Relative mineralisation of C and Si from biogenic particulate matter in the upper water column during the North East Atlantic diatom bloom in spring 2001

Journal of Marine Systems 63 (2006) 79 – 90 www.elsevier.com/locate/jmarsys

Relative mineralisation of C and Si from biogenic particulate matter in the upper water column during the North East Atlantic diatom bloom in spring 2001 Louise Brown a,⁎, Richard Sanders a , Graham Savidge b a

National Oceanography Centre Southampton, Empress Dock, European Way, Southampton, Hampshire, SO14 3ZH, UK b 3 Queen's University Marine Laboratory, 12-13 The Strand, Portaferry, Co. Down BT22 1PF Northern Ireland, UK Received 15 May 2005; accepted 6 March 2006 Available online 26 July 2006

Abstract The standing stocks and production rates of particulate organic carbon (POC) and biogenic silica (bSiO2) were measured in the upper water column at 10 stations in the North East Atlantic during the spring 2001 diatom bloom. The elemental composition of the particulate pool was rather homogeneous with depth, suggesting that any material being exported from the photic zone was generally similar in composition to the ambient pool. Pronounced vertical structure was observed in uptake ratios resulting from the strong light dependence of the carbon fixation and the weak light dependence of biogenic silica production. The integrated C/Si molar ratios of particulate material were found to be generally larger than the corresponding assimilation ratios. We interpret this discrepancy as implying a preferential mineralization of Si relative to C from particulate matter during the earliest stages of processing in the upper water column. The preferential mineralisation of Si relative to C in the early stages of particle processing contrasts with processes occurring deeper in the water column, where C is typically mineralised preferentially to Si, and particulate matter becomes enriched in bSiO2. In the northern North Atlantic, the balance of mineralisation of Si relative to C from sinking organic matter with depth is likely to strongly influence the role of diatoms in export production. © 2006 Elsevier B.V. All rights reserved. Keywords: Diatom blooms; Biogenic silica; Particulate organic carbon; Euphotic zone; Mineralization; North Atlantic

1. Introduction The flux of carbon across the thermocline from the surface layer of the ocean into the deep waters (the biological carbon pump) is central to the oceanic carbon budget (Eppley and Peterson, 1979). A key component of this flux is the export of organic particulate material ⁎ Corresponding author. Present address: School of Geography and Geosciences, University of St. Andrews, Irvine Building, North Street, St. Andrews KY16 9AL, UK. Tel.: +44 1355 463992. E-mail address: [email protected] (L. Brown). 0924-7963/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2006.03.001

generated by primary producers in the surface ocean to the ocean's interior (Martin et al., 1987). The loss of particulate carbon from the surface waters must ultimately be balanced by the invasion of atmospheric CO2, and thus, the export flux has a potential role in climate regulation. The upper limit on carbon export is set by the rate of new phytoplankton production; that is, the fraction of primary production supported by ‘new’ inorganic nitrogen (nitrate) uptake relative to the uptake of total nitrogen, which includes recycled, organic forms (Dugdale and Goering, 1967). The principal source of ‘new’

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dissolved nitrate in the surface layer is the upward flux, either via overturning or diffusive mixing, of deep, nutrient-rich waters. One important source of nutrients in the deep water is the mineralization of sinking particulate organic matter. This mineralization of organic matter, either in deep or shallow water, also results in the production of dissolved inorganic carbon (DIC), such that an upward flux of this component to the surface layer of the ocean occurs in parallel with the nutrient flux. A net export of carbon from the surface waters can only occur over multi-year timescales if the elemental ratio of DIC to nutrients associated with the upward flux of water is lower than the elemental ratio of the particulate material associated with the corresponding downward flux of carbon (Christian et al., 1997). This is because the mixing up of nutrients will thus be associated with a stoichiometrically inadequate quantity of DIC, and hence, a net air– sea flux of CO2 must occur for some nutrients used in new production. If the opposite is true, and DIC is released from sinking organic matter faster than nutrients, then a reduced net export can occur. This is because outgassing of DIC will result if upwelled waters have a stoichiometric excess of DIC relative to the amount needed to balance the upwelled nutrients. Preferential mineralisation of particulate organic nitrogen (PON) and particulate organic phosphorus (POP) relative to particulate organic carbon (POC) is observed almost ubiquitously throughout the ocean (Copin-Montegut and Copin-Montegut, 1983; Priddle et al., 1995; Shaffer, 1996; Loh and Bauer, 2000). It likely reflects the complex suite of physico-chemical and bacterially mediated reactions involved in the remineralisation of organic material in the oceans (Hurd, 1973; Tezuka, 1990; Anderson, 1992; Sterner, 1992; Bidle and Azam, 1999). It results in increases in the C/N and C/P ratios of sinking particles with depth (Martin et al., 1987; Knauer et al., 1979), a vertical decoupling of the concentrations of inorganic nutrients and DIC and an increase in the pool of dissolved nutrients in subsurface waters relative to DIC (Christian et al., 1997). Within the Pacific subtropical gyre, it has been estimated that this decoupling of the nutrient and carbon cycles supports 17–27% of total air–sea CO2 drawdown into the surface layer of the ocean (Christian et al., 1997). Preferential mineralisation of POP relative to POC has also been documented in areas where phytoplankton blooms result in rapid export of large quantities of particulate matter to the deep ocean (Paytan et al., 2003). Unlike nitrogen and phosphorus, which are fundamental to the metabolism of all primary producers, a third macronutrient, silicic acid, is utilised primarily by

