Tropical mangrove forests are important carbon sinks, the soil
being the main carbon reservoir. Understanding the variability and the key
factors that control fluxes is critical to accounting for greenhouse gas
(GHG) emissions, particularly in the current scenario of global climate
change. This study is the first to quantify carbon dioxide (CO2) and
methane (CH4) emissions using a dynamic chamber in natural mangrove
soil of the Amazon. The plots for the trace gases study were allocated at
contrasting topographic heights. The results showed that the mangrove soil
of the Amazon estuary is a source of CO2 (6.66 g CO2 m-2 d-1) and CH4 (0.13 g CH4 m-2 d-1) to the
atmosphere. The CO2 flux was higher in the high topography (7.86 g CO2 m-2 d-1) than in the low topography (4.73 g CO2 m-2 d-1) in the rainy season, and CH4 was higher in the low
topography (0.13 g CH4 m-2 d-1) than in the high topography
(0.01 g CH4 m-2 d-1) in the dry season. However, in the dry
period, the low topography soil produced more CH4. Soil organic matter,
carbon and nitrogen ratio (C/N), and redox potential influenced the annual
and seasonal variation of CO2 emissions; however, they did not affect
CH4 fluxes. The mangrove soil of the Amazon estuary produced 35.40 Mg CO2eq. ha-1 yr-1. A total of 2.16 kg CO2 m-2 yr-1 needs to be sequestered by the mangrove ecosystem to counterbalance
CH4 emissions.
Introduction
Mangrove areas are estimated to be the main contributors to greenhouse gas
emissions in marine ecosystems
(Allen
et al., 2011; Chen et al., 2012). However, mangrove forests are highly
productive due to a high nutrient turnover rate
(Robertson et al., 1992), and have mechanisms that
maximize carbon gain and minimize water loss through plant transpiration
(Alongi and Mukhopadhyay, 2015). A study
conducted in 25 mangrove forests (between 30∘ latitude and
73∘ longitude) revealed that these forests are the richest in
carbon (C) storage in the tropics, containing on average 1023 Mg C ha-1 of which 49 % to 98 % is present in the soil
(Donato et al., 2011).
The estimated soil CO2 flux in tropical estuarine areas is 16.2 Tg C yr-1 (Alongi, 2009). However, soil efflux
measurements from tropical mangroves revealed emissions ranging from 2.9 to
11.0 g CO2 m-2 d-1
(Castillo
et al., 2017; Chen et al., 2014; Shiau and Chiu, 2020). In situ CO2
production is related to the water input of terrestrial, riparian, and
groundwater brought by rainfall
(Rosentreter et al.,
2018b). Due to the periodic tidal movement, the mangrove ecosystem is
flooded daily, leaving the soil anoxic and consequently reduced, favoring
methanogenesis (Dutta et al.,
2013). Thus, estuaries are considered hotspots for CH4 production and
emission (Bastviken et al., 2011;
Borges et al., 2015). Organic material decomposition by methanogenic
bacteria in anoxic environments, such as sediments, inner suspended
particles, zooplankton gut (Reeburgh, 2007;
Valentine, 2011), and the impact of freshwater should change the electron
flow from sulfate-reducing bacteria to methanogenesis
(Purvaja et al., 2004), which also results
in CH4 formation. On the other hand, high salinity levels, above 18 ppt, may result in an absence of CH4 emissions
(Poffenbarger et al., 2011), since
CH4 dissolved in pores is typically oxidized anaerobically by sulfate
(Chuang et al., 2016). Currently the uncertainty in
emitted CH4 values in vegetated coastal wetlands is approximately
30 % (EPA, 2017). Soil flux
measurements from tropical mangroves revealed emissions range from 0.3 to
4.4 mg CH4 m-2 d-1
(Castillo
et al., 2017; Chen et al., 2014; Kreuzwieser et al., 2003).
The production of greenhouse gases from soils is mainly driven by
biogeochemical processes. Microbial activities and gas production are
related to soil properties, including total carbon and nitrogen
concentrations, moisture, porosity, salinity, and redox potential
(Bouillon
et al., 2008; Chen et al., 2012). Due to the dynamics of tidal movements,
mangrove soils may become saturated and present reduced oxygen availability,
or suffer total aeration caused by the ebb tide. Studies attribute soil
carbon flux responses to moisture perturbations because of seasonality and
flooding events (Banerjee et al.,
2016), with fluxes being dependent on tidal extremes (high tide and low
tide), and flood duration (Chowdhury et
al., 2018). In addition, phenolic compounds inhibit microbial activity and
help keep organic carbon intact, thus leading to the accumulation of organic
matter in mangrove forest soils (Friesen et
al., 2018).
