rates of dissolved organic carbon production and bacterial ...bacteria, virus and protozoa,...

MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 249: 53–67, 2003 Published March 10

INTRODUCTION

Microbial food webs, basically constituted byautotrophic pico- and nanoplankton, heterotrophicbacteria, virus and protozoa, predominate inoligotrophic stratified waters (e.g. Legendre & LeFèvre 1989, Kiørboe 1993, Legendre & Rassoul-zadegan 1995). In these systems, the dissolved organicpathway has been recognised as of great relevancefor the transfer of matter through the planktonic foodweb (e.g. Azam et al. 1983, Legendre & Le Fèvre 1995).

Given that most oceanic regions are oligotrophic (seeLonghurst 1998), major fluxes of organic matter inthe ocean are likely to be channelled through thedissolved pool into bacteria and the microbial loop(Azam 1998), making it necessary to invoke processessuch as cell lysis (e.g. Bratbak et al. 1990, Agustí etal. 1998) or grazing (e.g. Jumars et al. 1989, Nagata &Kirchman 1992), besides algal physiology, to explainthe relatively large fluxes of recently photosynthesisedorganic matter to the dissolved organic carbon (DOC)pool.

© Inter-Research 2003 · www.int-res.com*Email: [email protected]

Rates of dissolved organic carbon production andbacterial activity in the eastern North Atlantic

Subtropical Gyre during summer

E. Teira1, 5,*, M. J. Pazó1, M. Quevedo2, M. V. Fuentes3, F. X. Niell4, E. Fernández1

1Departamento de Ecología y Biología Animal, Universidad de Vigo, 36200 Vigo, Spain2Departamento de Biología de Organismos y Sistemas, Universidad de Oviedo, 33071 Oviedo, Spain

3Departamento de Microbiología, and 4Departamento de Ecología, Universidad de Málaga, 29071 Málaga, Spain

5Present address: Royal Netherlands Institute for Sea Research (NIOZ), Department of Biological Oceanography, PO Box 59, 1790 AB Den Burg, The Netherlands

ABSTRACT: Rates of particulate organic carbon (POC) production, dissolved organic carbon (DOC)production and bacterial production were measured at 8 stations in the eastern North Atlantic Sub-tropical Gyre during August 1998. The euphotic-depth-integrated POC rate was on average 27 mgCm–2 h–1. The corresponding averaged integrated DOC production rate was 5 mgC m–2 h–1, i.e. about20% of the total primary production. No statistically significant relationship was found between therates of POC and DOC production, suggesting that other processes besides phytoplankton exudation,such as cell lysis or protist grazing, could be implied in the release of dissolved organic materials tothe oceanic environment. Euphotic-depth-integrated bacterial biomass and production were on aver-age 214 mgC m–2 and 1.4 mgC m–2 h–1, respectively. The lack of correlation between the rates ofDOC release and bacterial activity and a bacterial carbon demand (BCD, calculated using an esti-mated bacterial growth efficiency ranging from 11 to 18%) in excess of DOC production suggestedthe existence of additional organic carbon sources (both allochthonous and/or autochthonous reser-voirs), apart from in situ phytoplankton-derived DOC production, for the maintenance of bacterialactivity in this region during summer 1998. This uncoupling between phytoplankton and bacterio-plankton could partially explain the heterotrophic metabolic balance in this oligotrophic regionduring summer 1998.

KEY WORDS: Phytoplankton · Bacteria · Primary production · DOC production · Bacterial activity ·Coupling · North Atlantic Subtropical Gyre

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Mar Ecol Prog Ser 249: 53–67, 2003

About 50% of daily photosynthetic production isutilised by heterotrophic bacteria (e.g. Ducklow &Carlson 1992, Williams 2000); however, estimations ofthe magnitude of DOC fluxes through the microbialsystem are highly variable, representing from 2 to1000% of primary production (Williams 2000). Most ofthese estimations derive from modelling or indirectapproaches (e.g. from bacterial growth rate or micro-bial respiration measurements), and therefore are con-strained by the uncertainty and difficulty concerningthe conversion of microbial metabolism rates into geo-chemical mass units (C-based estimates). On the otherhand, direct measurements of DOC production ratesresulting from short incubations are very rare, espe-cially in the oligotrophic ocean.

