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.

  • Perspective
  • Published:

Global-change controls on soil-carbon accumulation and loss in coastal vegetated ecosystems

Abstract

Coastal seagrass, mangrove and salt-marsh ecosystems—also termed blue-carbon ecosystems—play an important role in the global carbon cycle. Much of the organic carbon they store rests in soils that have accumulated over thousands of years. Rapidly changing climate and environmental conditions, including sea-level rise, warming, eutrophication and landscape development, will impact decomposition and thus the global reservoir of blue soil organic carbon. Yet, it remains unclear how these disturbances will affect the key biogeochemical mechanisms controlling decomposition—mineral protection, redox zonation, water content and movement, and plant–microbe interactions. We assess the spatial and temporal scales over which decomposition mechanisms operate and how their effectiveness may change following disturbances. We suggest that better integration of decomposition mechanisms into blue-carbon models may improve predictions of soil organic carbon stores and facilitate incorporation of coastal vegetated ecosystems into global budgets and management tools.

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

Fig. 1: Four key mechanisms affect blue SOC decomposition.
Fig. 2: Disturbances impact decomposition by changing environmental conditions.

Similar content being viewed by others

References

  1. National Academies of Sciences, Engineering, and Medicine Negative Emissions Technologies and Reliable Sequestration: A Research Agenda (The National Academies Press, 2019).

  2. Duarte, C. M., Losada, I. J., Hendriks, I. E., Mazarrasa, I. & Marbà, N. The role of coastal plant communities for climate change mitigation and adaptation. Nat. Clim. Change 3, 961–968 (2013).

    Google Scholar 

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

    Google Scholar 

  4. Atwood, T. B. et al. Global patterns in mangrove soil carbon stocks and losses. Nat. Clim. Change 7, 523–528 (2017).

    Google Scholar 

  5. Fourqurean, J. W. et al. Seagrass ecosystems as a globally significant carbon stock. Nat. Geosci. 5, 505–509 (2012).

    Google Scholar 

  6. Hinson, A. L. et al. The spatial distribution of soil organic carbon in tidal wetland soils of the continental United States. Glob. Change Biol. 23, 5468–5480 (2017).

    Google Scholar 

  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).

    Google Scholar 

  8. Hopkinson, C. S., Morris, J. T., Fagherazzi, S., Wollheim, W. M. & Raymond, P. A. Lateral marsh edge erosion as a source of sediments for vertical marsh accretion. J. Geophys. Res. -Biogeo. 123, 2444–2465 (2018).

    Google Scholar 

  9. Pendleton, L. et al. Estimating global “blue carbon” emissions from conversion and degradation of vegetated coastal ecosystems. PLoS ONE 7, e43542 (2012).

    Google Scholar 

  10. Portnoy, J. W. & Giblin, A. E. Biogeochemical effects of seawater restoration to diked salt marshes. Ecol. Appl. 7, 1054–1063 (1997).

    Google Scholar 

  11. Sanderman, J. et al. A global map of mangrove forest soil carbon at 30 m spatial resolution. Environ. Res. Lett. 13, 055002 (2018).

    Google Scholar 

  12. Ewers Lewis, C. J., Carnell, P. E., Sanderman, J., Baldock, J. A. & Macreadie, P. I. Variability and vulnerability of coastal ‘blue carbon’ stocks: a case study from southeast Australia. Ecosystems 21, 263–279 (2018).

    Google Scholar 

  13. Belshe, E. F., Mateo, M. A., Gillis, L., Zimmer, M. & Teichberg, M. Muddy waters: unintentional consequences of blue carbon research obscure our understanding of organic carbon dynamics in seagrass ecosystems. Front. Mar. Sci. 4, 125 (2017).

    Google Scholar 

  14. Arndt, S. et al. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth-Sci. Rev. 123, 53–86 (2013).

    Google Scholar 

  15. Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).

    Article  Google Scholar 

  16. Kelleway, J. J., Saintilan, N., Macreadie, P. I. & Ralph, P. J. Sedimentary factors are key predictors of carbon storage in SE Australian saltmarshes. Ecosystems 19, 865–880 (2016).

    Google Scholar 

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

    Google Scholar 

  18. Kirwan, M. L., Guntenspergen, G. R. & Langley, J. A. Temperature sensitivity of organic-matter decay in tidal marshes. Biogeosciences 11, 4801–4808 (2014).

