western Pacific warm pool (WPWP) region, data are shown separately for El Niño, La Niña, and the entire period (including the normal phase). Chl a was integrated from the surface to a depth of 200 m. Size-fractionated chl a is shown as percentages of the total chl a. Primary production was integrated from the surface to a depth of 120 m. Euphotic depth is 1% light depth. Percentages of the total vertical profile (above 50 m) are shown for total chl a and primary production. Numbers in parentheses represent the number of sampling stations included in each mean. NS denotes not significant. b Comparison between El Niño and La Niña (WPWP region). c Comparison between WPWP region (total mean) and transition region. d Comparison between transition region and upwelling region. Picoeukaryotes abundance increased toward the east at depths above 50 m, and the highest abundance was observed in the upwelling region (Figure 4l). Picoeukaryotes showed a deep maximum in the WPWP region Variations in Physicochemical and Biological Properties in Relation to ENSO Strength [27] We examined variations in physicochemical and biological properties in the WPWP region with respect to changes in ENSO strength (Figure 5). The thermocline depth (Figure 5a), 1-mM nitrate isopleth depth (Figure 5b), and isothermal depth (Figure 5c) were negatively correlated (P < 0.01) with the development of El Niño conditions. The depth of the thermocline, which was defined as the steepest thermal gradient, became shallower as El Niño conditions developed (Figure 5a). Regression indicated that the shallowest depth of the thermocline was 80 m at the highest MEI. The 1-mM nitrate isopleths was indicated into 103 m at the lowest MEI, and it was brought up into 61 m at the highest MEI (Figure 5b). The thermocline depths were slightly greater than the 1-mM nitrate isopleths (Figures 5a and 5b), but they deepened during La Niña periods (i.e., with negative MEIs). The isothermal depths were shallower than the 1-mM nitrate isopleths, which were located between the thermocline and the isothermal layer (Figure 5c). The barrier layer thickness varied considerably, up to 80 m, regardless of the ENSO state (Figure 5d). [28] Phosphate concentrations at the surface decreased significantly (P < 0.01) as El Niño conditions developed (Figure 5e). Phosphate was never exhausted during La Niña, but it declined along with the progress of El Niño and occasionally became exhausted. In contrast, surface nitrate was almost completely exhausted during La Niña, but high concentrations (>0.1 mm) were observed during the strong El Niño. Because of these high concentrations, a significant positive correlation (P < 0.01) was noted between MEI and surface nitrate (Figure 5f). Therefore, the ratio of nitrate to phosphate at the surface increased as El Niño conditions developed Variations in Primary Production Associated With ENSO [29] Depth-integrated primary production increased significantly toward the east and was about twice as high in the upwelling region as in the WPWP region (Table 2). Primary production in the upper 50 m of the water column accounted for >50% of the depth-integrated primary production in the three regions (Table 2). The mean vertical profiles of primary production, as determined by 24-h in situ incubations, differed markedly among regions (Figure 6a). The highest production was observed in the upwelling region, where the production maximum occurred at depths of 10 to 30 m, followed by the transition region. [30] In the WPWP region, the vertical profiles of primary production showed a subsurface maximum during El Niño (Figures 6a and 6c). The subsurface maximum was most marked during the strong El Niño (Figure 6c), when the maximum was observed at all seven sampling stations in the WPWP region. A similar subsurface elevation of primary production was observed during the moderate El Niño, although the marked enhancement of primary production disappeared by averaging (Figure 6a). The enhancement was observed at 4% to 5% light depth, or shallower. The shallowest maximum of >10 mg C m 3 d 1 was found during the MR02-K06 cruise at 40- to 50-m depths at 151 E; here, the light depth relative to the surface was 6% to 10%, with ample nitrate concentrations of 0.12 to 1.28 mm. However, enhancement of primary production did not necessarily occur, even during El Niño. The 24-h incubation shown in Figure 6a was conducted at four sampling stations during El Niño; there was one enhancement of primary production, as stated above, but enhancement was absent at the three other stations. At those stations lacking enhancement, the 1-mM nitrate isopleth was located at 1%, 2%, and 5% light depths. [31] Interestingly, primary production at depths of 70 to 90 m was significantly higher during La Niña than during El Niño in the WPWP region (P < 0.05, Figure 6a), although 11 of 16

