the seasonal development of the bacterioplankton … seasonal development of the bacterioplankton...

Deep-Sea Research II 48 (2001) 4199–4221

The seasonal development of the bacterioplankton bloom inthe Ross Sea, Antarctica, 1994–1997

Hugh Ducklowa,*, Craig Carlsonb, Matthew Churcha, David Kirchmanc,David Smithd, Grieg Stewarde

aThe College of William and Mary School of Marine Science, Box 1346 Rte 1208 Greate Road,Gloucester Point, VA 23062, USA

bBermuda Biological Station for Research, Ferry Reach, St. Georges GE-01, BermudacCollege of Marine Studies, University of Delaware, Lewes, DE 19958, USA

dGraduate School of Oceanography, University of Rhode Island, Narragansett, RI 02882, USAeMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA

Received 12 February 2000; received in revised form 9 October 2000; accepted 16 November 2000

Abstract

We report on investigations of bacterioplankton growth dynamics and carbon utilization in the full watercolumn of the Ross Sea, Antarctica carried out on six cruises in 1994–1997, using epifluorescencemicroscopy, thymidine and leucine incorporation to estimate bacterial abundance and production,respectively. The Ross Sea experienced a bacterial bloom with an amplitude equaling similar bloomsobserved in the North Atlantic and North Pacific, reaching 3� 109 cells l�1 or 35 mmol C m�2 in lateJanuary. Increases in bacterial biomass were driven both by increases in abundance and in cell volume. Cellvolumes ranged from 0.03 mm3 cell�1 in early spring to over 0.15 mm3 cell�1 in midsummer. Larger cells wereassociated with faster division rates. Bacterial growth rates ranged 0.02–0.3 divisions d�1, equal to rates atlower latitudes. Bacterial biomass accumulated steadily in the upper water column at a net rate of 0.03 d�1.While there is clear evidence of a bacterial bloom in the Ross Sea, equal to bacterioplankton bloomsobserved in other oceanic systems, the magnitude of bacterial response relative to the phytoplankton bloomwas modest. For example, euphotic zone bacterial production (BP) rates were equivalent to 1–10% ofparticulate primary production (PP) except in April 1997 when PP was very low and BP : PP was somet-imes >1. BP integrated over the upper 300 m was a more substantial fraction of the overlying PP than BPin the euphotic zone alone, with bacterial carbon demand in the upper 300 m about 30% of the seasonal PP.There was significant seasonal variation of bacterial biomass below the euphotic zone, indicating dynamicbacterial growth in the lower layer, and a supply of labile organic matter for bacteria. Bacterial metabolismis apparently limited by DOC flux in the upper layer. There is little evidence of temperature limitation,independent of substrate concentration. The relatively small diagenesis of phytoplankton biomass in the

*Corresponding author. Fax:+1-804-684-7293.

E-mail address: [email protected] (H. Ducklow).

0967-0645/01/$ - see front matter r 2001 Elsevier Science Ltd. All rights reserved.

PII: S 0 9 6 7 - 0 6 4 5 ( 0 1 ) 0 0 0 8 6 - 8

euphotic zone implies that there is relatively more organic matter available to support bacterial metabolismin the lower water column. r 2001 Elsevier Science Ltd. All rights reserved.

1. Introduction

At least as suggested by the growing number of original articles, reviews and reports, there ispossibly as much, if not more, known about bacterioplankton ecology in Antarctic seas andmarginal ice zones as anywhere in the world ocean, with the exception of estuaries (Ducklow andCarlson, 1992; Ducklow, 1999). In spite of the remote location and daunting logistical andclimatic challenges, there have even been several comprehensive studies extending across thegrowth season at several coastal sites (Billen and Becquevort, 1991; Bird and Karl, 1991, 1999;Karl et al., 1991, 1996; Rivkin, 1991; Karl, 1993; Clarke and Leakey, 1996; Leakey et al., 1996).There have been fewer investigations in winter (Mordy et al., 1995). However, despite theaccumulating data on bacterial stocks and dynamics in the Antarctic, there is little agreement onthe principal factors regulating bacterial growth in cold waters. For example, Karl (1993)suggested that bacterial production in the Antarctic was uncoupled from primary production(PP), and speculated that bacterial–phytoplankton interactions were fundamentally different fromother systems. However, Lochte et al. (1997) disagreed, finding only a greater temporal shiftbetween phytoplankton and bacterial development. The temperature of Antarctic coastal seas ispersistently cold (o21C) and previously was thought to prevent significant bacterial activity(Sorokin, 1971). But bacteria are active and numerous in these waters (Fuhrman and Azam, 1980;Azam et al., 1991; Karl, 1993), and different seasonal patterns are found in the same temperatureregime, so clearly temperature limitation alone cannot explain bacterial variability in theAntarctic.

Using a numerical model Billen and Becquevort (1991) showed that temporal and spatial lagsbetween Antarctic phytoplankton and bacterial production maxima were similar to temperatesystems, a result of bacterial reliance on polymeric organic matter, which was hydrolyzed toutilizable monomers over a time scale of weeks. Pomeroy and co-workers (Pomeroy and Deibel,1986; Pomeroy et al., 1991; Wiebe et al., 1992, 1993) redefined the debate on heterotrophic activityin cold waters by focusing on the interaction between temperature and organic matter availability.They showed that bacterial activity could be severely limited near the low end of the annualtemperature range in a given system (e.g., �1.81C in the Antarctic) in the absence of a sufficientconcentration of available dissolved organic matter. When organic matter exceeded some limitingconcentration, temperature inhibition was alleviated (Wiebe et al., 1993). The ‘‘PomeroyHypothesis’’ might now be considered the governing paradigm for investigating bacterialdynamics in cold waters, or for reacting against (Rivkin et al., 1996).

The central Ross Sea is covered seasonally with sea ice 1–3 m thick, and experiences one of themost spatially extensive and pronounced phytoplankton blooms on the planet (Arrigo andMcClain, 1994). The bloom is dominated by the colonial haptophyte Phaeocystis antarctica(Smith and Gordon, 1997; Sweeney et al., 2000), usually begins in early to mid-November, andreaches its peak in mid-December–early January, with peak Chl a concentrations exceeding10mg l�1. The bloom is initiated earlier than in other Antarctic locations, following the formation

H. Ducklow et al. / Deep-Sea Research II 48 (2001) 4199–42214200

of a polynya, which usually opens near the Ross Ice Shelf by early November. Because of theannual development of the Ross Sea Polynya, which can be detected by remote sensing, the RossSea bloom is both predictable and easily located. The central to western Ross Sea circulation ischaracterized by a still poorly defined cyclonic gyre and by a warm (>�11C) deep inflow acrossthe shelf break (Modified Circumpolar Deep Water, MCDW) and a cold (o�21C) deep inflow tothe north from under the Ross Ice Shelf (Picco et al., 1999; Jacobs and Giulivi, 1999). The polynyais maintained by northward ice and water transport driven by katabatic winds. This regionbecame the primary focus of United States Joint Global Ocean Flux Study’s AntarcticExperiment Southern Ocean Process Study (US JGOFS AESOPS) cruises in 1996–1997.

Carlson et al. (1998, 2000) showed that in the Ross Sea, even with very high rates of PP andphytoplankton biomass, the time-integrated flux of carbon through the DOC pool, and throughthe bacterioplankton, was very low, averaging 11% of the net drawdown of dissolved inorganiccarbon (net community production, NCP). This geochemical estimate of DOC flux places a strongconstraint on seasonal to annual estimates of bacterial carbon demand. Carlson et al. (1998, 2000)suggested that bacterial production was limited by carbon availability, and they also showed thatthe DOC produced over the growing season was labile on a time scale of B6 months. That is, allthe accumulated or excess DOC above the background concentration was consumed by the end ofthe season (Carlson et al., 2000), in contrast to other regions where accumulated DOC persistsuntil the following winter (e.g., Bermuda, Carlson and Ducklow, 1994) or persists more or lessindefinitely as a result of continuous production, slow remineralization and export (e.g.,equatorial Pacific, Carlson and Ducklow., 1995; Hansell and Carlson, 1998). It is notable that lowtemperature does not prevent bacterial utilization of the net DOC production within the growthseason in the Ross Sea.

Here we present a comprehensive data set on bacterial stocks and production in the Ross Seaextending from late winter to late autumn, and show that even though the ratio of BP to PP is low,the region experiences on an absolute scale one of the largest amplitude bacterial blooms in theworld ocean. Bacteria in the upper 300 m utilize about 30% of the annual PP.

