Deep-Sea Research I 53 (2006) 1616–1634 Vertical distribution of phytoplankton biomass, production and growth in the Atlantic subtropical gyres Valesca Pe´rez a, , Emilio Ferna´ndez a , Emilio Maran˜o´n a , Xose´ Anxelu G. Mora´n b , Mike V. Zubkov c a Departamento de Ecologı´a y Biologı´a Animal, Facultad de Ciencias del Mar, Universidad de Vigo, Ctra. Colexio Universitario s/n, 36310 Vigo, Spain b Instituto Espan˜ol de Oceanografı´a, Centro Oceanogra´fico de Xixo´n, Camı´n de L’Arbeyal, s/n, E 33212 Xixo´n, Spain c George Deacon Division for Ocean Processes, Southampton Oceanography Centre, University of Southampton, Southampton SO14 3ZH, UK Received 26 October 2005; received in revised form 28 July 2006; accepted 31 July 2006 Available online 2 October 2006 Abstract Ninety-four stations were sampled in the Atlantic subtropical gyres during 10 cruises carried out between 1995 and 2001, mainly in boreal spring and autumn. Chlorophyll a (Chl-a) and primary production were measured during all cruises, and phytoplankton biomass was estimated in part of them. Picoplankton (o2 mm) represented 460% of total Chl-a concentration measured at the surface, and their contribution to this variable increased with depth. Phytoplankton carbon concentrations were higher in the upper metres of the water column, whereas Chl-a showed a deep maximum (DCM). At each station, the water column was divided into the upper mixed layer (ML) and the DCM layer (DCML). The boundary between the two layers was calculated as the depth where Chl-a concentration was 50% of the maximum Chl-a concentration. On average DCML extends from 67 to 126 m depth. Carbon to Chl-a (C:Chl-a) ratios were used to estimate phytoplankton carbon content from Chl-a in order to obtain a large phytoplankton carbon dataset. Total C:Chl-a ratios averaged (7s.e.) 10377(n ¼ 22) in the ML and 2474(n ¼ 12) in the DCML and were higher in larger cells than in picoplankton. Using these ratios and primary production measurements, we derived mean specific growth rates of 0.1770.01 d 1 (n ¼ 173) in the ML and 0.2070.01 d 1 (n ¼ 165) in the DCML although the differences were not significant (t-test, p40.05). Our results suggest a moderate contribution of the DCML (43%) to both phytoplankton biomass and primary production in the Atlantic subtropical gyres. r 2006 Elsevier Ltd. All rights reserved. Keywords: Phytoplankton; Biomass; Primary production; Growth; Atlantic subtropical gyres; AMT 1. Introduction The deep chlorophyll maximum (DCM) is a consistent oceanographic feature of tropical and subtropical oceans. Several mechanisms have been proposed to explain its formation and maintenance, including higher in-situ growth at the nutricline ARTICLE IN PRESS www.elsevier.com/locate/dsr 0967-0637/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2006.07.008 Corresponding author. Tel.: +34 986 81 40 87; fax: +34 986 81 25 56. E-mail address: [email protected] (V. Pe´rez).
Transcript
ARTICLE IN PRESS
0967-0637/$ - se
doi:10.1016/j.ds
�Correspondifax: +34986 81
E-mail addre
Deep-Sea Research I 53 (2006) 1616–1634
www.elsevier.com/locate/dsr
Vertical distribution of phytoplankton biomass, production andgrowth in the Atlantic subtropical gyres
Valesca Pereza,�, Emilio Fernandeza, Emilio Maranona,Xose Anxelu G. Moranb, Mike V. Zubkovc
aDepartamento de Ecologıa y Biologıa Animal, Facultad de Ciencias del Mar, Universidad de Vigo,
Ctra. Colexio Universitario s/n, 36310 Vigo, SpainbInstituto Espanol de Oceanografıa, Centro Oceanografico de Xixon, Camın de L’Arbeyal, s/n, E 33212 Xixon, Spain
cGeorge Deacon Division for Ocean Processes, Southampton Oceanography Centre, University of Southampton,
Southampton SO14 3ZH, UK
Received 26 October 2005; received in revised form 28 July 2006; accepted 31 July 2006
Available online 2 October 2006
Abstract
Ninety-four stations were sampled in the Atlantic subtropical gyres during 10 cruises carried out between 1995 and 2001,
mainly in boreal spring and autumn. Chlorophyll a (Chl-a) and primary production were measured during all cruises, and
phytoplankton biomass was estimated in part of them. Picoplankton (o2mm) represented 460% of total Chl-a
concentration measured at the surface, and their contribution to this variable increased with depth. Phytoplankton carbon
concentrations were higher in the upper metres of the water column, whereas Chl-a showed a deep maximum (DCM). At
each station, the water column was divided into the upper mixed layer (ML) and the DCM layer (DCML). The boundary
between the two layers was calculated as the depth where Chl-a concentration was 50% of the maximum Chl-a
concentration. On average DCML extends from 67 to 126m depth. Carbon to Chl-a (C:Chl-a) ratios were used to estimate
phytoplankton carbon content from Chl-a in order to obtain a large phytoplankton carbon dataset. Total C:Chl-a ratios
averaged (7s.e.) 10377 (n ¼ 22) in the ML and 2474 (n ¼ 12) in the DCML and were higher in larger cells than in
picoplankton. Using these ratios and primary production measurements, we derived mean specific growth rates of
0.1770.01 d�1 (n ¼ 173) in the ML and 0.2070.01 d�1 (n ¼ 165) in the DCML although the differences were not
significant (t-test, p40.05). Our results suggest a moderate contribution of the DCML (43%) to both phytoplankton
biomass and primary production in the Atlantic subtropical gyres.
r 2006 Elsevier Ltd. All rights reserved.
Keywords: Phytoplankton; Biomass; Primary production; Growth; Atlantic subtropical gyres; AMT
e front matter r 2006 Elsevier Ltd. All rights reserved
The deep chlorophyll maximum (DCM) is aconsistent oceanographic feature of tropical andsubtropical oceans. Several mechanisms have beenproposed to explain its formation and maintenance,including higher in-situ growth at the nutricline
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1617
than in the upper mixed layer, physiologicalacclimation to low irradiance and high nutrientconcentrations, accumulation of sinking phyto-plankton at density gradients, behavioural aggrega-tion of phytoplankton groups, and differentialgrazing on phytoplankton (e.g. Cullen, 1982;Gould, 1987).
