Skip to main content

Advertisement

SpringerLink
Log in

Negative effects of ocean acidification on calcification vary within the coccolithophore genus Calcidiscus

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

A large percentage of CO2 emitted into the atmosphere is absorbed by the oceans, causing chemical changes in surface waters known as ocean acidification (OA). Despite the high interest and increased pace of OA research to understand the effects of OA on marine organisms, many ecologically important organisms remain unstudied. Calcidiscus is a heavily calcified coccolithophore genus that is widespread and genetically and morphologically diverse. It contributes substantially to global calcium carbonate production, organic carbon production, oceanic carbon burial, and ocean–atmosphere CO2 exchange. Despite the importance of this genus, relatively little work has examined its responses to OA. We examined changes in growth, morphology, and carbon allocation in multiple strains of Calcidiscus leptoporus in response to ocean acidification. We also, for the first time, examined the OA response of Calcidiscus quadriperforatus, a larger and more heavily calcified Calcidiscus congener. All Calcidiscus coccolithophores responded negatively to OA with impaired coccolith morphology and a decreased ratio of particulate inorganic to organic carbon (PIC:POC). However, strains responded variably; C. quadriperforatus showed the most sensitivity, while the most lightly calcified strain of C. leptoporus showed little response to OA. Our findings suggest that calcium carbonate production relative to organic carbon production by Calcidiscus coccolithophores may decrease in future oceans and that Calcidiscus distributions may shift if more resilient strains and species become dominant in assemblages. This study demonstrates that variable responses to OA may be strain or species specific in a way that is closely linked to physiological traits, such as cellular calcite quota.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arrigo KR (2007) Carbon cycle: marine manipulations. Nature 450:491–492. doi:10.1038/450491a

    Article  CAS  Google Scholar 

  • Bach LT, Riebesell U, Georg Schulz K (2011) Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi. Limnol Oceanogr 56:2040–2050. doi:10.4319/lo.2011.56.6.2040

    Article  CAS  Google Scholar 

  • Baumann K-H, Bockel B, Frenz M (2004) Coccolith contribution to South Atlantic carbonate sedimentation. In: Young JR, Thierstein HR (eds) Coccolithophores: from molecular processes to global impact. Springer, Berlin, pp 367–402

    Chapter  Google Scholar 

  • Baumann K-H, Andruleit H, Bockel B et al (2005) The significance of extant coccolithophores as indicators of ocean water masses, surface water temperature, and palaeoproductivity: a review. Paläontol Z 7:93–112

    Article  Google Scholar 

  • Beaufort L, Probert I, de Garidel-Thoron T et al (2011) Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476:80–83. doi:10.1038/nature10295

    Article  CAS  Google Scholar 

  • Benner I, Diner RE, Lefebvre SC et al (2013) Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and pCO2. Philos Trans R Soc B 368:20130049. doi:10.1098/rstb.2013.0049

    Article  Google Scholar 

  • Berger WH (1973) Deep-sea carbonates: evidence for a coccolith lysocline. Deep Sea Res 20:917–921

    Google Scholar 

  • Bradshaw AL, Brewer PG, Shafer DK, Williams RT (1981) Measurements of total carbon dioxide and alkalinity by potentiometric titration in the GEOSECS program. Earth Planet Sci Lett 55:99–115. doi:10.1016/0012-821X(81)90090-X

    Article  CAS  Google Scholar 

  • Brand LE (1982) Genetic variability and spatial patterns of genetic differentiation in the reproductive rates of the marine coccolithophores Emiliania huxleyi and Gephyrocapsa oceanica. Limnol Oceanogr 27:236–245. doi:10.4319/lo.1982.27.2.0236

    Article  Google Scholar 

  • Brownlee C, Taylor A (2004) Calcification in coccolithophores: a cellular perspective. In: Young JR, Thierstein HR (eds) Coccolithophores: from molecular processes to global impact. Springer, Berlin, pp 31–49

