Biogeochemistry of total organic carbon and nitrogen in the Sargasso Sea: control by convective overturn
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Deep-Sea Research II 48 (2001) 1649}1667 Biogeochemistry of total organic carbon and nitrogen in the Sargasso Sea: control by convective overturn Dennis A. Hansell*, Craig A. Carlson Bermuda Biological Station for Research, Inc., St. George's, 17 Biological Station Lane, Ferry Reach GE-01, Bermuda Abstract The contributions of total organic carbon and nitrogen to elemental cycling in the surface layer of the Sargasso Sea are evaluated using a 5-yr time-series data set (1994}1998). Surface-layer total organic carbon (TOC) and total organic nitrogen (TON) concentrations ranged from 60 to 70 M C and 4 to 5.5 M N seasonally, resulting in a mean C : N molar ratio of 14.4$2.2. The highest surface concentrations varied little during individual summer periods, indicating that net TOC production ceased during the highly oligotrophic summer season. Winter overturn and mixing of the water column were both the cause of concentration reductions and the trigger for net TOC production each year following nutrient entrainment and subsequent new production. The net production of TOC varied with the maximum in the winter mixed-layer depth (MLD), with greater mixing supporting the greatest net production of TOC. In winter 1995, the TOC stock increased by 1.4 mol C m\ in response to maximum mixing depths of 260 m. In subsequent years experienc- ing shallower maxima in MLD ((220 m), TOC stocks increased (0.7 mol C m\. Overturn of the water column served to export TOC to depth ('100 m), with the amount exported dependent on the depth of mixing (total export ranged from 0.4 to 1.4 mol C m\ yr\). The exported TOC was comprised both of material resident in the surface layer during late summer (resident TOC) and material newly produced during the spring bloom period ( fresh TOC). Export of resident TOC ranged from 0.5 to 0.8 mol C m\ yr\, covarying with the maximum winter MLD. Export of fresh TOC varied from nil to 0.8 mol C m\ yr\. Fresh TOC was exported only after a threshold maximum winter MLD of +200 m was reached. In years with shallower mixing, fresh TOC export and net TOC production in the surface layer were greatly reduced. The decay rates of the exported TOC also covaried with maximum MLD. The year with deepest mixing resulted in the highest export and the highest decay rate (0.003 d\) while shallow and low export resulted in low decay rates (0.0002 d\), likely a consequence of the quality of material exported. The exported TOC supported oxygen utilization at C : O molar ratios ranging from 0.17 when TOC export was low to 0.47 when it was high. We estimate that exported TOC drove 15}41% of the annual oxygen utilization rates in the 100}400 m depth range. Finally, there was a lack of variability in the surface-layer TON signal during summer. The lack of a summer signal for net TON production suggests a small role for N "xation at the site. * Corresponding author. Fax: #1-305-361-4689. E-mail address: dhansell@rsmas.miami.edu (D.A. Hansell). 0967-0645/01/$ - see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 1 5 3 - 3
1650 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 We hypothesize that if N "xation is responsible for elevated N : P ratios in the main thermocline of the Sargasso Sea, then the process must take place south of Bermuda and the signal transported north with the Gulf Stream system. 2001 Elsevier Science Ltd. All rights reserved. 1. Introduction Total organic carbon (TOC) and nitrogen (TON) are increasingly recognized as important constituents of the oceanic carbon and nitrogen cycles. Over the past decade many advances have been made in our understanding of these pools, including wide scale distribution (Dileep Kumar et al., 1990; Guo et al., 1994; Peltzer and Hayward, 1996; Hansell and Waterhouse, 1997; Hansell and Carlson, 1998a; Hansell and Peltzer, 1998; Doval and Hansell, 2000), net production (Bronk et al., 1994; Hansell et al., 1997a, b; Zhang and Quay, 1997; Hansell and Carlson, 1998b), composition (Benner et al., 1992; McCarthy et al., 1996; Opsahl and Benner, 1997; Aluwihara et al., 1997), seasonal dynamics (Carlson et al., 1994; Copin-Montegut and Avril, 1993; Borsheim and Myklestad, 1997; Carlson et al., 1998), age (Williams and Dru!el, 1987; Dru!el et al., 1989; Bauer et al., 1992), and microbial turnover (Zweifel et al., 1993; Amon and Benner, 1994; Carlson and Ducklow, 1995, 1996; Cherrier et al., 1996; Hansell et al., 1995; Carlson et al., 1999). Even with these advances we have not developed an adequate understanding of the physical and biological controls on the cycling of carbon and nitrogen through the pools. Evaluation of biogeochemical and physical variability within a long-term time series such as the US JGOFS Bermuda Atlantic Time-Series Study (BATS) provides valuable insight into the seasonal dynamics of TOC and TON and the role of these pools in biogeochemical processes. The Sargasso Sea, particularly in the region of the BATS site, is perhaps the most intensively studied region of the world's ocean in terms of carbon and nitrogen biogeochemistry (Steinberg et al., 2001 and citations within). The physical setting and the meteorological forcing that in#uence the BATS site have been detailed elsewhere (Deuser, 1986; Michaels et al., 1994). Brie#y, the waters surrounding BATS are strongly strati"ed in the summer months, taking on the characteristics of an oligotrophic system. During the fall and winter months the BATS site is in#uenced by weekly to biweekly storm fronts that bring strong, cold and dry winds. These storms cool the surface water and lead to a deepening of the mixed layer by convective overturn. When the mixed-layer depth (MLD) reaches '200 m, the nutricline is breached and nutrients are entrained into the euphotic zone. The entrained nutrients support spring phytoplankton blooms (Michaels et al., 1994; Michaels and Knap, 1996). In addition to the entrainment of nutrients into the surface waters, seasonal overturn can be important in mixing suspended particulate and dissolved organic matter out of the euphotic zone to depth, thereby contributing to vertical export (Copin-MonteH gut and Avril, 1993; Carlson et al., 1994). In this paper, we evaluate the seasonal and interannual variability of TOC and TON in the Sargasso Sea at the BATS site over a 5-yr period (1994}1998). We consider the relationship between the maximum mixed-layer depth attained during winter and the subsequent net produc- tion of TOC. We evaluate the export of the surface accumulated TOC during winter overturn of the water column, including a determination of decay rates and contributions to oxygen utilization rates. We evaluate the seasonality of the TON pool, and discuss the implications for the role of
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1651 N "xation in the local nitrogen cycle. All of the evaluations are made in two dimensions * depth and time. We have inadequate spatial data with which to assess the impact of horizontal mixing and advective processes to the results. 2. Sampling and analyses 2.1. Sampling program Sampling of hydrographic, biological and geochemical properties in the Sargasso Sea at the Bermuda Atlantic Time-Series Study (BATS) site (31350N, 64310W) has taken place since October 1988 (Steinberg et al., 2001). Since November 1993 and February 1994, respectively, samples for determination of concentrations of TOC and TON have been collected at the site. Samples were collected aboard the RV Weatherbird II at monthly intervals, except during the annual winter overturn and spring bloom periods (nominally during the period of February through March each year) when sampling was conducted approximately biweekly. Samples were collected un"ltered using 12-l Niskin bottles mounted on a CTD rosette. Normally, 12 depths were sampled in the upper 250 m on one cast, and 12 on a second cast from 300 to 4500 m. Samples were collected with multiple rinsing into acid-cleaned and precombusted (4503C) EPA vials with Te#on-lined caps or acid-cleaned 60-ml polyethylene bottles. The vials and bottles were stored frozen (!203C) until analysis, normally within 3 months of collection. All analyses were performed at the Bermuda Biological Station for Research, Inc. 2.2. Total organic carbon analyses TOC samples were analyzed by a high-temperature combustion (HTC) method using custom- made instruments. From 1994 to 1996 samples were analyzed using a single-zone furnace heated to 8003C. After 1996 all samples were analyzed with a furnace divided into two zones (Hansell and Peltzer, 1998; Carlson et al., 1999), resulting in improved precision. Deep-water ('1000 m) variability (standard deviation) throughout this time-series record was $0.6 M C (n"295), useful as an index of our precision and of the stability of the deep-ocean DOC concentrations. Ultra high-purity O #owed through the machine at 175 ml min\. Samples were acidi"ed (10 l of 85% H PO per 10 ml of sample) and sparged with CO -free oxygen for at least 10 min to remove inorganic carbon. One hundred microliters of sample was injected manually through a septumless port into the quartz combustion tube packed with Pt gauze (Aldrich), 7% Pt on alumina catalyst (Shimadzu), Sul"x (Wako Pure Chemical Industries, Inc.) and CuO wire (Leeman Labs). The Pt gauze and Pt beads were heated to 8003C in the upper zone while the remaining packing material was heated to 6003C in the lower zone. The resulting CO #owed through two water traps and a "nal copper halide trap then detected with a LiCor 6252 CO analyzer. The signal was integrated with chromatographic software (Dynamax Macintegrator I version 1.3; Rainin Inst.). Extensive conditioning of the combustion tube was essential to minimize the machine blank. The system blank ((10 M) was assessed daily with ampoulated low-carbon waters (LCW) that were referenced against blank water provided by Dr. Jonathan Sharp for the 1994 DOC community
