Variable export fluxes and efficiencies for calcite, opal, and organic carbon in the Atlantic Ocean: A ballast effect in action?

Variable export fluxes and efficiencies for calcite, opal, and organic

carbon in the Atlantic Ocean: A ballast effect in action?

Sandy J. Thomalla,1 Alex J. Poulton,2 Richard Sanders,2 Robert Turnewitsch,3

Patrick M. Holligan,2 and Mike I. Lucas2,4

Received 27 March 2007; revised 17 July 2007; accepted 4 September 2007; published 8 February 2008.

[1] Latitudinal variability in export fluxes and efficiencies (ThE) of calcite, opal, andparticulate organic carbon (POC) were examined during a basin-scale Atlantic Oceancruise. A clear relationship between integrated euphotic zone POC and calcite exportcombined with similarities in average ThE for calcite (0.26), opal (0.31), and POC(0.29) implies a potential association between biomineral and POC export. However,such similarity conceals substantial uncorrelated variability when ThE values arecompared on regional scales, with ThE of POC often being much higher than that ofcalcite or opal. High-euphotic zone ThE for POC (0.3–0.4) relative to that found indeep sea sediment traps (<0.05) suggests that considerable remineralization occursbelow the euphotic zone. We suggest (1) that regional variability in the mechanisms bywhich biominerals and POC become associated are more important in determining theefficient export of organic carbon than that of ballast materials; and (2) that, because ofthe preferential remineralization of POC relative to calcite/opal dissolution duringsubeuphotic processes, the potential for effective ballasting increases with depth in thewater column.

Citation: Thomalla, S. J., A. J. Poulton, R. Sanders, R. Turnewitsch, P. M. Holligan, and M. I. Lucas (2008), Variable export fluxes

and efficiencies for calcite, opal, and organic carbon in the Atlantic Ocean: A ballast effect in action?, Global Biogeochem. Cycles, 22,

GB1010, doi:10.1029/2007GB002982.

1. Introduction

[2] The capacity of the biological carbon pump to transferatmospheric CO2 into the deep ocean is dependent upon theefficiency of particulate organic carbon export and thedegree of remineralization as particles sink [Sarmiento etal., 2004]. The fate of particulate matter produced within theeuphotic zone is governed by competition between disso-lution/remineralization and export, with a return to thesolution phase being enhanced by increasing residencetimes in the upper ocean. Strong correlations observed inthe deep ocean between the vertical fluxes of particulateorganic carbon (POC) and of inorganic material (calcite,opal, clay) have been used to suggest that mineral phasesmay enhance the export and survival of organic matter as itsinks into the deep ocean (the ‘‘ballast effect’’), by increas-ing the density and sinking speeds of particle aggregates[Klaas and Archer, 2002], and by providing some protec-

tion from remineralization [Armstrong et al., 2002]. How-ever, the underlying processes are not well understood andthe contrary has been suggested whereby organic aggregatesscavenge nonsinking mineral material, so that the flux ofPOC determines the flux of minerals to the deep sea and notthe reverse [Passow, 2004; Passow and De La Rocha, 2006].Rapid sinking of material will prevent significant dissolu-tion of opal and calcite and remineralization of organiccarbon [Ragueneau et al., 2000]. However, biomineraldissolution in the upper ocean may preclude the efficientexport of inorganic, and any associated organic material[Nelson et al., 1995; Milliman et al., 1999; Feely et al.,2002; Brzezinski et al., 2003].[3] Realistic modelling of the biological pump and the

oceanic pathways for atmospheric CO2 sequestration[Sarmiento et al., 2004] depends on developing animproved understanding of the mechanisms of particleformation and rates of remineralization/dissolution, andtheir variability with respect to depth and regional hy-drography [Buesseler et al., 2001; Cochran et al., 2000,Ragueneau et al., 2006]. Although there are relatively fewmeasurements of biomineral formation, the accepted par-adigm is that a substantial proportion (�50–80%) of thecalcite and opal produced in the euphotic zone dissolveswithin the upper (<1 km) ocean [Nelson et al., 1995;Milliman et al., 1999; Feely et al., 2002; Brzezinski et al.,2003]. Opal dissolution is mediated by low, undersaturatedconcentrations of silicate relative to particulate concentra-

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1Department of Oceanography, University of Cape Town, Cape Town,South Africa.

2National Oceanography Centre, Southampton, University ofSouthampton, Waterfront Campus, Hampshire, UK.

3Scottish Association for Marine Science, Dunstaffnage MarineLaboratory, Oban, UK.

4Also at Department of Zoology, University of Cape Town, Cape Town,South Africa.