    Chapter  Google Scholar 

  • Burd AB, Jackson GA (2009) Particle aggregation. Ann Rev Mar Sci 1:65–90

    Article  Google Scholar 

  • Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365. doi:10.1038/425365a

    Article  CAS  Google Scholar 

  • Collins S, Rost B, Rynearson TA (2014) Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl 7:140–155. doi:10.1111/eva.12120

    Article  CAS  Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part II 34:1733–1743

    Article  CAS  Google Scholar 

  • Engel A, Delille B, Jacquet S et al (2004) Transparent exopolymer particles and dissolved organic carbon production by Emiliania huxleyi exposed to different CO2 concentrations: a mesocosm experiment. Aquat Microb Ecol 34:93–104

    Article  Google Scholar 

  • Findlay HS, Calosi P, Crawfurd KJ (2011) Determinants of the PIC:POC response in the coccolithophore Emiliania huxleyi under future ocean acidification scenarios. Limnol Oceanogr 56:1168–1178. doi:10.4319/lo.2011.56.3.1168

    Article  CAS  Google Scholar 

  • Fiorini S, Middelburg JJ, Gattuso J-P (2011) Testing the effects of elevated pCO2 on coccolithophores (Prymnesiophyceae): comparison between haploid and diploid life stages. J Phycol 47:1281–1291. doi:10.1111/j.1529-8817.2011.01080.x

    Article  CAS  Google Scholar 

  • Friederich GE, Walz PM, Burczynski MG, Chavez FP (2002) Inorganic carbon in the central California upwelling system during the 1997–1999 El Niño–La Niña event. Prog Oceanogr 54:185–203

    Article  Google Scholar 

  • Gran G (1952) Determination of the equivalence point in potentiometric titration. Part II. Analyst 77:661–671

    Article  CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms I. Cyclotella nanna (Hustedt) and Detonula convervacea (Cleve). Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  • Henriksen K, Young JR, Bown PR et al (2004) Coccolith biomineralisation studied with atomic force microscopy. Palaeontology 47:725–743

    Article  Google Scholar 

  • Hirokawa Y, Fujiwara S, Tsuzuki M (2005) Three types of acidic polysaccharides associated with coccoliths of Pleurochrysis haptonemofera: comparison with Pleurochrysis carterae and analysis using fluorescein-isothiocyanate-labeled lectins. Mar Biotechnol 7:634–644. doi:10.1007/s10126-004-5148-9

    Article  CAS  Google Scholar 

  • Hofmann GE, Barry JP, Edmunds PJ et al (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu Rev Ecol Evol Syst 41:127–147. doi:10.1146/annurev.ecolsys.110308.120227

    Article  Google Scholar 

  • Iglesias-Rodriguez DM, Schofield OM, Batley J et al (2006) Intraspecific genetic diversity in the marine coccolithophore Emiliania Huxleyi (Prymnesiophyceae): the use of microsatellite analysis in marine phytoplankton population studies. J Phycol 42:526–536. doi:10.1111/j.1529-8817.2006.00231.x

    Article  CAS  Google Scholar 

  • Iglesias-Rodriguez MD, Halloran PR, Rickaby REM et al (2008) Phytoplankton calcification in a high-CO2 world. Science 320:336–340. doi:10.1126/science.1154122

    Article  CAS  Google Scholar 

  • Klaas C, Archer DE (2002) Association of sinking organic matter with various types of mineral ballast in the deep sea: implications for the rain ratio. Glob Biogeochem Cycles 16:63-1. doi:10.1029/2001GB001765

    Article  Google Scholar 

  • Kleijne A (1990) Distribution and malformation of extant calcareous nannoplankton in the Indonesian seas. Mar Micropaleontol 16:293–316

    Article  Google Scholar 

  • Knappertsbusch M, Cortes MY, Thierstein HR (1997) Morphologic variability of the coccolithophorid Calcidiscus leptoporus in the plankton, surface sediments and from the Early Pleistocene. Mar Micropaleontol 30:293–317

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434. doi:10.1111/j.1461-0248.2010.01518.x

    Article  Google Scholar 

  • Langer G, Bode M (2011) CO2 mediation of adverse effects of seawater acidification in Calcidiscus leptoporus. Geochem Geophys Geosyst 12:Q05001. doi:10.1029/2010GC003393

