Contribution of mangroves to coastal carbon cycling in low latitude seas

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Contribution of mangroves to coastal carbon cycling in low latitude seas Daniel M. Alongi a,∗ , Sandip K. Mukhopadhyay b a b

Australian Institute of Marine Science, PMB 3, Townsville MC, Townsville 4810, QLD, Australia Department of Marine Science, University of Calcutta, 35, B. C. Road, Kolkata 700019, India

a r t i c l e

i n f o

Article history: Received 13 March 2014 Received in revised form 2 October 2014 Accepted 13 October 2014 Available online xxx Keywords: Carbon cycling Coastal ocean Carbon sequestration, Deforestation Mangrove

a b s t r a c t The contribution of mangrove carbon to the coastal ocean in low latitudes was evaluated. Mangrove forests occupy only 2% of the world’s coastal ocean area yet they account for about 5% of net primary production, 12% of ecosystem respiration and about 30% of carbon burial on all continental margins in subtropical and tropical seas. Mangroves also account for nearly one-third of all riverine DIC discharging into low latitude coastal waters. Mangrove forests fix, release and sequester more carbon by area than all other coastal ecosystem types, except perhaps for subtropical and tropical seagrass meadows for which data are lacking. Globally, mangrove waters release to the atmosphere more than 2.5 times (−42.8 Tg C y−1 ) the amount of CO2 emitted from all other subtropical and tropical coastal waters. The global destruction of the large carbon stocks (956 Mg C ha−1 ) of mangroves at the current annual rate of about 1% results in an additional annual release of roughly 133 Tg C y−1 to the atmosphere. Mangroves account for only 0.7% of tropical forest area globally, but their destruction currently adds another 10% to global CO2 release from tropical deforestation. Despite considerable uncertainty upscaling small numbers of measurements with large coefficents of variation, our calculations suggest that mangroves are a globally significant contributor to the carbon cycle in low latitude seas, and to greenhouse emissions resulting from tropical deforestation. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Mangroves function like other forests in exchanging gases with the atmosphere and, like other tidal ecosystems, exchange gases, solutes and particles with the coastal ocean. Because they inhabit the margin between land and sea, mangroves are tightly linked to land, ocean and atmosphere, yet still manage to store carbon and other elements in their biomass and soils. These tidal forests have unique ecological characteristics, but also have some features of both terrestrial and marine ecosystems, that enable them to efficiently utilize and sequester carbon and limiting nutrients (Alongi, 2009; Feller et al., 2010). Mangroves are, on average, highly productive tidal forests utilizing an advantageous strategy of maximizing carbon gain and minimizing water loss with high water-use and nutrientuse efficiencies and low transpiration rates. These physiological mechanisms result in rapid rates of CO2 uptake and respiratory

∗ Corresponding author. Tel.: +61 7 4753 4444. E-mail addresses: [email protected] (D.M. Alongi), [email protected] (S.K. Mukhopadhyay).

release despite living in waterlogged saline soils (Ball, 1988). Unlike other forests, mangroves tidally exchange solutes and particulates, including inorganic and organic particles, with the coastal ocean (Adame and Lovelock, 2011). This pathway usually (but not always) results in net sediment and carbon accumulation. Some of this carbon is buried in forest soils as is some fixed mangrove carbon which is stored in above- and below-biomass, albeit on a much shorter time scale; while some mangrove biomass is buried, most is eventually harvested, destroyed or exported by tides (Alongi, 2014). Recent debate on the possible use and reforestation of mangroves to sequester carbon to offset increasing greenhouse gas emissions (Alongi, 2012; Pendleton et al., 2012; Van Lavieren et al., 2012) has led to renewed interest of the role of mangroves in the coastal carbon cycle, especially with respect to carbon capture (Bouillon et al., 2007a; Breithaupt et al., 2012). Recent calculations indicate that mangroves are indeed a significant store of carbon by area. For instance, based on new carbon biomass and soil measurements to a depth of 1 m in Southeast Asian mangroves, Donato et al. (2011) calculated that mangroves have among the richest carbon stocks compared with other wetland and coastal ecosystems implying that, if extrapolated globally, mangroves are the greatest coastal carbon habitats per area. However, when the reverse

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Fig. 1. Map of the locations and types of subtropical and tropical continental margins inhabited by the world’s mangrove forests. These labelled areas are keyed to the province list in Table 1.

