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Mangroves dramatically increase carbon storage after 3 years of encroachment

  • L. T. SimpsonEmail author
  • C. M. Stein
  • T. Z. Osborne
  • I. C. Feller
Primary Research Paper

Abstract

In North America, the dynamic ecotonal boundary between mangrove and salt marsh is currently fluctuating in response to freeze-free winters, which can cause rapid alterations in a number of wetland processes and attributes. Permanent plots were established in pure salt marsh habitat along the Atlantic coast of Florida in 2015, and by 2018, mangrove saplings had encroached into plots. In this study, above- and belowground biomass measurements and soil C in the top 10-cm soil profile were quantified in 2018 and compared to 2015 data to better understand the effects of mangrove encroachment on C storage in salt marsh habitat. Plant and soil fractions were tested for δ13C stable isotopic signatures to elucidate soil C sources. In 3 years, mangrove biomass increased dramatically and soil C doubled in pure salt marsh plots, consequently increasing total C in the system. Soil organic matter increased, while there was no change in soil C:N. δ13C values suggest that soil C was derived mainly from salt marsh soil organic matter, especially that of belowground, rather than aboveground biomass. These results provide real-time, quantitative data on the encroachment of mangroves into salt marshes over a relatively short period of time.

Keywords

Climate change Ecotonal boundary Blue carbon Vegetation shift Stable isotopes Salt marsh 

Notes

Acknowledgements

This research was funded by the National Aeronautics and Space Administration (NASA) Climate and Biological Response program (NNX11AO94G) and the National Science Foundation (NSF) MacroSystems Biology program (EF1065821). The authors would like to thank Florida State Parks, the Merritt Island National Wildlife Refuge, Guana-Tolmato-Matanzas National Estuarine Research Reserve, and Canaveral National Seashore for permits and unabridged access to their parks. We also thank L.J. Duckett, M.L. Lehmann, K.V. Curtis, and Z.R. Foltz for field and lab assistance. We sincerely thank the two anonymous reviewers for their edits and suggestions, which significantly improved this manuscript.

