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Use of cyanobacterial pigments to characterize the ocean surface mixed layer in the western Pacific warm pool
Journal of Marine Systems 75 (2009) 245–252
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Journal of Marine Systems j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s
Use of cyanobacterial pigments to characterize the ocean surface mixed layer in the western Pacific warm pool Kazuhiko Matsumoto a,⁎, Kentaro Ando b a b
Mutsu Institute for Oceanography, Japan Agency for Marine–Earth Science and Technology, 690 Kitasekine, Sekine, Mutsu 035-0022, Japan Institute of Observational Research for Global Change, Japan Agency for Marine–Earth Science and Technology, 2-15, Natsushima, Yokosuka 237-0061, Japan
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Article history: Received 26 October 2007 Received in revised form 3 October 2008 Accepted 14 October 2008 Available online 26 October 2008 Keywords: Mixed layer Vertical mixing Turbulent kinetic energy Zeaxanthin Chlorophyll a Photoacclimation Equatorial Pacific
a b s t r a c t We collected biological and physical oceanographic data simultaneously from shipboard observations and mooring buoys in the Pacific equatorial warm pool during the 2002–2003 El Niño event and found that the vertical profiles of cyanobacterial pigments reflected the turbulent kinetic energy (TKE) better than did analyses of the mixed layer by temperature and salinity profiling. Zeaxanthin, an accessory pigment of cyanobacteria, was abundant and almost homogeneous in the warm pool within the surface mixed layer, although chlorophyll a concentrations were low. The intracellular content of chlorophyll a increases with increasing depth and decreasing light in a photoprotective response, but the zeaxanthin content does not change with depth. Hence, we hypothesized that the profile of the ratio of zeaxanthin to chlorophyll a would decrease with increasing depth if the water column were stable, without vertical mixing. On the contrary, vertically constant ratios would indicate vertical mixing. Our analysis using a numerical model showed a good agreement between profiles of these ratios and the profiles of TKE and supported the hypothesis. However, a comparative analysis of the zeaxanthin:chlorophyll a ratio profiles with mixed layer depth based on temperature and salinity data revealed two distinct patterns. In the first pattern, the ratio was uniform in the mixed layer when TKE was strong. In the second, the ratio decreased with increasing depth, even in the mixed layer, because of reduced TKE. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Cyanobacteria belong to the prokaryotic picophytoplankton, and are often abundant in oligotrophic open oceans (Campbell and Vaulot, 1993). They are predominant in the nitrate-depleted western Pacific warm pool (WPWP) overlying eutrophic deep water, and in one study accounted for 70% of total phytoplankton chlorophyll a (chl-a) in their size fraction (b2 μm) (Matsumoto et al., 2004). Cyanobacteria contain zeaxanthin as a major accessory pigment. Kana et al. (1988) showed that the high concentrations of zeaxanthin relative to chl-a in cyanobacteria when grown under high irradiance results from a photoprotective response. In addition, Moore et al. (1995) showed that intracellular chl-a content increases with decreasing irradiance levels, whereas ⁎ Corresponding author. Tel.: +81 175 45 1011; fax: +81 175 45 1079. E-mail address: [email protected] (K. Matsumoto). 0924-7963/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2008.10.007
zeaxanthin content does not. This suggests that the deep chl-a maximum observed in the equatorial Pacific is a function of increased chl-a/cell in response to decreases in irradiance with depth, rather than an increase in cell numbers (Chavez et al., 1996). The intracellular content of chl-a in cyanobacteria varies vertically through the water column because of adaptation of the photosynthetic apparatus to different light levels. Since cyanobacteria are dominant in the WPWP region, the chl-a contribution from other phytoplankton is minimal there. We hypothesized that the downward gradient in the zeaxanthin:chl-a ratio in cyanobacteria-dominated water would reflect the intracellular pigment content and serve as an indicator of the stability of the water mass. If the water column was stable, with no vertical mixing, the ratio should decline with depth. In contrast, if the water column was vertically well mixed by strong turbulence, the ratio should be uniform in the mixed layer. However, in this study we found a discrepancy between the mixed layer as indicated by the
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K. Matsumoto, K. Ando / Journal of Marine Systems 75 (2009) 245–252
pigment ratio profiles and the conventional mixed layer as determined from the temperature and salinity profiles. We performed a detailed analysis to compare these two views of the mixed layer, and we investigated the importance of the gradient of the zeaxanthin:chl-a ratio by performing a comparative analysis of the mixed layer properties and turbulent kinetic energy (TKE) in the WPWP region during the 2002–2003 El Niño event. 2. Methods We conducted a detailed comparative analysis of the mixed layer and TKE using data collected from the R/V Mirai between December 2002 and February 2003 (cruise MR02K06) in the western equatorial Pacific. The detailed description of the cruise and some data are available at the cruise data site (http://www.jamstec.go.jp/cruisedata/mirai/e/index.html). The lower boundary of the mixed layer and the upper boundary of the isothermal layer were computed on the basis of a net change criteria of 0.125 σθ and 0.5 °C from the surface density and temperature, respectively, and the barrier layer (BL) thickness was estimated as the interval between these two depths (Lukas and Lindstrom, 1991). The phytoplankton pigments chl-a and zeaxanthin were quantified by high performance liquid chromatography (HPLC) (Waters Corporation, Milford, Massachusetts, USA). Values for chl-a concentrations are the sums of chlorophyll a and divinyl chlorophyll a concentrations. TKE was simulated by using a one-dimensional numerical mixed layer model with a secondorder turbulent closure scheme (Noh and Kim, 1999; Matsuura, 2001) from 0.5- to 100 m depth, with a vertical resolution of 0.5 m and a time–step interval of 1 min. The turbulence, temperature, and salinity in the surface layer were simulated with the numerical model after it was initialized by using the observed current profile from an acoustic Doppler current profiler (ADCP) mooring and the vertically-interpolated temperature and salinity profiles as recorded by two TRITON buoys operated by JAMSTEC at 147°E and 156°E on the equator (http:// www.jamstec.go.jp/jamstec/TRITON/real_time/php/top.php; http://www.pmel.noaa.gov/tao/jsdisplay). The surface boundary conditions were given by the heat, freshwater, and momentum fluxes calculated by the bulk method (Fairall et al., 1996 for heat and freshwater fluxes; Kondo, 1975 for momentum flux) based on meteorological data recorded by the TRITON buoys every 10 min. The reliability of the model was confirmed by comparing the results of a series of simulations with actual observational data. The simulations were performed for the same days as the shipboard observations, which were carried out near the TRITON buoys during cruises from 2000 to 2004 (cruises MR00-K08, MR02-K01, MR02-K06, and MR04-K07, see cruise data site). Although the model is onedimensional, the simulated profiles of temperature and salinity from this model can reproduce the observed temperature and salinity from the TRITON buoy after running the simulation for a few days. This model can estimate TKE to identify the instantaneous mixing depth.