2. Methods and materials

2.1. Study area and sampling

All sampling was conducted in the central Ross Sea during six cruises aboard RVIB NathanielB. Palmer (Table 1). The cruises in 1994 and 1995–1996 formed the Ross Sea Polynya Project(Carlson et al., 1998). The four cruises in 1996–1997 were cruises P1–P4 of the US JGOFSAESOPS. The six cruises distinguish five seasonal periods: late winter/early spring, 1996; latespring 1994 and 1997; summer, 1995; late summer, 1997 and autumn, 1997 (Table 1). CruisesP1–P3 were all conducted in the 1996–1997 growing season. The 1994 cruise and P4 coveredalmost the same dates in 1994 and 1997 and allowed us to examine interannual variations duringthe spring season. Most sampling was on a transect along latitude 76.51S, extending generallybetween longitude 1781W (Station Orca) and 1691E (Station Minke) (see map in Carlson et al.,2000). At most stations, sampling was conducted through the entire water column, from thesurface to within 10 m of the bottom (depths 300–800 m), with sampling density emphasizing the

H. Ducklow et al. / Deep-Sea Research II 48 (2001) 4199–4221 4201

euphotic zone. Rate measurements were conducted in the upper 150 m on the R94-95 cruises, andthroughout the water column on the AESOPS cruises.

All bacteriological sampling was conducted during hydrocasts using Niskin bottles with epoxyresin-coated springs and coated metal hardware, on a CTD-Rosette system. Core hydrographicproperties and dissolved organic carbon (DOC) were measured on the same casts. Primaryproductivity (PP) sampling was conducted using the same CTD-Rosette system on the R94-95cruises, and most bacteriological sampling was synoptic with the PP sampling. On the AESOPSP1–P4 cruises, PP sampling was conducted using a separate trace metal-free (TM) rosette system,whereas the corresponding bacteriological data are from Niskin casts immediately preceding orfollowing the TM casts. Water for bacteriological work was subsampled from the Niskin bottlesusing acid-washed, distilled water and sample-rinsed opaque polycarbonate bottles in the ‘‘BalticRoom’’ of the NB Palmer under near in situ temperature and subdued light.

2.2. Measurements

Bacterial abundance was determined using digital image analysis of video images of acridineorange (AO) stained samples prepared following the JGOFS Protocols (Knap et al., 1994). Forour work, 10–100 ml of water, depending on the abundance, were concentrated on black, 0.2-mmpore size polycarbonate filters to deposit B30 cells within the 10� 10mm field of view of the videocamera. Filters were prepared and mounted on microscope slides within 24 h of sampling andstored frozen until analysis at Virginia Institute of Marine Science (VIMS) using a Zeiss Axiophotepifluorescence microscope (1250� magnification) equipped with a solid-state video camera

Table 1Ross Sea cruises, 1994–1997 with mean surface layer hydrography in the vicinity of 73–76oS lat., 164oE–1681W long.a

Season Espr96 LSpr94 LSpr97 Sum95 LSum97 Aut97

Cruise P1 R94 P4 R95 P2 P3

Dates 17 Oct–06Nov 96

14 Nov–06 Dec 94

14 Nov–12 Dec 97

16 Dec 95–13 Jan 96

12 Jan–09 Feb 97

12 Apr–02 May 97

Days of year 291–311 318–340 319–346 354–013 012–037 102–118

Temp. (1C) Mean �1.85 �1.76 �1.60 �0.276 0.01 �1.84Upper 20 m Std 0.07 0.06 0.29 0.723 0.45 0.10

n 1194 364 428 445 421 379

NO3 (mmol l�1) Mean 31.04 26.29 26.72 19.432 12.87 26.86

Upper 20 m Std 0.38 2.94 4.16 4.312 5.62 2.11n 808 364 276 435 355 182

Chl a (mg l�1) Mean 0.19 2.85 1.71 4.39 2.50 0.03EZ meansb Std 0.19 2.22 2.12 2.55 1.39 0.02

n 12 38 28 33 14 11

a Columns and cruises are arranged in order of seasons (dates) not years. The three italicised columns are part of onecontinuous growing season (1996–1997).

b Calculated from the integrated Chl stock (mg m�2) in the euphotic zone (EZ) at each station, divided by the EZ

depth (0.1% of surface illumination). Thus n is the number of stations.


(Photometrics CH250 CCD) and ImagePro image analysis software. Details of biomass analysisconducted during theses cruises is presented in Ducklow et al. (1999) Between-operator estimatesof total biovolume (abundance times mean cell volume) varied by 5–10%.

Bacterial production was estimated from simultaneous measurements of high specific activitymethyl-3H-thymidine (TdR; SA >70 Ci mmol�1) and 3,4,5-3H-leucine (Leu: SA >140 Ci mmol�1)incorporation into cold, 5% trichloroacetic acid extracts generally following the JGOFS Protocols(Knap et al., 1994). In 1994, triplicate 50-ml water samples were incubated and filtered onto 0.45-mm mixed cellulose ester filters for liquid scintillation analysis (Ducklow et al., 1995). On allsubsequent cruises, we followed the microcentrifuge method (Smith and Azam, 1992), incubatingand processing triplicate 1.7-ml samples in polypropylene microcentrifuge tubes. All samplepreparation and processing was conducted in subdued light near in situ temperature in a radiationvan. Samples were incubated in darkened, refrigerated circulator baths at in situ temperatures(Table 1) for 6–24 h depending on the ambient activity levels, and assayed by liquid scintillationspectroscopy on board the vessel. We did not purify labeled DNA (Ducklow et al., 1992) and thusdid not determine the extent of nonspecific labeling with 3H-thymidine in this study. Nonspecificlabeling has consistently been found to be low in most coastal, shelf and oceanic habitats, but theproblem has not been studied in the Antarctic.

2.3. Data analysis and conversion factors

Bacterial biomass, B; was calculated from measurements of abundance, A (cells l�1), and cellvolume, V (mm3 l�1), determined as described above, using the equation B ¼ A� V � CCF;where CCF is carbon conversion factor 1.07� 10�13 g C mm�3 determined from a series ofexperimental incubations and carbon mass balance on the same cruises (Carlson et al., 1999).Thus biomass is dependent on the abundance and cell volume, and not on abundance alone.Bacterial production ðBPTÞ was calculated from thymidine incorporation rates (T ; pmol l�1 h�1)using a thymidine conversion factor (TCF) of 8.6� 1017 cells mol�1 determined in the sameexperimental incubations as the CCF (Ducklow et al., 1999), with the equation BPT ¼ T �TCF � CCF: Note that BPT depends simultaneously on the measured rates of thymidineincorporation and the measured cell volume in each sample. Finally bacterial production ðBPLÞalso was calculated from leucine incorporation rates using the factor 1.5 kg C produced mol�1

leucine, following Simon and Azam (1989). The lower value of 1.5 kg C mol�1 was chosen byconstraining the estimated bacterial contribution to the measured total (dark) planktonrespiration (Bender and Dickson, 2000; Ducklow et al., 2000a). In this analysis, bacterialrespiration was estimated from experimental determinations of the bacterial carbon conversionefficiency, made in the same incubation experiments already described (Carlson et al., 1999;Ducklow et al., 1999). Thus all carbon-based estimates of bacterial mass and fluxes werecalculated using empirical factors determined on the same cruises.

Phytoplankton biomass was estimated using a phytoplankton carbon to chlorophyll a ratio of75 and primary productivity was determined via 14C bicarbonate incubation, both as described inSmith et al. (2000).

Areal standing stocks and productivities were calculated for the euphotic zone, to the depth of0.1% of the surface irradiance, as well as to 50, 150 and 300 m using trapezoidal integration.Values at the integration depths were calculated by linear interpolation from surrounding


samples. Surface values were assumed to be equal to the next-shallowest sample. Statisticalcomparisons were performed using one-way ANOVA and Model I regression.

3. Results

3.1. Environment and hydrography

Under pre-bloom, wintertime conditions, Chl a was o0.1 mg l�1. Day length ranged from o1 hin late April 1997 to continuous sunlight in November–February. The euphotic zone was 150 m inOctober, 40–50 m in spring and summer, and >150 m in late autumn. The study area had50–100% ice cover in October–early December and in April, and was essentially ice-free duringJanuary–February, except near the Victoria Land coast. Surface water temperature ranged from�1.91C to +11C, but averaged �1.85–01C on our cruises (Table 1). Surface nitrate concentrationswere near the wintertime maximum of B30 mM except on the summertime cruises, when thePhaeocystis bloom depleted them by 10–20mM (Table 1). Thus our observations encompassednearly the entire range of physical and biogeochemical variability characteristic of the region,from near-wintertime conditions to the peak of the spring-summer Phaeocystis bloom.

