Abstract
Response of phytoplankton to increasing CO2 in seawater in terms of physiology and ecology is key to predicting changes in marine ecosystems. However, responses of natural plankton communities especially in the open ocean to higher CO2 levels have not been fully examined. We conducted CO2 manipulation experiments in the Bering Sea and the central subarctic Pacific, known as high nutrient and low chlorophyll regions, in summer 2007 to investigate the response of organic matter production in iron-deficient plankton communities to CO2 increases. During the 14-day incubations of surface waters with natural plankton assemblages in microcosms under multiple pCO2 levels, the dynamics of particulate organic carbon (POC) and nitrogen (PN), and dissolved organic carbon (DOC) and phosphorus (DOP) were examined with the plankton community compositions. In the Bering site, net production of POC, PN, and DOP relative to net chlorophyll-a production decreased with increasing pCO2. While net produced POC:PN did not show any CO2-related variations, net produced DOC:DOP increased with increasing pCO2. On the other hand, no apparent trends for these parameters were observed in the Pacific site. The contrasting results observed were probably due to the different plankton community compositions between the two sites, with plankton biomass dominated by large-sized diatoms in the Bering Sea versus ultra-eukaryotes in the Pacific Ocean. We conclude that the quantity and quality of the production of particulate and dissolved organic matter may be altered under future elevated CO2 environments in some iron-deficient ecosystems, while the impacts may be negligible in some systems.
Similar content being viewed by others
References
Aguilar-Islas A, Hurst M, Buck K, Sohst B, Smith G, Lohan M, Bruland K (2007) Micro- and macronutrients in the southeastern Bering Sea: insight into iron-replete and iron-depleted regimes. Prog Oceanogr 73(2):99–126. doi:10.1016/j.pocean.2006.12.002
Aoyama M, Becker S, Dai M, Daimon H, Gordon LI, Kasai H, Kerouel R, Kress N, Masten D, Murata A, Nagai N, Ogawa H, Ota H, Saito H, Saito K, Shimizu T, Takano H, Tsuda A, Yokouchi K, Youenou A (2007) Recent comparability of oceanographic nutrients data: results of a 2003 intercomparison exercise using reference materials. Anal Sci 23(9):1151–1154
Biswas H, Gadi S, Ramana V, Bharathi M, Priyan R, Manjari D, Kumar M (2012) Enhanced abundance of tintinnids under elevated CO2 level from coastal Bay of Bengal. Biodivers Conserv 21(5):1309–1326. doi:10.1007/s10531-011-0209-7
Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, Buesseler KO, Coale KH, Cullen JJ, de Baar HJ, Follows M, Harvey M, Lancelot C, Levasseur M, Owens NP, Pollard R, Rivkin RB, Sarmiento J, Schoemann V, Smetacek V, Takeda S, Tsuda A, Turner S, Watson AJ (2007) Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315(5812):612–617. doi:10.1126/science.1131669
Breitbarth E, Bellerby RJ, Neill CC, Ardelan MV, Meyerh’Ufer M, Z’Ullner E, Croot PL, Riebesell U (2010) Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7(3):1065–1073. doi:10.5194/bg-7-1065-2010
Brzezinski MA (1985) The Si: C: N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J Phycol 21(3):347–357. doi:10.1111/j.0022-3646.1985.00347.x
Bucciarelli E, Pondaven P, Sarthou G (2010) Effects of an iron-light co-limitation on the elemental composition (Si, C, N) of the marine diatoms Thalassiosira oceanica and Ditylum brightwellii. Biogeosciences 7(2):657–669. doi:10.5194/bg-7-657-2010
Buitenhuis ET, Geider RJ (2010) A model of phytoplankton acclimation to iron-light colimitation. Limnol Oceanogr 55(2):714–724
Chierici M, Fransson A, Nojiri Y (2006) Biogeochemical processes as drivers of surface fCO2 in contrasting provinces in the subarctic North Pacific Ocean. Glob Biogeochem Cycles 20: GB1009. doi:10.1029/2004GB002356
Culberson CH, Pytkowicz RM, Hawley JE (1970) Seawater alkalinity determination by the pH method. J Mar Res 28:15–21
Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2H2(g) = Ag(s) + HCl(aq), and and the standard acidity constant of the ion HSO4 − in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodynamics 22(2):113–127. doi:10.1016/0021-9614(90)90074-z
