Progress in Oceanography 65 (2005) 145–158

Progress inOceanography

www.elsevier.com/locate/pocean

The nitrogen cycle in the Arabian Sea

Hermann W. Bange a,*, S. Wajih A. Naqvi b, L.A. Codispoti c

a Forschungsbereich Marine Biogeochemie, Leibniz-Institut fur Meereswissenschaften, Dusternbrooker Weg 20, 24105 Kiel, Germanyb National Institute of Oceanography, Dona Paula, Goa 403 004, India

c Horn Point Laboratory, University of Maryland Center for Environmental Science, Cambridge, MD 21613-0775, USA

Available online 29 April 2005

Abstract

Despite their importance for the global oceanic nitrogen (N) cycle, estimates of N fluxes in the Arabian Sea remain in

considerable uncertainty. In this report, we summarize current knowledge of important processes, including denitrifi-

cation, N2 fixation and nitrous oxide emissions. Additionally, we discuss anthropogenic impacts on the N cycle in the

region. Existing studies suggest that the Arabian Sea is a significant source of N2O, and a major sink for fixed-N mainly

due to enhanced rates of denitrification that occur in suboxic portions of the water column in the Arabian Sea. Sedi-

mentary denitrification is small compared to water column denitrification, and additions of fixed-N via N2 fixation also

are small compared to pelagic denitrification. As a consequence, the fixed-N budget of the Arabian Sea is dominated by

an advective supply from the south, and by the sink arising from pelagic denitrification. Although relatively small com-

pared to the advective supply, inputs of fixed-N from runoff and from the atmosphere may have significant impacts on

surface waters and on the coastal waters of western India, and these inputs are rising because of human activities. Over-

all, the Arabian Sea�s nitrogen cycle is likely to respond sensitively to climate change and, in turn, have an impact on

climate via its N2O and denitrification components.

� 2005 Elsevier Ltd. All rights reserved.

Keywords: Denitrification; Nitrogen fixation; Nitrous oxide; Indian Ocean; Arabian Sea

1. Introduction

The oceans play a very significant role in global budgets of key biogenic elements including nitrogen

(N) as highlighted in recent reviews of the oceanic nitrogen cycle by Capone (2000), Codispoti et al.

(2001), and Zehr and Ward (2002). Within the oceans, the contribution of the Arabian Sea to biogeo-

chemical cycling of N is disproportionately large. For example, it is one of three major sites where

fixed-N (e.g., nitrate, NO�3 ) is transformed in the water column to dissolved gaseous nitrogen (N2). This

0079-6611/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.pocean.2005.03.002

* Corresponding author. Tel.: +49 431 600 4204; fax +49 431 600 1515.

E-mail address: hbange@ifm-geomar.de (H.W. Bange).

146 H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158

process, called pelagic denitrification (to distinguish it from sedimentary denitrification), also occurs at

comparable magnitude in regions of the eastern tropical North Pacific Ocean and the eastern tropical

South Pacific Ocean. Denitrification is the major loss term for fixed-N in the global N cycle and is there-

fore crucial for controlling the oceanic inventory of nitrogen (Codispoti et al., 2001). The Arabian Sea is

also a ‘‘hot spot’’ for nitrous oxide (N2O) emissions to the atmosphere. This is particularly important inview of the fact that N2O is an atmospheric trace gas, which directly and indirectly influences Earth�sclimate. In the troposphere, N2O acts as a greenhouse gas, and in the stratosphere it is involved in ozone

cycling (Montzka et al., 2003; Prather et al., 2001).

The three aspects of the N cycle in the Arabian Sea that we focus on are denitrification, N2O cycling, and

N2 fixation; the understanding of the first two has been greatly improved as a result of the Joint Global

Ocean Flux Study (JGOFS) – Arabian Sea Process Study. Processes of apparently minor significance to

the N cycle of the Arabian Sea, such as input of N compounds from marginal seas (Persian Gulf and

Red Sea), N sedimentation and emissions of ammonia are not addressed. For further details about theseprocesses, the reader is referred to overview articles by Naqvi, Noronha, Shailaja, Somasundar, and Sen

Gupta (1992) and Bange et al. (2000). We do consider atmospheric and riverine N inputs within the context

of anthropogenic impacts. Major fluxes of the N cycle in the Arabian Sea are summarized in Fig. 1.

2. Denitrification

Denitrification – the bacterial conversion of fixed nitrogen to N2 – is one of the most important processesin the N cycle because it refluxes back to the atmosphere some of the N added to the ocean through N2

fixation, atmospheric deposition and river runoff (Codispoti et al., 2001). The sequence of nitrogeneous

products involved in canonical denitrification may be summarized as: NO�3 ! NO�

2 ! NO !N2O ! N2 (Knowles, 1996), but the importance of alternate pathways to N2 are becoming evident

(e.g., Codispoti et al., in press). Our definition of pelagic denitrification includes all microbially mediated

Shelf sediments

Photic Zone

Troposphere

(Export flux)

P : D33

32

3.3

N2 fixation

N2

(Diffusion)

(New production)

6

Sun

hν

(Remin.)(Sed. rem.)

