Abundances and distributions of picoplankton populations in the central equatorial Pacific from 12°N to 12°S, 140°W

Deep-Sea

Pergamon

PII: SO967~645(96)00018-5

Research

II. Vol. 43. No. 46. pp. 871-890. 1996 Copyright D 1996 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0967+)615/96 $15.00+0.00

Abundances and distributions of picoplankton populations in the central equatorial Pacific from 12”N to 12”S,14O”W MICHAEL

R. LANDRY,*

JULIE KIRSHTEIN*

and JOHN CONSTANTINOU*

(Received 2 1 July 1994; in revisedform 18 April 1995; accepted 7 January 1996)

Abstract-Abundances and distributions of picoplankton were studied on two cross-equatorial transect cruises (12”N, 14o”W-12”S, 135”W) during February-March (TT007) and AugustSeptember 1992 (TTOl 1). Samples were collected in the upper 200 m from early-morning and lateafternoon hydrocasts at 15 stations on each cruise (60 depth profiles, 820 samples). Populations of heterotrophic bacteria, Prochlorococcus, Synechococcus and small autotrophic eukaryotes were enumerated by dual-beam flow cytometry. At the northern end of the transect (7-12”N), abundances and vertical distributions were similar to those reported for the oligotrophic North Pacific gyre, with Prochlorococcus and heterotrophic bacteria dominating in the upper euphotic zone, and Synechococccus and eukaryotes exhibiting peaks in cell abundance at depth. All populations were abundant throughout the euphotic zone close to the equator and at the southern end of the transect. Heterotrophic bacteria and Synechococcus were generally more abundant in late-afternoon hydrocasts. The die1 enhancement followed the temporal pattern in beam c and suspended particulates, and was particularly strong in the equatorial upwelling region where it averaged 13.6% of the morning population for heterotrophic bacteria and 22.3% for Synechococcus. Conservative estimates of daily growth rates from these data are 0.25 and 0.40 day-i, respectively, for the two populations. Near-surface maxima in heterotrophic bacteria were symmetrical around the equator, centered around 5”s and 5”N. Prochlorococcus was most abundant during local summer conditions at the respective ends of the transect. A minimum occurred in association with a dense aggregation of buoyant diatoms at the convergent front of a tropical instability wave (2”N, TTOl 1). The ratio of Prochlorococcus to total bacteria was generally in the range of O.lH.2 for the upper water column, but varied during TTOl 1 from > 0.3 for the most northern stations to ~0.1 at the 2”N front. At higher latitudes, Synechococcus was more numerous during El Nifio conditions (TTO07) on both sides of the equator and at southern stations on both cruises. Autotrophic eukaryotes were more abundant during local winters at the ends of the transect and during the “cold tongue” conditions (TTOl 1) at the equator. Picoplankton account for most of the chlorophyll biomass and primary production in the central equatorial Pacific. Nonetheless, their abundances and distributions are relatively stable and conservative while other populations, such as diatoms, respond more dramatically to environmental forcing. Copyright 8 1996 Elsevier Science Ltd

INTRODUCTION Although plankton of extremely small size are now widely recognized as dominating biomass, production and metabolic activity in the open oceans (e.g. Williams, 198 1; Azam et al., 1983; Li et al., 1983; Takahashi and Bienfang, 1983; Murphy and Haugen, 1985; Iturriaga and Mitchell, 1986) the abundances and distributions of these organisms are still far from understood. Progress in this area has proceeded in rapid spurts with the introduction and refinement of new tools. Epifluorescence microscopy, for instance, *Department

of Oceanography,

University

of Hawaii at Manoa, 871

1000 Pope Road,

Honolulu,

HI 96822, U.S.A.

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et al

allowed direct enumeration of bacteria (e.g. Hobbie et al., 1977) enabled the discovery of ubiquitous coccoid cyanobacteria (Waterbury et al., 1979; Davis et al., 1985; Murphy and Haugen, 1985) and distinguished populations of autotrophic and heterotrophic flagellates (Davis and Sieburth, 1982; Haas, 1982; Booth, 1987). On the other hand, vast populations of photosynthetic bacteria (new genus Prochlorococcus) were entirely unknown, and in fact confounded with heterotrophic bacteria, until discovered with flow cytometry (Chisholm et al., 1988, 1992). Only recently (e.g. Olson et al., 1990a, 1990b; Monger and Landry, 1993) have the sensitivity and techniques of flow cytometry advanced to the point where the approach can provide precise quantitative assessments of four major groups of open ocean picoplankton-heterotrophic bacteria, Prochlorococcus spp., Synechococcus spp. and small autotrophic eukaryotes. This latter group overlaps the formal 2-pm size separation between pica- and nanoplankton and has been variously referred to as the picoeukaryotes (Campbell and Vaulot, 1993) the nanoeukaryotes (Landry et al., 1995b) and the eukaryotic ultraplankton (e.g. Li and Wood, 1988; Li et al., 1993). The JGOFS Equatorial Study (EqPac) provided a significant opportunity for understanding the distributional patterns and relationships among picoplankton populations across a major environmental gradient in the tropical open ocean. Not only were cross-equatorial transect cruises undertaken seasonally with a large supporting array of complementary biological, chemical and physical measurements, the cruises also occurred during classic El Nifio and “cold-tongue” phases, representing the extremes in regional environmental variability. In the present study, dual-beam flow cytometric techniques are used to elucidate abundances and distributions of picoplankton populations in the central equatorial Pacific.