The Amazonian coastal areas in the state of Pará (Brazil) cover 2176.8 km2 where mangroves develop under the macro-tide regime, representing approximately 85 % of the
entire area of Brazilian mangroves (Souza Filho, 2005). The objective of
this study is to investigate the monthly flux of CO2 and CH4 from
the soil, at two topographic heights, in a pristine mangrove area in the
Mojuim River estuary, belonging to the Amazon biome. The gas fluxes were
studied together with the analysis of the vegetation structure and soil
physical–chemical parameters.
Material and methodsStudy site
This study was conducted in the Amazonian coastal zone, Macaca Island
(-0.746491 latitude and -47.997219 longitude), located in the Mojuim River
estuary, at the Mocapajuba Marine Extractive Reserve, municipality of
São Caetano de Odivelas (Fig. 1), state of Pará (Brazil). The Macaca
island has an area of 1322 ha of pristine mangroves, and belongs to a
mangrove area of 2177 km2 in the state of Pará (Souza
Filho, 2005). The climate is type Am (tropical monsoon) according to the
Köppen classification (Peel et al.,
2007). The climatological data were obtained from the Meteorological
Database for Teaching and Research of the National Institute of Meteorology
(INMET). The area has a rainy season from January to June (2296 mm of
precipitation) and a dry season from July to December (687 mm). March and
April were the rainiest months with 505 and 453 mm of precipitation, while
October and November were the driest (53 and 61 mm, respectively). The
minimum temperatures occur in the rainy period (26 ∘C) and the
maximum in the dry period (29 ∘C). The Mojuim estuary has a
macrotidal regime, with an average amplitude of 4.9 m during spring tide and
3.2 m during low tide
(Rollnic et
al., 2018). During the wet season, the Mojuim River has a flow velocity of
1.8 m s-1 at the ebb tide and 1.3 m s-1 at the flood tide, whereas
in the dry season, the maximum currents reach 1.9 m s-1 at the flood
and 1.67 m s-1 at the ebb tide
(Rocha, 2015). The annual
mean salinity of the river water is 26.95 PSU
(Valentim et al., 2018).
The Mojuim River region is geomorphologically formed by partially submerged
river basins consequent of the increase in the relative sea level during the
Holocene (Prost et al., 2001)
associated with the formation of mangroves, dunes, and beaches
(El-Robrini et al., 2006). Before reaching the
estuary, the Mojuim River crosses an area of a dryland forest highly
fragmented by family farming, forming remnants of secondary forest
(<5.0 ha) of various ages
(Fernandes and Pimentel, 2019). The
population economically exploited the estuary, primarily by artisanal
fishing, crab (Ucides cordatus L.) extraction, and oyster farms.
The flora of the mangrove area of Macaca Island is little anthropized and
comprises the plant genera Rhizophora, Avicennia, Laguncularia, and Acrostichum
(Ferreira, 2017; França et
al., 2016). The estuarine plains are influenced by macro-tide dynamics and
can be physiographically divided into four sectors according to the
different vegetation covers, associated with the landforms distribution,
topographic gradient, tidal inundation, and levels of anthropic
transformation (França et al., 2016). The Macaca
Island is ranked as being from the fourth sector, which implies having woods
of adult trees of the genus Rhizophora with an average height of 10 to 25 m, being
located at an elevation of 0 to 5 m, and having silt–clay soil
(França et al., 2016).
Four sampling plots were selected in the Macaca Island (Fig. 1) on
19 May 2017, when the moon was in the waning quarter phase: two plots where
flooding occurs every day (plots B1 and B2; Fig. 1), called low topography
(Top_Low), and two plots where flooding occurs only at high
tides during the solstice and on the high tides of the rainy season of the
new and full moons (plots A1 and A2; Fig. 1), called high topography
(Top_High).
Greenhouse gas flux measurements
In each plot, eight polyvinyl chloride rings with 0.20 m diameter and 0.12 m
height were randomly installed within a circumference with a diameter of 20 m. The rings had an area of 0.028 m-2 (volume of 3.47 L), were fixed
0.05 m into the ground, and remained in place until the study was completed.