a particular class of phytoplankton, the diatoms. Diatoms are considered to be important primary producers and exporters of carbon (Treguer et al., 1995; Nelson et al., 1995), and the availability of silicic acid acts as a major control on diatom production (Brzezinski and Nelson, 1996; Boyd et al., 1999; Franck et al., 2000; Leynaert et al., 2001). In further contrast, sediment trap data shows better preservation of bSiO2 relative to POC in deep waters of the Southern Ocean (Nelson et al., 2002) and oligotrophic low-latitude Atlantic and Pacific Oceans (Martin et al., 1991; Ragueneau et al., 2002). However, on shorter timescales, the rate of bSiO2 mineralisation in the upper ocean varies both seasonally and spatially, with rapid remineralisation in upwelling areas (Nelson and Goering, 1977) and subtropical gyres (Brzezinski and Nelson, 1995; Nelson and Brzezinski, 1997), and during periods of high productivity in temperate and highlatitude waters (Nelson et al., 1991; Brzezinski et al., 2001, 2003). The North East Atlantic is of potential importance in global biogeochemical cycling, due to the predicted high export production (> 100g C m−3 year−1; Falkowski et al., 1998) of the region. Export production occurs mainly as a result of the spring bloom (Ducklow and Harris, 1993), fuelled by nutrients replenished by winter overturning and initiated by thermal stratification of the water column. In the North Atlantic, diatoms play a major role in export production (Dugdale et al., 1995), with non-siliceous phytoplankton including flagellates, coccolithophores and mixotrophic ciliates (Savidge et al., 1995) dominating a recycled production regime once silicic acid depleted. The zooplankton community in the open northeastern North Atlantic is dominated by the copepod Calanus finmarchics (> 90% zooplankton biomass) (Gislason and Astthorson, 1995). Population maxima occur in two peaks; typically following the spring bloom, in (May–June) and another in late summer (July–September). Like phytoplankton, the highest abundances are in the coastal and shelf waters, decreasing in the open waters. In the present study, we examine the stoichiometry of C and Si assimilation and early mineralisation within the photic zone in the North East Atlantic during the highly productive spring bloom. This approach enables us to examine rates and controls of fluxes of biogenic materials between different pools (e.g., Reiners, 1986; Hassett et al., 1997). Here, we compare the C/Si ratios of newly formed biogenic particles (i.e., the elemental ratios of assimilation corrected for algal respiration and short-term losses of silicon) with the ratios in the particulate pool (which we hypothesise represents the

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material produced as above modified by grazing, bacterial processing and solubilisation) as a means of assessing the relative mineralization of C and Si in the photic zone during the earliest stages of particle diagenesis. We then interpret our results in terms of their implications for the role of diatoms in export production in the northern North East Atlantic during the spring bloom. 2. Methods 2.1. Sampling The assimilation rates of inorganic C and Si into particulate matter and the concentrations of POC and bSiO2 in the photic zone were determined at 10 stations in the North East Atlantic during RRS Discovery cruise D253 (Faeroes–Iceland–Scotland Hydrographic and

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Environmental Survey) in May 2001 (Fig. 1). At each station, seawater samples for assimilation rate and particulate concentration measurements were collected at seven depths (97%, 45%, 17.6%, 8.0%, 2.9%, 1.3% and 0.1% of the surface photosynthetically active radiation [PAR]). Samples were collected on a pre-dawn CTD cast using 20L Go-Flo bottles mounted on a rosette sampler and decanted into acid-cleaned 4-L polycarbonate bottles. Subsamples for carbon and nutrient assimilation studies were prepared for incubation immediately after collection under minimal light conditions; those for particulate composition analysis were kept refrigerated (4 °C) in the dark until filtration. Detailed analyses of C and Si assimilation rates and the fluorescence characteristics of the plankton community structure are presented elsewhere (Brown et al., 2003; Moore et al., 2005).