N assimilationduring photosynthesis

PONDIN

N2O

0.2-0.4

SD :0.4-3.5Advective Input

Advective Input

N2

Fig. 1. Simplified scheme of the N cycling in the Arabian Sea north of 6�N. All fluxes are given in Tg N yr�1. DIN stands for the sum

of dissolved inorganic nitrogen ðNO�3 ; NO�

2 and NHþ4 Þ and PON stands for particulate organic nitrogen. The denitrification fluxes are

abbreviated as follows: PD, pelagic denitrification and SD, sedimentary denitrification. Sed. rem. stands for remineralization of PON

in the shelf sediments.

H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158 147

processes that convert fixed-N to dinitrogen (N2). These processes are enhanced when oxygen is depleted

and high denitrification rates are largely confined to sediments and a few well-defined zones in the water

column that experience complete or nearly complete oxygen (O2) exhaustion.

One of our planet�s major sites of enhanced denitrification in the water column is in the Arabian Sea

which contains one of the most pronounced oxygen minimum zones (OMZs) found anywhere in the world�socean. Its vertical span is largest in the northeastern sector where O2 concentrations are <5 lM between

�150 and 1200 m and <1 lM within the upper half of this depth range (Fig. 2). In the Atlantic and Pacific

Oceans the most severe O2 depletion occurs in the east. The northwesterly location of the site of maximal

O2 depletion in the Indian Ocean is thus unusual, and is apparently related to its low latitude northern

boundary. The resulting monsoon forcing brings about large-scale fertilization of surface waters through

upwelling in summer and convective mixing in winter. These nutrient inputs sustain high rates of carbon

dioxide (CO2) fixation in the surface layer and support the export of particulate organic matter to the deep

sea [estimated to be 84–91 Tg Carbon (C) yr�1 through the 100 m horizon for the region bounded by 6�Non the south and the 2-km depth contour (Rixen, Guptha, & Ittekkot, 2005)]. Moreover, the low-latitude

boundary prevents the establishment of a deep convective regime in the northern Indian Ocean. Conse-

quently, the O2 demand for organic matter decomposition cannot be met by local production of well-oxy-

genated intermediate waters. The water masses formed in the two marginal seas, the Persian Gulf and the

Red Sea, do bring about some ventilation at mid-depths, but the total amount of O2 transported by these

outflows probably does not exceed 1 T mol yr�1, which would support the decay of only about 10% of the

carbon exported to depth. Therefore, most of the mesopelagic O2 renewal should be through advection of

waters from the south. However, since equatorial dynamics act as a barrier for inter-hemispheric water ex-change, such advection is concentrated along the western boundary during the Southwest (SW) Monsoon

(Schott & McCreary, 2001). Although the total volume of intermediate water flowing into the Arabian Sea

Fig. 2. Distributions of (a) O2 (lM) and (b) NO�2 ðlMÞ in the upper kilometer along the track of TN039 cruise of US JGOFS

(September–October, 1994). The inset in (b) shows the station locations and the approximate geographical extent of the Arabian Sea�s‘‘permanent’’ denitrification zone as demarcated by the 0.5 M NO�

2 contour (Naqvi, 1991).

148 H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158

is fairly large (�5 · 106 m3 s�1), the associated O2 supply is quite modest because of the long trajectories of

flow from the source regions in the southern hemisphere (Olson, Hitchcock, Fine, & Warren, 1993; Swal-

low, 1984; Warren, 1994). Nonetheless, renewal by these waters, as well as by those formed in the adjacent

marginal seas, maintains generally southeast–northwest gradients in O2 (Fig. 2).

As the O2 levels decline farther from the points of renewal and fall below a value of �1–5 lM (�0.02–0.11 mL L�1), there occurs a shift to what is often referred to as the suboxic ecosystem. Under these con-

ditions, facultative heterotrophs switch over to alternate respiratory oxidants (electron acceptors) such as

NO�3 ; IO

�3 , and Mn(IV) with NO�

3 being the most abundant in seawater (e.g., Codispoti et al., in press). A

major portion of the biological conversion of fixed-N to N2 arises from canonical denitrification

ðNO�3 ! NO�

2 ! N2O ! N2Þ as described above, but there are several other potential pathways for N2

production such as the anaerobic ammonium ðNHþ4 Þ oxidation (anammox), NO�

2 þNHþ4 ! N2 þ 2H2O

(Codispoti et al., in press; Devol, 2003). The accumulation of nitrite ðNO�2 Þ, the first intermediate of deni-

trification, provides a diagnostic tool for its occurrence (Fig. 2(b)) within the OMZ. The zone of denitrifi-cation in the Arabian Sea is fairly well demarcated (Fig. 2(b), inset), but denitrification at low rates may

occur outside this zone without much accumulation of NO�2 (e.g., Codispoti et al., 2001). The denitrifica-

tion zone is most intense in the open central Arabian Sea. Occurrences of suboxic conditions with accumu-

lation of NO�2 occur only sporadically beneath the highly productive coastal upwelling sites in the western

Arabian Sea, apparently because this region is more effectively ventilated as pointed out above (note, for

example, the significantly higher O2 concentrations and the absence of NO�2 in the northernmost part of

the US JGOFS section, stations associated with the Persian Gulf Outflow; Fig. 2(a)).

