First assessment of seagrass carbon accumulation rates in Sweden: A field study from a fjord system at the Skagerrak coast

Martin Dahl; Maria E. Asplund; Sanne Bergman; Mats Björk; Sara Braun; Elin Löfgren; Elisa Martí; Pere Masque; Robin Svensson; Martin Gullström

doi:10.1371/journal.pclm.0000099

Abstract

Seagrass meadows are globally important blue carbon sinks. In northern cold-temperate regions, eelgrass (Zostera marina) is the dominant seagrass species, and although their sedimentary carbon stocks have been quantified across regions, information regarding the CO₂ withdrawal capacity as carbon sinks remains scarce. Here we assessed the carbon (C_org) accumulation rates (CARs) and stocks as well as the organic matter sources in five seagrass meadows in the Gullmar Fjord area on the Swedish Skagerrak coast. We found that the mean (±SD) CAR was 14 ± 3 g C_org m^-2 yr^-1 over the last ~120–140 years (corresponding to a yearly uptake of 52.4 ± 12.6 g CO2 m^-2). The carbon sink capacity is in line with other Z. marina areas but relatively low compared to other seagrass species and regions globally. About half of the sedimentary carbon accumulation (7.1 ± 3.3 g C_org m^-2 yr^-1) originated from macroalgae biomass, which highlights the importance of non-seagrass derived material for the carbon sink function of seagrass meadows in the area. The C_org stocks were similar among sites when comparing at a standardized depth of 50 cm (4.6–5.9 kg C_org m^-2), but showed large variation when assessed for the total extent of the cores (ranging from 0.7 to 20.6 kg C_org m^-2 for sediment depths of 11 to at least 149 cm). The low sediment accretion rates (1.18–1.86 mm yr^-1) and the relatively thick sediment deposits (with a maximum of >150 cm of sediment depth) suggests that the carbon stocks have likely been accumulated for an extended period of time, and that the documented loss of seagrass meadows in the Swedish Skagerrak region and associated erosion of the sediment could potentially have offset centuries of carbon sequestration.

Citation: Dahl M, Asplund ME, Bergman S, Björk M, Braun S, Löfgren E, et al. (2023) First assessment of seagrass carbon accumulation rates in Sweden: A field study from a fjord system at the Skagerrak coast. PLOS Clim 2(1): e0000099. https://doi.org/10.1371/journal.pclm.0000099

Editor: Matthieu Carré, Centre National de la Recherche Scientifique, FRANCE

Received: June 8, 2022; Accepted: November 25, 2022; Published: January 5, 2023

Copyright: © 2023 Dahl 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.

Data Availability: All data is presented in the manuscript and Supporting information files.

Funding: MD was supported by Helge Ax:son Johnson foundation (grant number: F21-0103), Bolin Centre for climate research, the foundation for Baltic and East European studies (Östersjöstiftelsen) (grant number: 21-PD2-0002) and Albert och Maria Bergström foundation. PM was funded through the Australian Research Council LIEF Project (LE170100219). The IAEA is grateful for the support provided to its Marine Environment Laboratories by the Government of the Principality of Monaco. MG, MEA, MB, SB was supported the foundation for Baltic and East European studies (Östersjöstiftelsen) (grant number: 21-GP-0005). 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.

Introduction

Natural carbon sinks are vital for mitigating climate change [1] and seagrass meadows have the potential for accumulating large amounts of carbon in the sediment, and thereby constitute a globally important long-term sink for atmospheric CO₂ [2,3]. The accumulated sedimentary carbon is usually of both autochthonous and allochthonous origin as seagrass meadows trap and store organic matter produced within as well as outside the meadow, with most of the externally produced carbon derived from terrestrial and pelagic (seston) sources [4]. Recently, macroalgae have also been highlighted as an important external carbon donor to blue carbon ecosystems [5]. It is worth noting that macroalgae are an integral part of many seagrass ecosystems and can equally constitute an autochthonous carbon source, as they grow epiphytically on the seagrass leaves or attached to the sediment substrate, and contribute to the overall biomass production of seagrass meadows [6]. The high community production, low degradation of organic matter in the sediment and the allochthonous carbon contributions are the main reasons for seagrass meadows’ ability to build up large organic carbon (C_org) sedimentary deposits [7]. These sediment deposits can extend several meters in thickness accumulated over centuries or millennia [8], but there is also a large variability in the seagrasses’ capacity to sequester C_org, ranging from as low as 2 to more than 250 g C_org m^-2 yr^-1 (see for example [9–12]) This variability highlights the need to assess the seagrass carbon sink function in understudied geographical regions and species, to accurately estimate the capacity of seagrass meadows as natural carbon sinks for climate change mitigation.