3.2. Seasonal evolution of the bacterial bloom

3.2.1. Bacterial biomassThe Ross Sea experienced a bacterial bloom with a peak amplitude equal to blooms observed

elsewhere in the world ocean outside estuaries, and which contrasted greatly with bacterialaccumulations elsewhere in the Antarctic. Bacterial abundance in the euphotic zone was very lowat the beginning of the growing season, and distributed homogeneously throughout watercolumn, averaging 9� 107 cells l�1 in October 1996, peaked at an average euphotic zoneabundance of 1.5� 109 cells l�1 (1–2 mmol C m�3) in late summer, 1996–1997 then declined to avertically homogeneous abundance of B2� 108 cells l�1 (0.2 mmol C m�3) in April 1997 (Figs. 1and 2). The maximum abundance of 3–5� 109 cells l�1 was observed in late summer. Bacterialbiomass, a function of abundance and cell volume (see below), was concentrated in the upper150 m of the water column (Figs. 2 and 3), approaching 2 mmol C m�3 in the 1996–1997 and 1997–1998 growing seasons. The upper layer biomass increased by over an order of magnitude from alate winter minimum of 1.8–45 mmol C m�2 in summer (Fig. 2, Table 2). Most of the seasonalincrease occurred in the upper 150 m. However significant accumulation of bacterial biomassoccurred in the 150–300 m layer (Fig. 2, Table 2), which was well below the euphotic zone duringthe growing season. The biomass increase in the upper 150 m was driven in part by increases inabundance but also cell volume, from about 0.04mm3 cell�1 in October, 1996 and early November,1994 to over 0.15mm3 cell�1 in December–January 1995–1996. Cell volumes were smaller inJanuary–February 1997 (Fig. 4).

3.2.2. Bacterial productionRates of 3H-thymidine and 3H-leucine incorporation were strongly correlated (Fig. 5A), but the

average incorporation rates of the two precursors changed independently from season to season


and between years (Table 3). For example, the ratio of Leu : TdR incorporation was 2.6 inOctober 1996 and 15.7 the following April, and was 8.6 and 5.9 in the two November–Decemberperiods, respectively. Across all cruises, euphotic zone bacterial production rates determined bythe two tracers were well-correlated (Fig. 5B), although with the conversion factors utilized, Leu-based estimates were about twice as great on average as the TdR-based estimates. In this paper,we report the leucine-based estimates for two reasons: conversion of leucine incorporation toproduction only requires a single assumption about conversion factor values (Simon and Azam,1989), and because leucine incorporation results in about 10 ten times more radioisotopeaccumulation in the samples, affording greater sensitivity. Since the Leu : TdR incorporation ratiovaried seasonally, we did not feel reporting a BP rate based on the average of the two methods wasjustified. BP estimates were based on incubations under reduced light conditions in refrigeratedcirculators. In Antarctic waters, especially under continuous light in summer, bacterial activity isinhibited by sunlight down to about 30 m depth; thus our estimates might overestimate discrete,shallow in situ BP values by as much as a factor of two (W. Jeffrey, Univ. S. FL, pers. comm.).Even with this overestimate, BP was very low relative to PP (see below).

Bacterial production was vertically distributed similarly to biomass (Table 2). Production rateswere vertically homogeneous and low in October and April, and reached a peak of6.6 mmol C m�2 d�1 in January–February 1997 (Table 2) in the surface 50 m. In comparison,the 0–50 m mean was 2–3 mmol C m�2 d�1 in 1994–1995, about the same as in the 150–300 m layerin January–February, 1997. Production rates also increased seasonally by an order of magnitudebelow the euphotic zone and were still elevated in the deeper layers in April 1997 (Table 2).

Fig. 1. Mean bacterial abundance in the upper 50 m in the Ross Sea, 1994–1997 (closed circles). Data are composited

from six cruises (Table 1) and presented as means of 10-day intervals. Observations from the North Atlantic near 471N,201W (Ducklow et al., 1993) are shifted by 182 days and superimposed for comparison (5-day means, open circles).Data from the equatorial Pacific in 1992 (Ducklow et al., 1995; diamonds, 01N, 1401W) are plotted against the upper(southern hemisphere) time axis. The lower time axis gives the northern hemisphere dates for the N Atlantic.


3.2.3. Bacterial growth ratesCell division rates, calculated for the entire bacterial assemblage, also varied seasonally and

interannually during our study (Fig. 6). The division rates in November–December 1994 weresomewhat greater than in the same period in 1997 (Fig. 6), and considerably less in April than allthe other cruises. In general however, division rates were 0.02–0.24 d�1 in all seasons exceptautumn. Cell-specific rates of TdR and Leu incorporation were significantly, though weaklyrelated to temperature within the 1996–1997 growing season in the upper 20 m (TdR/cell,po0:001; r2 ¼ 0:21; n ¼ 157; Leu/cell, po0:001; r2 ¼ 0:36; n ¼ 148), and even more weaklycorrelated in 1994–1995 (TdR/cell, ns, n ¼ 167; Leu/cell, po0:001; r2 ¼ 0:09; n ¼ 151). Cellvolumes were weakly correlated with growth rates, as indicated by cell-specific leucineincorporation rates (Fig. 7). The large cells, which dominated the assemblage later in the growingseason, grew faster than the small cells characteristic of the early and late seasons. Therelationship was similar, but cells were smaller in 1994 (Fig. 7).

Fig. 2. Bacterial biomass (mmol C m�3) in the 0–50, 50–150, and 150–300 m layers of the Ross Sea, 1994–1997. The

shaded boxes show the four AESOPS cruises, P1–P4 in 1996–1997. The line inside each box is the 50% percentile value,and the upper and lower boundaries of the boxes are the 75 and 25 percentiles, respectively. The capped bars showthe 10 and 90 percentiles of the data. The layer mean biomass was determined by dividing the integral stock by the

appropriate layer depth at each station. The shaded boxes indicate a single continuous growing season.


Table 2

Bacterial biomass (mmol C m�2) and production (mmol C m�2 d�1) in the upper water column of the central Ross Sea,Antarctica in 1996–1997a

Season (months) ESpr96 (Oct–Nov) Lsum97 (Jan–Feb) Aut97 (April) LSpr97 (Nov–Dec)Cruise P1 P2 P3 P4

Property BB

ðn ¼ 19ÞBP

ðn ¼ 19ÞBB

ðn ¼ 16ÞBP

ðn ¼ 13ÞBB

ðn ¼ 12ÞBP

ðn ¼ 12ÞBB

ðn ¼ 23ÞBP

ðn ¼ 17Þ

Avg 0–50 1.81 0.10 45.69 6.64 6.09 0.20 13.81 0.42

Std 0.34 0.09 24.12 2.76 0.81 0.14 13.16 0.18n 19 19 16 13 12 12 23 17

Avg 50–150 3.61 0.18 34.93 4.97 10.50 0.51 13.99 0.29Std 0.62 0.20 25.32 2.88 2.65 0.31 7.81 0.14

n 19 19 16 13 12 12 23 17

Avg 150–300 5.05 0.24 21.32 2.42 11.78 0.71 12.79 0.18Std 0.86 0.28 7.48 1.69 4.08 0.38 4.65 0.14n 19 19 16 13 12 12 23 17

Avg Total 10.47 0.52 101.95 14.04 28.38 1.43 40.58 0.89Std 0–300 1.51 0.55 48.47 5.88 7.02 0.79 22.02 0.30n 19 19 16 13 12 12 23 17

a The groups of rows in the table give the integral standing stocks and production in the layers 0–50, 50–150, 150–300and 0–300 m layers, for AESOPS cruises P1–P4, respectively (see Table 1). Production was not measured below ca.150 m in 1994–1995. The first three entry columns constitute a single consecutive growing season.

Fig. 3. Vertical distribution of bacterioplankton biomass in the central Ross Sea, 1994–1997. The lines indicate meanbiomass profile for each cruise, calculated from data binned into depth strata depending on sampling resolution anddensity.


3.2.4. Seasonal and interannual variabilityThe seasonal and interannual variability of bacterial biomass and production is summarized in

Fig. 8 and Table 4. Bacterial biomass in the euphotic zone was o7% of the phytoplanktonbiomass, except in April, under strongly light-limited conditions after the decline of the

Fig. 5. Relationships between (A): 3H-leucine and 3H-thymidine incorporation rates on the six cruises (po0:001;r2 ¼ 0:81; n ¼ 508), and (B): the estimated euphotic zone bacterial production rates (mmol C m�2 d�1) derived using

empirically determined or constrained conversion factors (see Methods section; po0:001; r2 ¼ 0:76; n ¼ 87). Symbols:November–December 1994, open circles; December–January 1996, closed circles; October 96, triangles; January–February 1997, inverted triangles; April 1997, diamonds; November–December 1997, open squares. The dashed lines

are Model I regression fits to the data shown (A: log–log, B: linear).