MATERIALS

AND

METHODS

Sample collection Samples for analyses of picoplankton populations were collected on EqPac cruises TT007 (February-March 1992) and TTOl 1 (August-September 1992) along a 15-station transect from 12”N to 12”s. Stations between 12”N and 5’S (12”, 9”, 7”, 5”, 3”, 2” and IoN, O”, 1”. 2”, 3” and 5’S) were nominally on longitude 14O”W. The remaining three stations diverged progressively to the east (7% 138.5”W; 9”S, 137.2”W; and 12”S, 135”W) to minimize the influences of the South Pacific islands. Samples were collected from routine hydrocasts using a CTD rosette sampler with 10-l Niskin bottles. For most stations, 3-ml samples for flow cytometric analysis (FCM) were taken from an early-morning cast (approximately 06:00-07:OO h) and a late-afternoon cast (approximately 17:00-18:00 h). Sampling depths were fixed at 10-m intervals from the surface to 120 m, with additional samples from 150 and 200 m. The FCM samples were preserved in cryogenic tubes with a final concentration of 0.9% paraformaldehyde (filtered and adjusted to pH 7.4 before each use). Samples were frozen in liquid nitrogen and stored at -85°C until analysis (Vaulot et al., 1989). Flow cytometric analyses Frozen samples final concentration)

were thawed and stained in the dark with Hoechst 33342 (0.8 pg ml-’ for 1 h before analysis of picoplankton populations (Monger and

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Landry, 1993). Subsamples of 100 ~1 were enumerated on a Coulter EPICS 753 flow cytometer equipped with dual argon lasers and MSDS II automatic sampling. The lasers were aligned colinearly with the first laser tuned to the UV range at 200 mW to excite Hoechst-stained DNA. The second was tuned to the 488 nm at 1.3 W to excite the pigment molecules of autotrophic cells. Sensitivity of the optical system was enhanced with the use of a Biosense flow cell and focusing the laser beams through confocal lens assemblies (e.g. Olson et al., 1990a, 1990b). Fluorescence signals and right-angle light scatter (RALS) were collected with asperic pick-up lenses, split into colors (red, orange and blue) by dichroic filters and directed to photomultiplier tubes (for a more detailed description of system set-up see Monger and Landry, 1993). List-mode files were transferred to a microcomputer and analyzed on CYTOPC software (Vaulot, 1989). Correction factors were applied to raw data to correct for dilution of samples by paraformaldehyde and stain. Counting efficiency of the flow cytometer was calibrated as a function of cell density using E. coli cells enumerated with an Elzone/ Celloscope 8OXY. Populations of heterotrophic bacteria, Prochlorococcus, Synechococcus and small eukaryotic algae were distinguished by characteristic autofluorescence, size (RALS) and the presence of DNA. Synechococcus cells were identified principally by their orange fluorescence (575 nm k40 d.f.; phycoerythrin) but were also separate from the distributions of other populations in scatterplots of red (680 nm f40 d.f.; chlorophyll) vs blue (450 nm +40 d.f.; DNA) florescence. Among the smaller bacteria, Prochlorococcus were distinguished from heterotrophic cells by the presence of red autofluorescence. Heterotrophic bacteria contained no red fluorescence, but fluoresced blue from the Hoechst-stained DNA (Monger and Landry, 1993). Eukaryotic algae stood out as having substantially larger RALS (a function of size and refractive index) and red chlorophyll fluorescence compared with the bacterial populations.

Contour plots

Population abundances from multiple depth profiles at a given station (generally morning and evening samples) were averaged before contouring. Files were gridded according to the Kriging method, and contour maps were created using the program SURFER (version 4).

RESULTS Picoplankton abundances were enumerated in 820 samples comprising 60 depth profiles (30 profiles from each of the two cruises). The magnitude of the dataset precludes detailed scrutiny of subtle differences among samples taken at different stations, depths, times of day and seasons for the four populations of interest. The present analysis therefore is limited to major features. A subset of depth profiles (Figs l-3) illustrates characteristic distributional patterns in the equatorial upwelling zone relative to subtropical stations, as well as some of the differences observed between morning and evening sample collections and seasonal cruises. Time of day differences are further explored from depth-averaged abundances (Figs 4 and 5). Lastly, transect contour plots and depth-integrated abundances (Figs 6-10) show the latitudinal differences in abundance patterns between cruises. The full dataset from the U.S. JGOFS Data Management Office via the World Wide Web (http://wwwl.whoi.edu/ jgofs.html).

