Seasonal and spatial patterns of heterotrophic bacterial production, respiration, and biomass in the subarctic NE Pacific

Deep-Sea Research II 46 (1999) 2557}2578

Seasonal and spatial patterns of heterotrophic bacterial production, respiration, and biomass in the subarctic NE Paci"c Nelson D. Sherry*, Philip W. Boyd, Kugako Sugimoto, Paul J. Harrison School of Earth and Ocean Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 Received 9 September 1998; received in revised form 7 November 1998; accepted 7 November 1998

Abstract Heterotrophic bacterial biomass, production, and respiration rates were measured during winter, spring, and summer in the subarctic NE Paci"c from September 1995 to June 1997. Sampling took place on six cruises at "ve hydrographic stations 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). Interannual variability was small relative to seasonal and spatial variability. Biomass, derived from cell counts (assuming 20 fg C cell\), was ca. 12 lg C l\ in the winter and increased to 20}35 lg C l\ in the spring and summer all along line-P. Bacterial production from [H]-thymidine and [C]-leucine incorporation rates was lowest in the winter (ca. 0.5 lg C l\ d\) with little spatial variability. Production increased 10-fold in spring at P4 (to ca. 4.5 lg C l\ d\). In contrast, only a 2-fold increase in bacterial production was observed over this period at the more oceanic stations. Rates of production in late summer were highest over the annual cycle at all stations ranging from ca. 6 at P4 to ca. 2 lg C l\ d\ at OSP. Bacterial ((1 lm size fraction) respiration, measured from dark-bottle O  consumption over 24 or 48 h, was (10 lg C l\ d\ during the winter and spring. Respiration rates increased '10-fold to ca. 100 lg C l\ d\ at P4 in the summer, but, interestingly, did not increase from spring to summer at the more oceanic stations. Thus bacterial growth e$ciency, de"ned as production/(production#respiration), decreased in the spring westwards from the slope waters (P4) to the open-ocean (OSP), but increased westwards in the summer. Bacterial production was highly correlated with temperature at OSP (r"0.88) and less so at P4 (r"0.50). The observed temporal and spatial trends presented in this study suggest that seasonal changes in bacterial biomass were greatly a!ected by changes in loss processes, that * Corresponding author. Fax: 001-604-822-6091. E-mail address: [email protected]  Present Address: NIWA Centre for Chemical and Physical Oceanography, Department of Chemistry, University of Otago, Dunedin, New Zealand. 0967-0645/99/$ - see front matter  1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 9 9 ) 0 0 0 7 6 - 4

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bacterial biomass is regulated by di!erent processes than bacterial production, and that bacterial production alone, without respiration measurements, is not a robust proxy for bacterial activity in the subarctic NE Paci"c.  1999 Elsevier Science Ltd. All rights reserved.

1. Introduction Free-living heterotrophic bacteria in the marine environment play a multifaceted biogeochemical role (Cho and Azam, 1988). Bacteria break down organic material releasing excess macronutrients and micronutrients and thus further stimulate phytoplankton growth (Berman et al., 1987). Conversely, they may, under nutrient limitation, compete with phytoplankton for nutrients (Kirchman, 1994; Tortell et al., 1996) and thus contribute to the limitation of phytoplankton production. As secondary producers, bacteria consume dissolved organic material (DOM), originating from phytoplankton photosynthesis, and convert it to particulate organic material (POC) that sustains grazers within the microbial food web (Ducklow, 1994). Furthermore, the magnitude of bacterial respiration (BR) is often a considerable proportion of the total community respiration (TR) (del Giorgio et al., 1997). Thus, bacteria may not only in#uence rates of primary production, but they also play a major role in the ocean carbon balance and thus the ability of the ocean to absorb or release atmospheric CO .  One of the primary goals of the Joint Global Ocean Flux Study (JGOFS) program is to reduce the uncertainties in our understanding of the oceanic carbon cycle. Before useful models addressing the role of biological processes on carbon cycling can be developed, a basic understanding of the variability in and the factors controlling biological standing stocks and rate processes must be established. To this end, a number of studies have attempted to compare bacterial production rates (BP) and bacterial biomass (BB) with various other parameters including primary production (PP) and/or phytoplankton biomass (Bird and Kal!, 1984; Cole et al., 1988; Ducklow et al., 1993; Ducklow et al., 1995; Kirchman et al., 1995; Carlson et al., 1996; Lochte et al., 1997), temperature (Kirchman et al., 1995; Kirchman and Rich, 1997), and dissolved organic carbon (DOC) (Kaehler et al., 1997; Kirchman and Rich, 1997), with varying success. Experiments have been performed to address the factors controlling bacterial production and biomass including iron limitation (Pakulski et al., 1996; Tortell et al., 1996), nitrogen limitation (Rivkin and Anderson, 1997; Kirchman and Wheeler, 1998), bacterivory (Rivkin et al., 1999), and DOC/DON limitation (Kirchman, 1990). Probably, the biggest gap in most of these studies is the lack of respiration measurements, which are needed to estimate bacterial growth e$ciency, bacterial carbon demand, and ultimately balance the ocean carbon budget and determine CO  mineralization rates (Cole and Pace, 1995; Jahnke and Craven, 1995; del Giorgio et al., 1997; Williams, 1998). The subarctic NE Paci"c is of particular interest for understanding ocean biogeochemical processes. It is one of the major high nitrate low chlorophyll (HNLC) regions of the world ocean, where phytoplankton production is thought to be limited

