Seasonal and interannual trends in heterotrophic bacterial processes between 1995 and 1999 in the subarctic NE Pacific

Deep-Sea Research II 49 (2002) 5775–5791

Seasonal and interannual trends in heterotrophic bacterial processes between 1995 and 1999 in the subarctic NE Pacific Nelson D. Sherry*, Behzad Imanian, Kugako Sugimoto, Philip W. Boyd1, Paul J. Harrison Department of Earth and Ocean Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 Received 25 April 2001; received in revised form 6 October 2001; accepted 6 January 2002

Abstract Heterotrophic bacterial abundance and productivity were measured in the euphotic zone over 4 years during winter, late spring, and late summer in the subarctic NE Pacific from September 1995 to February 1999. Sampling took place during 11 cruises at five hydrographic stations spaced along the east/west line-P transect from slope waters at P4 (1200 m depth) to the open-ocean waters at Ocean Station Papa (OSP) (4250 m depth). P4 exhibits a spring bloom and summer nutrient depletion, whereas OSP exhibits no spring bloom, consistently replete macronutrients, and iron limitation of primary productivity. Bacterial biomass, derived from cell abundance (assuming 10 fg C cell
1), ranged from an average of B6 mg C l
1 in the winter to 10 and 14 mg C l
1 in the spring and summer all along line-P. Factors for converting the uptake of radiolabeled substrate to bacterial productivity were determined empirically from dilution experiments. The empirically derived conversion factors for both thymidine and leucine were positively correlated to in situ cell abundance. Bacterial productivity estimated from [3H]-thymidine and [14C]-leucine incorporation rates was lowest in the winter (B0.2 mg C l
1 d
1), with little spatial variability. Bacterial productivity increased 4–10-fold in spring at P4 compared with 0–4-fold at the more oceanic stations. Between 1995 and 1998, the average summer bacterial abundance all along line-P decreased by B50%, while bacterial productivity decreased by B90%. These decreases reduced summer bacterial productivity and growth rates to nearly winter levels in both the open-ocean and slope waters during late summer 1998. The average bacterial productivity at OSP is similar to other open-ocean regions while bacterial abundance is slightly higher providing for relatively lower growth rates and inferring lower associated loss rates. r 2002 Elsevier Science Ltd. All rights reserved.

1. Introduction Heterotrophic prokaryotes (referred to herein as bacteria), are estimated to constitute >50% of the *Corresponding author. Fax: +1-604-822-6091. E-mail address: [email protected] (N.D. Sherry). 1 Present address. NIWA Centre for Chemical and Physical Oceanography, Department of Chemistry, University of Otago, Dunedin, New Zealand.

total biomass of the ocean (Wilhelm and Suttle, 1999). They consume a large portion of primary production (2–130%) (Williams, 2000 and references within), and they mineralize most of the dissolved organic carbon that they consume, back into CO2 through respiration (del Giorgio and Cole, 2000 and references within). Understanding the magnitude of, and mechanisms driving, both seasonal and interannual changes in bacterial processes in the ocean are critical to our ability

0967-0645/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 2 ) 0 0 2 1 4 - X

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N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

to understand ocean biological and chemical processes. It is also critical for predicting the ocean’s response to climate change. Line-P, with Ocean Station Papa (OSP), is one of the few openocean time series and the only one in the subarctic northern hemisphere waters where bacterial biomass (BB) and bacterial productivity (BP) have been sampled over sufficient time and at high enough frequency to begin addressing both interannual and seasonal patterns in a robust manner. We exploit this time series in both seasonally dynamic slope waters and in an oceanic highnitrate, low-chlorophyll (HNLC) region, where primary productivity has been shown to be limited by the availability of Fe (Martin et al., 1989; Boyd et al., 1996; Coale et al., 1996). Estimates of water column BB and BP began at OSP with the SuPER program that visited OSP in 1987 and 1988. Kirchman et al. (1993) found a 2–5-fold increase in both BB and BP in spring and summer 1988 and consistently low growth rates (o0.1 d
1). Boyd et al. (1995a, b) and Doherty (1995) measured BB and BP in the euphotic zone along line-P providing the first transect of these measurements from a shelf-break to HNLC openocean waters, which included both the winter and spring of 1993 and 1994. Sherry et al. (1999) extended these historical data over two more years, adding both deep sampling and respiration measurements. Euphotic zone data presented by Sherry et al. (1999) for September 95–June 97 have been integrated into the data and analysis presented herein. This study addresses uncertainties in the methods associated with determining the conversion factors used in estimating BP from the uptake rates of labeled macromolecule precursors. It presents BB and BP estimates for winter, spring, and summer over 4 years (including the 1997 El * along a 1420-km long transect (line-P) from Nino) the continental slope to the open-ocean HNLC waters off the coast of British Columbia, Canada. This study and Sherry et al. (1999) are the first studies in the subarctic NE Pacific to address changes in bacterial properties across the transition from the seasonally nutrient-depleted slope waters to open-ocean HNLC waters over three seasons and during multiple years. Because this

study compares more historical data and adds two more years of measurements to the data presented by Sherry et al. (1999), it provides more robust seasonal averages and a longer time series from which to draw conclusions about interannual variability and trends.

2. Methods and materials Data were collected during 11 cruises over a 4-year period along the line-P transect from Juan de Fuca Strait to OSP (501N, 1451W). Sampling took place in late winter, spring, and late summer between summer 95 and winter 99 (Table 1). Sampling was carried out, weather permitting, at all five of the CJGOFS line-P stations (P4, P12, P16, P20, and OSP) on each cruise (Boyd et al., 1999). 2.1. Bacterial productivity and biomass Euphotic zone sampling for bacterial abundance and BP was done using acid-cleaned 10 L GOFLO bottles mounted on a Kevlar line. Sampling was done following an early morning light meter cast used to select six sampling depths corresponding to 100%, 55%, 20%, 10%, 3.5%, and 1% of surface irradiance (PAR) from summer 95 through spring 97 and was reduced to four depths corresponding to 100%, 50%, 10%, and 1% from summer 97 through winter 99 (see Table 1 for 1% light depth). Duplicate slides for the determination of bacterial abundance were made within 2 h of water sampling by filtering 5 ml of a DAPI-stained sample onto black 0.2-mm pore size 25-mm diameter polycarbonate track-etched Poretics filters (Turley, 1993). At least 300 cells were counted in a minimum of 10 fields. Bacterial abundance was converted to BB (see Section 4) using the conversion factor of 10 fg C cell
1 (Fukuda et al., 1998). BP estimates were based on either [3H]thymidine (Bell, 1993) or dual-labeled [3H]-thymidine/[14C]-leucine (Chin-Leo and Kirchman, 1988) incorporation in 30 ml of sample during a 4 h incubation in the dark. Incubations were maintained within 721C of ambient sea-surface