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Fig.

1.

Depth

plankton abundances for heterotrophic bacteria (H-BACT), and small autotrophic eukaryotes (A-EUK) in the upper 200 m of the water column at 12”N, 14O”W. Upper profiles are for TT007; bottom profiles for TTOl 1, Dates and times of sample collections are noted in boxed legends. Open symbols are for early-morning profiles: dark symbols are late-afternoon+arly-evening profiles. Proddorococcus,

Characteristic

profiles

et al.

of

Synechococcus

depth profiles

Stations at the northern end of the 14O”W transect were distinguished by relatively strong and deep maxima in the depth distributions of all analyzed populations. Profiles from 12”N (Fig. 1) are representative of this pattern, which was also well developed in profiles at 9”N but not at 7”N. At 12”N, near-surface abundances of 5 x 105-6 x 10’ heterotrophic bacteria per ml were relatively constant in the top 50 m before increasing by at least 10’ cells ml-’ in subsurface maxima at 70 m on TT007 and at 80-100 m on TTOl 1. Bacterial densities dropped off rapidly below the maxima to about 1 x 105-2 x 105cellsml-1 at 200 m. Prochlorococcus were more numerous in surface waters at 12”N during TTOll than TT007 (2.3 x 10’ vs 1.6 x 10’ cells ml-‘), but the depth distributions showed similar broad maxima in the range of 40-70 m. In both cases the maxima were at least 20 m above those for heterotrophic bacteria. The subsurface maxima for Synechococcus (60-70 m on TT007 and 7&80 m on TTOl 1) were typically slightly above that for heterotrophic bacteria and slightly below that for Prochlorococcus. In contrast, the peak density for autotrophic eukaryotes (7&80m on TT007 and 90-100 m on TTOll) was the deepest of the four population analyzed and generally about 10m below the maximum for heterotrophic bacteria. In addition, while the deep maxima for heterotrophic bacteria and Prochlorococcus

Picoplankton populations in the equatorial Pacific

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Depth profiles of plankton abundances at l”N, 14O”Wduring TT007 (upper panels) and TTOl 1 (lower panels) cruises. Abbreviations and symbols as in Fig. 1.

represented an increase of only 15-25% over surface concentrations, the deep maxima were major population centers for Synechococcus and eukaryotes, with cell densities many times higher than those observed in surface waters. Depth profiles in the equatorial region (5”N-5”s as represented by the collections from 1”N; Fig. 2) showed high population densities of all picoplankton populations in nearsurface waters. Where subsurface maxima occurred, they were more subtle and closer to the surface than at 12”N, and they also tended to be somewhat ephemeral. At l”N, heterotrophic bacteria were more or less uniformly distributed from the surface to 70100 m. Prochlorococcus, Synechococcus and eukaryotes exhibited no subsurface maxima in early-morning samplings; however, evening profiles showed well-developed subsurface peaks. In contrast to the profiles from 12”N, peak Synechococcus (about 20 m) abundance was higher in the water column than the peak for Prochlorococcus (30-40 m). If the distributions of populations were symmetrical around the equator, we would expect depth profiles at the southern end of the transect (12”s) to be similar to those at 12”N. This was not the case. In fact, the distributions at 12”s appeared to be in most respects an extension of the patterns observed in the equatorial upwelling zone. Population abundances of Synechococcus and eukaryotic picoplankton were high in the surface waters and did not exhibit the pronounced abundance peaks at depth characteristic of the northern gyre stations (Fig. 3). Among the populations enumerated, only the Prochlorococcus profiles for TTOl 1 showed consistent and significant deep maxima (70-80 m). The patterns for 12”N

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Fig. 3.

Depth profiles of plankton abundances at 12% TTOl 1 (lower panels) cruises. Abbreviations

135”W during TT007 (upper panels) and and symbols as in Fig. 1.

and 12”s were similar in one respect, however, as neither exhibited large differences in morning-evening population abundances which was a common feature of the profiles from around the equator (Fig. 2). Sampling

variability

such as heterotrophic bacteria and with high cell densities, the analytical precision for our flow cytometric estimates of abundance is on the order of + l-2% (Monger and Landry, 1993). For less numerous populations, such and the eukaryotic algae, standard deviations of f 3-7% of the sample as Synechococcus mean are typical for count estimates (e.g. Landry et al., 1993). Errors of these magnitudes are associated with subsampling and machine counting, and are expected to apply to the abundance estimates from individual samples. In order to estimate the errors associated with population abundance estimates for given stations and depths on the sampling transect, we determined the mean coefficient of variation based on the data from the upper 80 m of the water column from morning and evening profiles. This approach incorporates systematic differences in morning-evening abundances (see below) as part of sampling variability and thus exaggerates the error expected from replicated hydrocast samples taken closer together in time. Even so, the mean coefficients of variation (6.9%-heterotrophic bacteria, 9.5%-Prochlorococcus, 15.5%Synechococcus, 14.0%-eukaryotic algae) were relatively modest. Corresponding median For

