ARTICLE IN PRESS
Deep-Sea Research II 53 (2006) 1649–1665
www.elsevier.com/locate/dsr2
Concentrations and uptake of nitrate and ammonium in the
Atlantic Ocean between 60N and 50 S
Andrew P. Rees, E. Malcolm S. Woodward, Ian Joint
Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, PL1 3DH, UK
Received 28 October 2005; received in revised form 22 February 2006; accepted 18 May 2006
Available online 2 August 2006
Abstract
The uptake rates and concentrations of nitrate and ammonium were determined during three research cruises in the
Atlantic Ocean: At 20 W between 60 N and 37 N during June and July 1996, between the UK and Falkland Islands
ð48 N250 SÞ during September and October 1997, and between South Africa and the UK ð33 S248 NÞ during May and
1
June 1998. Euphotic zone concentrations of NO
in the northern and southern gyres to a
3 varied between 0:005 mmol l
maximum of 33 mmol l1 within the Benguela upwelling system. At 70% of stations occupied in oligotrophic conditions
1
(nominally defined as where NO
3 o0:05 mmol l ), surface elevations of NO3 were attributed to the photoinhibition of
þ
uptake mechanisms. NH4 concentrations were much less variable ð0:109 0:150 mmol l1 Þ than NO
3 , and showed the
same general trend of minima within the gyres and maximum concentration (of 5:2 mmol l1 ) in the Benguela upwelling
þ
system. The microbial uptake of NO
3 was significantly correlated to NO3 and chlorophyll concentrations, whilst NH4
þ
uptake was less dependent on NH4 concentration and showed no association with other environmental variables.
Variability in the nitrogen uptake:concentration ratio between oceanographic provinces was associated with physical
conditions including the mixed-layer depth and the rate of diapycnal mixing; therefore, uptake rates cannot be predicted
simply from the nutrient concentration. In contrast, the relationship between f-ratio (where the NO
3 source is undefined,
and may have both new and regenerated components) and NO
concentration
is
defined
robustly,
so
that the f-ratio can
3
be predicted (within 95%) by either surface or depth integrated concentrations of NO
3.
r 2006 Elsevier Ltd. All rights reserved.
Keywords: Nitrate; Ammonium; Uptake; Atlantic Ocean; 60 N250 S; 58 W218 E
1. Introduction
All organisms require nitrogen in stoichiometric
proportions to carbon and other essential elements
for balanced growth (Capone, 2000). In the marine
environment the supply of nitrogen to phytoplankton is largely through the uptake of nitrate (NO
3)
and ammonium (NHþ
4 ), although dissolved organic
Corresponding author. Fax: +44 1752 633101.
E-mail address: [email protected] (A.P. Rees).
0967-0645/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2006.05.008
nitrogen (DON) and dissolved di-atomic N2 often
contribute significantly to microbial nutrition, and
it is becoming apparent that their roles are greater
than was previously recognised (e.g., Zubkov et al.,
2003 and Capone, 2001, respectively). During this
study we restrict our focus to the rates of NO
3 and
þ
NHþ
4 uptake and NH4 oxidation relative to their
ambient concentrations. The mechanisms of supply
and of uptake differ for both substrates. The
traditional conceptual view of these two nutrients
has been as regenerated (NHþ
4 ) and new (NO3 )
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
nitrogen sources as defined by Dugdale and Goering
(1967). This followed from the view that the
dominant supply of NHþ
4 to phytoplankton was
recycled or regenerated within the euphotic zone
and that NO
3 entered the surface layers as new
nitrogen from the deep ocean following vertical
diffusion across a pycnocline. Dugdale and Goering
recognised several alternative supply pathways of
both nitrogen species and the potential role of
DON, and following extensive work performed
largely under the auspices of the Bermuda Atlantic
Time Series (BATS) and the Hawaii Ocean Time
(HOT) series; the current view of new productivity
has changed to a more complex scenario, which
includes, amongst several other considerations,
atmospheric deposition, nitrogen fixation, eddy
pumping and zooplankton migration (Lipschultz
et al., 2002). Current paradigms of new production
therefore must accommodate a whole suite of
variables that are beyond the scope of this work;
in this paper, we will largely consider the standing
stock and uptake rate of a nutrient rather than
investigate the source or rate of supply.
þ
Interactions between NO
3 and NH4 are complex, and are likely to be defined in some way by
uptake and regeneration mechanisms: NHþ
4 is
assimilated directly, whereas NO
must
first
be
3
reduced to NHþ
;
this
increases
the
energy
require4
ment of cells growing on NO
3 . Phytoplankton cells
with the Redfield C:N ratio of 6.6 require a 25%
greater rate of photosynthetic electron transfer for
growth on NO
than is required for NHþ
3
4supported growth (Geider and MacIntyre, 2002).
In general terms it is considered that NHþ
4 is
preferred as a substrate over NO
3 and that the
presence of NHþ
4 can reduce the rate of NO3 uptake
(e.g., Dortch, 1990), though each of these conceptual ideas is very reliant on relative concentrations,
light availability and indeed phytoplankton community composition.
Previous authors have investigated the concentration dependency of uptake (Harrison et al., 1996;
Rees et al., 1999a) for sections of the northern
Atlantic; Varela et al. (2005) have performed a
comprehensive assessment of the uptake of nitrogen
relative to phytoplankton size along a transect of
the Atlantic that is comparable to this study. Our
aim here is to investigate the relationships existing
between the concentrations, and uptake and regenþ
eration of NO
3 and NH4 by considering data
collected during three meridional transects of the
Atlantic which in total covered 113 of latitude and
sampled the eastern and western boundaries of the
south Atlantic, upwelling regions, temperate waters
and extensive tracks through both north and south
Atlantic sub-tropical gyres.
2. Methods
Data are presented from three temporally and
spatially distinct cruises in the Atlantic Ocean
(Fig. 1). The main focus of this paper is on two of
the cruises that formed a part of the NERC funded
Atlantic Meridional Transect (AMT) programme
(www.pml.ac.uk/amt/) onboard the RRS James
Clark Ross. The first during September and October
1997 (AMT5) was southbound, between Grimsby,
UK and Port Stanley, Falkland Islands; whilst the
second cruise (AMT6) was a northwards transect
between Cape Town, South Africa and Grimsby,
UK in May and June 1998. The third data set
included is from the NERC funded PRIME
cruise (Savidge and Williams, 2001), onboard RRS
60°W
30°W
0°
30°E
60°N
NADR
NAST (E)
30°N
CNRY
WTRA
ETRA
0°
SATL
BENG
30°S
BRAZ
FKLD
60°S
Fig. 1. Location of sampling stations in the Atlantic Ocean
during AMT5 ðÞ, AMT6 ðÞ and PRIME ( ) cruises. Oceanographic provinces according to Longhurst (1998) are indicated.
