A global marine-fixed nitrogen isotopic budget

Transcrição

GLOBAL BIOGEOCHEMICAL CYCLES, VOL. 16, NO. 0, XXXX, doi:10.1029/2001GB001856, 2002
A global marine-fixed nitrogen isotopic budget: Implications for
Holocene nitrogen cycling
Jay A. Brandes
Marine Sciences Institute, The University of Texas at Austin, Port Aransas, Texas, USA
Allan H. Devol
Department of Oceanography, University of Washington, Seattle, Washington, USA
Received 18 December 2001; revised 24 July 2002; accepted 1 August 2002; published XX Month 2002.
[1] A nitrogen stable isotopic model was constructed in order to constrain the Holocene
marine-fixed nitrogen budget. The primary sources and sinks considered were riverine
and atmospheric sources, nitrogen fixation, sedimentary and water column denitrification,
and sediment burial. The source budget was found to be insensitive to changes in nitrogen
fixation rates, and thus could not be used to constrain this term. However, the isotopic
value of fixed nitrogen losses was very sensitive to the amount of sedimentary
denitrification. If the isotopic value of marine-fixed nitrogen has not changed during the
Holocene, as supported by sedimentary records, then in order to balance the isotopic
value of sinks and sources, approximately 280 Tg N yr1 of sedimentary denitrification is
required. If such a high rate of denitrification has been sustained throughout the
Holocene, it implies that present-day estimates of marine nitrogen fixation are grossly
underestimated. It also implies that the marine nitrogen budget has a residence time of
INDEX TERMS: 0330 Atmospheric Composition and Structure: Geochemical
less than 2000 years.
cycles; 4805 Oceanography: Biological and Chemical: Biogeochemical cycles (1615); 4842 Oceanography:
Biological and Chemical: Modeling; 4845 Oceanography: Biological and Chemical: Nutrients and nutrient
cycling; 4870 Oceanography: Biological and Chemical: Stable isotopes; KEYWORDS: nitrogen, isotopes,
nitrate, denitrification, budget, marine, model
Citation: Brandes, J. A., and A. H. Devol, A global marine-fixed nitrogen isotopic budget: Implications for Holocene nitrogen
cycling, Global Biogeochem. Cycles, 16(0), XXXX, doi:10.1029/2001GB001856, 2002.
1. Introduction
[2] The marine nitrogen budget has been a subject of
much debate over the last three decades. Initial budgets in
the 1970s and early 1980s [Wada et al., 1975; Codispoti
and Christensen, 1985] were linked to the idea that such
budgets were balanced, i.e., sources equaled outputs. However, more recent studies have suggested that the fixed
nitrogen budget has possibly swung between periods of
deficit and excess, and that these swings might be linked to
observed changes in atmospheric CO2 and N2O concentrations over the last 100,000 – 1,000,000 years [Altabet et
al., 1995, 1999a; Ganeshram et al., 1995, 2000; Suthhof et
al., 2001]. Even the most recent attempts at establishing a
budget have been met with some controversy. At the heart
of the debate are the sizes of sedimentary denitrification
sinks and nitrogen fixation sources. As methods to measure
sediment, denitrification rates have improved [Devol, 1991],
and the aerial extent over which these measurements have
been made has grown [Balzer et al., 1998; Devol and
Christensen, 1993; Devol et al., 1997; Hammond et al.,
Copyright 2002 by the American Geophysical Union.
0886-6236/02/2001GB001856$12.00
1999; Hulth et al., 1997; Jahnke and Jahnke, 2000],while
denitrification rate estimates have grown to greater than 100
Tg N yr1. This has presented a difficulty in establishing a
balanced fixed nitrogen budget, as total sinks (including
water column denitrification and sediment burial) then
exceed 200 Tg N yr1. Some of these sinks are balanced
by riverine and groundwater inputs, but the burden of
replenishing marine-fixed nitrogen stocks falls upon nitrogen fixation, the other primary source of nitrogen to the
oceans [Codispoti et al., 2001; Codispoti and Christensen,
1985]. However, direct measurements of nitrogen fixation
have rarely supported rates in excess of 100 Tg N yr1
[Capone, 2001]. It must be noted that neither fixation nor
sediment denitrification rates are well constrained and they
are subject to rapid episodic events that may dominate their
overall rates [Gehlen et al., 1997; Lipschultz and Owens,
1996]. Furthermore, in most cases, global budgets are based
upon a handful of values.
[3] In conjunction with the nitrogen budget work discussed previously, studies of present and past isotopic
values of nitrate in seawater have become increasingly
important. In the modern ocean, investigations of surface
ocean nitrogen cycling [Altabet, 2001; Altabet et al., 1999b;
Liu et al., 1996; Sigman et al., 1997b; Wu et al., 1997],
X-1
X-2
BRANDES AND DEVOL: NITROGEN ISOTOPIC BUDGET
denitrification [Brandes et al., 1998; Naqvi et al., 1998a;
Voss et al., 2001], and nitrogen fixation [Karl et al., 1997]
have all used nitrogen isotopic patterns to determine these
processes. The close correlation between nutrient uptake,
d15N of NO3, and the d15N of sinking particulate matter
has been used as a tracer for nutrient usage in the Pleistocene-Holocene surface ocean [Altabet and Francois, 1994;
Giraud et al., 2000; Haug et al., 1999; Muller and Opdyke,
2000; Sigman et al., 1999b, 2000b; Teranes and Bernasconi, 2000]. This last usage is particularly dependent upon
assumptions of isotopic constancy of marine nitrate over
time.
[4] There is a long history of using isotopes to constrain
elemental budgets (e.g., 18O in the hydrologic cycle). There
have only been a few attempts to use nitrogen isotopes to
constrain all or parts of the fixed nitrogen budget [Altabet
and Curry, 1989; Liu and Kaplan, 1988; Wada et al., 1975],
and these attempts were limited by the lack of information
on the isotopic values and fractionations associated with
many of the major source and sink terms controlling the
global oceanic nitrate budget. Work over the past decade
has improved this situation, although care has to be taken to
separate anthropogenic influences from baseline values.
Given new information on the isotopic composition of the
various marine nitrogen pools and fractionations associated
with the processes that affect them, we have constructed a
global isotopic budget to help constrain the Holocene
marine-combined nitrogen cycle and understand the factors
that control it.
