Journal of Oceanography, Vol. 60, pp. 719 to 729, 2004

Review

Effects of CO2 Enrichment on Marine

ULF RIEBESELL*

Leibniz Institut für Meereswissenschaften, IFM-GEOMAR, Kiel, Germany

(Received 14 October 2003; in revised form 5 May 2004; accepted 5 May 2004)

Rising atmospheric CO2 and deliberate CO2 sequestration in the ocean change Keywords: ⋅ chemistry in a similar way, lowering seawater pH, carbonate ion CO2 effects, ⋅ carbonate chemis- concentration and carbonate saturation state and increasing dissolved CO2 concen- tration. These changes affect marine in various ways. On the organismal try, ⋅ level, a moderate increase in CO facilitates photosynthetic fixation of some phytoplankton, 2 ⋅ biocalcification, phytoplankton groups. It also enhances the release of dissolved , most ⋅ , notably during the decline of -limited phytoplankton blooms. A decrease in ⋅ re- the carbonate saturation state represses biogenic of the predominant sponses, marine calcifying , and coccolithophorids. On the ecosystem ⋅ biological carbon level these responses influence phytoplankton species composition and succession, pump, ⋅ favouring algal species which predominantly rely on CO2 utilization. Increased biogeochemical phytoplankton exudation promotes particle aggregation and formation, feedbacks. enhancing the vertical flux of biogenic material. A decrease in calcification may af- fect the competitive advantage of calcifying organisms, with possible impacts on their distribution and abundance. On the biogeochemical level, biological responses to CO2 enrichment and the related changes in carbonate chemistry can strongly alter the cycling of carbon and other bio-active elements in the ocean. Both decreasing calcifi- cation and enhanced carbon overproduction due to release of extracellular carbohy- drates have the potential to increase the CO2 storage capacity of the ocean. Although the significance of such biological responses to CO2 enrichment becomes increasingly evident, our ability to make reliable predictions of their future developments and to quantify their potential ecological and biogeochemical impacts is still in its infancy.

1. Introduction driven by earth’s orbital patterns, the extent of change in The gas composition of the and the cli- climate, CO2 and other climate-relevant gases is control- mate of planet earth are products of the co-evolution of led by a variety of mechanisms, the exact balance of which the biospheric and climatic systems. Over earth’s history is still unknown. Among these mechanisms, biologically- these have evolved gradually as a result of external driven reactions and feedbacks, involving both terrestrial forcings, such as solar irradiance and orbital patterns, and and marine , are bound to play a critical role. internal feedbacks between the atmosphere and biosphere. In the past 200 years, man has become a distinct fac- During its latest phase this co-evolution settled into a tor of the earth system by influencing the , persistent pattern of glacial-interglacial cycles, with at- mainly through the injection of by the µ mospheric CO2 fluctuating between 180 atm in glacial burning of fuels and by changes in land use. The and 280 µatm in interglacial times (Petit et al., 1999). current period, frequently termed the “anthropocene”, has For about the last 20 million years atmospheric pCO2 has no direct analogue in the geological past. Although hu- never exceeded 300 µatm (Berner et al., 1990). While man activities impact most strongly on the carbon cycle, the periodic cycle of glacial-interglacial changes is clearly this has repercussions for the earth system as a whole, since the carbon cycle is coupled with climate, the , nutrient cycles and photosynthesis on land and in * E-mail address: [email protected] the oceans. It is also central to human society as it is di- Copyright © The Oceanographic Society of Japan. rectly linked to the production of energy. Growing world