Copyright 2008 by the American Geophysical Union.0886-6236/08/2007GB002982$12.00

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tions [Nelson et al., 1995; Brzezinski et al., 2003] andbacterial action [Passow, 2004; Bidle and Azam, 1999],while calcite dissolution may be mediated by localizedacidic conditions, such as within (micro-/macro-) zooplank-ton guts [Harris, 1994; Pond et al., 1995; Hansen et al.,1996; Jansen and Wolf-Gladrow, 2001; Langer et al., 2007]and in microenvironments during aggregate (faecal pellets,marine snow) formation [Milliman et al., 1999].[4] A comparison of measurements of primary production

and biomineralization in the (sub)tropical Atlantic withpublished sediment trap data [Poulton et al., 2006a] indi-cated that the proportion of organic carbon associated withmineralizing phytoplankton production is greater than thatexported to the deep sea, that calcite is the major biomineraland has a turnover time within the euphotic zone compara-

ble to that of the phytoplankton (�3 d), and that �70% ofthe calcite being formed is dissolved in the upper 2–3 km ofthe ocean. Clearly, the nature of the association betweenparticulate organic carbon and mineral material both withinand below the euphotic zone is fundamental to understand-ing how organic carbon export is controlled. Within theeuphotic zone, ballasting may result from physical associ-ations during biomineral and organic carbon formation(cellular), packaging (grazing) or aggregation [Passow,2004].[5] In this study, we compare the production and export

of biominerals and organic carbon from the euphotic zonein the (sub)tropical Atlantic Ocean in order to examine(1) whether the strong correlations observed between par-ticulate and biomineral fluxes in deep (>2 km) sedimenttrap data [e.g., Klaas and Archer, 2002] are evident atshallower water depths (i.e., within the euphotic zone); and(2) if the export efficiencies (ThE = export/surface produc-tion) of the different particle types are related. Exportefficiencies of POC, calcite, and opal are determined bycomparing surface production rates of organic carbon (i.e.,photosynthetic rates) and biomineral phases (calcification,silicification) [from Poulton et al., 2006a], to shallow(<100 m) particulate export fluxes of organic carbon,calcite and opal. High organic carbon export can resultfrom low-productivity systems with efficient export (littleremineralization) or from high-productivity systems withinefficient export (extensive remineralization) [see Francoiset al., 2002]. Thus in order to examine the relationshipsbetween biomineral and organic carbon export, it is neces-sary to consider both the magnitude of export and theamount of export relative to surface production asexpressed by the export efficiency (ThE).

2. Sampling and Methods

[6] Measurements of particulate production and exportwere made during a cruise of the Atlantic MeridionalTransect (AMT-14) programme between the FalklandIslands (50�S) and the UK (50�N) (see Figure 1) [Robinsonet al., 2006]. Samples of large particulate (>50 mm) materialwere collected from predawn (0000–0700 LT) deploymentsof Stand Alone Pumps (SAPS; 1 depth) filtering �1500 L,while water samples (�20 L) were collected from Niskinbottles attached to a CTD rosette sampler (10 depths).Simulated in situ phytoplankton organic carbon and bio-mineral production measurements were made on deck for 5‘‘light’’ depths (97, 55, 33, 14, and 1% incident irradiance)as determined from the in situ PAR sensor on the CTDframe. In this study, the euphotic zone was defined as thelayer between the surface and the depth of 1% incidentirradiance.[7] The methods for determining calcite, opal, and POC

concentration (precision <15%) and their rates of produc-tion can be found in the work of Poulton et al. [2006a]. Themean relative standard deviation (RSD) for calcite, opal,and POC production rates, calculated as the average of allthe relative standard deviations for production rates derivedfrom triplicate measurements, were 31%, 28% and 14%respectively [Poulton et al., 2006a]. The small volumes

Figure 1. Cruise track and positions of export samplingstations for the June 2004 Atlantic Meridional Transect(AMT-14). Cruise track is overlaid on a monthly sea surfacechlorophyll-a (mg m�3) composite (April–June 2004).Note station positions relative to surface chlorophyll-aconcentrations: (1) relatively high chlorophyll-a temperatewaters in both hemispheres (48.6�N, 41.6�S); (2) relativelyhigh chlorophyll-a waters of both the northern (38.4�N) andsouthern (32.6�S) subtropical convergences; (3) intermedi-ate chlorophyll-a concentrations for equatorial stations(0.1�S, 11.2�N); and (4) low chlorophyll-a concentrationsin the northern (22.3�N, 29.3�N) and southern (12.2�S,24.1�S) subtropical gyres. Image courtesy of ORBIMAGE.

