Letter | Published:

Wetland carbon storage controlled by millennial-scale variation in relative sea-level rise

Naturevolume 567pages9195 (2019) | Download Citation

Abstract

Coastal wetlands (mangrove, tidal marsh and seagrass) sustain the highest rates of carbon sequestration per unit area of all natural systems1,2, primarily because of their comparatively high productivity and preservation of organic carbon within sedimentary substrates3. Climate change and associated relative sea-level rise (RSLR) have been proposed to increase the rate of organic-carbon burial in coastal wetlands in the first half of the twenty-first century4, but these carbon–climate feedback effects have been modelled to diminish over time as wetlands are increasingly submerged and carbon stores become compromised by erosion4,5. Here we show that tidal marshes on coastlines that experienced rapid RSLR over the past few millennia (in the late Holocene, from about 4,200 years ago to the present) have on average 1.7 to 3.7 times higher soil carbon concentrations within 20 centimetres of the surface than those subject to a long period of sea-level stability. This disparity increases with depth, with soil carbon concentrations reduced by a factor of 4.9 to 9.1 at depths of 50 to 100 centimetres. We analyse the response of a wetland exposed to recent rapid RSLR following subsidence associated with pillar collapse in an underlying mine and demonstrate that the gain in carbon accumulation and elevation is proportional to the accommodation space (that is, the space available for mineral and organic material accumulation) created by RSLR. Our results suggest that coastal wetlands characteristic of tectonically stable coastlines have lower carbon storage owing to a lack of accommodation space and that carbon sequestration increases according to the vertical and lateral accommodation space6 created by RSLR. Such wetlands will provide long-term mitigating feedback effects that are relevant to global climate–carbon modelling.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Data availability

The data used in the global analysis of carbon concentration with respect to Holocene RSLR are provided in the Supplementary Information. The data that support the Chain Valley Bay study site analysis are available from the corresponding author upon reasonable request.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Donato, D. C. et al. Mangroves among the most carbon-rich forests in the tropics. Nat. Geosci. 4, 293–297 (2011).

  2. 2.

    Mcleod, E. et al. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front. Ecol. Environ. 9, 552–560 (2011).

  3. 3.

    Duarte, C. M., Middelburg, J. & Caraco, N. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2, 1–8 (2005).

  4. 4.

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

  5. 5.

    DeLaune, R. & White, J. Will coastal wetlands continue to sequester carbon in response to an increase in global sea level? A case study of the rapidly subsiding Mississippi river deltaic plain. Clim. Change 110, 297–314 (2012).

  6. 6.

    Schuerch, M. et al. Future response of global coastal wetlands to sea-level rise. Nature 561, 231–234 (2018).

  7. 7.

    Holmquist, J. R. et al. Accuracy and precision of tidal wetland soil carbon mapping in the conterminous United States. Sci. Rep. 8, 9478 (2018); corrigendum 8, 15219 (2018).

  8. 8.

    Murray-Wallace, C. V. & Woodroffe, C. D. Quaternary Sea-Level Changes: A Global Perspective (Cambridge Univ. Press, Cambridge, 2014).

  9. 9.

    Clark, J. A., Farrell, W. E. & Peltier, W. R. Global changes in postglacial sea level: a numerical calculation. Quat. Res. 9, 265–287 (1978).

  10. 10.

    Redfield, A. C. Development of a New England salt marsh. Ecol. Monogr. 42, 201–237 (1972).

  11. 11.

    Morris, J. T., Sundareshwar, P. V., Nietch, C. T., Kjerfve, B. & Cahoon, D. R. Responses of coastal wetlands to rising sea-levels. Ecology 83, 2869–2877 (2002).

  12. 12.

    Lovelock, C. E. et al. The vulnerability of Indo-Pacific mangrove forests to sea-level rise. Nature 526, 559–563 (2015).

  13. 13.

    Adam, P. Saltmarsh Ecology (Cambridge Univ. Press, Cambridge, 1990).

  14. 14.

    Hiraishi, T. et al. (eds) 2013 Supplement to the 2006 IPCC Guidelines for National Greenhouse Gas Inventories: Wetlands. Technical Report (IPCC, 2014).

  15. 15.

    Saintilan, N. & Hashimoto, T. R. Mangrove-saltmarsh dynamics on a bay-head delta in the Hawkesbury River estuary, New South Wales, Australia. Hydrobiologia 413, 95–102 (1999).

  16. 16.

    Woodroffe, C. D., Thom, B. G. & Chappell, J. Development of widespread mangrove swamps in mid-Holocene times in northern Australia. Nature 317, 711–713 (1985).

  17. 17.

    Allen, J. R. L. Morphodynamics of Holocene salt marshes: a review sketch from the Atlantic and Southern North Sea coasts of Europe. Quat. Sci. Rev. 19, 1155–1231 (2000).

  18. 18.

    Pethick, J. S. Long-term accretion rates on tidal salt marshes. J. Sediment. Res. 51, 571–577 (1981).

  19. 19.