Fig. 1. Map of the FISHES study area and cruise track. The 10 stations sampled for particle composition and carbon and nutrient uptake measurements are labelled.

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2.2. Nutrient assimilation The methodologies used to measure C and Si assimilation are described fully in Brown et al. (2003). Net primary production was determined using the 14C incubation technique outlined in Parsons et al. (1984), and bSiO2 production by the 32Si radiotracer method of Brzezinski and Phillips (1997). All incubations were run from dawn until midday; approximately a 6-h period. This time period was chosen primarily to minimise effects of silicic acid depletion over the course of the experiment. Each experiment also included a sample incubated in a foil-covered bottle, to obtain a blank correction for the photosynthetic C assimilation, and to determine rates of assimilation in dark conditions for bSiO2. No correction for abiotic bSiO2 assimilation was made as previous work has shown this to be inconsequential (Leynaert et al., 2001). As expected, primary production was minimal in dark conditions; however, significant dark production (typically 80% of production measured in daylight condition) of biogenic silica was observed. Daily primary production rates were calculated by scaling the values obtained (corrected for minor [< 5% total uptake] inorganic production measured in the dark bottles) in the 6h incubations to a full dawn-to-dusk time period. A 24h bSiO2 production rate was obtained by calculating dawn-to-dusk rates from the 6-h incubation as for primary production, and adding a night-time value calculated by scaling the bSiO2 production observed in the dark incubation bottles to the period of darkness. Dissolved nutrient concentrations, required for calculation of bSiO2 assimilation rates, were determined using standard colorimetric methods on a Skalar Sanplus autoanalyser, following Sanders and Jickells (2000). All carbon and nutrient assimilation experiments were run in triplicate; the mean precision of all measurements above detection limit was 9.2% for C, 13.7% for Si and 13.2% for P. Dissolved inorganic nutrient samples were run in duplicate and included both internal and external standard reference materials; the mean precision for all nutrients was <3%. 2.3. Particulate matter composition Biogenic silica concentrations were determined by filtering a 500-mL subsample onto a 0.8-μm polycarbonate filter under gentle vacuum, followed by a 2h digestion with 0.2 M NaOH at 80°C (Ragueneau and Treguer, 1994). Silicic acid concentrations of the digested samples were determined using standard autoanalyser methods as described above. A further 500-mL

subsample was filtered using gentle vacuum through GF/F (nominally 0.7μm pore size) filter and immediately frozen at − 20 °C for POC analysis, using a Carlo Erba CHN analyser on return to shore. Precision of the analyses was 11% for POC and 3.3% for bSiO2. 3. Results and discussion 3.1. The Iceland basin spring bloom: nutrient and biological background The 0.1% PAR depth during the cruise was between 29 and 99m, and the range of the surface mixed layer depth (estimated as the depth at which a > 0.2 °C change occurs in the CTD temperature profile) was between 5 and 75m. The surface mixed layer depth exceeded that of the photic zone at 3 of the 10 stations. Neither parameter displayed a robust correlation with either time or latitude. Surface chlorophyll, silicic acid and phosphate concentrations ranged from 0.53 to 7.7 μg L− 1, 0.3 to 3.4μmol L− 1 and 0.03 to 0.77 μmol L− 1 respectively, representing a range of conditions from the early stages of diatom spring bloom development through to silicic acid exhaustion and bloom collapse. The progression of the diatom bloom was assessed by considering the mean silicic acid concentration within the photic zone, reaffirming previous studies (Egge and Aksnes, 1992), which demonstrated diatom dominance of primary production at silicic acid concentrations above 2 μmol L− 1. Excess surface nitrate (4–10 μmol L− 1) was present at 9 out of 10 stations, including those where total silicic acid depletion was observed, implying further production potential by nonsiliceous phytoplankton. Primary production and bSiO2 assimilation rates during the FISHES cruise are detailed fully elsewhere (Brown et al., 2003). Primary production ranged between 0.49 and 3.2g C m− 2 day− 1, with five stations identified as active spring bloom sites. At most sites, bSiO2 assimilation was between 5 and 20mmol Si m− 2 day− 1, in the range of non-bloom bSiO2 assimilation observed in the Southern Ocean (Brzezinski et al., 2001; Gall et al., 2001); substantially higher rates of 78 and 167mmol Si m− 2 day− 1 were recorded at two stations. The phytoplankton taxonomy and ecosystem observed during the FISHES study have been described in detail elsewhere (Moore et al., 2005). Briefly, the basin is divided into five representative areas. Southeast of Iceland, diatoms, predominantly Nitzschia sp. are abundant. Diatoms also dominate the region of the Iceland Faeroes front, but here, a broader variety of species are present, including Chaetoceros sp., Thalassosira gravida

