Carbon accumulation rates in salt marsh sediments suggest high carbon storage capacity

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Introduction
Salt marshes are intertidal vegetated wetland ecosystems, dominant on protected shorelines and on the edge of estuaries in a range of climatic conditions, from subarctic to tropical, while most extensive in temperate latitudes (Mitsch et al., 1994;Butler and Weis, 2009;Laffoley and Grimsditch, 2009).The combination of characteristic vegetation, geomorphology and habitat conditions of salt marshes provide essential ecosystem goods and services, including biogeochemical cycling and transportation of nutrients, habitat or food for coastal biota, shield and protecting coastal areas from storms and floods, water filtration, recreation and cultural benefits.However, salt marshes also critically suffer from losses due to dredging, filling, draining, construc-Introduction

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Full tion and are particularly threatened by sea level rise as a result of "coastal squeeze" (Doody, 2004;Craft et al., 2008;Polunin, 2008;Gedan et al., 2009;Koch et al., 2009).Salt marshes appear to be highly efficient in carbon burial, but studies on global carbon accumulation of salt marshes lag behind other coastal ecosystems.Firstly, data on salt marsh extent and carbon stock are patchy.A reliable estimate of global saltmarsh extent is lacking, and large areas of saltmarsh have never been mapped.Existing studies of carbon stock on salt marshes tend to focus on specific sites and lack a broader global perspective (Callaway et al., 2012).Chmura et al. (2003) examined global carbon sequestration of salt marshes, but their study only covered a latitudinal range from 22.4 • S to 55.5 • N. Secondly, carbon sequestration by mangroves and seagrasses has been analyzed with specific hypotheses in mind, such as the existence of clear latitudinal gradients (McLeod et al., 2011), while such an approach has rarely been attempted for salt marshes.The lack of a global view of carbon accumulation and storage in salt marshes contributes to this deficiency.Considerable studies have investigated carbon accumulation of salt marshes in different sites, including elevation gradients from low to mid or high marsh (Callaway et al., 1996(Callaway et al., , 2012;;Connor et al., 2001;Elsey-Quirk et al., 2011;Adams et al., 2012;Schuerch et al., 2012), but these studies focused on carbon density, organic matter and sediment accretion and no direct estimates have been reached concerning carbon accumulation capacity.Finally, how sediment carbon accumulation may respond to tidal range and species occurrence has been studied individually in specific sites and for various genera of salt marshes (Rothman and Bouchard, 2007;Zhou et al., 2007;Mahaney et al., 2008), but a global consideration of pattern is still lacking.Even though salt marshes have been intensively investigated for more than fifty years, the global capacity for carbon sequestration by salt marshes is yet to be assessed.A global analysis will provide an opportunity to identify the role of these hotspots in climate change impact in terms of carbon storage and to inform future global conservation efforts.Carbon sinks in salt marshes generally consist of aboveground biomass, belowground biomass and soils.Globally, it is recognized that soils contain the largest quan-Figures

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Full tity of carbon in a range of ecosystems and two thirds of carbon is in the form of organic matter (Batjes, 1996).Likewise, the largest carbon stock of salt marshes is soil organic carbon (Murray et al., 2011), which is influenced by the carbon accumulation rate (CAR).Estimating global salt marsh CAR is significant to understanding carbon sequestration by salt marsh sediments.
CAR is calculated as the product of sediment accretion rate (SAR) and average carbon density of the soil (Connor et al., 2001;Ford et al., 2012).To date, studies on CAR have been restricted in geographic extent, whereas comprehensive data are available on SAR and soil carbon density in salt mash ecosystems.Combining data of the two parameters will establish a global CAR inventory of salt marshes.This paper aims to refine the global CAR inventory of salt marshes, on the basis of published studies on specific regions, and to explore regional differences (including latitudinal and biogeographic differences) in CAR, as well as the nexus of CAR with tidal range, latitude and halophyte genera.Then the relationship between CAR and elevation change from low marsh to high marsh will be addressed.Finally, CAR and carbon budget of salt marsh sediments are compared with those of other coastal wetland and forested terrestrial ecosystems.

