Nitrogen biogeochemical cycling in the northwestern Indian Ocean

Deep-Sea Research1L Vol.40, No. 3, pp. 651~071,1993. Printedin Great Britain.

09674~645/93 $6.00+ 0.00 PergamonPressLtd

Nitrogen biogeochemical cycling in the northwestern Indian Ocean R . F A u z I C. MANTOURA,* CLIFFORD S. LAW, NICHOLAS J. P. OWENS, PETER H . BURKILL, E . MALCOLM S. WOODWARD, ROBIN J. M . HOWLAND a n d CAROLE A . LLEWELLYN (First received 12 April 1991 ; in revised form 2 October 1992; accepted 28 October 1992)

Abstract--The vertical distribution and fine scale structure of nitrate (NO 3), nitrite (NO 2), nitrous oxide (N20), phosphate (PO4) , oxygen (02) and chlorophyll a (chl a) were determined in the North Western Indian Ocean (NWIO) along a meridional section (67°E) from the Equator to the Gulf of Oman using an Autoanalyser for micromolar levels of nutrients, and chemiluminescence and gas chromatographic methods for nanomolar levels of NO 3 and NO2 and N20 respectively. Three biogeochemically contrasting regimes were investigated: (1) the highly oligotrophic nutrient-depleted subtropical gyre; (2) the monsoonal upwelling of nutrient-rich intermediate waters off the southeastern Arabian Coast; and (3) the denitrifying Oz-depleted zone (ODZ; ca 150-1200 m depth) in the Arabian Sea. Concentrations of NO 3 and NO 2 were severely depleted in surface oligotrophic waters from the equator (average 43 and 3.6 nM respectively) to the subtropical gyre (12-15°N; average 13.3 and 2.0 nM respectively) with similar levels in the more stratified Gulf of Oman. Upwelling waters off Southern Arabia had three orders of magnitude higher NO 3 levels, and throughout the NWIO, the calculated NO3-fuelled primary production appeared to be regulated by NO 3 concentration. Existing Redfield AO2/ANO 3 regeneration ratios (=9.1) previously derived for the deep Indian Ocean were confirmed (= 9.35) within the oxic upper layers of the NWIO. The "NO"-potential temperature relationship (BROECKER, 1974, Earth and Planetary Science Letters, 23, 100-107) needed for the derivation of expected NO3 and NO3-deficits within the denitrifying ODZ were refined using an isopycnal, binary mixing model along the o 0 = 26.6%0 density layer to take into account the inflowing contribution of NO3-depleted Persian Gulf Water. Vertically integrated NO3-deficits increased northwards from 0.8 mol NO3-N m -2 at Sta. 2 (04°N), up to 6.49 mol NO3-N m 2 at Sta. 9, at the mouth of the Gulf of Oman, then decreased to 4. I0 moles NO 3-N m 2 toward Sta. 11, near the Straits of Hormuz. When averaged for the denitrification area of the Arabian Sea, this corresponds to a deficit of 118 Tg NO3-N. Adopting a recent Freon-ll based estimate of water residence time of 10 years (OLsoN et al., 1993, Deep-Sea Research H, 40, 673685) for the Oz-depleted layer, we calculate an annual net denitrification flux of 11.9 Tg N to thc atmosphere or approximately 10% of the global water column denitrification rates. Supersaturated N20 concentrations were found in both surface oxic and upwelling waters (up to 246%) and peaked at the base of the ODZ (up to 1264%) in the northern Arabian Sea. Both nitrification in oxic waters and denitrification in hypoxic layers can be invoked as sources of N20. The inventory of excess N20 amounted to 2.55 _+ 1.3 Tg NzO-N , corresponding to annual production of 0.26 + 0.13 Tg from denitrification. This is comparable to earlier (LAW and OWEYS, 1990, Nature, 346, 826-828) estimates of the ventilation flux of NzO (0.22~).39 Tg yr-1 ) from the upwelling region of the Arabian Sea. The decadal response times for circulation, deoxygenation, denitrification and ventilation of the ODZ-derived NzO and CO 2 greenhouse gases and their monsoonal coupling implies the Arabian Sea is a sensitive oceanic recorder of global climate change.

*Author to whom correspondence should be addressed at: Plymouth Marine !,aboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, Devon, United Kingdom. 651

652

R.F.C. MANTOURAet al. INTRODUCTION

NUTRIENTcycling in the northwestern Indian Ocean (NWIO) uniquely encompasses three biogeochemically extreme and globally important regimes (see reviews by QASIM, 1982; ZEITZSCHEL,1973; SEN GUPTA and NAQVI, 1984) including: (1) monsoonal upwelling of nutrient-rich and hence productive waters in the Arabian Sea (BANSE and MCCLAtN, 1986); (2) the oligotrophic subtropical gyre; and (3) the denitrifying oxygen-depleted zone (ODZ) at intermediate depths (150-1200 m). These three biogeochemical provinces arise from the unique combination of climate, circulation and geology (SWALLOW, 1984; WYRTKI, 1971; ZEITZSCHEL, 1973). Although the oxygen-deficient conditions in the Arabian Sea have been known since the John Murray Expedition in 1932-1934 (GILSON, 1937), it is only in the last 15 years that detailed aspects of the chemical and microbial oceanography of nitrogen (N) have been investigated (see reviews by SEN GUPTA and NAQVI, 1984; NAQVIet al., 1991). More recent studies have focused on N-mass balance (SOMASUNDERet al., 1990), sedimentation (NAIRet al., 1989) and denitrification fluxes derived from nitrate deficits (NAQvI et al., 1990), nitrous oxide distributions (LAw and OWENS, 1990) and respiratory electron transport activity (NAQvI and SHAILAJA,1991). In September 1986, we carried out a nutrient oceanographic and microbial cycling study along a meridional section (67°E) from the Equator, via the Arabian Sea and into the Gulf of Oman, transecting all three of the above biogeochemical regimes. The aim of this paper is to report: (1) the results of nanomolar nitrate and nitrite analyses in the surface NWIO in relation to primary production; (2) isopycnal budgeting of NO3-deficits within Freon-11 dated (OLsoN et al., 1993) ODZ; and (3) N20 distribution and production relative to ventilation fluxes from the upwelling region of the Arabian Sea.

SAMPLING AND METHODS Our oceanographic studies were carried out towards the end of the southwesterly monsoons from 6 September to 10 October 1986, during Cruise 16 of the R.R.S. Charles Darwin (see Fig. 1 and Table 1), starting at the Equator and following essentially the 67°E longitude into the Gulf of Oman to within 160 km of the Straits of Hormuz (Stas 1-11). Another track, focusing on the coastal upwelling South of Oman (Stas 13-16), was also accomplished. All water sampling was carried out using a stainless steel CTD-rosette sampler fitted with 12 pre-cleaned Teflon-coated GoFlo bottles (General Oceanics). Most vertical profiles consisted of two overlapping casts (i.e. 24 samples, see Table 2) to ensure adequate vertical resolution down to ca 40 m off the seabed. The CTD system was also fitted with an in situ fluorometer (Aquatracka MkII, Chelsea Instruments, UK) and an oxygen polarographic electrode (BECKMAN Model 147737), and the raw data was outputted on a Neil Brown CTD console, logged and reprocessed for display on VDU. All the CTD-F-O2 parameters were calibrated at sea using reversing digital thermometers, salinometer (Guildline), chlorophyll a analyses (MANTOURAand LLEWELLYN,1983) and automated oxygen Winkler titrations (WILLIAMSand JENKINSON,1982). The GoFlo bottles were triggered during the upcast at both standard depths and at key features (e.g. oxycline, fluorescence maxima etc) observed during the CTD-F-O2 downcast. Once onboard, the bottles were transferred to a racking system fitted with a low pressure supply of N 2 for headspace displacement of water samples for 02 Winkler titrations and for

653

Nitrogen biogeochemical cycling 30 ~

f.O o

50 °

60 °

70 o

80 ~ ~LC °

Cruise RRSCHARLES 08, Sept.

t r ack DARWIN

10. Oct. 1986

14

'ochin

EYCHELLES

Momb

i l~'>

J

Mahel,

30 ° E

~.0 ~

50 o

60 °

70 o

8C o

Fig. 1. Cruise track and Station positions of the R.R.S. Charles Darwin cruise CD 16/86: 8 September-10 October 1986.

nitrous oxide (N20). Nitrous oxide was stripped using the static vacuum technique and then analysed by a gas chromatography-electron capture detector (LAw and OWENS, 1990) with a standard deviation for the entire procedure of 3.8% (LAW, 1989). The precision and detection limit of the Winkler titrations were < 1% down 50 j~M. Reliable titrations could not be obtained for 02 < 5 ~tM, defined here as our detection limit. Standard colorimetric Autoanalyser (R) techniques were used for the shipboard determination of nutrients including nitrate (NO3, BREWER and RILEY, 1965), nitrite (NO2; GRASSHOFF, 1976), p h o s p h a t e (PO4, CHAN and RILEY, 1966) and ammonia (NH3; MANTOURAand WOODWARD, 1983). Surface NO3-depleted samples were invariably below the colorimetric detection limit (ca 0.1/~M) of the Autoanalyser, and these were also analysed for NO3 and NO2 using a modification (WooDWARDand OWENS, 1990) of the NO× chemiluminescence technique of GARSIDE (1982). Finally, pigment concentrations were determined by highperformance liquid chromatography (MANTOURAand LLEWELLYN, 1983) of 90% acetone extracts of filtered (Whatman GFF) particulates with only chlorophyll a values reported here. Apparent Oxygen Utilisation (AOU) values were calculated from observed oxygen

654

R . F . C . MANTOURAet al.

Table 1. Station positions occupied during cruise 16/86 of R.R.S. Charles Darwin Depth range (m)

Latitude °N

Longitude °E

700-3900 04i00

00°02.4' 00o03.7'

64°59.9' 65005.6'

0-600 0-3100

03o59.6' 03o59.3 '

67o00.1' 67o00.8 '

18/9/86 18/9/86

600-4500 0-500

08°00.8' 07°59,6'

66°59.7' 67°00.4'

0401 0402

20/9/86 21/9/86

600-4200 0--500

11°59.8' 11°59.6'

66°58.8' 66°58.9'

5

0502 0503 0506 0507

22/9/96 22/9/86 23/9/86 23/9/86

0-3900 0-500 100-300 60-400

14o25.6' 14°22.4' 14°21,6' 14°20.3'

66°55.3' 66°54.2' 66°50.6' 66°54.5'

6

060 l 0602

25/9/86 25/9/86

0-3200 [-)-200

18°59.9' 18°58.6'

67°0(1!.5' 66°59.5"

7

0704 0705

27/9/86 27/9/86

175-3300 0-175

21o15.5 ' 21°14. t'

63o21.9' 63°27.1'

8

0801 0802

28/9/86 28/9/86

175-3000 0-200

22°39.6' 22°39.3'

60o40.6' 60°42.4'

9

0905 0906

2/10/86 2/10/86

175-275t) 0-140

23°38.1' 23°35.4'

59°01.4' 59°00.0'

I0

1001 1002

29/9/86 29/9/86

150-2700 0-200

24°20.5' 24°18.2'

58°09.7' 58°10.0'

11

1101 1103

30/9/86 30/9/86

60-1200 0-55

24°49.3 ' 24049.5 '

57°12.8 ' 57o12.9 '

13

1301 1302

3/10/86 3/10/86

0-3500 0-300

19°58.0' 19°58.1'

60°47.7' 60°48.9'

14

1403 1405

5/10/86 5/10/86

0-3500 0-400

17°25.6' 17°26.2'

61 °29.1' 61 °35.3'

15

150l 1502

6/10/86 6/10/86

0-4000 0-300

18° 12.2' 18° 13.2'

59°42.2' 59°44.3'

16

1602

7/10/89

0-580

19°24.1'

58°18.1'

Sta.

Cast

Date

1

0103 0104

13/9/86 13/9/86

2

0201 0202

16/9/86 16/9/86

3

0302 0303

4

l e v e l s a n d s a l i n i t y a n d p o t e n t i a l ~ c m p e r a t u r e o f s e a w a t e r (RILEY a n d SKIRROW, 1975). N i t r o u s o x i d e v a l u e s a r e expresse¢.l as N 2 0 s a t u r a t i o n (AN2, n M ) r e l a t i v e t o a t m o s p h e r i c l e v e l s o f 3 0 3 . 9 p p b v/v so as t o d i s t i n g u i s h w a t e r s in e q u i l i b r i u m (AN2 = s u p e r s a t u r a t e d ( A N 2 0 > 0) N 2 0 - p r o d u c i n g w a t e r s .