719 population and changing styles put an increasing pres- sure on energy production and, hence, man-made changes in the carbon cycle proceed at an unprecedented rate. While the impact of human existence on the carbon cycle may have been unintended, attempts to regulate or manage it, however, will require an intentional global effort on an unprecedented scale. No single measure is likely to provide the capacity to stabilize atmospheric CO2 concentration in the presence of continued CO2 emissions at the present-day level. Among the wide range of possi- ble mitigation strategies ocean CO2 sequestration, either through an enhancement of biological or through direct CO2 injection, is receiving increasing at- tention. Obviously, any responsible effort aiming to miti- Fig. 1. Seawater pH and the dissolved carbon dioxide (CO2) 2Ð gate the green-house problem through purposeful CO2 and carbonate ion (CO3 ) concentrations in the surface layer sequestration in the ocean requires a solid understanding of the ocean assuming a “business as usual” (IS92a) an- of marine ecosystem regulation and biogeochemical cy- thropogenic CO2 emission scenario (Houghton et al., 1995). cling. While the study of terrestrial ecosystem responses Dashed lines represent the predicted changes in carbonate chemistry if CO emissions are reduced according to the to man-made environmental changes, including CO2 en- 2 richment, has been a topic of intense research over more Kyoto Protocol (modified after Wolf-Gladrow et al., 1999). than a decade, research of this kind in the marine bio- sphere is developing only recently. The limited informa- tion presently available indicates, however, that marine fect of CO2-related changes in seawater carbonate chem- ecosystems are indeed sensitive to CO2 enrichment. This istry caused by the uptake of anthropogenic CO2 by the paper provides examples of marine planktonic responses surface ocean. to increased seawater CO2 levels and the related changes in seawater carbonate chemistry. While the initial response 2. Effects of CO2 Enrichment on Seawater Carbon- typically occurs at the organismal level, the effects can ate Chemistry carry on to the ecosystem level, which in turn can impact The present rise in atmospheric CO2 and the result- marine biogeochemical cycling. Corresponding changes ing net flux of CO2 into the surface ocean causes a con- in biologically-mediated carbon cycling can have both tinuous change in seawater carbonate chemistry. The dis- positive and negative feedbacks on oceanic CO2 storage solved CO2 reacts with water according to: and air/ CO2 exchange. − How does this relate to deep ocean CO2 sequestra- CO+⇔+ H O H+ HCO tion? Ideally, it should not, at least not on centennial time 22 3 scales. If properly conducted, the sequestered CO would 2 −−⇔++ 2 be cut off from exchange with the surface layer for at HCO3 H CO3 . least several hundred years. Phytoplankton and the bulk of zooplankton thrives in or close to the sunlit surface At a typical surface ocean pH value of 8.2, less than 1% layer of the ocean, i.e. outside the waters which would be of the added CO2 remains as dissolved CO2, while the Ð 3Ð considered for CO2 injection. Hence, the effect rest is converted into HCO3 (ca. 90%) and CO3 (ca. of deep ocean CO2 sequestration on the upper ocean 9%). The reaction of CO2 with water generates one pro- Ð 3Ð plankton would be—if anything—to contribute to miti- ton for each HCO3 and two protons for each CO3 gating adverse effects of a human-induced increase in formed. This acidification causes a shift of the pH-de- Ð 3Ð atmospheric CO2 on marine plankton. The surface ocean, pendent equilibrium between CO2, HCO3 and CO3 to- on the other hand, experiences an unintentional, gradual wards higher CO2 levels and lower carbonate ion con- 3Ð and global CO2 enrichment due to the continuous rise of centrations, [CO3 ]. The net result of CO2 addition there- atmospheric CO2. Changes in atmospheric pCO2 are mir- fore is an increase in the concentration of dissolved CO2, 3Ð rored by corresponding changes in the carbonate system [CO2], a decrease in [CO3 ] and seawater pH (Fig. 1), Ð of surface seawater with a time lag of less than one year and a slight increase in the concentrations of HCO3 and (Zeebe and Wolf-Gladrow, 2001). Responses of the ma- dissolved inorganic carbon, DIC. rine plankton to CO2 enrichment therefore can be expected The recent increase in atmospheric CO2 from a pre- to occur in phase with the present increase in atmospheric industrial level of 280 µatm to the present level of 370 µ CO2. The focus of this paper will therefore be on the ef- atm has decreased surface ocean pH values by approxi-

720 U. Riebesell µ mately 0.12 units. At atmospheric CO2 levels of 700 atm, as expected for the end of this century in a “business as usual” scenario (IS92a, Houghton et al., 1995, 2001), seawater pH will decrease by an additional 0.3 units. While the concentration of dissolved CO2 will have tri- pled by this time, the carbonate ion concentration will decrease by nearly 50%. The projected pH shift covers the entire range of pH variations between 7.7Ð8.3 pres- ently observed in open ocean surface waters. The pro- 3Ð jected increase in [CO2] and decrease in [CO3 ] is out- side the natural range of the past 20 Million years. Changes in surface ocean carbonate chemistry caused by the present rise in atmospheric CO2 are slow and mod- est compared to those occurring in the vicinity of CO2 injection plumes. Depending on the method of injection and the surface area of the hydrate formed, seawater pH in close vicinity of the injected CO2 can decrease by as much 2Ð3 pH units (Brewer et al., 2000). With the for- Fig. 2. Photosynthesis of phytoplankton species differs with mation of a thin hydrate film after slow injection of liq- respect to CO2 sensitivity: While most species (here uid CO2, on the other hand, pH values became indistin- Skeletonema costatum and Phaeocystis globosa) are at or guishable from the in situ background level. While these close to CO2 saturation at present day CO2 levels (8Ð20 short-term changes in seawater chemistry occur on very µmol LÐ1), such as Emiliania huxleyi have small scale, from an impact assessment point of view the comparatively low affinities for inorganic carbon and ap- longer-term and larger-scale effects of CO injection, in- pear to be carbon-limited in today’s ocean. This raises the 2 possibility that coccolithophores may benefit directly from cluding the risk of re-surfacing of sequestered CO2, need the present increase in atmospheric CO2. The range in half- to be considered. µ Ð1 saturation concentrations (K1/2; in mol L ) for photosyn- Following sections outline potential effects of CO2 thesis shown here reflects the degree of regulation as a func- enrichment and the related changes in seawater carbon- tion of pCO2 during growth (according to Rost et al., 2003). ate chemistry on the marine phytoplankton from the Highest apparent affinities for CO2 were generally observed organismal (Section 3) to the ecosystem level (Section 4) in cells which were grown under low pCO2. and will give examples of possible implications for ma- rine biogeochemical cycling (Section 5).