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by iron supply (Martin et al., 1989; Boyd et al., 1996). In addition, Tortell et al. (1996) provided evidence suggesting that heterotrophic bacteria may be iron-limited in this region. Furthermore, line-P, a transect from the coast (Juan de Fuca Strait) to OSP, provides a unique gradient of physical (Whitney et al., 1998) chemical (Whitney et al., 1998; Varela and Harrison, 1999), and biological (LaRoche et al., 1996; Boyd et al., 1998; Boyd and Harrison, 1999) gradients from slope waters to HNLC oceanic waters. This region has one of the world's longest running oceanic time series with sea surface temperature measurements dating back to 1949 at Ocean Station Papa (OSP) and extensive biological data sets including PP dating back to 1956 (Tabata and Peart, 1985). However, despite these large data sets, the "rst research into heterotrophic bacterial processes in the subarctic NE Paci"c only took place at OSP in the late 1980s as part of the subarctic Paci"c Ecosystem Research (SUPER) program (Miller, 1993). Heterotrophic BB and BP were measured at OSP during four cruises in spring and summer of 1987 and 1988 (Kirchman et al., 1993). Kirchman (1990) also investigated the factors potentially limiting the bacterial growth rate (BGR) at OSP during these periods. Kirchman et al. (1993) reported relatively low BGR compared to other oceanic regions, and suggested that BGR was limited by temperature and DOM supply. While the SUPER study included 3-week occupations of OSP, and observed changes on the scale of weeks during both the spring and summer of 1987/1988, they did no winter studies and did not investigate respiration rates or the slope to open-ocean gradients. Also in 1987, the Vertical Transport and Exchange (VERTEX) program (Martin et al., 1989) visited OSP as part of their vertical particle #ux program, but focused primarily on particle-associated bacterial activity. Doherty (1995) and Boyd et al. (1995a,b) addressed BB and BP both along line-P and at OSP in May and February of 1993 and 1994, providing the "rst winter bacterial data set and the "rst bacterial data set across the slope to open-ocean gradient of line-P. However, Doherty (1995) and Boyd et al. (1995a,b) did not attempt to address factors controlling BB and BP, did not include data below the euphotic zone, and did not measure respiration. This study had three goals: (1) to extend the collection of data on heterotrophic bacterial processes in the subarctic NE Paci"c to encompass more years and more seasons to aid in the understanding of both seasonal and interannual variability, (2) to measure both total and bacterial respiration rates for the "rst time in this region, to provide a better understanding of bacterial in#uences on the ocean carbon budget, and (3) to address potential mechanisms of control for bacterial biomass, production, and respiration in the subarctic NE Paci"c.

2. Methods Data were collected during six cruises over a two-year period along the line-P transect (see map in the introduction to this issue). Sampling took place in late winter, spring, and late summer between September 95 and June 1997 (Table 1). Sampling was carried out, weather permitting, at all "ve of the JGOFS-Canada line-P stations (P4, P12, P16, P20, and OSP) on each cruise.

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Table 1 Cruise dates and labels Season

Date label

Cruise C

From}To

Summer

Sep 95 Sep 96 Feb 96 Feb 97 May 96 Jun 97

9512 9618 9601 9702 9609 9711

21-Aug}15-Sep 12-Aug}6-Sep 19-Feb}8-Mar 10-Feb}28-Feb 6-May}31-May 2-Jun}27-Jun

Winter Spring

Sampling for BB (bacterial cell counts) and BP was done using acid-cleaned 10 l GoFlo bottles mounted on a Kevlar line for euphotic zone sampling and from 10 l Niskin bottles mounted on a 24 bottle CTD/rosette for deeper samples. The GoFlo bottles were cleaned before each cruise with a 10% HCl acid soak for '24 h. Niskin bottles were not maintained under trace-metal clean conditions and the closure springs were well-aged latex tubing. Euphotic zone 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). Deep samples were collected at various times of the day. The six deep sampling depths were based on logarithmically increasing depth increments between the shallowest (1% light depth) and the deepest sample (&10 m above the seabed). Samples for the PP measurements discussed in this paper, and presented by Boyd and Harrison (1999) were drawn from the same bottle casts as the euphotic zone bacterial samples. Duplicate slides for the determination of bacterial abundance were made within 2 h of water sampling by "ltering 5}20 ml of DAPI stained sample onto black 0.2 lm pore size 25 mm diameter polycarbonate track-etched Poretics "lters (Turley, 1993). At least 300 cells were counted in a minimum of 10 "elds. Bacterial numbers were converted to BB (see discussion) using the conversion factor of 20 fg C cell\ (Lee and Fuhrman, 1987). BP estimates were based on either [H]-thymidine (September 1995 and May 1996) (Bell, 1993) or dual-labeled [H]-thymidine/[C]-leucine (September 1996}June 1997) (Chin-Leo and Kirchman, 1988) incorporation in 30 ml of sample during a 4 h incubation in the dark. Incubations were maintained at $23C of ambient sea-surface temperature in a dark deckboard incubator with a continuous #ow of surface seawater. An incubation time series was run to assess the in#uence of incubation time on incorporation rate and incorporation rate was linear over at least 8 h. Converting [H]-thymidine and [C]-leucine incorporation rates into production of cells was done empirically using the dilution method described by Kirchman and Ducklow (1993). The isotope conversion factors, calculated for the mixed layer at various stations between September 1996 and June 1997, were not signi"cantly di!erent from those found by Kirchman (1992) and thus 2;10 cells mol\ was used for [H]-thymidine and 0.11;10 cells molU was used for [C]-leucine. Final cell production was calculated as the average of the [H]-thymidine and [C]-leucine cell production values. Conversion of the "nal cell production into lg C l\ d\ was done based on 20 fg C cell\ (Lee and Fuhrman, 1987) (see discussion). No correction