During the last 25 years there have been several attempts to quantify the amount of N lost by pelagicdenitrification in the Arabian Sea. These estimates are based largely on calculations of NO�

3 deficits quan-

tified as the departure of observed NO�3 concentrations from the values expected from some combination of

other physico-chemical properties such as temperature, salinity, O2 and phosphate ðPO3�4 Þ. The earliest esti-

mate was in the range from 0.1 to 1 Tg (=1012 g) N yr�1 (Deuser, Ross, & Mlodzinska, 1978). However, this

value has since undergone substantial upward revision due both to new, high-quality NO�3 data sets and the

application of improved deficit estimation and extrapolation approaches. Recently published values mostly

lie in the range of 21–34 Tg N yr�1 (Bange et al., 2000; Howell, Doney, Fine, & Olson, 1997; Naqvi, 1987).

That N2 is the dominant end product of denitrification is evident from large increases in N2/Ar ratiowithin the denitrifying zone as compared to those ratios outside this zone, but the excess N2 inventory com-

puted from the N2/Ar data may substantially exceed NO�3 deficits implying that the NO�

3 deficit approach

might lead to a systematic underestimation of the microbial production of N2 (Codispoti et al., 2001). This

is in part due to the fact that the denitrified nitrogen is derived not only from NO�3 undergoing reduction

but also from NHþ4 and organic N that are oxidized by NO�

3 and possibly also by other electron acceptors

such as IO�3 , Fe(III) and Mn(IV) (e.g. Codispoti et al., 2001; Farrenkopf, Luther, Truesdale, & Van der

Weijden, 1997; Luther, Sundby, Lewis, Brendel, & Silverberg, 1997). In addition, the organic substrates

used by denitrifiers may have N:P ratios higher than the traditionally employed Redfield ratios (Codispotiet al., 2001; Van Mooy, Keil, & Devol, 2002).

Pelagic denitrification rates in the Arabian Sea also have been estimated following an enzymatic ap-

proach involving the activity of the respiratory electron transport system (ETS). In this method, activity

of the enzyme system that controls respiration is measured by extracting the enzymes from microorganisms

and incubating the extract with an electron acceptor and natural substrates of the enzyme system. However,

this technique yields potential rates that need to be converted into denitrification rates using a suitable con-

version factor. While the denitrification rate so deduced (24–33 Tg N yr�1) has been found to compare well

with that derived from the physico-chemical technique, it should be pointed out that the latest stoichiom-etric relationships (e.g., Van Mooy et al., 2002) and newly appreciated pathways such as the anammox reac-

tion could produce more N2 for a given respiratory electron flow than originally contemplated (e.g.,

Codispoti et al., in press). Finally, model studies by Yakushev and Neretin (1997) and Kawamiya and

H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158 149

Oschlies (2003) led to estimates of 11–24 and 34 Tg N yr�1, respectively, comparable to the above-men-

tioned NO�3 -deficit and ETS-based estimates. However, as in the case of the ETS-based estimates, these

models did not incorporate all of the latest information on pathways and stochiometry. Codispoti et al.

(2001) suggested that the current global pelagic denitrification rate might in fact be as high as 150 Tg N

yr�1, much higher than the generally accepted value of �80 Tg N yr�1 (Gruber & Sarmiento, 1997), witha contribution of �40% (60 Tg N yr�1) coming from the Arabian Sea alone. A more detailed investigation

of total N2 production is needed to settle this issue.

In addition to the perennial suboxic zone of the open ocean, denitrifying conditions also develop

seasonally (during late summer and autumn) over the continental shelf off western India. Upwelling oc-

curs along this coast during summer and autumn due to both local and remote forcing by monsoon

winds (Shetye & Gouveia, 1998). The upwelled water is O2-depleted to begin with, but not suboxic.

