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Polar Biology

, Volume 40, Issue 3, pp 727–734 | Cite as

Mechanisms driving Antarctic microbial community responses to ocean acidification: a network modelling approach

  • Roshni C. Subramaniam
  • Jessica Melbourne-Thomas
  • Andrew T. Davidson
  • Stuart P. Corney
Short Note

Abstract

Rising atmospheric CO2 concentrations and the subsequent changes to ocean chemistry may have pronounced effects on marine microbial communities, particularly for the cold Southern Ocean. Changes to the microbial community in this region could affect the way nutrients are cycled, impact the efficiency of carbon drawdown, and cause shifts in food supply to higher trophic levels. Increased CO2 could affect the bioavailability of iron to phytoplankton. Fertilisation experiments show that iron can influence phytoplankton community composition, favouring large phytoplankton species in iron-replete conditions. The potential interactive effects of CO2 and iron bioavailability are currently poorly understood but are likely to be important in determining CO2-induced changes to the microbial community. We employ a qualitative network modelling approach to evaluate alternative hypotheses regarding the effects of elevated CO2 on Antarctic microbial communities in incubation experiments. We used a sequential approach to model development and testing, where we first formulated a base model for microbial community interactions, and then sequentially added direct and indirect effects of elevated CO2 on particular groups. We found that model simulations were most consistent with observations from incubation experiments when we assumed an indirect effect of CO2 on phytoplankton. In particular, when we assumed a negative effect of elevated CO2 on the uptake of iron by large phytoplankton, as a result of a decrease in iron bioavailability. Our findings show that qualitative network models can be used to test hypotheses relating to results from experimental studies, and help identify key processes to target in future studies.

Keywords

Model CO2 Iron Antarctic microbial community 

Notes

Acknowledgments

The authors would like to thank the two anonymous reviewers for providing valuable comments and suggestions. This study was supported by the Australian Government’s Cooperative Research Centres Programme through the Antarctic Climate and Ecosystems Cooperative Research Centre.

