Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Progress Article
  • Published:

Biophysical controls on organic carbon fluxes in fluvial networks

A Corrigendum to this article was published on 20 July 2009

This article has been updated

Abstract

Metabolism of terrestrial organic carbon in freshwater ecosystems is responsible for a large amount of carbon dioxide outgassing to the atmosphere, in contradiction to the conventional wisdom that terrestrial organic carbon is recalcitrant and contributes little to the support of aquatic metabolism. Here, we combine recent findings from geophysics, microbial ecology and organic geochemistry to show geophysical opportunity and microbial capacity to enhance the net heterotrophy in streams, rivers and estuaries. We identify hydrological storage and retention zones that extend the residence time of organic carbon during downstream transport as geophysical opportunities for microorganisms to develop as attached biofilms or suspended aggregates, and to metabolize organic carbon for energy and growth. We consider fluvial networks as meta-ecosystems to include the acclimation of microbial communities in downstream ecosystems that enable them to exploit energy that escapes from upstream ecosystems, thereby increasing the overall energy utilization at the network level.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Heuristic concept of downstream changes of channel geomorphology, geophysical opportunity and microbial lifestyles.

Similar content being viewed by others

Change history

  • 20 July 2009

    In the version of this of this Progress Article originally published, Table 1 was incorrect and subsequently the values of global fluvial respiration and global net heterotrophy reported in text were incorrect. These errors have been corrected in the HTML and PDF versions.

References

  1. Cauwet, G. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. A. & Carlson, C. A.) 579–602 (Academic Press, New York, 2002).

    Book  Google Scholar 

  2. del Giorgio, P. A. & Williams, P. J. B. Respiration in Aquatic Ecosystems (Oxford Univ. Press, USA, 2005).

    Book  Google Scholar 

  3. Cole, J. J. et al. Plumbing the global carbon cycle: Integrating inland waters into the terrestrial carbon budget. Ecosystems 10, 172–185 (2007).

    Article  Google Scholar 

  4. Richey, J. E. in Encyclopedia of Hydrological Sciences Vol. 5 (ed. Anderson, M. & McDonnell, J. J.) 184 (Wiley, New Jersey, 2005).

    Google Scholar 

  5. Trumbore, S. E. Potential responses of soil organic carbon to global environmental change. Proc. Natl Acad. Sci. USA 94, 8284–8291 (1997).

    Article  Google Scholar 

  6. Cole, J. J. & Caraco, N. F. Carbon in catchments: connecting terrestrial carbon losses with aquatic metabolism. Mar. Freshwater Res. 52, 101–110 (2001).

    Article  Google Scholar 

  7. Richey, J. E., Melack, J. M., Aufdenkampe, A. K., Ballester, V. M. & Hess, L. L. Outgassing from Amazonian rivers and wetlands as a large tropical source of atmospheric CO2 . Nature 416, 617–620 (2002).

    Article  Google Scholar 

  8. Mayorga, E. et al. Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436, 538–541 (2005).

    Article  Google Scholar 

  9. Paola, C. et al. Toward a unified science of the Earth's surface: Opportunities for synthesis among hydrology, geomorphology, geochemistry, and ecology. Wat. Resour. Res. 42, doi:10.1029/2005WR004336 (2006).

  10. Battin, T. J., Kaplan, L. A., Newbold, J. D. & Hansen, C. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426, 439–442 (2003).

    Article  Google Scholar 

  11. Seitzinger, S. P. et al. Molecular-level chemical characterization and bioavailability of dissolved organic matter in stream water using electrospray-ionization mass spectrometry. Limnol. Oceanogr. 50, 1–12 (2005).

    Article  Google Scholar 

  12. Frazier, S., Kaplan, L. A. & Hatcher, P. G. Molecular characterization of biodegradable dissolved organic matter using bioreactors and [12C/13C] tetramethylammonium hydroxide thermochemolysis GC-MS. Environ. Sci. Technol. 39, 1479–1491 (2005).

    Article  Google Scholar 

  13. Kim, S., Kaplan L. A. & Hatcher, P. G. Biodegradable dissolved organic matter in a temperate and a tropical stream determined from ultra-high resolution mass spectrometry. Limnol. Oceanogr. 51, 1054–1063 (2006).

    Article  Google Scholar 

  14. McCallister, S. L., Bauer, J. E., Cherrier, J. E. & Ducklow, H. W. Assessing sources and ages of organic matter supporting river and estuarine bacterial production: A multiple-isotope (Δ14C, δ13C, and δ15N) approach. Limnol. Oceanogr. 49, 1687–1702 (2004).

    Article  Google Scholar 

  15. McCallister, S. L., Bauer, J. E. & Canuel, E. A. Bioreactivity of estuarine dissolved organic matter: A combined geochemical and microbiological approach. Limnol. Oceanogr. 51, 94–100 (2006).