3. Effects on the Organismal Level species (Badger et al., 1998). Typical seawater CO2 con- centrations, ranging between 10 and 25 µmol kgÐ1, are 3.1 Photosynthesis therefore insufficient to ensure effective operation of Photosynthesis involves a series of reactions that start RUBISCO carboxylation. To overcome the low CO2 af- with capturing light energy, transferring it into the en- finity of their main carboxylating enzyme, algae have ergy-conserving compounds NADPH and ATP, and using developed mechanisms to actively increase the CO2 con- centration at the site of carboxylation. These include ac- these compounds to fix CO2 in the . Actively Ð growing algae allocate about 50% of recent photosynthate tive uptake of CO2 and HCO3 into the algal cell and/or into the chloroplasts. In concert with active carbon trans- to synthesis, resulting in a competition for Ð port, algae catalyse the conversion between HCO3 and NADPH and ATP between CO2 fixation, transport proc- esses, nitrate reduction and protein formation (Geider and CO2 intra- and extracellularly with the enzyme carbonic MacIntyre, 2001). Thus photosynthesis and downstream anhydrase. Which ever the pathways for this so-called processes leading to cellular growth are primarily light- carbon concentrating mechanism (CCM) may be, its op- dependent processes. Photosynthesis-irradiance response eration requires additional energy. Since marine curves are commonly used to assess the photosynthetic phytoplankton live in an environment in which light (en- performance. ergy) is one of the primary limiting resources, the energy available for active transport of inorganic carbon and other In the dark reaction of photosynthesis CO2 is fixed by the carboxylating enzyme, ribulose-1,5-bisphosphate is often limited. Energy-limitation may be one carboxylase/oxygenase (RUBISCO). RUBISCO uses CO of the reasons why phytoplankton do not rely entirely on 2 the active uptake of inorganic carbon from the abundant as the only carbon substrate and has a half-saturation con- Ð µ Ð1 pool of HCO3 , but are drawing part of their carbon from stant of 20 to 70 mol kg of CO2, depending on the the small and variable pool of CO2.

Effects of CO2 Enrichment on Marine Phytoplankton 721 Fig. 3. Rising CO2 decreases the ratio of calcification to or- ganic carbon production (PIC/POC) in E. huxleyi. The de- crease in PIC/POC is caused by enhanced photosynthetic carbon fixation and reduced or constant calcification. This Fig. 4. Scanning electron microscopy (SEM) photographs of trend is consistent over a range of photon flux densities Emiliania huxleyi (A, C) and Gephyrocapsa oceanica (B, µ Ð2 Ð1 (PFDs; in mol photons m s ), yet declines under severe D) collected from cultures incubated at pCO2 levels of ca. light-limitation (modified after Zondervan et al., 2002). 300 µatm (upper panel) and 780Ð850 µatm (lower panel). Scale bars represent 1 µm. Note the difference in the coccolith structure (including distinct malformations) and in the degree of calcification of cells grown at normal and

Recent studies indicate that dominant phytoplankton elevated CO2 levels (adapted form Riebesell et al., 2000). species differ in their CO2 requirement. Whereas some species preferably use CO2 as a carbon source, others mainly draw their inorganic carbon from the large pool of HCO Ð (e.g. Elzenga et al., 2000). Group-specific dif- 3 coccolithophorids (Fig. 3), and foraminifera (Gattuso et ferences in CO sensitivity also exist in the carbon me- 2 al., 1998; Kleypas et al., 1999; Bijma et al., 1999; tabolism (Fig. 2). Most notably, the photosynthetic car- Riebesell et al., 2000). Diminished calcification in bon fixation rate of all diatom species tested so far and of coccolithophorids was accompanied by an increased pro- the prymnesiophyte Phaeocystis globosa are at or close portion of malformed coccoliths and incomplete to CO -saturation at present day CO levels (Burkhardt 2 2 coccospheres (Fig. 4) in the two bloom-forming species et al., 1999, 2001; Rost et al., 2003). In contrast, the Emiliania huxleyi and Gephyrocapsa oceanica (Riebesell coccolithophorids Emiliania huxleyi and Gephyrocapsa et al., 2000). oceanica are well below saturation at these levels Although the sensitivity of the different groups of (Riebesell et al., 2000; Rost et al., 2003). These findings calcifying organisms to CO -related changes in carbon- suggest large differences in CO -sensitivity between ma- 2 2 ate chemistry is very similar, suggesting a common jor phytoplankton taxonomic groups. CO -sensitive taxa, 2 mechanism for the observed responses in each of these such as the calcifying coccolithophorids, should there- groups, it is not clear yet which is the physiologically fore benefit more from the present increase in atmospheric relevant factor ultimately causing the slow down in bio- CO compared to the non-calcifying diatoms and 2 genic calcification. While the pH value, carbonate ion Phaeocystis. concentration and carbonate saturation state each may directly impact the calcification process, a reasonable 3.2 Calcification representation of the effect of carbonate chemistry on The formation of calcareous is a wide- biologically-mediated CaCO precipitation can be based spread phenomenon in various groups of marine plank- 3 on the carbonate saturation state of seawater, Ω, which is tonic organisms. Their production and subsequent sink- expressed as: ing generates a continuous rain of to the deep ocean and the . CO2-related changes − in seawater carbonate chemistry were recently shown to []Ca2+ × [] CO2 Ω= sw 3 sw affect marine biogenic calcification. A doubling in ∗ Ksp present-day atmospheric CO2 concentrations is predicted to cause a 20Ð40% reduction in biogenic calcification of 2+ 2Ð the predominant calcifying organisms, the corals, where [Ca ]sw and [CO3 ]sw are the calcium and car-