Fig. 4. Vertical distribution of bacterioplankton cell volume (mm3 cell�1) in the central Ross Sea, 1994–1997. The linesindicate mean cell volume profile for each cruise, calculated from data binned into depth strata depending on samplingresolution and density.


Phaeocystis bloom. Similarly, the euphotic zone bacterial production was equivalent to 1–11% ofthe particulate PP (see Ducklow (2000) for a discussion of this basis of comparison), except inApril, when BP and PP were both very low. The seasonal succession of bacterial andphytoplankton production in the Ross Sea is conspicuous, with BP peaking in the late summer,after the decline of the Phaeocystis bloom. Note however, that in 1994 BP and PP were closelycoupled during the early phases of the bloom, rising in parallel, with no apparent lag period(Fig. 8B and C). This coupling was not evident during the same period in 1997 (Fig. 8B and C). Itappears that the phytoplankton bloom may have started later in 1997 than 1994, and that thebacterial response had not yet begun by the time of the November 1997 cruise. Log-transformedBP and PP were weakly correlated overall (po0:05; r2 ¼ 0:06; n ¼ 78) but were not significantlycorrelated for individual cruises.

Table 3Rates of 3H-thymidine and 3H-leucine incorporation in the upper 50 m. Entries arranged in seasonal order, not by

yearsa

Season/year (cruise) TdR (pmol l�1 h�1) Leu (pmol l�1 h�1) Leu : TdR ratiob

Espr96 (P1) 0.12 0.57 2.62Std ðn ¼ 72Þ 0.09 0.55 0.62R2 0.20***

LSpr94 (R94) 1.75 23.31 8.68Std ðn ¼ 104Þ 1.46 17.00 0.78R2 0.55***

LSpr97 (P4) 0.69 3.57 5.87

Std (n ¼ 81) 0.62 4.53 0.5R2 0.64***

Sum95 (R95) 1.59 18.64 7.88Std ðn ¼ 131Þ 0.82 10.05 0.83

R2 0.42***

LSum97 (P2) 4.24 44.17 8.18Std ðn ¼ 73Þ 2.41 22.11 0.49r2 0.79***

Aut97 (P3) 0.03 1.20 15.7Std ðn ¼ 46Þ 0.02 0.87 7.7r2 0.09*

All mean 1.51 16.70 9.61

Std ðn ¼ 505Þ 1.78 19.09 0.21r2 0.81***

1996–1997 1.67 17.38 9.61Std (n ¼ 191) 2.51 25.12 0.19

r2 0.93***

a The italicised rows refer to the 1996–1997 growing season.b Determined from Model I linear regression of Leu on TdR. Slope values (ratio of Leu : TdR), their standard errors,

r2 and significance (***, po0:001; *, po0:05) are reported in column 4.


4. Discussion

Our study focussed on a more remote, deeper water system than previous work in Antarctica,and moreover one dominated by Phaeocystis antarctica. In all other Antarctic locations studiedextensively, diatoms dominated the phytoplankton bloom, although Phaeocystis might be anoccasional or even common member of the flora. The Ross Sea is also distinctive with regard tobacterial growth. This seasonal progression encompasses the entire observed range of upper oceanvariability in the global ocean (Ducklow, 1999), with an amplitude about as high as anywhere inthe world except estuaries (Fig. 1). Although bacterial blooms seem to be common in lakes andestuaries (Simon, 1987; Simon et al., 1992; Hoch and Kirchman, 1993), they are greatly attenuatedover large expanses of the ocean, including the coastal zone. For instance, bacterial abundancewas uniform and usually o5� 108 cells l�1 in the equatorial Pacific in 1992 (Ducklow et al., 1995),and did not bloom appreciably in response to the southwest monsoon in the Arabian Sea in 1995(Wiebinga et al., 1997; Pomroy and Joint, 1999; Ducklow et al., 2000b; Ducklow, 1999). Bacterialbiomass is also relatively uniform off Bermuda in the Sargasso Sea (Carlson et al., 1996). Therewas a bacterial bloom in the subarctic North Pacific Ocean in May 1988 (Kirchman, 1992), duringwhich the net accumulation rate was the same as the bacterial specific growth rate. A bacterialbloom in the North Atlantic in 1989 reached 2–3� 109 cells l�1 and lagged the phytoplanktonbloom by less than a month (Ducklow et al., 1993; Lochte et al., 1993; Kirchman et al., 1994). Anotable bacterial bloom also occurred in the Chukchi Sea under 80% ice cover in June, 1998

Fig. 6. Vertical distribution of bacterioplankton cell division (doubling) rates estimated from 3H-thymidineincorporation (divisions d�1) in the central Ross Sea, 1994–1997. The lines indicate mean rate profile for each cruise,calculated from data binned into depth strata depending on sampling resolution and density. Division rates calculatedusing the empirical thymidine conversion factors (see Methods) and the expression m=[P=A]/0.693 where A is

abundance and P is the calculated production rate.


Fig. 8. A composite seasonal view of primary and bacterial production in the Ross Sea, 1994–1997. Primary production(Panel B, PP) was integrated through the euphotic zone to 0.1% of surface irradiance at each station, while bacterial

production (Panel C, BP) is depicted as the integral to 150 m (i.e., about the same as the euphotic zone in October 1996,shallower than in April 1997, and deeper than on the spring-summer cruisesFsee Table 4). The ratio BP to 150 m : PP isshown in Panel A. Note that the low but nonzero PP values in April 1997 do not show up due to the axis scaling (seealso Table 4).

Fig. 7. Relationship between mean cell volume (mm3 cell�1) and the specific rate of 3H-leucine incorporation(10�21 mol cell�1 h�1, an index of the specific turnover rate). The lines show Model I regressions for the R95 and P1-4cruises (po0:001; r2 ¼ 0:23; n ¼ 401) and the R94 cruise (po0:001; r2 ¼ 0:23; n ¼ 128). Symbols as in Fig. 5.


(Yager et al., 2001). The Ross Sea bacterial bloom in 1996–1997 reached the same level as the 1989North Atlantic event (3� 109 cells l�1) but started with abundances an order of magnitude lower(Fig. 1). Overall, bacteria in the Ross Sea increased exponentially at a net rate of 0.03 d�1 betweenmid-October and mid-February (Fig. 9). This net accumulation rate is lower than the specificgrowth rates indicated in Fig. 6, but still more than sufficient to result in nearly a two-order ofmagnitude increase in the 100-day growing season. While the bacterial bloom in the Ross Sea wasconspicuous, bacterial production was surprisingly low relative to the PP in the region (Tables 2and 4; Carlson et al., 1998). Thus the Ross Sea, a system with a minimal flux of DOC throughbacterioplankton (relative to the PP), experiences seasonal bacterial accumulation of greatabsolute magnitude.

In coastal waters of the Antarctic Peninsula, members of the Archaea have been observed to bean important component of the ‘‘bacterial’’ assemblage detected by epifluorescence microscopy(Murray et al., 1998). Archaea have not been investigated in the open Ross Sea, although it isprobable they are present (Murray et al., 1999). We do not know the relative contributions ofArchaea and Bacteria to be the blooms we observed.

In spite of many studies in Antarctica, and others in cold waters outside the Antarctic (e.g.,Pomeroy and Deibel, 1986; Rivkin et al., 1996), there remains a lack of consensus about the

Table 4Euphotic zone (EZ, to the depth of 0.1% surface illumination) means and standard deviations for bacterial and

phytoplankton standing stocks and production rates in the Ross Sea, 1994–1997a

Season and

dates (Cruise)

Depth

(m)

Standing stocks (mmol C or mg Chl m�2) Production (mmol C m�2 d�1)

Bacteria(B)

Phyto-plankton(P)

RatioB : P

Bacteria(B) (Leu)

Phyto-plankton(P)

RatioB : P

Espr96 (P1) Mean 150 5.2 119 0.07 0.3 28 0.04

Oct 96 SD (n) 61 (12) 2.5 (12) 69 (12) 0.05 (12) 0.3 (12) 30 (12) 0.05 (12)

LSpr94 (R95) Mean 57 5.1 739 0.01 3.1 179 0.03

Nov–Dec 94 SD (n) 31 (38) 2.5 (38) 524 (38) 0.01 (38) 1.9 (13) 222 (38) 0.03 (12)

LSpr97 (P4) Mean 68 17.0 381 0.06 0.5 100 0.01

Nov–Dec 97 SD (n) 45 (28) 12.9 (28) 261 (28) 0.06 (28) 0.4 (20) 58 (20) 0.01 (20)

