Plant–microbial competition for nitrogen increases microbial activities and carbon loss in invaded soils

Abstract

Many invasive plant species show high rates of nutrient acquisition relative to their competitors. Yet the mechanisms underlying this phenomenon, and its implications for ecosystem functioning, are poorly understood, particularly in nutrient-limited systems. Here, we test the hypothesis that an invasive plant species (Microstegium vimineum) enhances its rate of nitrogen (N) acquisition by outcompeting soil organic matter-degrading microbes for N, which in turn accelerates soil N and carbon (C) cycling. We estimated plant cover as an indicator of plant N acquisition rate and quantified plant tissue N, soil C and N content and transformations, and extracellular enzyme activities in invaded and uninvaded plots. Under low ambient N availability, invaded plots had 77% higher plant cover and lower tissue C:N ratios, suggesting that invasion increased rates of plant N acquisition. Concurrent with this pattern, we observed significantly higher mass-specific enzyme activities in invaded plots as well as 71% higher long-term N availability, 21% lower short-term N availability, and 16% lower particulate organic matter N. A structural equation model showed that these changes were interrelated and associated with 27% lower particulate organic matter C in invaded areas. Our findings suggest that acquisition of N by this plant species enhances microbial N demand, leading to an increased flux of N from organic to inorganic forms and a loss of soil C. We conclude that high N acquisition rates by invasive plants can drive changes in soil N cycling that are linked to effects on soil C.

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Acknowledgements

This project was supported by a grant from the National Science Foundation to the Coweeta Long Term Ecological Research (LTER) program (DEB-0,823,293), and by an Odell Soil Science Fellowship, Garden Club of Downer’s grove scholarship, and Spaeth-Boggess scholarship for M. Craig. We acknowledge S. Pearson for his expertise and guidance during field work. We thank M. Hamilton, E. McGrath, C. Grabowski, and J. Horton for their contributions to this work, and two anonymous reviewers and the Editor, Pascal Niklaus, for their helpful feedback on the manuscript. Finally, we thank the many landowners and agencies who allowed access to field sites.

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MEC and JMF conceived and designed the study. MEC carried out the study and analyzed the data. MEC and JMF wrote the manuscript.

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Correspondence to Matthew E. Craig.

Additional information

We find evidence that intensified competition for a limiting resource enhances the microbial breakdown of organic matter in soils occupied by invasive plants, ultimately leading to a shift in soil nutrients from organic to inorganic forms and a decrease in soil carbon storage. This work proposes a mechanism by which invasive plants might enhance nutrient acquisition in nutrient-limited soils and is one of the first investigations to demonstrate linkages between carbon and nutrient cycling in invaded systems.

Communicated by Pascal A. Niklaus.

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Craig, M.E., Fraterrigo, J.M. Plant–microbial competition for nitrogen increases microbial activities and carbon loss in invaded soils. Oecologia 184, 583–596 (2017). https://doi.org/10.1007/s00442-017-3861-0

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Keywords

  • Invasive plants
  • Nutrient uptake
  • Soil carbon
  • Enzyme activities
  • Nitrogen limitation