Biogeochemistry of total organic carbon and nitrogen in the Sargasso Sea: control by convective overturn

Page created by Julia Chan
 
CONTINUE READING
Biogeochemistry of total organic carbon and nitrogen in the Sargasso Sea: control by convective overturn
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
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667                       1665

samples over the several years these data represent. The o$cers and crew of the RV Weatherbird II
were instrumental in the success of this program. Support for DAH was provided by NSF
OCE9726091 and for CAC by NSF OCE 9617795 and OCE 9619222. This manuscript is BBSR
Contribution C1556 and C549 to the US JGOFS program.

References

Aluwihare, L.I., Repeta, D.J., Chen, R.F., 1997. A major biopolymeric component to dissolved organic carbon in surface
   seawater. Nature 387, 166}169.
Amon, R.M.W., Benner, R., 1994. Rapid cycling of high-molecular weight dissolved organic matter in the ocean. Nature
   369, 549}552.
Anderson, L.A., 1995. On the hydrogen and oxygen content of marine phytoplankton. Deep-Sea Research I 42,
   1675}1680.
Bauer, J.E., Williams, P.M., Dru!el, E.R.M., 1992. C activity of dissolved organic carbon fractions in the northcentral
   Paci"c and Sargasso Sea. Nature 357, 667}670.
Benner, R., Pakulski, J.D., McCarthy, M., Hedges, J.I., Hatcher, P.G., 1992. Bulk chemical characterization of dissolved
   organic matter in the ocean. Science 255, 1561}1564.
Borsheim, K.Y., Myklestad, S.M., 1997. Dynamics of DOC in the Norwegian Sea inferred from monthly pro"les collected
   during 3 years at 663N, 23E. Deep-Sea Research I 44, 593}601.
Bronk, D.A., Glibert, P.M., Ward, B.B., 1994. Nitrogen uptake, dissolved organic nitrogen release, and new production.
   Science 265, 1843}1846.
CadeH e, G.C., 1986. Organic carbon in the water column and its sedimentation, Fladen ground (North Sea), May 1983.
   Netherlands Journal of Sea Research 20, 347}358.
Capone, D.G., Zehr, J.P., Paerl, H.W., Bergman, B., Carpenter, E.J., 1997. Trichodesmium, a globally signi"cant marine
   cyanobacterium. Science 276, 1221}1229.
Carlson, C.A., Bates, N.R., Ducklow, H.W., Hansell, D.A., 1999. Estimations of bacterial respiration and growth
   e$ciencies in the Ross Sea, Antarctica. Aquatic Microbial Ecology 19, 229}244.
Carlson, C.A., Ducklow, H.W., 1995. Dissolved organic carbon in the upper ocean of the central Equatorial Paci"c, 1992:
   Daily and "nescale vertical variations. Deep-Sea Research II 42, 639}656.
Carlson, C.A., Ducklow, H.W., 1996. Growth of bacterioplankton and consumption of dissolved organic carbon in the
   Sargasso Sea. Aquatic Microbial Ecology 10, 69}85.
Carlson, C.A., Ducklow, H.W., Hansell, D.A., Smith, W.O., 1998. Organic carbon partitioning during spring phytoplan-
   kton blooms in the Ross Sea Polynya and the Sargasso Sea. Limnology and Oceanography 43, 375}386.
Carlson, C.A., Ducklow, H.W., Michaels, A.F., 1994. Annual #ux of dissolved organic carbon from the euphotic zone in
   the Northwestern Sargasso Sea. Nature 371, 405}408.
Cherrier, J., Bauer, J.E., Dru!el, E.R.M., 1996. Utilization and turnover of labile dissolved organic matter by bacterial
   heterotrophs in eastern North Paci"c surface waters. Marine Ecology Progress Series 139, 267}279.
Copin-Montegut, G., Avril, B., 1993. Vertical distribution and temporal variation of dissolved organic carbon in the
   northwestern Mediterranean Sea. Deep-Sea Research I 40, 1963}1972.
Deuser, W.G., 1986. Seasonal and interannual variations in deep-water particle #uxes in the Sargasso Sea and their
   relation to surface hydrography. Deep-Sea Research I 33, 757}766.
Dileep Kumar, M., Rajendran, A., Somasundar, D., Haake, B., Jenisch, A., Shuo, Z., Ittekkot, V., Desai, B.N., 1990.
   Dynamics of dissolved organic carbon in the northwestern Indian Ocean. Marine Chemistry 31, 299}316.
Doval, M.D., Alvarez-Salgado, X.A., PeH rez, F.F., 1997. Dissolved organic matter in a temperate embayment a!ected by
   coastal upwelling. Marine Ecology Progress Series 157, 21}37.
Doval, M., Hansell, D.A., 2000. Organic carbon and apparent oxygen utilization in the western South Paci"c and central
   Indian Oceans. Marine Chemistry 68, 249}264.
Dru!el, E.R.M., Williams, P.M., Suzuki, Y., 1989. Concentrations and radiocarbon signatures of dissolved organic
   matter in the Paci"c Ocean. Geophysical Research Letters 16, 991}994.
1666                    D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667

