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Variability in the Carbon Storage of Seagrass Habitats

and Its Implications for Global Estimates of Blue Carbon
Ecosystem Service
Paul S. Lavery1*, Miguel-Ángel Mateo2, Oscar Serrano1,3, Mohammad Rozaimi1,4
1 School of Natural Sciences and Centre for Marine Ecosystems Research, Edith Cowan University, Joondalup, WA, Australia, 2 Centro de Estudios Avanzados de Blanes,
Consejo Superior de Investigaciones Cientificas, Blanes, Girona, Spain, 3 The UWA Oceans Institute, The University of Western Australia, Crawley, WA, Australia, 4 School of
Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia, Bangi, Selangor, Malaysia

Abstract
The recent focus on carbon trading has intensified interest in ‘Blue Carbon’–carbon sequestered by coastal vegetated
ecosystems, particularly seagrasses. Most information on seagrass carbon storage is derived from studies of a single species,
Posidonia oceanica, from the Mediterranean Sea. We surveyed 17 Australian seagrass habitats to assess the variability in their
sedimentary organic carbon (Corg) stocks. The habitats encompassed 10 species, in mono-specific or mixed meadows,
depositional to exposed habitats and temperate to tropical habitats. There was an 18-fold difference in the Corg stock (1.09–
20.14 mg Corg cm23 for a temperate Posidonia sinuosa and a temperate, estuarine P. australis meadow, respectively).
Integrated over the top 25 cm of sediment, this equated to an areal stock of 262–4833 g Corg m22. For some species, there
was an effect of water depth on the Corg stocks, with greater stocks in deeper sites; no differences were found among sub-
tidal and inter-tidal habitats. The estimated carbon storage in Australian seagrass ecosystems, taking into account inter-
habitat variability, was 155 Mt. At a 2014–15 fixed carbon price of A$25.40 t21 and an estimated market price of $35 t21 in
2020, the Corg stock in the top 25 cm of seagrass habitats has a potential value of $AUD 3.9–5.4 bill. The estimates of annual
Corg accumulation by Australian seagrasses ranged from 0.093 to 6.15 Mt, with a most probable estimate of 0.93 Mt y21
(10.1 t. km22 y21). These estimates, while large, were one-third of those that would be calculated if inter-habitat variability
in carbon stocks were not taken into account. We conclude that there is an urgent need for more information on the
variability in seagrass carbon stock and accumulation rates, and the factors driving this variability, in order to improve global
estimates of seagrass Blue Carbon storage.

Citation: Lavery PS, Mateo M-Á, Serrano O, Rozaimi M (2013) Variability in the Carbon Storage of Seagrass Habitats and Its Implications for Global Estimates of
Blue Carbon Ecosystem Service. PLoS ONE 8(9): e73748. doi:10.1371/journal.pone.0073748
Editor: John F. Valentine, Dauphin Island Sea Lab, United States of America
Received May 9, 2013; Accepted July 24, 2013; Published September 5, 2013
Copyright: ß 2013 Lavery et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was funded by a Visiting Research Fellows grant from the Faculty of Health, Engineering & Science at Edith Cowan University, project
number 25139.9256.RG.06.01 (http://www.ecu.edu.au/faculties/computing-health-and-science). Part of this study was funded by the Spanish Ministry for Science
and Innovation (MICINN) with the grant CTM2006-12492/MAR. The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected]

Introduction content of sediments from Mediterranean Posidonia oceanica

meadows (e.g. [2,4]. However, P. oceanica is unusual in its ability
There is considerable interest in quantifying the capacity of the to capture C. Its vertical growth dynamics and recalcitrant tissues
World’s ecosystems to trap and sequester carbon (C). The recent produce a deep mat of plant debris that can extend many meters
focus on C trading and C pricing has intensified this interest, since down into the sediment and persist for millennia, resulting in
net C storage provides one means of valuing these ecosystems. In massive C storage, up to 40–410 kg Corg m22 [5–7]. As far as is
the early 1980s, [1] highlighted the importance of vegetated known, no other seagrass has this attribute and, in a functional
coastal habitats as carbon sinks, though since then most work on form model of seagrasses, Walker et al. [8] placed P. oceanica as an
the ability of ecosystems to capture C has focused on terrestrial outlier. Nelleman et al. [2] recognized that their assumptions were
ecosystems. However, the publication of the ‘Blue Carbon’ report likely to have produced an upper estimate of the Blue Carbon sink,
[2] has highlighted the potential of coastal marine ecosystems to in part because of uncertainties in the C burial rates of different
sequester carbon. For example, they estimate that coastal marine seagrass ecosystems.
systems capture up to half of the CO2 emissions from the World’s The other 70-plus species of seagrasses [9] have a wide variation
transport sector. These ecosystems include mangroves, coral reefs, in traits relevant to C capture and storage. This includes
saltmarshes and seagrasses, with seagrasses having a dispropor- differences in their rates of primary production, their below
tionately large C storage potential relative to their global area [3]. ground biomass, the recalcitrance of the Corg in their organs, the
From necessity, there has been a tendency to generalise the ability of their canopies to trap allochthonous carbon and the
Corg-capture attributes of seagrasses from a very limited data set, conditions in their sediments that drive Corg preservation (see
with almost all of the estimates being based largely on the Corg review of factors in [10]). For most of the World’s seagrass species,

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 Carbon Stocks in Seagrass Ecosystems

