Review

Carbon Cycling in the World’s Mangrove Ecosystems

Revisited: Significance of Non-Steady State
Diagenesis and Subsurface Linkages between the
Forest Floor and the Coastal Ocean
Daniel M. Alongi
Tropical Coastal & Mangrove Consultants, 52 Shearwater Drive, Pakenham, VIC 3810, Australia;
dmalongi@[Link]; Tel.: +61-471448687




Received: 6 August 2020; Accepted: 7 September 2020; Published: 10 September 2020


Abstract: Carbon cycling within the deep mangrove forest floor is unique compared to other marine
ecosystems with organic carbon input, mineralization, burial, and advective and groundwater
export pathways being in non-steady-state, often oscillating in synchrony with tides, plant uptake,
and release/uptake via roots and other edaphic factors in a highly dynamic and harsh environment.
Rates of soil organic carbon (CORG ) mineralization and belowground CORG stocks are high, with rapid
diagenesis throughout the deep (>1 m) soil horizon. Pocketed with cracks, fissures, extensive roots,
burrows, tubes, and drainage channels through which tidal waters percolate and drain, the forest
floor sustains non-steady-state diagenesis of the soil CORG, in which decomposition processes at
the soil surface are distinct from those in deeper soils. Aerobic respiration occurs within the upper
2 mm of the soil surface and within biogenic structures. On average, carbon respiration across
the surface soil-air/water interface (104 mmol C m−2 d−1 ) equates to only 25% of the total carbon
mineralized within the entire soil horizon, as nearly all respired carbon (569 mmol C m−2 d−1 ) is
released in a dissolved form via advective porewater exchange and/or lateral transport and subsurface
tidal pumping to adjacent tidal waters. A carbon budget for the world’s mangrove ecosystems
indicates that subsurface respiration is the second-largest respiratory flux after canopy respiration.
Dissolved carbon release is sufficient to oversaturate water-column pCO2, causing tropical coastal
waters to be a source of CO2 to the atmosphere. Mangrove dissolved inorganic carbon (DIC) discharge
contributes nearly 60% of DIC and 27% of dissolved organic carbon (DOC) discharge from the world’s
low latitude rivers to the tropical coastal ocean. Mangroves inhabit only 0.3% of the global coastal
ocean area but contribute 55% of air-sea exchange, 14% of CORG burial, 28% of DIC export, and 13%
of DOC + particulate organic matter (POC) export from the world’s coastal wetlands and estuaries to
the atmosphere and global coastal ocean.

Keywords: biogeochemistry; carbon; carbon cycling; coastal ocean; export; non-steady-state;

mangrove; mangrove carbon budget; moil; subsurface transport

1. Introduction
Mangrove forests have the largest organic carbon (CORG ) stocks of any tropical terrestrial or
marine ecosystem [1,2], with a global mean total forest stock of 738.9 ± 27.9 (±1 standard error, SE)
Mg CORG ha−1 , of which 76.5% is stored in the soil, 14.8% vested in aboveground biomass and the
remaining 8.7% vested in belowground roots [3]. These large amounts of organic carbon reflect high
mangrove primary productivity, equal to those of tropical humid evergreen forests and coral reefs [2]
and rapid rates of soil accretion on the forest floor.