Once a month, gas fluxes were measured during periods of waning or crescent
moon, as these are the times when the soil in the low topography is more
exposed. To avoid the influence of mangrove roots on the gas fluxes, the
rings were placed in locations without any seedlings or aboveground mangrove
roots. The CO2 and CH4 concentrations (ppm) were measured using
the dynamic chamber methodology
(Norman
et al., 1997; Verchot et al., 2000), sequentially connected to a Los Gatos
Research portable gas analyzer
(Mahesh
et al., 2015). The device was calibrated monthly with a high quality
standard gas (500 ppm CO2; 5 ppm CH4). The rings were sequentially
closed for 3 min with a PVC cap, being connected to the analyzer
through two 12.0 m polyethylene hoses. The gas concentration was measured
every 2 s and automatically stored by the analyzer. CO2 and
CH4 fluxes were calculated from the linear regression of
increasing/decreasing CO2 and CH4 concentrations within the
chamber, usually between 1 and 3 min after the ring cover was
placed
(Frankignoulle,
1988; McEwing et al., 2015). The flux is considered zero when the linear
regression reaches an R2<0.30
(Sundqvist et al., 2014). However, in our
analyses, most regressions reached R2>0.70, and the
regressions were weak and considered zero in only 6 % of the samples. At
the end of each flux measurement, the height of the ring above ground was
measured at four equidistant points with a ruler. The seasonal data were
analyzed by comparing the average monthly fluxes in the wet season and dry
season separately.
Vegetation structure and biomass
The floristic survey was conducted in October 2017 using circular 1256.6 m2 plots (Kauffman et al., 2013) divided into
four 314.15 m2 subplots, which is the equivalent to 0.38 ha, at the
same topographies as the gas flux analysis (Fig. 1). We recorded the
diameter above the aerial roots, the diameter of the stem, and total height
of all trees with DBH (diameter at breast height; m) greater than 0.05 m. The
allometric equations (Howard et al., 2014) to
calculate tree biomass (aboveground biomass; AGB) were the following: AGB = 0.1282 * DBH2.6; (R2= 0.92) for R. mangle; AGB = 0.140 * DBH2.4 (R2= 0.97) for A. germinans; and total AGB = 0.168 ×ρ * DBH2.47 (R2= 0.99), where ρR. mangle= 0.87; ρA. germinans= 0.72 (ρ= wood density).
Soil sampling and environmental characterization
Four soil samples were collected with an auger at a depth of 0.10 m in all
the studied plots for gas flux measurements (Fig. 1) in July 2017 (beginning
of the dry season) and January 2018 (beginning of the rainy season). Before
the soil samples were removed, pH and redox potential (Eh; mV) were measured
with a Metrohm 744 equipment by inserting the platinum probe directly into
the intact soil at a depth of 0.10 m
(Bauza et al., 2002). The soil
samples collected in the field were transported to the laboratory (chemical
analysis laboratory of the Museu Paraense Emílio Goeldi) in thermal boxes containing ice. The soil
samples were analyzed on the day after collection at the laboratory, and the
samples were kept in a freezer. Salinity (Sal; ppt) was measured with
PCE-0100, and soil moisture (Sm; %) by the residual gravimetric method
(EMBRAPA, 1997).
Organic matter (OM; g kg-1), total carbon (TC; g kg-1), and
total nitrogen (TN; g kg-1) were calculated by volumetry
(oxidoreduction) using the Walkley–Black method (Kalembasa and
Jenkinson, 1973). Microbial carbon (Cmic; mg kg-1) and microbial
nitrogen (Nmic; mg kg-1) were determined through the 2.0 min of
irradiation–extraction method of soil by microwave technique
(Islam and Weil,
1998). Microwave heated soil extraction proved to be a simple, fast,
accurate, reliable, and safe method to measure soil microbial biomass
(de Araujo,
2010; Ferreira et al., 1999; Monz et al., 1991). The Cmic was
determined by dichromate oxidation
(Kalembasa
and Jenkinson, 1973; Vance et al., 1987). The Nmic was analyzed
following the method described by
Brookes et al. (1985),
changing fumigation to irradiation, which uses the difference between the
amount of TN in irradiated and non-irradiated soil. We used the flux
conversion factor of 0.33 (Sparling and West,
1988) and 0.54
(Almeida
et al., 2019; Brookes et al., 1985),
for carbon and nitrogen, respectively.
Particle size analysis was performed separately on four soil samples
collected at each flux plot, in the two seasons (October 2017 and March 2018), according to EMBRAPA (1997).
At each gas flux measurement, environmental variables such as air
temperature (Tair, ∘C), relative humidity (RH, %), and
wind speed (Ws, m s-1) were quantified with a portable
thermo-hygrometer (model AK821) at the height of 2.0 m above the soil
surface. Soil temperature (Ts, ∘C) was measured with a
portable digital thermometer (model TP101) after each gas flux measurement.
Daily precipitation was obtained from an automatic precipitation station
installed at a pier on the banks of the Mojuim River in São Caetano das
Odivelas (coordinates: -0.738333 latitude; -48.013056 longitude).