and for most of their global distribution, there is little knowledge of incorporated tropical, sub-tropical and temperate climates as well
their carbon stocks or regional cover [11], though for a wide range as inter-tidal and sub-tidal habitats. The sampling design was not
of seagrass species an absolute C flux to the refractory orthogonal as not all species occurred in all habitat types; thus,
compartment was estimated ranging from 1.8 to 177.8 g C some species were sampled in only one location, while others were
m22 y21 (median: 56.2 g C m22 y21), representing from around sampled in both inter- and sub-tidal habitats or in sub-tidal
5% to 65% of total plant production (median:18% [10]). Also, a habitats of different depths.
review of 219 seagrass sediment data sets, encompassing 20 At all sites except the Posidonia australis meadow at Waychinicup
species, showed significant variation in organic matter content, Inlet, PVC cores (i.d. 47 mm) were manually inserted into the
with Corg ranging from 0.1 wt % to 11.0 wt % [12]. Recently, a sediments to a depth of 30 cm at three randomly located positions.
first attempt to compile global Corg data [13] examined 946 The cores had serrated bottom edges to assist in cutting through
distinct seagrass meadows across the globe. They estimated an seagrass rhizomes and were gently turned while being pushed or
average Corg in the top meter of seagrass soils at 2.5 wt % (median hammered into the sediments. The cores were retrieved, capped
1.8 wt %). Using the rough latest estimates of total area of the and returned to the boat where they were stacked vertically in a
Earth covered by seagrass meadows (between 300,000 and cool box until returning to the laboratory. At Waychinicup Inlet,
600,000 km2), they come to a conservative estimate of a global PVC cores were inserted by manual hammering to the maximum
stock from 4.2 to 8.4 Pg Corg for the top meter. A preliminary possible depth (. 2.5 m). Sample compaction during coring was
regional breakdown of the areal stock is also provided showing the less than 25% in all cases.
highest areal stocks in the Mediterranean (372.4 Mg Corg ha21 6 In the laboratory, the sediments were extruded by inserting a
74.5, n = 29; [13]) but no details on habitat or species stock plunger at the bottom of the cores and carefully drawing the PVC
distribution can be given because of data set limitations. liner down over the plunger. The cores were sliced into 3 cm
In addition to the variability among seagrass species, the range sections, at 0–3, 6–9, 12–15, 18–21 and 24–27 cm intervals. The
of habitats in which they occur is also likely to affect their C slices were split into two sub-samples, with one sub-sampled
storage potential. Seagrasses occur across a range of depositional retained for organic carbon analysis and the other for organic
environments, from estuaries to exposed coastal environments matter (Loss on Ignition, or LOI) and carbonate analyses. Cores
[14]. They occur at a range of water depths which influences their from Waychinicup Inlet were sliced every cm for the first 30 cm.
net C balances [15,16] and the organic C preservation due to Analyses were performed on 1 cm sections corresponding to the
differences in sediment grain-size [17]. They also occur across depth ranges analysed for the other cores (e.g. usually the 2 cm
latitudinal ranges and habitats with significant temperature section to correspond with the 0–3 cm section of the other cores).
variation that can affect sediment respiration and remineralisation
rates [18]. Consequently, there are likely to be species-habitat
interactions that will strongly influence the capture and retention Organic Content and Carbonate Content
of sedimentary Corg. Each sub-sample was weighed before and after drying at 50uC
This paper presents the results of an initial survey of several for 48 h to determine bulk density and porosity. The samples were
species of Australian seagrasses to assess the variability in their then ground in a ball mill and combusted at 450uC for 4 h to
sedimentary C stocks. While not fully comprehensive in the determine LOI [19] and then for 2 h at 950uC to determine the
diversity of species examined it does, nonetheless, include about carbonate content [20]. All combustions included reference
one-third of the Australian seagrass species, with estimates of Corg samples of pure glucose and calcium carbonate to correct for
accumulation rates, and provides an initial contribution to incomplete combustion of Corg and carbonates.
broadening our understanding of the variability in the sedimentary
Corg stocks of seagrass habitats. We also set out to test whether the Organic Carbon Content
variability in sedimentary Corg stocks among seagrasses was The sub-sample for organic carbon analysis was dried, weighed
sufficient to warrant its inclusion in regional and global estimates and then dry-sieved through a 1 mm mesh to remove coarse
of seagrass Corg storage, or whether a single global seagrass inorganic particles. The remaining samples were then acidified
average (such as that currently based largely on P. oceanica) with 4% HCl to remove inorganic carbon, washed in deionised
produces similar estimates. While our study focuses on Australian water then centrifuged (3400 revolutions per minute, for 5
seagrasses, Australia is in a unique position of having some of the minutes) and the supernatant with acid residues carefully removed
World’s largest and most diverse seagrass resources over a wide by pipette, avoiding resuspension. The residual samples were re-
range of climates and habitat types, and encompasses much of the dried and then capsulated for %C and d13C analyses using an
kind of variability found in seagrass ecosystems globally. ANCA-NT 20–20 Stable Isotope Analyser connected to an
ANCA-NT Solid/Liquid Preparation Module (PDZ Europa
Methods and Materials instruments). d13C values were reported relative to v-PDB
standard. Percentage C was calculated for the bulk (pre-sieved
Ethics Statement and pre-acidified) samples.
This research was approved by the Edith Cowan University
Ethics Committee following submission of an ethics declaration. Estimating Australian Seagrass Corg Stocks and
The collection of seagrass and sediment core samples undertaken
Accumulation Rates and the Effect of Including Inter-
for this research were approved through the issuing of collection
permits by the Department of Conservation and Environment in habitat Variability on Estimates
Western Australia and the Department of Primary Industries in To examine the effect of incorporating the natural variability in
Queensland. sedimentary organic carbon storage of seagrasses into regional
estimates of seagrass Corg stocks and accumulation rate, we
estimated the total sedimentary Corg stock (Cstock) of the top 25 cm
Sedimentary Carbon Characteristics
of seagrass habitat in Australia as:
Sediment cores were extracted from 17 mono-specific or mixed-
species meadows of seagrass (Table 1). The meadows sampled

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 Carbon Stocks in Seagrass Ecosystems

Table 1. Location of seagrass meadow sampling sites.

Species Zone Location Habitat S E

Amphibolis antarctica subtropical Shark Bay, WA Sub-tidal 7144460 772637

Inter-tidal 7144289 772989
temperate Geographe Bay, WA Sub-tidal5m 6280864 353582
Sub-tidal 10m 6282348 342501
C. rotundata /H.uninervis tropical Green Is., QLD Sub-tidal 8147054 390456
C. rotundata/S. isoetifolium tropical Green Is., QLD Sub-tidal 8147003 390468
Cymodocea serrulata tropical Trinity Inlet, QLD Sub-tidal 8132670 369620
Halodule uninervis tropical Trinity Inlet, QLD Sub-tidal 8131418 373498
Inter-tidal 8131418 373510
Halophila ovalis tropical Trinity Inlet, QLD Sub-tidal 8131053 371447
Posidonia australis subtropical Shark Bay, WA Sub-tidal 7144460 772637
Inter-tidal 7144289 772989
temperate Waychinicup Inlet Sub-tidal 6137832 621812
Posidonia sinuosa temperate Geographe Bay, WA Sub-tidal5m 6275712 336571
Sub-tidal 10m 6277434 336006
T. hemprichii/C. rotundata tropical Green Is., QLD Sub-tidal 8146599 390891
Zostera muelleri tropical Trinity Inlet, QLD Sub-tidal 8131308 373498

