ARTICLE https://doi.org/10.1038/s41467-019-08842-6 OPEN Role of carbonate burial in Blue Carbon budgets V. Saderne 1, N.R. Geraldi 1, P.I. Macreadie2, D.T. Maher 3, J.J. Middelburg 4, O. Serrano 5, H. Almahasheer 6, A. Arias-Ortiz 7, M. Cusack1, B.D. Eyre8, J.W. Fourqurean 9, H. Kennedy10, D. Krause-Jensen11,12, T. Kuwae13, P.S. Lavery5, C.E. Lovelock14, N. Marba 15, P. Masqué 5,7,16, M.A. Mateo5,17, I. Mazarrasa18, K.J. McGlathery19, M.P.J. Oreska19, C.J. Sanders20, I.R. Santos 20, J.M. Smoak 21, T. Tanaya13, K. Watanabe 13 & C.M. Duarte 1 1234567890():,; Calcium carbonates (CaCO3) often accumulate in mangrove and seagrass sediments. As CaCO3 production emits CO2, there is concern that this may partially offset the role of Blue Carbon ecosystems as CO2 sinks through the burial of organic carbon (Corg). A global collection of data on inorganic carbon burial rates (Cinorg, 12% of CaCO3 mass) revealed global rates of 0.8 TgCinorg yr−1 and 15–62 TgCinorg yr−1 in mangrove and seagrass ecosys- tems, respectively. In seagrass, CaCO3 burial may correspond to an offset of 30% of the net CO2 sequestration. However, a mass balance assessment highlights that the Cinorg burial is mainly supported by inputs from adjacent ecosystems rather than by local calcification, and that Blue Carbon ecosystems are sites of net CaCO3 dissolution. Hence, CaCO3 burial in Blue Carbon ecosystems contribute to seabed elevation and therefore buffers sea-level rise, without undermining their role as CO2 sinks. 1 KingAbdullah University of Science and Technology (KAUST), Red Sea (RSRC) and Computational Bioscience (CBRC) Research Centers, Thuwal 23955- 6900, Saudi Arabia. 2 School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Geelong, Victoria 3216, Australia. 3 Southern Cross Geoscience, Southern Cross University, Lismore, New South Wales 2480, Australia. 4 Department of Earth Sciences, Utrecht University, Vening Meineszgebouw A, Princetonlaan 8a, Utrecht 3584, The Netherlands. 5 School of Science and Centre for Marine Ecosystems Research, Edith Cowan University, 270 Joondalup Drive, Joondalup, West Australia 6027, Australia. 6 Department of Biology, College of Science, Imam Abdulrahman Bin Faisal University (IAU), Dammam 31441-1982, Saudi Arabia. 7 Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Bellaterra, Barcelona 08193, Spain. 8 Centre for Coastal Biogeochemistry, School of Environment, Science and Engineering, Southern Cross University, Lismore, New South Wales 2480, Australia. 9 Department of Biological Sciences, Center for Coastal oceans Research, Institute of Water and Environment, Florida International University, Miami 11200 SW 8th Street, Miami, Florida 33199, USA. 10 School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, Wales LL59 5AB, UK. 11 Department of Bioscience, Aarhus University, Vejlsøvej 25, Silkeborg 8600, Denmark. 12 Arctic Research Centre, Department of Bioscience, Aarhus University, Ny Munkegade 114, Building 1540, Århus C 8000, Denmark. 13 Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1 Nagase, Yokosuka 239-0826, Japan. 14 School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia. 15 Department of Global Change Research, IMEDEA (CSIC-UIB), Institut Mediterrani d’Estudis Avançats Miquel Marquès 21, Esporles (Illes Balears) 07190, Spain. 16 Oceans Institute and School of Physics, University of Western Australia, 35 Stirling Highway, Crawley, West Australia 6009, Australia. 17 Centro de Estudios Avanzados de Blanes, Consejo Superior de Investigaciones Cientificas, Blanes 17300, Spain. 18 Environmental Hydraulics Institute “IH Cantabria”, C/Isabel Torres No 15, Parque Científico y Tecnológico de Cantabria, Universidad de Cantabria, Santander 39011, Spain. 19 Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22904, USA. 20 National Marine Science Centre, School of Environment, Science and Engineering, Southern Cross University, Cos Harbour, New South Wales 2450, Australia. 21 University of South Florida, St. Petersburg, Florida 33701, USA. Correspondence and requests for materials should be addressed to V.S. (email: vincent.saderne@kaust.edu.sa) NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 M angrove forests and seagrass meadows have the capacity Results to elevate the seabed through the accretion of inorganic Global disparities in Blue Carbon sediments. CaCO3 supports and organic particles1 at global rates of ~0.5 and ~0.2 an important part of sediment accretion rates (SARs) in seagrass −1 cm yr , respectively1. Sediment accretion in mangrove forests ecosystems, although with large geographical disparities and a and seagrass meadows leads to the sequestration of organic car- non-normal distribution (Shapiro–Wilks test, p < 0.001). Indeed, bon (Corg)2,3 originating from within and outside of the vegetated in 40% of global locations, the CaCO3 concentration was under ecosystem4. Although mangroves and seagrass ecosystems occupy 10% dry weight (DW), whereas in 28% of locations the CaCO3 only a small fraction of the total coastal