In the subtropical gyres, the DCM has beensuggested to be the result of a physiologicalacclimation of phytoplankton to low light levelsin the presence of high nutrient concentrations(Cullen,1982) resulting in an increase in cellularchlorophyll a (Chl-a) content and, consequently, ina decrease in the carbon to Chl-a (C:Chl-a) ratio.These areas, considered as the oligotrophic extremeof the ‘‘typical tropical structure’’ (TTS) regionsdescribed by Herbland and Voituriez (1979), arecharacterised by an upper mixed layer, wherenutrients are usually undetectable, a light-limiteddeep layer, and the presence of a Chl-a maximumlocated in the vicinity of the nutricline. In thesubtropical gyres, therefore, the use of Chl-aconcentration as an indicator of phytoplanktonbiomass could very likely result in the falseidentification of the DCM as a carbon-biomassmaximum.
Studies based on Chl-a size fractionation (Herb-land et al., 1985; LeBouteiller et al., 1992) show thatin areas characterised by the TTS, the contributionof small phytoplankton cells to total Chl-a is higherin surface waters and decreases with depth, reaching50% at the DCM. However, studies based on flowcytometry show that the slope of the size-abundancespectrum, which is a log–log plot of cell abundance(y-axis) versus cell size (x-axis), becomes morenegative from surface to the DCM and thenincreases with depth. These results reveal a growingimportance of small phytoplankton cells at theDCM and a progressive change toward larger cellsunderneath (Gin et al., 1999), and they suggest thatthe phytoplankton community structure showssignificant vertical variability in oligotrophic envir-onments. Species, pigment analyses and flow-cytometry studies reveal a two-layered structure ofthe phytoplankton composition in the tropical andsubtropical Atlantic and Pacific (Gieskes andKraay, 1986; Ondrusek et al., 1991; Venrick 1999;Veldhuis and Kraay, 2004). Usually, Prochloro-phytes and Cyanophytes dominate the upper mixedlayer while pico and nanoeukaryotes constitute ahigh portion of phytoplankton biomass at theDCM. In terms of abundance, Prochlorococcus
dominates the picophytoplankton communitythroughout the water column in tropical andsubtropical oceans (Campbell and Vaulot, 1993;Partensky et al., 1996; Zubkov et al., 1998).However, Prochlorococcus dominance in terms ofcell numbers does not always translate into aparallel dominance in terms of biomass (Claustreand Marty, 1995; Barlow et al., 2002; Veldhuis andKraay, 2004).
Primary production rates measured in the gyres(Letelier et al., 1996; Maranon et al., 2000) arehigher in the upper metres of the water column.Moreover, small differences (less than 10%) havebeen observed in satellite-derived primary produc-tion estimates of the North Atlantic and Pacificsubtropical gyres, depending on whether parame-terized or uniform Chl-a profiles are used (Sathyen-dranath et al., 1995; Ondrusek et al., 2001). Theseresults suggest a relatively low contribution of theDCM to depth-integrated primary production.Equally, phytoplankton turnover rates are generallyhigher in the upper mixed layer than in theproximity of the DCM (Malone et al., 1993;Goericke and Welschmeyer, 1998; Quevedo andAnadon, 2001), although a large variability ingrowth rate, ranging from 0.15 to 1.3 d�1, has beenreported in the subtropical gyres (e.g., Maranon,2005), revealing the existence of a more dynamicenvironment in the upper mixed layer of theoligotrophic oceans.
Most previous analyses of the vertical variabilityof phytoplankton biomass, production and sizestructure in the subtropical ocean have been basedon a relatively small number of observations, orhave limited spatial or temporal coverage. A recentstudy (Teira et al., 2005) aimed to characterise thetemporal and spatial variability of primary produc-tion and Chl-a in the northeastern subtropicalAtlantic based on observations collected for 12years in the region. In the present study, we use partof the Teira et al. data together with data from theSouth Atlantic subtropical gyre to obtain a largedataset (490 stations) of total and size-fractionatedChl-a and primary production, together withphytoplankton C biomass measured in the Northand South Atlantic subtropical gyres on 10 cruisesconducted during different seasons from 1995 to2001. While Teira et al. (2005) focussed on thetemporal and spatial variability, we used thisextensive dataset to characterize the patterns ofphytoplankton vertical variability in the subtropicalgyres. In order to assess the biogeochemical and
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341618
ecological role that the DCM plays in the oligo-trophic ocean, we aim to answer the followingspecific questions: (1) How does phytoplanktonsize structure change with depth? (2) Is the DCM aphytoplankton biomass maximum? (3) Is theDCM a productivity maximum? and (4) Dophytoplankton grow faster at the DCM than insurface water?
Fig. 1. Location of sampling stations over SeaWiFS
2. Methods
Sampling was carried out at 94 oligotrophicstations (surface chlorophyll o0.2mgm�3, unde-tectable surface nitrate concentration, sharp ther-mocline) of the subtropical gyres of the AtlanticOcean during 10 cruises conducted from 1995 to2001 (Fig. 1, Table 1). Fifty-five stations were
September 1997–August 2000 Chl-a composite.
ARTICLE IN PRESS
Table 1
Summary of cruises conducted from 1995 to 2001 in the subtropical NE Atlantic (NASTE) and in the subtropical S Atlantic (SATL)
Ocean where the results presented in this study were obtained
Cruise Ship NASTE St Dates NASTE SATL St Dates SATL
AMT-1 RRS James Clark Ross 3 30/09–03/10 (1995) 4 12/10–15/10 (1995)
AMT-2 RRS James Clark Ross 3 14/05–16/05 (1996) 4 04/05–07/05 (1996)
AMT-3 RRS James Clark Ross 2 28/09–29/09 (1996) 7 07/10–13/10 (1996)
AMT-4 RRS James Clark Ross 3 16/05–18/05 (1997) 5 02/05–08/05 (1997)
AMT-5 RRS James Clark Ross 2 26/09–27/09 (1997) 5 05/10–09/10 (1997)
AMT-6 RRS James Clark Ross 2 08/06–09/06 (1998)
Azores-1 BIO Hesperides 4 02/08–05/08 (1998)
Azores-2 BIO Hesperides 27 08/04–17/04 (1999)
AMT-11 RRS James Clark Ross 5 18/09–20/09 (2000) 14 01/10–08/10 (2000)
CIRCANA-1 BIO Hesperides 4 30/10–2/11 (2001)
Number of stations (St) and sampling dates are indicated for each cruise.