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(<0.3 L) used for production measurements undersamplelarge and rare mineralizing plankton (foraminifera, ptero-pods, radiolarians), whereas SAPS (�1500 L) should bettersample such organisms. This difference in sampling vol-umes implies that estimates of export efficiency for calciteand opal may be based on underestimates of total calcifi-cation and silicification. However, large calcifiers andsilicifiers are relatively rare in (sub)tropical waters. Forexample, in the upper ocean coccolithophores and diatomsare present at cell densities of 104–107 cells m�3, whereasforams, pteropods, and radiolarians are present at celldensities of 102–104 cells m�3 [Baumann et al., 2004].Thus any overestimation of mineral export efficiencies islikely to be small. In interpreting the data set we presenthere, it is important to note that the biomineralizing com-ponent of the planktonic community was dominated bycalcite rather than opal producing organisms [Poulton et al.,2006a].[8] Export of POC, calcite, and opal were calculated from

water column 234Th/238U disequilibria [e.g., Buesseler,1998; Thomalla et al., 2006]. Estimates of the total meth-odological error in export fluxes were based on propagatedmethodological uncertainties (full details in the work ofThomalla et al. [2006]) for the 234Th deficit calculations andan average relative standard deviation for particulate meas-urements of 15%. Single activity profiles as obtained duringthis study lack information on spatial-temporal variabilityand necessitate the assumption of steady state. The datatherefore do not allow estimation of horizontal and verticaladvective contributions to thorium sinking fluxes, but theyare assumed insignificant compared to scavenging rates andexport on sinking particles. This assumption provides ade-quate resolution of 234Th fluxes in many steady statesettings [e.g., Tanaka et al., 1983; Wei and Murray, 1991;Moran and Buesseler, 1993; Buesseler et al., 2001]. Non-steady-state effects are however important during periods ofsignificant 234Th drawdown, such as during phytoplanktonblooms and postbloom conditions [Buesseler et al., 1992,1998, 2001; Cochran et al., 1997], as well as in regions of

high upwelling velocity [Buesseler et al., 1995; Bacon etal., 1996; Dunne and Murray, 1999]. As we have ignoredthe upwelling term, it is likely that our 234Th and subse-quent POC, calcite, and opal flux estimates in equatorialupwelling waters may represent lower limits. At two sta-tions where Poulton et al. [2006a] report biomineral pro-duction data the depletion of 234Th in the upper ocean wasnot statistically significant, therefore estimates of exportfrom these stations are given in Table 1 as zero.[9] Ratios of particulate 234Th to POC (range 6–15, mean

8.6 ± 2.9), to calcite (0.07–0.82, 0.42 ± 0.25) and to opal(0.01–0.25, 0.10 ± 0.07) were used to calculate the exportof the various phases from the 234Th deficit measurements.These ratios were determined from samples obtained from50 mm filters fitted on SAPS deployed at, or close to, the baseof the euphotic layer [see Thomalla et al., 2006, Table 3].To calculate export efficiencies (the numerical ratio ofexport/production; ThE after Buesseler et al. [1998]) forthe different particle types, we have used the depth ofthe euphotic zone as the depth of integration for the steadystate 234Th disequilibria model.

3. Results and Discussion

3.1. Export Fluxes and Efficiencies for OrganicCarbon, Calcite, and Opal

[10] The magnitude of (molar) export fluxes for thedifferent particulate materials (Figure 2) were higher fororganic carbon (range 2.53–11.76 mmol C m�2 d�1) thanfor either calcite (0.03–0.61 mmol C m�2 d�1) or opal(0.01–0.24 mmol Si m�2 d�1) (Table 1). Calcite exportfluxes were generally an order of magnitude higher thanopal fluxes (Table 1). The station at 38.4�N with the highestorganic carbon flux (11.76 mmol C m�2 d�1) was also thestation with the highest biomineral fluxes (0.61 mmol Cm�2 d�1 for calcite and 0.24 mmol Si m�2 d�1) (Table 1).[11] The export efficiencies (ThE) of all three particulate

phases were highly variable (Figure 2) and ranged from 0.1to 0.7 for POC, from 0.05 to 1.51 for opal and from 0.02 to

Table 1. Compilation of Station Positions, Euphotic Zone Depths (Zeup), Estimates of Particulate Organic Carbon (POC), Calcite and

Opal Export Fluxes, and Export Efficienciesa

Latitude Zeup, m

Export, mmol m�2 d�1 Export efficiencies, ThE

POC Calcite Opal POC Calcite Opal

41.6�S 65 5.36 ± 1.86 0.39 ± 0.13 0.02 ± 0.01 0.14 0.09 0.0432.6�S 103 3.69 ± 2.87 0.11 ± 0.08 0.04 ± 0.03 0.28 0.04 0.1324.1�S 122 2.53 ± 3.26 0.10 ± 0.13 0.02 ± 0.02 0.20 ND 0.1212.2�S 130 3.29 ± 3.25 0.05 ± 0.05 0.01 ± 0.01 0.22 0.02 0.050.1�S 59 6.33 ± 3.58 0.34 ± 0.19 0.01 ± 0.01 0.26 0.14 0.0111.2�N 81 6.26 ± 6.81 0.41 ± 0.45 0.08 ± 0.09 0.21 0.79 0.1422.3�N 115 0.00 0.00 0.00 ND ND ND29.3�N 132 0.00 0.00 0.00 ND ND ND38.4�N 50 11.76 ± 5.15 0.61 ± 0.27 0.24 ± 0.11 0.71 0.70 1.5148.6�N 28 2.84 ± 2.33 0.03 ± 0.03 0.08 ± 0.06 0.11 0.03 0.48Mean 5.26 0.26 0.06 0.27 [0.25]b 0.26 [0.12]b 0.31 [0.19]b