area (< 2%), they con- content exceeded 80 %DW (see Supplementary Figure 1a). tribute 10% and 25% to the yearly Corg sequestration in the Overall, the median (interquartile range: IQR) global concentra- coastal zone1,5, respectively. Recognition of mangrove and sea- tion of CaCO3 in seagrass meadow sediments was 61 (56) %DW grass meadows, together with saltmarshes, as sites of intense Corg (mean ± SE of 54 ± 7). burial led to the formulation of Blue Carbon strategies to mitigate In mangrove forests, we observe a large difference between the and adapt to climate change, through conservation and restora- mean (± SE) and the median (IQR) CaCO3 concentration: 21 ± tion of these ecosystems1,6–8. The focus on Blue Carbon has 11% and 3 (31)%, respectively. This is explained by the strong provided substantial impetus to assess sediment Corg concentra- non-normal distribution between the eight study locations tions and burial rates in vegetated coastal ecosystems, which examined, including a group of five locations with < 5 %DW recently have been widely reviewed9. CaCO3 in their sediments and three locations with CaCO3 Corg generally represents a minor fraction (2–3%) of buried contents between 20 and 75 %DW (Shapiro–Wilks test, p < 0.001, material within mangrove and seagrass sediments10,11 (although see Supplementary Fig. 1b). Converted into Cinorg concentrations this is highly variable12), the rest being siliciclastic and carbonate (after normalization for the sediment bulk density), we obtain particles. A global assessment of the concentration of inorganic median (IQR) Cinorg concentrations in seagrass and mangrove carbon concluded that Cinorg can exceed Corg concentration in sediments of 59 (66) and 1 (21) mgCinorg cm−3, respectively seagrass sediments13. Seagrass and mangrove plants do not calcify (means ± SE of 63 ± 11 and 35 ± 17 mgCinorg cm−3) (Fig. 2a). per se; however, they provide habitats for an abundant associated Using the median SARs in seagrass and mangrove ecosystems calcifying fauna and flora (e.g., crabs, sea stars, snails, bivalves, compiled in this study (0.22 and 0.23 cm yr−1, respectively; Fig. 2b), calcified algae, foraminifera), whose shells and skeletons may be we estimate median (IQR) Cinorg burial rates in seagrass and deposited and buried in the sediment along with the plant litter, mangrove ecosystems of 87 (154) and 6 (207) gCinorg m−2 yr−1, and the organic and inorganic particles imported from adjacent respectively (means ± SE of 182 ± 94 and 90 ± 43 gCinorg m−2 yr−1) ecosystems. (Fig. 2c, Fig. 3). These values correspond to vertical accretion rates of Counterintuitively, CaCO3 production represents a source of CaCO3 of the order of 0.1 and 0.001 cm yr−1 in seagrass and CO2 to the atmosphere, as calcification produces CO2 with a ratio mangrove ecosystems, respectively. Our mean SAR values agree with of ~0.6 mol of CO2 emitted per mol of CaCO3 precipitated14. This previously reported global values1,3. However, our new estimates of has led to the argument that high CaCO3 burial may partially burial rates are lower than the previous, indirect median estimate offset CO2 sequestration associated with Corg burial in some of Cinorg burial rate of 108 gCinorg m−2 yr−1 (mean ± seagrass meadows and mangrove forests15. However, there are SE of 126 ± 31 gCinorg m−2 yr−1) reported by Mazarrasa et al.13. several caveats that affect these arguments and render inferences on the role of Blue Carbon ecosystems as net CO2 sinks or sources inconclusive13,16, based on the comparison of Corg and Global annual burial rates of Cinorg. Scaling up to the global Cinorg sediment burial rates. To date, very few articles report the seagrass coverage (150,000–600,000 km2)9, the annual burial rate burial rates of CaCO3 in mangrove and seagrass ecosystems15–17, of Cinorg ranged from 13 to 52 TgCinorg yr−1 for the twentieth and the role of CaCO3 burial in sediments and CO2 emissions century (Table 1). Partitioning between tropical and non-tropical depends on the balance between dissolution and production. If seagrass meadows as in Mazarrasa et al.13 showed that 90% of the CaCO3 dissolution equals local calcification, then the burial of global Cinorg burial occurs in the tropics (Table 1). In seagrass CaCO3 is supported exclusively by allochthonous inputs and is meadows, our estimates of global burial of Cinorg are equivalent to neutral in terms of CO2 emissions or sequestration. If dissolution 31–55% of the available estimates of contemporary Corg burial exceeds local calcification, then CaCO3 dynamics add to the CO2 rates (48–112 TgCorg yr−1)1,7, depending on the estimated global sink capacity of Blue Carbon ecosystems, even if CaCO3, which seagrass coverage considered. If all buried CaCO3 is locally pro- must be subsidized from allochthonous sources, is buried in the duced (i.e., of autochthonous origin), the burial rates of Cinorg in sediments. Only if CaCO3 dissolution is lower than local calcifi- seagrass meadows would represent emissions of 8–37 TgC yr−1 to cation does CaCO3 burial result in CO2 emissions. the atmosphere and thus would offset their role as CO2 sinks Here we address the current gap in global estimates of Cinorg through the sequestration of Corg by ~17–33%. burial in seagrass and mangrove ecosystems by providing first The extent of global mangrove coverage yields a median burial estimates of contemporary (last century) Cinorg burial rates. We rate of 0.8 TgCinorg yr−1 (mean of 13 TgCinorg yr−1) (Table 1). This rely on a compilation and analysis of data on sediment chron- value should be considered as a first-order estimate because of the ologies (i.e., including radiometric dating of sediment cores with scarcity of data available on Cinorg burial rates in mangroves and 210Pb) and C inorg concentrations from around the world (Fig. 1). because of the non-normal distribution between CaCO3-rich and We compare burial, calcification and dissolution rates in three CaCO3-poor mangrove sediments (Supplementary Figure 1b). locations where most of the carbon mass balance terms were When comparing with the global Corg burial rates estimate of 31 available. We then address the role of CaCO3 burial in CO2 TgCorg yr−1 3, the median Cinorg burial rates would correspond to emissions by resolving the source of the CaCO3 buried in seagrass a negligible reduction of net atmospheric CO2 uptake. However, meadows as either allochthonous or autochthonous (i.e., from assuming that all sedimentary CaCO3 was produced in situ, the associated flora and fauna). We conclude that the high amounts Cinorg burial rates can largely outweigh Corg burial in CaCO3-rich of CaCO3 found in Blue Carbon sediments can not be converted mangroves. For example, the Cinorg burial rate corresponds to into CO2 emissions. 10–20 times the Corg burial rate in the Arabian Peninsula17–19. 2 NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 ARTICLE Fig. 1 World map of sediment cores locations. Brown circles: mangrove cores locations; blue: seagrass cores locations; yellow: seagrass cores non-dated but with inorganic carbon content measured13 Discussion Similarly, in Shark Bay, the burial of Cinorg is four times higher CaCO3 burial in Blue Carbon ecosystems is the balance between than the independently reported net calcification rate22 (Table 2). inputs (autochthonous and allochthonous) and losses (dissolution This again could require large allochthonous carbonate inputs. and export). Assessments of the mass balance of CaCO3 in sea- In Florida Bay, the low ratio between Corg and Cinorg con- grass meadows are few and none have been reported, to our centration in the sediment (g cm−3) implied that seagrass mea- knowledge, in mangrove forests. For seagrass ecosystems, we dows may be a net source of CO2 to the atmosphere15. However, assessed the balance between calcification, dissolution and burial such assessment requires consideration of the full carbon mass of CaCO3 in three locations: the Balearic Islands, Spain20,21, balance, including accounting for allochthonous inorganic carbon Shark Bay in Western Australia22 and Florida Bay, USA23,24 inputs and the balance between calcification and dissolution in the (Table 2). meadows. The contemporary Cinorg burial rates in Florida Bay are The most comprehensive assessment of seagrass carbon budgets is approximately ninefold higher than the global median, whereas that reported for a Mediterranean Posidonia oceanica meadow at median SAR is about fourfold higher than estimated globally, in Magalluf (Mallorca Island, Spain)20,21,25,26. In this meadow, Barrón an area where 80% of the sediment dry mass is composed of et al.21 estimated a net CO2 uptake by primary production of 8.4 gC CaCO3. However, attempts to assess the gross or net calcification m−2 yr−1. This estimate was corroborated by the Corg burial rate, rates in the area yielded values one and two orders of magnitude estimated independently, at 9 ± 2 gCorg m−2 yr−1 27. Barrón et al.21 lower than the estimated CaCO3 burial rates (Table 2)23,24. In also estimated net calcification rates of 51 gCaCO3 m−2 yr−1, cor- contrast, past geological work in the Bay has suggested that it is a responding to 6 gCinorg m−2 yr−1. This amount of calcification would net producer of CaCO328. It is likely to be that some areas within result in a CO2 emission of 3.6 gC m−2 yr−1 (0.6-fold the net cal- this large Bay act as sources of CaCO3 and some others as sinks, cification14). The CO2 emission by calcification therefore represents helping explain the discrepancy between reported production and an offset of 40% of the CO2 uptake from net primary production burial estimates. Hence, internal redistribution of CaCO3 pro- (thereby yielding a total CO2 sequestration of 4.8 gC m−2 yr−1 21). duction within Florida Bay needs to be considered when drawing However, the Cinorg burial rate in this meadow is estimated here at inferences on the role of seagrass meadows from sediment 226 gCinorg m−2 yr−1. This is two orders of magnitude greater than composition. the net calcification