Jan 15, 1992 - JOHN J.CULLEN, 1,2 MARLON R. Lp. wIs, 3 CtmxISS O. DAVIS, 4 AND ...... Caldwell, 1985; Carr et al., this issue], can produce a diel cycle.
JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 97, NO. C1, PAGES 639-654, JANUARY 15, 1992
Photosynthetic Characteristics andEstimatedGrowthRatesIndicateGrazingIs the
Proximate Controlof PrimaryProduction in theEquatorial Pacific JOHN J.CULLEN, 1,2MARLON R. Lp. wIs,3 CtmxISS O. DAVIS, 4AND RICHARD T. BARBER S Macronutrients persistin the surfacelayer of the equatorialPacificOceanbecausethe productionof
phytoplankton is limited;thenatureof thislimitation hasyet to be resolved. Measurements of photosynthesisas a function of irradiance (P-I) provide information•on the control of primary productivity,a questionof great biogeochemicalimportance.Accordingly, P-I was measuredin the equatorial Pacificalong150øW,duringFebruary-March 1988. Diel variabilityof P-I showeda pattern consistentwith nocturnalverticalmixing in the upper20 m followedby diurnal stratification,causing photoinhibition nearthe surfaceat midday.Otherwise,the distribution of photosynthetic parameters with
depthand the stabilityof P-I duringsimulatedin situ incubations over 2 daysdemonstrated that photoadaptation was nearlycompleteat the time of sampling:photoadaptation had not been effectively countered by upwellingor verticalmixing,Measurements of P-I andchlorophyll duringmanipulations of
traceelements showed that simpleprecautions to minimizecontamination weresufficientto obtainvalid ratemeasurements andthatthespecific growthratesof phytoplankton werefairlyhighin situ,a minimum
of 0.6d-1.Dielvariability of beamattenuation alsoindicated highspecific growth ratesof phytoplankton anda strongcoupling of production withgrazing. It appears thatgrazingis theproximate controlon the standing cropof phytoplankton. Nonetheless, the supplyof a tracenutrientsuchas ironmightultimately regulateproductivity by influencingspecies composition andfood-webstructure.
1. LNTRODUCTION
canlimittheproduction ofopen-ocean phytoplankton. They
suggested that the potentialfor growthof phytoplankton in Concentrations of chlorophylla and ratesof primary the eastern equatorial Pacific might be limited by the supply of productionare elevatedalongthe equator,wherethe vertical flux of nutrientsis enhanced by upwellingat the equatorial iron, which in the open oceancomesprin6ipallyfrom sources. Theconclusions of Martinandcolleagues divergence [ChavezandBarber,1987;Berger,1989].Primary atmospheric have been questioned [Banse, 1990] andtheconcept of ironproductivity andphytoplankton biomassare not as highasthe limitationhasbecomethe subjectof activedebate. Theperspective of DugdaleandWilkerson [1989;Dugdaleet al., this issue] is somewhat different: they suggest that theequatorial oceanandthisunexploited nutrientis thoughtto phytoplankton in upwellingsystemssuchas at the equatorfail indicatelimitation of the yield of phytoplankton biomass. to exploit suppliesof nitrate becauseinitial concentrations of This condition has been labeled a high-nutrient, lownitrateare too low to supporta rapid "shift-up"of assimilatory chlorophyllsituation(HNLC [Minaset al., 1986]). Thus,the flux of macronutrients could support,however:near-surface concentrations of nitrateare elevatedover a broadexpanseof
pathways. Suboptimal nitrate assimilationis therefore seen as
questionconfrontingoceanographers is not "Why is the the result of physicalforcing (rate of upwellingcoupledwith tropicalregionso rich?,"but rather"Why isn't the equator
nitrate concentration in the source water) rather than nutritionallimitation per se. Incompleteshift-up is regarded Incomplete utilizationof nitrateat theequatormightbe due here as a type of physiologicalimpairment,i.e., suboptimal to physiological impairmentof phytoplankton. For example, adaptationof phytoplanktonto ambient conditions. Barber and Ryther [1969] found a local minimum in productivity index(g C g Chl'1d'l) attheequator in theeastern A different explanation for the apparentimpairmentof nitrate assimilationin equatorialupwelling is that the neritic greener?"
PacificOcean.Theirexperimental results indicated thatspecific bloom-formingdiatomswhich characterizecoastalupwelling growth rates of phytoplanktonwere depressedbecausethe systems [Smetacek, 1985] are absent from the offshore
waterswerelow in thenaturalorganicchelators whichfacilitate regions,possiblybecauseof inadequateseed-stocks [Chavez, trace element nutrition [Huntsmanand Sunda, 1980]. More 1989]. The small oceanic species that dominate may be recently,Martin et al. [1989] supported the conceptthatiron geneticallyincapableof the shift-up responsedescribedby Dugdaleet al. [this issue]. Nutritional limitation of phytoplankton need not be Main e . invoked to explain persistenceof macronutrientsin surface 2Nowat Department of Oceanography, Dalhousie University,waters at the equator. Walsh [1976] assertedthat rates of Halifax, Nova Scotia, Canada. productivitynormalizedto chlorophyllwere similarover much
1Bigelow Laboratory forOcean Sciences, WestBoothbay Harbor,
3Department of Oceanography, Dalhousie University, Halifax, of the ocean,includingthe equatorialdivergence.He suggested that growth rates of phytoplankton at the equator are 4jet Propulsion Laboratory, California Institute of Technology,
Nova Scotia, Canada.
unimpaired but that a lack of significant environmental
Pasadena.
5Duke University Marine Laboratory, Beaufort, North Carolina. variability on the scaleof 5 - 10 days allowspersistenceof a
coupled phytoplankton-herbivoresystem so that herbivory
Copyright1992by the AmericanGeophysical Union. Papernumber91JC01320.
limitsthe standingcropof phytoplankton. Minaset al. [ 1986] alsofelt thatgrazingwasthe mostplausibleexplanation of the
0148-0227/92/91J
HNLC
C-0 1320505. O0 639
situation in open-ocean upwelling. The small
640
Cu•JJENETAL.:PHYTOPIJO•TONIN THE EQUATORIAL PACIFIC
phytoplankton that dominate the equatorial phytoplankton to remove obvious spikes and then averaged over 1-m [Chavez, 1989; Chavez et al., 1990; Pe•a et al., 1990] are
intervals.
especiallysusceptibleto control by small grazerswith short Photosynthesis VersusIrradiance generation times. Questionsabout limitation of primary productionat the The method of Lewis and Smith [1983] was usedto measure equatorcan be partially resolvedby looking at the physiology
photosynthesis as a function of irradiance(P-I) on samples of phytoplankton. One approach,describedhere,is to examine obtainedfrom four depthsat dawn, middayand dusk.Samples their photosyntheticcharacteristics.Becausephotosynthetic wereinoculated with14C-bicarbonate (finalactivity,about10 performanceis extremely adaptableto growth conditions •tCi mL -1) and aliquots of 1 mL were dispensed intoglass [Falkowski, 1980; Osborneand Geider, 1986; Harding et al., scintillationvials (7-mL capacity,not speciallycleaned)in a 1987; Cullen and Lewis, 1988; Cullen, 1990], we expectthat temperature-controlled aluminumblock. The exact amountof hindrancesto the growth of phytoplankton,whether due to label addedwas determinedby subsampling into a scintillation nutritional deficiencies or to inadequate time to adapt to vial nearly filled with the non-acidicfluor, AquasolII, thereby physical forcing, can be detected in measurementsof avoidingthe problemof losinglabeledinorganicC from acidic photosynthesis as a functionof irradiance.Here we describe fluor [Iversonet al., 1976]. A rangeof irradiancewas provided such measurements.We show that the photosyntheticsystems from below with 2 ENH-type tungsten-halogenprojection of phytoplanktonin much of the euphoticzone were well lampsdirectedthrougha heat filter of circulatingwater, and adapted to ambient conditions, indicating that neither attenuated with neutral density screens. Quantum scalar upwelling nor vertical mixing impaired the growth of irradiancein each positionwas measuredwith a Biospherical phytoplankton. Different measuresof primaryproductivityare InstrumentsQSL-100 4g sensor with a modified collector, comparedand severalestimatesof phytoplanktongrowthrates small enoughto fit in the bottomhalf of a scintillationvial for are examined. All of these estimates indicate fairly rapid the measurements.Incubations began within 30 rain of growth of phytoplankton,balancedby grazing.We conclude samplingand were terminatedafter 1 hour. Inorganiccarbon that specificgrowth rates of phytoplanktonin the equatorial was expelledby adding0.5 mL 6N HC1 and agitatingthe open Pacific were fairly high and that grazing was an important vialsfor at least1 hourin a hood.AquasolII fluor wasaddedand factor controlling the standingcrop of phytoplankton. the vials were agitatedagainbefore countingwith a Beckman LS1800 scintillationcounter.Countswere correctedfor quench 2. METHODS with the H# method. No correctionfor isotopediscrimination
wasmade.TotalCO2 wasassumed tobe2.1mM.