References

  1. Aberle N, Schulz KG, Stuhr A, Malzahn A, Ludwig A, Riebesell U (2013) High tolerance of microzooplankton to ocean acidification in an Arctic coastal plankton community. Biogeosciences 10:1471–1481. doi: 10.5194/bg-10-1471-2013 CrossRefGoogle Scholar
  2. Allgaier M, Riebesell U, Vogt M, Thyrhaug R, Grossart H-P (2008) Coupling of heterotrophic bacteria to phytoplankton bloom development at different pCO2 levels: a mesocosm study. Biogeosci Discuss 5:317–359. https://hal.archives-ouvertes.fr/hal-00297965 CrossRefGoogle Scholar
  3. Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696. doi: 10.1126/science.280.5364.694 CrossRefGoogle Scholar
  4. Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, Murdoch R, Bakker DCE, Bowie AR, Buesseler KO, Chang H, Charette M, Croot P, Downing K, Frew R, Gall M, Hadfield M, Hall J, Harvey M, Jameson G, LaRoche J, Liddicoat M, Ling R, Maldonado MT, McKay RM, Nodder S, Pickmere S, Pridmore R, Rintoul S, Safi K, Sutton P, Strzepek R, Tanneberger K, Turner S, Waite A, Zeldis J (2000) A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407:695–702. doi: 10.1038/35037500 CrossRefPubMedGoogle Scholar
  5. Breitbarth E, Bellerby R, Neill C, Ardelan M, Meyerhöfer M, Zöllner E, Croot P, Riebesell U (2010) Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7:1065–1073. doi: 10.5194/bg-7-1065-2010 CrossRefGoogle Scholar
  6. Brussaard C, Noordeloos A, Witte H, Collenteur M, Schulz KG, Ludwig A, Riebesell U (2013) Arctic microbial community dynamics influenced by elevated CO2 levels. Biogeosciences 10:719–731. doi: 10.5194/bg-10-719-2013 CrossRefGoogle Scholar
  7. Dambacher JM, Ramos-Jiliberto R (2007) Understanding and predicting effects of modified interactions through a qualitative analysis of community structure. Q Rev Biol 82:227–250. doi: 10.1086/519966 CrossRefPubMedGoogle Scholar
  8. Dambacher JM, Li HW, Rossignol PA (2002) Relevance of community structure in assessing indeterminacy of ecological predictions. Ecology 83:1372–1385CrossRefGoogle Scholar
  9. Davidson AT, McKinlay J, Westwood K, Thompson PG, van den Enden R, de Salas M, Wright S, Johnson R, Berry K (2016) Enhanced CO2 concentrations change the structure of Antarctic marine microbial communities. Mar Ecol Prog Ser. doi: 10.3354/meps11742
  10. 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 CrossRefGoogle Scholar
  11. Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281:200–206. doi: 10.1126/science.281.5374.200 CrossRefPubMedGoogle Scholar
  12. Feng Y, Hare C, Rose J, Handy S, DiTullio G, Lee P, Smith W, Peloquin J, Tozzi S, Sun J (2010) Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep-Sea Res Part I 57:368–383. doi: 10.1016/j.dsr.2009.10.013 CrossRefGoogle Scholar
  13. Flynn KJ, Blackford JC, Baird ME, Raven JA, Clark DR, Beardall J, Brownlee C, Fabian H, Wheeler GL (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nat Clim Change 2:510–513. doi: 10.1038/nclimate1489 CrossRefGoogle Scholar
  14. Grossart H-P, Allgaier M, Passow U, Riebesell U (2006) Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol Oceanogr 51:1–11. doi: 10.4319/lo.2006.51.1.0001 CrossRefGoogle Scholar
  15. Haberman KL, Ross RM, Quetin LB (2003) Diet of the Antarctic krill (Euphausia superba Dana): II. Selective grazing in mixed phytoplankton assemblages. J Exp Mar Biol Ecol 283:97–113. doi: 10.1016/S0022-0981(02)00467-7 CrossRefGoogle Scholar
  16. Hare CE, Leblanc K, DiTullio GR, Kudela R, 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. doi: 10.3354/meps07182 CrossRefGoogle Scholar
  17. Hoffmann LJ, Peeken I, Lochte K, Assmy P, Veldhuis M (2006) Different reactions of Southern Ocean phytoplankton size classes to iron fertilization. Limnol Oceanogr 51:1217–1229. doi: 10.4319/lo.2006.51.3.1217 CrossRefGoogle Scholar
  18. Hoppe CJ, Hassler CS, Payne CD, Tortell PD, Rost B, Trimborn S (2013) Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS ONE 8:e79890. doi: 10.1371/journal.pone.0079890 CrossRefPubMedPubMedCentralGoogle Scholar
  19. IPCC (2014) Climate change 2014. Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core writing team Pachauri R.K, Meyer L.A. (eds)]. IPCC, Geneva, Switzerland, p 151Google Scholar
  20. Kawaguchi S, Ichii T, Naganobu M (1999) Green krill, the indicator of micro-and nano-size phytoplankton availability to krill. Polar Biol 22:133–136. doi: 10.1007/s003000050400 CrossRefGoogle Scholar
  21. Laws RM (1985) The Ecology of the Southern Ocean: The Antarctic ecosystem, based on krill, appears to be moving toward a new balance of species in its recovery from the inroads of whaling. Am Sci 73:26-40. http://www.jstor.org/stable/27853059