However, as it moves up the shelf it loses O2 due to the degradation of organic matter sinking from

productive surface waters. The O2 deficiency is accentuated by the presence of a warm, low-salinity lensformed due to the intense rainfall in the coastal zone; the low salinity lens floats over the cold, saline

upwelled water resulting in strong near-surface stratification. The sub-pycnocline waters in the inner

and mid-shelf regions turn suboxic by mid-summer (July) supporting intense denitrification. Denitrifica-

tion often removes all NO�3 , and as sulphate reduction sets in, NHþ

4 accumulates in the anoxic subsur-

face waters. With the reversal of coastal circulation, the water column becomes oxygenated again in

November. Although O2 deficiency in the shallow waters of this region is primarily of natural origin

and has been known to exist since the 1950s (Banse, 1959; Carruthers, Gogate, Naidu, & Laevastu,

1959), it has probably intensified in recent years as a result of coastal eutrophication (Naqvi et al.,2000). The overall impact of denitrification in the shallow, seasonal suboxic zone is smaller than in

the deep water denitrification zone, probably amounting to no more than 5 Tg N yr�1, even though

the specific rate is much higher, up to 1 lmol NO�3 L�1 d�1 (Naik & Naqvi, 2002), than in the

deep-water denitrification zone.

Denitrification in the Arabian Sea also seems to undergo substantial temporal variability on scales rang-

ing from seasonal to geological (Morrison et al., 1998; Naqvi, Noronha, Somasundar, & Sen Gupta, 1990).

This variability has the potential to alter the oceanic nitrogen inventory and hence the capability of the oce-

anic biological pump to sequester atmospheric CO2 thereby affecting climate. There is a growing body ofevidence indicating that large changes in denitrification intensity did indeed occur in conjunction with the

global climate changes in the past (Altabet, Higginson, & Murray, 2002; Suthhof, Ittekkot, & Gaye-Haake,

2001). This evidence is based on 15N/14N data in sedimentary organic matter, an approach involving the

following premise: NO�3 is seldom removed completely in the open ocean suboxic zone, and denitrification

in the water column strongly fractionates N isotopes, rendering the residual NO�3 isotopically heavy

(d15N � 15 per mil) (Brandes, Devol, Jayakumar, Yoshinari, & Naqvi, 1998). This value is much higher

than the average isotopic composition of NO�3 dissolved in deep-water; deep-water NO�

3 is geographically

highly invariant at �5 per mil (Sigman, Altabet, McCorkle, Francois, & Fischer, 2000). As the upwelling ofthis NO�

3 would tend to increase 15N/14N in sinking particulate organic nitrogen, the isotopic ratio in sed-

iments should in some way reflect the intensity of denitrification at the time they were deposited. Fraction-

ation of isotopes also occurs during NO�3 assimilation by phytoplankton. Consequently, partial utilization

of NO�3 can also produce 15N-enrichment in organically bound nitrogen. However, such a scenario is un-

likely in the Arabian Sea where NO�3 brought up from the thermocline is eventually fully consumed in the

surface layer.

Downcore records of d15N in sediments do in fact show large oscillations that are remarkably similar

in structure and timing to the interstadial (Dansgaard/Oeschger) events recorded in Greenland ice cores(Altabet et al., 2002; Suthhof et al., 2001). The magnitude of these oscillations is too large to be caused

by any changes in isotopic composition of NO�3 in source waters, and it is reasonable to assume that

they represent changes in intensity of denitrification in the Arabian Sea. When smoothed with a

150 H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158

3000-year running average, to account for the dampening effect of the residence time of nitrogen in the

ocean, the patterns of changes in d15N in the sediment cores from the Arabian Sea are remarkably sim-

ilar to those in temperature proxies and CO2 in Antarctic ice cores (Altabet et al., 2002). Pelagic deni-

trification in this region could thus play a role in modulating the climate of our planet on geological

time scales.While our knowledge of pelagic denitrification in the Arabian Sea has been considerably advanced by

recent studies, less effort has been directed at studying this process in Arabian Sea sediments. Sediments

along the Indian and Pakistani coasts are expected to experience vigorous denitrification due to the high

biological productivity of the overlying waters. The only available estimates of sedimentary denitrification

from this region, however, are derived from a few acetylene block-based measurements from the central

west coast of India during the upwelling period (Naik & Naqvi, 2002). The results of this study, when

extrapolated to all Arabian Sea shelves, lead to modest sedimentary denitrification rates (0.4–3.5 Tg N

yr�1). However, these observations were made during periods when suboxic conditions prevailed in thenear-bottom waters. Such conditions are expected to result in lower estimates of sedimentary denitrification

rate for several reasons. First, the supply of NO�3 to sediments from the overlying water column would be

limited by low NO�3 concentrations in the overlying water. Second, both reduced bioturbation and low bot-

tom water O2 concentrations might inhibit coupling of nitrification and denitrification because a major por-

tion of the NO�3 undergoing reduction in sediments overlain by oxygenated waters results from the

oxidation of NHþ4 (Devol, 1991). Finally, under these conditions the acetylene block technique itself

may underestimate the denitrification rate by as much as 30–50% (Seitzinger, Nielsen, Caffrey, & Christen-

sen, 1993). Notwithstanding these limitations, the results obtained suggest that sedimentary denitrificationprobably plays a minor role in nitrogen cycling in the Arabian Sea.