2. Methodology: Important Terms in the
Marine Nitrogen Budget
[5] There have been several attempts to build a marinefixed (or combined) nitrogen budget [Codispoti et al., 2001;
Codispoti and Christensen, 1985; Gruber and Sarmiento,
1997; Middelburg et al., 1996]. All studies agree on the
important terms: terrestrial runoff, atmospheric precipitation
and nitrogen fixation for inputs, denitrification (sediment
and water column), and sediment burial for the sink terms
(Table 1). Other minor, but potentially important terms
include N2O and organic nitrogen losses from the sea
[Naqvi et al., 1998b], and groundwater inputs [Moore,
1996]. Values for both source and sink terms have risen
as new techniques have been applied, and in some cases as a
result of anthropogenic inputs [Codispoti et al., 2001]. As
these values have been updated, cases have been made for
both balanced [Codispoti and Christensen, 1985; Gruber
and Sarmiento, 1997] and unbalanced [Codispoti, 1995;
Codispoti et al., 2001; Middelburg et al., 1996] budgets.
[6] The argument over a balanced versus unbalanced
fixed nitrogen budget has centered upon the relative sizes
of the sediment denitrification versus nitrogen fixation
terms. As more precise estimates of sedimentary denitrification have been made, the total loss rate for fixed nitrogen
has grown markedly, from less than 30 Tg yr1 [Wada et al.,
1975] to well over 100 Tg yr1 [Codispoti et al., 2001;
Gruber and Sarmiento, 1997]. In a similar fashion, estimates of marine nitrogen fixation have grown from 15 Tg N
yr1 [Codispoti and Christensen, 1985] to 110 Tg N yr1
[Gruber and Sarmiento, 1997], although the larger values
have been justified primarily upon the need for a somewhat
balanced budget and not upon field measurements.
[7] To help resolve both the issues of quantity and
balance, we model a budget focusing upon the major terms,
using the following terminology to describe the fractionations taking place. We will use the term ‘‘combined nitrogen’’ to refer to all forms of nitrogen except molecular
nitrogen (N2). As the vast majority of this fixed nitrogen
exists in the oceans in the form of NO3, this is the species
we will examine. The isotopic composition of nitrogen is
defined as d15N = (15N/14N)sample/(15N/14N)reference 1) 1000, with atmospheric N2 as the reference [Mariotti,
1983]. Isotopic fractionation from sources in the marine
nitrogen cycle is represented as either a = 15R/14R or edenit =
(1 a) 1000, where 15R and 14R are the rates of gain (or
14
NO
loss) for 15NO
3 and
3 , respectively, for each process.
Because the modern N budget is heavily impacted by
anthropogenic inputs [Codispoti et al., 2001; Falkowski et
al., 1998; Galloway et al., 1995; Nevison and Holland,
1997], careful examination of data from a variety of sources
is necessary to examine Paleocene and Holocene nitrogen
budgets. We have focused upon the available literature from
pristine sites. In some cases, no specific data are available
and inferences must be made from spatial or concentration
patterns.
2.1. Sources
2.1.1. Atmospheric Precipitation
2.1.1.1. Mass Estimate
[8] Establishing an isotopic value for atmospheric inputs
is difficult due to the large size and ubiquitous nature of
anthropogenic inputs. These involve both inorganic NOx
emissions from combustion engines and power plants,enhanced NH3 and NxO emissions from fertilized soils [Asner
et al., 2001; Nevison and Holland, 1997; Perez et al., 2001],
and possibly organic nitrogen emissions from combustion
and soil releases [Cornell et al., 1995]. Duce et al. [1991]
and Galloway et al. [1995] give a value of 15 Tg N yr1 for
preindustrial inorganic nitrogen inputs. The situation for
organic nitrogen inputs is less clear. Cornell et al. [1995]
give a range of 24– 84 Tg N yr1, but assumed that most of
this flux is of anthropogenic origin. A conservative estimate
of 10 Tg N yr1 for organic sources provides a total
preindustrial atmospheric flux of 25 Tg N yr1.
2.1.1.2. Isotopic Composition
[9] A number of studies have investigated the d15N of
inorganic nitrogen compounds in rainwater and dry deposition [Cornell et al., 1995; Fogel and Paerl, 1993].
Isotopic values reported for this source ranges from a low
of 12 to 8%, with higher values generally associated with
oxide phases. Wada and Hattori [1991] reported an average,
based upon available literature, of 4 ± 5% for both
ammonium and nitrate in precipitation. The more recent
studies have tended to support this light isotopic value as
well [Fogel and Paerl, 1993]. Atmospheric inputs of
organic forms of nitrogen are thought to be significant
[Cornell et al., 1995, 2001; Cornell et al., 1998; Cornell
and Jickells, 1999; Fogel and Paerl, 1993], accounting for
perhaps a third of total sources. Isotopic values of +0.7 to
X-3
Table 1. Fluxes and Isotopic Values for Source and Sink Nitrogen
Budgetsa
Term
Flux, Tg N yr1
Isotopic Value, %
Riverine source
Atmosphere sources (DON + DIN)
Nitrogen fixation
Total sources
Sedimentary denitrification
Water column denitrification
Organic burial
Total sinks
Net
25
25
110 – 330
160 – 380
200 – 280
75
25
300 – 380
200 – 0
4 (±4)
4 (±5)
1 (±1)
1
3.5 (±2)
20 (±3)
6 (±4)
1
1 (±2)
a
Values in parentheses for isotopic values are estimated variances for
each term. See text for references.
7.7% have been reported for low nitrate content rainwaters [Cornell et al., 1995]. The nominal average of these
is 4%, which matches the inorganic average.
[10] There is some theoretical justification for a preanthropogenic atmospheric source less than 0%. Preindustrial
inorganic nitrogen inputs were likely to be dominated by
two sources: soil NH3 volatilization and conversion of N2 to
NOx by lightning [Dawson, 1980; Kumar et al., 1995;
Noxon, 1976; Owens et al., 1992; Raven and Yin, 1998].
Due to the very high temperatures involved, lightning
sources convert N2 to fixed forms with little to no fractionation [Wada and Hattori, 1991]. Ammonium volatilized
from soils is also likely to be very isotopically depleted,
given the large fractionation during this process (e = 20%,
[Wada and Hattori, 1991]) and moderate soil d15N values
(see section 4 below). Indeed, studies of ecosystems dominated by ammonium volatilization support this contention
[Mizutani et al., 1986; Mizutani and Wada, 1988].