12 Figure 5. Variations in (a) thermocline depth, (b) nitrate isopleth depth, (c) isothermal depth, (d) barrier layer thickness, (e) sea-surface phosphate, and (f) sea-surface nitrate as functions of the multivariate ENSO index (MEI) in the western Pacific warm pool region. Significant correlation was not observed between MEI and barrier layer thickness. the mean profiles from the surface to depths of 60 m did not differ significantly between the two periods (P > 0.05, Figure 6a). Chl a-specific primary production was significantly lower between 60 m and 90 m during El Niño than during La Niña (P < 0.05 at 60 m and P < 0.01 at 70 to 90 m), although it did not differ in the upper 50 m of the water column between the two periods (Figure 6b). [32] The contribution of size-fractionated primary production to the total was estimated for the <1-mm, 1- to 3-mm, 3- to 10-mm, and >10-mm fractions during El Niño in the western area of the WPWP region (156 E), at the eastern edge of the WPWP region (179 E), and in the transition region (165 W) (Figure 7). At 156 E, the 1-mM nitrate isopleth shoaled to nearly 60 m (Figure 7), and the thickness of the barrier layer declined to 48 to 58 m. In contrast, the 1-mM nitrate isopleth deepened to nearly 90 m at 179 E (Figure 7), and the barrier layer became thicker (54 to 89 m). Nitrate was depleted within the isothermal layer in both areas of the 12 of 16

13 Figure 6. Mean vertical profiles of primary production and chl a-specific primary production in each region, as determined by (a, b) 24-h and (c) 3-h in situ incubations. The 24-h incubations were performed during four cruises MR99-K07, MR00-K08, MR02-K01, and MR02-K06. The 3-h incubations were performed during the strong El Niño. Closed circle with solid line and open circle with dashed line in Figure 6c represent primary production and chl a-specific primary production, respectively. Bars denote standard errors. The number of stations used in the 24-h incubations is given in Table 2. The 3-h incubations were performed at seven stations. WPWP region. In contrast, high concentrations of nitrate (exceeding 1.5 mm) were observed throughout the upper 100 m at 165 W (Figure 7). At 165 W, primary production was highest in the 1- to 3-mm fraction in waters. The fraction was also major at a depth of 70 m at 156 E, where the light intensity was 5% of that at the surface (Figure 3) and the nitrate concentration was high (>3 mm). Picoeukaryotes exhibited a subsurface maximum in their abundance in this layer. Flow cytometry showed that picoeukaryotes were major components of the 1- to 3-mm fraction. 4. Discussion 4.1. Effects of Large-Scale Climatic Forcing on Primary Production [33] Along with the eastward advection of WPWP water during El Niño, nitrate depletion at the surface extends toward the central and eastern equatorial Pacific. This reduced nutrient availability reduces primary production in the central and eastern equatorial Pacific, and the overall primary productivity of the equatorial Pacific is consequently decreased during El Niño [Chavez et al., 1999]. However, our study demonstrated enhancement of primary production in the subsurface layer of the poorly productive WPWP region. Nutrient availability was increased in the lower part of the euphotic zone during El Niño because of uplift of the nitracline (Figure 5b) due to shoaling of the thermocline (Figure 5a). This was caused by the eastward advection of the WPWP water [McPhaden, 1999]. During the strong El Niño, the least-saline water shifted far eastward, beyond the dateline, and thermocline shoaling was observed in the whole study area (Figure 3). As a result, enhancement of primary production was observed at the subsurface. In the mean vertical profile of primary production, the subsurface maximum was located at 60 m depth during the strong El Niño (Figure 6c), at which time the 1-mM nitrate isopleth was lifted up to this depth (Figure 5b). Even during the moderate El Niño, the subsurface maximum of primary production was observed at 40 to 50 m in conjunction with replete nitrate concentrations, where the light intensity relative to that at the surface was 6% to 10% (Figure 3). Thus, primary production will be enhanced at the subsurface in the WPWP region during El Niño, although such enhancement will not have occurred when uplift of the nitracline was insufficient in terms of light depth. These inferences are in good agreement with the findings of Turk et al. [2001], who showed that during El Niño, new production in the subsurface layers of the WPWP region was stimulated. However, we found that, at the few stations where enhancement of primary production did not occur, the 1-mM nitrate isopleth had still been elevated to within the euphotic zone (>1% light depth). We cannot explain the absence of enhancement at these stations. [34] At depths of 70 to 90 m, primary production was significantly higher during La Niña than during El Niño (Figure 6a). Nitrate was not exhausted at these depths during either period (Figure 4d) and the depths of the euphotic zone were similar, but there was significantly higher incident light intensity during La Niña (Table 2). The low surface PAR 13 of 16

