Abstract
The organic carbon (Corg) stored in seagrass meadows is globally significant and could be relevant in strategies to mitigate increasing CO2 concentration in the atmosphere. Most of that stored Corg is in the soils that underlie the seagrasses. We explored how seagrass and soil characteristics vary among seagrass meadows across the geographic range of turtlegrass (Thalassia testudinum) with a goal of illuminating the processes controlling soil organic carbon (Corg) storage spanning 23° of latitude. Seagrass abundance (percent cover, biomass, and canopy height) varied by over an order of magnitude across sites, and we found high variability in soil characteristics, with Corg ranging from 0.08 to 12.59% dry weight. Seagrass abundance was a good predictor of the Corg stocks in surficial soils, and the relative importance of seagrass-derived soil Corg increased as abundance increased. These relationships suggest that first-order estimates of surficial soil Corg stocks can be made by measuring seagrass abundance and applying a linear transfer function. The relative availability of the nutrients N and P to support plant growth was also correlated with soil Corg stocks. Stocks were lower at N-limited sites than at P-limited ones, but the importance of seagrass-derived organic matter to soil Corg stocks was not a function of nutrient limitation status. This finding seemed at odds with our observation that labile standard substrates decomposed more slowly at N-limited than at P-limited sites, since even though decomposition rates were 55% lower at N-limited sites, less Corg was accumulating in the soils. The dependence of Corg stocks and decomposition rates on nutrient availability suggests that eutrophication is likely to exert a strong influence on carbon storage in seagrass meadows.
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References
Armitage, A.R., and J.W. Fourqurean. 2016. Carbon storage in seagrass soils: long-term nutrient history exceeds the effects of near-term nutrient enrichment. Biogeosciences 13: 313–321.
Armitage, A.R., T.A. Frankovich, K.L.J. Heck, and J.W. Fourqurean. 2005. Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries 28: 422–434.
Arndt, S., B.B. Jorgensen, D.E. LaRowe, J.J. Middelburg, R.D. Pancost, and P. Regnier. 2013. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth-Science Reviews 123: 53–86.
Atkinson, M.J., and S.V. Smith. 1983. C:N: P ratios of benthic marine plants. Limnology and Oceanography 28: 568–574.
Barry, S.C., T.S. Bianchi, M.R. Shields, J.A. Hutchings, C.A. Jacoby, and T.K. Frazer. 2018. Characterizing blue carbon stocks in Thalassia testudinum meadows subjected to different phosphorus supplies: a lignin biomarker approach. Limnology and Oceanography 63: 2630–2646.
Bouillon, S., R.M. Connolly, and S.Y. Lee. 2008. Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research 59: 44–58.
Burdige, D.J. 2007. Preservation of organic matter in marine sediments: controls, mechanisms, and an imbalance in sediment organic carbon budgets? Chemical Reviews 107: 467–485.
Burdige, D.J., R.C. Zimmerman, and X.P. Hu. 2008. Rates of carbonate dissolution in permeable sediments estimated from pore-water profiles: the role of sea grasses. Limnology and Oceanography 53: 549–565.
Callaway, J.C., E.L. Borgnis, R.E. Turner, and C.S. Milan. 2012. Carbon sequestration and sediment accretion in San Francisco Bay tidal wetlands. Estuaries and Coasts 35: 1163–1181.
Campbell, J.E., et al. In review. Herbivore effects increase with latitude across a foundational seagrass: implications for the tropicalization of the Western Atlantic. Proceedings of the National Academy of Sciences of the United States of America.
Campbell, J.E., E.A. Lacey, R.A. Decker, S. Crooks, and J.W. Fourqurean. 2015. Carbon storage in seagrass beds of Abu Dhabi, United Arab Emirates. Estuaries and Coasts 38: 242–251.
Carney, K.M., B.A. Hungate, B.G. Drake, and J.P. Megonigal. 2007. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proceedings of the National Academy of Sciences of the United States of America 104: 4990–4995.
Carruthers, T.J.B., P.A.G. Barnes, G.E. Jacome, and J.W. Fourqurean. 2005. Lagoon scale processes in a coastally influenced Caribbean system: implications for the seagrass Thalassia testudinum. Caribbean Journal of Science 41: 441–455.
Carruthers, T.J.B., W.C. Dennison, G.A. Kendrick, M. Waycott, D.I. Walker, and M.L. Cambridge. 2007. Seagrasses of south-west Australia: a conceptual synthesis of the world’s most diverse and extensive seagrass meadows. Journal of Experimental Marine Biology and Ecology 350: 21–45.
de Boer, W.F. 2007. Seagrass-sediment interactions, positive feedbacks and critical thresholds for occurrance: a review. Hydrobiologia 591: 5–24.