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3. Results 3.1. Hydrological conditions in the WPWP region during the 2002–2003 El Niño The WPWP, broadly characterized by high sea surface temperature (−28 °C) and low surface salinity (b35 psu), was advected eastward during the MR02-K06 cruise in association with the 2002–2003 El Niño event. This period during the cruise corresponded to the mature stage of the El Niño event (McPhaden, 2004). The eastern edge of the WPWP, characterized by a sharp salinity front (Maes et al., 2006), was clearly evident between 176°W and 170°W (Fig. 1a; note also the BL superimposed on Fig. 1). The 29 °C isotherm ascended westward from 165°E, although it stayed deep toward the east in the WPWP region (Fig. 1b). A deepening thermocline in the eastern WPWP region and shoaling in the western WPWP region were associated with the weakening trade winds along the equator during the El Niño (McPhaden, 2004). The surface mixed layer depth shoaled in both zonal directions from 165°E, and deepened again at 170°W, which corresponds to the equatorial upwelling region. In the eastern WPWP region, the shoaling of the mixed layer depth was probably due to heavy precipitation and the formation of salinity stratification near the surface (Ando and McPhaden, 1997; McPhaden, 2004). Thus the BL was thinner in the western WPWP region and thicker in the eastern WPWP region. Since a nitracline typically forms in the vicinity of the thermocline, the nitracline also shoaled in the western WPWP region (Fig. 1c), and nitrate was almost completely depleted in the surface isothermal layer throughout the WPWP region. 3.2. Profiles of the zeaxanthin:chl-a ratio and comparisons with the simulated TKE The vertical distribution of chl-a concentrations in the WPWP region showed a deep maximum (Fig. 1d). Because nitrate was almost completely depleted in the surface isothermal layer beyond the surface mixed layer here (Fig. 1c), the chlorophyll maxima formed in the vicinity of the thermocline and were closely associated with the nitracline. The depths of the chlorophyll maximum shoaled slightly toward the west of 165°E in accordance with the shoaling of the nitracline. The chl-a concentration decreased rapidly towards the surface, however zeaxanthin was found throughout the region almost uniformly in the isothermal layer (Fig. 1e). The observed zeaxanthin:chl-a ratios produced three typical profiles in the WPWP region (Fig. 2). At 156°E, in the western region with a thin BL, the mixed layer depth determined by conventional means was estimated as 48 m. However, the zeaxanthin:chl-a ratio, which should reveal whether the mixed layer water mass was circulating within the mixed layer, decreased with increasing depth in a steep gradient of 0.013 m− 1, from the surface down to 50 m (Fig. 2a). Thus, the nature of the mixed layer at 156°E, as determined by the ratio method, was different than that determined by the
Fig. 1. Vertical sections along the Equator of (a) salinity, (b) temperature, (c) nitrate, (d) chl-a, and (e) zeaxanthin. The thickness of the barrier layer between the mixed layer and the isothermal layer is indicated by the solid white lines superimposed on each panel. The region of the western Pacific warm pool (WPWP) is identified above the top panel. Dots indicate sampling depths.
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Fig. 2. Temperature (T), salinity (S), density (σθ), and nitrate (NO3) profiles (upper panels), and chl-a (◯), zeaxanthin (×), and zeaxanthin:chl-a ratio (●) profiles (lower panels) from equatorial stations at (a) 156°E, (b) 160°E, and (c) 175°E. Solid horizontal lines delineate the barrier layer.
conventional method. However, in the same region of thin BL, at 160°E, both methods for describing the mixed layer agreed. At 160°E, the conventionally determined mixed layer was above the thermocline at 64 m depth, and the zeaxanthin: chl-a ratio varied little between the surface and 50 m, with only a slight gradient of 0.001 m− 1 (Fig. 2b); the downward gradient of the ratio was calculated using the data from the top and bottom of the jagged profile in places like this where the ratio did not show a smooth downward curve. At 175°E in the eastern region of the WPWP where the BL was thick (Fig. 2c), the ratio showed a steep gradient below the shallow mixed layer within the BL. The efficiency of vertical mixing is reduced in a thick BL, and this restricts the entrainment of water from the thermocline into the surface mixed layer (Lukas and Lindstrom, 1991). Therefore, the ratio method verified that the water mass was stable with no vertical mixing as evidenced by the steep gradient (0.015 m− 1) within the thick BL between 30 and 80 m (Fig. 2c).
To confirm the robustness of the relationship between the zeaxanthin:chl-a ratio and the turbulence in the surface mixed layer, the gradients of the zeaxanthin:chl-a ratio were plotted against the mean TKE (Fig. 3). The profiles of the zeaxanthin: chl-a ratio were roughly characterized into two types depending on whether the ratios were vertically homogeneous or not. The downward gradients of the ratio were calculated within the surface mixed layer. The mean TKE values were calculated from the surface down to the minimum energy value (−10) in common log of TKE by using the results of the simulated TKE to the corresponding depths estimated from each of the ratio profiles. These ratio profiles were based on pigment samples collected from near the TRITON buoys during cruises from 2000 to 2004. There was a significant negative correlation (P b 0.05, n = 17) between the gradient of the zeaxanthin:chl-a ratio and the mean TKE (Fig. 3), indicating that a steep (slight) vertical gradient was associated with a weak (strong) turbulence energy.
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4. Discussion 4.1. Usefulness of cyanobacterial pigments in characterizing circulation within the mixed layer The zeaxanthin distribution in the WPWP region was fairly constant in the surface isothermal layer (Fig. 1e) suggesting that the vertical distribution of the cyanobacteria was roughly homogeneous from the surface to the isothermal depth. The chl-a profile peaked at the isothermal depth or below (Fig. 1d). Zeaxanthin should be a good indicator of the abundance of cyanobacteria in tropical regions because its intracellular content does not change even under high irradiance, although the intracellular chl-a content of cyanobacteria decreases with increasing irradiance (Kana et al.,1988; Moore et al.,1995). The downward decrease of the zeaxanthin:chl-a ratio is frequently observed in the western equatorial Pacific (Mackey et al., 1998; Higgins and Mackey, 2000) and it is generally accepted as a photoacclimation response of phytoplankton to increasing depth and decreasing light in stable, stratified water. In contrast, it is generally assumed that the ratio will be constant if the water mass is circulated by vertical mixing. The zeaxanthin profiles from this study indicate that the prokaryotic cyanobacteria Prochlorococcus and Synechococcus are abundant in the surface isothermal layer in the WPWP region (Fig. 1e). However, chl-a concentrations were very low in the surface isothermal layer, although they increased rapidly below this layer and formed a deep maximum. Because of the supply of nitrate from deeper water, the numbers of eukaryotic phytoplankton and cyanobacteria would increase at the deep chl-a maximum (Matsumoto et al., 2004). Since eukaryotic phytoplankton do not contain zeaxanthin, the increase in eukaryotes introduces an error into the ratio method of tracing vertical mixing. However, because there was no notable increase in eukaryotes in the nitrate-depleted surface mixed layer (Matsumoto et al., 2004), the downward
Fig. 3. Relationship between common log of TKE and the zeaxanthin:chl-a ratio gradient within the surface mixed layer.