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1619
sampled in the eastern North Atlantic subtropicalgyre between 201 and 351N and 39 stations in theSouth Atlantic gyre between 51 and 301S. Hereafter,we shall use the terms NASTE and SATL to referthe two areas, although we are aware that they donot include the whole extension of the provinces asdescribed by Longhurst (1998). Sampling wasconducted between 1000 and 1200 local time, exceptduring AMT-11, when two stations were sampleddaily predawn and at noon. All chemical andmicrobiological measurements from AMT-11 pre-sented here were carried out on water collectedduring the early morning stations, except for Chl-aconcentration, which was measured on everystation.
During AMT cruises, vertical profiles of photo-synthetically active irradiance (PAR, 400–700nm)were obtained by integrating the measurements ofdownwelling irradiance at seven SeaWiFS wavelengthbands as measured with an optical profiler (SeaOPS).The downwelling irradiance in the water column wasdetermined with a Licor Li-1800UW spectroradi-ometer during Azores cruises and with a SatlanticOCP-100 FF sensor during the CIRCANA-1 cruise.Vertical profiles of temperature and salinity wereobtained at each station with a CTD probe attachedto a rosette sampler equipped with Niskin bottles.CTD temperature and salinity sensors were calibratedwith digital reversing thermometers and water samplesdrawn for salinity determinations. In this study thebeginning of the thermocline was defined as the depthwhere the thermal gradient was 40.1 1C/m. Samplingstrategy and the acquisition of complementaryphysical and chemical variables followed JGOFSprotocols (http://www.uib.no/jgofs/Publications/
Report_Series/), although there were slight variationson some of the cruises.
During Azores-1, Azores-2 and AMT cruises,dissolved inorganic nitrogen was determined with aTechnicon segmented flow colorimetric auto-analy-zer as described in Treguer and LeCorre (1975)(Azores-1 and Azores-2 cruises) and in Woodward(1994) (AMT cruises). Nitrate detection limits rangefrom 25 nM during the AMT-11 cruise to 0.1 mMduring the rest of the AMT cruises. The nitraclinedepth was considered as the first depth where nitratevalues were detectable.
Sampling depths for Chl-a and primary produc-tion were determined after examination of theirradiance, temperature, salinity and fluorescenceprofiles. Typically, 2–3 sampling depths werelocated in the upper mixed layer, 2–3 in the DCMzone, and 1–2 below the DCM. Water samples(100–250ml) for Chl-a determination were collectedfrom 5–7 depths in the upper 200m of the watercolumn and sequentially filtered through 20, 2 and0.2 mm polycarbonate filters. Chl-a concentrationwas measured fluorometrically after extraction in90% acetone at �20 1C overnight. During AMT-1and AMT-2 cruises the acidification technique ofHolm-Hansen et al. (1965) was used. During the restof the cruises Chl-a concentration was measured bythe non-acidification technique of Welschmeyer(1994). Total Chl-a was determined from theaddition of size-fractionated measurements. DuringAMT-1, only total, unfractionated Chl-a wasmeasured. All stations were characterised by theexistence of a deep (450m depth) chlorophyllmaximum where the Chl-a concentration was atleast twice the surface value. At each station, the
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341620
boundary between the low Chl-a upper mixedlayer (ML) and the DCM layer (DCML) waschosen as the depth where Chl-a concentrationwas 50% of the maximum Chl-a concentration. Thisconcentration also defined the bottom of theDCML, which, on average, extended from 67 to126m depth.
During AMT-1, AMT-2, AMT-3, and AMT-4,100ml samples were preserved with Lugol0s solutionfor identification to species level and counting ofnano- (2–20 mm) and microplankton (420 mm). Atleast two samples, one from surface and the otherfrom the DCM, were taken at each station. Sampleswere allowed to settle in sedimentation chambersfor 2–3 d and subsequently examined at 187 and 750magnifications under an inverted microscope. Cellnumbers were converted into carbon biomass asdescribed by Holligan et al. (1984). The abundanceof phototrophic picoplankton (o2 mm) was deter-mined with a flow cytometer (Zubkov et al., 1998;Moran et al., 2004) during AMT-3, AMT-4, andCIRCANA-1 cruises. Synechococcus spp. and Pro-
chlorococcus spp. cyanobacteria, and small photo-synthetic eukaryotes (picoeukaryotes) werediscriminated. Samples were taken at 10–12 depthsfrom the surface down to 200m. Picoplanktonabundance was transformed to biomass with theempirical conversion factors obtained by Zubkovet al. (2000): 32 fgC cell�1 for Prochlorococcus spp.,103 fgC cell�1 for Synechococcus spp. and1496 fgC cell�1 for picoeukaryotes.
For the determination of primary production,water samples from five to seven depths weretransferred, immediately after collection, to four75-ml acid-cleaned polystyrene bottles (3 light and 1dark), inoculated with 370–740 kBq (10–20 mCi)NaH14CO3 and incubated for 6–7 h. Incubationswere started within 30min of sampling and wereterminated at sunset, except during AMT-11, whenincubations lasted 24 h. Samples were placed in anon-deck incubator that simulated the irradiance atthe original sampling depths and were cooled withsurface seawater. Average temperature differencebetween surface and the DCM depth was 2.5 1C.Temperature difference was higher than 5 1C at 13of the 94 stations. After the incubation period,samples were sequentially filtered through 20, 2, and0.2 mm polycarbonate filters at very low vacuum(o50mmHg). During AMT-1 only total primaryproduction was estimated by filtration through glassfibre filters. Removal of inorganic 14C that had notbeen incorporated by phytoplankton as organic
carbon from the filters was achieved by exposingthem to concentrated hydrochloric acid (HCl)fumes for 12 h. Then the filters were transferred toscintillation vials to which 4ml of scintillationcocktail were added. Radioactivity in each samplewas measured on a scintillation counter on board(AMT cruises, Azores-2 and CIRCANA-1) orashore (Azores-1). Quenching was corrected withan external standard. Dark-bottle values weresubtracted from the counts obtained in the lightsamples. Total primary production was determinedby addition of the size fractionated rates. Daily rateswere calculated by taking into account the daylightperiod and assuming that dark respiratory lossesamount to 20% of the carbon incorporation duringthe light period (Marra and Barber, 2004).
Euphotic-zone-integrated values of size-fractio-nated and total Chl-a and particulate carbonproduction were obtained by trapezoidal integra-tion of the volumetric data down to the depth of 1%surface incident irradiance.