  22. Liu J, Weinbauer M, Maier C, Dai M, Gattuso J (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat Microb Ecol 61:291–305. doi: 10.3354/ame01446 CrossRefGoogle Scholar
  23. Martin JH, Fitzwater SE, Gordon RM (1990) Iron deficiency limits phytoplankton growth in Antarctic waters. Glob Biogeochem Cycles 4:5–12. doi: 10.1029/GB004i001p00005 CrossRefGoogle Scholar
  24. McNeil BI, Matear RJ (2008) Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc Natl Acad Sci USA 105:18860–18864. doi: 10.1073/pnas.0806318105 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Melbourne-Thomas J, Wotherspoon S, Raymond B, Constable A (2012) Comprehensive evaluation of model uncertainty in qualitative network analyses. Ecol Monogr 82:505–519. doi: 10.1890/12-0207.1 CrossRefGoogle Scholar
  26. Melbourne-Thomas J, Constable A, Wotherspoon S, Raymond B (2013) Testing paradigms of ecosystem change under climate warming in Antarctica. PLoS ONE 8:e55093. doi: 10.1371/journal.pone.0055093 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Midorikawa T, Inoue HY, Ishii M, Sasano D, Kosugi N, Hashida G, S-i Nakaoka, Suzuki T (2012) Decreasing pH trend estimated from 35-year time series of carbonate parameters in the Pacific sector of the Southern Ocean in summer. Deep-Sea Res Part I 61:131–139. doi: 10.1016/j.dsr.2011.12.003 CrossRefGoogle Scholar
  28. Millero FJ, Woosley R, Benjamin D, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:72–85. doi: 10.5670/oceanog.2009.98 CrossRefGoogle Scholar
  29. Moore SE, Huntington HP (2008) Arctic marine mammals and climate change: impacts and resilience. Ecol Appl 18:S157–S165. doi: 10.1890/06-0571.1 CrossRefPubMedGoogle Scholar
  30. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. doi: 10.1038/nature04095 CrossRefPubMedGoogle Scholar
  31. Pearce I, Davidson AT, Thomson PG, Wright S, van den Enden R (2010) Marine microbial ecology off East Antarctica (30–80°E): rates of bacterial and phytoplankton growth and grazing by heterotrophic protists. Deep-Sea Res Part II 57:849–862. doi: 10.1016/j.dsr2.2008.04.039 CrossRefGoogle Scholar
  32. Piontek J, Borchard C, Sperling M, Schulz KG, Riebesell U, Engel A (2013) Response of bacterioplankton activity in an Arctic fjord system to elevated pCO2: results from a mesocosm perturbation study. Biogeosciences 10:297–314. doi: 10.5194/bg-10-297-2013 CrossRefGoogle Scholar
  33. 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. doi: 10.3354/meps08134 CrossRefGoogle Scholar
  34. Schulz KG, Bellerby R, Brussaard CP, Büdenbender J, Czerny J, Engel A, Fischer M, Koch-Klavsen S, Krug SA, Lischka S (2013) Temporal biomass dynamics of an Arctic plankton bloom in response to increasing levels of atmospheric carbon dioxide. Biogeosciences 10:161–180. doi: 10.5194/bg-10-161-2013 CrossRefGoogle Scholar
  35. Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science 327:676–679. doi: 10.1126/science.1183517 CrossRefPubMedGoogle Scholar
  36. Smetacek V, Assmy P, Henjes J (2004) The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarct Sci 16:541–558. doi: 10.1017/S0954102004002317 CrossRefGoogle Scholar
  37. Suffrian K (2008) Microzooplankton grazing and phytoplankton growth in marine mesocosms with increased CO2 levels. Biogeosciences 5:1145–1156. doi: 10.5194/bg-5-1145-2008 CrossRefGoogle Scholar
  38. 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)1. J Phycol 49:475–488. doi: 10.1111/jpy.12054 CrossRefPubMedGoogle Scholar
  39. Sugie K, Yoshimura T (2016) Effects of high CO2 levels on the ecophysiology of the diatom Thalassiosira weissflogii differ depending on the iron nutritional status. ICES J Mar Sci 73:680–692. doi: 10.1093/icesjms/fsv259 CrossRefGoogle Scholar
  40. Sugie K, Endo H, Suzuki K, Nishioka J, Kiyosawa H, Yoshimura T (2013) Synergistic effects of pCO2 and iron availability on nutrient consumption ratio of the Bering Sea phytoplankton community. Biogeosciences 10:6309–6321. doi: 10.5194/bg-10-6309-2013 CrossRefGoogle Scholar
  41. Sunda W, Huntsman S (2003) Effect of pH, light, and temperature on Fe–EDTA chelation and Fe hydrolysis in seawater. Mar Chem 84:35–47. doi: 10.1016/S0304-4203(03)00101-4 CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Roshni C. Subramaniam
    • 1
    • 3
  • Jessica Melbourne-Thomas
    • 1
    • 2
  • Andrew T. Davidson
    • 1
    • 2
    • 3
  • Stuart P. Corney
    • 1
  1. 1.Antarctic Climate and Ecosystems Cooperative Research Centre (ACE CRC)University of TasmaniaHobartAustralia
  2. 2.Department of the EnvironmentAustralian Antarctic DivisionKingstonAustralia
  3. 3.Institute for Marine and Antarctic Studies (IMAS)University of TasmaniaHobartAustralia

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