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in BP to account for the di!erence between ambient temperature below the mixedlayer and the mixed-layer temperature at which all samples were incubated was attempted. Therefore, the reported deep BP estimates are likely to be an overestimate of the in-situ conditions for stations where the euphotic zone was deeper than the mixed-layer depth. Sampling for water column respiration rates was carried out in September 1996, June 1997, and June 1997 only. Water from 10 l Niskin bottles, mounted on a 24 bottle CTD/rosette was drawn either directly into 125 ml oxygen #asks for whole water samples or gravity fed directly from the Niskin bottles through a 1 lm nominal pore size capsule "lter (Gelman PN 12023) into the same type of oxygen #asks for the (1 lm size fraction. It was assumed that the majority of respiration in the (1 lm fraction was attributable to heterotrophic bacteria (see discussion in Williams, 1981a, b). Triplicate samples for both TR (whole water samples) and BR (sizefractionated samples) were drawn for both t"0 controls and incubation bottles, resulting in a total of 12 bottles per depth. Incubations were for 24 h for all cruises except June 1997 during which they were 48 h. Oxygen consumption was estimated from the di!erence in total oxygen between the t"0 controls and the incubated samples as measured using an automated microwinkler titration (after Furuya and Harada, 1995). The conversion of oxygen consumption in ml O to respiration in lg  C was based on the assumption of a 0.8 respiratory quotient (RQ) (Johnson et al., 1981) and gave a conversion factor of 429 lg C ml\ O .  Since bacterial processes can be sensitive to handling and may be enhanced by "ltration, it is possible that the BR derived from size-fractionated dark bottle O consumption over 24}48 h are an overestimate of the actual BR. To minimize this  bias, data from size-fractionated samples were carefully compared to both nonfractionated samples and killed controls (t"0) as discussed below. Since no coincident bacterial production measurements were made along with the dark-bottle incubations during this study, the most robust defense of BR values reported herein is that both the BGE and the BR : TR ratios were within the range of other published oceanic studies and the percentage of the samples eliminated as having clearly anomalous O consumption were minimal. Respiration values reported herein were  calculated from data that were passed through a data "lter, which removed `bada data points according to the following rules: (1) Incubated bottles containing more O than the matched t"0 bottle were removed; and (2) Size-fractionated incubated  samples with less O than the matched whole water incubated sample were removed.  The data "lter removed 15% of the samples from the respiration data set. Mean values reported throughout this paper for euphotic zone measurements were calculated as the stepwise integrated values for each of the six light depths divided by the depth of the euphotic zone (depth of 1% of surface irradiance). Thus, if these data are to be directly compared to the typically reported integrated PP (m\), the value reported here must be multiplied by the depth of the euphotic zone (Table 2). Other de"nitions used include: Bacterial growth rate (BGR)"BP/BB. Bacterial growth e$ciency (BGE)"BP/(BP#BR). Bacterial carbon demand (BCD)"BP#BR.

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Table 2 Depth (m) of the euphotic zone as de"ned by 1% of surface irradiance. Depth (m) of the primary seasonal thermocline shown in parentheses Season

Date

OSP

P20

P16

P12

P4

Spring

May 96 Jun 97 Sep 95 Sep 96 Feb 96 Feb 97

60 70 30 40 80 60

35 70 30 35 * *

40 65 30 40 80 60

60 75 30 40 50 60

35 75 25 30 40 45

Summer Winter

(50) (20) (25) (25) (100) (100)

(50) (30) (25) (25)

(50) (20) (25) (25) (100) (100)

(50) (30) (25) (20) (100) (100)

(50) (15) (25) (20) (100) (100)

Baterial sampling was not done at P20 during either winter cruise.

Calculations of BCD for stations P16 and OSP in February 1997 (when data were not collected) were based on the assumption that the measure of bacterial processes was nearly invariant along line-P in the winter (Fig. 1). Therefore, the values for BCD at P16 and OSP during February 97 were calculated from the BP using BCD"BP(1/BGE) with an assumed BGE of 10% (the average BGE for P4 and P12 where respiration was measured).