    Article  Google Scholar 

  16. Raymond, P. A. & Bauer, J. E. Riverine export of aged terrestrial organic matter to the North Atlantic Ocean. Nature 409, 497–500 (2001).

    Article  Google Scholar 

  17. Leopold, L. B., Wolman, M. G. & Miller, J. P. Fluvial Processes in Geomorphology (Freeman, San Francisco, 1964).

    Google Scholar 

  18. Packman, A. I. & Bencala, K. E. in Streams and Ground Waters (eds Jones, J. A. & Mulholland, P. J.) 45–80 (Academic Press, San Diego, 2000).

    Book  Google Scholar 

  19. Harvey, J. W. & Wagner, B. J. in Streams and Ground Waters (eds Jones, J. A. & Mulholland, P. J.) 3–43 (Academic Press, San Diego, 2000).

    Book  Google Scholar 

  20. Wörman, A., Packman, A., Marklund, L., Harvey, J. & Stone, S. Fractal topography and subsurface water flows from fluvial bedforms to the continental shield. Geophys. Res. Lett. 34, L07402 (2007).

    Article  Google Scholar 

  21. Bencala, K. E. in Encyclopedia of Hydrological Sciences Vol. 3 (ed. Anderson, M. & McDonnell, J. J.) 113 (Wiley, New Jersey, 2005).

    Google Scholar 

  22. Bianchi, T. S. Biogeochemistry of Estuaries (Oxford Univ. Press, New York, 2007).

    Google Scholar 

  23. Crump, B. C., Hopkinson, C. S., Sogin, M. L. & Hobbie, J. E. Microbial biogeography along an estuarine salinity gradient: Combined influences of bacterial growth and residence time. Appl. Environ. Microbiol. 70, 1494–1505 (2004).

    Article  Google Scholar 

  24. Martin, J. B., Cable, J. E., Jaeger, J., Hartl, K. & Smith, C. G. Thermal and chemical evidence for rapid water exchange across the sediment-water interface by bioirrigation in the Indian River Lagoon, Florida. Limnol. Oceanogr. 51, 1332–1341 (2006).

    Article  Google Scholar 

  25. Simon, M., Grossart, H. P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211 (2002).

    Article  Google Scholar 

  26. Besemer, K., Moeseneder, M. M., Arrieta, J. M., Herndl, G. J. & Peduzzi, P. Complexity of bacterial communities in a river-floodplain system (Danube, Austria). Appl. Environm. Microbiol. 71, 609–620 (2005).

    Article  Google Scholar 

  27. Besemer, K. et al. Biophysical controls on community succession in stream biofilms. Appl. Environ. Microbiol. 73, 4966–4974 (2007).

    Article  Google Scholar 

  28. Ploug, H. Small-scale oxygen fluxes and remineralization in sinking aggregates. Limnol. Oceanogr. 46, 1624–1631 (2001).

    Article  Google Scholar 

  29. Kiørboe, T. & Jackson, G. A. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol. Oceanogr. 46, 1309–1318 (2001).

    Article  Google Scholar 

  30. Battin, T. J., Wille, A., Psenner, R. & Richter, A. Large-scale environmental controls on microbial biofilms in high-alpine streams. Biogeosciences 1, 159–171 (2004).

    Article  Google Scholar 

  31. Hullar, M. A. J., Kaplan, L. A. & Stahl, D. A. Recurring seasonal dynamics of microbial communities in stream habitats. Appl. Environ. Microbiol. 72, 713–722 (2006).

    Article  Google Scholar 

  32. Winter, C., Hein, T., Kavka, G., Mach, R. L. & Farnleitner, A. H. Longitudinal changes in the bacterial community composition of the Danube River: a whole-river approach. Appl. Environ. Microbiol. 73, 421–431 (2007).

    Article  Google Scholar 

  33. Maranger, R. J., Pace, M. L., del Giorgio, P. A., Caraco, N. F. & Cole, J. J. Longitudinal spatial patterns of bacterial production and respiration in a large River-Estuary: Implications for ecosystem carbon consumption. Ecosystems 8, 318–330 (2005).

    Article  Google Scholar 

  34. Vannote, R. J., Minshall, G. W., Cummins, K. W., Sedell, J. R. & Cushing, C. E. The river continuum concept. Can. J. Fish. Aquat. Sci. 37, 130–137 (1981).

    Article  Google Scholar 

  35. Findlay, S. E. G. & Sinsabaugh, R. L. Large-scale variation in subsurface stream biofilms: A cross-regional comparison of metabolic function and community similarity. Microb. Ecol. 52, 491–500 (2006).

    Article  Google Scholar 

  36. Fischer, H., Kloep, F., Wilzcek, S. & Pusch, M. T. A river's liver – microbial processes within the hyporheic zone of a large lowland river. Biogeochemistry 76, 349–371 (2005).

