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Dec 15, 1998 - al., 1994; Quinn et al., 1996; Charles et al., 1997; Kuhnert et al.,. 1998] ...... Muscatine, L., J. W. Porter, and I. R. Kaplan, Resource partitioning by.
JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 103, NO. C13, PAGES 30,731-30,739, DECEMBER 15, 1998

Vertical water mass mixing and plankton blooms recorded in skeletal stable carbon isotopesof a Red Sea coral Thomas Felis and JfirgenPfitzold FachbereichGeowissenschaften, UniversitfitBremen,Bremen,Germany

Yossi Loya Department of Zoology, Tel Aviv University,Ramat Aviv, Israel

Gerold

Wefer

FachbereichGeowissenschaften, UniversitfitBremen,Bremen,Germany

Abstract.Theenvironmental interpretation of the13C/12C variations in theskeletons of massive coralsis stilla matterof debate. A 19-yearseasonal skeletal13C/12C recordof a shallow-water Poritescoral from the northernRed Sea (Gulf of Aqaba) documents

interannual events of extraordinarily largeplankton blooms, indicated byanomalous •3C depletionsin the coral skeleton.These bloomsare causedby deep verticalwater mass mixing,convectively drivenin colderwinters,whichresultsin increasedsuppliesof nutrientsto the surfacewaters.The deepverticalmixingscan sometimesbe drivenby the coolingoccurringthroughoutthe Middle East after largetropicalvolcaniceruptions.We

therefore haveevidence in ourcoralskeletal 13C/12C recordfor anindirectvolcanic signal of the eruptionsof E1 Chich6n(1982) and Mount Pinatubo(1991). Deep mixinginduced

13C/12C variations of thedissolved inorganic carbonin thesurface waterscanbe neglected at thislocation. We therefore suggest thatthe•3Cskeletal depletions canbebest explainedby changesin the coral'sautotrophy-heterotrophy diet, throughincreased

heterotrophic feedingonzooplankton duringtheblooms. Increased feedingon •3Cdepletedzooplankton or increasedheterotrophyat the expenseof autotrophycan both •3 resultin a C-depletedcoral skeleton.However,this suggestion requiresmore testing.If

ourconclusions aresubstantiated, seasonal skeletal •3C/r2C records of coralswhichchange from autotrophyunder normal conditionsto increasedheterotrophyduring bloom events may be usedas indicatorsof oceanpaleoproductivityat interannualresolution,available from no other source.

1.

Introduction

The 180/160 variations in the skeletonsof massivecorals have been shownto provide a high-resolutionseasonalproxy for seasurfacetemperature(SST) and/orseasurfacesalinity (SSS)for the pastseveralcenturies[Coleet al., 1993;Linsleyet al., 1994; Quinn et al., 1996; Charleset al., 1997;Kuhnertet al.,

1995].Endosymbiotic photosynthesis preferentially fixes12C relativeto 13Cintoorganiccarbon,thusenriching theinternal dissolved inorganiccarbon(DiC) "pool"from whichcalcifica-

tionin coralstakesplacewith13C.In general, periods of higher photosynthesis shouldleadto increased concentrations of 13C in coral skeletons[Fairbanksand Dodge, 1979; Swart, 1983; McConnaughey, 1989a].It iswidelyassumedthat photosynthe-

1998].The interpretation of seasonal coralskeletal13C/12C siswithdraws andrespiration adds13C-depleted carbonto the variationsin environmentalterms is still a topic of debate internal DIC pool [McConnaughey et al., 1997]. Variations in [Swan et al,, 1996] becauseof complicatedinteractionswith the 8•3C of the DIC of the seawater have also been shown to physiological processes suchas symbiontphotosynthesis and affectthecoralskeletal813Csignal[Swartetal., 1996].On the respiration. Thereforethe applicability of the seasonal 8•3C other hand, the possibleimportanceof changesin the autotdietof coralsfor the 813Csignalin their signalmeasuredin coral skeletonsas a recorderof pastocean- rophy-heterotrophy skeletons has also been pointed out [Carriquiryet al., 1994; atmospherevariabilityhas been hamperedin paleoclimatic Swart et al., 1996]. Heterotrophy means coral feeding on alresearch.Exceptionsincludethe work of Shenet al. [1992].The mostprevalent opinionis thatskeletal8•3Cin photosyntheticlochthonoussourcesof organic carbon, mainly zooplankton coralson the seasonaltimescaleis mainly controlledby the photosyntheticactivityof the coral'sendosymbioticalgae,and it is thereforeattributedto the seasonallight cycle,cloudiness, or water column transparency[Fairbanksand Dodge, 1979; Piitzold,1984;McConnaughey,1989a; Wellingtonand Dunbar, Copyright1998by the AmericanGeophysical Union. Paper number98JC02711. 0148-0227/98/98JC-02711509.00

withitstypical13C-depleted isotopic signature, anda resulting contribution of 13C-depleted respiratory CO2 to the coral's internal DIC pool. This is oppositeto the processwhere organic carbon is usually derived by photosyntheticcorals,i.e., from photosynthesis of the endosymbiotic algae(autotrophy). Relativechangesof the proportionof thesetwo organiccarbon food sources,with their different isotopic signatures,could influencethe isotopiccompositionof the coral'sinternal DIC pool from which calcificationtakesplace [Swartet al., 1996].

