Sea-level rise enhances carbon accumulation in United States tidal wetlands

Abstract

•Relative sea-level rise is the dominant driver of coastal wetland carbon accumulation•Balances between soil growth and erosion determine landscape-scale carbon budgets•Even submerging marshes sequester carbon at rates that increase with sea-level rise Coastal wetlands are well-known hotspots for carbon sequestration. However, they are vulnerable to sea-level rise, and there is concern that this important carbon sink may weaken under climate change. We synthesized 503 measurements of soil carbon accumulation rates from coastal wetlands across the United States and show that carbon accumulation rates are positively correlated with local rates of sea-level rise. We then examined the rapidly submerging Louisiana coast to investigate the balance between carbon loss in eroding marshes and carbon gain in surviving marshes. We find that carbon accumulation rates are generally fastest in portions of Louisiana where rates of sea-level rise and land loss are highest, allowing a net carbon sink to persist. Although erosion will eventually lead to net carbon loss, our results suggest a strong negative carbon-climate feedback for coastal marshes, where even submerging marshes sequester carbon at rates that increase with sea-level rise. Coastal wetlands accumulate soil carbon more efficiently than terrestrial systems, but sea-level rise potentially threatens the persistence of this prominent carbon sink. Here, we combine a published dataset of 372 soil carbon accumulation rates from across the United States with new analysis of 131 sites in coastal Louisiana and find that the rate of relative sea-level rise (RSLR) explains 80% of regional variation in carbon accumulation. A carbon mass balance for the rapidly submerging Louisiana coast demonstrates that carbon accumulation rates in surviving marshes increase with RSLR and currently exceed the rate of carbon loss due to marsh drowning and erosion. Although continued erosion will eventually lead to net carbon loss, our results suggest a strong negative carbon-climate feedback for coastal marshes, where even submerging marshes sequester carbon at rates that increase with RSLR. Coastal wetlands accumulate soil carbon more efficiently than terrestrial systems, but sea-level rise potentially threatens the persistence of this prominent carbon sink. Here, we combine a published dataset of 372 soil carbon accumulation rates from across the United States with new analysis of 131 sites in coastal Louisiana and find that the rate of relative sea-level rise (RSLR) explains 80% of regional variation in carbon accumulation. A carbon mass balance for the rapidly submerging Louisiana coast demonstrates that carbon accumulation rates in surviving marshes increase with RSLR and currently exceed the rate of carbon loss due to marsh drowning and erosion. Although continued erosion will eventually lead to net carbon loss, our results suggest a strong negative carbon-climate feedback for coastal marshes, where even submerging marshes sequester carbon at rates that increase with RSLR. There is a growing effort to understand how feedback between climate and carbon cycling influences the ability of ecosystems to absorb and store carbon. Models and empirical observations in marine, peatland, and terrestrial systems point to positive carbon-climate feedback whereby warming reduces the capacity of ecosystems to accumulate carbon and thus amplifies global warming.1Friedlingstein P. Carbon cycle feedbacks and future climate change.Philos. Trans. R. Soc. 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Asynchronous nitrogen supply and demand produce nonlinear plant allocation responses to warming and elevated CO2.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21623-21628Crossref PubMed Scopus (20) Google Scholar The anaerobic conditions in marsh soils are predicted to limit the temperature sensitivity of soil respiration.10Davidson E.A. Janssens I.A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change.Nature. 