GEOPHYSICALRESEARCHLETTERS,VOL. 25, NO. 1, PAGES81-84,JANUARY 1, 1998
Biogeochemical significance of transportexopolymerparticles in the Indian
Ocean
M. Dileep Kumar, V. V. S.S.Sarma, N. Ramaiah, M. Gatms, andS.N.deSousa NationalInstituteof Oceanography, DonaPaula,Goa, India
and winter monsoons [Madhupratapet Abstract. The behaviorof Transparent ExopolymerParticles cial!y duringsouthwest microbialnitrification/denitrifica(TEP),produced by biochemical processes, wasstudiedfor the al., 1996],andthe associated greenNorth IndianOcean,an areaof globalbiogeochemical signifi- tion maketheseregionsimportantsourcesto atmospheric cance,during1996southwest monsoon. Verydifferentbehavior housegases[Owenset al., 1991;Kumar et al., 1995].In spiteof of TEP was found between waters of the Arabian Sea and the the relativelylargephytoplankton productionin AS than in BB, the sinkingfluxesof organiccarbonare lower in the formerregion[Nair et al., 1989;Ittekkotet al., 1991]. This hasled to the in whichtemgenouspartiinteractionwith mineralparticles.They were higher and oc- generationof the ballasthypothesis curredevenin intensesub-oxiclayersin the ArabianSea. Our cles broughtin by Indian rivers scavengethe organicmaterial resultssupport themineralballasttheoryin the Bayof Bengal from water column[Ittekkotet al., 1992]. However,no direct so far. In view of the andalsorevealthe hithertonot noticedorgamcmatterreservoir, evidenceis availablefor this hypothesis whichseenisto be in surplus,to meetthehighercarbondemand intensewater columndenitrificationin AS and higherratesof sinkingparticlesin BB, we comparedthe distributionof TEP by bacteriain denitrifying watersof theArabianSea. betweenthesetwo regionsby obtainingdatafrom centralparts of the former(in August),as a part of the JGOFS(India) Program,andin thelatter(in September) duringthe 1996southwest Introduction monsoon(Fig. 2a),
BayofBengal. TheTEPconcentrations werelowerin theBayof Bengaldueto fasterscavenging fromwatercolumnbecause of
Someof the particlespresentin naturalwatersare formed from extracellular metabolites and are transparentunless Material
and Methods
stained.Theseparticles,firstidentifiedandnamedas TransparSamples weretakenat stations located at onedegreeinterval ent Exopolymer Particles(TEP) by Alldredgeet al. [1993], are thatat -•20øN(19ø45'Nand64ø37'E). formedfrompolysaccharides exudedby phytoplankton. Figure1 along64øEin AS, except weretwo degrees apartalong90øEin BB. Data were depictsa schematic representation highlightingthe significant Stations collected on board ORV Sagar Kanyacruises115 and116from role of TEP in the oceaniccarboncycle.Photosynthetically prothe respective regions. A Sea-Bird CTD systemfitted with ducedphytoplankton releasesextracellularorganicmaterials 1.8/12 litre Niskin/Go Flo bottleswas usedfor collectingsam[Anderson and Zeitschel,1970] of whichdissolved polysacchafides cancondense and form aggregates of TEP facilitatingor- plesfromthe upper1000mof watercolumn.Samplingdepths gatticcarbonsedimentation [Passow et al., 1994].Anderson and are shownin Fig. 2b,c. Watersamples werecollected in cleanglassbottles(125 ml), Zeitschel[1970]founda closecorrelationbetweenthe dissolved aftersampling for dissolved gases,pH andalkalinorganicmatterreleased by phytoplankton andthe production of immediately particulateorganicmatter(POM). Alternately,bacteriahoused in TEP candecompose theseparticlesreleasingcarbondioxide 'Mineral' to seawater.On the otherhand,availabilityof mineralparticles would enablefastersinkingof TEP in the ocean(Fig. 1). Despitetheir expectedubiquitousoccurrence studiesof TEP are largelyconfinedto coastalwaters[PassowandAlldredge,1994; Schusterand Herndl, 1995;Mari and Kiorboe, 1996], and laboratory and mesocosmicexperiments[Alldredgeand Jackson, 1995] and their behaviorin the openoceanis not well known. We believethatalbeitTEP maybe a partof the POM its formis of vital importancein the biogeochemical cyclesof carbon,nitrogenandseveralotherelementsincludingmetalsin the ocean. The North IndianOcean,encompassing the ArabianSea (AS) andthe Bay of Bengal(BB), represents two hydrologically and biogeochemically contrasting areasof significance to globalcycling of carbonand nitrogen.The AS and BB housethe most intenselyoxygendeficient intermediatewaters in the world oceans[Kumaret al., 1995]. High biologicalproduction, espe-
'
' r•.