Statistical analyses
On the Macaca Island, two treatments were allocated (low and high
topography), with two plots in either treatment. In each plot, eight
chambers were randomly distributed, which were considered sample
repetitions. The normality of the data of CH4 and FCO2 flux, and
soil physicochemical parameters was evaluated using the Shapiro–Wilks
method. The soil CO2 and CH4 flux showed a non-normal
distribution. Therefore, we used the non-parametric ANOVA (Kruskal-Wallis, p<0.05) to test the differences between the two treatments among
months and seasons. The physicochemical parameters were normally
distributed. Therefore, a parametric ANOVA was used to test the statistical
differences (p<0.05) between the two treatments among months and
seasons. Pearson correlation coefficients were calculated to determine the
relationships between soil properties and gas fluxes in the months (dry and
wet season) when the chemical properties of the soil were analyzed at the
same time as gas fluxes were measured. Statistical analyses were performed
with the free statistical software Infostat 2015®.
ResultsCarbon dioxide and methane fluxes
CO2 fluxes differed significantly between topographies only in January
(H= 3.915; p= 0.048), July (H= 9.091; p= 0.003), and November (H= 11.294; p<0.001) (Fig. 2; Supplement S1),
with generally higher fluxes at the high topography than at the low
topography. At the high topography, CO2 fluxes were significantly
higher (H= 24.510; p= 0.011) in July compared to August and December,
March, October, and May, not differing from the other months of the year.
Similarly, at the low topography, CO2 fluxes were statistically
significantly higher (H= 19.912; p= 0.046) in September and February
when compared to January and November, not differing from the other months.
We found a mean monthly flux of 7.9 ± 0.7 g CO2 m-2 d-1
(mean ± standard error) and 5.4 ± 0.5 g CO2 m-2 d-1 at the high and low topographies, respectively.
CO2(a) and CH4(b) fluxes (g CO2 or CH4 m-2 d-1) monthly (July 2018 to June 2019) (n= 16). Seasonal
(dry and rainy) and annual fluxes of CO2(c) and CH4(d), at high
(Top_High) and low (Top_Low) topographies (n= 96), in a mangrove forest soil compared to tide level (tide level). The
bars represent the standard error of the mean.
The CH4 fluxes were statistically different between topographies only
in November (H= 9.276; p= 0.002) and December (H= 4.945; p= 0.005), with higher fluxes at the low topography (Fig. 2, Supplement S1). At the high
topography, CH4 fluxes were significantly (H= 40.073; p<0.001) higher in April and July compared to the other months studied, and in
November CH4 was consumed from the atmosphere (Fig. 2; Supplement S1).
Similarly, CH4 fluxes at the low topography did not vary significantly
among months (H= 10.114; p= 0.407).
Greenhouse gas fluxes (Fig. 2) were only significantly different between
topographies in the dry season (Fig. 3), the period when CO2 fluxes were
higher (H= 7.378; p= 0.006) at the high topography and CH4 fluxes
at the low topography (H= 8.229; p<0.001). In Macaca
Island, the mean annual fluxes of CO2 and CH4 were 6.659 ± 0.419 g CO2 m-2 d-1 and 0.132 ± 0.053 g CH4 m-2 d-1, respectively. During the study year, the CO2 flux
from the mangrove soil ranged from -5.06 to 68.96 g CO2 m-2 d-1 (mean 6.66 g CO2 m-2 d-1), while the CH4 flux
ranged from -5.07 to 11.08 g CH4 m-2 d-1 (mean 0.13 g CH4 m-2 d-1), resulting in a total carbon efflux rate of 1.92 g C m-2 d-1 or 7.00 Mg C ha-1 yr-1 (Fig. 2).
Weather data
There was a marked seasonality during the study period (Fig. 2), with
2155.0 mm of precipitation during the rainy period and 1016.5 mm during
the dry period. The highest tides occurred in the period of greater
precipitation (Fig. 3) due to the rains. However, the rainfall distribution
was different from the climatological normal (Fig. 3). The precipitation in
the rainy season was 553.2 mm below and in the dry season was 589.1 mm above
the climatological normal. Thus, in the period studied, the dry season was
rainier and the rainy season drier than the climatological normal, which may
be a consequence of the La Niña event
(Wang et al., 2019).
Monthly climatological normal in the municipality of Soure
(1981–2010, mm), monthly precipitation (mm), and maximum tide height (m)
from 2017–2018, in the municipality of São Caetano de Odivelas (PA).
Tair was significantly higher (LSD = 0.72, p= 0.01) at the high
(31.24 ± 0.26 ∘C) than at the low topography (30.30 ± 0.25 ∘C) only in the rainy season (Fig. 4a). No significant
variation in Ts was found between topographies in either season (Fig. 4b). RH was significantly higher (LSD = 2.55, p= 0.01) at the high
topography (70.54 ± 0.97 %) than at the low topography (66.85 ± 0.87 %) only in the rainy season (Fig. 4c). Ws (Fig. 4d) was
significantly higher (LSD = 0.15, p<0.00) at the low (0.54 ± 0.06 m s-1) than at the high topography (0.24 ± 0.04 m s-1) also in the rainy season.