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gradient of the zeaxanthin:chl-a ratio is applicable for identifying vertical mixing within the surface mixed layer in the WPWP region. Changes of intracellular chl-a content results from phytoplankton photoacclimation. The first response identified when irradiance levels change from high to low is an increase in the abundance of the messenger RNA that encodes the light-harvesting chlorophyll proteins; this response was detectable within 2 h prior to changes in intracellular chl-a content (LaRoche et al., 1991). Müller (2004) found that the zeaxanthin:chl-a ratio in cyanobacteria did not change within 2 h after exposure to higher irradiance, but it began increasing after 1 additional hour of exposure due to the decrease in chla content and stable zeaxanthin content. Based on these results, it appears that there is a time lag of a few hours between a transition in photostimulation and a change in the zeaxanthin:chl-a ratio. The response to the transition in irradiance level may appear in the zeaxanthin:chl-a ratio in a relatively short time, but it takes a few days until chl-a synthesis or regulation reaches a maximum, e.g. for diatoms (Post et al., 1984). Post et al. (1984) indicated that diatom cells entrained a light–dark cycle maintain a diel periodicity in chla content, but acclimation to overall changes in light levels takes a long time. This implies that photoacclimation is not completely achieved at night, and that the cells acclimate to the irradiance level to which they are exposed during daytime. Therefore, changes in the zeaxanthin:chl-a ratio will be intensified over several days if stratification is prolonged after vertical mixing is reduced, resulting in a steep downward gradient in the ratio. A steeper downward gradient, therefore, means that the water mass was stable for a longer time. The intracellular content of pigments for individual cells shows a diel oscillation simply due to dilution by cell division (Post et al., 1984), but this should not influence the concentration per unit of water volume. Many studies have found no change in the intracellular content of zeaxanthin with changes in light level (Kana et al., 1988; Moore et al., 1995; Müller, 2004; Six et al., 2004) However, it is possible that the intracellular content changes because Bidigare et al. (1989) found differences in zeaxanthin pigmentation with changes in the spectral quality of the irradiance. Moreover, Claustre et al. (2002) observed a diel oscillation of the zeaxanthin:chl-a ratio, which increased during daytime and decreased during the night. Such diel oscillations suggest that is it not simply cell division that is affecting intracellular pigment content, but that there are different mechanisms controlling the pigmentation of chl-a and zeaxanthin. These mechanisms may result in higher ratios during daytime than during the night, but this is not necessarily an obstacle to identifying the downward gradient in the ratio as long as the diel periodicity is synchronized vertically in the water column. The downward gradient of the zeaxanthin:chl-a ratio indicates whether the water column is stable or disturbed by vertical mixing in the surface mixed layer. If the water mass undergoes vertical mixing, the ratio would be homogeneous for the duration of the mixing. However, if the water mass is stable, the ratio would decrease with increasing depth and the gradient would gradually increase in steepness as long as the stability persisted. We believe it is better to measure the ratio during daytime, but not in the early morning to avoid the lag
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time in the pigmentation response to the changing photostimulation from dark to light. 4.2. Simulated TKE and the mixed layer during the 2002–2003 El Niño The negative correlation between the gradient of the zeaxanthin:chl-a ratio and the TKE (Fig. 3) supported our hypothesis that the slope of the downward gradient of the ratio was indicative of water mass stability. That is, a steep gradient in the ratio indicated stable water, without mixing, and a homogeneous ratio profile indicated vertical circulation within the mixed layer. However, we found a discrepancy between the nature of the mixed layer as determined by the conventional temperature and salinity method and that determined by our pigment-based method. In our hypothesis, the downward gradient of the zeaxanthin:chl-a ratio is an indicator of the vertical mixing. However on 2 January 2003 at 156°E, the surface mixed layer
depth as determined by conventional methods was 48 m, although the ratio decreased from the surface to 50 m with a steep gradient of 0.013 m− 1 (Fig. 2a). To investigate this contradiction, we simulated the profile of TKE. The simulations started at 0:00 UTC on 28 December 2002 using data from the TRITON buoy at 0°N, 156°E. On 31 December 2002, strong wind (daily average wind stress, 0.05 N m− 2) was observed at the TRITON buoy. Strong wind events generally result in deep vertical mixing (Lukas and Lindstrom, 1991), and the model indicated high TKE from the surface down to 50 m (Fig. 4a). The water mass was considered to be well mixed at that point. Surface winds were strong from 29 to 31 December 2002, but the wind forcing subsequently diminished after 1 January 2003 until the shipboard observations conducted on 2 January 2003 (daily average wind stress, 0.005 N m− 2). As a result, the simulated profile of TKE on 2 January 2003 indicated that strong energy was limited to near the surface (Fig. 4b). The vertical profile of the zeaxanthin:chla ratios revealed stable water without mixing on 2 January
Fig. 4. Results of one-dimensional model simulations. Simulated daily mean vertical profiles of temperature (solid line), salinity (dashed line), and common log of TKE (red dotted line) at 0°N, 156°E on (a) 31 December 2002; (b) 2 January 2003; and (c) 15 January 2003. Wind stresses observed by the TRITON buoy are shown above the simulated profiles.