Data sources and collation
We searched for relevant studies using the databases Science Citation Index Expanded, Conference Proceedings Citation Index-Science and Book Citation Index-Science within ISI Web of Science (Thomson Reuters), using the Boolean search statement: Topic = (salt * marsh Introduction

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Full (a) Some studies recorded CAR by sequestered CO 2 .The values were considered as CAR, because salt marshes produce negligible methane (Connor et al., 2001;Callaway et al., 2012).
(b) As far as studies regarding accumulation rate of organic matter were concerned, the conversion factor of soil carbon was adopted as 0.55 of soil organic matter (Lovelock et al., 2010).
(c) As for studies only reporting soil carbon density, related research was searched in the same regions with respect to vertical SAR, which may involve a variety of markers (Ouyang et al., 2013), including long-term 137 Cs, 210 Pb markers and short-term marker horizons.Then CAR was obtained by multiplying SAR and soil carbon density.As SAR could be variable over small spatial scales, CAR estimation is expectedly influenced by data availability.Despite the absence of method description in 9 % of the studies, most (64 %) employed radionuclide (i.e. 137Cs, 210 Pb markers) to measure SAR, while another 27 % of studies used marker horizons.CAR derived from different methods for SAR measurement may generate biases in comparison of CAR.
Following the above rules, we examined individual studies to confirm the validity of the data.Studies were excluded if they were based on model simulation.This process filtered the studies down to 50, including 37 studies that SAR and soil carbon density data were used to calculate CAR, while the remaining 13 studies directly reported CAR.In addition, among the 50 studies, 47 were based on sediment samples of short Introduction

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Full cores (< 1 m), whereas only 3 studies sampled using deeper cores.Overall, the studies covered a latitudinal range from 40 • S to 78.3 • N (Table 1).
A considerable amount of literature has reported the area of salt marshes by specific sites and regions (Dijkema, 1987;O'Callaghan, 1990;Shi-lun and Ji-yu, 1995;Hanson and Calkins, 1996;Saint-Laurent, 1996;Lawrence et al., 2012), while reports of estimates of the global area are scarce.In this study, data of published studies were compiled and to provide an estimate of the present global extent of salt marshes.The global total C stock in salt marshes was then estimated by multiplying region-specific CAR and the respective regional areal extent of salt marshes.

Data analysis
Analyses were conducted using SPSS 21.0.0.0 (SPSS Inc., Chicago, IL, USA) and R version 3.0.2(R Core Team, 2013).Deviations are reported as the standard error (SE).For statistical comparisons, data were tested for normality with the Kolmogorov-Smirnov test and for homogeneity of variance with the Levene's test (α = 0.05).When homogeneity of variance between groups was violated, data were transformed (ln(x), 1/x, or x 1/2 ) to satisfy the assumption.Boxplots were used to describe latitudinal distribution of CAR data.Paired-sample t test was used to compare the paired CAR from marshes with different elevations at the same site.One-way analysis of variance (ANOVA) was applied to compare more than two means and Tukey's test was used as post-hoc pairwise test where there was a significant treatment effect.
Stepwise multiple regression was used to determine which of the independent variables, viz.tidal range, latitude (a proxy of temperature) and halophyte genera, accounted for most of the variation in CAR.The six major genera were included as a categorical variable with five levels, while Elymus and Sarcocornia were excluded owing to few available data.Each level has two values, namely 0 and 1.The categorical variable, serving as a qualitative variable, was included as a block with the default Introduction

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Full "Enter" method, whereas tidal range and latitude were included as another block with the default "Stepwise" method in the multiple regression model.