3. Results Since the di!erences between P4, the slope station, and OSP, the most oceanic station, were indicative of the overall line-P gradient, data from these two stations will be presented in the greatest detail. Generally speaking, OSP was similar to the other two oceanic stations (P16 and P20) while P4 was unique unto itself and P12 showed either intermediate or anomalous characteristics compared to P4 and P16 on either side of it. 3.1. Slope waters P4 euphotic zone BB (Fig. 1) ranged from 16 lg C l\ in the winter to 33 lg C l\ in the spring with an intermediate summer value of 24 lg C l\. In contrast to the other seasons, the spring BB peak observed in the euphotic zone continued down the whole water column (Fig. 2). However, the summer estimates of BB, which were intermediate in the euphotic zone, were the lowest below the euphotic zone. In general, BB decreased exponentially between the bottom of the euphotic zone and 1000 m. P4 euphotic zone BP ranged from 0.3 lg C l\ d\ in the winter, up to 15 and 20-fold higher in the spring and summer with values of 4.4 and 6.2 lg C l\ d\, respectively (Fig. 1). The peak summer BP was associated with only intermediate BB values, and the '10-fold increase in winter to spring BP was accompanied by only a 2-fold BB increase, indicating that changes in BB were strongly in#uenced by changes in loss processes (top}down control) and to a lesser extent by changes in BP.

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Fig. 1. Bacterial biomass (BB) and bacterial production (BP) along line-P during winter, spring, and summer. Data points represent the 2-year mean seasonal euphotic zone BB or BP calculated by stepwise integration of euphotic zone measurements divided by the depth of the euphotic zone. Bars represent the interannual range (n"2). Solid data points represent values based on a single station occupation.

If changes in BB were controlled strictly by production rates (bottom}up control) then higher BP would be accompanied by higher BB, which was not the case in the spring to summer transition, and only partially true for the winter to spring shift. The 1996 summer peak in upper ocean BP at P4 (Fig. 3) decreased by '10-fold between the bottom of the mixed layer (0}20 m) and the bottom of the euphotic zone (&30 m), giving rise to deep summer BP closer to winter values than to spring. Spring BP below the mixed layer was high relative to other seasons, showing a similar pattern to spring BB. A regression of P4 euphotic zone BP against temperature (Fig. 4)

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Fig. 2. Vertical depth pro"les of bacterial biomass at stations P4 and OSP during winter, spring, and summer. Line breaks between data points indicate di!erent casts (separate sampling periods).

Fig. 3. Vertical depth pro"les of bacterial production at stations P4 and OSP during winter, spring, and summer. Line breaks between data points indicate di!erent casts (separate sampling periods).

revealed a general increase in BP associated with increased temperature (r"0.50, n"33). Respiration rates at P4 in the summer (September 1996) were '10-fold higher than in either winter (February 1997) or spring (June 1997) for both TR and BR (Fig. 5). BR accounted for ca. 20% of the TR in the spring and ca. 60% in the summer (Table 3). However, BR was indistinguishable from TR in the winter. The calculated BCD of 120 lg C l\ d\ in the summer was ca. 20-fold greater than the winter and

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Fig. 4. P4 bacterial production regressed against temperature in the euphotic zone during winter (䊐), spring (䉭), and summer (*). y"0.869x !5.8, n"33, r"0.50. The euphotic zone was deeper than the mixed layer in several cases.

Fig. 5. Total respiration (TR, "lled symbols) and bacterial respiration (BR, open symbols) along line-P during winter, spring, and summer. Data points were calculated from a stepwise integration of euphotic zone measurements divided by the depth of the euphotic zone. The error associated with each data point is $50% at a 95% con"dence (not shown).

spring BCD of 4 and 7 lg C l\ d\, respectively (Fig. 6). However, BGE showed a strikingly di!erent picture with summer and winter being comparable at 5}10% and spring BGE being '60% or ca. 10-fold higher. The summer euphotic zone BP : PP ratio at P4 was 0.3 and 0.1 (derived from Boyd and Harrison, 1999) in September 1995 and September 1996 respectively (Fig. 7). The

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Table 3 Percent of community respiration accounted for by bacterial respiration Season

OSP

P20

P16

P12

P4

Spring (June 97) Summer (Sep 96) Winter (Feb 97)

83 25 *

77 24 *

42 51 *

10 53 54

16 58 *


Samples not collected due to weather conditions.
Size-fractioned incubation samples showed greater respiration than the whole water samples.