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2003 (Fig. 2a); this was consistent with the profile of the simulated TKE, although the conventionally determined mixed layer calculation indicated a deeper mixed layer depth of 48 m. The mixed layer determined by temperature and salinity profiles on 2 January 2003 (Fig. 2a) suggested a continuation of the wind-driven vertical mixing seen on 31 December 2002, but analysis of the zeaxanthin:chl-a ratios indicated that vertical mixing had already ceased on 2 January 2003. The zeaxanthin:chl-a ratio analysis thus represented the true vertical structure of the mixing better than that determined by the conventional mixed layer analysis. The model also indicated high TKE at the same location on 15 January 2003 in a simulation initialized to the 11 January observational data from the TRITON buoy at 0°N, 156°E. Strong wind was again observed, and the simulation demonstrated strong TKE from the surface to 60 m (Fig. 4c). From shipboard observations, the zeaxanthin:chl-a ratio was relatively constant in the surface mixed layer on 15 January 2003 at 160°E, near the TRITON buoy (Fig. 2b). This indicated strong turbulence in the surface mixed layer. The depth of the conventionally determined mixed layer was also consistent with the strong turbulent depth at 160°E (Fig. 2b). This demonstrated good agreement in the profiles obtained from the conventional mixed layer analysis and from zeaxanthin:chl-a ratios. The ability of the model to reproduce water column conditions is validated by comparing the differences between observed and model-predicted temperature and salinity. The differences within the mixed layer (mean± SD) were only 0.19 ± 0.03 °C and 0.08 ± 0.01 psu on 2 January 2003 at 156°E, and 0.17 ± 0.22 °C and 0.23 ± 0.05 psu on 15 January 2003 at 156–160°E in Fig. 2a to b for observed profiles and Fig. 4b to c for simulated profiles, respectively. In addition, the model simulation confirmed that the water mass was being circulated within the surface mixed layer by strong wind forcing. The thick BL along the equator in the eastern part of the WPWP region is thought to reduce the efficiency of vertical mixing (Lukas and Lindstrom, 1991) and this water-column structure is maintained by the combined effects of air–sea interactions (Maes et al., 2006), ocean responses to wind and zonal pressure balances (Cronin and McPhaden, 2002), and the basin-scale zonal subduction of saltier waters below the fresher mixed layer (Lukas and Lindstrom, 1991). Therefore, the windinduced vertical mixing at the sea surface will be restricted to shallow depths, since these processes work to prevent the welldeveloped BL from being easily broken. Salinity increased vertically with increasing depth within the BL, which demonstrates a stable water column, without mixing (Fig. 2c). The zeaxanthin:chl-a ratio decreased with increasing depth at a steep gradient (0.015 m− 1) within the thick BL, as seen at 175°E (Fig. 2c), verifying the stability of the BL. Zonal wind weakened in the WPWP region after midDecember 2002 because the peak of the El Niño event began to wane at this time (McPhaden, 2004). This reduction in zonal wind leads to surface warming in accordance with reduced turbulent mixing and buoyancy flux. The weakened trade winds led to shoaling of the thermocline through reduced vertical mixing in the western region with a thin BL during El Niño. However, the deepening of the mixed layer, in response to the enhanced vertical mixing by strong wind forcing derived from the intermittent westerly winds, caused deepening of the top of thermocline (Fig. 2b). The zeaxanthin:
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chl-a ratio directly represents such impacts of vertical mixing on phytoplankton promptly in the tropical and subtropical oceans where cyanobacteria are dominant. 5. Conclusions Cyanobacteria are predominant in the WPWP. We investigated differences in the vertical gradients of the phytoplankton pigments chlorophyll a and zeaxanthin, which are found in cyanobacteria. Our analysis of vertical differences in the zeaxanthin:chl-a ratio revealed the following: 1. The ratio is highest at the surface because of the different mechanisms of photosynthetic adaptation of each pigment to irradiance. Intracellular chl-a content decreases under high irradiance at the surface, but zeaxanthin content remains relatively constant. 2. A profile of zeaxanthin:chl-a ratios that is uniform with depth can be an indicator of vertical mixing, and a ratio that decreases with increasing depth can indicate stability of the water column. 3. The conventionally determined mixed layer reflects the homogeneous vertical profiles of temperature and salinity that result from vertical mixing. However, we found particular situations in which the two mixed layer indicators did not agree. For these situations, the profile of the pigment ratios reflected the extent of TKE, which was verified by the numerical model simulations. Therefore, we propose that the downward gradient of the zeaxanthin:chl-a ratio exhibits a quicker response to vertical mixing, through photoacclimation, as compared with conventional mixed layer indicators which reflect earlier mixing events. This result presents a new aspect of the linkage between surface biological and physical processes. Acknowledgements The numerical model that we used was provided by T. Matsuura of the National Research Institute for Earth Science and Disaster Prevention (NIED), Japan. We thank K. Furuya and T. Kawano for their helpful advice and critical reading of the manuscript. We also acknowledge the captain and crew of R/V Mirai for their assistance. Many thanks are due to the staff of Marine Works Japan Co., Ltd., and Global Ocean Development, Inc., for their cooperation in the collection of samples and on-board analyses. References Ando, K., McPhaden, M.J., 1997. Variability of surface layer hydrography in the tropical Pacific Ocean. Journal of Geophysical Research 102 (C10), 23063–23078. Bidigare, R.R., Schofield, O., Prézelin, B.B., 1989. Influence of zeaxanthin on quantum yield of photosynthesis of Synechococcus clone WH7803 (DC2). Marine Ecology Progress Series 56, 177–188. Campbell, L., Vaulot, D., 1993. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep-Sea Research I 40 (10), 2043–2060. Chavez, F.P., Buck, K.R., Service, S.K., Newton, J., Barber, R.T., 1996. Phytoplankton variability in the central and eastern tropical Pacific. Deep-Sea Research II 43 (4–6), 835–870. Claustre, H., Bricaud, A., Babin, M., Bruyant, F., Guillou, L., Gall, F.L., Marie, D., Partensky, F., 2002. Diel variations in Prochlorococcus optical properties. Limnology and Oceanography 47 (6), 1637–1647.