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

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Table 1 Dates of cruises, depth (m) of the euphotic zone as defined by 1% of surface irradiance, and depth (m) of the mixed layer (shown in parentheses) determined subjectively as the shallowest abrupt change with depth in either temperature or salinity. Euphotic zone depths for September 95–June 97 were previously presented in Sherry et al. (1999) Season

Cruise dates

Year

OSP

Summer

22 12 25 24

1995 1996 1997 1998

35 40 75 55

Winter

20 February–8 March 10 February–28 February 16 February–6 March 8 February–28 February

1996 1997 1998 1999

80 (95) 60 (1 0 5) 50 (85) 75 (1 1 5)

Spring

7 May–30 May 2 June–26 June 1 June–26 June

1996 1997 1998

60 (9) 70 (20) 50 (20)

August–13 September August–6 September August–17 September August–20 September

P20 (20) (25) (18) (40)

30 35 50 60

(10) (20) (15) (32)

P16 35 40 56 55

P12

P4

(16) (20) (17) (22)

30 40 40 45

(12) (17) (11) (18)

25 (15) 30 (7) 55 (8) 33 (20)

80 (95) ND 80 (80) 75 (94)

80 (1 2 0) 60 (80) 60 (80) 60 (92)

50 60 ND ND

(40) (55) (75) (95)

40 45 40 40

35 (60) 70 (25) 58 (21)

40 (63) 65 (23) 52 (23)

60 (28) 75 (20) 40 (15)

(70) (55) (65) (11)

35 (8) 35 (6) 33 (22)

ND signifies missing data.

temperature in a dark deckboard incubator with a continuous flow of surface seawater. The conversion of [3H]-thymidine (TdR) and [14C]-leucine (Leu) incorporation rates into productivity of cells was calibrated empirically using the dilution method as described by Kirchman and Ducklow (1993). The isotope conversion factors used were 3.5  1018 cells mol
1 for TdR and 0.106  1018 cells mol
1 for Leu (see Section 2.3). Final cell productivity was calculated as the average of the TdR and Leu cell productivity values. Conversion of the final cell productivity into mg C m
3 d
1 was done based on 10 fg C cell
1 (Fukuda et al., 1998) (see Section 4). No attempt was made to correct estimates of BP to account for the difference between the ambient temperature below the mixed layer and the mixed layer temperature at which all samples were incubated. Therefore, the reported BP estimates may be overestimates of the in situ conditions for stations where the euphotic zone was deeper than the mixed layer depth (Table 1). 2.2. Calculations Mean values reported throughout this paper for euphotic zone measurements were calculated by taking the integral over the light depths and dividing it by the depth of the euphotic zone

(depth of 1% of surface irradiance). Thus, if these data are to be directly compared to often-reported integrated primary productivity (m
2), the value reported here must be multiplied by the depth of the euphotic zone (Table 1). Because the range of values (the maximum and minimum) measured either within the euphotic zone or across years is an ecologically relevant variable, euphotic zone and interannual variability are discussed within this context and not some other statistical measure of variability. Other definitions used throughout include:   BB þ ðBP  tÞ ln BB Bacterial growth rate; Bm ¼ ; t Assemblage doubling time; Td ¼

ln 2 : Bm

2.3. Determination of conversion factors Filtration/dilution incubations, also referred to as grow-out experiments, were carried out intermittently during all three sampling seasons to determine the conversion factors for the calculation of cell production from label uptake rates (TdR and/or Leu) (Table 2). Dilutions were 100 ml of sample diluted into 900 ml of seawater

Winter 98

Summer 97

Spring 97

Cruise

P26

P4 P26

P4 P4 P12 P16 P20 P26 P26 P26

P4

Station

10

10 10

50 300 10 10 10 5 45 1500

10

Depth (m)

(2) (2) (2) (2) (2) (2) (2) (2)

4.072.3 (3)

2.770.6 (3) 4.571.4 (3)

2.470.7 3.170.3 5.070.3 5.070.4 2.270.1 2.471.0 1.670.3 0.870.4

7.171.9 (2)

FTdR (1018 cells mol
1) 7SE (n)

(2) (2) (2) (2) (2) (2) (2) (2)

7.574.0 (3)

6.471.9 4.170.1 11.471.9 16.771.1 7.170.1 7.273.0 4.770.9 2.470.8

23.076.4 (2)

FLeu (1016 cells mol
1) 7SE (n)

7.40

2.42 4.68

1.88 0.34 0.90 0.75 0.85 1.84 1.28 2.30

0.07

TdR

t0 :in situ ratio

6.24

0.94 1.25 2.00 1.52 2.58 3.72 2.23 4.09

0.32

Leu

0.55

1.40 1.12

1.70 0.43 1.23 1.77 1.13 1.02 1.08 0.08

2.39

In situ cell Abundance (1012 cells m
3)

Non-linear cummulative (decreasing)

Cummulative Non-linear cummulative (decreasing)

Non-linear cummulative (increasing) Cummulative Cummulative Cummulative Cummulative Cummulative Cummulative Cummulative Cummulative

Calculation method

Table 2 Conversion factors (FTdR ; FLeu ) for the determination of bacterial production from [3H]-thymidine and [14C]-leucine incorporation rates as determined by linear and nonlinear cumulative methods (see text). Also shown are the in situ cell abundance and the ratio between the initial label incorporation rate during filtration/dilution incubations and the in situ incorporation rate from the same locations (t0 :in situ ratio)

5778 N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

previously filtered through a 0.2 mm capsule filter (Gelman PN12117). Grow-out experiments were run in either duplicate or triplicate parallel incubations over 2–5 d with sampling for both bacterial abundance and label uptake rates done every 12–24 h and processed in the same manner as described above for in situ measurements. Incubations were done in 1-l polycarbonate bottles incubated at 50% of ambient light and 721C of ambient surface temperature. Conversion factor (F ) calculations were done for each filtration/dilution incubation time series, the results of which were averaged across replicates (Table 2). The cumulative method (Bj
rnsen and Kuparinen, 1991) was used as the default calculation method. After plotting cell increase on the integrated label uptake (plots used for the calculation of F using the cumulative method), the data were examined for linearity. If the first few points were linear and then deviated from linearity with time, the later points were removed from the calculations. If all the points were non-linear, but showed a constantly increasing (or decreasing) trend, they were fit to the following equation: y ¼ ax þ bx2 ; where a is an estimate of F at t0 and b is the rate of change in F relative to the cumulative label uptake.