Basic Measurements
The P-I equationof Platt et al. [1980] wasusedto modelthe
Observationswere made during cruiseWEC88 on the R/V Wecoma,February-March1988, extendingfrom 15øN to 15øS along 150øW. This analysisfocuseson the equatorialstation, occupiedfrom March 2 to 7, 1988.
results:
I/Ps)) P•/=Ps (1-e(-o•I /es))(e(-•l
(1)
where pB/(gC (g Chl)-1h'1) is the instantaneous rateof
photosynthesis normalized to Chlat irradiance I (•tmolm'2 s'l, rosettesampler.Siliconerubbertubingwas usedfor o-ringsand PAR); Ps (g C (g Chl)'1 h'l) is the maximumrate of Seawater was obtained with 5-L Niskin bottles attached to a
for securingthe closures[Chavezand Barber, 1987;Price et al., 1986; Williams and Robertson, 1989]. Sampleswere drawn into clean polycarbonate containers, shielded from direct sunlight. Cleaning procedures are described below. Temperature,conductivity and pressure(depth) (CTD) were measuredwith a Neil Brown Mark III CTD. The sampling rosettewas also equippedwith a fluorometer,but it failed early in
the
cruise.
Solar
irradiance
at
the
sea
surface
(photosyntheticallyavailable radiation (PAR), 400-700 nm,
photosynthesisin the absence of photoinhibition; oc(g C
(g Chl)'1 h'1 (•tmolm'2 s'1)-l) is theinitialslopeof theP-I curve, and• (gC (gChl)'1h'1 ([lmolm'2s'l)'1)isaparameter to characterizephotoinhibition. Parameterswere fit simultaneouslyusing the multivariate secant method [Ralston and Jennrich, 1978] of the NLIN
procedure of SAS[SASInstitute,1985].An intercept, Po,(g C (g Chl)'1 h'l) wasincluded as a parameter andsubsequently
subtracted fromestimates ofpB/asonewoulddowitha dark
I.tmolm'2 s'l) wasrecorded continuously with a Biosphericalbottle value. The parameter Po is not a reliable measureof respiration because of limitations of tracer methodology [Jassbyand Platt, 1976; Peterson, 1980]. Rather, the inclusion Optical data were collected with a Bio-Optical Profiling of Po increasesthe amount of variability explained and Po from System(BOPS), an updatedversionof the packagedeveloped improvesthe distributionof residuals.By subtracting Instruments QSR-240 hemispherical quantum irradiance reference
sensor.
by R. C. Smith et al. [1984]. Central to the system is a BiosphericalInstrumentsMER-1048 spectroradiometer which measures upwelling and downwelling spectral irradiance, upwelling spectral radiance, and quantum scalar irradiance (PAR). The MER-1048 also has sensorsfor pressure(depth), tilt and roll. The BOPS measuresconductivityand temperature (Sea-Bird CTD), chlorophyll fluorescence (Sea Tech fluorometer) and beam attenuation (Sea Tech 25-cm transmissometer,660 nm). Deck sensorsrecord downwelling spectralirradiancein four channels.Data are acquiredat 16 Hz, averagedto 4 Hz, then sentto a Compaq-286computer,where they are storedon a hard disk. Data from the BOPS were filtered
estimates of pB/ratherthan includingit, the modeled photosynthesisin the dark is always zero. The realized
maximum rateof photosynthesis, Pmax (g C (g Chl)'1 h'l), was calculated according to Platt et al. [1980] and its error was determined according to the principles described by Zimmerman et al. [1987]. For many of the P-I experiments,one or more of the 24
valuesfor carbonassimilation deviatedquitesubstantially from a continuousfunction of irradiance.These were high values, possiblydue to large, rare cells or to aggregates of cells,but
conceivably theresultof inadequate purging of inorganic 14C. The pointswere excludedfrom the analysisat an earlystagein
CULLENETAL.:PHYTOP•TON
IN THE EQUATORIAL PACIFIC
641
ß
data reduction,when sampleswere identified only by sequence average, 1-100 m, 1-m intervals). Irradiance as a function of numbers. Decisions to omit points were therefore not depthan.dtime(I(z,t)) is theproduct of Io(t) andI(z)/lo. Photosynthesis normalized to chlorophyll. The influencedby expectedresultsfor any particularsample. Concentrations of chlorophyll a (Chl), corrected for photosynthetic parametersa, Ps, and•5were averaged overthe pheopigment, were determinedfluorometricallyusinga Turner 6 daysfor each of the four depthsand threetime periods.From Designs 10-005R fluorometer fitted with a Corning 5-60 theseparameters andthe appropriate irradiance, PB(z,t)was excitation filter and a 2-64 emission filter and calibrated with calculated(1) for each of 12 primary coordinatesin depth and PB(z,t)at the other(secondary) depth-time purified Chl. Sampleswere collectedin triplicateon Whatman time.To estimate GF/F filters and extracted in 10 mL of 90% acetone in the dark
coordinates, fourvaluesof P• werecalculated usingP-I
for at least 24 hours at -4øC.
parametersfrom each of closestprimary coordinatesand I(z,t)
Model of Primary Production
weighted linearly as a function of their relative proximity to the secondarycoordinatein depthand time, and averaged. Profiles of photosynthesis.Modeled photosynthesis, P(z,t)
fromthesecondary coordinate. Thefourestimates of pB/were Photosynthesis was modeledas a functionof depthand time for a representativeday at the equatorialstationusingestimates is theproductof PB(z,t) andChl(z). Verticalprofileswere of solar irradiance,light penetration,in situ fluorescence, Chl, constructedfor 30-min intervals and integrated over time to and P-I. Profiles of photosynthesis were constructedwith 1-m obtain a vertical profile of daily photosynthesisat 1-m resolution for 30-min intervals from dawn until dusk. The intervals. To estimate daily photosynthesis in the water approachwas much like severalChl-light models[e.g., Jitts et column,this vertical profile was integratedto 100 m. al., 1976;Harrison et al., 1985] exceptthat the temporaland spatial resolution was substantially enhanced and the P-I ConventionalMeasurementof Primary Production relationshipwas modeledas a functionof depthand time. Primaryproductivitywas measureddirectlyas the uptakeof Eachestimateof photosynthesis requireda valuefor Chl,/, InC-bicarbonate during 24-hoursimulatedin situ (SIS)
and pB/. These values wereobtained asfollows.
incubations[Chavezet al., 1990]. Measurementspresented here were made on samplescollectedbetween0830 and 0930 contemporaneous measurements of Chl was not possible hoursfrom depthscorrespondingto l(z)/Io = 100, 50, 30,15, 5, because the in situ fiuorometer on the CTD rosette failed, so and 1% as estimatedfrom optical profiles.Water was drawn detailedprofiles of Chl were obtainedby calibratingaverage into screw-capped"Vitro" glass 150-ml bottles (Wheaton profilesof fluorescence from the opticalcastswith averagesof Corporation)encasedin nickel screens(PerforatedProducts) Chl from the hydrocasts. Fluorescence from the in situ that act as neutraldensityfilters, reducingthe fight intensityto fiuorometer[Flis] was averagedat 1 m intervalsof depth(z) for the appropriaterelative irradiance.Each bottle was inoculated the 13 daytime optical casts at the equatorial station. The with10I.tCi of NaHlnCO3 andincubated for24 hoursondeck concentration of Chl was averaged at the four hydrocast under natural sunlight in open, seawater-cooledPlexiglas Chlorophyll. A calibration of fluorescenceprofiles with
sampling depths (0, 20, 40, 60 m) for which P-I was incubators. A time-zerosamplewas inoculatedwith radioactive determined.From these averageddata, the fluorescenceyield tracerand filtered immediatelyto determineabioticparticulate [Flis/Chl(z)], was calculatedat the four depths.Fluorescence 14Cincorporation. For determination of particulate carbon yield increasedwith depth. To constructa vertical profile of fixation during the incubations,sampleswere filtered onto chlorophyllwith 1-m resolution,Flis/Chl(z) was estimatedby Whatman GF/F filters, rinsed with 0.01 N HC1, and counted in linear interpolation between depths, maintaining the 60-m 10 mL of Aquasol II. Thetotalinorganic Inc-activity in each value for greater depths.The estimateof chlorophyll,Chl(z) sample was determinedby adding 1.0 mL of water from the was obtainedby dividing Flis(Z)by Flis/Chl(z). bottleto a scintillationvial containing20 mL of AquasolII. A Irradiance. Irradianceat the seasurfacethroughoutthe day samplefor fluorometricdeterminationof Chl [cf. Chavezet al., (Io(t), where the subscriptindicatesirradiancejust above the 1990] was taken from eachdepthin the productivityeastand surface)was obtainedby choosingfrom the 6-day recordof on- from the otherhydrocasts(F. ChavezandR. Barber). deck PAR the 75th percentlievalue for each 10-min interval. Thesepointsrepresentedirradianceunderclear skies.A four- ProductivityFrom Changesin BeamAttenuation parametermodel was chosento describeirradianceat depth Morning (about 0830 hours) and afternoon (about 1330 (l(z)): hours)profilesof beam attenuationwere comparedto examine diel changes of attenuation at 660 nm and their relation to primary productivity.The analysiswas very similar to that The parameterT (dimensionless) accountsfor reflectionat the presentedby Siegel et al. [1989]. Attenuationis presentedas