14 Figure 7. Vertical distributions of nitrate, picophytoplankton numerical abundance, chl a, and sizefractionated primary production of <1-mm, 1- to 3-mm, 3- to 10-mm, and >10-mm fractions in the western WPWP (western Pacific warm pool) region (156 E), the eastern WPWP region (179 E), and the transition region (165 W) during cruise MR02-K06. On-deck incubation experiments for primary production were conducted under the following light conditions: 100% (surface), 25%, and 5% at 156 E and 165 W and 100% (surface), 10%, and 1% at 179 E. PP denotes primary production. during El Niño to the WPWP region was suspected to being rainier and more overcast because of the rising of air over the warm water [Lukas and Lindstrom, 1991; Ando and McPhaden, 1997]. Thus, we attribute the higher level of primary production at the bottom of the euphotic zone during La Niña to the favorable light conditions in this region. This inference is supported by the significantly higher chl a-specific primary production at depths of 60 to 90 m depths during La Niña than during El Niño (Figure 6b). [35] Analysis of size-fractionated primary production revealed the major contribution of picoeukaryotes to primary production at 5% light depth under nitrate replete conditions as a result of thermocline shoaling at 156 E (Figure 7). Increased nitrate availability likely favored both picoeukaryotes and Synechococcus: Prochlorococcus cannot utilize nitrate or nitrite, because generally it lacks reductase activity [García-Fernández and Diez, 2004; Palinska et al., 2002], although some strains that are adapted to low light conditions are able to utilize nitrite [Moore et al., 2002]. Prochlorococcus is therefore largely dependent on ammonium and other reduced forms of nitrogen. Synechococcus can utilize a variety of nitrogen sources and requires substantial amounts of nitrogen from nitrate and ammonium to maintain the nitrogen-rich phycobilisomes in its light-harvesting apparatus [Moore et al., 2002]. However, it is not advantageous for Synechococcus to extend its distribution down to parts of the water column with low light conditions [Partensky et al., 1999]. The observed contribution of picoeukaryotes at the subsurface to primary production at 156 E (Figure 7) therefore likely reflected increased nitrate availability due to uplift of the nitracline during El Niño Effects of Intraseasonal Forcing on Primary Production [36] If the nitracline is uplifted during El Niño, winddriven vertical mixing is likely to bring nutrients to the surface and enhance primary production in the WPWP region. Episodic wind events are evident from TRITON/ TAO array data ( obtained for the regions monitored in our study. The phytoplankton bloom that developed during April June 1998, at the end of a strong El Niño period, was revealed by satellite-based observations of 165 E of the WPWP region [Ryan et al., 2002]. These authors showed that the Equatorial Undercurrent (EUC) shoaled to 70 m and they theorized that rich nutrients were transported into the euphotic zone by turbulent vertical mixing and wind-driven upwelling. [37] We occasionally detected increased phosphate and nitrate concentrations in the surface layer during the strong El Niño (Figures 5e and 5f). This implies that shoaled nutrient-rich water was brought into the surface mixed layer as a result of wind-driven vertical mixing by episodic strong winds. However, enhancement of primary production near the surface was not evident, possibly owing to the limited number of primary production experiments we were able to perform at this time (Figure 6b). During the moderate El Niño of the MR02-K06 cruise in December 2002 to January 2003, enhancement of primary production in the lower euphotic zone was observed at 156 E, although primary production did not appear to be enhanced at the surface (Figure 7). Matsumoto and Ando [2009] found that wind-forcing was weak and the water mass was stable in the 14 of 16

15 surface mixed layer during the time when shipboard observations were being conducted on cruise MR02-K06 at 156 E. However, TRITON data and numerical modeling showed that wind-driven vertical mixing at the sampling station had reached the depth of the thermocline 2 days in advance of the sampling [Matsumoto and Ando, 2009]. The enhancement of primary production associated with episodic winds is likely terminated by the cessation of strong wind events, because phytoplankton can consume nutrient supplies rapidly. [38] In addition, well-stratified water coupled with the barrier layer was evident in the WPWP region (Figure 5d), whereas the water column was well mixed in the surface layer at the transition and upwelling regions (Figure 4c). Strong wind events generally produce deep vertical mixing, but a thick barrier layer reduces vertical mixing, thus preventing entrainment of nutrient-rich water from the thermocline into the surface mixed layer [Lukas and Lindstrom, 1991]. Enhancement of primary production by intraseasonal wind-forcing is therefore not a common situation, although it could be an important factor occasionally Potential Factors Increasing Primary Production in the WPWP Region [39] Macronutrients are not the only factors considered to control primary production. For