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Review

Lateral Export and Sources of Subsurface Dissolved Carbon and Alkalinity in Mangroves: Revising the Blue Carbon Budget

by
Daniel M. Alongi
Tropical Coastal & Mangrove Consultants, Pakenham, VIC 3810, Australia
J. Mar. Sci. Eng. 2022, 10(12), 1916; https://doi.org/10.3390/jmse10121916
Submission received: 30 October 2022 / Revised: 25 November 2022 / Accepted: 26 November 2022 / Published: 6 December 2022
(This article belongs to the Special Issue Chemical Oceanography Reviews)
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Abstract

:
Mangroves are carbon-rich ecosystems that store large quantities of carbon, mostly in soils. Early carbon (C) budgets indicated that >50% of mangrove C fixation was unaccounted for. This ‘missing C’ has now been discovered to be a large release (423 Tg C a−1) of porewater dissolved DIC (dissolved inorganic carbon), dissolved organic carbon (DOC), and total alkalinity (17 TMOL a−1) via lateral export derived from bacterial decomposition of soil organic matter. This large export originates from DIC produced over at least a 1.0–1.5 m soil profile (280–420 Tg C a−1) via decomposition of autochthonous and allochthonous inputs and/or likely mineralization in deep (≥1 m) ancient soils. DOC and DIC export from mangroves equate to 41% and ≈100% of export from the world’s tropical rivers, respectively. A newly revised blue carbon budget for the world’s mangroves indicates a mean ecosystem gross primary production (GPPE) to ecosystem respiration (RE) ratio of 1.35 and a net ecosystem production (NEP) of 794 g C m−2 a−1 (= global NEP of 117 Tg C a−1), reflecting net autotrophy. CORG burial is 5% and 9% of GPPE and NEPE, respectively. Mean RE/GPPE is 0.74 and carbon use efficiency averages 0.57, higher than for tropical humid forests (0.35).

1. Introduction

Biological and physicochemical linkages between intertidal wetlands and adjacent coastal waters are complex, and crucial to the structure and function of estuarine and inshore ecosystems. These interrelationships are greatly influenced by a variety of forces, including climate, and are central to our understanding of the dynamics of the coastal zone, from the upper estuary to the edge of the continental shelf [1].
Early research in salt marshes [2,3] led Odum [4] to propose his outwelling hypothesis, which asserted that nutrient cycles and productivity offshore are subsidized by particulate organic matter (POM), mostly salt marsh detritus, that is exported by tides. This paradigm led to much subsequent research, with crucial revisions to the outwelling paradigm [5,6]. Early mangrove studies [7,8,9] similarly measured POM export as mangrove litter, with further studies [10,11] also demonstrating export of DOC presumably derived from leaching from mangrove leaf litter during decomposition [12].
Initially, the mechanisms of exchange between mangroves and adjacent coastal waters were not greatly considered beyond the obvious tidal connections, until hydrological measurements showed that many mangroves exhibit complex water circulation patterns and flows [13]. In most forests, tidal circulation is characterized by a pronounced asymmetry between ebb and flood tides, with the ebb tide being shorter but with stronger current velocity than the flood tide, thereby facilitating material export. Further, mangrove vegetation and the forest floor exert a drag and subsequent time delay on the movement of water within the forest, resulting in latitudinal and longitudinal mixing and trapping. Animal structures impact water flow as crabs and other benthic organisms produce biogenic structures such as burrows and tubes through which tidal waters flow [14,15]. These structures, especially crab burrows, facilitate the movement of groundwater, which is an adaptive advantage, in that groundwater is likely to be an important pathway for removal of salt derived from tree roots and reduced by-products of microbial decomposition of organic matter [13]. The influence of groundwater-derived nutrients on biogeochemical cycles in mangrove waterways can be significant [16], but until recently, the influence of other microbial by-products such as dissolved organic carbon (DOC), dissolved inorganic carbon (DIC) and alkalinity has not been well understood.
This paper reviews the growing evidence of lateral transport of porewater DOC, DIC and alkalinity from mangrove forests with a view to reassessing their role in the mangrove carbon (C) mass balance. Further, the possible source(s) of these dissolved by-products are considered together with published data concerning vertical distribution of microbial (mostly bacterial) abundance, community composition, and decomposition rates with increasing soil depth, especially in deep soils mainly below the root layer.

2. The ‘Missing Carbon’ Problem

Two preliminary C budgets for mangrove ecosystems [17,18] indicated that more than half of the carbon fixed by mangroves (112–160 Tg C a−1) was unaccounted for in estimates of various carbon outputs, representing a large global flux of C. Bouillon et al. [17] suggested that much of the missing C may be exported as DIC and/or lost directly to the atmosphere as CO2. From mangrove studies in macrotidal settings, Alongi [18,19] suggested that substantial amounts of mineralized dissolved carbon were unaccounted for, especially in these latter environments, where mangroves sit atop highly sloped escarpments from which a large quantity of porewater is alternately drained and replenished by the large tides. Further, it was found that mineralization rates measured across the soil-water interface represent microbial activities mainly in surface soils and thus significantly underestimate depth-integrated rates in mangrove deposits [20]. Therefore, much of the DOC and DIC produced may be exported via groundwater exchange. Evidence for advective transport of DIC- and DOC-enriched groundwater first came from studies in Tanzania [21] and Vietnam [22] with the latter study concluding that porewater DIC derived from sulfate reduction was a significant contributor to the total DIC pool, based on stoichiometry and alkalinity measurements. In fact, alkalinity is also a significant lateral component in blue carbon dynamics in mangrove environments [23].

