Decreasing Marine Biogenic Calcification: a Negative Feedback

GLOBAL BIOGEOCHEMICALCYCLES, VOL. 15, No. 2, PAGES507-516, JUNE 2001

Decreasing marine biogenic calcification' A negative feedback on rising atmospheric pCOe Ingrid Zondervan,Richard E. Zeebe1, BjSrn Rost,and Ulf Riebesell Alfred WegenerInstitute for Polar and Marine ResearchBremerhaven, Germany

Abstract. In laboratory experimentswith the coccolithophorespecies Emiliania huxleyiand Gephyrocapsaoceanica, the ratio of particulate inorganiccarbon (PIC) to particulateorganic carbon (POC) productiondecreased with increasingCOe concentration([CO2]). This was due to both reducedPIC and enhancedPOC productionat elevated[CO2]. Carbondioxide concentrations covered a rangefrom a preindustrial level to a value predicted for 2100 accordingto a "businessas usual" anthropogenicCO2 emissionscenario. The laboratory results were used to employ a model in which the immediate effect of a decreasein global marine calcification relative to POC production on the potential capacity for oceanic CO2 uptake was simulated. Assumingthat overall marine biogeniccalcification shows a similar responseas obtained for E. huxleyi or G. oceanicain the present study, the model revealsa negative feedbackon increasingatmospheric CO2 concentrationsowing to a decreasein the PIC/POC ratio.

1. Introduction and then transported as particulate organic carbon The ocean plays a major role in the global carbon (POC) to deeperwater layers. The carbonatepump cycle, representingthe largest reservoir of carbon that transportsparticulate inorganic carbon (PIC) to the deepsea, which is formedin the surfaceocean: is exchangedwith the atmospherein the form of CO2 on timescales< 1000 years. The uptake of atmospheric Ca2+ + 2 HCO• --• CaCO3q- CO2 q- H20. (2) CO2 by the oceans is driven by physicochemicalpro- cessesas well as biologicalfixation of inorganiccarbon As the uptake of 2 molesof alkalinity in the form of species. The biogenic production of organic material HCO• (or COl-) and1 moleof DIC duringcalcifica- and carbonate minerals in the surface ocean and their tion causesa shift in the equilibrium of the carbonate subsequenttransport to depth, termed the "biological systemtoward higher [CO2] (seesection 4), bioõenic carbonpumps" [Volk and Hoffert, 1985], generate a gra- calcificationrepresents a potential CO2 sourceto the dient of dissolvedinorganic carbon (DIC), with rela- environment[Holligan et al., 1993; Robertsonet al., tively low values in the surface and higher values at 1994]. Sincecalcification often occursin combination depth. The biologicalcarbon pumps are thought to be with productionof organicmatter, part of the CO2 gen- responsiblefor approximately three-quarters of the ver- erated may be taken up by photosyntheticcarbon fixa- tical DIC gradient[Volk and Hoffert, 1985].Depending tion [$ikeset.al., 1980;Holligan and Robertson, 1996]. on their effecton ocean-atmosphereCO•. exchange,two Thus comparedto noncalcifyingnew productionsys- different biological pumps can be distinguished. The tems (for examplediatom blooms), calcifying commu- organic carbon pump is a sink for CO•., which is taken nities are a smaller sink or form a net potential source up during photosyntheticcarbon fixation: of CO2 to the atmosphere[Ware et al., 1991;Holligan et al., 1993]. 6 CO2 + 12H•.O -• C6H1206+ 6 O2 + 6 H•.O (1) Althoughcorals are the mostconspicuous calcifying organismsin the ocean and are widely distributed in tropical shelf regions, they account for only 10% of 1Alsoat Lamont-Doherty Earth Observatoryof Columbia the globalCaCO3 production [Ware et al., 1991;Milli- University, Palisades, New York man and Droxler, 1996]. From a quantitativepoint of view, the most important groupsof marine calcifying Copyright 2001 by the American GeophysicalUnion. organismsare pelagic organismslike coccolithophores Paper number 2000GB001321. [Westbroeket al., 1994; Winteret al., 1994],plank- 0148-0227/01/2000GB001321512.00 tonicforaminifera, and pteropods[Morse and Macken-