Io=T[(R e(-k• z))+((1-R) e(-k2 z))]
(2)
andcw, the surface.The attenuationof irradiancewith depthfollows the beamc- cw, wherec (m'l) is totalattenuation dueto water,is takenas0.364m'l, asspecified by modelof Simpsonand Dickey [1981], accountingfor the rapid attenuation attenuationof longer wavelengthsnear the surface.The two the manufacturer. The carbon-specific beam attenuation
(c•) to convertvariations of c to variations of attenuationcoefficientsare k• andk2 (m'l) andR is a coefficient
dimensionless parameterwhich determineswhat proportionof particulateorganiccarbon(POC) was takenfrom Siegelet al. the irradianceis attenuatedrapidly. Only PAR is considered [1989]:3.92x 10'3 m2 mgC'! (255(mgC m'3)m).Thevalidity here.Valuesfor l(z)/l o were averagesfor daytimeprofiles:l(z) of this assumptionwill be discussedbelow. camefrom the PAR sensoron theprofiler andIo wascalculated ExperimentalManipulations from the on-deckspectralirradiancedatarecordedby the BOPS. For experimentson photoadaptationand the influence of Valuesfor T, R, kl andk2 were obtainedby a nonlinearcurve-fit of equation (2) to a profile of l(z)/Io versus depth (6-day trace metals on phytoplankton,a combinedsample of water
642
CULLENET AL.:PHYTO•TON
IN •
EQUATORIAL PACIFIC
Similar, but less comprehensive experiments were performed at stations between 6øN and 2øS. Treatments dispensedinto 265-ml polycarbonate bottlesand placedin included:"NI-I4" (0.8 IxM NH4CI in one experiment;5 IxM in PlexiglasSIS incubators cooledby surfacewater[Eppleyand another);"NH4 + EDTA" (0.8 IxM NH4CI + 0.4 gM Na2EDTA); bottles,which were Holm-Hansen,1986].Light wasattenuated by perforated nickel and one experimentin 2-L polycarbonate screen. The bottles were incubated on deck at 11% relative held in an on-deckincubatorand subsampledduring the timeirradianceandone from eachtreatmentwasanalyzedfor Chl and course. P-I on subsequent days at 1400 h. Irradiancein the incubator 3. RESULTS was measuredwith a BiosphericalInstrumentsQSL-100 4n sensoron a sunnyday while the coolingwater was running. Percenttransmittance is reportedrelativeto irradiancereCOrded Vertical Structure by the deck sensor. Hydrography,the distributionsof nutrients,and vertical Collectingbottlesandthe incubations bottleswereinitially elsewhere in thisvolume[Carr et al., this prepared by rinsingwithdeionized water,soaking in 2% Micro mixingarediscussed detergentfor at least2 days,thoroughrinsingwith Nanopure issue].We presenthere somevertical profilesthat describe (reagent-grade) water,a soakingof at least2 daysin 2% HCI, meanconditionsover six days at the equatorand someof the andthoroughrinsingwith Nanopurewater.At sea,the bottles changesthat occurredbetweenthe morningand afternoon wererinsedwith Milli-Q (reagent-grade) waterbetweenusesand opticalprofilesand bottle casts(Figure 1). Profiles of temperature (Figures la and lb) reflect well rinsedwith samplewaterprior to filling. The concentrationsand availability of trace elementswere stratificationin the upper 100 m, which was disruptedto at by solar manipulatedexperimentally.The three treatmentsand final least 20 m by nocturnalmixing and reestablished concentrationswere: EDTA (Na2EDTA, 400 nM), copper heatingduringthe day [Carr et al.• thisissue].In situ (CuNO3, 5 nm) andiron (Fe(NO3)3,10 nM). Stocksolutions fluorescence shows a broad subsurface maximum centered at were kindly provided by John Martin. Controls were not about50 m (Figureslc andld), wherel(z) wasabout2.5%I o.Of modified, but we recognize that some trace-element the profiles consideredhere, beam attenuationdisplaysthe diurnalvariation(Figuresl e andIf), with contaminationis likely to have occurred.Thus, toxic trace mostpronounced in the afternoon, especiallyat depthsof 20elementssuchas copperandzinc mighthaveinfluenced results greaterattenuation [Fitzwateret al., 1982], andiron, a tracenutrient,wouldlikely 40 m, where the relative increase over 5 hours was as much as have been enriched even in the controls.These possibilities 53%. The concentrationof Chl alsoincreasedduringthe day in muchof the euphoticzone, an averageof 17% betwee. n the are consideredin our analysis. from 30 and 40 m (about 5% - 15% Io) was collectedat the equatorial station at midday on March 2. Sampleswere
Temperature(øC) 16
18
20
22
24
26
0
28 ß
;; ;;
2O
0
5
10
15
0
20
Chlorophyll a (mgm'•)
Beamc-Cw (rrr9
Fluorescence[relative) 0
25
0.02 0.04 0.06 0.08 0.1
0
ß
00;00.10.20.30.40.50.6
,
2O
20
20
•,
4O
4O
40
40.
•'
60
6O
60
60
8O
8O
80
100
100
0
16 18 20 22 24 26 28 ....
,
....
0
c
,:' 0
5
10
15
20 ß
25 ,
0
40
60
80
100 ,'
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;:
20
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E
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......
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-
0.2
0.3
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•; ", ':- :,t. 20
20
40
40
• ,. o
20 40
60 . ,';;60 60
80
100
80
D
100
80
F
i 00
Fig. 1. Mean vertical profiles (+ s.d.) from the equatorialstationat 150øW, March 2-7, 1988. Data from the
biooptical profilingsystem:(a) temperature (morning profiles,0830hours);(b) temperature (afternoon profiles,1330 hours);(c) in situ fluorescence(morningprofiles);(d)in situfluorescence(afternoonprofiles); (e) beam attenuation (c- cw, morningprofiles);(f)beam attenuation (c- cw, afternoonprofiles).Data from bottle casts:(g) Chl (morning profiles,0600 hours);(h) Cid (afternoonprofiles,1200hours).
0.5
0.6 ß
•
CULLEN ETAL.:PHYTO•TON
IN THEEQUATORIAL PACIFIC
643
depths of 30 and80m (Figures lg andlb). However, nearthe photosynthetic performance well. Three patternsare surfacethe afternoon meanwas slightlylowerthanthe particularly clear(Figure 3).
morning mean.
1. Diurnal variation of maximum photosynthesis, Pmax [Harding et al., 1982a],is clearlyevident at eachdepth,with
Photosynthesis Versus Irradiance
thehighest rates near midday.
Measurements of P-I at theequatorial station (Figure2)
2. Verticalpatterns of a•andPmaxarecharacteristic of
show strong patterns withdepth andtimeofday.Good fitsto photoadaptation: Pmaxdecreases withdepth(irradiance) theP-I model(equation (1)) wereobtained so thatthe [Falkowski, 1980,1983;CullenandLewis,1988]anda is photosynthetic parameters Pmax,a•, andfl describelowernearthesurface, where irradiance is high[Cullen and
0630 h
1200 h
•: -' 4s
0m
. 20 m
•
2 0'
•
5
•.•
•
4 51
0
500
'
•
.•
2 500
3
•
2
500
1000 1500 2000 2500
0
•
•
•
'
1000 1500 2000 2500
......
2 .,,.., .-•.. O' 0
500
1000 1500 2000 2500
500
1000 1500 2000 2500
0
500
•000 •500 2000 2500
0
500
•000 •500 2000 2500
5
3
'
2
500
1000 1500 2000 2500
5
0
-'
5
•
5
5
5
4
4
4
•c:4
•
5
4
0
60 m
•
0
5
0
40 m
4 • '.--n-••'•'•---• 5
2 0
1000 1500 2000 2500
1800 h
500
' 0
500
•000 •500 2000 2500
0
• •000 •500 2000 2500
4 500
•000 •500 2000 2500
0
0 0
500
•000 •500 2000 2500
Fig. 2. Measurements of photos•thesis versusi•adianceat the equator, 150øW,March4, 1988.Linesarebestfits to equation(1).
700
7
A
0.75
• --a,-, ---I•--t-'
600
500
Om 20m 40 m 60m
(_.+ s.c.)
rO.50
400
•300 0
0.25
200
100
0
.
i . i . i . 0600 1200 1800
Time
ß
,
.
i
.
,
0600 1200 1800
0
.
i
.
,
i
i
,
0600 1200 1800
0.00
.
i
.
,
.
Fig.3. Photosynthetic parameters andChl at theequatorial station, March2-7, 1988.Averaj•es andstandard errorsat eachof
--2 1 1 fourdepths, three times perday: (a)Pmax (gCgChl '1h'l);(b)a (gCgChl '1h'1)(gmol rn' s')' );(c)Ik(grnol m'2 s'l);
d)Chl(mgm'3).
ß
.
0600 1200 1800
644
CULLEN ETAL.:PHYTO•TON
Lewis, 1988]. Also consistent with photoadaptationto ambient irradiance, the saturation parameterlt• (Pmax/O• [Tailing, 1957;Platt et al., 1980]) decreases with depth. 3. Nocturnal mixing [Carr et al., this issue] homogenized the phytoplanktonassemblage in the upper20 m, eliminating to a great extent the differentiation of chlorophyll concentration and photosyntheticparametersthat occurred between0 and 20 m duringthe day (Figure3; seealsoVincent et al. [1984]). Diurnal stratification [Vincent et al., 1984] led to a responsecharacteristicof photoinhibitionnear the sea surface [Vincent et al., 1984; Neale and Richerson, 1987;
Cullen and Lewis, 1988]: comparedto the assemblage at 20 m, phytoplanktonat the surfaceat midday had lower Prnaxand o•, and showedlessnet synthesisof Chl.
IN TH• EQUATORIAL PACIFIC
of productivity[seeRyther and Yentsch,1957;Cullen, 1990],
with aboutthe sameinitial slope,but the maximumaverage
dailyrate(3.3g C g Chl'1 h'l) is lowerthanin othergeneral modelsof p/t versusI.