Seagrass meadows are found in most coastal waters around the world and eelgrass (Zostera marina) is a dominant seagrass species in cold-temperate regions of the Northern Hemisphere [13]. The species show a great variability in carbon stocks and the Z. marina sediments on the Swedish Skagerrak coast has been found to be particularly rich in C_org compared to many other regions, with mean C_org stocks almost two times larger (~4900 g C_org m^-2, down to 25 cm sediment depth) than the Z. marina average (~2700 g C_org m^-2; [14]). However, seagrass meadows along the Swedish Skagerrak coast have suffered from severe decreases in areal distribution (about 60% loss) between the 1980s and early 2000s [15,16] due to coastal eutrophication and overexploitation of large predatory fish (leading to cascading effects), resulting in overgrowth of filamentous algae [17,18], and this has led to erosion of the sedimentary C_org stocks [19]. The C_org stocks of Z. marina have been studied across the Northern Hemisphere (e.g. [19–21]), but there are still only a few estimates on the species’ C_org sequestration rates from any of its distribution range (but see [22–24]) and to our knowledge the carbon accumulation rates (CAR) has not yet been quantified in Swedish seagrass meadows. This information is useful for incorporating natural carbon sinks into national greenhouse gas inventories or in carbon credit schemes [25]. With focus on natural carbon sinks on the Swedish Skagerrak coast, we aimed to (1) estimate the carbon accumulation rates and stocks in Z. marina meadows within the area of a fjord environment, and (2) assess and determine the organic matter sources contributing to the sedimentary C_org pool of the seagrass meadows.

Methods

Study site

The sediment core sampling was conducted in the area of the Gullmar Fjord on the Swedish Skagerrak coast during August 2020. The Gullmar Fjord is a species-rich fjord, about 25 km in length, 1–3 km wide and with a deeper area in the central part (max. depth: 118.5 m). It is the only true fjord in Sweden and became the first marine conservation area (IUCN category V) in Sweden in 1983. The fjord is characterized by a mix of steep cliffs along the sloping fjord sides and fringing shallow-water areas composed of soft bottoms with numerous seagrass (Z. marina) meadows and other rooted macrophyte vegetation at water depths between 0.5 to 6 m. Generally, the fjord is located within a diverse coastal archipelago characterized by a mosaic of bays, inlets and small islands. The water body in the shallows comprises water from the Baltic current mixed with Kattegat and Skagerrak water, local runoff and supply of water from the Örekil river in the inner most part of the fjord [26]. The mean tidal amplitude is about 0.3 m, with oscillations up to 2 m due to variability in air pressure and wind conditions [27]. Five seagrass meadows in or near the fjord were selected, covering the most interior parts and areas towards the open ocean in the southwest, and represent typical environmental conditions for seagrasses in the area (Fig 1). The two meadows at Gåsö (located in sheltered bays in the north and south of the small island right outside of the fjord sill) have a similar hydrodynamic exposure and water depth distribution (ranging from ~0.5 to 4 m). The cores were collected at 1.8 m in Gåsö S and 3 m in Gåsö N. The Kristineberg site is more exposed to winds and waves [19] and the sediment ranges from a coarser sand-mud mixture in the shallower part of the meadow (about 10% mud content at 1–3 m water depth) to muddier in the deeper part (~35–50% mud content at 3–6 m water depth), where the cores were collected (at 4.3 to 4.5 m water depth) [28]. The Getevik site is situated in a highly sheltered embayment with low hydrodynamic exposure [29], and the seagrass meadow is found on 0.5 to 5 m water depth and the core was collected in the middle of the meadow at a depth of 2.5 m. The seagrass meadow at Västra Korsvik is situated next to the Örekil river mouth in the inner part of the fjord and due to high water discharge the water is turbid with low visibility. The water depth of the sampling site was 0.8 m, but the maximum water depth of the meadow is not known.

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Fig 1. Map over the Gullmar Fjord area with sampling sites and mapped seagrass areas.