Direct determinations by Teira et al. (2001b), cover-ing a wide productivity spectrum in the AtlanticOcean, showed that the contribution of DOC produc-tion by microbial populations to primary productionranged between 4 and 42%, being larger in oligo-trophic waters. Unfortunately, the technique usuallyemployed for direct measurement of DOC productionrates by natural microbial populations is based on therelease of labelled dissolved organic materials anddoes not distinguish between the DOC contributions ofdifferent processes within the microbial community.Nevertheless, the analysis of the relationship betweenthe rates of particulate organic carbon (POC) andDOC production provides valuable information aboutchanges in the relative magnitude of DOC fluxes alongproductivity gradients (Baines & Pace 1991) as wellas about the processes involved in the release of dis-solved organic matter. A significant relationship be-tween POC and DOC production rates would beexpected if algal exudation were the main mechanismcontrolling DOC production. Moreover, if the recentlyreleased DOC, either through trophic or physiologicalprocesses, constituted the major supply of substratefor pelagic bacterial production, a positive relationshipmight be observed between rates of bacterial produc-tion and phytoplankton-derived in situ DOC produc-tion. The analysis of the relationship between bacterialproduction and phytoplankton-derived in situ DOCproduction allows the study of the coupling betweenbacteria and phytoplankton, whereby coupling repre-sents the general dependence of bacteria on the DOCsupplied by algae (see Morán et al. 2001).

Bacterial production in the open ocean depends notonly on DOC supply, which largely originates fromphytoplankton, but also on DOC composition (e.g.Kirchman 1990). Therefore, the production of semi-labile phytoplankton-derived DOC, mainly associatedwith grazing and/or cell lysis, could induce uncouplingbetween the autotrophic and heterotrophic compart-ments (Blight et al. 1995), which would ultimately

result in temporal offsets between the processes ofDOC production and consumption. In this connection,recent studies have measured rates of bacterial carbonutilisation exceeding rates of primary production inoligotrophic environments (e.g. Hansell et al. 1995, delGiorgio et al. 1997).

Within this context, we measured rates of DOC pro-duction by microbial populations as well as bacterialbiomass and production in the oligotrophic easternNorth Atlantic Subtropical Gyre during August 1998,with the aims of (1) investigating the spatial variabilityin the fraction of recently photosynthesised carboncontributed by the DOC pool to the total amount of car-bon photoassimilated by phytoplankton, commonlydefined as percentage of extracellular release (PER),(2) determining which processes or variables are rele-vant in the control of DOC production in this region,and (3) establishing the extent of coupling betweenphytoplankton and bacteria in relation to the carbonfluxes through the microbial community.

MATERIALS AND METHODS

Sampling region. The rate of DOC production bymicrobial populations as well as bacterial abundanceand production rates were measured at 8 stations (bio-logical stations) along 2 transects (A and B) duringCruise ‘Azores-1’ in the eastern North Atlantic Sub-tropical Gyre in August 1998 (Fig. 1). Vertical profilesof temperature, salinity and fluorescence were ob-tained at the biological stations and at additional(CTD) stations with a Neil Brown Mark III CTDattached to a rosette sampler equipped with 10 l Niskinbottles. Photosynthetically available radiation (PAR)was measured with a light PAR sensor. Rates of POC,

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Fig. 1. Map of sampling stations visited in August 1998. (n) Bio-logical stations, and (m) CTD stations along Transects A and B

Teira et al.: DOC and bacterial activity in the North Atlantic Subtropical Gyre

DOC and bacterial production, as well as bacterial andmicrozooplankton abundance and biomass were mea-sured only at biological stations.