Denitrification is undoubtedly a major process affecting the biogeochemical cycles in the Arabian Sea.

According to the stoichiometric relationship proposed by Richards (1965), the molar ratio between organic

carbon oxidized and NO�3 reduced is 106:94.4. This implies that the denitrification rate occurring in deep-

water accounts for the mineralization of roughly one-third (�30 Tg C yr�1) of the particulate organic car-

bon (POC) exported below 100 m in the Arabian Sea as a whole. Locally, however, the supply of POC

through sedimentation from the surface does not appear to be sufficient to meet the carbon requirement

within the suboxic zone as inferred from data on bacterial production (Ducklow, 1993; Ducklow, 2000)as well as ETS activity (Naqvi & Shailaja, 1993; Naqvi et al., 1993). In fact, respiration rates are not only

higher within the suboxic zone, as compared to those just above it, but the denitrifying layer is also asso-

ciated with a pronounced intermediate nepheloid layer (INL; Morrison et al., 1999; Naqvi et al., 1993). It is

believed that the INL is largely composed of bacteria, most of which are genetically capable of denitrifica-

tion (B.B. Ward, unpublished). On the other hand, the increased zooplankton biomass close to the lower

suboxic–oxic boundary (O2 � 0.05–0.1 mL L�1, 2.2–4.5 lM) implies an abundant supply of relatively fresh

organic matter that may have escaped degradation in the overlying suboxic layer (Wishner, Gowing, &

Gelfman, 1998). One possible explanation of this apparent discrepancy is that the denitrifying bacteriamay also utilize carbon other than, or in addition to, that sinking directly from the surface, a subject that

has not yet been adequately addressed.

What balances the loss of fixed-N in the Arabian Sea? There are modest riverine and atmospheric inputs,

and inputs from nitrogen fixation that we will discuss later, but most of the re-supply is in the form of dis-

solved NO�3 in the water masses entering the Arabian Sea from the south. A recent estimate of the N input

flux via the advection of waters from the south is 38 Tg N yr�1, of the same magnitude as recent estimates

of the net excess of local sinks over local sources (Bange et al., 2000). While the waters entering the Arabian

Sea at mid-depths are O2-depleted, they contain NO�3 in high concentrations such that denitrification in the

open Arabian Sea never results in complete exhaustion of NO�3 . This prevents the occurrence of full anoxia

in the mesopelagic Arabian Sea, since respiration supported by NO�3 proceeds almost to completion before

the onset of sulphate reduction.

H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158 151

3. Nitrogen fixation

While most photosynthetic organisms are not equipped to utilize N2 as a nutrient because of the high

strength of the N„N bond, a few cyanobacteria are capable of reducing N2 to NHþ4 , commonly known

as ‘‘fixing’’ nitrogen. The Arabian Sea is known to be an active site for this process (Capone et al.,1998; Devassy, Bhattathiri, & Qasim, 1978). One factor that favors the growth of N2 fixers in the Arabian

Sea is the NO�3 deficit arising from local and far-field denitrification. The NO�

3 : PO3�4 ratio is substantially

lower than 15 at all depths in the Arabian Sea (e.g., Morrison et al., 1998). As the N-deficient subsurface

waters are brought to the surface through upwelling and vertical mixing, the nutrients are taken up by the

phytoplankton in a (Redfield) ratio of �15 (by atoms), and this leads to a surplus of PO3�4 in surface waters.

This excess PO3�4 is observed most strikingly within the coastal anoxic zone where PO3�

4 concentrations in

excess of 3 lM occur when denitrification removes all dissolved NO�3 (Fig. 3). The organisms that fix N2

also require relatively large amounts of iron (Fe), which could be supplied by atmospheric deposition,mobilization from shelf and slope sediments, upwelling, and vertical entrainment from more Fe-replete,

subsurface layers. Consequently, blooms of N2 fixing cyanobacteria (mainly Trichodesmium spp.) occur

over large parts of the Arabian Sea, mostly during the Spring Intermonsoon season when surface waters

are NO�3 -depleted. During this season, calm seas allow the establishment of warm surface waters, reduced

turbulence and high euphotic zone light intensities, conditions that also favor nitrogen fixation (Capone,

Zehr, Paerl, Bergman, & Carpenter, 1997; Capone et al., 1998; Devassy et al., 1978).

Apart from the experimentally measured N2-uptake rates (Capone et al., 1998; Dugdale, Goering, &

Ryther, 1964), evidence for N2-fixation in the Arabian Sea is also provided by data on natural isotopeabundances in NO�

3 (Brandes et al., 1998). Within the core of the denitrifying layer, the d15N of NO�3

reaches a maximum of �15 per mil due to the strong isotopic fractionation associated with denitrification.