Forests 2020, 11, 977; doi:10.3390/f11090977 [Link]/journal/forests

Forests 2020, 11, 977 2 of 17

Mangroves function like other forested ecosystems in exchanging gases with the atmosphere but
are like other coastal tidal wetlands in exchanging gases and dissolved and particulate materials with
adjacent coastal waters. Mangrove ecosystems are thus tightly linked to land, ocean, and atmosphere,
yet still, store vast quantities of CORG and other elements in their soils and forest biomass.
While mangroves have some features of both terrestrial and coastal ecosystems, they do have a
number of unique ecological and physiological characteristics [4] that enable them to efficiently utilize
and sequester carbon and nutrient elements, especially nitrogen, phosphorus, iron, and copper [5,6].
The biogeochemical connections between mangroves and adjacent tidal waters are complex,
with variable concentrations of dissolved organic and inorganic solutes and particulates imported
and exported by both tides, porewater pumping, and subsurface groundwater advection [7].
Tidal circulatory processes, such as a pronounced asymmetry between ebb and flood tides (with the
ebb tide being shorter in duration but with stronger current velocity than the flood tide); friction,
flow resistance, drag of tidal waters due to the presence of aboveground and belowground structures,
lateral trapping (water flowing in and out of a waterway is temporarily retained in the forest to be
returned to the main channel later), and lateral gradients due to high evapotranspiration [8]. Interrelated
processes exert control over sediment transport and deposition: (1) tidal pumping, (2) baroclinic
circulation, (3) particle trapping in the turbidity maximum, (4) flocculation, (5) the mangrove tidal
prism, (6) physiochemical reactions that destroy cohesive flocs, and (7) microbial production of mucus.
Sedimentation of particles is often rapid in quiescent mangrove environments, resulting in a global
mean carbon sequestration rate of 179.6 ± 16.4 gC m−2 a−1 [3]. Over decades, after initial colonization
of a mudflat, the forest develops and the floor builds up further, adjusting to sea-level, subsidence,
and uplift, with the net result being several meters of soil [9]. Over time, these deposits are penetrated
further by mangrove trees and their extensive root systems, various other flora (e.g., microalgae) and
fauna, especially burrowing crabs, and highly abundant and productive microbial communities [10].
The forest floor is thus ordinarily pockmarked with mounds, burrows, tubes, cracks, fissures, coarse
and fine living and dead roots and root hairs, and layered with decayed wood, litter, crawling epifauna,
and various forms of micro- and macroalgae. Mangrove deposits contribute about 30% to carbon
storage on the coastal margins in subtropical and tropical latitudes [11]
Mangrove ecosystems similarly contribute a disproportionate share of various forms of carbon to
the coastal ocean in low latitudes. Although they occupy only 1.5% of the world’s subtropical and
tropical coastal ocean area, mangroves account for about 5% of net primary production and 12% of
ecosystem respiration. How much mangrove particulate carbon (i.e., litter) is exported to adjacent
waters is well-known [7,12], but how much mangrove ecosystems contribute to dissolved inorganic
carbon (DIC) discharging into low latitude coastal waters is unclear [11], as are the amounts of carbon
gases released from mangrove waters to the atmosphere. How much soil carbon is mineralized
throughout the entire soil horizon is poorly understood, with the current knowledge based mostly
on measurements of oxygen consumption and DIC and CO2 production at the surface soil-air/water
interface. The functional link between these processes within the forest floor and the adjacent coastal
zone has remained similarly unquantified until only very recently [13].
This paper critically examines the traditionally measured rates of soil respiration and compares
these data with rates of belowground DIC production, highlighting any discrepancies to accurately
estimate rates of CORG mineralization throughout the deep forest floor. This information is then
compared with recent estimates of DIC export via subsurface pathways to determine its significance in
mangrove carbon cycling and the functional links between the mangrove forest floor and the adjacent
coastal ocean. A revised carbon mass balance for the world’s mangroves is then presented to identify
the major and minor pathways of carbon flow as well as what further empirical measurements are
needed to improve our knowledge of carbon balance in these tidal ecosystems
Forests 2020, 11, 977 3 of 17

2. Rates of Surface and Subsurface Soil CORG Mineralization

Microbial decomposition of soil organic matter in mangroves involves several anaerobic diagenetic
reactions and transport processes. Once oxygen is depleted in surface soils (upper 2 mm) by aerobic
respiration, several groups of anaerobic bacteria decompose soil organic carbon via the reduction of
sulfate, iron, and manganese, production of methane (methanogenesis); the production of gaseous
nitrogen (denitrification) also occurs but are ordinarily minor carbon decomposition processes [14].
However, the availability of organic carbon molecules for anaerobic microbial breakdown requires
prior fermentation to generate low molecular weight organic substrates, such as lactate, butyrate,
propionate, and acetate. Which reaction dominates early diagenesis depends on several drivers, such as
geomorphologic setting, salinity, frequency of tidal inundation, temperature, the degree of freshwater,
marine and terrestrial inputs, root physiological activities, the quantity and quality of organic matter,
the intensity of disturbance from benthic organisms (i.e., bioturbation), and accretion rates [14,15] as
does forest age, soil CORG and nutrient content, tree densities, and mangrove species composition.
Soil properties vary widely among mangrove forests, and although these soils are often described
as highly reducing and sulfidic, most forest deposits cannot be so simplistically described [15].
Soil texture and associated physicochemical properties depend on the nature of the environment
(quiescent or physically dynamic), the distribution of trees and their roots, geomorphology, rainfall,
and the source of the organic matter and parent rock. Forests located in large river deltas and in
quiescent areas most often possess soils that are predominantly well-sorted silt and clay, with large
quantities of fibrous root matter; higher concentrations of sand occur in soils in forests in more active
locations, such as swift-flowing rivers. Below a thin veneer of oxidized surface soil, animal burrows,
and tube walls, mangrove soils are usually suboxic (no free oxygen but solutes with bound oxygen,
e.g., nitrate) and anoxic (no oxygen), but rarely sulfidic (containing HS− , H2 S); sulfidic zones occur
where roots and other biogenic structures are absent and commonly where there are large surface
deposits of litter, especially leaves and clumps of dead roots. In subsurface soils to a depth of 1 m,
redox potential (Eh) is usually within the range of −200 to +300 mV [15]. In short, there is no one
simplistic definition of what constitutes mangrove soil.

2.1. Respiration at the Soil Surface

Aerobic decomposition of labile CORG at and near the soil surface usually occurs rapidly, resulting
in O2 rarely penetrating more than 2 mm into the soil. Except for translocation of O2 into deeper
soils via tree roots and crab burrows, most decomposition is suboxic and/or anoxic. Measurements of
dissolved and gaseous O2 consumption across the forest floor surface are common as the methodology
is comparatively simple, especially with technological advances in the sensitivity and stability of oxygen
probes; gas measurements are somewhat more complex, requiring the need for gas chromatography.
The notion that measurements of O2 consumption and CO2 and DIC release at the soil/sediment
surface in aquatic sediments reflect carbon mineralization within the entire soil/sediment deposit
assumes that (1) the molecular diffusion of these solutes from the sediment/soil surface is constant;
(2) in the case of oxygen, most of the O2 is driven by oxidation of reduced metabolites (e.g., HS− ,
Fe2+ ) diffusing from deeper sediment layers, thus represents total carbon oxidation within the deposit;
and (3) these measurements assume steady-state diagenetic conditions, that is, that the rate of molecular
diffusion of gases and solutes from soils/sediments to overlying waters or the atmosphere is constant.
Non-steady state conditions mean that the rate of diffusion is a function of time (i.e., it changes
with time).
Rates of O2 and dissolved oxygen (DO) consumption and DIC and CO2 release from
mangrove soils (Figure 1) were rapid compared with those from other estuarine and marine benthic
environments [10,16]. Rates of O2 consumption in exposed soils were significantly higher than DO
consumption rates from inundated soils (one-way analysis of variance on rank and Dunn’s method
for multiple comparisons; Dunn’s Q = 3.051). Similarly, rates of CO2 release from exposed soils were
higher than rates of DIC release from inundated soils (Dunn’s Q = 2.701). Rates of DO and DIC
Forests 2020, 11, 977 4 of 17