(S.D.) (3.03) (0.21) (0.08) (0.19) (0.34) (0.51)

aCalculated errors for export fluxes are based on accounting for methodological uncertainties [Thomalla et al., 2006; see section 2]. ND indicates notdetermined. Square brackets contain values calculated from mean values of production and export. Parentheses indicate standard deviations.

bMeans calculated from average values of production [Poulton et al., 2006a] and export.

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0.79 for calcite (Table 1). The mean values of ThE for thethree phases (Table 1) were however similar (0.26 forcalcite, 0.31 for opal, and 0.29 for organic carbon), suggest-ing that similar processes determine the efficiencies ofmineral and organic carbon export. However, when ThEvalues for the three phases are compared on a station bystation basis (Figures 3c and 3d) they appear unrelated (overthe euphotic zone) in a way that is not predictable fromsurface rates of primary or biomineral productivity (Figure 2and Table 1) and it becomes clear that such averages maskconsiderable variability (spatial and/or temporal) in theprocesses that determine ThE.[12] As is found in deep sediment trap data [e.g., Klaas

and Archer, 2002], there do appear to be linear relationshipsbetween organic carbon, calcite (Figure 3a) and opal fluxes(Figure 3b). Regression analysis on the statistical relation-ships between standing stocks, production rates, exportfluxes and ThE for all three phases (Table 2) were carriedout to examine whether processes leading to the efficient

export of the various phases were correlated and couldpotentially have similar causal mechanisms. No significantrelationships were found between the production rate of anyof the phases and the export or ThE of any of the phases(Table 2). Clearly, high production rates do not automati-cally lead to high rates of export. For the full data set, POCThE was found to be significantly correlated with POCexport flux, opal export flux, and opal ThE (Table 2). Hencethe processes leading to POC and opal export could besimilar, whereas the absence of significant correlationsbetween POC ThE and calcite fluxes and calcite ThE mayindicate the lack of similar mechanisms. However, if thehigh export station (38.4�N) is ignored in the analysis, theserelationships break down (Table 2) and thus the linkbetween POC and opal export appears to be driven by highexport fluxes.[13] There are no relationships between POC standing

stocks and biomineral ThE (Table 2), as would be expectedif POC scavenging were an important process in the(sub)tropical Atlantic Ocean (Table 2). Furthermore, POCfluxes and standing stocks are relatively large compared tobiomineral fluxes and standing stocks [Poulton et al.,2006a, Table 1], suggesting that biomineral protection fororganic matter [Armstrong et al., 2002] is likely to be ofsecondary importance in regulating organic carbon exportin the upper ocean of the (sub)tropical Atlantic Ocean.Finally, there is no relationship between PIC or opalstanding stocks and organic carbon flux or ThE, implyingthat a directly mediated ballast effect (i.e., only organiccarbon directly associated with coccolithophore and diatomcells is exported) is unlikely to be occurring within our dataset.[14] The general pattern displayed at nearly all stations

is for ThE of all three phases to be relatively low and forThE of organic carbon to be higher than ThE for eitherbiomineral (Figures 3c, 3d, and Table 1). However, at38.4�N (G in Figures 3c and 3d; also see Table 1) ThE ofall three phases were large and the biomineral exportefficiencies were larger than or comparable to that oforganic carbon. A comparison of biomineral to organiccarbon ratios for material synthesised in the euphotic zonerelative to the exported material provides a proxy for therelative changes in the characteristics of exported particles(Figure 4) [see Brown et al., 2006]. At most stations, theseratios show that if the ecosystem is operating at steadystate, there is relatively more dissolution of biominerals inthe euphotic zone than remineralization of organic carbon,although there is considerable variability between stations(Figure 4).[15] Although the reasons for generally higher ThE for

POC than biominerals are unclear, it is an extremelyimportant point to note since below the euphotic zone thetwo biomineral phases are better preserved than organiccarbon [Poulton et al., 2006a]. Hence there must be a depthhorizon within the twilight zone (below the euphotic zone)at which the relative labilities of the biomineral and organiccarbon phases become reversed. It is also noticeable that atthe one station where ThE were high (38.4�N), those forbiominerals were comparable to or higher than those fororganic carbon. Thus the mean conditions whereby organic

Figure 2. Euphotic zone integrated (molar) rates ofproduction (bottom white bars) and export (top gray bars)for (a) calcite (mmol C m�2 d�1), (b) opal (mmol Si m�2

d�1), and (c) organic carbon (mmol C m�2 d�1). Ratio ofexport to production (export efficiency) for each particletype is provided. ND indicates not determined. Note thatexport fluxes from stations in the northern subtropical gyre(22.3�N, 29.3�N) were below the detection limits of the234Th technique.

