Skip to main content

Fast mineralization of land-born C in inland waters: first experimental evidences of aquatic priming effect

Abstract

In the context of global change, eroded soil carbon fate and its impact on aquatic ecosystems CO2 emissions are subject to intense debates. In particular, soil carbon mineralization could be enhanced by its interaction with autochthonous carbon, a process called priming effect, but experimental evidences of this process are scarce. We measured in a microcosm experiment simulating oligo-mesotrophic and eutrophic aquatic conditions how quickly soil organic matter (SOM) sampled in diverse ecosystems was mineralized as compared to mineralization within soil horizons. For both nutrient loads, 13C-glucose was added to half of the microcosms to simulate exudation of labile organic matter (LOM) by phytoplankton. Effects of LOM on soil mineralization were estimated using the difference in δ13C between the SOM and the glucose. After 45 days of incubation, the mean SOM mineralization was 63% greater in the aquatic context, the most important CO2 fluxes arising during the first days of incubation. Nutrients had no significant effect on SOM mineralization and glucose addition increased by 12% the mean SOM mineralization, evidencing the occurrence of a priming effect.

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

Fig. 1
Fig. 2
Fig. 3

References

  • Aufdenkampe, A. K., E. Mayorga, P. A. Raymond, J. M. Melack, S. C. Doney, S. R. Alin, R. E. Aalto & K. Yoo, 2011. Riverine coupling of biogeochemical cycles between land, oceans, and atmosphere. Frontiers in Ecology and the Environment 9: 53–60.

    Article  Google Scholar 

  • Balabane, M. & A. Plante, 2004. Aggregation and carbon storage in silty soil using physical fractionation techniques. European Journal of Soil Science 55: 415–427.

    Article  Google Scholar 

  • Barré, P., T. Eglin, B. T. Christensen, P. Ciais, S. Houot, T. Kätterer, F. van Oort, P. Peylin, P. R. Poulton, V. Romanenkov & C. Chenu, 2010. Quantifying and isolating stable soil organic carbon using long-term bare fallow experiments. Biogeosciences 7: 3839–3850.

    Article  Google Scholar 

  • Berhe, A. A., E. Carpenter, L. Codispoti, A.-M. Izac, J. Lemoalle, F. Luizao, M. Scholes, P. Tréguer & B. Ward, 2005. Nutrient cycling, Chap. 12. In Hassan, R. et al. (eds) Ecosystems and Human Well-Being: Current State and Trends. Millennium Ecosystem Assessment, Island Press, Washington, DC: 722.

  • Blagodatskaya, E. V., S. A. Blagodatsky, T. H. Anderson & Y. Kuzyakov, 2007. Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Applied Soil Ecology 37: 95–105.

    Article  Google Scholar 

  • Carlson R. E. & J. Simpson, 1996. A Coordinator’s Guide to Volunteer Lake Monitoring Methods. North American Lake Management Society, Madison: 96 pp.

  • Carlson, C. A., S. J. Giovannoni, D. A. Hansell, S. J. Goldberg, R. Parsons, M. P. Otero, K. Vergin & B. R. Wheeler, 2002. Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquatic Microbial Ecology 30: 19–36.

    Article  Google Scholar 

  • Cheng, W., 1999. Rhizosphere feedbacks in elevated CO2. Tree Physiology 19: 313–320.

    Article  PubMed  Google Scholar 

  • Cole, J. J., Y. T. Prairie, N. F. Caraco, W. H. McDowell, L. J. Tranvik, R. G. Striegl, C. M. Duarte, P. Kortelainen, J. A. Downing, J. J. Middelburg & J. Melack, 2007. Plumbing the global carbon cycle: integrating inland waters into the Terrestrial Carbon Budget. Ecosystems 10: 172–185.

    Article  Google Scholar 

  • Craine, J. M., C. Morrow & N. Fierer, 2007. Microbial nitrogen limitation increases decomposition. Ecology 88: 2105–2113.

    Article  PubMed  Google Scholar 

  • Danger, M., J. Cornut, E. Chauvet, P. Chavez, A. Elger & A. Lecerf, 2013. Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect? Ecology. doi:10.1890/12-0606.1.

  • De Haan, H., 1977. Effect of benzoate on microbial decomposition of fulvic acids in Tjeukemeer (Netherlands). Limnology and Oceanography 22: 38–44.

    Article  Google Scholar 

  • Dean, W. E. & E. Gorham, 1998. Magnitude and significance of carbon burial in lakes, reservoirs, and peatlands. Geology 26: 535–538.