Sum95 (R95) Mean 41 13.9 896 0.02 1.9 98 0.04

Dec 95–Jan 96 SD (n) 22 (34) 10.4 (33) 460 (34) 0.03 (34) 0.9 (20) 71 (34) 0.03 (20)

Lsum97 (P2) Mean 42 37.2 527 0.08 5.4 57 0.11

Jan–Feb 97 SD (n) 15 (15) 19.5 (14) 193 (15) 0.05 (14) 1.7 (14) 29 (14) 0.06 (13)

Aut97 (P3) Mean 226 22.8 32 0.94 1.1 1.6 0.81

April 97 SD (n) 36 (11) 6.1 (11) 18 (11) 0.54 (11) 0.6 (11) 1.1 (11) 0.46 (11)

a All values integrated to depths given in column 3. The number of stations is given in parentheses following thestandard deviations (SD). Euphotic zone means calculated as the quotient of the integral and the depth of the EZ. The

italicised rows are all from the 1996–1997 growing season (NB: cf. also Fig. 8, in which all bacterial properties areintegrated to 150 m).


relative importance of temperature, organic matter and grazing as factors limiting thedevelopment of bacterial populations in polar seas. In exploring how these factors interact inthe Ross Sea, we focus on two aspects of bacterioplankton ecology in the region. First we considerthe relationship between increases in cell size and the role of removal processes in regulating theamplitude and temporal succession of the bacterial bloom. Next we address the relationshipbetween the phytoplankton and bacterial blooms, concentrating on the possible importance ofPhaeocystis antarctica in structuring bacterioplankton carbon dynamics. Finally, we contrast theRoss Sea with other Antarctic regimes in regard to bacterioplankton ecology, and sum up bydescribing the role of bacterioplankton in carbon flux in the Ross Sea.

4.1. Cell volume, growth and removal

Cell volume varied by a factor of four in the Ross Sea. Bacterioplankton cell volumes were veryuniform and low in the equatorial Pacific and Arabian Sea (o0.05mm3 cell�1; Ducklow et al.,1995, 2000b; Pomroy and Joint, 1999), but cell-specific biomass was more variable in the GerlacheStrait, Antarctica (Bird and Karl, 1999, biomass estimated from lipopolysaccharide concentra-tions). Cell volumes also vary widely in lakes (Simon, 1987). In the Ross Sea, cell volumesincreased from 0.04 to 0.15mm3 cell�1.

The bacterial biomass could only increase as shown in Fig. 9 if growth consistently exceededremoval and if bacteriovores were either not strongly size-selective (Gasol et al., 1995; Cole, 1999)or not capable of balancing the production of enlarging bacterial cells. Rates of bacterivoryduring the 1996–1997 growing season (P1–P3 cruises) were low compared to other ocean regions(Dennett et al., 2001), and bacteriovore abundance was low relative to bacterial abundance. Theratio of prey to predator abundance, an index of grazing intensity (Sanders and Berninger, 1992;Gasol and Vaqu!e, 1993) ranged from 500 in November–December 1997 (spring–early summer) to

Fig. 9. Net bacterial biomass accumulation in the upper 50 m, 1994–1997. Symbols as in Fig. 5. The Y-axis shows

ln(biomass) to indicate the exponential accumulation.


1700 in October 1996, and was B800 during the summer period when bacteriovore abundancewas at its highest level. These values are typical of other oceanic regions, but much higherthan observed near the Antarctic Peninsula (Bird and Karl, 1999Fsee below). Bacteria alsogrew exponentially at 0.06–0.27 d�1 in experimental incubations of unfiltered seawater performedduring our cruises (Ducklow et al., 1999), further indicating that bacterial growth exceededmortality during the October–February period of increasing abundance. The quotient ofmean production and biomass values from Table 2 shows that specific bacterial growth rateswere 0.05, 0.15 and 0.03 d�1 in October, January and April 1996–1997, respectively. Takingthe mean net accumulation rate (i.e. growth minus removal) of 0.03 d�1 (Fig. 9), we inferthat removal rates due to grazing, viral lysis and other unspecified processes, were around0.02 and 0.12 d�1 in October and January. Thus the bacterial bloom proceeds notbecause removal was necessarily low in absolute terms, but because it was just slightlylower than growth. In fact, removal remains as a strong constraint on bacterial accumulat-ion. Even at a net rate of 0.05 d�1, bacterial abundance would reach B1� 1010 cells l�1 bylate January in the absence of removal. About 2/3 of this potential accumulation is lostto mortality.

The bacterial assemblage must decline in winter due to slow or nonexistent growth and someunspecified mortality term, to set the abundance levels we observed in October. These levels arevery low relative to those seen in the same season in the North Atlantic (Fig. 1). Removalprocesses in winter reduce bacterial stocks to at least 1� 108 cells l�1, values characteristic of1000 m depths at lower latitudes (Nagata et al., 2000).

The existence of a conspicuous bacterial bloom in the Ross Sea is notable, though not unique,for the world oceans, and stands in marked contrast with other Antarctic regions. Clarke andLeakey (1996) observed a small bacterial bloom (to 3� 108 cells l�1, an order of magnitude lowerthan in the Ross Sea) at Signy, South Orkney Islands, a coastal site with a marine climate notdissimilar to the Ross Sea, except for year-round solar irradiance (lat. 601S), and a diatom bloominstead of Phaeocystis. At Prydz Bay, East Antarctica, the maximum abundances of bacteria andbacteriovores were 8.6� 108 and 4.5� 106 cells l�1, with a prey : predator ratio of 80–300 (Leakeyet al., 1996). However the bacteriovores only removed 10–36% of the daily bacterial production,allowing a small bloom (from 2 to 8� 108 cells l�1). Bacterial growth was under strong top–downcontrol in the coastal ecosystem of the Gerlache Strait, off the Antarctic Peninsula, in the spring of1989 (Bird and Karl, 1999). The prey : predator ratio had a median of 85, almost an order ofmagnitude lower than in the Ross Sea in the same month. However, the median ratios of growthto grazing rates in the Gerlache area were 1.65, 1.28, 0.65 and 0.99 on four grid sampling surveysconducted during the November 1989 cruise (Bird and Karl, 1999), and net bacterial growth wasstrongly negative at times. Bird and Karl (1999) suggested that the bacteriovores attained highabundances in the relative absence of predation by larger zooplankton, allowing the bacteriovoresto crop down the bacterial biomass, which never exceeded 7� 108 cells l�1. The common featuresof the Signy, Prydz Bay and the Gerlache Strait areas are coastal location, a diatom-dominatedphytoplankton bloom, the attenuated amplitude of the bacterial accumulation and relativelyintense top–down control on the bacteria, which nonetheless allows a slight excess of growth overgrazing. Contrasts between the Ross Sea and other Antarctic ecosystems raise the question as towhy the bacterial bloom is so much larger in the Ross Sea, or conversely, why it is so slightelsewhere.


4.2. Relationship to the Phaeocystis bloom

The bacterial bloom lagged the phytoplankton bloom by about 1 month. The peakphytoplankton stocks were observed in late December 1995; stocks in mid-December 1997 weremuch lower (Table 4). The bacterial bloom reached its peak in early February 1997, althoughbacterial stocks were nearly comparable in late November and as late as April (Table 4). The lag isneither unusual nor universal. There was a similar 1-month lag between the peaks of primary andbacterial production off Newfoundland (Pomeroy et al., 1991). Data from Prydz Bay suggest thatthe phasing of bacterial and phytoplankton blooms might vary interannually. Billen andBecquevort (1991) attributed a 1-month lag between the diatom and bacterial blooms in 1986–1987 to delayed production and utilization of macromolecular, polymeric DOC. Lancelot et al.(1991) hypothesized a similar scenario for a Phaeocystis bloom in Prydz Bay. High reliance of BPon polysaccharides in the Ross Sea (Kirchman et al., 2001) indicates a similar mechanism toexplain the lag we observed. However, Leakey et al. (1996) observed that the diatom and bacterialblooms occurred more or less together in the same area in 1993–1994. Rivkin (1991) did notresolve a lag in McMurdo Sound, close to our study area, but the cycle of observations wasassembled over two successive growth seasons (1984–1985 and 1985–1986), which may haveobscured any lag. Alternatively, the absence of a lag may be because Phaeocystis is advected intothe Sound (Palmisano et al., 1986). Interpretation of our observations is also complicated byinterannual variability, but counterclockwise trajectories in the bacteria–phytoplankton phaseplanes do suggest clear lags for both production and biomass (Fig. 10).