example, previous studies have demonstrated that limitation of iron levels decreases primary production in the equatorial Pacific [Barber et al., 1996; Coale et al., 1996; Cavender-Bares et al., 1999]. Hence, in the equatorial Pacific, both aeolian processes (i.e., the winds) and upward iron flux are potentially important. However, aeolian iron fluxes generally appear to be minimal in both the western and eastern equatorial Pacific [Duce and Tindale, 1991]; hence, the main source of iron is expected to be the EUC [Barber et al., 1996; Coale et al., 1996; Landry et al., 1997]. In the eastern Pacific, the EUC is located just beneath the euphotic zone, and upward supply of iron to the euphotic zone is considered important to primary production [Mackey et al., 2002]. In contrast, in the western Pacific the EUC is located much deeper, and upward supply of iron to the euphotic zone is much smaller. Furthermore, upward supply of iron in WPWP water is further reduced by stratification of the water column, which is more pronounced there than in the transition and upwelling regions. This point has been confirmed by observations of the vertical profiles of dissolved iron [Mackey et al., 2002; Slemons et al., 2010]. Thus, concentrations of dissolved iron are very low throughout the euphotic zone, and the iron supply could limit primary production in the western equatorial Pacific. [40] We found enhanced primary production at 60 m depth during the strong El Niño (Figure 6b). Mackey et al. [2002] reported on the vertical profiles of dissolved iron in the same region 4 months before our observations. Elevation of the thermocline was apparent during both our study and that of Mackey et al. [2002]: the mechanism has been defined by McPhaden [1999] as shoaling of a 20 C-isotherm. However, Mackey et al. [2002] found consistently low concentrations of dissolved iron from the surface to a depth of 100 m. In addition, the EUC remained well below the euphotic zone during our observation period [Ryan et al., 2002]. This observation stands in contrast to the enhanced primary production that we recorded at a depth of 60 m (Figure 6b). Taken together, these findings suggest that the observed enhancement of primary production is associated with the upward supply of macronutrients, rather than with the supply of dissolved iron. 5. Conclusions [41] Primary production showed substantial regional variations between the WPWP region and the upwelling region of the equatorial Pacific, and the variations were associated with differences in nutrient availability. The progress of El Niño reduced primary production at the central and eastern equatorial Pacific owing to the eastward advection of the nitrate-depleted WPWP water [Chavez et al., 1999], but it enhanced primary production concurrently at subsurface layers in the WPWP region. This was attributed to the elevated nitrate availability at the 4% to 5% light depths, or shallower layers. [42] Intraseasonal forcing, for example by wind, occasionally superseded the effect of large-scale climatic forcing on primary production. When the thermocline shoaled in the WPWP region during the strong El Niño, increased phosphate and nitrate concentrations in the surface were detected. This indicated that shoaled nutrient-rich water was brought into the surface mixed layer through turbulent vertical mixing during episodic strong wind events. As a natural consequence, this increase in nutrient availability should enhance primary production, but the enhancement was not detected at the surface in our observations, probably because the enhancement was an occasional event of short duration. [43] Acknowledgments. We thank I. Asanuma, T. Kawano, the captains, and crew members of the research vessels Kaiyo and Mirai, for their cooperation at sea. Thanks are also due to the staff of Nippon Marine Enterprises, Ltd., Marine Works Japan Co., Ltd., and Global Ocean Development, Inc. for their logistic assistance during cruises. References Ando, K., and M. J. McPhaden (1997), Variability of surface layer hydrography in the tropical Pacific Ocean, J. Geophys. Res., 102(C10), 23,063 23,078, doi: /97jc Barber, R. T., and F. P. Chavez (1983), Biological consequences of El Niño, Science, 222, , doi: /science Barber, R. T., M. P. Sanderson, S. T. Lindley, F. Chai, J. Newton, C. C. Trees, D. G. Foley, and F. P. Chavez (1996), Primary productivity and its regulation in the equatorial Pacific during and following the El Niño, Deep Sea Res. Part II, 43(4 6), , doi: / (96) Blanchot, J., and M. Rodier (1996), Picophytoplankton abundance and biomass in the western tropical Pacific Ocean during the 1992 El Niño year: Results from flow cytometry, Deep Sea Res. Part I, 43(6), , doi: / (96)00026-x. Cavender-Bares, K. K., E. L. Mann, S. W. Chisholm, M. E. Ondrusek, and R. R. Bidigare (1999), Differential response of equatorial Pacific phytoplankton to iron fertilization, Limnol. Oceanogr., 44(2), , doi: /lo Chavez, F. P., P. G. Strutton, G. E. Friederich, R. A. Feely, G. C. Feldman, D. G. Foley, and M. J. 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