winter and spring BP : PP ratios were ca. 0.05. The BCD : PP ratio was ca. 0.5 in the winter and ca. 0.1 in the spring, but '1.0 in the summer (September 1996) due to high BP and low BGE (Fig. 7). 3.2. HNLC open-ocean waters BB in the euphotic zone at OSP was low in the winter (ca. 11 lg C l\) and increased ca. 2-fold to around 24 lg C l\ in the spring and summer (Fig. 1). Below 100 m depth there was only a small di!erence in BB between seasons (Fig. 2), indicating a minimal seasonal response below the mixed layer to the stronger seasonality above. Samples from near the sea bed (4000 and 4200 m) typically showed a slight increase in BB relative to shallower samples. BP in the euphotic zone at OSP (Fig. 1) was the highest in the summer (1.7}2.6 lg C l\ dU), lowest in the winter (0.2}0.6 lg C l\ d\) and intermediate during the spring (0.6}0.1 lg C l\ d\). Intriguingly, a similar BB in spring and summer, was associated with a seasonal increase in BP from spring to summer, suggesting that the increased summer BP was countered by increased summer loss processes. A regression of BP against temperature (Fig. 8) showed a strong relationship (r"0.88, n"33) between temperature and BP. BP was nearly constant with depth in the mixed layer during all seasons, then decreased immediately below it, regardless of euphotic zone depth (Fig. 3). Unlike BB, there was substantial variability in BP below 100 m during most cruises, indicating a patchiness in BP that was not apparent in the BB pro"les. BR at OSP was indistinguishable from TR during spring (June 1997) and was ca. 10 lg C l\ d\ (Fig. 5). However, TR in the summer was ca. 15 lg C l\ d\ compared with BR at ca. 4 lg C l\ d\. Thus, BR accounted for the majority of the TR in spring and ca. 25% in summer (Table 3). Since BP was low relative to BR, BCD was dominated by the respiration signal, giving a high spring BCD of ca. 11 lg C l\ d\ and a summer low of ca. 6 lg C l\ d\, similar to that estimated for winter (Fig. 6). High BR and low BP in the spring provided for a low BGE of ca. 10%, increasing to ca. 40% during the summer. The mean BP : PP ratio in both winter and spring was ca. 0.7, whereas the summer BP : PP ratio ranged from 0.2 in September 1995 to 0.08 in September 1996

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Fig. 6. Bacterial growth e$ciency and bacterial carbon demand (BCD) along line-P during winter, spring, and summer. Data were collected only over 1 yr (September 1996, February 1997, and June 1997). Filled symbols were calculated from bacterial production assuming 10% growth e$ciency based on P4 and P12 winter measurements. Error bars represent 95% con"dence intervals (n"6).

(Fig. 7). From the BP : PP ratios alone, it would appear that bacterial utilization of phytoplankton-derived carbon may be proportionately highest in the summer; however, taking into acccount BGE, the opposite appears to be the case. The BCD : PP ratio was '1.0 during the spring, decreasing to (0.5 in the summer (Fig. 7). 3.3. Trends along the line-P In general, there was little di!erence in the magnitude of either BB or BP (Fig. 1) between any of the line-P stations during the winter. Spring and summer BB along line-P was much more variable than winter and averaged about twice the winter BB. BP was highest at P4 during the spring and summer, with the three most oceanic stations showing little di!erence among them. Respiration (Fig. 5) and BCD (Fig. 6)

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Fig. 7. Bacterial production to primary production ratios (BP : PP) and bacterial carbon demand to primary production ratios (BCD : PP) along line-P during winter, spring, and summer. Data points were calculated from a stepwise integration of euphotic zone measurements divided by the depth of the euphotic zone. Bars represent the interannual range for BP : PP (n"2) and the 95% con"dence intervals (n"6) for BCD : PP.

Fig. 8. OSP bacterial production regressed against temperature in the euphotic zone during winter (䊐), spring (䉭), and summer (*). y"0.221x!0.852, n"33, r"0.88. The euphotic zone was deeper than the mixed layer in several cases.

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were much higher at P4 in the summer compared with the rest of line-P. BGE showed opposite spring and summer trends, with spring BGE being high nearshore and decreasing o!shore compared to summer BGE being low nearshore and increasing further o!shore (Fig. 6).

4. Discussion When considering the data presented in this paper, it must be kept in mind that both BB and BP numbers are based on an assumed cellular carbon content of 20 fg C cell\, which has been used widely in the literature (Lee and Fuhrman, 1987). The cellular carbon content was not directly measured in this study, and recent work by Fukuda et al. (1998) suggests that the cellular carbon in open-ocean bacteria averages closer to 12 fg C cell\ and is lower still in the HNLC equatorial Paci"c and southern oceans, with values of 5.9 and 6.5 fg C cell\, respectively. These uncertainties in cellular carbon content are inconsequential to the comparisons between BB and BP presented in this study because any errors in estimating bacterial carbon are matched in both BB and BP. However, if bacterial production was overestimated by 50% (20 vs. 10 fg C cell\), then BP : PP and BGE would be overestimated by about a factor of 2, and since the respiration calculations were independent of cellular carbon conversion factors, the BCD reported herein would be overestimated by 3}30% depending whether BGE was low or high. 4.1. Slope waters vs. the HNLC Open ocean There is little di!erence in the magnitude of BB observed at the two end-members of line-P (P4 and OSP) during either summer or winter. Boyd and Harrison (1999) also report low and constant levels of phytoplankton biomass and production along line-P in the winter. However, in the spring, BB was elevated in the slope waters relative to the open ocean. Although winter BP was similar at both P4 and OSP, BP increased 20-fold between winter and summer at P4 compared to a reduced seasonality (5-fold di!erences in BP) at OSP. These elevated BB and BP at P4 may be indicative of the di!erent annual phytoplankton cycles observed in these regions with P4 experiencing spring bloom conditions (Boyd and Harrison, 1999; Thibault et al., 1999), and OSP displaying little seasonal variability in chlorophyll (Parslow, 1981; Miller, 1993). At P4, the magnitudes of BP in the spring and summer were similar, whereas at OSP, the spring and winter BP were similar indicating a slower seasonal response at OSP than closer to shore. At P4, the biggest increase in BP relative to BB was between winter and spring, suggesting a substantial increase in loss processes in the spring relative to the winter at P4. At OSP, the biggest increase in BP relative to BB (biggest increase in loss processes) was between spring and summer. Interestingly, both these increases in apparent loss processes coincided with the disappearance of the copepod Neocalanus plumchrus from the surface waters (Goldblatt et al., 1999) (discussed further below).