(a) Air temperature (∘ C), (b) soil temperature
(∘C), (c) relative humidity (%), and (d) wind speed (m s-1)
at high and low topographies, from July 2017 to June 2018 in a mangrove area
in the Mojuim River estuary. Bars highlighted in grey correspond to the
rainy season (n= 16). The bars represent the standard error.
Soil characteristics
Silt concentration was higher at the low topography (LSD: 14.763; p= 0.007) and clay concentration was higher at the high topography plots (LSD:
12.463; p= 0.005), in both seasons studied (Table 1). Soil particle size
analysis did not differ statistically (p>0.05) between the two
seasons (Table 1). Soil moisture did not vary significantly (p>0.05) between topographies at each season, or between seasonal periods at
the same topography (Table 1). The pH varied statistically (LSD: 5.950; p= 0.006) only at the low topography when the two seasons were compared, being
more acidic in the dry period (Table 1). The pH values were significantly
(LSD: 0.559; p= 0.008) higher in the dry season (Table 1). No variation in
Eh was identified between topographies and seasons (Table 1), although it
was higher in the dry season than in the rainy season. However, Sal values
were higher (LSD: 3.444; p= 0.010) at the high topography than at the low
topography in the dry season (Table 1). In addition, Sal was significantly
higher in the dry season than in the rainy season, in both high (LSD: 2.916;
p<0.001) and low (LSD: 3.003; p<0.001) topographies
(Table 1).
Analysis of sand (%), silt (%), clay (%), moisture (%),
pH, redox potential (Eh, mV), and salinity (Sal; ppt) in the mangrove soil of
high and low topographies, and in the rainy and dry seasons (Macaca island,
São Caetano das Odivelas). Numbers represent the mean ± standard
error of the mean. Lowercase letters compare topographies in each seasonal
period and uppercase letters compare the same topography between seasonal
periods. Different letters indicate statistical difference (LSD, p<0.05).
The Cmic did not differ between topographies in the two seasons (Table 2). However, TC was significantly higher in the low topography in the
dry season (LSD: 5.589; p<0.000) and in the rainy season (LSD:
5.777; p= 0.024). In addition, Cmic was higher in the dry season in
both the high (LSD: 11.325; p<0.010) and low (LSD: 9.345; p<0.000) topographies (Table 2). Nmic did not vary between
topographies seasonally. However, Nmic in the high (LSD: 9.059; p= 0.013) and low topographies (LSD: 4.447; p= 0.001) was higher during the
dry season (Table 2). The C/N ratio (Table 2) was higher in the low than in
the high topography in both the dry (LSD: 3.142; p<0.000) and
rainy seasons (LSD: 3.675; p= 0.033). However, only in the low topography
was the C/N ratio higher (LSD: 1.863; p<0.000) in the dry season
than in the rainy season (Table 2). Soil OM was higher at the low topography
in the rainy (LSD: 9.950; p= 0.024) and in the dry seasons (LSD: 9.630; p<0.000). Only in the lowland topography was the OM concentration
higher in the dry season than in the rainy season (Table 2).
Seasonal and topographic variation in microbial carbon (Cmic;
mg kg-1), microbial nitrogen (Nmic, mg kg-1), total carbon
(TC; g kg-1), total nitrogen (NT; g kg-1),
carbon/nitrogen ratio (C/N), and soil organic matter (OM; g kg-1).
Numbers represent the mean (± standard error). Lowercase letters
compare topographies at each season, and uppercase letters compare the
topography between seasons.
Only the species R. mangle and A. germinans were found in the floristic survey carried out. The
DBH did not vary significantly between the topographies for either species
(Table 3). However, R. mangle had a higher DBH than A. germinaris at both high (LSD: 139.304; p= 0.037) and low topographies (LSD: 131.307; p= 0.001). The basal area
(BA) and AGB did not show significant variation (Table 3). A total
aboveground biomass of 322.1 ± 49.6 Mg ha-1 was estimated.
Summed diameter at breast height (DBH; cm), basal area (BA; m2 ha-1), and aboveground biomass (AGB; Mg ha-1) at high and low
topographies in the mangrove forest of the Mojuim River estuary. Numbers
represent the mean ± standard error of the mean. Lowercase letters
compare topographic height for each species, and uppercase letters compare
species at each topographic height, using Tukey's test (p<0.05).
The equations for biomass estimates (AGB) were the following: R. mangle= 0.1282 * DBH2.6;
A. germinans= 0.14 * DBH2.4; and Total = 0.168 *ρ* DBH2.47, where
ρR. mangle= 0.87; ρA. germinans= 0.72 (Howard et al., 2014).