Deegan, L.A., D.S. Johnson, R.S. Warren, B.J. Peterson, J.W. Fleeger, S. Fagherazzi, and W.M. Wollheim. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490: 388–392.
DeLaune, R.D., and J.R. White. 2012. 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. Climatic Change 110: 297–314.
Dennison, W.C. 1987. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquatic Botany 27: 15–26.
Diefendorf, A.F., K.E. Mueller, S.L. Wing, P.L. Koch, and K.H. Freeman. 2010. Global patterns in leaf C-13 discrimination and implications for studies of past and future climate. Proceedings of the National Academy of Sciences of the United States of America 107: 5738–5743.
Duarte, C.M. 1992. Nutrient concentrations of aquatic plants: patterns across species. Limnology and Oceanography 37: 882–889.
Duarte, C.M. 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41: 87–112.
Duarte, C.M., and J. Cebrián. 1996. The fate of marine autotrophic production. Limnology and Oceanography 41: 1758–1766.
Duarte, C.M., J.J. Middelburg, and N. Caraco. 2005. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2: 1–8.
Duarte, C.M., H. Kennedy, N. Marbà, and I. Hendriks. 2011. Assessing the capacity of seagrass meadows for carbon burial: current limitations and future strategies. Ocean & Coastal Management 51: 671–688.
Enriquez, S., C.M. Duarte, and K. Sand-Jensen. 1993. Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N: P content. Oecologia 94: 457–471.
Erftemeijer, P.L.A., J. Stapel, M.J.E. Smekens, and W.M.E. Drossaert. 1994. The limited effect of in situ phosphorus and nitrogen additions to seagrass beds on carbonate and terrigenous sediments in South Sulawesi, Indonesia. Journal of Experimental Marine Biology and Ecology 182: 123–140.
Ferdie, M., and J.W. Fourqurean. 2004. Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnology and Oceanography 49: 2082–2094.
Fonseca, M.S., and J.S. Fisher. 1986. A comparison of canopy friction and seciment movement between four species of seagrass with reference to their ecology and restoration. Marine Ecology Progress Series 29: 15–22.
Fonseca, M.S., J.W. Fourqurean, and M.A.R. Koehl. 2019. Effect of seagrass on current speed: importance of flexibility vs. shoot density. Frontiers in Marine Science 6: 376.
Fontaine, S., A. Mariotti, and L. Abbadie. 2003. The priming effect of organic matter: a question of microbial competition? Soil Biology & Biochemistry 35: 837–843.
Ford, R.B., S.F. Thrush, and P.K. Probert. 2001. The interacting effect of hydrodynamics and organic matter on colonization: a soft-sediment example. Estuarine Coastal and Shelf Science 52: 705–714.
Fourqurean, J.W., and L.M. Rutten. 2003. Competing goals of spatial and temporal resolution: monitoring seagrass communities on a regional scale. In Monitoring ecosystem initiatives: interdisciplinary approaches for evaluating ecoregional initiatives, ed. D.E. Busch and J.C. Trexler, 257–288. Washington, D. C.: Island Press.
Fourqurean, J.W., and J.C. Zieman. 1991. Photosynthesis, respiration and whole plant carbon budget of the seagrass Thalassia testudinum. Marine Ecology Progress Series 69: 161–170.
Fourqurean, J.W., and J.C. Zieman. 2002. Seagrass nutrient content reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys, USA. Biogeochemistry 61: 229–245.
Fourqurean, J.W., J.C. Zieman, and G.V.N. Powell. 1992. Phosphorus limitation of primary production in Florida Bay: evidence from the C:N: P ratios of the dominant seagrass Thalassia testudinum. Limnology and Oceanography 37: 162–171.
Fourqurean, J.W., A.W. Willsie, C.D. Rose, and L.M. Rutten. 2001. Spatial and temporal pattern in seagrass community composition and productivity in south Florida. Marine Biology 138: 341–354.
Fourqurean, J.W., C.M. Duarte, H. Kennedy, N. Marba, M. Holmer, M.A. Mateo, E.T. Apostolaki, G.A. Kendrick, D. Krause-Jensen, K.J. McGlathery, and O. Serrano. 2012a. Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience 5: 505–509.
Fourqurean, J.W., G.A. Kendrick, L.S. Collins, R.M. Chambers, and M.A. Vanderklift. 2012b. Carbon, nitrogen and phosphorus storage in subtropical seagrass meadows: examples from Florida Bay and Shark Bay. Marine and Freshwater Research 63: 967–983.