2.1.2. Terrestrial Runoff
2.1.2.1. Mass Estimates
[11] Inputs from terrestrial sources include dissolved
inorganic nitrogen (DIN) in rivers, streams, and groundwaters, as well as particulate and dissolved organic nitrogen
(DON) carried by rivers. Codispoti and Christensen [1985]
give a value of 25 Tg N yr1 for preindustrial riverine
sources. More recently, Seitzinger and Kroeze [1998] estimated DIN sources of 5 Tg yr1 for the world’s oceans. The
particulate nitrogen loading to the oceans may be significantly more than this, roughly 20 Tg N yr1 [Duce et al.,
1991; Galloway et al., 1995]. Some of this may be lost by
denitrification or sedimentation in estuaries [Nixon et al.,
1996; Seitzinger and Nixon, 1985]. It has been speculated
that groundwater fluxes of fresh water may equal riverine
sources [Moore, 1996]. Little is known, however, about the
fate of nitrogen carried into coastal marine systems and
estuaries. There is evidence that groundwaters can be an
important nitrogen source to estuaries [Holmes et al., 2000;
McClelland and Valiela, 1998; McClelland et al., 1997;
Valiela et al., 2000]. Some may be lost due to denitrification
in suboxic sediments, and in terrestrial riparian systems
suboxic regions have been shown to be very effective traps
for groundwater nitrogen [Brandes et al., 1996]. However,
groundwater studies suffer the same anthropogenic pollution problems as do riverine studies and to date no study has
attempted to constrain this term. Given the uncertainties, we
choose to use the 25 Tg yr1 term for terrestrial fixed N
sources, but we are cognizant that this term may need
revision in the future.
[12] Studies of the isotopic composition of DIN and DON
in rivers have been primarily done on heavily polluted
systems [Feast et al., 1998; Fry, 1999; Harrington et al.,
1998; Kellman and Hillaire-Marcel, 1998; Mariotti, 1977;
Mariotti et al., 1976; Mariotti and Letolle, 1977; Sweeney et
al., 1980c; Sweeney and Kaplan, 1980a, 1980b; Voss and
Struck, 1997]. These studies have generally found relatively
enriched d15N values for dissolved nitrogen species, presumably due to the presence of fertilizer and wastewater
inputs [Bachtiar et al., 1996; Mariotti, 1977; Mariotti et al.,
1976; Sweeney et al., 1980c]. Very few studies have been
done on unambiguously pristine river systems. An exception
is a study by Sweeney and Kaplan [1980a] of two northern
California river systems, for which they reported d15N values
of 4% for nitrate. We have measured the d15N of nitrate in
the Amazon main stem above Manaus and in several source
rivers in the Andes (Table 2). Although there is some spread
among these values, the average for all the Amazonian rivers
was also around 4%, and thus we adopt this value for
preanthropogenic dissolved riverine nitrogen sources.
[13] The particulate isotopic flux is more difficult to
determine. Numerous studies have shown that particulate
organic carbon carried by rivers is quickly remineralized
before reaching the coastal oceans, and thus it is reasonable
to assume that much of the organic nitrogen associated with
this material will also be remineralized. However, in the
absence of suboxic conditions this nitrogen will ultimately
be released as nitrate, perhaps with little fractionation.
Hedges et al. [2000], summarizing data collected from a
1800-km-reach of the Amazon River, reported values
between 2 and 5%, with a mean of 3.5% for DON, fine
particulate, and coarse particulate organic material. This
value agrees well with our estimates for inorganic nitrogen
in the same river system. Finally, groundwater nitrogen
sources are poorly constrained. In general, estimates of
‘‘pristine’’ or ‘‘source’’ nitrate isotopic values in these
systems are relatively enriched, from 2 to 10% [Burg and
Heaton, 1998; Feast et al., 1998; Harrington et al., 1998;
Kellman and Hillaire-Marcel, 1998; Wassenaar, 1995].
Table 2. d15N of Dissolved Nitrate in Amazon Main Stem and
Tributary Riversa
River
d15N Versus Air
Madre de Dios
Orton
Beni at Arriba
Beni at Riberalta
Beni at Sapecho
Beni at Rurrenabaque
Mamore Guaya
Athumani
Yara at Caranaui
Solemoies at Marchaneria
Amazon at Manaus
3.05 ± 0.5
4.76 ± 0.3
4.43 ± 0.1
5.19 ± 0.1
2.93
1.03
2.88 ± 0.3
1.16 ± 0.1
2.67
2.2 ± 0.1
4.1 ± 0.3
Number of
Determinations
n
n
n
n
n
n
n
n
n
n
n
=
=
=
=
=
=
=
=
=
=
=
3
2
3
2
1
1
2
2
1
2
6
a
Samples were acidified onsite and filtered (precombusted GFF) prior to
shipment to the US. Nitrate isotopic values were determined using the
method of Velinsky et al. [1989].
X-4
[14] Overall, we choose a moderately enriched value, 4 ±
4%, for preanthropogenic terrestrial nitrogen sources. The
bulk of the studies listed previously suggests such a value is
reasonable. Terrestrial nitrogen sources include both Nfixation and nitrogen released from bedrock and soil weathering [Holloway and Dahlgren, 1999; Holloway et al.,
1998]. The nitrogen released from rocks should have a
value between 0 and 6%, similar to marine sediments and
other crustal rocks from which they are derived. Finally, soil
denitrification and NH3 losses will tend to enrich groundwater nitrogen pools above these end-members.
2.1.3. Nitrogen Fixation
[15] The amount of nitrogen fixed by diazotrophs remains
one of the more contentious subjects in the marine biogeochemistry community. Arguments based upon water
column N:P relationships have been made [Gruber and
Sarmiento, 1997] to support a nitrogen fixation term in the
range of 110 Tg N yr1, yet direct measurements of fixation
have tended toward smaller numbers than this [Capone and
Carpenter, 1982; Carpenter and Romans, 1991]. However,
recent discoveries of additional species capable of nitrogen
fixation [Carpenter et al., 1999; Zehr and Capone, 1996;
Zehr et al., 2000, 2001] may increase overall marine nitrogen fixation rates. We will examine nitrogen fixation in light
of the global isotopic nitrogen balance to be constructed
below.
[16] The process of nitrogen fixation is thought to produce organic nitrogen with relatively little fractionation.