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34(10):1733–1743
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Res 1(1):169–192. doi:10.1146/annurev.marine.010908.163834
Endo H, Yoshimura T, Kataoka T, Suzuki K (2013) Effects of CO2 and iron availability on phytoplankton and eubacterial community compositions in the northwest subarctic Pacific. J Exp Mar Biol Ecol 439:160–175. doi:10.1016/j.jembe.2012.11.003
Feng Y, Hare CE, Leblanc K, Rose JM, Zhang Y, DiTullio GR, Lee PA, Wilhelm SW, Rowe JM, Sun J, Nemcek N, Gueguen C, Passow U, Benner I, Brown C, Hutchins DA (2009) Effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Mar Ecol Prog Ser 388:13–25
Feng Y, Hare CE, Rose JM, Handy SM, DiTullio GR, Lee PA, Smith WO Jr, Peloquin J, Tozzi S, Sun J, Zhang Y, Dunbar RB, Long MC, Sohst B, Lohan M, Hutchins DA (2010) Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep Sea Res I 57(3):368–383
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281(5374):237–240. doi:10.1126/science.281.5374.237
Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64(9):3352–3358
Gao K, Xu J, Gao G, Li Y, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Hader D-P, Li W, Xu K, Liu N, Riebesell U (2012) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Clim Change 2(7):519–523. doi:10.1038/nclimate1507
Geider RJ (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 106:1–34
Geider RJ, La Roche J (1994) The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth Res 39(3):275–301. doi:10.1007/bf00014588
Gifford DJ, Caron DA (2000) Sampling, preservation, enumeration and biomass of marine protozooplankton. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES Zooplankton Methodology Manual. Academic, London, pp 193–221. doi:10.1016/b978-012327645-2/50006-2
Grossart HP, Allgaier M, Passow U, Riebesell U (2006) Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol Oceanogr 51(1):1–11
Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of Seawater Analysis, 3rd edn. Wiley-VCH, Weinheim, pp 159–228. doi:10.1002/9783527613984.ch10
Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee PA, Riseman S, Hutchins DA (2007) Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Mar Ecol Prog Ser 352:9–16
Harrison PJ, Whitney FA, Tsuda A, Saito H, Tadokoro K (2004) Nutrient and plankton dynamics in the NE and NW gyres of the subarctic Pacific Ocean. J Oceanogr 60(1):93–117
Holmes RM, Aminot A, Kerouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56(10):1801–1808
Hopkinson BM, Xu Y, Shi D, McGinn PJ, Morel FMM (2010) The effect of CO2 on the photosynthetic physiology of phytoplankton in the Gulf of Alaska. Limnol Oceanogr 55(5):2011–2024
Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Natl Acad Sci USA 108(10):3830–3837. doi:10.1073/pnas.1018062108
Hutchins DA, Mulholland MR, Fu F (2009) Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22(4):128–145
Johnson KM, King AE, Sieburth JM (1985) Coulometric TCO2 analyses for marine studies; an introduction. Mar Chem 16(1):61–82. doi:10.1016/0304-4203(85)90028-3
Kim JM, Lee K, Shin K, Kang JH, Lee HW, Kim M, Jang PG, Jang MC (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnol Oceanogr 51(4):1629–1636
Langer G, Nehrke G, Probert I, Ly J, Ziveri P (2009) Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6(11):2637–2646
Lee K, Tong LT, Millero FJ, Sabine CL, Dickson AG, Goyet C, Park GH, Wanninkhof R, Feely RA, Key RM (2006) Global relationships of total alkalinity with salinity and temperature in surface waters of the world’s oceans. Geophys Res Lett 33(19):L19605. doi:10.1029/2006GL027207
Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10(12):1170–1181. doi:10.1111/j.1461-0248.2007.01117.x
Liu H, Suzuki K, Saino T (2002) Phytoplankton growth and microzooplankton grazing in the subarctic Pacific Ocean and the Bering Sea during summer 1999. Deep Sea Res I 49(2):363–375. doi:10.1016/s0967-0637(01)00056-5