fluxes across inundated soils were significantly different, with higher DIC fluxes (Dunn’s Q = 2.739).
Forests 2020, 11, x FOR PEER REVIEW 4 of 17
In contrast, differences in O2 and CO2 gas fluxes were not significantly different (Dunn’s Q = 1.891).
The mean
soils was respiratory
1.73 ± 0.35. quotient
O2 and(RQ)
CO2for inundated
fluxes soils wassoils
from exposed ± 0.24more
1.83 were (±1 SE) andasthe
rapid RQ for
gases exposed
diffuse more
soils was 1.73 ± 0.35.
quickly than solutes. 2 O and CO 2 fluxes from exposed soils were more rapid as gases diffuse more
quickly than solutes.

2500

O2 (inundated)
O2 (exposed)
Mangrove soil respiration (mg C m -2 d -1 )

CO2 (inundated) 1868.8 (n = 139)

2000 CO2 (exposed)
1636.3 (n =72)

1500
1258.3 (n = 65)

1000 867.5 (n =106)

500

0
O2 CO2

Figure 1. Mean (±1 standard error) rates of dissolved and gaseous oxygen consumption and dissolved
Figure 1.
inorganic Mean(DIC)
carbon (±1 standard error)
production andrates
CO2of dissolved
release and
(mg C gaseous
m−2 oxygen
d−1 ) from consumption
tidally andexposed
inundated and dissolved
inorganic carbon( DIC) production and CO 2 release (mg C m−2 d−1) from tidally inundated and exposed
mangrove soils, respectively. Field measurement and soil incubation data from references [17–54] were
mangrove
obtained fromsoils, respectively.
searches Field
of the Web measurement
of Science and Scholar.
and Google soil incubation data from references [17–54]
were obtained from searches of the Web of Science and Google Scholar.
2.2. Rates of DIC Production within the Forest Floor
2.2. Rates of DIC Production within the Forest Floor
The production of respired CO2 by microbial communities in mangrove soils has been measured
using aThesimple technique
production ofof incubating
respired CO2 subsamples
by microbialofcommunities
soils taken atindifferent
mangrove depths
soilsunder oxygen-free
has been measured
conditions and obtaining
using a simple technique DICofbuilt up in the
incubating incubated samples
subsamples over several
of soils taken days [53,54].
at different This method
depths under oxygen-
has its conditions
free drawbacks,and such as possible
obtaining DICloss
builtofupDICin via
the authigenic mineral formation
incubated samples over several (i.e., precipitation
days [53,54]. This
of method
carbonates)
has and lack of linearsuch
its drawbacks, increase in DIC production
as possible loss of DICover viathe time course
authigenic of theformation
mineral experiments. (i.e.,
Asprecipitation
most of the of incubations were conducted using soils from a depth of 10–50
carbonates) and lack of linear increase in DIC production over the time course of the cm or less, all data
were extrapolated
experiments. As here
mosttoof100
the cm by simplewere
incubations multiplication,
conducted using basedsoils
on thefromfacta that
depth noofDIC
10–50production
cm or less,
profiles
all dataindicate a clear increasing
were extrapolated here toor 100
decreasing trend with
cm by simple soil depth [53–63].
multiplication, based onAn theexample
fact thatofnosuch
DIC
profiles (Figure 2) from four Australian mangrove sites depicts the typical
production profiles indicate a clear increasing or decreasing trend with soil depth [53–63]. An lack of clear tends with
increasing
example depth,
of suchsuggesting that extrapolation
profiles (Figure 2) from fourtoAustralian
1 m depth mangrove
is [Link] irregular
depicts the pattern with of
typical lack
soil depth
clear is likely
tends with the result ofdepth,
increasing severalsuggesting
interrelated factors:
that (1) subsurface
extrapolation to 1 m microbial
depth isdecomposition
reasonable. The
stimulated
irregular by root and
pattern withbioturbation
soil depth isactivities;
likely the(2)result
tidal offlushing
severaland percolation
interrelated of rainwater
factors: into
(1) subsurface
themicrobial
forest floor keeps the interstitial
decomposition stimulatedwater by circulating, preventing the
root and bioturbation buildup(2)
activities; of toxic
tidal metabolites;
flushing and
(3)percolation
while labileof organic matter
rainwater content
into usually
the forest declines
floor keepswith soil depth, water
the interstitial there iscirculating,
usually no clear trend inthe
preventing
dissolved
builduporganic
of toxiccarbon (DOC)(3)
metabolites; and nitrogen
while labileconcentrations;
organic matterand (4) mangrove
content roots typically
usually declines with soilexcrete
depth,
labile
thereorganic metabolites
is usually no clear into
trendthein soil, likelyorganic
dissolved stimulatingcarbonmicrobial
(DOC) andactivity [15]. concentrations;
nitrogen From a microbial and
perspective, the forest floor acts like a sponge, serving as a deep diagenetic
(4) mangrove roots typically excrete labile organic metabolites into the soil, likely stimulating reactor that is alternately
drained andactivity
microbial replenished [15]. with
Fromoxidized
a microbialsolutes and gases.
perspective, the forest floor acts like a sponge, serving as a
deep diagenetic reactor that is alternately drained and replenished with oxidized solutes and gases.
 Forests 2020, 11, 977 5 of 17
Forests 2020, 11, x FOR PEER REVIEW 5 of 17