    Article  Google Scholar 

  • del Giorgio, P. A., J. J. Cole & A. Cimbleris, 1997. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385: 148–151.

    Article  Google Scholar 

  • Dodds, W. K. & J. J. Cole, 2007. Expanding the concept of trophic state in aquatic ecosystems: it’s not just the autotrophs. Aquatic Sciences 69: 427–439.

    Article  CAS  Google Scholar 

  • Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers & F. Smith, 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28: 350–356.

    Article  CAS  Google Scholar 

  • Farjalla, V., C. C. Marinho, B. M. Faria, A. M. Amado, F. A. Esteves, R. L. Bozelli & D. Giroldo, 2009. Synergy of fresh and accumulated organic matter to bacterial growth. Microbial Ecology 57: 657–666.

    Article  PubMed  CAS  Google Scholar 

  • Fontaine, S., G. Bardoux, L. Abbadie & A. Mariotti, 2004. Carbon input to soil may decrease soil carbon content. Ecology Letters 7: 314–320.

    Article  Google Scholar 

  • Fontaine, S., S. Barot, P. Barré, N. Bdioui, B. Mary & C. Rumpel, 2007. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450: 277–280.

    Article  PubMed  CAS  Google Scholar 

  • Gastine, A., M. Scherer-Lorenzen & P. W. Leadley, 2003. No consistent effects of plant diversity on root biomass, soil biota and soil abiotic conditions in temperate grassland communities. Applied Soil Ecology 24: 101–111.

    Article  Google Scholar 

  • Goodman, K. J., M. A, Baker & W. A., Wurtsbaugh, 2011. Lakes as buffers of stream dissolved organic matter (DOM) variability: temporal patterns of DOM characteristics in mountain stream-lake systems. Journal of Geophysical Research 116:G00N02.

    Google Scholar 

  • Guenet, B., M. Danger, L. Abbadie & G. Lacroix, 2010a. Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecology 91: 2850–2861.

    Article  PubMed  Google Scholar 

  • Guenet, B., J. Leloup, X. Raynaud, G. Bardoux & L. Abbadie, 2010b. Negative priming effect on mineralization in a soil free of vegetation for 80 years. European Journal of Soil Science 61: 384–391.

    Article  CAS  Google Scholar 

  • Guenet, B., C. Neill, G. Bardoux & L. Abbadie, 2010c. Is there a linear relationship between priming effect intensity and the amount of organic matter input? Applied Soil Ecology 46: 436–442.

    Article  Google Scholar 

  • Hamer, U., B. Marschner, S. Brodowski & W. Amelung, 2004. Interactive priming of black carbon and glucose mineralization. Organic Geochemistry 35: 823–830.

    Article  CAS  Google Scholar 

  • Hamilton, D. & S. Mitchell, 1996. An empirical model for sediment resuspension in shallow lakes. Hydrobiologia 317: 209–220.

    Article  Google Scholar 

  • Houghton, R. A., 2007. Balancing the global carbon budget. Annual Review Earth and Planetary Sciences 35: 313–347.

    Article  CAS  Google Scholar 

  • Johnsen, K., C. S. Jacobsen, V. Torsvik & J. Sørensen, 2001. Pesticide effects on bacterial diversity in agricultural soils – a review. Biology and Fertility of Soils 33: 443–453.

    Article  CAS  Google Scholar 

  • Kilham, S. S., D. A. Kreeger, S. G. Lynn, C. E. Goulden & L. Herrera, 1998. COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377: 147–159.

    Article  CAS  Google Scholar 

  • Kraus, T. E. C., R. A. Dahlgren & R. J. Zasoski, 2003. Tannins in nutrient dynamics of forest ecosystems – a review. Plant and Soil 256: 41–66.

    Article  CAS  Google Scholar 

  • Kuzyakov, Y., J. K. Friedel & K. Stahr, 2000. Review of mechanisms and quantification of priming effects. Soil Biology and Biochemistry 32: 1485–1498.

    Article  CAS  Google Scholar 

  • Lal, R., 2003. Soil erosion and the global carbon budget. Environment International 29: 437–450.

    Article  PubMed  CAS  Google Scholar 

  • Lal, R., 2005. Soil erosion and carbon dynamics. Soil and Tillage Research 81: 137–142.

    Article  Google Scholar 

  • Lal, R. & D. Pimentel, 2008. Soil erosion: a carbon sink or source? Science 319: 1040–1041.