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
Discovery to the North East Atlantic (60 N237 N
along the 20 W meridian) during June and July
1996.
2.1. Nutrient concentrations
Dissolved inorganic nutrient concentrations were
analysed within 2 h of collection. NO
3 , NO2 and
þ
NH4 were measured with a Technicon segmented
flow colorimetric auto-analyser when concentrations were greater than 0:1 mmol l1 ; the methodologies used were adapted from those of Brewer and
Riley (1965) for NO
3 , Grasshoff (1976) for NO2
þ
and Mantoura and Woodward (1983) for NH4 .
Where NO
3 and NO2 concentrations were at low
nanomolar concentrations, they were analysed by a
chemiluminescence technique, as described by Garside (1982) and Woodward and Owens (1990). Low
nanomolar NHþ
4 concentrations were measured
using a fluorescence analysis method developed
from Jones (1991) as described by Woodward and
Rees (2001).
1651
and 15 N atom% were determined by continuous
flow stable isotope mass spectrometry using techniques described by Barrie et al. (1989) and Owens
and Rees (1989). Rates of uptake were calculated
according to Dugdale and Goering (1967) and when
appropriate were corrected for over addition of 15 N
tracer according to Rees et al. (1999b). Samples
collected for NHþ
4 regeneration determination were
lost and so NHþ
4 uptake rates were corrected for
isotope dilution according to the equations of
Kanda et al. (1987):
x¼
1 þ ð1 bÞ1a
,
ða 1Þb
where x is the ratio of actual and apparent uptake
rates, b is the apparent consumption of NHþ
4 and a
is the ratio of regeneration (R) and uptake (U),
which was estimated from Elskens et al. (1997)
a¼
þ
R
¼ 0:36 102:5½NH4 .
U
2.3. Nitrogen uptake kinetics
2.2. Nitrate and ammonium uptake
NO
3
NHþ
4
Assimilation rates for
and
were
determined following the incorporation of the stable
isotope 15 N. Triplicate samples of water from each
depth sampled were distributed into 640-ml clear
15
polycarbonate bottles and 15 NO
NHþ
3 and
4 were
added ideally at a final concentration of 10%
þ
ambient NO
3 or NH4 concentration; in oligotrophic conditions, the minimum addition was
5 nmol l1 . Incubations were made in an on-deck
incubator. This consisted of a series of tanks with
neutral density and blue filters, which permitted
transmission of ambient irradiance in the range
97%–1% and was maintained at surface seawater
temperature. For all stations on all cruises, shortterm incubations (o4 h) were performed on samples
collected from the depth equivalent to 33% of
surface irradiance, whilst during PRIME and
AMT6 cruises incubations were also made on
samples collected from eight and six depths,
respectively, throughout the euphotic zone (nominally assumed to be from the sea surface to a depth of
1% of surface irradiance) for 24 h (see Donald et al.,
2001; Rees et al., 2001). Incubations were terminated by filtration (o40 cm Hg vacuum) onto ashed
Whatman GF/F filters, which were dried onboard
and stored over silica gel dessicant until return to
the laboratory. Particulate nitrogen concentration
At a number of stations during AMT6, a series of
experiments were performed to allow examination
þ
of the uptake rate kinetics of NO
3 and NH4 .
þ
15
15
NO3 and NH4 were added (at six concentrations ranging from 5 to 120 nmol l1 ) to 640-ml
samples, which were incubated for o4 h in the ondeck incubator under a light screen appropriate to
the depth of collection. Incubations were terminated
by filtration onto GF/F filters and dried prior to
analysis in the laboratory as described above.
2.4. Nitrification
During AMT6, the bacterial oxidation of NHþ
4
was estimated following the incorporation of 14 C in
the dark with and without the nitrification inhibitor—allylthiourea (ATU). The 6 150ml polycarbonate bottles were filled from a number of depths,
which were generally two within, and three below
the euphotic zone. ATU was added to half of the
bottles at a final concentration of 10 mg l1 and
5 mCi NaH14 CO
3 to all bottles. Incubations were
carried out in the dark at the temperature from
which samples were collected for between 6 and 8 h,
and were terminated by filtration onto 0:2mm
polycarbonate filters, which were then stored over
silica gel dessicant prior to analysis in the laboratory
by liquid scintillation counting. To convert carbon
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
1652
incorporation into NHþ
4 oxidation, a factor of
8:3 mol NHþ
oxidised
per mol C fixed (Billen,
4
1976) was used as suggested by Dore and Karl
(1996). This is at the low end of published
conversion factors (8:3242 mol NHþ
4 per mol C)
and is likely to provide a conservative estimate of
the NHþ
4 oxidation rate.
oceanic provinces and conditions sampled. Extremes of conditions in terms of nutrients vary
from the Benguela upwelling system (max
33:0 mmol l1 NO
3 ) through to the North and South
Atlantic oligotrophic gyres, which had typical NO
3
concentrations of o0:01 mmol l1 .
3.1. Nitrate and ammonium concentrations
3. Results
Detailed descriptions of the oceanographic regimes encountered during these cruises and of other
associated research can be found elsewhere (e.g.,
Aiken and Bale, 2000; Savidge and Williams, 2001;
SATL
WTRA
10
20
0.1
0
0
1.0 .32
3.2
0.1
0
1.0
10
10
3.2
10
0.01
0.003
3.2
1.
0
0.03
0.32
-100
0.03
3.2
1
0.0
0
0.1
1.0
0.32 1.0
10
0.0.32
3
0.10
0.003
0.0
NADR
0.01
0.01
-50
Depth (m)
CNRY NAST
T (E)
0.03
0.01
0.03
0.32
3.2
10
0.01
FKLD BRAZ
10
--30
-20
--10
˚S
(B)
BENG
ETRA
1
0.0
1
0.0
3 0.32
0.0
.10
NADR
NAST (E)
-100
0.01
20
20
3.2
10
Depth (m)
40
0.321.0
0
0
10 3.2 1.
-50
CNRY
0.01 0.03
0.10
0.01
30
˚N
Latitude
0
0.03 0.1
0.32 1.0
3.2
10
3.2
10
20
0
0.01
-40
1.
0
-150
0.0
0.30.10 3
2
(A)
0.03
The concentration and uptake of nitrogen have
been determined over very large scales of time and
space, and enormous variability was found in the
1.0
-1
-150
-30
--20
-10
0
˚S
10
Latitude
1
20
30
3.2
0.3
2
20
0.10.03
0
b)
40
˚N
Fig. 2. Contoured profiles of nitrate concentration (mmol l ) for latitudinal transects throughout the Atlantic Ocean during (A) AMT5 in
September–October 1997, and (B) AMT6 in May–June 1998.