    Ouyang, X. & Lee, S. Updated estimates of carbon accumulation rates in coastal marsh sediments. Biogeosciences 11, 5057–5071 (2014).

  20. 20.

    Kirwan, M. L. & Guntenspergen, G. R. Influence of tidal range on the stability of coastal marshland. J. Geophys. Res. 115, F02009 (2010).

  21. 21.

    Krauss, K. W. et al. How mangrove forests adjust to rising sea level. New Phytol. 202, 19–34 (2014).

  22. 22.

    Langley, J. A., McKee, K. L., Cahoon, D. R., Cherry, J. A. & Megonigal, J. P. Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise. Proc. Natl Acad. Sci. USA 106, 6182–6186 (2009).

  23. 23.

    Sloss, C. R., Murray-Wallace, C. V. & Jones, B. G. Holocene sea-level change on the southeast coast of Australia: a review. Holocene 17, 999–1014 (2007).

  24. 24.

    Lambeck, K. & Nakada, M. Late Pleistocene and Holocene sea-level change along the Australian coast. Palaeogeogr. Palaeoclimatol. Palaeoecol. 89, 143–176 (1990).

  25. 25.

    Kelleway, J. J. et al. Seventy years of continuous encroachment substantially increases ‘blue carbon’ capacity as mangroves replace intertidal salt marshes. Glob. Change Biol. 22, 1097–1109 (2016).

  26. 26.

    Duke, N. C. et al. A world without mangroves? Science 317, 41–42 (2007).

  27. 27.

    Duarte, C., Dennison, W., Orth, R. & Carruthers, T. The charisma of coastal ecosystems: addressing the imbalance. Estuaries Coasts 31, 233–238 (2008).

  28. 28.

    Crooks, S., Herr, D., Tamelander, J., Laffoley, D. & Vandever, J. Mitigating Climate Change through Restoration and Management of Coastal Wetlands and Near-Shore Marine Ecosystems: Challenges and Opportunities (World Bank Environment Department, Washington DC, 2011).

  29. 29.

    Pontee, N. Defining coastal squeeze: a discussion. Ocean Coast. Manage. 84, 204–207 (2013).

  30. 30.

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

  31. 31.

    Chmura, G. L., Anisfeld, S. C., Cahoon, D. R. & Lynch, J. C. Global carbon sequestration in tidal, saline wetland soils. Glob. Biogeochem. Cycles 17, 1111 (2003).

  32. 32.

    Craft, C., Seneca, E. & Broome, S. Loss on ignition and Kjeldahl digestion for estimating organic carbon and total nitrogen in estuarine marsh soils: calibration with dry combustion. Estuaries Coasts 14, 175–179 (1991).

  33. 33.

    Shennan, I. & Horton, B. Holocene land- and sea-level changes in Great Britain. J. Quaternary Sci. 17, 511–526 (2002).

  34. 34.

    Pluet, J. & Pirazzoli, P. World Atlas of Holocene Sea-Level Changes Vol. 58 (Elsevier, Amsterdam, 1991).

  35. 35.

    Verbeke, G. in Linear Mixed Models in Practice (eds Verbeke, G. & Molenberghs, G.) 63–153 (Springer, New York, 1997).

  36. 36.

    von Ende, C. N. in Design and Analysis of Ecological Experiments (eds Scheiner, S. M. & Gurevitch, J.) 134–157 (Oxford Univ. Press, New York, 2001).

  37. 37.

    Hollins, S. et al. Reconstructing recent sedimentation in two urbanised coastal lagoons (NSW, Australia) using radioisotopes and geochemistry. J. Paleolimnol. 46, 579–596 (2011).

  38. 38.

    Appleby, P. in Tracking Environmental Change Using Lake Sediments (eds Smol, J. P. et al.) 171–203 (Kluwer, Dordrecht 2001).

Download references

Acknowledgements

This research was supported by the Australian Research Council (FT130100532), AINSE (ALNGRA13046) and the UOW Global Challenges Program. The Smithsonian Environmental Research Center supported J.P.M., J.R.H, M.L. and L.S.-B. The data curation efforts of J.R.H. and data collection and synthesis efforts of J.P.M. were supported by United States National Science Foundation grants to the Coastal Carbon Research Coordination Network (DEB-1655622) and the Global Change Research Wetland (DEB-0950080, DEB-1457100 and DEB-1557009) and by a NASA Carbon Monitoring System programme grant (NNH14AY67I). L.S.-B. was supported by a Smithsonian Institution MarineGEO Postdoctoral Fellowship. This is contribution number 32 of the Smithsonian’s MarineGEO Network. The authors acknowledge J. Curran for assistance with sample preparation, S. Rasel, S. Oyston and M. Rupic for assistance with data collation and the students who undertook fieldwork as part of this research.