POC and DOC production rates. At each station, five30 ml samples were collected at 5 selected depths fromthe euphotic layer, inoculated with 1480 kBq (40 µCi)of NaH14CO3 and incubated in an on-deck incubatorthat simulated the irradiance experienced by the cellsat the original sampling depths. Incubations were runfor 2 h to minimise concurrent bacterial consumption ofrecently released DOC during the incubation period(see review in Fogg 1983). The bottles were keptrefrigerated by pumping surface seawater into theincubator. Previous studies did not show statisticallysignificant differences between primary productionestimates derived from on-deck and in situ incubationprocedures (Joint et al. 1993). After the incubationperiod, two 8 to 10 ml subsamples were drawn fromeach bottle and filtered by gravity through Milli-pore APFF glass-fibre filters (approximate pore size0.45 µm). Filtrates were acidified with 40 to 75 µl ofHCl 50% (until a pH value around 2 was reached) andbubbled with CO2-free air for 12 h. Filters were decon-taminated by exposure to concentrated HCl fumesfor 12 h. Scintillation cocktail was then added to bothfilters and filtrates. Duplicate blank tests were run inparallel by inoculating and immediately processing0.2 µm-filtered seawater in the same way. This blanktest was used as control for 14C stock purity and tocheck the efficiency of the decontamination process(Berman & Holm-Hansen 1974, Mague et al. 1980).This control is recommended since the zero-time val-ues for filtrates are always significantly higher thanblank values due to some interaction with particulatematter during the few seconds of exposure afterinoculation (see Mague et al. 1980). Radioactivity wasmeasured on both filters (POC production, POCP)and filtrates (DOC production, DOCP) with an LKBβ-scintillation counter. Quenching corrections weremade using an external standard. Filtrate blank valueswere on average 187 ± 22 SE dpm for all the ex-periments. The mean (± SE) variation coefficient for thereplicate measurements of POC and DOC productionrates was 19 ± 1 and 32 ± 2%, respectively.

Daily POCP rates were calculated from hourly ratesusing the equation of Straskraba & Gnauck (1985).Daily DOCP rates were estimated assuming thateither the release of dissolved material occurs onlyduring the light period (DOCPlight), which would beexpected if DOCP were closely related to the photo-synthetic process, or that DOC release takes place atthe same rate during the light and dark periods(DOCP24h), which may be reasonable if trophic-related processes (grazing, cell lysis) were mainly im-plicated in the release of dissolved materials. There-

fore, the actual rate of daily DOCP must lie withinthese 2 extreme estimations.

Two recent papers have explicitly questioned theadequacy of using glass-fibre filters for measuringPOC and DOC production (Karl et al. 1998, Morán etal. 1999) because of 14C-DOC adsorption onto thesetype of filters. Consequently, the DOC production ratesreported here should be considered as conservativeestimations. However, the use of different type offilters (e.g. membrane filters) has not been proved torender more accurate estimations of POC and DOCproduction rates (Karl et al. 1998, Morán et al. 1999).The high capacity of glass-fibre filters to retain pico-eukaryotes has frequently been reported (e.g. Gasol &Morán 1999). Accordingly, we are confident that thedissolved fraction can include only bacteria, virus andcolloidal particles.

Daily gross primary production (GPP) was calculatedas the sum of POCP and DOCPlight. Daily net primaryproduction (NPP) was estimated as in Marañón et al.(2000), assuming that dark respiratory losses represent20% of daily POCP (NPP = POCP · 0.8 + DOCPlight).

Bacterial abundance. Using an epifluoresce micro-scope, bacterial abundance was measured by directcounts of samples collected on black polycarbonatefilters (Porter & Feig 1980). Samples were fixed withglutaraldehyde (final concentration 2.5% vol/vol) andkept in the dark at 4°C until further processing ashore.Subsamples (2 ml) were taken and stained with DAPI(4’-6-dianimo-2-penylindone) for 5 min in the dark,and then filtered through 0.2 µm, 25 mm diameterpolycarbonate filters under a low vacuum pressure(


terial carbon content of 12 fg C cell–1. The average bac-terial carbon content estimated in this study lies withinthe range of values reported by Bode et al. (2001) foroceanic waters near the Canary Islands in summer1998 (17 fg C cell–1), by Zubkov et al. (2000) for theAtlantic Ocean (7 fg C cell–1) and by Carlson et al.(1996) for the Sargasso Sea (4 to 7 fg C cell–1), and isvery similar to the average bacterial carbon contentcalculated from direct measurements by Fukuda et al.(1998) for oceanic environments.

Bacterial production. Bacterial production was esti-mated from [3H] thymidine incorporation rates. Threewater subsamples (20 ml) and 2 controls containing1% (vol/vol) formaldehyde were incubated in thedark at in situ temperature for 60 min with 10 nM[3H-methyl] thymidine (70 to 85 Ci mmol–1). After in-cubation, an equal volume of ice-cold 5% (wt/vol)trichloroacetic acid was added to each subsample.After 5 min on ice, the samples were filtered through0.2 µm pore-size cellulose ester membrane filters witha vacuum pressure of


both transects. The vertical distribution of salinity(Fig. 2b) also distinguishes the STF boundary. Up-lifting of isotherms and isohalines at Stn 14 indicatesthe presence of colder and fresher water in the sub-

tropical side of the frontal zone. A more detailed de-scription of the large and meso-scale hydrographicvariability during this cruise has been made by Pérezet al. (2003).