Regional difference in carbon accumulation rate
In order to assess the regional difference in carbon sequestration by salt marshes, soil CAR was calculated for the eight salt marsh groups (Table 3), for the six dominant halophyte genera (Table 4), and for latitudinal intervals of 10 • from 28.4 • N to 78.5 • N. Region-specific CAR and area were combined to produce a global CAR of salt marshes.Globally, mean CAR in salt marshes sediment is 242.2 ± 25.9 g C m −2 yr −1 (Table 5).
In contrast to existing studies, our results showed both differences and common features.Firstly, the average CAR of our study was higher than those from earlier reports, averaged 151 g C m −2 yr −1 (Chmura et al., 2003;Duarte et al., 2005).Our estimate has revised the former estimates upward by roughly 60 %.The underpinning source of the difference may relate to the fact that the earlier reports (1) have smaller latitudinal ranges (from 22.4 • S to 55.5 • N); (2) suffer from the lack of data from significant regions, including the Asia-Pacific, Arctic and Australasia; (3) used a simplistic method for upscaling CAR from individual sites to the global coverage.
The highest average accretion rate of soil carbon, i.e. 477.1 g C m −2 yr −1 , was recorded from the Mediterranean, with vegetation dominated by Spartina spp.The largest carbon stock was stunningly in accordance with data of soil carbon stores in seagrass ecosystems, which was also found in Mediterranean meadows dominated by Posidonia oceanica (Fourqurean et al., 2012).However, the average CAR of salt marsh soils in the Arctic is an order of magnitude lower (34.9 g C m −2 yr −1 ) than those of all other regions (128.5 to 477.1 g C m −2 yr −1 ).Furthermore, as shown in Table 3, among the six halophyte genera, Halimione demonstrated the highest capacity for soil Introduction

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Full carbon accumulation, with average CAR at 486.9 g C m −2 yr −1 , while average CAR of Puccinellia (34.4 g C m −2 yr −1 ) ranked the lowest.Significant differences in CAR exist among genera (ANOVA, P < 0.001), basically due to the significantly lower average CAR of Puccinellia than those of other genera (Tukey's test, P < 0.001).As Puccinellia is distributed in the coldest Arctic, in contrast to others growing in temperate or tropical regions in our studying sites, the difference may be attributed to the interregional difference in temperature.Lastly, there is significant latitudinal variation of CAR in saltmarsh sediments (ANOVA, P < 0.001) (Fig. 2).
For exploring the drivers of CAR variation, the nexus of CAR with tidal range, latitude and the dominant halophyte genera was analyzed using multiple linear regressions.
Latitude accounted for most of the variation (51.7 %) in CAR (P < 0.01).Similarly, tidal range and halophyte genera represented 29.3 % and 18.2 % of the variation in CAR (P < 0.01).
These results suggest that carbon sequestration by salt marsh sediments is affected by multiple biogeochemical and biotic factors.Tidal range determines belowground carbon dynamics (root production, carbon burial) through influencing sediment aeration and porewater flow, also affecting sediment and organic matter import/export dynamics.Soil CAR for saltmarshes was shown positively related to belowground biomass productivity and negatively related to organic matter decomposition (Elsey-Quirk et al., 2011;McLeod et al., 2011;Gonzalez-Alcaraz et al., 2012), which are the predominant biotic processes for carbon accumulation.Both processes are affected by tidal range.For a given inundation depth, biomass productivity should be greatest in low tidal range environment (Schuerch et al., 2012).Where biomass productivity may be low (e.g.some Mediterranean marshes), retention of organic matter is usually high in these micro-tidal environments (Ibañez et al., 2000).Thus CAR could be higher in micro-tidal marshes.Further, tidal range may result in differences in the frequency of tidal flooding (Chmura et al., 2011) litter input.A number of studies have revealed that different species of halophyte inhabiting salt marshes contributed different quality and quantities of litter to salt marsh sediments (Zhou et al., 2007;Mahaney et al., 2008).Soil microbe mediated decomposition also changes with litter species (Rothman and Bouchard, 2007).These factors combined would result in variation in the quality (e.g.stoichiometry and form of essential elements) as well as quantity (e.g.different production and turnover rates) of organic matter in salt marsh sediments.
As latitude is a proxy of temperature, this study suggests that CAR changes markedly with temperature.This result is in contrast to earlier reports suggesting that average annual temperature explains only 5 % of CAR variability, and the relationship between temperature and CAR was limited (Chmura et al., 2003).Generally, this study suggests CAR of salt marsh sediments peaks at mid-latitudinal range 48.5 ∼ 58.5 • N, and decreases towards the poles and the equator.This pattern corresponds with the general latitudinal pattern of salt marsh development.