If NO�3 within the euphotic zone were to be derived solely from subsurface waters, the high d15N values

occurring within the denitrifying zone should influence the surface layer, even if we ignore the fractionation

associated with NO�3 assimilation by phytoplankton which also enriches 15N in NO�

3 . The observations

actually show a sharp decrease in d15N across the suboxic–oxic transition, with the value in the shallowest

sample that contains sufficient NO�3 for isotopic analysis being only slightly higher than the oceanic average

(�6 per mil; (Brandes et al., 1998). These results strongly suggest the existence of a source of light nitrogen

Fig. 3. Plot of dissolved inorganic phosphorus (DIP) versus dissolved inorganic nitrogen ðDIN ¼ NO�3 þNO�

2 þNHþ4 Þ for all

samples taken from depths <200 m. Triangles denote samples having NHþ4 concentration >0.5 mM, and the straight line represents the

Redfield N:P slope of 15 (modified from Naqvi et al., 2000) expected to arise from oxic regeneration of marine organic matter.

152 H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158

in the surface layer. This source is most likely N2 fixation as this process adds new, fixed N to surface waters

with an isotopic composition (�0 per mil) similar to that of atmospheric N2 (Brandes et al., 1998). The esti-

mated N2 fixation rate for the region is 3.3 Tg N yr�1 (Bange et al., 2000). However, the input of new N

through this process is greatly overwhelmed by the loss through denitrification, which is an order of mag-

nitude higher, as discussed above.

4. Nitrous oxide production

Nitrous oxide (N2O) is an important greenhouse constituent of the atmosphere which also plays a role in

ozone destruction in the stratosphere. The oceans serve as a significant source of atmospheric N2O. Follow-

ing the studies of Law & Owens (1990) and Naqvi & Noronha (1991), the upwelling-dominated, western

portion of the Arabian Sea was thought to be a ‘‘hot spot’’ for oceanic N2O emissions that might makea substantial contribution to the atmospheric budget of N2O. However, the Arabian Sea may be an even

larger source than originally suggested, because recent results show that seasonal N2O emissions from the

continental shelf of India are also important (Naqvi et al., 2000). On the basis of more than 2400 measure-

ments of N2O concentrations in the Arabian Sea surface layer, obtained during 16 cruises undertaken from

1977 to 1997, the emissions to the atmosphere have been recently reassessed (Bange et al., 2001a; Naqvi

et al., 2005). Based on these data, which do not include the high values observed by Naqvi et al. (2000) over

the Indian shelf, the annual N2O emissions ranged from 0.2 to 0.4 Tg N and were dominated by fluxes from

coastal regions during the Southwest (SW) and Northeast (NE) Monsoons. Thus, even if we ignore N2Oemissions from the Indian Shelf that might be enhanced by human activities (Naqvi et al., 2005), the

N2O flux from the Arabian Sea forms a very substantial fraction of the total annual oceanic flux (1.3–11

Tg N yr�1, Bange, Rapsomanikis, & Andreae, 1996; Nevison, Weiss, & Erickson, 1995; Suntharalingam

& Sarmiento, 2000).

What are the major pathways of N2O formation in the Arabian Sea? Upwelling regions, such as the east-

ern tropical Pacific Ocean and the Arabian Sea, have been recognized as sites of enhanced N2O production

via early-stage denitrification and/or nitrification (the microbial oxidation of NHþ4 ) at low O2 concentra-

tions, processes that occur at the boundaries of the associated OMZs (Codispoti et al., 1992; Suntharalin-gam, Sarmiento, & Toggweiler, 2000). On the basis of various studies of the N2O concentrations and

isotopic signatures in the central Arabian Sea, a scheme for the vertical distribution of N2O production

and consumption pathways has been proposed for the suboxic zone and adjacent waters (Bange, Rapso-

manikis, & Andreae, 2001b). This consists of four compartments (A-D) that could explain the characteristic

double-peak structure of N2O within the suboxic zone (Fig. 4).

Compartment A, 0–150 m. N2O is mainly produced by nitrification as indicated by DN2O–AOU corre-

lations (Bange et al., 2001b). However, the dual isotope signatures of N2O revealed that nitrification may

not be the only source. N2O may also be produced via coupling of nitrification and denitrification associ-ated with the steep O2 gradient at the top of the OMZ, forming the sharp N2O peak at about 150 m (Naqvi

et al., 1998).

Compartment B, 150–1000 m. N2O consumption occurs at 300–500 m, the denitrifying core of the OMZ.

At the lower boundary of the OMZ, N2O seems to be mainly produced by denitrification where the O2 con-

centrations are increasing again (Naqvi et al., 1998).