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
Robinson et al., 2006). In Fig. 1, the major
oceanographic provinces as defined by Longhurst
(1998) encountered during these cruises are identified relative to the cruise tracks, these are: BENG—
Benguela Current Coastal Province, ETRA—Eastern Tropical Atlantic Province, CNRY—Eastern
(Canary) Coastal Province, NAST(E)—North
Atlantic Tropical Gyral Province (East), NADR—
North Atlantic Drift Province, WTRA—Western
Tropical Atlantic Province, SATL—South Atlantic
Gyral Province, BRAZ—Brazil Current Coastal
Province, and FKLD—Southwest Atlantic Shelves
Province.
NO
3 concentrations (Fig. 2) during both AMT
cruises show similar patterns, with elevated concentrations in the south due to the influence of
vertical mixing due to the confluence of the Falkland and Brazil Currents (14:7 mmol l1 ) in the west
and of the Benguela upwelling
system
(33:0 mmol l1 ) off South Africa in the east. In the
oligotrophic gyres, concentrations of NO
3 are
typically on the order of 0:01 mmol l1 ; it is
interesting to note that concentrations in the
immediate surface are often relatively elevated and
that minimum concentrations occur at sub-surface
depths (Fig. 3). Conditions during the PRIME
cruise were typical of the northeast Atlantic spring
bloom at 60 N, and during the transect south to
37 N showed a progression typical of the development of post-bloom into oligotrophic conditions,
with NO
3 concentrations decreasing from approxi-
NO3 (µmol l-1)
(A)
Depth (m)
0
0.01
0.02
mately 6 mmol l1 at the northern end to
0:005 mmol l1 in the south of the transect (Donald
et al., 2001).
The gross pattern of NHþ
4 distribution is similar
to that of NO
(Fig.
4),
in
that concentrations are
3
highest at the south of AMT5 and AMT6 transects
(max 0.6 and 5.0) in association with the Brazil and
Falklands Currents and the Benguela upwelling
system, respectively, though the range of concentrations is much narrower. For the AMT5 transect
north of 38 S the mean concentration was 0:060 0:037 mmol l1 ð1 s.d.Þ, n ¼ 227. During the AMT6
(north of 15 S) and PRIME cruises, mean concentrations were higher and showed greater variability
(0:109 0:167 mmol l1 , n ¼ 175; and 0:157
0:247; n ¼ 111, respectively). However, it should be
noted that the AMT6 track was selected to
specifically bisect a number of upwelling and high
productivity areas, and conditions in the northern
part of the PRIME cruise were typical of the North
Atlantic post-spring bloom; at a number of stations,
1
elevated NHþ
4 (max 1:54 mmol l ) concentrations
were interpreted as being associated with microbial
activity at the base of the mixed layer (Donald et al.,
2001).
3.2. Nitrate and ammonium uptake kinetics
During AMT6 only, a series of experiments
were performed to determine the kinetic uptake
þ
parameters of microbial NO
3 and NH4 uptake
NO3- (µmol l-1)
(B)
0
1653
0.01
NO3- (µmol l-1)
(C )
0.02
0
0
0
0
10
10
10
20
20
20
30
30
30
40
40
40
50
50
50
60
60
60
0.01
Fig. 3. Near-surface nitrate profiles in oligotrophic waters during (A) AMT5, (B) AMT6 and (C) PRIME cruises.
0.02
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
FKLD BRAZ
SATL
WTRA
0.05
NADR
0.0
5
08
0.
0.
10
0
0.
8
0.0
8
05
0.05
0.05
0.
0.05
0.05
0.05
-100
0.
08
De p th ( m )
NAST (E)
05
0.
0.05
8
0.00.10 0
0.2 0.30
-50
CNRY
0.05
(A)
0.05
1654
-150
-30
-40
-20
-10
°S
(B)
BENG
0
10
CNRY
40
NAST (E)
NADR
0.10
0.50
0.05
0.10
0.05
0.
07
0
0 .1
0.07
7
0.0
Depth (m)
30
°N
Latitude
ETRA
-50
20
-100
-150
b)
-30
-20
-10
0
°S
10
Latitude
20
30
40
°N
1
Fig. 4. Contoured profiles of ammonium concentration (mmol l ) for latitudinal transects throughout the Atlantic ocean during (A)
AMT5 in September–October 1997, and (B) AMT6 in May–June 1998. The isolines south of 20 S in (B) are omitted due to rapid gradients
in concentration associated with the Benguela upwelling system.
(Table 1). These were largely in nutrient-depleted
1
surface waters (NO
3 ¼ 0:00520:036 mmol l ),
though with one experiment performed in the
CNRY waters in the vicinity of the North West
1
African upwelling (NO
3 ¼ 1:48 mmol l ). Maxi
mum uptake rates for NO3 (rmax N ) in oligotrophic
waters were correlated to NO
3 and chlorophyll
concentration, po0:01. Half-saturation parameters
for NO
(K N ) did not correlate significantly
3
ðp40:1Þ to any of the variables tested. In reflection
of the very dynamic nature of the balance between
NHþ
4 supply and demand, the kinetic parameters
for rNHþ
4 appear independent of all variables tested
including ambient NHþ
4 concentration, and in
contrast to the relationship between rNO
3 and
concentration ðr40:97Þ, the relationship between
NHþ
4 uptake and concentration, even under controlled conditions such as these, shows a degree of
variability ðr ¼ 0:5020:99Þ.
3.3. Short-term nitrogen uptake
For all of the stations identified in Fig. 1, a shortterm ðo4 hÞ incubation was performed to determine
þ
NO
3 and NH4 uptake for surface waters. A routine
sampling depth was chosen as 33% of surface
ARTICLE IN PRESS
0.98
—
0.081
—
0.0254
—
0.99
0.97
0.0034
0.0208
0.06
2.00
0.067
0.075
0.96
0.033
0.0111
0.94
0.0028
0.06
0.037
0.57
0.429
0.1392
0.99
0.0674
1.96
1.543
0.74
0.71
0.50
0.99
0.049
0.033
0.019
0.081
0.0160
0.0211
0.0104
0.0259
0.97
—
—
0.97
0.012
—
—
0.035
0.0031
—
—
0.0055
0.25
0.29
0.28
0.31
0.005
0.036
NADR
0.053
0.045
0.008
NAST
0.033
1.480
CNRY
0.327
0.009
0.009
0.006
0.016
ETRA
0.037
0.061
0.046
0.038
K A (mmol l1 )
rmax A
(mmol l1 h1 )
rmax N
(mmol l1 h1 )
K N (mmol l1 )
r
rNHþ
4
rNO
3
Chlorophyll
(mg l1 )
1
[NO
3 ] (mmol l )
1
[NHþ
4 ] (mmol l )
1655
irradiance in order to minimise the potential for
photoinhibition effects. For a number of stations
occupied during AMT6, additional depths were
selected which approximated to 97%, 55% and
33% of incident irradiance to specifically investigate
the elevated nutrient concentrations in the near
surface. Fig. 5 shows data from stations between
11:62 S and 41:07 N. It can be seen that, for 8 out
of 10 profiles the rNO
3 is lower at the shallowest
depth than for deeper samples, and that this effect is
maximal on samples collected from 1 m. For rNHþ
4
the effect is not so obvious, although 6 out of 10
stations displayed minima at the surface with again
the greatest anomaly being observed in samples
collected from 1 m.