References

  1. Adame, M. F. & B. Fry, 2016. Source and stability of soil carbon in mangrove and freshwater wetlands of the Mexican Pacific coast. Wetlands Ecology and Management 24: 129–137.CrossRefGoogle Scholar
  2. Alongi, D. M., 2011. Carbon payments for mangrove conservation: ecosystem constraints and uncertainties of sequestration potential. Environmental Science & Policy 14(4): 462–470.CrossRefGoogle Scholar
  3. Alongi, D. M., 2014. Carbon cycling and storage in mangrove forests. Annual Review of Marine Science 6: 195–219.CrossRefGoogle Scholar
  4. Asner, G. P., S. Archer, R. F. Hughes, R. J. Ansley & C. A. Wessman, 2003. Net changes in regional woody vegetation cover and carbon storage in Texas drylands, 1937–1999. Global Change Biology 9(3): 316–335.CrossRefGoogle Scholar
  5. Armitage, A. R., W. E. Highfield, S. D. Brody & P. Louchouarn, 2015. The contribution of mangrove expansion to salt marsh loss on the Texas Gulf Coast. PLoS ONE 10: e0125404.CrossRefGoogle Scholar
  6. Ball, M. C., 1980. Patterns of secondary succession in a mangrove forest of southern Florida. Oecologia 44(2): 226–235.CrossRefGoogle Scholar
  7. Bertness, M. D., 1991. Zonation of Spartina patens and Spartina alterniflora in New England salt marsh. Ecology 72: 138–148.CrossRefGoogle Scholar
  8. Camilleri, J. C., 1992. Leaf-litter processing by invertebrates in a mangrove forest in Queensland. Marine Biology 114: 139–145.Google Scholar
  9. Castañeda-Moya, E., R. R. Twilley, V. H. Rivera-Monroy, K. Zhang, S. E. Davis & M. Ross, 2010. Sediment and nutrient deposition associated with Hurricane Wilma in mangroves of the Florida Coastal Everglades. Estuaries and Coasts 33(1): 45–58.CrossRefGoogle Scholar
  10. Cavanaugh, K. C., J. R. Kellner, A. J. Forde, D. S. Gruner, J. D. Parker, W. Rodriguez & I. C. Feller, 2014. Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proceedings of the National Academy of Sciences 111: 723–727.CrossRefGoogle Scholar
  11. Cheng, X., Y. Luo, X. Xu, R. Sherry & Q. Zhang, 2011. Soil organic matter dynamics in a North America tallgrass prairie after 9 yr of experimental warming. Biogeosciences 8: 1487–1498.CrossRefGoogle Scholar
  12. Chmura, G. L., P. Aharon, R. A. Socki & R. Abernethy, 1987. An inventory of 13 C abundances in coastal wetlands of Louisiana, USA: vegetation and sediments. Oecologia 74(2): 264–271.CrossRefGoogle Scholar
  13. Chmura, G. L., S. C. Anisfeld, D. R. Cahoon & J. C. Lynch, 2003. Global carbon sequestration in tidal, saline wetland soils. Global Biogeochemistry Cycles 17(4): 1111–1123.CrossRefGoogle Scholar
  14. Choi, Y., Y. Wang, Y. P. Hsieh & L. Robinson, 2001. Vegetation succession and carbon sequestration in a coastal wetland in northwest Florida: evidence from carbon isotopes. Global Biogeochemical Cycles 15: 311–319.CrossRefGoogle Scholar
  15. Comeaux, R. S., M. A. Allison & T. S. Bianchi, 2012. Mangrove expansion in the Gulf of Mexico with climate change: implications for wetland health and resistance to rising seas. Estuarine, Coastal and Shelf Science 96: 81–95.CrossRefGoogle Scholar
  16. Currin, C. A., S. Y. Newell & H. W. Paerl, 1995. The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotope analysis. Marine Ecology Progress Series 121: 99–116.CrossRefGoogle Scholar
  17. Dangremond, E. M. & I. C. Feller, 2016. Precocious reproduction increases at the leading edge of a mangrove range expansion. Ecology and Evolution 6: 5087–5092.CrossRefGoogle Scholar
  18. Donato, D. C., J. B. Kauffman, D. Murdiyarso, S. Kurnianto, M. Stidhman & M. Kanninen, 2011. Mangroves among the most carbon-rich forests in the tropics. Nature Geoscience 4: 293–297.CrossRefGoogle Scholar
  19. Doughty, C. L., J. A. Langley, W. S. Walker, I. C. Feller, R. Schaub & S. K. Chapman, 2016. Mangrove range expansion rapidly increases coastal wetland carbon storage. Estuaries and Coasts 39: 385–396.CrossRefGoogle Scholar
