Skip to main content

Enhanced dissolved organic carbon production in aquatic ecosystems in response to elevated atmospheric CO2

Abstract

Although aquatic ecosystems are a major carbon reservoir, how their carbon dynamics will respond to increasing concentrations of atmospheric CO2 is not well understood. The availability of essential nutrients has the potential to modify carbon fluxes under elevated CO2 by altering carbon processing and storage in the biota. Here, we describe a semi-continuous culture experiment with natural phytoplankton and bacteria assemblages designed to investigate (1) how carbon dynamics in aquatic ecosystems respond to continuously elevated atmospheric CO2, and (2) whether carbon fluxes resulting from elevated CO2 are modified by changes in inorganic nitrogen and phosphorus availability. Our results showed that elevated CO2 led to significant increases in photosynthetic carbon uptake, despite a decrease in the algal chlorophyll a concentrations and no significant change in total algal biovolume. This enhancement of inorganic carbon uptake was accompanied by a significant increase in dissolved organic carbon (DOC) production. Concurrent increases in the C/N and C/P ratios of dissolved organic matter also suggested that DOC stability increased. Nutrient availability, especially nitrogen availability, had strong effects on inorganic carbon uptake and biomass carbon pools. In contrast, CO2-enhanced DOC production was not significantly affected by varying concentrations of inorganic nitrogen and phosphorus. Our study underscores the importance of DOC as a potential carbon sink in aquatic ecosystems. The observed responses to changes in CO2 and nutrient availability could have important implications for long-term carbon cycling in aquatic ecosystems, and highlight the potential buffering capacity of aquatic ecosystems to future environmental change.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alldredge AL, Passow U, Logan BE (1993) The abundance and significance of a class of large, transparent organic particles in the ocean. Deep Sea Res 40(6):1131–1140

    Article  Google Scholar 

  2. Ballantyne F, Menge D, Ostling A, Hosseini P (2008) Nutrient recycling affects autotroph and ecosystem stoichiometry. Am Nat 171(4):511–523

    Article  Google Scholar 

  3. Bauer JE, Williams PM, Druffel ERM (1992) 14C activity of dissolved organic carbon fractions in the north-central Pacific and Sargasso Sea. Nature 357(6380):667–670

    Article  Google Scholar 

  4. Borchard C, Engel A (2012) Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions. Biogeoscience 9(8):3405–3423

    Article  Google Scholar 

  5. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425(6956):365

    Article  Google Scholar 

  6. Campbell W, Song P, Barbier G (2006) Nitrate reductase for nitrate analysis in water. Environ Chem Lett 4(2):69–73

    Article  Google Scholar 

  7. Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10(1):172–185

    Article  Google Scholar 

  8. Ducklow HW, Steinberg DK, Buesseler KO (2001) Upper ocean carbon export and the biological pump. Oceanography 14(4):50–58

    Article  Google Scholar 

  9. Elrifi IR, Turpin DH (1986) Nitrate and ammonium induced photosynthetic suppression in N-limited Selenastrum minutum. Plant Physiol 81(1):273–279

    Article  Google Scholar 

  10. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10(12):1135–1142

    Article  Google Scholar 

  11. Engel A (2002) Direct relationship between CO2 uptake and transparent exopolymer particles production in natural phytoplankton. J Plankton Res 24(1):49–53

    Article  Google Scholar 

  12. Engel A, Thoms S, Riebesell U, Rochelle-Newall E, Zondervan I (2004) Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 428(6986):929–932

    Article  Google Scholar 

  13. Engel A, Zondervan I, Aerts K et al (2005) Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol Oceanogr 50(2):493–507

    Article  Google Scholar 

  14. Eppley RW, Peterson BJ (1979) Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282(5740):677–680

    Article  Google Scholar 

  15. Falkowski PG (1994) The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth Res 39(3):235–258

    Article  Google Scholar 

  16. Falkowski PG, Raven JA (2007) Aquatic photosynthesis. Princeton University Press, Princeton

    Google Scholar 

  17. Geider RJ, Delucia EH, Falkowski PG et al (2001) Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats. Glob Change Biol 7(8):849–882