    Article  Google Scholar 

  37. Oliver, R. L. & Merrick, C. J. Partitioning of river metabolism identifies phytoplankton as a major contributor in the regulated Murray River (Australia). Freshwat. Biol. 51, 1131–1148 (2006).

    Article  Google Scholar 

  38. Junk, W. J., Bayley, P. B. & Spark, R. E. in Proceedings of the International Large River Symposium (LARS) (ed. Dodge, D. P.) 110–127 (Canadian Special Publication of Fisheries and Aquatic Sciences, Ottawa, Canada, 1989).

    Google Scholar 

  39. Robertson, A. I., Bunn, S. E., Boon, P. I. & Walker, K. F. Sources, sinks and transformations of organic carbon in Australian floodplain rivers. Mar. Freshwater Res. 50, 813–829 (1999).

    Article  Google Scholar 

  40. Ryder, D. S. Response of epixylic biofilm metabolism to water level variability in a regulated floodplain river. J. N. Am. Benth. Soc. 23, 214–223 (2004).

    Article  Google Scholar 

  41. Hopkinson, C. S. & Smith, E. M. in Respiration in Aquatic Ecosystems (eds Del Giorgio, P. A. & Williams, P. J. B.) (Oxford Univ. Press, USA, 2005).

    Google Scholar 

  42. Borges A. V., Delille, B. & Frankignoulle, M. Budgeting sinks and sources of CO2 in the coastal ocean: Diversity of ecosystems counts. Geophys. Res. Lett. 32, L14601 (2005).

    Article  Google Scholar 

  43. Crump, B. C., Baross, J. A. & Simenstad, C. A. Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquat. Microb. Ecol. 14, 7–18 (1998).

    Article  Google Scholar 

  44. Decho, A. W. Microbial biofilms in intertidal systems: an overview. Cont. Shelf Res. 20, 1257–1273 (2000).

    Article  Google Scholar 

  45. Loreau, M., Mouquet, N. & Holt., R. D. Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecol. Lett. 6, 673–679 (2003).

    Article  Google Scholar 

  46. Elwood, J. W., Newbold, J. D., O'Neill, R. V. & van Winkle, W. in Dynamics of Lotic Ecosystems (eds Fontaine, T. D & Bartell, S. M.) 3–27 (Ann Arbor Science Publisher, Ann Arbor, Michigan, 1983).

    Google Scholar 

  47. Rothman, D. H. & Forney, D. C. Physical model for the decay and preservation of marine organic carbon. Science 316, 1325–1328 (2007).

    Article  Google Scholar 

  48. Kaplan, L. A. & Newbold, J. D. in Aquatic ecosystems. Interactivity of Dissolved Organic Matter (eds Findlay, S. E. G. & Sinsabaugh, R. L.) (Academic Press, Massachusetts, 2003).

    Google Scholar 

  49. Tranvik, L. J. & Bertilsson, S. Contrasting effects of solar UV radiation on dissolved organic sources for bacterial growth. Ecol. Lett. 4, 458–463 (2001).

    Article  Google Scholar 

  50. Grossart, H.-P. & Ploug, H. Bacterial production and growth efficiencies: Direct measurements on riverine aggregates. Limnol. Oceanogr. 45, 436–445 (2000).

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank Kenneth Bencala, Robert Runkel and Björn Gücker for making available data from tracer experiments. Patrick J. Mulholland, Robert Hall, Jeff Houser, Urs Ühlinger and Walter Dodds provided data on whole-ecosystem metabolism. Wilfred F. Wollheim, Balazs M. Feteke and Charles Vörösmarty generously made available unpublished data on stream and river surface area. Our work in this area is supported by the FWF (P16935-B03, S10005-B17) and ESF (I43-B06) to T.J.B., NSF (DEB-0516516, EAR 0450331) to L.A.K., NSF (OCE-0423565, DEB-0614282, BCS-0709685) to C.S.H., NSF (EAR-0408744) to A.I.P. and the Spanish Ministry of Education and Science to E.M. T.J.B. and A.I.P. are affiliates of NSF EAR-0636043.

Author information

Authors and Affiliations

Authors

Contributions

T.J.B. initiated, conceived and coordinated the paper; L.A.K. contributed to the concept and writing; C.S.H. contributed the estuarine part; A.I.P. and J.D.N. contributed the description of solute transport dynamics; S.F., E.M. and F.S. contributed the opportunity, capacity and performance concept.

Corresponding author

Correspondence to Tom J. Battin.

Supplementary information

Supplementary Information

Supplementary information S1 and S2 (PDF 214 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Battin, T., Kaplan, L., Findlay, S. et al. Biophysical controls on organic carbon fluxes in fluvial networks. Nature Geosci 1, 95–100 (2008). https://doi.org/10.1038/ngeo101

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo101

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing