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Summary
1. Seagrass meadows are sites of high rates of carbon sequestration and they potentially support
‘blue carbon’ strategies to mitigate anthropogenic CO2 emissions. Current uncertainties on the fate
of carbon stocks following the loss or revegetation of seagrass meadows prevent the deployment of
‘blue carbon’ strategies.
2. Here, we reconstruct the trajectories of carbon stocks associated with one of the longest moni-
tored seagrass restoration projects globally. We demonstrate that sediment carbon stocks erode fol-
lowing seagrass loss and that revegetation projects effectively restore seagrass carbon sequestration
capacity. We combine carbon chronosequences with 210Pb dating of seagrass sediments in a mea-
dow that experienced losses until the end of 1980s and subsequent serial revegetation efforts.
3. Inventories of excess 210Pb in seagrass sediments revealed that its accumulation, and thus sedi-
ments, coincided with the presence of seagrass vegetation. They also showed that the upper sedi-
ments eroded in areas that remained devoid of vegetation after seagrass loss. Seagrass revegetation
enhanced autochthonous and allochthonous carbon deposition and burial. Carbon burial rates
increased with the age of the restored sites, and 18 years after planting, they were similar to that in
continuously vegetated meadows (26.4 0.8 gCorg m2 year1).
4. Synthesis. The results presented here demonstrate that loss of seagrass triggers the erosion of his-
toric carbon deposits and that revegetation effectively restores seagrass carbon sequestration capac-
ity. Thus, conservation and restoration of seagrass meadows are effective strategies for climate
change mitigation.
Key-words: aquatic plant ecology, blue carbon, burial, carbon sink, climate change mitigation,
erosion, Oyster Harbour, Posidonia australis, restoration
piece of evidence (Greiner et al. 2013). The consequences of appropriate decay–ingrowth corrections (i.e. 210Po decay during
habitat loss for the fate of sediment carbon stocks have been counting, 210Po decay between plating and counting and 210Pb decay
assessed for mangroves (Lovelock, Ruess & Feller 2011; Si- between sampling and analyses) and accounting for blank (for each
dik & Lovelock 2013; Kauffman et al. 2014), but designing batch of 10 samples) and detector background, which were both
almost negligible (1–2105 cs1). Analyses of replicates and refer-
similarly robust tests for seagrass meadows has proved chal-
ence materials were carried out in parallel to the analyses of the sam-
lenging (Duarte et al. 2013b).
ples to ensure reproducibility of the results. Concentrations of 226Ra
Here, we demonstrate that loss of seagrass meadows causes were determined by gamma spectrometry using a high-purity Ge
erosion of the sediment carbon stock and that seagrass resto- well-type detector (CANBERRA, mod. GCW3523). Samples were
ration projects preserve sediment carbon deposits and restore stored in sealed containers for 3 weeks prior to counting to attain
the carbon sink capacity of the seagrass ecosystem. This dem- equilibrium between 226Ra and its shot-lived decay products. 226Ra
onstration is based on detailed reconstructions of the decadal was determined through the 295 and 351 keV emission lines of
214
trajectory of carbon stocks, combining carbon chronosequenc- Pb. The concentrations of 226Ra were in agreement with those of
210
es with 210Pb dating of seagrass sediments in meadows (Oys- Pb in the deepest sections of the cores, where no excess 210Pb
ter Harbour, SW Australia) that experienced losses until the (210Pbex) was present. All sediment cores had similar concentrations
end of 1980s but have had subsequent increases in seagrass of supported 210Pb (i.e. in equilibrium with 226Ra;
1
210
Pbsup = 8.7 0.4 Bqkg ). Concentrations of 210Pbex were
cover through serial revegetation efforts.
obtained by subtracting the 210Pbsup from the total 210Pb at each sec-
tion. We used the model of constant rate of supply (CRS; Appleby &
Materials and methods Oldfield 1978), which assumes a constant flux of 210Pbex to the sedi-
ment surface, to date the sediment based on 210Pbex inventories and
This study was conducted at Oyster Harbour (Western Australia; Fig. estimate sediment accretion rates in the cores. The CRS model was
S1 in Supporting Information), which is a 16 km2 shallow (average adapted for those sites with missing inventories of 210Pbex (i.e. reveg-
depth 1–2 m) coastal inlet colonized by luxuriant seagrass (Posidonia etated in 1994 and 2004, unvegetated) following Appleby (2001).
australis) meadows until the early 1960s. Between mid-1960s and Sediment accretion rates measured in the cores allowed estimation of
1988, about 80% of seagrass cover was lost (Hillman et al. 1990) the thickness of the carbon stock accumulated in restored sites since
due to elevated nutrient inputs and silt discharges into the inlet during planting. During sediment coring, the sediment samples were verti-
periods of heavy rain associated with land clearing and application of cally compressed by 36.5% (i.e. 100 cm of original sediment thick-
fertilizers for agriculture over much of Oyster Harbour’s catchment ness resulted in sediment cores 63.5 cm long) due to the low bulk
(Cambridge, Bastyan & Walker 2002). A seagrass (P. australis) density. We provide the values measured in the cores and, when indi-
planting project was initiated in November 1994 and finished in Janu- cated (i.e. carbon density, sediment accretion rate), estimated by
ary 2006, encompassing a total of 5 planting events (Table S1 in Sup- assuming linear sediment compression during sampling.
porting Information).
In March 2012, we collected 3-replicated sediment cores (9 cm
Results
diameter and 12–15 cm long) per restored site along the planting
chronosequence (i.e. years 1994, 1997, 2003, 2004, 2006). Similarly, The concentration and density of Corg measured in the sedi-
we collected three sediment cores in two bare sites, previously colo- ments at Oyster Harbour ranged between 1.6% DW and
nized by seagrasses, and in a large seagrass patch that survived the 16.9% DW and 0.01 g Corg cm3 and 0.06 g Corg cm3 (i.e.
disturbances in the second half of the 20th century that we considered
0.01 g Corg cm3 and 0.04 g Corg cm3 after correcting for
a mature and thus reference meadow. We measured sediment bulk
sediment compression), respectively. Corg concentration and
density and organic matter content and pools along all sediment cores
density varied with sediment depth and tended to increase
sliced at 1-cm interval. Organic carbon content was estimated from
loss of ignition (LOI) at 550 °C for 5 h using an empirically fitted from unvegetated to restored sites and the continuously vege-
equation for Oyster Harbour sediments (see Fig. S2 in Supporting tated meadow (Figs 1 and 2). On average, Corg concentration
Information). and density in the upper 12 cm of sediments in the reference
We analysed the d13C of the organic carbon in the top 3 cm sedi- meadow were, respectively, 63% and 37% higher than those
ment layer (d13Csediment) along the chronosequence to estimate the in unvegetated sediments and restored meadows. Differences
fraction of seagrass (X) and sestonic (1–X) deposition as in concentration and density of Corg across sites were more
pronounced in surface sediments (top 3 cm), both parameters
d13 Csediment ¼ ½Xd13 Cseagrass þ ½ð1 XÞd13 Cseston
significantly increasing along the planting chronosequence
being d13Cseagrass 9.65& and d13Cseston 22& (Dauby 1989). (regression analysis, P < 0.0001). Corg density in the top
We determined the profiles of 210Pb concentrations of sediment 3 cm sediment layer of the earliest replanted site (planted in
cores harvested in the continuously vegetated meadow, one bare site 1994) was 79% of that in the continuously vegetated mea-
and from sites that were revegetated in 1994 and 2004. Concentra-
dow. Seagrass tissues (with epiphytes) and seston particles
tions of 210Pb were determined through the analysis of its decay prod-
were the main sources of sediment Corg at Oyster Harbour.
uct 210Po, in equilibrium with 210Pb (Sanchez-Cabeza, Masque &
The proportion of seston in the surface sediment Corg pool
Ani-Ragolta 1998). Sediment samples were spiked with known
amounts of 209Po and acid digested using a microwave oven. The Po varied from 0.12 in the bare sites to 0.30 in the continuously
isotopes were plated onto silver discs and their emissions were mea- vegetated meadow (Fig. 3). The sestonic contribution to sedi-
sured by alpha spectrometry using Passivated Implanted Planar Sili- ment Corg increased with increasing time after the sediments
con (PIPS) detectors (CANBERRA, Mod. PD-450.18 A.M). The were revegetated, but this relationship was not significant
concentrations of 210Pb at sampling time were calculated applying (regression analysis, P > 0.05).