happens and biomass and soils are removed, the resultant carbon gas emissions to the atmosphere is extraordinarily large. While there is little doubt that individual mangrove forests (necessarily sampled over small temporal and spatial scales) are net accumulators of carbon, this paper attempts to answer an unresolved question: to what extent does mangrove carbon flux and storage contribute both regionally and globally to the carbon cycle in subtropical and tropical seas, and does their destruction lead to large losses of CO2 to the atmosphere? 2. Carbon production, CO2 exchange and respiration The subtropical and tropical coastal margins are defined here as consisting of 13 provinces (Fig. 1) as identified by Jahnke (2010) based on boundary currents and climate. These provinces (Table 1) consist of western boundary current (N.W. Atlantic, W. Indian, N.W. Pacific, S.W. Pacific, eastern boundary current (N.E. Pacific), monsoonal (W. and E. Indian) and tropical (W. and E. Atlantic, W. and E. Indian, W. and E. Pacific) ecosystems. Mangrove net primary production, CO2 exchange with the atmosphere, and carbon burial rates will be compared with these same processes in the coastal margin (estuary to shelf edge) of each province. Upscaling of all C values was done using the area estimates in Table 1. Rates of mangrove phytoplankton NPP were multiplied by total mangrove area (150,790 km2 ; Spalding et al., 2010) based on my conclusion from measurements on Google Earth that mangrove creeks and waterways and mangrove-associated inshore waters (up to one km offshore) roughly equal total forest area. The seaward boundary of mangrove waters was set at 1 km offshore, based on the fact that the export of most mangrove material is usually restricted to within that distance offshore (Alongi, 1998).

100% (Alongi, 2009). Alongi (2014) used the average of seven studies (see references and discussion in section 2.5.2 in Alongi, 2009) to derive a global value of 75 Tg C y−1 . I have used this value to estimate total mangrove net primary production (see footnote ‘d’ in Table 1). Given these caveats and assumptions, global mean mangrove NPP equates to roughly 210 (±1 SD = 137) Tg C y−1 with the most productive regions being in the N.W. Atlantic (WBC), E. Atlantic and the tropical western Pacific (Southeast Asia) provinces (Table 1). Whether or not these regions are the most productive is problematical; the magnitude of these values are just as likely to reflect the magnitude of the provincial mangrove areas than the actual rates of NPP; for four provinces (asterisked with a ‘e’ in Table 1) no reliable mangrove NPP data exist so the global average value was used (1204 g C m−2 y−1 ; Table 1). Nevertheless, these crude estimates suggest that mangroves residing in the dry tropics are less productive than those living in the wet tropics, in agreement with ecophysiological studies comparing photosynthetic performances of wet and dry tropical mangroves (e.g., Cheeseman et al., 1997). The empirical database for coastal phytoplankton NPP is much greater than for mangroves but similarly there is considerable uncertainty (Table 1) as annual averages were used to derive these values (Jahnke, 2010). Rates of coastal phytoplankton appear to be fairly uniform across the low latitudes although some of these rates mask clear seasonal patterns. On average, although subtropical and tropical coastal margins account for only 24% of global coastal ocean area, subtropical and tropical phytoplankton account for about 38% of global coastal ocean productivity. Coastal phytoplankton in the low latitudes are smaller in size but more highly productive than their counterparts in higher latitudes. It is therefore not surprizing that mangrove NPP is very small (≈210 Tg C y−1 ) compared with coastal phytoplankton production (≈4250 Tg y−1 ) in the world’s subtropical and tropical waters.

2.1. Net primary production 2.2. Pelagic release of CO2 to the atmosphere Arguably the best and most reliable method to estimate mangrove above-ground net primary production is to combine measurements of litter fall over at least a year and changes in incremental stem growth (as DHB, diameter-at-breast height) over several years (Alongi, 2009). Such estimates are still comparatively few (n < 30), with most measurements performed in the Atlantic, the western Pacific, and Indian Ocean provinces. Despite the sparse data, the global rate of mangrove above-ground NPP (11.1 tDW ha−1 y−1 ) is in good agreement with the global average NPP for tropical terrestrial forests (11.9 tDW ha−1 y−1 ) suggesting that the few empirical mangrove measurements are reasonable estimates. The coefficient of variation is high (CV = 66%), as it is for terrestrial (CV = 55%) systems (Clark et al., 2001). Below-ground mangrove production has been measured less often (n < 10) (Alongi, 2009) due to the difficulty and time consumed in measuring root growth; this of course introduces great uncertainty in regional and global estimates as the CV approximates