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and Astellioneriopsis glacialis. North of the Iceland– Faeroes Front and in the Rockall Trough region, flagellates are present in large numbers, but with significant contributions from cryptomonads and coccoliths, respectively. In the central Iceland Basin, a mixed community of flagellates and ciliates is present. 3.2. Spatial and vertical variation in C/Si C/Si molar ratios were calculated for the assimilation (C/Siassimilation) rates and for the particulate standing stock (C/Siparticulate) (Fig. 2). The C/Si assimilation ratios were calculated on the basis of the 24-h assimilation rates estimated as described in Section 2.2. An overall value for each station was calculated by vertically integrating the data to the depth of 0.1% surface PAR. Little variation in C/Siparticulate with depth was observed at individual stations (Fig. 2), suggesting that the vertical mixing of particles and nutrients in the surface mixed layer was sufficiently rapid to prevent any depth variability in mineralisation or fixation ratios introducing vertical structure to elemental composition. In contrast, C/Siassimilation (Fig. 2) always decreased from the surface to the base of the photic zone, as a

Fig. 2. Vertical profiles of assimilation (a) and particulate composition (b) for C/Si. The vertical line indicates the mean of the depthintegrated C/Si values for all stations. The errors bars are the analytical error as described in the text.

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consequence of the strong light dependence of photosynthetic carbon uptake and the light-independent uptake of silicic acid (Azam and Chisholm, 1976; Brzezinski et al., 1997). The station-averaged C/Siparticulate ranged from 3.3 to 108.9 (mean 21.2 ± 34.4). The highest value was observed at station 14029, which was atypical in that nitrate was fully depleted, yet excess silicic acid was present. This suggests that primary production at that site had been dominated by non-siliceous phytoplankton, consistent with the high elemental C/Si ratio. The second highest value (station 14078) was 51.5, half that at 14029. C/Siassimilation varied from 1.6 to 22.6, again with the highest value at station 14029 being substantially greater than the second highest value (station 13984, 16.0). The mean value for C/Siassimilation was 8.2 ± 7.4, lower than the mean C/Siparticulate; thus, the elemental composition of particulate matter in the photic zone did not reflect the stoichiometry of the processes involved in its synthesis, but instead was comparatively carbon rich. 3.3. Vertical structure of particulate matter composition Our observation that the particulate material in the photic zone is systematically carbon rich relative to the processes involved in creating it could either be caused by an export of nutrient-rich particulate matter from the photic zone or a preferential mineralisation of bSiO2 relative to carbon from particulate matter in the photic zone. We examined the former possibility by looking in detail at the vertical variability in C/Si ratios at individual stations, based on the assumption that particles at the base of the euphotic zone will be representative of the exported particulate matter. C/Siparticulate at the deepest sampling depth was lower than that of the surface material (i.e., consistent with an export of nutrient-rich particulate matter) at only two stations, 14005 and 14060. Overall then, it seems likely that the generally high C/Siparticulate relative to processes involved in its synthesis is most likely to have been caused by a preferential mineralisation of Si relative to C in the upper water column. At the anomalous stations where the deep pool is Si rich relative to the surface pool, it is possible that the low C/Si ratio of the deep particles relative to the surface pool was caused by the strong light dependency of carbon assimilation compared to the short-term light independence of silicon assimilation. Both stations show deep subsurface maxima in the concentration of the diatom-diagnostic pigment fucoxanthin, which correspond with gradients in silicic acid concentration, but are not mirrored in other photosynthetic pigments