The map has been generated in ArcGIS pro, version 2.5.0 (ESRI, 2020). The base map was provided by the EEA geospatial data catalogue and available from: https://sdi.eea.europa.eu/catalogue/srv/eng/catalog.search#/metadata/db4cfdd3-0687-4460-a2c7-fd10ca29c214.

https://doi.org/10.1371/journal.pclm.0000099.g001

Sediment sampling and analysis

The sediment cores were collected using SCUBA and 2 m long PVC-cores (with an internal diameter of 7.5 cm). In each seagrass meadow site, one sediment core was sampled, except for in Kristineberg where two cores were taken approximately 50 m apart. Core compression was assessed by measuring the inner and outer parts of the core when pressed down into the sediment and based on the difference between these two values a linear compression factor was calculated. The core compression ranged from 7 to 69%, with the highest value found in Getevik (Table 2). The cores were sliced into 1 cm thick layers for the entire length of a core and dried at 60°C until constant weight to obtain the dry weight of the sediment slices. For the determination of the sedimentation rates, an aliquot of the slices for the top 21 cm was analyzed for ²¹⁰Pb. The concentrations of ²¹⁰Pb were determined by measuring its decay product ²¹⁰Po in equilibrium using alpha spectrometry [30]. The concentrations of ²²⁶Ra were also analyzed in three evenly distributed slices along the sediment profiles based on the decay products ²¹⁴Pb and ²¹⁴Bi using gamma spectrometry. The concentrations of excess ²¹⁰Pb were calculated from the difference between total ²¹⁰Pb and the average ²²⁶Ra and used to obtain an age model for each profile. The mean sedimentation rates were calculated using the Constant Flux:Constant Sedimentation (CF:CS, [31,32] model for the sections of the sediment profiles where a clear decline in excess ²¹⁰Pb concentrations was present, usually below an upper mixed layer [31]. The Constant Rate of Supply (CRS, [33]) model was applied where possible (i.e. in the Gåsö cores where all sediment sections down to 21 cm were analyzed for ²¹⁰Pb). Only in the Gåsö cores, the age along the depth of the ²¹⁰Pb horizon was calculated as they showed constant decreasing ²¹⁰Pb trends from the surface down to the supported ²¹⁰Pb levels. Average sedimentation rates based on the concentration profiles of excess ²¹⁰Pb were calculated using the CF:CS model, frequently below the upper mixed layers, which implies that they need to be taken as upper limits.

For determining the C_org content (in % dry weight) and δ¹³C and δ¹⁵N stable isotopes of the slices, a carbon and nitrogen elemental analyzer interfaced with an isotope ratio mass spectrometer was used. The delta isotope ratios are expressed in permille relative to the VPDB (Vienna PeeDee Belemnite) for δ¹³C and to atmospheric nitrogen for δ¹⁵N, and by using acetanilid (δ¹³C = −26.14 ± 0.15‰, δ¹⁵N = 0.38 ± 0.12‰) as reference material. The C_org content and δ ¹³C and δ ¹⁵N stable isotope values of the topmost 50 cm layer were measured in each cm from 0 to 5 cm, followed by at 7 and 10 cm depths and at each 5 cm from 10 cm to the maximum extent of the sediment core. In Gåsö S, Gåsö N and Västra Korsvik, the total seagrass depth layers were found from 11 to 62 cm depth. Below this depth horizon, there were homogeneous clay layers, distinctly different from the organic sediment of the seagrass layer, which we interpreted as the sediment condition before establishing of the seagrass meadow. Prior to analysis, the samples were homogenized into a fine powder using a mixing mill, and treated with 1M HCl (direct addition using a pipet), following the protocol of Dahl et al. [34] in order to remove carbonates. The addition of HCl was continued until the reaction with the carbonate was complete.

Quantification of C_org sequestration rates and stocks

To calculate the CAR (g C_org m^-2 yr^-1), the mass accumulation rate (MAR, g cm^-2 yr^-1) was multiplied by the weighted %C_org concentration, as described in Arias-Ortiz et al. [31] for the section of the sediment profile where the CF:CS model was applied. As sediment mixing was present in some of the cores, we assumed that the MAR obtained from the underlying section (where sediment mixing was not present) was the same for the mixed layer. The average CAR for the most recent decades was then calculated for the length of the core where excess ²¹⁰Pb was present. The sediment dry bulk density (DBD, g cm^-3) was derived from the weight of each slice divided by the volume of the core slice. The C_org density (g C_org cm^-3) was calculated by multiplying the %C_org content with the sediment density of each slice. The C_org stocks were obtained by adding up the C_org density for each slice to the standardized depth of 50 cm for comparison between sites.