DIC production (nmol cm-3 d-1)

100 150 200 250 300 350 400 450 500 550 600 650 700 750 800
0

10

20

30
Soil depth (cm)

40

50

60

70

80
Hinchinbrook Channel, R. stylosa, Low Intertidal
90 Hinchinbrook Channel, R. stylosa, Mid Intertidal
Darwin Harbour, S. alba, Low Intertidal
Darwin Harbour, R. stylosa-B. exaristata, Mid Intertidal
100

Figure 2. Vertical profiles of mean rates of DIC production at intervals to a soil depth of 1 m.
Figure 2. Vertical profiles of mean rates of DIC production at intervals to a soil depth of 1 m. Core
Core samples and sample processing details were identical to the methods described in [54–63].
samples and sample
The mangroves processing Channel,
at Hinchinbrook details were
northidentical to the
Queensland, methods
Australia, described
were sampled in [54–63].
in June 2014,The
mangroves at Hinchinbrook
and the Darwin Channel,
Harbour mangroves north
in the Queensland,
Northern Australia,
Territory, Australia,were
were sampled inOctober
sampled in June 2014,
[Link]
the Darwin Harbour mangroves in the Northern Territory, Australia, were sampled in October 2014.
2.3. Comparing Surface and Subsurface CO2 Fluxes
2.3. Comparing Surface
Ten studies andhave
to date Subsurface CO2 Fluxesmeasured CO fluxes across the soil surface and in
simultaneously 2
subsurface deposits
Ten studies in mangrove
to date forests in Australia,
have simultaneously Southeast
measured CO2 Asia,
fluxesChina,
across andtheEast
soilAfrica [54–63].
surface and in
Rates of CO production across the soil-water/air interface averaged 1878.3 ± 230.0 mg C m −2 d−1 and
2
subsurface deposits in mangrove forests in Australia, Southeast Asia, China, and East Africa [54–63].
ratesof
Rates of CO
subsurface DIC production were nearly three times greater, averaging 5188.0 ± 630.3 mg C m−2
2 production across the soil-water/air interface averaged 1878.3 ± 230.0 mg C m−2 d−1 and
−1
d . Even assuming inaccuracies from methodological shortcomings, subsurface DIC production is
rates of subsurface DIC production were nearly three times greater, averaging 5188.0 ± 630.3 mg C
clearly greater than CO2 production at the soil surface. Nevertheless, there was a positive correlation
m−2 d−1. Even assuming inaccuracies from methodological shortcomings, subsurface DIC production
between both sets of measurements (Figure 3), indicating that mineralization rates in surface and
is clearly greater than CO2 production at the soil surface. Nevertheless, there was a positive
subsurface soils respond to identical factors, such as temperature, salinity, pH, frequency of tidal
correlation between both sets of measurements (Figure 3), indicating that mineralization rates in
inundation, forest age and composition, root activities, microbial community composition, and soil
surface and subsurface soils respond to identical factors, such as temperature, salinity, pH, frequency
nutrient and CORG content.
of tidalThe
inundation,
extent of theforest age and composition,
discrepancy between bothroot sets activities, microbial
of measurements community
increases composition,
with increasing
and soil nutrient
topographic and(mCabove
height ORG content.
mean sea level), indicating that there is a ‘DIC reservoir-pump system’ [2]
beneath the forest floor discrepancy
The extent of the (Figure 4). Thebetween both
greater the sets
tidal of measurements
elevation of a forest, theincreases
greater thewith increasing
discrepancy
topographic height
between carbon (m above
respiration atmean sea
the soil level),and
surface indicating that there
in deep soils. is athe
That is, ‘DIC reservoir-pump
volume system’
of soil susceptible
[2]tobeneath
drainage increases with forest height above mean sea level. The cause of this phenomenon is thatthe
the forest floor (Figure 4). The greater the tidal elevation of a forest, the greater
discrepancy
the deeper between carbon
soils act like respiration
a sponge through at the soilporewater
which surface and in deep soils.
is pumped by tidalThat is, the volume
advection and/or of
soil susceptible
seeps to drainage
from the forest increases
floor laterally with forest
to adjacent height
waters. Such above
drainage mean sea been
has also [Link]
The cause of this
in tidal
phenomenon
marshes [64,65].is that the deeper soils act like a sponge through which porewater is pumped by tidal
advection and/or seeps from the forest floor laterally to adjacent waters. Such drainage has also been
observed in tidal marshes [64,65].
 Forests 2020, 11, x FOR PEER REVIEW 6 of 17