2006; 440: 165-173Crossref PubMed Scopus (4212) Google Scholar,11Wilson R.M. Hopple A.M. Tfaily M.M. Sebestyen S.D. Schadt C.W. Pfeifer-Meister L. Medvedeff C. McFarlane K.J. Kostka J.E. Kolton M. et al.Stability of peatland carbon to rising temperatures.Nat. Commun. 2016; 7: 13723-13733Crossref PubMed Scopus (106) Google Scholar Field studies of marshes across latitudinal gradients suggest that the temperature sensitivity of primary productivity is greater than that of decomposition, leading to predictions that warming will enhance CAR.12Kirwan M.L. Guntenspergen G.R. Langley J.A. Temperature sensitivity of organic-matter decay in tidal marshes.Biogeosciences. 2014; 11: 4801-4808Crossref Scopus (35) Google Scholar However, there does not appear to be a strong relationship between marsh CAR and mean annual temperature at the global scale.13Chmura G.L. Anisfeld S.C. Cahoon D.R. Lynch J.C. Global carbon sequestration in tidal, saline wetland soils.Glob. Biogeochem.Cycles. 2003; 17https://doi.org/10.1029/2002GB001917Crossref Google Scholar, 14Ouyang X. Lee S.Y. Updated estimates of carbon accumulation rates in coastal marsh sediments.Biogeosciences. 2014; 11: 5057-5071Crossref Scopus (148) Google Scholar, 15Wang F. Lu X. Sanders C. Tang J. Tidal wetland resilience to sea level rise increases their carbon sequestration capacity in United States.Nat. Commun. 2019; 10https://doi.org/10.1038/s41467-019-13294-zCrossref Scopus (34) Google Scholar Instead, model16Kirwan M.L. Mudd S.M. Response of salt-marsh carbon accumulation to climate change.Nature. 2012; 489: 550-553Crossref PubMed Scopus (196) Google Scholar and experimental results8Noyce G.L. Kirwan M.L. Rich R.L. Megonigal J.P. Asynchronous nitrogen supply and demand produce nonlinear plant allocation responses to warming and elevated CO2.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21623-21628Crossref PubMed Scopus (20) Google Scholar suggest that the effect of temperature is modulated by factors such as dominant vegetation species, nitrogen availability, and hydrology. Soil carbon is the dominant pool of carbon in coastal wetlands.3Mcleod E. Chmura G.L. Bouillon S. Salm R. Björk M. Duarte C.M. Lovelock C.E. Schlesinger W.H. Silliman B.R. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2.Front. Ecol. Environ. 2011; 9: 552-560Crossref Scopus (1646) Google Scholar Coastal wetland soil carbon accumulation is tied to a well-characterized set of ecogeomorphic feedbacks, where plant growth is stimulated by increased flooding up to some threshold, so that a moderate increase in relative sea-level rise (RSLR) is predicted to be accompanied by an increase in organic matter accumulation, mineral sediment deposition, and vertical soil growth.17Fagherazzi S. Kirwan M.L. Mudd S.M. Guntenspergen G.R. Temmerman S. D'Alpaos A. van de Koppel J.M. Rybczyk E.R. Craft C. Clough J. Numerical models of salt marsh evolution: ecological, geomorphic, and climatic factors.Rev. Geophys. 2012; 50: RG1002Crossref Scopus (434) Google Scholar, 18Morris J.T. Sundareshwar P.V. Nietch C.T. Kjerve B. Cahoon D.R. Responses of coastal wetlands to rising sea level.Ecology. 2002; 83: 2869-2877Crossref Scopus (1189) Google Scholar, 19Redfield A.C. Development of a New England salt marsh.Ecol. Monogr. 1972; 42: 201-237Crossref Google Scholar These feedbacks lead to model-based predictions that CAR should be enhanced at higher rates of SLR.16Kirwan M.L. Mudd S.M. Response of salt-marsh carbon accumulation to climate change.Nature. 2012; 489: 550-553Crossref PubMed Scopus (196) Google Scholar,20Mudd S.M. Howell S.M. Morris J.T.