1652 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 intercomparison program. The system response was standardized daily with a four-point calibration curve of glucose solution in LCW. Deep Sargasso seawater ('2000 m), which had been acidi"ed and ampoulated, served as reference material. Analyzing low-carbon water and reference deep seawater several times daily allowed us to assess the system stability from run to run and day to day, ensuring con"dence in our analysis. TOC is comprised of suspended organic particles and dissolved organic material, with the latter operationally de"ned as material passing through a combusted GF/F "lter. Organic particles retained on a GF/F "lter accounted for only 1}4% of TOC at the BATS site, thus the temporal and spatial dynamics of the TOC pool are largely due to changes in the DOC pool (Carlson et al., 1998; Hansell and Carlson, 1998b). 2.3. Total organic nitrogen analyses Concentrations of TON were determined by UV photo-oxidation according to the method described by Walsh (1989). In this method, TON is calculated as the di!erence between the measured concentrations of total nitrogen (sum of organic and inorganic constituents, determined after UV oxidation of the sample) and inorganic nitrogen (here NO\ plus NO\, determined colorimetrically). Ammonium is included in the TON value, normally contributing only 15}20 nM to the signal (Lipschultz, 2001). Hansell (1993) describes the propagation of errors associated with calculation of TON concentrations by di!erences. Error is highest where the inorganic N concen- trations are highest. The standard deviation of replicate samples from the oligotrophic surface layer was +10%. Placing sample bottles in a warm-water bath thawed frozen samples. A 10 ml aliquot was removed from each sample bottle and placed in a 20-ml fused quartz tube equipped with a ground stopper (Quartz Scienti"c, Inc.). Fifty microliters of 30% hydrogen peroxide were added to each tube and placed in a homemade irradiation unit overnight (17}20 h). The irradiation unit contained a 1200 W UV lamp (Hanovia) protected by a quartz jacket. A two-tiered aluminum tube holder (40 tubes total) "tted around the lamp and held the samples 8 cm from the lamp. A fan placed at the bottom of the unit blew air across the samples for cooling. A hinged aluminum cylinder, open at the top and bottom, was "tted around the samples to keep stray UV light from leaving the system. This system was operated in a fume hood, the front of which was covered with a black curtain while in use (to collect stray UV light). After irradiation, aliquots of the samples (which were refrigerated overnight) that had not been oxidized, and the photo-oxidized aliquots, were analyzed for nitrate plus nitrite using a colorimet- ric method on a Technicon Autoanalyzer II (Knap et al., 1997). Daily calibration was achieved from four-point calibration curves using both KNO and NaNO . Cadmium column e$ciency was determined by comparing the slope of the NO\ calibration curve with the slope obtained from NO\ calibration curve. Due to the photo-reduction of NO\ to NO\ (Walsh, 1989), it is important that the cadmium column be e$cient when analyzing samples containing high concentrations of nitrate. Therefore, a new column (i.e. e$ciency '98%) was employed when analyzing nitrate samples '10 M. The column e$ciency was generally '90% when running the low nitrate samples. Low-nutrient Sargasso Sea surface water was always processed with the samples as a daily quality control measure. Oxidation e$ciency of glycine, ammonium chloride, and urea was normally '90%, in general agreement with the "ndings by Walsh (1989).
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1653 2.4. Other measurements Oxygen samples were collected in duplicate from the Niskin bottle and analyzed via the Winkler titration method (Winkler, 1888). Automated titration and endpoint detection system were used as described in the BATS methods manual (Knap et al., 1997). A Seabird 9/11 Plus CTD system was used to measure continuous pro"les of salinity, temperature and pressure. Discrete salinity measurements collected from Niskin bottles were used to calibrate CTD data (Knap et al., 1997). All data reported here are available on the BATS public data set (http:// www.bbsr.edu). 3. Results 3.1. Spatial and temporal variability of TOC, TON and the C/N molar ratio TOC * Vertical pro"les of TOC showed a general pattern of elevated concentrations in the surface 50}100 m with values ranging from 60 to 70 M C (Fig 1a). Variability in the surface water concentrations was forced by the seasonal dynamics of TOC production and consumption and by physical processes such as mixing and advection. Below 100 m TOC decreased exponentially to Fig. 1. Vertical pro"le of all TOC (a) and TON (b) data collected at the BATS site from 1994 to 1998. Molar C : N ratios are presented as a mean pro"le of all data; error bars represent standard errors. Concentrations are M.
1654 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 a depth of approximately 1000 m, beyond which TOC was distributed homogeneously at 43.6$0.6 M C (n"295) throughout the remainder of the water column. The variability of TOC concentrations in the upper water column followed a regular pattern each year (Fig. 2a). The lowest surface concentrations occurred during periods of winter convective overturn (Fig. 2c), with the decrease in concentration due to vertical mixing and dilution with the underlying, lower TOC water. Overturn of the water column moved surface accumulated TOC to depths of up to 260 m, as evidenced by deepening of the concentration isolines each winter (Fig. 2a). A gradual interannual increase in the winter minimum concentration was apparent (from 61 M in 1995 to 65 M in 1998; Fig. 3a) and linked to interannual shoaling of the winter MLD. Fig. 2. Contour plot of TOC (a) TON (b) and temperature (c) in the surface 300 m at the BATS site from 1994 to 1998. TOC and TON values are expressed in M concentrations. Temperature unit is 3C.