Variation of CAR with marsh elevation
Data from a wide range of sites, with regard to marsh elevation, i.e. from low, mid to high marsh, were analyzed to evaluate how CAR varies with salt marsh elevation.Soil CAR presents a clear declining trend from low marsh to mid or high marsh across all locations, while transition from mid to high marsh can result in opposite changes (Fig. 3).Significant heterogeneity (paired-sample t test, P < 0.05) exists between CARs of low and mid or high marsh (Table 6), with CAR being highest in the low marsh irrespective of location.
The variation of CAR with respect to elevation could be explained by its determining variables.CAR is decided by three parameters, i.e.SAR, dry bulk density of the soil (DBD) and its organic carbon content, which is positively related to loss on ignition (LOI).Connor et al. (2001) reported that low marsh sediments were characterized by higher soil bulk densities and lower LOI.According to Chmura and Hung (2004), SAR decreases with distance from the nearest creek, i.e. low marsh have higher SAR than Introduction

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Full high marsh, probably due to shorter inundation time and thus sediment input.Moreover, Oenema and Delaune (1988) developed a function describing the relationship between SAR and the distance of marsh from the major creeks, and further showed that SAR of low marsh is higher than that of high marsh.As provided above, CAR can be expressed as the following equation.
In the above equation, CAR is promoted by high SAR and DBD in the low marsh, while the lower carbon content pushes values the opposite direction.High marsh sediments, however, are likely to have a higher carbon content (Connor et al., 2001;Zhou et al., 2007).The pattern of low marsh having higher CARs suggests that this increase in carbon content is more than offset by the decrease in SAR and DBD while going landward.
In our collated literature, CAR of mid marsh was lower than high marsh in general.The reason for this lack of a clear-cut pattern from low to high marsh is unclear but differences in tidal inundation duration and flow dynamics between the mid and high marsh elevations are expected to be smaller than those between low and mid elevations.

Global CAR in salt marsh sediments compared with other ecosystems
Our global estimate of salt marsh carbon stocks was based on the mean value of the 158 sites so that the high CAR of the Mediterranean did not unduly affect the global figure.The product of our mean regional CAR and the area of salt marshes for the reported regions estimates the global CAR of salt marsh sediments to be about 10.1 Tg C yr −1 (Table 7).
Our estimate of global sediment CAR in salt marshes (10.1 ± 1.1 Tg C yr −1 ) is lower than both its neighbouring coastal mangrove and seagrass ecosystems (31.extent of this habitat.The high capacity of carbon sequestration in salt marsh sediments is attributed to oxygen-depleted conditions reducing mineralisation rate, continual sediment deposition, and the combined high primary production but low export rates which facilitate accumulation of organic matter (Hussein et al., 2004;Loomis and Craft, 2010;Callaway et al., 2012;Keller et al., 2012).
Our data demonstrate that salt marshes are significant habitats for carbon accumulation in the biosphere, acting as important but previously neglected carbon sequesters.The remarkable combination of their high capacity for carbon-sequestration but low carbon stock in salt marshes could reflect the past management approach to these habitats, which has resulted in significantly reduced areal extent.The "coastal squeeze" phenomenon affects salt marshes most significantly and, if not managed timely, will continue to erode the importance of salt marshes as potential carbon storage.Despite their high capacity of carbon accumulation, when compared with terrestrial forests, carbon buried in salt marshes, as part of "blue carbon", can be stable over longer time scales (millennia) (Duarte et al., 2005;McLeod et al., 2011) and decompose at lower rate (Reddy and DeLaune, 2004), while most forest carbon stocks are eventually released to atmosphere during forest fires (Fourqurean et al., 2012).
However, this global estimate of CAR in salt marshes needs to be interpreted with caution since the estimate is limited by the quality and quantity of available data.Firstly, the reported global area of salt marshes is far from complete and has not covered all habitats of saltmarsh halophytes.Secondly, there are some compromises made when making extrapolations from a limited data base.For example, CAR of the Mediterranean was estimated from the more humid south European countries, which may overestimate the regional value encompassing also marshes of the arid north African regions, i.e.Tunisia and Morocco, even though these regions belong to the Mediterranean.Accordingly, further studies will be needed to refine CAR of this study when more data are available from a more comprehensive coverage of halophyte habitats in the future.

