BGBiogeosciencesBGBiogeosciences1726-4189Copernicus GmbHGöttingen, Germany10.5194/bg-12-4993-2015Seagrass meadows as a globally significant carbonate reservoirMazarrasaI.imazarrasa@imedea.uib-csic.esMarbàN.https://orcid.org/0000-0002-8048-6789LovelockC. E.SerranoO.LaveryP. S.https://orcid.org/0000-0001-5162-273XFourqureanJ. W.KennedyH.MateoM. A.Krause-JensenD.StevenA. D. L.DuarteC. M.Department of Global Change Research, IMEDEA (CSIC-UIB) Institut
Mediterrani d'Estudis Avançats, C/Miguel Marqués 21, 07190 Esporles
(Mallorca), SpainSchool of Biological Sciences, The University of Queensland, St Lucia,
QLD, 4072, AustraliaThe UWA Oceans Institute, University of Western Australia, 35 Stirling
Highway, Crawley 6009, AustraliaSchool of Natural Sciences, Centre for Marine Ecosystems Research, Edith
Cowan University, Joondalup WA 6027, AustraliaDepartment of Biological Sciences and Southeast Environmental Research
Center, Florida International University (FIU), 11200 SW 8th Street, Miami,
Florida 33199, USASchool of Ocean Sciences, College of Natural Sciences, Bangor University,
Askew Street, Menai Bridge, LL59 5AB, UKCentro de Estudios Avanzados de Blanes, Consejo Superior de
Investigaciones Científicas, Acceso Cala St. Francesc 14, 17300 Blanes,
SpainDepartment of Bioscience, Aarhus University, Vejlsøvej 25, 8600
Silkeborg, DenmarkArctic Research Centre, Aarhus University, C.F. Møllers Allé 8,
8000 Aarhus, DenmarkCSIRO, EcoSciences Precinct, Dutton Park 41 Boggo Road Dutton Park QLD
4102, AustraliaRed Sea Research Center, King Abdullah University of Science and
Technology, Thuwal 23955-6900, Kingdom of Saudi ArabiaI. Mazarrasa (imazarrasa@imedea.uib-csic.es)24August201512164993500319December20146March201517July201524July2015This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/12/4993/2015/bg-12-4993-2015.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/12/4993/2015/bg-12-4993-2015.pdf
There has been growing interest in quantifying the capacity of seagrass
ecosystems to act as carbon sinks as a natural way of offsetting
anthropogenic carbon emissions to the atmosphere. However, most of the
efforts have focused on the particulate organic carbon (POC) stocks and accumulation
rates and ignored the particulate inorganic carbon (PIC) fraction, despite important
carbonate pools associated with calcifying organisms inhabiting the meadows,
such as epiphytes and benthic invertebrates, and despite the relevance that carbonate
precipitation and dissolution processes have in the global carbon cycle. This
study offers the first assessment of the global PIC stocks in seagrass
sediments using a synthesis of published and unpublished data on sediment
carbonate concentration from 403 vegetated and 34 adjacent un-vegetated
sites. PIC stocks in the top 1 m of sediment ranged between 3 and
1660 Mg PIC ha-1, with an average of 654 ± 24 Mg PIC ha-1,
exceeding those of POC reported in previous studies by about a factor of 5. Sedimentary
carbonate stocks varied across seagrass communities, with meadows dominated
by Halodule, Thalassia or Cymodocea supporting the
highest PIC stocks, and tended to decrease polewards at a rate of
-8 ± 2 Mg PIC ha-1 per degree of latitude (general linear
model, GLM; p<0.0003).
Using PIC concentrations and estimates of sediment accretion in seagrass
meadows, the mean PIC accumulation rate in seagrass sediments is found to be
126.3 ± 31.05 g PIC m-2 yr-1. Based on the global extent
of seagrass meadows (177 000 to 600 000 km2), these ecosystems
globally store between 11 and 39 Pg of PIC in the top metre of sediment and
accumulate between 22 and 75 Tg PIC yr-1, representing a significant
contribution to the carbonate dynamics of coastal areas. Despite the fact that these
high rates of carbonate accumulation imply CO2 emissions from
precipitation, seagrass meadows are still strong CO2 sinks as
demonstrated by the comparison of carbon (PIC and POC) stocks between vegetated
and adjacent un-vegetated sediments.