3. Results
3.1. The DCM in the subtropical gyres
Table 2 shows averaged values of selectedphysical, chemical and biological variables in thesubtropical gyres during the present study. Nitra-cline depth was similar in the NASTE and theSATL (t-test, p40.05), while the thermocline wassignificantly deeper in the SATL than in the NASTE(t-test, po0.001). The depth of the DCM was alsosignificantly higher in the SATL (t-test, po0.001).Mean temperature difference between the DCMdepth and surface was 2.29 1C in the NASTE and2.70 1C in the SATL. Chl-a concentrations wereo0.1 and o0.4mgm�3 at the surface and at theDCM, respectively, and slightly higher Chl-a con-centrations were measured in the SATL as com-pared to the NASTE at the surface (t-test, po0.001)and at the DCM (t-test, po0.05). Euphotic-depth-integrated primary production rates and picoplank-ton (o2mm ) contributions to total primaryproduction showed no differences between thetwo gyres (t-test, p40.05). On the contrary, depth-integrated Chl-a concentrations and picoplanktoncontributions to total Chl-a were significantly higherin the SATL than in the NASTE (t-test, po0.001),although the differences in total Chl-a between gyresdisappeared upon division by the euphotic-layerdepth. Picophytoplankton contribution to Chl-a was
ARTICLE IN PRESS
Table 2
Averaged values7standard error (s.e.) and sample size (n) of selected variables at the sampling stations
Contribution of o2mm cells to total Chl-a (%) 7171 (52) 7971 (32) 7471 (84)
Contribution of o2mm cells to total primary production (%) 5172 (33) 5473 (25) 5272 (58)
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1621
significantly larger than to primary production(t-test, po0.001).
3.2. Chl-a and phytoplankton carbon biomass
(Phyto C)
The averaged vertical distribution of Chl-aconcentration measured in the subtropical gyres(NASTE+SATL; Fig. 2a) remained almost con-stant in the upper 50m of the water column, thenChl-a concentration increased progressively downto the DCM, located at 80–110m, where maximumvalues of �0.26mgm�3 were reached. Chl-a con-centrations decreased steadily from the DCM downto 200m depth. A very similar averaged verticalChl-a distribution was found in each gyre separately(Figs. 2b and c), although in the SATL Chl-aconcentrations at the DCM were higher. Bycontrast, the vertical distribution of total phyto-plankton carbon biomass (Phyto C) (Figs. 2d–f)presented higher concentrations (�10mgm�3) inthe upper 90m of the water column and decreasedto �5mgm�3 in the lower part of the DCML.However, it is difficult to get a real trend given thescarce number of Phyto C measurements.
The contribution of picoplankton to total Chl-awas always higher than 60% (Fig. 3a) and increasedfrom 60% at the surface to 80% at 160m depth.A similar pattern was observed in the NASTE(Fig. 3b), where higher percentages were observedat 130m (75%). In the SATL (Fig. 3c), the trend wasslightly different. The contribution of picoplanktonto total Chl-a increased from 72% at the surface to90% at 200m, although a subsurface maximum(�80%) was present at 20–30m. The contribution ofpicoplankton to Phyto C ranged from 38% to 63%(Figs. 3d–f) and did not show a clear vertical pattern.
Averaged (7s.e.) Chl-a and Phyto C values in theML (whose lower boundary is defined as the depthwhere Chl-a concentration is 50% of the maximumChl-a concentration; see Section 2) and in theDCML are shown in Table 3. Very low Chl-aconcentrations were measured in the ML. Total,unfractionated Chl-a concentrations ranged from0.01 to 0.23mgm�3 in the ML and from 0.05 to0.64mgm�3 in the DCML. Chl-a concentration wasalso low in the larger (42 mm) phytoplankton sizefraction as picophytoplankton (o2 mm) dominatesChl-a concentrations throughout the water column(Fig. 3a). On the contrary, averaged Phyto Cconcentration was similar in the ML and in theDCML (t-test, p40.05) and was significantly higherin the small than in the large size fraction (t-test,po0.001).
We calculated C:Chl-a ratios using total and size-fractionated Phyto C and Chl-a concentrationsmeasured in both gyres during AMT-3 and AMT-4 cruises, when size-fractionated Chl-a and Phyto Cwere measured simultaneously. The datasets fromboth hemispheres were pooled together, given thescarce number of Phyto C measurements availableand the relatively constant vertical pattern followedby Chl-a and Phyto C in the two gyres (see Fig. 2).Ratios 4500 were excluded from the analysis(4 values). Total C:Chl-a ratios ranged from 56 to200mgCmgChl�1 in the ML and from 11 to54mgCmgChl�1 in the DCML. Size-fractionatedC:Chl-a ratios in the ML ranged between 47 and155 for o2 mm phytoplankton, and between 74 and493 for the 42 mm. In the DCML, C:Chl-a ratiosvaried between 8 and 30 in the o2 mm size fractionand between 29 and 147 in the 42 mm size fraction.Averaged C:Chl-a ratios (Table 3) were significantlyhigher in the ML than in the DCML and in the
ARTICLE IN PRESS
Fig. 2. Averaged vertical profiles of total Chl-a (left panels) and total Phyto C (right panels), both in mgm�3, at all sampling stations
(a and d), at the stations located in the Northern gyre (b and e) and at the stations located in the Southern gyre (c and f). Horizontal bars
represent the standard error (s.e.). Numbers indicate the number of values making up each average. No number (or error bar) indicates
only a single value. Dashed lines represent the vertical limits of the DCML.
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341622
ARTICLE IN PRESS
Fig. 3. Averaged vertical profiles of the picoplankton contribution (%) to total Chl-a (% Chl-a o2mm; left panels) and to total Phyto C
(% Phyto C o2 mm; right panels) at all sampling stations (a and d), at the stations located in the Northern gyre (b and e) and at the
stations located in the Southern gyre (c and f). Horizontal bars represent the standard error (s.e.). Numbers indicate the number of values
making up each average. No number (or error bar) indicates only a single value. Dashed lines represent the vertical limits of the DCML.
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1623
ARTICLE IN PRESS
Table 3
Averaged values7standard error (s.e.) and data number (n) of selected variables in the mixed layer (ML) and in the DCM layer (DCML)
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341624
42 mm than in the o2 mm size fraction (t-test,po0.001). We estimated the phytoplankton carbonbiomass (Est Phyto C) for each layer by multiplyingthe average Chl-a concentration by the averagedC:Chl-a estimated for each layer. Unlike themeasured Phyto C biomass, Est Phyto C concentra-tions were significantly higher in the ML than in theDCML (t-test, po0.001) in all size fractions. EstPhyto C was also higher in the o2 mm size fractionthan in large size fraction in the DCML (t-test,po0.05), although there was no difference betweenthe two size fractions in the ML.