Drivers of greenhouse gas fluxes
In the rainy season, CO2 efflux was correlated with Tair (Pearson = 0.23, p= 0.03), RH (Pearson =-0.32, p<0.00), and Ts
(Pearson = 0.21, p= 0.04) only at the low topography. In the dry season,
CO2 flux was correlated with Ts (Pearson = 0.39, p<0.00) at the low topography. The dry season was the period in which we found
the greatest amount of significant correlations between CO2 efflux and
soil chemical parameters, while the C/N ratio, OM, and Eh were correlated
with CO2 efflux in both seasons (Table 4). The negative correlation
between TC, NT, C/N, and OM, along with the positive correlation
of Nmic with soil CO2 flux, in the dry period, indicates that
microbial activity is a decisive factor for CO2 efflux (Table 4). Soil
moisture in the Mojuim River mangrove forest negatively influenced CO2
flux in both seasons (Table 4). However, soil moisture was not correlated
with CH4 flux. No significant correlations were found between CH4
efflux and the chemical properties of the soil in the mangrove of the Mojuim
River estuary (Table 4).
Correlation coefficient (Pearson) of CO2 and CH4 fluxes
with chemical parameters of the soil in a mangrove area in the Mojuim River
estuary.
Gas fluxSeasonTCTNCmicNmicC/NOMSalEhpHMoisture(g m-2 d-1)(g kg-1)(g kg-1)(mg kg-1)(mg kg-1)(g kg-1)(ppt)(mV)(%)CO2Dry-0.68∗∗-0.59∗0.18NS0.61∗∗-0.66∗∗-0.67∗∗-0.07NS0.51∗0.21NS-0.49∗Rainy-0.44NS-0.20NS-0.15NS-0.32NS-0.50∗-0.63∗∗-0.54∗0.53∗0.47NS-0.54∗Annual-0.50∗∗-0.35∗-0.18NS0.00NS-0.53∗∗-0.48∗∗-0.30NS0.39∗0.23NS-0.56∗∗CH4Dry0.30NS0.07NS-0.14NS-0.24NS0.34NS0.02NS-0.04NS-0.38NS0.26NS0.26NSRainy0.05NS-0.09NS0.44NS-0.27NS0.09NS-0.11NS-0.04NS-0.13NS-0.07NS0.04NSAnnual0.04NS-0.10NS-0.01NS-0.18NS0.08NS-0.01NS-0.17NS-0.21NS-0.08NS0.02NS
total carbon (TC; g kg-1); total nitrogen (TN; g kg-1);
microbial carbon (Cmic, g kg-1); microbial nitrogen (Nmic, g kg-1); carbon and nitrogen ratio (C/N); organic matter (OM; g kg-1); salinity (Sal; ppt); redox potential (Eh; mV); soil moisture
(moisture, %). NS represents not significant; * significant effects at p≤ 0.05; ** significant effects at p≤ 0.01.
DiscussionCarbon dioxide and methane flux
It is important to consider that the year under study was rainier in the dry
season (2017) and less rainy in the wet season (2018) when the
climatological average is concerned (1981–2010) (Fig. 3). Perhaps this
variation is related to the La Niña effects (extreme event), taking into
account that the intensification and higher frequency of extreme events
result from climate change (Barichivich et al.,
2018). Under these conditions, negative and positive fluxes of the two
greenhouse gases were found (negative values represented gas consumption).
The negative CO2 flux is apparently a consequence of the increased
CO2 solubility in tidal waters or of the increased sulfate reduction,
as described in the literature
(Borges
et al., 2018; Chowdhury et al., 2018; Nóbrega et al., 2016).
Fluctuations in redox potential altered the availability of the terminal
electron acceptor and donor, and the forces of recovery of their
concentrations in the soil, such that a disproportionate release of CO2
can result from the alternative anaerobic degradation processes such as
sulfate and iron reduction (Chowdhury et
al., 2018). The soil carbon flux in the mangrove area in the Amazon region
was within the range of findings for other tropical mangrove areas (2.6 to
11.0 g CO2 m-2 d-1; Shiau and Chiu,
2020). However, the mean flux of 6.2 mmol CO2 m-2 h-1
recorded in this Amazonian mangrove was much higher than the mean efflux of
2.9 mmol CO2 m-2 h-1 recorded in 75 mangroves during low tide
periods (Alongi, 2009).