30,731

30,732

FELIS ET AL.: PLANKTON BLOOMS RECORDED IN CORAL SKELETAL 8•3C

32 øN

35.0øE

34'9øE iSRAEL Ellat

30øN

Sinai

coral

location

Aqaba 28øN

29.5øN

RDAN

5 kilometres i

Figure 1. Samplinglocationof the coralcore (EILAT-1) near the northernend of the Gulf of Aqaba (Red Sea). The coralcolonyis closelylinked to open-seaconditionsdue to the narrowfringingreef and the steep submarineslope.

Recently,Gaganet at. [1994,1996]reportedthat •3Cenrich- [Wolf-l/echtet at., 1992; Genin et at., 1995].Interannualvariaments

in the

skeleton

of corals

from

Australia

culminate

build the reproductivetissueprior to spawning.Gagan et al. suggestedthat the reproductivemodulation of the coral skel-

tionsin winter air temperatureare directlylinked to variations in maximummixing depth [Genin et al., 1995]. Anomalously coldwintersdrive the verticalmixingto depthsexceeding600850 m [Wolf-l/echt et al., 1992; Genin et al., 1995]. During summerthe stratified surfacewaters of the Gulf are depleted

etal 15•3C signalcanbe usedas an accuratetime markerfor

of nutrients.

sharplyat the time of the annual coral spawningevent. This

wasexplainedby the rapidsequestering of •2C requiredto

Because

the concentration

of nutrients

increases

constructingcoral time series. with depth [Reissand Hotfinger,1984;Lindell and Post, 1995], Here we presentevidencefrom the moderatelyoligotrophic winterswith deepverticalmixingresultin increasedsuppliesof Gulf of Aqaba [Reissand Hotfinger,1984]in the northernRed nutrientsto the surfacewaters,leadingto extraordinarilylarge Sea that coral skeletal •3C variations record interannual planktonbloomsin spring(mid-Marchto mid-May) [Geninet oceanographicand climatic variability. A seasonal 19-year al., 1995;Lindell and Post, 1995]. skeletal •3C record derived from a shallow-water coral docuWinterswhich drive a deepverticalmixinghaveonly slightly ments interannual events of extraordinarilylarge plankton lower SSTs than averagewinter minimum SSTs.This is made blooms.These bloomsare causedby deep verticalwater mass possibleby the unusuallyweak water-columnstratificationof mixing,which sometimescan be driven by the coolingfollow- the Gulf of Aqaba. The contributionof salinity to vertical variationsin water densityis negligiblein the Gulf; becauseof ing major tropicalvolcaniceruptions[Geninet al., 1995]. The Gulf of Aqaba is a 1830-m-deep,narrow(180 km long, this, vertical profilesof densityand potential temperatureare with 14 km averagewidth), desert-surrounded basinforming almostmirror imagesof eachother [Reissand Hotfinger,1984; the northeasternextensionof the Red Sea (Figure 1). The Genin et al., 1995]. The averagelowestdaily SST from 19881995, a period encompassingwinters with and without deep climate is arid, with high insolation,high evaporation(-400 cm/yr), and negligibleprecipitation(-2.2 cm/yr) and runoff. verticalmixing,had a rangeof only 0.7øC.The minimummixing Nutrient levelsand primary productionare very low, and thus depth duringthat period occurredin the winter of 1990-1991 light penetrationis deep [Reissand Hotfinger,1984].The evap- (300m), andthe maximummixingdepthoccurredin thewinterof orative lossis compensatedby inflow from the Red Sea in the 1991-1992(>850 m). However,the mixingdepthis alsodepensouth.This inflow is confinedto the upper warmer layer by a dent on the lengthof the sea-cooling periodduringwinter. The shallowsill at a water depth of 252 m (Straitsof Tiran). This deepverticalmixingeventsat the northernend of the Gulf of resultsin unusuallyhigh temperaturesat depth, for example, Aqabaare amplifications of rather small-scale interannualvaria20.6øCat 1200 m. Consequently,the vertical stratificationin tionsin winter minimumSST, and they are possiblyuniqueto the Gulf is unusuallyweak [Klinkeret at., 1976].During sum- deepmarginalseaswith shallowsills[Geninet at., 1995]. mer (April-October) an upper200-300 m thermallystratified layer with temperaturesbetween21ø and 26øCat the surface 2. Material and Methods overliesa thermallyhomogenouslayerof -21øC [Klinkeret al., 1976; Wolf-l/echtet al., 1992]. Winter cooling (NovemberA coral core (EILAT-1) was collectedfrom a 0.85-m coral March) of the surfacewaters causesdestabilizationof the colony(Potiressp.)near the northernend of the Gulf of Aqaba water column, which can result in deep convectivemixing in (29ø31'N,34ø56'E),usingan underwaterpneumaticdrill (Figlate winter (February/March)at the northernend of the Gulf ure 1). The coral is locatedat a water depth of 4.5 m in front