ATMOSPHERE '
particles
•,,•C.rbon Dioxide I / '/'
,y•e,,•
f f Polymer substances Bacl• rlal metaboll•tm
ILarge particles • t
8Inking
, , Copyright 1998bytheAmerican Geophysical Union.
•1 F
SEDIMENTS
Figure 1. Transparent Exopolymer Particlesformationandimplications to biogeochemical cyclingof carbonin theoceans.
Papernumber97GL03481. 0094-8534/98/97G
, ,,
L-03481 $05.00
81
82
KUMAR ET AL.: SIGNIFICANCE OF TRANSPARENT PARTICLES IN INDIAN OC-EAN
from AS were analysed,but thesewere replicatedwherever possible, whereas thoseofBB weredonein quadmplicates. The quadruplicate analyses indicated a meancoefficient of variation of-•5% (witha rangeof 0.2-20%)in TEP concentrations while
LONGITUDE (øE) $o
70
6O
90
80
INDIA
theduplicate measurements in AS exhibited anaverage of 11% (range: 2-25%).Dissolved oxygen wasanalysed colorimetrically, and nitrate and nitrite were found using a SKALAR autoana-
(a)
•
lyser.Also,watersamples at selected stations werecollected for microscopic counting andsizingof TEP [Passow andAlldredge, 1995a,b]with and withoutmineralparticles.Total bacterial numbersin all thesesampleswere alsoenumerated [UNESCO/
.
SCOR, 1994;Parsonset al., 1984]. Results and Discussion
15
16
17
18
19
20
21
Concentrations of TEP were higherin AS than in BB (Fig. 2b,c). HigherTEP in AS couldhavebeena directconsequence of Phaeocystis bloomswith diatomsin significantnumbersduring the studyperiod [M. Madhupratap,PersonalCommunication, 1997].Phaeocystis bloomsgenerallyfollowdiatomblooms [Gieskesand Kraay, 1975] and polysaccharide exudatesfrom Phaeocystis [LancelotandMethot, 1985] and diatoms[Passow et al., 1994] might have led to the observedTEP levels in AS (Fig. 2b). Lancelot[1984]observedthatabout50% of the carbon fixed by photosynthesis is secretedas mucusby Phaeocystis. SurfaceTEP concentrations werehigher(> 25 mg equivalents of
AA 14)at 18-20ON inAS(Fig.2b),where upwelling signatures wereevidentwith a temperature of 26.3ø(2andnitrate>1 gM. The availabilityof nutrientsin thesewatersmighthavetriggered intense biologicalproduction leadingto a higherreleaseof ex(c) tracellularmaterials.Thick mucus materials in this region cloggedthe net in a multinetassemblythat hauledzooplankton 6 8 10 12 14 16 18 abovethe thermocline.The higher surfacesignatures of TEP, LATITUDE (øN) between18ø and20ON,wereconspicuous downto 300m.Very Figure 2. (a) Stationsoccupied during1996southwest monsoon highconcentrations of TEP (-102 and94 mg equivalents of AA in theArabianSeaandtheBayof Bengal.TEP (ragequivalents 14,respectively) were,however, foundat -q500m at 18ø and
ofAA14)distribution (b)intheArabian Seaand(c)in theBay -20øN, whereupwellingoccurred. Theseanomalous highcon-
of Bengal.