722 U. Riebesell bonate ion concentrations in seawater and Ksp* is the stoi- While compelling evidence for or against such a chiometric product, defined as Ksp* = mechanism is still lacking, it appears that calcification in 2+ × 2Ð 2+ 2Ð [Ca ]sat [CO3 ]sat. [Ca ]sat and [CO3 ]sat refer to the coccolithophores is neither a prerequisite for efficient equilibrium ion concentrations in a seawater solution satu- photosynthesis nor is it particularly effective in mitigat- rated with CaCO3. ing CO2 limitation. This is indicated, for example, by the Concerning the question which is the relevant pa- fact that photosynthesis continues unaltered when calci- rameter determining the sensitivity of biogenic calcifica- fication ceases, such as when cells are grown in calcium- tion to seawater carbonate chemistry, it may help to take free medium (Paasche, 1964). Likewise, non-calcifying a look at the geological past. Recent evidence from fluid cells can photosynthesise as efficient or even more effi- inclusions suggests that calcium concentrations in the ciently than calcifying ones, as indicated by P vs. E rela- Cretaceous were more than twice as high as in the mod- tionships of non-calcifying compared to calcifying strains ern ocean (Horita et al., 2002). As CaCO3 compensation of E. huxleyi (Rost and Riebesell, 2004). Moreover, mass tends to restore the saturation state of the ocean towards spectrometric measurements indicate that non-calcifying Ð CaCO3 saturation, higher calcium concentrations would cells of E. huxleyi are capable of direct uptake of HCO3 Ð correspond to lower carbonate ion concentrations. In spite (Rost and Riebesell, 2004), which implies that HCO3 2Ð of lower expected CO3 concentration, massive accumu- utilisation is not tied to calcification. Further evidence lation of biogenic occurred in the Cretaceous, that calcification is unsuited to prevent CO2 limitation of suggesting that the carbonate saturation state may exert a coccolithophores comes from observations that the rate stronger control on biogenic calcification than any of the of photosynthesis decreases with decreasing CO2 concen- 2Ð other possible candidates, e.g. pH, CO2, or CO3 con- tration despite a concomitant increase in calcification rate centrations. (Riebesell et al., 2000; Zondervan et al., 2002). In es- What effect reduced CaCO3 production has for cal- sence, if supply of CO2 for photosynthesis is indeed a cifying organisms ultimately depends on the role of cal- primary role of calcification, this mechanism is rather cification and calcareous skeletons in the cell inefficient when compared to CO2 concentrating mecha- and ecology of these organisms. Despite intensive re- nisms of non-calcifying phytoplankton such as diatoms search on coccolithophores the function of calcification and Phaeocystis (Burkhardt et al., 2001; Rost et al., 2003). in this group is still not well understood (Young, 1994; Whatever the purpose of calcification in Paasche, 2002). It has been hypothesized that the cell- coccolithophores, continued acidification of surface covering layer of coccoliths, the coccosphere, serves to seawater due to rising atmospheric CO2 will further dete- protect against grazing and/or viral attack and that riorate the chemical conditions for biogenic calcification. coccoliths could bundle and modify the light intercepted Despite a wealth of information on the effect of environ- by the algal cell (Young, 1994). While these hypotheses mental conditions on coccolith production, the mecha- remain speculative, there is some support for the “trash- nism of calcification by coccolithophores is not com- can function” of calcification, whereby CaCO3 precipita- pletely understood. It is too early, therefore, to make any tion serves as a mechanism to facilitate the use of bicar- predictions regarding the physiological or ecological con- Ð bonate in photosynthesis. Provided that HCO3 is the car- sequences of a CO2-related slow down in biogenic calci- bon source used for calcification, one possible benefit for fication. Obviously, a better mechanistic understanding photosynthesis could be the release of CO2 or protons in of the process of biogenic calcification will help to better the course of calcification according to the following re- constrain the effects of global changes, including changes actions: in temperature and light availability, on bio-calcification.