3. Results 3.1. Empirical conversion factors Euphotic zone conversion factors (F ) ranged from 1.6–7.1  1018 cells mol
1 for TdR and 0.047–0.23  1018 cells mol
1 for Leu (Table 2). With three noted exceptions, the plots of cell increase against integrated label uptake (plots used to calculate F with the cumulative method) were linear, suggesting little if any change in F during the first 48 h of the grow-out experiments. The three exceptions to the linearity of F were also the three grow-out incubations where the label/cell at t0 was the furthest from in situ values, suggesting that these filtration/dilution incubations were substantially different from the in situ conditions, raising the question of whether any F calculated

5779

from such data should be considered valid (see Table 2). When present, the same non-linear characteristics were apparent in both the TdR and the Leu F calculations. The cell-specific label uptake rates at the start of the grow-out experiments varied substantially about the in situ values. Following the dilution, the cell-specific Leu uptake rates (t0 values) averaged two-fold higher than in situ values (po0:01) (Table 2) suggesting a regular shift-up in Leu incorporation (maybe more protein per cell and/or bigger cells) associated with the grow-out experiments. The increase in cell volume (and thus Leu/cell) that is commonly reported in grow-out experiments (Bj
rnsen and Kuparinen, 1991; Ducklow et al., 1992) supports the practice of calibrating F for Leu in terms of measured biomass instead of cell abundance. Calculating the F for Leu in terms of cell abundance alone, without accounting for biomass, would lead to a regular underestimate of Leu-based BP. During both spring and summer (but not winter) Leubased BP estimates in this study were consistently lower than TdR-based BP estimates (cf. Fig. 2) using conversion factors for both labels that were calculated from the same samples in the same way. Estimates of cell volume were not made during this study, and thus corrections for changes in estimated cellular carbon were not done. During this study, the mean F for the mixed layer was 3.5  1018 cells mol
1 for TdR and 0.106  1018cells mol
1 for Leu. In spring 97, there was a distinctive trend, with F (in the mixed layer) decreasing in the off-shore direction for both TdR and Leu (Table 2). The lowest values for F in the euphotic zone were those below the mixed layer. Other than spring 97, sampling was insufficient to determine with confidence whether there were any persistent spatial, seasonal or interannual trends in F and therefore a constant average F was used for this study. However, spatial and temporal patterns in BP may have been blurred by the use of an invariant F : 3.2. Bacterial biomass The depth-averaged euphotic zone bacterial biomass ranged from 3.4 to 25 mg C m
3 over this study (at P16 in winter 99, and P20 in summer 95,

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

5780

OSP in winter 99 and P4 in summer 96, respectively; Fig. 2) Winter BP was low and constant all along line-P (B0.2 mg C m
3 d
1) and showed little interannual or within euphotic zone variability (Figs. 1 and 2). West of P4 during the spring and summer, BP averaged 3 and 5-fold higher than winter (0.7–1.0 mg C m
3 d
1) and showed much greater variability. At P4, BP was 2–3-fold higher (B2.5 and B3.0 mg C m
3 d
1) and more variable than the more oceanic stations (Figs. 1 and 2). At P4, summer BP decreased almost 10-fold between 1996 and 1997, while it decreased B5-fold at OSP between 1996 and 1998 (Fig. 2).

3.3. Bacterial productivity

3.4. Growth rates and doubling times

The depth-averaged euphotic zone BP ranged from 0.01 to 4.3 mg C m
3 d
1 over this study (at

The depth-averaged euphotic zone bacterial growth rate (Bm) ranged from 0.02 to 0.3 d
1

P12

P4

Bacterial Biomass (mg C m-3) Bacterial Productivity (mg C m-3 d-1 )

20

2

15

10

1

5

0 150 5

145

140

135

130

0 125 0.5

4

0.4

3

0.3

2

0.2

1

0.1

0 150

145

140

135

Longitude (˚W)

130

0.0 125

Winter Spring Summer

OSP

P20

P16

P12

P4 4 0.02 e

30

0.03 e3 20 2 e 0.05

10

Growth Rate (d-1)

P16

Assemblage Doubling Time (d)

P20

Bacterial Productivity (1012 cells m-3 d-1 )

OSP 25

Bacterial Abundance (1012 cells m-3 )

respectively). Winter BB was low and constant all along line-P (B6 mg C m
3), showing little variability either interannually or within the euphotic zone. In contrast, spring and summer BB averaged 2–3-fold higher (7–17 mg C m
3) and showed much greater interannual and within euphotic zone variability. There were no consistent trends in magnitude or interannual variability along line-P, although relative to P4, OSP showed lower variability within the euphotic zone (Figs. 1 and 2). Summer BB at P4 dropped B60% between 1995 and 1997, while it dropped B45% at OSP over the same time period.

0.10 e1

0 150

145

140

135

130

e0 125

Longitude (˚W)

Fig. 1. Bacterial biomass, productivity, and growth rates at five stations along line-P during winter, spring, and summer (see Table 1). Data represent the mean seasonal euphotic zone values calculated by stepwise integration of euphotic zone measurements divided by the depth of the euphotic zone. Note: Bars represent the range of values measured (not statistical error). Markers for summer and winter are offset slightly on either side of the actual station longitude for clarity. Data for September 95–June 97 are also presented in Sherry et al. (1999).

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

Growth Rate (d-1)

-3 Bacterial Productivity (mg C m-3 d-1) Bacterial Biomass (mg C m )

P4

OSP

20

20

10

10

0

0

Winter Spring Summer

5781

between 1996 and 1998 and decreased B3-fold at OSP between 1995 and 1998. This change led to summer growth rates with the greatest interannual variability of the three seasons sampled. Winter growth rates decreased at OSP by B2-fold between 1996 and 1999 (Fig. 2). Overall, P4 showed a much greater range in growth rates than OSP.