Direct measurements of Trichodesmium species in situ
[Capone et al., 1997] and other diazotrophs in culture
[Hoering and Ford, 1959; Minagawa and Wada, 1986]
have given a range of 1.5 to 0%. This represents a small
offset from dissolved N2, which has a value of 0.6%
[Emerson et al., 1991, 1999]. However, one published
report of Trichodesmium species grown in culture has
indicated much lower numbers (3 to 2%, [Carpenter
et al., 1997]). One possibility is that field isotopic measurements may be influenced by other nitrogen sources, such as
uptake of nitrate. Another unknown possibility is the
possible production and release of dissolved organic substances by diazotrophs [Bronk and Ward, 2000], about
which little is known isotopically. If this material is labile,
it could represent an additional source of fixed nitrogen
from these organisms. Given the available information, we
will assume that nitrogen fixation represents a nitrogen
source to the sea of 1%, with a relatively small uncertainty of ±1%.
2.2. Sinks
2.2.1. Water Column Denitrification
[17] There are two marine regions where water column
denitrification is globally significant: the Eastern Tropical
North and South Pacific (ETNP and ETSP) suboxic zones
and the Arabian Sea. [Bange et al., 2000; Cline and Kaplan,
1975; Codispoti and Christensen, 1985; Codispoti and
Packard, 1980; Codispoti and Richards, 1976]. The eastern
Pacific regions together support a denitrification rate of
about 50 Tg N yr1 [Codispoti and Christensen, 1985;
Codispoti and Packard, 1980; Codispoti and Richards,
1976; Deutsch et al., 2001], while the Arabian sea supports
a rate about half this [Deutsch et al., 2001; Naqvi, 1994].
There is some evidence for higher rates than these, based
upon dissolved gas N2/Ar ratios [Brandes, 1996; Codispoti
et al., 2001]. We therefore adopt a conservative estimate for
total marine water column denitrification of 75 Tg N yr1,
similar to rates used by other investigators [Codispoti and
Christensen, 1985; Gruber and Sarmiento, 1997].
[18] Brandes et al. [1998], Altabet et al. [1999b], and
Voss et al. [2001] have reported an average value for
isotopic fractionation during water column denitrification,
e, of 25– 27%. This value was based upon isopycnal mixing
models for both the Arabian Sea and ETNP suboxic regions.
Given the similarity of data from the ETSP [Liu, 1979], it
appears that water column denitrification exhibits a globally
consistent fractionation factor. This value also agrees well
with a recent laboratory estimate of fractionation by marine
denitrifiers [Barford et al., 1999], but is slightly greater than
older estimates [Delwiche and Steyn, 1970]. The isotopic
value of nitrogen lost within the denitrifying water column
is a function of the source nitrate isotopic value; in the
Arabian Sea the apparent source waters are slightly lighter
than those found in the Pacific (5% versus 6%, [Brandes et
al., 1998]). Although suboxic basins (e.g., Cariaco Trench,
Black Sea) can be locally important to nitrogen budgets, the
amount of nitrogen lost in these regions is small compared
to the large marine suboxic regions. The integrated isotopic
value of fixed nitrogen lost via water column denitrification
can be calculated using a closed system (Rayleigh) assumption [Wada and Hattori, 1991] or by numerically integrating
losses within advection-diffusion (A – D) models [Brandes
et al., 1998]. Depending upon the method, the isotopic
value of fixed nitrogen lost is from 19 to 21%. Closed
system calculations always result in slightly less apparent
fractionation than those done for open (A– D) systems. An
open system allows some ‘‘light’’ nitrate into the denitrification zone; thus in order to duplicate the isotopic enrichments observed in the data, the model fractionation factor
must be larger. However, the differences are small in
comparison to the uncertainty in calculating e. Thus we
adopt a value of 20 ± 3% for this process.
2.2.2. Sediment Denitrification
[19] As with nitrogen fixation, the rate of marine sediment
denitrification remains one of the important unresolved
issues in marine nitrogen budgets. Early estimates [Codispoti and Christensen, 1985] indicating rates less than 100
Tg N yr1 have been used by recent investigators to support
the notion of a balanced fixed nitrogen budget [Gruber and
Sarmiento, 1997]. However, other researchers have revised
these estimates up to nearly three times this level in recent
years [Codispoti, 1995; Devol et al., 1997; Middelburg et
al., 1996]. These higher rates may be partly due to anthropogenic influences [Codispoti et al., 2001], although much
of the discrepancy in estimates may be due to denitrification
in slope and deep-sea sediments, which should be less
influenced by terrestrial and atmospheric anthropogenically
X-5
Figure 1. Sampling locations for sediment denitrification studies.
influenced sources. We will use the isotopic budget in this
paper to constrain this rate (see section 4 subsequently).
[20] Although one report has been published on the
isotopic fractionation during denitrification in sediments
[Brandes and Devol, 1997], the data are from an estuarine
location not necessarily typical of ocean margin sediments.
To expand the database of sediment denitrification isotopic
values, a series of measurements were made along the
Washington and Mexican continental margins (Figure 1)
X-6
using an in situ tripod incubation system [Brandes and
Devol, 1997; Devol, 1987]. Briefly, 24 –48 hour sediment
incubations were conducted with the lander in ‘‘coring’’
mode, where a small-scale box core attachment was
included on each incubation chamber to allow retrieval of
overlying waters and intact sediments. Overlying waters
were subsampled, frozen, and returned for later isotopic and
compositional analysis. Isotopic analysis for d15N-NO3
was performed using the method of Velinsky et al. [1989].
Further details of the methods used are described by
Brandes [1996] and Brandes and Devol [1997]. Sediments
in this region are overlain by a strong oxygen minimum,
with O2 concentrations off Mexico decreasing to below 10
mM l1 in the depth interval between 150 and 800 m. The
fraction of nitrate remaining versus change in isotopic
concentration is shown in Figure 2. All data plot with
fractionations between 0 and 3% fractionation, with an
average value of 1.5%. This is slightly larger than that
measured for estuarine Puget Sound sediments [Brandes
and Devol, 1997], but it is still much lower than that noted
for water column denitrification. Given the average oceanic
15
N-NO
3 value of 5% [Liu and Kaplan, 1989; Liu et al.,
1996; Sigman et al., 1999b, 1997b], sediment denitrification
would therefore remove nitrogen at an isotopic value of 3.5
± 2%.