centrations mighthavebeengenerated throughbacterialactivities,in situ [Passow andAlldredge,1994]and/ordueto sinking
ity, andre.fifgerated. Well shakensamples werepassed through polycarbonate (0.4 gm) or Durapore(0.45 grn) filters within a few hoursof collectionfor colorimetricanalysis.Boththe filters werefoundto behavesimilarlywith the resultsagreeingwithin 0.3-27% (average13%). The concentration of TEP, expressed as
Table 1. Transparent Exopolymer ParticleCharacteristics and BacterialCountsat Mid-depthin theNorthIndianOcean TEP Bacteria mean
equivalents of alginicacid(AA) per litre, wasestimated using the alcianbluemethod[PassowandAlldredge,1995a]with mi-
TEP total
TEP with TEP withmineral out mine-
Lat. Long.Depthcounts a length b counts particles ralparti-
normodifications. We observed thatalthough TEPfromsamples (øN) (øE) (m)
(perml) (Ixm) (perml) (%)
cles(%)
dissolvedin 80% sulphuficacid showedmaximalabsorbance at 787 nm, the AA (Sigma, productno. 7128, high viscosity -14000 cps)in the sameacidmediumexhibitedan inverserela-
15
64
600
2.94
37ñ42
260
46
tion between its concentration and absorbance. Our AA standard
17
64
500
1.64
92ñ97
130
46
54
yieldeda .better(positive)linear relation at 745nm. Nevertheless,TEP spectraof samplesrevealedproportional changesin absorbances at both 745 and 787 nm. Consequently, we measured the TEP concentration at 745 nm sincewe representthe sameas equivalentsof AA. Despitethis minormodification,the presentlyobservedTEP abundances are comparable to the range reportedby Passowand Alldredge[1995a]. Other TEP results from elsewhereusinggum xanthan(GX) as standard[Passow and Alldredge, 1994; Passowet al., 1994] may be compared
19
64
500
1.29
21+23
330
38
62
21
64
500
3.40
42ñ67
350
33
67
withourresults aspertherelation: 1 mgAA 14= 10ggGX 14 givenby Passowand Alldredge[1995a]Mostly singlesamples
Arabian
Sea
54
Bay of Bengal 8
90
500
10.45
9ñ10
4400
84
16
10 16
90 90
500 500
7.41 4.28
16ñ18 11ñ18
6690 7790
75 80
25 20
18
90
500
0.94
7ñ12
4800
86
14
•Bacteria (xl04)andTEPcounts weretotalnumbers inseawater. bThe lengths ofTEPweredetermined fromaminimum of30particles. CTEPS associated withandwithoutmineralparticles werebasedonthose counted in randomlyselected 40 fieldsoneachfilter.
KUMAR ET AL.' SIGNIFICANCE OF TRANSPARENT PARTICLES IN INDIAN OCEAN Nitrite
TEP 40
o
80
120 0
NO3-Deficit
2
I I_.
o
t
I
83
t
4 40
0
I I +.-,--
I
10
,
2o
I
+ ii
400
e •
+ _T++
800
1200 j (a)
(b)
(c)
Figure3. Vertical profiles of(a)TEP(mgequivalents ofAA1-]),(b)rotrite (I•M)and(c)nitrate deficit (gM)intheArabian Sea. Solidlinesareaveragecurves.Pointsin dashedcircleswerenotconsidered whileaveraging TEP.
afteradding anmountof3.5mgC m'2d-1tothedata of aggregates fromhighlyproductive surfacewaters.Suchcon- at 100m; by Banse[1994]) is insufficient centration gradients werenotseenin BB whereTEP varied of Ducklow[1993] as suggested demands of denitrification (155mgC m'2d-1 withina verynarrow range (7-13mgequivalents ofAA14).Al- tomeetthecarbon
though theTEP concentrations werehigherin AS theirnumbers [Naqviet al., 1993])andbacterialproduction(105 to 157 mg C
1994])in thesub-oxic layers ofAS.Despite the (Table1) werelow(130to350ml4) in contrast tothose in BB m-2d'l [Banse, (4400to7790ml4) since theTEPsizeswererelatively largein inverse relation between TEP and nitate deficits, a TEP conof-10 mgequivalents of AA 1'l persisted in theAS the formerregionthanin the latter.Here, we havepresented centration that TEP datafrom-500m to understand the role of mineral-organic mat- oxygenminimumzone(Fig. 3). This stronglysuggests
ter interactions in particlesinkingmechanism. Higherproduc- providemore than enoughorganiccarbonto sustainbacterial TEP canactivity in AS mighthaveresultedin enhanced stickiness and activitiesin thesedenitrifyinglayers.Consequently, hencein largeTEP sizes.Bacterial numbers werehigherin the countfor the hithertounknown'carbonsubstrate'requiredto layersof AS. baythusaidingreduction in stickiness [Passow andAltdredge, meetthe bacterialdemandsin subsurface 1995b] and particlebreakdowntherebyincreasingthe TEP The percentage of TEP harbouringmineral(terrestrialor manumbers. While theseare the first measurements of bacteria fine solid)gramswasmore(75 to 86) in BB thanin AS (33 to fromthecentralbay,thebacterial populations in AS seasonally46). Thistrendis in concurrence with the totalnmber of TEP varybya factorof-q 000 [Madhupratap etal., 1996;Ramaiahet counted (Table1). SmallerTEP sizeswith moremineralpartial., 1996].