    Article  Google Scholar 

  18. Gordillo FJL, Jiménez C, Figueroa FL, Niell FX (1999) Effects of increased atmospheric CO2 and N supply on photosynthesis, growth and cell composition of the cyanobacterium Spirulina platensis (Arthrospira). J Appl Phycol 10(5):461–469

    Article  Google Scholar 

  19. Gruber DF, Simjouw JP, Seitzinger SP, Taghon GL (2006) Dynamics and characterization of refractory dissolved organic matter produced by a pure bacterial culture in an experimental predator–prey system. Appl Environ Microbiol 72(6):4184–4191

    Article  Google Scholar 

  20. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chantey MH (eds) Culture of marine invertebrate animals. Plenum Publishers, New York, pp 29–60

    Chapter  Google Scholar 

  21. Halterman SG, Toetz DW (1984) Kinetics of nitrate uptake by freshwater algae. Hydrobiologia 114(3):209–214

    Article  Google Scholar 

  22. Hansell DA, Carlson CA, Repeta DJ, Schlitzer R (2009) Dissolved organic matter in the ocean: a controversy stimulates new insights. Oceanography 22(4):202–211

    Article  Google Scholar 

  23. Harpole WS, Ngai JT, Cleland EE et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14(9):852–862

    Article  Google Scholar 

  24. Hein M, Sand-Jensen K (1997) CO2 increases oceanic primary production. Nature 388(6642):526–527

    Article  Google Scholar 

  25. Hessen DO (2008) Efficiency, energy and stoichiometry in pelagic food webs: reciprocal roles of food quality and food quantity. Freshw Rev 1(1):43–57

    Google Scholar 

  26. Hessen DO, Anderson TR (2008) Excess carbon in aquatic organisms and ecosystems: physiological, ecological and evolutionary implications. Limnol Oceanogr 53(4):1685–1696

    Article  Google Scholar 

  27. Hessen DO, Ågren GI, Anderson TR (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85(5):1179–1192

    Article  Google Scholar 

  28. Hopkinson CS, Vallino JJ (2005) Efficient export of carbon to the deep ocean through dissolved organic matter. Nature 433(7022):142–145

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. Hutchins D, Fu FX, Zhang Y, Warner ME, Feng Y, Portune K, Bernhardt PW, Mulholland MR (2007) CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 52(4):1293–1304

    Article  Google Scholar 

  31. Jansson M, Karlson J, Jonsson A (2012) Carbon dioxide supersaturation promotes primary production in lakes. Ecol Lett 15(6):527–532

    Google Scholar 

  32. Jiao N, Herndl GJ, Hansell DA et al (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8(8):593–599

    Article  Google Scholar 

  33. Kilham P, Hecky RE (1988) Comparative ecology of marine and freshwater phytoplankton. Limnol Oceanogr 33(4):776–795

    Article  Google Scholar 

  34. Langner CL, Hendrix PF (1982) Evaluation of a persulfate digestion method for particulate nitrogen and phosphorus. Water Res 16(10):1451–1454

    Article  Google Scholar 

  35. Lefebvre SC, Benner I, Stillman JH, Parker AE, Drake MK, Rossignol PE, Okimura KM, Komada T, Carpenter EJ (2012) Nitrogen source and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle. Glob Change Biol 18(2):493–503

    Article  Google Scholar 

  36. Leonardos N, Geider RJ (2005) Elevated atmospheric carbon dioxide increases organic carbon fixation by Emiliania huxleyi (Haptophyta), under nutrient-limited high-light conditions. J Phycol 41(6):1196–1203

    Article  Google Scholar 

  37. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45(3):569–579

    Article  Google Scholar 

  38. Morel FMM, Reinfelder JR, Roberts SB, Chamberlain CP, Lee JG, Yee D (1994) Zinc and carbon co-limitation of marine phytoplankton. Nature 369(6483):740–742

    Article  Google Scholar 

  39. Ogawa H, Amagai Y, Koike I, Kaiser K, Benner R (2001) Production of refractory dissolved organic matter by bacteria. Science 292(5518):917–920