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Cronin, M.F., McPhaden, M.J., 2002. Barrier layer formation during westerly wind bursts. Journal of Geophysical Research 107 (C12), 8020. doi:10.1029/2001JC001171. Fairall, C.W., Bradley, E.F., Rogers, D.P., Edson, J.B., Young, G.S., 1996. Bulk parameterization of air–sea fluxes for Tropical Ocean–Global Atmosphere Coupled–Ocean Atmosphere Response Experiment. Journal of Geophysical Research 101 (C2), 3747–3764. Higgins, H.W., Mackey, D.J., 2000. Algal class abundances, estimated from chlorophyll and carotenoid pigments, in the western Equatorial Pacific under El Niño and non-El Niño conditions. Deep-Sea Research I 47 (8), 1461–1483. Kana, T.M., Glibert, P.M., Goericke, R., Welschmeyer, N.A., 1988. Zeaxanthin and β-carotene in Synechococcus WH7803 respond differently to irradiance. Limnology and Oceanography 33 (6, part 2), 1623–1627. Kondo, J., 1975. Air–sea bulk transfer coefficient in diabatic conditions. Boundary-Layer Meteorology 9 (1), 91–112. LaRoche, J., Mortain-Bertrand, A., Falkowski, P.G., 1991. Light intensityinduced changes in cab mRNA and light harvesting complex II apoprotein levels in the unicellular chlorophyte Dunaliella tertiolecta. Plant Physiology 97 (1), 147–153. Lukas, R., Lindstrom, E., 1991. The mixed layer of the western equatorial Pacific Ocean. Journal of Geophysical Research 96, 3343–3357. Mackey, D.J., Higgins, H.W., Mackey, M.D., Holdsworth, D., 1998. Algal class abundances in the western equatorial Pacific: estimation from HPLC measurements of chloroplast pigments using CHEMTAX. Deep-Sea Research I 45, 1441–1468. Maes, C., Ando, K., Delcroix, T., Kessler, W.S., McPhaden, M.J., Roemmich, D., 2006. Observed correlation of surface salinity, temperature and barrier
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Journal of Marine Systems j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s
Use of cyanobacterial pigments to characterize the ocean surface mixed layer in the western Pacific warm pool Kazuhiko Matsumoto a,⁎, Kentaro Ando b a b
Mutsu Institute for Oceanography, Japan Agency for Marine–Earth Science and Technology, 690 Kitasekine, Sekine, Mutsu 035-0022, Japan Institute of Observational Research for Global Change, Japan Agency for Marine–Earth Science and Technology, 2-15, Natsushima, Yokosuka 237-0061, Japan
a r t i c l e
i n f o
Article history: Received 26 October 2007 Received in revised form 3 October 2008 Accepted 14 October 2008 Available online 26 October 2008 Keywords: Mixed layer Vertical mixing Turbulent kinetic energy Zeaxanthin Chlorophyll a Photoacclimation Equatorial Pacific
a b s t r a c t We collected biological and physical oceanographic data simultaneously from shipboard observations and mooring buoys in the Pacific equatorial warm pool during the 2002–2003 El Niño event and found that the vertical profiles of cyanobacterial pigments reflected the turbulent kinetic energy (TKE) better than did analyses of the mixed layer by temperature and salinity profiling. Zeaxanthin, an accessory pigment of cyanobacteria, was abundant and almost homogeneous in the warm pool within the surface mixed layer, although chlorophyll a concentrations were low. The intracellular content of chlorophyll a increases with increasing depth and decreasing light in a photoprotective response, but the zeaxanthin content does not change with depth. Hence, we hypothesized that the profile of the ratio of zeaxanthin to chlorophyll a would decrease with increasing depth if the water column were stable, without vertical mixing. On the contrary, vertically constant ratios would indicate vertical mixing. Our analysis using a numerical model showed a good agreement between profiles of these ratios and the profiles of TKE and supported the hypothesis. However, a comparative analysis of the zeaxanthin:chlorophyll a ratio profiles with mixed layer depth based on temperature and salinity data revealed two distinct patterns. In the first pattern, the ratio was uniform in the mixed layer when TKE was strong. In the second, the ratio decreased with increasing depth, even in the mixed layer, because of reduced TKE. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Cyanobacteria belong to the prokaryotic picophytoplankton, and are often abundant in oligotrophic open oceans (Campbell and Vaulot, 1993). They are predominant in the nitrate-depleted western Pacific warm pool (WPWP) overlying eutrophic deep water, and in one study accounted for 70% of total phytoplankton chlorophyll a (chl-a) in their size fraction (b2 μm) (Matsumoto et al., 2004). Cyanobacteria contain zeaxanthin as a major accessory pigment. Kana et al. (1988) showed that the high concentrations of zeaxanthin relative to chl-a in cyanobacteria when grown under high irradiance results from a photoprotective response. In addition, Moore et al. (1995) showed that intracellular chl-a content increases with decreasing irradiance levels, whereas ⁎ Corresponding author. Tel.: +81 175 45 1011; fax: +81 175 45 1079. E-mail address: [email protected] (K. Matsumoto). 0924-7963/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2008.10.007
zeaxanthin content does not. This suggests that the deep chl-a maximum observed in the equatorial Pacific is a function of increased chl-a/cell in response to decreases in irradiance with depth, rather than an increase in cell numbers (Chavez et al., 1996). The intracellular content of chl-a in cyanobacteria varies vertically through the water column because of adaptation of the photosynthetic apparatus to different light levels. Since cyanobacteria are dominant in the WPWP region, the chl-a contribution from other phytoplankton is minimal there. We hypothesized that the downward gradient in the zeaxanthin:chl-a ratio in cyanobacteria-dominated water would reflect the intracellular pigment content and serve as an indicator of the stability of the water mass. If the water column was stable, with no vertical mixing, the ratio should decline with depth. In contrast, if the water column was vertically well mixed by strong turbulence, the ratio should be uniform in the mixed layer. However, in this study we found a discrepancy between the mixed layer as indicated by the
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pigment ratio profiles and the conventional mixed layer as determined from the temperature and salinity profiles. We performed a detailed analysis to compare these two views of the mixed layer, and we investigated the importance of the gradient of the zeaxanthin:chl-a ratio by performing a comparative analysis of the mixed layer properties and turbulent kinetic energy (TKE) in the WPWP region during the 2002–2003 El Niño event. 2. Methods We conducted a detailed comparative analysis of the mixed layer and TKE using data collected from the R/V Mirai between December 2002 and February 2003 (cruise MR02K06) in the western equatorial Pacific. The detailed description of the cruise and some data are available at the cruise data site (http://www.jamstec.go.jp/cruisedata/mirai/e/index.html). The lower boundary of the mixed layer and the upper boundary of the isothermal layer were computed on the basis of a net change criteria of 0.125 σθ and 0.5 °C from the surface density and temperature, respectively, and the barrier layer (BL) thickness was estimated as the interval between these two depths (Lukas and Lindstrom, 1991). The phytoplankton pigments chl-a and zeaxanthin were quantified by high performance liquid chromatography (HPLC) (Waters Corporation, Milford, Massachusetts, USA). Values for chl-a concentrations are the sums of chlorophyll a and divinyl chlorophyll a concentrations. TKE was simulated by using a one-dimensional numerical mixed layer model with a secondorder turbulent closure scheme (Noh and Kim, 1999; Matsuura, 2001) from 0.5- to 100 m depth, with a vertical resolution of 0.5 m and a time–step interval of 1 min. The turbulence, temperature, and salinity in the surface layer were simulated with the numerical model after it was initialized by using the observed current profile from an acoustic Doppler current profiler (ADCP) mooring and the vertically-interpolated temperature and salinity profiles as recorded by two TRITON buoys operated by JAMSTEC at 147°E and 156°E on the equator (http:// www.jamstec.go.jp/jamstec/TRITON/real_time/php/top.php; http://www.pmel.noaa.gov/tao/jsdisplay). The surface boundary conditions were given by the heat, freshwater, and momentum fluxes calculated by the bulk method (Fairall et al., 1996 for heat and freshwater fluxes; Kondo, 1975 for momentum flux) based on meteorological data recorded by the TRITON buoys every 10 min. The reliability of the model was confirmed by comparing the results of a series of simulations with actual observational data. The simulations were performed for the same days as the shipboard observations, which were carried out near the TRITON buoys during cruises from 2000 to 2004 (cruises MR00-K08, MR02-K01, MR02-K06, and MR04-K07, see cruise data site). Although the model is onedimensional, the simulated profiles of temperature and salinity from this model can reproduce the observed temperature and salinity from the TRITON buoy after running the simulation for a few days. This model can estimate TKE to identify the instantaneous mixing depth.