507 508 ZONDERVAN ET AL.' NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO•. zie, 1990].Among these groups, which contribute up to [C02] in the oceanwill decreasethe CaCO3saturation 70%to globalCaCOs precipitation [Wollast, 1994; Mil- state, which will make the conditions for calcification limanand Droxler, 1996], coccolithophores are thought lessfavorable [Wollast, 1994]. The CaCO3 saturation to be the mostproductive calcifying group [Westbrock state • is defined as et al., 1993]. They form intensiveblooms extending overlarge parts of the globalocean, mainly at subpolar n- [C•+][CO]-]K* ' (3) latitudes[Brown and Yoder,1994]. Theseblooms are sp mostlymonospecific and formedby only a few coccol- whereK•*p is the stoichiometricsolubility product for ithophore species,of which the most prominent rcp- the mineral phasesof CaCO3 (calcite or aragonite). resentatives are Emiliania huxleyi and Gephyrocapsa Sensitivity to the CaCO3 saturation state has been oceanica[Winter et al., 1994]. Massdevelopment of shownfor corals[Gattuso et al., 1998; Kleypaset al., coccolithophoresis a main driving forcefor the export 1999, Langdonet al., 2000] and foraminifera[Bijma of calcium carbonateto the deep ocean. Although cal- et al., 1999],where decreasing CaCO3 saturationstate cium carbonatecycling represents only a smallËaction caused a decrease in calcification rates. of the globalcarbon cycle, atmospheric CO2, whichis It has been calculated that marine calcification con- largelya functionof DIC and all•linity in the surface stitutes a larger source for CO2 when the seawater ocean[Broecker and Peng, 1982], is intimatelyrelated buffer capacity decreasesin the surfaceocean as a conse- to CaCOs production. E. huxleyiand G. oceanicaare quenceof increasingatmospheric CO2, a positive feed- thereforeof main importancein globalcarbon cycling. back on increasingCO2 concentrations[Frankignoulle Estimates of global calcium carbonateproduction et al., 1994; Gattusoet al., 1996]. However,these cal- rangesfrom 0.64 to 2 Gt C per year(1.03 Gt C [Morse culationswere done under the assumptionthat global and Mackenzie,1990]); (0.64 Gt C [Milliman,1993]); calcification rates remain constant over time. If calcifi- (1-2 Gt C [Shaffer,1993]); (1.0-1.3 Gt C [Westbrocket cation by the dominant calcifying group, i.e., the coc- al., 1993]);(1.13 Gt C [Wollast,1994]); (1 Gt C [Mil- colithophores,also showsto be sensitiveto changing limanand Droxler, 1996]). Modern estimates of global carbonate chemistry in the sea surface,potential CO2 annualmarine primary production are ~45 Gt C [An- exchangebetween ocean and atmospherecould be af- toine et al., 1996],of which~10 Gt C are exported fected over large areas of the world ocean. Riebesellet to the deepsea [Palmer and Totterdell,2001]. The es- al. [2000]showed that the ratio of calcificationto POC timated export ratio of CaCO3 to particulate organic production in the coccolithophoridspecies E. huxleyi carbon(rain ratio) is thereforerelatively high, ranging and G. oceanicais sensitiveto the carbonate chemistry from0.17 to 0.4 (0.18 [Shaffer,1993]); (0.17-0.33[West- in the growth medium. In both laboratory experiments brocket al., 1993]); (0.25 [Broeckerand Peng,1982]); and natural phytoplankton assemblagesthis ratio de- (0.4 [Sigmanet al., 1998]); (seeHolligan and Robert- creasedwith increasingCO2 concentrationcorrespond- son[1996] for review). Sincethe exportof CaCO3and ing to surfaceocean conditionsranging from preindus- POC have opposite effects on the surface ocean CO2 trial levels to values expected in the year 2100. partial pressure,a change in the rain ratio affects the In this study we present results of laboratory exper- partitioning of CO2 betweenocean and atmosphere.It iments with E. huxleyi, where the effects of changing has been suggestedthat the rain ratio is not constant carbonatechemistry on calcificationand particulate or- through time and is an important factor in the regula- ganic carbon production were tested. We comparethe tion of globalclimate [Archer and Maier-Reimer, 1994]. resultswith data obtainedby Riebesellet al. [2000]. From the middle of the 18th century, the atmo- In addition, a model was employedto simulate short- spheric partial pressureof CO2 has increasedsteadily term effectsof increasingatmospheric CO2 concentra- from 280 to 366 patm in the year 1998 [Keelingand tions on the CO2 release due to CaCO3 precipitation Whorl,1999]. This risein atmosphericCO2 concentra- in the surface ocean. As input to the model, we used tion has led to changesin the surfaceocean chemistry the data from laboratory experimentswith E. huxleyi [Brewer,1978, 1997; Chen and Millero,1979] and will and G. oceanicapresented by Riebesellet al. [2000]and continueto causecorresponding changes in the future. in the present study, to simulate different scenariosof Followingthe International Panel on Climate Change changingcalcification rates in the surfaceocean. (IPCC) "businessas ususal" scenario (IS92a, [Houghton et al., 1995]),it can be predictedthat by the year2100, 2. Methods when atmospheric pCO2 is expected to have reached about 700 patm, sea surface[CO2] will have tripled, Monospecificcultures of E. huxleyi (strain P ML and [CO]-] and pH will havedropped by 50%and B92/11) and G. oceanica(strain PC 7/1) weregrown in 0.35 units, respectively,relative to preindustrial values filtered (0.2 pm) seawaterenriched with NOs and PO4 [Wolf-Gladrowet al., 1999]. The presentincrease of to concentrationsof 100 and 6.25 pmol L -•, respec- ZONDERVAN ET AL.' NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO2 509

Table 1. Productionof ParticulateOrganic Carbon (POC, pg C cell-• d-•), ParticulateInorganic Carbon (PIC, pgC cell-• d-•), andthe PIC/POC Ratioin G. oceanicaand E. huxleyiUnder Two L/D Cyclesand at Different CO2 Concentrations(/•mol L -•) in the GrowthMedium a

E. huxleyi(16/8 L/D) E. huxleyi(24/0 L/D) G. oceanica(16/8 L/D) CO2 POC PIC PIC/POC CO2 POC PIC PIC/POC CO2 POC PIC PIC/POC

5.61 9.02 9.24 1.02 11.68 11.08 9.75 0.88 5.68 21.41 25.26 1.18 (0.26) (0.27) (0.51) (0.83) (0.87) (1.06) 12.36 9.76 9.28 0.95 16.77 12.59 9.16 0.73 11.95 26.46 22.56 0.97 (0.19) (O.35) (0.84) (O.73) (•.3•) (O.07) 18.45 9.44 8.00 0.85 17.95 14.03 9.43 0.67 16.94 25.22 19.26 0.77 (0.12) (0.25) (0.21) (0.39) (1.18) (2.27) 21.32 10.66 8.53 0.80 22.56 11.76 7.83 0.67 24.78 25.68 19.81 0.78 (0.24) (0.54) (0.52) (0.30) (1.29) (2.97) 27.25 9.78 7.56 0.77 30.00 13.26 7.38 0.56 33.71 32.22 5.60 0.17 (0.15) (0.23) (1.10) (0.38) (1.51) (1.61)