© 2015 The Authors. Journal of Ecology © 2015 British Ecological Society, Journal of Ecology, 103, 296–302
298 N. Marba et al.
–2
–4
–6
–8
–10
–12
Sediment depth (cm)
–14
Revegetated Revegetated
Unvegetated 1 Unvegetated 2 in 2006 in 2004
–16
0 4 8 12 0 4 8 12 0 4 8 12 0 4 8 12
0
–2
–4
–6
–8
–10
–12
Fig. 1. Measured sediment profiles of Corg concentration (%DW) where seagrasses were lost, in revegetated plots and the continuously vegetated
meadow at Oyster Harbour. The data shown are not corrected for (35%) sediment compression during coring. Error bars show the standard error
of the mean (n = 3). Error bars not available when n = 1.
The 210Pbex concentrations in seagrass sediments declined revegetated in 1994 and 2004 (159 43 Bqm2) compares
below the upper layer of mixed sediments (2–3 cm) until the extremely well to the actual amount of 210Pb (i.e 166
horizon of supported 210Pb, reached at about 7–9 cm depth 6 Bqm2) expected to accumulate from 1994 to 2004, after
(or 5–6 gcm2) (Fig. 4a). In contrast, unvegetated sediments correction for decay during the 10-year period and to sam-
had 210Pbex only in the uppermost 2 cm (Fig. 4a). The differ- pling time. Similarly, the time when seagrasses in restored
ences in the 210Pbex concentration profiles between the contin- sites were lost can be calculated from the 210Pbex inventories
uously vegetated meadow, restored sites and unvegetated in sediments using:
sediments translated into significant disparities in the accumu-
If ¼ I0 e k t
lated 210Pbex (i.e. 210Pbex inventories, in Bqm2, Fig. 4b).
The sediment in the continuously vegetated meadow had the where If and Io are the measured and expected inventories,
largest 210Pbex inventory (Io = 800 28 Bqm2), corre- respectively. This reveals that seagrass meadows at the studied
sponding to an annual flux (Fo) of 210Pbex of sites were lost 28 3 years before our collection of samples.
25 1 Bqm2year1 (calculated as Fo = kIo, where k is However, the missing inventory of 210Pbex in unvegetated sedi-
the decay constant of 210Pb: 0.03118 year1). The 210Pbex ments was much larger than expected by decay of 210Pb during
inventories at the revegetated sites were smaller than in sedi- the last decades. Considering that the seagrass meadows at the
ments from the continuously vegetated meadow, while unveg- three sites where vegetation was lost disappeared approxi-
etated sediments were even more significantly depleted in mately in the early 1980s, and that no 210Pbex accumulation
210
Pbex. The difference in 210Pbex inventories in sediments occurred in the absence of seagrass cover, the 210Pbex inventory
© 2015 The Authors. Journal of Ecology © 2015 British Ecological Society, Journal of Ecology, 103, 296–302
Seagrass loss, revegetation and carbon sequestration 299
0.01 0.02 0.03 0.04 0.05 0.01 0.02 0.03 0.04 0.05 0.01 0.02 0.03 0.04 0.05 0.01 0.02 0.03 0.04 0.05
0
–2
–4
–6
–8
–10
–12
Sediment depth (cm)
–14
Revegetated Revegetated
Unvegetated 1 Unvegetated 2
in 2006 in 2004
–16
0.01 0.02 0.03 0.04 0.05 0.01 0.02 0.03 0.04 0.05 0.01 0.02 0.03 0.04 0.05 0.01 0.02 0.03 0.04 0.05
0
–2
–4
–6
–8
–10
–12
–14
Revegetated Revegetated Revegetated Continuously
in 2003 in 1997 in 1994 vegetated
–16
Fig. 2. Measured sediment profiles of Corg density (gC cm3) where seagrasses were lost in the revegetated plots and the continuously vegetated
meadow at Oyster Harbour. The data shown are not corrected for (35%) sediment compression during coring. Error bars show the standard error
of the mean value (n = 3). Error bars not available when n = 1.
in the unvegetated site should have been of 340 12 Bqm2, for 6 years to 25.2 4.7 Corg m2 year1 in sites restored
whereas only 75 11 Bqm2 remained. The lack of 210Pb for 18 years (Fig. 5b). The fitted equation between Corg burial
accumulation in unvegetated sediments since vegetation loss rate and the age of revegetated plots indicated that restored
can account for about 65% of the missing inventory of 210Pbex, sites reach a similar Corg burial rate as that in the continu-
but the other 35% must have been lost through sediment ero- ously vegetated meadow (26.4 0.8 Corg m2 year1,
sion. Fig. 5b) 18 years after restoration.