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Fig. 2. Vertical distribution of (a) temperature (°C), (b) salinity, and (c) chlorophyll a fluorescence (arbitrary units) along Transects A and B. Numbers on upper axis indicate biological stations

a

b

c

Mar Ecol Prog Ser 249: 53–67, 200358

Fig. 3. Vertical profiles of primary production (PP) of POC (grey bars) and DOC (black bars) at biological stations along TransectsA and B. Superimposed continuous and dotted lines: percentage of extracellular release (PER) and chlorophyll a fluorescence,

respectively; fluorescence scale (arbitrary units) is the same as that for PP

Table 1. Daily depth-integrated variables and biological stations sampled in North Atlantic Subtropical Gyre during summer1998. See ‘Materials and methods’ for calculations. POCP: particulate organic carbon production; DOCPlight, DOCP24h: dissolvedorganic production during light period only and during light plus dark periods, respectively; NPP: net primary production;PERlight, PER24h: percent extracellular release during light period only and during light plus dark periods, respectively;

BB: bacterial carbon biomass; BP: bacterial production; BCD: bacterial carbon demand

Variable Transect A, Stns; Transect B, Stns; Mean ± SE11 14 17 19 21 27 34 35

POCP (mg C m–2 d–1) 195 129 483 329 452 216 715 360 ± 72DOCPlight (mg C m–2 d–1) 59 77 58 59 101 29 96 69 ± 9DOCP24h (mg C m–2 d–1) 106 137 102 106 180 51 171 122 ± 16NPP (mg C m–2 d–1) 215 180 444 322 463 202 668 356 ± 63PERlight (%) 23 37 11 15 18 12 12 18 ± 3PER24h (%) 42 67 19 27 32 20 21 33 ± 6BB (mg C m–2) 202 209 230 239 192 188 207 247 214 ± 7BP (mg C m–2 d–1) 32 14 8 48 61 29 30 46 33 ± 6BCD (mg C m–2 d–1) 227 104 57 303 385 186 261 251 222 ± 35BP:NPP 0.15 0.08 0.02 0.15 0.13 0.14 0.07 0.11 ± 0.02BCD:DOCPlight 3.85 1.35 0.98 5.14 3.81 6.41 2.61 3.45 ± 0.69BCD:DOCP24h 2.14 0.76 0.56 2.86 2.14 3.65 1.47 1.94 ± 0.39


The lowest chlorophyll a fluorescence values (


the northern side of the STF boundary (Stns 11 and 35).About 74% of the total biomass corresponded to the>20 µm microzooplankton size fraction, with a rela-tively higher contribution of small organisms (38%) atStn 35. Ciliates were less abundant than dinoflagel-lates, and represented on average 62% of the totalmicrozooplankton biomass. We failed to find any sta-tistically significant relationship between DOC pro-duction rates and microzooplankton biomass, eitherbetween total microzooplankton biomass and DOCproduction or between ciliate or dinoflagellate biomassand DOC production (p > 0.7, n = 14).

Bacterial biomass and production

Bacterial abundance and biomass ranged between1 and 4 × 105 cells ml–1 and between 1.2 and 4.9 mgCm–3, respectively (Fig. 4). The bacterial abundancemeasured in this investigation, was well within the

range of typical values reported for comparable waters.It was very similar to that reported by Zubkov et al.(1998) for oligotrophic regions in the Atlantic Oceanduring fall 1996, to the average values of Harrison etal. (2001) for the North Atlantic Subtropical Gyral Eastprovince (derived from 2 cruises conducted in Sep-tember-October 1992 and May-June 1993), and to thedata of Bode et al. (2001) for the nearby Canary Islandsregion (1 to 6 × 105 cells ml–1). However, our measure-ments were, on average, about 2-fold lower than thevalues reported by González et al. (2001) for the sub-tropical North Atlantic in August 1998 and by Kuiperset al. (2000) for the same region in August 1996.Although the bacterial abundances reported by Gon-zález et al. (2001) and ourselves were obtained on thesame cruise, caution must be taken in comparing thetwo sets of data, since different methods for bacterialquantification were used—flow cytometry by Gonzá-lez et al. (2001) and microscopic observation in the pre-sent study (see Sieracki et al. 1995).