3. Rates of DOC, DIC, and Alkalinity Flux in Mangrove Ecosystems

Up to fifty sets of measurements have been taken to date in various mangrove creeks and estuaries worldwide, encompassing a wide variety of geomorphological settings, mangrove forest types, areas and dominant species and physical factors, in which dissolved carbon (DC) and alkalinity flux rates have been determined (Table 1).
DOC fluxes averaged 386.6 ± 159 (±1SE) g C m−2 mangrove area a−1 of 41 measurements (Table 1 and Table 2), with mean global DOC export averaging 5.68 × 1013 g C a−1 (= 56.8 Tg C a−1). Only 5 of the 41 measurements indicated net import into the mangroves (Table 1 and Table 2). DIC fluxes averaged 2481.96 ± 1274 (±1SE) g C m−2 mangrove area a−1 of 32 measurements (Table 1 and Table 2). Mean global DIC export averaged 3.65 × 1014 g C a−1 (= 365 Tg C a−1). Alkalinity fluxes averaged 117.51 ± 62 (±1SE) mol m−2 mangrove area a−1 of 22 measurements (Table 2). Mean global alkalinity export averaged 1.73 × 1013 mol a−1 (= 17.3 Tmol a−1). Mean annual global exports (Tmol) were 4.7, 30.4, and 17.3 for DOC, DIC and alkalinity, respectively.
DOC, DIC and total alkalinity fluxes did not correlate with mangrove area, latitude, temperature, tidal amplitude, annual precipitation, or salinity, but DOC and DIC both correlated with alkalinity (DOC and DIC vs. alkalinity, r = 0.934, p < 3.6 × 10−8 and r = 0.994; p < 1.586 × 10−19, respectively). Thus, no one factor determines export rates. The net direction and rates of DC and alkalinity exchange between mangroves and adjacent coastal waters depend on many interrelated factors including tidal range, extent of groundwater discharge, ratio of evaporation to precipitation, rates of primary productivity, geomorphology, soil granulometry, salinity, turbidity, pH, dissolved oxygen concentrations, seasonality, weather events, and rates of microbial assimilation [18]. The highly significant correlations of both DOC and DIC with alkalinity show close interlinkage with metabolic processes in soils.
The ratio of DIC to alkalinity export follows a stoichiometric relationship specific to the pathways of organic matter decomposition, where the slopes for these diagenetic processes are: aerobic respiration = −0.2; sulfate reduction = 1.0; denitrification = 0.8; CaCO3 dissolution = 2.0; ammonification = 0.1; manganese reduction = 4.4; iron reduction = 8.0 [66]. Mangrove studies that have plotted salinity-normalized concentrations of DIC and alkalinity have measured regression slopes of between 0.44–1.1 (Table 3) with an average of 0.80 (Table 3). While some sites indicated that DIC and alkalinity were derived from denitrification and iron reduction, most results indicated the dominance of sulfate reduction and, to a lesser extent, aerobic mineralization, which agrees with many empirical measurements of rates and pathways of bacterial diagenesis in mangrove soils and sediments [18,67]. Further, the driver of alkalinity production is likely to be the burial of reduced sulfides, probably from the recycling of Fe from terrestrial sources [42].
Pyrite production is a dominant alkalinity producing process, although not all production could account for all alkalinity export. Further, estimated global total alkalinity production coupled to pyrite formation (~3 mol m−2 a−1) is equal to about 24% of global carbon burial rate [68] underscoring the importance of including total alkalinity export in blue carbon budgets. Total alkalinity remains dissolved in the ocean for centuries, representing a long-term sink for atmospheric carbon. A modelling exercise of benthic alkalinity fluxes from mangroves (Figure 1) shows that rates of alkalinity release from mangrove soils are greater in mature restored forests than in young, restored stands and lowest in sediments without mangrove vegetation, which show about 3–9 t CO2 ha−1 a−1 [69]. This estimate is close to the facilitation of the alkalinity export of 117.5 mol m−2 a−1 to ~2.8 Tg C a−1 of the annual CO2 uptake of global mangrove waterways and creeks. Thus, alkalinity production has a twofold impact on blue carbon fluxes, in that carbon is retained as alkalinity rather than being lost to the atmosphere as CO2, and is exported to the coastal ocean. Further, the export of alkalinity buffers water-column pH, facilitating the uptake of extra CO2 [42], ameliorating coastal acidification.
The export of porewater DOC, DIC and alkalinity from the world’s mangrove forests are disproportionate to their 0.3% of global coastal ocean area. Using the data in Table 2, which assumes a global mangrove area of 147,359 km2 [65], DOC and DIC export from mangroves equate to 41% and ≈100% of export from the world’s tropical rivers [70] and mangrove DIC export equates to 92% from the world’s rivers [71]. Export of POC + DOC combined results in export equivalent to 43% of tropical river export [70]. Mangrove DOC export equates to 10% of total export from the global coastal ocean [71]. DIC export from mangroves equates to 24% from global continental margins [72]. Alkalinity export from mangroves equates to 58% and 69% of export from all global rivers and from the world’s continental shelves, respectively [73].
Global mangrove DOC export is two to four times higher than the earlier estimates of Bouillon et al. [17] and Alongi [18,74], and DIC and alkalinity export estimated here are eight times greater and four times greater, respectively, than the estimate of Sippo et al. [23]. Similarly, groundwater derived DIC + DOC export estimates by Chen et al. [47] underestimated percentage contributions (29–48%) of global riverine input to the coastal ocean.
However, carbon export from mangroves is now changing due to losses from deforestation and dieback from extreme weather events. For example, in the Gulf of Carpentaria, northern Australia, massive dieback of mangroves due to extreme climate resulted in a 189% increase in soil CO2 efflux and a decrease in DIC export of 50% relative to areas with live forests [52]. Extrapolating this event globally, Sippo et al. [52] estimated that global mangrove carbon losses could be 13.7 ± 9.4 Tg C a−1, eightfold greater than previous estimates, and offsetting burial in mangroves by ~60%. A drought-induced mortality event in southeastern Brazil resulted in a 15% decrease in total ecosystem carbon stocks and a 20% loss of soil carbon within less than 2 years after the beginning of the event [75]. Both drought events indicate severe losses of carbon from mangrove ecosystems due to climate change.