RESULTS

AND

0) f r o m

DISCUSSION

H y d r o c h e m i c a l sectiofz. O c e a n o g r a p h i c s e c t i o n s o f s a l i n i t y , 0 2 , P O 4 a n d N O 3 c o n t o u r e d f o r t h e u p p e r 1500 m a n d o f N O 3 a n d c h l o r o p h y l l a ( C h l a) f o r t h e u p p e r 150 m f r o m t h e E q u a t o r ( S t a . 1) t o t h e

Nitrogen biogeochemicalcycling

655

Table 2.

Properties of o0 = 26.6%0layer Station

Position Depth (m)

0 (°C)

Sal. (%0)

Oz

64°59.9'E

240

12.2

35.09

92

A-I! 2367 16/2/77

26°34'N 56°40.0'E St of H o r m u z 1

60

21.5

37.80

205

A-II 2371 18/2/77

26°15'N 53°54.0'E Persian Gulf Outcrop 1

0

21.5

38.9/I

FP 10

26'~110.5'S 49°56.8'E S Indian Ocean Outcrop z

0

10.6

33.69

Date

Eat.

Long.

CD16/01 13/9/86

00°02'N Equator

NO 3

24.5

NO 2 CuM)

PO 4 " N O "

0

1.45

314.7

1.35

0

0.55

217.3

220

0

0

11.31 220.0

281"

17.4

(L2

1.22

End member

441.2

I From BREWERet al. (1978); 2from NAQVI et al. (1990): * assumed 0 2 saturation.

Straits of Hormuz (Sta. 11) are shown in Fig. 2(A)-(F). Surface salinities (and temperature) increased northwards because evaporation exceeds precipitation and river runoff, in the Arabian Sea, the landlocked Persian Gulf and Red Sea (WvRTKk 1971 ; SEN GUeTA and NAQVI, 19841. At Stas 9-11 in the Gulf of Oman, there is a pronounced southerly overflow of a saline water mass [S ma× = 37.45%0 at 240 m (Sta. 11)] tracking the sigma-t (~0) = 26.5 _+ 0.2%0 density layer and deepening from 240 m at Sta. 11 near the sill of the Straits of Hormuz, to 300 m by Sta. 9. This is the characteristic signature of the Persian Gulf Water ( P G W ; WYRTKI, 1971; DEUSER et al., 1978; BREWER and DRYSSEN, 1985; SEN GUPTA and NAQVI, 1984). This southerly subsurface outflow of the P G W is interrupted by the northeasterly extension of upwelled water driven by the southwesterly monsoons and originating from the coastal South Eastern Arabian Peninsula (Stas 13-16). This is dramatically seen as a 380 m uplift of the 36.2%0 isohaline [Fig. 2(A)] and a 210 m uplift of the 17.3°C isotherm (not shown). The Red Sea Water mass (RSW) characterised by intermediate maxima in S and Oz, was found between 400 and 800m from the Equator to Sta. 5 (14°N) along the o0 = 27.2%0 surface (WYRTKk 1971). The deep and bottom waters are of polar origin transported by deep western boundary currents (SEN GUPTA and NAQVI, 1984). The 02 section for Stas 1-11 [Fig. 2(B)] is consistent with WYRTKI (1971) and NAQVl et al.'s (1990) results showing pronounced Oz-depletion throughout the northern Arabian Sea. The depth of the subsurface oxycline generally tracked the 23°C isotherm. Although Oz-depletion is apparent even at the equatorial Sta. 1 (<60 ~tM at 850 m), hypoxic ( < 1 0 ~ M ) and potentially denitrifying conditions appear only from Sta. 3 (9°N) northwards, where the thickness of the hypoxic layer increases from 45 m at Sta. 3 to 1010 m at Sta. 11. At the same time the oxycline shoals from 113 m at Sta. 5 to <40 m at Sta. 9-11. Supersaturated oxygen concentrations were found in the productive mixed layer usually at or just above the Chl a maximum. Phosphate levels were low but detectable (0.2-0.4 ~M) in surface waters, reached maximum concentrations of 2.9 # M at 1300 m at the northern end of the O D Z (see also

656

R . F . C . MANTOURAet al.

Figs 3-5) and then decreased to 2/~M in the deep and bottom waters of the NWIO. Nitrate was severely depleted (<1 #M) in the surface mixed layer [Fig. 2(F)] down to nanomolar levels (see later). The outcrop of the 1/~M nitracline at Stas 7-9 originated from upwelling off the South Arabian Coast. A pronounced NO 2 maximum, attaining 3.8 ~M, was found below the oxycline at 250-350 m (commonly referred to as "Secondary Nitrite M a x i m u m " , NAQVI etal., 1990) and confined to Stas 5-7 within the Arabian Sea and absent in the Gulf of Oman. The distribution of Chl a [Fig. 2(E)] was characterised by very low surface concentrations (<0.2/~g 1-1) characteristic of oligotrophic waters both south of Sta. 6 and in the Gulf of Oman (Stas 10 and 11). However, much higher surface concentrations (up to 1.1/~g 1-1) were encountered in the upwelling Stas 7-9. A deep Chl a maximum (0.5-0.7/~g 1-1) was found at all stations, tracking the nitracline from a depth of 50-70 m in the tropical and subtropical waters, shoaling to 25 m and increasing to over 2/~g

(B)

(A)

500 .

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5

10

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800

900

0

300

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1200 I 6

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1500

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1800 0 300 Linear miles

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600

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0

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10

35

40

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Vertical profiles at Sta. 2 for potential temperature, oxygen, Chl a, phosphate (Figs A and C) and of nitrate, nitrite, nitrate-deficit and nitrous oxide (Figs B and D) plotted for the upper 500 m (A and B) and the entire water column 3000m (C and D).

G', tm --...I

5

10

15

20

25

-10

30

10

20

30

40

50

I

I

Sta.5

* ~ ~ ~ ~ ~ ~ , ~ ~

L./I

Concentration

Sta.5

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200

300

NO3(PM) ,11

200

NO2(PM x 10) 17 NOaDeficit(pM) 4* 300

400

delN20 (nM) 0

40O

Depth (m)

0

o~,

5

10

15

20

25

40

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Sta.5

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500

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~

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Vertical profiles at Sta. 5 for potential temperature, oxygen, ('hi a, phosphate (Figs A and C) and of nitratc, nitrite, nitrate-delicit and nitro,> oxide {Fig'; B and D) plotted for the upper 5()0 m (A and B) and the entire watel column 4000m (C and D).