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(Brown et al., 2003). It has previously been shown that nutrient-depleted diatoms sink faster than nutrient replete cells (Bienfang et al., 1982, Brzezinski and Nelson, 1988), and that nutrient-depleted diatoms can ‘mine’ deep silicic acid reserves (Allen et al., 2005). Thus, it would seem at these sites that nutrient depletion-induced vertical variation in the phytoplankton community structure, combined with the rapid uptake of silicic acid by Si-depleted diatoms at depth is capable of affecting the particulate composition in the short term. Thus, it is possible that, even at these stations, the high C/Siparticulate relative to C/Siassimilation is caused by a preferential mineralization of nutrients relative to carbon from particulate matter rather than an export of nutrientrich particulate matter. 3.4. Preferential remineralisation in the FISHES data set The relative mineralisation rates of POC and bSiO2 at each station are investigated by comparing the photic zone averaged C/Siassimilation ratio to the C/Siparticulate ratio (Fig. 3) for each station. There is substantial variation between stations in both C/Siassimilation and C/ Siparticulate (Fig. 3a); however, there is a reasonably good, although non-linear, correspondence between C/ Siparticulate and C/Siassimilation at individual stations. This variability is assessed by examining the ratio of C/ Siparticulate to C/Siassimilation at each station. The mean value of C/Siparticulate:C/Siassimilation is 3.7 ± 2.8; thus, in general, the particulate matter is about four times as rich in carbon relative to silicon as would be expected from the elemental uptake ratios. C/Siparticulate is higher than C/Siassimilation at 7 out of 10 stations, suggesting bSiO2 is preferentially mineralised relative to POC in the surface waters at these stations. Preferential mineralisation of bSiO2 relative to POC, as suggested by the FISHES data set, is apparently in conflict with much of the existing data on POC and bSiO2 fluxes in the surface ocean (e.g., Wong et al., 1999; Buesseler et al., 2001; Shipe and Brzezinski, 2001; Nelson et al., 2002; Queguiner and Brzezinski, 2002). All these studies suggest a preferential mineralization of POC relative to bSiO2 in the upper water column. However, most of these data originate from sediment trap samples taken deeper in the water column than our euphotic zone samples or are averaged over annual cycles, in contrast to the much shorter timescale and surface ocean focus of the FISHES observations. They are also often in HNLC waters where silicic acid exhaustion is less likely to occur, and where Fe-

Fig. 3. (a) Depth-integrated values of C/Si particles (filled symbols) and C/Si assimilation (open symbols) for each of the FISHES stations, shown on a logarithmic scale for clarity. Error bars are the station mean of the analytical error on each measurement. (b) The ratio of mixed layer depth to euphotic zone depth.

limitation may affect Si/C assimilation ratios (Hutchins and Bruland, 1998). Although typically considered less labile than POC, rapid recycling of bSiO2 has been observed in low nutrient waters of the tropical Atlantic (Nelson and Brzezinski, 1997) and in highly productive upwelling areas (Nelson and Goering, 1977). Further, Wong et al. (1999) observed that bSiO2 was less efficiently transferred from the surface ocean during rapid sinking events in the North Pacific, and globally, absolute rates of bSiO2 recycling were fastest during periods of rapid diatom production, such as experienced in the North East Atlantic diatom spring bloom (Brzezinski et al., 2003; Beucher et al., 2004). It therefore seems reasonable to conclude that rapid recycling of bSiO2 relative to POC in the upper water column is a general feature of the spring diatom bloom in this region. 3.5. Influence of the relationship between the mixed layer and photic depths on C/Si ratios Comparison of the mean C/Si ratios of assimilation and of the particulate pool across the whole basin

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suggests frequent preferential mineralisation of bSiO2 relative to POC. However, C/Siassimilation is larger than C/Siparticulate, suggesting preferential mineralisation of POC relative to bSiO2 at three stations (13971, 13984 and 14010). The cause of these anomalies must be examined before the apparent preferential mineralisation of bSiO2 over POC during the North Atlantic spring bloom can be accepted as a general pattern. We now consider the possibility that the anomalies are a result of overestimation of C/Siparticulate or an underestimation of C/Siassimilation. Particulate C/Si ratios vary little with depth (Fig. 2), and thus, it is likely that the integrated POM data are representative of particulate ratios throughout the upper water column. However, with regard to carbon and nutrient assimilation, carbon fixation by photosynthesis is a highly light-dependent process, unlike the biological uptake of silicic acid (Raven, 1983; Martin-Jezequel et al., 2000). Since our measurements were limited to the depth of 0.1% PAR, it is possible that, at stations where the depth of the surface mixed layer exceeded that of the photic zone, additional Si (but not C) assimilation may have been occurring at depths within the mixed layer but below the limit of photosynthesis. We now assess whether these conditions, which would result in an undersampling of deeper waters and, hence, an overestimate of the true mixed layer C/Siassimilation, may explain the anomalous data obtained from some stations. The hypothesis is addressed by examining the relationship between the mixed layer depth and photic zone depth at the stations sampled (Fig. 3b). At the three anomalous stations (13971, 13984, 14010), the surface mixed layer was substantially undersampled because it was much deeper than the depth of the photic zone, which was used to define the sampling depth. Thus, at these sites, the biogenic silica production is likely to have been underestimated, leading to an overestimate of the C/Siassimilation ratio. Whether this effect is sufficiently large to make a more realistic estimate of C/Siassimilation lower than the corresponding value of C/Siparticulate and, hence, imply a preferential mineralization of nutrient relative to carbon from particulate matter is now addressed. To examine this possibility, we extended the depth of integration of assimilation or particulate concentration to the depth of the surface mixed layer rather than the photic zone at the anomalous stations, using the 0.1% PAR measurements to represent the sub-photic zone waters. This recalculation yields C/Siassimilation values 12–20% less than the photic zone-only ratios. The values are still greater than the corresponding C/