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3. Results 3.1. Hydrological conditions in the WPWP region during the 2002–2003 El Niño The WPWP, broadly characterized by high sea surface temperature (−28 °C) and low surface salinity (b35 psu), was advected eastward during the MR02-K06 cruise in association with the 2002–2003 El Niño event. This period during the cruise corresponded to the mature stage of the El Niño event (McPhaden, 2004). The eastern edge of the WPWP, characterized by a sharp salinity front (Maes et al., 2006), was clearly evident between 176°W and 170°W (Fig. 1a; note also the BL superimposed on Fig. 1). The 29 °C isotherm ascended westward from 165°E, although it stayed deep toward the east in the WPWP region (Fig. 1b). A deepening thermocline in the eastern WPWP region and shoaling in the western WPWP region were associated with the weakening trade winds along the equator during the El Niño (McPhaden, 2004). The surface mixed layer depth shoaled in both zonal directions from 165°E, and deepened again at 170°W, which corresponds to the equatorial upwelling region. In the eastern WPWP region, the shoaling of the mixed layer depth was probably due to heavy precipitation and the formation of salinity stratification near the surface (Ando and McPhaden, 1997; McPhaden, 2004). Thus the BL was thinner in the western WPWP region and thicker in the eastern WPWP region. Since a nitracline typically forms in the vicinity of the thermocline, the nitracline also shoaled in the western WPWP region (Fig. 1c), and nitrate was almost completely depleted in the surface isothermal layer throughout the WPWP region. 3.2. Profiles of the zeaxanthin:chl-a ratio and comparisons with the simulated TKE The vertical distribution of chl-a concentrations in the WPWP region showed a deep maximum (Fig. 1d). Because nitrate was almost completely depleted in the surface isothermal layer beyond the surface mixed layer here (Fig. 1c), the chlorophyll maxima formed in the vicinity of the thermocline and were closely associated with the nitracline. The depths of the chlorophyll maximum shoaled slightly toward the west of 165°E in accordance with the shoaling of the nitracline. The chl-a concentration decreased rapidly towards the surface, however zeaxanthin was found throughout the region almost uniformly in the isothermal layer (Fig. 1e). The observed zeaxanthin:chl-a ratios produced three typical profiles in the WPWP region (Fig. 2). At 156°E, in the western region with a thin BL, the mixed layer depth determined by conventional means was estimated as 48 m. However, the zeaxanthin:chl-a ratio, which should reveal whether the mixed layer water mass was circulating within the mixed layer, decreased with increasing depth in a steep gradient of 0.013 m− 1, from the surface down to 50 m (Fig. 2a). Thus, the nature of the mixed layer at 156°E, as determined by the ratio method, was different than that determined by the
Fig. 1. Vertical sections along the Equator of (a) salinity, (b) temperature, (c) nitrate, (d) chl-a, and (e) zeaxanthin. The thickness of the barrier layer between the mixed layer and the isothermal layer is indicated by the solid white lines superimposed on each panel. The region of the western Pacific warm pool (WPWP) is identified above the top panel. Dots indicate sampling depths.
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Fig. 2. Temperature (T), salinity (S), density (σθ), and nitrate (NO3) profiles (upper panels), and chl-a (◯), zeaxanthin (×), and zeaxanthin:chl-a ratio (●) profiles (lower panels) from equatorial stations at (a) 156°E, (b) 160°E, and (c) 175°E. Solid horizontal lines delineate the barrier layer.
conventional method. However, in the same region of thin BL, at 160°E, both methods for describing the mixed layer agreed. At 160°E, the conventionally determined mixed layer was above the thermocline at 64 m depth, and the zeaxanthin: chl-a ratio varied little between the surface and 50 m, with only a slight gradient of 0.001 m− 1 (Fig. 2b); the downward gradient of the ratio was calculated using the data from the top and bottom of the jagged profile in places like this where the ratio did not show a smooth downward curve. At 175°E in the eastern region of the WPWP where the BL was thick (Fig. 2c), the ratio showed a steep gradient below the shallow mixed layer within the BL. The efficiency of vertical mixing is reduced in a thick BL, and this restricts the entrainment of water from the thermocline into the surface mixed layer (Lukas and Lindstrom, 1991). Therefore, the ratio method verified that the water mass was stable with no vertical mixing as evidenced by the steep gradient (0.015 m− 1) within the thick BL between 30 and 80 m (Fig. 2c).
To confirm the robustness of the relationship between the zeaxanthin:chl-a ratio and the turbulence in the surface mixed layer, the gradients of the zeaxanthin:chl-a ratio were plotted against the mean TKE (Fig. 3). The profiles of the zeaxanthin: chl-a ratio were roughly characterized into two types depending on whether the ratios were vertically homogeneous or not. The downward gradients of the ratio were calculated within the surface mixed layer. The mean TKE values were calculated from the surface down to the minimum energy value (−10) in common log of TKE by using the results of the simulated TKE to the corresponding depths estimated from each of the ratio profiles. These ratio profiles were based on pigment samples collected from near the TRITON buoys during cruises from 2000 to 2004. There was a significant negative correlation (P b 0.05, n = 17) between the gradient of the zeaxanthin:chl-a ratio and the mean TKE (Fig. 3), indicating that a steep (slight) vertical gradient was associated with a weak (strong) turbulence energy.