Introduction
Calcium carbonate (CaCO3) accounts for about a 25 % of the surface
marine sediments (Balch et al., 2005). Contemporary oceanic carbonate
sediments are mainly composed of two main mineral forms of calcium carbonate,
calcite (including Mg calcite, magnesium-rich calcite) and aragonite, both
primarily formed by biogenic precipitation (Smith, 2013). The coastal ocean
accounts for around 33 % of the global CaCO3 production (Smith,
2013), but it is where the highest proportion of carbonate sediment
accumulation takes place (nearly two-thirds of its production), whereas in
open ocean sediments only one-third of the CaCO3 produced is accumulated
(Milliman and Droxler, 1996; Smith, 2013). A broad range of communities are
involved in the production and subsequent accumulation of CaCO3 in
marine sediments, including benthic ecosystems dominated by coral reefs
(Chave et al., 1972; Smith, 2013), calcareous algae (Milliman, 1993) and
maerl beds (Bosence and Wilson, 2003); and planktonic communities including
coccolithophores (Westbroek et al., 1989), foraminifera (Langer et al.,
1997), and pteropods (Fabry, 1990). More recently the important contribution
of echinoderms (Lebrato et al., 2010), molluscs (Chauvaud et al., 2003) and
fish (Wilson et al., 2009) to CaCO3 production has been revealed.
Relative to other ecosystems, the production of CaCO3 in seagrass
meadows ecosystems and its accumulation in the sediments is poorly studied
and not explicitly considered in any of the existing assessments of the
global ocean carbonate budget (Milliman et al., 1993; Milliman and Droxler,
1996; Lebrato et al., 2010), despite the important load of carbonate often
found in their sediments and leaves (Canals and Ballesteros, 1997; Gacia et
al., 2003; Perry and Beavington-Penney, 2005; Serrano et al., 2012;
Enríquez and Schubert, 2014) and their role as a source of carbonate
sand for beach formation and preservation (De Falco et al., 2003; Tigny et
al., 2007). Indeed, a global estimate of the carbonate stock in seagrass
sediments is not yet available and the potential contribution of these
systems to the global ocean carbonate budget remains to be evaluated.
There is considerable interest in quantifying the capacity of the world's
ecosystems to trap and store carbon, as this can offset anthropogenic carbon
emissions to the atmosphere. To date, most work on the carbon pools in
seagrass ecosystems has focused on the amount of particulate organic carbon
(POC) stored (Fourqurean et al., 2012; Lavery et al., 2013), whereas, except
for Posidonia oceanica in the Mediterranean Sea (Serrano et al., 2012), the inorganic
component, particulate inorganic carbon (PIC), has not yet been considered
in the assessment of carbon deposits in seagrass meadows. Seagrass
ecosystems support diverse and active communities of calcifying organisms
and through their photosynthetic activity their canopies provide pH
environments that facilitate carbonate deposition (Hendriks et al., 2014).
While PIC, in the form of shells and other skeletal remains represent a
substantial carbon stock, the production of PIC through calcification may
act as a source of CO2 to the atmosphere (Frankignoulle et al., 1994;
Gattuso et al., 1998; Smith, 2013). Thus, understanding the amount of
carbonate in seagrass ecosystems is crucial to determining its role in the
global atmospheric carbon cycle. The evaluation of carbonate
accumulation rates and stocks in seagrass sediments is also relevant as it
may significantly contribute to sediment accretion in coastal areas, a
fundamental mechanism supporting the role of seagrass in coastal protection
(Duarte et al., 2013).
Seagrass meadows accumulate PIC through calcium carbonate production by
calcifying organisms inhabiting the meadows, such as epiphytes (Frankovich
and Zieman, 1994; Perry and Beavington-Penny, 2005; James et al., 2009;
Enríquez and Schubert, 2014) and benthic invertebrates (Jeudy de Grissac
and Boudouresque, 1985) and the deposition of carbonate associated with
sedimentation of particles (Gacia et al., 2003). In addition, a recent study
demonstrates a direct implication of the seagrass Thalassia testudinum in the formation of aragonite needles that accumulate internally
in the cell walls and as external deposits on the blades (Enríquez and
Schubert, 2014). Other evidence for the existence of active carbonate
processes in seagrass beds include calcification and carbonate dissolution in
the canopy, associated with the daily cycles of photosynthesis and
respiration (Frankovich and Zieman, 1994; Barrón et al., 2006; Yates and
Halley, 2006), and the dissolution of calcium carbonate in the sediment as a
result of below-ground release of CO2 by respiratory processes (Hu and
Burdige, 2007).
Distribution of the data of PIC stocks in seagrass meadows (average
top metre; Mg PIC ha-1) compiled in this study by the biogeographic
regions described by Hemminga and Duarte (2000). The size of the pie charts
is proportional to the top metre of PIC stocks in each region. The fraction of
PIC stocks estimated from surface sediments (yellow) and short sediment cores
(P< 100 cm, orange) and longer cores than 100 cm (P> 100 cm, brown)
is indicated.
All the processes mentioned (precipitation, dissolution and sedimentation)
partially depend on seagrass metabolic activity and plant structural features
and thus CaCO3 stocks in seagrass sediments are likely to vary across
meadows of different species (Duarte, 1991). In addition, CaCO3 stocks
in seagrass meadows will likely vary with latitude, as temperature regulates
the seawater saturation state for carbonate minerals that increases with
increasing temperature (Zeebe and Ridgwell, 2011), thereby favouring biogenic
carbonate precipitation in warmer waters (Mutti and Hallock, 2003).