[21] One significant concern is that all the available data
are from relatively organic-rich sediments with thin oxic
zones. It may be possible that the fractionation factors for
this process are greater in low carbon shelf sediments (as
found in some US Atlantic Margin sediments, [Jahnke and
Jahnke, 2000] or slope and deep-sea sediments. However, a
recent study [Sigman et al., 2001] of the isotopic composition of pore water nitrate in a deep-sea sediment also
indicated a small degree of fractionation during denitrification. We do not currently know the reasons for the lack of
isotopic fractionation in the sediments studied so far.
Possible explanations include the presence of steep concentration gradients that reduce the effective fractionation
factor experienced by waters in contact with sediments
[Bender, 1990; Brandes and Devol, 1997], abiotic or
inorganic (e.g., Mn oxidation) reactions [Luther et al.,
1997] with intrinsically small fractionations, or some other
unknown process. However, it will be shown subsequently
that sedimentary denitrification must proceed with little
fractionation in order for the marine isotopic budget to
approach a reasonable balance.
2.2.3. Sediment Burial
[22] Gruber and Sarmiento [1997] gave an estimate of 25
Tg N yr1 for sediment nitrogen burial. This value agrees
well with carbon budget estimates of Hedges and Keil
[1995], who estimated a global carbon burial rate of 160
Tg C yr1. This translates into a putative nitrogen burial rate
of 25 Tg N yr1, given a C:N ratio of 7.
[23] As no global database exists for sediment d15N
values, a precise estimate of this term is unavailable. In
continental shelf and slope regions where mixed-layer
nitrogen is assumed to be completely removed by primary
producers, the d15N of buried organic nitrogen is close to
Figure 2. Normalized changes in isotopic composition of
nitrate during water column (triangles) and sedimentary
(circles) denitrification. Solid circles are data from Washington Shelf lander deployments, while open circles are
data from the oxic Mexican shelf station. Water column data
(open triangles, Mexican shelf hydrocast station; filled
triangles, Indian Ocean), from Brandes et al. [1998] are
plotted for comparison. Lines represent isotopic trajectories
for estimated fractionation factors assuming a closed (i.e.,
Rayleigh) system.
that of upwelled marine nitrate [Altabet et al., 1995, 1999a,
1999b; Ganeshram et al., 1995, 2000; Giraud et al., 2000].
Little diagenetic fractionation during burial has been found
for shelf and slope sediments [Altabet et al., 1999b; Freudenthal et al., 2001]. As continental margin environments
account for >90% of the total organic material permanently
buried in the sea [Hedges and Keil, 1995], the average for
all the organic material buried should be similar to average
oceanic nitrate. The situation for deep-sea sediments is more
complicated. There exists a significant uptake fractionation
by photosynthetic organisms [Altabet, 2001; Sigman et al.,
1999b; Waser et al., 1998; Wu et al., 1997]. This is not a
concern if all upwelled nitrogen is eventually removed by
phytoplankton, but there are exceptions to this, especially
the southern Pacific HNLC and Antarctic regions [Altabet
and Francois, 1994; Sigman et al., 1997b] (this may also be
the case for some continental shelf and slope environments
as well). Downwelling of waters containing appreciable
amounts of nitrate will tend to remove isotopically enriched
nitrate from the surface, leading to isotopically depleted
nitrogen in sediments. Counteracting this possibility is the
observation that low organic content marine sediments can
exhibit significant diagenetic shifts (up to +4%) from
source-sinking organic material [Freudenthal et al., 2001;
Holmes et al., 1996]. To balance this, overall material
X-7
buried in deep-sea sediments may be slightly enriched over
source nitrate. Thus the isotopic value for organic matter
burial is set slightly higher than the average isotopic
composition of source nitrate, 6 ± 2%.
2.3. Existing Nitrogen Pools
[24] As discussed previously, the average isotopic composition of nitrate in the sea is about 5%, although this
value varies from about 4% in the North Atlantic to 6% in
the North Pacific [Liu and Kaplan, 1989; Liu et al., 1996;
Sigman et al., 1997b]. There are a few anomalous basins,
such as the Mediterranean (1%, [Sachs and Repeta,
1999]), and the overall database of nitrate d15N measurements is very limited; however, the main ocean basins are
well represented. Dissolved organic forms, which represent
3 – 5% of total marine-fixed nitrogen, are not well represented. Benner et al. [1997] report values ranging from 7.2
to 14.6% for ultrafiltered dissolved organic matter (DOM)
in the equatorial Pacific. However, Abell et al. [1999]
reported very low values (0.5%) for total DOM collected
from the same region. There is some debate over how
rapidly this material cycles in the oceans [Abell et al.,
2000; McCarthy et al., 1997; McCarthy et al., 1998], but
over the residence time of fixed nitrogen (1500 years) the
DON pool may play a role. Given the inconsistencies in
reported DON isotopic values, we choose to neglect this
term in our isotopic budget, although this will need to be
revised in the future, especially if the results of Benner et al.
[1997] are typical.
3. Results: A Marine Stable Isotopic Budget
[25] Our objective in modeling the marine-fixed nitrogen
stable isotope budget is twofold. First, can the isotopic
budget constrain overall source and sink rates to determine
if marine-fixed nitrogen inventories have been at steady
state during the Holocene? Failing that, can the isotopic
budget constrain either the source or sink terms so that
conclusions can be made about the overall rates of nitrogen
cycling in the sea? In order to answer these questions fluxweighted source and sink model budgets were constructed,
using the values given in Table 1. Because there are eight
unknowns (source and output 15N/14N ratios, riverine,
atmospheric and nitrogen fixation sources, sedimentary
denitrification, water column denitrification, and organic
burial sinks) and only two equations, six of the terms need
to be fixed. The best known of these terms are sediment
burial, water column denitrification, riverine sources, and
atmospheric sources. With these values fixed, the fluxweighted budget model then examines the effects of varying
the nitrogen fixation and sediment denitrification terms. The
model equations are as follows:
h
15
N=14 N
¼ 15 N=14 N
Fluxrivers
ðsourcesÞ
rivers
þ 15 N=14 N
Fluxrain þ 15 N=14 N
Figure 3. Isotopic value of combined marine-fixed nitrogen sources versus changes in nitrogen fixation rates.