Coastal seas in the low latitudes, unlike those in temperate and boreal regions, are a net source of CO2 (−16.2 Tg C y−1 ) to the atmosphere (denoted as negative values in Table 2), reflecting high rates of respiration and supersaturated concentrations of dissolved CO2 ; much of the latter is the result of high discharge of dissolved limestone from river catchments. Many provinces show no net exchange of CO2 . But those regions that do show net exchange are characterized by high levels of discharge from medium and large tropical rivers, such as in the SW Pacific province, where the island of New Guinea discharges huge amounts of freshwater and associated DIC (Table 2). Mangroves have similarly high rates of CO2 flux with the atmosphere (Okimoto et al., 2014). Canopy respiration, the largest component of gas exchange, has until recently been derived by extrapolation from leaf respiration and leaf area indices (Alongi, 2009). Using these leaf data, Alongi (2014) calculated that the

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Table 1 Estimates of coastal net phytoplankton production (NPP) and mangrove above-ground (NPPAG ) + below-ground (NPPBG ) net primary production in subtropical and tropical coastal provinces. All data except those listed in footnotes are from Jahnke (2010). See Fig. 1 for location of each coastal margin province. Subtropical & tropical coastal provinces

Coastal area (km2 × 106 )

NW Atlantic(WBC)—S. Florida/Caribbean Islands to Venezuela W Atlantic (T)—Guyana to SE Brazil E. Atlantic (T)—Senegal to Gabon W Indian (M)—Somalia to W India/Red & Arabian Sea W Indian (T)—Kenya to Tanzania W Indian (WBC)—Mozambique to South Africa E. Indian (M)—E. India to Burma E. Indian (T)—Thai/Malay Peninsula to Java Sea Islands NW Pacific (WBC)—S. Vietnam/S. China Sea to Taiwan W. Pacific (T)—Sunda Sea/Philippine Sea SW Pacific (WBC)—Great Barrier Reef to S.E. Papua New Guinea NE Pacific (EBC)—W. Mexico to N. Panama E. Pacific (T)—S. Panama to Peru Total

1.04

22,717

350

359.3

1080

24.5

0.62 0.18 0.5

11,800 14,184 2649

350 150 1000

215.6 152.4 2043.6

1361 1469 1204e

16.1 20.8 3.2

0.08 0.11 0.62 0.23

1959 5930 13,396 10,246

150 175 300 150

78.6 21.5 186 167.1

1204e 1077 1414 1708

2.4 6.4 18.9 17.5

0.34

12,270

350

119

1140

14.3

2.15 1

30,248 6660

188 150

404.2 150.8

1708 1698

51.7 11.3

0.13 0.1 7.1a

6597 12,135 150,791

345 225

237.7 118.4 4254.2c

1204e 1204e

7.9 14.6 209.6

a b c d e

Mangrove areab (km2 )

Coastal NPP (g C m−2 yr−1 )

Total coastal NPP (Tg C yr−1 )

Mangrove NPPAG + NPPBG d (g C m−2 yr−1 )

Total mangrove NPP (Tg C yr−1 )

24% Of global coastal ocean area. From country estimates in Spalding et al. (2010). 38% Of global coastal ocean NPP. Above-ground net primary production (NPPAG ) from Table 2.9 in Alongi (2009) and assuming that NPPBG = 36% of NPPAB , calculated from Fig. 5 in Alongi (2014). Global mean mangrove NPPAG + NPPBG , from Fig. 5 in Alongi (2014) was used due to lack of empirical data for this province.

world’s mangrove canopies (plus algae) respire 425 Tg C y−1 or 4413 g C m−2 y−1 ). On average, nearly 70% of GPP is respired back to the atmosphere by the canopy + algae, in general agreement with data from tropical humid forests (Luyssaert et al., 2007). The CV for these mangrove data is 48%. Despite the considerable uncertainty, tropical humid forests (for which a much more extensive database exists) respire back roughly a similar percentage (75%) of GPP (Litton et al., 2007; Luyssaert et al., 2007). These global estimates must be considered cautiously, given the lack of empirical measurements of mangrove forest GPP and R. Fortunately, despite some serious problems, technological advances have now made it possible to measure whole-forest CO2 dynamics using atmospheric methods (see critical review of Rivera-Monroy et al., 2013). These methods operate on the premise that eddies

of upward- and downward-air parcels transport gases across the forest-atmosphere boundary; net gas flux is estimated from highfrequency measurements as the covariance between changes in vertical wind velocity and the mixing ratios of gases. A negative covariance denotes a net flux from the atmosphere to the forest (CO2 uptake) while a positive covariance indicates CO2 release from the forest. These measures incorporate GPP and R, and provide a value for a given forest of net ecosystem exchange (NEE) which entails the sum of the exchange between the forest and atmosphere (Rivera-Monroy et al., 2013). Another source of gas exchange with the atmosphere is respiration in mangrove creeks and waterways which has only recently emerged as an important pathway of carbon loss. Pelagic respiration averages 70.5 mmol C m−2 d−1 , ranging from