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20

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Vertical profiles at Sta. 11 for potential temperature, oxygen, Chl (~, phosphate (Figs A and (') and of nitrate, nitrite, nitrate-deficit and nitrous oxide (Figs B and D) plotted for the upper 200 m (A and B) and the entirc xvalcr column 1200m (C and D).

O', L~

660

R.F.C. MANTOURAet al.

1-1 at the upwelling Stas 7-9. In the Gulf of Oman (Stas 10 and 11) the Chl a maximum deepened to 40 m and was much more pronounced than further south. Vertical profiles and nitrogen speciation Detailed vertical profiles of potential temperature (0), 02, Chl a, NO3, NO2, PO4, N20 and NO3-deficit for three contrasting Stas 2, 5 and 11 are shown in Figs 3-5, respectively. The subtropical Sta. 2 was characterised by a 60 m surface mixed layer of nutrient-depleted [(NO3) = 11-12 nM; ( P 0 4 ) = 0.23 ktM], oligotrophic (Chl a = 0.15 ~g 1-1) water overlying a deeper (79 m) and broad Chl a peak of 0.67~g I 1, and a weak primary NO2 maximum (0.16/zM). The steep oxycline at 90 m is reversed by an intermediate 02 maximum (108 ~tM, 39.6% saturation) at 300 m, which also coincides with the Subantarctic Mode Water with a o0 = 26.8%0 density layer (WYRTI~I, 1971). The deep oxygen minimum [02 = 45.1 /~M; 15.4% saturation] at 800 m coincides with maxima of both NO3-deficit (ANO 3 = 2.8 ~tM; see also ANO 3 section Fig. 10A) and N20 (AN20 = +31.8 nM), and corresponds with the salinity maximum (35.17%o) of the Red Sea Water (or0 = 27.21%o). Finally, the 02 recovery in deeper waters arises from the cold oxygenated North Indian Deep Water and the Antarctic Bottom Water. Station 5 was profiled with higher vertical resolution via four overlapping hydrocasts of 12 bottles [Fig. 4, (A-D)]. Again, the surface mixed layer (top 100 m) was severely nutrient-depleted [(NO3) = 13,2 nM; ( P 0 4 ) = 0.42/~M] but featured within it a Chl a maximum (1.3~tg 1-1) and a weak primary NO2 maximum of (0.18~tM) which extended to 90 m. Within the O D Z (<10/~M; 110-1000 m) there was a pronounced vertical sequence of concentration maxima in NO, (3.8~tM at 200 m), NO3-deficit (ANO3 = 7/~M at 350 m), N20 production (AN20 = + 50 nM at 900 m) and NO3 and PO4 regeneration maxima (34.8 and 2.58 ~tM, respectively, at 1400 m). Station 11, located in the inner shelf edge (1200 m) of the Gulf of Oman 90 miles south of the Straits of Hormuz, was a highly stratified multilayered water column [Fig. 5(A-D)]. A shallow (20 m) mixed layer of very warm (31-32°C), saline (37.2%o), oligotrophic [(NO3) = 8-10 nM; (P04) = 0.3ktM; Chl a = 0.28~g I i and oxygenated [(O2) = 175¢tM, 106% saturation] water originating from the summer-stratified waters of the Persian Gulf overlies a broad 9°C thermocline at 22-39 m depth. At the base of this thermocline is a productive 10 m thick layer of very high levels of Chl a (3.1/~g 1-1), and oxygen [(02) = 230-240~tM, ~ 120% saturation], and a primary NO2 maximum (0.3/~M) coincident with a pronounced nitracline [(NO3) = 0.6 --~ 14.1/~M]. The deeper Persian Gulf Water (PGW), with its characteristically high salinity (37.45%0) and density (or0 = 26.5 + 0.1%o), appears at 210 m as an easily discernible intrusion of partially oxygenated (48-51 /~M, 21% saturation), nutrient-depleted warm outflow into an otherwise hypoxic [(O2) < 10 ~tM] and nutrient-rich deep water. These deep (250-1350 m) waters are also characterised by pronounced maxima in NO3-deficit (ANO 3 = 8.1 ktM at 398 m) and N20 (AN20 = +32 nM at 793 m) but no secondary N O 2 maximum as seen at the actively denitrifying Sta. 5 (Fig. 4), indicating that the deep waters of the inner Gulf of Oman were denitrified during their advective history through the Arabian Sea. The weak primary NO2 maximum of <0.2/~M coincident with the Chl a maximum at the base of the euphotic zone detected at all stations e.g. Sta. 2, 80 m [Fig. 3(B)]; Sta. 5, 80m [Fig. 4(B)] and Sta. 11, 40m [Fig. 5(B)] can be attributed to phytoplankton release following NO3 assimilation at low light levels and to photo-inhibition of bacterial nitrifi-

661

Nitrogen biogeochemical cycling

cation (OLSON, 1981; WARD and ZAFmIOU, 1988). A pronounced secondary NO2 maximum of up to 3.8 #M was found between 150 and 450 m depth, immediately below the upper boundary of the oxygen-depleted and NO3-deficient zone between of Stas 5-7 [Fig. 2(D)] of the Arabian Sea. This geographic confinement of NO2 [See Fig. 2(D)] is consistent with previous reports from the region (DEusER et al., 1978; NAQVIet al., 1990) and which were explained in terms the build up of NO 2 intermediate at low oxygen tensions during active denitrification of sedimenting phytogenic organic matter. However, the high levels of surface chlorophyll [Fig. 2(E)], primary production (OWENS et al., 1993) and sedimentation r a t e s (ZEITZSEHEL, in prep) obtained during this cruise for Stas 6-8 and off the Southern Oman Coast (Stas 14-16 not shown) are geographically uncoupled from the denitrifying layer located further south (NAOvI and SHAILAJA, 1993) and which actually underlies oligotrophic waters. This argues strongly for an advective transport mechanism for particulate and dissolved organic matter in fuelling denitrification in the Arabian Sea. All stations in the NWIO were supersaturated with N20 (average 302%, n = 309), exhibiting generally similar profiles of increasing AN20 with depth particularly between 200-1000 m (Figs 4-6), coincident with the oxygen minimum. A vertical section of AN20 from Stas 1 to 11 is shown in Fig. 10(B). LAW and OWENS (1990) have already demonstrated a bimodal relation between AN20 and A O U and concluded that N20 could originate from nitrification processes in the upper oxic water column, and from denitrification in the ODZ. The marked AN20 minimum coincident with the secondary NO2 maximum (see e.g. Sta. 5, Fig. 4) has been noted in other oceans (ELKINS et al., 1978; COHEN and GORDON, 1979), and may be attributed to competition between denitrifiers and other bacteria for nitrate in the presence of an enhanced supply of organic matter. Nitrate depletion in surface waters