•The numbers in parenthesesrepresent 1 s.d. tively and with metalsand vitaminsaccording to was calculated as the difference between TPC and POC. [Guillardand Ryther, 1962]. Cultures were preadapted Samplesfor cell countswere fixed with 400/•L/20 mL to the experimentalconditions for •12 generationsand sample of a 20% formaldehydesolution buffered with maintaineddilute by starting the experimentwith low hexamethylenetetramine, and counted within one day cell concentrations. The incident photon flux density by meansof a Coulter "Multisizer II". The growth rate was 150 y,mol m-2 s-• and the temperature15øC. (/•) wascalculated as E. huxleyiwas grown at a 16/8 and24/0 hoursL/D cycle,whereas G. oceanicawas grown at a 16/8 hoursL/D (In½1 --In co) (4) cycleonly. Five different CO2 levels (Table 1) weread- /•= At ' justedby addingI N HC1or 1 N NaOH to the medium. where co and c• are the cell concentrationsat the begin- At the end of the experiment,after 8 generations,less ning and the end of the experiment, respectively,and than 7% of the DIC in the medium had been taken up by At is the duration of the incubation in days. Inorganic the cells. After inocculationin triplicate 2.4 L borosil- andorganic carbon production (P, pg C cell-• d-•) was icate bottles,the bottleswere closed immediately with calculated accordingto teflonlined screw caps without headspace to avoidCO2 exchangewith the atmosphere. P-/•(cellular carboncontent). (s) Samplesfor DIC and alkalinity measurementswere taken in 300 mL borosilicatebottles, fixed with I mL of 3. Experimental Results a HgC12solution (35 g L-•) andstored, in caseof DIC samplesfree of air bubblesat 4øC. DIC wasmeasured Changesin the productionof PIC and POC and the coulometrically[Johnson et al., 1985]in duplicateand PIC/POC ratio are analyzedin relationto [CO2].Data alkalinitywas calculated from linear Gran plots [Gran, of E. huxleyigrown at a 16/8 L/D and of G. ocean- 1952]after duplicate potentiometric titration [Bradshaw ica are taken from Riebesellet al. [2000]. PIC and et al., 1981;Brewer et al., 1986]. The carbonatesys- POC data for G. oceanicawere incorrectly plotted by tem of the medium was calculated from temperature, Riebesellet al. [2000]and have been correctedin the salinity, and the concentrationsof DIC, alkalinity, and present study. However, note that trends remain ex- PO4, usingequilibrium constantsof Goyet and Poisson actly the same. With increasing[CO2] in the growth [1989].Subsamples for the determinationof total par- medium and correspondingchanges in pCO2, pH, and ticulate carbon (TPC) and particulateorganic carbon [CO•-],POC production increases slightly in E. hux- (POC) werefiltered on precombusted(12 hours,500øC) leyi at a 16/8 L/D. When grownat a 24/0 L/D cycle QM-A filters(pore width •0.6/•m) and storedat -20øC. there wasno siginificantchange in the POC production Prior to analysis,the POC filters were fumed for 2 hours in E. huxleyi.(Figure la, Table 1). In contrast,there with a saturated HC1 solution to remove all inorganic was a pronouncedincrease in the POC production in C. TPC and POC were subsequentlymeasured on a G. oceanicaover the CO2 rangetested (Figure l d, Ta- massspectrometer. Particulate inorganic carbon (PIC) ble 1). The cellularorganic carbon content of G. ocean- E. huxle yi G. oceanica pH pH 8.5 8.3 8.1 8.0 7.9 8.5 8.3 8.1 8.O 7.9 , I I I I I i i i pCO2 (patm) pCO2 (patre) 200 400 600 800 200 400 600 800 15 I I i i I i i Io 40- 'o I (.o o I•,- le It,,, 14- I I I I 35- I I I I I I I I I, I, • (1312_ 30- I I I I .t • (.3 I I I 1::)311- I I I 25- I (.3 I I I I OlO - i , I I 20- I I I I I I I A I I 15-D I I I 8 I I I I I I I • • I I I 13 I I 30 I I I I I I I 12- I I I I I 25-•• 'LI I I I i I, I 2o- I -•10- ...I I I I I• I I I 9- 15- I I I I (.3 8- 10- I I I I I I 7- I I I I I I 5- E I I 6, ii Ii i l I I I I I I I I I 1.2-1a I I • I I 1- •1 I I I Ix S.,I I 1- I I I I • I \ 0 I I I o.8- I I • I I I I • I I I • I I • I 0.6- I I ox I I I 0.7- I I o I I I I I I • I 0.4- I I I 0.6- I I I I I I I I •0 o.2- I I I _- ß ß c a ! 0.5 i i i i 5 lO 15 21o 215 5 110 15 20 2i5 30 35 [C02] (#molkg-•) [C02] (#molkg-1) 3•0 2(;0 •,•0 •(;0 7• 340 2(•0 •0 •(•0 7• [C032'] (#molkg-•) [C032-] (#molkg-• ) Figure1. (a-c)Rates of production ofparticulate organic carbon (POC), particulate inorganic carbon(PIC), and the ratio of PIC[POC in E. huxleyiat L[D cyclesof 16/8 hours (closed symbols)and 24[0 hours (open symbols) and (d-f) G. oceanicaat 16[8 L[D. Errorbars represent onestandard deviation (n=3). Thevertical dashed lines indicate atmospheric pCO2 at preindustrialtimes, at present,and as expected in 2100according to a "businessasusual scenario" IHoughtonet al., 1995].Note that thevertical axes have different scales and that DIC andtotal alkalinitydiffered slightly between theexperiments, sothat values for pH, pCO2, and ICO•-] are approximations.Reprinted by permission from Nature (Riebesell et al. 2000)copyright (2000) Macmillan MagazinesLtd. ZONDERVAN ET AL.: NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO•. 511