− Ca2+ +→2 HCO CaCO++ CO H O 3.3 Elemental composition 3322 One of the few canonical numbers in marine biogeochemical sciences is the , the ratio or of C:N:P in marine particulate matter. When Redfield dis- covered an unexpected congruence of this value in nu- − 2+ +→ + + Ca HCO33 CaCO H . merous regions of the world’s ocean (Redfield et al., 1963), it soon became one of the cornerstones in biologi- Either CO2 could be used directly in photosynthesis or cal oceanography and geochemistry, commonly used to Ð protons could be used in the conversion of HCO3 to CO2. infer about the large-scale operation of the marine In either case this would provide the calcifying cell with biogeochemical system. Recent studies have challenged Ð a mechanism to access HCO3 , the largest pool of inor- the concept of a constant Redfield ratio and have high- ganic carbon in seawater, for photosynthetic carbon fixa- lighted the importance to better constrain the factors de- tion. termining phytoplankton stoichiometry (for review see

Effects of CO2 Enrichment on Marine Phytoplankton 723 Sterner and Elser, 2002). Phytoplankton indeed show a molar C:N:P ratio much higher than the Redfield ratio high degree of variability in their stoichiometric compo- (Engel and Passow, 2001). CO2 sensitivity of TEP pro- sition C:N:P. While a large body of literature exists on duction may therefore cause significant shifts in elemen- the role of nutrients, light and temperature on algal stoi- tal composition of particulate matter towards higher than chiometry (Sterner and Elser, 2002), comparatively little Redfield ratios. is known about the effects of inorganic carbon and CO2 availability on phytoplankton elemental composition. 4. Effects on the Ecosystem Level Initial studies by Burkhardt and Riebesell (1997) and The ecological success of a phytoplankton species Burkhardt et al. (1999) showed considerable changes in is ultimately determined by its ability to optimise the bal- C:N:P composition in response to increasing pCO2 but ance between growth and loss processes. While the former also revealed large species-specific differences. Whereas is largely controlled by the availability and optimal utili- in some microalgae cellular C:N and C:P increased with sation of essential resources, such as light and nutrients, increasing pCO2, other species responded with lower the latter includes factors such as cell sinking, cell mor- C:nutrient ratios under increased CO2 availability. More- tality due to grazing, viral and parasite infection, as well over, algal C:N:P mainly responded to altered CO2 at as autolysis. Any investment successfully reducing mor- pCO2 levels lower than current values and remained more tality therefore weighs equally strong as cellular meas- or less stable at higher than present pCO2 values. It should ures capable of increasing cell growth by the same mag- be noted, however, that these experiments were conducted nitude. Although the role of CaCO3 production in under nutrient replete conditions. Strongest deviations coccolithophores is not clear, reduced calcification is from Redfield proportions typically occur in nutrient lim- likely to affect both resource utilization and cellular pro- ited phytoplankton and under conditions of unbalanced tection with possible adverse effects on the competitive nutrient supply. Clearly, more work is needed to further fitness of this group. Although it would be premature to examine the effect of CO2 availability on phytoplankton speculate on possible implications of reduced calcifica- stoichiometry. tion for distribution and productivity, a Research on microalgal stoichiometry has commonly likely scenario would be a shift in the relative distribu- focussed on the cellular composition of phytoplankton. tion and productivity of the calcareous primary produc- Although it is well-recognized that the proportion of pri- ers relative to their siliceous counterpart, the diatoms. mary produced lost from the cell through Both groups are important components of the pelagic food exudation can be substantial, particularly under nutrient- web and major drivers of biogeochemical cycling in the limitation, this fraction of is fre- ocean. Due to their specific roles in plankton ecosystem quently neglected in biogeochemical analyses. As dis- regulation, a shift in the ratio of coccolithophores to dia- solved organic matter can be subject to rapid bacterial toms is likely to also affect higher trophic levels. A ba- degradation, this material is thought to contribute little sin-wide shift in the opal:carbonate ratio of sedimenting to vertical carbon transport in the ocean. However, re- particles has in fact occurred across the entire North At- cent work demonstrated the spontaneous assembly of dis- lantic and is attributed to large-scale changes in climatic solved organic matter into polymer gels (Chin et al., forcing (Antia et al., 2001). The observed steady decrease 1998). Colloidal organic matter is an important precur- in this ratio since the early eighties may reflect an in- sor for the formation of transparent exopolymer particles crease in the abundance and productivity of (TEP) which are shown to accelerate particle aggrega- coccolithophores relative to diatoms. tion and thereby enhance vertical particle flux (Passow, To examine the direct effect of CO2 enrichment on 2002). This process may therefore provide an efficient the ecosystem level, CO2 perturbation experiments were pathway to channel dissolved and colloidal organic mat- conducted in outdoor mesocosms with natural plankton ter into the particulate pool. Analyses on the variability communities, in Raunafjorden south of Bergen, Norway. of Redfield proportions should therefore include dissolved Nine 11 m3 enclosures moored to a floating raft were aer- organic components. ated in triplicate with normal air, CO2-enriched and CO2- µ That the production of dissolved organic matter may depleted air to achieve pCO2 levels of 190 atm, 370 µ µ be sensitive to CO2 availability is indicated in a recent atm, and 710 atm, simulating glacial, present day, and study by Engel (2002), showing that in a natural plank- predicted year 2100 conditions (assuming IPCC scenario ton assemblage TEP production increases with increas- 92a; Houghton et al., 1995), respectively (Fig. 5). The ing pCO2. A similar response was also observed in mono- enclosures were covered with gas tight tents made of specific cultures of the diatom Thalassiosira weissflogii ETFE foil (Foiltec, Bremen, Germany), which allowed and the coccolithophorid Emiliania huxleyi (Heemann, for 95% light transmission of the complete spectrum of 2002). Since transparent exopolymer particles primarily sunlight. To allow the seawater carbonate system to freely form from exuded polymeric carbohydrates they have a change in response to biological activities, aeration of the

724 U. Riebesell also observed with respect to the phytoplankton compo- sition. Whereas under glacial CO2 conditions diatoms dominated at the end of the bloom, the devel- oping under CO2 conditions as expected for the end of this century was dominated by Emiliania huxleyi (Huonic et al., unpubl.). These findings are consistent with ob- served differences in carbon acquisition mechanisms be- tween diatoms and coccolithophorids as outlined above (Subsection 3.1). In principle, coccolithophores may benefit from the present increase in atmospheric pCO2 and related changes in seawater carbonate chemistry. At pre-industrial CO2 levels, rates of photosynthetic carbon fixation of E. huxleyi and Gephyrocapsa oceanica are well below CO2 Data logger saturation. In comparison, photosynthesis of other bloom-

CO2-absorber Air CO2 flow meter forming phytoplankton groups such as diatoms and analysis air-compressor Phaeocystis are less CO2-sensitive due to their efficient CO 2 CO2 mixing-chamber Air air-compressor CCMs (Rost et al., 2003). Although under natural condi- compressor tions CO2 limitation is likely to be of minor importance Air for the proliferation of E. huxleyi compared to other lim- air-compressor iting resources and loss processes, increasing CO2 avail- ability may improve the overall resource utilisation of E. huxleyi and possibly of other fast-growing coccolithophore species. If this provides an ecological advantage for coccolithophores, rising atmospheric CO2 could potentially increase the contribution of calcifying Enclosure 7 Enclosure 8 Enclosure 9 Enclosure 1 Enclosure 2 Enclosure 3 Enclosure 4 Enclosure 5 Enclosure 6 phytoplankton to overall primary production. Fig. 5. Upper panel: Mesocosm facilities of the University of CO2 effects on the taxonomic composition and nu- Bergen Large-Scale-Facilities in the Raunefjorden, 60.3°N, trient utilization were also observed in a natural 5.2°E. Shown are the nine enclosures covered by tents made phytoplankton assemblage by Tortell et al. (2002). A de- of gas-tight ETFE foil. Lower panel: Sketch of the aeration crease in the abundance of diatoms and an increase in systems for CO2 manipulation of the seawater inside the that of Phaeocystis occurred when pCO2 levels were mesocosms. Ambient air was pumped either directly to the µ µ raised from 150 atm to 750 atm. This CO2-dependent mesocosms (4Ð6), enriched with CO2 in a mixing chamber shift was associated with a significant change in nutrient (1Ð3), or depleted in CO2 through adsorption onto Na2CO3 utilization, with higher ratios of nitrate: and platelets (7Ð9). nitrate: consumption by phytoplankton in the low CO2 treatment. Despite these changes, total biomass and primary productivity did not differ significantly be- enclosed water column was discontinued after target CO2 tween CO2 treatments. This and the mesocosm study de- values were achieved. At this point the nutrient depleted scribed above indicate that CO2 sensitivity of microalgae water was fertilized with nitrate and phosphate to initiate is not limited to species relying entirely on CO2 utiliza- the development of a phytoplankton bloom. Aeration of tion. Even for species capable to access the large pool of Ð Ð the atmosphere underneath the tents at target CO2 levels HCO3 , either through direct uptake of HCO3 or its con- continued throughout the investigation. version to CO2 via carbonic anhydrase, increased CO2 During the course of this study the development and availability can reduce the allocation of resources into decline of a bloom consisting of a mixed phytoplankton carbon acquisition. In cases of resource (energy and/or community was followed. Significantly higher net com- nutrient) limitation, the ability to regulate resource allo- munity production (as measured by DIC drawdown) was cation accordingly could provide these species a competi- observed under elevated CO2 levels during the build-up tive advantage over those incapable to regulate in response the bloom (Bellerby et al., unpubl.). CO2-related differ- to changes in CO2 availability (Rost et al., 2003). ences in primary production continued after nutrient ex- haustion, leading to higher production of transparent 5. Effects on the Biogeochemical Level exopolymer particles (TEP) under high CO2 conditions Despite a high degree of structural complexity, the (Engel et al., unpubl.). CO2-dependent differences were energy flow and elemental cycling of many ecosystems