Conventional Measurement of PrimaryProductivity The 24-hourSIS incubations yieldedestimates of primary productivitythat were higherthanthosefrom the productivity model(Figure5a). Daily productivityfrom the morningcasts,
Carbon Uptake (mg C m- 3 d- 1) 0
5
10
15
20
0
Model of Productivity
The modelof productivity yieldsa verticalprofilewith 1 m resolution(Figure4a). Integralprimaryproductivitywas469
mgC m'2 d'1. Maximum productivity wasat 10-15m and photoinhibition of photosynthesis nearthe surfacehadonly a minor effect on integrated water column production.A compositeP-I curve for the water columnis obtainedby
plotting thedailymeanvalues of PB(z)against average l(z)
2O
• 4O
(Figure4b). Thecurveis similarto a simpleexponential model
PrimaryProductivity (rngCm-3d'1) 0
2
4
6
8
C3 60 10
A
I
8O 2O
•
4O
- Productivity
100
6O
Assimilation Index (g C g Chl-• d'•) 8O
0
A Chlorophyll
100 0.0
0.1
I
I
I
I
0.2
0.3
0.4
0.5
Chlorophyll a(rng rn-3)
20
40
60
80
i
i
i
I
!
20
I
I
5
•
rO
•360
2
• •'
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0
. I 0
500
1000
I 1500
I 2000
Irradiance (•molm-2s-•)
80 I
2500
100
•i8. 4. Resultsof the m•e] of •uctivi• at the e•uatod• station, Fig. 5. Resultsof SIS incubations to determine primaryproductivity at ]50øW, 2-? •amh, ]•88: (a) daily pdma• p•od•ctjvi• •d • venus the equatorial station.Mean+ s.d.for 6 days,morningstations only. (a)2 Daily productivity. Integralproductivity to 100 m was710 mg C depth; •) p•oductivi• no•alized tobiomass 1 1 1 ove• •e day) as a f•ctio• of averoSekmdianceove•the da•. m' d' . (b) Assimilation index(g C g Chl- d- ).
CUI.I.F.N ETAL.:PttYFOPLANKTON IN THEEQUATORIAL PACIFIC integratedto an assumedzero point at 100 m, was 710 mg C
645
ExperimentalManipulations
m'2 d'l, higherthanall otherstations alongthetransect from et al., 1990]. Inhibition at the surface was observed, and
Measurements of P-I on freshsamples areinformative, but more can be learned by measuringchangesin the P-I relationship andthe increaseof Chl duringexperimental SIS
maximum ratesaveraging 16mgC m'3 d'l weremeasured at 10-
incubations. Accordingly, we incubated samples for 1-4daysto
15øN to 15øS on 150øW
and consistent
with
several other
estimatesof equatorialproductivity[Chavezet al., 1990;Petra
25 m.
examine the extent of photoadaptationin situ and the possibilitythat the specific growth rates of the dominant phytoplankton wereregulated by tracemetalssuchas chlorophyll (assimilation index,g C g Chl'l d'l; Figure5b) equatorial was59 g C g Chl'1 d'1 in theproductivity maximum. Assuming copperandiron.Theprincipalexperiment wasperformed at the The mean rate of photosynthesisnormalized to initial
a C:Chl ratio of 58 by weight [Eppley et al., this issue],this assimilationindex correspondsto a phytoplanktongrowth rate
equatorial stationon March2 to 6, usinga combined sample from30 and40 m (seemethods section).
of 0.7 d'l (1 doubling d'l). Photoinhibition of photosynthesis Possibleartifacts.The resultsfrom suchincubationsshould was evidentnear the surface,as was light-dependence at depth. be evaluated with care,so we designed the experiments to Integratedproductionnormalizedto biomass([PflB: 0-100 m)
assess possible biases associated with SIS incubations.
was31.2g C g Chl'1 d'1. Somegeneral models of productivity Specifically, if contamination with toxic divalent cations predict that [PflB is a positive function of surfaceirradiance duringsampling and containment weresevereenoughto [e.g., Falkowski, 1983; Platt et al., 1988; Cullen, 1990]. inhibitphotosynthesis [Carpenter andLively,1980;Fitzwater Considering that daily insolation at the equator was near et al., 1982],thetoxicitycouldbe countered by treatment with maximum for the world oceans, our measuredvalue for [P/IB is thechelator EDTA andgrowthandphotosynthetic rateswould on the low end of what wouldbe expected. behigherin EDTA-treated samples thanin controls [Sharpet al., 1980; Cullen et al., 1986]. Instead,we found that Chl
ProductivityFrom Changesin BeamAttenuation
increased in controls (Figure7), P-I didnotchange fromtime
A vertica•profile of estimatedprimaryproductivitywas zero (Figures 8 and 9), and that there was no consistent of apparent growth ratewithEDTA(Figure 7b), constructed from daily measurements of the changeof beam enhancement attenuation [Siegel et al., 1989] over the 5-hour interval between morning and afternoonoptical casts(Figure 6). For lack of a robust method of describingoptical changesnear dawn and dusk and duringthe late afternoon,hourlyrateswere multiplied by 10 to obtain rough estimates of daily productivity.The calculatedrate was depressed nearthe surface
norwasthereaneffectonPmax (Figure9). Therewasonlythe suggestion of consistent effectson theinitialslopeof theP-I
curve, a (Figure 9).
Depletion of nitratewouldconfound results by curtailing growththat wouldotherwisehavebeenstimulated by an experimentaltreatment.We saw no evidenceof this curtailment
reportedhere.Also, severalmeasurements andwasmaximal at about15mgC m'3 d'l between 25 and30 in the experiments of nitrate, plus mass-balancecalculationsshow that nitrate
m. Estimatedproductivitydeclinedwith depth to 0 at the 1% light level, 65 - 70 m. Daily productivityintegratedto 100 m
depletion wouldnothaveseriously influenced theaccumulation
be interpretedcautiously.
assemblage, transported by upwelling,had not yet fully adapted to theirradiance regimeat thedepthof sampling,
was702mgC m'2 d'l, quitesimilarto theestimate fromSIS of chlorophyll. Theextentofphotoadaptation in situ.If thephytoplankton incubations.Later, we will discusswhy theseestimatesshould characteristic photosynthetic responses to increased irradiance wouldbe observedduringthe SIS incubations over hoursto
Productivity (mgCm-3d-l) -10
10 20 30
-5
0
5
10
15
20
days[cf.CullenandLewis,1988]:photosynthetic capacity (Prnax)andIt• would increaseand susceptibilityto photoinhibition (•) woulddecrease. Instead,duringSIS incubation of 2 days,P-I for the controlsamplewas indistinguishable fromtime-zero (Figures8 a and8b), even thoughtheconcentration of Chl increased by a factorof 2.9 (Figure 7), aswouldbeexpected if thedominant phytoplankton in situwerefully adaptedto the photicenvironment at the
E 40
depthof sampling.
•:
50
The constancyof the P-I relationshipover incubations of up to 2 daysis stronglyconsistentwith balancedgrowth,whereby
r•
60
all cellular constituents increase at the same rates over 24 hours
[Eppley, 1981]. Accordingly,this is one of a restrictedset of situations in which changes of Chl can be interpreted as changesin phytoplanktonbiomass[cf. Eppley, 1968; Cullen,
70 80
1982].