Estimate of contribution of potential C_org sources to the seagrass meadow C_org storage

The contribution of potential sources (i.e. terrestrial organic matter, macroalgae biomass and seagrass biomass) to the sedimentary C_org pool was analyzed using the Simmr package in R version 3.6.3 [35,36] with stable isotopes of δ¹³C and δ¹⁵N as tracers down to 50 cm sediment depth, with the exception of Västra Korsvik, where the maximum seagrass sediment depth of 11 cm was used. The 50 cm sediment depth was used to align the C_org sources to the standardized sediment depth of the C_org stocks. As degradation of organic matter can alter the δ¹³C over time [37], we also assessed the proportion of C_org sources in the surface sediment only (down to ~10 cm) but with no noticeable differences compared to the 0–50 cm depth (Table A in S1 Text). The three potential sources were selected based on previous findings from Gullmar Fjord [14], the high amount of macroalgae found in the meadows when sampling and the meadows relative proximity to land. For the terrestrial and macroalgae endmembers, we used literature values, while samples of seagrass biomass (average values of above- and belowground plant tissue) was collected (n = 3) at two sites (i.e. Getevik and Kristineberg) for this study. The isotopic values of the potential sources were distinct with stable isotopes for terrestrial organic matter of −28.9 ± 1.3‰ (δ¹³C) and 0.8 ± 2.5‰ (δ¹⁵N) [38,39], macroalgae biomass of −19.8 ± 1.8‰ (δ¹³C) and 3.2 ± 0.7‰ (δ¹⁵N) [40] and seagrass plant biomass of −9.8 ± 1.8‰ (δ¹³C) and 1.0 ± 1.1‰ (δ¹⁵N) (this study). The macroalgae species used as potential sources were the brown algae Saccharina latissima and Laminaria hyperborea, which are commonly found on rocky shores in vicinity of the seagrass meadows on the Swedish Skagerrak coast. Other species of the macroalgae flora of the seagrass ecosystem in this coastal region are Chorda filum (δ¹³C = −19.9), Fucus serratus (δ¹³C = −17.6), Pilayella sp. (δ¹³C = −15.57), Ceramium rubrum (δ¹³C = −19.56) and Ulva intestinalis (δ¹³C = – 20.3) [41], which all have similar δ¹³C values.

Results

The concentrations of total ²¹⁰Pb in cores Gåsö N and Gåsö S decreased with depth to about 25 Bq kg^-1 at around 10 cm and 18 cm depth, respectively, although the concentrations were relatively constant between 3 and 7 cm for core Gåsö S (Fig 2). A constant ²¹⁰Pb was interpreted as mixing or a sudden input of sediment [31]. For core Kristineberg 1, the concentrations of total ²¹⁰Pb were constant between 3 and 10 cm and decreased with depth thereafter, down to 32 Bq kg^-1 at about 20 cm depth. For core Kristineberg 2, the concentrations of total ²¹⁰Pb decreased with depth to 24 Bq kg^-1 at 20 cm, although the levels were relatively constant between 8 and 13 cm, coincidentally with somewhat lower values of DBD. The concentrations of total ²¹⁰Pb in core Getevik decreased with depth from 220 Bq kg^-1 at the surface to about 25 Bq kg^-1 at 16 cm depth, albeit with constant values between 2 and 6 cm. The concentrations of total ²¹⁰Pb in core Västra Korsvik decreased with depth to about 22 Bq kg^-1 at 4 cm (Fig 2). For all cores, the concentrations of ²²⁶Ra (²¹⁰Pb supported) ranged from 23 to 25 Bq kg^-1.

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Fig 2. Concentration profiles of ²¹⁰Pb for the sediment cores.

The blue fields represent the supported ²¹⁰Pb levels and the green fields show the sections for which sedimentation rates could be calculated.