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Fig. 4. Vertical profiles of bacterial biomass (BB) (dashed line) and production rates (BP) (continuous line) at biological stations along Transects A and B


The vertical distribution of bacterial biomass wasfairly homogeneous, with no marked maximum, ex-cept at Stn 19 where a maximum value of 4.9 mgC m–3

was measured at 80 m. A general decreasing trend ofbacterial biomass was observed with increasing depth.Average bacterial biomass was 2.2 ± 0.1 (SE) mgC m–3.Bacterial production varied from 0.13 to 2.98 nmolthymidine m–3 h–1, and from 0.002 to 0.055 mgC m–3

h–1, averaging 0.014 ± 0.002 (SE) mgC m–3 h–1 (Fig. 4).Maximum values were observed at between 60 and120 m in Transect A, whereas maximum rates werefound at the surface in Transect B. Specific growth rateof the bacterial assemblage, calculated as the naturallogarithm of the relative increase in bacterial carbonbiomass, ranged from 0.017 to 0.523 d–1, correspondingto generation times from 57.8 to 1.9 d. These ratesare similar to those reported by Bode et al. (2001) foroligotrophic waters around the Canary Islands (0.064to 0.437 d–1), but higher than those found by Zubkov etal. (2000) in the subtropical North Atlantic duringSeptember 1995 and April 1997 (between 0.04 and0.17 d–1), and by Carlson et al. (1996) in the NW Sar-gasso Sea from 1991 to 1994 (mean seasonal valuesfrom 0.057 in autumn to 0.096 in spring).

Daily euphotic-depth-integrated values of BB and BPare given in Table 1. Whereas BB remained almostconstant in the region, BP varied between 8 and61 mgC m–2 d–1, with minimum rates at Stns 14 and 17

located in the southern end of Transect B. On average,BP represented 11% of net primary production NPP(Table 1). Comparisons between bacterial stocks andproduction rates are highly constrained by the method-ological approach as well as the conversion factorsused. The averaged integrated bacterial biomass re-ported here was very similar to that reported byZubkov et al. (2000) (ca. 0.15 to 0.20 g C m–2) in thesubtropical North Atlantic during September 1995. Allthese estimations are lower than the euphotic zoneaverage (0.5 to 2 g C m–2) across a range of oceanicsystems given in a recent review by Ducklow (2000),even considering that all his biomass estimations werebased on a conversion factor of 20 fg C cell–1. The aver-age BP rate obtained in this study (Table 1) was 3-foldhigher than the rate reported by Zubkov et al. (2000)during September 1995 for the subtropical NorthAtlantic, and very similar to the mean value givenby Carlson et al. (1996) for the Sargasso Sea and byGonzález et al. (2001) for the same region during April1999. The mean BP:NPP ratio was in the lower extremeof the global average (0.1 to 0.2) calculated for theoceans (Ducklow 2000).

No significant relationship was found between BB orBP and DOC production (p > 0.2, n = 34), which sug-gests that recently phytoplankton-derived DOC pro-duction was not the main carbon source for bacterialmetabolism in this oligotrophic region at the time of

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Fig. 5. Log-log relationship between bacterial carbon demand(BCD) and DOC production (DOCP) obtained using estimatedbacterial growth efficiency (BGE) ranging from 0.11 to 0.18(Rivkin & Legendre 2002). Dashed line: line of Slope 1;continuous line: regression line obtained using data belowline of Slope 1 (data below line of Slope 1 represented by

open symbols)

Fig. 6. Carbon flow through microbial community in euphoticzone of the eastern North Atlantic Subtropical Gyre insummer. Fluxes expressed in mgC m–2 d–1; calculations andconversion factors are explained in ‘Materials and methods’.PHYT: phytoplankton; BACT: bacteria; BGE: bacterialgrowth efficiency; ZOO: zooplankton; *microbial respiration