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matter is exported more efficiently from the euphotic zone iscompensated for by phytoplankton bloom conditions withrelatively more efficient export of biominerals. It may be the

latter process that accounts for better preservation of bio-minerals than organic carbon over the full depth of the watercolumn.

Figure 3. Comparison of export fluxes (mmol m�2 d�1) and export efficiencies (export/production) forcalcite, opal, and particulate organic carbon: (a) calcite and particulate organic carbon fluxes, (b) opal andparticulate organic carbon fluxes, (c) calcite and particulate organic carbon export efficiencies (ThE), and(d) opal and particulate organic carbon export efficiencies (ThE). Dashed lines (c, d) represent a 1:1 line.

Table 2. Regression Analysis for the Relationships Between Standing Stocks, Production Rates, Export Fluxes, and Export Efficiencies

(ThE) for the Different Particle Types: Particulate Organic Carbon (POC), Calcite (PIC), and Opal (BSi)a

Standing Stocks Production Rates Export Fluxes Export Efficiencies

POC PIC BSi POC PIC BSi POC PIC BSi POC PIC BSi

Standing stocks POC - - - - - - - - - - - -PIC NS - - - - - - - - - - -BSi NS NS NS - - - - - - - - -

Production rates POC NS NS NS - - - - - - - - -PIC 0.85b

(0.83a)NS NS NS - - - - - - - -

BSi NS NS NS NS NS - - - - - - -Export fluxes POC NS NS NS NS NS NS - - - - - -

PIC NS NS NS NS NS NS 0.94c(0.90b)

- - - - -

BSi NS NS NS NS NS NS 0.82a(NS)

NS - - -

Export efficiencies POC NS NS NS NS NS NS 0.87b(NS)

NS 0.85b(NS)

- - -

PIC NS NS �0.76a(0.96b)

NS NS NS NS 0.77b(NS)

NS NS - -

BSi NS NS NS NS NS NS 0.77a(NS)

NS 0.97c(NS)

0.87b(NS)

NS -

aSignificant correlation coefficients are shown along with the level of significance as (a) p < 0.05, (b) p < 0.01, and (c) p < 0.001. NS indicatesnonsignificant. Values in parentheses refer to correlation coefficients for relationships where the high export station (38.4�N) has been omitted. Values oforganic carbon and biomineral standing stocks are taken from Poulton et al. [2006a].

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[16] Comparison of both the magnitude of export fluxesand the export relative to surface production (ThE) fororganic carbon, calcite, and opal in the (sub)tropicalAtlantic Ocean show that (1) although linear relationshipsappear to characterise the relationship between absolutefluxes of organic carbon, calcite and opal, there issignificant regional variability and high biomineral fluxesare not always related to high organic carbon fluxesparticularly with respect to opal (Figure 3b and Table 2);and (2) although average ThE were similar for the threeparticulate types, there is considerable station to stationdifferences suggesting that the efficient export of biomin-erals does not necessarily enhance ThE of organic carbon(Table 2). Such regional disparity in export fluxes and ThEare likely to be related to regional patterns in hydrographyand planktonic ecosystem structure in the (sub)tropicalAtlantic Ocean and are examined in the context of thesefactors in section 3.2.

3.2. Regional Variability in Export Flux and ExportEfficiency

[17] A variety of hydrographic provinces and ecosystemsare sampled along the AMT transect, including the perma-nently stratified oligotrophic subtropical gyres, tropicalequatorial upwelling waters, seasonally variable subtropicalconvergences and the seasonally mixed temperate waters ateither end of the transect [Robinson et al., 2006]. Surfaceand upper ocean (<50 m) chlorophyll-a concentrations arelow (<0.10 mg m�3) within both subtropical gyres of theAtlantic Ocean, with elevated chlorophyll-a concentrations(>0.3 mg m�3) associated with the equatorial upwelling(10�S–15�N), and seasonally in the subtropical convergen-ces and temperate waters of both hemispheres [Robinson etal., 2006, Figure 1].[18] Generally, small picophytoplankton (<2 mm) domi-

nate both biomass and organic carbon production through-out the AMT transect [Zubkov et al., 1998; Maranon et al.,2000; Poulton et al., 2006b], although there are slightincreases in the biomass and productivity of larger phyto-