Forests 2020, 11, 977 6 of 17

Forests 2020, 11, x FOR PEER REVIEW 6 of 17

-2 C-1m d )
-1
-2
30000

CO2 production extrapolated to 1 m soil depth (mg C m d )

CO2 prod = 2128.786 + (1.628 x CO 2 flux)
CO2 production extrapolated to 1 m soil depth (mg
30000 r2 = 0.353
25000
F1,48
CO=2 prod
26.169; p < 0.001+ (1.628 x CO flux)
= 2128.786 2

r2 = 0.353
25000
20000 F1,48 = 26.169; p < 0.001

20000
15000

15000
10000

10000
5000

5000
0
0 2000 4000 6000 8000 10000 12000
0 Surface soil CO2 respiration (mg C m-2 d-1)
0 2000 4000 6000 8000 10000 12000

Figure 3. The relationship between surface -2 -1

Surface soilsoil
COCO 2 respiration and DIC production extrapolated to a
2 respiration (mg C m d )
soil depth of 1 m (see text for explanation) in mangrove forests across several locations worldwide.
Figure
The 3. The relationship
regression between surface soil CO2 respiration and DICmeasurements.
production extrapolated to a
Figure 3. Theequation and
relationship coefficient
between are
surface significant
soil CO for n = 50
2 respiration total
and DIC production extrapolated to a
soil depth of 1 m (see text for explanation) in mangrove forests across several locations worldwide.
soil depth of 1 m (see text for explanation) in mangrove forests across several locations worldwide.
The regression equation and coefficient are significant for n = 50 total measurements.
The regression equation and coefficient are significant for n = 50 total measurements.

400
Cm d )

200
-1

400
-2

0
Magnitude of discrepancy (mg C m d )

200
-2 -1

-200
Magnitude of discrepancy (mg

0
-400
-200
-600
-400
-800
-600
-1000
-800
-1200
-1000
-1400
-1200
-1600
-1400 0.0 0.5 1.0 1.5 2.0 2.5 3.0

-1600 Topographic height ( m above mean sea-level)

0.0 0.5 1.0 1.5 2.0 2.5 3.0
Figure4.4. An
Figure An inverse
inverse relationship
relationship of
of increasing
increasing discrepancies
discrepancies between
between surface
surface and
andsubsurface
subsurface
mineralization
mineralizationrates
rateswith Topographic
withincreasing
increasingtopographic
topographicheight ( minin
height
height above mean
various
various sea-level)
mangrove
mangrove forests
forestsof
ofTimor-Leste,
Timor-Leste,
Thailand,
Figure Malaysia,
Thailand, 4. Indonesia,
Malaysia, Indonesia,
An inverse and
andAustralia.
Australia.
relationship Data
Dataobtained
of increasing obtained from
fromreferences
discrepancies references
between[54–63].
[54–63].
surface and subsurface
mineralization rates with increasing topographic height in various mangrove forests of Timor-Leste,
Seepage
Seepage ofofgroundwater
groundwater isiscontrolled
controlled bybycomplex
complex hydrologic
hydrologic factors [8]
[8]that
thatresult
resultininporewater
Thailand, Malaysia, Indonesia, and Australia. Data obtained from factors
references [54–63]. porewater
oozing
oozingout
outthrough
throughthethebottom
bottomsoil soillayers,
layers,seen
seenmost
mostclearly
clearlyatatlow
lowtide
tideasaswater
watermoving
movingthrough
through
seepage
seepagerunnels between
runnelsofbetween
Seepage the forest
the forest
groundwater and the adjacent
and the adjacent
is controlled creek
creek
by complex bank.
bank.
hydrologic factors [8] that result in porewater
oozing out through the bottom soil layers, seen most clearly at low tide as water moving through
seepage runnels between the forest and the adjacent creek bank.
Forests 2020, 11, 977 7 of 17

3. Composition of Mangrove Tidal Waters

The transport of porewater from the forest floor results in the supersaturation of total alkalinity,
pCO2 , free CO2 , DIC, and CH4, and CO2 outgassing of adjacent mangrove tidal waters (Table 1).
Most measurements have been made of pCO2 and carbon gas fluxes, and vary seasonally and over
tidal cycles, but the data are consistent among locations in showing high concentrations that are above
saturation thresholds calculated on the basis of salinity and temperature [34,66–93].

Table 1. Mean (±1SE) and median concentrations of alkalinity (µM), pCO2 (µatm), CO2 (µM), dissolved
inorganic carbon (DIC, µM), and CH4 (nM) and CO2 (mmol m2 d−1 ) and CH4 fluxes (µmol m−2 d−1 )
across the water-air interface in mangrove waters worldwide. Data from [66–93].