Reviewer information

Nature thanks Andrew Ashton and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

  1. School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, New South Wales, Australia

    • Kerrylee Rogers
    •  & Colin D. Woodroffe
  2. Department of Environmental Sciences, Macquarie University, Sydney, New South Wales, Australia

    • Jeffrey J. Kelleway
    •  & Neil Saintilan
  3. Smithsonian Environmental Research Center, Edgewater, MD, USA

    • J. Patrick Megonigal
    • , James R. Holmquist
    • , Meng Lu
    •  & Lisa Schile-Beers
  4. Department of Botany, Nelson Mandela University, Port Elizabeth, South Africa

    • Janine B. Adams
  5. School of Ecology and Environmental Sciences, Yunnan University, Kunming, China

    • Meng Lu
  6. Australian Nuclear Science and Technology Organisation, Sydney, New South Wales, Australia

    • Atun Zawadzki
    •  & Debashish Mazumder

Authors

  1. Search for Kerrylee Rogers in:

  2. Search for Jeffrey J. Kelleway in:

  3. Search for Neil Saintilan in:

  4. Search for J. Patrick Megonigal in:

  5. Search for Janine B. Adams in:

  6. Search for James R. Holmquist in:

  7. Search for Meng Lu in:

  8. Search for Lisa Schile-Beers in:

  9. Search for Atun Zawadzki in:

  10. Search for Debashish Mazumder in:

  11. Search for Colin D. Woodroffe in:

Contributions

K.R., N.S. and C.D.W. developed the premise of the study. J.J.K., N.S., J.P.M., J.B.A., J.R.H., M.L., L.S.-B. and K.R. gathered and produced input data for the global analysis. J.J.K. carried out global-scale statistical analyses. K.R., D.M. and A.Z. undertook local-study fieldwork, sample preparation, laboratory and statistical analyses. K.R., J.J.K., N.S. and C.D.W. wrote the paper. All authors contributed to editing and revising the paper.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Kerrylee Rogers.

Extended data figures and tables

  1. Extended Data Fig. 1 Relationship between late-Holocene RSLR and carbon concentration for data-poor late-Holocene RSLR zones and transitional zones.

    ad, Box plots of tidal-marsh soil C concentration for data-poor Holocene RSLR zones and transitional regions: zone I (a), zone II–III transition (b), zone III (c) and zone IV–V transition (d).

  2. Extended Data Fig. 2 210Pb and 137Cs activity of submerged and mangrove sediments.

    ad, Submerged-core supported and total (a) and unsupported (b) 210Pb activity, 137Cs activity (c) and CRS-based 210Pb chronology (d). eh, Mangrove-core supported and total (e) and unsupported (f) 210Pb activity, 137Cs activity (g) and CRS-based 210Pb chronology (h). The grey validation lines confirm that the 137Cs activity peak corresponds to a sediment date of 1963, in agreement with CRS-based 210Pb chronology (core dating occurred in 2014). Source Data

  3. Extended Data Fig. 3 Relationship between sea-surface salinity and C concentration over three depth intervals.

    ac, Regression analysis of C concentration and global-scale sea-surface salinity, derived from the NASA Aquarius Satellite Mission, exhibited extremely weak relationships over the depth intervals 0–20 cm (a; R2 = 0.07, P < 0.001), 20–50 cm (b; R2 = 0.07, P < 0.01) and 50–100 cm (c; R2 = 0.06, P < 0.001). Soil %C values are low for zones I and IV in part owing to the removal of roots before analysis (see Supplementary Table 1). Source Data

  4. Extended Data Fig. 4 Relationship between late-Holocene RSLR and C density for data-rich late-Holocene RSLR zones and transitional zones.

    ad, Box plots of tidal-marsh soil C density for data-rich Holocene RSLR zones and transitional regions: zone I–II transition (a), zone II (b), zone IV (c), and zone V (d). Source Data

  5. Extended Data Table 1 Results of the linear mixed model used for the dependent variable of tidal-marsh soil carbon concentration
  6. Extended Data Table 2 Results of linear-mixed-model pairwise comparisons among Holocene RSLR zones for the dependent variable of tidal-marsh soil carbon concentration
  7. Extended Data Table 3 Results of global data compilation of tidal marsh soil carbon concentration and RM-ANOVA
  8. Extended Data Table 4 Results of the linear mixed model for the dependent variable of tidal marsh soil carbon density (in grams of carbon per cubic centimetre)
  9. Extended Data Table 5 Results of linear-mixed-model pairwise comparisons among Holocene RSLR zones for the dependent variable of tidal-marsh soil carbon density (in grams of carbon per cubic centimetre)
  10. Extended Data Table 6 Results of global data compilation of tidal marsh soil carbon density and RM-ANOVA

Supplementary information

  1. Supplementary Information

    This file contains Supplementary Methods, Supplementary Table and Supplementary References. The Supplementary Methods includes a detailed site description of Chain Valley Bay, Lake Macquarie, Australia, and the method for analysing C density, and the influence of global scale climatic and sea surface salinity variability on carbon concentration. The Supplementary Table includes the compilation of tidal marsh soil carbon concentration used in this study and associated Supplementary References.

Source data

About this article

Publication history

Received

Accepted

Published

Issue Date

DOI

https://doi.org/10.1038/s41586-019-0951-7

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.