plankton cells in equatorial upwelling waters [Perez et al.,2005] and in temperate waters during (northern) spring[Tarran et al., 2006]. The grazer community is morevariable over the AMT transect, with nanoflagellate (2–20 mm) and microzooplankton (20–200 mm) grazersdominant in the subtropical gyres, while mesozooplankton(>200 mm) biomass and grazing pressure are relativelymore important in equatorial and temperate waters [Huskinet al., 2001; Isla et al., 2004].[19] Low rates of calcification and especially silicifica-

tion characterised the central subtropical gyres (Figure 2)[Poulton et al., 2006a], highlighting the low biomass ofcoccolithophores and diatoms in the subtropical and trop-ical ocean [Nelson et al., 1995; Haider and Thierstein,2001]. In the southern subtropical gyre (12.2�S, 24.1�S,32.6�S), low ThE for calcite (0.02–0.04), opal (0.05–0.13)and organic carbon (0.20–0.28) also suggest that a largeproportion of surface production was retained in the upperocean. A comparison of biomineral to organic carbonratios for surface production and in exported material forstations in the southern subtropical gyre (Figure 4) bothindicate preferential dissolution of mineral material (opal,calcite) relative to organic carbon.[20] Efficient nanoflagellate and microzooplankton graz-

ing, as well as bacterial activity, are likely to enhance silicadissolution in subtropical surface waters by exposing indi-vidual diatom frustules to warm, undersaturated surfacewater silica concentrations [Nelson et al., 1995; Passow etal., 2003; Ragueneau et al., 2006] and by facilitatingintracellular or aggregate associated calcite dissolution[Hansen et al., 1996; Milliman et al., 1999]. Dominanceof the community by small cells, with slow sinking rates,may also promote the dissolution of calcite and opal byincreasing their residence times in surface waters. Thebiological pump in the subtropical gyres, characterised byan active microbial loop, is likely to lead to efficientrecycling of biomineral and organic carbon production[Brzezinski et al., 2003].[21] By contrast, in equatorial waters of the Atlantic

Ocean (0.1�S, 11.2�N), elevated nutrient concentrations

Figure 4. Relative changes in the molar ratios of particulate material composition between surfaceproduction and export: (a) calcite to particulate organic carbon (calcite: organic carbon) and (b) opal toparticulate organic carbon (opal: organic carbon). Values above the 1:1 (dashed lines) line indicaterelatively high mineral dissolution from relatively high organic carbon remineralization.

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due to localized upwelling [Longhurst, 1993; Perez et al.,2005] cause increases in chlorophyll-a concentrations(Figure 1) [Robinson et al., 2006] and increased rates oforganic production relative to the subtropical gyres (Figure2c) [Maranon et al., 2000; Poulton et al., 2006b]. Becauseof the strong grazing pressure by meso- and microzooplank-ton, there is little change in the size structure of thephytoplankton community [Perez et al., 2005]. Neverthe-less, increases in the integrated rates of calcification andsilicification (Figures 2b and 2c) [Poulton et al., 2006a]indicate that larger phytoplankton cells are present andefficiently grazed (therefore exported) by the high meso-zooplankton biomass found in equatorial waters [Huskin etal., 2001; Isla et al., 2004]. Export efficiencies were highfor calcite (0.14–0.79) and organic carbon (0.21–0.26) butlow for opal (0.01–0.14) in equatorial waters (Figure 2 andTable 1). A comparison of biomineral to organic carbonratios of surface production and export implies preferentialorganic carbon remineralization relative to calcite dissolu-tion and preferential opal dissolution relative to carbonremineralization (Figure 4).[22] Significant dissolution of opal in equatorial waters

(Figure 3b) is likely to be mediated by enhanced mesozoo-plankton grazing [Huskin et al., 2001; Isla et al., 2004],which exposes individual diatom frustules to relatively lowambient silicate concentrations [Nelson et al., 1995], andalso increases the number of broken diatom frustules[Roman and Rublee, 1980] and their subsequent coloniza-tion by bacteria [Ragueneau et al., 2006]. High-calcite ThE(0.79) in the northern equatorial station (11.5�N) wasassociated with relatively low ThE for organic carbon(0.21), which implies that there was no enhancement oforganic carbon ThE associated with relatively high calciteThE. Rather, in equatorial waters there was preferentialexport of calcite relative to organic carbon. Several mech-anisms could be responsible for this; for example, feedingby equatorial mesozooplankton on coccolithophores, asopposed to the dominant picophytoplankton community,would produce calcite rich faecal pellets and promote calciteexport. Another mechanism may be spatial-temporal uncou-pling in production and export caused by mesoscale eddies,which are characteristic of low-latitude current systems[Longhurst, 1993; Perez et al., 2005]. Our observations ofhigh-calcite ThE in the equatorial Atlantic also explainobservations of high equatorial calcification rates coupledwith low standing stocks of calcite [Poulton et al., 2006a].[23] The subtropical convergences of the Atlantic Ocean