Ducklow, H.W., Carlson, C.A., Bates, N.R., Knap, A.H., Michaels, A.F., 1995. Dissolved organic carbon as a component
    of the biological pump in the North Atlantic Ocean. Philosophical Transactions of the Royal Society, Series A 348,
    161}167.
Duursma, E.K., 1963. The production of dissolved organic matter in the sea, as related to the primary gross production of
    organic matter. Netherlands Journal of Sea Research 2, 85}94.
Eberlein, K., Leal, M.T., Hammer, K.D., Hickel, W., 1985. Dissolved organic substances during a Phaeocystis pouchetii
    bloom in the German Bight (North Sea). Marine Biology 89, 311}316.
Gruber, N., Sarmiento, J.L., 1997. Global patterns of marine nitrogen "xation and denitri"cation. Global Biogeochemi-
    cal Cycles 11, 235}266.
Guo, L., Coleman, C.H., Santchii, P.H., 1994. The distribution of colloidal and dissolved organic carbon in the Gulf of
    Mexico. Marine Chemistry 45, 105}119.
Hansell, D.A., 1993. Results and observations from the measurement of DOC and DON using high temperature catalytic
    combustion techniques. Marine Chemistry 41, 195}202.
Hansell, D.A., Bates, N.R., Carlson, C.A., 1997a. Predominantly vertical losses of carbon from the surface layer of the
    Equatorial Paci"c Ocean. Nature 386, 59}61.
Hansell, D.A., Bates, N.R., Gundersen, K., 1995. Mineralization of dissolved organic carbon in the Sargasso Sea. Marine
    Chemistry 51, 201}212.
Hansell, D.A., Carlson, C.A., 1998a. Deep ocean gradients in dissolved organic carbon concentrations. Nature 395,
    263}266.
Hansell, D.A., Carlson, C.A., 1998b. Net community production of dissolved organic carbon. Global Biogeochemical
    Cycles 12, 443}453.
Hansell, D.A., Carlson, C.A., Bates, N.R., Poisson, A., 1997b. Horizontal and vertical removal of organic carbon in the
    equatorial Paci"c Ocean: a mass balance assessment. Deep-Sea Research II 44, 2115}2130.
Hansell, D.A., Peltzer, E.T., 1998. Spatial and temporal variations of total organic carbon in the Arabian Sea. Deep-Sea
    Research II 45, 2171}2193.
Hansell, D.A., Waterhouse, T.Y., 1997. Controls on the distribution of organic carbon and nitrogen in the eastern Paci"c
    Ocean. Deep-Sea Research I 44, 843}857.
Herndl, G.J., Brugger, A., Hager, S., Kaiser, E., Obernosterer, I., Reitner, B., Slezak, D., 1997. Role of
    ultraviolet-B radiation on bacterioplankton and the availability of dissolved organic matter. Plant Ecology 128,
    42}51.
Ittekkot, V., Brockmann, U., Michaelis, W., Degens, E.T., 1981. Dissolved free and combined carbohydrates during
    a phytoplankton bloom in the northern North Sea. Marine Ecology Progress Series 4, 299}305.
Jenkins, W.J., Goldman, J.C., 1985. Seasonal oxygen cycling and primary production in the Sargasso Sea. Journal of
    Marine Research 43, 465}491.
Karl, D.M., Letelier, R., Hebel, D., Bird, D.V., Winn, C.D., 1992. Trichodesmium blooms and new production in the North
    Paci"c gyre. In: Carpenter, E.J., et al. (Eds.), Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs.
    Kluwer Academic Publishers, Netherlands, pp. 219}237.
Kieber, D.J., McDaniel, J., Mopper, K., 1989. Photochemical source of biological substrates in seawater: implications for
    carbon cycling. Nature 341, 637}639.
Knap, A.H., Michaels, A.F., Steinberg, D., Bahr, F., Bates, N.R., Bell, S., Countway, P., Close, A., Doyle, A., Howse, F.,
    Gundersen, K., Johnson, R., Little, R., Orcutt, K., Parsons, R., Rathbun, C., Sanderson, M., Stone, S., 1997. BATS
    methods manual. US JGOFS Planning O$ce, Woods Hole.
Lehninger, A.L., 1975. Biochemistry. 2nd Edition. Worth Publishers, Inc., New York, 1104pp.
Lipschultz, F., 2001. A time-series assessment of the nitrogen cycle at BATS. Deep-Sea Research II 48, 1897}1924.
McCarthy, M., Hedges, J.I., Benner, R., 1996. Major biochemical composition of dissolved high molecular weight organic
    matter in seawater. Marine Chemistry 55, 281}297.
Michaels, A.F., Knap, A.H., 1996. Overview of the US JGOFS Bermuda Atlantic Time-series Study and Hydrostation
    S programs. Deep-Sea Research II 43, 157}198.
Michaels, A.F., Knap, A.H., Dow, R.L, Gundersen, K., Johnson, R.J., Sorensen, J., Close, A., Knauer, G.A., Lohrenz, S.E.,
    Asper, V.A., Tuel, M., Bidigare, R., 1994. Seasonal patterns of ocean biogeochemistry at the US JGOFS Bermuda
    Atlantic Time-series Study site. Deep-Sea Research I 41, 1013}1038.
D.A. Hansell, C.A. Carlson / Deep-Sea Research II 48 (2001) 1649}1667                         1667