Parameters Mean Median Number of Measurements

Total alkalinity 1317.6 ± 153.3 1211.0 41
pCO2 3202.8 ± 306.6 1233.0 219
CO2 1446.3 ± 162.3 1270.5 44
DIC 1838.0 ± 71.4 2024.0 83
CH4 244.7 ± 49.1 135.5 60
CO2 fluxes 78.9 ± 8.0 50.0 143
CH4 fluxes 530.4 ± 78.5 260.1 134

4. Estimates of Tidal Export of DIC, DOC, POC, CH4 , and Alkalinity

High concentrations of DIC, DOC, CH4 , and total alkalinity in the interstitial water pool and
subsurface transport results in significant export to adjacent tidal waters of the coastal ocean (Table 2).
Only comparatively few locations, most in Australia, have been used to measure transport, but they
are consistent in revealing high rates of export. Mean DIC, alkalinity, DOC, and CH4 exports were
339.6, 211.5, 229.1, and 0.66 mmol m−2 d−1 , respectively (Table 2).
Unlike the data for DIC, alkalinity, and CH4 , there are earlier estimates of DOC export, as summarized
by Adame and Lovelock [7]. Combining the data in Table 2 and in [7], DOC export averaged
85.3 ± 35.8 (±1 SE) mmol m−2 d−1 over 41 measurements. POC export, derived from data in [7,10],
averaged 25.1 ± 9.2 (±1 SE) mmol m−2 d−1 over 63 measurements.

Table 2. Mean (±1 SE) rates (mmol m−2 d−1 ) of DIC, total alkalinity, dissolved organic carbon (DOC),
and CH4 export from mangrove forests to adjacent mangrove and coastal waters measured recently
from various locations worldwide. These empirical estimates were derived from using a Eularian
approach of time-series water sampling and tracing of radium isotopes. ND = no data.

Location DIC Export Alkalinity Export DOC Export CH4 Export Reference
186 ± 37 69 ± 14 72 ±15 0.014 ± 0.0023
Southern Moreton Bay,
205 ± 41 88 ±18 65 ±13 0.0056 ± 0.0011 [94]
Queensland, Australia
247 ± 49 132 ± 26 40 ± 8 0.017 ± 0.0034
125 ± 82 51 ± 34 136 ± 89 0.6 ± 0.4
Evans River estuary,
559 ± 292 321 ± 172 562 ± 293 2.3 ± 1.4
New South Wales, [95]
165 ± 102 59 ± 37 202 ± 125 0.8 ± 0.6
Australia
177 ± 100 67 ± 39 233 ± 132 0.9 ± 0.6
Maowei Sea, Guangxi
700 ± 820 310 ± 300
Province, ND ND [96]
250 ± 240 250 ± 230
south China
440.4 ± 232.6 365.5 ± 177.2 846.1 ± 936.5
Eastern Gulf of 146.2 ± 125.1 896.4 ± 459.3 176.2 ± 529.9
Carpentaria, 610.9 ± 342.0 564.0 ± 383.5 2110.5 ± 1762.8 ND [97]
Australia 774.3 ± 223.5 726.9 ± 261.0 294.2 ± 1276.2
730.0 ± 416.5 679.2 ± 367.3 153.4 ± 626.7
Forests 2020, 11, 977 8 of 17

Table 2. Cont.

Location DIC Export Alkalinity Export DOC Export CH4 Export Reference
351.6 ± 33.9 20.6 ± 1.9
480.0 ± 35.6 31.0 ± 2.3
Can Gio, Saigon River,
677.7 ± 79.0 ND 67.7 ± 7.9 ND [98]
southern Vietnam
612.2 ± 71.4 60.0 ± 3.7
338.9 ± 39.5 33.3 ± 2.0
85 116
Six mangrove estuaries,
22 21 7.5 ± 0.2
north,
−97 81 3.3 ± 0.4
northeast, and ND [99]
83 12 5.1 ± 0.5
southeast
77 116 4.2 ± 0.2
Australia
−3 −1
79 ± 28 48 ± 17 35 ± 12
Badeldaob Island, Palau ND [100]
10 ± 4 2±1 8±3
Indian Sundarbans 202.3 ND 162.1 ND [101]
Korogoro Creek,
New South Wales, 687 23 294.8 ND [102]
Australia
Harney and Shark
574.5
Rivers, ND ND ND [103]
1031.5 ± 291.3
Florida Everglades
Mean ± 1SE 339.6 ± 51.5 211.5 ± 58.2 229.1 ± 78 0.66 ± 0.29

5. Carbon Flow through the World’s Mangrove Ecosystems and Contributions to the Coastal Ocean
Until the availability of the empirical data referenced in Tables 1 and 2 indicating supersaturated
conditions in adjacent mangrove waters, large subsurface pools of interstitial DIC and DOC implied
that large amounts of dissolved carbon might be exported from the forest, possibly accounting for as
much as 112–160 Tg a−1 of mangrove carbon to balance the budgets constructed by Bouillon et al. [104]
(as revised by Beithaupt et al. [105]) and Alongi [2,10]. This discrepancy was called the ”missing
carbon”. Without empirical data, Alongi [2] estimated DOC and DIC export by difference, resulting in
estimates of 15 Tg a−1 and 86 Tg a−1 for DOC and DIC, respectively.
Here, the mass balance model of carbon flow through the world’s mangrove ecosystems constructed
by Alongi [2] is revised, using the data in Sections 2.1–2.3 and in Table 2, and newer data for soil +
root burial [3,106], root production [107], mangrove gross primary production (GPP), POC, and DOC
export [7,10], and canopy respiration (Rc ) [19,66,108–114], and extrapolated using the most recent
estimate of global mangrove area [115]. The revised carbon flow model (Figure 5) shows that ∼64% of
GPP is respired by the canopy with NPP vested nearly equally in the litter, wood, and belowground
root production. About 41% of litter production is exported to adjacent tidal waters, and as estimated
by difference, about 40% is buried and 44% incorporated and eventually decomposed in the massive
soil CORG pool (5396 Tg). CORG burial (14 Tg C a−1 ) equates to about 12% of NPP. Of the combined
total carbon mineralization (subsurface DIC production + CO2 respiration at the soil surface), 25%
is released at the forest floor surface in a separate process, and approximately all subsurface DIC
production is exported to adjacent tidal waters in the form of DOC (∼30%), dissolved CH4 (<0.2%) and
DIC (∼70%). A considerable, but unquantified, amount of exported DIC, DOC, and CH4 is derived
from groundwater derived from adjacent upland [13,74–76,94–97,101,103], so it is unclear exactly how
much dissolved carbon exported from mangroves is derived from soil mineralization.
 Forests 2020, 11, 977 9 of 17
Forests 2020, 11, x FOR PEER REVIEW 9 of 17