Table 2 Estimates of coastal CO2 air-sea exchange and mangrove CO2 air-sea exchange in subtropical and tropical coastal provinces. All data in first two columns are derived from Jahnke (2010). See Fig. 1 for location of each coastal margin province. Subtropical & tropical coastal provinces

Coastal CO2 -air-sea exchange (g C m−2 yr−1 )

Total coastal CO2 -air-sea exchange (Tg C yr−1 )

Mangrove CO2 -air-sea exchangea (g C m−2 yr−1 )

Total mangrove CO2 -air-sea exchange (Tg C y−1 )

NW Atlantic(WBC)— S. Florida/Caribbean Islands to Venezuela) W Atlantic (T)—Guyana to SE Brazil E. Atlantic (T)—Senegal to Gabon W Indian (M)—Somalia to W India/Red & Arabian Sea W Indian (T)—Kenya to Tanzania W Indian (WBC)—Mozambique to South Africa E. Indian (M)—E. India to Burma E. Indian (T)—Thai/Malay Peninsula to Java Sea Islands NW Pacific (WBC)—S. Vietnam/S. China Sea to Taiwan W. Pacific (T)—Sunda Sea/Philippine Sea SW Pacific (WBC)—Great Barrier Reef to S.E. Papua New Guinea NE Pacific (EBC)—W. Mexico to N. Panama E. Pacific (T)—S. Panama to Peru Total

−8.2

−8.44

−136.2

−3.1

0 0 −4.5

0 0 −2.25

−766.8 −189.6b −189.6b

−9.1 −2.7 −5

0 −3.24 1.3 0

0 −3.51 0.81 0

−144.0 −39.6 −292.8 −189.6b

−2.8 −2.3 −3.9 −1.4

1.1

−297.6

−3.7

−0.68 −3.24

−525.6 −523.2

−1.6 −3.5

0 0 −16.21

−189.6b −189.6b

−1.3 −2.4 −42.8

a b

3.24 −0.32 −3.24 0 0

From regional values in Table 6.2 in Alongi (2009). Global mean CO2-air-sea exchange derived from Table 6.2 in Alongi (2009) was used due to lack of empirical data from this province.

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Table 3 Estimates of coastal organic carbon sedimentation and burial rates, and total mangrove organic carbon burial rates in subtropical and tropical coastal provinces. All data except those listed in footnotes are from Jahnke (2010). See Fig. 1 for location of each coastal margin province. Total sedimentation (Tg C y−1 )

Total coastal C burial (Tg C yr−1 )

Total C burial in mangrovesg (Tg C yr−1 )

Subtropical & tropical coastal margins

Sedimentation rate (g C m−2 yr−1 )

NW Atlantic (WBC)—S. Florida/Caribbean Islands to Venezuela) W Atlantic (T)—Guyana to SE Brazil E. Atlantic (T)—Senegal to Gabon W Indian (M)—Somalia to W India/Red & Arabian Sea W Indian (T)—Kenya to Tanzania W Indian (WBC)—Mozambique to South Africa E. Indian (M)—E. India to Burma E. Indian (T)—Thai/Malay Peninsula to Java Sea Islands NW Pacific (WBC)—S. Vietnam/S. China Sea to Taiwan W. Pacific (T)—Sunda Sea/Philippine Sea SW Pacific (WBC)—Great Barrier Reef to S.E. Papua New Guinea NE Pacific (EBC)—W. Mexico to N. Panama E. Pacific (T)—S. Panama to Peru Total

2.04

2.1

0.24b

0.25

−3.95h

3.6 6.12 7.08

2.23 1.1 3.54

0.72c 1.2c 0.6b

0.45 0.22 0.30

−2.05 −2.47 −0.46

3.6 3.6 7.08 3.6

0.29 0.4 4.4 0.8

0.36b 0.24b 1.44d 0.6e

0.03 0.03 0.89 0.14

−0.34 −1.03 −2.33 −1.78h

2.04

0.7

0.24b

0.082

−2.13h

3 1.44

6.45 1.44

0.6e 0.12b

1.29 0.12

−5.26h −1.16h

6.12 7.08

0.8 0.71 24.96a

0.6b 0.6b

0.08 0.06 3.942f

−1.15 −2.11 26.22

Carbon burial rate (g C m−2 yr−1 )