Mahowald NM, Engelstaedter S, Luo C, Sealy A, Artaxo P, Benitez-Nelson C, Bonnet S, Chen Y, Chuang PY, Cohen DD, Dulac F, Herut B, Johansen AM, Kubilay N, Losno R, Maenhaut W, Paytan A, Prospero JM, Shank LM, Siefert RL (2009) Atmospheric iron deposition: global distribution, variability, and human perturbations. Annu Rev Mar Res 1(1):245–278. doi:10.1146/annurev.marine.010908.163727
Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18(6):897–907
Millero FJ, Woosley R, DiTrolio B, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22(4):72–85
Mochizuki M, Shiga N, Saito M, Imai K, Nojiri Y (2002) Seasonal changes in nutrients, chlorophyll a and the phytoplankton assemblage of the western subarctic gyre in the Pacific Ocean. Deep-Sea Res II 49(24–25):5421–5439. doi:10.1016/s0967-0645(02)00209-6
Moore JK, Lindsay K, Doney SC, Long MC, Misumi K (2013) Marine ecosystem dynamics and biogeochemical cycling in the community earth system model [CESM1(BGC)]: comparison of the 1990s with the 2090s under the RCP4.5 and RCP8.5 Scenarios. J Clim. doi:10.1175/JCLI-D-12-00566.1
Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchmann DL (ed) Microbial Ecology of the Oceans. Wiley-Liss, New York, pp 121–152
Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55(3–4):287–333. doi:10.1016/s0079-6611(02)00138-6
Pierrot D, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee
Price NM (2005) The elemental stoichiometry and composition of an iron-limited diatom. Limnol Oceanogr 50(4):1159–1171
Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34(6):1097–1103
Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of seawater. In: Hill MN (ed) The Sea, vol 2. Wiley, New York, pp 26–77
Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Res 3:291–315
Ridal JJ, Moore RM (1990) A re-examination of the measurement of dissolved organic phosphorus in seawater. Mar Chem 29:19–31. doi:10.1016/0304-4203(90)90003-u
Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361(6409):249–251
Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhofer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zollner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450(7169):545–548. doi:10.1038/nature06267
Roberts K, Granum E, Leegood R, Raven J (2007) Carbon acquisition by diatoms. Photosynth Res 93(1–3):79–88. doi:10.1007/s11120-007-9172-2
Rose JM, Feng Y, Gobler CJ, Gutierrez R, Hare CE, Leblanc K, Hutchins DA (2009) Effects of increased pCO2 and temperature on the North Atlantic spring bloom. II. Microzooplankton abundance and grazing. Mar Ecol Prog Ser 388:27–40
Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science 327(5966):676–679
Strathmann RR (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol Oceanogr 12:411–418
Strickland JDH (1960) Measuring the production of marine phytoplankton. Fish Res Bd Can Bull 122:1–172
Sugie K, Yoshimura T (2013) Effects of pCO2 and iron on the elemental composition and cell geometry of the marine diatom Pseudo-nitzschia pseudodelicatissima (Bacillariophyceae). J Phycol 49(3):475–488. doi:10.1111/jpy.12054
Sunda WG (2010) Iron and the carbon pump. Science 327(5966):654–655. doi:10.1126/science.1186151
Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N. N-dimethylformamide. J Oceanogr 46(4):190–194
Suzuki K, Handa N, Nishida T, Wong CS (1997) Estimation of phytoplankton succession in a fertilized mesocosm during summer using high-performance liquid chromatographic analysis of pigments. J Exp Mar Biol Ecol 214(1–2):1–17. doi:10.1016/s0022-0981(97)00003-8
Suzuki K, Liu H, Saino T, Obata H, Takano M, Okamura K, Sohrin Y, Fujishima Y (2002) East-west gradients in the photosynthetic potential of phytoplankton and iron concentration in the subarctic Pacific Ocean during early summer. Limnol Oceanogr 47(6):1581–1594
Suzuki K, Hinuma A, Saito H, Kiyosawa H, Liu H, Saino T, Tsuda A (2005) Responses of phytoplankton and heterotrophic bacteria in the northwest subarctic Pacific to in situ iron fertilization as estimated by HPLC pigment analysis and flow cytometry. Prog Oceanogr 64(2–4):167–187. doi:10.1016/j.pocean.2005.02.007
Takata H, Kuma K, Iwade S, Isoda Y, Kuroda H, Senjyu T (2005) Comparative vertical distributions of iron in the Japan Sea, the Bering Sea, and the western North Pacific Ocean. J Geophys Res 110(7):1–10