Location of seagrass meadow sampling sites. The locations are given in UTM using WSG84 map datum and are central points of the study sites. C.
rotundata = Cymodocea rotundata; T. hemprichii = Thalassia hemprichii.
doi:10.1371/journal.pone.0073748.t001

layers, which better represents the medium-to long-term accumu-

X lation of C than considering only the top layer.
Cstock ~ Si |Ai |D
i The rate of C accumulation is highly dependent on the rate of
sediment accumulation. In the absence of dating for each of the
where, i refers to the 6 regions of Australia for which seagrass areas
cores, we assumed a range of sedimentation rates based on
have been reported (Table 2), Si is the mean Corg stock of the
published literature and unpublished dating results that we have
seagrasses representative of each region and measured in this study
recently obtained for other seagrass areas throughout Australia
expressed in mg m23, Ai is the estimated area of seagrass in each
(Table 3). The published rates show a large range of sediment
region expressed in m2) (Table 2), and D is the depth of sediment
accumulation rates from as low as 0.15 mm y21 to 9.9 mm y21 in
layer in m (in this case, 0.25 m). The stock was integrated over
seagrass habitats and over 17 mm y21 in tropical lagoon habitats.
25 cm as our deepest section of sediment sampled bracketed the
Therefore, we applied a range of accumulation rates. We ignored
24–27 cm range, and 25 cm is convenient for normalization to the
the highest reported rate as this applied to tropical lagoon
top 1 m of sediment, which has been examined in other studies
environments with no evidence that these supported seagrasses.
(e.g. Fourqurean et al. 2012). The seagrass species considered
Within the remaining range (0.15 to 9.9 mm y21) are data derived
representative of each region was based by matching [22]
from seagrass core dating studies. The maximum sediment
assessment of the dominant species in each region (Table 2) with
accumulation rate of 9.9 mm y21 [23] was based on Pb-210
the most morphologically similar species for which we had
dating at one site and relates to the past 60 years. For a nearby
measured Corg stocks (Table 1). Where more than one species
meadow they estimated an accumulation rate of 4.7 mm y21 for
was likely to contribute significantly to the total area of seagrass,
the past 60 years and for the Holocene an average of 0.44 mm y21
we weighted the contribution to the C stock equally among all the
(based on 14C dating). This range illustrate the wide range of
species.
accumulation rates when considering short- vs long-term periods,
For accumulation rates, a similar approach was taken to
reflecting a combination of factors such as human impacts on
produce a range of possible accumulation rates and to assess the
sedimentation dynamics as well as diagentic process (i.e. organic
effect of incorporating inter-habitat and inter-species variability in
matter decomposition and sediment compaction with ageing). We
the estimates. The organic carbon accumulation rate Caccum (t
have a number of dated Posidonia australis sediment core profiles
Corg y21) was determined as:
from Oyster Harbour, Western Australia that indicate sediment
X accumulation rates in the order of 1.45–2.43 mm y21 over the
Caccum ~ i
Si Ai R past 70–80 years (unpublished data). Together, these data
indicated that sediment accumulation rates in seagrass meadows
where, i refers to the 6 regions for which seagrass areas have been are likely to be in the range of 0.15–9.9 mm y21 but C and lead
reported (Table 2), Si is the mean organic carbon stock (mg m23) dating suggesting accumulation rates for Posidonia species in the
in the top 25 cm of the seagrasses representative of each region order of 1–1.5 mm y21 in recent times. To capture this
and that were measured in this study, Ai is the estimated area (m2) uncertainty, we used three representative sediment accumulation
of seagrass in each region (Table 2) and R is the rate of sediment rates in seagrass meadows (0.15, 1.5 and 9.9 mm y21) to calculate
accumulation (m y21). The stocks were the mean of all depth Corg accumulation rates:.

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 Carbon Stocks in Seagrass Ecosystems

Table 2. Estimates of seagrass area in various region of Table 3. Published sediment accumulation rates (by depth)
Australia. for Australian coastal marine ecosystems and P. oceanica from
the Mediterranean Sea.

Area Pre-dominant
State (km2) Habitat species Source Sedimentation
1 Site Habitat rate (mm y21) Reference
New South 15 Estuarine P, Z, H
Wales Morton Bay Inter-tidal 1.3–2.7 [56]
2
154 Estuarine Ningaloo Reef Fringing 1.46–9.88 [57]
161 Estuarine 3 reef

Tasmania 60 Embayments P, Aa, Z, H 1 SE Australia Depositional 14.2–17.3 [58]

111 NW coast 4 Fitzroy R., QLD Estuary 15 [59]

845 Varied 5 Herbert R., QLD Depositional 1.11–11.4 [60]

1
bay
Victoria 10 Embayments P, A, Z, H
5
GBR Nara Inlet Inlet 1 [61]
470 Estuarine
1
Sydney Nearshore 2–4 [62]
South .5230 Varied P, A, Z shelf
Australia
6
Port Phillip Bay Embayment 1.5 [63]
9620 Varied
1,7, 5, 8
Far North QLD Inner shelf 0.4–1 [64]
QLD/NT/TS 2320 Embayments H, Hd, C + small
areas of Herbert R., QLD, Tidal 0.3–8.5 [65]
mud flats
6000 Embayments Th, E and Tc
Spencer Gulf Seagrass 0.15–0.25 [66]
56473 Varied
1
Sydney, Botany Bay Seagrass 4.7–9.9 [23]
Western 2200 Varied P, A in the SW;
Australia $26 species Mediterranean Sea Seagrass 0.61–4.1 [5]