    Article  Google Scholar 

  • Langer G, Geisen M, Baumann K-H et al (2006) Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem Geophys Geosyst 7:Q09006. doi:10.1029/2005GC001227

    Article  Google Scholar 

  • Langer G, Nehrke G, Probert I et al (2009) Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6:2637–2646. doi:10.5194/bg-6-2637-2009

    Article  CAS  Google Scholar 

  • Langer G, Probert I, Ziveri P (2011) The morphological response of Emiliania huxleyi to seawater carbonate chemistry changes: an inter-strain comparison. J Nannoplankton Res 32:29–34

    Google Scholar 

  • Langer G, Oetjen K, Brenneis T (2012) Calcification of Calcidiscus leptoporus under nitrogen and phosphorus limitation. J Exp Mar Bio Ecol 413:131–137. doi:10.1016/j.jembe.2011.11.028

    Article  CAS  Google Scholar 

  • Lee C, Peterson ML, Wakeham SG, Armstrong RA, Cochran JK, Miquel JC, Fowler SW, Hirschberg D, Beck A, Xue J (2009) Particulate organic matter and ballast fluxes measured using time-series and settling velocity sediment traps in the northwestern Mediterranean Sea. Deep Sea Res II 56:1420–1436

    Article  CAS  Google Scholar 

  • Logan BE, Passow U, Alldredge AL et al (1995) Rapid formation and sedimentation of large aggregates is predictable from coagulation rates (half-lives) of transparent exopolymer particles (TEP). Deep Sea Res Part II 42:203–214. doi:10.1016/0967-0645(95)00012-F

    Article  Google Scholar 

  • Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351. doi:10.1038/ngeo1441

    Article  CAS  Google Scholar 

  • Lohbeck KT, Riebesell U, Reusch TBH (2014) Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification. Proc R Soc B 281:20140003. doi:10.1098/rspb.2014.0003

    Article  Google Scholar 

  • Mackinder L, Wheeler G, Schroeder D et al (2010) Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiol J 27:585–595. doi:10.1080/01490451003703014

    Article  CAS  Google Scholar 

  • Mackinder L, Wheeler G, Schroeder D et al (2011) Expression of biomineralization-related ion transport genes in Emiliania huxleyi. Environ Microbiol 13:3250–3265. doi:10.1111/j.1462-2920.2011.02561.x

    Article  CAS  Google Scholar 

  • Marsh ME, Chang DK, King GC (1992) Isolation and characterization of a novel acidic polysaccharide containing tartrate and glyoxylate residues from the mineralized scales of a unicellular coccolithophorid alga Pleurochrysis carterae. J Biol Chem 267:20507–20512

    CAS  Google Scholar 

  • McIntyre A, McIntyre R (1970) Coccolith concentration and differential solution in oceanic sediments. In: Funnell EM, Riedel WR (eds) Micropaleontology of the Oceans. Cambridge University Press, Cambridge, pp 253–261

    Google Scholar 

  • Medlin LK, Barker GL, Campbell L et al (1996) Genetic characterization of Emiliania huxleyi (Haptophyta). J Mar Syst 9:13–31

    Article  Google Scholar 

  • Meehl GA, Stocker TF, Collins WD et al (2007) Global climate projections. In: Soloman S, Qin D, Manning M et al (eds) Climate change 2007: The physical science basis. Contribution of working group I in the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 748–845

    Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE et al (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Miller N, Stillman J (2013) Seasonal and spatial variation in the energetics of the invasive clam Corbula amurensis in the upper San Francisco Estuary. Mar Ecol Prog Ser 476:129–139. doi:10.3354/meps10149

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. doi:10.1038/nature04095

    Article  CAS  Google Scholar 

  • Paasche E (2002) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40:503–529

    Article  Google Scholar 

  • Passow U (2004) Switching perspectives: do mineral fluxes determine particulate organic carbon fluxes or vice versa? Geochem Geophys Geosyst 5:1–5. doi:10.1029/2003GC000670