4. Discussion

6 2

4

This study compares the more seasonally dynamic continental slope waters with the openocean, high-nitrate, low-chlorophyll (HNLC) waters within the subarctic NE Pacific. We also focus on three central themes: seasonal patterns, interannual variability, and the uncertainties associated with the empirically derived conversion factors used in calculating the bacterial productivity reported herein.

2

0 0.4

0 0.2

0.3

0.1

0.2

0.1

4.1. Conversion factors Jan-99

Jan-97

Jan-95

Jan-93

Jan-99

Jan-97

Jan-95

0.0 Jan-93

0.0

Fig. 2. Bacterial biomass, productivity, and growth rates at P4 and OSP during winter, spring, and summer. For bacterial productivity, filled and open symbols indicate rates based on Leu and TdR incorporation, respectively. Values for spring 1993 and 1994 are from Doherty (1995). Values for winter 1994 are from Boyd et al. (1995a, b). Data represent the mean euphotic zone values calculated by stepwise integration and divided by the depth of the euphotic zone. Note: Bars represent the range of values measured in the euphotic zone (not statistical error). Markers for TdR- and Leu-based productivity are offset from each other on either side of the actual cruise dates for clarity.

(doubling time (Td ) from 32 to 2 d, at P4 in winter 98 and summer 96, respectively; Fig 2). The average winter doubling time was about twice as long (B18 d) as spring (B9 d) and summer (B8 d) (Fig. 1). Due to the disproportionate increase in BP relative to abundance at P4 during spring and summer, the average growth rate was higher at P4 than the more oceanic stations (Figs. 1 and 2). Summer growth rates decreased by B10-fold at P4

The conversion factor (F ) used to convert the label uptake rates into BP is variable and probably the most uncertain factor associated with determining BP and Bm (Sherry, 2002). Conversion factors have been derived theoretically based on estimates of label dilution, precursor content within macromolecules and macromolecule content within cells, etc. for both TdR (Furman and Azam, 1982; Moriarty, 1986) and Leu (Simon and Azam, 1989). However, since these various factors can vary depending on the community composition and environmental conditions, there is the potential for significant and unknown accumulated error (Kirchman et al., 1982; Kirchman, 1992; Ducklow, 2000). To account for the unknown variability as well as label incorporation into non-target macromolecules, the use of empirically determined conversion factors was introduced by Kirchman et al. (1982) and is now widely used. However, running carefully controlled replicate grow-out experiments consumes time and resources that might be better spent measuring other experimental parameters or in situ productivity. Unfortunately, this study further

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

5782

emphasizes the need for even more consistent empirical conversion factor determinations when bacterial productivity estimates are based on macromolecule precursor uptake rates. This study found a positive linear relationship between TdR and Leu conversion factors (FLeu ¼ 0:03  FTdR ; R2 ¼ 0:75) as would be expected when biological and/or environmental factors influencing TdR and Leu uptake rates are similar (Fig. 3). A similar pattern has been observed in many studies that have reported empirically derived conversion factors (cf. Kirchman, 1992; Sherr et al., 1999). However, this strong correlation did not lead to in situ TdR and Leu productivity estimates that always agreed (Fig. 2). This observation suggests that the real F values for TdR and Leu did vary independently of each other to some degree, and that variable F values for both TdR and Leu that accounted for seasonal and spatial changes would likely improve this discrepancy. These data show Leu-based productivity estimates to be pTdR-based esti-

F Leu (1018 cells mol-1)

0.3

y = 0.068x 2 R = 0.38

0.2

y = 0.029x R2 = 0.86

0.1

0.0 0

2 F TdR (10

4 18

6

8

-1

cells mol )

Fig. 3. Linear regressions of Leu conversion factors on TdR conversion factors (FLeu on FTdR ) determined from dilution/ incubation grow-out experiments using either duplicate or dual labeled samples from Kirchman (1992) (—J—) and from Table 2 of this study (- -n- -). Open symbols are values from OSP. Closed symbols are from other line-P stations (see Table 2).

mates during the spring and summer suggesting a lower protein content relative to DNA (smaller cell size?) during these times of higher bacterial abundance. Interestingly, the empirically derived conversion factors (F ) calculated in this study for both TdR and Leu increased as bacterial abundance increased (TdR R2 ¼ 0:41; po0:02; Leu R2 ¼ 0:67; po0:003) (cf. Table 2). If F is allowed to change in association with BB as suggested by this relationship, the overall trends in BP are exaggerated and suggest generally lower winter and higher summer BP, along with a greater overall decrease in BP between 1995 and 1998. These data also suggested a decrease of B40% for the TdR conversion factor and a decrease of 50–60% for the Leu conversion factor during summers from 1995 to 1997. The range of F ; when calculated from cell abundance, varied within the range of commonly reported conversion factors (1.5–5  1018 for TdR, 0.05–0.20  1018 for Leu) (cf. Table 3). Some of the relationship between F and cell abundance may be a handling artifact. Sherr et al. (1999) show evidence of reduced cell-specific uptake of label (relative to in situ) immediately following filtration to remove grazers from coastal, shelf, and slope waters off Oregon. In the present study, the cell-specific label uptake rates immediately after dilution (t0 of the dilution incubation experiments) differed from the in situ cell-specific uptake rates in a non-random manner relative to bacterial abundance (Fig. 4). During times of greater cell abundance, this handling anomaly became negative (and vise versa). The negative correlation was stronger for Leu than for TdR. This anomaly might be explained by isotope dilution (Moriarty, 1986) and/or enhanced growth rates. To explain these observations with isotope dilution, handling must have reduced the uptake of the label, which means that isotope dilution must have increased with biomass. This could happen if cell damage or other particle disruption increased with cell abundance and occurred during the filtration process making more unlabeled leucine available to the bacteria in the dilution cultures. However, this does not explain the increase in the cell specific label uptake observed at lower cell abundance. These observations might

N. Atl. Subtropical Gyre Sargasso Sea (BATS) Equatorial Atl. S. Atl. Subtropical Gyre Atl. Subantarctic Atl. Antarctic Circumpolar Current

N. Atl. Drift

N. Atl. Drift

N. Atl. Drift

NW Atlantic N. Atl. Drift

Subarctic NE Pac. Subarctic NE Pac. California Current California Upwellingb California Upwellingc Eastern Equatorial Pac. Eastern Equatorial Pac. Ross Sea

Spring Subarctic NE Pac.