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Though concurrent grazing experiments were only done at OSP (see Rivkin, 1999), the discrepancies between BP and BB at both stations suggest top}down control of BB. At P4 the seasonal temperature change described a relatively small proportion of the seasonal change in BP, whereas at OSP temperature may be responsible for a substantial portion of the seasonal change in rates of BP in both the present, and in previous studies (Kirchman et al., 1993). Although based on a limited data set, these "ndings suggest that di!erent processes were controlling BP in the slope waters than in the open ocean. Spring levels of BB and BP showed an increase relative to winter over the entire water column at P4, whereas at OSP there was no clear seasonal response below 100 m, the approximate depth of the permanent pycnocline. If increases in BB and BP are associated with increased substrate derived from surface phytoplankton production, then increased bacterial activity at depth implies an increased input of surface material to depth. Conversely, a reduction in bacterial seasonality at depth may imply a reduction in the export of surface material to depth. Also export ratios, from thorium disequilibria, indicate more seasonality and higher rates of downward POC #ux over the annual cycle at P4 than at OSP (Charette et al., 1999). These observations support the idea that spring PP at P4 may consist of larger phytoplankton, contributing to greater downward export #ux, whereas at OSP and during late summer at P4 PP may be dominated by smaller phytoplankton that are primarily recycled in the mixed layer and contribute little to downward export #ux. There was relatively little di!erence in respiration rates between P4 and OSP during spring. However, during summer, P4 showed a '10-fold increase in both BR and TR relative to other seasons. BCD followed the trends observed for respiration including a pronounced increase in BCD at P4 in the summer. BGE showed strikingly opposite spring and summer trends at P4 and OSP with BGE being lowest ((10%) during the summer at P4 and during the spring at OSP. Conversely, BGE was highest in the spring at P4 ('50%) and in summer at OSP (ca. 40%). The high summer BGE at OSP and the low summer BGE at P4 may be counterintuitive since P4 and OSP are generally characterized by high and low dissolved iron levels, respectively (LaRoche et al., 1996), and Tortell et al. (1996) suggest that low iron may reduce BGE. However, the low BGE in the slope water may be explained by nitrogen stress since nitrate depletion is a summer feature of the P4 region (Whitney and Freeland, 1999), and it has been suggested that nitrogen limitation can signi"cantly reduce BGE (Goldman et al., 1987). There was not a discernible di!erence between P4 and OSP in the ratio of BP : PP despite pronounced di!erences in BP between these stations. These ratios are within the range presented in a review of both marine and freshwater systems by Bird and Kal! (1984). These data suggest that if there is a direct relationship between BP and PP, then regardless of the absolute level of PP, the proportion utilized by heterotrophic bacteria was relatively constant regardless of the di!erences between these two systems. BCD, dominated by BR, was a signi"cant percentage of PP at P4 in the summer (September 1996) and at OSP in the spring (June 1997) (Fig. 7), suggesting that

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bacteria respire a signi"cant proportion of PP and possibly an excess of DOC beyond the concurrent PP. BR'PP would imply that the system was not in steady-state during these times as suggested by VeH zina and Savenko! (1999) for the spring at OSP, and that the heterotrophic bacteria were consuming DOM either accumulated at a previous time or advected into the area. Alternatively, the phytoplankton could have lost a signi"cant portion of their "xed carbon to the DOC pool via excretion, sloppy zooplankton feeding and/or viral lysis (i.e. autochthonous DOC not measured as part of the net primary production), and thus account for an apparent BR'PP in a steady-state system. 4.2. Trends along line-P In general, there was little di!erence 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 and averaged about twice the winter BB, a trend also noted for this transect in 1993/4 (based on a limited data set) by Doherty (1995). BP was highest at P4 during the spring and summer with the three most oceanic stations showing little di!erence between them. Boyd and Harrison (1999) report little di!erence in PB or PP levels between P16, P20 or OSP in spring and summer. Summer respiration rates and BCD were much higher at P4 than further west along line-P. BGE showed opposite spring and summer trends, with spring BGE being high nearshore and decreasing o!shore compared to summer BGE being low inshore and increasing further o!shore. 4.3. Bacterial respiration, carbon demand, and growth ezciency The contribution of BR to TR, although variable in the present study, falls within the range noted for marine systems (see review by Williams, 1981a,b). The large changes in BGE with season, both in the slope waters and in the open ocean, were driven primarily by changes in BR rates, supporting the plea by Jahnke and Craven (1995) for more microbial respiration measurements. Data for the molecular marker for algal iron stress, #avodoxin, indicates that algal cells were not iron-stressed at P4 in summer when low BGE was observed, but were iron-stressed at OSP in summer when a high BGE was observed (LaRoche et al., 1996). Thus, it appears that reduction in BGE was not driven by reduced levels of iron, su$cient to stress the algal community, but that low BGE may be tied to low nitrogen at P4 and to substrate quality or other yet unexplained interactions at OSP. 4.4. Comparison to other studies The levels of BB and BP in the present study at OSP in winter and spring/summer are comparable to, though at the high end of, those reported by Boyd et al. (1995a,b) and Kirchman et al. (1993) (Table 4). As in the present study, the previous studies noted the homogeneous distributions of BB, and of rates of BP in the surface mixed