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Siparticulate ratios, suggesting at these sites C/Siparticulate may indeed be larger than C/Siassimilation, and that preferential mineralization of carbon over nutrients may be occurring. However, many of the North Atlantic bSiO2 production profiles show large increases at the base of the thermocline, possibly due to uptake supported by silicic acid mixed across the boundary (Brown et al., 2003). The above calculations may therefore still be underestimates of C/Siassimilation, and the possibility that our calculations of C/Siassimilation might exceed C/Siparticulate had measurements had been made across the whole surface mixed layer cannot be excluded. Overall, the majority of sites display behaviour consistent with greater nutrient mineralisation relative to POC; hence, we conclude that preferential mineralisation of bSiO2 relative to POC in the photic zone during the NE Atlantic spring diatom bloom is a frequent feature of this event, particularly when the mixed layer is shallow relative to the depth of the photic zone. 3.6. Qualification of steady-state assumption 3.6.1. Experimental conditions Our comparison of uptake stoichiometry in the bottles relative to the elemental particulate stoichiometry is intended to shed light on the processes which modify the pool of material created by phytoplankton uptake after initial respiration and silicic acid release and transform it into the pool of material in the water column. The underlying assumption in our analysis is that the uptake rates within the bottle reflect all of the algal-mediated cycling and none of the longer term diagenetic processes, and that the particles are then transformed into the particle field present in the water column by processes which do not occur in vitro. Clearly, we cannot fully distinguish between those processes mediated by algal physiology from processes acting on the particles mediated by bacterial processes, grazing and solubilisation on the basis of time. Thus, our assumption is not strictly valid; some of these processes will occur in the incubations, and some of the particles sampled will have been only recently synthesised. Thus, the measured C/Si is partly controlled by (a) the amount of processing in the assimilation experiments and (b) the proportion of living cells making up the particulate pool. However, on the whole, the assimilation rates measured in the bottle incubation will be more representative of short-term particle synthesis, and the particulate pool will be more representative of the effects of longer term processing on the particle pool. Thus, that the

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assumption does not strictly hold true does not invalidate our conclusion; however, it does imply that the difference in stoichiometry between the fresh pool and the bulk POM pool may be smaller than our analysis suggests. 3.6.2. Changes in plankton community structure Rather than being a consequence of preferential mineralisation of biogenic material, the generally higher values of C/Siparticulate compared to C/Siassimilation may be caused by temporal changes in one or both parameters over the duration of the bloom; i.e., the assumption of steady state within the surface layer pool may be invalid. Measurements of particulate pool composition and assimilation rates represent processes occurring on different timescales; particle composition measurements reflect nutrient assimilation and mineralisation processes integrated over several days, whilst assimilation rate measurements are determined within a timeframe of hours associated with the experimental incubation. Thus, the measured C/Si assimilation ratio could increase in response to silicic acid limitation, either by diatoms altering their metabolism or by replacement of the diatom population by non-silicifying phytoplankton, faster than the associated changes in the C/Si ratios of the particulate pool. These would then lag the change in uptake ratios given the longer residence time of material in this pool compared to the duration of the incubations. Should this be the case, our analysis would conclude, erroneously, from observations of C/Siparticulate being systematically larger than C/Siassimilation that a preferential mineralization of silicon relative to carbon must be occurring. The possibility that C/Siassimilation and C/Siparticulate change systematically within the data set as a function of diatom bloom development is considered by plotting