Neither Billen and Becquevort (1991), Carlson et al. (1998) nor our observations indicate adirect role for low temperature in causing the delay in bacterial development, when it occurs.Resource limitation appears to be more likely. Bacterial production is exceptionally high in theArctic Ocean, even under the sea ice (Rich et al., 1998), perhaps in response to large riverineinputs of DOC, which do not occur in the Antarctic. Carlson et al. (1998) demonstrated an order-of-magnitude increase in BP in the Ross Sea in response to increased PP without any change intemperature. These relationships suggest, but do not prove, that bacterial production is limitedprimarily by relatively low DOM fluxes in the Ross Sea.

The reason for the low DOC flux (Carlson et al., 1998, 2000) remains unclear. Possiblemechanisms limiting net DOC production and its transient accumulation are discussed at lengthby Carlson et al. (2000). Two principal reasons seem likely. DOC release from phytoplankton,especially release of high C : N ratio material, is often associated with macronutrient (i.e. nitrate)depletion (Williams, 1995; Smith et al., 1998). In many temperate areas Phaeocystis pouchettiblooms are followed by copious DOC accumulation and microbial growth as a consequence ofcell lysis in response to nutrient depletion (van Boekel et al., 1992; Brussard et al., 1996). PossiblyP. antarctica behaves differently, but the simplest explanation is that macronutrient depletionseldom occurs in the Ross Sea and direct release from Phaeocystis is minimized. DOC productionby P. antarctica was copious when nutrient depletion was induced experimentally (Smith et al.,1998). The other likely factor is the structure of the plankton community. For example there is adearth of mesozooplankton grazing in the Ross Sea, a process known to enhance DOC release(Strom et al., 1997). Bird and Karl (1999) concluded that the near-absence of mesozooplanktongrazers, which released bacteriovores from top-down control, also limited DOC production bydiatoms, causing a trophic cascade that suppressed bacterial growth in the Gerlache Strait, at least


in spring. Formation of Phaeocystis colonies is possibly a grazing-defense adaptation (Verity andSmetacek, 1996). The literature on vulnerability of Phaeocystis to grazers is ‘‘confused andcontradictory’’ (Verity et al., 1988, p. 761). There are few helpful reports on zooplankton grazingin the Ross Sea. Hopkins (1987) concluded that most of the PP escaped predation, a fact that isbest revealed by the spectacular phytoplankton blooms in the region (Arrigo and McClain, 1994).Microzooplankton grazing also induces DOC release (Nagata, 2000), and microzooplanktonherbivory was notably absent from the Ross Sea (Caron et al., 2000), further minimizing potentialDOC release rates.

Why does a bacterial bloom occur even though DOC release rates and accumulation (both netand gross, Carlson et al., 2000) are relatively low in the Ross Sea? One reason is that the DOC thatis released is relatively labile on a short time scale (Carlson et al., 1998, 1999; Smith et al., 1998;Ducklow et al., 1999). Further, bacteria use it with relatively high efficiency (30–40% in summer,Carlson et al., 1999). Kirchman et al. (2001) showed that free monosaccharides and dissolvedcombined sugars comprise up to 50% of the accumulated, ‘‘semilabile’’ DOC pool, showing thatthis pool is made up largely of easily utilized material. Removal by bacteriovores is just low

Fig. 10. Seasonal development of the phytoplankton–bacterial bloom in the Ross Sea. (A): euphotic zone productionrates, and (B) stocks. The symbols are means for each cruise, and the bars indicate the standard errors of the values and

days of sampling. In some cases bars are smaller than symbols. The general counterclockwise trajectories in timeindicate the lag of bacteria behind the phytoplankton development.


enough to allow net growth throughout the long growing season, which starts early due topolynya formation (Smith and Gordon, 1997). It may be that microzooplankton are suppressedby mesozooplankton forced to seek alternate food sources in the presence of unpalatablePhaeocystis colonies. Thus high efficiency growth on labile DOC by bacteria in slight excess ofgrazing removal over a 100-day growing season results in a bacterial bloom equal in magnitude toany seen elsewhere in the world ocean.

4.3. Bacterial role in the Ross Sea carbon system

Although bacterial biomass attains relatively high levels, production rates are undeniably low,both relative to high PP (Table 4) and in absolute terms. By way of comparison, mean 3H-leucineincorporation rates in the upper 50 m (Table 3) were lower than in most other productive oceanicregions, except in summer. Rates of 3H-leucine incorporation in the upper 50 m averaged 84, 31–46 and 56 pM h�1 in the North Atlantic, Equatorial Pacific and Arabian Sea, respectively (dataavailable at: http://www1.whoi.edu/jg/dir/jgofs/). Cell-specific rates of leucine incorporation inthe upper 50 m (euphotic zone) averaged 7� 10�20 mol cell�1 h�1 in November–December, 1994and 3.5� 10�20 mol cell�1 h�1 in January–February 1997 (Fig. 7). By comparison, the value forthe equatorial Pacific (281C) was 8� 10�20 mol cell�1 h�1 in April 1992 (Ducklow et al., 1995).Clearly temperature alone cannot explain this effect. In addition, data on sugars do not supportthe hypothesis that high levels of labile organic matter relieved temperature inhibition of bacterialmetabolism. Kirchman et al. (2001) showed that sugar concentrations are low, with free glucoseconcentrations being among the lowest ever measured. We suggest that the main control onbacterial production in the Ross Sea is the flux of labile carbon to bacteria. It is low in winter,spring and autumn, and briefly high following the Phaeocystis bloom in summer, when BP is at itsseasonal maximum. At this time, some of the BP may be sustained by direct utilization ofsenescent Phaeocystis, via exoenzymatic hydrolysis (Smith et al., 1992).

Focussing only on the productive layer in the upper 50 m does not convey the whole story.Bacterial production was 14 mmol C m�2 d�1 over the upper 300 m in summer 1997 (Table 4, P2cruise), or 24% of the PP (cf. Table 4). Conservatively assuming a 30% conversion efficiency forthe entire water column implies that bacteria were processing carbon at a rate equivalent to about0.24/0.3 or 72% of the PP at that time. Some of this carbon demand must have been satisfied byutilization of semilabile DOC accumulated earlier in the growing season, which disappears byApril (DDOC, Carlson et al., 2000). Since the flux of DOC is usually low, however (Carlson et al.,2000), other carbon sources must be more important. Over the growing season, bacterialutilization of bulk DOC (production plus respiration) cannot be greater than B11% of the annualPP (Carlson et al., 2000). An alternative source is direct utilization of phytoplankton cellularmaterial, which is heavily colonized by attached bacteria in January–February (Ducklow, unpubl.obs.; Putt et al., 1994). Below 150 m, where DDOC is always near zero, the bacterial carbondemand (BCD) might be satisfied by decomposition of some part of the vertical POC flux. Carbonfluxes through 100 m during the P1–P3 cruises ranged from 2–30 mmol C m�2 d�1 (with oneoutlier of 80; Cochran et al., 2000). These rates of supply of fresh material are roughly sufficient tomeet BCD of 0.6–2.4 mmol C m�2 d�1 (calculated from Table 4 assuming 0.3 efficiency) in the150–300 m layer. Sweeney et al. (2000) and Carlson et al. (2000) demonstrate that a significantportion (>4 mol C m-2) of the seasonal NCP is exported vertically out of the surface 150 m. It


appears that BP is low in the euphotic zone because much organic matter escapes consumption inthat layer. But a relatively large fraction of that exported below the upper 100 m might bemetabolized by bacteria. Thus consideration of whole water column metabolism placesconstraints on levels of BP in the euphotic zone. The relationship between bacterial metabolismin the upper and midwater layers, and whole-system carbon budgeting remains to be investigatedin other regions.

Acknowledgements

This research was supported by NSF OPP grants 9319222 and 9530734 to HWD, 9531977 toDLK, OPP 93-17200 to D.A. Hansell, OCE 9530845 to D.A.H. and C.A. Carlson, and 9530851 toFarooq Azam. Helen Quinby and Flynn Cunningham analyzed bacterial abundance and biomassand Alison Sanford assisted in fieldwork on several cruises. We thank Captain Joe Borkowski andthe officers and crew of RVIB NB Palmer for outstanding support in the ice. J. Alberts, S.Kottmeier, C. Peterson, B. Scott and many other ASA staff helped with this work. Nutrient dataand hydrography, as well as Chl and PP data were obtained from the US JGOFS DataManagement Office at http://usjgofs.whoi.edu:1824/southern-data.html.

References

Arrigo, K.R., McClain, C.R., 1994. Spring phytoplankton production in the Western Ross Sea. Science 266, 261–263.Azam, F., Smith, D.C., Hollibaugh, J.T., 1991. The role of the microbial loop in Antarctic pelagic ecosystems. Polar

Research 10, 239–243.Bender, M.L., Dickson, M.-L., 2000. Net and gross production in the Ross Sea during JGOFS process studies. Deep-

Sea Research II 47, 3141–3158.Billen, G., Becquevort, S., 1991. Phytoplankton–bacteria relationship in the antarctic marine ecosystem. Polar Research

10, 245–253.Bird, D.F., Karl, D.M., 1991. Spatial patterns of glutamate and thymidine assimilation in Bransfield Strait, Antarctica

during and following the austral spring bloom. Deep-Sea Research I 38, 1057–1075.