(González et al. 2001)


the survey. Also, no correlation was observed betweenBB or BP and microzooplankton biomass (p > 0.1,n = 15). Using the BGE derived form the model byRivkin & Legendre (2002) (see ‘Materials and meth-ods’), the bacterial carbon demand (BCD) globallyexceeded DOC production (Fig. 5) and no statisticalrelationship was observed between the 2 variables(p = 0.816, n = 34), indicating that phytoplankton-derived in situ DOC production by the microbial com-munity was not enough to fulfil bacterial metabolism.However, a significant relationship between BCD andDOC production was found when considering onlydata below the line of Slope 1 (log BCD = 0.70 logDOCP –0.67, r2 = 0.69, p = 0.0016, n = 11). IntegratedBCD was, on average, 2- to >3-fold higher than inte-grated DOC production when DOCP is assumed totake place during 24 h or during the light period,respectively (Table 1). There were 2 stations whichhad a BCD:DOCP24h ratio 0.1 to >45 mgCm–3 h–1, while the rates of particulate production mea-sured in the present investigation varied between only0.04 and 0.59 mgC m–3 h–1. One possible explanationfor the lack of correlation between POC and DOC pro-duction could be a higher error associated with themeasurement of the abovementioned rates in low-production environments. However, we discarded this

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possibility as the mean variation coefficient for repli-cate DOC production measurements calculated for aproductive coastal system using the same methodolog-ical protocol (Teira et al. 2001a) was not significantlydifferent from that calculated in this study (Student’st-test, p = 0.057). As suggested in ‘Results’, the lack ofcorrelation between the rates of carbon fixation andextracellular release in oligotrophic conditions canbe interpreted as a predominance of trophic versusphysiological processes as sources of DOC in the watercolumn. Earlier (Teira et al. 2001b), we showed that inoligotrophic environments a higher percentage of PERvariability could be better explained by changes inphytoplankton size-structure than by the magnitude ofcarbon incorporation rates. Important fluxes of photo-synthesised materials to the dissolved organic matter(DOM) pool as a result of processes such as phyto-plankton cell lysis (Brussaard et al. 1995, Gobler et al.1997, Agustí et al. 1998) or grazing by protozoa (Na-gata 2000 and references therein), have been recentlyrelated to stratified oligotrophic environments in whichsmall primary producers form the bulk of the photo-synthetic organisms and the microbial trophic pathwaydominates. Predominance of small phytoplankton is aregular pattern observed in the North Atlantic Sub-tropical Gyre (Marañón et al. 2000). Size-fractionatedprimary production measurements conducted duringthe Azores-1 cruise along a latitudinal transect be-tween 30 and 38° N and centred at 22° W showed thatpicophytoplankton accounted for >55% of the totalprimary production. In order to investigate the potent-ial role of trophic processes in the release of dissolvedmaterials in the upper water column we first analysedthe relationship between DOC production rates andmicrozooplankton biomass and did not find a signifi-cant relationship between the 2 variables. Conceptu-ally, rates of DOC release might be related to protistgrazing rates instead of biomass. Although concurrentmeasurements of microzooplankton grazing and DOCproduction rates were not carried out in this study, veryhigh rates of microzooplankton grazing (about 80% ofdaily primary production) were measured in the areaby Quevedo & Anadón (2001), which supports thepotentially relevant role of grazing activity on DOCproduction expected for oligotrophic environments.On the other hand, rates of cell lysis and DOC produc-tion could not be compared, as the former were notmeasured in this study. Agustí et al. (2001) estimatedDOC excretion rates derived from phytoplankton celllysis in the eastern subtropical North Atlantic as about30% of net primary production, which is within thePER range obtained in this study (20 to 67%) assumingthat DOC release occurs over 24 h.

All these considerations suggest that the major sup-ply of substrate for pelagic bacterial production in the

oligotrophic subtropical NE Atlantic Ocean might betrophic processes rather than direct algal exudation. Ifalgal exudation were the main source of DOC for bac-teria, a positive relationship between BP and DOC pro-duction rates should be observed (Søndergaard et al.1995). No significant relationships were found betweeneither BB or BP and DOC production rates, whichfurther support the hypothesis of the trophic controlof phytoplankton-derived DOC production. Moreover,protist grazing on heterotrophic bacteria (e.g. Ferrier-Pagès et al. 1998, Kuipers & Witte 2000), bacterial celllysis by virus infection (e.g. Fuhrman & Noble 1995,Thingstad 2000), and direct release of DOM from bac-teria (Stoderegger & Herndl 1998) would lead to thepresence of bacterial-derived DOM in the water col-umn, thus contributing to the DOM cycling within themicrobial food web.