Uptake rates varied from undetectable to maxima
þ
of 0.073 and 0:057 mmol l1 h1 for NO
3 and NH4 ,
respectively. For rNO3 , maxima were measured at
the Benguela and North West African upwelling
systems and were associated with high NO
3
concentrations (0:41213:62 mmol l1 ). In the BENG
province the relationship between rNO
3 and NO3
was well described by an exponential relationship
0:4832 NO3
(rNO
, r2 ¼ 0:98). Although
3 ¼ 0:1015e
this relationship is significant, it cannot simply be
transferred to other oceanic provinces with similar
NO
3 concentrations. For example, in the FKLD
province (where NO
ranges from 3.32 to
3
14:12 mmol l1 ) and the Atlantic subarctic at 60 N
(3:7326:70 mmol l1 ), uptake rates reach maxima of
0.006 and 0:007 mmol l1 h1 , respectively. The
þ
relationship between rNHþ
4 and NH4 is even less
clear than for NO3 . Maximum rates were measured
in the northwest African upwelling, at a station
1
where NO
3 was very deplete (0:015 mmol l ) and
þ
NH4 , although elevated over mean concentrations,
was only 0:071 mmol l1 .
3.4. Nitrification
Province
Table 1
Concentration-dependent parameters for the uptake of nitrate and ammonium according to a hyperbolic relationship determined during AMT6, May–June 1998
r
A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
Daily rates have been estimated from the duration of the incubation (6–8 h) in order to allow
direct comparison with NO
3 uptake rates. Olson,
1981 observed linearity in 24-h time course NHþ
4
oxidation experiments, while two time course
experiments performed during this cruise within
the Benguela upwelling system showed linearity
between 4 and 24 h (r2 ¼ 0:80 and 0.88). As has been
found previously (Dore and Karl, 1996; Bianchi et
al., 1999) variability was high; rates 1 standard
error (SE) are shown in Fig. 6, and are calculated by
propagating the SE between replicate samples
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
1656
ρNO3- (µmol l-1 h-1)
(A)
0.000
0
0.001
+
-1 -1
ρNH4 (µmol l h )
(B)
0.002
0.000
0
0.003
5
10
10
0.010
0.015
0.020
Depth (m)
Depth (m)
5
0.005
15
15
20
20
25
25
þ
Fig. 5. Near-surface profiles of nitrate uptake (rNO
3 ) and ammonium uptake (rNH4 ) from oligotrophic waters during AMT6.
Nitrification (µmol l-1 d-1)
(A)
0.00
0
0.05
0.10
0.15
0.20
0.00 0.05 0.10 0.15 0.20 0.25 0.30
0
20
20
40
40
40
60
60
60
80
Depth (m)
20
Depth (m)
Depth (m)
0.00 0.10 0.20 0.30 0.40 0.50
0
-
(C) Nitrification (µmol l-1 d-1), NO2 (µmol l-1)
Nitrification (µmol l-1 d-1)
(B)
80
80
100
100
100
120
120
120
140
140
140
160
0.00
0.05
0.10
-
NO2 (µmol
0.15
l-1)
0.20
160
0.00
160
0.20
-
0.40
0.60
-
l-1)
NO2 ,NH4 (µmol
0.80
0
0.01 0.02 0.03 0.04 0.05
NH4- (µmol l-1)
Fig. 6. Profiles of nitrification rate ðÞ, nitrite concentration ðÞ and ammonium concentration (D) during AMT6 within provinces: (A)
BENG, (B) ETRA and (C) NAST(E). (Error bars on nitrification rate estimates are 1 SE propagated throughout the rate equation.)
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
incubated with and without ATU. In Fig. 6, selected
profiles of nitrification, NHþ
4 and NO2 from the
BENG, ETRA and NAST provinces are presented.
Nitrification rates were generally less than
0:14 mmol l1 d1 . Maximum rates recorded were
0:26 mmol l1 d1 associated with a peak in the NHþ
4
concentration at 75 m in the NAST, and
0:19 mmol l1 d1 at 17 m at a station in the southern
BENG, which was characterised by euphotic depth
1
of 25 m and NO
3 concentration of 14:1 mmol l .
þ
Peaks in NH4 oxidation can be seen to vary with
depth relative to NHþ
4 and NO2 . In Fig. 6A, the
apparent peak coincides with a maxima of NO
2
concentration, in Fig. 6C it coincides with an NHþ
4
maximum, whilst in Fig. 6B maximum nitrification
rate appears just shallower than both NO
2 and
NHþ
peaks.
4
1657
and 60–80 m, creating a nutrient-deplete surface
layer with a nitracline at 50 m; this created a
strong gradient to the base of the euphotic zone
1
(NO
3 46 mmol l l ). As a result, depth-integrated
NO3 uptake rates were of the order of three times
greater at the southern end of the transect compared
to stations occupied further north. There was no
comparable increase in NHþ
4 concentrations or
rNH4 , with the result that maximum f-ratios (where
f-ratio is defined as rNO
3 as a proportion of
þ
rNO
þ
rNH
uptake)
were
recorded in oligo3
4
trophic waters at 37 N.