Season and location

Zubkov et al. 2000 Lochte et al. (1997), K.aehler et al. (1997)

Carlson et al. (1996) Zubkov et al. 2000 Zubkov et al., 2000

Li et al. (1993) Ducklow et al. (1992 and 1993) Ducklow et al. (1992, 1993) Fasham et al. (1999) Zubkov et al. 2000 Zubkov et al. 2000

1–4 2–6

0.3–0.5

B1

B0.1

0.1–0.6

7

18.7

7

7

6.6

2.0–2.4 2–5

7

0.3–0.7

B2

B0.3

7

20

20

20 20

20

5.9

20

19.6

0.3–0.6

4–10

2–3

20–50

30–40 20–50

2–6

1.4–5.2

0.6–1.4

0.1–0.15

1–2.5

1.5–2 1–2.5

0.1–0.3

Ducklow et al. (1999)

8–11

0.2–0.9

20

18

0.9

0.3–0.8

Cochlan (2001)

20

2 12–20

0.1

0.6–1

10

10

Cherrier et al. (1996) Kirchman et al. (2000) Kirchman et al. (2000) Ducklow et al. (1995)

10–13

6–12

1–1.3

20

0.6–1.2

7–25

11–16

36–107

5–18

107–143

12–36

18–107

71–161

57–201

75–189

96–170 75–189

16

—

0.2–0.3

0.2–0.6

0.03–0.1

0.2–0.8

0.1–0.4

0.1–0.2

0.4–0.9

2–7

1.8–4.5

2–7 4–10

0.19

—

2

—

— 36–84

—

0.6

a

0.5–0.9

0.4–0.6

0.1–1.3

—

—

15–27

11–16

2.9–37

C/cell fg TdR BPTdR mg C cell
1 nmol m
3 d
1 C m
3 d
1

This study

0.4–1.3

B#s 1012 BB mg cells m
3 C m
3

Kirchman (1992), Kirchman et al. (1993) Doherty (1995)

Reference

1.00

0.80

0.80

0.80

1.63

0.80

0.80

1.74

1.2

1, 2.3 2.65

0.6

—

2.17

—

—

—

3.50

3.50

1.74

—

0.80

0.80

0.80

0.4–0.6

0.80

0.80

—

0.67–1.5

1, 2.3 2.03–3.69

0.4–0.9

—

—

—

—

—

2.0

—

1.5–3.4

0.07–0.1

0.42–2.1

0.42–0.84

0.84–2.5

0.24–0.84

0.63–1.3

0.84–3.4

—

1.6

2.7–5.0 1.6

0.14

1.0–1.3

0.72–1.32

0.6–14.6

2.5–3.9

—

0.3–0.8

—

—

0.2–0.3

0.1–0.5

0.1–0.2

0.2–0.6

0.1–0.4

0.15–0.3

0.2–0.8

—

3

3–17 6

0.11

0.7–0.9

1.7–3.0

1.4–33.6

5.8–9.0

—

0.3–0.8

—

—

0.16

0.034

0.034

0.034

0.078

0.034

0.034

—

0.095

0.055, 0.17 0.183

0.04

0.115

0.115

0.115

0.115

—

0.106

—

0.108

—

0.034

0.034

0.034

0.030

0.034

0.034

—

0.04–0.13

0.055, 0.17 0.14–0.22

0.03–0.05

—

—

—

—

—

0.060

—

0.027

FTdRðusedÞ 1018 FTdRðmeasuredÞ 1018 Leu BPLeu FLeuðusedÞ 1018 FLeuðmeasuredÞ mmol m
3 d
1 mg C m
3 d
1 cells mol
1 cells mol
1 cells mol
1 1018 cells mol
1

Cumulative

Cumulative

Cumulative

Cumulative

Cumulative

Cumulative

Cumulative

—

Cumulative

Cumulative Mod Der

Cumulative

—

—

—

—

—

Cumulative

—

Integrative

F Method

Table 3 Summary of literature values for open-ocean euphotic zone and/or mixed-layer measurements related to bacterial biomass and bacterial productivity from various regions and seasons

B0.06

B0.13

0.03–0.14

B0.13

0.10

B0.09

B0.08

B1.0

0.05–0.12

0.08, 0.25 0.1–0.3

0.06–0.5

0.2

0.2

0.07–1.1

0.4

0.3

0.03–0.6

0.04–0.08

0.03–0.1

m d
1

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791 5783

N. Atl. Subtropical Gyre

Eastern Equatorial Pac. N. Atl. Drift

Autumn Subarctic NE Pac.

Sargasso Sea (BATS)

Winter Subarctic NE Pac. Subarctic NE Pac. Eastern Equatorial Pac. W. Equatorial Pac

Scotia Sea

Sargasso Sea (BATS)

Ross Sea

Subarctic NE Pac. Eastern Equatorial Pac. Antarctic Circumpolar Current Ross Sea

Summer Arctic Ocean Subarctic NE Pac.

Season and location

Zubkov et al., 2000 Zubkov et al., 2000

Kirchman (1992), Kirchman et al. (1993) Ducklow et al. (1995) 2–4 B1

B0.1

9–18

0.5–1.2

0.3–0.6

10–14

0.5–0.7

1.6–1.8

0.3–0.5

Carlson et al. (1996), Carlson and Ducklow (1996)

5–9

0.2–0.5

Shiah et al. (1998)

4–7 8–13

0.4–0.7

0.4–0.7

7.0

0.70

Kirchman et al. (1995)

Boyd et al. (1995a, b) This study

10

1

7

7

20

20

4.8

20

20

10

10

10

6

B3

20

0.3–0.7

4–24

9–36

36–161

48–84

23–32

12–24

40–130

19–35

2–8

13–19

24

12–60

—

39

40

B4

6.7

0.2–1.2

Ducklow et al. (1999) Ducklow et al. (2000) Carlson et al. (1996), Carlson and Ducklow (1996) Bj
rnsen and Kuparinen (1991)

3.5

10–70 16–47

10

6–7 17–66

20

10

0.8

Church et al. (2000)