rate of 6 gCinorg m−2 yr−1 21(Table 2). This These three example locations are in areas close to coral implies that about 90% of the CaCO3 burial in this seagrass meadow reefs and/or terrestrial lithogenic sources of CaCO3. We could not must be supported by allochthonous inputs. Therefore, calculation of find estimates of calcification rates (net or gross) in areas the CO2 sequestration by comparing Corg and Cinorg burial rates or without external sources of CaCO3. The discrepancies between stocks would have concluded that this meadow is a strong source of calcification rates and burial rates in the three example locations CO2, whereas estimates of calcification rates and net primary pro- could indicate that an important fraction of CaCO3 burial duction concludes that it is a sink (as confirmed independently (> 90%) is supported by CaCO3 produced elsewhere and trapped through air–sea flux measurements26). in the seagrass sediments. This conclusion is consistent with NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications 3 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 a 140 b 0.9 c 600 0.8 550 120 0.7 500 100 300 Cinorg concentration 0.6 Cinorg burial rate g m–2 yr–1 250 cm yr−1 80 mg cm–3 0.5 SAR 0.4 200 60 0.3 150 40 0.2 100 20 0.1 50 0 0.0 0 Seagrass Mangrove Seagrass Mangrove Seagrass Mangrove Fig. 2 Sediment cores data. a Inorganic carbon (Cinorg) concentration, b sediment accumulation rates (SAR), and c Cinorg burial rates. The x represents the mean. Bars are the first and last quartile 800 8 700 600 Cinorg burial rates 500 g m–2 yr–1 400 2 2 20 7 300 8 4 7 4 200 1 1 2 1 1 100 1 2 1 3 5 3 2 1 3 2 1 3 0 Ea sc lan a, ia Ar uth ns au str a lia W W n I nd ust lia Ba va ny us lia es ha S ay ico pi kai d, in ch llis nd us lia m Al let, ust lia tn s y s a up ke us lia Q uri Ba Au bia ar I e s ia or u ia ic in us ia nl n us lia s G id M ico N ia e d Ar a A So Gu Flo us ia h Sa a lia Vi les i Ar A , G , Ja ly H I ,S A d i ot en Ba , Au rali re pa ab W lan di ali ha Ba di A S th I Is sul tral So uee , S Au ral a d S Ka ok slan pa G ess Lak , Au tral st hia ds US ct , A ab l a b an tra de sla , A tra ar ba A ra ay a sla , A ra in , A tra in La , A tra le pe , A tra , A ra ut lf, rid tra W t S ulf, a B ex Ea n or n, x J rk y, ra t S rk au , U si do It ew n s , A a W u ,U ia Fl ata Me Q ea d, st ue en y st ia st st d S lan Au e c n, Ea e Is n, Yu ta h l R k wi th ca ar n llit ut tra roo ar t or u N st Y So n b D ic e W ab n el h C chi R ut D Ar or So N in h ut e H So Seagrass Mangrove Fig. 3 Inorganic carbon burial rates in all locations. Mean Cinorg burial rates in all locations in sediment cores for seagrass meadows and mangrove forests, organized from low to high latitudes. Bars are the SE. Labels are the number of cores per location Table 1 Median (mean) global Cinorg burial rates for seagrass meadows and mangrove forests considering one, and, for seagrass, two world regions (tropical and higher latitudes) Burial rate, (TgCinorg yr−1) Global Tropical Higher lat. Sum Seagrass This study 13(27)–52(109) 14(41)–57(163) 1(3)–5(14) 15(43)–62(177) Mazarassa et al.13 19(28)–65(79) Mangrove This study 0.8(12) comparable Cinorg concentrations within and outside seagrass marine plants release organic compounds and oxygenate meadows, whereas, in contrast, Corg concentrations are higher in the sediments during the day, promoting microbial aerobic seagrass sediments13. A large role of Cinorg import is also con- remineralization of organic matter, thereby increasing sedimen- sistent with the large CaCO3 export from coral reefs to adjacent tary respiratory CO229,30 and/or stimulating the re-oxidation of waters, equivalent to 25–50% of the CaCO3 production, pre- reduced metabolites. These processes result in the release of dominantly to reef lagoons27, where seagrass meadows and strong acids (e.g., H2SO4, HNO3)31–33, which leads to CaCO3 mangroves often grow. Mangroves, seagrass and saltmarsh eco- dissolution in the sediment34,35 (although re-precipitation can systems are likely to be sites of net carbonate dissolution. Roots of occur34). 4 NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 ARTICLE Table 2 Burial rates of CaCO3 compared to calcification rates in seagrass ecosystems Community production rate of Community net calcification rate Sediment CaCO3 gCaCO3 m−2 yr−1 gCinorg m−2 yr−1 gCaCO3 m−2 yr−1 gCinorg m−2 yr−1 %CaCO3 gCaCO3 m−2 yr−1 gCinorg m−2 yr−1 Florida Bay, USA 62623,24 75 1825 2.2 82 ± 2 4792 ± 756 756 ± 91 Balearic Islands, Spain 6820 8 5121 6 81 ± 3 1886 ± 214 226 ± 30 West Shark Bay, 375 ± 6222 45 ± 7 29522 35 60 ± 5 1240 ± 232 149 ± 30 Australia Comparison between seagrass-associated community production rate of carbonate (obtained from standing stock assessments and leaves or calcifiers turnover rates) and community net calcification rates (balance between calcification and dissolution, calculated from variations of total alkalinity) from the literature, and carbonate burial rate in three locations with carbonate-rich sediments