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Nitrogen status regulates morphological adaptation of marsh plants to elevated CO2

Nature Climate Change volume 9, pages 764–768 (2019)Cite this article

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Abstract

Coastal wetlands provide valuable ecosystem services that are increasingly threatened by anthropogenic activities1. The atmospheric carbon dioxide (CO2) concentration has increased from 280 ppm to 404 ppm since the Industrial Revolution and is projected to exceed 900 ppm by 2100 (ref. 2). In terrestrial ecosystems, elevated CO2 typically stimulates C3 plant photosynthesis and primary productivity leading to an increase in plant size3. However, compared with woody plants or crops4, the morphological responses of clonal non-woody plants to elevated CO2 have rarely been examined. We show that 30 years of experimental CO2 enrichment in a brackish marsh increased primary productivity and stem density but decreased stem diameter and height of the dominant clonal species Schoenoplectus americanus. Smaller, denser stems were associated with the expansion of roots and rhizomes to alleviate nitrogen (N) limitation as evidenced by high N immobilization in live tissue and litter, high tissue C:N ratio and low available porewater N. Changes in morphology and tissue chemistry induced by elevated CO2 were reversed by N addition. We demonstrate that morphological responses to CO2 and N supply in a clonal plant species influences the capacity of marshes to gain elevation at rates that keep pace with rising sea levels.

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Fig. 1: The response ratios of key parameters from the two experiments.
Fig. 2: Elevated CO2 responses of individual stems of S. americanus in the C3 community of Experiment 1 from 1987 to 2016.
Fig. 3: A conceptual framework for the responses of clonal plant aboveground growth pattern to CO2 enrichment and nitrogen availability.

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Data availability

Morphometric and derived biomass data from the experiments are posted on the Global Change Research Wetland website (http://serc.si.edu/gcrew/data) and all data are available from the corresponding authors upon request.

References

  1. Kirwan, M. L. & Megonigal, J. P. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504, 53–60 (2013).

    Article  CAS  Google Scholar 

  2. Collins, M. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) Ch. 12 (IPCC, Cambridge Univ. Press, 2013).

  3. Curtis, P. S. & Wang, X. Z. A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113, 299–313 (1998).

    Article  Google Scholar 

  4. Long, S. P. et al. Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312, 1918–1920 (2006).

    Article  CAS  Google Scholar 

  5. Luethi, D. et al. High-resolution carbon dioxide concentration record 650,000–800,000 years before present. Nature 453, 379–382 (2008).

    Article  CAS  Google Scholar 

  6. Ainsworth, E. A. & Rogers, A. The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant Cell Environ. 30, 258–270 (2007).

    Article  CAS  Google Scholar 

  7. Pritchard, S. G. et al. Elevated CO2 and plant structure: a review. Glob. Change Biol. 5, 807–837 (1999).

    Article  Google Scholar 

  8. Wand, S. J. E. et al. Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob. Change Biol. 5, 723–741 (1999).

    Article  Google Scholar 

  9. Ainsworth, E. A. & Long, S. P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol. 165, 351–371 (2005).

    Article  Google Scholar 

  10. Yang, L. X. et al. Seasonal changes in the effects of free-air CO2 enrichment (FACE) on growth, morphology and physiology of rice root at three levels of nitrogen fertilization. Glob. Change Biol. 14, 1844–1853 (2008).

    Article  Google Scholar 

  11. Schwinning, S. & Weiner, J. Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113, 447–455 (1998).

    Article  Google Scholar 

  12. White, K. P. et al. C3 and C4 biomass allocation responses to elevated CO2 and nitrogen: contrasting resource capture strategies. Estuaries Coasts 35, 1028–1035 (2012).

    Article  CAS  Google Scholar 

  13. Terrer, C. et al. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353, 72–74 (2016).

    Article  CAS  Google Scholar 

  14. Hutchings, M. J. & Dekroon, H. Foraging in plants: the role of morphological plasticity in resource acquisition. Adv. Ecol. Res. 25, 159–238 (1994).

    Article  Google Scholar 

  15. Callaghan, T. V. et al. Clonal plants and environmental change: introduction to the proceedings and summary. Oikos 63, 341–347 (1992).

    Article  Google Scholar 

  16. Lu, M. et al. Allometry data and equations for coastal marsh plants. Ecology 97, 3554 (2016).

    Article  Google Scholar 

  17. Reynolds, H. L. & Pacala, S. W. An analytical treatment of root-to-shoot ratio and plant competition for soil nutrient and light. Am. Nat. 141, 51–70 (1993).

    Article  CAS  Google Scholar 

  18. Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115 (1991).

    Article  Google Scholar 

  19. Luo, Y. et al. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54, 731–739 (2004).

    Article  Google Scholar 

  20. Craine, J. M. et al. Isotopic evidence for oligotrophication of terrestrial ecosystems. Nat. Ecol. Evol. 2, 1735–1744 (2018).

    Article  Google Scholar 

  21. Niu, S. L. et al. Nitrogen regulation of the climate-carbon feedback: evidence from a long-term global change experiment. Ecology 91, 3261–3273 (2010).

    Article  Google Scholar 

  22. Nie, M. et al. Altered root traits due to elevated CO2: a meta-analysis. Glob. Ecol. Biogeogr. 22, 1095–1105 (2013).

    Article  Google Scholar 

  23. Ikegami, M. Functional Specialization of Ramets in a Clonal Plant Network. PhD thesis, Utrecht Univ. (2004).

  24. Gedan, K. B. et al. The present and future role of coastal wetland vegetation in protecting shorelines: answering recent challenges to the paradigm. Climatic Change 106, 7–29 (2011).