(41.6�S, 38.4�N) are sites of seasonally enhanced biomass(Figure 1), production (Figure 2), and seasonal differencesin the structure of the plankton community [Maranon et al.,2000; Poulton et al., 2006b; Robinson et al., 2006]. DuringAMT-14 (May 2004), early autumn conditions of enhancedmixing, low irradiance and moderate nutrient concentrationscharacterised the southern subtropical convergence whilethe northern subtropical convergence was experiencing latespring conditions of reduced mixing, high irradiance butdecreasing nutrient concentrations [Maranon et al., 2000;Poulton et al., 2006a, 2006b; Robinson et al., 2006].[24] In the southern subtropical convergence (32.6�S),

rates of calcite, opal, and organic carbon production were

all high, whereas the corresponding ThE values were allvery low (0.09, 0.04, and 0.14, respectively; Figure 2 andTable 1). However, in the northern subtropical convergence(38.4�N) the opposite trends were found with low calcite,opal, and organic carbon production, whereas the ThEvalues were among the highest values found in this study(0.70, 1.51, and 0.71, respectively; Figure 2 and Table 1). Acomparison of biomineral to organic carbon ratios forsurface production and export also showed different patternsin the two subtropical convergences (Figure 4). In thesouthern subtropical convergence (32.6�S) there was pref-erential dissolution of both calcite and opal relative toorganic carbon remineralization, whereas in the northernsubtropical convergence (38.4�N) there was preferentialorganic carbon remineralization relative to opal dissolu-tion, and to a lesser extent, calcite dissolution (Figure 4).As such differences are based on rather few data points,we cannot yet extrapolate to characterise seasonal orregional patterns in the relationships between POC andbiominerals.[25] Nevertheless, differences in ThE and relative bio-

mineral dissolution/organic carbon remineralization patternsbetween the two subtropical convergences may be causedby seasonal differences in the temporal coupling of produc-tion and export. In the northern subtropical convergence,material being exported may represent the remnants of thespring bloom community settling out of the water column aslow-nutrient conditions develop. Thorium-based measure-ments of export integrate over relatively long timescales(�31 d; Buesseler [1998]) compared to relatively instanta-neous measurements of primary production (<1 d). ElevatedThE may therefore result from significant temporal decou-pling between export and primary production. Indeed,averaged SeaWiFS chlorophyll-a estimates obtained forthe 34�N station clearly reveal elevated chlorophyll-a con-centrations in the region �2 weeks prior to our in situsampling and suggest that high-234Th flux rates measuredhere could represent export from a previous episode ofelevated productivity [Thomalla et al., 2006].[26] In contrast, consistently low ThE in the southern

subtropical convergence suggest that the autumnal bloommay not have progressed to the export phase because ofcontinuing high-nutrient conditions at the time of sampling[see Poulton et al., 2006a, Figure 2]. Spatial decoupling ofproduction and export may also be important in the patternsobserved in the northern subtropical convergence, as bothconvergences are strongly influenced by mesoscale physicalinstabilities [Garcon et al., 2001; Mourino et al., 2003],with stations close to 38.4�S (35.5�N, 41.6�N) having highdiatom and coccolithophore cell densities (A. Poulton,unpublished results, 2004, and T. Adey, personal commu-nication, 2005) and high rates of calcification and silicifi-cation [Poulton et al., 2006a].[27] It is likely that seasonal export from the northern

subtropical convergence is due to large aggregates whichsink much faster (�100 m d�1) than the timescale forsignificant biotic dissolution of calcite [Jansen et al.,2002], or opal [Hill, 1992; Alldredge and Jackson, 1995],although there is evidence of preferential organic carbonremineralization relative to opal dissolution (Figure 4b).

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Under these conditions, it is possible for sinking material toscavenge other particulate material present in the watercolumn (i.e., calcite, opal, and other phytoplankton cells)[Passow and De La Rocha, 2006] to further enhance ThEfor all components.[28] High opal ThE (0.48) relative to calcite (0.03) and

organic carbon (0.11) ThE values was observed for thenorthern temperate waters (48.6�N) indicating that the largeamount of material exported at this time contained relativelylittle calcite or organic carbon, although some export ofeach was measured (Table 1). Comparison of the ratio ofopal to organic carbon in material produced in the surfacewaters relative to that exported (Figure 4b) showed rela-tively more organic carbon remineralization than opaldissolution. These differences may result from either (1) aphytoplankton community that is dominated by opal exportoriginating from heavily silicified nutrient-stressed diatoms[Hutchins and Bruland, 1998; Timmermans et al., 2004], (2)the significant remineralization of organic carbon as mate-rial is repackaged and/or sinks, and/or (3) the export ofpredominantly aggregated diatoms which would reduceopal dissolution [Moriceau et al., 2007], while organiccarbon continues to be utilised by bacteria within theaggregates [Smith et al., 1992].