During AMT6, stations were occupied in each of
the provinces identified in Fig. 1 on at least one
occasion. Table 2 summarises the depth-integrated
þ
concentrations and uptake rates of NO
3 and NH4 ,
for each of the provinces. Maxima of all four
variables were associated with areas of intense
upwelling within the BENG, though it is clear that
each of these provinces is not homogenous in terms
of nutrient distribution and uptake, and each
possesses an inherent variability. So, for example,
the lowest concentration and uptake rates measured
in the BENG are comparable to rates determined in
each of the other provinces. Variability of nitrogen
uptake within provinces can be attributed to a
number of other variables. In Figs. 7A and B, two
stations within upwelling areas (NO
3 ¼ 10:7 and
8:7 mmol l1 ; NHþ
¼
0:5
and
0:4
mmol
l1 at the
4
surface) had mean depth-integrated rates of 9 times
þ
and 11 times greater for NO
3 and NH4 , respectively, than the two stations shown out of the
1
þ
upwelling (NO
3 ¼ 1:0 and 0:3 mmol l ; NH4 ¼
1
0:05 and 0:04 mmol l at the surface). Each of the
stations shown in Figs. 7C and D from within the
NAST(E) have quite different euphotic depths,
ranging from 55 to 145 m, over which rates
are integrated. NO
3 concentrations were fairly
3.5. 24 h nitrogen uptake
Twenty four-hour uptake experiments were performed during PRIME and AMT6 cruises. The
PRIME data have been discussed previously in
detail by Donald et al. (2001). In summary,
surface NO
3 concentrations ranged from 3.6 to
0:004 mmol l1 along a southwards transect between
þ
54 N and 37 N, whilst NO
3 and NH4 uptake rates
2 1
ranged between 0.2 and 3:2 mmol m d and 1.2
and 5:3 mmol m2 d1 , respectively. Maximum uptake rates coincided with a frontal system at
50:34 N with maximum chlorophyll concentrations
of 31:8 mg m2 (1:54 mg l1 at 5 m). A 7-day lagrangian study at the southern end of this transect,
revealed interesting characteristics of the vertical
NO
3 uptake profile, which were determined by the
physical structure. The euphotic depth extended
below 100 m (max. 120 m), whilst temperature
gradients were evident between approximately 30
Table 2
Depth integrated concentrations and rates of uptake of nitrate and ammonium during AMT6
2
[NO
3 ] ðmmol m Þ
2 1
rNO
d Þ
3 ðmmol m
Mean
Range
Mean
Range
BENG
ETRA
CNRY
NAST
NADR
325.1
295.2
16.1
9.8
8.7
23–937
133–561
5.7–27
1.6–23
—
15.0
5.3
4.8
0.9
4.0
0.9–53.9
1.5–11.9
0.8–9.2
0.4–2.2
—
ALL
214.4
1 s:d:
233.3
7.5
1 s:d:
11.4
2
[NHþ
4 ] ðmmol m Þ
2 1
rNHþ
d Þ
4 ðmmol m
Mean
Range
Mean
Range
7
8
2
4
1
9.4
3.9
5.6
4.9
5.9
3.1–23
2.1–8.2
5.0–6.2
2.8–6.5
—
7.9
2.6
3.7
2.7
3.8
1.7–31
1.4–4.3
2.4–5.3
1.6–3.4
—
5
8
2
4
1
22
5.8
1 s:d:
4.6
4.4
1 s:d:
6.6
20
n
n
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
1658
ρNO3- (µmol l-1 d-1)
(A)
0.0
1.0
2.0
3.0
ρNO3- (µmol l-1 d-1)
(C)
0.00
4.0
0
0
5
20
0.05
0.10
0.15
40
10
Depth (m)
Depth (m)
60
15
20
80
100
25
120
30
140
35
160
+
-1 -1
ρNH4 (µmol l d )
(B)
0.0
0.5
1.0
1.5
0.00
0
0
Depth (m)
20
0.04
0.06
40
10
15
0.02
20
5
Depth (m)
ρNH4+ (µmol l-1 d-1)
(D)
60
80
100
25
120
30
140
35
160
Fig. 7. Daily rates of nitrate uptake (A and C) and ammonium uptake (B and D) throughout the euphotic zone during AMT6 within
provinces BENG (A and B) and NAST (C and D). The deepest point for each profile is at the 1% irradiance level.
homogenous (o0:01 mmol l1 ) throughout most of
the euphotic layer, increasing to a mean of
0:3 mmol l1 at the base for 3 of the stations. For
the station with a euphotic depth of 55 m, the
maximum at the base was 1:7 mmol l1 , whilst
the maximum rate of 0:12 mmol l1 d1 was coin1
cident with NO
3 concentration of 0:39 mmol l
1 1
and nitrification rate of 0:11 mmol l d . In
Fig. 7D, maximum volumetric rates are related to
NHþ
4 concentration, with the two stations repre-
sented by circles having mean concentration
of 0:038 mmol l1 and the other two 0.074
(filled square) and 0:091 mmol l1 (open square). As
rates of NHþ
4 uptake do not vary a great deal
over these four stations, mean (1 s:d:) uptake
rate ¼ 0:033 0:012 mmol l1 d1 ðn ¼ 24Þ, it is
the station with greatest euphotic depth that
has the greatest depth-integrated NHþ
4 uptake
rate of 3:68 mmol m2 d1 (cf. 1.74, 3.23,
2:60 mmol m2 d1 ).
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4. Discussion
It is well recognised that primary and bacterial
productivity in the upper water column ultimately
relies on the supply of nutrients to the surface layers
of the oceans. The conditions of the supply and
removal of nitrogenous material over this large
geographical range vary enormously, and environmental regimes span sub-polar to tropical provinces
for both hemispheres; oceanographic conditions
range from eastern boundary upwelling to midocean gyres. The aim of this work was to investigate
the relationships between the ambient concentrations of NO
and NHþ
and their rates of
3
4
uptake. The use of onboard instrumentation
with the capability of providing near real-time
þ
analysis of NO
3 and NH4 to low nanomolar
concentrations meant that the addition of 15 N
tracers was largely done at 10% of the ambient
concentration. When additions were made in excess
of 10%, rates of uptake were adjusted to account
for stimulation of uptake according to Rees et al.
(1999b) using appropriate values of K s (Table 1).
Previous studies including those of Harrison
et al. (1996), Rees et al. (1999a) and Lipschultz
(2001), have highlighted the importance of not
making excessive additions of tracer. Indeed,
Lipschultz intimated that in some published studies,
the rate of uptake may be correlated to the tracer
concentration.
The kinetic data presented here confirm some of
our expectations regarding the uptake of both NO
3
and NHþ
4 . At all stations rA 4rN confirming that
NHþ
4 is consistently the preferred nitrogen species
for uptake; for oceanic waters K A is generally larger
than K N and the range of both is 1–2 orders of
magnitude. In their study of the North Atlantic,
Harrison et al. (1996) found that concentrationþ
dependent uptake of NO
3 and NH4 , according to
Michaelis–Menten kinetics, occurred throughout
the oligotrophic North Atlantic and that rNO
3
was correlated to ambient concentrations. However,
variability in maximum uptake rates of NO
3 could
be explained largely by phytoplankton diversity and
water temperature. In oligotrophic waters, kinetic
experiments of the type performed during this
study, support this finding; rmax N was significantly
correlated ðpo0:01Þ to NO
3 ðr ¼ 0:98Þ and chlorophyll ðr ¼ 0:99Þ, and appeared to show an inverse
correlation with temperature ðr ¼ 0:67; po0:1Þ
þ
and although rNO
3 and rNH4 co-varied, neither
of the kinetic parameters measured for NHþ
4
1659
showed significant relationships with any environmental parameters tested.