FELIS ET AL.: PLANKTON

BLOOMS RECORDED

of the reef crest near the H. Steinitz Marine Biology Laboratory at Eilat (Israel). The site is characterizedby a steepsubmarine slope;the proximityto the 500- to 700-m-deepcentral trough of the Gulf is ---3 km. The Gulf becomesincreasingly deeperto the southwest;the locationis thereforecloselylinked to open-seaconditions.We only analyzedthe top 0.16 m of the corebecausechangesin the coral'sgrowthaxisdid not provide a continuousrecord below this depth. X radiograph positive prints of the sliced 5-cm-diameter coral core were used as guidesfor continuousspot sampling along the axis of maximumcoral growth, following precisely the major growthaxisof a singlefan of corallites(Figure 2). This samplingtechniquelimits the influenceof "kinetic" isotope disequilibriaeffects[McConnaughey, 1989a,b]. Samples were collectedby low-speeddrilling usinga dental tool with a 0.8-mm-diameterbit. For isotopicanalysiswe useda Finnigan MAT 251 mass spectrometercoupled to a Finnigan MAT automatedcarbonatedeviceat the stableisotopelaboratoryof the Department of Geosciencesat Bremen University,Germany.Long-termreproducibility,deducedfrom replicatemea-

IN CORAL SKELETAL

813C

30 733

'1985

surements of an internal carbonate standard, is less than

_+0.07%0 for •80 and_+0.05%0 for •13C,respectively (lrr over a 1-yearperiod). Values are reported relative to the Pee Dee belemnite(PDB) referencestandard. The growthrate of the coral decreasedmore or lesscontinuouslyfrom 10 (1974) to 4.5 mm/yr (1992). We sampledat approximately1-mmintervals,whichresultsin an averagesampling frequencyof 7-8 samplesper year, providingapproxi-

matelybimonthly resolution. Coralskeletal•80 variations at

1

l

1980

the northern end of the Gulf of Aqaba primarily reflect the seasonalSST cycleof •--5øC[Klein et al., 1992, 1993]; SSS is nearly constantand variesby lessthan 0.5%0 throughoutthe year [Wolf-Vechtet al., 1992]. The coral chronologyis con-

l

structedby settingthe maximum•80 valuein a givenyear equal to mid-March (on average,the time of winter minimum SST) and by assuminga constantcoral growth rate between March of each year. Therefore we interpolated linearly between thesefixed pointsfor further age assignments.

Watersamples for •3C analysis of the DIC werecollected duringthe dayin glassbottles(3-m water depth)and poisoned, and bottle capswere sealedwith wax.Total dissolvedinorganic carbonwas extractedby acidification.The cryogenicallypurified, resultantgaswasanalyzedusinga FinniganMAT Delta-E massspectrometerat the stable isotope laboratory,Department of Geosciences, BremenUniversity.Values are reported relativeto PDB with an analyticalerror of •--+0.1%o (lrr). Before applyingthe leastsquaressmoothingfilter [Savitzky

1975

andGolay,1964]to the •3C datain Figure3b,the serieswas interpolatedlinearly to six equallyspacedvaluesper year for the filter to be optimal, providinga bimonthly resolution.All these procedures were performed using the AnalySeries (1.0a7) softwarepackage[Paillardet al., 1996]. 3.

3.1.

Results

and Discussion

Figure 2. X radiograph positive print of the coral slab (Poritessp.). The skeletaldensitybandingpattern of alternat-

ingbandsof high(dark color)andlow density(lightcolor)can be clearly seen. One year is representedby a low and high density-bandpair. Also shownare the correspondingyears of skeletonprecipitation.The samplingtransectappearsaswhite circles.The black bar in the upper right corner is 1 cm.