25000 Varied in NW, incl. Mediterranean Sea Seagrass 1 [42]

H, Hd & C Albany, WA Seagrass 1.45–2.43 Unpublished
Total 92569 data
Total Range 0.15–17.3
Estimates of seagrass area in various region of Australia. Bold indicate the
estimates which were used in the calculations of national seagrass Corg stocks Seagrass range 0.15–9.9
and accumulation rates.
P = Posidonia spp.; NB: Mass Accumulation Rates (MAR) were not used unless sediment bulk
Z = Zostera spp.; density data were available to convert the MAR to depth accumulation rates.
H = Halophila spp.; doi:10.1371/journal.pone.0073748.t003
A = Amphibolis spp;
Aa = Amphibolis antarctica;
Hd = Halodule spp.; sub-habitats mixed meadows of tropical species had the lowest
C = Cymodocea spp.;
stocks, generally less than 2.7 mg Corg cm23.
Th = Thalassia hemprichii;
E = Enhalus acroides; Several species of seagrass were sampled in more than one sub-
Tc = Thalassodendron ciliatum. habitat and generally showed significant variability in Corg stocks
Sources: among sub-habitats. Thus, while a temperate P. australis meadow
1
[22]; 2[48]; 3[49]; 4[50]; 5[51]; 6[52]; 7[53]; 8[54]cited [55].
doi:10.1371/journal.pone.0073748.t002
had the highest absolute stock recorded in any single sub-habitat
(20.156 10.95 mg Corg cm23 ), a sub-tropical meadow in Shark
Bay had a relatively low stock of 4.92 6 0.89 mg Corg cm23.
Results Similarly, among P. sinuosa the Corg stock ranged from 1.09 6
Seagrass Sediment Characteristics 0.32 mg Corg cm23, in a shallow temperate meadow, the absolute
The mean organic matter content of the sediments in the lowest value recorded in any of the sampled sub-habitats, to 3.16
Australian seagrass habitats sampled ranged from 0.67 to 9.09% 6 2.17 mg Corg cm23 in a deeper temperate meadow.
DW, with a mean of 3.74 6 3.13% (Mean 6 SD; Table 4). The Integrated over the depth profile of 24 cm that was sampled, the
bulk % Corg ranged from 0.1 to 2.14% DW, with a mean of 0.64 Corg content of the upper meadows ranged from 262 6 75.8 g
6 0.68%. The range across all 17 sub-habitats was 1.09 6 Corg m22 for the temperate Posidonia sinuosa meadow to 4833 6
0.32 mg Corg cm23, in a shallow temperate Posidonia sinuosa habitat 2040 g Corg m22 for temperate, estuarine P. australis
to 20.15 6 10.95 mg Corg cm23 in a temperate, estuarine P. meadow.(Table 4).
australis habitat (Table 4). When averaging over all the sub-habitats While there were significant differences in the total Corg stock of
in which a species was sampled, the mean Corg stocks in the top the different meadows, these did not consistently fall into a
25 cm of the different seagrass habitats differed significantly (Fig. 1; temperate-tropical divide; while the smallest stocks were found in a
ANOVA d.f = 9, 269; F = 17.87; p ,0.001). P australis had the tropical species, tropical H. ovalis had the second largest stock.
highest mean Corg stock (11.42 6 9.55 mg Corg cm23; Fig. 1). The Post-hoc pairwise comparisons (Fig. 1) indicated that highest stocks
mean Corg stocks for Halophila ovalis, and Zostera muelleri habitats were found in the temperate Posidonia australis and the tropical H.
were not significantly different to those of P. australis, while a mixed ovalis, Zostera muelleri and Cymodocea serrulata meadows, while the
meadow of T. hemprichii/C. rotundata had the lowest stock (2.38 6 lowest stocks were found in a mixture of tropical, sub-tropical and
0.85 mg Corg cm23, though this was not significantly lower than a temperate meadows (Amphibolis antarctica, P. sinuosa and mixed
variety of sub-tropical and temperate habitats. Averaged over all meadows of C. rotundata with other species).

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 Carbon Stocks in Seagrass Ecosystems

Table 4. Sediment characteristics of Australian seagrass habitats and Posidonia oceanica.

Species Climate Habitat N % OM s.d. % C (bulk) s.d. mg C cm23 s.d. g C m22 s.d.

Posidonia australis all 47 6.43 3.88 1.31 1.06 11.42 9.55 2741.10 2292.35
temperate subtidal 18 5.88 2.82 2.14 1.19 20.14 10.94 4832.88 2040.08
subtropical all 29 6.78 4.43 0.79 0.50 6.01 1.98 1442.75 474.36
intertidal 14 4.31 1.81 0.55 0.19 4.92 0.89 1179.76 214.20
subtidal 15 9.09 4.94 1.01 0.60 7.03 2.18 1688.21 523.18
Halophila ovalis tropical subtidal 15 6.21 3.45 1.18 0.38 8.64 2.86 2072.77 685.41
Zostera muelleri tropical subtidal 15 4.48 1.30 1.33 0.83 8.06 3.38 1933.85 810.48
Cymodocea serrulata tropical subtidal 15 3.02 0.88 0.68 0.19 6.32 1.74 1516.70 417.02
Halodule uninervis tropical all 27 5.87 2.51 0.69 0.36 5.19 2.55 1244.96 610.93
intertidal 13 4.66 2.05 0.62 0.48 5.50 3.36 1319.62 805.92
subtidal 14 7.00 2.42 0.75 0.21 4.90 1.54 1175.63 369.02
Amphibolis antarctica all 59 2.43 2.41 0.36 0.32 3.33 2.26 799.34 543.57
subtropical intertidal 15 2.47 1.15 0.25 0.10 2.80 1.20 672.28 288.77
subtidal 15 4.16 3.56 0.54 0.28 4.84 1.60 1162.70 384.96
all 30 3.32 2.74 0.39 0.26 3.82 1.74 917.49 417.14
temperate subtidal 5m 15 0.79 0.73 0.13 0.05 1.54 0.45 369.01 108.49
subtidal 10m 14 2.29 1.90 0.55 0.45 4.20 3.29 1007.23 790.54
all 29 1.51 1.59 0.33 0.38 2.82 2.64 677.12 633.55
C. rotundata/ S. isoetifolium tropical subtidal 15 3.08 0.39 0.32 0.11 2.67 0.85 640.15 204.87
Posidonia sinuosa temperate all 43 1.72 1.70 0.28 0.31 2.44 2.01 585.35 482.62
subtidal 5m 15 0.67 0.24 0.10 0.04 1.09 0.32 261.93 75.81
subtidal 10m 28 2.26 1.87 0.39 0.35 3.16 2.17 758.61 519.71
C. rotundata/H. uninervis tropical all 28 2.55 2.89 0.28 0.10 2.43 0.85 582.33 203.38
intertidal 13 3.74 3.80 0.28 0.10 2.28 0.73 546.42 174.33
subtidal 15 1.51 1.12 0.28 0.10 2.56 0.95 613.45 226.91
T. hemprichii/C. rotundata tropical intertidal 15 2.94 2.36 0.30 0.10 2.38 0.85 571.82 204.72
All Species (Australia) 280 3.74 3.13 0.64 0.68 5.26 5.46 1262.05 1483.37
Posidonia oceanica 7 42.99 12.09 17.85 6.08 20.16 9.49 4837.42 2276.62
P. oceanica/Australian Spp 116 286 46 46