Regulationof photosynthesis by copper. Manipulationsof
90
trace 100
-
elements
were
used to assess the influence
of trace
elementson photosynthesis in situ. Considerthe regulationof Fig. 6. Primaryproductivity at the equatorial station(mean_+s.d.), equatorial primary productivity by copper toxicity: if the estimated fromtheaverage hourlychange in beamattenuation between chelationcapacityof the waterweresolow thatfreecopperwas morning (about 0830hours) andafternoon (about 1330hours) optical toxic to phytoplankton in situ [cf. Huntsman and Sunda, casts over 6 days at the equatorialstation.The conversion from attenuation to POCwastakenfromSiegeletal. [1989]:3.92x 10'3 m2 1980], an experimental addition of Cu would further inhibit mgC'1. growth(increaseof Chl) or photosynthetic capacityrelative to
646
CLfiJ.F.NETAL.:PHYTO•TON
IN THE EQUATORIAL PACtFIC
a control, and a sample treated with the chelatorEDTA would show better growth and photosynthesis than a control. Conversely,if naturalchelationwere morethanenoughto bind free copperin situ, an additionof Cu sufficientto limit growth only in unchelatedwater would alter neitherthe rate of increase of Chl nor photosynthetic performancerelative to an untreated
9). Also, treatmentwith EDTA did not influenceresults(Figures 7 and 9). Regulation of photosynthesisby iron. Our sampleswere probably contaminatedwith iron, so all of our incubated samples,including controls, should be consideredenriched with iron. We thereforecannotdetermineif the availability of sample. To testthis,we useda treatment withCu at 5 x 10'9M. iron in situ limits the terminal yield of equatorial Calculations showthat 93% of thatcopperwouldbe complexed phytoplankton[cf. Martin et al., 1989], but we can assessthe by inorganic ions [Morel, 1983], so the activity of added degree to which enrichmentwith iron influencesthe specific copper, in the absenceof chelation from organics,would be growth rates and photosynthetic characteristics of the 3.5 x 10'1øM. Thisactivityof Cu++inhibitsgrowthof many dominantphytoplankton.Copperand EDTA had no significant clonesof phytoplankton[Gavis et al., 1981] and would likely influence on our measurementsduring the incubations,so we have influenced equatorial phytoplankton if their rate of can includethem in this analysis. photosynthesis had been regulatedby the activityof Cu++ at Measurableresponses to iron enrichmentseemto requireat the time of sampling.Apparently,it was not: copperhad little least one and usuallyseveraldays [Martin et al., 1989], so if effect on the increaseof Chl (Figure7) or on P-I (Figures8c and iron regulatedthe specific growth rates of phytoplanktonin situ, we would expectinitial ratesto reflect thosein natureand the rates after several days to reflect any stimulation 1.5 attributable to iron. In other words, we can discount the influence of iron contamination over the first 24 hours, and ß
A
compare early changesin growth and P-I to those observed over days 2-4. The concentration of Chl increased over 48 hours in each of
[3 Control
the four treatmentson the sample from the equatorialstation (Figure 7a), averagingan increaseof 83% betweentime zero and day 1, 96% betweendays 1 and 2 (exponentialrates of
171Copper • •
EDTA Iron
increase are0.60d'1and0.67d'l, respectively). Thedifferences between treatments were not large and not the same on consecutive days. The average change of Chl during this experimentwas consistentwith other experimentsin equatorial waters: for all available data from incubations,the increaseof
E 0.5 o
chlorophyllwas roughlyexponential over the first two days, o
witha specific rateof increase of 0.59d'1 (Figure7b).Between days 2 and 4, when effects of iron enrichmentmight be expected, thespecific rateof increase was0.89d'l. Forall data combined, there were no consistent effects of treatments on the 0.0
increaseof chlorophyllduringSIS incubations. Time 0
Day 1
Day 2
The apparent acceleration of growthrateover4 days(Figure 7b) couldhavebeendueto a numberof factors, butit maywell
lOO
B
lO
o
EDTA
x
Cu
[]
Fe
•
NH4+EDTA
x
NH4
ß
Control
Day 1-2 fit
Day 2-4 fit 0.1
0
I
I
I
I
I
1
2
3
4
5
Time (days) Fig.7. Changes of Chlconcentration during SiSincubations withmanipulations of traceelements. (a) Equatorial station, 11%Io, March2-4, 1988,treatments described in text.Errorbarsarestandard errors of triplicates fromonebottle.(b)
Results fromall SISincubations between 2øSand6øN,>10%Io; treatments described in section 2. Results normalized to Chl concentration at time zero.Therewereno consistent differences betweentreatments, so all werecombined to calculate
specific ratesof increase. Thelinesarebestfits for days1-2 (regression forcedthrough 0, on_log-transformed data:
slope=0.59 d'l, n=21, r2=0.82) and days 2-4(regression onlog-transformed data, slope=0.89, n=21, rZ=0.92).
C•N
ETAL.:PHYTOPLANKTON IN THE EQUATORIAL PACIFIC
o
A
o
7
.
o$
o
.o.oo.o•
647
ß
ß
O• 0 0ß
o
O
$ .
o
C
00 0
o
ß •
o
i
!
i
500
1000
1500
i
i
2000
o
o
2500
B
i
i
i
500
1000
1500
i
i
2000
o
2500
D o
$
o
o
$
o
500
1000
i
i
1500
2000
2500
0
500
Irradiance (#tool rn'2s'l)
1000
1500
2000
2500
Irradiance (#tool rn'2s'•)
Fig.8. Effects of experimental treatments during SISincubations at 11%I oovertwodays.Measurements of photosynthesis
(gCgChl '1h'l) versus irradiance (pmol m'2s'l) during anexperiment attheequatorial station, March 2-4,1988. Ineach
plot,results fromanexperimental treatment (solidcircles) areplotted withthetime-zero (TOßopencircles) measurements. Thecurveisthebestfit toequation (1) forTOP-I:(a) control sample after24h; (b)control sample after48h; (c)Cu-treated sampleafter48 h; (d) Fe-treated sampleafter48 h.
havereflectedenhanced growthof largecellsstimulated by iron of the low-latitude Pacific Ocean [Barber and Kogelschatz, or released from grazing pressure[Banse, 1991]. Species 1988]. In the central equatorial Pacific, proximate effects of compositionwas not determined,but visual inspectionof the ENSO include warmer surface temperatures, a deeper bottles showed that after incubations of 4 days, many thermocline and lower near-surface nutrient concentrations as aggregateshad formed. compared to the climatological mean. These changes in thermal structure and nutrient concentrations must influence the
4. D•SCUSSION
Influenceof PhysicalForcingon Photosynthetic Performance In equatorial upwelling systems, physical forcing influencesprimary productivityon a number of spatial and temporal scales. Wind-induced turbulent mixing, when suppressedduring the day by solar heating [Mourn and Caldwell, 1985;Carr et al., thisissue],canproducea diel cycle of mixing and stratification that disrupts the adaptationof phytoplankton to their photic regime [cf. Vincent et al., 1984]. Upwelling at the equatorial divergencecan replace surfacewaterson the time scaleof severaldays:if growthand adaptationof phytoplanktonkeep pace, the upwelling will enhance local productivity, but if vertical advection moves phytoplanktonthroughthe light gradientfaster than they can adaptandgrow, primaryproductivityandenrichmentof higher trophiclevels will be displacedlaterally [Walsh, 1976;Minas et al., 1986; Dugdale and Wilkerson, 1989]. The E1 Nifio SouthernOscillation (ENSO) cycle, an aperiodicperturbation of the ocean/atmosphere system,strongly modifies the heat contentand productivityof the Pacific Basin on an annualtime scale,actingas a major determinantof the ecologicalcharacter
effects of vertical mixing and upwelling on phytoplanktonso that physical forcing mechanismsinteract on several scales. Here, we examined responsesof phytoplanktonto physical forcing on time scalesfrom hoursto days. The
effects
of
diel
variation
in irradiance
and vertical
mixing were measured directly: photosyntheticparameters varied with time of day and showedverticalpatternsreflecting nocturnal mixing, diurnal stratification, and near-surface photoinhibition. Photoinhibition was observed in conventional incubations, but such static incubations over 24 hours
at surface
irradiance
are unnatural
because
vertical
movementsare not simulated[Marra, 1978;Gallegosand Platt, 1985]. Short-term measurementsof P-I showed depressed photosyntheticcapacity at the surface,a direct manifestation of photoinhibitionin situ; independentof incubationartifacts. The diurnal increase of beam attenuationwas also depressed near the surface. It seems clear, therefore, that nocturnal
mixing and diurnal stratificationpromotedphotoinhibition in the equatorialPacific, much as it doesin the tropicalalpine Lake Titicaca [Vincent et al., 1984; Neale and Richerson, 1987]. Nocturnal mixing at the equatorial station was relatively weak during March 1988 [Carr et al., this issue],so
648
C•N
ETAL.:PHYTOPLANKTON IN THEEQUATORIAL PACI•C
0.06
SIS incubations. We
A
I-! Control
I'1 Copper •
EDTA
.:• ß Iron
conclude that with respect to
photosyntheticcharacteristics,the dominantphytoplankton assemblageat 30-40 m on the equatorwas well adaptedto ambientirradiance.Neither upwellingnor vertical mixing was sufficientlyintenseto overwhelmphotoadaptation [of. Lewis et al., 1984]. This conclusionis consistentwith estimatesof
0.04
mixingand upwellingthat indicatea minimumresidence time of 20 daysfor passiveparticlesin the upper30 m at theequator (M.E. Cam personalcommunication, 1991). This studywas concernedprimarily with photosynthesis. Dugdaleet al. [this issue],studyingthe uptakeof nitrateand ammonium, concluded that the equatorial phytoplankton assemblagewas not well adapted to ambient conditions,
0.02
particularlythe nutritionalenvironment.In their words,the assemblagewas not "shifted-up."Could the assemblage be "photoadapted" but not shifted-up?The questioncan not be answered at this time because too, litfie is known about the
0.00
Time 0
Day 1
Day2
relationshipsbetween carbon and nitrogen assimilationin thesephytoplankton:uptakeof nitrogencan be substantially uncoupledfrom photosynthesis [Morris, 1981;Cullen, 1985], and it is possible that the equatorial phytoplankton
assemblage is physiologically distinctfrom the cultured lO
B
phytoplanktonon which our understanding of phytoplankton physiologyis based.More studyis clearlywarranted. The Model of Primary Productivity
Our methodof modelingproductivityfromP-I, fluorescence, Chl and irradianceis basedon establishedprinciplesrecenfiy
•T
appliedandevaluatedby Harrisonet al. [1985].Here, we use more information to improve the vertical and temporal resolution
of
the
estimates:
instead
of
describing
photosynthesis in the watercolumnwith oneP-I relationship, we use 12 (four depths,threetimesper day) to encompass diel variability [Harding et al., 1982b] and photoadaptive differentiationof P-I with depth [Falkowski, 1983;Lewis et
x
al., 1984 and references therein]; measurementsof Chl at four
depthsare usedto modelfluorescence yield as a functionof depth[cf. Cullen, 1982]; a profile of fluorescence is usedto estimateChl at 1-m intervals; and productivityis estimated from irradianceprofilesat 30-min intervals.The result is a
iiii
Time 0
Day 1
Day 2
Fig. 9. Photosyntheticparameters(best fit to equation (1) +s.e.) during an experimentat the equatorial station, March 2-4, 1988.