Mean mass accumulation rates (MAR) and sediment accu-
mulation rates (SAR) estimated by applying the CRS model
Discussion
adapted when necessary to those sites with missing invento-
ries of 210Pb (and, thus, representing MAR and SAR when Our results demonstrate that seagrass vegetation enhances car-
sediments were vegetated) were similar for all sites (MAR = bon burial and preserves sediment carbon stocks and that
400 20 g m2 year1, SARmeasured = 0.066 0.003 cm revegetation projects effectively restore seagrass carbon
year1, SARestimated = 0.103 0.008 cm year1). sequestration within short, manageable time-scales.
The sediment Corg stock developed since seagrass planting The sediments at Oyster Harbour were relatively Corg-rich
increased with the age of the restored sites at an average rate when compared with global estimates in seagrass sediments
of 28.2 1.4 g Corg m2 year1 (Fig. 5a). Corg burial rates (Fourqurean et al. 2012). However, the rate of Corg burial in
increased substantially over the first 2 decades after planting, the reference meadow from Oyster Harbour (Fig. 5b) was 1/3
increasing from 16.2 2.4 Corg m2 year1 in sites restored slower than average seagrass burial rates previously reported
© 2015 The Authors. Journal of Ecology © 2015 British Ecological Society, Journal of Ecology, 103, 296–302
300 N. Marba et al.
0.3 0 10 20 30 40 50
(a) 0
0.2 –2 plot
plot
–4
–6
0
–5 0 5 10 15 20 –8
Time since planting (year)
–10
Fig. 3. Variability of sestonic fraction of the organic carbon stored in
the top 3 cm of seagrass sediments across time since planting. Data
from the top 3 cm sediment samples of one sediment core per site are –12
provided. Error bars indicate standard error of the mean (n = 3). The
horizontal line and grey area, respectively, indicate the average and 210
Pb sup
95% confidence limit of sestonic fraction of sediment Corg stock in –14
the continuously vegetated site. (b)
1000
800
Kennedy et al. 2010). The low Corg burial by seagrasses at
Oyster Harbour is most probably due to the slow sediment
600
accretion rate in these meadows, about half of that reported
for seagrass meadows globally (0.20 cm year1, assessed
400
using 14C dating and surface elevation table data; Duarte
ex
et al. 2013b).
210Pb
200
Seagrass revegetation at Oyster Harbour has recovered car-
bon sequestration capacity (per unit of area) within two dec-
ades (Fig. 5b). Our results support the only other study 0
Continuously 1994 2004 Unvegetated
available, that of Greiner et al. (2013) on Zostera marina vegetated revegetated revegetated site
plot plot
meadows in the Virginia coastal bays, USA. In Virginia bays,
Corg burial accelerated 5 years after eelgrass planting, reached Fig. 4. Measured depth profiles of 210Pb concentration (a) and inven-
rates of 36.7 gC m2 year1 after 10 years, and the authors tory of excess 210Pb (210Pbex) (b) in sediments continuously vege-
estimated that burial rates in restored seagrasses would equal tated, revegetated in 1994 and 2004 and unvegetated. Error bars
those of natural meadows 12 years after planting. The time- indicate the standard error. The grey area indicates the concentration
of supported 210Pb (210Pbsup). The data shown are not corrected for
scales of recovery of seagrass carbon sinks by restoration pro-
(35%) sediment compression during coring.
grammes are similar to those reported for mangroves
(~20 years; Osland et al. 2012) and can be longer than for
saltmarshes (1 to >28 years; Craft et al. 2003). inventories, we calculated the time when seagrasses were lost
The increase of carbon burial rate in seagrass restored sites (and planted) by comparing observed and estimated (i.e.
younger than 2 decades partially reflects the effects of sea- assuming continuous deposition) 210Pbex inventories in
grass vegetation on trapping of particles from the water col- restored sites. This exercise revealed that vegetation was lost
umn (Fig. 3; Hendriks et al. 2007) and thus the important around 1984, in very close agreement with the reported exten-
role of seagrass revegetation for allochthonous carbon seques- sive seagrass loss in the 1980s at Oyster Harbour Bay (Bast-
tration (Kennedy et al. 2010). Our results confirm that sea- yan & Cambridge 2008). This analysis of the 210Pbex
grass revegetation through restoration additionally restores the inventories and our results highlight the potential that the
210
capacity of coastal areas to bury allochthonous carbon within Pb dating technique has in ecological studies beyond esti-
18 years, when sestonic inputs already accounted for 27% of mation of sediment accretion rates.