Data are means for the top 25 cm of sediment. s.d. = standard deviation. %C is for the bulk sample. Bold indicates mean of all habitats for a species; italics relates to
individual habitats for a given species.
doi:10.1371/journal.pone.0073748.t004

The profiles of Corg stocks through the top 25 cm of the Estimates of Australian Seagrass Sedimentary Carbon
sediment cores also showed no consistent difference among Stocks & Accumulation Rates
climatic zones (Fig. 2). Temperate and sub-tropical meadows The estimated Corg stock of the top 25 cm of sediment in
showed a general pattern of declining Corg stocks with depth. Australian seagrass habitats that took into account inter-habitat
While some tropical meadows showed the opposite trend variability was in the order of 155 Mt (Table 6). The majority of
(increasing Corg stocks with depth in Halophila ovalis and meadows this stock (54%) was in the temperate seagrass habitats, dominated
of Cymodocea rotundata mixed with Thalassia hemprichii, Syringodium by the larger, meadow-forming species of Posidonia and Amphibolis.
isoetifolium or Halodule uninervis), others showed the same trend as The remaining 46% was in tropical seagrass habitats of northern
the temperate meadows, of declining stocks with depth. Australia, which are dominated by a variety of smaller-sized
Of those species that were sampled in more than one habitat, seagrasses that typically have a lower sedimentary Corg stock than
some showed significant among-habitat differences in Corg stocks the larger temperate species but a larger reported areal coverage.
while others did not. For both Posidonia sinuosa and Amphibolis The estimates of annual Corg accumulation for Australia ranged
antarctica there was a significant effect of water depth on the Corg from 0.093 Mt when applying a sedimentation rate of 0.15 mm
stocks (Table 5), with greater stocks in the 10 m deep sites than the y21 to 6.157 Mt at 9.9 mm y21 (Table 7). At a sedimentation rate
5 m deep sites (Fig. 3a). In both cases, the stock was also much of 1.5 mm y21, which, on limited dating evidence, we believe is
more variable in the deeper sites. In contrast, for species sampled more representative of accumulation rates in seagrass ecosystems,
in both inter- and sub-tidal habitats, there was no habitat effect on the annual organic carbon accumulation rate was 0.932 Mt.
the Corg stocks (Table 5), though there were differences in stocks
among species (Fig. 3b).

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 Carbon Stocks in Seagrass Ecosystems

Figure 1. Organic carbon stocks (Mean ±SD) in the top 25 cm of sediment cores from different Australian seagrass meadows.
Shared letters above the bars indicate no significant difference (p.0.05) among habitats.
doi:10.1371/journal.pone.0073748.g001

Discussion larger, more persistent rhizomes, often characterised by more

refractory forms of structural carbon, more likely to be preserved
Variability in C Stocks in marine sediments than simpler, more labile forms of carbon
This spatially-limited study has demonstrated a significant [18]. The deeper canopy of larger seagrasses may also reduce
variability in the Corg stock in sediments beneath different seagrass near-bottom mean water velocities [24] enhancing particle
habitats. Among the finding is a strong indication that a variety of trapping [25,26] and reducing the resuspension of particles within
biotic (species) and abiotic (habitat physic-chemical conditions) the canopy [27], leading to higher inputs of allocthonous
exert a strong influence on the carbons tocks of seagrass meadows, sedimentary organic matter inside macrophyte beds compared to
producing significant inter-habitat variability. unvegetated areas [25].
Posidonia australis had the highest Corg stocks, both averaged over Despite P. australis having the largest stock of organic carbon,
all the sub-habitats in which it was sampled and in any individual there was considerable variability among habitats for this species.
sub-habitat sampled. This is consistent with a general expectation Among the three sub-habitats sampled, there was a 4-fold range in
that larger seagrasses are likely to have larger carbon stocks due the stocks, with the inter-tidal sub-tropical habitat having least and
factors that affect the production, form and preservation of organic the sub-tidal, temperate habitat the most. This indicates a strong
carbon. Larger seagrasses, such as P. australis, tend to have deeper, effect of abiotic variables on the carbon storage capacity of this

Figure 2. Profiles of organic carbon stocks in the top 25 cm of cores from different Australian seagrass meadows. All data are means
6 std error.
doi:10.1371/journal.pone.0073748.g002

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 Carbon Stocks in Seagrass Ecosystems

Figure 3. Carbon stocks in sediments of seagrass meadows occurring at different water depths: A) comparison of sub-tidal habitats
(5 m vs 10 m depth); and B) comparison of inter-tidal and sub-tidal habitats.
doi:10.1371/journal.pone.0073748.g003

species. The temperate meadow was located in Waychinicup inlet, Surprisingly, Halophila ovalis, which has small leaves and a very
a small, relatively sheltered coastal estuary. The combination of short canopy and root system relative to the other species, had the
sheltered conditions and the inputs of allocthonous carbon from its second-highest mean Corg stock, which was not significantly
small catchment [28] may contribute to the higher carbon stock at different to that of Posidonia australis and was greater than many
this site. In contrast, the sub-tropical meadow was located in very larger species. The relatively high C stocks in H. ovalis meadows
shallow water (,0.1 m at spring low tide), which would enhance may be explained by their morphology and their habitat
hydrodynamic exposure and associated resuspension and export of characteristics. Despite having smaller leaves than other seagrass
sedimentary carbon matter. It is also likely that the generally species, Halophila decipiens increased the threshold velocity for
warmer conditions of Shark bay where the meadow was located, sediment motion similar to larger seagrasses [31]. The allocation
and the shallowness of the site would result in higher mean of leaf biomass and rhizomes closer to the sediment-water interface
temperatures that would facilitate enhanced remineralisation of when compared to other seagrasses was hypothesized as the main
sedimentary carbon [29]. Elsewhere, shallow P. oceanica meadows physical basis for the significant sediment stabilization effects
were observed to have higher rates of carbon remineralisation proved by H. decipiens. It has also been observed that at some water
than deeper meadows [30], attributed to higher respiratory rates at velocities denser seagrass canopies can induce ‘skimming flow’
the shallow sites. The effect of depth on carbon stocks is discussed which directs particles over the canopy and reduces the capture
further below. efficiency [32], which may explain some of the differences between
H. ovalis and the larger meadows. Further, a global study of