populations

Prochlorococcus,

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in the equatorial 1.61

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877

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Fig. 4. Comparison of mean abundances of Prochlorococcus and autotrophic eukaryotes (A-EUK) in early-morning (open symbol) and late-afternoon (closed symbol) hydrocasts for cross-equatorial transect stations from 12”N, 14O”W to 129, 135”W. Mean abundances are the depth-integrated averages from the surface to 200 m. TT007 results are on the left-hand side; TTOl 1 results are on the right.

coefficients populations, Between

of variation were + 5.6, 7.8, 13.0 and 12.1% of sample means for the four respectively. cruises, mean sample variability was slightly lower for bacteria and Synechococcus on TTOl 1 and slightly higher for Prochlorococcus and eukaryotes. However, only the coefficient of variation for eukaryotes deviated between cruises by more than 1% from the overall mean. Within different hydrographic regions on the transect, the coefficients of variation for bacteria (+ 5.3%) and Prochlorococcus (f 8.3%) were less

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Fig. 5. Comparison of mean abundances of heterotrophic bacteria (H-BACT) and Synechococcus in early-morning (open symbol) and late-afternoon (closed symbol) hydrocasts for cross-equatorial transect stations from 12”N, 14O”W to 12”S, 135”W. Mean abundances are the depth-integrated averages from the surface to 200 m. TT007 results are on the left-hand side; TTOl1 results are on the right.

for waters to the north and south of the equator (5-12”N; 5-12”s) compared with the equatorial upwelling zone (3”N-3”s; + 8.5X-bacteria, + 10.7%-Prochlorococcus). Moreover, the patterns of variability appeared to differ somewhat between these regions. For example, at the more northern latitudes highest variability was often concentrated near the deep abundance peaks due to the influence of internal waves (e.g. Fig. 1). We did not correct for wave displacement of peak depth by normalizing to distributions to gt. Within the equatorial region, population abundance in the upper water column often shifted

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Fig. 6. Contour plots of population abundances (cells ml-‘) for heterotrophic bacteria along a cross-equatorial transect from 12”N, 14O”W to 12”S, 135”W. The top panel is from TT007 (February-March 1992); the lower panel is from TTOl 1 (August-September 1992).

Latitude (degrees north)

-1

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Fig. 7. Contour plots of population abundances (cells ml-‘) for Prochlorococcus along a crossequatorial transect from 12”N, 14O”W to 12”S, 135”W. The top panel is from TTOO7 (FebruaryMarch 1992); the lower panel is from TTOl 1 (August-September 1992).

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Latitude (degrees north)

Fig. 8. Contour plots of population abundances (cellsml-‘) for Synechococcus along a crossequatorial transect from 12”N, 14O”W to 125, 135”W. The top panel is from TT007 (FebruaryMarch 1992); the lower panel is from TTOl 1 (August-September 1992).

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Fig. 9. Contour plots of population abundances (cells ml-‘) for small autotrophic eukaryotes along a cross-equatorial transect from 12”N, 14o”W to 12”5, 135”W. The top panel is from TT007 (February-March 1992); the lower panel is from TTOll (August-September 1992).

Picoplankton

populations

in the equatorial

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Latitude (degrees north)

Fig. 10. Contour plots of population abundances (cellsml-‘) for the ratio of Prochlorococcus to total bacteria (Prochlorococctrs + heterotrophic bacteria) along a cross-equatorial transect from 12”N, 14O”W to 12”S, 135”W. The top panel is from TT007 (February-March 1992); the lower panel is from TTOl1 (August-September 1992).

uniformly to another level between hydrocasts (e.g. TT007 heterotrophic resulting in high variability at all depths.

bacteria in Fig. 2),

Abundances in morning vs evening profiles

Mean abundances for Prochlorococcus and autotrophic eukaryotes in the &200 m water column showed no consistent difference between early-morning and evening samplings (Fig. 4). In contrast, both heterotrophic bacteria and Synechococcus were generally present at higher abundances in the evening hydrocasts (Fig. 5). This pattern was evident, with a few exceptions, throughout the transect, but it was particularly strong in the 3”S-3”N equatorial region where 11 of 12 comparisons for bacteria and 12 of 12 for Synechococcus gave higher abundances in the evening. For heterotrophic bacteria, the mean (median) difference between morning and evening abundances in the equatorial region was 13.6% (12.5%) of the morning population. At higher northern and southern latitudes, this difference was 2.4% (3.9%). For Synechococcus, the disparity between morning and evening estimates represented 22.3% (26.3%) of the morning population in the equatorial region and 18.9% (16.6%) at the other stations. Population distributions on the cross-equatorial transect