The concentrations of NO 3 and NO2 for the surface mixed layer above the nitracline of Stas 1-11 [Figs 2(F), 3(B), 4(B) and 5(B)] were below the 0.1/~M detection limit of colorimetric analyses, but well within the sensitivity range of the NOx chemiluminescence

Average surface concentrations of

NO3 & NO2 in the N W Indian Ocean [NO3], [NO2] nM 1ooooo

1oooo ii

lOOO

--

ill

10o i ,

m

NO3

~

ii

iii

2

3

NO2

lO

1 1

Fig. 6.

4

5

6

7

8 9 10 STATION

11

12

13

14

15

16

17

Average surface concentrations (nM) of NO 3 and NO z in the North West Indian Ocean, determined by NO x chemiluminescence technique.

662

R.F.C. MANTOURAet al.

system (GARS1DE,1982; WOODWARDand OWENS,1990). These are shown in Fig. 6 for all stations in the NW Indian Ocean. Nitrate ranged over three orders of magnitude, from the extraordinarily low levels of 10.8 _+5.6 nM (average _ range) at Sta. 6 to 13.5 _+ 11.2~tM at the strongly upwelling Sta. 16. Throughout, NO2 levels (Fig. 6) were generally one order of magnitude lower than NO3. The slightly elevated levels of NO3 and NO2 in Equatorial surface waters (Sta. 1:43.0 _+ 18.9 nM and 3.6 _+ 1.6 nM respectively) decreased progressively northward to the subtropical oligotrophic gyre around Sta. 6 (NO 3 = 10.8 _+ 5.6 nM; NO2 = 2.4 + 1.4 riM) and into the Gulf of Oman where surface water concentrations remained at about the same depleted levels (e.g. Sta. 11:NO3 = 13.8 + 13.0; NO2 = 1.5 + 0.3 riM). These oligotrophic NO3 concentrations are comparable to recent findings (EPPLEYet al., 1990) in the surface waters of the tropical Pacific Ocean (8.4 + 7.2 nM) and subtropical North and South Atlantic Ocean (9.5 _+ 4.6 nM and 6.0 _+ 2.1 nM, respectively, and the summer-stratified central North Sea (10 _+ 5 nM; WOODWARD and OWENS, 1990) but somewhat lower than the Sargasso Sea (20 _ 10 riM; GARSIDE, 1985). Concentrations at Stas 7 and 8 were intermediate (NO 3 = 440-1026 riM) between the oligotrophic levels and those encountered at the upwelling Stas 14-16 confirming the chemical hydrographic conclusions that Stas 7 and 8 were influenced by an easterly extension of the upwelling regime off the Southern Arabian Coast. Both NH 4 and urea were generally undetectable (DL < 0.1 ~tM) in surface waters, whereas PO4 levels ranged between 0.2-0.4ktM. The corresponding molar NO3/PO 4 ratio of 0.02-0.09 for Stas 1-6 is significantly lower than the Redfield ratio of 16 (REDFIELDetal., 1963). This, taken together with measured nanomolar levels of NO2 and NO3, quantitatively confirm that phytoplankton production in surface oligotrophic waters (Stas 1-6, 911) is potentially severely nitrogen-limited (OWENS et al., 1993). Indeed, the near surface (0-10 m) integrated nitrogen production by phytoplankton, expressed as both total N assimilation rates and as NO3-fuelled or "new" production, appear to correlate with the ambient NO3 levels (Fig. 7) confirming nitrogen control on the overall production in the NWIO. The turn-over time (T) of NO 3 can be calculated by assuming steady state and combining the above NO 3 levels with the vertically integrated production and f-values derived by OWENS et al. (1993). T values of 0.15-4.3 days for oligotrophic waters (Stas 9 and 1 respectively) were generally faster than the upwelling waters (T = 2.4--48 days, Stas 14 and 7 respectively) and compared with 0.2--0.5 days inferred from EPPLEYet al. (1990) for the subtropical North Atlantic Ocean. It is possible that ammonia concentrations below our 0.1 ~tM detection limit could be regulating NO3 utilisation by phytoplankton (EPPLEY et al., 1990). Finally, it is interesting to note that there was no evidence from vertical profiles of any net N20 uptake (AN20 < O) by the N-starved phytoplankton despite there being higher levels (AN20 = 0.4-7.53 nM or 108-241% saturation) than NO3 in the oligotrophic surface mixed layer. Nitrate deficit in the o x y g e n depleted z o n e

Recent studies in the Arabian Sea (DEUSERet al., 1978; NAQVIet al., 1982, 1990; NAQVI, and SEN GUVrA, 1985 have revealed significant deficiencies of inorganic combined nitrogen, mainly NO3, within a large body of oxygen depleted (<10 IzM) intermediate water covering the depth range of 100-ca 1100 m. This denitrifying layer (DNL) is confined to the northeast Arabian Sea (East of 56°E) up to the Indian Continental shelf

Nitrogenbiogeochemicalcycling

663

Total and NO3-fuelled surface production in relation to [NO3] in northwest Indian Ocean N Assimilation surface 10 m ( nM N day -1 ) 10000.0O

1000.0(

);

Total N Assimilation 100.0(

10.0(

NO3 Assimilatic

1.0( lO.00

1oo.oo

1ooo.oo

[NO3] s u r f a c e

1oooo.oo

1ooooo.oo

nM

Fig. 7. Relationship between total Nitrogen and NO3-fuelled ("new") production in the surface layer of the NWIO (derived from OWENSet al., 1991) and the average surface concentrations of NO3.