( Impact of dynamic feedbacks between sedimentation, sea-level rise, and biomass production on near-surface marsh stratigraphy and carbon accumulation.Estuar Coast Shelf Sci. 2009; 82: 377-389Crossref Scopus (205) Google Scholar,21Morris J.T. Edwards J. Crooks S. Reyes E. Assessment of carbon sequestration potential in coastal wetlands.in: Lal R. Lorenz K. Hüttl R.F. Schneide B.U. von Braun J. Recarbonization of the Biosphere. Springer, 2012: 517-530Crossref Scopus (32) Google Scholar Field-based studies show that carbon accumulation is generally higher in places with higher RSLR15Wang F. Lu X. Sanders C. Tang J. 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Salt marsh ecosystem restructuring enhances elevation resilience and carbon storage during accelerating relative sea-level rise.Estuar Coast Shelf Sci. 2019; 217: 56-68Crossref Scopus (36) Google Scholar However, these point-based studies cannot address the feedbacks that control the spatial extent and distribution of wetlands.24Braun K.N. Theuerkauf E.J. Masterson A.L. Curry B.B. Horton D.E. Modeling organic carbon loss from a rapidly eroding freshwater coastal wetland.Sci. Rep. 2019; 9: 4204Crossref PubMed Scopus (10) Google Scholar Coastal wetlands are vulnerable to RSLR and human activity,25Kirwan M.L. Megonigal J.P. Tidal wetland stability in the face of human impacts and sea-level rise.Nature. 2013; 504: 53-60Crossref PubMed Scopus (957) Google Scholar, 26Törnqvist T.E. Jankowski K.L. Li Y.X. Gonzalez J.L. Tipping points of mississippi delta marshes due to accelerated sea-level rise.Sci. 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Relationships between salinity and short-term soil carbon accumulation rates from marsh types across a landscape in the Mississippi river Delta.Wetlands. 2017; 37: 313-324Crossref Scopus (27) Google Scholar, 31Theuerkauf E.J. Stephens J.D. Ridge J.T. Fodrie F.J. Rodriguez A.B. Carbon export from fringing saltmarsh shoreline erosion overwhelms carbon storage across a critical width threshold.Estuar Coast Shelf Sci. 2015; 164: 367-378Crossref Scopus (33) Google Scholar, 32Saintilan N. Khan N. Ashe E. Kelleway J. Rogers K. Woodroffe C. Horton B. Thresholds of mangrove survival under rapid sea level rise.Science. 2020; 368: 1118-1121https://doi.org/10.1126/science.aba2656Crossref PubMed Scopus (98) Google Scholar Here, we explore the link between CAR and RSLR in coastal wetlands across the continental United States (CONUS), and use higher-resolution observations from the Louisiana coast to determine how the balance between wetland size and carbon accumulation impact the net carbon balance across a rapidly submerging coastal landscape. To examine the drivers of CAR, we compiled a dataset of 372 CAR measurements in wetlands from across the CONUS (mangroves and marshes)15Wang F. Lu X. Sanders C. Tang J. Tidal wetland resilience to sea level rise increases their carbon sequestration capacity in United States.Nat. Commun. 2019; 10https://doi.org/10.1038/s41467-019-13294-zCrossref Scopus (34) Google Scholar and 131 additional salt and brackish marshes across coastal Louisiana (Louisiana Coastwide Reference Monitoring System [CRMS])33Coastal Protection and Restoration AuthorityLA Coastwide Reference Monitoring System Soil and Vegetation Data.2019https://lacoast.gov/crms2/home.aspxGoogle Scholar (see experimental procedures, Figure 1, and Table S1). For the United States dataset, we collated data on carbon accumulation (CAR, soil accretion rate [SAR], and soil carbon density) and environmental parameters (RSLR, tide range, mean annual temperature, and precipitation) directly from Wang et al.15Wang F. Lu X. Sanders C. Tang J. Tidal wetland resilience to sea level rise increases their carbon sequestration capacity in United States.Nat. Commun. 2019; 10https://doi.org/10.1038/s41467-019-13294-zCrossref Scopus (34) Google Scholar For the Louisiana dataset, we started with 274 CRMS sites27Jankowski K.L. Törnqvist T.E. Fernandes A.M. Vulnerability of Louisiana’s coastal wetlands to present-day rates of relative sea-level rise.Nat. Commun. 