    Article  PubMed  CAS  Google Scholar 

  • Lehmann, J., D. Solomon, J. Kinyangi, L. Dathe, S. Wirick & C. Jacobsen, 2008. Spatial complexity of soil organic matter forms at nanometre scales. Nature Geoscience 1: 238–242.

    Article  CAS  Google Scholar 

  • Loranger-Merciris, G., L. Barthes, A. Gastine & P. W. Leadley, 2006. Rapid effects of plant species diversity and identity on soil microbial communities in experimental grassland ecosystems. Soil Biology and Biochemistry 38: 2336–2343.

    Article  CAS  Google Scholar 

  • Lowry, O. H., N. J. Rosebrough, A. L. Farr & R. J. Randall, 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193: 265–275.

    PubMed  CAS  Google Scholar 

  • Martin-Olmedo, P., R. M. Rees & J. Grace, 2002. The influence of plants grown under elevated CO2 and N fertilization on soil nitrogen dynamics. Global Change Biology 8: 643–657.

    Article  Google Scholar 

  • McCallister, S. L. & P. A. Del Giorgio, 2012. Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams. Proceedings of the National Academy of Sciences of the United States of America 109: 16963–16968.

    Article  PubMed  CAS  Google Scholar 

  • Moorhead, D. & R. Sinsabaugh, 2006. A theoretical model of litter decay and microbial interaction. Ecological Monographs 76: 151–174.

    Article  Google Scholar 

  • Myklestad, S., 1995. Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Science of the Total Environment 165: 155–164.

    Article  CAS  Google Scholar 

  • Nugteren, P., L. Moodley, G.-J. Brummer, C. H. Heip, P. M. J. Herman & J. J. Middelburg, 2009. Seafloor ecosystem functioning: the importance of organic matter priming. Marine Biology 156: 2277–2287.

    Article  Google Scholar 

  • Nunan, N., K. Wu, I. M. Young, J. W. Crawford & K. Ritz, 2003. Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil. FEMS Microbiology Ecology 44: 203–215.

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team, 2008. R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing. Vienna, Austria.

  • Shimp, R. & F. K. Pfaender, 1985. Influence of naturally occurring humic acids on biodegradation of monosubstituted phenols by aquatic bacteria. Applied and Environmental Microbiology 49: 402–407.

    PubMed  CAS  Google Scholar 

  • Smith, S., W. Renwick, R. Buddemeier & C. Crossland, 2001. Budgets of soil erosion and deposition for sediments and sedimentary organic carbon across the conterminous United States. Global Biogeochemical Cycles 15: 697–707.

    Article  CAS  Google Scholar 

  • Terrence, J. T., G. R. Foster & K. G. Renard, 2002. Soil Erosion: Processes, Prediction, Measurement, and Control. Wiley, New York.

    Google Scholar 

  • Van Oost, K., T. A. Quine, G. Govers, S. De Gryze, J. Six, J. W. Harden, J. C. Ritchie, G. W. McCarty, G. Heckrath, C. Kosmas, J. V. Giraldez, J. R. M. da Silva & R. Merckx, 2007. The impact of agricultural soil erosion on the global carbon cycle. Science 318: 626–629.

    Article  PubMed  Google Scholar 

  • vön Lutzow, M., I. Kogel-Knabner, K. Ekschmitt, E. Matzner, G. Guggenberger, B. Marschner & H. Flessa, 2006. Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions – a review. European Journal of Soil Science 57: 426–445.

    Article  Google Scholar 

  • Wetzel, R. G., 1990. Landwater interfaces: metabolic and Limnological regulators. Verhandlungen der Internationalen Vereinigung fur Theoretische und Angewandte Limnologie 24: 6–24.

    Google Scholar 

Download references

Acknowledgments

The authors thank ANR Biofun and R2DS for financial support, J.P. Petraud and the INRA Versailles for maintaining the Closeaux and 42 plots long-term experiments. The authors acknowledge Emma Rochelle-Newall, Philippe Ciais, and Sebastian Luyssaert for providing comments and suggestions. Bertrand Guenet was a visiting international fellow funded by the Fund for Scientific Research-Flanders (FWO).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bertrand Guenet.

Additional information

Handling editor: Luigi Naselli-Flores

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 220 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Guenet, B., Danger, M., Harrault, L. et al. Fast mineralization of land-born C in inland waters: first experimental evidences of aquatic priming effect. Hydrobiologia 721, 35–44 (2014). https://doi.org/10.1007/s10750-013-1635-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-013-1635-1

Keywords