ica is 2 times higher than the organiccarbon content of E. huxleyi. Moreover,E. huxleyicells grown under continuouslight have a higherorganic carbon content than thosegrown at a 16/8 L/D cycle. In contrastto 2.$ POC production, the production of PIC significantly decreaseswith increasing[CO2] in E. huxleyiand even morepronounced in G. oceanica(Figures lb and e, Ta- .•2.25 ble 1). There is no significantdifference in PIC content betweenE. huxleyicells grown at differentL/D cycles. The decreaseand increasein the production of PIC and POC, respectively,caused a decreasein the ratio of PIC to POC with increasing[CO2] in bothE. huxleyi(r 2 = 0.98 and 0.94 at 16/8 and 24/0 L/D, respectively)and G. oceanica(r2 - 0.95) (Figureslc andf). 2.2•,,,•.O.6•'" When these data are interpolated between preindus- 2.1,•.9 1.95 2 2.05 2.1 2.15 2.2 DIC(mmol kg -1) trial pCO2 valuesand valuesexpected in 2100 (280 and 700 ppm, respectively,indicated in Figure 1), an 8.5 and Figure 2. Changesin the concentrationsof DIC, total 10% increasein POC productionand a 15.7 and 25.7% alkalinity,and CO2 owingto calcification(light-shaded vectors)at (left) preindustrialtimes and in (right)2100. decreasein PIC production is observed in E. huxleyi Numbers at the vectors are relative numbers. Thus under a L/D cycle and continuouslight, respectively. when 1 mole C as DIC is taken up during calcification, This causesthe PIC/POC ratio to decreaseby 21 and 0.63 mole C as CO2 is released to the environment dur- 31.5%, respectively. In G. oceanicathe POC produc- ing preindustrialtimes, and 0.79 C in 2100, owingto tion increasesby 18.6% over this range, whereasthe a decreasingbuffer capacity (light-shadedvectors, see PIC productionand PIC/POC ratio decreasesby 44.7 text). Assumingcalcification is only 70% of the prein- and 52.5%, respectively. dustrial value in 2100, CO2 releasedue to calcification wouldthen be 0.56 C (solidblack vectors, see text). 4. Effects of Calcification on the Surface Ocean Carbonate removalof 50/•mol calciumcarbonate per kg seawater. Chemistry SinceDIC and TA decreasein a ratio of 1:2, the slope of a line throughthe vectorin this representationis 2. From (2) it can be seenthat dissolvedinorganic car- The concentrationof dissolvedCO• increasesfrom 10.5 bon (DIC) and total alkalinity(TA) drop by one and two units, respectively,for eachunit of CaCO3 precip- to 12.4/•molkg -1 duringthis process. Thus, for values itated. The new equilibrium concentrationsof the car- of DIC, TA, T, and $ givenabove, the productionof 50 bonate speciesin solution after calcificationcan there- •umolcalcium carbonate results in an increaseof [CO•] fore be calculatedfrom the changein DIC and TA. DIC of 1.9 •umolkg -1. After the formation of calcium carbonate the water and TA are defined as is left oversaturatedin CO2 with respectto the atmo- DIC - [CO2]+ [HCO•]+ [CO]-], (6) sphere,so that CO2 is subsequentlyreleased in orderto reestablishequilibrium. This effectis indicatedby the where[CO2]- [CO•(aq)]+ [H•CO•I and horizontalsolid light-shaded vector in Figure 2. Start- ing at conditionsafter calcificationat [CO2] = 12.4 TA - 2[CO]-]+[HCO•] + •umolkg -1, carbondioxide is releaseduntil aqueous [B(OH)•-]+ [OH-]- [H+], (7) CO2 (and the correspondingpCO2) is restoredto the valueof the atmosphere.Concomitantly, the DIC con- where minor contributions to the TA from seawater concentration decreases, while the TA remains constant. stituents such as phosphateand silicate have been ne- The precipitationof 50 •umolkg -1 CaCO3and the sub- glected.Figure 2 showsan exampletypical for surface sequentequilibration with the atmospherethen finally oceanconditions (T = 15øC,$ = 35), with initial val- leadsto degassingof ,,•32•umol CO2 kg-1 in this exam- uesof DIC = 2.0 mmolkg -1, TA = 2.3 mmolkg -1, ple. and[CO•] = 10.5•umol kg -1. The surfaceocean is as- With risingatmospheric CO2 and the resultingde- sumedto be in equilibrium with the atmospherewith creasein pH of the surfaceseawater, the buffer capac- respectto CO2. The effect of calcificationon the car- ity of the oceanfor CO2 decreases.The ratio of CO2- bonate systemis illustrated by the light-shadedvector. released:carbonate-precipitated(•) during CaCO3 pre- The originof the vectoris locatedat initial conditions, cipitationdepends on the physicochemicalproperties of whereasthe final point correspondsto conditionsafter the seawaterand will increasewith decreasingbuffer ca- 512 ZONDERVAN ET AL.: NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO2 pacity [Frankignoulleet al., 1994;Gattuso et al., 1996]: o.9 • 0.8 . . : . ' ' .1.• ._ _ ) 5(co-) [•(co•.)]pco. ' 0 0.7 ß where5(CO•.) and 5(CO]-) referto variationof dis- g•ß 0.50.6 ...... -.....',:-..-' ....;...... •,•, . ".'''",•,3 -•' • .,•-,,,• solvedCO•. and COl-, respectively.The buffer factors 5pCO•./5(CO•.)and 5pCO•./5(CO]-) can be used to de- 0 0.4 .... scribe the dynamics of the seawater carbonate system 0• 4-•%%%• . . during calcification and to estimate the resulting re- • 0.3 ' o lease of CO•.. Here ß is expected to increasefrom the a. 0.2 ...... '...... ß...... calculatedpreindustrial value of 0.63 [Frankignoulleet :