Bird, D.F., Karl, D.M., 1999. Uncoupling of bacteria and phytoplankton during the austral spring bloom in GerlacheStrait, Antarctic Peninsula. Aquatic Microbial Ecology 19, 13–27.

Brussard, C.P.D., Gast, G.J., van Duyl, F.C., Riegman, R., 1996. Impact of phytoplankton bloom magnitude on a

pelagic microbial foodweb. Marine Ecology Progress Series 144, 211–221.Carlson, C.A., Ducklow, H.W., 1994. Annual flux of dissolved organic carbon from the euphotic zone in the

northwestern Sargasso Sea. Nature 371, 405–408.Carlson, C.A., Ducklow, H.W., 1995. Dissolved organic carbon in the upper ocean of the central equatorial Pacific

Ocean, 1992: daily and finescale vertical variations. Deep-Sea Research II 42, 639–656.Carlson, C.A., Ducklow, H.W., Sleeter, T.D., 1996. Stocks and dynamics of bacterioplankton in the northwestern

Sargasso Sea. Deep-Sea Research II 43, 491–516.

Carlson, C.A., Ducklow, H.W., Smith, W.O., Hansell, D.A., 1998. Carbon dynamics during spring blooms in the RossSea polynya and the Sargasso Sea: contrasts in dissolved and particulate organic carbon partitioning. Limnologyand Oceanography 43, 375–386.

Carlson, C.A., Bates, N.R., Ducklow, H.W., Hansell, D.A., 1999. Estimation of bacterial respiration and growthefficiency in the Ross Sea, Antarctica. Aquatic Microbial Ecology 19, 229–244.

Carlson, C.A., Hansell, D.A., Peltzer, E.T., Smith Jr., W.O., 2000. Stocks and dynamics of dissolved and particulate

organic matter in the Southern Ross Sea, Antarctica. Deep-Sea Research II 47, 3201–3226.


Caron, D.A., Dennett, M.R., Lonsdale, D.J., Moran, D.M., Shalapyonok, L., 2000. Microzooplankton herbivory inthe Ross Sea, Antarctica, October 1996–December 1997. Deep-Sea Research II 47, 3249–3272.

Clarke, A.R., Leakey, J.G., 1996. The seasonal cycle of phytoplankton, macronutrients and the microbial communityin a nearshore Antarctic marine ecosystem. Limnology and Oceanography 40, 1281–1294.

Cochran, J.K., Buesseler, K.O., Bacon, M.P., Wang, H.W., Hirschberg, D.J., Ball, L., Andrews, J., Crossin, G., Fleer

A., 2000. Short-lived thorium isotopes (234Th, 228Th) as indicators of POC export and particle cycling in the RossSea, Southern Ocean. Deep-Sea Research II 47, 3451–3490.

Cole, J.J., 1999. Aquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology.

Ecosystems 2, 215–225.

Dennett, M.R., Mathot, S., Caron, D.A., Smith Jr., W.O., Lonsdale, D.J., 2001. Abundance and distribution ofphototrophic and heterotrophic nano- and microzooplankton in the southern Ross Sea. Deep-Sea Research II 48,

4019–4037.

Ducklow, H.W., 1999. The bacterial content of the oceanic euphotic zone. FEMS Microbiology-Ecology 30,1–10.

Ducklow, H.W., 2000. Bacterioplankton production and biomass in the oceans. In: Kirchman, D. (Ed.), Wiley, New

York, pp. 85–120, (Chapter 4).

Ducklow, H.W., Carlson, C.A., 1992. Oceanic bacterial productivity. Advances in Microbial Ecology 12,113–181.

Ducklow, H.W., Kirchman, D.L., Quinby, H.L., 1992. Bacterioplankton cell growth and macromolecular synthesis inseawater cultures during the North Atlantic spring phytoplankton bloom, May 1989. Microbial Ecology 24,125–144.

Ducklow, H.W., Kirchman, D.L., Quinby, H.L., Carlson, C.A., Dam, H.G., 1993. Stocks and dynamics ofbacterioplankton carbon during the spring phytoplankton bloom in the eastern North Atlantic Ocean. Deep-SeaResearch II 40, 245–263.

Ducklow, H.W., Quinby, H.L., Carlson, C.A., 1995. Bacterioplankton dynamics in the equatorial pacific during the1992 El Nino. Deep-Sea Research II 42, 621–638.

Ducklow, H.W., Carlson, C.A., Smith, W.O., 1999. Bacterial growth in experimental plankton assemblages and

seawater cultures from the Phaeocystis antarctica bloom in the Ross Sea, Antarctica. Aquatic Microbial Ecology 19,215–227.

Ducklow, H.W., Dickson, M.-L., Kirchman, D.L., Steward, G., Orchardo, J., Marra, J., Azam, F., 2000a.

Constraining bacterial production, conversion efficiency and respiration in the Ross Sea, Antarctica, January-February, 1997. Deep-Sea Research II 47, 3227–3248.

Ducklow, H.W., Smith, D.C., Campbell, L., Landry, M.R., Quinby, H.L., Steward, G., Azam,. F., 2000b.Heterotrophic bacterioplankton distributions in the Arabian Sea: Basinwide response to high primary productivity.

Deep-Sea Research II 48, 1303–1323.

Fuhrman, J.A., Azam, F., 1980. Bacterioplankton secondary production estimates for coastal waters of BritishColumbia, Antarctica, California. Applied Environmental Microbiology 39, 1085–1095.

Gasol, J.M., Vaqu!e, D., 1993. Lack of coupling between heterotrophic nanoflagellates and bacteria: a generalphenomenon across aquatic ecosystems? Limnology and Oceanography 38, 657–665.

Gasol, J.M., del Giorgio, P.A., Massana, R., Duarte, C.M., 1995. Active versus inactive bacteria: size-dependence in a

coastal marine plankton community. Marine Ecology Progress Series 28, 91–97.

Hansell, D.A., Carlson, C.A., 1998. Net community production of dissolved organic carbon. Global BiogeochemicalCycles 12, 443–453.

Hoch, M.P., Kirchman, D.L., 1993. Seasonal and interannual variability in bacterial production and biomass in atemperate estuary. Marine Ecology Progress Series 98, 283–295.

Hopkins, T.L., 1987. Midwater food web in Mcmurdo Sound, Ross Sea, Antarctica. Marine Biology 96, 93–106.

Jacobs, S.S., Giulivi, C.F., 1999. Thermohaline data and ocean circulation on the Ross Sea continental shelf. In: Spezie,G., Manzella, G.M.R. (Eds.), Oceanography of the Ross Sea, Antarctica. Milano: Springer-Verlag Italia. 286pp,pp. 3–16.

Karl, D.M., 1993. Microbial processes in the Southern Oceans. In: Friedmann, E.I. (Ed.), Antarctic Microbiology.Wiley, New York, pp. 1–63.


Karl, D.M., Holm-Hansen, O., Taylor, G.T., Bird, D.F., 1991. Microbial biomass and productivity in the WesternBransfield Strait, Antarctica, during the 1986–87 austral summer. Deep-Sea Research I 38, 1029–1055.

Karl, D.M., Christian, J.R., Dore, J.E., 1996. Microbiological oceanography in the region west of Antarctic Peninsula:microbial dynamics, nitrogen cycle and carbon flux. AGU Antarctic Research Series 70, 303–332.

Kirchman, D.L., 1992. Incorporation of thymidine and leucine in the subarctic Pacific: application to estimating

bacterial production. Marine Ecology Progress Series 82, 301–309.

Kirchman, D.L., Ducklow, H.W., McCarthy, J.J., Garside, C., 1994. Biomass and nitrogen uptake by heterotrophicbacteria during the spring phytoplankton bloom in the North Atlantic Ocean. Deep-Sea Research I 41, 879–895.

Kirchman, D.L., Meon, B., Ducklow, H.W., Carlson, C.A., Hansell, D.A., Steward, G.F., 2001. Glucose fluxes andconcentrations of dissolved combined sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica.Deep-Sea Research II 48, 4179–4197.

Knap, A., Michaels, A., Close, A., Ducklow, H.W., Dickson, A. (Eds.). 1994. Protocols for the Joint Global OceanFlux Study (JGOFS) Core Measurements. JGOFS Report No. 19, Reprint of the IOC Manuals and Guides No. 29,UNESCO, vi+170pp.