Here we provide the first global assessment of the PIC deposits in seagrass ecosystems. We do so through a synthesis of
published and unpublished data on carbonate stocks in seagrass sediments. We
examine the variability of PIC stocks with biogeographic region, latitude and
taxonomic composition of the seagrass community. We also compare the PIC and
POC stocks in seagrass ecosystems with those in adjacent un-vegetated
sediments, provide a first global assessment of the PIC : POC ratio over
sediment depth profiles and discuss its implications for current estimates of
CO2 sequestration in seagrass ecosystems.
Material and methods
We compiled published data available on carbonate stocks in seagrass
meadows and adjacent un-vegetated sediments. We considered the total pool of
CaCO3 reported without distinguishing between the different possible
biogenic carbonate mineral forms (calcite, Mg calcite and aragonite).
Fourqurean et al. (2012) provided data for 201 sites, and a literature search
using both the Web of Knowledge (using the search terms “seagrass*” AND
“inorganic carbon*” AND [“calcific* OR sediment* OR CaCO3 OR
dissolut* OR diagenesis”]) and Google Scholar (using the search terms
“seagrass carbonate”) yielded data for an additional 82 sites. We amended
the database with unpublished values for 154 additional sites sampled by the
authors. This yielded a total of 437 sites with data on sediment carbonate
concentration in coastal areas occupied by seagrasses, of which 34
corresponded to sand patches adjacent to seagrass meadows (Supplement). The final database comprised estimates for 403 seagrass
vegetated sites, of which 219 consisted of values for sediment surface
samples (ca. 1–30 cm depth) and 184 consisted of values for sediment cores
of variable length (149 cores < 100 cm long, and 35 cores ≥ 100 cm long).
The greatest proportion of the sites (46 %) was located in tropical and
subtropical regions (20–40 degrees latitude) for both the Southern and
Northern hemispheres, whereas the data from higher latitude regions were
scarce (Fig. 1). Data on surface sediment carbonate was broadly distributed,
but most (80 %) core data available were from subtropical and temperate
seagrass meadows (Fig. 1).
Lithogenic characteristics of the sites were not considered in this study,
as we assume that carbonate sediment stocks have a biogenic
origin. We cannot avoid mentioning that this could lead to an overestimation of carbonate
deposition rates in areas where lithogenic carbonate might be important.
However, as the biogenic carbonate pool is considered to be dominant in
contemporary oceanic sediments (Smith, 2013), local geological
characteristics might not have a highly relevant impact on the results of
this study.
When only one of the variables, CaCO3 or PIC, was reported, the other was
estimated assuming that PIC in 12 % of the total molar mass of
CaCO3. In most cases, PIC was reported as
a percentage of dry weight (% DW). To estimate the PIC concentration (mg PIC cm-3), we multiplied the PIC (% DW) by the sediment dry bulk density (DBD; g cm-3).
When DBD was not reported (n=113 sites), we used the average DBD
(1.03 g cm-3) reported by Fourqurean et al. (2012) for seagrass
sediments in the calculations. The error introduced by this assumption was
small, as a paired t test revealed an average deviation of 3.3 %
(t ratio = 4.32; p< 0.0001) when we tested the differences between
estimating PIC concentration using the observed DBD and the assumption of
1.03 for the sites where an observed DBD was reported.
Frequency distribution of observed (i.e. sites reporting data to at
least 1 m, n= 35) and estimated (i.e. sites where shallower
depths were reported, n= 368) PIC stocks (Mg PIC ha-1) in the top
metre of seagrass sediments.
Due to the variability in length of the sediment cores available for the
study, mean PIC concentration in seagrass sediments was estimated for the top
10 cm of sediment for a total of 385 sampled sites, for which at least one
measurement of PIC was reported for this depth zone. To estimate the carbonate
stock within the top metre of sediment for the total database available we
assumed a constant concentration of PIC in the top metre for those cores
where shallower profiles were reported, as almost half (46 %) of the long
cores (length > 100 cm, n=35) showed no significant change in PIC
concentration with depth within the first top metre and the remaining long
cores showed only a slight increase of 0.011 % DW cm-1 on average.
Number of observations, mean ± standard error, median and
range of values for the PIC stocks in each biogeographic region (Tropical
Western Atlantic, Indo-Pacific, Mediterranean, Southern Australia and
Northern Atlantic). The results of the comparison among different regions
(Tukey–Kramer HSD (honest significant difference) test) are shown in the last column where different letters
represent a significant difference (p< 0.05).