  20. Duarte, C. M., S. Agustí, P. A. Del Giorgio & J. J. Cole, 1999. Regional carbon imbalances in the oceans. Science 284: 1735.Google Scholar
  21. Duarte, C. M., J. J. Middleburg & N. Caraco, 2005. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2: 1–8.CrossRefGoogle Scholar
  22. Duarte, C. M., I. J. Losada, I. E. Hendriks, I. Mazarrasam & N. Marba, 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nature Climate Change 3: 961–968.CrossRefGoogle Scholar
  23. Ehleringer, J. R., N. Buchmann & L. B. Flanagan, 2000. Carbon isotope ratios in belowground carbon cycle processes. Ecological Applications 10: 412–422.CrossRefGoogle Scholar
  24. Feng, J., J. Zhou, L. Wang, X. Cui, C. Ning, H. Wu, X. Zhu & G. Lin, 2017. Effects of short-term invasion of Spartina alterniflora and the subsequent restoration of native mangroves on the soil organic carbon, nitrogen and phosphorus stock. Chemosphere 184: 774–783.CrossRefGoogle Scholar
  25. Florida Fish and Wildlife Conservation Commission-Fish and Wildlife Research Institute. “Salt Marshes in Florida” [vector digital data]. 1:24,000. 2009. http://geodata.myfwc.com/datasets/20ab7447d9424929bf0e7a2a633d6407_3 Accessed Nov 2015
  26. Florida Fish and Wildlife Conservation Commission-Fish and Wildlife Research Institute. “Counties 1:24,000 Scale Polygon Florida” [vector digital data]. 1:24,000. 10067. http://geodata.myfwc.com/datasets/982d999dda774cc4a1cf0ac8908f4c92_3 Accessed Nov 2015
  27. Guo, H., C. Weaver, S. P. Charles, A. Whitt, S. Dastidar, P. D’Odorico, J. Fuenter, J. A. Kominoski, A. R. Armitage & S. C. Pennings, 2017. Coastal regime shifts: rapid responses of coastal wetlands to changes in mangrove cover. Ecology 98: 762–772.CrossRefGoogle Scholar
  28. Haines, E. B., 1976. Relation between the stable carbon isotope composition of fiddler crabs, plants, and soils in a salt marsh 1. Limnology and Oceanography 21(6): 880–883.CrossRefGoogle Scholar
  29. Henry, K. M. & R. R. Twilley, 2013. Soil development in a coastal Louisiana wetland during a climate-induced vegetation shift from salt marsh to mangrove. Journal of Coastal Research 29: 1273–1283.CrossRefGoogle Scholar
  30. Hibbard, K. A., S. Archer, D. S. Schimel & D. W. Valentine, 2001. Biogeochemical changes accompanying woody plant encroachment in a subtropical savanna. Ecology 82: 1999–2011.CrossRefGoogle Scholar
  31. Kauffman, J. B. & D. C. Donato, 2012. Protocols for the measurement, monitoring and reporting of structure, biomass and carbon stocks in mangrove forests. Working paper 86. Center for International forestry research (CIFOR) Bogor, Indonesia.Google Scholar
  32. Kelleway, J. J., N. Saintilan, P. I. Macreadie, C. G. Skilbeck, A. Zawadzki & P. J. Ralph, 2016. Seventy years of continuous encroachment substantially increases ‘blue carbon’ capacity as mangroves replace intertidal salt marshes. Global Change Biology 22: 1097–1109.CrossRefGoogle Scholar
  33. Kelleway, J. J., K. Cavanaugh, K. Rogers, I. C. Feller, E. Ens, C. Doughty & N. Saintilan, 2017. Review of the ecosystem service implications of mangrove encroachment into salt marshes. Global Change Biology 23: 3967–3983.CrossRefGoogle Scholar
  34. Kelleway, J. J., D. Mazumder, J. A. Baldock & N. Saintilan, 2018. Carbon isotope fractionation in the mangrove Avicennia marina has implications for food web and blue carbon research. Estuarine, Coastal and Shelf Science 205: 68–74.CrossRefGoogle Scholar
  35. Komiyama, J. E., S. Ong & S. Poungparn, 2008. Allometry, biomass and productivity of mangrove forests: a review. Aquatic Botany 89: 128–137.CrossRefGoogle Scholar
  36. Lewis, R. R. & F. M. Dunstan, 1975. The possible role of Spartina alterniflora Loisel. In establishment of mangroves in Florida: 82–100. In Proc. Second Annual Conference on Restoration of Coastal Vegetation in Florida Lewis, R. (ed.), Hillsborough Community College, Tampa, Florida: 203 p.Google Scholar