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1655 Fig. 3. (a) Seasonal variability of mixed-layer depth (dashed line) and TOC concentrations (solid line), (b) TON concentrations, and (c) C : N molar ratio in the surface 40 m of the water column at BATS. The TOC and TON values were "rst integrated over 40 m then normalized to the depth of integration. These values thus represent depth weighted means within the surface 40 m. The MLD estimate was based on a variable sigma-t criterion (Sprintall and Tomczak, 1992). It was determined as the depth where sigma-t is equal to sea surface sigma-t plus an increment in sigma-t equivalent to a 0.23C temperature decrease. During periods of restrati"cation (seasonal shoaling of the mixed layer) summer-time surface concentrations of TOC were regained. The highest surface concentrations varied little during individual summer periods (Fig. 3a), indicating that net TOC production ceased during the summer season. TOC concentrations remained relatively unchanged during summer increases of SST (Fig. 4), a process occurring after restrati"cation of the water column. TON * TON concentrations in the surface water were elevated above deep-water concentra- tions, ranging from 4 to 5.5 M (Fig. 1b). Below 1000 m, TON concentrations had a mean of 3.1$0.4 M (n"262). There was no clear seasonal trend in the TON concentrations (Fig. 2b). The depth weighted mean concentration ("TON/z; where integration is over depth z) in the upper 40 m had a seasonal amplitude of +0.5 M from 1994 to 1996, with the lowest concentrations during winter overturn (Fig. 3b). Although a clear seasonal signal was absent, the lowest concentra- tions reported occurred during winter overturn in 1995, coincident with the deepest and most prolonged mixing event. C : N ratio * The C : N molar ratio in the upper 40 m ranged from 11.5 to 15.5 (Fig. 3c), with a mean of 14.4$2.2 (n"240). Variability in the C : N molar ratio of the organic matter was not linked to seasonality. The mean C : N ratio decreased to values of +13.5 at depths of 150}500 m, and then increased to values generally '14 at depths '1000 m (Fig. 1c). The lowest C : N values
1656 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 Fig. 4. Scatter plot of TOC concentrations and temperature in the upper 40 m using all data, 1995}1996. were located at the depth of 183C mode water, indicating an input of this low C : N organic matter to the BATS site by horizontal transport. 3.2. Interannual variability of integrated TOC stocks The extent of deep mixing during winter in#uenced the size of the integrated stocks of TOC (upper 250 m), both during the period of winter overturn and in the following summer (Fig. 5a). During the 5-yr time series the maximum winter MLD ranged from '300 m in 1994 to (180 m in 1998 (Table 1). The 1995 winter overturn, for example, was characterized by a deep, lengthy mixing event and a large buildup in TOC stock (Fig. 5a). In subsequent years, each experiencing maximum winter MLDs of (220 m (Fig. 5a, Table 1), seasonal increases in TOC stocks were (0.5 mol C m\. Summer stocks of TOC increased through the time series (Fig. 5a), also coinciding with the decreasing winter maximum MLD. The deep winter mixed layer observed in 1994 coincided with the passage of a sub-mesoscale feature of uncharacteristically warm, nutrient-poor water (likely an anticyclonic eddy). This feature, while mixing deeply, did not result in measurable entrainment of inorganic nutrients to the surface waters, nor was there a measurable spring phytoplankton bloom associated with the passage of this feature (Steinberg et al., 2001). As such, we have not included this feature or the associated TOC variability in our analysis of TOC/TON dynamics driven by the spring blooms in other years. 3.3. TOC export The vertical export of TOC from the surface layer (de"ned as the introduction of surface accumulated TOC to depths '100 m) occurred with deep, turbulent mixing of the water column. The maximum depth of mixing reported here (and excluding 1994) was +260 m in 1995, so this
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1657 Fig. 5. (a) Time-varying integrated stocks of TOC (mol C m\; solid line) in the surface 250 m and mixed-layer depth (m; dashed line), (b) time-varying integrated TOC stocks in the 100}250 m depth layer. The dashed line is the slope of the regression of summer/fall minimum TOC values vs. time (TOC"0.1x!1.7 (R"0.77), where x is the decimal date on the x-axis) and represents baseline values of TOC stocks between 100 and 250 m (see text for further explanation). Table 1 Yearly maximum winter time mixed-layer depth (MLD), TOC export (to '100 m), seasonal drawdown in oxygen stocks (100}250 m), annual oxygen utilization rate (OUR; 100}250 m), and the molar ratio of TOC export and OUR. C : O -C is calculated with delta oxygen expressed in carbon equivalents, assuming an RQ of 0.72 (Anderson, 1995). See text for full explanations of the data Year MLD (m) TOC export Seasonal O OUR Estimate Molar ratio C : O -C (mol C m\ yr\) stocks mol C m\ mol O m\ yr\ C : O 1992 290 1.2 2.3 3.5 0.34 0.47 1993 256 0.9 2.3 3.5 0.26 0.36 1994 318 * * * * * 1995 263 1.4 2.0 3.0 0.47 0.64 1996 213 0.7 2.2 3.3 0.21 0.29 1997 196 0.6 2.3 3.5 0.17 0.24 1998 179 0.4 * * * * MLD observed during the passage of a sub-mesoscale eddy. This feature was not included in the remainder of seasonal DOM dynamics. was the maximum depth to which surface accumulated TOC was exported that year by non- di!usive processes. There was a small interannual increase in the late summer/fall TOC stock at 100}250 m, from a mean of +7.8 mol C m\ prior to 1995 winter overturn to +8.1 mol C m\ prior to the 1998