Figure 5. A mass balance model of carbon flow through the world’s mangrove ecosystems, updated
Figure 5. A mass balance model of carbon flow through the world’s mangrove ecosystems, updated
from [2]. Units are Tg C−1 a−1 . The budget assumes a global mangrove area of 86,495 km2 [116].
from [2]. Units are Tg C a . The budget assumes a global mangrove area of 86,495 km2 [116]. Solid
Solid blue arrows represent mean values based on empirical data (see text for explanation and
blue arrows represent mean values based on empirical data (see text for explanation and references.)
references.) Dashed red arrows represent mean values estimated indirectly (by difference). The Corg
Dashed red arrows represent mean values estimated indirectly (by difference). The Corg pool (both
pool (both roots and soil) in soils to a depth of 1 m is presented as a box in the forest floor with units of Tg
roots and soil) in soils to a depth of 1 m is presented as a box in the forest floor with units of Tg C.
C. Unquantified inputs of dissolved carbon from land-derived groundwater and organic matter inputs
Unquantified inputs of dissolved carbon from land-derived groundwater and organic matter inputs
from adjacent marine and catchments are not depicted. Abbreviations: GPP = gross primary production;
from adjacent marine and catchments are not depicted. Abbreviations: GPP = gross primary
NPP = net primary production; RAa = algal respiration; RC = canopy respiration; RS = soil respiration
production; NPP = net primary production; RAa = algal respiration; RC = canopy respiration; RS = soil
at soil surface; RWATER = waterway respiration; POC = particulate organic matter; DIC = dissolved
respiration at soil surface; RWATER = waterway respiration; POC = particulate organic matter; DIC =
inorganic carbon; DOC = dissolved organic carbon; CH4 = methane; EDOC = exchangeable dissolved
dissolved inorganic carbon; DOC = dissolved organic carbon; CH4 = methane; EDOC = exchangeable
organic carbon.
dissolved organic carbon.
The supersaturation of mangrove waters leads to significant CO2 (40 Tg C a−1 ) and CH4
(0.19 Tg supersaturation
The C a−1 ) release toofthe
mangrove
[Link] leads
rates to of
significant CO2 (40 Tg imply
soil mineralization C a−1) andthatCH the4 (0.19 Tg
turnover
Ctime
a ) release
−1 to the atmosphere.
of the entire soil CORG pool Theisrates of soil
on the ordermineralization
of 25 [Link] turnover
frame time of the
is supported by
entire soil C ORG pool is on the order of 25 years. This time frame is supported by empirical findings
empirical findings that mangrove roots decompose slowly [106] and that mangrove soil organic
that
mattermangrove roots decompose
is composed slowly [106] and
mostly of allochthonous, that mangroveplant-derived
highly-refractory, soil organic matter
material is that
composed
is high
mostly of allochthonous, highly-refractory, plant-derived material that is
in lignocellulose, and hemicellulose derived mostly from leaves [116] that decompose slowly [117].high in lignocellulose, and
hemicellulose derived mostly from leaves [116] that decompose slowly
About 58% of soil carbon is mangrove-derived, a value that comes from stable isotope signatures [117]. About 58% of soilof
carbon
mangrove is mangrove-derived,
soils [118], and abouta value that of
one-third comes
the total from soilstable
carbonisotope
pool issignatures
composedof of mangrove
dead roots soils [2,10]
[118], and about one-third of the total soil carbon pool is−1composed of dead
that also decompose slowly [106]. Assuming that 4 Tg C a of litter is buried and that all POC export roots [2,10] that also
decompose slowly [106]. Assuming that 4 Tg C a −1
−1 of litter is buried and that all POC
is derived from litter, then the remaining 16 Tg a of litter produced must fall to the forest floor where export is derived
from litter, then the
it is presumably remaininginto
incorporated 16 Tg a−1 of food
detritus litterwebsproduced must fall mineralized
and eventually to the forest in floor
[Link]
Wooditthat is
presumably incorporated into detritus food webs and eventually mineralized
falls to the forest floor may be eventually incorporated into the soil pool, but decomposition is veryin situ. Wood that falls
to the forest floor may be eventually incorporated into the soil pool, but decomposition is very slow
[119] and likely a minor flux, so it is not included in the mass balance; also not included are benthos
Forests 2020, 11, 977 10 of 17