Dissolution of CaCO3 might also be influenced by the CO2 DW in the presence of both allochthonous sources was less than system in the water column of Blue Carbon ecosystems. would be expected if these variables were additive. The presence/ Respiration and photosynthesis of the flora and fauna, together absence of coral reefs and lithogenic sources accounted for 36% of with sediment redox processes in seagrass and mangrove eco- the variation in CaCO3, whereas the random variables (study, systems, strongly influence the chemistry of the water column, lithology grouping and marine province) accounted for 54% of generating large diel amplitudes of the saturation state for CaCO3 the variation in CaCO3 (see Methods for model description). (Ω) with a tendency towards dissolution or the reduction of Mangrove sediment samples showed a similar pattern to the calcification at nighttime, amplified at low tide36–40. The dis- seagrass meadows and the presence of allochthonous sources had solution of allochthonous CaCO3 in carbonate platform areas, a marginally significant positive effect on the amount of CaCO3 caused directly or indirectly by metabolism of the marine vege- in the sediment (t-value = 4.29, df = 1.81, p = 0.0596). The pre- tation and associated biota, leads to a reduction in pCO2 through sence/absence of a CaCO3 source accounted for 71% of the var- the release of fossilized total alkalinity. This sink of atmospheric iation of in CaCO3 within mangrove sediments, whereas the CO2 should be incorporated into the Blue Carbon framework. A random variables accounted for 20% of the variation in CaCO3. recent assessment considers alkalinity addition through the dis- In testing for biases of outlying cores and studies, we found that solution of allochthonous carbonate as a very effective geo- one study from Western Florida had an outlying data point that engineering approach to remove atmospheric CO2 and mitigate disproportionality skewed the results. The study from Western climate change41,42. Florida had relatively low CaCO3 but did have an allochthonous Similarly, saltmarshes are not known to host high levels of source of CaCO3. When this study was removed from the ana- calcifying organisms but can accumulate CaCO3 from alloch- lysis, the presence of an allochthonous source became significant thonous sources. In arid tropical saltmarshes of the Western (t-value = 7.92, df = 4.16, p = 0.0012). This highlights the need Arabian Gulf, dominated by succulent shrubs, a concentration of for more studies in mangrove sediments to determine the global CaCO3 of 57 ± 8% in sediments and a contemporary burial rate of influence of allochthonous sources on CaCO3 content. Cinorg of 100 ± 15 gCinorg m−2 yr−1 (mean ± SE) were found17. In In seagrass meadows, the median (IQR) Cinorg burial rate a temperate saltmarsh of the Western Scheldt estuary in the found in areas where no allochthonous sources were identified Netherlands, a concentration of CaCO3 of 14 ± 1% and a high was 1 (13) gCinorg m−2 yr−1 (mean ± SE of 8 ± 4), only 1.1% of the contemporary burial rate of 467 ± 99 gCinorg m−2 yr−1, mostly global median. This contrast is consistent with our hypothesis due to high SAR (1.1 ± 0.3 cm yr−1), were measured43. Yet, this that much of the Cinorg buried in seagrass and mangrove sedi- does not imply that CaCO3 dynamics have a negligible role in ments is allochthonous. It explains the non-normal distribution saltmarsh carbon budgets, as they may still act as sites of net of CaCO3 concentrations observed in sediments of seagrass and dissolution of CaCO3, adding to the removal of CO2 associated mangroves (Supplementary Figure 1), and indicates that the with Corg burial. A dissolution rate of 24–96 gCinorg m−2 yr−1 was import of CaCO3 from carbonate-forming ecosystems or adjacent estimated in the sediment of the saltmarshes of the Eastern karstic areas is the norm27. The global burial rate of Cinorg in Scheldt estuary, corresponding to ~85% of the Cinorg burial rate44. seagrass meadows is between a third to a half of their Corg burial To further examine the conclusion that Blue Carbon ecosys- rate1,7, whereas for mangroves our first estimate of global Cinorg tems are sites of substantial allochthonous CaCO3 deposition, burial rates is only 3% of the Corg burial rate3. If the buried based on existing mass balances for Blue Carbon sediments, we CaCO3 and Corg in seagrass sediments were produced entirely examined (qualitatively) the relationship between the CaCO3 % in situ, Cinorg burial would offset up to a third of CO2 seques- DW in sediments and the presence/absence of sources of CaCO3 tration through Corg burial, particularly in tropical seagrass eco- adjacent to the coring locations, including coral reefs and ter- systems where ~90% of the global Cinorg burial occurs. However, restrial lithogenic sources of CaCO3 (Fig. 4, see dataset in Sup- imbalances between production, dissolution and burial, and the plementary Information). Seagrass and mangrove ecosystems observation of