Vertical Mixing, Plankton Blooms, and Volcanic

EruptionsRecordedin Coral Skeletal•3C

Figure3bshows theskeletal •80 and•13Crecords obtained water depth [Reissand Hottinger,1984;Lindelland Post,1995], fromthecoralcore.Coralskeletal•80 isnotsensitive enough increasinglymore nutrientsare transportedsuccessively to the to detect the anomalouslycold winters driving a deep vertical mixing at the northern end of the Gulf becausethesewinters have only slightly lower SSTs than average winter minimum SSTs.

Because

the concentration

of nutrients

increases

with

surfacewaters when mixing is reachingincreasinglygreater depths.Thus a vertical mixingexceedinga thresholddepth of •--550m resultsin extraordinarilylarge blooms(B. Lazar, personal communication,1997). This critical depth is actually a

30,734

FELLS ET AL.: PLANKTON

BLOOMS RECORDED

IN CORAL SKELETAL

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Figure3. Coralrecord(EILAT-1) andenvironmental parameters forthenorthernendof theGulfof Aqaba (Red Sea). (a) Annualcoralgrowthrate is calculated from mid-Marchto mid-Marchand plottedon

mid-September. (b)Coralskeletal alSOand&]3C records areshown. Thethicklinerepresents a 21-point least squaressmoothing filter [Savitzky and Golay,1964].The dottedbarsindicatedeepverticalmixingand

increased plankton bloomevents, derived fromthecoral&]3Crecord.(c) Maximum wintermixingdepth, mainlybasedontemperature versus depthprofiles, isplottedonmid-March(1,Klinkeretal. [1976];2, Reiss etal. [1976];3, Reiss etal. [1977];4, Geninetal. [1995]andWolf-Vecht etal. [1992];5-7, Geninetal. [1995]; 8, Geninetal. [1995]andLindellandPost[1995]).Arrowsindicate thatmixingexceeded themaximum depth thatwasmeasured. Mixingsexceeding thecriticaldepthbandof -550 m (horizontal dashed line)resultin extraordinarily largespringblooms(B. Lazar,personal communication, 1997).(d) Averageconcentration of surface chlorophyll a duringspringbloom[Geninetal., 1995],asanindicator of bloomintensity andsurface zooplankton concentration (A. Genin,personal communication, 1997),isplottedonmid-April.(e) Average monthly winterairtemperature (December-February) forEilat[Bakeretal., 1994]isplottedonmid-January; thehorizontal solidlinerepresents theaverage of thisrecord.Verticaldashed linesindicatethetwolargest tropicalvolcanic eruptions duringtherecordIRebeck andMao,1992].(f) Sunshine hourspermonthforEilat (IsraelMeteorological Service,unpublished data, 1991).PDB, Pee Dee belemnite.

FELLSET AL.: PLANKTON BLOOMS RECORDED IN CORAL SKELETAL 813C

band and can not be consideredas a definite depth limit (B. Lazar, personalcommunication, 1997). Figure 3c showsmaximum winter mixingdepthsat the northern end of the Gulf of Aqaba. Figure 3d presentsthe averageconcentrationof surface chlorophylla duringspringbloom, revealingthe relationshipbetweenthe critical mixingdepth of 550 m and increased

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blooms[Geninet al., 1995].The coralskeletal813Crecord shows anomalous •3Cdepletions in thewintersof 1975-1976,

'•

1988-1989, 1991-1992, and 1992-1993, which correspondto all the availableinstrumentallydocumenteddeepverticalmixing and increasedplankton bloom events, using the 550-m

•

.T

•+•

'

+ ß •M

:

+

' ß Seasonala180 maxima

threshold depthascriterion(Figure3c).Theseanomalous •3C

' • Seasonala•80 maxima associatedwith deep ve•ical mixing

skeletaldepletionsriseup duringwinter from a groundlevelof

i

a moreor lessclearseasonal skeletal•3C cyclein the coral record,asemphasized bysmoothing of the 8•3Cdata(Figure

i

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Corala•80 (%0PDB) 3b). On the other hand, in the wintersof 1976-1977, 19891990 and 1990-1991, with only shallowto moderatemaximum Figure4. Scatterplot of coralskeletal8•80 versus8•3C.Seamixingdepth,resultingin only minor springblooms,no anom- sonal8•sOmaxima arelabeled(mostenriched 8•sOvaluein a

alous•3Cdepletions canbe identified in thecoralrecord.The givenyearincluding adjacent values>8•8Omax--0.1%o ). Seatypicalpatternof theanomalous •3Cskeletal depletions in the sonal8•SOmaximawhichare associated with deepvertical coral record can be describedas (1) extraordinarilynegative mixingand increasedplankton bloom eventsare additionally

8•3Cvalues(1.0%ofol-

labeled.