, al., 1994; Gattusoet al., 1996] to ~0.79 in the year o'oo 2100 and to ~0.84 in 2150, following an IPCC "busi- Year nessas usual scenario" (IS92a, [Houghtonet al., 1995]). Thus, assumingthat calcium carbonate production in Figure 3. PotentialCO2 releasein Gt C yr-• from 1850 to 2150 when annual CaCO• production remains the oceans stays constant this representsan additional constantat I Gt C yr-1 (scenario1, solidline), CaCOs source of CO•.. productiondecreases as in E. huxleyiat a 16/8 L/D A decreasein the production of CaCO3 with increas- cycle(scenario 2, dashedline), or at a 24/0 L/D cy- ing atmosphericCO•. concentrations,as found in corals cle (scenario3, dashedline), and CaCO• production [6attusoet al., 1998],foraminifera [Bijma et al., 1999], decreasesas in G. oceanica(scenario 4, dashed-dotted and coccolithophores[Riebesell et al., 2000;this study], line). will immediately influence the surface ocean carbonate chemistry.In order to quantify this effect we employed a model where we used the laboratory results of the leyi grown at a 24/0 L/D cycle, (4) calcificationde- present study and those obtained by Riebesell et al. creasesas in G. oceanicagrown at a 16/8 L/D cycle, [2000]to simulatethe possibleimpact of decreasingma- (5) PIC/POC ratio decreasesas in E. huxleyigrown at rine calcification on the CaCO3-related CO•. release in a 16/8 L/D cycle, (6) PIC/POC ratio decreasesas in the surface ocean. E. huxleyigrown at a 16/8 L/D cycleand (7) PIC/POC ratio decreasesas in G. oceanica. Since the POC pro- 5. Model Simulation ductionin E. huxleyigrown at a 16/8 L/D cycleshows no significanttrend, a decreasein the PIC/POC ratio Changes in the surface ocean carbonate chemistry is only due to decreasingcalcification rates. The model from conditions prevailing in preindustrial times to resultsfor this scenario(5) are thus very similarto the those expected for the years 2100 and 2150 were sim- results for scenario 2. ulated according to the "businessas usual" anthro- When globalCaCO• productionis kept at a preindus- pogenicCO•. emissionscenario (IS92a) of the IPCC re- trial level of I Gt C per year, the annual CO•. releaseto port 1995[Houghton et al., 1995;see also Wolf-Gladrow the environment increaseswith time due to increasing et al., 1999]. The atmosphericCO•. concentrationsfor atmosphericCO•. and the subsequentdecreasing buffer the period from 2100 to 2150 were obtained from a pro- capacityof the surfaceocean (a positivefeedback, see jection of the IS92a scenarioby fitting an exponential section4; scenario1, Figures3 and 4). When global function to the atmosphericCO2 concentrationsgiven CaCO3 production decreasesas in scenario 2 and 3, by Houghtonet al. [1995].Simulation of the temporal the decreasein CO•. release integrated between 1850 changeof global calcificationrates are basedon the lab- and 2100 (2150) is 8.7 (19.1) or 10.7 (23.5) Gt C, re- oratory results describedin this study. We assumethat spectively(Figure 3, see also Figure 2). When global COl.-related responsesof the coccolithophoresE. hux- CaCO3 precipitation decreasesas in scenario 4, the in- leyi or G. oceanicaas describedin this study are repre- tegrated decreasein CO•. releasewould be 20.1 (44.2) sentative for overall marine biogeniccalcification. Gt C. The potential impact of decreasingcalcification on In our laboratory experiments E. huxleyi grown at a the CO• releaseto the environmentis investigatedus- 24/0 L/D cycleand G. oceanicaincreased their cellu- ing the followingscenarios (see Figure 3): (1) calcifica- lar POC productionwith increasingCO•. concentrations tion staysat a constantrate of I Gt C per year (similar (Figure 1). When an increasein the POC production to present-oceanvalues [Milliman and Droxler,1996]), by marine calcifyingorganisms is accountedfor in our (2) calcificationdecreases as in E. huxleyigrown at a model, the integrated differencein CO•. releasedto the 16/8 L/D cycle,(3) calcificationdecreases as in E. hux- environmentbetween 1850 and 2100 (2150) is 8.7 (19.1) ZONDERVAN ET AL' NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO2 513

0.9 i ! i i i

ß . Why G. oceanicashows higher sensitivity to chang-

•. 0.8 ing carbonate chemistry than E. huxleyi remains un- clear. Furthermore, the reason why E. huxleyi cells o 0.7 grown under continuouslight show higher POC pro- ductioncompared to cellsgrown at a 16/8 L/D cycle • o.s (Figure la), whereasthere is no differencein the PIC decreasebetween both conditions(Figure lb), is also • 0.5 ß . %'•,,•,•' • ß \ ß not clear. One explanation might be the time of sam- o"' • '•,_ o 0.4 7-.•, pling in the L/D experiment,which was at the end of ._• the dark phase.At this point in the L/D cyclethe cells c: 0.3 have the lowest carbon content due to cell division dur- ß o .

n 0.2 ß ing the dark period[Van Bleijswijket al., 1994].If calcification continued in the dark, as was shown in some i i i i •, 0•1•5o 19'00 1950 2000 2050 21O0 2150 studies[e.g., Balch et al., 1992],this couldexplain the Year decouplingof POC and PIC production,yielding a sim- Figure 4. Potential CO2 releasein Gt C yr-• ilar PIC productionunder a 16/8 L/D cycle as under from 1850 to 2150 when annual CaCO3 productionre- continuouslight. This raisesthe questionwhether the mainsconstant at I Gt C yr-x (scenario1, solidline), quantitativenature of the CO2 effectson the PIC/POC PIC/POC ratiodecreases as in E. huxleyiat a 16/8 L/D ratio may be due to the time of sampling and whether cycle(scenario 5, dashedline), or at a 24/0 L/D cycle resultsmay be differentwhen the PIC/POC ratio is (scenario6, dashedline), andPIC/POC ratio decreases as in G. oceanica(scenario 7, dashed-dotted line). averagedover a L/D cycle. We tested this by moni- toring diurnal variation in cellular carboncontent over a 38-hour period at a 16/8 L/D cycle. A consistent significantoffset in cellular PIC and POC content and and 14.2 (31.3) Gt C for scenario5 and 6, respectively, the PIC/POC ratio wasobserved between high and low and 23.3 (51.2) for scenario7 (Figure4). This larger CO2 treatmentsthroughout the diurnal cycle (I. Zon- difference in CO•. release is due to a further reduction dervan et al., Effect of increasingCO2 concentrationon in the PIC/POC ratio when cellularPOC production the PIC/POC ratio in the coccolithophoreEmiliania increases.The relatively strongdecrease in CO•. release huxleyigrown under light-limiting conditionsand differ- in the differentscenarios after 2100 (Figures3 and 4) ent daylengths,submitted to Marine EcologyProgress is due to the exponentialincrease in atmosphericCO•. Series,2000), showingthat the CO2 effectreported here concentrationswith time and the decreasingcalcifica- is not an artifact due to the time of sampling. tion correlatinglinearly to the CO• concentration. In our model we assumethat CO2-related responses of the coccolithophoresE. huxleyi or G. oceanicaas 6. Discussion described in the present study are representativefor In previousstudies, COl.-related effectson calcifi- overall marine biogenic calcification. We used two cation have been demonstratedin corals [Gattusoet coccolithophorespecies, one of them at two different al., 1998; Kleypas et al., 1999, Marubini and Atkin- daylengths,obtaining different scenariosfor the model son,1999], in a corallinealgae [Gao at al., 1993],and simulation. Assuminga constantannual global carbon- in a foraminiferalspecies [Bijma et al., 1999]. The ate productionof I Gt C through time, it can be calcu- responseof the two coccolithophorespecies to CO•.- lated that as a result of increasinganthropogenic CO2 relatedchanges in carbonatechemistry shown by Riebe- and the subsequentdecrease in the seawaterbuffer ca- sell et al. [2000] and in the presentinvestigation, pacity, biogeniccalcification would act as an additional agreeswith previousstudies on other marine calcify- sourcefor CO•. Frankignoulleet al. [1994]calculated ing organisms.Compared to preindustrialtimes, the an additional input of 5 Gt C to the atmosphere from PIC-productionin E. huxleyimay decreaseby 16-26% 1880 to 2030-2050 as a result of the change of the car- and in G. oceanicaby 45% when surfaceocean chem- bonate buffer in the surface ocean. When CO2-related istry changesto conditionsexpected in 2100. This effectson biogenic calcification are accountedfor, our is consistentwith a predicted decreasein calcification model predicts a significantdecrease in potential CO2 over a similar rangeof CO•. in corals[Langdon et al., releaseto the atmospherewhen PIC/POC ratios de- 2000(40%); Kleypas et al., 1999(17-35%)] and in the crease. Thus the expected positive feedback on in- foraminiferaOrbulina universa [Bijma et al., 1999 (18- creasingCO2 concentrationsis completelyreversed by 21%)],although decreases are lowerthan the maximal the effectof decreasingglobal calcificationand becomes reduction of 83% in calcificationshown in natural plank- a negative feedback. This effect is rather small com- ton assemblages[Riebesell et al., 2000]. pared to the current anthropogenicCO2 emission(--7 514 ZONDERVAN ET AL.: NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO2