    Article  Google Scholar 

  25. Sheng, Y. P. et al. The reduction of storm surge by vegetation canopies: three-dimensional simulations. Geophys. Res. Lett. 39, L20601 (2012).

    Article  Google Scholar 

  26. Vandolah, R. F. Factors regulating the distribution and population dynamics of the amphipod Gammarus palustris in an intertidal salt marsh community. Ecol. Monogr. 48, 191–217 (1978).

    Article  Google Scholar 

  27. Bertness, M. D. Fiddler crab regulation of Spartina alterniflora production on a New England salt marsh. Ecology 66, 1042–1055 (1985).

    Article  Google Scholar 

  28. Zedler, J. B. Canopy architecture of natural and planted cordgrass marshes: selecting habitat evaluation criteria. Ecol. Appl. 3, 123–138 (1993).

    Article  Google Scholar 

  29. Drake, B. G. Rising sea level, temperature, and precipitation impact plant and ecosystem responses to elevated CO2 on a Chesapeake Bay wetland: review of a 28-year study. Glob. Change Biol. 20, 3329–3343 (2014).

    Article  Google Scholar 

  30. Nyman, J. A. et al. Marsh vertical accretion via vegetative growth. Estuar. Coast. Shelf Sci. 69, 370–380 (2006).

    Article  Google Scholar 

  31. Cherry, J. A., McKee, K. L. & Grace, J. B. Elevated CO2 enhances biological contributions to elevation change in coastal wetlands by offsetting stressors associated with sea-level rise. J. Ecol. 97, 67–77 (2009).

    Article  Google Scholar 

  32. Langley, J. A. et al. Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise. Proc. Natl Acad. Sci. USA 106, 6182–6186 (2009).

    Article  CAS  Google Scholar 

  33. Morris, J. T. et al. Responses of coastal wetlands to rising sea level. Ecology 83, 2869–2877 (2002).

    Article  Google Scholar 

  34. Darke, A. K. & Megonigal, J. P. Control of sediment deposition rates in two mid-Atlantic Coast tidal freshwater wetlands. Estuar. Coast. Shelf Sci. 57, 255–268 (2003).

    Article  Google Scholar 

  35. Mudd, S. M. et al. How does vegetation affect sedimentation on tidal marshes? Investigating particle capture and hydrodynamic controls on biologically mediated sedimentation. J. Geophys. Res. Earth Surf. 115, F03029 (2010).

    Google Scholar 

  36. Kirwan, M. L. & Mudd, S. M. Response of salt-marsh carbon accumulation to climate change. Nature 489, 550–553 (2012).

    Article  CAS  Google Scholar 

  37. Deegan, L. A. et al. Coastal eutrophication as a driver of salt marsh loss. Nature 490, 388–393 (2012).

    Article  CAS  Google Scholar 

  38. Rasse, D. P., Peresta, G. & Drake, B. G. Seventeen years of elevated CO2 exposure in a Chesapeake Bay wetland: sustained but contrasting responses of plant growth and CO2 uptake. Glob. Change Biol. 11, 369–377 (2005).

    Article  Google Scholar 

  39. Pastore, M. A. et al. Elevated CO2 and nitrogen addition accelerate net carbon gain in a brackish marsh. Biogeochemistry 133, 73-87 (2017).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank B. Drake for conceiving the original study and leading it until 2010 and G. Peresta for operating the experiment and leading the annual census for nearly all of the 30-year record. We also thank J. Duls, A. Peresta, A. Cawood and the hundreds of volunteers who helped collect data during annual censuses. D. Whigham, T. Jordan, C. Gallegos, J. O’Neill, C. Zhu and H. Guo provided insights or contextual data. This research was supported by the DOE-TES programme (grant no. DE-SC0008339), the NSF-LTREB programme (grant nos. DEB-0950080 and DEB-1457100), the Maryland Sea Grant programme (grant no. SA7528114-WW) and the Thousand Young Talents Program of Yunnan Province.

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Authors and Affiliations

  1. Smithsonian Environmental Research Center, Edgewater, MD, USA

    Meng Lu, J. Adam Langley & J. Patrick Megonigal

  2. School of Ecology and Environmental Sciences, Yunnan University, Kunming, China

    Meng Lu

  3. Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, USA

    Ellen R. Herbert & Matthew L. Kirwan

  4. Department of Biology, Villanova University, Villanova, PA, USA

    J. Adam Langley

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  1. Meng Lu
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  4. Matthew L. Kirwan
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  5. J. Patrick Megonigal
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Contributions

The analysis was conceived by M.L. and J.P.M. The ongoing operation of the experiments was conducted by J.P.M. and J.A.L. The data were compiled and analysed by M.L. Accretion modelling was performed by E.H. All authors contributed to writing the paper.

Corresponding authors

Correspondence to Meng Lu or J. Patrick Megonigal.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Ming Nie and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Information

Supplementary Tables 1–3, Figs. 1–7 and references.

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Lu, M., Herbert, E.R., Langley, J.A. et al. Nitrogen status regulates morphological adaptation of marsh plants to elevated CO2. Nat. Clim. Chang. 9, 764–768 (2019). https://doi.org/10.1038/s41558-019-0582-x

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