lowedby a > 1.4%oincreaseproducingpronouncedspikes,and (3) the timing in late winter-earlyspring.In the winter of 1974-1975, vertical mixing exceeded500 m [Klinker et al., 1976]but probablynot the 550-m thresholddepth,as our coral

eters(solarradiation,relativehumidity,wind speed,and cloud cover) were shownto be not significantlycorrelatedwith the skeletal8•3C recordindicatesno deepverticalmixingand maximum mixing depth of the water column [Genin et al., increasedplankton bloom event. 1995]. Using thesefactorsascriteria,we detectedtwo more winters Coral Skeletal•3C Cycle with a deep vertical mixing and increasedplankton bloom 3.2. The Seasonal In many locationsthroughout the tropics and subtropics, event (1977-1978 and 1982-1983) during a period without availableinstrumental-based records(Figures3b and 3c). The coral skeletal 8•3C variations on the seasonal timescale have 1982-1983 event has been previouslysuggestedbecauseof an been attributedto the seasonalcycleof light [Fairbanksand extraordinarilylarge springbloom only observedby the naked Dodge,1979;P•itzold,1984;McConnaughey,1989a;Shenet al., eye and the anomalouslycold winter air temperatures[Genin 1992;Wellingtonand Dunbar, 1995].This hasalsobeen shown et al., 1995] (Figures 3d and 3e). A commonphenomenon for the northern end of the Gulf of Aqaba [Kleinet al., 1992, throughoutthe Middle East is a cold air temperatureanomaly 1993],where the warm summerseasonis more sunnierand the occurringduring the first winter after major tropical volcanic cold winter seasonis more cloudier. Light intensityand SST eruptions[Robockand Mao, 1992].The 1991-1992 deep ver- are positivelycorrelated,with a time lag of about one to three tical mixingand increasedplanktonbloom eventwasdrivenby months.Annual light intensityminima (December-February) the anomalouslycold air temperaturesfollowingthe eruption precede SST minima (March), and light intensitymaxima of Mount Pinatubo (Philippines,June 1991) [Genin et al., (July)precede SSTmaxima(August). For coralskeletal8•sO 1995]. The event in the winter of 1982-1983 followed the and8•3Cvariations thisshouldresultin a weaknegative coreruption of E1 Chich6n (Mexico, April 1982). We therefore relationat the seasonalscaleand a shiftin phase.A scatterplot

haveevidence in ourskeletal813Crecordfor a coralresponse of 8•80 versus8•3Cis shownin Figure4. For the period from the northern Red Sea to the two largesttropicalvolcanic 1974-1983,skeletal8180 and 813Cin our coralrecordreveal eruptionswhichoccurredduringthat period [RobockandMao, sucha negativecorrelation(Figure 3b). The correlationcoef1992]. The effect of volcanism-induced coolingon coral skel- ficient r = -0.35 is significantat the 99.5% level. This negetal8•80hasrecently beendescribed [Gagan andChivas, 1995; ative correlationcan be explainedwith increasedendosymbiCrowley et al., 1997].Crowley et al. [1997]alsodiscussed 8•3C otic photosynthesisdue to higher insolationduring the warm

enrichments coinciding withthe 8•80 enrichments associatedsummerseason, resulting in a 13C-enriched and180-depleted with volcanic eruptions in their coral record. However, we coral skeleton,and vice versafor the winter season[Fairbanks presentevidencefor an indirectvolcanicsignalin the skeletal and Dodge,1979;Swan, 1983;McConnaughey,1989a].For the 8•3C record of a coral from a location where coral 8•80 is not period 1984-1993 this correlation breaks down; there is no sensitiveenough to detect suchevents. statistically significant correlation betweenskeletal8180and Apparently,the deepverticalmixingand increasedplankton 813C(r = -0.11), owingto changes in the patternof the bloom eventsoccurringduring the 1970swere not as strongly seasonal 813Ccycle.This changein correlation, whenintercoupledto anomalouslycoldwinter air temperaturesas those preted as a decreasedinfluenceof the seasonallight cycleon in the waterwhich occurredsincethe beginningof the 1980s.During the coralskeletal813C,couldbe due to disturbances 1970s,probably other forcing factorswere driving the deep column transparency,probably causedby increasedbuilding vertical mixingin the northern Gulf of Aqaba. The reasonfor activitiesalongthe shoresincethe early 1980s.In summary,the this is beyondthe scopeof this paper. However, for the period seasonal cycleof lightprobably affectsthe skeletal813Cvari1988-1995, winter averagesof other potential forcingparam- ationsof our coral,especiallyduring1974-1983,but it cannot

30,736

FELLSET AL.: PLANKTON BLOOMS RECORDED IN CORAL SKELETAL 813C

accountfor the variabilityin the seasonalamplitude,and in no

casefor the anomalous •3Cdepletions whichoccurduringthe entireperiodof thecoralrecord(Figures 3band3f). The•3C

2.1

1.9

depletions are superimposedon this more or less light-

controlled coralskeletalt513C cycle.Thereforetheprocess creatingthe •3Cskeletaldepletions hasto haveits originin the

1.7

watercolumn,asrunoff-induced t5•3Cvariationsof the surface water DIC shouldalsobe negligiblein this desert-surrounded arid setting.