these parameters against mean mixed layer silicic acid concentration (Fig. 4) as an indicator of diatom bloom progression, following Brown et al. (2003). Neither uptake ratios nor the elemental composition of the particulate pool decline systematically as the bloom subsides. Hence, our conclusion regarding the frequent preferential mineralisation of bSiO2 relative to POC from particulate matter appears robust. Our general conclusion is also supported by simple calculations of the residence time of material in the particulate pool (calculated as pool size/assimilation rate), which yield values of 10 ± 10 days for POC and 3.8 ± 3 days for bSiO2. These residence times are relatively short compared to the typical 3–4 weeks duration of the North Atlantic spring phytoplankton bloom (Sieracki et al., 1993; Savidge et al., 1995; Bury et al., 2001). This suggests that POC is contained within the bulk pool for approximately two to three times as long as bSiO2, consistent with it being less susceptible to mineralisation. 3.7. Role of grazing in modification of C/Si Thus far, we have considered mainly the physical– chemical aspects of cycling of particulate organic material in the water column. However, in addition to these passive mechanisms, the active grazing and processing of POM by zooplankton may selectively modify particles. During the North Atlantic spring bloom, there is evidence to demonstrate that no significant grazing occurs during the spring bloom while it is composed of large (> 20 μm) phytoplankton, typically Nitzschia sp. diatoms, but that when the bloom is in decline and composed predominantly of <20 μm cells, grazing by microzooplankton can account for up to 100% of primary production (Gifford et al., 1995). Grazing of the large phytoplankton fraction by mesozooplankton

Fig. 4. The depth-integrated values of C/Si in particulate (open triangles) and assimilated (open squares) material, ordered by decreasing mean mixed layer silicic acid concentration (solid diamonds, bold line). The latter term has been used as an indicator of diatom bloom progression (Brown et al., 2003), with stations of mean Si(OH)4 < 2 μmol L− 1 designated as ‘post-bloom.’ The errors are the standard deviation of the value at all stations.

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may occur; however, reports indicate that consumption by C. finmarchicus, the dominant mesozooplankton, accounts for at most a few percent of primary production (Morales et al., 1993; Gifford et al., 1995) and may have a preference for non-diatom food sources (Nejstgaard et al., 2001; Van Niewerburgh et al., 2004). Like most phytoplankton, the zooplankton which consume them have no or little requirement for silicon. Consumption of diatoms would therefore likely lead to assimilation of carbon and nutrients in the zooplankton and higher trophic levels, whilst silicon would be excreted. Such a mechanism could lead to an increase in C/Si ratios in particulate material relative to the C/Si ratio of assimilated material. This was not generally observed in the study, suggesting grazing is not an important factor in particle transformation during the North Atlantic spring bloom. At stations 13971, 13984, and 14010 C/Siparticulate was lower than C/Siassimilation. These stations were significantly different from each other in terms of diatom bloom development (Brown et al., 2003) and are also likely to have been differentially impacted by grazing. Thus, although we cannot exclude the possibility that grazing may increase C/Siparticulate values, it would seem not to have a very significant impact.

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is likely to be a carbon sink over multi-year timescales, and the selective regeneration of carbon relative to silicon below this depth will be of reduced importance. If, however, a preferential mineralisation of POC relative to bSiO2 begins at the base of the summer mixed layer (< 100 m), then the water mixed up into the photic zone during overturning will not contain an excess of dissolved Si relative to C, and the significance of diatoms in long-term export production may be reduced. Evidence from deep sediment traps in the North Atlantic shows clearly the better preservation of bSiO2 relative to particulate organic carbon (Honjo and Manganini, 1993; Jickells et al., 1996) at depths below about 1000 m. Thus, if our observations of significant preferential mineralization of Si relative to C from particulate matter in the upper water column are typical, then there must exist a horizon between 100 and 1000m where a switch between preferential mineralization of bSiO2 relative to POC (above 100 m) to a preferential preservation of bSiO2 relative to POC (below 1000 m) occurs. Further measurements of the relative magnitude of C and Si mineralisation in the upper ocean, especially in the 100–1000-m depth range are needed to fully establish the role of diatoms in the biological carbon pump.