9–18 9–15

20 20

0.05–0.2

0.2–0.9

1–2

0.8–1.1

0.1–0.2

1–3

0.8–1.5

0.1–0.3

0.5–0.7

0.3

0.1–0.6

—

2

0.34

0.7–2

0.4–2.5

0.5–2 0.6–2.3

C/cell fg TdR BPTdR mg C cell
1 nmol m
3 d
1 C m
3 d
1

1.5

0.5–0.8

Kirchman et al. (1995)

8–28 12–25

B#s BB 1012 mg cells m
3 C m
3

Rich et al. (1997) 0.4–1.4 0.6–1.3 Kirchman (1992), Kirchman et al. (1993) This study 0.9–1.8

Reference

Table 3 (Continued)

0.80

0.80

2.17

1.74

1.63

1.18

2.15

3.50

3.50

1.23

1.63

—

2.5

2

2.15

3.50

2.15 1.74

FTdRðusedÞ 1018 cells mol
1

0.80

0.80

—

3.4

0.2–3.7

—

—

4.0

—

1.23

0.8

—

2.5

—

—

4.5

— 1.1–2.4

FTdRðmeasuredÞ 1018 cells mol
1

B0.63

0.84–4.2

0.48–0.84

—

0.19–0.48

—

0.34—0.65

0.1–0.4

—

0.13

0.24–0.72

1.0

0.66

0.075

0.30–0.87

0.83

0.36–4.2 —

B0.15

0.2–1

1.1–1.9

—

0.1–0.2

—

0.8–1.5

0.1–0.4

—

0.4

0.1–0.3

1.5

3.4

—

0.7–2

0.88

0.8–4 —

0.034

0.034

0.115

0.108

0.078

—

0.115

0.106

—

0.3

0.078

0.224

0.26

—

0.115

0.106

0.115 0.108

0.034

0.034

—

0.15

0.02–0.3

—

—

0.075

—

0.3

0.03

—

0.26

—

—

—

— 0.03–0.3

Leu BPLeu FLeuðusedÞ 1018 FLeuðmeasuredÞ mmol m
3 d
1 mg C m
3 d
1 cells mol
1 1018 cells mol
1

Cumulative

Cumulative

—

Integrative

Cumulative

—

—

Cumulative

—

Cumulative

Cumulative

—

Cumulative

—

—

—

— Integrative

F Method

B0.12

B0.18

0.1

0.07

0.07

0.2–0.4

B0.1

0.02–0.05

0.09

0.04

0.08

0.15

0.3–0.4

0.09

B0.1

0.04–0.12

0.03–0.45 0.04–0.1

m d
1

5784 N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

Zubkov et al., 2000

Carlson et al. (1996), Carlson and Ducklow (1996) Zubkov et al., 2000 Zubkov et al., 2000

0.4

7

4–7

20

7

7

1–2

0.6–1.0

7

1–5

5.4

0.1–0.3

2.4

0.1–0.7

0.4–0.6

—

107–161

B1d

0.2–0.9

0.05–0.8 B0.1

B18

0.1–0.3

9–143

12–36

—

0.80

0.80

0.80

1.63

—

0.80

0.80

0.80

1.1–4.1

—

0.42–2.1

B0.84

0.42–3.4

0.24–0.6

—

0.1–0.5

B0.2

0.1–0.8

0.1–0.3

—

0.034

0.034

0.034

0.078

—

0.034

0.034

0.034

0.100

—

Cumulative

Cumulative

Cumulative

Cumulative

0.13

B0.09

B0.10

B0.13

0.06

d

c

b

BP derived from 3H-adenine uptake instead of TdR.

Data from regions considered by authors to be Fe replete.

Data from regions considered by authors to be of low Fe.

The isotope-uptake:bacterial-production conversion factor is denoted by F in the following notes. Doherty (1995)—BB and BP recalculated from the author’s B#s and TdR incorporation based on cellular carbon and conversion factors used in this study. Cherrier et al. (1996)—BP was based on change in POC, not radiolabel uptake rates. Ducklow et al. (1995)—TdR is taken from profile plots, BP is taken from time-series plots (mean of 120 m, 1% Lt). Cochlan (2001)—Leu provided by author. Ducklow et al. (1999)—m calculated from incubations experiments and associated cell yield. Only treatments at ambient temperature and without amendments are included. Ducklow et al. (1992/93)—the two entries are to show the difference in values depending on how F is calculated (either cumulative or modified derivative). Leu uptake is back-calculated from the reported Leu BP assuming that the F used by the authors was the average of the values determined via the modified derivative method in the 1992 paper. The label uptakes associated with the cumulative method are assumed to be the same as those back-calculated from the modified derivative method above. Fasham et al. (1999)—TdR F is assumed to be the same as Kirchman et al., 1993 (F ¼ 1:74 and C/cell=20), since the methods of Kirchman et al. (1993) were referenced within. Zubkov et al. (2000)—the cellular Leu F was estimated from the reported carbon based Leu F and C/cell. The conversion reported by the authors is not correct because g C mol
1 should be divided, not multiplied by g C cell
1. Carlson et al. (1996)—C/cell is based on reported cell volume and authors’ choice of 120 fg C mm
3. Lochet et al. (1997), K.ahler et al. (1997)—BP values are TdR and Leu averaged. Cellular-based Leu F was calculated from the reported carbon-based Leu F using 18.7 fg/cell as reported by the authors. Kirchman et al. (1995)—BP is the average of both TdR and Leu values. Church et al. (2000)—Leu BP was not calculated because the authors consider absolute magnitude to be erroneous due to isotope dilution associated with the experimental protocol. Bj
rnsen and Kuparinen (1991)—the Leu F was converted from biovolume mol
1 to cells mol
1 using reported biovolume to C conversion and assuming 10 fg cell
1. Jones et al. (1996)—the authors reported BB and m based on the assumption that 15% of the cells were active. This table shows BB and m values based on 100% of the DAPI positive cells. The authors’ values are, thus, multiplied by 6.67 to be comparable with other cited works. BP was based on 3H-adenine uptake into DNA instead of TdR uptake. Li et al. (1993)—values were measured under both early bloom and fully developed bloom conditions. The F derived using both cumulative and integrative methods agreed with each other, although cumulative is stated in the table. For the present study, the winter conversion factor was calculated based on a non-linear fit to cumulative data (see text). Reported data include bacterial abundance (B#s, 1012 cells m
3), biomass (BB, mg C m
3), carbon per cell used for BB calculations (C/cell, fg C cell
1), [3H]-thymidine uptake rate (TdR, nmol m
3 d
1), TdRbased bacterial production (BPTdR, mg C m
3 d
1), TdR conversion factor (FTdR ; 1018 cells mol
1), [3H]-leucine or [14C]-leucine uptake rate (Leu, mmol m
3 d
1), Leu-based bacterial production (BPLeu, mg C m
3 d
1), Leu conversion factor (FLeu ; 1018 cells mol
1). All reported values were converted to standard units either directly or by using conversion factors listed in the table. Values in italics were not reported by the cited authors, but rather assumed or derived for this table from other values in the same row to provide more complete comparisons between the various works. Many values are extrapolated from published plots and should thus not be considered actual values, but rather reasonable approximations. In some table entries, it appears that authors have chosen conversion factors outside the range of those measured. This is because their choice of the conversion factor was based on an average over several seasons or regions, not just the values shown in this table. a BP derived from change in particulate organic carbon, not TdR uptake rates.