Contour plots of heterotrophic bacteria showed lower near-surface abundances and subsurface population maxima at the northern latitudes (Fig. 6). Although the magnitudes

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of peak abundances varied between cruises, they were similarly distributed and more-or-less symmetrical around the equator with population maxima around 4-5”N and 45”s. The equatorial region represented a local bacterial minimum on both cruises, with the lowest concentration at 2”s. As seen previously in depth profiles (Fig. 3), the most southern stations lacked the deep maxima of the northern end of the transect. Highest abundances of Prochlorococcus were shifted more to the southern end of the transect on TT007 and to the northern end on TTOll (Fig. 7). Abundances in excess of 2.5 x lo5 cells ml-’ were noted at 9”N on TTOl 1. Local minima in Prochlorococcus occurred between 2”s and 2”N on both cruises. The most striking reduction in Prochlorococcus abundance was observed in stations around 2”N on TTOl 1. Synechococcus were present at low abundances on the northern end of the transect on both cruises (Fig. 8). As was the case for heterotrophic bacteria, local maxima of Synechococcus occurred in the vicinity of 3-5”s and 3-5”N. However, the highest density on TT007 ( > 2 x lo4 cells ml-‘) was found at 9”S, and a local maximum was noted at the equator on TTOl 1. Local minima occurred near the equator on TT007 and at 2”N on TTOll. Deep maxima in abundances of eukaryotic algae were a strong feature on the northern end of the transect on both cruises (Fig. 9). However, maxima at 70-80 m also were apparent between 3 and 5”s on TT007. In contrast to the pattern for Prochlorococcus, highest nearsurface abundances of eukaryotes occurred on the northern side of the transect on TT007 and the southern side on TTOll. In addition, a local maximum of > lo4 cells ml-’ was evident throughout the upper 60 m of the water column at the equator on TTOl 1.

Prochlorococcus

vs total bacterioplankton

Since the chlorophyll fluorescence of Prochlorococcus is generally too faint and fast fading to distinguish these autotrophic bacteria from heterotrophic forms by standard microscopy, Prochlorococcus are usually included in total epifluorescence bacterioplankton counts as if they were heterotrophic (e.g. Fuhrman et al., 1989; Cho and Azam, 1990). As noted by Campbell et al. (1994) this methodological problem has strongly biased the interpretation of biomass structure and growth rate potential in the open oceans by overstating the importance of heterotrophs relative to primary producers. Figure 10 shows spatial patterns in the ratio of Prochlorococcus abundance relative to the combined total of Prochlorococcus and heterotrophic bacteria across the equatorial transects on TT007 and TTOl 1. Throughout most of the upper 100 m of the water column on the two cruises, Prochlorococcus accounted for l&25% of the bacterioplankton abundance that would have resulted if the samples had been enumerated microscopically. For stations north of 7”N on TTOl 1, however, Prochlorococcus consistently accounted for 25-35% of total bacterial counts from the surface to 70-80 m. Samples from 2”N on the same cruise stand out as anomalously deficient in Prochlorococcus with less than 10% photosynthetic bacteria at all depths throughout the euphotic zone. Mean water-column

abundances

Depth-integrated means in population abundances are compared for the two cruises in Fig. 11. All populations had local minima near the equator (O”-2”s) on TT007 and substantially higher abundances at the equator on TTOl 1. Also, higher abundances tended

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Fig. 11. Latitudinal comparison ofmean abundances for populations of heterotrophic bacteria (HBACT), Prochlorococcus, Synechococcus and autotrophic eukaryotes during TT007 (FebruaryMarch 1992) and TTOll (August-September 1992). Mean abundances are the depth-integrated averages from the surface to 200 m. TT007 results are open symbols and light lines; TTOl 1 results are closed symbols and heavy lines.

to be distributed bimodally around the equator with local maxima in the vicinity of 3”N and 3”s on TT007 and 5”N and 5”s on TTOl 1. Mean abundances of heterotrophic bacteria were consistently higher on TTOl 1 from the northern end of the transect to 29, but higher for TT007 from 7” to 12”s. Over the extent of the transect, the abundance of heterotrophic bacteria was 15% higher during TTOl 1 than TT007. For stations north of YN, Prochlorococcus was 50-70% more abundant on TTOl 1 than