Treatments described inthetext:(a)(z(gCgCid'1h'1)(limo1 m'2s'1) ' 1);(b)Pmax (gCgCh1-1 h-l).
photoinhibitionat the surfacemight be more severeat other times of year. Responsesof phytoplanktonto physical forcing on the time scaleof dayscan be inferredfrom directmeasurements and experimentalresults.Vertical differentiationof photosynthetic characteristics (Figure 3), a processthat requireshoursto days [Cullen and Lewis, 1988], demonstratesthat throughmuch of the euphotic zone, the photosynthetic systems of phytoplanktonhad time to adapt at least partially to ambient irradiance.Measurementsof P-I on freshsamplesdid not reveal the extent to which phytoplanktonhad adapted,however.We determined the degree of adaptation by incubating samples under SIS conditionsto see if the phytoplanktonwould adapt further. For the assemblagesampledat the equator,there was little or no indication of photoadaptivechangesof P-I during
detaileddepictionof primaryproductivityat the equatorial
station, wRh•superb vertical andtemporal resolution. Butis the model accurate?
Modeleddaily productivityin the watercolumnis 34% lower thanthat measured by conventional SIS methods(Figure 5). At 10 - 20 m, modeledratesof daily productivity areonly about 50% the rates measuredby SIS incubations.Several factorscould contributeto this discrepancy.
Unnatural accumulation of chlorophyll. The concentration of Chl changedlittle fromdayto dayin thewater column,but during24-hourSIS incubations, Chl increased by as muchas 80% (samplesfrom > 10% Io; Figure 7). This accumulation was an artifact of containment,so the SIS method
overestimated productivity to the extentthatChl in thebotfies exceeded natural levels [Eppley, 1968]. If the unnatural increase of Chl in bottles were linear, an artifactual 80% increase over 24 hours would lead to a 40% overestimate of
primary productivityfor SIS incubations.If we assume constantphotosynthetic rate in daylight and an artifactual
exponential increase in Chl of 0.6 d'1 duringa 24-hour incubationbeginningat 1000 hours,the estimateof bias is 31%. This estimatemaybe valid for 10 - 30 m, but it overstates
CUIJ.F.NETAL.:PHYTOPLANKTON IN •
the bias for other depths:increasesof Chl during incubation were small or nonexistentat surfaceirradiance(data not shown) and below about30 In, changesdeclinedwith depthdue to light limitation (results from one experimentnot shown). Changes of Chl were measuredin polycarbonatebottles:increasesmay
havebeenlessduringthe14Cincubations in glassbottles(F. Chavez, personalcommunication,1990). The unnaturalaccumulationof chlorophyllwas presumably due to disruptionof grazing. Sinking is anotherpotentialloss that is eliminated in bottles,but it was not importanthere: the dominantphytoplankton[Chavez, 1989;Pe•qaet al., 1990] are smalland incapableof rapid sinking;andduringthe nightthere was no downward displacementof the beam c maximum, as wouldbe expectedhad sinkingof particlesbeenimportant. Diel variability of P-I. Our data (Figures 3a and 3b)
specifytlie minimum amplitudeof diel variability in o• and Pmax'Maximum chlorophyll-specific rates may have occurred beforeor after midday [MacCaull and Platt, 1977; Harding et al., 1982a]. If these peaks had been measured,the model estimatesof productivity would have been higher. Even if maximumrateshad occurredat midday,the linear functionused to describe diurnal changes of P-I might have led to underestimationof productivity. In nature, Pmax can be near
EQUATORIAL PACIFIC
649
Toxicity associated with P-I incubation technique. Perhaps the simplest explanation for lower rates in the P-I model would be trace element toxicity associated with incubatingsmall samplesin borosilicateglasscontainers(see P-I methods)that are known to harbor contaminants[Fitzwater et al., 1982]. The questionhere is whetherrate measurements were affectedduring short(1 hour) incubations.If toxicity had been important, measurementsof photosynthesiswould not only have been low, but also variable [Fitzwater et al., 1982] and sensitiveto treatmentwith the chelatorEDTA [Sharpet al., 1980; Cullen et al., 1986]. Results presentedhere show no indicationof trace metal toxicity: mostof the data fit modeled P-I curvesquite well (Figure 1), and outlierswere high, not low as expected from toxicity. Further, in a test for short-term effects of trace elements,rates measuredon a sample treated with EDTA were very similar to those measuredon a control (Figure 10). We conclude that the time scale of our P-I measurementswas too short for toxicity to have had a significant effect. 4
maximal for several hours [MacCaull and Platt, 1977]. We
Conclude thatthemodeled values of PB(z,t)areunderestimates of true rates becausediel variability is inadequatelydescribed. Data are not sufficient to quantify the error: it might be 10 20%, in the light-saturatedupper30 m. Irradiance spectrain the incubators. The light sourcein the P-I incubator,qualitativelysimilar to that usedby Harrison et al. [1985], has relatively less blue light and more red light than does the attenuatedsolar spectrumin the SIS incubator, and both incubatorshave relatively lessblue light than what is presentin situ [Herman and Platt, 1986]. Becausethe action spectrum of photosynthesishas a major peak in the blue region, red light is inefficiently utilized and the P-I incubator should yield underestimates of photosynthesis at lightlimiting irradiancewhen comparedto the sameirradiancein a SIS incubator. Both incubation methods should yield
0
500
1000
1500
2000
2500
Irradiance (#mol m'2s'•) Fig. 10. Assessmentof the effects of trace-metal contaminationon
measurement of P-I. Samplefrom 18 m at 6øN, 150øW.Controlsample, treatedas described in section2 (opencircles).Solidline is the bestfit to equation(1). Parallelsampletreatedwith 1 IJM Na2EDTA (solid circles).If toxicityfrom copperor zinc had inhibitedphotosynthesis underestimates when comparedto the same subsaturatingin the control,the EDTA treatmentwould showhigherrates[ Cullen et
irradiancein situ [Lewiset al., 1985]. Spectralqualityshould have little influenceon short-termmeasurements of light-
al., 1986].
saturatedrates, but I/, will be affected.Calculationsshow that estimatesof light-limitedphotosynthesis from the P-I model couldbe about60% lower,andSIS resultsmightbe 40% lower than thosefrom in situ incubations[Harrison et al., 1985]. Thus,spectralquality can accountfor the observeddifferenceof
It could nonetheless be argued that substantial and irreversible toxic effects had occurredprior to the first measurements. This dauntingcriticismwasaddressed by Cullen et al. [1986]. Using the criteria describedin that paper, we excludethe possibilityof irreversibleand catastrophic damage about20% betweenthe modelandSIS resultsat depthswhere to phytoplanktonduring sampling.Particularlyrelevant are
SIS photosynthesis was light-limited. The contributionof large, rare cells or aggregateswas excludedfrom the model.Aliquotsfor measurement of P-I were only 1 mL, so large cells or aggregatesof cells presentin
concentrations of lessthanabout10 mL'1 wouldnotbeevenly distributedbetween samples.A large amountof the biomass and production of phytoplankton in the central equatorial Pacific can passa 5 [lm filter [Chavez, 1989; Pe•qaet al., 1990], so we expecteda relatively small contributionby large, rare cells or aggregates.Nonetheless,a few measurements in each set of 24 were substantiallyhigher than the othersand were excludedfrom analysis.If large, rare cells or aggregates had been responsiblefor these high points, our estimatesof P(z,t) would be low. Future studies should assess this potentially seriouscomplication.