Uncoupling between phytoplankton and bacteriain the upper subtropical North Atlantic Ocean

during summer

As already stated, we use here the term ‘coupling’ torepresent the dependence of bacteria on the concurr-ent phytoplankton-DOC release by microbial popula-tions. Therefore, only concomitant and accurate de-terminations of bacterial production and dissolvedorganic carbon production will allow a proper analysisof the degree of coupling between phytoplankton andbacteria. The results presented in this paper clearlyindicate uncoupling between phytoplankton and bac-terioplankton at most of the studied stations in theoligotrophic subtropical North Atlantic during summer1998.

Comparison of BCD with DOC production rates(Fig. 5), revealed no significant relationship betweenthe 2 variables, and (using an estimated BGE of 0.11 to0.18) daily euphotic-depth-integrated DOC productionaccounted only for 30 to 50% of the correspondingaverage daily BCD (Fig. 6, Table 1). Although uncou-pling between bacteria and phytoplankton can be con-cluded from the data in Figs. 5 & 6, it is essential tostress that whereas a negative balance between DOCproduction and consumption does imply uncouplingbetween bacteria and phytoplankton, the converse isnot necessarily true.

The clear uncoupling between bacteria and phyto-plankton derived from the lack of correlation betweenboth variables (as shown in Fig. 5) does not depend onmethodological assumptions; however, the negativebalance between phytoplankton-derived DOC pro-duction and subsequent bacterial consumption shownin Fig. 6 was highly dependent on the conversion fac-tors used for the estimation of BP and BR, and therefore

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conclusions based on this balance must be made withcaution, given that BR varies by up to 1 order ofmagnitude when using the theoretic range of BGE foropen-ocean regions (0.03 to 0.27). BCD is usually esti-mated from BP and an assumed BGE value due to thetechnical difficulties associated with the measurementof bacterial respiration. Such an assumed value iseither taken from the literature or derived by applica-tion of an empirical model. The model of del Giorgio &Cole (1998) allows BR to be derived directly from BPrates, whereas a recent model of Rivkin & Legendre(2002) directly relates BGE to temperature. When weapplied the model by del Giorgio & Cole (1998) weobtained a mean BGE of 0.03, which represents thelower extreme of the theoretical range for open-oceanregions (del Giorgio & Cole 2000). Consequently, weused the temperature–BGE relationship of Rivkin& Legendre (2002), which gives more conservativevalues for BR. In addition, the uncertainty concerningthe transformation of BP rates to carbon units (whichdepends both on the thymidine conversion factor, TCF,and on bacterial carbon content, BCC) must also beconsidered. In this regard we also used rather con-servative conversion factors compared with thosemost commonly used in the literature (for TCF, 2.2 ×1018 cells mol–1, and for BCC, 20 fg C cell–1). The rela-tively low mean BP:NPP (0.11) obtained in the presentstudy may result from an underestimation of the BPrates as a consequence of the conservative conversionfactors employed.

The uncertainties involved in the estimation of BR donot allow us to conclude from our results whether thestations studied in the subtropical NE Atlantic showeda net heterotrophic, a balanced or a net autotrophicproduction/respiration (P:R) balance at the time thisstudy was conducted. Thus, in situ phytoplankton-derived DOC production would be sufficient to supportbacterial consumption if a BGE > 0.27 were assumed,although such a value would be higher than the aver-age value (median 0.09, mean ± SD = 0.15 ± 0.12)reported for open-ocean systems (del Giorgio & Cole2000). Also, the average daily-integrated BCD wouldrepresent >100% of NPP using a BGE < 0.10. Thiswould lead to a net heterotrophic P:R balance, as inde-pendently derived for the same region and samplingperiod by (González et al. 2001) from measurements ofcommunity respiration estimated from in vitro changesin O2 concentration after 24 h incubations. A net het-erotrophic P:R on short timescales within the NorthAtlantic Subtropical Gyre was also reported by Duarteet al. (2001) and Serret et al. (2001), who measuredrates of community respiration similar to thoseobtained by González et al. (2001). A detailed and rig-orous analysis of in vitro determinations of planktoncommunity respiration conducted by Robinson et al.

(2002) in the eastern Atlantic showed that the unex-pected respiration rates, in excess of gross production,found in the picoautotroph-dominated oligotrophicregions of the Atlantic Ocean was consistent with mea-sured and estimated autotrophic and heterotrophicactivity; Robinson et al. (2002) concluded that thecommunity respiration data were not grossly overesti-mated. Hansell et al. (1995) also found that rates ofDOC mineralization represented between 100 and220% of the primary production of the Sargasso Seabetween September 1993 and April 1994. These imbal-ances clearly indicate an allochthonous supply and/oran autochthonous reservoir of organic carbon (delGiorgio et al. 1997, Duarte & Agustí 1998, Duarte et al.1999, 2001, Robinson et al. 2002), and thus couldpartially result from a temporal delay in the consump-tion by bacteria of previously released phytoplankton-derived DOC.