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 Carbon Stocks in Seagrass Ecosystems

Table 5. Results of statistical testing (2-way ANOVA) for from algal production but, more likely (given the location of the H.
significant effects of Species and Habitat (Deep v Shallow (A) ovalis meadows sampled for this study), from terrestrial inputs.
or Tidal v Inter-tidal (B)) on the Corg storage in the top 25 cm Further studies into the sources of C would help to clarify the
of seagrass sediments. relative importance of seagrasses in contributing to C stocks.
The data indicate that both the species of seagrass and the
abiotic habitat characteristics are important in driving variability
A) Deep v Shallow sub-tidal meadows of P. sinuosa and A. antarctica of sedimentary Corg stocks. While the habitats we studied were
characterised by one or two dominant seagrasses, we cannot
Effect SS d.f. MS F p
conclude that these same species were dominant at the study sites
Species 9.13 1 9.13 2.28 0.135 over the duration of carbon accumulation to a depth of 25 cm.
Depth 92.98 1 92.98 23.25 ,0.001 However, given typical sediment accumulation rates in seagrass
Spp x D 1.45 1 1.45 0.36 0.549 habitats of between 1 and 10 mm y21 (Table 3), the 25 cm deep
cores may represent a period in the order of 25–250 years. For
Error 271.91 68 3.99
some of the smaller, disturbance-adapted species, it is likely that
Pairwise (Tukeys HSD) comparisons on significant effect: depth
the seagrass composition at the sites may have changed during that
A. antarctica Deep v shallow p = 0.003 time, while the larger, perennial species might be expected to have
P. sinuosa Deep v shallow p = 0.010 dominated the sites for most, if not all, of that time, and at least
B) Inter-tidal v Sub-tidal meadows of four different seagrass species some of the variability in Corg stocks is related to the species of
Species 252.5 1 2159.5 526.6 ,0.001 seagrass.
Water depth had a significant effect on Corg stocks. For Posidonia
Tidal regime 12.1 1 12.1 2.9 0.088
sinuosa and Amphibolis griffithiii, in Geographe Bay there were larger
Spp x Tide 27.1 3 9.0 2.2 0.090
Corg stocks in the deeper sites than the shallow sites. The higher
Error 271.91 68 3.99 net productivity of meadows at shallow sites compared to deep
doi:10.1371/journal.pone.0073748.t005
sites [15,34] would suggest greater carbon inputs and sedimentary
organic carbon at shallow sites. However, shallower meadows may
also be exposed to greater hydrodynamic forces and export of C
seagrass sediments found that, on average, 50% of the sedimentary
(as wrack) may be greater than at deeper sites which, in addition,
Corg matter in seagrass meadows was derived from allocthonous
can be receiving environments for organic matter from shallower
sources [12]. In the case of Halophila, it is possible that despite its
sites [30]. This hydrodynamic exposure may also result in greater
low biomass the canopy is capable of trapping a variety of C
exposure to oxygenated conditions for the shallower sediments
sources resulting in the relatively high carbon stocks. However, it
[35], promoting higher respiration rates and detrital decay than in
seems more probable that this species is adapted to living in
deeper sites, as observed in P. oceanica meadows [30]. Furthermore,
naturally depositional environments and the seagrass itself is a
higher sediment deposition rates at deeper sites (due to lower
relatively minor contributor to the stocks. This hypothesis is
hydrodynamic forces) may contribute to greater vertical growth
supported by the stable C isotopic composition of the sediments
rates of seagrasses and, therefore, Corg accumulation rates and
studied for H. ovalis. While the average d13C value of the tissues of
stock. Based on our results, even very similar meadows may have
this species has been determined to be below 214 % (e.g. [12,33]),
significantly different C storage capacities due to a combination of
the value for the sediments analysed for H. ovalis averaged 224.7
factors other than species composition. Water depth in particular
% (data not shown), indicating a potentially strong contribution

Table 6. Carbon storage in the top 25 cm of Australian seagrass ecosystems and those that would be estimated by applying the
carbon storage values of P. oceanica to the same area of seagrass.

Region Area Habitat Corg stock Corg stock

2 23
(km ) (mg cm ) (Mt)

NSW 161 Zm/Pa 11.74 0.472

TAS 845 Pa/Ps/Aa(Temp.) 8.47 1.788
VIC 470 Pa(subtidal)/Aa(Temp.) 11.48 1.349
SA 9620 Pa, Ps, Aa, 8.47 20.361
QLD/NT/TS 56473 Ho, Zm, Cs, Hu, Cr/Si, Cr/Hu, Th/Cr 5.10 71.957
WA 25000 Pa, Ps, Aa, 9.53 59.558
Total* 92569 155.487
% emissions 104
P. oceanica 92569 Po 20.16 466.545
% emissions 313

Corg stock is the product of the area of seagrass (see Table 6) and the mean carbon storage (Table 2) of the seagrasses most likely to dominate those areas. % emission
refers to the sedimentary Corg in Australian seagrass ecosystems as a % of annual CO2 carbon emissions in Australia. (Zm = Zostera muelleri; Pa = Posidonia australis;
Ps = Posidonia sinuosa; Aa = Amphibolis antarctica; Ho = Halophila ovalis; Cs = Cymodocea serrulata; Hu = Halodule uninervis; Cr = Cymodocea rotundata; Si = Syringodium
isoetifolium; Th = Thalassia hemprichii; Po = Posidonia oceanica).
doi:10.1371/journal.pone.0073748.t006

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 Carbon Stocks in Seagrass Ecosystems

Table 7. Estimated annual carbon accumulation rates of Australia’s seagrass habitats.