NE Paci"c NE Atlantic NW Atlantic Sargasso Sea

Spring NE subarctic Paci"c

Equatorial Paci"c Sargasso Sea

Winter NE subarctic Paci"c

Season and location

Jun-87 May-88 May-93 May-94 May-96 Jun-97 Jun-92 May-89 Apr}May 89 Apr-92

Mar-93 Feb-94 Feb-96 Feb-97 Feb}Mar 92 Oct-91 Nov-92 Jan-94 Mar-92 Mar-93

Date of study

12}23 7}25 19.7 18.4 25 21 2 26.1 8}40 2.1

13 13 9 10.4 2.4 2.3 1.8 2.4 1.7

BB

0.24 0.5 0.5

1.82 0.87

1.7 1 0.6 6.1 1.3}7.1 0.19

0.69 0.08 0.64 0.98 1.3 0.76 0.49 0.7 0.18

BB : PB

0.86 1.04

10 52

10

16

4

BR

0.2}11 0.1}1.5 0.76

0.55 0.77 0.6 0.2 1.04 0.12 0.13 0.08 0.19 0.14

BP

0.28 0.1-0.3 0.02

0.03 0.12

0.053 0.134

0.29 0.22 0.11 0.04 0.21 0.05 0.15 0.02 0.07 0.06

BP :PP

Kirchman et al. (1993) Kirchman et al. (1993) Doherty (1995) Doherty (1995) This study This study Cherrier et al. (1996) Ducklow et al. (1993) Li et al. (1993) Carlson et al. (1996)

Boyd (1995) Boyd (1995) This study This study Kirchman et al. (1995) Carlson et al. (1996) Carlson et al. (1996) Carlson et al. (1996)
Carlson et al. (1996) Carlson et al. (1996)


Reference

Table 4 Europhotic zone bacterial biomass (BB), bacterial production (BP), bacterial respiration (BR), bacteria to phytoplankton biomass ratios (BB : PB), bacteria to phytoplankton production ratios (BP : PP) selected from the literature. Biomass units are lg C l\ and production and respiration units are lg C l\ d\. Where only bacterial cell counts were reported, they were converted to biomass assuming 20 fg C cell\. Where only Chlorophyll-a was reported, it was converted to biomass assuming a C : Chl ratio of 50 : 1

2572 N.D. Sherry et al. / Deep-Sea Research II 46 (1999) 2557}2578

Oct-92 Nov-92 Oct-92 Nov-92

Sep-87 Aug-88 Sep-95 Sep-96 Aug}Sep 92 Jul-92 Jul}Aug 93 4}10 8}20 2-6 2-6

12}25 16}24 27 24 12 2.9 2.8 0.4}1.4 0.5}2 0.2}0.3 0.2}0.3

0.6}1.5 0.8}2.3 2.6 1.7 1.2 0.14 0.26

Value extrapolated from data collected at more coastal stations (see text).
BR values calculated from Carlson and Ducklow (1996).

Circumpolar Current

Southern Ocean Polar Frontal Region

Equatorial Paci"c Sargasso Sea

Summer NE subarctic Paci"c

0.5}5

3

3.8

0.37

0.23

0.91 0.94 1.29 1.49 0.87 1.29 1.07

0.22

0.16

0.151 0.124 0.21 0.08 0.17 0.08 0.05 Lochte et al. (1997) Lochte et al. (1997) Lochte et al. (1997) Lochte et al. (1997) Kaehler et al. (1997)

Kirchman et al. (1993) Kirchman et al. (1993) This study This study Kirchman et al. (1995) Carlson et al. (1996)
Carlson et al. (1996)