much higher CaCO3 concentrations in sediments without potentially large adjacent allochthonous CaCO3 sources near lithogenic formations and coral reefs, suggest that, where have a remarkably lower median (IQR) sediment CaCO3 content present, allochthonous CaCO3 inputs are substantial and support of 4 (15) and 1 (1) %DW (means ± SE of 11 ± 4 and 1.7 ± 0.8 % most of the net CaCO3 burial. DW), respectively, compared with59 (51) and 61 (27) %DW Locally, despite supporting significant CaCO3 burial, Blue (means ± SE of 56 ± 5 and 53 ± 16 %DW) when at least one Carbon ecosystems may be sites where imported CaCO3 dis- allochthonous CaCO3 source was present (Fig. 3). For sediments solves, strengthening rather than weakening the capacity of these in seagrass meadows, the presence of coral reefs (t-value = 4.68, ecosystems to sequester CO2. Whereas there is emphasis on df = 48.5, p < 0.0001) and lithogenic sources (t-value = 4.76, df = apportioning the sources of autochthonous and allochthonous 57.3, p < 0.0001) increased the amount of CaCO3 in the sediment. Corg in Blue Carbon sediments (up to 50% of the buried Corg)4,9, However, there was a significant interaction between these factors determining the sources of CaCO3 in Blue Carbon sediments is (t-value = − 3.29, df = 53.2, p = 0.0018), because the CaCO3 % just as important, to resolve the role of vegetated coastal NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications 5 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 a 100 b 14 9 12 90 80 3 70 CaCO3 %DW 60 50 23 40 30 20 10 5 0 No sources Lithogenic Coral reef Coral reef No sources At least only only and Lithogenic one source Seagrass Mangrove Fig. 4 Allochthonous sources and inorganic carbon in sediments. a %DW of carbonates (CaCO3) in seagrass sediments depending on the presence of potential allochthonous sources (lithogenic and/or coral reefs). All data distributions for locations with allochthonous sources are significantly different to the distributions for locations without allochthonous sources (Mann–Whitney U-tests, all p < 0.001). b %DW CaCO3 in mangrove sediments with and without allochthonous sources (coral reef and lithogenic source). Number on top of the box plots indicate the number of locations. The x represents the mean. Bars are the first and last quartile ecosystems as CO2 sinks and, hence, their potential to support sediments, respectively. To obtain the CaCO3 or Cinorg concentrations needed to climate change mitigation. The current focus on Corg budgets in calculate Cinorg burial rates, we used the database of Mazarrasa et al. 13, which was the most recent exhaustive compilation of sediment cores from Blue Carbon vegetated coastal ecosystems needs to be augmented with inte- habitats, for data on CaCO3 in seagrass sediments. We also contacted experts in grative assessments of organic and inorganic carbon fluxes and Blue Carbon studies (published studies using cores from Blue Carbon habitats) for budgets, including both allochthonous and autochthonous inputs. unpublished CaCO3 sediment concentration data (see data and references in Sup- Moreover, these assessments must consider the sources and fate plementary Data 1). In total, we compiled 42 and 53 210Pb dated cores with CaCO3 of carbon exchanged between Blue Carbon and adjacent ecosys- content in mangrove and seagrass ecosystems, respectively (see PRISMA checklist and flow diagram48 in Supplementary Note 1). tems, as Blue Carbon ecosystems export important amounts of The SARs (cm yr−1) from the literature were re-calculated according to the their organic production45–47 but also import significant amounts constant flux–constant sedimentation model49, to have a coherent and comparable of CaCO3 and organic matter from adjacent sources. A com- dating system between all cores. The CaCO3 concentration (% sediment DW) was parison of paired vegetated and unvegetated sediment CaCO3 % calculated as the mean between all slices younger than 1900, for cores with the contemporary 210Pb chronologies. The Cinorg concentration in sediment (gCinorg m−3) DW showed that vegetated and adjacent unvegetated sediments was calculated from the dry bulk density (g m−3) and the percentage of CaCO3 have similar carbonate concentrations, both using standard content (using sediment DW), considering a mass ratio of 12% carbon in CaCO3. The parametric statistics (general linear model (GLM), t-value = 1.32, Cinorg burial rate (gCinorg m−2 yr−1) was then calculated as the product of the SAR df = 83.1, p = 0.191) and meta-analysis (z-value = 0.88, p = and the Cinorg concentration for each sediment core. Cores with negligible content of CaCO3 were also included in the calculation (see Supplementary Figure 1). 