4. Blue Carbon Cycling

The expanded dataset published in recent years allows for construction of a fourth iteration [18,74,76] blue carbon budget. One of the largest differences from the earlier versions, aside from the larger export values, is determining the least arguable global mangrove area. In this version, we used the latest estimate of 147,359 km2 [65], based on the most accurate maps to date.
The carbon model (Figure 2) indicates that the export of POC, DOC, DIC, and CH4 are equivalent to ~99% of ecosystem gross primary production (GPP) and about 1.8 times ecosystem net primary production. DIC accounts for about 81% of total carbon export. Total carbon (POC + DC) export is equal to total ecosystem respiration (RE), which is the sum of all respiration measurements presented in Figure 2. Root production (70 Tg C a−1) was estimated as the difference between net mangrove primary production (177 Tg C a−1) and wood (50 Tg C a−1) and litter (57 Tg C a−1) production. The contribution of dissolved carbon from land-derived groundwater remains unquantified. Two sets of flows were revised in this budget iteration owing to new (and previously overlooked) data: (1) mangrove forest gross primary production and canopy respiration [77,78,79,80,81,82,83,84,85,86,87] with a small adjustment in mangrove NPP; and (2) inclusion of epiphytic macroalgal productivity (92 Tg C a−1) and respiration (44 Tg C a−1) [88,89,90,91,92,93]. What is clear is that, although DIC export alone is sufficient to account for the ‘missing carbon’ (Section 2), there is a clear imbalance between inputs and outputs regarding DC exports and the CORG required to balance these large losses. This problem as discussed further in Section 5.3.

5. Reconciling Organic Matter Sources and Subsurface Mineralization

The estimate of total carbon mineralization in mangrove soils (423 Tg C a−1) in the budget was determined by assuming that all dissolved C exports originate from bacterial decomposition of soil organic matter. This is a reasonable assumption given that nearly all evidence (Table 1 and Table 3) shows that dissolved C is derived from bacterial processes such as sulfate reduction and transported as metabolic by-products in the porewater via lateral subsurface transport. Surface respiration is not considered as a part of the subsurface mineralization rates as the former arguably reflects bacterial–algal–fungal processes in surficial soils rather than deeper microbial processes [76]. Similarly, pelagic respiration reflects plankton respiration and efflux of CO2 due to supersaturated conditions. Porewater alkalinity release facilitates an annual uptake of ~2.8 Tmol CO2.
The total soil organic carbon pool (SOC) to one meter depth averages 9195 Tg C (Figure 2). Assuming that all SOC is available for mineralization, complete decomposition would average 21.7 years with a turnover of 0.046 a−1 over the upper 1 m. There are, however, several problems with this estimate: (1) only a small to moderate, but highly variable, fraction of mangrove SOC is thought to be readily labile [67,94], (2) only 93 Tg C a−1 has been identified as being incorporated into the soil organic carbon pool (from root and litter production), which is insufficient to balance the estimated microbial mineralization rates (Figure 2 and Figure 3); these estimates do not include SOC in mangrove deposits >1 m depth [67,94].
These problems raise several possibilities. First, if we assume that C burial plus C mineralization equates to total C input (i.e., steady-state conditions which may not exist [76]), total global C input to the forest floor from allochthonous sources must be within the range of C sequestration in mangroves [74], which is much smaller (mean = 15 Tg C a−1) than the DC export rates. However, if soil CORG is more labile than previously believed, then there may be sufficient mineralization to account for these large export rates. Recent work [95] has indeed highlighted the fact that decomposition rates of fine root detritus, a major component of mangrove SOC, can be very rapid, on the order of 2.5–18.8 g C m−2 d−1 and likely 50–200% higher than the estimated total annual loss of C derived by summing rates of bacterial metabolism and surface and subsurface C export. Root detritus may therefore not be as refractory as previously believed. In Section 5.1 we will examine the issue of quality and origin of mangrove SOC.

5.1. Quality and Origin of SOC

How do we reconcile these estimates of rapid mineralization and associated dissolved carbon export with biogeochemical processes within the forest floor? The first possibility already noted is that unconsolidated mangrove soils are often several meters deep, suggesting the potential for a much larger SOC pool available for mineralization. Several studies [96,97,98,99] have measured mangrove SOC mineralization efficiencies ranging from 14–92% (mean = 59%), which indicate that at least half of the SOC pool is readily labile. Kristensen et al. [94] found that 58% of δ13C data was lower than −25‰, suggesting a significant mangrove litter source (δ13C~−28 to −30‰). However, relatively high δ13C data (−17 to −23‰) indicate large inputs of allochthonous (phytoplankton, seagrass, seaweed, riverine POC, microphytobenthos, macroalgae) 13C-enriched carbon sources (δ13C~−16 to −24‰) rather than mangrove-derived plant litter (Table 4).
The data (Table 4), in fact, show that SOC at about 60% of the study sites are derived mostly from non-mangrove, allochthonous sources, such as seagrass and coral reef detritus, seaweed, higher land plants, bacterial necro-mass, microalgae, phytoplankton, and riverine, coastal, and oceanic POC. The contribution of mangrove matter to the SOC pool appears to be a function of stand age [107,109] with an increasing percentage of mangrove-derived carbon (litter, roots, wood) contributing to SOC in stands of increasing age. Thus, the old idea [7,8] that mangrove SOC is primarily derived from mangrove detritus is apparently the exception rather than the rule. Thus, it may be reasonable to conjecture that the organic carbon fueling the high export of DOC and DIC is directly linked to in-situ microbial mineralization of material originating as much as from allochthonous sources as from mangroves, as suggested from the data in Table 4.