The sites were classified based on (1) the seagrass biogeographic regions
described by Hemminga and Duarte (2000) (North East Pacific, South East
Pacific, Tropical Western Atlantic, North Atlantic, South Atlantic,
Mediterranean, Indo-Pacific, Western Pacific and Southern Australia), (2)
10∘ latitude bins and (3) the genus of the dominant seagrass species
(Amphibolis, Halophila, Halodule,
Enhalus, Thalassia, Zostera, Posidonia,
Syringodium, Thalassodendron and Cymodocea).
PIC and POC concentrations were compared along the sediment depth profiles
when both variables were reported in the same site (n= 392). The depth
profile of POC, PIC and POC : PIC within the top metre was explored for the
longest cores (length > 100 cm) when at least three different data points were
reported within the top metre (n= 26). For those sites from which data
for sediments from adjacent vegetated and un-vegetated patches were reported
(n=34), POC and PIC concentrations were also compared.
We used a paired sample t test to assess the difference between the frequency
distribution and average of observed values and estimated values of top metre
stocks and the difference between PIC and POC across the data set and between
adjacent vegetated and un-vegetated patches. Analyses of variance (ANOVA) and
post hoc Tukey tests were applied to compare the PIC stocks among the
biogeographic regions and among the dominant genera. We used general linear
models (GLMs) to test the effect of latitude on the PIC stocks, the
depth variability in the POC and PIC concentrations and their POC : PIC ratio and the variability in POC and PIC concentrations in vegetated
and un-vegetated patches. All statistical analyses were conducted using the
statistical software JMP 5.01a.
Results
Particulate inorganic carbon concentrations within the top 10 cm of seagrass
sediments ranged between 0.3 and 174 mg PIC cm-3, with an average of
62.5 ± 1.7 mg PIC cm-3 and a median of 54 mg PIC cm-3 (n= 385). The PIC stock in the top metre of sediment in seagrass meadows
showed a wide variability, ranging between 3 and 1660 Mg PIC ha-1,
with an average ± standard error and a median of 654 ± 24 and
643 Mg PIC ha-1, respectively (n= 403; Fig. 2). Estimated stocks
(mean ± SE, 676 ± 26 Mg PIC ha-1, Table S1 in Supplement)
were significantly higher than those derived from direct measurements
(mean ± SE, 423 ± 52 Mg PIC ha-1, Table S1, p> 0.05);
however, estimated and measured paired values did not show a significant
difference (Fig. 2; paired t test, p> 0.05).
Mean ± standard error (SE), median, minimum and maximum values
of particulate inorganic carbon (PIC), particulate organic carbon (POC) and
the estimated POC : PIC ratio for the data set where both POC and PIC were
reported (392 sites; n=3076).
The PIC stocks differed significantly among seagrass biogeographic regions
(ANOVA, F ratio = 12.64, p< 0.0001). The largest stocks were found
in the Tropical Western Atlantic similar to those from the Indo-Pacific and
the Mediterranean regions. The North Atlantic PIC stocks were significantly
lower (Table 1). The largest PIC stocks were found in equatorial and
subtropical regions and tended to decrease polewards by -8 ± 2 Mg PIC ha-1 per degree of latitude (Fig. 4; GLM, ChiSquare = 13.43,
p< 0.0002). The low PIC values found between -10∘ and
-20∘ in the Southern Hemisphere are derived from Queensland (Australia),
and the low values between 50–60∘ and 60–70∘ (Northern
Hemisphere) correspond to meadows in northern Denmark and south-west
Greenland, respectively (Fig. 4).
The PIC stocks also differed among dominant species (ANOVA, F
ratio = 13.98; p< 0.0001). The highest PIC stocks were found
underlying Halodule, Thalassia and Cymodocea
meadows, while the lowest stocks were supported by Zostera and
Halophila meadows (Fig. 3). Posidonia meadows had
intermediate PIC stocks.
Where both PIC and POC were measured concurrently (392 sites; n=3076),
mean PIC concentrations tended to exceed mean POC concentrations (paired t
test: T ratio = 64.77, p< 0.0001). The POC : PIC ratio ranged
from nearly 0 to 108, with an average of 0.74 ± 0.05 and a median of
0.20 (Table 2; Fig. 5). For the longest cores in the database (length ≥ 100 cm) which had a minimum of three different observations reported over
1 m depth (n=26), the POC concentration (mg POC cm-3) along
the sediment profile of these cores tended to decrease with depth whereas PIC
(mg PIC cm-3) was more variable (Fig. S1 in Supplement). The
POC : PIC ratio declined consistently with depth in the top metre of
sediment in 69 % of these cores at an average of
-0.00054 % cm-1.
Average PIC stocks (Mg PIC ha-1) ± SE across the
dominant seagrass genera forming the meadows. Only genera with more than 10
observations are shown. Identical letters indicate no significant
differences between dominant species forming the meadows (ANOVA and post hoc
Tukey test).