Gt C annually[Houghton et al., 1995]).Riebesell et al. Third, sinking of coccolithophore-derivedparticulate [2000]showed a reductionin calcificationrates by 36 - material may become reduced when coccolithophore 83% in high relative to low CO2 treatmentsin natural cellsare lesscalcified [Fritz and Balch, 1996; Lecourt plankton assemblages,which were dominated by coc- et al., 1996]or when the compositionof faecalpellets colithophores.E. huxleyi is the most abundant coccol- changesowing to changesin the phytoplankton species ithophoreand possiblythe most productivecalcifying compositionor abundance[Harris, 1994;Holligan et al., organismon Earth today [Holligan,1992; Westbroeket 1993].A decreasein calcificationcould actually reduce al., 1994]. If the observedresponse to increasingCO2 sinkingrate of E. huxleyicells [Fritz and Balch,1996; concentrationsof the two coccolithophorespecies in this Lecourtet al., 1996],and thus CO• uptakein the sur- studyand in the studyby Riebesellet al. [2000]is a gen- face water, due to a decreaseof organic carbon export eral phenomenonin the worlds oceans,a decreasein the to depth. However, we find an increasein POC produc- PIC/POC ratio couldaffect different processes in areas tion at elevated[CO•], whichcould also affect particle where coccolithophoresplay a dominant role. sinking rate. Thus it remains speculativewhat the ul- First, as mentioned above, it directly affects the car- timate effect of a decreasein the PIC/POC ratio on bonate system. When coccolithophorecarbonate pro- particle sinking rate will be. Since this topic is beyond duction in the surfaceocean slowsdown, the potential the scopeof the present study we will not discussthis releaseof CO• to the atmosphere,as a consequenceof in further detail here. calcification,is reduced[Holligan and Robertson,1996] Finally, the optical properties in the surface ocean (see section4 and Figure 2b). In addition to a de- may be altered due to decreasingcalcification or coc- creasein PIC content, we found higher cellular POC colithophoreabundance in regionswere coccolithophore production with increasingCO• concentrationin both bloomsoccur [Balch et al., 1991]. Tyrrell et al. [1999] E. huxleyiand G. oceanica(the cellsbecome larger). In modeled the optical impacts of coccolithophoreblooms a natural field situation, growth is ultimately limited and demonstratedan increasein the reflectanceof light by nutrient availability. Total production of POC will due to the abundanceof coccoliths,a strongerstratifica- therefore not changeif nutrient concentrationremains tion and a decreasein total water column productivity constant. However, when the cellular POC content in- due to intense shading and stratification in these ar- creasesrelative to the P IC content, this decreasesthe eas. All potential changesmentioned above could alter PIC/POC ratio. Experimentsin the presentstudy were ecosystemstructure and regulation ever large areas of done under nutrient replete conditions, which poorly the ocean, although the responseof a complex, multi- mimics the natural situation. Therefore we also tested ple speciesecosystem, where each speciesreacts in its CO•-relatedeffects on the PIC/POC ratio undernutri- own particular way remains extremely difficult to pre- ent limitation• Preliminary results showa similar effect dict [Kheshgiet al., 1991; Westbroeket al., 1994]. as describedin the present study, i.e., a decreasein the In summary, what the responseof marine biogeo- PIC/POC ratio at elevated[CO•] (I. Zondervanand U. chemistry on increasingatmospheric CO• concentra- Riebesell,unpublished data, 2000). tions will be with respect to CO• partitioning between Second, trophic interactions may be influenced if ocean and atmosphereremains speculative. Our model feeding on coccolithophoresby microzooplanktonand showsa completereversal of the expectedpositive feed- copepodsis dependenton cell size or the PIC/POC back on atmospheric CO2 increase when CaCO3 pro- ratio. A decrease in the calcification rate could also duction remains constant,turning into a negativefeed- decreasethe competitivenessof coccolithophoreswith back when calcification rates decreasewith increasing other phytoplanktonfunctional groups. The malforma- CO2. The effect is small compared to the annual an- tion of the coccospheresunder high CO2 concentrations thropogenic CO2 emissions. However, further investi- asshown by Riebesellet al. [2000]may be an indication gation is needed on potential secondaryeffects on the for this. However, sincethe function and regulation of ocean-atmosphereCO• exchange.If the observedCO•- calcificationby coccolithophoresis not known[Young, related responsesin calcification and POC production 1994],it remainshighly speculative what the roleof cal- of coccolithophoresare a general phenomenon,changes cificationfor coccolithophorephysiology and ecologyis. in ecosystemstructure and functioningcan be expected Nejstgaardet al. [1997]demonstrated in a mesocosm with increasingatmospheric CO• concentration. experiment that E. huxleyi dominated bloomsprovided a superior food sourcefor reproduction of the copepod Acknowledgments. We like to thank Anke Dauels- Calanus finmarchicus compared to diatom-dominated berg,B/irbel HSnisch, Klaus-Uwe Richter, and Anja Ter- blooms. Holligan et al. [1993]found selective grazing brfiggenfor laboratoryassistance. The E. huxleyistrain on E. huxleyi cells by microzooplankton in the North PML B92/11 wasgenerously supplied by JohnGreen, Ply- mouth Marine Laboratory, and the G. oceanicastrain PC Atlantic. Thus a shift in the dominanceof phytoplank- 7/1 wassupplied by the CODENET algaecollection in Caen. ton speciesmay affect regulation at higher trophic lev- This workwas supported by the Netherlands-BremenCoop- els. eration in Oceanography(NEBROC). ZONDERVANET AL.: NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO•. $15