Effects of CO2 Enrichment on Marine Phytoplankton 725 the organic carbon pump, thereby causes a net draw down of CO2 from the atmosphere into the ocean. In contrast, the production and export of calcium carbonate not only binds dissolved carbon into particulate carbon and thereby reduces total dissolved inorganic carbon, it also lowers seawater and changes the equilibrium between the different forms of dissolved inorganic carbon, caus- ing a net release of CO2 to the atmosphere. Due to its counteracting effect on CO2 flux, this process is often referred to as the carbonate counter pump. The relative strength of the two biological carbon pumps, represented by the so-called rain ratio (the ratio of particulate inor- ganic to organic carbon in exported biogenic matter), determines to a large extent the flux of CO2 between the Fig. 6. Changes in the concentrations of DIC, total alkalinity, surface ocean and the overlying atmosphere. and CO2 as a result of calcification at pre-industrial times But how can a process transporting inorganic car- (left vectors) and in year 2100 (right vectors). Numbers at bon from the surface to the deep ocean release CO to the the vectors are relative values. The difference in the effect 2 atmosphere? The formation of one unit of calcium car- of calcification on seawater carbonate chemistry in the two bonate according to scenarios results from a CO2-related change in the seawater buffer capacity (see text for details, modified after Zondervan et al., 2001). 2+ +→2− () Ca CO3 CaCO3 1

lowers the dissolved inorganic carbon (DIC) concentra- are dominated by a comparatively small number of spe- tion, with cies. A first step in understanding possible consequences of environmental change on ecosystem functioning, there- −− DIC =[] CO+ [] HCO+ [] CO2 ()2 fore, is to determine the relevant responses of these key 233 species. This also holds true for the marine pelagic sys- tem, the largest ecosystem on our planet. While the base by one unit. Due to its double negative charge the con- of its complex food web is formed by more than 5000 centration of carbonate ions carries the factor 2 in the species of marine phytoplankton, only a few taxonomic expression of total alkalinity (TAlk), with groups of phytoplankton, and within these groups a rela- −− − − tively small number of species, are responsible for most TAlk= [] HCO+ 23[] CO2++ [] B() OH+ [] OH− [] H . () of the system’s primary production, the energy transfer 33 4 to higher trophic levels and the vertical export of bio- genic material to the deep ocean. These key species can Thus, the precipitation of one unit of calcium carbonate be further distinguished into so-called “functional lowers seawater alkalinity by two units. How this affects groups”, i.e. phytoplankton building siliceous or calcare- the concentration of dissolved CO2 is best illustrated, fol- ous shells, such as the diatoms and coccolithophores, re- lowing Zondervan et al. (2001), by plotting CO2 concen- spectively, flagellates forming organic plates or mucilagi- tration as a function of DIC and TAlk (Fig. 7). Starting at Ð1 nous colonies, and cyanobacteria fixing atmospheric ni- typical surface ocean conditions of DIC = 2.0 mmol kg Ð1 trogen. Each of these functional groups has a distinct ef- and TAlk = 2.3 mmol kg (beginning of diagonal vector fect on elemental fluxes, both between the surface and on left side), the corresponding CO2 concentration, [CO2], Ð1 deep ocean as well as the overlying atmosphere. is 10.5 µmol kg (assuming T = 15°C, S = 35). Precipi- µ Ð1 With regard to the oceanic carbon cycle, the effect tating 50 mol kg of CaCO3 lowers DIC and TAlk by Ð1 of calcifying plankton, including coccolithophores as the 0.05 and 0.1 mmol kg , respectively. With the new DIC Ð1 Ð1 dominant calcifying phytoplankton, differs greatly from and TAlk values of 1.95 mmol kg and 2.2 mmol kg that of other primary producers. The fixation of inorganic (end of diagonal vector), the corresponding CO2 concen- Ð1 carbon via photosynthesis in the sunlit upper mixed layer tration now is 12.4 µmol kg . Assuming that the seawater and the vertical export of part of this organic material initially was in equilibrium with the atmosphere with re- spect to CO , it is now CO over-saturated. To restore cause a draw down of CO2 in the surface ocean. 2 2 Remineralisation of the particulate organic carbon on its equilibrium, 0.63 units of CO2 need to be released for way to depth releases organically-bound CO , which then each unit of inorganic carbon precipitated via calcifica- 2 µ Ð1 accumulates in deeper layers (Fig. 6). This process, termed tion. In our example, 50 mol kg CaCO3 production