5.2. Are Deep, Old Soil Deposits a Source of Dissolved Carbon?

Few mangrove studies have measured SOC stocks and composition and rates and pathways of microbial activity below 1 m depth; most studies have examined sediments and soils only over the upper 20–50 cm, as it was thought that most microbial activity took place in association with roots and rhizomes, animal tubes and burrows, and on the soil surface [18]. More recent evidence points to large SOC stocks with few clear depth-related patterns, to a depth of 2–3 m in mangroves in the Rufiji River delta in Tanzania [113]; in Baja California, Mexico [122]; and in Pongara National Park in Gabon [123]; to a depth of 3.5 m in A.marina, R. apiculata and R. mucronata, and X. granatum forests in That, Thailand [110] and to a depth of 6 m in southern Thailand [117]. In the That Thai forests, roots (>2 mm) were found mostly in the upper 1 m but were observed throughout the 3.5 m cores, mainly in the Rhizophora and Xylocarpus forests (Figure 3); C:N ratios (15–28) reflected the influence of root biomass and mangrove inputs. In the A. marina forest, C:N ratios were significantly lower (13–19) than in the other two forests, suggesting that mangrove litter or woody tissue did not contribute significantly to the SOC pool, and may represent microbial decomposition and/or inputs of marine OM. The vertical C:N profiles likely also reflect differences in sedimentary history between surface and deep (>1 m) deposits.
CORG is stored as peat under the right conditions [121,124,125,126]. Peat formation is a function not only of OM inputs, tree species, litter composition, microbial and faunal activities, but also moisture and temperature, slow decay rates of refractory material, and the magnitude and frequency of tides. This material may be stored for hundreds to thousands of years, facilitated by several unique physical, chemical, and hydrological drivers. Most mangrove deposits, especially below the dense live root layer, originate from at least the early Holocene. Radiocarbon dating [121,124,125,126] indicates that mangrove deposits beneath the root layer are from 1000–4000 14C B.P. to depths of about 1 m, with sediments increasing in age with greater depth (>6800 14C B.P. at 3 m depth [126]).
Considering these ages, such deep deposits are derived from extinct habitats, such as intertidal flats or even extinct mangrove forests; they are not directly linked historically to the present mangrove environment; thus, in a sense, they represent a previous ecological habitat. Any biogeochemical activities occurring within these deep soils can therefore be considered as ‘allochthonous’ inputs to the present mangrove ecosystem, along with any modern inputs from upstream terrestrial sources, seagrass, coral reefs, seaweeds, benthic algae, and plankton-derived organic matter, having profound consequences for the blue carbon budget.
Studies have found that aged porewater can enter the export pool and that bioturbation activities may enhance the mineralization of old buried carbon [127,128]. Gleeson et al. [127] measured 226Ra (half-life = 1600 years) enrichment at low tide in a subtropical mangrove creek. This enrichment could only be explained by the construction of new crab burrows during each tidal cycle exposing old sediments. Further, they conjectured that mineralization of old carbon may be enhanced by deep soil oxygenation via crab reworking. In another subtropical mangrove estuary in Australia, Maher et al. [128] measured ∆14C in the exported DIC as well as soil ∆14C profiles and found that the source of DIC to surface waters had a δ13C-DIC value of −29.4 ± 1.9‰ and ∆14C-DIC value of −73 ± 9‰, indicating release of isotopically depleted old DIC. This DIC came from an average soil depth of ~40 cm, equivalent to ~100 years of sediment accumulation. Thus, century-old, sequestered carbon is still being mineralized and exported via porewater exchange or submarine groundwater discharge. This result is very similar to work in a coastal salt marsh [129], where soil C∆14C profiles showed that decadal carbon sequestration rates were 10-fold higher than millennial-scale rates, indicating this was due to either continual mineralization of buried carbon or recent productivity increases. Some deep mangrove peat deposits still cycle nitrogen but apparently not measurable amounts of carbon [121]; however, there is considerable bacterial diversity to at least depths of 250 cm, with increasing percentages of both genera Cyloroflexi and Dehalococcoidaeae, which are ordinarily involved in sulfate reduction and dehalogenation of aromatic compounds, supporting their potential role as bacterial consumers of recalcitrant peat organic matter [121].
Microbial metabolic processes such as sulfate reduction, nitrogen fixation, and DIC production have been measured to a depth of 1 m with little or no attenuation of rates with depth, implying that such activities may persist to greater depths, as suggested by the 226Ra and ∆14C-DIC measurements. Alongi (Figure 2, [76]) measured high rates of DIC production over 1 m soil profiles from four different mangrove forests, all without clear depth-related trends. Using these data from Australia, Southeast Asia, China, and East Africa [76], rates of subsurface DIC production averaged 5.2 g C m−2 d−1 or 280 Tg a−1 over the upper 1 m of soil (assuming a global mangrove area of 147,359 km2). Considering relative and systematic errors, 280 Tg C a−1 is very close to the estimated value of 330 Tg C a−1 (423 Tg C a−1 minus the contributions from root and litter decomposition) (Figure 2). If DIC was still being produced in soils to a depth of 1.5 m, the value would be ≈ 420 Tg C a−1, equal to the rate of total C mineralization and export.
Microbial communities in mangrove soils have long been recognized as being highly abundant, productive, and diverse with many species and functional types of archaea, bacteria, cyanobacteria, microalgae, fungi, and protozoa [18]. Diagenetic reactions such as sulfate, iron, and manganese reduction as well as anabolic reactions such as nitrogen fixation have been measured to depths greater than usually measured in estuarine and marine deposits [1] where there are, in theory, distinct aerobic, suboxic, and anoxic zones with increasing depth into the seabed. The depth distribution of various bacterial pathways in mangrove deposits is thus reminiscent of those in tropical deltaic deposits where the diagenetic zones are vertically elongated [130,131], with low, but sustainable, rates of sulfate reduction and dominated by measurable rates of iron and manganese reduction.
In mangroves, aerobic decomposition occurs at the soil surface and within the linings of burrows and tubes, as well as within the root–rhizosphere complex. Mangrove deposits are rarely wholly anoxic, although such layers must exist, as methanogenesis has been measured [18]. Most mangrove deposits are mixtures of spatially variable diagenetic zones where sulfate reduction, metal reduction, and denitrification co-occur in subsurface soils.
Our current understanding of nitrogen fixation (and other nitrogen metabolic processes) is mainly limited to measurements from fallen wood and litter, live stems, and cyanobacterial mats and, to a much lesser extent, in surface (0–10 cm) soils [18]. However, more recent studies [132,133] have measured nitrogen fixation and phosphorus solubilization potentials to a soil depth of 1 m. Vertical depth profiles of rates of nitrogen fixation in S. apetala soils of the Qi’ao Mangrove Wetland Park, China (Figure 4), fluctuated from 0–0.20 nmol g−1 h−1, with rates attaining a maximum at a depth of 90–100 cm, with elevated abundance of N2- fixation genes (nifH/D/K) in deep soils [132].The genomes of diazotrophs from deep deposits indicate their facilitatively anaerobic and mixotrophic lifestyles, as they contained genes for low O2 metabolism, hydrogenotrophic respiration (molecular hydrogen metabolism), carbon fixation, and pyruvate fermentation. In a nearby mangrove system (Beibu Gulf, China), metagenomic sequences indicated a decline in relative abundances of various bacterial types at a depth of 1 m [133], but genes were still present for nitrogen fixing and P solubilizing microbes. There was a clear shift in bacterial composition with soil depth, with genes encoding inorganic pyrophosphatase and exopolyphosphatase most abundant in the upper 25 cm.
Another reason that highly active microbial communities exist in deep mangrove deposits is that crabs, depending on the species, burrow down several meters, stimulating SOC decomposition with their bioturbation and feeding activities [134,135].
Thus, it is likely that microbial communities in deep, old soil deposits are, at least to a limited extent, metabolically active. Even if rates of microbial mineralization were slow compared to rates in upper soils, slow rates over elongated diagenetic zones may indeed translate into a significant contribution towards the measured high rates of porewater DC export.