2017; 8: 14792Crossref PubMed Scopus (144) Google Scholar and filtered the data to isolate salt and brackish marshes, leaving us with a total of 131 saline and brackish marsh locations in our analysis. SARs and estimates of RSLR for the CRMS sites were taken directly from Jankowski et al.27Jankowski K.L. Törnqvist T.E. Fernandes A.M. Vulnerability of Louisiana’s coastal wetlands to present-day rates of relative sea-level rise.Nat. Commun. 2017; 8: 14792Crossref PubMed Scopus (144) Google Scholar We compiled measurements of organic content and bulk density of marsh soil using publicly available data,33Coastal Protection and Restoration AuthorityLA Coastwide Reference Monitoring System Soil and Vegetation Data.2019https://lacoast.gov/crms2/home.aspxGoogle Scholar and calculated CAR for each of the CRMS sites following established methods.14Ouyang X. Lee S.Y. Updated estimates of carbon accumulation rates in coastal marsh sediments.Biogeosciences. 2014; 11: 5057-5071Crossref Scopus (148) Google Scholar,15Wang F. Lu X. Sanders C. Tang J. Tidal wetland resilience to sea level rise increases their carbon sequestration capacity in United States.Nat. Commun. 2019; 10https://doi.org/10.1038/s41467-019-13294-zCrossref Scopus (34) Google Scholar,34Craft C. Clough J. Ehman J. Joye S. Park R. Pennings S. Guo H. Machmuller M. Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services.Front. Ecol. Environ. 2009; 7: 73-78Crossref Scopus (549) Google Scholar The combined database featured 503 measurements of carbon accumulation, spanning broad gradients in mean annual temperature, tide range, and dominant vegetation. We used a simple regression approach to examine the extent to which and the scale at which tidal wetland soil carbon accumulation (i.e., CAR) responded to physical (e.g., RSLR, accretion) and/or climatic (e.g., temperature) drivers (see experimental procedures). We use the term carbon accumulation as it has commonly been used in coastal wetland literature13Chmura G.L. Anisfeld S.C. Cahoon D.R. Lynch J.C. Global carbon sequestration in tidal, saline wetland soils.Glob. Biogeochem.Cycles. 2003; 17https://doi.org/10.1029/2002GB001917Crossref Google Scholar,14Ouyang X. Lee S.Y. Updated estimates of carbon accumulation rates in coastal marsh sediments.Biogeosciences. 2014; 11: 5057-5071Crossref Scopus (148) Google Scholar,30Baustian M.M. Stagg C.L. Perry C.L. Moss L.C. Carruthers T.J.B. Allison M. Relationships between salinity and short-term soil carbon accumulation rates from marsh types across a landscape in the Mississippi river Delta.Wetlands. 2017; 37: 313-324Crossref Scopus (27) Google Scholar to describe the accumulation of soil carbon in surficial sediments (<1 m soil depth) as measured by physical marker horizons (i.e., accumulated above ceramic tiles or feldspar layers), permanent benchmarks, and radioisotope or radiocarbon dating. Short-term (<50 years) CAR measurements include labile carbon that will decay with time and cannot be equated with the long-term carbon burial or sequestration. Nevertheless, short-term CAR measurements are useful because they correspond entirely to the period of accelerated RSLR (i.e., not averaged over periods of slow RSLR) and correspond to the depths of erosion typically observed in submerging salt marshes (<1 m).31Theuerkauf E.J. Stephens J.D. Ridge J.T. Fodrie F.J. Rodriguez A.B. Carbon export from fringing saltmarsh shoreline erosion overwhelms carbon storage across a critical width threshold.Estuar Coast Shelf Sci. 2015; 164: 367-378Crossref Scopus (33) Google Scholar,35Wilson C.A. Allison M.A. An equilibrium profile model for retreating marsh shorelines in southeast Louisiana.Estuar Coast Shelf Sci. 2008; 80: 483-494Crossref Scopus (103) Google Scholar Relationships between CAR and RSLR were generally weak across individual sites and within regions. CAR was significantly correlated with RSLR among all individual sites with estimates of both CAR and RSLR (n = 408, R2 = 0.42, root-mean-square error [RMSE] = 123.7), but