our measurementsof high in vivo fluorescencenormalizedto
chlorophyllin dark-adaptedsamples(J. Cullen and C. Davis, unpublished data, 1988), an observation that is inconsistent with toxic contamination. We conclude that both the P-I method and the SIS method
havepotentiallyseriousbiasesthat are largeenoughto account for the discrepanciesbetween methods.These biases should
eliminated or betterquantified in futurestudies. TheP-I method doesnot includethe contributionof large cells or aggregates, so we must assume that those measurementsrepresentthe dominant, small phytoplankton. BeamAttenuationand Phytoplankton Primary productivity.Siegelet al. [1989] hypothesizedthat diel changes of attenuation were due to photosynthetic
650
CULLENETAL.:PHYTOPLANKTON IN THE EQUATORIAL PACIFIC
production of ultraplankton offset by losses through phytoplanktonat 30 m, calculatedfrom meanbeam c, varied microzooplanktoningestion.It was assumedthat micrograzer between 50 (morning profiles) and 66 (afternoon profiles) abundances were not sampled by the transmissometer. whereas at the chlorophyll maximum (60 m) C:Chl varied Regardlessof the exact nature of growth and loss terms, between 27 and 33 for morning and afternoon profiles, primary productivity could be estimatedfrom the apparent respectively.Thesenumbersagreewith C:Chl ratioscalculated accumulationof particles during the day. The assumptions by œppley et al. [this issue] on the basis of regressions implicit in the calculationof productivityfrom changesin between POC and Chl, are consistent with other estimatesfrom attenuationare •1) the carbon-specificattenuationcoefficient equatorialwaters[œppleyet al., this issue],and havethe same (c•; 3.92x10 '3m2 mgC'l) isaccurate, and(2)c• is constantverticalpatternas describedby Pak et al. [ 1988]. œppleyet al., [this issue]estimatedthat only about30% of throughout the day. To validate the method by direct comparisonto conventionalmeasurements, it is also assumed the POC was phytoplankton carbon. If we assume for that the accumulation of small particles sensed by the discussion that phytoplankton contributed only 30% to transmissometer representsprimary productivityas measured attenuation,then calculated C:Chl would be about 10 in the Chl
withthe14Cmethod. Theseassumptions aretenuous atbest,so
maximum and 20 at 30 m. The latter estimatesof C:Chl are low,
the agreementbetweenproductivitycalculatedfrom changesin beamc (Figure6) and SIS estimates(Figure5) is encouraging. Let us examinethe relationshipbetweenthe accumulation of
but it is not possibleto determineon the basis of lab studies [Geider, 1987] that they are unreasonable. We
do
not
know
the
relative
contributions
of
ultraplankton andmeasurements of 14Cuptake. R. E. H. Smith phytoplankton,bacteria, and detritus to beam c, but we can et al. [1984] modeledproductivityand carbonflow usingrates of growth and grazingsimilar to thosepresentedhere. In the model of R. E. H. Smith et al., the only lossesfrom the pools of autotrophsand microheterotrophs were to respiration.Here we recognizethat grazing by larger organismsshouldalso be considered. For simple models of carbon flow through autotrophsand microheterotrophs, lossesfrom thesepools to grazingare equivalentto respiration,so the modelof Smith et al. shouldstill apply. The pertinentobservationis that in a tightly coupled autotroph-microheterotroph system, the
assessabsorptionby photosynthetic pigmentsas a component of measuredattenuation[Pak et al., 1988]. The concentration
of Chl at theequatorial station rarelyexceeded 0.5 mgm'3. A typical Chl-specific absorptioncoefficientfor phytoplankton
at theredpeak(675nm)is about0.02m2 (mgChl)'1 [Iturriaga and
Siegel,
1989]. We assume that for the beam
transmissometer (peakwavelength in air660nm),0.0I m2 (mg Chl)'1 is an appropriatespecificabsorption coefficient. Therefore,raa•hiiaii• absorptionby phytoplanktonwas about
0.005 m'1. Thisis lessthan10%of beamc- Cwin themixed accumulation of particulate14C is nearlyequivalentto layer,thusattenuationis dominatedby scaRering. " autotrophicgrowth plus the autotrophicproductionassimilated
by heterotrophs. Duringincubations, 14Caccumulates in the
Specific growth rates of phytoplankton.At the equatorial station, attenuation at 28 m increased 53% over 5 hours
microheterotrophic pool so that for the systemsthey modeled, between morning and early afternoon (Figures l e and l f). If the increaseof phytoplanktoncarbonaccountsfor only about exponentialincreaseof particlesis assumed,thesechangesin 50 - 70% of net productionin the light. Thus,net accumulation attenuation can be used to estimate growth rates of of photosynthetic ultraplankton in the light should be an phytoplankton [Siegel et al., 1989]. The specific particle underestimate of what the 14C methodmeasures. If only productionrate, r, is estimatedfrom the changein attenuation: phytoplankton contribute to beam attenuation, daytime 1 ct productivityfrom beam c shouldbe multipliedby 1.5 to 2 for
comparison with 14Cuptake.Whenthiscorrection is applied, productivity frombeamc is muchhigherthanmeasured 14C
r=7In(•)
(3)
at timet (hours)andtime uptake. This would indicate that either our carbon-specific wherect andco arebeamattenuation to r = attenuation coefficient is highor 14Cmeasurements arelow. zero, respectively.The increaseat 28 m corresponds
Anotherpossibilityis that c• varies duringthe day, 0.085 h'1. This increasereflectsthe balancebetweenlightgrazing(g): r = #. exaggerating the diurnalincrease[Acklesonet al., 1990;Olson dependentgrowth(#) andlight-independent g. We follow the reasoningof Siegelet al. [1989], but for this et al., 1990]. Beam c was measuredroutinely only twice per day, so the discussionwe assume that (1) the rate of light-dependent diel variability of attenuationcould not be describedin detail. growthis constant•rnax) from 0800 until 1600 hours,when exceeds 200 I•molm'2 s'l; (2)the specific rateof To calculate productivity from changes in beam c, we irradiance (rmax)is likewiseconstant at 0.085h'1 multipliedby 10 the hourlyratesdeterminedbetween0830 and particleproduction 1330 hours,implicitly assuminglinear accumulation of POC between 0800 and 1400 hours; (3) # is zero in the dark, duringthe day, curtailedneardawnanddusk.Belowwe describe increaseslinearly from 0600 until 0800 hours,and decreases an exponentialmodel that'can be usedto estimateproductivity, linearlyfrom 1600 until 1800 hours;and (4) a constantgrazing rate (g) balancesgrowth over 24 hours (Figure 11a). The yielding similar results. ratewascalculated by iteration(g = 0.061h'l). The Chemical composition of phytoplankton.Siegel et al. grazing [1989] clearly recognized that attenuation could not be maximum light-dependent growth rate was r,nax + g contributeto attributedexclusivelyto phytoplankton,but it is difficult to (#,nax= 0.146 h'l). If only •hytoplankton quantify the degreeto which phytoplanktoncontributeto the attenuation,the specific growth rate for phytoplanktonover from the measurement.If we assumethat phytoplanktonare entirely 24 hoursis thus1.46 d'l. Productivitycalculated responsible for beam attenuation,we can calculatethe C:Chl model (Figure 11b) was only 4% higher than an estimate ratio (w:w) of phytoplanktonfrom beam c and Chl. This obtainedby multiplying the mean hourly increaseby 10 (of. estimate will be too high by an amount correspondingto Figure 6). Siegel et al. [1989] recognized that if detritus or other detrital and heterotrophicattenuation at 660 nm. At the equatorial station, the maximum C:Chl ratio (g:g) of particles contributed to beam c, these rates would be
CUIZ•N ETAL.:PHYTOPLANKTON IN THE EQUATORIAL PACIHC 300
0.20
ß
250
0.15
200
O.lO
150
0.05
100
#
0.00 -0.05
50 ;-
-0.10
_
0000
0600
1200
1800
2400
Time
beam
attenuation
until
6• 1 the
relative
contributions
of
phytoplankton,microheterotrophsand detritus are resolved. In summary, a vertical profile of primary production, calculatedfrom changesin beam c, lendscredenceto the utility of transmissometry as a tool to examine productivity: calculated production is low close to the surface, where photoinhibitionwas documented,and it is zero at the 1% light
level.High (about1.5 d'1) to extremelyhighspecificgrowth rates of phytoplanktonare indicated by changesin beam c, suggesting vigorous growth of phytoplankton, effectively controlled by grazing. Even though changes of beam attenuationseemto reflect primaryproductionquite accurately, rigorousinterpretationsare very difficult becausethe relative contributions of phytoplankton, microheterotrophs and
detritus arenotknownandtheconstancy of c• is questionable. These uncertaintiesare being addressedbut they have not yet been resolved [cf. Morel and Bricaud, 1986; Pak et al., 1988;
Spinrad et al., 1989; Morel and Ahn, 1990; Stramski and
0.14
Morel, 1990; Ackleson et al., 1990].
B 0.12
Trace Elementsand the Measurementof Primary Productivity
If trace-metal contamination during sampling and incubation[Carpenterand Lively, 1980;Fitzwateret al., 1982] 0.08 had seriously affected photosynthesis or growth, our study would have been greatly compromised.Toxicity would have 0.06 causedunderestimation of productivity;enrichmentcould have 0.O4 stimulatedgrowth and lead to overestimation.To examinethe potential effects of trace elements on the measurementof 0.02 primary productivity, we measuredP-I, a very sensitive indicatorof phytoplanktonphysiology.We addedcopper,to 0 600 1200 1800 2400 exacerbate any toxicity, and EDTA, to alleviate toxic contamination [Sharp et al., 1980; Cullen et al., 1986]. Also, Time we enriched with iron, which conceivably could have Fig. 11. Model of phytoplankton growthand grazingat the equatorial stimulatedproductionin the shortterm. Effectswere examined station,28 m. (a) The threelines representthe constantgrazingrate,g (dashed line), thelight-dependent growthrate,# (stippledline), andthe on time scalesfrom I hour to 2 days.All resultswere compared o.1
specificrateof particleproduction, r (solidline). Irradianceat 28 m, 10 min averages, observationsover 6 days, calculated as 10% I o (rectangles). (b) Changesof beamattenuation (c - Cw)from the model: the arrows indicate 0830
and 1330 hours, the times at which
attenuationwas measured.Averagesof beam c at thesetimes over 6 daysconstrained the model.
to time-zero controls as well as to other treatments or controls.
All resultswere negative.Changesof P-I over 48 hoursat 11% I o were negligible (Figure 8). Our conclusionis that with respectto the uptake of bicarbonate,our samplingand SIS
incubationsdid not discerniblyperturb the physiologyof the dominant phytoplankton. We did not take all possible [Fitzwateret underestimates. Assume the extreme, that phytoplankton precautionsto preventtrace-metalcontamination accountfor only 30% of beam attenuation.The sink for the al., 1982], but we were carefuland we did eliminatea principal loss term, g, is still assumed to be unsampled by the culprit, the black neoprenerubber closureson conventional transmissometer. In essence, 70% of the attenuation at time Niskin samplers[Chavez and Barber, 1987; Williams and zero (the morning observation)is consideredas a constant Robertson, 1989]. Our resultsstronglysupportthe conclusion can be obtainedif simple background.Our model showsthat autotrophswould have to that legitimate rate measurements are observed[Marra and Heinemann,1984;Cullen producecarbonat a high specificrate to supportthe inferred precautions 53% increaseof total particlesin 5 hours at 28 m: ].lma x is et al., 1986; Price et al., 1986; Williams and Robertson,
0.349 h-1, andg is 0.145h'1. The specificgrowthrate for 1989]. phytoplankton over 24 hourswouldbe 3.48 d'1. Thisis Trace Elementsand Limitationof Primary Productivity extremelyhigh. Resultsfrom laboratoryculturesindicatethat
themaximumspecificgrowthratefor phytoplankton at 26øCis about3.0 d'l, evenundercontinuous light[Eppley,1972].