5.3. A Revised Mangrove Blue Carbon Mass Balance

The carbon mass balance (Figure 2) was constructed based the assumption that total DC exports (423 Tg C a−1) originate from the contribution of autochthonous inputs (root and litter production = 62 and 31 Tg C a−1, respectively), and an unknown amount of allochthonous carbon inputs and inputs via the decomposition of the SOC pool (= 330 Tg C a−1), including decomposition of centuries-old, deep sediments that were formed prior to the existing mangrove ecosystem (Figure 2, Table 5). Total inputs (59.2 Mg C a−1) and outputs (54.8 Mg C ha-1 a−1) are in approximate balance, considering the inherent seasonal and spatial variations in flows and systematic and relative errors and unknowns. Other issues that may affect the mass balance are (1) mangrove and/or algal production may be underestimates; (2) one or more outputs may be overestimates; and (3) fluxes such as faunal production and chemical defenses (not included) may be more important than previ ously recognized. Further, there is no data on groundwater DC derived from adjacent land, such as neighboring farms, human wastes, and aquaculture effluents, all of which can export significant quantities of carbon and nutrients locally. Thus, anthropogenic inputs and effects of climate change are likely to alter the mass balance for mangrove blue carbon.
The largest inputs are both mangrove GPP and DIC production from SOC decomposition in centuries-old, pre-existing deep sediments, while the largest output by far is DIC export which is also the largest flux, being great than mangrove GPP and three times greater than canopy respiration, which is the second largest C loss from the system. At the ecosystem level, and including all primary producers, the mean GPP/R ratio is 1.35 and NEP (net ecosystem production = total GPP − RE) is 794 g C m−2 a−1. The mean global NEP is 117 Tg C a−1. Carbon burial is only 5% and 9% of ecosystem GPP and NPP, respectively. Mean RE/GPP is 0.74 and CUE (carbon use efficiency) equals 0.57, which is greater than the average (0.35) for tropical humid forests [136,137]. Compared to the other world’s forests, mangrove NEP is greater, but ecosystem respiration is within the global forest average, while mangrove ecosystem GPP is at the upper end of the range of rates [138]. Comparisons of both mangrove NEP and ecosystem respiration versus GPP with these relationships in all terrestrial forests indicate a best-fit of mangrove forests with terrestrial forest ecosystems that are nutrient-poor [139].