https://doi.org/10.1371/journal.pclm.0000099.g002

An average sedimentation rate of 0.0193 ± 0.0007 g cm^-2 yr^-1 (1.21 ± 0.05 mm yr^-1) was estimated for core Gåsö N (Table 1), but it could also be possible to interpret the ²¹⁰Pb concentration profile as evidencing a higher sedimentation rate from the 1960s (at around 5 cm; Fig 2), which would have increased from 0.009 to 0.026 g cm^-2 yr^-1 (or from 0.6 to 1.2 mm yr^-1). This interpretation is in good agreement with the results obtained when applying the CRS model. For core Gåsö S, an average sedimentation rate for the upper 11 cm was estimated of 0.0165 ± 0.0013 g cm^-2 yr^-1 (1.18 ± 0.09 mm yr^-1; Table 1). However, while this estimate is comparable to the results of the CRS model, it needs to be taken with caution because of the presence of the layer at 3–7 cm, likely evidencing some local mixing. For core Kristineberg 1, the average sedimentation rate was of 0.074 ± 0.006 g cm^-2 yr^-1 (1.86 ± 0.14 mm y^-1), but it could be possible that there had been a change of the sedimentation rate in the past (at around 13 cm), which would have decreased from 0.09 to 0.03 g cm^-2 yr^-1 (from 2.2 to 1.3 mm yr^-1). For core Kristineberg 2, the upper 8 cm had accumulated at an average rate of 0.079 ± 0.005 g cm^-2 yr^-1 (1.96 ± 0.13 mm yr^-1), while in the past it would have been of 0.063 ± 0.013 g cm^-2 yr^-1 (0.83 ± 0.17 mm yr^-1) below 13 cm (Table 1). The average accumulation in Kristineberg 2 was 0.069 ± 0.001 g cm^-2 yr^-1 and 1.39 ± 0.15 mm yr^-1. For the Getevik core, an average sedimentation rate of 0.0154 ± 0.0005 g cm^-2 yr^-1 (1.66 ± 0.05 mm yr^-1) can be calculated below the upper layers applying the CF:CS model. Finally, for core Västra Korsvik, the horizon of excess ²¹⁰Pb was reached at 4 cm, precluding the estimation of a sedimentation rate for this core, that, in any case, would be very low.

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Table 1. Summary of sediment and mass accumulation rates (SAR and MAR, respectively) and C_org content.

For Kristineberg 1 and 2 and Getevik, SAR and MAR could not be established for the entire excess ²¹⁰Pb depth section (see Fig 2) due to sediment mixing and the values were therefore extrapolated towards the sediment surface. Bold values show the average sedimentation rates and were used for calculating the CARs in the cores. All values are presented as mean ± SD and SAR is corrected for core compression.

https://doi.org/10.1371/journal.pclm.0000099.t001

The lowest average (±SD) CAR values were found in Gåsö S and Gåsö N (10.9 ± 0.7 and 12.2 ± 0.4 g C_org m^-2 yr^-1, respectively), followed by Getevik (15.3 ± 0.5 g C_org m^-2 yr^-1) and Kristineberg, with a mean (±SD) for the two cores of 18.6 ± 8.0 g C_org m^-2 yr^-1 (Kristineberg 1: 24.5 ± 1.9 g C_org m^-2 yr^-1, Kristineberg 2: 12.7 ± 1.4 g C_org m^-2 yr^-1) (Fig 3). The difference in CAR seen at the Kristineberg site was due to a slightly higher accumulation rate and %C_org content in the topmost sediment of Kristineberg 1 (Table 1). The mean (±SD) CAR in the seagrass meadows averaged 14.3 ± 3.4 g C_org m^-2 yr^-1, which corresponds to an uptake of 52.4 ± 12.6 g CO₂ yr^-1.

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Fig 3. Carbon accumulation rate (CAR) for the different sites.

Literature CAR values for Z. marina in other regions [22–24,42–44] are shown as dashed lines and shaded box (the width of the box covers the range of values for the referenced studies). The estimated mean value for Posidonia oceanica, which is considered the most efficient seagrass species for carbon sediment sequestration, is included as a reference for the seagrasses’ potential as carbon sinks.

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The cumulative C_org stocks corrected for core compression show a similar accumulation level across cores (Fig 4A) and for C_org stocks calculated to 50 cm sediment depth. The 0–50 cm C_org stocks were slightly lower in Gåsö S (4.61 kg C_org m^-2) and Getevik (4.67 kg C_org m^-2) compared to the other meadows, while the highest levels were found in Kristineberg (mean ± SD) and Gåsö N (5.11 ± 1.31 g m^-2 and 5.88, respectively) (Fig 4B). For Västra Korsvik, no C_org stock value was calculated for the standardized depth as the seagrass sediment depth horizon was only 11 cm thick, while for the other sites the seagrass sediment ranged from 59 to at least 149 cm deep. The total C_org stocks in the entire core reflects the difference in sediment length of the core, with the highest value seen in the Kristineberg site (Kristineberg 1: 11.6 kg C_org m^-2 at the depth of 111 cm, Kristineberg 2: 20.6 kg C_org m^-2 at the depth of 149 cm) (Fig 4C).

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Fig 4.

C_org stocks (kg C m^-2) shown as (A) cumulative accumulation of the sediment depths, (B) standardized stocks down to 50 cm sediment depth and (C) the total accumulation for the entire sediment core depths.