and extends 1700 km southward from the Gulf of Oman to ca 12°N (NAQVI, 1987), and was thus transected by our main section (Stas 1-11). Sources of water to the DNL include outflows of Persian Gulf Water (PGW) and Red Sea Water (RSW) at intermediate depths along the a0 = 26.6 and 27.2%0 density layers, respectively (WYRTKI, 1971; SEN GUPTAand NAQVI, 1984). Estimation o f nitrate deficits

The concentrations of NO3 for Stas 1, 5, 7 and 11 were regressed against PO4 (REDFIELO et al., 1963; NAQVI et al., 1982) as a first attempt to detect nitrate deficits (ANO3). The plots

[Fig. 8(A)] reveal four features. A PO4 intercept of 0.25-0.45 ~tM indicates NO3 depletion for all surface waters along the Stas 1-11 section. Although nutrient regeneration at intermediate depths generally conforms to the Redfield NO3/PO 4 ratio of 16, this slope breaks down due to denitrification at intermediate depths and to a change in the degree of PO 4 regeneration relative to NO3 evident in the deeper waters of the NW Indian Ocean (MINSTER and BOULAHDID, 1987). In addition, another NO3-depletion anomaly, evident at Stas 11, arises from the outflow of NO3-depleted PGW along the ao - 26.6%0 density layer. This complicates the calculation of ANO3 from P O 4 correlations, especially since it is necessary to invoke additional corrections due to PO4 regeneration during denitrification (e.g. NAQVIet al., 1990). In order to calculate the nitrate deficit in the denitrifying layer (DNL), we extended the use of "NO" conservative water mass tracer (BROECKER, 1974) previously applied to the Arabian Sea (NAQVI and SEN GUPTA, 1985) and Indian Shelf edge waters (NAQVI et al.,

664

R.F.C. MANTOURAet al.

1990) and the Indian Ocean as whole (MINSTER and BOULAHDID, 1987), to explicitly include the contributions of the NO3-depleted Persian Gulf Waters within the DNL of the Arabian Sea. The concept of "NO" as a biogeochemically conservative water mass tracer (BROECKER, 1974) originates from Redfield's studies (REDFIELD et al., 1963) of the deep aerobic degradation of phytobiomass. For each mole of oxygen consumed, roughly 1/9 mole of combined nitrogen is released as NO 3 following the Redfield stoichiometry: (CH20)Io3(NH3)16(H3PO4)

T

NO3

+

135 02---> 103 CO2 + 16 HNO3

119H20.

+ H3PO 4 +

Redleld Ratio

(pM) DeepOcean NO3/PO4 RegenerationRatio

40 +

=16

" " ' ~ " ' ~ ~ , / "

A

35 + 30 + 25 420 4-

-

15 4-

\

10 4NO3 Deficit NO3_depleted PGW outflow

O I 1

I 1.5

I 2

I 2.5

I PO4 (pM) 3

[NO3] vs AOU within sigma-t < 25.5 surface layer Sta's 1-11 northwest Indian Ocean

B

30 [NO3]

(pM) 25 .

-

20 15 10

5 ~10 J q ~

-5O /

-5

~

[NO31=0.108 AOU + 0.832, r=0.95, n=125

--0 0 0 I

I~

50

100

I

I

I

150

200

250

Apparent Oxygen Utilisation (pM)

Fig. 8. (A) Regression of N O 3 vs PO 4 for Stas 1, 5, 7 and 11 in relation to the Redfield slope in intermediate and deep waters of the N W l O . NO 3 depletion due to denitrification and to the input of NO3-deficient Persian Gulf Water are also highlighted. (B) Regression of N O 3 against apparent oxygen utilisation ( A O U ) for the o 0 -< 25.5%0 surface layer in the N W l O .

Nitrogen biogeochemicalcycling

665

BROECKER (1974) recognised that for any submerged water mass, the composite property

"NO", "NO" = [021 + RN[NO3] (where RN ~ 9), should be a conservative property of that water mass. This provides a means of not only disentangling the degree of mixing of different water masses with different concentrations of preformed nutrients, but also in quantitatively estimating NO3 deficits in multicomponent denitrifying layers as in the Arabian Sea (see NAQVlet al., 1990 and references cited therein). Recently, MINSTER and BOULAHDID (1987) achieved a more rigorous verification of BROECKER'S(1974) equation by evaluation of GEOSECS and TTO nutrient/oxygen data for the Atlantic and oxic portion of the Indian Ocean, along four isopycnal mixing surfaces. A depth-independent value of R N = 9.1 + 0.4 was found, and this led NAQVlet al. (1990) to revise their earlier estimate of R N = 8.65 (NAQVIand SEN GUPTA, 1985) used in their previous denitrification budget of the Arabian Sea. Since these different values of Rx reported (e.g. 8.65, NAQVIand SEN GUVrA, 1985; 10.75 by TAKAnASnIet al., 1985; and 9.1 by MINSTER and BOULAHDID, 1987) can significantly affect calculations of ANO3, it was necessary to verify, where possible, the value of R N. Given the limited number of hydrocasts, we regressed the apparent oxygen utilisation (AOU) and [NO3] data for Stas 1-11 sectored over five density layers (oo -< 25.5, 25.5-26.5, 26.5-26.9, 26.9-27.3, 27.3-27.7 and ->27.7%0) of the water column. As expected, in the oxygen minimum zone covering 00 > 25.5%o, NO3 vs AOU relationships deviated significantly from Redfield ratios due to denitrification. Only the o 0 < 25.5%0 density layer, which included the surface mixed and upper oxygenated [(02) > 10 pM] portions of the DNL, yielded a good correlation [see Fig. 8(B); r = 0.95] with a n R N = 9.28 + 0.36, in good agreement with MINSTERand BOULAHDID'S(1987) value of 9.1 + 0.4 for the regions outside the Arabian Sea. We therefore adopted their equation "NO" = [02] + 9.1 [NO3] to calculate values of "NO". Figure 9(B), shows "NO" plotted against 0 for the entire water column of Stas 1-11, clearly features a negative "NO" anomaly between 0 = 1122°C associated with the DNL. Although this agrees with N A Q V I et al.'s (1990) twocomponent "NO" vs 0 observations in the Arabian Sea (from which they calculated the expected "NO" from 0), their isopycnal treatment was based on PO 4 endmembers and needed to be verified particularly along the PGW core layer entering the denitrifying layer. We therefore used a two-component isopycnal mixing model to derive the expected "NO" ("NOexp") for the o 0 = 26.6%o density layer in the NWIO. The northern "NO" endmember was calculated from BREWERet al.'s (1978) nutrient and oxygen data for the Persian Gulf summarised in Table 2. The "NO" values for the PGW outcrop within the Gulf and for the Persian Gulf Water outflow at the Straits of Hormuz were essentially indistinguishable, indicting little nutrient regeneration occurring in the outer Persian Gulf. For the Southern endmember we used the "NO" value derived for Sta. 1 (Table 2) rather than NAQVIet al.'s (1990) anomalously high NO3 and "NO" value for the Southern Indian Ocean outcrop, since this would imply that NO3 deficit extends well into the Southern Indian Ocean! The resultant conservative isopycnal mixing line for "NO" vs 0 [Fig. 9(A)] is described by the equation

666

R . F . C . MANTOURAet al.