There was a strong relationship between PIC content (% DW) in paired
vegetated and un-vegetated sediments (R2=0.92, Fig. 6a), with a slope
very close to 1 (0.99 ± 0.02) and an intercept not different from 0
(0.17 ± 0.99), indicating that the PIC content in seagrass sediments
did not differ significantly from that in adjacent un-vegetated sediments
(paired t test, T ratio = 1.67, p> 0.05; n= 195) (Fig. 6a).
However, no relationship was found between the POC content (% DW) in
seagrass sediments and adjacent bare sediments (Fig. 6b). POC content was
significantly higher in vegetated sediments (mean ± SE,
0.66 ± 0.04) compared to adjacent bare sediments (mean ± SE,
0.35 ± 0.017, paired t test, T ratio = -6.57, p< 0.0001; n= 195).
Average PIC stocks (Mg PIC ha-1) ± SE by 10∘
latitude bins. The number above each bar indicates the number of observations
reported for each latitude bin.
DiscussionPIC global stocks and the effect of species and latitudinal
distribution
Available data on PIC stocks in seagrass meadows showed an important
geographic bias. Whereas seagrass meadows are distributed along the coast of
all continents except Antarctica (Hemminga and Duarte, 2000), data on PIC
stocks in seagrass sediments are mostly restricted to tropical and temperate
regions, with a particularly important contribution to the data set by
meadows in Australia and the Mediterranean, especially for the profiles of at
least 1 m deep. Fourqurean et al. (2012) also found a similar bias on the
distribution of data available for their review of particulate organic carbon
(POC) stocks in seagrass meadows, although the data were more widely
distributed. The geographic bias in data availability and the great
variability in PIC stocks among the sites included in this study, add
uncertainty in the assessment of the global estimates provided here. Even
scarcer are data from un-vegetated sediments adjacent to seagrass meadows,
with a comparative approach possible in only 34 of the total of 437 sites,
limiting the certainty of comparisons of PIC and POC stocks in vegetated
versus un-vegetated habitats.
The median PIC sediment top metre stocks of 643 Mg PIC ha-1 (n= 403) is nearly 5 times larger than the median stock of POC recently
estimated by Fourqurean et al. (2012) at around 140 Mg POC ha-1
(n=89). Based on the available range of estimates of global seagrass area,
between 177 000 and 600 000 km2 (Mcleod et al., 2011), seagrass
meadows store globally between 11 and 39 Pg of PIC in the top metre of
sediment.
Frequency distribution of the POC : PIC ratio in the seagrass
sediments examined (392 sites; n= 3076).
Relationship between (a) PIC content (% DW) in seagrass
sediments (x axis) and adjacent un-vegetated sediments (y axis) and (b) POC
content (% DW) in seagrass sediments (x axis) and adjacent un-vegetated
sediments (y axis). The dashed line shows the 1:1 relationship whereas the
continuous line in (a) represents the linear regression model between
PIC content (% DW) in vegetated patches vs. adjacent un-vegetated
patches.
Our results show that the PIC stocks of seagrass meadows vary depending on
the seagrass genera. Large genera, with larger leaf size and extended leaf
life span (Duarte, 1991) were expected to sustain a higher amount of
calcareous epiphytes and favour a higher accumulation of PIC. The age of the
leaves affects the colonisation of seagrass leaves by epiphytes (including
calcareous organisms; Heijs, 1985; Borowitzka et al., 1990; Cebrián et
al., 1994), and the mineral load has been found to increase with increasing
leaf age (Gacia et al., 2003). The height of the canopy, which correlates
with shoot size, has also been shown to determine the epiphyte biomass and
species biodiversity in meadows of Amphibolis (Borowitzka et al., 1990). Sedimentation
process and particle trapping in a meadow are also linked to canopy height
(Gacia et al., 2003) and leaf density (Fonseca and Cahalan, 1992), and
therefore PIC sedimentation and retention may be also favoured in seagrass
meadows dominated by larger species, where long leaves effectively slow
water currents and increase particle settling. In addition, larger seagrass
species may favour carbonate precipitation through their metabolic activity
as the leaf area index has been seen to be directly related to maximum and
range of carbonate saturation state (Ω) values in seagrass meadows (Hendriks et al., 2014). Hence,
we expected to find high storage of PIC in the sediment of large seagrass
genera. However, some large genera, such as Posidonia, did not support particularly
large stocks, while some small genera, such as Halodule, supported large stocks. The
lack of a clear effect of the seagrass genera size could be due to other
controlling factors on the precipitation and preservation of carbonate in
the sediment at regional and local scales not covered by the current study.
These may involve differences in geomorphology, salinity, water depth, tidal
and current regimes, nutrient and light availability and CO2 balance
(Lees, 1975) as well as the presence of nearby ecosystems, such as corals in
tropical regions, which may act as sources of carbonates to seagrass
sediments.