Atmospheric and riverine sources were held at 25 Tg N yr1
each. Dotted lines represent one SE of model results.
and
15
N=14 N
ðsinksÞ
N=14 N
Fluxsed:denit:
sed:denit:
þ 15 N=14 N
Fluxwater denit:
water denit:
i h
þ 15 N=14 N
Fluxburial = Fluxsed:denit:
¼
h
15
burial
þFluxwater denit: þ Fluxburial
i
ð2Þ
[26] The effects of varying the rate of nitrogen fixation
were examined by generating an artificial ‘‘data set’’ [Press
et al., 1992] consisting of 10,000 isotopic values for each
source term (e.g., (15N/14N)rivers), each with a standard
deviation as given in Table 1. Standard deviations were
assumed to be independent. Mass flux values for riverine
and atmospheric sources were held constant. Using these
values in equation (1), a corresponding set of estimates for
the (15N/14N)(sources) was compiled, the average taken, and
the standard deviation computed. This estimate was done
for values of nitrogen fixation between 0 and 400 Tg N
yr1. The effect of varying nitrogen fixation on the isotopic
value of marine-fixed nitrogen sources is shown in Figure 3.
The average isotopic value remains nearly constant,
between 0 and 1, across the range of fixation rates.
Riverine and atmospheric sources tend to offset each other,
giving a net 0% for that contribution, although the large
rain
fix
i h
i amount of variability in each term is manifested in a high
Fluxfix = Fluxrivers þ Fluxrain þ Fluxfix variance at low fixation rates. Because the isotopic value for
nitrogen fixation is close to the average of river + atmosð1Þ pheric sources, the overall isotopic value for sources is
X-8
insensitive to changes in this term. This prevents the use of
the isotopic budget as a constraint upon nitrogen fixation,
but it does have the benefit of establishing a relatively
narrow range of possible source isotopic values. This is
especially true for fixation rates greater than 100 Tg N yr1,
where the budget is dominated by the relatively well
isotopically constrained nitrogen fixation term.
[27] The effect of varying estimates for sedimentary
denitrification on the isotopic composition of fixed nitrogen
sinks was investigated using the flux-weighted isotopic
budget given by equation (2). As with the source model,
10,000 values for each sink term (e.g., (15N/14N)burial) each
with a standard deviation as given in Table 1. Mass flux
values for water column denitrification and sediment
organic nitrogen burial were held constant. Using these
values in equation (2), a corresponding set of estimates
for the (15N/14N)(sinks) was compiled, the average taken, and
the standard deviation computed as a function of sedimentary denitrification rate. Model results are shown in Figure 4.
In contrast to the source model where little isotopic effect
was seen in shifting the nitrogen fixation term, average
isotopic values for sinks were very sensitive to changes in
sedimentary denitrification. Model results ranged from
12.75% for the case of no sedimentary denitrification,
to +0.25% for 400 Tg N yr1 sedimentary denitrification
(Figure 4). Because fixed N losses due to sedimentary
denitrification are not strongly enriched in 15N, a large
amount of sedimentary denitrification is necessary to balance water column denitrification and bring overall isotopic
values of the losses into the range of sources.
[28] In order to construct a complete isotopic budget for
the marine nitrogen cycle during the Holocene, one has to
constrain the average isotopic value of nitrate. There is
considerable evidence that the isotopic composition of fixed
nitrogen in the ocean has remained constant over the last
10,000 years. Kienast [2000] has explicitly stated that
Holocene (and prior) d15N values have remained constant.
A host of other studies from different regions [Altabet et al.,
1999a; Francois et al., 1997; Ganeshram et al., 2000;
Nakatsuka et al., 1995a, 1995b; Sigman et al., 1999a] have
shown changes of <1% in Holocene sediment d15N values.
There have been cases where shifts of 1 – 2% have been
noted between surface samples and those found just below
[Bertrand et al., 2000; Emmer and Thunell, 2000; Pedersen
and Bertrand, 2000]. In some cases, even nearby cores
show conflicting shifts [Holmes et al., 1997; Muller and
Opdyke, 2000; Schubert et al., 2001]. Where Holocene
shifts have been observed, they have been attributed either
to changes in local nutrient uptake [Giraud et al., 2000], or
to diagenesis effects, for which there is some evidence
[Freudenthal et al., 2001; Holmes et al., 1996]. The overall
lack of a clear trend in global Holocene sediment d15N
values strongly suggests that fixed nitrogen isotopic values
have remained roughly constant. This constancy of marinefixed nitrogen isotopic values provides an important constraint upon the total fixed nitrogen budget.
[29] If one assumes a constant Holocene value of 5% for
marine-dissolved NO
3 , then the isotopic value of combined
sinks must lie in the range covered by sources, 0 to 1%.
Given the best estimates of water column denitrification
Figure 4. Isotopic value of combined marine-fixed nitrogen losses as a function of the global sedimentary
denitrification rate. Sediment burial and water column rates
were held constant at 25 and 75 Tg N yr1, respectively.
Dotted lines represent one SE of model results.
and sediment burial, this requires a minimum of 250 –300
Tg N yr1 in sedimentary denitrification, and a total
marine-fixed nitrogen loss rate of nearly 400 Tg N yr1
(Figure 5). This rate is in excess of most previously
published estimates for global sedimentary denitrification
rates [Codispoti and Christensen, 1985; Devol et al., 1997];
however, the database for sedimentary denitrification rates
is relatively small and many estimates made prior to the
1990s are marred by measurement difficulties such as the
neglect of coupled nitrification-denitrification reactions.
Middelburg et al. [1996] suggested a total rate of 220–
280 Tg N yr1 based upon a global sediment denitrification
model. They suggested that much of the global rate was
due to denitrification within slope and deep-sea sediments.
What is critical to note about both Middelburg’s estimate
and ours is that these are long term, not anthropogenically
influenced, rates.