Spring and Autumn combined Jones et al. N. Pac. (1996) Subtropical Gyre

Equatorial Atl. S. Atl. Subtropical Gyre Atl. Subantarctic

Sargasso Sea (BATS)

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791 5785

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

5786

TdR, t0 - in situ (10-20 mol cell-1)

8

200

4 100 0 TdR

0

-4

TdR p = 0.05, R2 = 0.31 Leu p = 0.005, R2 = 0.61

Leu

-8

Leu, t0 - in situ (10-20 mol cell-1)

300

12

abundance and not with BP, F must increase in association with increasing bacterial abundance regardless of BP. An increase in abundance without an increase in BP suggests reduced loss processes (e.g. reduced grazing) and increased competition for limiting resources. Thus, more competitive or ‘‘efficient’’ cells may dominate under higher abundance conditions, enabling greater growth with lower label uptake. Determining the mechanism and extent of this relationship between F and BB will require further study.

-100 0.0

0.5

1.0

1.5 12

Abundance (10

2.0

2.5

4.2. Cellular carbon content

-3

cells m )

Fig. 4. Linear regressions of perturbation induced anomalies on in situ bacterial abundance for TdR and Leu. Perturbation induced anomalies in the label uptake rate were calculated as the initial uptake rate in the dilution/incubation experiments minus the in situ label uptake rate.

be explained through enhanced growth rates. Growth rates might be enhanced following manipulation if more substrate was available due to contamination or other filtration artifacts as discussed above. The substrate enhancement would lead to enhanced growth, but a reduced level of enhanced growth when more cells were present (times of greater cell abundance) and sharing the resource. However, a shared resource enhancement only explains the response in the low range of cell abundance, because on the higher end, the differential label uptake rate becomes negative. Neither of these speculations alone readily explains both ends of the relationship between cell abundance and in situ vs. in vivo cellspecific label uptake rates. Aside from handling artifacts, other mechanisms also might explain at least some of the relationship between F and bacterial abundance. Higher cell abundance may be correlated with smaller cells containing less DNA and protein (these measurements were not made in this study). Samples with greater cell abundance may be associated with higher rates of isotope dilution because of associated increases in de novo synthesis of the precursors under highly competitive conditions. Since F correlates only with bacterial

Both BB and BP numbers in this study are based on an assumed cellular carbon content of 10 fg C cell
1, not the more commonly used 20 fg C cell
1 (Lee and Fuhrman, 1987) and cellular carbon content was not directly measured in this study. Fukuda et al. (1998) suggest that the cellular carbon in open-ocean bacteria averages B12 fg C cell
1 and it is lower still in the HNLC equatorial Pacific and the Southern Ocean with values of 5.9 and 6.5 fg C cell
1, respectively. Because the subarctic NE Pacific is an open-ocean HNLC region, 10 fg C cell
1 was chosen as a reasonable and convenient estimate. The uncertainties in cellular carbon content are unimportant when comparing between BB, BP, and Bm in this study because a consistent cellular carbon content was used throughout. However, if carbon per cell was higher in the shelf break region (P4) than at the open-ocean HNLC stations, then the trends toward increasing BB and BP closer to shore would be further exaggerated. These uncertainties support a more universal practice of measuring cell carbon content or at least cell size as a proxy for carbon. Although this study used a significantly higher TdR conversion factor (3.5  1018 instead of B2  1018 cells mol
1) than either Kirchman et al. (1993) or Sherry et al. (1999), the productivity values reported herein are similar because the estimate used for cellular carbon content was lower (10 instead of 20 fg C cell
1). Accordingly, the BB reported herein is 50% less than that reported for the same cell abundance values in the previous studies.

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

4.3. Slope waters vs. the HNLC open ocean Data from OSP and P4 are presented in most detail since they were the end-members of line-P and highlight the differences along the transect from the continental slope to the open ocean. Generally speaking, OSP was similar to the other two oceanic stations (P16 and P20), while P4 was unique and P12 showed either intermediate or anomalous characteristics compared to P4 and P16 on either side of it. There is little difference in the magnitude of BB observed at the two end-members of line-P (P4 and OSP) during either summer or winter. Although winter BP was similar at both P4 and OSP, BP increased 10–15-fold between winter and summer at P4 compared to a reduced seasonality (0–5-fold differences in BP) at OSP. Elevated BP at P4 may be indicative of the different annual phytoplankton cycles observed in these regions with P4 experiencing spring bloom conditions followed by nitrate depletion (Boyd and Harrison, 1999; Thibault et al., 1999), and OSP displaying little seasonal variability in chlorophyll, typical of iron-limited HNLC regions (Parslow, 1981; Miller, 1993; Boyd and Harrison, 1999). At P4 the >10-fold average increase in BP from winter to spring was accompanied by only a 2-fold average increase in BB. A similar but smaller discrepancy was observed at OSP between spring and summer. Unless BB is rapidly increasing, the large increase in BP must be balanced by a large proportional increase in loss processes. Grazing experiments (Rivkin et al., 1999) done concurrently with the present study showed a substantial increase in summer bacterivory rates relative to winter and spring, supporting the idea that changes in loss processes limited increases in BB during the summer. It is unclear whether the seasonal changes in loss processes were due to a functional feeding response of the grazers (change in clearance rates or prey preference) (Strom et al., 2000), due to a change in grazer community (either composition or abundance), due to faster growing bacteria being more readily consumable, or a combination of the above. It is interesting to note that Neocalanus plumchrus, an abundant copepod that