Independent of this metabolic balance controversy,our results suggest that to assume that the DOC fluxequals total BCD is not necessarily valid when phyto-plankton and bacterioplankton dynamics are notcoupled. Although several studies focussing on therelationship between phytoplankton and bacterio-plankton have shown a close coupling between therelease of DOC and BP rates (e.g. Lancelot & Billen1984, Panzenböck et al. 2000, Morán et al. 2001),other studies have found that the in situ production ofphytoplankton-derived DOC would be insufficient tosupport the heterotrophic population (e.g. Williams& Yentsch 1976, Bode et al. 2001).

A possible explanation for the bacterial-phytoplank-ton uncoupling could be the accumulation of DOCduring a previous productive period. Several investi-gations have observed temporal shifts between auto-trophic and heterotrophic processes, as reflected by anet heterotrophic P:R balance following periods of highprimary production (e.g. Blight et al. 1995, Sherr &Sherr 1996, Serret et al. 1999). The production andaccumulation of semilabile DOC, deriving mainly fromgrazing or cell lysis, would act as a transient carbonreservoir which could sustain microheterotrophic res-piration after the decline of the productive period(Blight et al. 1995). Williams (1995) suggested that dis-solved inorganic nitrogen limitation of heterotrophicbacteria consuming DOM with high C:N ratios couldexplain the accumulation of DOC during summer inthe North Atlantic Ocean. The seasonal accumulationof semilabile DOC in the surface layer of the oceanis at present well documented (Carlson et al. 1994,Yamanaka & Tajika 1997, Hansell & Carlson 1998) andhas been reported by Doval et al. (2001), who mea-sured an accumulation of semilabile DOC in the upper100 m of 16.8 g C m–2 in the Azores Front region duringAugust 1998. This seasonal DOC excess could have

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acted as an autochthonous reservoir and, at least par-tially, have supported the excess of BCD over DOCproduction measured in this study. If we assume thatBP rate and BGE remain constant over time, theturnover of the accumulated carbon would be, on aver-age, 106 ± 27 (SE) d.

Uncoupling between bacteria and phytoplanktoncould also result from an allochthonous supply oforganic carbon. The potential heterotrophic carbonsources in the eastern Atlantic Ocean have been ex-haustively discussed by Robinson et al. (2002). Duarteet al. (2001) proposed lateral inputs from the produc-tive upwelling areas in the NW African coast as apotentially relevant allochthonous carbon source in thesubtropical NE Atlantic. Other allochthonous sourcesof organic matter that should also be taken into con-sideration would be atmospheric deposition of DOMthrough marine rain (Willey et al. 2000) or dust storms(Cornell et al. 1995, Bory & Newton 2000), and photo-chemical production of labile DOC from more refrac-tory molecules (e.g. Mopper et al. 1991, Bushaw et al.1996, Moran & Zepp 2000). Robinson et al. (2002) esti-mated that photodegradation would account for only1 to 2% of the bacterial carbon demand in the easternAtlantic.

In conclusion, the present study shows a great vari-ability in PER values in the subtropical NE AtlanticOcean during the summer period that is hypothesisedto be related to the predominant role of trophic pro-cesses (grazing, cell lysis) as sources of DOC in theoligotrophic ocean. The lack of correlation betweenthe rates of phytoplankton-derived DOC release andbacterial activity during the summer in this oceanicregion reflects the uncoupling between both microbialcompartments and implies additional organic carbonsources, apart from in situ phytoplankton-derived DOCproduction, for the maintenance of bacterial activity.

Acknowledgements. This work was supported by EU contractCANIGO (MAS3CT960060). E.T. was funded by a PFPI fel-lowship from the Ministerio de Ciencia y Tecnología (Spain).We are indebted to the captain and crew of BIO ‘Hespérides’as well as to all the colleagues on board during the CruiseAzores-1.

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Editorial responsibility: Otto Kinne (Editor), Oldendorf/Luhe, Germany

Submitted: July 17, 2002; Accepted: December 17, 2002Proofs received from author(s): February 14, 2003

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