    Google Scholar 

  19. Morris, J. T. & Bowden, W. B. A mechanistic, numerical model of sedimentation, mineralization, and decomposition for marsh sediments. Soil Sci. Soc. Am. J. 50, 96–105 (1986).

    Google Scholar 

  20. Fagherazzi, S. et al. Numerical models of salt marsh evolution: ecological, geomorphic, and climatic factors. Rev. Geophys. 50, RG1002 (2012).

    Google Scholar 

  21. Day, J. W. Jr et al. Soil accretionary dynamics, sea-level rise and the survival of wetlands in Venice Lagoon: a field and modelling approach. Estuar. Coast. Shelf Sci. 49, 607–628 (1999).

    Google Scholar 

  22. Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).

    Google Scholar 

  23. Morris, J. T. et al. Contributions of organic and inorganic matter to sediment volume and accretion in tidal wetlands at steady state. Earth’s. Future 4, 110–121 (2016).

    Google Scholar 

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

    Google Scholar 

  25. Yang, J., Gao, J., Liu, B. & Zhang, W. Sediment deposits and organic carbon sequestration along mangrove coasts of the Leizhou Peninsula, southern China. Estuar. Coast. Shelf Sci. 136, 3–10 (2014).

    Google Scholar 

  26. Zhou, J., Wu, Y., Kang, Q. & Zhang, J. Spatial variations of carbon, nitrogen, phosphorous and sulfur in the salt marsh sediments of the Yangtze Estuary in China. Estuar. Coast. Shelf Sci. 71, 47–59 (2007).

    Google Scholar 

  27. Bouillon, S. & Boschker, H. T. S. Bacterial carbon sources in coastal sediments: a cross-system analysis based on stable isotope data of biomarkers. Biogeosciences 3, 175–185 (2006).

    Google Scholar 

  28. Hedges, J. I. & Keil, R. G. Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 49, 81–115 (1995).

    Google Scholar 

  29. Keil, R. G. & Mayer, L. M. in Treatise on Geochemistry 2nd edn (ed. Turekian, K. K.) 337–359 (Elsevier, 2014).

  30. Blair, N. E. & Aller, R. C. The fate of terrestrial organic carbon in the marine environment. Annu. Rev. Mar. Sci. 4, 401–423 (2012).

    Google Scholar 

  31. Zhao, B. et al. The role of reactive iron in the preservation of terrestrial organic carbon in estuarine sediments. J. Geophys. Res. -Biogeo. 123, 3556–3569 (2018).

    Google Scholar 

  32. Liu, Z. & Lee, C. Drying effects on sorption capacity of coastal sediment: the importance of architecture and polarity of organic matter. Geochim. Cosmochim. Acta 70, 3313–3324 (2006).

    Google Scholar 

  33. Liu, Z. & Lee, C. The role of organic matter in the sorption capacity of marine sediments. Mar. Chem. 105, 240–257 (2007).

    Google Scholar 

  34. Canfield, D. E. Factors influencing organic carbon preservation in marine sediments. Chem. Geol. 114, 315–329 (1994).

    Google Scholar 

  35. Cook, P. L. M., Wenzhöfer, F., Glud, R. N., Janssen, F. & Huettel, M. Benthic solute exchange and carbon mineralization in two shallow subtidal sandy sediments: effect of advective pore-water exchange. Limnol. Oceanogr. 52, 1943–1963 (2007).

    Google Scholar 

  36. Cloern, J. E., Canuel, E. A. & Harris, D. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnol. Oceanogr. 47, 713–729 (2002).

    Google Scholar 

  37. Trevathan-Tackett, S. M. et al. A global assessment of the chemical recalcitrance of seagrass tissues: implications for long-term carbon sequestration. Front. Plant Sci. 8, 925 (2017).

    Google Scholar 

  38. Kristensen, E., Bouillon, S., Dittmar, T. & Marchand, C. Organic carbon dynamics in mangrove ecosystems: a review. Aquat. Bot. 89, 201–219 (2008).

    Google Scholar 

  39. Enríquez, S., Duarte, C. M. & Sand-Jensen, K. Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N:P content. Oecologia 94, 457–471 (1993).

    Google Scholar 

  40. Brodersen, K. E. et al. Oxygen consumption and sulfate reduction in vegetated coastal habitats: effects of physical disturbance. Front. Mar. Sci. 6, 14 (2019).