Gacia, E., and C.M. Duarte. 2001. Sediment retention by a Mediterranean Posidonia oceanica meadow: the balance between deposition and resuspension. Estuarine, Coastal and Shelf Science 52: 505–514.
Gacia, E., C.M. Duarte, and J.J. Middleburg. 2002. Carbon and nutrient deposition in a Mediterranean seagrass (Posidonia oceanica) meadow. Limnology and Oceanography 47: 23–32.
Goericke, R., and B. Fry. 1994. Variations of marine plankton delta-C-13 with latitude, temperature, and dissolved CO2 in the world ocean. Global Biogeochemical Cycles 8: 85–90.
Goni, M.A., K.C. Ruttenberg, and T.I. Eglinton. 1998. A reassessment of the sources and importance of land-derived organic matter in surface sediments from the Gulf of Mexico. Geochimica Et Cosmochimica Acta 62: 3055–3075.
Greiner, J.T., K.J. McGlathery, J. Gunnell, and B.A. McKee. 2013. Seagrass restoration enhances “Blue Carbon” sequestration in coastal waters. Plos One 8: e72469.
Hansen, V.D., and J.A. Nestlerode. 2014. Carbon sequestration in wetland soils of the northern Gulf of Mexico coastal region. Wetlands Ecology and Management 22: 289–303.
Hansen, J.C.R., and M.A. Reidenbach. 2012. Wave and tidally driven flows in eelgrass beds and their effect on sediment suspension. Marine Ecology Progress Series 448: 271–287.
Heck, K.L.J., and J.F. Valentine. 2006. Plant-herbivore interactions in seagrass meadows. Journal of Experimental Marine Biology and Ecology 330: 420–436.
Hemminga, M.A., P.G. Harrison, and F. van Lent. 1991. The balance of nutrient losses and gains in seagrass meadows. Marine Ecology Progress Series 71: 85–96.
Hendriks, I.E., T. Sintes, T.J. Bouma, and C.M. Duarte. 2008. Experimental assessment and modeling evaluation of the effects of seagrass (P. oceanica) on flow and particle trapping. Marine Ecology Progress Series 365: 163–173.
Howard, J.L., A. Perez, C.C. Lopes, and J.W. Fourqurean. 2016. Fertilization changes seagrass community structure but not blue carbon storage: results from a 30-year field experiment. Estuaries and Coasts 39: 1422–1434.
Howard, J.L., C.C. Lopes, S.S. Wilson, V. McGee-Absten, C.I. Carrion, and J.W. Fourqurean. 2021. Decomposition rates of surficial and buried organic matter and the lability of soil carbon stocks across a large tropical seagrass landscape. Estuaries and Coasts 44: 846–866.
Howarth, R.W. 1988. Nutrient limitation of net primary production in marine ecosystems. Annual Review of Ecology and Systematics 19: 89–110.
Hughes, A.R., K.J. Bando, L.F. Rodriguez, and S.L. Williams. 2004. Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Marine Ecology-Progress Series 282: 87–99.
Keith, H., B.G. Mackey, and D.B. Lindenmayer. 2009. Re-evaluation of forest biomass carbon stocks and lessons from the world’s most carbon-dense forests. Proceedings of the National Academy of Sciences of the United States of America 106: 11635–11640.
Kennedy, H., J. Beggins, C.M. Duarte, J.W. Fourqurean, M. Holmer, N. Marba, and J.J. Middelburg. 2010. Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochemical Cycles 24: GB4026.
Kennedy, H., J.F. Pagès, D. Lagomasino, A. Arias-Ortiz, P. Colarusso, J.W. Fourqurean, M.N. Githaiga, J.L. Howard, D. Krause-Jensen, T. Kuwae, P.S. Lavery, P.I. Macreadie, N. Marbà, P. Masqué, I. Mazarrasa, T. Miyajima, O. Serrano, and C.M. Duarte. 2022. Species traits and geomorphic setting as drivers of global soil carbon stocks in seagrass meadows. Global Biogeochemical Cycles 36: e2022GB007481.
Keuskamp, J.A., B.J.J. Dingemans, T. Lehtinen, J.M. Sarneel, and M.M. Hefting. 2013. Tea Bag Index: a novel approach to collect uniform decomposition data across ecosystems. Methods in Ecology and Evolution 4: 1070–1075.
Kirschbaum, M.U.F. 1995. The temperature-dependence of soil organic-matter deposition, and the effect of global warming on soil organic-C storage. Soil Biology & Biochemistry 27: 753–760.