726 U. Riebesell is often correlated with glacial-interglacial transitions, indicating a predominance of coccolithophores during interglacial periods (McIntyre et al., 1972; Henrich, 1989). The presumably lower contribution of coccolithophores relative to non-calcifying phytoplankton may have contributed to the lower atmospheric CO2 lev- els in glacial times (Harrison, 2000; Ridgwell et al., 2002). Estimates of global calcium carbonate production range from 0.64 to 2 Gt C per year (e.g. Milliman and Droxler, 1996). Recent estimates of global annual ma- rine primary production are between 40 and 50 Gt C an- nually (Antoine et al., 1996), of which about 10 Gt C are exported to the deep sea. The estimated export ratio of Fig. 7. The biological carbon pumps: Photosynthetic produc- CaCO3 to particulate organic carbon (rain ratio) is there- tion of organic matter in the surface layer and its subse- fore relatively high, ranging from 0.17 to 0.4 (see Holligan quent transport to depth, termed organic carbon pump, gen- and Robertson, 1996 for review). Since the export of erates a CO2 sink in the ocean. In contrast, calcium carbon- CaCO3 and POC have opposite effects on the surface ate production and its transport to depth, referred to as the ocean CO , a change in the rain ratio af- carbonate counter pump, releases CO in the surface layer. 2 2 fects the partitioning of CO between ocean and atmos- The relative strengths of these two processes (rain ratio) 2 largely determine the biologically-mediated ocean atmos- phere. It has been suggested that the rain ratio is not con- stant through time and is an important factor in the regu- phere CO2 exchange. lation of global climate (Archer and Maier-Reimer, 1994). Changes in marine production and phytoplankton species composition and succession will also impact other would require a degassing of 32 µmol kgÐ1 of CO in or- 2 biogeochemical cycles, such as the , opal, and der to maintain CO equilibrium between our parcel of 2 sulphur cycles, which in turn is bound to feedback on seawater and the overlying atmosphere. Due to the de- climate. Despite the potential importance of global crease in the buffer capacity with increasing [CO ] (de- 2 change-induced biogeochemical feedback, our under- creasing pH) of seawater, the ratio of CO released per 2 standing of these processes is still in its infancy. It is now carbonate precipitated increases with rising atmospheric becoming increasingly clear, however, that the assump- CO (Frankignoulle et al., 1994). Under conditions ex- 2 tion of a constant oceanic biosphere, implicitly used in pected for the year 2100 (see Fig. 1), the surface ocean many assessments of future global change, is no longer equilibrium CO concentration would be ca. 27 2 viable. µmol kgÐ1. Under these conditions, precipitation of 50 µmol kgÐ1 CaCO would release ca. 40 µmol kgÐ1 of CO , 3 2 6. Outlook corresponding to 0.79 units of CO for each unit of CaCO 2 3 In view of the rapid changes in environmental con- (right vectors). If global calcification were to remain con- ditions presently occurring on a global scale, a major chal- stant over this time, increased calcification-induced CO 2 lenge in earth system sciences is to predict biospheric release results in a positive feedback to rising atmospheric responses to global change. Any attempt to forecast bio- CO (Zondervan et al., 2001). With the observed decrease 2 logically-mediated changes in marine biogeochemical of bio-calcification with increasing pCO this positive 2 cycling critically depends on our ability to explain the feedback turns into a negative one, leading to an increase distribution and succession of the dominant plankton in the CO storage capacity of the surface ocean (Riebesell 2 groups in relation to biotic and abiotic environmental et al., 2000). conditions. The importance of a fundamental understand- Obviously, the ratio of coccolithophore calcification ing of marine ecosystem regulation becomes even more to organic matter production, but even more so the ratio pressing in view of recent considerations to manage or of calcareous to non-calcareous primary production, manipulate oceanic CO sequestration. While the ocean’s strongly determine the relative strengths of the two bio- 2 capacity to store anthropogenic CO is immense, its sen- logical carbon pumps. CaCO may also act as a “ballast” 2 3 sitivity to related changes in environmental conditions is that increases the transfer efficiency of POC from likely to be high. In contrast to the terrestrial biosphere, the surface to the deep sea (Armstrong et al., 2002; Klaas marine ecosystems have evolved in a comparatively ho- and Archer, 2002). The presence of coccoliths could thus mogenous environment under conditions of relative sta- enhance the sedimentation of POC such as in faecal pel- bility over evolutionary timescales. Even subtle changes lets (Buitenhuis et al., 1996). On geological time-scales in the environmental conditions may therefore have strong variation in coccolith abundance in the sedimentary record

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