Lancelot, C., Billen, G., Veth, C., Becquevort, S., Mathot, S., 1991. Modeling carbon cycling through phytoplanktonand microbes in the Scotia-Weddell Sea area during sea ice retreat. Marine Chemistry 35, 305–324.

Leakey, R.J.G., Archer, S.D., Grey, J., 1996. Microbial dynamics in coastal waters of East Antarctica: bacterialproduction and nanoflagellate bacterivory. Marine Ecology Progress Series 142, 3–17.

Lochte, K., Ducklow, H.W., Fasham, M.J.R., Stienen, C., 1993. Plankton succession and carbon cycling at 471N 201Wduring the JGOFS North Atlantic Bloom Experiment. Deep-Sea Research II 40, 91–114.

Lochte, K., Bjornsen, P.K., Giesenhagen, H., Weber, A., 1997. Bacterial standing stock and production and their

relation to phytoplankton in the Southern Ocean. Deep-Sea Research II 44, 321–340.

Mordy, C.W., Penny, D.M., Sullivan, C.W., 1995. Spatial distribution of bacterioplankton biomass and production inthe marginal ice zone of the Weddell-Scotia sea during austral winter. Marine Ecology Progress Series 122, 9–19.

Murray, A.E., Preston, C.M., Massana, R., Taylor, L.T., Blakis, A., Wu, K.Y., DeLong, E.F., 1998. Seasonal andspatial variability of bacterial and archaeal assemblages in the coastal waters off Anvers Island, Antarctica. AppliedEnvironmental Microbiology 64, 2585–2595.

Murray, A.E., Wu, K.Y., Moyer, C.L., Karl, D.M., DeLong, E.F., 1999. Evidence for circumpolar distribution ofplanktonic Archaea in the Southern Ocean. Aquatic Microbial Ecology 18, 263–273.

Nagata, T., 2000. Production mechanisms of dissolved organic matter. In: Kirchman, D. (Ed.), Wiley, New York, pp.

121–152 (Chapter 5).

Nagata, T., Fukuda, H., Fukuda, R., Koike, I., 2000. Bacterioplankton distribution and production in deep Pacificwaters: large-scale geographic variations and possible coupling with sinking particle fluxes. Limnology and

Oceanography 45, 426–435.

Palmisano, A.C., SooHoo, J.B., SooHoo, S.L., Kottmeier, S.T., Craft, L.C., Sullivan, C.W., 1986. Photoadaptation inPhaeocystis pouchetti advected beneath annual sea ice in Mcmurdo Sound, Antarctica. Journal of PlanktonResearch 8, 891–906.

Picco, P., Bergamasco, A., Demicheli, L., Manzella, G., Meloni, R., Paschini, E., 1999. Large-scale circulation featuresin the Central and Western Ross Sea (Antarctica). In: Faranda, F.M. Guglielmo, L. Ianora, A. (Eds.), Ross SeaEcology. Berlin: Springer, pp. 95–105, 604pp.

Pomeroy, L.R., Deibel, D., 1986. Temperature regulation of bacterial activity during the spring bloom inNewfoundland coastal waters. Science 233, 359–361.

Pomroy, A., Joint, I., 1999. Bacterioplankton activity in the surface waters of the Arabian Sea during and after the 1994

SW Monsoon. Deep-Sea Research II 46, 767–794.

Pomeroy, L.R., Wiebe, W.J., Deibel, D., Thompson, R.J., Rowe, G.R., Pakulski, J.D., 1991. Bacterial responses totemperature and substrate concentration during the Newfoundland spring bloom. Marine Ecology Progress Series

75, 143–159.

Putt, M., Miceli, G., Stoecker, D.K., 1994. Association of bacteria with phaeocystis sp. in Mcmurdo Sound, Antarctica.Marine Ecology Progress Series 105, 179–189.

Rich, J., Gosselin, M., Sherr, E., Sherr, B., Kirchman, D.L., 1998. High bacterial production, uptake andconcentrations of dissolved organic matter in the Central Arctic Ocean. Deep-Sea Research II 44, 1645–1663.


Rivkin, R., 1991. Seasonal patterns of planktonic production in Mcmurdo Sound, Antarctica. American Zoologist 3,5–16.

Rivkin, R.B., Anderson, M.R., Lajzerowicz, C., 1996. Microbial processes in cold oceans. 1. Relationship betweentemperature and bacterial growth rate. Aquatic Microbial Ecology 10, 243–254.

Sanders, R.W., Caron, D.A., Berninger, U.G., 1992. Relationships between bacteria and heterotrophic nanoplankton

in marine and fresh waters: an inter-ecosystem comparison. Marine Ecology Progress Series 86, 1–14.Simon, M., 1987. Biomass and production of small and large free-living and attached bacteria in Lake Constance.

Limnology and Oceanography 32, 591–607.

Simon, M., Azam, F., 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Marine EcologyProgress Series 51, 201–213.

Simon, M., Cho, B.C., Azam, F., 1992. Significance of bacterial biomass in lakes and the ocean: comparison tophytoplankton biomass and biogeochemical implications. Marine Ecology Progress Series 86, 103–110.

Smith, D.C., Azam, F., 1992. A simple, economical method for measuring bacterial protein synthesis in seawater using3H-leucine. Marine Microbial Food Webs 6, 107–114.

Smith Jr., W.O., Gordon, L.I., 1997. Hyperproductivity of the Ross Sea (Antarctica) polynya during austral spring.

Geophysical Research Letters 24, 233–236.Smith, D.C., Simon, M., Alldredge, A.L., Azam, F., 1992. Intense hydrolytic enzyme activity on marine aggregates and

implications for rapid particle dissolution. Nature 359, 139–142.

Smith, W.O., Carlson, C.A., Ducklow, H.W., Hansell, D.A., 1998. Large-volume experiments with natural assemblagesof Phaeocystis antarctica from the Ross Sea. Marine Ecology Progress Series 168, 229–244.

Smith Jr., W.O., Marra, J., Hiscock, M.R., Barber, R.T., 2000. The seasonal cycle of phytoplankton biomass andprimary productivity in the Ross Sea, Antarctica. Deep-Sea Research II 47, 3119–3140.

Sorokin, Y.I., 1971. Bacterial populations as components of oceanic ecosystems. Marine. Biology 11, 101–105.Strom, S.L., Benner, R., Ziegler, S., Dagg, M.J., 1997. Planktonic grazers are a potentially important source of marine

dissolved organic carbon. Limnology and Oceanography 42, 1364–1374.

Sweeney, C., Hansell, D.A., Carlson, C.A., Codispoti, L.A., Gordon, L.I., Marra, J., Millero, F., Smith, W.O.,Takahashi, T., 2000. Biogeochemical regimes, net community production and carbon export in the Ross Sea,Antarctica. Deep-Sea Research II 47, 3395–3423.

Van Boekel, W.H., Hansen, M.F.C., Riegman, R., Bak, R.P.M., 1992. Lysis-induced decline of of phaeocystis springbloom and coupling with the microbial foodweb. Marine Ecology Progress Series 81, 269–276.

Verity, P.G., Smetacek, V., 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems.

Marine Ecology Progress Series 130, 277–293.Verity, P.G., Villareal, T.A., Smayda, T.J., 1988. Ecological investigations of blooms of colonial Phaeocystis pouchetii.

2. The role of life-cycle phenomena in bloom termination. Journal Plankton Research 10, 749–766.Wiebe, W.J., Sheldon Jr., W.M., Pomeroy, L.R., 1992. Bacterial growth in the cold: evidence for an enhanced substrate

requirement. Applied Environmental Microbiology 58, 359–364.Wiebe, W.J., Sheldon Jr., W.M, Pomeroy, L.R., 1993. Evidence for an enhanced substrate requirement by marine

mesophilic bacterial isolates at minimal growth temperatures. Microbial Ecology 25, 151–159.

Wiebinga, C.J., Veldhuis, M.J.W., De Baar, H.J.W., 1997. Abundance and productivity of bacterioplankton in relationto seasonal upwelling in the northwest Indian Ocean. Deep-Sea Research I 44, 451–476.

Williams, P.J.le.B., 1995. Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale in

comparison with changes in particulate material and consequential effect on net C/N assimilation rates. MarineChemistry 51, 17–29.

Yager, P.L., Connelly, T.L., Mortazavi, B., Wommack, K.E., Bano, N., Bauer, J.E., Opsahl, S., Hollibaugh J.T., 2001.Dynamic bacterial and viral response to an algal bloom at sub-zero temperatures. Limnology and Oceanography 46,

790–801.


the seasonal development of the bacterioplankton … seasonal development of the bacterioplankton...

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