a

13% Of total C sedimentation in the global coastal ocean. Derived by multiplying the sedimentation rate by the mean percentage burial efficiency (9%) on the Great Barrier Reef shelf (Alongi et al., 2007, 2008) based on similar sedimentary facies in this province (Burk, 1974). c Derived by multiplying the sedimentation rate by the percent burial efficiency (19%) on the Amazon shelf (Aller et al., 1996) based on similar sedimentary facies in this province (Burk, 1974). d Derived by multiplying the sedimentation rate by the percent burial efficiency (20%) in the Gulf Papua, Papua New Guinea (Aller et al., 2008) based on similar sedimentary facies in this province (Burk, 1974). e Derived by multiplying the sedimentation rate by the percent burial efficiency (18%) in the Aru Sea, Indonesia (Alongi et al., 2012; unpublished data) based on similar sedimentary facies in this province (Burk, 1974). f 10% Of total C burial in the global coastal ocean. g A global mean carbon burial rate of 173.9 g C m−2 yr−1 (Alongi, 2014) was used due to lack of empirical data for most provinces, and multiplied by provincial mangrove area, except for values denoted by ‘h’ where empirical data exist (see references for these data in Alongi, 2012). b

8–292 mmol C m−2 d−1 , and correlates most often with chlorophyll standing stocks, temperature, dissolved and particulate nutrient concentrations, grazing intensity, bacterioplankton growth rates and substrate availability (see references in Section 4.5 in Alongi, 2009). These high rates of pelagic respiration lead directly to supersaturated conditions with respect to CO2 and, as measured beginning only last decade, to significant emissions of CO2 to the atmosphere (Borges et al., 2003; Bouillon et al., 2003; Koné and Borges, 2008; Ralison et al., 2008; Zablocki et al., 2011). These emissions from mangrove waters average 43 mmol C m−2 d−1 (CV = 93%), varying in synchrony with the tides and somewhat also with seasonal changes in water temperature and rainfall. These values are disproportionate to the small areas of mangrove creeks and waterways so the total net relese of 428 Tg C y−1 is more than twice the net emissions (−16.2 Tg C y−1 ) from the tropical coastal ocean (Koné and Borges, 2008; Jahnke, 2010). As we shall see in Section 3.2, this pathway of CO2 release from mangrove waters represents a large proportion of the carbon metabolized in mangrove ecosystems.

2.3. Sedimentation and burial Static measurements of carbon stocks in mangrove forests and soils give us some perspective on the long-term ability of these ecosystems to store carbon, but only flux measurements of actual deposition rate of sediment and associated carbon particles, and separate measures of total soil carbon decomposition, export and consumption (CLOSSES ) can provide us with a carbon burial rate (CBURIAL ), CBURIAL = CDEPOSITION − CLOSSES

(1)

Sedimentation must not be confused with burial. Mangroves actively and passively capture particles, so the rate of sediment deposition depends on a number of factors, such as the tidal prism, tree densities, baroclinic circulation, particle concentrations and size spectra in the water column, flocculation and mucus production, and disaggregation processes, such as turbulence (Wolanski, 1995; Mazda et al., 1999). Methods that integrate these processes over time (e.g., radionuclides) are favored over shorter-term methods to measure rates of particle accumulation. Mangrove soils accrete at rates of 0.1 to 10.0 mm y−1 (Alongi, 2012; Breithaupt et al., 2012) averaging 5 mm y−1 (median = 2.7 mm y−1 ) with frequency of tidal inundation being the main driver of sedimentation. In many cases, however, vertical accretion resulting from belowground root growth and peat accumulation is greater than particle accumulation (McKee, 2011). Currently, measured rates of sediment accretion show that mangroves are on average outpacing the rate of sea-level rise (Alongi, 2008). However, the global mean rate of 5 mm y−1 masks the reality that sediments accreting at a particular location are often derived from eroding mangroves within the same estuary or embayment. In that sense, accretion rates measured from a few cores in a mangrove forest can be overestimates of true accumulation on a larger, whole-estuary scale. Further, natural subsidence and changes in sea level over long timescales play a major role in fostering changes in vertical accretion and surface elevation and thus long-term changes in sedimentation (Krauss et al., 2010; Sanders et al., 2010; LópezMedellín et al., 2011; Smoak et al., 2013). Global mean burial rates of 134, 211 and 163 g C m−2 y−1 were calculated by Bouillon et al. (2007a), Alongi, 2009 and Breithaupt et al. (2012) independently. Carbon burial rates correlate significantly with accretion rates (linear regression r = 0.73; P < 0.01) but the lack of a perfect fit reflects the reality of wide variations in