Latitude also influenced the size of the PIC stocks in seagrass sediments,
which tended to decrease with increasing latitude, consistent with the higher
epiphyte carbonate loads in seagrass leaves in tropical compared to temperate
regions (Gacia et al., 2003). This general trend of decline with increasing
latitude has been observed in other carbonate-intense ecosystems, such as
reef-building corals (Veron and Minchin, 1992; Veron, 1995) and encrusting
red algae communities, which are more heavily calcified in warm tropical than
in cold temperate waters (Lowenstam and Weiner, 1989). The latitudinal
distribution of carbonate stocks may be explained by temperature and salinity
dependence of the saturation state of carbonate minerals (Ω) (Zeebe
and Wolf-Gladrow, 2001). The saturation of calcium carbonate in seawater is
mostly dependent on the availability of CO32-, as Ca2+
concentration is 2 orders of magnitude higher than CO32-
concentrations (Gattuso et al., 1998). From a thermodynamic perspective, cold
and fresh water generally promotes lower Ω saturation states and
prevents CaCO3 precipitation (Mucci, 1983). As both salinity and
temperature tend to decrease with increasing latitude, the carbonate
saturation state decreases polewards with respect to tropical and temperate
waters (Hoegh-Guldberg et al., 2007). Hence, the precipitation of biogenic
CaCO3 is favoured in tropical and subtropical areas compared to
temperate regions (Mutti and Hallock, 2003). Discrepancies from the general
trend, such as the low carbonate stocks reported in the latitudinal bins 10∘ S
to 20∘ S are probably explained by local factors that alter the
Ω saturation states, such as inputs of fresh water and terrigeneous
sediments from river discharges in the sites of study (Mellors et al., 2002;
Fisher and Sheaves, 2003).
Estimated area, and PIC accumulation rates globally (Tg PIC yr-1) and per surface area (g PIC m-2 yr-1) for different
carbonate producing ecosystems including the results found for seagrasses in
this study and a global estimation considering neritic, slopes, and pelagic
areas along with organism-level data.
EcosystemAreaGlobalPer surface areaReference(1012 m2)(Tg PIC yr-1)(g PIC m-2 yr-1)Planktonic communities290100–1320.34–0.45Catubig et al. (1998);Milliman and Droxler (1996)Coral reefs0.684140Milliman and Droxler (1996)Halimeda bioherms0.0520400Milliman and Droxler (1996)Bank/Bays0.82430Milliman and Droxler (1996)Seagrass meadows0.6–0.17722–75126.3Mcleod et al. (2011);This studyGlobal1500Lebrato et al. (2010)PIC estimated accumulation rates in seagrass meadows
Our review of the literature indicated that PIC accumulation in seagrass
sediments is high and comparable to other carbonate producing ecosystems.
Based on our identified mean PIC concentration of 62.5 ± 1.7 mg PIC cm-3 in the top 10 cm of seagrass sediments (sites = 385, n=802) and a mean rate of sediment accretion in seagrass meadows of
0.2 ± 0.04 cm yr-1 (Duarte et al., 2013), we estimate that the
PIC accumulation rates in seagrass sediments would average
126.3 ± 31.05 g PIC m-2 yr-1. This rate is somewhat below
the range of PIC sedimentation rates reported by Gacia et al. (2003) in
seagrass meadows of SE Asia, based on direct measures of daily sediment
deposition at eight different sites (145–9443 g PIC m-2 yr-1) but
higher than the average PIC accumulation rate in sediments of
Posidonia oceanica meadows (54.3 ± 1.9 g PIC m-2 yr-1) estimated from sediment stock assessment and
sediment dating (Serrano et al., 2012). Extrapolation, assuming an estimated
range of global area of seagrass meadows between 177 000 and 600 000 km2
(Mcleod et al., 2011), suggests a total accumulation of PIC in seagrass
sediments ranging between 22 ± 5 and 76 ± 19 Tg PIC yr-1.
These estimates are subject to uncertainties derived from the high
variability in PIC stocks among regions and species, and the absence of
estimates on seagrass extent for each region/system considered in this study.
Assuming that tropical seagrass represent two-thirds of the total seagrass, PIC
accumulation rates can be calculated separately for tropical
(17.6 ± 4.5 and 59.7 ± 15.2 Tg PIC yr-1) and temperate
meadows (4.5 ± 1.5 and 15.3 ± 4.9 Tg PIC yr-1, for the low
and high global seagrass area estimates, respectively), yielding a range for
global PIC sequestration in seagrass meadows from 22 ± 6 to
75 ± 20 Tg PIC yr-1, depending on the global seagrass extent
considered.