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The δ¹³C values were lowest in Västra Korsvik, followed by Kristineberg, while Gåsö S, Gåsö N and Getevik showed similarly higher values (Table 2). The δ¹³C values showed only minor variation along the upper 50 cm in all sites (Table 2; Fig A in S1 Text). In all cores, there was a high proportion of macroalgae biomass contribution (ranging from 41 to 64%) to the sedimentary C_org pool. The terrestrial source input was generally low (7–11%), except for Västra Korsvik, where terrestrial organic material contributed with 36% of the C_org and the seagrass plant biomass isotopic signal was low (9%). For the other sites, seagrass input varied from 29% in Kristineberg to a maximum of 49% in Getevik (Fig 5). Given the C_org accumulation rates of the seagrass meadows (Table 1), an estimate of 5.2–7.4 g C_org m^-2 autochthonous seagrass biomass, 4.8–11.9 g C_org m^-2 macroalgae material and 0.9–1.6 g C_org m^-2 of terrestrial organic matter is being stored annually.

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Fig 5. The proportion of seagrass, macroalgae and terrestrial organic matter contributing to the sedimentary C_org pool for the sediment depth of 0–50 cm, except for Västra Korsvik, for which the seagrass sediment depth was 0–11 cm.

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Table 2. Seagrass sediment depth, sediment compression, and mean (± SD) of C_org content and stable isotopic signatures for 0–50 cm depth layer.

https://doi.org/10.1371/journal.pclm.0000099.t002

Discussion

This first estimate of seagrass carbon sink capacity in Sweden, which was performed in the Gullmar Fjord area on the Skagerrak coast showed an average (±SD) CAR of 14 ± 3 g C_org m^-2 yr^-1 during the last century. In a Swedish perspective, this rate of seagrass C_org accumulation is comparable to more well-documented carbon sink habitats, such as forest soils (18 g C m^-2 yr^-1) [45] and peatlands in Sweden (around 12–16 g C m^-2 yr^-1) ([46], and references within). The Z. marina carbon sink function in the Gullmar Fjord area was highly dependent on the accumulation of macroalgae biomass (ranging from 41 to 64% of the total C_org pool), being equal or even higher than the seagrass plant contribution (that ranged from 9 to 49%). The findings from this study highlight that the Z. marina meadows in the area of the Gullmar Fjord is a sink of atmospheric CO₂ (of both autochthonous and allochthonous organic matter), with a yearly CO₂ uptake of 52 ± 13 g yr^-1. Given the extensive loss of seagrass meadows on the Swedish Skagerrak coast [15], it is crucial to protect the seagrass meadows to avoid C_org erosion and for continuous atmospheric CO₂ uptake.

The C_org accumulation in the seagrass meadows varied from 11 to 25 g C_org m^-2 yr^-1, with the highest CAR found in Kristineberg and due to mixing of the topmost sediment in some of the cores, the CAR values should be seen as upper estimates. The Kristineberg site is relatively exposed to hydrodynamic forces (with a mean wave height of 0.25 m) in relation to the other sites (for instance 0.10 m in Getevik) [29], which in this area has been shown to positively influence the carbon storage in these low sediment density and silty seagrass beds [28,47] and with a high input of allochthonous sources transported by waves and currents could promote the C_org accumulation of the meadow [14]. The Gåsö and Getevik sites had similar CAR (11–15 g C_org m^-2 yr^-1) and with equivalent autochthonous–allochthonous source ratios of the sedimentary C_org pool. Gåsö and Getevik are both located in sheltered embayments of the fjord area with comparable hydrodynamic conditions, and this could explain the similarity in C_org accumulation and organic matter sources, as hydrodynamic exposure is highly affecting the sediment deposition and allochthonous C_org input [48], in smaller and fast-growing seagrass species, including Z. marina [12,49–51]. The cores at Gåsö also displayed an increase in sedimentation rates during the 1960s but this needs further investigation as the island is located in a relatively remote area with no major coastal development or human activities, such as dredging, which could alter the sedimentation processes [52]. This study only presents one core from each site (except for Kristineberg) and in order to account for seagrass meadow heterogeneity, several cores should ideally be collected [53] as C_org accumulation can vary within a meadow due to e.g. edge effects [54] and water depth [55]. Indeed, the difference in CAR for the two Kristineberg cores (13–25 g m^-2 yr^-1) indicates within-meadow variability, which in this case may have been influenced by differences in sediment properties, such as mud content, between the two sampling sites [56]. Though, this was not assessed in this study and needs to be evaluated in more detail. As Västra Korsvik is located on shallow water depth and close to the Örekil river mouth in the interior of the fjord, the water discharge of the river could cause high turbidity (the high turbidity was also visually noticed during core sampling) and sediment resuspension preventing organic matter deposition and seagrass sediment stabilization. This might explain the shallow seagrass sediment accumulation (down to 11 cm) in the core. The influence of the river in Västra Korsvik is further seen by the relatively large proportion of terrestrial organic matter sources in the sediment (36%), likely derived from the outflow of the river [57] compared to the other sites in this study, although this site was generally low in C_org content.