  37. Liao, J. D., T. W. Boutton & J. D. Jastrow, 2006. Storage and dynamics of carbon and nitrogen in soil physical fractions following woody plant invasion of grassland. Soil Biology and Biochemistry 38: 3184–3196.CrossRefGoogle Scholar
  38. Lunstrum, A. & L. Chen, 2014. Soil carbon stocks and accumulation in young mangrove forests. Soil Biology and Biochemistry 75: 223–232.CrossRefGoogle Scholar
  39. Lovelock, C. E., 2008. Soil respiration and belowground carbon allocation in mangrove forests. Ecosystems 11(2): 342–354.CrossRefGoogle Scholar
  40. Lovelock, C. E., M. F. Adame, V. Bennion, M. Hayes, J. O’Mara, R. Reef & N. S. Saintilan, 2014. Contemporary rates of carbon sequestration through vertical accretion of sediments in mangrove forests and saltmarshes of South East Queensland, Australia. Estuaries and Coasts 37: 763–771.CrossRefGoogle Scholar
  41. Mateo, M. A., J. Romero, M. Pérez, M. M. Littler & D. S. Littler, 1997. Dynamics of millenary organic deposits resulting from the growth of the Mediterranean seagrass Posidonia oceanica. Estuarine Coastal and Shelf Science 44: 103–110.CrossRefGoogle Scholar
  42. McKee, K. L., I. A. Mendelssohn & M. W. Hester, 1988. Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans. American Journal of Botany. 75(9): 1352–1359.CrossRefGoogle Scholar
  43. McKee, K. L., D. R. Cahoon & I. C. Feller, 2007. Caribbean mangroves adjust to rising sea level through biotic controls on change in soil elevation. Global Ecology and Biogeography 16: 545–556.CrossRefGoogle Scholar
  44. McKee, K. L. & J. E. Rooth, 2008. Where temperate meets tropical: multi-factorial effects of elevated CO2, nitrogen enrichment, and competition on a mangrove-salt marsh community. Global Change Biology 14: 971–984.CrossRefGoogle Scholar
  45. Middleton, B. A. & K. L. McKee, 2001. Degradation of mangrove tissues and implications for peat formation in Belizean island forests. Journal of Ecology 89(5): 818–828.CrossRefGoogle Scholar
  46. Nilsson, C., R. L. Brown, R. Jansson & D. M. Merritt, 2010. The role of hydrochory in structuring riparian and wetland vegetation. Biological Reviews 85: 837–858.PubMedGoogle Scholar
  47. Odum, E. P., 1966. The strategy of ecosystem development. Science 164: 262–270.CrossRefGoogle Scholar
  48. Osland, M. J., A. C. Spivak, J. A. Nestlerode, J. M. Lessmann, A. E. Almario, P. T. Heitmuller, M. J. Russell, K. W. Krauss, F. Alvarez, D. D. Dantin, J. E. Harvey, A. S. From, N. Cormier & C. L. Stagg, 2012. Ecosystem development after mangrove wetland creation: plant–soil change across a 20-year chronosequence. Ecosystems 15: 848–866.CrossRefGoogle Scholar
  49. Osland, M. J., R. H. Day, C. T. Hall, M. D. Brumfield, J. L. Dugas & W. R. Jones, 2017a. Mangrove expansion and contraction at a poleward range limit: climate extremes and land-ocean temperature gradients. Ecology 98: 125–137.CrossRefGoogle Scholar
  50. Osland, M. J., L. C. Feher, K. T. Griffith, K. C. Cavanaugh, N. M. Enwright, R. H. Day, C. L. Stagg, K. W. Krauss, R. J. Howard, J. B. Grace & K. Rogers, 2017b. Climatic controls on the global distribution, abundance, and species richness of mangrove forests. Ecological Monographs 87: 341–359.CrossRefGoogle Scholar
  51. Ouyang, X., S. Y. Lee & R. M. Connolly, 2017. The role of root decomposition in global mangrove and saltmarsh carbon budgets. Earth-Science Reviews 166: 53–63.CrossRefGoogle Scholar
  52. Palomo, L. & F. X. Niell, 2009. Primary production and nutrient budgets of Sarcocornia perennis ssp. alpini (Lag.) Castroviejo in the salt marsh of the Palmones River estuary (Southern Spain). Aquatic Botany 91: 130–136.CrossRefGoogle Scholar
  53. Perry, C. L. & I. A. Mendelssohn, 2009. Ecosystem effects of expanding populations of Avicennia germinans in a Louisiana salt marsh. Wetlands 29: 396–406.CrossRefGoogle Scholar
  54. Peterson, J. M. & S. S. Bell, 2012. Tidal events and salt-marsh structure influence black mangrove (Avicennia germinans) recruitment across an ecotone. Ecology 93: 1648–1658.CrossRefGoogle Scholar