References Goyet, C., and A. Poisson,New determinationof carbonic acid dissociation constants in seawater as a function of Antoine, D., J.-M. Andre, and A. Morel, Oceanicprimary temperatureand salinity, Deep Sea Res., 36(11), 1635- production, 2, Estimation at global scale from satellite 1654, 1989. (coastalzone color scanner)chlorophyll, Global Biogeo- Gran, G., Determination of the equivalencepoint in poten- chem. Cycles, 10, 57-69, 1996. riometric titrations of seawater with hydrochloric acid, Archer, D., and E. Maier-Reimer, Effect of deep-seasedi- Oceanol. Acta, 5, 209-218, 1952. mentary calcite preservationon atmosphericCO2 concen- Guillard, R.R.L., and J.H. Ryther, Studiesof marine plank- tration, Nature, 367, 260-263, 1994. tonic diatoms,I, Cyclotellananna (Hustedt) and Detonula Balch, W.M., P.M. Holligan, S.G. Ackleson,and K.J. Voss, convervacea(Cleve), Can. J. Microbiol.,8, 229-239, 1962. Biologicaland optical propertiesof mesoscalecoccolitho- Harris, R.P., Zooplankton grazing on the coccolithophore phore blooms in the Gulf of Maine, Limnol. Oceanogr., Emiliania huxleyi and its role in inorganic carbon flux, 36(4), 629- 643, 1991. Mar. Biol., 119, 431-439, 1994. Balch, W.M., P.M. Holligan, and K.A. Kilpatrick, Calcifi- Holligan, P.M., Do marine phytoplanktoninfluence global cation, photosynthesisand growth of the bloom-forming climate?,in Primary Productivityand BiogeochemicalCy- coccolithophore, Emiliania huxleyi, Cont. Shelf Res., cles in the Sea, edited by P.G. Falkowskiand A.D. Wood- 12(12), 1353- 1374, 1992. head, pp. 487-501, Plenum, New York, 1992. Bijma, J., H.J. Spero,and D.W. Lea, Reassessingforamini- Holligan, P.M., and J.E. Robertson, Significanceof feral stable isotope geochemistry:Impact of the oceanic ocean carbonate budgets for the global carbon cycle, carbonatesystem (experimental results), in Useof Proxies Glob. Change Biol., 2, 85-95, 1996. in Paleoceanography:Examples From the South Atlantic, Holligan, P.M., et al., A biogeochemicalstudy of the coc- editedby G. Fischerand G. Wefer, pp. 489-512,Springer- cololithophore,Emiliania huxleyi, in the North Atlantic, Verlag, New York, 1999. Global Biogeochem.Cycles, 7, 879-900, 1993. Bradshaw,A.L., P.G. Brewer, D.K. Shaffer, and R.T. Wil- Houghton, J.T., et al., (Eds.) in Climate Change199•: liams, Measurementsof total carbon dioxide and alkalin- Radiative Forcing o.f Climate Change and An Evalua- ity by potentiometrictitration in the GEOSECSprogram, tion o.f the IPCC IS92 Emission Scenarios,Cambridge Earth Planet. Sci. Lett., 55, 99-115, 1981. Univ. Press, New York, 1995. Brewer, P.G., Direct observationof the oceanic CO2 in- Johnson, K.M., A.E. King, and J.M. Sieburth, Coulomet- crease,Geophys. Res. Lett., 5(12), 997-1000,1978. ric TCO•. analyses for marine studies; an introduction, Brewer, P.G., Ocean chemistryof the fossilfuel CO•. sig- Mar. Chem., 16, 61-82, 1985. nal: The haline signal of "businessas usual", Geo- Keeling, C.D., and T.P. Whorl, Atmospheric CO•. records phys.Res. Lett., 24(11), 1367-1369,1997. from sites in the SIO air sampling network, in Trends: A Brewer, P.G., A.L. Bradshaw,and R.T. Williams, Measure- Compendiumo.f Data on Global Change,Carbon Dioxide ment of total carbon dioxide and alkalinity in the North Info. Analysis Cent., Oak Ridge, Tenn., 1999. Atlantic ocean in 1981, in The ChangingCarbon Cycle - Kheshgi, H.S., B.P. Flannery, and M.I. Hoffert, Marine biota A GlobalAnalysis, edited by J.R. Trabalka and D.E. Re- effectson the compositionalstructure of the world oceans, ichle, pp. 358-381, Springer-Verlag,New York, 1986. J. Geophys.Res., 96(C3), 4957-4969,1991. Broecker, W.S., and T.-H. Peng, Tracers in the Sea, Kleypas, J.A., R.W. Buddemeier, D. Archer, J.-P. Gat- Lamont-Doherty Earth Observatory, Palisades, New tuso, C. Langdon, and B.N. Opdyke, Geochemical con- York, 1982. sequencesof increased atmospheric CO•. on coral reefs, Brown, C.W., and J.A. Yoder, Coccolithophoridblooms in Science, 28•, 118- 120, 1999. the globalocean, J. Geophys.Res., 99(C4), 7467-7482, 1994. Langdon, C., T. Takahashi, C. Sweeney, D. Chipman, J. Goddard, F. Marubini, H. Aceves, H. Barnett, and Chen, G.-T., and F.J. Millero, Gradual increaseof oceanic M.J. Atkinson, Effect of calcium carbonate saturation CO•., Nature, 277, 205-206, 1979. state on the calcification rate of an experimental coral Frankignoulle,M., C. Canon,and J.-P. Gattuso,Marine calcification as a source of carbon dioxide: Positive feedback reef, Global Biogeochem.Cycles, 1•, 639-654, 2000. of increasingatmospheric CO•., Limnol. Oceanogr.,39(2), Lecourt, M., D.L. Muggli, and P. Harrison, Comparison of growth and sinking rates of non- coccolith and coccolith- 458- 462, 1994. Fritz, J.J., and W.M. Balch, A light-limited continuous formingstrains of Emiliania huxleyi(Prymnesiophyceae) culture study of Emiliania huxleyi: determination of grown under different irradiances and nitrogen sources, J. Phycol., 32, 17-21, 1996. coccolith detachment and its relevance to cell sinking, J. Exp. Mar. Biol. Ecol., 207, 127-147, 1996. Marubini, F., and M.J. Atkinson, Effects of low- Gao, K., Y. Aruga, K. Asada, T. Ishihara, T. Akano, and ered pH and elevated nitrate on coral calcification, M. Kiyohara,Calcification in the articulatedcoralline alga Mar. Ecol. Prog. Set., 188, 117-121, 1999. Corallina piluli.fera,with special referenceto the effect Milliman, J.D., Productionand accumulationof calcium of elevated CO•. concentration, Mar. Biol., 117, 129-132, carbonate in the ocean: Budget of a nonsteady state, 1993. GlobalBiogeochem. Cycles, 7, 927-957, 1993. Gattuso,J.-P., M. Pichon,J. Jaubert,M. Marchioretti,and Milliman, J.D., and A.W. Droxler, Neritic and pelagiccar- M. Frankignoulle,Primary production,calcification and bonate sedimentation in the marine environment: igno- air-sea CO•. fluxes in coral reefs: Organism, ecosystem rance is not bliss, Geol. Rundsch.,85, 496-504, 1996. and globalscales, Bull. Inst. Oceanogr.,Monaco special, Morse, J.W., and F.T. Mackenzie, Geochemistry of Sedi- 1J, 39-46, 1996. mentary Carbonates,Dev. Sedimentol. Ser., Vol. 48, El- Gattuso, J.-P., M. Frankignoulle,I. Bourge, S. Ro- sevier Sci., New York, 1990. maine, and R.W. Buddemeier, Effect of calcium car- Nejstgaard, J.C., I. Gismervik, and P.T. Solberg, Feed- bonate saturation of seawater on coral calcification, ing and reproduction by Calanus finmarchicus, and Glob. Planet. Change, 18, 37-46, 1998. microzooplanktongrazing during mesocosmblooms of :516 ZONDERVAN ET AL.: NEGATIVE FEEDBACK ON RISING ATMOSPHERIC PCO2