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4. Discussion 4.1. Usefulness of cyanobacterial pigments in characterizing circulation within the mixed layer The zeaxanthin distribution in the WPWP region was fairly constant in the surface isothermal layer (Fig. 1e) suggesting that the vertical distribution of the cyanobacteria was roughly homogeneous from the surface to the isothermal depth. The chl-a profile peaked at the isothermal depth or below (Fig. 1d). Zeaxanthin should be a good indicator of the abundance of cyanobacteria in tropical regions because its intracellular content does not change even under high irradiance, although the intracellular chl-a content of cyanobacteria decreases with increasing irradiance (Kana et al.,1988; Moore et al.,1995). The downward decrease of the zeaxanthin:chl-a ratio is frequently observed in the western equatorial Pacific (Mackey et al., 1998; Higgins and Mackey, 2000) and it is generally accepted as a photoacclimation response of phytoplankton to increasing depth and decreasing light in stable, stratified water. In contrast, it is generally assumed that the ratio will be constant if the water mass is circulated by vertical mixing. The zeaxanthin profiles from this study indicate that the prokaryotic cyanobacteria Prochlorococcus and Synechococcus are abundant in the surface isothermal layer in the WPWP region (Fig. 1e). However, chl-a concentrations were very low in the surface isothermal layer, although they increased rapidly below this layer and formed a deep maximum. Because of the supply of nitrate from deeper water, the numbers of eukaryotic phytoplankton and cyanobacteria would increase at the deep chl-a maximum (Matsumoto et al., 2004). Since eukaryotic phytoplankton do not contain zeaxanthin, the increase in eukaryotes introduces an error into the ratio method of tracing vertical mixing. However, because there was no notable increase in eukaryotes in the nitrate-depleted surface mixed layer (Matsumoto et al., 2004), the downward
Fig. 3. Relationship between common log of TKE and the zeaxanthin:chl-a ratio gradient within the surface mixed layer.
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gradient of the zeaxanthin:chl-a ratio is applicable for identifying vertical mixing within the surface mixed layer in the WPWP region. Changes of intracellular chl-a content results from phytoplankton photoacclimation. The first response identified when irradiance levels change from high to low is an increase in the abundance of the messenger RNA that encodes the light-harvesting chlorophyll proteins; this response was detectable within 2 h prior to changes in intracellular chl-a content (LaRoche et al., 1991). Müller (2004) found that the zeaxanthin:chl-a ratio in cyanobacteria did not change within 2 h after exposure to higher irradiance, but it began increasing after 1 additional hour of exposure due to the decrease in chla content and stable zeaxanthin content. Based on these results, it appears that there is a time lag of a few hours between a transition in photostimulation and a change in the zeaxanthin:chl-a ratio. The response to the transition in irradiance level may appear in the zeaxanthin:chl-a ratio in a relatively short time, but it takes a few days until chl-a synthesis or regulation reaches a maximum, e.g. for diatoms (Post et al., 1984). Post et al. (1984) indicated that diatom cells entrained a light–dark cycle maintain a diel periodicity in chla content, but acclimation to overall changes in light levels takes a long time. This implies that photoacclimation is not completely achieved at night, and that the cells acclimate to the irradiance level to which they are exposed during daytime. Therefore, changes in the zeaxanthin:chl-a ratio will be intensified over several days if stratification is prolonged after vertical mixing is reduced, resulting in a steep downward gradient in the ratio. A steeper downward gradient, therefore, means that the water mass was stable for a longer time. The intracellular content of pigments for individual cells shows a diel oscillation simply due to dilution by cell division (Post et al., 1984), but this should not influence the concentration per unit of water volume. Many studies have found no change in the intracellular content of zeaxanthin with changes in light level (Kana et al., 1988; Moore et al., 1995; Müller, 2004; Six et al., 2004) However, it is possible that the intracellular content changes because Bidigare et al. (1989) found differences in zeaxanthin pigmentation with changes in the spectral quality of the irradiance. Moreover, Claustre et al. (2002) observed a diel oscillation of the zeaxanthin:chl-a ratio, which increased during daytime and decreased during the night. Such diel oscillations suggest that is it not simply cell division that is affecting intracellular pigment content, but that there are different mechanisms controlling the pigmentation of chl-a and zeaxanthin. These mechanisms may result in higher ratios during daytime than during the night, but this is not necessarily an obstacle to identifying the downward gradient in the ratio as long as the diel periodicity is synchronized vertically in the water column. The downward gradient of the zeaxanthin:chl-a ratio indicates whether the water column is stable or disturbed by vertical mixing in the surface mixed layer. If the water mass undergoes vertical mixing, the ratio would be homogeneous for the duration of the mixing. However, if the water mass is stable, the ratio would decrease with increasing depth and the gradient would gradually increase in steepness as long as the stability persisted. We believe it is better to measure the ratio during daytime, but not in the early morning to avoid the lag
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time in the pigmentation response to the changing photostimulation from dark to light. 4.2. Simulated TKE and the mixed layer during the 2002–2003 El Niño The negative correlation between the gradient of the zeaxanthin:chl-a ratio and the TKE (Fig. 3) supported our hypothesis that the slope of the downward gradient of the ratio was indicative of water mass stability. That is, a steep gradient in the ratio indicated stable water, without mixing, and a homogeneous ratio profile indicated vertical circulation within the mixed layer. However, we found a discrepancy between the nature of the mixed layer as determined by the conventional temperature and salinity method and that determined by our pigment-based method. In our hypothesis, the downward gradient of the zeaxanthin:chl-a ratio is an indicator of the vertical mixing. However on 2 January 2003 at 156°E, the surface mixed layer
depth as determined by conventional methods was 48 m, although the ratio decreased from the surface to 50 m with a steep gradient of 0.013 m− 1 (Fig. 2a). To investigate this contradiction, we simulated the profile of TKE. The simulations started at 0:00 UTC on 28 December 2002 using data from the TRITON buoy at 0°N, 156°E. On 31 December 2002, strong wind (daily average wind stress, 0.05 N m− 2) was observed at the TRITON buoy. Strong wind events generally result in deep vertical mixing (Lukas and Lindstrom, 1991), and the model indicated high TKE from the surface down to 50 m (Fig. 4a). The water mass was considered to be well mixed at that point. Surface winds were strong from 29 to 31 December 2002, but the wind forcing subsequently diminished after 1 January 2003 until the shipboard observations conducted on 2 January 2003 (daily average wind stress, 0.005 N m− 2). As a result, the simulated profile of TKE on 2 January 2003 indicated that strong energy was limited to near the surface (Fig. 4b). The vertical profile of the zeaxanthin:chla ratios revealed stable water without mixing on 2 January
Fig. 4. Results of one-dimensional model simulations. Simulated daily mean vertical profiles of temperature (solid line), salinity (dashed line), and common log of TKE (red dotted line) at 0°N, 156°E on (a) 31 December 2002; (b) 2 January 2003; and (c) 15 January 2003. Wind stresses observed by the TRITON buoy are shown above the simulated profiles.