[30] We have noted above that the evidence for a small
fractionation factor for sedimentary denitrification is based
upon a small data set from high carbon content shelf
sediments. However, the isotopic budget provides some
justification for this. If the fractionation factor for sedimentary denitrification were as much as one-fifth of the water
column factor (i.e., 5%), the source and output budgets
could not be balanced without making very unreasonable
assumptions (e.g., N2 fixation having a very large depleted
isotopic value). Water column denitrification has a very
large fractionation factor, removing relatively large amounts
of isotopically depleted fixed N. This term must be counteracted by a loss of enriched N. Sediment burial removes a
small amount, but sedimentary denitrification must act as a
sink of enriched fixed N, and thus must have a small (<5%)
Figure 5. Model source and sink isotopic values plotted as
a function of different levels of nitrogen fixation and
sediment denitrification, respectively. The solid line represents source model results for sources as a function of
nitrogen fixation rate (see Table 1). Dotted and dashed lines
represent sink model results for fixed nitrogen losses as a
function of sedimentary denitrification rates under different
conditions. The lowermost (large dashes) curve is the model
result with all parameters as given in Table 1. The other two
curves represent sink model results with estimated Holocene
sediment burial rates set to twice the modern estimates
(small dashes) and for results with a 33% reduction in
Holocene water column denitrification rates (i.e., 50 Tg N
yr1, dotted line), respectively. Large dots represent
conditions of isotopic balance (sources = sinks) for each
of the three loss models given equal nitrogen fixation and
sedimentary denitrification rates.
fractionation factor given average seawater fixed N isotopic
values. In other words, if both sedimentary and water
column denitrification exhibited the same fractionation
factor, seawater nitrate would have to increase to greater
than 20% in order for the isotopic value of sinks to equal
that of sources (0.5%). The smaller the apparent sedimentary denitrification factor, the lesser is the sedimentary
denitrification that takes place to balance the isotopic
budget. If sedimentary denitrification were to have no
isotopic fractionation (0%), then our estimate of its global
rate would fall to around 240 Tg N yr1, still larger than
traditional estimates of sedimentary denitrification.
[31] Another factor to consider is the possible enhancement/intensification of marine suboxic regions due to
anthropogenic nitrogen sources [Codispoti et al., 2001;
Naqvi and Jayakumar, 2000; Rabalais et al., 1996, 2001].
The result would be to inflate modern estimates relative to
those in the recent past and lead to erroneously high
sedimentary denitrification estimates. The first wide-scale
X-9
measurements of Eastern Tropical Pacific (ETP) denitrification rates were done in the early 1970s [Cline and
Kaplan, 1975; Codispoti and Richards, 1976]. It can be
argued that this region is an unlikely candidate for anthropogenically driven intensification, yet these studies agreed
upon a large value of 50 Tg N yr1 for this region alone.
This value has recently been upheld using more comprehensive measurements of circulation and water residence
times [Deutsch et al., 2001]. We have chosen a value of 75
Tg N yr1 for all marine suboxic regions, a value that
includes the ETNP and the ETSP and Arabian Seas. Recent
estimates for these regions have placed the global rate at
greater than 80 Tg N yr1 and there is some evidence for a
rate as much as twice this if one includes nitrogen sources
other than nitrate [Codispoti et al., 2001]. Sediment d15N
measurements from these regions [Altabet et al., 1995,
1999a; Ganeshram and Pedersen, 1998; Ganeshram et
al., 1995, 2000] show no significant changes in Holocene
denitrification intensities. Thus water column denitrification
rates and their corresponding losses of depleted fixed nitrogen are unlikely to have been less during this time period
(although short-term fluctuations may have occurred), and
nor are the fractionation factors likely to have shifted.
Brandes et al. [1998] revisited the isotopic data of Cline
and Kaplan [1975] and found no difference in fractionation
factors for the region over that time span. The fractionation
factor appears to be constant over the range of denitrification rates found in the Arabian Sea and ETNP regions
[Brandes et al., 1998]. Even if we postulate a water column
denitrification rate of 50 Tg N yr1, over 180 Tg N yr1 of
sedimentary denitrification is required for average fixed
nitrogen sinks to match the value of sources (Figure 5). A
doubling of sediment burial rates, which would remove
isotopically enriched (relative to nitrogen fixation) nitrogen
has an even smaller effect, with a requirement of at least 250
Tg N yr1 (Figure 5). These estimates are predicated upon a
nearly balanced fixed N budget, if nitrogen fixation rates are
less than a larger sediment, denitrification rates are required
to balance the isotopic budget.
4. Discussion: Consequences of Long-Term
400 TG N yr1 Marine-Fixed Nitrogen Losses
[32] A balanced marine nitrogen isotopic budget does not
require a balanced fixed nitrogen budget. As the source
isotopic budget is insensitive to changes in nitrogen fixation, it is possible to have a total marine nitrogen budget
that is wildly out of balance and yet still maintain a balanced
isotopic budget. However, there are several practical implications of a nearly 400-Tg yr1 loss rate. Given our sediment denitrification estimate of 280 Tg N yr1, if nitrogen
fixation rates were only 100 Tg N yr1, then the combined
budget would be out of balance by over 200 Tg N yr1.
Such a loss rate would deplete the ocean of fixed nitrogen
(at present inventory) within 3000 years. Thus the ocean at
the glacial-interglacial transition would have had to contain
three times the nitrate concentrations that it does today.
Losses of this extent would also generate about 100 1012
mol yr1 (0.1 Gt yr1) CO2 from lost productivity (assuming near-complete surface nitrogen usage by primary pro-
X - 10
ducers during the Holocene). This amount of carbon release
over a long time period poses difficulties as preindustrial
Holocene CO2 levels did not rise significantly [Falkowski,
1997; Falkowski et al., 1998; Gruber and Sarmiento, 1997].
A possible alternative might be shifts in C:N ratios of
primary producers, as has been speculated by some
researchers [Archer et al., 2000]. If early Holocene phytoplankton sequestered more nitrogen-rich compounds (C:N
ratios decreased) than their modern counterparts, then early
Holocene CO2 fixation rates might have been comparable to
modern values in spite of major changes in fixed nitrogen
availability. It is possible for phytoplankton to vary their
C:N ratios in the presence of excess nitrogen [Banse, 1994;
Goldman and McCarthy, 1978; Goldman et al., 1979; Laws
and Bannister, 1980; McCarthy and Goldman, 1979]. This
process, which occurs primarily under low-light conditions,
can lower C:N values to 5 from the Redfield 6.6 value, and
under some exceptional circumstances C:N ratios can drop
to near zero [Fraga et al., 1998; Rios et al., 1998]. It is an
open question whether or not this high-nitrogen content
material will survive remineralization to permanent burial,
and there have been no reports of significant decreases in
sediment C:N ratios during the Holocene. If C:N ratios are
assumed to be relatively constant, then one has to assume
either a decline in global nitrogen uptake percentages (not
supported by sediment 15N values, [Sigman et al., 1997a] or
shifts in carbon burial efficiencies (again not supported by
the sediment record). Finally, significantly higher fixed
nitrogen inventories are at odds with studies suggesting
increased nitrogen uptake in surface oceans during the last
interglacial [Sigman and Boyle, 2000a], when presumably
these inventories would have been at their highest [Ganeshram et al., 2000].