Compartment C, 1000–2000 m. In the central Arabian Sea, the denitrification signal (d15N of NO�3 ) is

assumed to be mixed down to 1500 m due to ventilation processes (Brandes et al., 1998). This implies that

N2O produced at the bottom of the OMZ is also mixed down, forming the broad second N2O peak. DN2O–AOU relationships are reasonably valid from 0 to 2000 m (Bange et al., 2001b). Thus, we conclude that

nitrification contributes significantly to N2O production throughout the water column. However, the

N2O produced by denitrification results in less clear DN2O–AOU relationships.

0

1000

2000

3000

0 20 40 60

N2O conc., nmol L-1

Wat

er d

epth

, m

D

C

B

A

Fig. 4. Overview of the processes responsible for the N2O vertical distribution in the central Arabian Sea at 20�N 65.8�E in May 1997.

(Bold solid line, measured dissolved N2O; dashed line, N2O theoretical equilibrium N2O concentration according to its atmospheric

concentration; thin solid line, measured O2.) Four compartments are indicated: A, <150 m, N2O from nitrification, at 150 m coupling

with N2O formation during denitrification; B, 150–1000 m, N2O reduction to N2 during denitrification; C, 1000–2000 m, N2O from

nitrification; >2000 m, N2O formation during nitrification with subsequent N2O reduction during denitrification within particles. For a

detailed discussion see Bange et al. (2001b).

H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158 153

Compartment D, below 2000 m. No statistically significant DN2O–AOU relationship was found (Bange

et al., 2001b). N2O produced by nitrification may be reduced subsequently by denitrification (Kim & Craig,

1990).

This scheme may also be valid for the western Arabian Sea; however, owing to complex hydrographic

conditions (e.g., seasonal variability, coastal upwelling, inflow of waters from the south and from the mar-

ginal seas), the N2O double-peak structure is not well established there. Furthermore, it is possible that

N2O at 600–800 m near the shelf break in the western Arabian Sea is formed via a different process such

as microbial oxidation of organic matter by reduction of iodate ðIO�3 Þ to iodide (I�) (Bange et al.,

2001b; Farrenkopf et al., 1997). These observations imply that the biogeochemical cycling of N2O in the

central and western Arabian Sea during the SW Monsoon is more complex than previously thought (Bange

et al., 2001b).

5. Anthropogenic impacts

The Arabian Sea is vulnerable to potential environmental and climatic changes arising from humanactivities. These include rapid population growth, intensification of agricultural activities including large

increases in the consumption of synthetic, N-based fertilizers, industrialization, and urbanization of coastal

zones in the major littoral countries (i.e., India, Pakistan and Iran). Bange et al. (2000) estimate that �1.2

Tg of N in the dissolved inorganic form is added annually to the Arabian Sea; this input represents about

29% of the total fixed-N in annual river runoff from South Asia (i.e., 4.2 Tg inorganic N; Seitzinger et al.,

2002), and increases in this input are likely. Because systematic, long-term investigations of biogeochemical

cycles are lacking, it is difficult to evaluate to what extent human activities have affected the biogeochemical

processes of the Arabian Sea. Nevertheless, there are indications that effects of human interference are al-ready beginning to be manifested in the N cycle of coastal areas.

The most convincing evidence in this regard comes from the eastern Arabian Sea where, as pointed out

earlier, coastal waters seem to have undergone a dramatic change during the last few years indicated by the

shift from seasonally low-O2 conditions (Banse, 1959; Carruthers et al., 1959) to suboxic and even anoxic

154 H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158

conditions (Naqvi et al., 2000). The most intriguing aspect of N cycling in the coastal, O2-deficient zone is

the enormous accumulation of N2O, resulting in record-breaking concentrations not observed previously

anywhere in the world�s ocean. Maximal N2O production seems to occur in waters experiencing intense

and relatively short-lived denitrification, a pattern that distinguishes the coastal suboxic system from the

one located offshore (also see Naqvi et al., 2005). This recent ecosystem shift is most likely a consequenceof increased fluxes of nutrients from land, but subtle changes in hydrography cannot be excluded as an

additional or alternate cause (Naqvi et al., 2000). The development of vast, temporarily occurring, coastal,

low-oxygen zones is not limited to the Arabian Sea. Such zones have also been observed in other coastal

areas such as the inner Gulf of Mexico (Goolsby, 2000) and the Namibian Coast off southwestern Africa

(Weeks, Currie, & Bakun, 2002). It has to be pointed out that the depletion of O2 in coastal waters will not

only lead to increased emissions of greenhouse gases such as N2O but will also change the food web struc-

ture and fisheries (Malakoff, 1998; Wu, 2002).

Today�s annual input of N by wet and dry aerosol deposition is estimated to be about 1.6 Tg N and thusrepresents a minor source of N for the Arabian Sea (Bange et al., 2000). However, as is the case for land

runoff, the atmospheric inputs of N through both dry and wet deposition are expected to increase steadily.