1658 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 winter overturn (Fig. 5b). The slope of the regression of the late summer/fall minimum TOC stock vs. time was TOC"0.1(x)!1.7 (R"0.77), where x is the decimal year found on the x-axis of Fig. 5b. The baseline TOC stock between 100 and 250 m, estimated from this regression, is depicted by the dashed line in Fig. 5b. Export from the upper 100 m is equal to the increase in TOC stock between 100 and 250 m, calculated as the di!erence between the baseline TOC value and the maximum TOC stock in the 100}250 m depth interval during or just following winter overturn (Fig. 5b). TOC export ranged from 0.9 to 1.4 mol C m\ in the years 1992, 1993 (data for 1992 and 1993 taken from Carlson et al., 1994) and 1995, and decreased to a range of 0.4}0.7 mol C m\ during 1996}1998 (Table 1). The total export of TOC varied with the maximum MLD during each overturn period (Fig. 6). The range in winter maximum MLD of 180}290 m (excluding 1994) corresponded to a four-fold range in export (0.4}1.4 mol C m\). The material exported to '100 m during an overturn event is of two sources. First, to be mixed down at the onset of the overturn event is accumulated TOC present in the surface layer at the end of each autumn season (Fig. 1a; referred to here as resident TOC). Second, the TOC freshly produced in the course of the overturn event is also mixed downward ( fresh TOC). The amount of resident TOC mixed down each year was calculated, following Carlson et al. (1994), according to the following: We selected the TOC pro"le immediately prior to deep overturn, de"ned as that existing when the MLD was still (100 m. The TOC stock from this pro"le, integrated to the maximum MLD from the subsequent overturn period, was normalized to the depth of the MLD to determine a mean resident TOC concentration after overturn. We determined the resulting TOC stocks in the 0}100 and the 100}250 m layers resulting from this simulated mixing event. These estimates re#ect the residual concentrations resulting from physical mixing, in which the surface- layer TOC was diluted and the deep layer enriched. For example, if the 14.5 mol TOC m\ found in Fig. 6. Relationship between annual TOC export by turbulent mixing and mixed-layer depth. Open symbols represent total TOC export during convective overturn of the water column. Solid symbols represent the export of TOC characterized as resident TOC (see text). The di!erence between the two regression lines (shaded gray) represents the export of fresh TOC. The deeper the maximum winter MLD, the greater the contribution of fresh TOC to annual TOC export.
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1659 late autumn 1995 was redistributed homogeneously over 213 m (the maximum MLD of the 1996 winter overturn) then the 0}100 m layer would decrease from 6.4 to 5.9 mol TOC m\ and the 100}250 m layer would increase from 8.1 to 8.6 mol TOC m\. The resident TOC export is the di!erence between 8.6 mol C m\ and the baseline TOC stock (Fig. 5b) present in the 100}250 m layer. The resident TOC export was then compared to the measured total export during the 1996 overturn period, and the di!erence was assigned to fresh TOC export (gray area in Fig. 6). TOC stocks in the surface layer at the end of summer were relatively constant from year to year (Fig. 1a), so the amount of this material exported each year depended largely on the depth of mixing to '100 m (Fig. 6). The deeper the mixing the more resident TOC delivered to depth. Fresh TOC was exported only after a threshold maximum winter MLD of +200 m was reached (Fig. 6). This condition exists because the threshold depth must be exceeded in order to have signi"cant net TOC production (Figs. 3a and 5a). The more the maximum winter MLD exceeded 200 m, the greater the net production and export of fresh TOC. Increasingly deeper winter mixing stimulates progress- ively larger spring blooms, which in turn generate larger amounts of fresh TOC. Because the maximum winter MLD must reach '200 m before fresh TOC export is measurable, the percent- age contribution of resident TOC to total TOC export (resident plus fresh pools) varied widely. When the maximum winter MLD was shallow ((200 m), resident TOC export accounted for essentially all of the carbon exported by overturn (Fig. 6). When the MLD was at its greatest, export of resident TOC contributed as little as half of the total. 3.4. Mineralization of exported TOC TOC delivered to depth during winter overturn begins to disappear at the onset of restrati"ca- tion. In this analysis we assume that the loss of TOC in the 100}250 m layer is due to biological remineralization, although horizontal advection cannot be ruled out. To estimate the "rst-order decay constant (Lehninger, 1975) for the seasonally exported TOC pool, the following steps were taken. The initial time point for estimating the decay constant each year was taken as the sampling date when the winter maximum TOC stock at 100}250 m was found. It was assumed that TOC on that date was uniformly mixed throughout the MLD. The TOC stock (mmol m\) from 100 m to the MLD was calculated, and then the depth weighted mean TOC concentration for that zone determined ("TOC/z; where integration is over depth z). Data from succeeding visits to the site were treated similarly, with the depth-normalized TOC concentrations determined for the same depth interval (100 m to the MLD found during the initial time point). The decay constant for each year was calculated from the seasonal change in the TOC concentration, from the period of maximum concentration to the asymptotic value at time t. The constants determined are applicable only to the TOC exported with the overturn event. Values of the decay constant k varied by 15-fold, decreasing from 0.003 d\ in 1995 to 0.0002 d\ in 1998 (Table 2). The years experiencing relatively low maximum mixed-layer depths and reduced TOC export had the lowest k values, while years with deep mixed layers and elevated TOC export had the highest values. The amount of TOC consumed ranged from 0.9 to 7.3 M C (Table 2), also varying with the maximum winter MLD (Table 1). The deepest MLD produced the largest TOC, likely because of the greater contribution of fresh TOC mixed to '100 m when the MLD was deep. The time required for exported TOC to mineralize to the seasonal asymptote value varied from 40 to 98 d, with longer decay periods associated with the shallower winter maximum MLD.