3.3. Causesfor the Anomalous•3C Depletions in the Coral

Skeleton

The coralstableisotoperecordseemsto be fairly robustwith respect to "kinetic" isotope disequilibria effects [McConnaughey,1989a, b]. Although the growth rate of the coral decreasesfrom 10 (1974) to 4.5 mm/yr (1992), the isotope

1.5 1.3

MIJ

IJ

IAISlOINID

Month

Figure5. Composite recordof theseasonal t5•3C cycleof the

dissolvedinorganiccarbon(DIC) in the surfacewatersat the northernend of the Gulf of Aqaba (solidcirclesare from 1993, with 3-m depth and daytimesampling;solid squaresare from valuesdonotshowa corresponding enrichment in skeletal 1sO 1979 to 1980,with the calculatedaverageof daytimesamples or •3Casexpected fromkineticisotope fractionations (Figures from the 0- to 10-m depth interval, derived from the data by et al. [1994]).The dottedbar indicatesthe periodof 3a and 3b). The calculatedannual coral growth rate (mid- Shemesh March to mid-March) revealsno pattern associated with the late winter-spring, where deep vertical mixing and increased

anomalous 13Cskeletaldepletions. Two furthermethodsof growth rate calculationwere performed by fixing the coral chronologyon mid-Marchand mid-Augustsimultaneously (on average,the time of minimum and maximumSSTs;resultsare not shownhere). Also, in this calculatedannual(mid-August to mid-August)as well as the seasonalgrowth rate (midAugustto mid-Marchand mid-Marchto mid-August),no pat-

planktonbloomeventsusuallyoccur.The t5•3Cof the surface

water DIC has a seasonalcycleof probablylessthan 0.4%o, consideringa correction for the 0.25%o offset between the mid-May measurementsfrom 1980 and 1993. This offset is

probablydue to an increased anthropogenic input of •3Cdepleted CO 2 into the atmosphere.For example, measurements of the t5•3C of the surface water DIC near Bermuda

duringthe period 1984-1992 indicatedan averagedecreaseof

ternassociated withthe 13Cskeletaldepletions wasdetected. ---0.022%o/yr[Bacastowe! al., 1996]. The t5•3C of theDIC in theupperwaters(0-200m) of the northern Gulf of Aqaba throughoutthe year (on average, 1.9%o)is controlledmainlyby the processof isotopicequilib- personal communication, 1997) and near-reef areas are rium with the atmosphere[Shemesh et al., 1994].Vertical mix- stronglyaffectedby zooplanktonbloomsat this location[Echingin winterresultsin a watermasswithupperwatert5•3C - elmanandFishelson,1990].In general,deepwatercorals(>30 DIC characteristics. Thereis no imprintof the •3C-depleted m), whichare growingat lowerlight intensitiescomparedwith t•13C-DICsignature of the summerdeepwater(on average, shallow-watercorals,largelyfeed on allochthonoussourcesof 1.55%oin 200-600 m) on the upper waters duringvertical carbon(e.g.,zooplankton)[Muscatine etal., 1989],owingto the mixing[Shemesh etal., 1994].Deepmixinginducedt5•3C vari- attenuation of photosyntheticallyavailable radiation with ations of the surface water DIC therefore can be excluded to depth and thereforelower photosynthetic rates.This has also createtheanomalous •3Cdepletions in ourcoralskeletal t5•3C been describedfor the reef at Eilat [Muscatineet al., 1989]. record.The t5•3C of thesurface waterDIC (0-10 m) shows a Earlier studiesin the Caribbeandescribedtypicalfeedingreweak seasonalcycleof probablylessthan 0.4%o (Figure 5), sponsesfor Poritesspp.coralson zooplankton[LewisandPrice, which has a roughlynegativecorrelationto the averagesea- 1975].Recently,controlledfield experimentsin the Caribbean sonal coral skeletal t5•3C variations. Thus it seems to be of demonstratedrelativelyhigh capture rates of massivecorals

minorinfluenceon the t5•3Cvariabilityin the coralskeleton. for zooplankton [Sebens et al., 1996].The t5•3Cof average The seasonal t5•3C variations of the surface water DIC are

marine plankton from the Gulf has values of about -21%o [Shemeshet al., 1994].That the isotopicsignatureof a coral's sultingin •3Cenriched valuesduringthe periodof increased food producesan imprint on the isotopiccompositionof a

probablymodulatedby the seasonalcycleof productivity,re-

productivity in winterandspringand •3C-depleted valuesin summer due to increasedoxidation of organicmatter in the reef.