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mineralization efficiency and site-to-site variations in soil C content. Nevertheless, using the average of the three estimates, Alongi (2014) calculated a mean global burial rate of 24 Tg C y−1 . I used this value to estimate regional carbon burial in mangroves (last column, Table 3) where the empirical data is either nonexistent or miniscule (e.g., derived from 1–2 sediment cores); other regions have sufficient data to derive a true (or as true as possible) burial figure (see references for these provinces in Alongi, 2012). Like the previous C data discussed earlier, the highest C burial occurs in provinces of the wet tropics and/or where river discharge is a dominant feature, for example, in the W. Pacific (T) and NW Atlantic (WBC) regions. Globally, carbon burial in mangroves sums to 26.2 ± 4.9 Tg C y−1 (Table 3). Burial of carbon in mangroves is much greater than in coastal margin sediments of the subtropics and tropics (Table 3). Coastal carbon burial rates derived by multiplying the sedimentation rates from Jahnke (2010) by burial efficiencies on some tropical shelves (see footnotes ‘b’ to ‘e’, Table 3) show low rates of burial to the extent that only 13% of sedimentation and 10% of carbon burial in the global coastal ocean occurs in the low latitudes (Table 3). There are many reasons for this phenomenon of low carbon burial. First, there is little sedimentation of dead phytoplankton cells to the seabed because warm-water phytoplankton communities are dominated by pico- rather than net-sized organisms, the remains of which settle more quickly to the seabed (Alongi, 1998). Second, most tropical subtidal sediments are poised for suboxic diagenesis of organic matter with microbial pathways dominated by ironand manganese-reducing bacteria rather than sulfidic flora (Alongi et al., 2012). Such deposits often have vertically extended zones (2–3 m deep) of intense bacterial decomposition of sedimentary organic carbon (Aller et al., 1996, 2008). These diagenetic conditions result in coastal margin sediments in the low latitudes acting as efficient ‘incinerators’ of organic carbon with the net result being little burial of carbon (Aller et al., 1996, 2008).

3. Forest-coastal ocean exchange 3.1. Tidal exchange of mangrove POC and DOC Most of the data on tidal exchange of mangrove carbon are of particulate litter, the net result of much research effort on the contribution of wetlands to estuarine outwelling and subsequent fertilization of the coastal ocean. The reality of their contribution to coastal productivity is much more complex than originally envisioned, but still, few studies have measured dissolved carbon exchange to give a more complete picture of tidal export. We do know that most, but not all, mangroves export carbon because ebb tides tend to be stronger than flood tides, and in most instances, carbon concentrations are greater in mangrove waters compared to offshore, leading to strong concentration gradients. The longterm drivers of litter export are rainfall and temperature as these factors impact directly on mangrove productivity; both parameters account for 77% of litterfall variability around the globe (Adame and Lovelock, 2011). Roughly one-half of mangrove litterfall (POC) is exported, averaging 202 g C m−2 y−1 or 28 ± 21 Tg C y−1 (Alongi, 2014). Most of mangrove POC as well as DOC exported (15 ± 13 Tg C y−1 ; Alongi, 2014) is ordinarily restricted to 1–2 km offshore due to local geomorphology, hydrodynamics within mangrove estuaries (e.g., high salinity plugs) and coastal hydrodynamics, especially the presence of a coastal boundary zone which effectively traps material inshore (Alongi, 1998). The rate and distance of transport varies seasonally; in the wet season, these hydrodynamic traps break down when large quantities of freshwater are discharged. The origin of DOC has been deducted

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Table 4 Contribution by mangroves to DIC, DOC and POC discharge from the world’s lowlatitude rivers to the coastal ocean. River data from Huang et al. (2012). Mangrove data from Fig. 5 in Alongi (2014). Carbon source

Rivers (Tg C yr−1 )

Mangroves (Tg C yr−1 )

Percent mangrove contribution (%)