    Google Scholar 

  41. Ward, L. G., Zaprowski, B. J., Trainer, K. D. & Davis, P. T. Stratigraphy, pollen history and geochronology of tidal marshes in a Gulf of Maine estuarine system: climatic and relative sea level impacts. Mar. Geol. 256, 1–17 (2008).

    Google Scholar 

  42. Spivak, A. C. & Reeve, J. Rapid cycling of recently fixed carbon in a Spartina alterniflora system: a stable isotope tracer experiment. Biogeochemistry 125, 97–114 (2015).

    Google Scholar 

  43. Fontaine, S. et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450, 277–280 (2007).

    Google Scholar 

  44. Klotzbücher, T., Kaiser, K., Guggenberger, G., Gatzek, C. & Kalbitz, K. A new conceptual model for the fate of lignin in decomposing plant litter. Ecology 92, 1052–1062 (2011).

    Google Scholar 

  45. Fahimipour, A. K. et al. Global-scale structure of the eelgrass microbiome. Appl. Environ. Microbiol. 83, e03391–16 (2017).

    Google Scholar 

  46. Kearns, P. J. et al. Nutrient enrichment induces dormancy and decreases diversity of active bacteria in salt marsh sediments. Nat. Commun. 7, 12881 (2016).

    Google Scholar 

  47. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. Bacterial persistence as a phenotypic switch. Science 305, 1622–1625 (2004).

    Google Scholar 

  48. Cúcio, C., Overmars, L., Engelen, A. H. & Muyzer, G. Metagenomic analysis shows the presence of bacteria related to free-living forms of sulfur-oxidizing chemolithoautotrophic symbionts in the rhizosphere of the seagrass Zostera marina. Front. Mar. Sci. 5, 171 (2018).

    Google Scholar 

  49. Bulseco, A. N. et al. Nitrate addition stimulates microbial decomposition of organic matter in salt marsh sediments. Glob. Change Biol. https://doi.org/10.1111/gcb.14726 (2019).

  50. Liang, C., Schimel, J. P. & Jastrow, J. D. The importance of anabolism in microbial control over soil carbon storage. Nat. Microbiol. 2, 17105 (2017).

    Google Scholar 

  51. Kirwan, M. L. & Gedan, K. B. Sea-level driven land conversion and the formation of ghost forests. Nat. Clim. Change 9, 450–457 (2019).

    Google Scholar 

  52. Saunders, M. I. et al. Coastal retreat and improved water quality mitigate losses of seagrass from sea level rise. Glob. Change Biol. 19, 2569–2583 (2013).

    Google Scholar 

  53. Fagherazzi, S. et al. Sea level rise and the dynamics of the marsh-upland boundary. Front. Environ. Sci. 7, 25 (2019).

    Google Scholar 

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

    Google Scholar 

  55. Mueller, P., Jensen, K. & Megonigal, J. P. Plants mediate soil organic matter decomposition in response to sea level rise. Glob. Change Biol. 22, 404–414 (2016).

    Google Scholar 

  56. Freeman, C., Ostle, N. J., Fenner, N. & Kang, H. A regulatory role for phenol oxidase during decomposition in peatlands. Soil Biol. Biochem. 36, 1663–1667 (2004).

    Google Scholar 

  57. Craft, C. et al. Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services. Front. Ecol. Environ. 7, 73–78 (2009).

    Google Scholar 

  58. Weston, N. B., Dixon, R. E. & Joye, S. B. Ramifications of increased salinity in tidal freshwater sediments: geochemistry and microbial pathways of organic matter mineralization. J. Geophys. Res. -Biogeo. 111, G01009 (2006).

    Google Scholar 

  59. Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    Google Scholar 

  60. Melillo, J. M. et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–105 (2017).

    Google Scholar 

  61. Pold, G., Grandy, A. S., Melillo, J. M. & DeAngelis, K. M. Changes in substrate availability drive carbon cycle response to chronic warming. Soil Biol. Biochem. 110, 68–78 (2017).

    Google Scholar 

  62. von Lützow, M. & Kögel-Knabner, I. Temperature sensitivity of soil organic matter decomposition—what do we know? Biol. Fert. Soils 46, 1–15 (2009).