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TT007. The opposite was true between latitudes 1”N and 3”N. At 2”N, in particular, the mean population abundance during TTOl 1 was less than one-third of the density observed during TT007. Although the spatial distribution of Prochlorococcus abundance shifted substantially between cruises, there was only a 6% increase in total abundance during TTOl 1 from cell counts averaged over the whole transect. S~nechococcus showed only a 4% increase in total abundance and no clear difference in distributional pattern between cruises. In contrast, 13 of the 15 stations showed an increase in autotrophic eukaryotes during TTOll. Mean population abundances in excess of 5000 cells ml-’ were observed for the upper 200 m of the water column at the equator, more 1“N, 5”N and 5”s on TTOl 1, with the increase at each of these stations representing than a doubling in cell density relative to TT007. For all stations on the transect, autotrophic eukaryotes were 50% more abundant in August-September than in February-March 1992

DISCUSSION Importance

of Prochlorococcus

in tropical oceans

Despite the presence of excess macronutrients in surface waters of the equatorial Pacific, the region is similar to others in the tropical and subtropical open oceans in being dominated by phytoplankton of extremely small size. Chavez (1989) showed, for instance, that cells < 1 Llrn accounted for about 50-60% of chlorophyll standing stock and 50% of 14C primary production over broad expanses of the equatorial Pacific from 5”N to 5”s and from 90” to 18O”W. More than 80% of chlorophyll and primary production was not retained on 5-pm filters. During EqPac studies, 92% of chlorophyll a passed through 2-pm filters during cruises from February to April (TT007 and TT008), and 8 1% passed during the second set of cruises in August-October 1992 (TTOl 1 and TT012) (Bidigare and Ondrusek, 1996). Most previous studies of phytoplankton abundance and distributions in the equatorial Pacific have been conducted without the benefit of flow cytometric analyses and, thus, have missed an important part of the picoplankton community, Prochlorococcus. Although Prochlorococcus (about 0.7~pm spherical diameter; Chisholm et al., 1988) are slightly smaller than Synechococcus (1 -pm diameter), their abundances are at least 1 (equatorial upwelling zone) and often 2 (oligotrophic stations) orders of magnitude greater than the probably accounts for most of the chlorophyll and latter. Thus, Prochlorococcus photosynthetic activity observed for the smallest (< 1 pm) size fraction. In the one depth profile that we are aware of where Prochlorophytes have been enumerated in the equatorial Pacific, Chavez et al. (1991) observed a near-surface concentration (1.8 x lo5 cells ml- ‘) in July 1990 that was approximately the average of what we measured at the equator on the present cruises. Prochlorococcus are generally more numerous in the Pacific Ocean than in other regions where they have been studied. Campbell and Vaulot (1993) reported abundance ranging from 1.0 x lo5 to 2.7 x lo5 cells ml-’ throughout the euphotic zone at Station Aloha (22”45’N, 158”W) north of the Hawaiian Islands. Depth-integrated abundances of Prochlorococcus to 200 m are about a factor of 3 lower in the northwest Atlantic and in the Sargasso Sea off Bermuda (Olson et al., 1990a) and more than 1 order of magnitude lower in the Mediterranean Sea (Vaulot et al., 1990; Vaulot and Partensky, 1992). However, there are compensating higher concentrations of Synechococcus in these other regions

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(Campbell and Vaulot, 1993). The abundances and depth structure of Synechococcus are similar at the northern end of our transect (7-12”N) to those described for Station Aloha. The relative importance of Prochlorococcus, as a component of total bacteria (Fig. 10) and compared to Synechococcus, is also greatest and more like Station Aloha at these stations, which are the most oligotrophic on the transect in terms of macronutrient concentrations. The high abundances of Prochlorococcus and low abundance of Synechococcus in these areas suggest that Prochlorococcus is a superior competitor for remineralized nutrients such as ammonium, which is consistent with recent findings that Synechococcus has a strong physiological response to nitrate (Kremer and Schreier, 1994). Further to the south, through the region influenced by equatorial upwelling and even to 12”S, the picoplankton community structure has characteristics of both the oligotrophic North Pacific and the subtropical North Atlantic. Specifically, both Prochlorococcus and Synechococcus are abundant, with high densities extending throughout the euphotic zone. The lowest near-surface abundances of Prochlorococcus in this study were observed in the vicinity of 2”N on TTOl 1 (Fig. 7). This location is interesting because it was the site of a major convergent front at the leading edge of a tropical instability wave, and it was a local area of accumulation of extremely high abundances of large buoyant diatoms (Yoder et al., 1994; Murray et al., 1994) Synechococcus densities also were somewhat depressed in this frontal area (Fig. 8), but heterotrophic bacteria were not (Fig. 6). In fact, the elevated subsurface concentrations of heterotrophic bacteria between 3” and 5”N on TTOll probably resulted from the subduction of phytoplankton debris and dissolved organic matter as richer water from the equatorial upwelling zone was overridden by more buoyant and oligotrophic waters from the north (Yoder et al., 1994). Seasonal and El Nifio influences