3.3. Vertical variability of phytoplankton primary
production and growth rates
Averaged vertical profiles of primary production,when both gyres are jointly considered (Fig. 4a),showed higher total C incorporation rates in theupper 90m of the water column (ranging from 1.0to 2.3mgm�3 d�1) than in the DCML. However,this pattern is slightly different in each gyre. In thenorthern gyre (Fig. 4b), the highest primaryproduction rates (up to 2.2mgm�3 d�1) weremeasured in the upper 40m, while in the southerngyre (Fig. 4c) the highest rates (up to 2.7mgm�3 d�1
at 80m) were found in the upper part of the DCML.In general, the contribution of picoplankton toprimary productivity (Fig. 4d) showed a slightincrease with depth from �45% in the upper 60mof the water column to �60% at 120m. Below thisdepth, picoplankton contribution to primary pro-duction decreased. This trend mirrored that of thenorthern gyre (Fig. 4e), while in the southern gyre(Fig. 4f) picoplankton contributions reached highervalues than in the NASTE. Averaged primaryproduction measured in the ML (Table 3) wassignificantly different from that averaged in the
DCML (t-test, po0.05 for total and the o2 mm sizefraction and po0.001 for the 42 mm size fraction).Primary production rates were higher in the ML forlarge (42 mm) and total phytoplankton sizes and inthe DCML for the small (o2 mm) cells.
We calculated the carbon-specific phytoplanktongrowth rate (m, d�1) from daily primary productionrates (DC) and the estimated phytoplankton carbonbiomass (Est Phyto C) according to the equation:m ¼ ln [(Est Phyto C+DC)/ Est Phyto C]. We havechosen estimated phytoplankton biomass (EstPhyto C) instead of measured phytoplanktonbiomass (Phyto C) because of the scarcity of PhytoC data available (see Figs. 2 and 3). The carbonspecific phytoplankton growth rate showed almostconstant values (�0.20 d�1) from surface to 110m,then decreased with depth (Fig. 5a). In the NASTE,m showed values 40.20 d�1 both in the ML and inthe DCML (Fig. 5b), while in the southern gyre thehighest rates (40.20 d�1) were found at 80–90mdepth coinciding with the beginning of the DCML(Fig. 5c). The highest picoplankton growth rateswere estimated at 70–80m depth (�0.30 d�1), whenthe two gyres were either jointly or separatelyconsidered (Figs. 5d–f). Relatively high picoplank-ton m values (up to 0.27 d�1) were also estimatedfor the upper water column in the northern gyre(Fig. 5e). It is worth mentioning the large variabilityassociated with picoplankton growth rate estimates.In the case of 42 mm phytoplankton (Figs. 5g–i),the highest growth rates were measured in the upper40m of the water column, reaching 0.23 and0.35 d�1 in the NASTE and the SATL, respectively,and decreasing rapidly downwards. Averaged phy-toplankton growth rates in the ML and in theDCML did not differ (t-test, p40.05, Table 3).However, significant differences were found in thesmall size fraction between the two layers. As for
ARTICLE IN PRESS
Fig. 4. Averaged vertical profiles of total primary production rates in mgm�3 d�1 (left panels) and picoplankton contribution to total
primary production expressed as percentage (right panels) at all sampling stations (a and d), at the stations located in the Northern gyre (b
and e) and at the stations located in the Southern gyre (c and f). Horizontal bars represent the standard error (s.e.). Numbers indicate the
number of values making up each average. No number (or error bar) indicates only a single value. Dashed lines represent the vertical limits
of the DCML.
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1625
ARTICLE IN PRESS
Fig. 5. Averaged vertical profiles of phytoplankton growth rates (m, d�1) for total phytoplankton (left panels), for the o2mmphytoplankton size fraction (central panels) and for the42mm phytoplankton size fraction (right panels) at all sampling stations (a, d and
g), at the stations located in the Northern gyre (b, e and h) and at the stations located in the Southern gyre (c, f and i). Horizontal bars
represent the standard error (s.e.). Numbers indicate the number of values making up each average. No number (or error bar) indicates
only a single value. Dashed lines represent the vertical limits of the DCML.
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341626
ARTICLE IN PRESS
Table 4
Averaged integrated values7standard error (s.e.) of selected variables in the upper mixed layer (ML) and in the DCM layer (DCML) for
Est Phyto-C (mgm�2) 854749 514725 452725 279714 372723 194716
6272% 3872% 6172% 3972% 6572% 3572%
Primary production (mgm�2 d�1) 115711 83710 6477 5377 5676 2974
5973% 4173 % 5573% 4573% 6674% 3474%
Numbers in bold represent the averaged contribution (%)7s.e. of each layer to the integrated value throughout the water column
(ML+CML).
V. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1627
primary production, picoplankton growth rateswere significantly higher in the DCML than in theML (t-test, po0.001).
3.4. Contribution of the DCM to the phytoplankton
biomass and productivity of the Atlantic subtropical
gyres
Phytoplankton carbon biomass and primaryproduction were depth-integrated in the ML, inthe DCML and throughout the water column(ML+DCML layer) to estimate the relative con-tribution of each layer to the total biomass andproductivity of the subtropical gyres (Table 4). Inthe NASTE, the DCML accounted for the samefraction of the water column picoplankton biomassand primary production as the ML (t-test, p40.05).For the large phytoplankton size fraction theDCML represented a significantly lower fractionof the water column primary production (3572%;t-test, po0.001) and biomass (4371%; t-test,po0.001). In the SATL, the ML layer showedsignificantly higher contributions to water columnphytoplankton biomass and primary productionthan the DCML (�60%; t-test, po0.001 forbiomass and po0.05 for primary production). Theexception, in this region, was the small phytoplank-ton size fraction, where no significant differenceswere found between the contribution of the DCMLand the ML to primary production (t-test, p40.05).