6. Conclusions

Recent advances in biogeochemical research have enabled a dramatic revision of our view of blue carbon dynamics in mangrove ecosystems. First, the ‘missing carbon’ problem has been solved after the discovery that mangroves laterally export large quantities of porewater DOC, DIC and alkalinity to adjacent waters. Second, the ratio of DIC to alkalinity export conforms to the stoichiometry of the major metabolic pathways of organic matter decomposition, especially aerobic respiration, denitrification, and sulfate reduction, indicating that DIC and alkalinity are bacterial metabolic by-products originating from mangrove deposits and transported via subsurface pathways. Third, alkalinity production is an important pathway, remaining dissolved in the ocean for millennia, representing a long-term sink for atmospheric carbon. Fourth, dissolved carbon export is two to eight times greater than early estimates and may be even greater in the future, with losses from deforestation and dieback. Fifth, the large export of DC is presumably balanced by equally high rates of carbon mineralization throughout the mangrove soil profile, which implies that a significant fraction of the DC is derived from decomposition of deep soil CORG and external marine and terrigenous sources, given the apparent modest contributions from root and litter production available for incorporation into the SOC pool. The possibility of a significant contribution of DC from deep soils and from land-derived groundwater needs to be further considered, requiring more research. Future lines of research must include more empirical data on algal productivity, canopy respiration, the relative contribution of mangrove versus allochthonous organic matter to soil carbon mineralization rates, rates of carbon mineralization in soil deposits > 1 m depth, and the effect of climate change on mangrove blue carbon fluxes and pathways. Nevertheless, it is clear more than ever before that mangroves are undoubtedly open ecosystems that are tightly linked to the adjacent seas and the ancient deposits upon which they reside.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The empirical data presented here can be obtained from the original publications cited in the References section.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. Model estimates of total alkalinity release from mature restored mangroves, young, restored mangrove stands and sediments without mangroves. Increasing rates of alkalinity release results in increasing rates of CDR (see text). Modified from Fakhraee et al. [69]. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0, accessed 3 October 2022).
Figure 1. Model estimates of total alkalinity release from mature restored mangroves, young, restored mangrove stands and sediments without mangroves. Increasing rates of alkalinity release results in increasing rates of CDR (see text). Modified from Fakhraee et al. [69]. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0, accessed 3 October 2022).
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Figure 2. Blue carbon flow and standing stocks through the world’s mangrove ecosystems, updated from Alongi [18,74,76], assuming a global mangrove area of 147,359 km2 [65]. Carbon fluxes are Tg C a−1. Total alkalinity flux is Tmol a−1. Solid blue arrows represent mean values based on published data (see text for explanation, Table 1 and Table 2). Dashed red arrows are mean values estimated by difference. The soil CORG pool (roots + soil) to a depth of 1 m is represented as a box in the forest floor with units of Tg C. Abbreviations: GPP = gross primary production; NPP = net primary production; Ra = microalgal respiration; REM = epiphytic macroalgal respiration; EM = epiphytic macroalgae; AOC = allochthonous CORG input from phytoplankton, seaweed, seagrass, coral reef, and upstream terrestrial C4 plant detritus, etc.; RC = canopy respiration; RS = surface soil respiration; RWATER = waterway respiration; DC = dissolved carbon; POC = particulate organic carbon; DIC = dissolved inorganic carbon; DOC = dissolved organic carbon; EDOC = exchangeable dissolved organic carbon; CH4 = methane; ND = no data. Total subsurface lateral DC flux from the forest floor (423 Tg C a−1) = ‘C’ (93 Tg C a−1) + ‘E’ (330 Tg C a−1), where ‘C’ is the sum of fluxes ‘A’ (roots) + ‘B’ (litter). Flux ‘E’ = unquantified input from allochthonous CORG (‘D’) plus total DIC production from the SOC pool, including unquantified DC flux from deep ancient deposits. These porewater DC components are then transported via subsurface water flow to the adjacent mangrove waterway. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0) accessed 4 October 2022.
Figure 2. Blue carbon flow and standing stocks through the world’s mangrove ecosystems, updated from Alongi [18,74,76], assuming a global mangrove area of 147,359 km2 [65]. Carbon fluxes are Tg C a−1. Total alkalinity flux is Tmol a−1. Solid blue arrows represent mean values based on published data (see text for explanation, Table 1 and Table 2). Dashed red arrows are mean values estimated by difference. The soil CORG pool (roots + soil) to a depth of 1 m is represented as a box in the forest floor with units of Tg C. Abbreviations: GPP = gross primary production; NPP = net primary production; Ra = microalgal respiration; REM = epiphytic macroalgal respiration; EM = epiphytic macroalgae; AOC = allochthonous CORG input from phytoplankton, seaweed, seagrass, coral reef, and upstream terrestrial C4 plant detritus, etc.; RC = canopy respiration; RS = surface soil respiration; RWATER = waterway respiration; DC = dissolved carbon; POC = particulate organic carbon; DIC = dissolved inorganic carbon; DOC = dissolved organic carbon; EDOC = exchangeable dissolved organic carbon; CH4 = methane; ND = no data. Total subsurface lateral DC flux from the forest floor (423 Tg C a−1) = ‘C’ (93 Tg C a−1) + ‘E’ (330 Tg C a−1), where ‘C’ is the sum of fluxes ‘A’ (roots) + ‘B’ (litter). Flux ‘E’ = unquantified input from allochthonous CORG (‘D’) plus total DIC production from the SOC pool, including unquantified DC flux from deep ancient deposits. These porewater DC components are then transported via subsurface water flow to the adjacent mangrove waterway. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0) accessed 4 October 2022.
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Figure 3. Vertical profiles of >2mm mangrove roots (left panel) and corresponding soil C:N in A. alba, Rhizophora spp., and X. granatum forests in the Trat River estuary, eastern Thailand to a depth of 3.5 m. Modified from Figure 2 in Kida et al. [110]. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0, accessed 5 October 2022).
Figure 3. Vertical profiles of >2mm mangrove roots (left panel) and corresponding soil C:N in A. alba, Rhizophora spp., and X. granatum forests in the Trat River estuary, eastern Thailand to a depth of 3.5 m. Modified from Figure 2 in Kida et al. [110]. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0, accessed 5 October 2022).
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Figure 4. Rates of nitrogen fixation over a 1 m depth profile, Qi’ao Mangrove Wetland Park, China. Boxplots depict the 25–75% quantile range of the measurements with the centerline depicting the median (50% quantile). Whiskers show the minimum and maximum values. Adapted from Luo et al. [132]. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0, accessed 6 October 2022).
Figure 4. Rates of nitrogen fixation over a 1 m depth profile, Qi’ao Mangrove Wetland Park, China. Boxplots depict the 25–75% quantile range of the measurements with the centerline depicting the median (50% quantile). Whiskers show the minimum and maximum values. Adapted from Luo et al. [132]. Reproduced via requirements of open access under the CC Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0, accessed 6 October 2022).
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Table
Table 1. Rates of porewater DOC, DIC and alkalinity flux from mangroves ecosystems worldwide. Values are g C m−2 a−1 for DOC and DIC and mol m−2 a−1 for total alkalinity. Positive values indicate export and negative values indicate import. Only data based on reliable methodology are presented.
Table 1. Rates of porewater DOC, DIC and alkalinity flux from mangroves ecosystems worldwide. Values are g C m−2 a−1 for DOC and DIC and mol m−2 a−1 for total alkalinity. Positive values indicate export and negative values indicate import. Only data based on reliable methodology are presented.
LocationMangrove Area (km2)DOCDICAlkalinityReference
Taylor R, USA2−0.46--[24,25]
Mandovi–Zuari, India160.1--[26,27]
Taylor R, USA2−67.3--[28,29]
Rookery Bay, USA1636.7--[10]
Rookery Bay, USA18044.3--[30]
Itacuruca, Brazil3813.1--[31]
Coral Creek, Australia5−13--[9,11]
Conn Creek, Australia620.9--[32]
Sawi Bay, Thailand3332--[33]
Furo de Meio, Brazil648--[34]
Celestun, Mexico22108.1--[35]
Caete Coast, Brazil10,000138.1--[36]
Shark R, SW Florida, USA140056--[37]
Mngazana, S. Africa10--[38]
Lobos Bay, Mexico5.4−0.4--[39]
Shark R, SW Florida, USA1400180--[40]
Moreton Bay, Qld, Australia21101095-[41]
Watson Inlet, SE Australia1.8109.52014.8113.15[42]
Chinaman Inlet, SE Australia0.560613.216.79[42]
Moreton Bay, Qld, Australia140157.7683.358.77[43]
Darwin Harbour, N Australia0.73-372.342.34[23]
Hinchinbrook Is, NE Australia3.6-96.47.67[23]
Seventeen Seventy, E Australia1.75-−424.929.57[23]
Jacobs Well, E Australia0.4-363.54.38[23]
Newcastle, E Australia1.26-337.342.34[23]
Barwon Heads, SE Australia0.38-−13.1−0.37[23]
Korogoro Creek, SE Australia25768.513,494.81300.86[44]
Shark R, SW Florida, USA140051.7603.5-[45]
Harney R, SW Florida, USA17.447.8223-[45]
Sundarbans, India4000757.5922.5-[46]
Maowei Sea, China231226.42080.5-[47]
Moreton Bay, Qld, Australia140258.4928.6 [48]
Creek 1, Airai Bay, Palau2153.334628.83[49]
Creek 2, Airai Bay, Palau23543.816.79[49]
Kooragang Island, SE Australia6.3865.9−1228.39[50]
Evans Head, SE Australia0.088.852.564.38[51]
Gulf of Carpentaria. N. Australia3.43635.16802.1566.12[52]
Shark Bay, SW Florida, USA1400368.21867.2147.43[53]
Fukido R, SW Japan0.19193.5859.6-[54]
Sinnamary estuary, French Guiana11.342971.1−328.5-[55]
Zhenzhu Bay, SW China17.33496.56101.6-[56]
central Red Sea, Saudi Arabia0.5--147.09[57]
Shark Bay, SW Florida, USA1400170.862235.41[58]
Iriomote Is, Japan20.0070.0150.0025[59]
Caete Estuary, N Brazil72101.287.65.55[60]
Panay Is, Philippines0.3975.3613.2-[61]
Coffs Creek, E Australia0.2−424.12.08[62]
Qinglan Bay, S China0.59795.739,055-[63]
Guayas R, Ecuador1121-7.7-[64]
Table
Table 2. Mean (±1SE) rates of DOC, DIC, and alkalinity (TALK) export from the world’s mangroves assuming a global area of 147,359 km2 [65].
Table 2. Mean (±1SE) rates of DOC, DIC, and alkalinity (TALK) export from the world’s mangroves assuming a global area of 147,359 km2 [65].
DOC (g C m−2 a−1)DIC (g C m−2 a−1)TALK (mol m−2 a−1)
Mean 386.62482117.5
±1SE159127462
N413222
Mean (Tg C/Tmol a−1)56.9365.917.3
Table
Table 3. Regression slopes and indicative metabolic processes affecting DIC–alkalinity relationships in mangrove waters.
Table 3. Regression slopes and indicative metabolic processes affecting DIC–alkalinity relationships in mangrove waters.
LocationRegression SlopeMetabolic ProcessReference
Nagada Creek, Papua New Guinea0.99sulfate reduction[66]
Gaderu Creek, India0.61aerobic respiration + sulfate reduction[66]
Darwin Harbour, N Australia0.82sulfate reduction + aerobic respiration[23]
Hinchinbrook Island, E Australia0.44aerobic respiration = sulfate reduction[23]
Seventeen Seventy, E Australia0.78sulfate reduction + aerobic respiration[23]
Jacobs Well, E Australia0.65sulfate reduction + aerobic respiration[23]
Barwon Heads, SE Australia0.85sulfate reduction[23]
Shark, Harney R, Florida, USA0.82, 0.84, 0.92,0.93, 0.95sulfate reduction, aerobic respiration, CaCO3 dissolution[45,53,58]
Creek 1, Palau, Micronesia0.7sulfate reduction + aerobic respiration[49]
Creek 2, Palau, Micronesia1.1sulfate reduction + CaCO3 dissolution[49]
Evans Head, E Australia0.68sulfate reduction + aerobic respiration + denitrification[51]
Central Red Sea, Saudi Arabia0.44aerobic respiration + denitrification+ CaCO3 dissolution[57]
Caete Estuary, N Brazil0.75, 0.95, 0.96sulfate reduction + aerobic respiration[60]
Upper Coffs Harbour, SE Australia0.63, 0.66Aerobic respiration + sulfate reduction[63]
Lower Coffs Harbour, SE Australia0.93, 1.09Denitrification, iron reduction[63]
Table
Table 4. Differences in sources, δ13C signatures and C:N ratios of soil organic carbon (SOC) in various mangrove forests worldwide.