1660 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 Table 2 First-order decay constants (k) of TOC exported into the 100}250 m layer. TOC represents the seasonal amplitude of the depth normalized TOC within the 100}250 m layer. Decay period represents the length of time it took for exported TOC to be removed to asymptotic values. The value for k was calculated by the following formula: k"(2.303/t) log (A /A ) where A is the initial TOC concentration, A is the "nal TOC concentration and t is the decay period Year TOC (M C) Decay period (days) k 1995 7.3 40 !0.0030 1996 5.3 66 !0.0010 1997 3.3 98 !0.0006 1998 0.9 78 !0.0002 While there was little vertical variability in TOC concentrations from 100 m to the bottom of the MLD at time zero each year, vertical gradients did develop with time past that point. The development of gradients suggests that diapycnal mixing introduced additional TOC to the top of the de"ned box and diluted TOC at the bottom of the box. Corrections were not made for these mixing terms on concentrations, nor were corrections possible for horizontal removal of the signals. 3.5. Contribution of TOC export to oxygen utilization TOC exported to depth during winter overturn is mineralized, thereby contributing to oxygen consumption in the subsurface layers. The goal here was to estimate the contribution of exported TOC to annual oxygen utilization rates (OUR) in the 100}250 m depth layer. We assumed that all of the exported TOC was mineralized over the same time scale as OUR development since TOC stocks in the 100}250 m depth zone generally returned to near initial values after the winter pulse of TOC. We "rst estimated the seasonal decrease in oxygen stocks between the maximum value found during the winter overturn period and the asymptotic value found in late summer (Table 1). The seasonal OUR values were extrapolated to the full year using a 1.5 multiplier, following Jenkins and Goldman (1985), since ventilation masks oxygen consumption during the winter months. The seasonal amplitudes in subsurface TOC stocks (i.e., the TOC exported to depths of 100}250 m; Fig. 5b) were then compared to annual OUR. TOC export covaried with the maximum winter MLD (varying by a factor of 3.5), but OUR did not follow that trend. OUR varied by only 0.5 mol m\ yr\, from a low of 3.0 mol m\ yr\ in 1995 to 3.5 mol m\ yr\ in 1992, 1993, and 1997 (Table 1). The C : O molar ratio ranged from 0.17 (when TOC export was low) to 0.47 (when TOC export was high). The contribution of exported TOC to the annual consumption of oxygen (in carbon equivalents; Table 1) between 100 and 250 m ranged from 24% (low TOC export year, 1997) to 64% (high TOC export year, 1995). We also need to determine the contribution of exported TOC to the total annual OUR. Above we assessed oxygen utilization in the 100}250 m box, but oxygen is consumed at greater depths as well, beyond the depth of TOC mixing. Jenkins and Goldman (1985) reported an OUR of 4.1 mol m\ yr\ between 100 and 400 m. Their total OUR is underestimated by 36% (reducing it to 2.6 mol m\ yr\) if their data only from the 100}250 m box are used. It follows that the OUR
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1661 values we calculated from 100 to 250 m underestimate the 100}400 m annual total by a similar amount. OUR, range from 3.0 to 3.5 mol m\ yr\ in the 100}250 m box, scales up to 4.7}5.5 mol m\ yr\ in the 100}400 m box. Given these corrections, the contribution of exported TOC to the total annual consumption of oxygen (in carbon equivalents) at 100}400 m ranged from 15% (low TOC export year, 1997) to 41% (high TOC export year, 1995). It should be noted that our original intent in this last calculation was to directly estimate OUR for the same 100}400 m depth zone as Jenkins and Goldman (1985). We found that the seasonal changes in oxygen stocks in that depth interval were far too inconclusive for such an estimate to be made for individual years of our time series. Instead we focused on the 100}250 m depth range where seasonality was more evident. Jenkins and Goldman (1985) had used a 10-yr climatology in their evaluation, so uncertainties in using single-year data were obscured. An evaluation of a multi-year mean seasonal amplitude of oxygen (as employed by Jenkins and Goldman, 1985) and TOC cannot be performed for the time series reported here because of the wide range in maximum winter MLDs and associated variability in TOC export. 