4. Discussion
4.1. Vertical distribution of phytoplankton size
fractions
The importance of small phytoplankton cells inthe oligotrophic regions of the ocean is wellestablished in terms of Chl-a concentrations, cellabundances and primary production rates (e.g.,Zubkov et al., 1998; Maranon et al., 2001).However, the vertical pattern of the relativecontribution of picoplankton to total phytoplank-ton biomass remains unclear. In the tropicalAtlantic, Herbland et al. (1985) found that thecontribution of the small (o1 mm) phytoplankton tototal Chl-a was maximum (�70%) in the nitrate-depleted upper mixed layer (NO�3 o0.1 mM),decreased to 50% at the nitracline depth and wasalways o50% in the nutrient-replete, light-limitedbottom layer. The same vertical distribution of Chl-a o1 mm was observed in the equatorial Pacific byLeBouteiller et al. (1992), who identified o1 mmphytoplankton size with photosynthetic prokar-yotes and 41 mm with eukaryotic microalgae, butthey did not measure the abundances of thesegroups. Although small cells absorb light moreefficiently in low-irradiance environments, as at thebottom of the euphotic layer in the tropical oceans,it seems that the influence of irradiance onphytoplankton vertical distribution in the tropical
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341628
oceans is less important than the effect of nutrientavailability. These results suggest that the verticaldistribution of phytoplankton in these areas iscontrolled largely by nutrient availability, as smallphytoplankton cells are more efficient in taking upnutrients at low nutrient levels. In contrast, ourstudy shows that the contribution of picoplankton(o2 mm) to total Chl-a in the subtropical gyresincreased with depth. Similar findings have beenreported by Lutz et al. (2003) in the North Atlanticand Taguchi et al. (1988) in the Caribbean Sea andin the subtropical western Atlantic. Our results alsoagree with those of Gin et al. (1999) in the SargassoSea, who found an increase in the relative contribu-tion of picoplankton cells down to the DCM depthand a slight shift towards large phytoplankton sizes,based on the slope of size-abundance spectrum,below the DCM. These authors explained thedominance of small cells at the DCM in terms ofthe competitive advantages of small-sized cells inreduced irradiance conditions.
The apparent discrepancy in the vertical distribu-tion pattern of phytoplankton size structure is likelyto be related to the different phytoplankton sizefractions considered in the studies. In their investi-gations, Herbland et al. (1985) and LeBouteilleret al. (1992) used 1 mm as the upper limit for thepicoplankton size class. According to Campbell andVaulot (1993), Prochlorococcus cells (0.5–0.7 mm)dominated the ML, and picoeukaryotes, which arelarger than 1 mm and therefore not included in theHerbland et al. (1985) and LeBouteiller et al. (1992)studies, dominated below the DCM. In general, thevertical distribution of Prochlorococcus in thesubtropical Atlantic is homogeneous in the MLand presents a maximum close to the DCM depth,where this taxonomic group dominates in terms ofcarbon biomass, Chl-a and cell abundance (e.g.,Zubkov et al., 1998). The vertical distribution ofpicoeukaryotes also shows increasing abundanceswith depth, reaching maximum values at the DCM,where they account for an important fraction ofphytoplankton biomass (Li, 1995; Partensky et al.,1996; Veldhuis and Kraay, 2004).
4.2. C to Chl-a ratios
Measurement of phytoplankton carbon biomassin natural populations is not straightforward.During this study we obtained Phyto C on onlytwo cruises from flow cytometry and microscopicalcount and identification. However, Chl-a was
obtained routinely on all cruises. So we decided toconvert the easily measured Chl-a to carbon bymeans of appropriate C:Chl-a ratio as an alternativeto the direct quantification of Phyto C. A widerange of C:Chl-a ratios, from ca. 20 to 4400, hasbeen reported in phytoplankton cultures growing atdifferent rates under different nutrient availability,light, and temperature conditions (Laws and Bann-ister, 1980; Sakshaug et al., 1989; Geider, 1993). Thedifferent patterns followed by the vertical distribu-tions of Phyto C and Chl-a observed in this studysuggested the C:Chl-a ratio might vary with depth.So, we calculated the corresponding C:Chl-a ratiosfor each depth where both variables were concur-rently measured. The averaged (7s.e.) C:Chl-a ratiowas 10377 (ranging from 56 to 200) in the ML and2474 (ranging from 11 to 54) in the DCML, whenthe data sets from both gyres were jointly con-sidered. Our C:Chl-a estimates for the ML areslightly lower than those previously reported in theeastern subtropical North Atlantic (�160–250;Taylor et al., 1997; Veldhuis and Kraay, 2004;Behrenfeld et al., 2005). The C:Chl-a ratios esti-mated for the western subtropical North Atlantic bydifferent authors were more variable, ranging from40–160 in the ML to 15–65 in the DCML (Li et al.,1992; Goericke and Welschmeyer, 1998; Lefevreet al., 2003). This wide range of values is probablyrelated to the different methods used in these studies(Maranon, 2005) and to the larger seasonalvariability characteristic of the upper water columnin the western subtropical Atlantic (e.g., Longhurst,1998). It is noteworthy that, despite the differencesin magnitude, all the studies carried out insubtropical and tropical oceans show that C:Chl-aratios are always 3–6 fold higher in surface watersthan at the DCM (Malone et al., 1993; Campbellet al., 1994; Veldhuis and Kraay, 2004), whichreflects the increasing chlorophyll content per cell asirradiance levels decrease, as has been reported forSynechococcus and Prochlorococcus (Olson et al.,1990; Campbell and Vaulot, 1993; Lutz et al., 2003).
In this study, we also observed differences in theC:Chl-a ratios as a function of phytoplankton size.We estimated higher ratios in the 42 mm than in theo2 mm size fraction (Table 3). These results,however, must be taken with caution, as phyto-plankton C biomass was estimated by differentmethods for the two size fractions (see Section 2).Although the comparison of our results is difficult,mainly because of the size classes considered in ourstudy and to the different methods used in the
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1629
literature to estimate phytoplankton biovolumesand carbon content, previous field and culturestudies have also reported an increase in C:Chl-aratio with phytoplankton size (Furuya, 1990;Finkel, 2001; Arin et al., 2002). This is expectedon theoretical grounds, since pigment content ismore closely related to cell surface area, whereascarbon content is more closely related to cell volume(Finkel, 2001). However, other studies show that theC:Chl-a ratio does not change with cell size (Blascoet al., 1982; Geider et al., 1986; Montagnes et al.,1994). Besides, we cannot rule out the possibilitythat the size dependence of the C:Chl-a ratio couldbe related to differences in taxonomic compositionbetween small (o2 mm) and large (42 mm) phyto-plankton. Thus, prokaryote phytoplankton usuallyshow higher C:Chl-a ratios than eukaryotes (Fur-uya, 1990; Odate et al., 1993; Geider, 1993), andalso dinoflagellates have been reported to showhigher ratios as compared to diatoms grown incultures (Chan, 1980).