the trend was driven mostly by sites in the Lower Mississippi region with RSLR rates >5 mm year−1 (Figure 2A). When assessed within regions, CAR-RSLR relationships were insignificant in all coastal regions except for the Lower Mississippi region (n = 171, R2 = 0.32, RMSE = 147.51) (Table S2). Statistical models for CAR using RSLR within regions had lower predictability than across regions (Table S2), likely due to subregional variation in RSLR that is not captured with a limited number of tide gauges, and lower statistical power associated with having fewer CAR data points. Moreover, factors other than RSLR (i.e., sediment supply, vegetation type, marsh platform elevation) may drive variability in CAR in regions with a narrow range of RSLR rates or very low rates of RSLR. In contrast to weak or insignificant relationships across sites and within regions, RSLR was a strong driver of CAR when both variables were averaged over contiguous coastal regions. RSLR explained 80% of the regional variation in CAR (R2 = 0.80, RMSE = 62.8) (Figure 2B and Table S2). A strong relationship between regional CAR and SLR persisted even when the high rates of RSLR in the Louisiana Gulf Coast were omitted (Figure S1 and Table S2). Eighty percent of the variation between CAR and RSLR was explained by the increase in vertical SAR under increased RSLR (Figures 3A and 3B; Table S3). Regional variation in soil carbon density was not significantly correlated with RSLR (Figure 3C). The inclusion of a carbon density × RSLR interaction in a mixed model showed similar power in predicting CAR (R2 = 0.45, RMSE = 124) compared with the least-squared model based on RSLR alone (R2 = 0.42, RMSE = 124) (Table S2). Together, these results suggest that the increase in CAR under elevated RSLR is primarily a product of increased vertical accretion (i.e., an increase in soil volume). A strong link between CAR, vertical accretion, and RSLR is consistent with a well-known ecogeomorphic feedback between flooding and increased sediment deposition,17Fagherazzi S. Kirwan M.L. Mudd S.M. Guntenspergen G.R. Temmerman S. D'Alpaos A. van de Koppel J.M. Rybczyk E.R. Craft C. Clough J. Numerical models of salt marsh evolution: ecological, geomorphic, and climatic factors.Rev. Geophys. 2012; 50: RG1002Crossref Scopus (434) Google Scholar,18Morris J.T. Sundareshwar P.V. Nietch C.T. Kjerve B. Cahoon D.R. Responses of coastal wetlands to rising sea level.Ecology. 2002; 83: 2869-2877Crossref Scopus (1189) Google Scholar a meta-analysis showing little spatial variability in carbon density across the United States,36Holmquist J.R. Windham-Myers L. Bernal B. Byrd K.B. Crooks S. Gonneea M.E. Herold N. Knox S.H. Kroeger K. Mccombs J. et al.Coastal Wetland Elevation and Carbon Flux Inventory with Uncertainty, USA, 2006-2011. ORNL DAAC, 2019Google Scholar and long-term data from sediment cores that show CAR has accelerated over time.23Gonneea M.E. Maio C.V. Kroeger K.D. Hawkes A.D. Mora J. Sullivan R. Madsen S. Buzard R.M. Cahill N. Donnelly J.P. Salt marsh ecosystem restructuring enhances elevation resilience and carbon storage during accelerating relative sea-level rise.Estuar Coast Shelf Sci. 2019; 217: 56-68Crossref Scopus (36) Google Scholar,37McTigue N. Davis J. Rodriguez A.B. McKee B. Atencio A. Currin C. Sea level rise explains changing carbon accumulation rates in a salt marsh over the past two millennia.J. Geophs. Res. 2019; 124: 2945-2957Crossref Scopus (12) Google Scholar As we discuss in the next section, a positive relationship between RSLR and CAR could potentially be explained by allochthonous carbon deposition, where fast RSLR leads to marsh erosion and enhanced deposition of eroded carbon onto surviving marsh (i.e., Figure 4). Alternatively, rapid vertical accretion has been suggested to enhance the preservation of organic matter by accelerating the advection of material below the surface soil layers where decomposition is most intense.16Kirwan M.L. Mudd S.M. Response of salt-marsh carbon accumulation to climate change.Nature. 