An emission of 0.01 Tg CH4 yr-1, 0.6 g CH4 m-2 d-1
(Rosentreter et al., 2018a), or 26.7 mg CH4 m-2 h-1, has been reported for tropical latitudes (0 and
5∘). In our study, the monthly average of CH4 flux was
higher at the low (7.3 ± 8.0 mg CH4 m-2 h-1) than at
the high topography (0.9 ± 0.6 mg C m-2 h-1), resulting in
0.1 g CH4 m-2 d-1 or 0.5 Mg CH4 ha-1 yr-1 (Fig. 2). Therefore, the CH4-C fluxes from the mangrove soil in the Mojuim
River estuary were much lower than expected. It is known that there is a
microbial functional module for CH4 production and consumption
(Xu et al., 2015) and diffusibility
of CH4 (Sihi et al.,
2018), and this module considers three key mechanisms: acetoclastic
methanogenesis (acetate production), hydrogenotrophic methanogenesis
(H2 and CO2 production), and aerobic methanotrophy (CH4
oxidation and O2 reduction). The average emission from the soil of 8.4 mmol CH4 m-2 d-1 was well below the fluxes recorded in the
Bay of Bengal, with 18.4 mmol CH4 m-2 d-1
(Biswas et al.,
2007). In the Amazonian mangrove studied, the mean annual carbon equivalent
efflux was 429.6 mg CO2eq. m-2 h-1. This value was very low
compared to the projected erosion losses of 103.5 Tg CO2eq. ha-1 yr-1 for the next century in tropical mangrove forests
(Adame et al., 2021). These higher
CO2 flux concomitantly with lower CH4 flux in this Amazonian
estuary are probably a consequence of changes in the rainfall pattern
already underway, where the dry season was wetter and the rainy season drier
when compared to the climatological normal. The most recent estimate between
latitude 0 to 23.5∘S shows an emission of 2.3 g CO2 m-2 d-1
(Rosentreter et al.,
2018b). However, the efflux in the mangrove of the Mojuim River estuary was
6.7 g CO2 m-2 d-1. For the same latitudinal range,
Rosentreter et al. (2018c) estimated an emission of 0.6 g CH4 m-2 d-1, and we found an efflux of 0.1 g CH4 m-2 d-1.
Drivers of greenhouse gas fluxes
Mangrove areas are periodically flooded, with a larger flood volume during
the syzygy tides, especially in the rainy season. The hydrological condition
of the soil is determined by the microtopography and can regulate the
respiration of microorganisms (aerobic or anaerobic), being a decisive
factor in controlling the CO2 efflux
(Dai et al.,
2012; Davidson et al., 2000; Ehrenfeld, 1995). No significant influence on
CO2 flux was observed due to the low variation in high tide level
throughout the year (0.19 m) (Fig. 2), although it was numerically higher at
the high topography. However, tidal height and the rainy season resulted in
a higher CO2 flux (rate high/low = 1.7) at the high topography (7.86 ± 0.04 g CO2 m-2 d-1) than at the low topography (4.73 ± 0.34 g CO2 m-2 d-1) (Fig. 2; Supplement S1). This result may
be due to the root systems of most flood-tolerant plants remaining active
when flooded (Angelov et
al., 1996). Still, the high topography has longer flood-free periods, which
only happens when the tides are syzygy or when the rains are torrential.
CO2 efflux was higher in the high topography than in the low topography
in the rainy season (when soils are more subject to inundation), i.e.,
39.8 % lower in the forest soil exposed to the atmosphere for less time.
Measurements performed on mangrove forest soils showed an average flux of
2.87 mmol CO2 m-2 h-1 when the soil was exposed to the
atmosphere (dry soil), while results on flooded mangrove forest soils showed
an average emission of 2.06 mmol CO2 m-2 h-1
(Alongi, 2007, 2009), i.e., 28.2 % less
than for the dry soil. This reflects the increased facility gases have for
molecular diffusion than fluids, and the increased surface area available
for aerobic respiration and chemical oxidation during air exposure
(Chen et al., 2010). Some
studies attribute this variation to the temperature of the soil when it is
exposed to tropical air (Alongi, 2009), which increases
the export of dissolved inorganic carbon (Maher
et al., 2018). However, despite the lack of significant variation
in soil temperature between topographies at each time of year (Fig. 4b),
there was a positive correlation (Pearson = 0.15, p= 0.05) between
CO2 efflux and soil temperature at the low topography.
Some studies show that CH4 efflux is a consequence of the seasonal
temperature variation in mangrove forest under temperate/monsoon climates
(Chauhan
et al., 2015; Purvaja and Ramesh, 2001; Whalen, 2005). However, in our
study, CH4 efflux was correlated with Ta (Pearson =-0.33, p<0.00) and RH (Pearson = 0.28, p= 0.01) only in the dry season and at
the low topography. The results show that the physical parameters do not
affect the fluxes in a standardized way, and their greater or lesser
influence depends on the topography and seasonality.