Region Area (km2) Storage (km2) Annual Corg accumulation at different sediment accumulation rates

(Mt y21)

0.15 mm y21 1.5 mm y21 9.9 mm y21

NSW 161 11.74 ,0.001 0.002 0.019

TAS 845 8.47 0.001 0.011 0.071
VIC 470 11.48 0.001 0.008 0.053
SA 9620 8.47 0.012 0.122 0.806
QLD/NT/TS 56473 5.10 0.043 0.432 2.850
WA 25000 9.53 0.036 0.357 2.358
Total 92569 0.093 0.932 6.157
% of annual emissions 0.063 0.625 4.129
Mediterranean 92569 20.16 0.280 2.799 18.476
% of annual emissions 0.188 1.877 12.389

Estimates are based on the area of seagrass in different regions of Australia (see Table 2), the mean Corg stocks (Table 4) of the seagrasses most likely to dominate those
areas, and a range of sediment accumulation rates derived from the literature and unpublished data (Table 3).
doi:10.1371/journal.pone.0073748.t007

should be considered potentially important in affecting Corg stocks matter with depth and other showing the inverse. The decrease
in the surficial sediments and warrants further study. with depth is typical of sedimentary systems where there is little
Surprisingly, and in contrast to sub-tidal water depth, when a turnover of the sediment profile and carbon diagenesis results in a
species occurred in both inter-tidal and sub-tidal habitats there gradual loss of first labile and then increasingly refractory C [18].
were no differences in sedimentary organic carbon stocks. The We did not examine the cores for faunal biomass, sediment grain
effects of intermittent submergence on primary production and size or sediment dating, which may provide insights into the
community respiration are complex. Inter-tidal habitats are likely degree of mixing of surface sediments, but these processes may
to experience higher temperatures and associated respiration rates contribute to the observed differences in profiles for those cores
which would enhance C remineralisation [18] and lower C that did not show a decline with depth. Also, it is probable that the
accumulation, particularly if tidal currents also contribute to the top 25 cm is not sufficiently deep to describe the expected negative
export of particulate matter and oxygenation of surface sediment exponential profile of organic matter decomposition with aging
layers. On the other hand, experimental studies have shown that (e.g. P. oceanica [42]).
some species of seagrass exhibit higher rates of photosynthesis
(ETR) in air than when submerged [36]. In addition, the rates of Implications of Variability among Seagrass Habitats for
plant respiration can be lower in inter-tidal sediments [37], and Regional Estimates of Carbon Accumulation
gross community metabolism is reduced during emersion periods While our data are limited in their spatial coverage and in the
[38], which may promote Corg preservation through reduced rates degree of habitat replication, the18-fold difference in the Corg
of remineralisation. A complex set of factors seems to be storage among the different seagrass sediments is clear evidence of
interacting as systems shift between intertidal and subtidal states. the significant variation among seagrass habitats. The Corg storage
As our study was not orthogonal in its design, it is not possible to values presented are likely to be significant under-estimates of the
draw definitive conclusions regarding the difference that climatic true storage on an areal basis as they only apply to the top 25 cm
region may make to Corg stocks. However, as with inter-tidal and of sediment. Many seagrass meadows have organic-rich sediment
sub-tidal habitats, there was no consistent difference in the C extended deeper than this, especially species of Posidonia, with mats
storage of tropical, sub-tropical and temperate seagrass habitats. It cored to depths of over 2.5 m depth [23,42,43]. Furthermore, the
is generally thought that the higher temperatures in tropical mapping of seagrass area is incomplete for much of the country,
regions promote more efficient remineralisation of soil organic including large regions such as the NW, and so the total area of
matter, and a similar process may well occur in shallow coastal seagrass is also likely to be an underestimate. Conservatively, it is
sediments. However, while this simple models may hold for labile reasonable to assume the storage is at least double that which we
forms of C the refractory nature of the C substrate and a range of have estimated. If we accept our estimated stock of 155 Mt (areal
physico-chemical process that protect C from remineralisation stock: 1.616109 g Corg km22), this equates to approximately 100%
may result in poor correlations between temperature and total C of the country’s annual CO2 emissions [44] stored in the top
stocks in soils [39]. Given the high proportion of complex forms of 25 cm of sediments beneath Australian seagrass meadows, a
C in seagrass rhizome material [40,41], their relative resistance to significant portion when considering that Australia is one of the
microbial degradation [29] and the likelihood of oxygen exclusion most intensive per capita greenhouse gas emitters in the World.
in deeper sediments, it is likely that similar complex degradation This stock represents 7.7–15.3% of the recent global estimate for
processes relate to seagrass sedimentary Corg and that simple the top meter of world seagrass soils [21]. The average areal stock
tropical-temperate divisions based on temperature are unlikely to estimated by these authors for all seagrasses studied was of
be the main drivers. 19.426109 g Corg km22, about 3 times higher than that estimated
The vertical profile of carbon accumulation varied among the in the present study for Australian seagrasses (after roughly
species, with most showing the expected decrease in organic normalizing for the top meter of sediment). This proportion

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 Carbon Stocks in Seagrass Ecosystems

increases to 4 times when comparing the Australian average Table 8. Estimated annual Corg stocks in soils of different
against the South Australia region considered by Fourqurean et al. ecosystems.
[21] (26.836109 g Corg km22), but declines to 2.3 times when
comparing the average for South Australia in our study with their
South Australian estimate. Again, these wide ranges and Soil/sediment Carbon Accumulation rate
Ecosystem
discrepancies between studies highlight the need to augment our
knowledge about the natural variability of organic carbon stocks in (g C m22 y21)
seagrass soils. Tropical Forests 2.3–2.5
Our estimates of the annual accumulation of Corg by Australian
Temp Forests 1.4–12
seagrass ecosystems was in the order of 0.09–6.15 Mt Corg. y21
Boreal Forests 0.8–2.2
(1.01–66.5 t km22 y21). As explained previously, we consider a
sediment accumulation rate of 1.5 mm y21 to be more typical for Temp grassland 2.2
seagrass ecosystems than the lower and upper estimates, and this Temperate desert 0.8
sediment accumulation rate yields an estimated Corg accumulation Tundra 0.2–0.7
rate of 0.93 Mt y21, or 10.06 t km22 y21. At this rate, Australian Posidonia oceanica 6–175
seagrass ecosystems would be sequestering up to 0.6% of the
Australian seagrasses 1.0–66.5*
country’s estimated annual CO2 emissions (Australian Govern-
ment Geoscience Australia; www.ga.gov.au). These estimates of C Soil/sediment Carbon Stock
accumulation by Australian seagrass ecosystems are significantly
lower than previously published estimates for seagrasses but still (g C m22)
significantly higher than those reported for most of the World’s
ecosystems (Table 8). This supports earlier assertions [2,11] that Tropical montane 6100
seagrasses have a high carbon sequestration potential, on a per Tropical wet 6100
unit area basis. The Australian Government has set the price of Tropical moist 5000
carbon at A$25.40 in 2014–15, after which it will be determined in
Tropical dry 2200
the market, with estimated trading price of $35 t21 in 2020 [45].
Using the estimated national seagrass Corg stock of 155 Mt and the Warm Temperate moist 7600
above pricing, seagrass habitat would have a market value of $3.9– Warm temperate dry 2600
5.4 bill. for its carbon sequestering function alone. While he free- Cool temperate moist 11600
market trading price of carbon will vary from this predicted value, Cool temperate dry 4900
these estimates serve to emphasise the value of seagrasses and the
Boreal 14900
need to conserve and restore these ecosystems.
Polar 11800