POC DOC DIC

127.6 133.9 210.5

28 15 86

18 10 29

from clear isotope signatures measured over tidal cycles, with mangrove DOC leaving the estuary during ebb tide, and marine DOC entering mangrove waterways on the flood tide (Schories et al., 2003; Bouillon et al., 2003, 2007b). 3.2. The ‘new’ DIC pathway Global carbon budgets produced by Bouillon et al. (2007a) and Alongi (2009) revealed that a significant amount of mangrove carbon production (112 Tg C y−1 and 160 Tg C y−1 , respectively) was either unaccounted for or unable to be identified as a specific output to close their budgets. Both papers suggested that this ‘missing’ carbon was exported as DIC via subsurface pathways. Alongi (2009) indicated that this was a reasonable idea because earlier data (e.g., Alongi et al., 2001) showed that (1) microbial decomposition occurs to at least 1 m soil depth so it is unlikely that the resultant CO2 and DIC produced would flow across the surface soil–air interface; (2) the sum of individual soil metabolic measurements (sulfate and metal reduction, methanogenesis, denitrification and aerobic respiration) are often much greater than the rate of carbon metabolism measured at the soil surface, especially in macrotidal environments; and (3) visual observations suggest significant lateral drainage of interstitial water during ebb tides. The sedimentary deposits that compose the forest floor are heavily populated by various microbial flora and invertebrates, such as ocypodid and sesarmid crabs and gastropods, that modify, eat and thoroughly bioturbate and riddle these deposits with wastes, tubes, mounds and burrows. Further, the forest floor has many cracks and fissures, and is thoroughly impregnated by roots and root hairs releasing oxygen and taking up dissolved solutes. The net result is that the forest floor acts like a sponge being drained and replenished by tides with water, dissolved gases and solutes. These physical and biological structures and activities result in a virtual, meters-thick mud cake containing high concentrations of metabolites such CO2 , DIC and NH4 . The production and transport of these metabolites were thought to be in steady-state, percolating up from deep soils to be released continuously at the soil surface, but recent evidence shows that the bulk of these solutes and gases are transported laterally by groundwater, seepage and tidal advection rather than as surface runoff (Miyajima et al., 2009; Alongi et al., 2012; Abril et al., 2013; Maher et al., 2013; Alongi, 2014). Subsurface transport of groundwater mixed with mangrove interstitial water is controlled by a number of physical forces (Mazda and Ikeda, 2006) that result in interstitial water oozing out through the bottom soil and often seen at low tide as water running down seepage channels or shallow gullies and emptying into adjacent waterways. In a test of this ‘missing carbon’ subsurface pump, Maher et al. (2013) measured concentrations and stable isotopic values of DIC, DOC, POC as well as 222 Rn (a tracer of groundwater) over tidal cycles in a mangrove tidal creek. They found that 93–99% of the DIC and 89–92% of the DOC exported from the creek was due to groundwater advection at rates equivalent to the missing carbon, when extrapolated to global mangrove area. The transport of this material also explains why adjacent mangrove waterways are supersaturated in CO2 and CH4 which leads to additional flux of metabolic

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Table 5 Total NPP, R, and burial of organic carbon and the percentage contribution of each ecosystem to the carbon cycle of the subtropical and tropical coastal seas. Ecosystem

Area (km2 )

NPP (Tg C yr−1 )

R (Tg C yr−1 )

Burial (Tg OC yr−1 )

Mangrove Seagrass Coral reef Coastal ocean Total

150,791 (1.9%) 360,000 (4.4%)a 527,027 (6.5)e 7100,000 (87.2%) 8137,818

209.6 (4.8%) 294.0 (6.8%)b 78.1 (1.8)c 4254.2 (86.6) 4332.3

623.5 (12.3%) 273.6 (5.4%)c 827.2 (16.3)c 3335.0 (66.0)g 5059.3

26.2 (30.4%) 53.0 (61.6%)d 3.0 (3.5%)f 3.9 (4.5%) 86.1

a Median of range of global seagrass area in Fourqurean et al. (2012) adjusted to percentage area (80%) of subtropical and tropical seagrasses in total global ocean area (Green and Short, 2003). b From mean NPP estimate in Mateo et al. (2006). c From Table 3 in Alongi (2014). d From mean burial value in Table 2 in Alongi (2014). e From Mora et al. (2006). f Value from Kinsey and Hopley (1991) . g Derived from mean coastal pelagic and benthic respiration rate values in del Giorgio and Williams (2005).