4. Conclusions

[29] The positive correlation observed between euphoticzone calcite and organic carbon export fluxes (Figure 3a andTable 2) and the similarities in average ThE for the differentparticle types (Table 1) suggests a mechanistic relationshipbetween efficient organic carbon and biomineral export inthe (sub)tropical Atlantic Ocean. However, when the dataare viewed on a regional basis, these relationships breakdown (Figure 3; see also Figure 2 and Tables 1 and 2).Similarly, a comparison of the biomineral to organic carbonratio of surface production and exported material generallysuggests preferential calcite or opal dissolution relative toorganic carbon remineralization (Figure 4). We suggest thatregional patterns of export and ThE for calcite, opal, andorganic carbon (Figure 2) and relative differences in calcite/opal dissolution versus organic carbon remineralization(Figure 4) result from variability in the mechanisms con-trolling export in the (sub)tropical Atlantic Ocean. Thesemay include latitudinal and seasonal differences in plank-tonic ecosystem structure, physical forcing and the degreeof spatial-temporal coupling of surface production andexport.[30] As calcite dominates ballasting material in the (sub)

tropical Atlantic ocean [Francois et al., 2002; Poulton et al.,2006a], a good relationship exists between calcite andorganic carbon fluxes (Figure 3a and Table 2) rather thanbetween opal and organic carbon fluxes (Figure 3b andTable 2). However, the lack of a distinct relationship betweenThE for calcite, opal, and organic carbon (Figures 3c, 3d, andTable 2) implies that efficient organic carbon export from theproductive euphotic zone may not always be enhanced byThE of biominerals. Instead, efficient particulate export fromthe euphotic zone may be more dependent on the character-istics of the planktonic community composition (e.g., size

spectra, taxa) and ecology (e.g., physiology, grazing pres-sure). Nevertheless, at one station in the northern subtropicalconvergence (38.4�N), the highest organic carbon fluxeswere associated with high biomineral export and ThE wasassociated with high biomineral ThE (Tables 1 and 2).Therefore important exceptions to the pattern of decouplingbetween organic carbon and biomineral fluxes exist and maysignificantly influence annual export.[31] At some stations (41.6�S, 32.6�S, 24.1�S, 12.2�S,

0.1�S), ThE for organic carbon (0.14–0.28) exceeded thatfor calcite (0.02–0.14) and opal (0.01–0.13) (Table 1);which is the reverse of ThE patterns observed in deepsediment traps, where only �1–2% of surface organiccarbon production reaches the deep sea [Sarmiento et al.,2004] relative to �30–50% for biominerals [see Poulton etal., 2006a, Table 3]. These patterns imply significantremineralization of organic carbon relative to biomineralsbelow the euphotic zone as particles sink and/or scavengebiomineral material as they settle [Passow and De LaRocha, 2006], such that opal and calcite are ‘‘chemically’’decoupled from organic carbon during sinking leading to anincrease in the biomineral to organic carbon ratio withdepth. The potential for effective ballasting of the remainingorganic carbon therefore increases with depth, which mayaccount for the observation of a ‘‘ballast effect’’ in sedimenttrap material [Klaas and Archer, 2002].[32] Overall, biomineral production at the stations sam-

pled in the (sub)tropical Atlantic Ocean was dominated bycalcite producing organisms rather than those producingopaline frustules [Poulton et al., 2006a]. Thus the resultspresented here cannot be considered representative of thosefrom highly productive systems such as the North Atlanticspring diatom bloom or coastal upwelling systems. Clearly,making parallel measurements of biomineral and organiccarbon production in such regions is a high priority for theglobal community.

[33] Acknowledgments. We thank the officers and crew of theRRS James Clark Ross and the technical support of the UKORS staff.We are grateful for assistance from M. Stinchcombe, T. Adey, L. Brown,P. Warwick, K. Chamberlain, M. Woodward, W. Balch, R. Head, D. Green,and R. Pearce. Support for this study came from the UK NERC through asmall grant awarded to R. Sanders, the Atlantic Meridional Transectconsortium (NER/O/S/2001/00680), and the George Deacon Division.S. Thomalla gratefully acknowledges support from a commonwealth split-site Ph.D. scholarship. This is contribution 153 of the AMT programme.

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�������������������������P. M. Holligan and R. Sanders, National Oceanography Centre,

Southampton, University of Southampton, Waterfront Campus, Hampshire,SO14 3ZH, UK.

M. I. Lucas, Department of Zoology, University of Cape Town, PrivateBag, Rondebosch, 7701, Cape Town, South Africa.A. J. Poulton, 135 St. Bedes Crescent, Cambridge, CB1 3UA, UK.S. J. Thomalla, Department of Oceanography, University of Cape Town,

Private Bag, Rondebosch, 7701, Cape Town, South Africa. ([email protected])R. Turnewitsch, Scottish Association for Marine Science, Dunstaffnage

Marine Laboratory, Oban, PA37 1QA, UK.

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