  55. Peterson, J. M. & S. S. Bell, 2015. Saltmarsh boundary modulates dispersal of mangrove propagules: implications for mangrove migration with sea-level rise. PLoS ONE 10: e0119128.CrossRefGoogle Scholar
  56. Pickens, C. N. & M. W. Hester, 2011. Temperature tolerance of early life history stages of black mangrove Avicennia germinans: implications for range expansion. Estuaries and Coasts 34: 824–830.CrossRefGoogle Scholar
  57. Poret, N., R. R. Twilley, V. H. Rivera-Monroy & C. Coronado-Molina, 2007. Belowground decomposition of mangrove roots in Florida coastal Everglades. Estuaries and Coasts 30(3): 491–496.CrossRefGoogle Scholar
  58. Rodriguez, W., I. C. Feller & K. C. Cavanaugh, 2016. Spatio-temporal changes of a mangrove–saltmarsh ecotone in the northeastern coast of Florida, USA. Global Ecology and Conservation 7: 245–261.CrossRefGoogle Scholar
  59. Ross, M. S., J. F. Meeder, J. P. Sah, P. L. Ruiz & G. J. Telesnicki, 2000. The southeast saline Everglades revisited: 50 years of coastal vegetation change. Journal of Vegetation Science 11: 101–112.CrossRefGoogle Scholar
  60. Ross, M. S., P. L. Ruiz, J. P. Sah, D. L. Reed, J. Walters & J. F. Meeder, 2006. Early post-hurricane stand development in fringe mangrove forests of contrasting productivity. Plant Ecology 185(2): 283–297.CrossRefGoogle Scholar
  61. Saintilan, N., K. Rogers, D. Mazumder & C. Woodroffe, 2013. Allochthonous and autochthonous contributions to carbon accumulation and carbon store in southeastern Australian coastal wetlands. Estuarine, Coastal and Shelf Science 128: 84–92.CrossRefGoogle Scholar
  62. Scharenbroch, B. C., M. L. Flores-Mangual, B. Lepore, J. G. Bockheim & B. Lowery, 2010. Tree encroachment impacts carbon dynamics in a sand prairie in Wisconsin. Soil Science Society of America Journal 74(3): 956–968.CrossRefGoogle Scholar
  63. Shafer, D. J. & T. H. Roberts, 2008. Long-term development of tidal mitigation wetlands in Florida. Wetlands Ecology and Management 16(1): 23–31.CrossRefGoogle Scholar
  64. Sherrod, C. L. & C. McMillan, 1985. The distributional history and ecology of mangrove vegetation along the northern Gulf of Mexico coastal region.Google Scholar
  65. Simpson, L. T., T. Z. Osborne, L. J. Duckett & I. C. Feller, 2017. Carbon Storages along a climate induced coastal wetland gradient. Wetlands 37: 1–13.CrossRefGoogle Scholar
  66. Smith, B. N. & S. Epstein, 1971. Two categories of 13C/12C ratios for higher plants. Plant physiology 47(3): 380–384.CrossRefGoogle Scholar
  67. Stevens, P. W., S. L. Fox & C. L. Montague, 2006. The interplay between mangroves and saltmarshes at the transition between temperate and subtropical climate in Florida. Wetlands Ecology and Management 14: 435–444.CrossRefGoogle Scholar
  68. Valiela, I., J. M. Teal, S. D. Allen, R. Van Etten, D. Goehringer & S. Volkmann, 1985. Decomposition in salt marsh ecosystems: the phases and major factors affecting disappearance of above-ground organic matter. Journal of Experimental Marine Biology and Ecology 89(1): 29–54.CrossRefGoogle Scholar
  69. Weiss, C., J. Weiss, J. Boy, I. Iskandar, R. Mikutta & G. Guggenberger, 2016. Soil organic carbon stocks in estuarine and marine mangrove ecosystems are driven by nutrient colimitation of P and N. Ecology and Evolution 6: 5043–5056.CrossRefGoogle Scholar
  70. Wooller, M., B. Smallwood, M. Jacobson & M. Fogel, 2003. Carbon and nitrogen stable isotopic variation in Laguncularia racemosa (L.)(white mangrove) from Florida and Belize: implications for trophic level studies. Hydrobiologia 499: 13–23.CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Whitney Laboratory for Marine BioscienceUniversity of FloridaSt. AugustineUSA
  2. 2.Soil and Water Sciences DepartmentUniversity of FloridaGainesvilleUSA
  3. 3.Univeristy of Missouri - Kansas CityKansas CityUSA
  4. 4.Smithsonian Environmental Research CenterEdgewaterUSA

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