    Google Scholar 

  63. Wilson, R. M. et al. Stability of peatland carbon to rising temperatures. Nat. Commun. 7, 13723 (2016).

    Google Scholar 

  64. Osland, M. J., Enwright, N., Day, R. H. & Doyle, T. W. Winter climate change and coastal wetland foundation species: salt marshes vs. mangrove forests in the southeastern United States. Glob. Change Biol. 19, 1482–1494 (2013).

    Google Scholar 

  65. Root, T. L. et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003).

    Google Scholar 

  66. Saintilan, N., Wilson, N. C., Rogers, K., Rajkaran, A. & Krauss, K. W. Mangrove expansion and salt marsh decline at mangrove poleward limits. Glob. Change Biol. 20, 147–157 (2014).

    Google Scholar 

  67. Mafi-Gholami, D., Zenner, E. K., Jaafari, A. & Ward, R. D. Modeling multi-decadal mangrove leaf area index in response to drought along the semi-arid southern coasts of Iran. Sci. Total Environ. 656, 1326–1336 (2019).

    Google Scholar 

  68. McKee, K. L., Mendelssohn, I. A. & Materne, M. D. Acute salt marsh dieback in the Mississippi River deltaic plain: a drought-induced phenomenon? Glob. Ecol. Biogeogr. 13, 65–73 (2004).

    Google Scholar 

  69. Jordà, G., Marbà, N. & Duarte, C. M. Mediterranean seagrass vulnerable to regional climate warming. Nat. Clim. Change 2, 821–824 (2012).

    Google Scholar 

  70. Van der Putten, W. H., Macel, M. & Visser, M. E. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos. Trans. R. Soc. B 365, 2025–2034 (2010).

    Google Scholar 

  71. Marbà, N. et al. Impact of seagrass loss and subsequent revegetation on carbon sequestration and stocks. J. Ecol. 103, 296–302 (2015).

    Google Scholar 

  72. Sanford, E., Holzman, S. B., Haney, R. A., Rand, D. M. & Bertness, M. D. Larval tolerance, gene flow, and the northern geographic range limit of fiddler crabs. Ecology 87, 2882–2894 (2006).

    Google Scholar 

  73. Kostka, J. E. et al. The rates and pathways of carbon oxidation in bioturbated saltmarsh sediments. Limnol. Oceanogr. 47, 230–240 (2002).

    Google Scholar 

  74. Kristensen, E. & Alongi, D. M. Control by fiddler crabs (Uca vocans) and plant roots (Avicennia marina) on carbon, iron, and sulfur biogeochemistry in mangrove sediment. Limnol. Oceanogr. 51, 1557–1571 (2006).

    Google Scholar 

  75. Burkholder, J. M., Tomasko, D. A. & Touchette, B. W. Seagrasses and eutrophication. J. Exp. Mar. Biol. Ecol. 350, 46–72 (2007).

    Google Scholar 

  76. Turner, R. E. et al. Salt marshes and eutrophication: an unsustainable outcome. Limnol. Oceanogr. 54, 1634–1642 (2009).

    Google Scholar 

  77. Sanders, C. J. et al. Elevated rates of organic carbon, nitrogen, and phosphorus accumulation in a highly impacted mangrove wetland. Geophys. Res. Lett. 41, 2475–2480 (2014).

    Google Scholar 

  78. Bowen, J. L., Crump, B. C., Deegan, L. A. & Hobbie, J. E. Increased supply of ambient nitrogen has minimal effect on salt marsh bacterial production. Limnol. Oceanogr. 54, 713–722 (2009).

    Google Scholar 

  79. Nowinski, N. S., Trumbore, S. E., Schuur, E. A. G., Mack, M. C. & Shaver, G. R. Nutrient addition prompts rapid destabilization of organic matter in an Arctic tundra ecosystem. Ecosystems 11, 16–25 (2008).

    Google Scholar 

  80. Richards, D. R. & Friess, D. A. Rates and drivers of mangrove deforestation in Southeast Asia, 2000–2012. Proc. Natl Acad. Sci. USA 113, 344–349 (2016).

    Google Scholar 

  81. Osland, M. J. et al. Ecosystem development after mangrove wetland creation: plant–soil change across a 20-year chronosequence. Ecosystems 15, 848–866 (2012).

    Google Scholar 

  82. Greening, H. & Janicki, A. Toward reversal of eutrophic conditions in a subtropical estuary: water quality and seagrass response to nitrogen loading reductions in Tampa Bay, Florida, USA. Environ. Manag. 38, 163–178 (2006).