clesin the bay suggestrelativelyhigherdensitiesfor thesepar-
Significantly, TEP levelswerelowerbetween200 and500m ticlesin thisareasincewe compare dataat a waterdensity(c•o)
thanthosein layersabove andbelowin AS,particularly to the of 27.1kg m-3(-•500m).LesserTEP associated withmineral northof 18øN(Fig.2b). In contrast, therewasno suchdecreaseparticlesin AS couldhavebeendueto lowerinputsof temgein TEP levelsin BB (Fig.2c). Interestingly, decreased levelsof nousparticlesthroughriversandatmosphere. In fact, flux of TEP coincide with highersecondary nitriteandnitratedeficits terrigenous materials in to BB is quitesubstantial. Riversfrom
(Fig.3) suggesting theutilization of TEPin bacterial respira-theIndiansub-continent alonecontribute-1387x106 tonsy-1to tion/production in denitrifying layers. A fewhighervalues, in- BBwhiletheASreceives only195x106 tonsy-1[Subramanian, sidethedashed circlesin Fig. 3, mighthavebeendueto sinking 1993]. Consequently, TEP can be more rapidly scavenged or in situ specificbacterial/coagulation processes. Enhancedthrough interaction withclayandbiogenic mineralgroinsraining bacterialactivityand denitrification in AS subsurface layers fromthesurface layersin BB. Possibly, TEP aresubject to shear havebeenshownto be relatedto theoccurrence of intermediatefromturbulence andtherebytrappingor sweeping the mineral nepheloid layers(detectable bya transmissometer) andenhancedparticles whichin turnballasttheorganic matrixthusfacilitating electrontransport activity[Naqviet al., 1993].A maximumm- its fastersedimentation [K. Banse,PersonalCommunication, tmtedeficitof-10 IxMoccurred around300min AS (Fig.3) but 1997].Thismightexplainthe highersinkingfluxesof organic
nodeficit wasestimated tooccur inBB.In agreement withthis, carbon inBB[2.04-3.59 gCm'2y-i;Ittekkot etal., 1991 ] thanin respiration ratesarecomparatively higher intheupper 1000m in AS[1.53-1.80 gCm-2y-l;Nairetal., 1989]andprovides a direct AS thanin BB [Naqviet al., 1996].Dissolvedorganiccarbon evidence,throughTEP and mineralgrainsassociation, to the hasbeenshownto be usedup duringdenitrification [Kumaret mineralballasthypothesis [Ittekkotet al., 1992];that links the al., 1990]while particulatecarbohydrates are lowerin interme- mechanism of long-termstorageof atmospheric carbondioxide diatewatersin AS, specifically to thenorthof 15øN[Bhosle and in oceanicsediments to the organic-mineral interactions in the
Wagh, 1989]. Sinking fluxofcarbon (11.8to29.1mgC m'2d'l water column.
84
KUMAR ET AL.: SIGNIFICANCE OF TRANSPARENT PARTICLES IN INDIAN OCEAN
Acknowledgements. We appreciate thehelpof Dr. T. Yoshinariin procuringthe alcianblue. We thank the Director,NIO, Goa, andthe JGOFS (India) team for encouragement. We appreciate the etfoas of Drs. S.W.A, Naqvi, S. Raghukumar,Alice Alldredge,Karl Banseandan anonymous reviewerfor their constructive comm•. We thankthe financialsupportfor thisprogrambythe Department of OceanDevelopment, New Delhi.
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George,andC. D'Silva, An intermediate nepheloid layerassociated with
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Sarma,NationalInstitmeof •ography, dia.(e-mail:
[email protected]. in)
DonaPaula,Goa403 004, In-
(ReceivedJuly 1, 1997;revisedOctober8, 1997; accepted October28, 1997.)