2012; 489: 550-553Crossref PubMed Scopus (196) Google Scholar,20Mudd S.M. Howell S.M. Morris J.T.( Impact of dynamic feedbacks between sedimentation, sea-level rise, and biomass production on near-surface marsh stratigraphy and carbon accumulation.Estuar Coast Shelf Sci. 2009; 82: 377-389Crossref Scopus (205) Google Scholar,38Choi Y. Wang Y. Dynamics of carbon sequestration in a coastal wetland using radiocarbon measurements.Glob. Biogeochem Cycles. 2004; 18https://doi.org/10.1029/2004GB002261Crossref Scopus (116) Google Scholar However, more efficient carbon preservation would be expected to lead to higher soil carbon densities in places with rapid vertical accretion, which is inconsistent with our findings. Therefore, we suggest that the relationship is driven primarily by increases in soil volume rather than increases in the concentration of carbon in the soil. Least-square models indicate that climatic variables had little influence on soil CAR (Figure S2). Mean annual temperature (MAT) and mean annual precipitation (MAP) were not correlated with CAR when averaged at regional scales (n = 7 regions, p < 0.05, Figures S2A and S2C). When individual site level data (n = 408) were included, statistical models showed a correlation between CAR, MAT, and MAP that was driven primarily by high CAR in the warm and wet Lower Mississippi Delta region (Figures S2B and S2D), but RMSE was high for both climate variables and they explained only 2%–3% of the variance in the data, respectively. Furthermore, mixed models including all physical, biotic, and climatic drivers showed no improved prediction with inclusion of these terms. These findings are consistent with other meta-analyses that show little relationship between temperature and CAR.13Chmura G.L. Anisfeld S.C. Cahoon D.R. Lynch J.C. Global carbon sequestration in tidal, saline wetland soils.Glob. 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Mudd S.M. Response of salt-marsh carbon accumulation to climate change.Nature. 2012; 489: 550-553Crossref PubMed Scopus (196) Google Scholar While a high rate of RSLR drives enhanced CAR, RSLR may also enhance marsh drowning and loss,34Craft C. Clough J. Ehman J. Joye S. Park R. Pennings S. Guo H. Machmuller M. Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services.Front. Ecol. Environ. 2009; 7: 73-78Crossref Scopus (549) Google Scholar,41Unger V. Elsey-Quirk T. Sommerfield C. Velinsky D. Stability of organic carbon accumulating in Spartina alterniflora-dominated salt marshes of the mid-Atlantic U.S.Estuar. Coast Shelf Sci. 2016; 182 pt A: 179-189Crossref Scopus (26) Google Scholar, 42Schuerch M. Spencer T. Temmerman S. Kirwan M.L. Wolff C. Lincke D. McOwen C.J. Pickering M.D. Reef R. Vafeidis A.T. et al.Future response of global coastal wetlands to sea-level rise.Nature. 2018; 561: 231-234Crossref PubMed Scopus (340) Google Scholar, 43Kirwan M.L. 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Thresholds of mangrove survival under rapid sea level rise.Science. 2020; 368: 1118-1121https://doi.org/10.1126/science.aba2656Crossref PubMed Scopus (98) Google Scholar,44Hopkinson C.S. Cai W.J. Hu X. Carbon sequestration in wetland dominated coastal systems-a global sink of rapidly diminishing magnitude.Curr. Opin. Environ. Sustain. 2012; 4: 186-194Crossref Scopus (151) Google Scholar,45Spivak A. Sanderman J. Bowen J. Canuel E. Hopkinson C. Global-change controls on soil-carbon accumulation and loss in coastal vegetated ecosystems.Nat. Geosci. 2019; 12: 685-692Crossref Scopus (80) Google Scholar To determine whether enhanced CAR in surviving marshes can offset significant carbon losses from declining marsh area, we estimated net changes in marsh soil carbon across the saline and brackish marshes of the Louisiana coast, where rates of RSLR and land-loss rates are among the highest in the world. We u