Michaels, A.F., Olson, D., Sarmiento, J.L., Ammerman, J.W., Fanning, K., Jahnke, R., Knap, A.H., Lipschultz, F.,
   Prospero, J.M., 1996. Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic
   Ocean. Biogeochemistry 36, 181}226.
Ogura, N., 1970. The relation between dissolved organic carbon and apparent oxygen utilization in the Western North
   Paci"c. Deep-Sea Research 17, 221}231.
Opsahl, S., Benner, R., 1997. Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 386,
   480}482.
Parsons, T.R., LeBrasseur, R.J., Barraclough, W.E., 1970. Levels of production in the pelagic environment of the Strait of
   Georgia, British Columbia: a review. Journal of the Fisheries Research Board of Canada 27, 1251}1264.
Peltzer, E.T., Hayward, N.A., 1996. Spatial distribution and temporal variability of total organic carbon along 1403W in
   the equatorial Paci"c Ocean in 1992. Deep-Sea Research II 43, 1155}1180.
Prospero, J.M., Barrett, K., Church, T., Dentner, F., Duce, R.A., Galloway, J.N., Levy II, H., Moody, J., Quinn, P., 1996.
   Atmospheric deposition of nutrients to the North Atlantic Basin. Biogeochemistry 35, 27}73.
Sambrotto, R.N., Savidge, G., Robinson, C., Boyd, P., Takahashi, T., Karl, D.M., Langdon, C., Chipman, D., Marra, J.,
   Codispoti, L., 1993. Elevated consumption of carbon relative to nitrogen in the surface ocean. Nature 363, 248}250.
Sprintall, J., Tomczak, M., 1992. Evidence of the barrier layer in the surface layer of the tropics. Journal of Geophysical
   Research 97, 7305}7316.
Steinberg, D. K., Carlson, C.A., Bates, N.R., Johnson, R.J, Michaels, A.F., Knap, A.H., 2001. Overview of the US JGOFS
   Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep-Sea
   Research II 48, 1405}1447.
Walsh, T.W., 1989. Total dissolved nitrogen in seawater: a new-high-temperature combustion method and a comparison
   with photo-oxidation. Marine Chemistry 26, 295}311.
Wetzel, R.G., Hatcher, P.G., Bianchi, T.S., 1995. Natural photolysis by ultraviolet irradiance of recalcitrant dissolved
   organic matter to simple substrates for rapid bacterial metabolism. Limnology and Oceanography 40, 1369}1380.
Williams, P.J.leB., 1995. Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale in
   comparison with changes in particulate material and the consequential e!ect on net C/N assimilation ratios. Marine
   Chemistry 51, 17}29.
Williams, P.M., Dru!el, E.R.M., 1987. Radiocarbon in dissolved organic matter in the central North Paci"c Ocean.
   Nature 330, 246}248.
Winkler, W.L., 1888. Di Bestimmund des in Wasser geloK sten Sauersto!en. Berichte der Duetschen Chemischen
   Gesellschaft 21, 2843}2855.
Zhang, J., Quay, P.D., 1997. The total organic carbon export rate based on C and C of DIC budgets in the equatorial
   Paci"c region. Deep-Sea Research II 44, 2163}2190.
Zweifel, U.L., Norrman, B., Hagstroem, A., 1993. Consumption of dissolved organic carbon by marine bacteria and
   demand for inorganic nutrients. Marine Ecology Progress Series 101, 23}32.
You can also read