Comparison with P. oceanica-based Estimates Australian seagrasses 1090 – 20140#

The mean Corg content of Australian seagrass habitats was P. oceanica 10500–40000 ‘

about 4 times lower than that recorded in P. oceanica meadows

Data from [67] except Australian seagrasses (this study) and P. oceanica (based
from the Mediterranean Sea. However, the highest Corg content of on the range reported [5,7,42,47].
any Australian seagrass habitat (estuarine P. australis – 4833 g Corg * Value assume sediment depth of 1 m, which is a conservative estimate for the
‘

m22) was almost identical to that of P. oceanica meadow in the higher values which are for Posidonia ecosystems with reported organic
Mediterranean Sea (4837 g Corg m22), when normalized to the sediment depths of .2.5 m ([23] and Pers. Obs. for Oyster Harbour and
Waychinicup Inlet in SW Australia; P. oceanica references as above).
top 25 cm. The similarity of the P. australis and P. oceanica values is doi:10.1371/journal.pone.0073748.t008
consistent with their similar morphology and meadow structure.
Both species have large, persistent rhizomes, placing them close to
for P. oceanica (20.16 mg cm23; derived from the data reported in
each other in seagrass functional-form models [8,14], which
Mateo et al. (1997) and Serrano et al. (2012), since this species has
accumulate in the sediments producing deep, organic-rich
typically been used as the representative seagrass in global C
sediment profiles. Importantly, the meadows of P. oceanica reported
accumulation exercises (note: while several studies report C
in the literature tend to have much deeper organic sediment
accumulation rates for P. oceanica [3,4,46], they ultimately rely
profiles than P. australis (reportedly up to 8 m compared with
2.5 m for P. australis) due to the vertical growth form of the on earlier C stock estimates [30,47], which are applied here.
rhizome. Consequently, P. oceanica habitat will still likely contain When inter-habitat variation in seagrass organic carbon stocks
much larger masses of sedimentary Corg than any of the Australian was ignored and we applied only the P. oceanica carbon storage
seagrass habitats we sampled, and probably represents a global values, the stock was estimated to be about 448 Mt and the annual
maximum among seagrasses. accumulation 0.28–18.4 Mt y21, 3-times the estimates we made
Until now, most of the global estimates of seagrass carbon using the range of carbon storage values we measured for the
storage have, necessarily, been based on indirect estimates and a Australian seagrass habitats and more than 300% of Australia’s
few direct measurements of sedimentary Corg stocks in Posidonia annual CO2 emissions (compared with 100% for the estimates
oceanica meadows, plus a single study of Cymodocea nodosa (e.g. incorporating inter-habitat variability). These simple comparisons
Duarte et al. 2005, Nellemann et al. 2009). The variation in Corg effectively demonstrate the need to better document inter-habitat
storage values among seagrass ecosystems reported here suggests variability in seagrass carbon storage and to incorporate this
that it is important to incorporate this variability into regional or variability into regional and global estimates of seagrass carbon
global estimates of seagrass C stocks. The effect of this inter- stocks. The significant point is not the absolute values of carbon
habitat variation is illustrated by re-calculating the C stocks and storage, but the significant effect on the estimate of incorporating
accumulation rates for the estimated area of Australian seagrass inter-habitat variability. A 3-fold discrepancy in estimates is
using a uniform Corg storage value. We applied the value reported sufficiently large to undermine confidence in Blue Carbon

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 Carbon Stocks in Seagrass Ecosystems

estimates among economic and political decision-makers. This capture and sequester carbon among the 70+ species of seagrasses
supports Nelleman et al.’s [2] identified need to incorporate inter- will potentially lead to erroneous estimates of global C storage and
habitat variability into global estimates if the uncertainties in these improving our understanding of the variability in C stocks and
estimates are to be reduced. accumulation rates is critical if we are to produce robust estimates
of regional and global C capture and storage in seagrass
Conclusions ecosystems.
There is considerable spatial variability in the Corg stock of
seagrass sediments. This variability may be related to both the Acknowledgments
species of seagrass and the habitat setting in which they occur, We thank the following people for their assistance in collecting sediment
particularly water depth. The data set presented here is limited cores: Kathrin Bacher (Shark Bay Dolphin Research Project), Jim
and the errors associated with the estimates are likely to be Fourqurean and the ‘Sharkies’ research team, at Monkey Mia in Shark
significant, though no more so than the global estimates of seagrass Bay, Len McKenzie at Cairns, Kathryn McMahon and the ‘GeoBay’
C capture extrapolated from a much more limited set from the research team in WA.
Mediterranean Sea, acknowledging that at the time those were the
best available data. However, our data serve to emphasise the need Author Contributions
for robust data sets on the carbon storage and accumulation rates Conceived and designed the experiments: PSL M-AM. Performed the
in different seagrass ecosystems. There is also a pressing need to experiments: PSL M-AM. Analyzed the data: PSL M-AM OS MR.
better understand the habitat features that drive this variability in Contributed reagents/materials/analysis tools: PSL OS MR. Wrote the
C storage and accumulation rates. Assuming a uniform ability to paper: PSL M-AM OS MR.

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