0.379; Supplementary Fig. 2A,B), which also showed no evidence All cores from the same site or area and with similar presence or absence of for reporting bias (all points within the 95% confidence lines of allochthonous sources of CaCO3 (see below) were treated as replicates for a global the funnel plot, Supplementary Fig. 2C. This provides further location and averaged for the analysis (geologic grouping). For seagrass, the 51 support to the hypothesis that much of the carbonate buried in cores dated with 210Pb were grouped into 17 locations (Figs. 2, 3). For mangroves, we compiled a total of 42 cores dated with 210Pb in 8 locations (Figs. 2, 3). Seagrass vegetated coastal sediments derives from allochthonous sources locations ranged from tropical to sub-arctic locations, with 50% of estimates rather than being produced within the habitat. derived from tropical and subtropical locations and 50% from higher latitudes. Inorganic carbon burial in Blue Carbon ecosystems has been Mangrove sediment derived mostly from subtropical locations (seven out of eight overlooked, with the rates compiled here representing the first locations), particularly in Australia and the Arabian Peninsula (Supplementary direct estimates reported in the literature. These estimates con- Figure 2). firm that seagrass ecosystems, and to lesser extent mangrove ecosystems, are intense sites of CaCO3 burial, supporting sedi- Determination of the influence of allochthonous sources of CaCO3. We ana- lysed the influence of the presence/absence of proximity of coral reefs and con- ment accretion. CaCO3 burial is a fundamental process sup- tinental surface lithology (qualitative data), as potential allochthonous sources of porting the role of Blue Carbon ecosystems in climate change CaCO3 in seagrass and mangrove sediments (in %DW) (see dataset in Supple- adaptation, which is underpinned by their capacity to rapidly mentary Data 1). For seagrass, we expanded our dataset by including CaCO3 accrete sediments, reducing relative SLR by raising the concentrations from 264 cores compiled by Mazarrasa et al.13, reaching a total of 341 cores with measured CaCO3 %DW. seafloor1,17. We estimated the presence/absence of coral reefs using the map of the global distribution of warm-water coral reefs compiled by the UNEP-WCMC50 and the Methods presence/absence of nearby lithogenic sources using the global lithology map of Hartmann and Moosdorf51 and the world soil map of the FAO/UNESCO (http:// Calculation of the Cinorg accretion rate. We searched the peer-reviewed literature www.fao.org/soils-portal/en/). The coring locations were associated with climate for data on sediment cores dated with 210Pb, including CaCO3 or Cinorg con- regions following the Köppen–Geiger classification system52. centration in seagrass and mangrove sediments. Search terms on Google Scholar were seagrass OR mangrove AND 210Pb OR SAR OR sediment accretion rate. We then searched returned articles that contained data on SAR and CaCO3 or Cinorg Statistical analysis. All data distributions were tested for normality to determine data. We found only one study presenting CaCO3 content in a dated sediment core. the most reliable central tendency measured with Shapiro–Wilks normality test However, we found 15 and 22 studies with SAR for seagrass and mangrove (Statistica, Dell Software). None of the datasets of SAR, Cinorg concentration, Cinorg 6 NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 ARTICLE burial rate or CaCO3 %DW were normally distributed (all p < 0.05). We therefore Calculation of global yearly burial rates of Cinorg. The global annual burial of chose to use the median (IQR) as the most appropriate description of central inorganic carbon (TgCinorg yr−1) in seagrass meadows was calculated as the pro- tendency. Traditional meta-analysis tools, which calculate effect sizes to standar- duct of the global median Cinorg burial rates and the estimated global seagrass area, dize the difference between control and experimental treatments, thereby allowing which ranges from 150,000 to 600,000 km29. We also calculated the global annual comparison among disparate response variables and weighting to account for burial of Cinorg as the sum of separate calculations for tropical and arid climates unequal variance among studies, could not be used for this analysis for multiple and meadows at higher latitude climates. Median Cinorg burial rates were calculated reasons. These reasons include that the question posed and the studies available did for tropical (core locations with tropical and hot desert climates) and non-tropical not include experimental designs with paired control and experimental plots areas (temperate, continental and polar climates) and multiplied by the global required for effect size calculations, that there was a single response variable seagrass cover range under the assumption that 2/3 of the seagrass area is in the facilitating direct comparison and data integration, and, most importantly, that we tropical and subtropical zone13. The global annual burial of inorganic carbon used the raw data for each core. Instead, we ran a statistical test using a mixed effect (TgCinorg yr−1) in mangroves was calculated as the product of the global median GLM to determine the effect of coral reefs and lithogenic sources on the CaCO3 % Cinorg burial rates and the estimated global mangrove cover of 137,760 km262. DW of the sediment. For sediments within seagrass meadows, the GLM included two fixed factors (presence/absence of coral reefs and of lithogenic sources), as well as the interaction between the two factors. For sediment within mangrove forests, Data availability the GLM included one fixed factor (presence/absence of allochthonous sources), The dataset is available as Supplementary Data 1. because replication did not exist for all combinations of the two factors. The data had unequal samples among studies and studies were not evenly distributed around Received: 3 June 2018 Accepted: 31 January 2019 the globe (Fig. 1), which could result in pseudo-replication and biased results. To account for the data structure and minimize non-independence, we included three separate random variables, which included study, lithology grouping and marine province. The marine province was determined for each sample location using the marine provinces of the world as defined by Spalding et al.53. Separate models where run for seagrass and mangrove sites. The statistical model was produced using the lmer function within the lme4 package54 and p-values were calculated References with the lmerTest package55. The R2 was calculated for the fixed and random 1. Duarte, C. M., Losada, I. J., Hendriks, I. E., Mazarrasa, I. & Marbà, N. The role effects using the r.squared GLMM function in the MuMIn package56. 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Kennedy, H. et al. Seagrass sediments as a global carbon sink: Isotopic package57. This analysis was conducted in R version 3.4.2. constraints. Glob. Biogeochem. Cycles 24, 1–8 (2010). Reporting bias and its effect on findings is an important consideration for meta- 5. Alongi, D. M. Carbon cycling and storage in mangrove forests. Ann. Rev. Mar. analyses58 and when the result from a meta-analysis is not the same as it would Sci. 6, 195–219 (2014). have been if data from all correctly conducted studies were included in the 6. Nellemann, C. et al. (eds.) Blue Carbon: A rapid response assessment. (United analysis59. A main cause of reporting bias is not publishing research because of a Nations Environment Programme, GRID-Arendal, 2009). lack of merit as determined by the researcher, reviewer or editor60. As indicated by 7. McLeod, E. et al. 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This research was supported by King Abdullah University of Science and Technology 36. Saderne, V., Fietzek, P. & Herman, P. M. J. Extreme variations of pCO2 and (KAUST) through baseline funding and workshop funding to C.M.D. Support from the pH in a Macrophyte Meadow of the Baltic Sea in summer: evidence of the Australian Research Council through grants LIEF Project LE170100219, DE160100443, effect of photosynthesis and local upwelling. PLoS ONE 8, e62689 DE170101524, DP150103286, DP150102092, DP160100248, DE130101084, (2013). LP160100242 and LE140100083 is acknowledged. J.J.M. was supported by the Nether- 37. Sippo, J. Z., Maher, D. T., Tait, D. R., Holloway, C. & Isaac, R. Are mangroves lands Earth System Science Center. J.W.F. was supported by the US National Science drivers or buffers of coastal acidification? Insights from alkalinity and Foundation through the Florida Coastal Everglades Long-Term Ecological Research dissolved inorganic carbon export estimates across a latitudinal transect. Glob. programme under Grant Number DEB-1237517. D.K.-J. received financial support from Biogeochem. Cycles 30, 753–766 (2016). the Independent Research Fund Denmark (8021-00222B, CARMA) and the COCOA 38. Challener, R. C., Robbins, L. L. & McClintock, J. B. Variability of the project under the BONUS programme, funded by the EU 7th Framework Programme carbonate chemistry in a shallow, seagrass-dominated ecosystem: and the Danish Research Council. A.A.-O. was supported by an “Obra Social la Caixa” implications for ocean acidification experiments. Mar. Freshw. Res. 67, fellowship (LCF/BQ/ES14/10320004). A.A.-O. and P.M. acknowledge the support by the 163–172 (2016). Generalitat de Catalunya (grant 2017 SGR-1588). This work is contributing to the ICTA 39. Ray, R., Baum, A., Rixen, T., Gleixner, G. & Jana, T. 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M.G., M.P.J.O., C.J.S., I.R.S., J.M.S., T.T., K.W. and C.M.D. discussed and commented on the manuscript. 8 NATURE COMMUNICATIONS | (2019)10:1106 | https://doi.org/10.1038/s41467-019-08842-6 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-08842-6 ARTICLE Additional information Open Access This article is licensed under a Creative Commons Supplementary Information accompanies this paper at https://doi.org/10.1038/s41467- Attribution 4.0 International License, which permits use, sharing, 019-08842-6. adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Competing interests: The authors declare no competing interests. Commons license, and indicate if changes were made. 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