The rates of PIC accumulation estimated in this study, both globally
(22–75 Tg PIC yr-1) and per surface area (126.3 ± 31.05 g PIC m-2 yr-1), highlight the importance of seagrass meadows as
major sites for CaCO3 accumulation and storage in the ocean. The global
PIC accumulation rates of seagrasses are substantially lower than in deep
oceans by pelagic communities (100–132 Tg PIC yr-1) but significantly
higher when considering their contribution per surface area (0.34–0.45 g PIC m-2 yr-1). Seagrass PIC accumulation rates were comparable to
those of coral reefs both globally (84 Tg PIC yr-1) and per surface
area (140 g PIC m-2 yr-1). Relative to Halimeda bioherms
(20 Tg PIC yr-1), seagrass PIC accumulation showed higher global rates
but significantly lower rates per surface area (400 g PIC m-2 yr-1) (Milliman and Droxler, 1996; Catubig et al., 1998;
Table 3).
Implications in the assessment of the CO2 sink capacity of
seagrass meadows
While PIC represents a substantial carbon stock, carbonate precipitation
results in a rise of the partial pressure of CO2 (pCO2), which,
can result in CO2 supersaturation and release of CO2 to the
atmosphere (Ware et al., 1992). The net release of CO2 with carbonate
deposition is defined by the molar ratio of CO2 flux : CaCO3
precipitation (Ψ), which decreases with decreasing temperature while
increasing with pCO2 (Frankignoulle et al., 1994). Ψ varies from
0.63 in surface waters in low to mid-latitudes, where carbonate precipitation
takes place, to 0.85 below 500 m depth throughout the ocean, where most
dissolution takes place (Smith, 2013). Due to the vertical variation in Ψ, Smith (2013) identified the pelagic carbonate system as a net sink of
CO2, as most of the surface production (Ψ= 0.63) dissolves as
it reaches deep waters (Ψ= 0.85) compensating for the CO2 emitted
by CaCO3 precipitation in surface waters. In contrast, carbonate
deposition in shallow ecosystems, such as seagrass meadows, would act as a
CO2 source as approximate two-thirds of the CaCO3 produced in
shallow benthic ecosystems accumulates in the sediment, and Ψ has the
same value for CaCO3 precipitation and dissolution (Milliman and
Droxler, 1996; Smith, 2013). Given that seagrass meadows are sites of strong
net primary production, any pCO2 increase due to calcification may be
more than compensated for, by organic production. Hence, Ψ has been
interpreted to imply a POC : PIC production ratio threshold, with a value
of 0.63 equivalent to no net change in pCO2 and values greater or
smaller than this value implying a net sink or source, respectively.
The median POC : PIC ratio of seagrass sediments found in this study was
0.2, independent of depth (median of surface sediments 0.17), well below the
POC : PIC ratio threshold of 0.63, with only 18 % of seagrass sediments
showing POC : PIC ratios > 0.6. Following the rationale above and
assuming that organic carbon and calcium carbonate accumulate in the sediment
in proportion to their production, these results could be interpreted to
imply that CO2 emissions derived from carbonate deposition may offset
the CO2 sink capacity associated with organic carbon burial in seagrass
sediments globally, as discussed before for Posidonia oceanica in
the Mediterranean (Mateo and Serrano, 2012; Serrano et al., 2012). However,
such interpretation would be premature. In general terms, the organic and
inorganic carbon cycles in the ocean run at very different rates and although
organic matter is produced at much faster rates than CaCO3, it is also
decomposed more rapidly (Smith, 2013). However, the carbonate precipitation
in seagrass meadows is intimately regulated by the organic metabolic rates of
the ecosystem (Smith and Atkinson, 1983; Barrón et al., 2006; Yates and
Halley, 2006; Hendriks et al., 2014), and when both organic and inorganic
carbon metabolic pathways have been measured in situ simultaneously, seagrass
meadows have been found to be mainly net CO2 sinks systems at a yearly
scale (Barrón et al., 2006), even despite the underestimated net
community production (NCP) rates that may result from the use of confined
incubation chambers related to photooxidation processes and subsequent
CO2 increase and O2 decrease during daytime (Champenois and Borges,
2012). In addition to carbon burial, a significant fraction of the net
community production of seagrass, supporting a CO2 sink, is also
exported as DOC and POC (Cebrián et al., 1997; Barrón and Duarte,
2009). Hence, the comparison of sediment standing stocks would reflect only a
fraction of the sink capacity of the seagrass ecosystems but not the net
effect of the organic and inorganic carbon metabolic pathways on the net
CO2 flux. Therefore, more research, which takes into account both the
organic and inorganic carbon cycles associated with these systems, is needed
to better assess the role of seagrass ecosystems as carbon sinks or sources.