4. Discussion 4.1. Dynamics of TOC Coincident to the deepening of the mixed layer, entrainment of nutrients into the euphotic zone, and the subsequent phytoplankton bloom, seasonally elevated stocks of TOC and DOC have been observed in the vicinity of BATS (Carlson et al., 1994, 1998; Hansell and Carlson, 1998b). The net production of TOC and DOC during or shortly following spring phytoplankton blooms have been demonstrated elsewhere (Duursma, 1963; Parsons et al., 1970; Ittekkot et al., 1981; Eberlein et al., 1985; CadeH e, 1986; Copin-MonteH gut and Avril, 1993; Doval et al., 1997). The accumulated organic matter is carbon rich, with C : N molar ratios ranging from 13 to 15 : 1, supporting earlier speculation of a carbon-rich organic pool (Sambrotto et al., 1993; Williams, 1995). The export of this organic matter by vertical mixing is recognized as an important component of the biological pump in some temperate and subtropical systems (Copin-MonteH gut and Avril, 1993; Carlson et al., 1994; Ducklow et al., 1995; Doval and Hansell, 2000). Carlson et al. (1994) speculated that the magnitude of seasonal DOC accumulation and export out of the euphotic zone was related to the intensity of the winter convective overturn in the Sargasso Sea. The data reported here support this idea by demonstrating a large degree of interannual variability in the net production of TOC, which in turn covaried with the maximum winter MLD. Mixing must reach the nutricline water before net TOC production during a spring bloom becomes signi"cant. The greater the mixing past the threshold depth of +200 m, the more export of newly produced TOC to depths '100 m (Fig 5). During 1995, for example, net buildup of TOC was high ('1.5 mol C m\) during the winter overturn period, with a maximum MLD of 263 m. From 1996 onward, with maximum winter MLDs of 179}213 m, net TOC production each winter was small ()0.7 mol C m\). The relative e!ects of shallow and deep maximum winter MLD on various biogeochemical processes involving TOC are listed in Table 3. During years of shallow winter mixing ((200 m), net TOC production, TOC export and the decay constant of exported TOC are low, while the
1662 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 Table 3 Relative e!ects of interannual variability in the maximum winter mixed-layer depth (MLD) on various biogeochemical processes involving TOC Maximum MLD E!ects Shallow ((200 m) 1. Net TOC production during spring bloom is small 2. Lowest winter time TOC concentration at surface is elevated 3. Summer stock of TOC is elevated 4. Resident TOC export during winter to '100 m moderate 5. Fresh TOC export during winter to '100 m depth is nil 6. Decay constant of exported TOC is low 7. Decay period of exported TOC is long 8. Contribution of exported TOC to annual OUR is low Deep ('200 m) 1. Net TOC production during spring bloom is elevated 2. Lowest winter time TOC concentration at surface is low 3. Summer stock of TOC is reduced 4. Resident TOC export during winter to '100 m increased 5. Fresh TOC export during winter to '100 m elevated 6. Decay constant of exported TOC is high 7. Decay period of exported TOC is short 8. Contribution of exported TOC to annual OUR is high decay period is lengthened. This follows from the reduced input of nutrients to the surface layer and the related reduced input of freshly produced TOC into the zones of export. Also, the winter minimum and summer maximum concentrations of TOC are relatively elevated. During years of deep mixing ('200 m), net TOC production, export and decay constants are elevated. Both the winter minimum and summer maximum stocks of TOC are reduced, due to entrainment of nutrient-rich, TOC-depleted water from depth. Each year in the surface 40 m, a small build up in the surface TOC concentration was observed coincident with the shoaling of the MLD. Net production of TOC is a result of the e!ective uncoupling of TOC consumption from production that occurs during or shortly after elevated rates of primary production. The increase in TOC stock in the surface 40 m must result from continued TOC production during the bloom, coincident with decreasing vertical mixing through shoaling of the MLD. While TOC stocks increase during deep mixing events ('200 m), surface water concentrations change little as a result of dilution from mixing. As the depth of mixing shallows and TOC production remains elevated, TOC accumulation becomes focused in the upper water column. A graphic depicting this process is shown in Fig. 7. After the water column becomes fully strati"ed by the end of May or early June there is no further net production of TOC in the surface waters (Fig. 4). The lack of net TOC production or consumption during summer suggests a tight coupling of the processes, but the mechanisms controlling the balance are not known. It is likely that as primary production decreases during summer the rate of semi-labile TOC production is also reduced. Perhaps photo-decomposition of a portion of the semi-labile or refractory pool (Kieber et al., 1989), and the subsequent removal by bacterioplankton (Wetzel et al., 1995; Herndl et al., 1997), o!sets the slow summertime production of recalcitrant TOC.