" N O " v e r s u s Potential T e m p e r a t u r e a l o n g t h e s l g m a - t = 26.6 ppt I s o p y c n a l s u r f a c e

A

"NO"= [02] + 9.1 x [NO3] (I.IM) 450 -

• StO

400 _

~

?

/

Sigma- t =26.6 NO-T conservative mixing

~

Mantoura et al(1991)

350

300

250

T > 10.3°C__ Naqvl et al (1 990)

/

&

- - " "'J~" " - - ' : - ~ ,

200 • 0 2 Saturation

~'/k /

Brewer et al (1974)

100

Pot l'emp (°C) I t

Straits of Hormuz

I

I

(

I

(

I

I

I

7

9

11

13

15

17

19

21

23

['NO'] v e r s u s potential t e m p e r a t u r e s for St 1 - 11 north west Indian O c e a n 'NO' 500

= [ 0 2 ] + 9.1 [ N O 3 ]

25

B

(pM)

45O 400 350 •

- .

.

•

300.

for Sigma-t=26.6 core layer -

•

/ -m

-m

250

•

• •

• -

•

0 2 sat curve at S=35 ppt 200

/~

150 -

"-

100 0

•

,

Deep water NO-Pot Temp regression I

I

I

I

I

5

10

15

20

25

otentlal " - Temperature I I 3O

35

Fig. 9. (A) Plot of the composite property " N O " vs potential temperature along the % - 26.6%o isopycnal surface for our Stas 1-16 and for Gulf of O m a n data derived from BREWERet al. (1978) in relation the " N O " - - P o t e n t i a l Temperature conservative mixing line. For comparison, NAQVl el al.'s (1990) "'NO" vs Potential Temperature relationship and the o0 = 26.6%0 outcrop in the Southern Indian Ocean (SIO) (see Table 2) are also shown, as well as oxygen saturation curve for S = 35%° (B) Plot of " N O " vs. Potential Temperature, as in (A), but for the entire water column of Stas 1-11 showing the two linear " N O " vs. Potential Temperature components, used to estimate expected " N O " values.

Nitrogen biogeochemicalcycling "NO"ex p = 437.9-10.810;

(o0 = 26.6%0;

667

12.2 < 0 < 21.5°C).

Over this temperature range, this equation is statistically indistinguishable from NAQVI et al.'s (1990) vertically-integrated " N O " vs 0 relationship obtained for 0 > 10.3°C. This

arises because the P G W outflow is as oligotrophic [(NO3) = 1.3 ~M; (PO4) = 0.55 ktM] and oxygenated (222 #M) as the surface nutrient-depleted waters of the Arabian Sea used in NAOVl et al.'s (1990) treatment. It is also clear from Fig. 9(A) that the isopycnal " N O " values for Stas 3-16 overlapped with values calculated from BREWERetal.'s (1974) data and that both deviated significantly from the expected conservative " N O " vs 0 line. This deviation allows one to distinguish nitrate deficits (ANO3) due to denitrification, from those due to inputs of NO3-deficient Persian Gulf Water into the Gulf of Oman. The effect of this correction is clearly seen in the vertical profiles of Sta. 11 [Fig. 5(D)], where the ANO3 maximum due to denitrification at 400 m occurs below the depth of NO3-minimum of the Persian Gulf Water outflow at 210 m. Having verified that the above isopycnal treatment of " N O " vs 0 yields similar results to the simpler vertically integrated treatment, we then derived two linear components for the variation of "NO"ex p with 0 [Fig. 9(B)] to be "NO"cxp = 437.88-10.810

(0 > 5.3°C)

"NO"cxp = 461.9-15.320

(0 < 5.3°C),

from which the nitrate deficit (ANO3) was calculated for the entire water column using: ~NO3 = (["NO"exp - (O2)]/9.1) - (NO3) - ( N Q ) as explained by NAQVI et al. (1990). The vertical profiles of ~NO3 thus calc:~lated were shown in Figs 3-5 for Stas 2, 5 and 11, and as a ANO3 section between Stas ~'i~d 11 in Fig. 10(A). A tongue of NO3-deficient (up to 10.5 ~M) intermediate water o v e q a p p e d with the oxygen-depleted zone [Fig. 2(B)] and extended 2900 km south from the '~mlf of Oman to approximately 7°N. The vertically integrated ANO3 values increased ~e,rthwards from 0.8 males ?':(~3-N m -2 at Sta. 2 up to 6.49 moles NO3-N m -2 at Sta.9 at the mouth of the Gulf o~ ~)man, then decreased to 4.11 moles NO3-N m-2 at Sta. 11 near the Straits of Hormuz. "ih,~ negative ~NO3 values shown for the surface mixed layers (Figs 3-5) are artifactual and arise from including the supersaturated oxygen levels (up to l 31 oVo) in the productive photic zone of the NWIO. Negative ANO3 are normally not plotted (see e.g. Fig. 3 in NAQVI and SEN GVvrA, 1985) and at any rate are excluded in the calculation of ANO3 inventories. The average NO3 deficit for Stas 1-16 was 4.34 _+ 1.84 mole NO3-N m 2, in excellent agreement with NAQVIand SEy GreTA'S (1985) estimate of 4.67 mole NO3-N m 2 calculated for 15-21°N sector of the Arabian Sea. When applied to the denitrification area of the Arabian Sea (1.95 x 106 km 2, SOMASUNDERet al., 1990) a total NO3 deficit of 118 + 50 Tg N is calculated. Based on F r e o n - l l distribution in the NW Indian Ocean determined by OLSON et al. (1993) during another cruise of R.R.S. Charles D a r w i n in 1987, a water residence time (r) of 10 years was derived for the oxygen-depleted layer (200-1000 m) north of 12°N. This implies that our annual denitrification rate is 11.9 -+_~5.0 Tg or 10 % of the global water column denitrification (NAQVI et al., 1993). This estimat,:: is lower than either ETS-based denitrification rates (32.6 Tg N yr -1) recently determinc't i~y NAQV!and SHAILAJA (1993) or from a box model of water exchange in the 5, :~ bian Sea (ca 31~ Tg ~yr ~; NAQW, 1987). The rates and boundaries used for the latter ,.,,, estimates also im?l~,~ that r = 0.8 and 3.4 years, respectively.