The cumulative accumulation of C_org stocks showed a relatively small variation between cores with similar C_org stocks at 50 cm, ranging from about 4.6 to 5.9 kg C_org m^-2, which are comparable to previous assessments in the Skagerrak-Kattegat region [14,19,29,58]. The main difference in C_org stocks between the cores was due to the variation in seagrass sediment depth thickness resulting in a storage from 0.7 kg C_org m^-2 at Västra Korsvik (with a seagrass sediment depth of 11 cm) up to 20.6 kg C_org m^-2 in the Kristineberg 2 core (accumulated in 149 cm thick seagrass sediment). The high C_org storage in Kristineberg 2 is in line with what has been reported in a deep seagrass sediment core (20.6 kg C_org m^-2 in 120 cm thick sediment deposit) in the area [19]. This highlights the importance of information on total sediment thickness for evaluating areas of high C_org stocks as standardized depths, such as 0.5 or 1 m, which might lead to erroneous conclusions on the extent of the C_org stock. Furthermore, due to variation in CAR for the different sites in the Gullmar Fjord, the sedimentary C_org deposits have been accumulated over different time periods. Although Gåsö N had a relatively high C_org stock, the CAR was approximately 40% higher in Kristineberg in comparison. While both measurements are relevant to quantify, this shows that the stocks per unit area and the CAR will provide with different information crucial for blue carbon management (standing stock or rate of efficiency) and highlights the need to assess the rate of accumulation over time in order to estimate and compare the C_org sequestration capacity of Z. marina meadows.

The contribution of seagrass plant material to the sedimentary C_org pool is estimated to about 50% in general [4] although there is large variation among species. In Z. marina sediments and other smaller species, the seagrass plant contribution to the carbon stocks is usually lower in comparison to e.g. P. oceanica [59], which build up thick carbon- rich seagrass root-rhizome “mattes” [8] that constitute a large proportion of the sedimentary C_org pool. In line with other studies in Z. marina [24,44], we found that substantial part of the accumulated C_org stocks (up to 64%) was of macroalgae origin. This shows that the seagrass meadows are not only relevant sinks for autochthonous seagrass-derived plant material but also for other macrophytes, such as macroalgae, and support the hypothesis that macroalgae are important C_org doners to blue carbon habitats [5]. The high proportion of macroalgae in the sediment could be a direct response to the increase in filamentous algae in the Gullmar Fjord [60]. This has been related to eutrophication, which a major environmental problem of the Swedish Skagerrak coast [61,62] and have caused (together with food web cascades) substantial decline in seagrass meadows [15,17,18]. Although eutrophication is of concern for the marine environment and the seagrass ecosystem health, this indicates that high macroalgae growth could increase the C_org accumulation rate in the seagrass meadows. However, there is clearly an upper limit for the seagrass meadows’ capacity to sequester macroalgae biomass as a high production of macroalgae can result in seagrass smothering and overgrowth with adverse effects on the seagrass ecosystem and C_org storage potential [63]. The yearly mean (± SD) uptake of 7.1 ± 3.3 g C_org m^-2 (ranging from 4.8 to 11.9 g C_org m^-2) of macroalgae material shows the seagrass meadows’ capability as filters of the coastal zone by tapping and storing organic matter of allochthonous origin [4]. Given the extensive distribution of both perennial and annual filamentous macroalgae in seagrass meadows of the Swedish Skagerrak coast and the fact that the carbon and nitrogen stable isotopes cannot distinguish between algae species, part of the macroalgae contribution to the sedimentary C_org pool is likely from species growing within the meadows, including Ectocarpus sp., Ceramium sp. and Ulva sp. [18], although the amount of algae drifting from elsewhere, such as F. serratus and Furcellaria lumbricalis could also be substantial.