When discussingthe regulationof primary productivityby nutrients, it is useful to distinguish between regulation of If insteadwe assumethat the 70% nonautotrophic particles growthrate and limitation of standingcrop. If standingcrop is are heterotrophic,and that they are linked to autotrophic kept low by grazing or some other loss process,productivity productionand increasein concertwith phytoplankton(i.e., can be limited even if the specific growth rates of phytoplanktonalwayscontribute30% of the attenuation),the phytoplanktonare maximal. Our experimentsexaminedirectly
carbon-specificrates of photosynthesisfor phytoplankton theinfluence of traceelements on thespecific growthratesof
fromFigure1la wouldhavetobe3.33timeshigher(0.49h'l) to supportthe observedincreaseof particleabundance in the light. These examplesshow that specific growth rates of phytoplankton cannotbe accuratelyestimatedfrom changesin
phytoplankton.We must infer the relationship between trace nutrientsand standingcrop. Trace elementlimitationof specificgrowthrate. Relatively
high specificgrowthrates of phytoplankton (1.5 d'1 or
652
CUI.I,la.N ET At,.:PHYTOPLANKTON IN THE EQUATORIAL PACIFIC
possibly more) are suggestedby diel changesin beam c. Experimental incubationsalso indicated that growth rates in situ were fairly high: during the first two days of incubations, when the P-I relationship, a sensitive indicator of perturbations to growth conditions, showed little change (Figures 8 and 9), the concentrationof Chl increasednearly
equatorialwatersand the SouthernOcean[Martin, 1990]. These conclusionshave beenquestioned[Banse,1990;de Baar et al., 1990].Becausewe couldnot preventiron contamination during
sampling,our experimentsare not appropriatefor examining iron limitation of final yield, so we cannot reject the hypothesisthat iron limits the potential standingcrop of
exponentially at a rateof 0.6 d'1. We takethisasa minimum phytoplanktonin the equatorial Pacific. It should be noted, estimateof phytoplanktongrowth rate in situ, given that some grazing was likely in the bottles.These estimatedgrowthrates are not consistentwith the notion that the supply of trace elements severely restricted the specific growth rates of phytoplanktonat the equatorialstation. Treatmentswith copper and the chelatorEDTA had little effect on the growthof phytoplanktonfrom equatorialwatersat 150øW (Figures7b, 8c, 9). Theseresultsindicatethat toxicity from divalent cation contaminantsdid not compromiseour results and that copper toxicity did not regulate the specific growth rates of the dominant phytoplanktonin situ. These conclusionsdo not exclude the possibility that toxic trace elements might influence equatorial phytoplankton assemblages by inhibiting the growth of somespecies. Because contamination with iron almost surely occurred during sampling, it can be argued that our experimentsare uselessfor examining the effects of iron on phytoplankton. This would be true except for the observation that the responsesof phytoplanktonto iron enrichment seem to be slow [cL Martin et al., 1989]. If growthratesin situ hadindeed been limited by Fe, low rates would have been maintained duringthe first 1-2 days,duringwhich time we mightexpectto see a change in photosyntheticcharacteristics,followed by rapid accelerationof growth.We saw no responseof P-I over 2 days,but subsequently we did observean apparentacceleration of growthrate (Figure 7b). This more rapid growthmay well characterize a distinct assemblage, released from grazing pressuresand responding to enhanced availability of iron [Banse, 1991]. Even if the abundanceof thosespeciesin situ had been regulatedby the availability of iron, grazing must have been responsiblefor maintaining the constantstanding crop of the dominant equatorial phytoplankton,which was
however,that incubationsto measurefinal yield are unnatural: grazingpressureis strongin the equatorialPacific, and grazing is reducedin incubationprocedures.The experimentsmight thereforeshow not what limits standingcrop in situ, but what limits standingcrop when the grazinglimitationis relaxedor removed. 5. CONCLUSIONS: WHAT LIMITS
PRIMARY PRODUCTIVITY?
The presence of nitrateat relativelyhighconcentrations in equatorialsurfacewatersindicatesthat the productivityof the systemis limitedby oneor moreprocesses or factors.Simply, assimilationof the excessnitrate would lead to more primary
productionbut somethingis preventingthat from happening. One possibilityis that physicalforcing (upwellingand verticalmixing)preven•ts the phytoplankton assemblage from adaptingto ambient conditionsso that specific growth rates are low. Our results strongly suggestthat phytoplanktonare well adapted to ambient conditions through much of the euphoticzone, so physical forcing does not seem to hamper photosynthetic performance. We cannot exclude the possibilitythat althoughphotosynthetic processesare adapted to ambient conditions, nitrate assimilationis not shifted-up [Dugdaleet at., this issue].
Severalsetsof measurements (14Cincubations, increase of Chl duringSIS incubations,diel variabilityof beamc) indicate that specific growth rates of phytoplanktonare relatively
high,about0.6 d'1 or possibly muchhigher. Nonetheless, Chl
was relatively constantday-to-day,indicatingthat the growth of phytoplankton was closely balanced by losses (e.g., grazing). The pronounceddiel variability of beam attenuation, interpretedaccordingto Siegel et al. [1989], also suggested tight coupling between autotrophicproductionand grazing. growing at a minimum specific rateof 0.6d'l. We cannot assert that the specific growth rates of This is perhapsour bestevidencethat grazingis the proximate phytoplanktonwere maximalfor the temperatureandirradiance control on standing crop, and thereby productivity, in regime at the equator. In fact, some biomass-specificrate equatorial waters [cf. Walsh, 1976; Minas et al., 1986]. estimateswere relatively low. Photosynthetic rates were well Unfortunately, the temporal change of beam attenuationis a below those measuredin other warm waters: Pmax was 5-6 poorly understood(althoughpromising) measureof particle g C g Chl'1 h'l in surfacewatersat the equatorwherethe dynamics.The possibilityexiststhat muchof the signalis due temperaturewas about26øC, whereasother studies[Maloneand to diel variabilityin c•, the carbon-specific attenuation Neale, 1981; Falkowski,1983;Keller, 1989] indicatethatPmax coefficient. We hypothesize that specific growth rates of can be as high as 20-25 at the sametemperature.Accordingly, integrated photosynthesisper unit Chl was lower than phytoplanktonwere adequateto exploit the excessnitrate in predicted from simple models of productivity and insolation the surface layer at the equator but that standingcrop was [Platt et al., 1988; Cullen, 1990]. The relatively low rates of controlledby grazing. If grazing is the proximatelimitation photosynthesis are not necessarily inconsistent with high on standing crop and thereby on primary production, the growthrates.Rapid growth can be supportedby relativelylow supply of a trace element such as iron might still be the pB if C:Chl is low.
ultimate
Trace-element limitation of standing crop. Martin et al. [1989] showed that during incubationsof samplesfrom the high-nutrient,low-chlorophyll subarcticNorth Pacific Ocean, the final yield of chlorophyllwas proportionalto addediron. This result suggeststhat iron limits standingcrop in those waters. Martin and colleagues have presented independent evidence to suggest that iron limits the growth of phytoplankton not only in the north Pacific, but also in
phytoplankton dominate the equatorial upwelling system becausethey are superiorcompetitorsfor iron [Brand et al., 1983], effectively excluding phytoplanktonsuch as diatoms that dominatein coastalupwelling. Small phytoplanktonare more susceptible than larger diatoms to grazing by microzooplankton,so it is possiblethat if the supplyof iron to the equatorialPacific were increasedsubstantially,diatoms would bloom, to someextent uncoupledfrom grazingso that
control.
It
is
conceivable
that
small
oceanic
C•N
ETAL.:PHYTOP•TON
IN TI• EQUATORIAL PACIFIC
653
in nitratewouldbe depleted.Alternatively,large-scalecirculation Cullen,J. J., andM. R. Lewis,The kineticsof algalphotoadaptation the contextof vertical mixing, J. PlanktonRes., 10, 1039-1063, might selectagainstdiatomsby isolatingsurfacewatersfrom 1988. seedpopulations[Chavez, 1989]. Cullen, J. J., M. Zhu, and D.C. Pierson,A techniqueto assessthe Thisstudyandtheothersin thisvolumehaveanswered a few harmfuleffectsof samplingand containment for determination of questions aboutplanktonicdynamicsin the equatorialPacific, primaryproduction, Limnol.Oceanogr.,31, 1364-1373,1986. but many have yet to be resolved.Some hypothesesseem de Baar, H. J. W., A. G. J. Buma, R. F. Nolting, G. C. Cad6e, G. Jacques,and P. J. Tr6guer,On iron limitationof the Southern mutuallyexclusive[Walsh,1976;Martin et al., 1989;Dugdale
et al., this issue],but we have demonstrated that components of each can be accommodatedin a coherentdescriptionof the
Ocean:Experimental observations in theWeddellandScotiaSeas,
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(ReceivedMay 24, 1990; acceptedApril 5, 1991)