coral'sskeletonhasbeenshownby experiments, where•4Cspikedfoodswere fed to coralsand •4C incorporation into skeletalcarbonateswasobserved[Pearse,1970].We therefore

Three possiblemechanisms,which are not mutually exclu-

suggest thattheanomalous •3Cskeletaldepletions in ourcoral

sive,aresuggested to explainthe anomalous •3Cdepletions in

record can be best explainedby changesin the coral'sautotrophy-heterotrophydiet throughincreasedheterotrophicfeeding on zooplanktonduring the extraordinarilylarge plankton

the coral skeleton.

1. During the extraordinarilylarge plankton blooms following a deep vertical mixing,the water-columntransparency at the northernend of the Gulf is reduced[Geninet al., 1995]. Becauseof the reduced light availability and therefore decreasedphotosyntheticallyavailableradiation, the photosynthesisof the coral's endosymbioticalgae should decrease,re-

blooms.It is assumed that the typical•3C-depleted isotopic signatureof the zooplanktonproducesan imprint on the isotopiccompositionof the coral'sskeletonthroughan increased

contribution of •3C-depleted respiratory CO2 to the coral's internal DIC pool. Possiblereasonsfor an increasedfeeding

sultingin a •3C-depleted coralskeleton[Fairbanks andDodge, on zooplankton during the blooms are increasedavailability 1979;Swart,1983;McConnaughey,1989a]. and/or decreasedautotrophydue to a reducedphotosynthetic 2. During the increasedblooms,consequently,the concen- activityof the coral'sendosymbioticalgaeduringtheseperiods tration of surfacezooplanktonis unusuallyhigh (A. Genin, of reducedwater columntransparency.

FELLSET AL.: PLANKTON BLOOMS RECORDED IN CORAL SKELETAL 813C

3. However, McConnaugheyet al. [1997] postulatedthat

30,737

affectedby the algal mat. Becausethe 1991-1992 bloom event

not much•3C-depleted respiratory CO2 is incorporated into is thoughtto be the largestduringthe last48 years[Geninetal., coral skeletonsbecausecoralscalcifymainly during the daytime, which is the period of active photosynthesis when photosyntheticCO2 uptake is severaltimesfaster than respiratory CO2 release,while feedingon planktonoccursmainlyat night. The carbonateisotopiccompositionof coral skeletonsshould thereforereflectperiodsof maximumphotosynthetic influence rather than periodsof strongrespiratoryinfluence[McConnaugheyet al., 1997]. Therefore a third possiblemechanism, which also postulatesincreasedheterotrophy,is suggestedto

1995], algae coveringof our colonyduring the period of the coralrecordcan thereforebe excluded.Consideringa possible effect of the algal mat on the DIC in the ambient water, an

enrichment in t5•3Cshouldbe expected, whichis opposite to the anomalous t5•3Cdepletions in the coralskeleton. On the other hand, the decay of the algal mat could have possibly

caused a depletion in the t5•3Cof thelocalDIC. However,as our coralcolonyis growingin front of the reef crestand closely linked to open-seaconditionsbecauseof the steepsubmarine

explainthe anomalous •3C skeletaldepletions in our coral slope,wedonotexpectanysignificant depletion in thet5•3C of record.Increasedheterotrophyat the expenseof autotrophy the local DIC owingto algal mat decayat this location. by the coral during the extraordinarilylarge planktonblooms Recently,Speroetal. [1997],on the basisof experiments with shouldreducethe "photosyntheticeffect" describedby McCo- foraminifers and discussions of the earlier results of McConnnaughey[1989a] through reducedphotosyntheticactivityof naughey [1989b],proposed that coralskeletalt5•3Cpossibly

thecoral'sendosymbiotic algae,andit shouldresultin a •3C- becomesmore depletedin •3C with increasingseawater watersof thenorthernGulf of depleted coral skeletonwithout any need for incorporating [CO•-] andpH. In thesurface more•3C-depleted respiratory CO2fromincreased zooplank- Aqaba there are no significantchangesin p H, carbonatealkatonfeeding. In summary, weinterpretourskeletalt5•3C record linity, or total dissolvedinorganiccarbonduringverticalmixing asbeingtypicalfor a coralwhichis fluctuatingbetweenautotrophy and heterotrophyon the interannual scale,where increased heterotrophy during extraordinarily large plankton

watersto createtheanomalous •3Cskeletaldepletions in our

bloomevents resultsin anomalous •3Cdepletions in thecoral

coral record.

in winter [Shemesh et al., 1994].Thereforewe canexcludedeep mixinginducedchangesin the carbonatesystemof the surface