3.8. Effects of preferential mineralisation on our understanding of carbon export

4. Conclusions

Results from the FISHES data set indicate preferential mineralisation of bSiO2 relative to POC in the surface mixed layer at most stations during the spring bloom in the North Atlantic. The lability of POP and PON relative to POC is widely recognised, and both dissolved organic and regenerated inorganic nutrients are important in generating further production (e.g., Jackson and Williams, 1985; Smith et al., 1986; Vidal et al., 1999). However, whether the observed preferential mineralisation of bSiO2 relative to POC in the upper water column is sufficient to make diatom productivity a net sink for inorganic carbon in the northern North Atlantic, where most particle mineralisation occurs above the depth of deepest winter mixing (ca. 800 m; Koeve, 2001), depends on processes deeper in the water column. Specifically, it will be a function of the variation in the stoichiometry of carbon and silicon regeneration with depth and the extent of the deep winter mixing which regenerates the surface nutrient pool. If bSiO2 is preferentially released from particulate matter relative to POC throughout the depth to which winter mixing penetrates (ca. 800 m; Koeve, 2001), diatom production

We suggest that bSiO2 is frequently preferentially mineralised relative to POC from particulate matter in the photic zone during the NE Atlantic spring diatom bloom. The strong coherence between C/Si assimilation and mineralisation ratios, and the short residence time of particulate material in the surface mixed layer pool relative to the length of the spring bloom support our inherent assumption of steady state over short timescales. High variability in the C/Si ratios of assimilation and of particulate matter in the photic zone was observed between stations. Within stations, particulate composition ratios were relatively invariant with depth, whereas the assimilation ratios often showed a decreasing C/Si with depth. This is likely due to a decoupling of the light-dependent primary production from the non-lightdependent assimilation of Si in the short term. The mean elemental composition of the particulate material (C/Si = 21.2) was carbon rich relative to the corresponding assimilation ratio, implying a preferential mineralisation of Si relative to C in the photic zone. Carbon is contained in the particulate pool for two to three times longer than silicon, consistent with it being

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more refractory and likely to be exported from the summer surface mixed layer. The rapid recycling of bSiO2 relative to POC, and in particular its magnitude relative to a preferential mineralisation of POC which occurs deeper in the water column may have important implications regarding the role of diatoms in export productivity. More estimates of silicon assimilation and depth variability in C and Si cycling are required to further address this point. Acknowledgements We thank the captain, crew and scientific team of RRS Discovery cruise D253 for their invaluable assistance on the cruise. This work was supported through UK Natural Environment Research Council small grant NER/B/S/2000/00815, awarded to Queen's University Belfast. References Allen, J.T., Brown, L., Sanders, R., Moore, C.M., Mustard, A., Fielding, S., Lucas, M., Rixen, M., Savidge, G., Henson, S., Mayor, D., 2005. Diatom carbon export enhanced by silicate upwelling in the northeast Atlantic. Nature 437, 728–733. Anderson, T.R., 1992. Modelling the influence of food C:N ratio and respiration on growth and nitrogen-excretion in marine zooplankton and bacteria. Journal of Plankton Research 14 (12), 1645–1671. Azam, F., Chisholm, S.W., 1976. Silicic acid uptake and incorporation by natural marine phytoplankton populations. Limnology and Oceanography 21, 427–435. Beucher, C., Treguer, P., Corvasier, R., Hapette, A.M., Elskens, M., 2004. Production and dissolution of biosilica and changing microphytoplankton dominance in the Bay of Brest (France). Marine Ecology. Progress Series 267, 57–69. Bidle, K.D., Azam, F., 1999. Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397 (6719), 508–512. Bienfang, P.K., Harrison, P.J, Quarmby, L.M., 1982. Sinking rate response to depletion of nitrate, phosphate and silicate in four marine diatoms. Marine Biology 67, 295–302. Boyd, P., LaRoche, J., Gall, M., Frew, R., McKay, M.L., 1999. Role of iron, light and silicate in controlling algal biomass in subantarctic waters SE of New Zealand. Journal of Geophysical Research 104 (C6), 13395–13408. Brown, L., Sanders, R., Savidge, G., Lucas, C.H., 2003. The uptake of silica during the spring bloom in the Northeast Atlantic Ocean. Limnology and Oceanography 48 (5), 1831–1845. Brzezinski, M.A, Nelson, D.M., 1988. Differential cell sinking as a factor influencing diatom species competition for limiting nutrients. Journal of Experimental Marine Biology and Ecology 119, 179–200. Brzezinski, M.A., Nelson, D.M., 1995. The annual silica cycle in the Sargasso Sea near Bermuda. Deep-Sea Research I 42 (7), 1215–1237. Brzezinski, M.A., Nelson, D.M., 1996. Chronic substrate limitation of silicic acid uptake rates in the western Sargasso Sea. Deep-Sea Research II 43 (2–3), 437–453.

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