[33] The alternative position is to assume that fixation
rates are much greater than those presently assumed and that
the Holocene nitrogen budget is close to being balanced.
This implies fixation rates 2 – 3 times the currently accepted
values. In this case, the difficulties with a shifting marine
nitrogen inventory are replaced with difficulties in justifying
high fixation rates. The highest such estimates (110 Tg
yr1) are given by Gruber and Sarmiento [1997] and even
though direct observations have begun to support such a
rate [Capone, 2001; Carpenter and Romans, 1991], a rate
double than this is controversial. The discrepancy may be
due to under- or insufficient sampling and methodological
problems [Lipschultz and Owens, 1996], or very tight
coupling between diazotrophs and other phytoplankton
species [Carpenter et al., 1999; Villareal, 1994]. Although
there are no definitive answers yet, there are some intriguing
studies which suggest that existing fixation studies seriously
underestimate total fixation. Sachs and Repeta [1999]
reported that the d15N of nitrate in the deep eastern Mediterranean is about 1%. They estimated that 40% of this
pool came from fixation, but given the published d15N
values of diazotrophs [Capone et al., 1998], this number
may be an underestimate. Several studies, including those
by Montoya et al. [2002], Sigman [1998], and J. A. Brandes
and A. L. Devol (unpublished data) have indicated that the
north Atlantic is isotopically depleted compared to the
southern ocean (<4% versus 4.8% [Sigman et al.,
2000b]. Given the small amount of deepwater exchange
with the Mediterranean (0.2 Sv, [Kinder and Parrilla,
1987]), it is likely that most is from local diazotroph
sources. If one assumes a value of 1% for this source,
then nitrogen fixation is responsible for roughly one sixth of
all nitrogen used by surface producers in the north Atlantic
alone. This is not unreasonable as at times the amount of
productivity fueled by fixation exceeds that from vertical
diffusion of nitrate [Carpenter et al., 1999]. It is more
difficult to assess the amount of nitrogen fixation in the
other basins, as there is either a paucity of data (South
Atlantic, South Pacific and South Indian Oceans) or the
presence of suboxic regions adds a second, enriched isotopic signal. Enriched nitrogen from the ETNP suboxic
region can be observed in the western Pacific [Liu et al.,
1996] and as far north as California [Emmer and Thunell,
2000; Liu and Kaplan, 1989]. Thus the lack of depleted
nitrogen in Pacific and Indian Ocean waters may not
indicate a lower amount of nitrogen fixation, but instead
indicate the presence of this additional denitrification signal
that masks the fixation signal.
5. Conclusions
[34] Recent work has made it apparent that the marinefixed nitrogen cycle is very dynamic, and has been so for
some time. This work and that of Middelburg et al. [1996]
suggest a very high rate of sediment denitrification, in the
order of 280 Tg N yr1. It is important to note that these two
estimates are based upon entirely different methodologies.
Middelburg et al. [1996] based their value upon a bottomup mechanistic model of sedimentary denitrification which
was scaled up using empirical relationships between global
carbon fluxes and ocean bathymetry. Our estimate is a ‘‘topdown’’ estimate using isotopic and mass balances. Given
that estimates for terrestrial and atmospheric nitrogen sources may have been overestimated due to anthropogenic
inputs [Seitzinger and Kroeze, 1998], this leads to a nitrogen
budget that is dominated by two terms: nitrogen fixation
and denitrification. The exact level of nitrogen fixation is as
yet unknown, but we argue that it must be far greater than
the 100-Tg N yr1 rates discussed in the literature. Our
Holocene isotope budget implies a marine nitrogen residence time of 1600 years (sum of loss rates/reservoir size).
Given this rapid turnover time, slight changes in source and
sink rates can have serious effects upon global productivity
and CO2 levels [Ganeshram et al., 2000]. Most of the fixed
nitrogen budget terms are centered upon the upper ocean or
at interfaces (land/sea, sediment/water, air/sea). Thus
changes may take place even more quickly than implied
by the overall residence time. Although short-term shifts
are likely [Ganeshram et al., 2000; Pride et al., 1999],
the existence of a long-term imbalance is unlikely given
the lack of evidence in the sediment record. Finally, the
disparate nature of the isotopic signatures implied by the
three major terms (nitrogen fixation, sediment denitrification, and water column denitrification) suggests that more
detailed studies of present and past marine 15N signatures
could yield useful information on relative shifts in these
three terms. For example, examining a detailed suite of
nitrate isotopic values from the different ocean basins could
provide an estimate of the relative contributions of N2
fixation and sediment denitrification on a basin-wide scale.
This possibility is suggested by the observed differences in
nitrate d15N values between Atlantic, Indian and Pacific
Ocean deep waters, as noted earlier. Furthermore, given
previously reported shifts in water column denitrification
rates [Altabet et al., 1995, 1999a; Ganeshram and Pedersen, 1998; Ganeshram et al., 1995, 2000] it is highly likely
that Pleistocene marine d15N nitrate values did not remain
constant, as is assumed/implied by most researchers, but
may have decreased during glacial interludes to reflect
reduced losses of isotopically light fixed nitrogen in suboxic
regions. Establishing a global fixed nitrogen isotopic signature during past era may well require examining sediment
d15N signatures from a wide range of locations (especially
those away from likely suboxic regions), but could provide
a strong constraint upon past global marine-fixed nitrogen
budgets.
[35] Acknowledgments. We thank Paul Quay for the use of his stable
isotope laboratory facilities. David Wilbur provided assistance in operating
the mass spectrometer and in data analysis. Michael McClain provided the
Amazon River and Amazon Tributary samples for d15N analysis. Lou
Codispoti and Jack J. Middelburg provided comments that greatly
improved this submission. This work was supported by NSF grants OCE
91-16275 and OCE 94-16626 (A.H.D) and by the Department of Defense
NDSEG fellowship program (J.A.B.).
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J. A. Brandes, Marine Sciences Institute, The University of Texas,
Austin, 750 Channel View Drive, Port Aransas, TX 78373, USA.
([email protected])
A. H. Devol, Department of Oceanography, University of Washington,
Seattle, WA 98125, USA.

A global marine-fixed nitrogen isotopic budget

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