slow [119] and likely a minor flux, so it is not included in the mass balance; also not included are
benthos and zooplankton production and chemical defenses. The total soil mineralization equates to
approximately 140% of mangrove NPP. This anomaly suggests that: (1) inputs from allochthonous
marine and terrestrial sources are necessary to balance the mineralization outputs (158 Tg C a−1 );
(2) a large proportion of the soil pool and its subsequent decomposition is derived from the intertidal
mudflat prior to mangrove colonization; (3) wood, algae, and fauna contribute to the soil pool; and/or
(4) the subsurface soil mineralization rates and subsequent export data are overestimated. It is
also conceivable that root production is underestimated given that the empirical dataset (mostly for
estimates of fine roots) is small and that there are some methodological shortcomings in deriving
production estimates [10,107].
Analysis of the origin of mangrove soil organic matter indicates that about 42% of the organic
matter may be derived from external sources [14,118]. Measurements of radiogenic and stable isotopes
in a subtropical Australian mangrove indicate that century-old sequestered carbon is still susceptible
to remineralization and tidal export [120], supporting the idea that organic carbon deposited prior to
mangrove colonization continues to be decomposed, as all mangroves colonize intertidal mudflats that
have considerable amounts of soil CORG [6]. Mangrove DIC export contributes nearly 60% of DIC,
and 27% of DOC discharged from the world’s tropical rivers to the coastal ocean, based on comparison
with tropical riverine export values in Huang et al. [121]. Mangroves inhabit only 0.3% of global coastal
ocean area but contribute 55% of air-sea exchange compared with the global average [122], 28% of
DIC export, 14% of C burial, and 13% of DOC + POC export, compared to global averages in [123] tor
the world’s coastal ocean. Mangrove ecosystems thus contribute a disproportionate share to carbon
cycling in tropical seas and in the global coastal ocean.
The mass balance model is only a tool to identify the major and minor pathways of carbon
flow in mangrove ecosystems and is not meant to be absolute as it does not distinguish known
site-specific differences in soil type, forest composition and age, tidal exchange, bioturbation, and rates
of forest productivity. As noted in the tables and figures, there are considerable variations in the
mean of most measurements that are not represented in the model. Nevertheless, the model is helpful
in suggesting where more research is needed, such as in more measurements of canopy GPP and
respiration, preferably using the eddy covariance method, root production, estimates of DOC, CH4,
and especially DIC export, as well as more empirical measurements of subsurface DIC production as
well as a clearer understanding of the contribution of groundwater derived from upland and inputs
from allochthonous sources, such as the adjacent catchment and coastal zone.
Net ecosystem production (NEP), derived by subtracting all respiratory losses (ecosystem
respiration, RE = RC + RS + RWATER + RMICROALGAE ) from all mangrove, algal, and phytoplankton
gross primary production (GPP) is 628 g C m−2 a−1 and 54 Tg C a−1 for the world’s mangroves.
Phytoplankton GPP and R in mangrove tidal creeks and waterways (total area = 7208 km2 assuming a
forest: waterway area ratio of 12 [10]) averaged 1524.4 and 846.9 mg C m−2 d−1 [10]. Subsurface soil
respiration was excluded from the ecosystem respiration estimate because (1) the core incubation
method used to measure subsurface respiration is crude and may be an overestimate; (2) it is unclear
how much porewater DIC is actually derived from groundwater; and (3) the proportional amounts of
dissolved carbon derived from groundwater and from subsurface respiration is unknown.) RE was
3558 g C m−1 a−1 for a global RE of 306 Tg C a−1, and total GPP was 4186 g C m−2 a−1 for a global
GPP of 360 Tg C a−1 . The ratio of PGPP /RE averaged 1.18, indicating that mangrove ecosystems are
net autotrophic.

6. Conclusions
The mangrove forest floor is unique, with cracks, fissures, extensive roots, burrows, tubes, and
drainage channels, and its dynamic nature facilitates non-steady-state early diagenesis of organic matter
in the soil. Rate processes and edaphic conditions (e.g., temperature, redox status, salinity) oscillate in
synchrony with tidal flushing and inundation and other factors such as the extent of bioturbation and
Forests 2020, 11, 977 11 of 17

weather. Rates of soil CORG mineralization and belowground CORG stocks are high, indicating rapid
accumulation and recycling of organic matter within the deep (>1 m) soil horizon. On average, carbon
respiration across the surface soil-air/water interface equates to only 25% of total carbon mineralized
within the entire soil horizon as most respired carbon is released in a dissolved form via advective
porewater exchange and/or lateral transport and subsurface tidal pumping to adjacent tidal waters.
A revised carbon budget for the world’s mangrove ecosystems indicates that subsurface respiration is
the second-largest respiratory flux after canopy respiration. The amounts of dissolved carbon released
to adjacent tidal waters are sufficient to cause pCO2 oversaturation of the water column, leading to
tropical coastal waters being a source of CO2 to the atmosphere. Mangrove DIC and DOC discharge
contribute disproportionately to dissolved carbon discharge from the world’s low latitude rivers to the
tropical coastal ocean and contribute 55% of air-sea exchange, 28% of DIC export, 14% of C burial,
and 13% of DOC + POC export from the world’s wetlands and estuaries to the coastal ocean.

Funding: This research received no external funding.

Conflicts of Interest: The author declares no conflict of interest.

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