The EqPac Program was originally designed to compare ecosystem dynamics in the central equatorial Pacific during two seasons. The two transect cruises (TT007, FebruaryMarch; TTOl 1, August-September) coincided, respectively, with late-summer seasons in the southern and northern hemispheres. Seasonal interpretations are confounded, however, by the fact that the former cruise occurred during the peak of the 1992 El Nifio event and the latter took place during a period of “cold-tongue” or La Nina conditions. For the sake of discussion, we interpret seasonal influences as those that effect the distributions of populations in a seasonally consistent manner on both the northern and southern ends of the transect. Prochlorococcus provides the best example of such a seasonal trend for the data collected between 7” and 12”s and between 7” and 12”N. Over these latitudinal bands, mean water-column densities of Prochlorococcus were 69% higher on average in the north during the boreal summer (TTOl 1) and 19% higher on average in the south during the austral summer (TT007). Only the mean values at 9”s were slightly inconsistent with this pattern (Fig. 11). However, all of the stations between 7” and 12”s had consistently elevated densities of Prochlorococcus in the upper 30m during TT007, with mean summer abundances (2.2 x lo5 cellsml-‘) about 35% higher than mean winter densities (1.6 x 10’cells ml- ‘). The same was true for the northern stations, where nearsurface summer densities (2.4 x lo5 cells ml-‘) averaged 48% higher than winter densities (1.6 x lo5 cells ml-‘). Heterotrophic bacteria also showed a consistent increase in abundance in the summer at the northern and southern ends of the transect. Watercolumn averaged densities were about 14% higher in the south and 17% higher in the north

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during their respective summers. This pattern was also apparent in near-surface abundances at five of the six stations in this comparison, the exception being 7”N. The higher watercolumn averaged density at this station during summer was due to higher population abundances at depth. While near-surface abundances of Prochlorococcus and heterotrophic bacteria were generally higher during summer periods at the northern and southern ends of the transect, populations of autotrophic eukaryotes showed the opposite trend. For the northern stations, mean winter densities (1900 cellsml-‘) were 50% higher than summer densities (1200 cells ml-‘). For the southern stations, winter near-surface densities (5800 cells ml-‘) averaged 83% higher than summer densities (3200 cells ml- ‘). This seasonal trend was not apparent in water-column averaged abundances for the northern stations due to higher population densities at depth during the “cold tongue” period (TTOl 1, northern summer). In contrast to the other picoplankton populations, Synechococcus did not display a seasonal pattern in abundance. Mean water-column densities of Synechococcus were generally higher on both ends of the transect during the El Niiio (TT007) cruise, averaging 16% higher in the south and 160% higher in the north compared with TTOl 1. Near-surface abundances were consistently highest during TT007. In the south, mean densities during El Niiio (17,100 cells ml-‘) averaged 36% higher for the upper 30 m compared with “cold tongue” conditions (12,600 cells ml - ‘). In the north, TT007 abundances (4800 cells ml- ‘) were over 6 times higher than those during TTOl 1 (780 cells ml-l). Despite the latitudinal asymmetry in percentage increase, both northern and southern ends of the transect showed about a 4000 cell ml- ’ increase for Synechococcus in surface waters during El Nina conditions. As previously noted, water-column averaged abundances of heterotrophic bacteria and autotrophic eukaryotes were generally higher in the equatorial upwelling region during TTOl 1 (cold tongue) compared with TT007 (El Nifio). For the seven stations defining the equatorial zone between 3’S and 3”N, this was a consistent pattern in near-surface (O-30 m) densities for both populations. Densities of heterotrophic bacteria averaged 26% higher during TTOll (8.5 x 1O’cells ml-‘) than TT007 (6.7 x lo5 cells ml-‘). Near-surface abundances of eukaryotes during TTOll (8700 cells ml-‘) were 63% higher than during El Nifio conditions (5300 cells ml-l). No consistent pattern was evident in equatorial waters for either of the photosynthetic bacteria, but near-surface densities of Prochlorococcus were about 23% higher on average during El Nifio conditions (1.5 x 10’ vs 1.4 x 10’ cells ml-‘) while Synechococcus densities were 15% higher on average on the “cold tongue” cruise (15,000 vs 13,50Ocellsml-I). Considered together, the seasonal and El Niiio effects on picoplankton abundances suggest differences in population responses to environmental forcing. Prochlorococcus, for example, tend to be more abundant under conditions of greater oligotrophy (tropical summers, El Niiio conditions), consistent with the seasonal dynamics of Prochlorococcus in the subtropical North Atlantic and North Pacific (Olson et al., 1990a; Campbell and Vaulot, 1993). On the other hand, the higher densities of autotrophic eukaryotes during equatorial “cold tongue” conditions and local winters at higher latitudes are presumably due to the the greater availability of nutrients due to upwelling or storm mixing. Since Synechococcus also would be expected to respond to increased nutrient availability, however, the specific circumstances leading to its greater abundance during El Niiio conditions, particularly for the local southern summer during the height of the El Nifio, are unclear. In the North Atlantic, S_rnec/zococcus blooms occur when nutrients are more available during winter