    Google Scholar 

  83. Dahl, M. et al. Sediment properties as important predictors of carbon storage in Zostera marina meadows: a comparison of four European areas. PLoS ONE 11, e0167493 (2016).

    Google Scholar 

  84. Röhr, M. E., Boström, C., Canal-Vergés, P. & Holmer, M. Blue carbon stocks in Baltic Sea eelgrass (Zostera marina) meadows. Biogeosciences 13, 6139–6153 (2016).

    Google Scholar 

  85. Serrano, O. et al. Can mud (silt and clay) concentration be used to predict soil organic carbon content within seagrass ecosystems? Biogeosciences 13, 4915–4926 (2016).

    Google Scholar 

  86. Liu, Z., Breecker, D., Mayer, L. M. & Zhong, J. Composition of size-fractioned sedimentary organic matter in coastal environments is affected by difference in physical forcing strength. Org. Geochem. 60, 20–32 (2013).

    Google Scholar 

  87. Arzayus, K. M. & Canuel, E. A. Organic matter degradation in sediments of the York River estuary: effects of biological vs. physical mixing. Geochim. Cosmochim. Acta 69, 455–464 (2005).

    Google Scholar 

  88. Luther, G. W., Ferdelman, T. G., Kostka, J. E., Tsamakis, E. J. & Church, T. M. Temporal and spatial variability of reduced sulfur species (FeS2, S2O3 2−) and porewater parameters in salt marsh sediments. Biogeochemistry 14, 57–88 (1991).

    Google Scholar 

  89. Koch, E. W. Beyond light: physical, geological, and geochemical parameters as possible submersed aquatic vegetation habitat requirements. Estuaries 24, 1–17 (2001).

    Google Scholar 

  90. Bowen, J. L. et al. Lineage overwhelms environmental conditions in determining rhizosphere bacterial community structure in a cosmopolitan invasive plant. Nat. Commun. 8, 433 (2017).

    Google Scholar 

  91. Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change 26, 152–158 (2014).

    Google Scholar 

  92. Wong, P. P. et al. in Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) 361–409 (Cambridge Univ. Press, 2014).

  93. Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

    Google Scholar 

  94. Yvon-Durocher, G., Jones, J. I., Trimmer, M., Woodward, G. & Montoya, J. M. Warming alters the metabolic balance of ecosystems. Philos. Trans. R. Soc. B 365, 2117–2126 (2010).

    Google Scholar 

  95. Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl Acad. Sci. USA 106, 12377–12381 (2009).

    Google Scholar 

  96. Perillo, G., Wolanski, E., Cahoon, D. & Hopkinson, C. S. Coastal Wetlands: An Integrated Ecosystem Approach 2nd edn (Elsevier, 2019).

  97. Hamilton, S. E. & Casey, D. Creation of a high spatio-temporal resolution global database of continuous mangrove forest cover for the 21st century (CGMFC-21). Glob. Ecol. Biogeogr. 25, 729–738 (2016).

    Google Scholar 

  98. Todd-Brown, K. E. O. et al. Causes of variation in soil carbon simulations from CMIP5 Earth system models and comparison with observations. Biogeosciences 10, 1717–1736 (2013).

    Google Scholar 

  99. Wang, Y. P. et al. Responses of two nonlinear microbial models to warming and increased carbon input. Biogeosciences 13, 887–902 (2016).

    Google Scholar 

Download references

Acknowledgements

A.C.S. was supported by Woods Hole Sea Grant (NA14OAR4170104) and NOAA NSC (NA14NOS4190145); J.L.B. by a CAREER award from NSF DEB (1350491/1719446); E.A.C. by NSF-DEB 1556554; and C.S.H. by NSF OCE-1238212, NSF-OCE 1637630, NSF-OCE 12-37140 and NSF-OCE18-32178.

Author information

Authors and Affiliations

Authors

Contributions

A.C.S. conceived and wrote initial drafts. All authors contributed to idea development and manuscript writing and editing.

Corresponding author

Correspondence to Amanda C. Spivak.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Spivak, A.C., Sanderman, J., Bowen, J.L. et al. Global-change controls on soil-carbon accumulation and loss in coastal vegetated ecosystems. Nat. Geosci. 12, 685–692 (2019). https://doi.org/10.1038/s41561-019-0435-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41561-019-0435-2

This article is cited by

Search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

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