4.1. Near-surface uptake and concentrations
During all three of these cruises, stations were
occupied where surface concentrations of NO
3 were
elevated at the immediate surface relative to
10–20 m below. This pattern of distribution appears
to be widespread throughout the oligotrophic
ocean, and was found for 60, 75 and 70% of
stations occupied during AMT5, AMT6 and
PRIME, respectively, wherever surface NO
3 concentration was less than 0:05 mmol l1 . In Fig. 3,
four selected profiles are shown from each of the
cruises to illustrate this. The latitudinal range for
the PRIME cruise is somewhat restricted
ð36:90 N244:46 NÞ, but the profiles from the two
AMT cruises cover 8:97 S235:49 S and 5:57 S2
36:62 N for AMT5 and AMT6, respectively. Haury
and Shulenberger (1998) presented a comprehensive
examination (1983–1995 quarterly surveys) of nutrient data from the California Current and found
that surface nutrient enrichment was displayed by
3
NO
3 , NO2 , PO4 and SiðOHÞ4 with a frequency of
occurrence of 8, 2, 28 and 51%, respectively.
Although their limit of detection was 0:1 mmol l1
for NO
3 , Haury and Shulenberger presents a
schematic representation of a vertical nutrient
profile with surface enrichment that is comparable
to those found in Fig. 4. The question of how these
elevated concentrations are maintained is not
straightforward as a number of processes may
potentially contribute. Haury and Shulenberger
(1998) discussed and discounted a number of these
including atmospheric deposition. Atmospheric
deposition can be an important source of nutrients
to surface waters of the Atlantic, and although high
levels of NO
3 are often supplied by this route, the
unequal distribution of deposition between northern
and southern hemispheres (Baker et al., 2003) and
the episodic nature of deposition events (Owens
et al., 1992) suggest that atmospheric inputs might
not be sufficient to support surface NO
3 elevation
on the scale noted here. Haury and Shulenberger
ultimately suggested that the most likely explanation is the difference between nutrient uptake and
regeneration. It would seem apparent that these
anomalously high values are indeed a result of an
inbalance between production and removal processes, for which incident irradiance may play an
important role. It is feasible that some or all of this
ARTICLE IN PRESS
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
surplus may be photochemically derived from the
breakdown of dissolved organic matter (Bushaw
et al., 1996; Kieber et al., 1999). This route may also
þ
produce NO
2 and NH4 , although Kitidis et al.
(2006) report on photobleached CDOM that is
unquantified, but considered unlikely to yield a
significant source. NO
3 uptake is an energetic
process which is reduced during the hours of
darkness, and whilst nitrification, which although
known to function within the euphotic zone (e.g.,
Fig. 6, Dore and Karl, 1996; Lipschultz, 2001) is
inhibited by light, it is likely to be active during the
night-time. It would seem possible then, that NO
3
could accumulate due to a combination of processes, which is further exacerbated by reduced
uptake at the near surface (Fig. 5). Similar
observations were made by Varela et al. (2005)
and Planas et al. (1999), who attributed this
apparent inbalance to be a consequence of the
photoinhibition of biological uptake of NO
3.
Photoinhibition, the reduction of activity as a
result of elevated light levels at the ocean surface, is
a phenomenon that is well-documented in studies of
primary productivity (e.g., Geider and MacIntyre,
2002; Wozniak et al., 2003), where damage is caused
to photosystem II during photosynthesis. Though
not often considered as an influence on other
cellular processes, Pakulski et al. (1998) observed
photoinhibition of bacterial production and respiration under conditions of ambient irradiance, whilst
Zevenboom (1986) showed that the growth rate of
Oscillatoria agardhii during NO
3 limited growth
was reduced under light-inhibiting conditions. In
þ
Fig. 5 it can be seen that rNO
3 and rNH4 are
reduced at the shallowest depths—at 70 and 50%,
respectively, of the stations occupied during AMT6.
At the same stations primary production showed
similar decreases at 82% of stations (G. Tilstone,
pers. comm.). It would appear that microbial
activity in oligotophic waters between at least 5 S
and 44 N is often inhibited by solar irradiance, so
that there is a net accumulation of NO
3 in the
waters immediate to the surface.
4.2. Concentration-dependent uptake
The range of uptake rates measured in surface
waters (1–35 m) during this study (0.0001–0.0021
þ
and 0:000720:0151 mmol l1 h1 for NO
3 and NH4 ,
respectively, in oligotrophic waters and 0.0010–
0.0731 and 0:000620:0098 mmol l1 h1 for NO
3
and NHþ
4 , respectively, in NO3 replete waters) are
consistent with the Atlantic data set compiled by
Varela et al. (2005). Whereas rNHþ
4 rarely shows
any significant dependence on NHþ
4 concentration
(e.g., Rees et al., 1999a), the uptake of NO
3 is
known to correlate well with concentration (e.g.,
Lipschultz, 2001). Within NO
3 replete waters this
relationship was found to be variable: in the
Brazilian and Falklands current provinces no
correlation was found, whereas stations occupied
in the BENG province deviated from the linear
relationships described above, but were connected
by an exponential relationship (r2 ¼ 0:80) between
uptake (0:001020:0731 mmol l1 h1 ) and concentration (0:41213:6 mmol l1 h1 ). More than 75% of
the stations occupied during this study had surfacewater NO
concentrations of less than
3
0:05 mmol l1 ; for these stations rNO
3 was strongly
correlated to NO
concentration
according
to linear
3
curves, which varied on a regional basis (Fig. 8A).
Although for most of the stations occupied, rNHþ
4
shows no significant relationship to NHþ
4 concentration (Fig. 8B), there is a striking resemblance
between the concentration:uptake patterns of NO
3
and NHþ
4 . The most obvious observation from the
rNO
3 data set is that all of the stations occupied
during AMT5 fit to the same curve, whereas for
AMT6, there are at least two distinct groups, which
are attributed to the southern ð14 S28 SÞ and
northern ð8 S212 NÞ ends of the ETRA, with
stations from NAST and CNRY provinces aligning
fairly closely to either of the two groups. The
southern section of the PRIME data set fit quite
closely to the AMT5 and ETRAsouth , though the
northernmost point suggests a different relationship
for this transect. It would seem that either the
microbial population in the ETRAnorth has a more
efficient mechanism for both the uptake of NO
3
and NHþ
4 than elsewhere in oligotrophic waters of
the Atlantic, or that the hydrography results in an
enhanced rate of nitrogen supply to the biota.