One wouldexpectthat the maximumcoralskeletalt5•80 That increased heterotrophy produces •3C-depleted coral value in a given year, indicating the period of coldest SST skeletonshas been suggestedto explaina generalincreasein (mid-March),alwaysprecedes an anomalous •3C depletion, theseasonal skeletal/5•3C variation withdepthin coralrecords indicatingextraordinarilylarge plankton blooms(mid-March skeleton.

of Poriteslobatafrom Costa Rica [Carriquiryet al., 1994] becausethis pattern is contraryto the expectedattenuationwith depth in proportionto the decreasein light-intensityvariation with depth [Fairbanksand Dodge, 1979]. In coral records (Poritesspp.) from Eilat also no attenuationin the seasonal

skeletalt5•3C variation withdepthon a profilefrom3 to 51 m is evidentin the dataofKlein et al. [1993],despiteonly20-30% of the measuredsurfacelight valuesbeing availableat 51-m depth [Reissand Hotringer,1984]. This additionallyimplies changesin the autotrophy-heterotrophy diet of Eilat Porites spp.coralson the seasonalscaleand a resultingmodulationof

to mid-May). However,as our resolutionis approximatelybimonthly,it can not be expectedthat the coralrecordpreserves 1- to 2-month-scaletime lags.Furthermore, differencesin the proxy signalpreservationof different environmentalforcing factorsduringskeletogenesis, e.g.,suddenpulseevents(plankton blooms)andannualcycles(SST), maycomplicatethe pres-

ervationof suchsmall-scale timelagsin thecoralskeletalt5•80 andt5•3Crecords[Tayloretal., 1995;Barnesetal., 1995].This probablyalsoexplains the anomalous •3C depletions apparentlypreceding the mostpositivet5•80valuesin oneor two

winters with deep vertical mixing and increased plankton bloomsin our coralrecord.Independentof theseuncertainties Additional geochemicaltests to verify our hypothesisthat in small-scaletiming, our resultsshowthat the coral successthe anomalous •3C skeletaldepletions are due to increased fully recordslarge-scalelate winter-springconditions(Februcoralheterotrophy couldincludemeasurements of the•SN/•4N ary to mid-May) in the water column.In summary,the coral ratio of the organiccontent of the coral skeleton.However, skeletalt5•3Crecordprovidesa proxyfor the interannual preliminarytestsrevealeda coral skeletalnitrogencontentof oceanographic variabilityin the northernGulf of Aqaba,which a few ppm in a roughapproximation(C. Gervaisand M. Segl, can sometimesbe influencedby the cooling following large personal communication, 1998).Because of this,tS•SN profiles tropicalvolcaniceruptions. with a resolutionof---2-4 years only would be possible,not usablefor verification.Further testscould includefeeding exthe seasonal t5•3Cvariations in their skeletons.

periments witht5•3Canalysis of thezooplankton, coraltissue,

4.

endosymbiotic algae,and coral skeletonor, for example,feed-

Our findingsprovidesupportfor the idea that changesin the autotrophy-heterotrophy diet of coralsplay an important role

ingexperiments with •4C-spiked zooplankton.

Conclusions

We excludethe possibilitythat the extensivealgalmat which coveredbroad sectionsof the underlyingreef duringthe large 1991-1992bloom event[Geninet al., 1995]wasresponsiblefor

in the 15•3C variabilityof theirskeletons. The anomalous •3C

front of the reef crest, and it can be assumedto have not been

tal evidence. If our conclusions are substantiated, then our

skeletaldepletionsin our coralrecord,indicatingdeepvertical mixing and increasedplanktonbloom eventsin the northern theanomalous •3Cdepletion in thecoralskeleton thatwinter- Gulf of Aqaba (Red Sea), can be best explainedby increased spring,consideringa possiblecoveringof the coral colonyand heterotrophicfeeding on zooplanktonduring extraordinarily anerobicconditionsat the baseof the mat. The algal mat had large plankton blooms. Increased heterotrophic feeding on a thicknessof only ---15 cm above the bottom, and therefore •3C-depleted zooplankton or increased heterotrophy at the corals growing on elevated substrateswere not covered by expense of autotrophy by the coralcanbothresultin a •3Calgae[Geninet al., 1995].The coralcolonyfrom whichthe core depletedcoral skeleton.Validation of our conclusionsawaits for this studywasrecoveredis 0.85 m high,growingsolitaryin testingwith coralrecordsfrom other locationsand experimen-

30,738

FELIS ET AL.: PLANKTON BLOOMS RECORDED IN CORAL SKELETAL 813C

resultspromotethe applicability of seasonal skeletal8•3C

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(ReceivedApril 14, 1998; revisedJuly 28, 1998; acceptedAugust 18, 1998.)