Koch, E.W. 1999. Preliminary evidence on the interdependent effect of current and porewater geochemistry on Thalassia testudinum Banks ex König seedling. Aquatic Botany 63: 95–102.
Koch, M., G. Bowes, C. Ross, and X.H. Zhang. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19: 103–132.
Lee, K.S., S.R. Park, and Y.K. Kim. 2007. Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. Journal of Experimental Marine Biology and Ecology 350: 144–175.
Li, L.L., Z.J. Jiang, Y.C. Wu, J.L. He, Y. Fang, J.Z. Lin, S.L. Liu, and X.P. Huang. 2021. Interspecific differences in root exudation for three tropical seagrasses and sediment pore-water dissolved organic carbon beneath them. Marine Pollution Bulletin 173: 113059.
Macreadie, P.I., M.E. Baird, S.M. Trevathan-Tackett, A.W.D. Larkum, and P.J. Ralph. 2014. Quantifying and modelling the carbon sequestration capacity of seagrass meadows - a critical assessment. Marine Pollution Bulletin 83: 430–439.
Macreadie, P.I., S.M. Trevathan-Tackett, C.G. Skilbeck, J. Sanderman, N. Curlevski, G. Jacobsen, and J.R. Seymour. 2015. Losses and recovery of organic carbon from a seagrass ecosystem following disturbance. Proceedings of the Royal Society B-Biological Sciences 282: 20151537.
Madsen, J.D., P.A. Chambers, W.F. James, E.W. Koch, and D.F. Westlake. 2001. The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444: 71–84.
Marba, N., A. Arias-Ortiz, P. Masque, G.A. Kendrick, I. Mazarrasa, G.R. Bastyan, J. Garcia-Orellana, and C.M. Duarte. 2015. Impact of seagrass loss and subsequent revegetation on carbon sequestration and stocks. Journal of Ecology 103: 296–302.
Mazarrasa, I., N. Marba, C.E. Lovelock, O. Serrano, P. Lavery, J.W. Fourqurean, H. Kennedy, M.A. Mateo, D. Krause-Jensen, A.D.L. Steven, and C.M. Duarte. 2015. Seagrass meadows as globally significant carbonate reservoir. Biogeosciences 12: 4993–5003.
Mazarrasa, I., P. Lavery, C.M. Duarte, A. Lafratta, C.E. Lovelock, P.I. Macreadie, J. Samper-Villarreal, C. Salinas, C.J. Sanders, S. Trevathan-Tackett, M. Young, A. Steven, and O. Serrano. 2021. Factors determining seagrass blue carbon across bioregions and geomorphologies. Global Biogeochemical Cycles 35: e2021GB006935.
McLeod, E., G.L. Chmura, S. Bouillon, R. Salm, M. Björk, C.M. Duarte, C.E. Lovelock, W.H. Schlesinger, and B.R. Silliman. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Frontiers in Ecology and the Environment 7: 362–370.
Miyajima, T., M. Hori, M. Hamaguchi, H. Shimabukuro, and G. Yoshida. 2017. Geophysical constraints for organic carbon sequestration capacity of Zostera marina seagrass meadows and surrounding habitats. Limnology and Oceanography 62: 954–972.
Nowicki, R.J., J.W. Fourqurean, and M.R. Heithaus. 2018. The role of consumers in structuring seagrass communities: direct and indirect mechanisms. In Seagrasses of Australian: structure, ecology and conservation, ed. A.W.D. Larkum, G.A. Kendrick, and P.J. Ralph, 491–540. Switzerland: Springer Nature Switzerland AG.
Parnell, A.C., R. Inger, S. Bearhop, and A.L. Jackson. 2010. Source partitioning using stable isotopes: coping with too much variation. Plos One 5: e9672.
Samper-Villarreal, J., C.E. Lovelock, M.I. Saunders, C. Roelfsema, and P.J. Mumby. 2016. Organic carbon in seagrass sediments is influenced by seagrass canopy complexity, turbidity, wave height, and water depth. Limnology and Oceanography 61: 938–952.
Serrano, O., P.S. Lavery, M. Rozaimi, and M.A. Mateo. 2014. Influence of water depth on the carbon sequestration capacity of seagrasses. Global Biogeochemical Cycles 28: 950–961.
Short, F.T. 1987. Effects of sediment nutrients on seagrasses: literature review and mesocosm experiment. Aquatic Botany 27: 41–57.
Stock, B.C., A.L. Jackson, E.J. Ward, A.C. Parnell, D.L. Phillips, and B.X. Semmens. 2018. Analyzing mixing systems using a new generation of Bayesian tracer mixing models. Peerj 6: e5096.