Nevertheless, it is necessary to note that ourresults could be biased by the use of constant C/cellconversion factors to estimate picoplankton carboncontent from cell abundances (see Section 2). It iswell known that, in the subtropical gyres, Prochlor-
ococcus, Synechococcus and picoeukaryotic cell sizes(Li et al., 1992; Sieracki et al., 1995), and thereforethe carbon content per cell, change with depth. Inorder to check the effect of the vertical variability ofthis factor on our results we applied different C/cellfactors obtained from the literature to our pico-plankton abundances. We estimated Prochloroccus
and Synechococcus biomass by assuming the con-version factors reported by Sieracki et al. (1995) inthe Sargasso Sea: 10 fgC/cell in the ML and 49 fgC/cell in the DCML for Prochlorococcus and 99 fgC/cell in the ML and 199 fgC/cell in the DCML forSynechococcus. For picoeukaryotes a constantfactor 1500 fgC/cell (Zubkov et al., 1998) was used,despite the fact that this group shows a slightdecrease of cell size with depth (Li et al., 1992; XeluMoran, pers. commun.). With these factors weobtained lower C:Chl-a ratios for the small sizefraction (39 in the ML and 25 in the DCML) andfor the total size fraction (77 in the ML and 30 inthe DCML) than those obtained assuming aconstant factor with depth (see Table 3). However,the C:Chl-a ratios are still higher in the ML than inthe DCML (t-test, po0.05 for the small sizefraction and po0.001 for the total size fraction).Recently, Veldhuis and Kraay (2004) used a slightly
higher conversion factor for Prochlorococcus
(35 fgC/cell in the ML and 50 fgC/cell in theDCML). Using these factors for Prochlorococcus
and maintaining Synechococcus and picoeukaryotesfactors as above we calculated C:Chl-a ratios andphytoplankton growth rates similar to those re-ported in our study. In any case, C:Chl-a ratios forpicoplankton are higher in the ML than in theDCML, suggesting that the increase in the C/cellratio with depth is lower than that of the Chl-a/cellratio.
4.3. DCML contribution to phytoplankton biomass
and productivity
In this study, the DCML, defined as depths whereChl-a concentrations are 0.5 times higher than thevalue measured at the Chl-a maximum, accountedfor 65–75% of the euphotic-depth-integrated Chl-aconcentration in the subtropical gyres of theAtlantic Ocean. However, our results show that,as reported in previous studies, the DCML does notrepresent either a phytoplankton biomass or aprimary production maximum (Table 4; Claustreand Marty, 1995; Goericke and Welschmeyer, 1998;Maranon et al., 2000). Using photosynthesis-irra-diance (P-E) experiments, Lorenzo et al. (2004)found a DCML contribution to primary production(54717%, average7s.d.) similar to that reported inour study (4672, average7s.e.) although theseauthors defined the DCML as the layer that showeda steady increase–decrease in the Chl-a concentra-tion above and below of the maximum Chl-a valueof the water column.
It is necessary to note that, although during ourstudy the DCML accounted for a similar or slightlylower amount of the water-column-integrated pri-mary production than the ML (Table 4), the highestprimary production rates were measured well abovethe DCM (Figs. 4a and b). These results suggestthat the reduced light environment at the DCMdepth may be partially compensated by an increasein the chlorophyll concentration, resulting in acontribution of the DCML to the water columnintegrated primary production similar to that of theML. Therefore, it would be necessary to considerthe Chl-a profile in primary productivity models.
4.4. Phytoplankton growth rates
There is a growing interest in the estimation ofphytoplankton growth rates in the ocean as they
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341630
largely determine the degree of coupling betweenautotrophic and heterotrophic components of theplanktonic community (Maranon et al., 2000) andtherefore affect the carbon fluxes through theplanktonic food web. Observed phytoplanktongrowth rates in the oligotrophic oceans are eitherclose to their theoretical maximum values, i.e.,1.5–2 d�1 in the subtropical Pacific (Laws et al.,1984, 1987; Jones et al., 1996), or well below thesevalues in the subtropical North Atlantic (Maloneet al., 1993; Goericke and Welschmeyer, 1998;Maranon et al., 2000). Phytoplankton growth ratesestimated in the upper layer of the subtropicalAtlantic during our study (averaged value of0.17 d�1) were lower than those previously reportedin the eastern subtropical North Atlantic(0.4–0.8 d�1; Stelfox-Widdicombe et al., 2000; Que-vedo and Anadon, 2001) and in the lower end of therange reported in the western subtropical Atlantic(0.1 �1.3 d�1; Malone et al., 1993; Goericke andWelschmeyer, 1998; Lessard and Murrell, 1998).
The low phytoplankton growth rates presentedhere are a direct consequence of the primaryproduction rates and phytoplankton biomass esti-mated in our study. Averaged euphotic-depth-integrated primary production rates measured inthe NASTE and SATL (156716 and205717mgCm�2 d�1, respectively) are lower thanthose reported in other oligotrophic areas such asthe Bermuda Atlantic and Hawaii Ocean times-series (BATS and HOT, respectively, with an annualaveraged rate �500mgCm�2 d�1) and slightlylower than those estimated with the bio-opticalmodel of Longhurst et al. (1995; 330 and210mgCm�2 d�1 in the NASTE and SATL, re-spectively). However, differences between theseareas could be explained by taking into accounttheir hydrographic characteristics. The HOT zonein the subtropical Pacific is a permanently stratifiedregion with mixed layer depth nearly always5100m, and therefore lower primary productionrates than in the subtropical North Atlantic couldbe expected. However, other factors, such as theavailability of dissolved inorganic phosphate, whichis much lower in the subtropical North Atlanticthan in the subtropical Pacific (Wu et al., 2000),could be influencing productivity differences be-tween the two areas. The BATS station is locatednear the edge of the subtropical gyre and experi-ences deep mixing during winter months(100–400m), leading to a modest spring bloom.Most of our data derive from AMT cruises carried
out in May and October, and therefore, we couldhave missed high primary production events in latewinter/early spring, which would be recorded in theBATS programme because of the monthly sam-pling. Nevertheless, averaged primary productionrate from Bermuda time series in May and Octoberfrom 1989 to 2001 (http://bats.bbsr.edu/) are stillhigher (472729mgCm�2 d�1, average7se) thanours. Another important difference is the intenseeddy activity in the BATS region (McGillicuddyet al., 1998), which has been suggested to representan important nutrient input to the euphoticlayer in the area in comparison to the eastern NorthAtlantic gyre, where we have never detectedinorganic nutrients in surface waters.