Table 4. Differences in sources, δ13C signatures and C:N ratios of soil organic carbon (SOC) in various mangrove forests worldwide.
LocationForest TypeC:N (Molar) and δ13C (‰)SOC SourcesReference
Ko Muk,
SW Thailand		Nypa fruticans, Rhizophora apiculata, Avicennia albaδ13C = −18‰ to −23.8‰42% seagrass, 23% mangrove, 13% coastal POC[100]
Ko Talibang,
SW Thailand		riverine Nypa fruticans, Rhizophora apiculata, Avicennia albaδ13C = −19.6 to −25.4‰36% seagrass, 23% mangrove, 19% POC[100]
Sinnamary R,
French Guiana		Pioneering A. germinansδ13C = −24‰ to −27‰
C:N = 7–19		Amazonian riverine OC, algal OC (surface soils)[101,102,103]
Sinnamary R,
French Guiana		Senescent A. germinansδ13C = −25‰ to −29‰
C:N = 30–82		Mangrove root and lignocellulosic material[101,102,103]
Godavari delta, IndiaA. officinalis–Excoecaria agallochaδ13C = −20‰ to −25‰
C:N = 8–10		Pelagic suspended matter and phytoplankton-derived matter[104]
Galle and Pambala, Sri LankaR. apiculata, R. mucronata,
A. officinalis, E. agallocha		δ13C = −27.5‰ to −30.5‰
C:N = 30–43		Mangrove-derived material[104]
Gazi Bay, Kenya
  • (upstream) R. mucronata, Ceriops tagal, Bruguiera gymnorrhiza, Xylocarpus granatum
  • (seaward fringe) Sonneratia alba
  • δ13C = −24.3‰ to −26.5‰
  • δ13C = −22.1‰ to −24.9‰
  • Mangrove + microalgae + seagrass
  • Seagrass + mangrove + microalgae
[105]
Betsiboka estuary, NW MadagascarR. mucronata, C. tagal,
B. gymnorrhiza		δ13C = −18.8‰ to −21.4‰
C:N = 9.1–11.0		Riverine suspended matter (mostly C4 derived plant material) plus algal sources[106]
Jiulongjiang estuary, ChinaKandel obovataδ13C = −23‰(12 year old stand)
δ13C = −24‰(24 year old stand)
δ13C = −23.3‰ to −25.9‰
(48 year old stand) 		Mangrove contribution to soil OC:
<20% (12 year old stand)
<40% (24 year old stand)
<80% (48 year old stand)		[107]
Okinawa, JapanR. mucronata, B. gymnorrhizaδ13C = 27.8‰ to −28.6‰
C:N = 27.6–33.6		Mangrove root matter[108]
Guayas delta,
Ecuador		Rhizophora mangle,
A. germinans		Young forest: δ13C = −26.6‰; C:N = 14.1
Old forest: δ13C = −27.0‰, C:N = 20.7		Young forest ≈ 80% allochthonous (POC water)
Old forests ≈ 60% autochthonous (vegetation)		[109]
Trat, ThailandA. marina, R. apiculata-R.
mucronata, X. granatum		Soil Fluorescence componentsRhizophora = 27% mangrove
X. granatum = 27% mangrove		[110]
Iriomote Is, JapanR. stylosa, B. gymnorrhiza,
A. marina		δ13C = −28.2‰
C:N = 20.5		88% = mangrove + riverine POM
4% = seagrass + coral+ seaweed + benthic microalgae
8% = oceanic OM		[59]
Cochin estuary,
SW India
  • officinalis, R. mucronata
C:N = 1.86–13.11; amino acid composition0–10 cm = phytoplankton + algae
20–25 cm = new bacterial biomass production
Deeper soil = mostly higher land plants		[111]
Kerala,
SW India		(Site 1) Munroe Island: E. agallocha, A. officinalis, R. mucronata
(Site 2) Kayamkulam estuary: A. officinalis, A. marina, A. alba,
Bruguiera cylindrica
(Site 3) Vypin/Valappu Island:
B. gymnnorhiza, B. cylindrica,
A. officinalis, E. agallocha		δ13C = −26.81‰ (site 1), −23.09‰ (site 2), −28.47‰ (site 3)
C:N = 14.34 (site 1), 7.07 (site 2), 14.98 (site 3)		Site 1 = mangrove litter
Site 2 = marine phytoplankton
Site 3 = mangrove litter		[112]
Rufiji delta, TanzaniaR. mucronata, C. tagal, B. gymnorrhiza, X. granatum, A. marina, S. alba, Heritiera littoralisInterior mangroves: C:N = 22.6; δ13C ≈ −24‰
Riverine mangroves: C:N = 20.1; δ13C ≈ −24.6‰
Seaward mangroves: C:N = 21.2 δ13C ≈ −24.8‰		Mangrove and upstream terrestrial plant matter sources. [113]
Pichavarum, SE IndiaA. marina, R. apiculataC:N = 14.2–16.6
δ13C = −24.3‰ to −27.2‰		Mangrove and upstream terrestrial plant material[114,115]
Zambesi delta, MozambiqueA. marina, B. gymnorrhiza, C. tagal, H. littoralis, Lumnitzera
racemosa, S. alba, X. granatum		δ13C = −21‰ to −26‰Mangrove contribution =
42–58%		[116]
Chumphon,
SE Thailand		R. apiculata, A. marina, S. albaδ13C = −24‰ to −26‰Mangrove, algae and
riverine POM		[117]
Okinawa, JapanR. mucronata, B. gymnorrhizaFatty acid analysisGreen macroalgae (Ulva pertusa, Enteromorpha intestinalis), diatoms, bacteria, mangrove POM[118]
Xuan Thuy National Park, VietnamS. caseolaris, K. obovata,
A. corniculatum, A. marina		C:N = 4.5–19.5 (mean = 11.0)
δ13C = −20.4‰ to −27.7‰ (mean = −24.1)		Mixture of mangrove litter and marine phytoplankton[119]
Ishigaki Is,
SW Japan		B. gymnorrhiza, R. stylosaδ13C = −27.0‰ to −29.3‰Below-ground dead roots[120]
Baja California,
Mexico		R. mangleC:N = 35–58
δ13C = −24.6‰ to −25.6‰		Mangrove peat, algal biomass, other coastal plants[121]
Table
Table 5. Blue carbon mass balance in an undisturbed mangrove forest (Mg C ha−1 a−1) based on globally averaged data from Figure 2 and reference [76]. Abbreviations: GPP = gross primary production; RCANOPY = forest canopy respiration; RMICROALGAE = benthic microalgal respiration; RTIDAL WATER = pelagic respiration; RSOIL = benthic respiration (CO2 air + DIC water); ND = no data.
Table 5. Blue carbon mass balance in an undisturbed mangrove forest (Mg C ha−1 a−1) based on globally averaged data from Figure 2 and reference [76]. Abbreviations: GPP = gross primary production; RCANOPY = forest canopy respiration; RMICROALGAE = benthic microalgal respiration; RTIDAL WATER = pelagic respiration; RSOIL = benthic respiration (CO2 air + DIC water); ND = no data.
InputsOutputs
Mangrove GPP20.0RCANOPY8.0
Macroalgal GPP6.2RMACROALGAE2.9
Microalgal GPP4.4RMICROALGAE2.3
Soil DIC production 22.4RTIDAL WATER3.3
Groundwater (land-derived)NDRSOIL6.1
DIC export24.8
DOC export3.8
POC export1.9
Burial1.6
CH4 export0.03
CH4 (air–soil release)0.015
CH4 (air–water efflux)0.012
Total53.0Total54.8
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Alongi, D.M. Lateral Export and Sources of Subsurface Dissolved Carbon and Alkalinity in Mangroves: Revising the Blue Carbon Budget. J. Mar. Sci. Eng. 2022, 10, 1916. https://doi.org/10.3390/jmse10121916

AMA Style

Alongi DM. Lateral Export and Sources of Subsurface Dissolved Carbon and Alkalinity in Mangroves: Revising the Blue Carbon Budget. Journal of Marine Science and Engineering. 2022; 10(12):1916. https://doi.org/10.3390/jmse10121916

Chicago/Turabian Style

Alongi, Daniel M. 2022. "Lateral Export and Sources of Subsurface Dissolved Carbon and Alkalinity in Mangroves: Revising the Blue Carbon Budget" Journal of Marine Science and Engineering 10, no. 12: 1916. https://doi.org/10.3390/jmse10121916

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