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 1663 Fig. 7. Schematic depiction of the e!ect of water column restrati"cation on TOC concentrations in the upper 40 m. During deep mixing freshly produced TOC is mixed to depth, resulting in little accumulation in the surface 40 m. As the MLD shoals (indicated by shoaling of the thin arrows indicating mixing) and TOC production remains elevated, TOC is concentrated in the surface waters (as indicated by variable gray scale). The large vertical arrows represent TOC export from surface 40 m. 4.2. TOC mineralization and oxygen consumption The molar ratios of organic carbon oxidation and oxygen consumption in the subsurface waters at the BATS site (0.17}0.47) are similar to the ratios of 0.15}0.34 found in the western South Paci"c (Doval and Hansell, 2000) and of 0.23 in the North Paci"c (Ogura, 1970). Both these latter estimates were made on isopycnal surfaces, lending credence to the results. The contribution of exported TOC to the total annual consumption of oxygen at 100}400 m ranged from 15% (1997) to 41% (1995). This range supports the earlier estimates by Carlson et al. (1994) from the Sargasso Sea of 23}42% in 1992 and 1993. 4.3. Total organic nitrogen The seasonal ranges in surface-layer TON concentrations were very small, generally not exceeding the analytical variability of the analysis. The absence of seasonal accumulation, parti- cularly during the summer months, provides insight on the recently proposed role of N "xation in the local nitrogen budget. Calculations of annual rates of N "xation in the North Atlantic suggest rates of 20}61;10 mol N yr\ (Michaels et al., 1996; Gruber and Sarmiento, 1997). Michaels et al. (1996) suggested that N "xation would likely be concentrated during the summer months in the western Sargasso Sea. It is during the summer that an unexplained 3 mol m\ drawdown of the surface-layer inorganic carbon pool takes place (Michaels et al., 1994); that the water column is particularly stable and warm, thereby favoring the most abundant diazotroph Trichodesmium (Capone et al., 1997); and that the atmospheric input of iron, a limiting element for N "xation, is highest (Prospero et al., 1996). The areal rate of N "xation in the North Atlantic calculated by Gruber and Sarmiento (1997) is 0.072 mol N m\ yr\. If this production takes place during 3 months of summer, and most of the
1664 D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667 newly "xed nitrogen accumulates in the surface layer during this period, then the mean TON concentration increase over the normal mixed-layer depth of 25 m would be 3 M N. At the BATS site, however, PON concentrations are generally no more than 0.3}0.4 M in the late summer (with no sign of increase over the summer period), and the summer time background TON concentration of 4}5 M does not change. These are not the expected "ndings if N "xation is a dominant local process. Karl et al. (1992) reported '3000-fold increase in particulate nitrogen and a 3.1-fold increase in DON in the presence of a Trichodesmium bloom near Station Aloha in the North Paci"c. Since we found no substantive summer time increases in TON, N "xation may not be as important as proposed at the BATS site during summer. If N "xation is responsible for elevated N : P ratios in the main thermocline of the Sargasso Sea, then the process must take place south of Bermuda and the signal transported north with the Gulf Stream system. 5. Summary (1) Variability in TOC stocks in the Sargasso Sea is largely driven by variability in physical forcing and its impact on biological processes. The maximum depth of mixing during the winter overturn period appears to be particularly important. The greater the depth of mixing, the greater the net production of TOC and the greater its export to depth. During years undergoing mixing to (200 m there was little net production of TOC. TOC export increased with increasing maximum depth of mixing past 200 m. (2) TOC stocks in the western Sargasso Sea are relatively invariant over the summer periods, indicating that net TOC production during this very oligotrophic period has ceased. This "nding indicates that nutrient depletion alone is not the causative agent for elevated rates of net TOC production. (3) Because vertical mixing controlled the export of TOC, so too did it control the contribution of exported TOC to oxygen utilization in the subeuphotic zone. Exported TOC supported oxygen utilization at C : O molar ratios ranging from 0.17 when TOC export was low to 0.47 when it was high. The amount of TOC export also in#uenced the exported TOC decay rates, with the lowest rates accompanying the lowest export. (4) There was little seasonality in the TON signal at the BATS site. TON did not accumulate during the summer months when N "xation would be expected to be at a seasonal maximum. Given the recently published suggestions that N "xation contributes greatly to export #ux in the Sargasso Sea, the "ndings at the BATS site were surprising. The results suggest that N "xation must be prevalent at sites in the North Atlantic other than near Bermuda. The region south of Bermuda must be evaluated for it's possible contribution to nitrogen cycling in the Sargasso Sea via N "xation. Acknowledgements We thank Paula Hansell, Rachel Parsons, Amy Ritchie, Catherine Adams and Heike Lueger for analyses of organic carbon and nitrogen reported in this paper. The many sta! and scientists working in the BATS program are recognized with thanks and appreciation for their collection of
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