    Article  Google Scholar 

  • Passow U, Alldredge AL (1995) A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol Oceanogr 40:1326–1335

    Article  CAS  Google Scholar 

  • Passow U, De La Rocha CL (2006) Accumulation of mineral ballast on organic aggregates. Glob Biogeochem Cycles 20:1–7

    Article  Google Scholar 

  • Pedrotti ML, Fiorini S, Kerros M-E et al (2012) Variable production of transparent exopolymeric particles by haploid and diploid life stages of coccolithophores grown under different CO2 concentrations. J Plankton Res 34:388–398. doi:10.1093/plankt/fbs012

    Article  CAS  Google Scholar 

  • Quinn P, Thierstein HR, Brand L, Winter A (2003) Experimental evidence for the species character of Calcidiscus Leptoporus morphotypes. J Paleontol 77:825–830. doi:10.1666/0022-3360(2003)077<0825:EEFTSC>2.0.CO;2

    Article  Google Scholar 

  • Read BA, Kegel J, Klute MJ et al (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213. doi:10.1038/nature12221

    Article  CAS  Google Scholar 

  • Renaud S, Ziveri P, Broerse ATC (2002) Geographical and seasonal differences in morphology and dynamics of the coccolithophore Calcidiscus leptoporus. Mar Micropaleontol 46:363–385

    Article  Google Scholar 

  • Richier S, Fiorini S, Kerros M-E et al (2010) Response of the calcifying coccolithophore Emiliania huxleyi to low pH/high pCO2: from physiology to molecular level. Mar Biol 158:551–560. doi:10.1007/s00227-010-1580-8

    Article  Google Scholar 

  • Ridgwell A, Zondervan I, Hargreaves JC et al (2007) Assessing the potential long-term increase of oceanic fossil fuel CO2 uptake due to CO2 calcification feedback. Biogeosciences 4:481–492

    Article  CAS  Google Scholar 

  • Riebesell U, Zondervan I, Rost B et al (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367

    Article  CAS  Google Scholar 

  • Riebesell U, Schulz KG, Bellerby RGJ et al (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–548. doi:10.1038/nature06267

    Article  CAS  Google Scholar 

  • Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc—a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). US Geol Surv Open File Rep 2010, pp 1–16

  • Rokitta SD, John U, Rost B (2012) Ocean acidification affects redox-balance and ion-homeostasis in the life-cycle stages of Emiliania huxleyi. Plos One 7:e52212. doi:10.1371/journal.pone.0052212

    Article  CAS  Google Scholar 

  • Rost B, Riebesell U (2004) Coccolithophores and the biological pump: responses to environmental changes. In: Young JR, Thierstein HR (eds) Coccolithophores: from molecular processes to global impact. Springer, Berlin, pp 99–125

    Chapter  Google Scholar 

  • Sabine CL, Feely RA, Gruber N et al (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371. doi:10.1126/science.1097403

    Article  CAS  Google Scholar 

  • Saez AG, Probert I, Geisen M et al (2003) Pseudo-cryptic speciation in coccolithophores. Proc Natl Acad Sci USA 100:7163–7168. doi:10.1073/pnas.1132069100

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to imagej: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

    Article  CAS  Google Scholar 

  • Schneidermann N (1977) Selective dissolution of recent coccolithophorids in the Atlantic Ocean. In: Ramsay ATS (ed) Oceanic micropalaeontology. Academic Press, London, pp 1009–1053

    Google Scholar 

  • Silva A, Palma S, Oliveira PB et al (2009) Calcidiscus quadriperforatus and Calcidiscus leptoporus as oceanographic tracers in Lisbon Bay (Portugal). Estuar Coast Shelf Sci 81:333–344. doi:10.1016/j.ecss.2008.11.010

    Article  Google Scholar 

  • Van Bleijswijk JDL, Kempers RS, Velhuis MJ (1994) Cell and growth characteristics of types A and B of Emiliania huxleyi (Prymnesiophyceae) as determined by flow cytometry and chemical analysis. J Phycol 30:230–241. doi:10.1111/j.0022-3646.1994.00230.x