R.F.C. MANTOURAet al.

668

Nitrous oxide distribution and fluxes

The Stas 1-11 section of AN20 [Fig. 10(B)] highlights two features: (1) that ANzO maximum occurred within the O D Z but consistently deeper than the ANO3 maximum [Fig 19(A)]; and (2) high values of AN20 (averaging AN20 = 4.49 _+ 2.21 nM) occurred in the upwelling zones of Stas 7-9 and Stas 14-16 (not shown). From this distribution, LAW and OWENS (1990) calculated an annual ventilation flux of N20 of 0.22-0.39 Tg N20 or 5-18% of the total marine flux of N20 to the atmosphere. It is also possible to estimate production fluxes of N 2 0 in the O D Z using the average vertically-integrated inventory of AN20 -1.28 + 0.70 g N m -2 (range 0.5-3.03 g N m -2 LAW, 1989) or 2.5 + 1.34 Tg N for the denitrifying area of the Arabian Sea. Again, assuming a water residence time of 10 years for the O D Z (OLSON et al., 1993), we calculate an annual N20 production rate of 0.25 _+ 0.06 Tg N--well within the range of sea-to-air flux values derived by LAW and OWENS

(A) 0

I

I

I

'

1000-

&NO

I

"~1."~"

/

3

15001 I

E

I

1

I

10 15 20 L a t i t u d e (°N)

25

I

I

(B)

N20 5 [

I

0

300

I

I

I

600 900 1200 Linear miles

I

I

I

1

2

3

I

I

I

4 5 6 Station number

I

I

1500

1800

I

I

I

7

8

91011

I I

Fig. 10 Oceanographicsectionsfor the upper 1500m of Stas 1-11 for (A) nitrate deficit (~M) and for (B) nitrous oxide production anomalies (AN20, nM).

Nitrogen biogeochemical cycling

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(1990). A p p a r e n t l y , N 2 0 p r o d u c t i o n within t h e O D Z is sufficient to s u p p o r t the ventil a t i o n fluxes c a l c u l a t e d for the u p w e l l i n g r e g i o n of the N W I O . H o w e v e r , t h e s e N 2 0 fluxes a c c o u n t for o n l y 2 % o f t h e t o t a l n i t r o g e n lost as N 2 as c a l c u l a t e d f r o m the n i t r a t e deficits in the A r a b i a n Sea. T h e s e ANO3 a n d A N 2 0 flux calculations clearly d e m o n s t r a t e that a l t h o u g h the p u b lished n u t r i e n t i n v e n t o r i e s a n d deficits a r e in g e n e r a l a g r e e m e n t , the c o r r e s p o n d i n g fluxes d e p e n d critically on t h e selection of the a p p r o p r i a t e b o u n d a r i e s a n d w a t e r r e s i d e n c e times. Since t h e r e is c o n s i d e r a b l e s e a s o n a l a n d i n t e r a n n u a l v a r i a b i l i t y in m o n s o o n a l forcing of u p w e l l i n g a n d p h y t o p l a n k t o n b l o o m s (BANsE a n d MCCLAIN, 1986), s e d i m e n t a t i o n (NAIR et al., 1989) a n d d e n i t r i f i c a t i o n (NAQvI et al., 1990) in the A r a b i a n Sea, it is essential that f u t u r e b i o g e o c h e m i c a l b u d g e t s s h o u l d i n c l u d e c o n c u r r e n t physical- a n d t r a c e r - b a s e d e s t i m a t e s of b o t h w a t e r r e s i d e n c e t i m e s a n d p a r t i c l e fluxes in a n d o u t of the o x y g e n d e p l e t e d z o n e o f the A r a b i a n Sea. It is c h a l l e n g i n g to r e c o g n i s e the climatic significance of a d e c a d a l r e s p o n s e t i m e for c a r b o n a n d n i t r o g e n t r a p p i n g a n d cycling in the o x y g e n d e p l e t e d z o n e of the A r a b i a n Sea. O n the o n e h a n d , m o n s o o n a l u p w e l l i n g s t i m u l a t e s surface p r o d u c t i o n a n d s e d i m e n t a t i o n of d e g r a d a b l e o r g a n i c c a r b o n for t e m p o r a r y p r e s e r v a t i o n and t r a p p i n g in the o x y g e n d e p l e t e d zone. O n the o t h e r h a n d u p w e l l e d w a t e r s efficiently v e n t i l a t e t h e i r r e s p i r e d g r e e n h o u s e gases including CO2, CH4 a n d N 2 0 to the a t m o s p h e r e , thus p r o v i d i n g a climatic f e e d b a c k . This b i o g e o c h e m i c a l p o i s e m u s t b e very sensitive to any climatic c h a n g e s affecting m o n s o o n a l u p w e l l i n g a n d c i r c u l a t i o n of i n t e r m e d i a t e w a t e r masses. This b e s t o w s a u n i q u e p r o p e r t y to the A r a b i a n S e a as a sensitive o c e a n scale b a r o m e t e r of g l o b a l c l i m a t e change. This c o u l d be a c h a l l e n g i n g focus for f u t u r e i n t e r n a t i o n a l o c e a n o g r a p h i c r e s e a r c h e n d e a v o u r s such as J G O F S a n d W O C E in the N W I O . Acknowledgements--We thank the officers and crew and RVS technicians of the Royal Research Ship Charles Darwin for excellent service, Mr Tim Fileman for help in computing and Mrs J. Morris for oxygen titrations. We benefited much from stimulating interactions with colleagues at the National Institute of Oceanography, Goa, India, during the ISOIO Symposium in January 1991.

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