diatoms and the coccolithophore Emiliania huxleyi, mospheric C02: Natural Variations Archcan to Present, Mar. Ecol. Prog. Set., 1•7, 197-217, 1997. Geophys.Monogr. Set., Vol. 32 edited by E.T. Sundquist Palmer, J.R., and I. Totterdell, Production and export in and W.S. Broecker,pp. 99-111, AGU, Washington,D.C., a global ocean ecosystemmodel, Deep Sea Res., in press, 1985. 2001. Ware, J.R., S.V. Smith, and M.L. Reaka-Kudla, Coral reefs: Riebesell, U., I. Zondervan, B. Rost, P.D. Tortell, sourcesor sinks of atmospheric CO•.?, Coral Reefs, 11, R.E. Zeebe, and F.M.M. Morel, Reduced calcification 127-130, 1991. of marine plankton in responseto increased atmospheric Westbrock, P., et al., A model system approachto biolog- CO•., Nature, •{07, 364- 367, 2000. ical climate forcing: The example of Eratitania huxleyi, Robertson, J.E., C. Robinson, D.R. Turner, P. Holligan, Glob. Planet. Change, 8, 27-46, 1993. A.J. Watson, P. Boyd, E. Fernandez, and M. Finch, The Westbrock, P., B. Buddemeter, M. Coleman, D.J. Kok, impact of a coccolithophorebloom on oceaniccarbon up- D. Fautin, and L. Stal, Strategiesfor the study of climate take in the northeast Atlantic during summer 1991, Deep forcing by calcification, Bull. Inst. Oceanogr., Monaco Sea Res., dl(2), 297-314, 1994. spdcial, 13, 37-60, 1994. Shaffer, G., Effects of the marine biota on global carbon cy- Winter, A., R.W. Jordan, and P.H. Roth, Biogeography cling, in The GlobalCarbon Cycle,edited by M. Heimann, of living coccolithophoresin ocean waters, in Coccol- NATO ASI Set., Set. I, 15, 431-455, 1993. ithophores,edited by A. Winter and W.G. Siesser,pp. 161- Sigman, D.M., D.C. McCorkle, and W.R. Martin, The cal- 179, Cambridge Univ. Press, New York, 1994. cite lysoclineas a constrainton glacial/interglaciallow- Wolf-Gladrow, D.A., U. Riebesell, S. Burkhardt, and J. Bi- latitude production changes,Global Biogeochern.Cycles, jma, Direct effects of CO2 concentration on growth and 12, 409-427, 1998. isotopic composition of marine plankton, Tellus, Set. B, Sikes, C.S., R.D. Roer, and K.M. Wilbur, Photo.synthesis 51(2), 461-476, 1999. and coccolith formation: Inorganic carbon sourcesand Wollast, R., The relative importance of biomineralization net inorganic reaction of deposition, Limnol. Oceanogr., and dissolution of CaCOa in the global carbon cycle, 25(2), 248-261,1980. Bull. Inst. Oceanogr.,Monaco special, 13, 13-34, 1994. Tyrrell, T., P.M. Holligan, and C.D MobIcy, Optical impacts Young, J.R., Functions of coccoliths, in Coccolithophores, of oceanic coccolithophore blooms, J. Geophys. Res., edited by A. Winter and W.G. Siesser,pp. 63-83, Cam- 104(C2), 3223-3241, 1999. bridge Univ. Press, New York, 1994. Van Bleijswijk, J.D.L., R.S. Kempers, and M.J. Veldhuis, Cell and growth characteristicsof types A and B of Emil- U. Riebesell, B. Rost, R. E. Zeebe, and I. Zondervan, iania huxleyi(Prymnesiophyceae) as determinedby flow Alfred Wegener Institute for Polar and Marine Research, cytometry and chemical analyses,J. Phycol., 30, 230-241, P.O. Box 120161, Bremerhaven, D-27515, Germany. 1994. ([email protected]) Volk, T., and M.I. Hoffert, Ocean carbon pumps: analysis of relative strengths and efficienciesin ocean-driven (ReceivedJuly 3, 2000; revisedOctober 30, 2000; atmosphericCO•. changes,in The Carbon Cycle and At- acceptedNovember 13, 2000.)