    Article  Google Scholar 

  • Van Emburg PR, de Jong EW, Daems WT (1986) lmmunochemical localization of a polysaccharide from biomineral structures (Coccoliths) of Emiliania huxleyi. J Ultrastruct Mol Struct Res 94:246–259

    Article  Google Scholar 

  • Westbroek P, De Jong EW, Van der Wal P et al (1984) Mechanism of calcification in the marine alga Emiliania huxleyi [and Discussion]. Philos Trans R Soc B 304:435–444

    Article  CAS  Google Scholar 

  • Young JR, Westbroek P (1991) Genotypic variation in the coccolithophorid species Emiliania huxleyi. Mar Micropaleontol 18:5–23. doi:10.1016/0377-8398(91)90004-P

    Article  Google Scholar 

  • Young JR, Davis SA, Bown PR et al (1999) Coccolith ultrastructure and biomineralisation. J Struct Biol 126:195–215

    Article  CAS  Google Scholar 

  • Young JR, Geisen M, Cros L et al (2003) A guide to extant coccolithophore taxonomy. J Nannoplankton Res 1:1–125

    Google Scholar 

  • Young JR, Geisen M, Probert I (2011) A review of selected aspects of coccolithophore biology with for paleobiodiversity estimation implications. Micropaleontol 51:267–288

    Article  Google Scholar 

  • Ziveri P, de Bernardi B, Baumann K et al (2007) Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean. Deep Sea Res Part II 54:659–675. doi:10.1016/j.dsr2.2007.01.006

    Article  Google Scholar 

  • Zondervan I, Zeebe RE, Rost B et al (2001) Decreasing marine biogenic calcification: a negative feedback on rising atmospheric pCO2. Global Biogeochem Cycles 15:507–516

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Richard Dugdale and Gerald Langer for suggestions and feedback, and Andrew Kalmbach and Roy Bartal for assistance with culturing and sampling. We thank Alex Parker, Frances Wilkerson, and Allison Johnson for assistance in measuring dissolved inorganic carbon and Julia Sweet for measurements of PABM. We gratefully acknowledge use of the Carl Zeiss Ultra 55 FE-SEM and supporting equipment at San Francisco State University, and the assistance of Clive Hayzeldon in acquiring SEM images. The FE-SEM and supporting facilities were obtained under National Science Foundation-MRI grant 0821619 and National Science Foundation -EAR grant 0949176, respectively. This work was funded by National Science Foundation grant BIO-OCE 0723908 to E.J.C., J.H.S. and T.K and Chem- OCE-1041038 to U.P. Funding to R.E.D. was provided by Sigma Xi, the California State University Council on Ocean Affairs, Science & Technology (COAST), the Achievement Rewards for College Scientists Foundation (ARCS), and San Francisco State University.

Author information

Authors and Affiliations

  1. Romberg Tiburon Center, San Francisco State University, 3150 Paradise Drive, Tiburon, CA, 94920, USA

    Rachel E. Diner, Ina Benner, Tomoko Komada, Edward J. Carpenter & Jonathon H. Stillman

  2. Marine Science Institute, University of California Santa Barbara, Santa Barbara, CA, 93106, USA

    Uta Passow

  3. Department of Biology, San Francisco State University, 1600 Holloway Ave, San Francisco, CA, 94132, USA

    Jonathon H. Stillman

  4. Department of Integrative Biology, University of California, Berkeley, 1005 Valley Life Sciences Building #3140, Berkeley, CA, 94720-3140, USA

    Jonathon H. Stillman

Authors
  1. Rachel E. Diner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ina Benner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Uta Passow
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomoko Komada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edward J. Carpenter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jonathon H. Stillman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathon H. Stillman.

Additional information

Communicated by U. Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 59 kb)

Supplementary material 2 (PDF 1204 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Diner, R.E., Benner, I., Passow, U. et al. Negative effects of ocean acidification on calcification vary within the coccolithophore genus Calcidiscus . Mar Biol 162, 1287–1305 (2015). https://doi.org/10.1007/s00227-015-2669-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2669-x

Keywords

Search

Navigation