Conclusions
With sediment CAR averaged at 242.2±25.9g C m −2 yr −1 , our global estimate indicates that salt marshes rank among the most effective ecosystems in carbon sequestration.
The highest CAR was in the Mediterranean, whereas the lowest CAR was in the Arctic.
Regarding the six major halophyte genera, Halimione-dominated marshes have the highest CAR, whereas the CAR of Puccinellia-dominated habitats have the lowest.
Owing to the comparatively small areal extent of salt marshes, global carbon buried in salt marshes is approximately 10.1 Tg C yr −1 , which is far lower than those of other coastal ecosystems and terrestrial forest ecosystems.Our analysis suggests that the CAR of salt marshes changes with latitude, tidal range, halophyte genera and habitat elevation.It is indicated that CAR of salt marshes varied significantly at latitude intervals of 10 • from 28.4 • N to 78.5 • N.These factors drive CAR variation through physical and biotic control on belowground biomass productivity, microbial decomposition and litter input.Furthermore, it is clear that the CAR of low marsh was higher than mid or high marsh, whereas the capacity of carbon sequestration in mid marsh was generally lower than that of high marsh.Further field studies and experiments are needed to investigate the underlying forces driving carbon sequestration with respect to marsh elevation.
The findings of this study confirm salt marshes as significant coastal hotspots in sequestering carbon.However, with an annual loss rate of 1 % to 2 % between 1980 and 2000 (Duarte et al., 2008), and with loss continuing, just like the mangroves (Kristensen et al., 2008), this trend seriously compromises the capacity of salt marshes for carbon storage unless proper management and rehabilitation is implemented.There are significant data gaps in salt marsh CARs.Further research on CAR of salt marshes in South America and South Asia as well as inclusion of the full range of salt marsh halophytes is strongly recommended.Introduction

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Fig. 1 .Fig. 2 .Fig. 3 .
Fig. 1.Groupings and CAR of global salt marsh ecosystems.The eight groups span latitudes from 40• S to 78.3• N, colonizing the coasts and estuaries of the Pacific, Atlantic, Indian and Arctic Oceans.The background graph indicating sites of salt marshes is based onMold (1974) andMurray et al. (2011).While significant salt marsh occurrences are present in South America, insufficient data is available for inclusion in this analysis since there are no pertinent references.Colour dots are used to account for CAR levels of individual sites that were indicated in Table 1 from 50 studies, whereas dull colour dots represent sites without CAR data.There are not substantial data for the Sino-Japan region, as such a big circle is used to represent the average CAR of this region.Only locations with published data allowing calculation of CAR are represented for clarity.NEP -NE Pacific; TWA -Tropical W. Atlantic; NWA -NW Atlantic; AR -Arctic; NE -N Europe; M -Mediterranean; SJ -Sino-Japan; AU -Australasia.

Table 1 .
The distribution and CAR of salt marshes from the literature.

Table 4 .
Comparison of CAR among halophyte genera.Post-hoc pairwise test (Tukey test) ANOVA was run to test which genera are different from the others.Since soil CAR of Distichlis and Juncus did not conform to normality, they were excluded from the ANOVA.There is a significant difference in CAR among the other four groups (ANOVA, P < 0.001).Groups sharing the same superscript are not significantly different from each other (P > 0.05).

Table 7 .
Comparison of carbon accumulation in sediments and soils of salt marshes and other ecosystems.