The Swedish Skagerrak coast has experienced a large reduction of seagrass area, with an average loss of 60% since the 1980s [15,16]. However, the loss rate for the Swedish Skagerrak regions has been widely different, with the Lysekil municipality area (where the Gullmar Fjord is situated) experiencing only a slight decrease in seagrass coverage (2%) between the 1980s and early 2000s. In contrast, other areas have suffered major seagrass regressions; for example Kungälv (located about 40 km south of the Gullmar Fjord) has experienced a catastrophic total decline of 82% (648 ha) [15] during this period, and with further decline being reported during the 2000s [64]. This could indicate that the loss of seagrass areas (estimated to 1069 ha) has reduced the meadows’ capacity to sequester carbon by 150 Mg C_org yr^-1 for the whole Swedish Skagerrak coast, and the region of Kungälv alone with 92 Mg C_org yr^-1. Furthermore, as seagrass meadows disappear, this does not only impair the carbon sequestration function but also risk sedimentary C_org stock erosion [65–67]. Given the sedimentation rates in the Gullmar Fjord area is slow (less than 2 mm yr^-1, which is below the average seagrass SAR [68]), and the thickness of the sediment deposits (from about 60 to at least 150 cm), carbon stocks in this region have been accrued over a long period of time and therefore a loss of seagrass areas would cause erosion of ancient C_org and potentially have counteracted centuries of carbon sequestration. However, the eroded C_org could avoid remineralization (and therefore not emitted as CO₂) if deposited in other areas where its preserved, e.g. the deeper part of the fjord [69].

The seagrass CAR in this study is similar to those reported for other Z. marina sites [22,23,43,44], although higher values (up to 60 g C_org m^-2 yr^-1) have also been reported [24,42]. The CAR in this study, and for Z. marina meadows in general, is however considerably lower compared to other species and regions (see e.g. [3,10–12,70]). For instance, the Mediterranean seagrass Posidonia oceanica, which has shown to have the highest CAR for seagrasses worldwide can have an accumulation rate of up to 249 g C_org m^-2 yr^-1 [10], but Z. marina meadows are still relevant carbon sinks for climate change mitigation, especially considering the low greenhouse gas (i.e. methane) emission from these ecosystems [71]. The low sedimentation and CAR found in cold-temperate Z. marina meadows could be related to the strong seasonality in these regions, which influences seagrass biomass growth and production [72,73] and carbon storage [29]. During the winter season (December to March), the seagrass shoot biomass is reduced (in some cases the aboveground is completely detached) [74] leading to a lower primary production [75] and presumably less seston filtering and trapping within the canopy [76]. Furthermore, storms tend to increase during autumn (September to November) and with a low shoot biomass to protect the sediment from the sudden increased hydrodynamic forces, this could lead to resuspension and erosion of surface sediments [77].

This study adds to the growing literature of seagrass C_org sink capacity, and we found that the cold-temperate Z. marina carbon sinks of the Gullmar Fjord area store large C_org stocks that have been slowly accumulated. The high accumulation of macroalgae biomass in the sedimentary C_org pool shows that organic matter sources besides the seagrass plants are important for blue carbon storage of these ecosystems. We also highlight the importance of assessing the total sediment deposits when quantifying C_org storage as the main difference in C_org stocks was related to the large difference in seagrass sediment thickness.

Supporting information

S1 Text.

Fig A. Sediment depth profiles down to ~50 cm showing sediment density, Corg density, δ13C isotopic values and percent Corg in the different sites. Table A. The proportion of Corg sources (mean ± SD) to the surface layer of the seagrass sedimentary pool. The estimated proportions are based on stable isotopes (δ13C and δ15N) analyzed with the Simmr package in R.

https://doi.org/10.1371/journal.pclm.0000099.s001

(DOCX)

S1 Data. Data.

https://doi.org/10.1371/journal.pclm.0000099.s002

(XLSX)

Acknowledgments

We wish to thank Petter Hällberg, Beat Gasser, Isabelle Levy and Carina Johansson for helping with laboratory analysis. We are also grateful for the constructive comments and feedback given by the three anonymous reviewers.

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Figures

Abstract

Introduction

Methods

Study site

Sediment sampling and analysis

Quantification of Corg sequestration rates and stocks

Estimate of contribution of potential Corg sources to the seagrass meadow Corg storage

Results

Discussion

Supporting information

S1 Text.

S1 Data. Data.

Acknowledgments

References

Quantification of C_org sequestration rates and stocks

Estimate of contribution of potential C_org sources to the seagrass meadow C_org storage