sediment Corg (Fig. 1). Our results of sediment dating and carbon density reveal
The flux of annual 210Pbex measured in the continuously that the sediment Corg stock preserved since ~1890 in Oyster
vegetated meadow is in agreement with reported atmospheric Harbour restored sites was 2770 117 g Corg m2. The Corg
fluxes of 210Pb in Western Australia (Preiss, Melieres & Pour- stock in revegetated sites represented about 80% of that in the
chet 1996). This supports the hypothesis that sediments in the continuously vegetated meadow, but it was 3.6-fold higher
continuously vegetated site efficiently accumulate 210Pbex. As than that in unvegetated sediments (Fig. 6). The reconstructed
a further verification of our interpretation of the 210Pbex trajectory of sediment Corg stock accumulated in restored sites
© 2015 The Authors. Journal of Ecology © 2015 British Ecological Society, Journal of Ecology, 103, 296–302
Seagrass loss, revegetation and carbon sequestration 301
500
Corg stock since planting
300
200 Revegetated
2000
Onset
Seagrass loss
100 restoration
0
0 5 10 15 20
1000
(b) 35
Unvegetated
30
25 0
Corg burial rate
20 Time (year)
sediments and plants in Princess Royal Harbour and Oyster Harbour. Tech.
Acknowledgements Series no. 40, Environmental Protection Authority of Western Australia,
Perth, Western Australia. 55 p.
This work has been funded by the projects CSIRO Marine and Coastal Carbon Kauffman, J.B., Heider, C., Norfolk, J. & Payton, F. (2014) Carbon stocks of
Biogeochemistry Cluster, Opera (EU FP7, Project No. 308393), MEDEICG intact mangroves and carbon emissions arising from their conversion in the
(CTM2009-07013) and EstresX (CTM2012-32603). We are grateful to A Gera Dominican Republic. Ecological Applications, 24, 518–527.
and D Provencßal for fieldwork assistance and A Zavala, P Carrillo and C Kennedy, H., Beggins, J., Duarte, C.M., Fourqurean, J.W., Holmer, M., Marba,
Alonso for analytical support. We thank R Hovey for providing d13C values of N. & Middelburg, J.J. (2010) Seagrass sediments as a global carbon sink:
Posidonia australis from Oyster Harbour and O Serrano for discussions during isotopic constraints. Global Biogeochemical Cycles, 24, GB4026.
the study. NM was supported by a mobility grant of CSIC (PA1003258) and a Lovelock, C.E., Ruess, R.W. & Feller, I.C. (2011) CO2 efflux from cleared
Gledden Visiting Fellowship of the Institute of Advanced Studies (UWA), IM mangrove peat. PLoS ONE, 6, e21279.
by a PhD fellowship by the Government of the Balearic Islands, PM by ICREA Marba, N., Arias-Ortiz, A., Masque, P., Kendrick, G.A., Mazarrasa, I., Bastyan,
Academia and a Gledden Visiting Fellowship of the Institute of Advanced G.R., Garcıa-Orellana, J. & Duarte, C.M. (2014) Carbon stocks and sources
Studies (UWA), PM and JGO by Generalitat de Catalunya to MERS (2014 in Oyster Harbor (W Australia) seagrass sediments [Dataset], http://digi-
SGR–1356), AAO by a PhD grant of Obra Social ‘la Caixa’ and GAK by two tal.csic.es/handle/10261/108758
concurrent Australian ARC Linkage projects (LP100200429, LP1301000155). McLeod, E., Chmura, G.L., Bouillon, S., Salm, R., Bj€ork, M., Duarte, C.M.,
Lovelock, C.E., Schlesinger, W.H. & Silliman, B.E. (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 Environ-
Data accessibility
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Nellemann, C., Corcoran, E., Duarte, C.M., Valdes, L., De Young, C., Fonseca,
The data set on sediment organic carbon concentration, density and sources is
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available at the public data repository digital CSIC (Marba et al. 2014). Data
United Nations Environment Programme, GRID-Arenal.
used to fit the empirical relationship between % LOI and % Corg are shown in
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Fig. S2.
Heitmuller, P.T. et al. (2012) Ecosystem development after mangrove wet-
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© 2015 The Authors. Journal of Ecology © 2015 British Ecological Society, Journal of Ecology, 103, 296–302