Two overarching questions are posed by this
condition. The first is: are the phytoplankton species
different in this province to elsewhere? And
secondly, has the supply rate of nitrogen enabled
the phytoplankton population to evolve a more
rapid rate of uptake per unit nitrogen? Along the
total length of a transect such as an AMT cruise, the
microbial diversity is vast. During AMT6, for
example, dominant phytoplankton groups ranged
from dinoflagellates (including Ceratium sp.) and
diatoms (Coscinodiscus wailsei) in the area of the
Benguela upwelling system, Synechococcus sp. and
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
1661
(A) 0.0025
ρNO3- (µmol l-1 h-1)
0.002
r 2 = 0.79
0.0015
0.001
r 2 = 0.97
r 2 = 0.96
0.0005
r 2 = 0.64
0
0
0.005
0.01
0.015
0.02
0.025
0.03
0.035
NO3- (µmol l-1)
(B)
0.020
ρNH4+ (µmol l-1 h-1)
0.018
r 2 = 0.74
0.016
0.014
0.012
0.010
0.008
r 2 = 0.01
0.006
0.004
r 2 = 0.34
0.002
0.000
0.00
r 2 = 0.06
0.02
0.04
0.06
0.08
0.10
+
-1
NH4 (µmol l )
Fig. 8. Nitrogen uptake versus concentration in surface waters (1–35 m) of the Atlantic. (A) Nitrate, and (B) ammonium during AMT6,
AMT5 ðÞ and PRIME (&) cruises. Stations occupied during AMT6 are indicated as ETRA-N (’), ETRA-S ðÞ, CNRY () and NAST
(þ). (Error bars are 1 SD, n ¼ 3.) Regression lines are indicated as ETRA-N (- - - - - - -); ETRA-S ð::::::::::::Þ; AMT5 (———); PRIME
ð Þ.
Nitzschia sp. off northwest Africa, and prymnesiophyte blooms including Phaeocystis sp. and Emiliania huxleyi on the northwest European shelf
(Barlow et al., 2004). Oligotrophic areas are
dominated by picoplankton; during AMT6, Barlow
et al. (2004) state that cyanobacteria populations
between 15 S and 40 N are similar and consist of
both Synechococcus and Prochlorococcus. Barlow et
al. (2002) compare conditions found on AMT6 and
AMT3. AMT3 was similar to AMT5 in that it
occurred during September/October (1996) between
the UK and the Falkland Islands. They found that
southern oligotrophic waters during both transects
were dominated by cyanobacteria (Synechococcus
and Prochlorococcus) and nanoflagellates, but that
pigment concentrations along the eastern boundary
(ETRA) were greater and tended to be at shallower
depths. In comparing southern and northern
oligotrophic areas during AMT6, Barlow et al.
(2004) found that chlorophyll-a concentrations in
the ETRA were double those found in northern
oligotrophic waters (0.19 compared to 0:08 mg m3 ).
It would seem then that the ETRAnorth has a
phytoplankton community that is similar in its
taxonomic composition but has elevated biomass
relative to oligotrophic waters of the ETRAsouth;
NAST, and SATL.
A comparison of carbon fixation measurements
made during four AMT transects by Maranon et al.
(2003), found that the rate of nutrient supply to
the euphotic zone in the sub-tropical gyres of the
Atlantic explained a significant degree of the
variability in euphotic zone integrated rates of
primary production. Although surface concentra-
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
1662
Table 3
Mean values of mixed layer depth, NO
3 gradient and NO3 flux across the pycnocline, and NO3 concentration and uptake in near-surface
waters (0–35 m) during AMT 5 and 6
Province
Mixed layer
depth (m)
NO
3 gradient
ðmmol m4 Þ
Vertical NO
3 flux
(mmol m2 d1 )
1
[NO
3 ] (mmol l )
rNO
3
(mmol l1 h1 )
AMT6–ETRAsouth
ð8 S214 SÞ
AMT6–ETRAnorth
ð12 N25 SÞ
AMT5 ð11 N213 SÞ
47
0:57 0:08
0.54
0:016 0:007
0:0002 0:0001
36
1:1 0:62
1.05
0:008 0:005
0:0010 0:0006
71
0:33 0:27
0.31
0:011 0:004
0:0001 0:0000
4.3. f-ratio
It is now well documented and recognised (Dore
and Karl, 1996; Lipschultz et al., 2002; Zehr and
(A)
0.9
y = 0.1032Ln(x) + 0.104
0.8
r 2 = 0.76
1.0
0.5
y = 0.1153Ln(x) - 0.021
0.3
0.2
r 2 = 0.92
r 2 = 0.92
0.6
0.4
0.2
0.0
0.1
0.0
y = 0.1153Ln(x) - 0.021
0.8
0.4
f'-ratio
f '-ratio
0.7
0.6
1
10
100
1000
NO3- (mmol m-2)
0
100
200
300
400
500
600
2
4
NO3- (mmol m-2)
(B)
1.00
0.80
f '-ratio
tions of NO
3 are similar in each of these provinces
(0:01 mmol l1 ) it is obvious from Fig. 2 that for
most of the ETRA occupied during AMT6, the
depth of the nitracline is consistently shallower than
other oligotrophic areas. In comparing stations
occupied in the ETRAnorth , ETRAsouth during
AMT6 and from similar latitudes in the SATL
and WTRA during AMT5 we found mean pycnocline depths of 47, 36 and 71 m for ETRAsouth ,
ETRAnorth and AMT5, respectively. However, the
diffusive supply of nutrients to surface waters is not
a simple function of the depth of the mixed layer,
but is a product of the vertical diffusivity K z
(Denman and Gargett, 1983) and the nutrient
gradient across the pycnocline (King and Devol,
1979). The vertical supply of NO
3 due to the
combination of a shallow mixed layer and the
relatively rapid rate of diffusion across the pycnocline found within the ETRAnorth (Table 3) is thus
able to maintain the rapid rates of rNO
3 displayed
in Fig. 9. It would appear that the phytoplankton
population of the ETRAnorth has adapted an
efficient uptake mechanism in order to remove in
the order of 80% of the NO
3 supply, compared to
approximately 45 and 60% in the ETRAsouth and
AMT5 sections, respectively. In large tracts of the
oligotrophic Atlantic Ocean the relationship be
tween rNO
3 and NO3 concentration can be
described by a linear function. It is apparent from
this discussion, that the slope of the curve, i.e. the
uptake:concentration ratio, is strongly influenced by
a number of environmental variables, and that an
appreciation of the rate of supply is required in
order to predict rates of uptake for any given
oceanic region.
y = 0.0907x + 0.502
r 2 = 0.92
0.60
0.40
0.20
0.00
-8
-6
-4
-2
-
Ln NO3 (µmol
0
l-1)
Fig. 9. f-Ratio versus nitrate for stations occupied throughout
the Atlantic during AMT5, AMT6 and PRIME cruises. (A)
Depth integrated over the euphotic zone showing f-ratios
corrected ( and solid curve) and uncorrected ( and dashed
curve) for isotope dilution of ammonium uptake. Inset shows
corrected f-ratios versus NO
3 plotted on a log scale to identify
the distribution on a province basis (BENG ’, ETRA D, CNRY
þ, NAST n, NADR ). (B) Volumetric data collected in nearsurface waters (1–35 m) during AMT5, AMT6 and PRIME
cruises, the regression line is shown by the solid line, the dashed
lines represent the 95% prediction interval.