It is necessary to take into account someprocesses that could be affecting our estimates ofphytoplankton growth, such as losses of 14C duringprimary production incubations due to the grazing,or the possible mixotrophic activity of the phyto-plankton. Firstly, if during primary productionexperiments zooplankton respired or excreted asignificant amount of the 14C previously ingested asa consequence of their grazing activity, we would beunderestimating primary production. Given that thesmall size of the incubation bottles used in our study(70ml) exclude mesozooplankton, the effect ofmicrozooplankton on primary production measure-ments could be estimated by using the model ofLaws et al. (1984). Assuming that 70% of labelledcarbon is respired or excreted by microzooplankton(Landry and Calbet, 2004), that grazing rate equals99% of phytoplankton growth rate, and a phyto-plankton growth rate close to the theoreticalmaximum of 2 d�1, during a incubation of 6–7 hthe model predict that microzooplankton activitywould reduce by 17% the estimated 14C particulateprimary production. Therefore, if actual phyto-plankton growth rates were that high, we would beunderestimating primary production rates, becauseof the grazing activity, and consequently phyto-plankton growth rates. However, these rates wouldstill be lower than 0.25 d�1. Secondly, as our growthestimates are based only on photosynthesis theymay underestimate real growth rates if the use oforganic substances by phytoplankton is widespreadand significant. Recent studies show that Prochlor-
ococcus spp. are able to use organic nitrogencompounds in the oligotrophic open ocean (Zubkovet al., 2003). These authors estimated that amino-acid uptake represents 10% of the nitrogen require-ments of Prochloroccocus in oligotrophic areas
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–1634 1631
assuming that Prochlorococcus accounts for 50% ofthe total primary production and 30% of theleucine-derived bacterioplankton production, anda C:N ratio of 6.6 for this group. Taking intoaccount these values the amino-acid uptake ofProchloroccocus in their study represents 5% oftotal primary production. These estimates suggestthat the use of amino acids is small in comparisonwith the use of inorganic carbon. Mixotrophy is alsocommon among flagellates. During our study, wehave included unidentified flagellate biomass ofunclear trophic status into the Phyto C. We checkedthe effect of considering different contributions ofautotrophs to total unidentified flagellates onC:Chl-a ratios. We found that it suffices thatautotrophs represent X30% of the unidentifiedflagellates in the ML (or 15% in the DCML) for theresulting C:Chl-a ratios to be higher in large than insmall phytoplankton. Besides, a smaller contribu-tion of autotrophs would imply total C:Chl-a ratioslower than those typically reported in the literature(for example, a contribution o30% would result inC:Chl-a ratios of 7674 in the ML and 2073 in theDCML).
Slow phytoplankton growth rates in the subtro-pical Atlantic have been explained in terms of theobserved assimilation numbers and C:Chl-a ratiosin a review by Maranon (2005). He estimated themaximum potential growth rate as mmax ¼
D� PBmax=C : Chl�a where PB
max is the light-satu-rated, chlorophyll normalised photosynthesis rate,obtained in short (2 h) incubations (therefore mini-mising effects of 14C respiration and bottle confine-ment) during the central hours of the day (whenPBmax is close to its maximum) and D is the duration
of the photoperiod to convert hourly into dailyrates. According to this equation, and given C:Chl-afrom the literature, the PB
max necessary to supportphytoplankton growth rates of 1 d�1 would be wellabove those reported in the subtropical Atlantic.The low phytoplankton growth rates measured inour study, together with the low heterotrophicbacteria growth rates reported for the upper watersof the subtropical Atlantic gyres (e.g. 0.12 d�1;Zubkov et al., 2000), suggest the existence of amicrobial community that turns over very slowly.
Small phytoplankton presented higher (t-test,po0.001) growth rates in the DCML (0.2570.02 d�1) than in the ML (0.1870.01 d�1), whilethe contrary (t-test, po0.05) occurred in the largersize fraction (0.1670.01 d�1 at ML vs. 0.1370.01 d�1 at the DCML). Our results suggested that
picoplankton might outcompete large cells in high-nutrient, low-light environment of the DCML.Although to our knowledge there are no studiesreporting in-situ phytoplankton growth rates fordifferent size classes, we can compare our pico-plankton growth rates with those of Prochlorococ-
cus, as this species is the main component ofpicoplankton in our study area. Our estimates agreewith those of Goericke and Welschmeyer (1998) inthe upper layer of Sargasso Sea; they measuredProchlorococcus growth rates of 0.2–0.3 d�1 usingthe 14C labelling of divinyl Chl-a. However,Prochlorococcus growth rates above the maximumvalues measured in cultures (from 0.5 to 0.6 d�1;Partensky et al., 1999) were estimated in thesubtropical Pacific (0.2–0.6 d�1) and in the ArabianSea (up to 1 d�1) by cell cycle analysis (Liu et al.,1997; Liu et al., 1998).
5. Conclusions
We have characterized the vertical variability ofphytoplankton biomass, size structure, productionand growth in the Atlantic subtropical gyres. Inanswer to the questions posed in the Introduction,we concluded that: (1) picophytoplankton contribu-tion to total Chl-a and primary production in-creased with depth to the DCM; (2) the deepchlorophyll maximum does not represent a phyto-plankton-biomass or primary-productivity maxi-mum but contributes a substantial fraction of thevertically integrated algal standing stocks andC-fixation rates; and (3) phytoplankton grew atthe same slow rate in the DCML as in the ML.
Acknowledgments
Thanks are given to Derek Harbour for providingdata on phytoplankton abundance and biomass.Comments by Alex Poulton and three anonymousreviewers improved an early version of the manu-script. We are indebted to the Captain and crew ofthe research vessels, as well as to all colleagues onboard during the 10 cruises. This study wassupported by the UK Natural Environment Re-search Council through the Atlantic MeridionalTransect programme (NER/O/S/2001/00680), theEU Contract CANIGO (MAS3CT960060), and agrant from the Spanish Ministry of Science andTechnology (McyT) (CIRCANA, MAR99-1072-01). V.P. was supported by a postgraduate
ARTICLE IN PRESSV. Perez et al. / Deep-Sea Research I 53 (2006) 1616–16341632
fellowship from the MCyT. This is AMT contribu-tion 109.
References
Arin, L., Moran, X.A.G., Estrada, M., 2002. Phytoplankton size
distribution and growth rates in the Alboran Sea (SW
Mediterranean): short term variability related to mesoscale
hydrodynamics. Journal of Plankton Research 24 (10),