Takeda S (1998) Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393(6687):774–777
Takeda S (2011) Iron and phytoplankton growth in the subarctic North Pacific. Aqua-BioSci Monogr 4(2):41–93. doi:10.5047/absm.2011.00402.0041
Taucher J, Schulz KG, Dittmar T, Sommer U, Oschlies A, Riebesell U (2012) Enhanced carbon overconsumption in response to increasing temperatures during a mesocosm experiment. Biogeosciences 9:3531–3545. doi:10.5194/bg-9-3531-2012
Taylor AH, Geider RJ, Gilbert FJH (1997) Seasonal and latitudinal dependencies of phytoplankton carbon-to-chlorophyll a ratios: results of a modelling study. Mar Ecol Prog Ser 152:51–66
Taylor BW, Keep CF, Hall RO, Koch BJ, Tronstad LM, Flecker AS, Ulseth AJ (2007) Improving the fluorometric ammonium method: matrix effects, background fluorescence, and standard additions. J North Am Benthol Soc 26(2):167–177. doi:10.1899/0887-3593
Thingstad TF, Bellerby RGJ, Bratbak G, Borsheim KY, Egge JK, Heldal M, Larsen A, Neill C, Nejstgaard J, Norland S, Sandaa RA, Skjoldal EF, Tanaka T, Thyrhaug R, Topper B (2008) Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455(7211):387–390. doi:10.1038/nature07235
Tomas CR (1997) Identifying Marine Phytoplankton. Academic, San Diego
Tortell PD, Payne CD, Li Y, Trimborn S, Rost B, Smith WO, Riesselman C, Dunbar RB, Sedwick P, DiTullio GR (2008) CO2 sensitivity of Southern Ocean phytoplankton. Geophys Res Lett 35 (L04605). doi:10.1029/2007GL032583
Trimborn S, Wolf-Gladrow D, Richter KU, Rost B (2009) The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms. J Exp Mar Biol Ecol 376(1):26–36
Uye S-I, Nagano N, Tamaki H (1996) Geographical and seasonal variations in abundance, biomass and estimated production rates of microzooplankton in the Inland Sea of Japan. J Oceanogr 52(6):689–703. doi:10.1007/bf02239460
Verity PG, Lagdon C (1984) Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. J Plank Res 6(5):859–868. doi:10.1093/plankt/6.5.859
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39(8):1985–1992
Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7(9):2915–2923. doi:10.5194/bg-7-2915-2010
Yamada N, Suzumura M (2010) Effects of seawater acidification on hydrolytic enzyme activities. J Oceanogr 66(2):233–241. doi:10.1007/s10872-010-0021-0
Yoshimura T, Nishioka J, Nakatsuka T (2010a) Iron nutritional status of the phytoplankton assemblage in the Okhotsk Sea during summer. Deep-Sea Res I 57(11):1454–1464. doi:10.1016/j.dsr.2010.08.003
Yoshimura T, Nishioka J, Suzuki K, Hattori H, Kiyosawa H, Watanabe YW (2010b) Impacts of elevated CO2 on organic carbon dynamics in nutrient depleted Okhotsk Sea surface waters. J Exp Mar Biol Ecol 395(1–2):191–198. doi:10.1016/j.jembe.2010.09.001
Zubkov MV, Sleigh MA, Tarran GA, Burkill PH, Leakey RJG (1998) Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S. Deep-Sea Res I 45(8):1339–1355. doi:10.1016/s0967-0637(98)00015-6
Acknowledgments
We acknowledge the field assistance of the captain, officers, crew, and scientists aboard the T/S “Oshoro-maru”. We thank K. Sugita and A. Tsuzuku for their help on land in preparing the experiments, A. Murayama for nutrients analysis, and A. Matsuoka for POC and PN analysis. We also thank C. Norman for his help in improving the English of the manuscript. We acknowledge the editor and two anonymous reviewers for providing valuable comments that significantly improved the manuscript. This work was conducted in the framework of the Plankton Ecosystem Response to CO2 Manipulation Study (PERCOM), and was supported by grants from CRIEPI (#060215) and Grants-in-Aid for Scientific Research (#22681004).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yoshimura, T., Suzuki, K., Kiyosawa, H. et al. Impacts of elevated CO2 on particulate and dissolved organic matter production: microcosm experiments using iron-deficient plankton communities in open subarctic waters. J Oceanogr 69, 601–618 (2013). https://doi.org/10.1007/s10872-013-0196-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10872-013-0196-2