Ward, 2002) that the simple derivation of an f-ratio
(Eppley and Peterson, 1979) following uptake
measurements of dissolved nitrogen species is
insufficient to assess fully the rate of new production, as defined by Dugdale and Goering (1967), in
oligotrophic conditions. The importance of nitrogen
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fixation (e.g., Gruber and Sarmiento, 1997) and
supply mechanisms in addition to winter mixing
which include atmospheric deposition (Baker et al.,
2003) have recently been recognised to be more
important in the supply of new nitrogen than was
previously recognised. Also the chemolithotrophic
oxidation of NHþ
4 by bacteria is now recognised as a
potential supply of regenerated NO
to the
3
euphotic zone (Dore and Karl, 1996). The f-ratio
is still used (e.g., Fernandez et al., 2005) in new
production estimates and to provide an excellent
tool to investigate the relationship between rNO
3
and rNHþ
4
f-ratio ¼
rNO
3
þ .
ðrNO
3 þ rNH4 Þ
Our use of f-here is for the latter purpose and
cannot be considered strictly as an index of new
production, as the source of NO
3 is undefined and
may have both new and regenerated components,
whilst no consideration is made for the contribution
of urea or other components of the DON (Rees et
al., 2002; Fernandez et al., 2005; Varela et al., 2005).
In Fig. 9A values for f-integrated over the euphotic
zone are plotted that have been derived using both
apparent and actual (corrected for isotope dilution)
values for rNHþ
4 . These show that not only do
apparent rates result in an overestimate of f, but
that the corrected data provide a much more robust
relationship between integrated NO
3 and the fratio, and correlation coefficients increase from 0.76
to 0.92. For this data set, the mean (1 s:d:)
overestimate of f-ratio at 12 out of 14 stations was
11:1% 5:2%. The two remaining stations were
associated with elevated NHþ
concentrations
4
(40:2 mmol l1 ) at the northwest African upwelling
and on the European continental shelf and were
found to change by 98 and 118%, respectively.
The impact of isotope dilution on rNHþ
4 varies
between experimental procedures; during short
ðo4hÞ incubations of surface waters the mean
(1 s:d:) ratio of actual:apparent rates was
1:03 0:05, whilst during 24-h incubations throughout the euphotic zone the relative difference was
1:99 2:51. This value is high relative to other
studies, which have reported a range of 1.4–1.8 (as
reported in Rees et al., 2002), and is a result of some
of the elevated NHþ
4 concentrations encountered in
high-productivity regions. Nitrification measurements made during this study were performed with
insufficient resolution vertically or latitudinally to
allow a rigorous investigation of the impact of in
1663
situ NO
3 , production on rNO3 and the f-ratio and
as yet no empirical relationships are known which
would enable the derivation of corrected rates. The
data though, do indicate that there is often the
potential for isotope dilution during rNO
3 experiments and for there to be a regenerated component
of the ambient NO
3 , which may at times account
for greater than 100% of the total. This is in
agreement with the findings of Fernandez et al.
(2005) who report that nitrification can support
between 5% and 100% of rNO
3 in the northeast
Atlantic. Isotope dilution of NO
3 during uptake
experiments would ultimately lead to an underestimate in the f-ratio, which we estimate from this
data set to be in the order of 10–23%. If we were to
attempt to assign new and regenerated labels to the
rNO
3 and treat the f-ratio according to the original
definition, then there are occasions in time and
space when ‘‘new production’’ will be equal to zero.
Because of the uncertainty in our assessment we
have not attempted to correct rNO
3 for isotope
dilution, neither have we attempted to differentiate
between new and regenerated NO
3 . However, as
with rNHþ
,
we
consider
these
effects
on short4
term incubations from the near surface to be
insignificant.
The hyperbolic dependence of the f-ratio on NO
3
has been described by other authors (e.g., Elskens
et al., 1997). In Fig. 9 we have shown that this
relationship is robust for both column integrated
and volumetric measurements over 113 of latitude
within the Atlantic Ocean. However, the hyperbolic
representation hides a huge amount of the detail at
lower concentrations, and so these data also are
represented as log-linear fits (Fig. 9A inset and
Fig. 9B). The volumetric data from surface waters
largely fall into two distinct groups, which can be
broadly described according to their NO
3 concentration as o0:10 and 43 mmol l1 , all of the points
except one (which was associated with an anom
alously high NHþ
4 concentration at 54 N during the
PRIME transect) fall within the 95% prediction
interval.
5. Conclusions
The cycling and uptake of nitrogen are fundamental to the health and function of the marine
ecosystem, and as such there is an obligation on us
to continually refine our understanding of these
processes. During the present study, sampling of
nutrient replete conditions did not allow rigorous
ARTICLE IN PRESS
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A.P. Rees et al. / Deep-Sea Research II 53 (2006) 1649–1665
investigation of the specific controls and dynamics
of nitrate and ammonium uptake at high ambient
concentrations. However, under nutrient-depleted
conditions, the physical environment was found to
impart a significant control over microbial nitrogen
uptake. Approximately 70% of the oligotrophic
ocean was found to have elevated NO
3 concentrations at the immediate surface; we consider that this
was likely to be a result of the photoinhibition of the
uptake mechanism. rNO
3 and rmax N were significantly correlated to NO
3 concentration (and to
temperature and chlorophyll a concentration).
These relationships varied between provinces being
very much influenced by the depth of the surface
mixed layer and the rate of diffusive supply. rNO
3
and rNHþ
4 tended to co-vary, and although on
þ
occasions rNHþ
4 varied with NH4 concentration,
no significant correlation was found. The f-ratio, as
an indicator of NO
3 supported productivity (as
opposed to new production), can be predicted with
confidence ð495%Þ from surface or the depth
integrated concentrations of NO
3 for the whole of
the study area, which includes the oligotrophic
ocean to upwelling conditions. If the f-ratio is to be
used as an estimate of new production, then in
addition to the considerations of external nitrogen
supply (e.g., the atmosphere and eddies), a full
assessment of isotope dilution of nitrogen source
and the impact of regenerated NO
3 should be
included.
Acknowledgements
We thank the officers, crews and scientific
colleagues onboard the RRS James Clark Ross
and RRS Discovery for their contribution to this
work. We are particularly grateful to Carol Robinson who played a major role during AMT6 and
throughout the development of this manuscript.
This work forms a part of the Core Strategic
Research programme of the Plymouth Marine
Laboratory, a component of the Natural Environment Research Council and is AMT contribution
no. 127.
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