During the NE Monsoon, air masses from the Indian subcontinent are transported to the central Arabian

Sea where the NHþ4 - and NO�

3 -containing aerosols that originate from agriculture and combustion pro-

cesses fertilize the N-depleted surface waters. Bange et al. (2000) estimated that, today, up to17% of the

N demand in the surface layer of the central Arabian Sea during the NEMonsoon is being met by the depo-

sition of nitrogenous aerosols. Assuming that the amount of N aerosols will increase in the future, this

source can have impacts on both biogeochemical cycling and ecosystem structure.In an area such as the Arabian Sea, where denitrification is a major respiratory process at mid-depths,

the impact of eutrophication on biogeochemical cycles could be much more profound than it would be in

areas with oxygenated water columns, because of the differences between C:N ratios maintained during

photosynthesis and oxic respiration on the one hand and denitrification on the other (Codispoti et al.,

2001). That is, during photosynthesis (or oxic decay), the atomic uptake/regeneration ratio between C

and N is 6.6 in organic matter, but during denitrification the ratio decreases to �1 (Richards, 1965) and

perhaps less if some of the alternate pathways for N2 production prove to be important (Codispoti

et al., 2001). As a result, while 1 atomic unit of N fixed in the surface layer corresponds to approximately6.6 atomic units of organic carbon, the decay of only �1 atomic unit of organic carbon via denitrification

converts one unit of NO�3 to 0.5 unit of N2. The factor of 6.6 amplification of the eutrophication signal

could be important in determining future NO�3 concentrations in intermediate waters in the Arabian

Sea, as well as influencing the extent of NO�3 exhaustion and consequent anoxia (sulphate reduction) over

the Indian Shelf.

6. Summary

Although changes in inputs of N from atmospheric deposition and runoff can have significant impacts as

outlined above, two processes, denitrification and advective N input from the south (Fig. 1) dominate the

fixed-N budget of the Arabian Sea, and they are of similar magnitude. The role of N-fixation in the Arabian

Sea is still difficult to assess owing to the small database available. While there are hints that it might be

more important than previously thought, this source appears to be approximately an order of magnitude

less than the denitrification sink. Although the net production of N2O in the Arabian Sea and its contribu-

tion of N2O to the atmosphere are small terms in its fixed-N budget, the Arabian Sea is a globally signif-icant N2O source.

We have noted earlier that examinations of the geologic record suggest that denitrification in the Ara-

bian Sea has varied significantly over geologic time periods, and our discussion and some recent studies

External insolation forcing

Climate

Monsoon

EcosystemN2O

NO3- / O2

Indian Oceanintermediatecirculation

N2

??

Denitrification

N2 fixation

Fig. 5. Possible climate/Arabian Sea feedback scenario. The question marks indicate interactions yet to be quantified.

H.W. Bange et al. / Progress in Oceanography 65 (2005) 145–158 155

(e.g., Codispoti et al., 2001; Naqvi et al., 2000) suggest that denitrification rates and N2O production andconsumption respond sensitively to environmental conditions. We present a schematic diagram of the con-

nections and feed backs that may control the denitrification and N2O regimes in the Arabian Sea (Fig. 5).

Following the concept for the forcing mechanisms of the Indian Ocean Monsoon Regime presented by

Clemens, Prell, Murray, Shimmield, & Weedon (1991), the external insolation forcing via variations in

the Earth�s orbit results in an internal climate response with variations in the strength of the Arabian Sea�sSW Monsoon. Variations of the SW Monsoon�s strength lead, in turn, to variations in nutrient supply to

the surface layer by coastal upwelling. Additionally, a change in the climate may also influence the inter-

mediate circulation of the Indian Ocean leading to changes in the supply of NO�3 and O2 to the Arabian

Sea. These processes feed back to the global climate system by modulating the N2O source term and by

impacting the ability of the oceanic biological pump to sequester atmospheric carbon dioxide. Sequestra-

tion depends partially on the impact of denitrification on concentrations of NO�3 , one of the limiting nutri-

ents for phytoplankton growth. We suggest that the processes outlined in Fig. 5 are worthy of inclusion in

models that seek to produce realistic scenarios of the ocean�s response to climate change.

Anthropogenic impacts on the N cycle might already be observable along the Indian continental shelf

areas, where the temporary shift of the coastal ecosystem from oxic to suboxic and anoxic conditions leads

to increasing denitrification and associated N2O emissions to the atmosphere (Naqvi et al., 2000).

Acknowledgements

We acknowledge the helpful comments of Karl Banse, Jerry Wiggert and two anonymous reviewers. The

investigations were supported financially by the Max Planck Society, the Institute for Marine Research,

Kiel, the German Bundesministerium fur Bildung, Wissenschaft, Forschung und Technologie through

Grants 03F0137A, 03F0183G and 03F0241C, the Council of Scientific & Industrial Research, New Delhi,the US National Science Foundation, and the US Office of Naval Research.

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