Tiegs, S.D., S.D. Langhans, K. Tockner, and M.O. Gessner. 2007. Cotton strips as a leaf surrogate to measure decomposition in river floodplain habitats. Journal of the North American Benthological Society 26: 70–77.
Trevathan-Tackett, S.M., A.C.G. Thomson, P.J. Ralph, and P.I. Macreadie. 2018. Fresh carbon inputs to seagrass sediments induce variable microbial priming responses. Science of the Total Environment 621: 663–669.
Trevathan-Tackett, S.M., K.E. Brodersen, and P.I. Macreadie. 2020. Effects of elevated temperature on microbial breakdown of seagrass leaf and tea litter biomass. Biogeochemistry 151: 171–185.
Udy, J.W., W.C. Dennison, W.J. Lee Long, and L.J. McKenzie. 1999. Responses of seagrasses to nutrients in the Great Barrier Reef, Australia. Marine Ecology Progress Series 185: 257–271.
Acknowledgements
This work would not have been possible without the support of numerous technicians, students, and volunteers who assisted in the collection of field data and the processing of samples in the lab. We thank those at FIU and the Smithsonian Marine Station who assisted with field work and project logistics: Clare Peabody, Victoria Jenkins, Scott Jones, Zachary Foltz, Skylar Carlson, Iris Segura-Garcia, Maggie Johnson, Audrey Looby, Olivia Carmack, and David Branson. We also thank Uriah Sun, Lindsey Spiers, Joe Kuehl, and Jon Clamp at the Cayman Islands; Ashley E. MacDonald at the Galveston site; Kathryn Coates and Khalil Smith at the Bermuda site; Aaron John, Anna Safryghin, Jade Reinhart, Kasia Malinowski, Laura Woodlee, Matthew Speegle, Michael England, Sam Glew, and Trinitti Leon at the Andros site; Sabine Engel and Julia van Duijnhoven at the Bonaire site; Scott Alford, Theresa Gruninger, Audrey Looby (again), Cayla Sullivan, Sawyer Downey, Whitney Scheffel, Jamila Roth, and Tim Jones at the Crystal River site; Tom Glucksman, Cameron Raguse, Isabella Primrose Hartman, William F. Bigelow, and Matheo Albury at the Eleuthera site; and M. Guadalupe Barba Santos at the Puerto Morelos site. We also thank Meghan Sarsich and the Blue Carbon Analysis Laboratory at Florida International University for assistance with elemental analyses. The work was conducted under the following permits: at Eleuthera under permit #s MAMR/FIS/17 and MAMR/FIS/9 issued by the Department of Marine Resources; at Bonaire under permit #558/2015-2015007762 issued by Openbaar Lichaam Bonaire; at Belize under permit #0004-18 issued by the Belize Fisheries Department; at Panama under permit #s SE/AP-23-17 and SE/AO-1-19 issued by the Ministerio de Ambiente de la Republica de Panama; at Andros by permits issued by The Bahamas National Trust and the Bahamas Environment, Science and Technology Commission; and at Cayman Islands by a permit issued by the Department of Environment. This is contribution #1564 from the Coastlines and Oceans Division of the Institute of Environment at Florida International University.
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Funding for this project was provided by the US National Science Foundation (grant #s OCE-1737247 to JEC, AHA, and VJP, OCE-2019022 to JEC, OCE-1737144 to KLH, and OCE-1737116 to JGD). MJAC was supported by NWO-Veni grant 181.002. JWF was also supported by the Florida Coastal Everglades Long Term Ecological Research program (grant # DEB-1832229).
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JEC, AHA, JGD, KLH, VJP, JWF, and MJAC conceived and designed the experiments; JWF, JEC, OKR, CJM, AHA, JGD, KLH, VJP, ARA, SCB, EB, LRC, MJAC, GD, KD, TKF, BMG, RG, JAG, RGV, OAAK, STL, CWM, IGML, AMM, VAM, SAM, CMM, DAO, OO, LKR, ARR, LMRB, AS, YS, FOHS, US, JT, BIvT, WLW, and SSW performed the experiments and laboratory analyses; JWF, JEC, JRK, OKR, CJM, and CP analyzed and interpreted the data. JWF and JEC wrote the manuscript with contributions from the other authors.
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Fourqurean, J.W., Campbell, J.E., Rhoades, O.K. et al. Seagrass Abundance Predicts Surficial Soil Organic Carbon Stocks Across the Range of Thalassia testudinum in the Western North Atlantic. Estuaries and Coasts 46, 1280–1301 (2023). https://doi.org/10.1007/s12237-023-01210-0
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DOI: https://doi.org/10.1007/s12237-023-01210-0