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2003 (Fig. 2a); this was consistent with the profile of the simulated TKE, although the conventionally determined mixed layer calculation indicated a deeper mixed layer depth of 48 m. The mixed layer determined by temperature and salinity profiles on 2 January 2003 (Fig. 2a) suggested a continuation of the wind-driven vertical mixing seen on 31 December 2002, but analysis of the zeaxanthin:chl-a ratios indicated that vertical mixing had already ceased on 2 January 2003. The zeaxanthin:chl-a ratio analysis thus represented the true vertical structure of the mixing better than that determined by the conventional mixed layer analysis. The model also indicated high TKE at the same location on 15 January 2003 in a simulation initialized to the 11 January observational data from the TRITON buoy at 0°N, 156°E. Strong wind was again observed, and the simulation demonstrated strong TKE from the surface to 60 m (Fig. 4c). From shipboard observations, the zeaxanthin:chl-a ratio was relatively constant in the surface mixed layer on 15 January 2003 at 160°E, near the TRITON buoy (Fig. 2b). This indicated strong turbulence in the surface mixed layer. The depth of the conventionally determined mixed layer was also consistent with the strong turbulent depth at 160°E (Fig. 2b). This demonstrated good agreement in the profiles obtained from the conventional mixed layer analysis and from zeaxanthin:chl-a ratios. The ability of the model to reproduce water column conditions is validated by comparing the differences between observed and model-predicted temperature and salinity. The differences within the mixed layer (mean± SD) were only 0.19 ± 0.03 °C and 0.08 ± 0.01 psu on 2 January 2003 at 156°E, and 0.17 ± 0.22 °C and 0.23 ± 0.05 psu on 15 January 2003 at 156–160°E in Fig. 2a to b for observed profiles and Fig. 4b to c for simulated profiles, respectively. In addition, the model simulation confirmed that the water mass was being circulated within the surface mixed layer by strong wind forcing. The thick BL along the equator in the eastern part of the WPWP region is thought to reduce the efficiency of vertical mixing (Lukas and Lindstrom, 1991) and this water-column structure is maintained by the combined effects of air–sea interactions (Maes et al., 2006), ocean responses to wind and zonal pressure balances (Cronin and McPhaden, 2002), and the basin-scale zonal subduction of saltier waters below the fresher mixed layer (Lukas and Lindstrom, 1991). Therefore, the windinduced vertical mixing at the sea surface will be restricted to shallow depths, since these processes work to prevent the welldeveloped BL from being easily broken. Salinity increased vertically with increasing depth within the BL, which demonstrates a stable water column, without mixing (Fig. 2c). The zeaxanthin:chl-a ratio decreased with increasing depth at a steep gradient (0.015 m− 1) within the thick BL, as seen at 175°E (Fig. 2c), verifying the stability of the BL. Zonal wind weakened in the WPWP region after midDecember 2002 because the peak of the El Niño event began to wane at this time (McPhaden, 2004). This reduction in zonal wind leads to surface warming in accordance with reduced turbulent mixing and buoyancy flux. The weakened trade winds led to shoaling of the thermocline through reduced vertical mixing in the western region with a thin BL during El Niño. However, the deepening of the mixed layer, in response to the enhanced vertical mixing by strong wind forcing derived from the intermittent westerly winds, caused deepening of the top of thermocline (Fig. 2b). The zeaxanthin:
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chl-a ratio directly represents such impacts of vertical mixing on phytoplankton promptly in the tropical and subtropical oceans where cyanobacteria are dominant. 5. Conclusions Cyanobacteria are predominant in the WPWP. We investigated differences in the vertical gradients of the phytoplankton pigments chlorophyll a and zeaxanthin, which are found in cyanobacteria. Our analysis of vertical differences in the zeaxanthin:chl-a ratio revealed the following: 1. The ratio is highest at the surface because of the different mechanisms of photosynthetic adaptation of each pigment to irradiance. Intracellular chl-a content decreases under high irradiance at the surface, but zeaxanthin content remains relatively constant. 2. A profile of zeaxanthin:chl-a ratios that is uniform with depth can be an indicator of vertical mixing, and a ratio that decreases with increasing depth can indicate stability of the water column. 3. The conventionally determined mixed layer reflects the homogeneous vertical profiles of temperature and salinity that result from vertical mixing. However, we found particular situations in which the two mixed layer indicators did not agree. For these situations, the profile of the pigment ratios reflected the extent of TKE, which was verified by the numerical model simulations. Therefore, we propose that the downward gradient of the zeaxanthin:chl-a ratio exhibits a quicker response to vertical mixing, through photoacclimation, as compared with conventional mixed layer indicators which reflect earlier mixing events. This result presents a new aspect of the linkage between surface biological and physical processes. Acknowledgements The numerical model that we used was provided by T. Matsuura of the National Research Institute for Earth Science and Disaster Prevention (NIED), Japan. We thank K. Furuya and T. Kawano for their helpful advice and critical reading of the manuscript. We also acknowledge the captain and crew of R/V Mirai for their assistance. Many thanks are due to the staff of Marine Works Japan Co., Ltd., and Global Ocean Development, Inc., for their cooperation in the collection of samples and on-board analyses. References Ando, K., McPhaden, M.J., 1997. Variability of surface layer hydrography in the tropical Pacific Ocean. Journal of Geophysical Research 102 (C10), 23063–23078. Bidigare, R.R., Schofield, O., Prézelin, B.B., 1989. Influence of zeaxanthin on quantum yield of photosynthesis of Synechococcus clone WH7803 (DC2). Marine Ecology Progress Series 56, 177–188. Campbell, L., Vaulot, D., 1993. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep-Sea Research I 40 (10), 2043–2060. Chavez, F.P., Buck, K.R., Service, S.K., Newton, J., Barber, R.T., 1996. Phytoplankton variability in the central and eastern tropical Pacific. Deep-Sea Research II 43 (4–6), 835–870. Claustre, H., Bricaud, A., Babin, M., Bruyant, F., Guillou, L., Gall, F.L., Marie, D., Partensky, F., 2002. Diel variations in Prochlorococcus optical properties. Limnology and Oceanography 47 (6), 1637–1647.
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