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layer. Kirchman et al. (1993) estimated that bacteria consumed from 10 to 24% of PP in the euphotic zone based on an assumed 50% BGE. The BP : PP ratios in the present study from spring and summer were similar to those reported by Kirchman et al. (1993). Furthermore, Kirchman et al. (1993) reported that observed increases in BB and BP during spring and summer 1987 and 1988 did not appear to correspond to changes in the magnitude of PB or PP. In the present study, increases in the summer BP as OSP were not re#ected in higher BB, suggesting that increased summer loss processes provided top}down control of BB. Grazing experiments done concurrently with the present study (Rivkin et al., 1999) showed a substantial increase in summer bacterivory rates relative to winter and spring, supporting the idea that changes in loss processes limited BB during the summer. Increased grazing e$ciency could come about because of changes in bacterial or grazer community structure, increases in the number of grazers, or a temperature increase driving increased grazer activity. Though the actual mechanisms responsible for the increase in loss processes are not elucidated in this study, it is interesting to note that N. plumchrus, an abundant copepod that migrates out of OSP surface waters in late spring (Goldblatt et al., 1999), is capable of grazing on the protists which graze on heterotrophic bacteria. The departure of N. plumchrus may release bacterivorous protists from grazing pressure and thus allow protist numbers to increase. The increased protist numbers may then provide a mechanism for increased bacterial loss processes in the summer relative to winter and spring at OSP. Unfortunately, this hypothesis is neither conclusively supported nor refuted by the observed seasonal changes in the total number of protists (Booth et al., 1993; Rivkin et al., 1999). Kirchman et al. (1993) calculated that BGR was low ((0.1 d\), relative to phytoplankton growth rates (0.1}0.8 d\), a trend also noted in the present study (BP/BB, not shown, but compare both panels in Fig. 1). They suggested that BGR was controlled by both temperature and DOM supply; the former also being observed (strong relationship between BP and temperature) in the present study. Kirchman (1990) found BGR to be limited by DOM supply in the late summer during both 1987 and 1988 when he reported increases in both BGR and BGE with the addition of DOM. Tortell et al. (1996) observed that resident bacteria at OSP in September 1995 had iron quotas similar to those in iron deplete cultures of both oceanic and coastal bacterial isolates. Tortell et al. (1996) presented indirect evidence that iron-de"cient cells at OSP would likely have carbon growth e$ciencies of 0.12}0.23. In the present study, BGEs of 0.1 and 0.4 were estimated from spring and summer. While the former BGE is consistent with iron-de"cient cells, the latter may not be, suggesting that the control of BGE is independent of iron stress at OSP. Compared with other oceanic regions (Table 4), the winter in the subarctic NE Paci"c appears to support a BB similar to the Equatorial Paci"c (another HNLC region) and roughly 5-fold greater than the Sargasso Sea. Winter BP in the subarctic NE Paci"c is about  that of the Equatorial Paci"c and about 4-fold greater than the  Sargasso Sea. In comparison, the summer increase in both BB and BP were about 2-fold in the subarctic NE Paci"c, whereas there is comparatively little increase in the summer values in either the Equatorial Paci"c or the Sargasso Sea. Thus the subarctic NE Paci"c supports greater summer BB and BP than either of these other two

N.D. Sherry et al. / Deep-Sea Research II 46 (1999) 2557}2578

2575

regions. In the Southern Ocean during austral spring, the polar frontal region shows values similar to or slightly lower than the summer values in the subarctic NE Paci"c, whereas the circumpolar current region (another HNLC area) shows values more in the range of the Sargasso Sea. Compared with the spring bloom in the North Atlantic, spring in the subarctic NE Paci"c boasts BB values of only  and BP values of ca. .   5. Conclusions The subarctic NE Paci"c and the line-P transect o!er a unique opportunity to study bacterial processes over a range of changing environments from slope waters, which are seasonally in#uenced by coastal processes and macronutrient depletion to open-ocean HNLC waters where macronutrients are plentiful and primary production appears to be limited by iron and grazing pressure. It appears that changes in loss processes, such as changes in grazer e$ciency or viral infection rates, played a signi"cant role in controlling BB along line-P. Seasonal changes observed in BP were strongly correlated with changes in temperature at OSP. At P4 the correlation between BP and temperature was weaker, implying that the mechanisms controlling BP di!ered between P4 and OSP. Seasonal changes in BP and BB were observed in the mixed layer, but not observed below 100 m (the permanent pycnocline), with the exception of spring at P4, implicating that seasonal changes in downward export of organic material was probably bu!ered by recycling within the mixed layer. BR and the associated BGE changed dramatically both seasonally and spatially, endorsing the need for regular respiration measurements as an integral part of any study attempting to quantify the microbial carbon budget. The enhanced seasonality of bacterial processes in the slope waters relative to the open-ocean probably re#ects the more dynamic physical environment associated with the continental slope. Compared to other oceanic regions, the subarctic NE Paci"c appears to have generally greater BB while supporting similar BP. This study represents the "rst comprehensive data set on bacterial processes for the line-P transect. Acknowledgements We thank the o$cers and crew of the CCG vessel John P. Tully, Frank Whitney, Tim Soutar, Bernard Minkley, and John Love (IOS, Canada) for technical advice and assistance, and Hugh Maclean and Michael Lipsen (UBC, Canada) for tremendous help with sampling and sample analysis. We acknowledge Julie LaRoche (BNL, USA) for the provision of unpublished data. Support for this work comes from NSERC (Canada) via grant awards to the JGOFS-Canada program. References Berman, T., Nawrocki, M., Taylor, G.T., Karl, D.M., 1987. Nutrient #ux between bacteria, bacterivorous nanoplanktonic protists and algae. Marine Microbial Food Webs 2, 69}82.

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