carbon to the atmosphere (see Section 2.2). The world’s mangroves transport 86 Tg C y−1 to adjacent coastal waters, with this estimate determined by difference in closing the latest mangrove C budget (Alongi, 2014) and seems reasonable in being considerably greater than the export of POC and DOC from mangroves, and in good agreement with the results of the above-mentioned empirical studies. How do these export numbers compare with carbon exported from the world’s subtropical and tropical rivers? Using the recent estimates for river export from Huang et al. (2012) and our mangrove estimates, export of mangrove DOC and POC contributes only 10% and 18% of total discharge to the subtropical and tropical seas (Table 4). However, mangroves are a large source of coastal DIC, accounting for nearly one-third (29%) of all riverine DIC discharge to the low latitude oceans (Table 4). 4. Global significance of mangrove carbon The significance of mangroves to the coastal ocean carbon cycle was assessed by comparing mangrove carbon fluxes with those of other major coastal habitats and with those calculated most recently for the coastal ocean (Bauer et al., 2013). While mangroves occupy only 1.9% of the world’s subtropical and tropical coastal ocean area (Table 5), they account for about 5% of NPP, 12% of R, and about 30% of carbon burial on low latitude continental margins. Mangroves are the world’s highest producers of fixed carbon per unit area in the ocean (Alongi, 2009), but their small global extent limits their contribution compared with more numerous seagrasses and coastal phytoplankton communities. And although coral reefs occupy roughly half a million square km of the coastal ocean, they are largely self-contained and well-balanced metabolically, accounting for only about 2% of NPP and 3–4% of burial of organic carbon, although they do account for a large share (16%) of coastal and shelf respiration. Rates of carbon storage in mangroves are, on average, high compared with other coastal habitats, with similar burial rates in salt marshes and seagrass beds (Alongi, 2009, 2014). The largest uncertainty in these estimates is the area of subtropical and tropical seagrass beds; their areal extent is highly uncertain as is their carbon contribution to the coastal ocean (Fourqurean et al., 2012). If their global area is at the high end (800,000 km2 ) of the area estimated by Fourqurean et al. (2012), then they are clearly the greatest carbon contributors other than phytoplankton to subtropical and tropical seas. However, assuming a median areal estimate of 360,000 km2 (see footnote ‘a’ in Table 5), they contribute at least about 7% to NPP, 5% to R, but can still account for more than half (≈60%) of the carbon storage in low latitude seas. Seagrasses may thus be greater contributors to the coastal carbon cycle, but the main importance of mangrove carbon may lie in its eventual fate, given that mangroves store more carbon per unit area (956 Mg C ha−1 ) than salt marshes (593 Mg C ha−1 ), seagrasses

(142 Mg C ha−1 ), peat swamps (408 Mg C ha−1 ) and rain forests (241 Mg C ha−1 ) (Donato et al., 2011; Alongi, 2014). A simple calculation shows that assuming an annual global deforestation rate of 1% (Van Lavieren et al., 2012) and further assuming that all mangrove carbon is completely removed and oxidized upon clearing (to a soil depth of 1 m), approximately 133 Tg C is returned annually to the atmosphere, which is nearly six times as much carbon as is stored in mangroves annually. Lovelock et al. (2011) estimated CO2 losses of 210–2900 Mg C km−2 y−1 from mangrove peat clearing and conversion, whereas Donato et al. (2011) calculated an annual range of CO2 emissions of 112–392 Mg C ha−1 , giving a potential global emissions range of 20–120 Tg C y−1 . Pendleton et al. (2012) estimated even greater mangrove emissions of 90–970 Tg C y−1 . My estimate and those of Donato et al. (2011) equate to about 2–10% of global deforestation emissions and those of Lovelock et al. (2011) may account for up to 50% of emissions from tropical peat lands. With respect to the role of mangroves in contributing to greenhouse emissions resulting from land-use change, we calculated that despite the fact that mangrove area equals only 0.7% of tropical terrestrial forest area (mangroves: 150,800 km2 ; tropical forests: 19,490,000 km2 , Pan et al., 2011), mangrove emissions derived from clearing are equivalent to 10% of emissions from tropical deforestation (1.3 Pg C y−1 , Pan et al., 2011). This calculation means that destruction of one hectare of mangrove forest results in 14 times more CO2 released back to the atmosphere than does destruction of one hectare of tropical humid forest. All of these calculations therefore suggest that mangroves are a globally significant contributor to the carbon cycle of the tropical ocean and to greenhouse emissions resulting from tropical deforestation. 5. Conclusions Major ecosystem characteristics of mangrove carbon cycling, such as the allocation of fixed carbon into biomass and patterns of respiratory CO2 release, are strikingly similar to tropical humid forests, with the largest fluxes of CO2 being between the forest canopy and the atmosphere, and with nearly identical rates of NPP. These similarities are useful in that they provide a baseline in deciding whether or not extrapolated mangrove fluxes seem reasonable. Mangrove NPP equates to only about 5% of coastal phytoplankton production in low latitude seas. Nevertheless, they store more about 6 times more carbon (26 Tg C yr−1 ) than is buried in sediments (≈4 Tg C yr−1 ) of subtropical and tropical coastal margins. The export of mangrove-derived POC, DOC and DIC accounts for 18%, 10% and nearly one-third (29%) of tropical river discharge of these compounds globally. Despite considerable uncertainty in extrapolating regionally and globally, mangrove waters release to the atmosphere more than 2.5 times the amount of CO2 (−16 Tg C y−1 ) released from all other subtropical and tropical coastal waters.

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