5787

migrates to depth in late spring at OSP and in early spring in coastal waters (Goldblatt et al., 1999; Mackas et al., 1998), is capable (during at least some developmental stages) of grazing on protists which graze on heterotrophic bacteria. The departure of N. plumchrus may release some bacterivorous protists from grazing pressure and thus allow protist numbers to increase. The increased protist numbers could then provide a mechanism for the increased bacterial loss processes in the summer at OSP and in the spring at P4. Unfortunately, this hypothesis is neither conclusively supported nor refuted by the observed seasonal changes in the total number of protists (Booth et al., 1993; Boyd et al., 1995a; Rivkin et al., 1999). 4.4. Trends along line-P In general, there was little difference in the magnitude of either BB or BP among any of the line-P stations during winter. Spring and summer BB along line-P was much more variable than in winter. Summer had the highest average BB while winter had the lowest (Fig. 1). BP was highest at P4 during the spring and summer, with the three most oceanic stations showing lower values and little difference between stations. These patterns may be linked to associated changes in the physics and/or primary productivity of the region (Sherry, 2002). One of the dominant characteristics of these data is the large (often 2–10-fold) interannual differences in BB and/or BP that occurred at all stations (Fig. 2). Summer BB and BP decreased dramatically between 1995 and 1998. Although not as extreme, the Hawaiian Ocean Time-series data2 show a B30% decrease in bacterial abundance from 1996 to 1998 in the subtropical Pacific. In the subarctic NE Pacific, there was a 2–31C mixed-layer temperature increase during summer * However, 97 in association with the 1997 El Nino. * temperature change alone does not the El Nino explain the continued low BB and BP values in 2

Data acquired from the Hawaii Ocean Time-series Data Organization & Graphical System. http://hahana.soest.hawaii.edu/hot/hot-dogs/interface.html

5788

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

summer 98 when the high temperature anomaly was no longer present (Brown, 1998). Perhaps average summer conditions provide for higher bacterial abundance and productivity than the * or La anomalous conditions of either El Nino * Possibly the warm shallow mixed-layer of Nina. * increased nutrient stress, while the the El Nino * reduced colder, deeper mixed-layer of the La Nina light availability to phytoplankton with both cases leading to reduced BB and BP (see Sherry, 2002). 4.5. Comparison to other studies Over the last decade that bacterial measurements have been made at OSP, bacterial abundance and productivity have generally ranged across similar values (Table 3, Fig. 2). During this study, the average bacterial abundance and TdR uptake rates for spring and summer at OSP were similar to those found in 1987/88 by Kirchman et al. (1993) as well as those reported by Boyd et al. (1995a, b) and by Doherty (1995) (Table 3, Fig. 2). In May 1988, sampling at OSP was done prior to the spring thermocline formation (Kirchman et al., 1993), and showed relatively low BB and BP, similar to the winter measurements made during this study. Liu et al. (2002) present bacterial abundance from station KNOT in the western gyre of the subarctic Pacific, a region that expresses greater seasonal variability in chlorophyll than the eastern gyre (the location of this study), but where primary productivity is still limited by the availability of iron during at least part of the year (Harrison et al., 1999). Liu et al. (2002) report bacterial abundance in the upper 50 m in autumn 1998 (0.14  1012 cells m
3) that is substantially lower than any reported during any season for the eastern subarctic gyre. The lowest summer bacterial numbers (B0.9  1012 cells m
3) reported from OSP in the present study were also in 1998. Other than autumn 1998, bacterial abundance at station KNOT falls within the range of values reported from OSP. Bacterial abundance throughout the year at OSP was generally on the high side (0.4–1.8  1012 cells m
3) compared to the subtropical gyres (0.1– 0.7  1012 cells m
3) or the other major HNLC

regions (0.2–1.2  1012 cells m
3), but lower than the N Atlantic spring bloom (1.0–2.5  1012 cells m
3) (Table 3). In contrast, BP at OSP (based on unconverted label uptake rates) was similar to other oceanic regions during summer and winter, while during the spring at OSP, BP was generally lower than the equatorial and temperate regions and more similar to the subtropical gyres and Southern Ocean (Table 3). These values suggest generally lower growth rates in the subarctic NE Pacific compared to other regions. The lower growth rates were due to greater than average cell abundance along with a typical or lower than average BP. These observations suggest generally lower loss rates in the subarctic NE Pacific compared to most other oceanic regimes. Seasonal changes in bacterial abundance and productivity at OSP (B2-fold) were generally greater than those reported for tropical and subtropical waters (Table 3). OSP seasonality was less than other high-latitude regions such as P4, the N Atlantic Drift region, and the Ross Sea, which experience large spring blooms and associated increases (>2-fold) in bacterial processes. None of these regional comparisons address potential uncertainties and differences in cell volume/carbon, or conversion factors for BP from TdR or Leu uptake rates. The lack of consistent empirical measurements of these parameters throughout all the various regions and seasons makes these comparisons untenable at this time.

5. Conclusions The subarctic NE Pacific with the line-P transect offers a unique opportunity to study bacterial processes over a range of changing environments from slope waters that are seasonally nitrogen depleted and influenced by coastal processes, to open-ocean HNLC waters, where macronutrients are plentiful and primary productivity is limited by the availability of iron. Winter BB and BP were surprisingly invariant all along line-P. BB was typically B2-fold higher in late spring and late summer than in winter. BP showed stronger and more variable spatial and temporal patterns than BB. The enhanced seasonality of bacterial

N.D. Sherry et al. / Deep-Sea Research II 49 (2002) 5775–5791

processes in the slope waters relative to the open ocean probably reflects the more dynamic physical environment associated with the continental slope including eddies, jets, upwelling, and nutrient variability. There was also a large decrease in summer BB and BP at both OSP and P4 between 1996 and 1998. Compared to other oceanic regions, the subarctic NE Pacific appears to have generally greater bacterial abundance while supporting similar BP and thus lower average growth rates.

Acknowledgements We thank the officers and crew of the CCG vessel John P. Tully, Hugh Maclean, Tara Ivanachko, Cathleen Vestfals, and Michael Lipsen for technical assistance and help with sampling and sample processing, and the reviewers for their insightful comments. Support for this work came from NSERC (Canada) via grant awards to the JGOFS-Canada program.

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