Understanding the balance between CO2 emissions from carbonate
deposition and CO2 sequestration from organic carbon storage in seagrass
sediments should not only focus on the POC : PIC ratio, but also on
resolving how seagrass affects the POC : PIC ratio compared to adjacent
un-vegetated sediments. When comparing the carbon content (% DW) between
vegetated and adjacent un-vegetated patches, there was no difference in PIC,
whereas the POC content was about two-fold larger in vegetated sediments
compared to adjacent un-vegetated sediments as previously observed (Duarte et
al., 2010; Kennedy et al., 2010). This result indicates that, despite the
significant carbonate sediment deposits identified and that seagrasses favour
carbonate precipitation and accumulation by epiphytes and other organisms
inhabiting the meadow, sediment PIC largely depends on local environmental
conditions that control carbonate precipitation and a significant fraction
may derive from external sources, such as adjacent carbonate producer systems
(corals). As a consequence, the POC : PIC ratio of seagrass sediments
(mean ± SE, 0.28 ± 0.06) exceeded that of adjacent un-vegetated
sediments (mean ± SE, 0.19 ± 0.040) in 73 % of the meadows
examined. Hence, the organic carbon stock present in seagrass sediments would
be expected to be reduced by half if seagrass cover was lost, while the
inorganic stock would be comparable, thereby confirming the role of seagrass
meadows as intense CO2 sinks. It is important to point out that the
rational above is related to the content (% DW) of both PIC and POC and not to
the rate of accumulation, which may be significantly higher in seagrass
compared to adjacent sand patches due to autotrophic production and sediment
trapping.
In addition there are possible interactions between carbonate and organic
carbon deposition that might enhance carbon sequestration in seagrass
meadows. One possibility may be that high carbonate deposition rates may
promote organic carbon sequestration and storage by enhancing sediment
accretion and by rapidly removing organic carbon from surface sediments and
away from the oxic zone, thereby enhancing preservation of organic carbon.
The accumulation of carbonates in seagrass sediments may also influence
below-ground biomass through the stimulation of vertical growth in the
sediments, or through alteration of sediment composition and nutrient
availability (Short, 1987; Ferdie and Fourqurean, 2004). In fact,
Erftemeijer (1994) found higher below-ground biomass in seagrass meadows
growing in carbonate sediments compared to meadows from the same species
that develop in terrigenous sediment. Thus, the potentially higher
below-ground production in carbonate-rich meadows may enhance organic carbon
burial.
Implications in the role of seagrass meadows as coastal
protection
Carbonate stocks represented an average of 51 ± 1 % of the dry
weight in the top 10 cm (range 0.2 to 100 %) of the seagrass sediments
examined, therefore contributing significantly to the sediment accretion rate
and coastal protection from increased sea level rise and storminess with
climate change (Duarte et al., 2013). The capacity of seagrass meadows to
raise the seafloor at speeds that could match or exceed current sea level
rise allows them to remain effective in protecting coastal areas (Duarte et
al., 2013). A recent review of coastal ecosystems sediment accretion rates
found an average accretion rate of 2 ± 0.4 mm yr-1 for seagrass
communities (Duarte et al., 2013; Mazarrasa et al., 2013), highlighting the
important role these ecosystems may play in climate adaptation in coastal
areas. Carbonate production and accumulation supports about half of this
accretion rate.
This study offers the first global compilation of carbonate deposits in
seagrass sediments. Despite some limitations in the geographic distribution
of the data available, the scarcity of data from adjacent sand patches and
the lack of local sediment accretion rates, we identified the significant role
of seagrass ecosystems in the carbonate dynamics of coastal areas, with
carbonate stocks and rates relevant at the global scale. Carbonate stocks,
markedly higher in tropical and subtropical meadows, play a significant role
in supporting the accretion rate of seagrass meadows, and while high
carbonate deposition lead to CO2 emissions, the comparison of vegetated vs.
adjacent un-vegetated sediments still identifies seagrass meadows as strong
CO2 sinks. In order to increase understanding of the effect of carbonate
accumulation in seagrass meadows on the function they play as CO2
sinks, further investigation is required, especially on the coupling of the
organic and inorganic metabolic processes that take place within the
meadows.
The Supplement related to this article is available online at doi:10.5194/bg-12-4993-2015-supplement.
Acknowledgements
This study was funded by the EU FP7 project Opera (contract no. 308393),
the project EstresX funded by the Spanish Ministry of Economy and
Competitiveness (contract no. CTM2012-32603), the CSIRO Marine and Coastal
Carbon Biogeochemistry Cluster and the Danish Environmental Protection Agency
within the Danish Cooperation for Environment in the Arctic (DANCEA).
I. Mazarrasa was supported by a PhD scholarship of the Government of the
Balearic Islands (Spain) and The European Social Founding (ESF), and
N. Marbà was partially supported by a Gledden visiting fellowship of The
Institute of Advanced Studies UWA. This is contribution no. 734 from the
Southeast Environmental Research Center at FIU. Edited by: G. Herndl
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