    Article  Google Scholar 

  40. Passow U (2000) Formation of transparent exopolymer particles, TEP, from dissolved precursor material. Mar Ecol Prog Ser 192:1–11

    Article  Google Scholar 

  41. Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environment. Prog Oceanogr 55(3–4):287–333

    Article  Google Scholar 

  42. Peeters F, Straile D, Lorke A, Livingstone DM (2007) Earlier onset of the spring phytoplankton bloom in lakes of the temperate zone in a warmer climate. Glob Change Biol 13(9):1898–1909

    Article  Google Scholar 

  43. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  44. Raven JA (1991) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant Cell Environ 14(8):779–794

    Article  Google Scholar 

  45. Raven JA, Johnston AM (1991) Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources. Limnol Oceanogr 36(8):1701–1714

    Article  Google Scholar 

  46. Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60(4):719–729

    Article  Google Scholar 

  47. Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361(6409):249–251

    Article  Google Scholar 

  48. Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407(6802):364–367

    Article  Google Scholar 

  49. Riebesell U, Schulz K, Bellerby R et al (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450(7169):545–548

    Article  Google Scholar 

  50. Sabine CL, Feely RA, Gruber N et al (2004) The oceanic sink for anthropogenic CO2. Science 305(5682):367–371

    Article  Google Scholar 

  51. Sarmiento J, Slater R, Barber R et al (2004) Response of ocean ecosystems to climate warming. Glob Biogeochem Cycles 18(3):GB3003

    Article  Google Scholar 

  52. Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114(3):177–187

    Article  Google Scholar 

  53. Schindler D (1977) Evolution of phosphorus limitation in lakes. Science 195(4275):260–262

    Article  Google Scholar 

  54. Schlesinger WH (1997) Biogeochemistry: an analysis of global change. Academic Press, San Diego

    Google Scholar 

  55. Simon M, Cho BC, Azam F (1992) Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Mar Ecol Prog Ser 86:103–110

    Article  Google Scholar 

  56. Smith VH (1979) Nutrient dependence of primary productivity in lakes. Limnol Oceanogr 24(6):1051–1064

    Article  Google Scholar 

  57. Smith VH (2006) Responses of estuarine and coastal marine phytoplankton to nitrogen and phosphorus enrichment. Limnol Oceanogr 51(1):377–384

    Article  Google Scholar 

  58. Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr 53(2):494–505

    Article  Google Scholar 

  59. Sun J, Liu D (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25(11):1331–1346

    Article  Google Scholar 

  60. van de Waal D, Verschoor A, Verspagen J, Van Donk E, Huisman J (2010) Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Front Ecol Environ 8(3):145–152

    Article  Google Scholar 

  61. Van Veldhoven PP, Mannaerts GP (1987) Inorganic and organic phosphate measurements in the nanomolar range. Anal Biochem 161(1):45–48

    Article  Google Scholar 

  62. Yue L, Chen W (2005) Isolation and determination of cultural characteristics of a new highly CO2 tolerant fresh water microalgae. Energy Convers Manage 46(11–12):1868–1876

    Article  Google Scholar 

Download references

Acknowledgments

We sincerely acknowledge Dr. Joy Ward, Dr. Jerry DeNoyelles, Ryan Behrens, LeeAnn Bennett and Kistie Brunsell for assistance in the experiment. Dr. Sharon Billings, Dr. Robert Buddemeier, Dr. Ron Benner and Dr. Frieda Taub gave insightful comments on an early draft of this paper. We also thank Dr. Stuart Grandy and two anonymous reviewers for their valuable and constructive comments.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Chao Song.

Additional information

Responsible editor: Stuart Grandy

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Song, C., Ballantyne, F. & Smith, V.H. Enhanced dissolved organic carbon production in aquatic ecosystems in response to elevated atmospheric CO2 . Biogeochemistry 118, 49–60 (2014). https://doi.org/10.1007/s10533-013-9904-7

Download citation

Keywords

  • Aquatic ecosystems
  • Carbon
  • Dissolved organic carbon
  • Elevated CO2
  • Nutrient availability