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(Olson et al., 1990b). Lastly, because of their nutritional dependency on dissolved organics, heterotrophic bacteria should follow the biomass or activity of primary producers that are the ultimate source of DOM. This would appear to explain the higher bacterial abundances in the equatorial upwelling zone when primary production was elevated during the “cold tongue” cruise. Higher bacterial abundances at southern stations during El Nitio and local summer conditions (TT007) were coincident with higher densities of photosynthetic bacteria, but not of the eukaryotes, implying that the former were probably more important as primary producers in this region. Given that the transect cruises covered extremes in environmental variability due to seasons and ENS0 events, the differences among cruises are perhaps less surprising that the similarities. Most of the patterns discussed above reflect differences in abundance substantially less than a 50% increase from one cruise to the next; differences of a factor of 2 or more were rare. All things considered, picoplankton abundances and community structure seemed to be relatively conservative within zonal boundaries in this tropical, open ocean, ecosystem. In contrast, analyses of taxa-specific phytoplankton pigments and microscopical studies from these cruises have revealed that populations of larger eukaryotic phytoplankton, particularly diatoms, responded dramatically to the changes in environmental conditions (e.g. Bidigare and Ondrusek, 1996; see also Chavez et al., 1990). In the western tropical Pacific (165”E), moreover, Blanchot et al. (1992) observed factor of 4.7 and 3.2 increases in Synechococcus and microalgae, respectively, during non-El Nifio (1988) relative to El Nifio (1987) conditions. Die1 patterns in picoplankton abundances

The differences observed in the present study between abundances of heterotrophic bacteria and Synechococcus in morning and evening hydrocasts conform to the die1 patterns in suspended particulates and beam c described from EqPac time-series cruises (TT008, March-April 1992; TT012, September-October 1992) (Gardner et al., 1995; Walsh et al., 1995). Conservative estimates of the growth rates of these populations can be computed from the die1 differences in abundances and the following assumptions: (1) constant loss to grazers; and (2) all growth occurs between morning and evening samplings. Such computations give mean growth-rate estimates for bacteria of 0.25 day- ’ (generation time = 2.8 days) for the equatorial upwelling region and 0.05 day- ’ (generation time = 14 days) for the higher latitudes. For Synechococcus, the corresponding estimates are 0.40 and 0.35 day-’ (generation times = 1.7 and 2.0 days), respectively. The estimates for Synechococcus are at least a factor of 2 underestimates relative to growth rates estimates from dilution experiments (Landry et al., 1995a, 1995b). The growth estimates for bacteria from the more oligotrophic ends of the transects are in the range of those expected from studies of community biomass structure, which confound abundances of photosynthetic and heterotrophic bacteria (e.g. Fuhrman et al., 1989). It is therefore reasonable to expect that they are also low. Rates estimates from the equatorial region are relatively high, however, and, if true, show strongly enhanced growth potential for bacteria in this tropical, open ocean, system. Timing of the hydrocast profiles was, unfortunately, not appropiate for observing a consistent die1 difference the abundance of Prochlorococcus. Synchrony in Prochlorococcus cell division was observed to be extremely strong at the equator during EqPac time-series cruises TT008 and TT012 (Vaulot et al., 1995). It begins at depth in the late afternoon and

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gradually moves toward the surface. Cell division rates are maximum in the vicinity of 2040 m depth, where they correspond to approximately one doubling per day. The lateafternoon peak in subsurface abundances of Prochlorococcus (Fig. 2) is consistent with this pattern of synchronized cell division. We probably sampled part of the daily increase at depth and missed the later increase in surface abundance. Had comparative hydrocasts been done earlier in the afternoon and later in the evening, we presumably would have seen a change in cell abundances indicative of the true growth potential of this species.

CONCLUSIONS The results of the present study are consistent with the notion that picoplankters, particularly Prochlorococcus, are an extremely abundant and dominant component of the phytoplankton assemblages of open ocean ecosystems. While the evidence suggests that they account for most of the chlorophyll biomass and primary production even in the equatorial upwelling zone, their abundances and distributions are relatively stable and conservative while other populations, such as diatoms, respond more dramatically to environmental forcing. Nonetheless, individual populations of the picoplankton community demonstrate high levels of activity and growth on a daily basis which must be balanced by equally high losses to grazers and other sinks to maintain the populations in dynamic steady state. Acknnlc,/efl~~n?enr.r--This work was supported by NSF grants OCE 90-22117 and 93-15432. We gratefully acknowledge the efforts of J. Murray, R. Barber and the captain and crew of the R.V. Thomas G. Thompson in facilitating the collection of this data. This paper is contribution no. 195 from the U.S. JGOFS Program and no. 4117 from the School of Ocean and Earth Science and Technology, University of Hawaii at Manoa, Honolulu. U.S.A.

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