A compilation of several studies showed that the total CH4 emissions
from the soil in a mangrove ecosystem range from 0 to 23.68 mg C m-2 h-1 (Shiau and Chiu, 2020), and our study showed a
range of -0.01 to 31.88 mg C m-2 h-1 (mean of 4.70 ± 5.00 mg C m-2 h-1). The monthly CH4 fluxes were generally higher at
the low (0.232 ± 0.256 g CH4 m-2 d-1) than at the high
(0.026 ± 0.018 g CH4 m-2 d-1) topography, especially
during the rainy season when the tides were higher (Fig. 2). Only in the dry
season was there a significantly higher production at the low than at the
high topography (Fig. 2; Supplement S1). The low topography produced 0.0249 g C m-2 h-1 more to the atmosphere in the rainy season than in the dry
season (Fig. 2), and a similar seasonal pattern was recorded in other
studies (Cameron et al., 2021).
The mangrove soil in the Mojuim River estuary is rich in silt and clay
(Table 1), which reduces sediment porosity and fosters the formation and
maintenance of anoxic conditions
(Dutta et al., 2013). In addition,
the lack of oxygen in the flooded mangrove soil favors microbial processes
such as denitrification, sulfate reduction, methanogenesis, and redox
reactions (Alongi and
Christoffersen, 1992). A significant amount of CH4 produced in wetlands
is dissolved in the pore water due to high pressure, causing
supersaturation, which allows CH4 to be released by diffusion from the
sediment to the atmosphere and by boiling through the formation of bubbles.
Studies show that the CO2 flux tends to be lower with high soil
saturation
(Chanda
et al., 2014; Kristensen et al., 2008). A total of 395 Mg C ha-1 was
found at the soil surface (0.15 m) in the mangrove of the Mojuim River
estuary, which was slightly higher than the 340 Mg C ha-1 found in
other mangroves in the Amazon (Kauffman et
al., 2018), however being significantly 1.8 times greater at the low
topography (Table 2). The finer soil texture at the low topography (Table 1)
reduces groundwater drainage which facilitates the accumulation of C in the
soil (Schmidt et al., 2011).
Mangrove biomass
Only the species R. mangle and A. germinans were found in the floristic survey carried out, which
is aligned with the results of other studies in the same region
(Menezes et al., 2008). Thus, the variations found
in the flux between the topographies in the Mojuim River estuary are not
related to the mangrove forest structure, because there was no difference in
the aboveground biomass. Since there was no difference in the species
composition, the belowground biomass is not expected to differ either (Table 3).
Assuming that the amount of carbon stored is 42.0 % of the total biomass
(Sahu and Kathiresan, 2019), the mangrove
forest biomass of the Mojuim River estuary stores 127.9 and 138.9 Mg C ha-1 at the high and low topographies, respectively. This result is
lower than the 507.8 Mg C ha-1 estimated for Brazilian mangroves
(Hamilton and Friess, 2018), but is near the
103.7 Mg C ha-1 estimated for a mangrove at Guará's island
(Salum et al., 2020),
108.4 Mg C ha-1 for the Bragantina region (Gardunho,
2017), and 132.3 Mg C ha-1 in French Guiana
(Fromard et al., 1998). Thus, the biomass
found in the Mojuim estuary does not differ from the biomass found in other
Amazonian mangroves. The estimated primary production for tropical mangrove
forests is 218 ± 72 Tg C yr-1
(Bouillon et al., 2008).
Biogeochemical parameters
During the seasonal and annual periods, CH4 efflux was not
significantly correlated with chemical parameters (Table 4), similar as
observed in another study (Chen
et al., 2010). Flooded soils present reduced gas diffusion rates, which
directly affects the physiological state and activity of microbes, by
limiting the supply of the dominant electron acceptors (e.g., oxygen), and
gases (e.g., CH4) (Blagodatsky and Smith,
2012). The importance of soil can be reflected in bacterial richness and
diversity compared to pore spaces filled with water
(Banerjee et al., 2016). On the other
hand, increasing soil moisture provides the microorganisms with essential
substrates such as ammonium, nitrate, and soluble organic carbon, and
increases gas diffusion rates in the water
(Blagodatsky and Smith, 2012). Biologically
available nitrogen often limits marine productivity
(Bertics et al., 2010), and
thus can affect CO2 fluxes to the atmosphere. However, a mangrove
fertilization experiment showed that CH4 emission rates were not
affected by N addition
(Kreuzwieser et al.,
2003). A higher concentration of Cmic and Nmic in the dry period
(Table 2), both in the high and low topographies, indicated that
microorganisms are more active when the soil spends more time aerated in the
dry period (Table 2), time when only the high tides produce anoxia in the
mangrove soil mainly in the low topography. Under reduced oxygen conditions,
in a laboratory-incubated mangrove soil, the addition of nitrogen resulted
in a significant increase in the microbial metabolic quotient, showing no
concomitant change in microbial respiration, which was explained by a
decrease in microbial biomass (Craig et al.,
2021).
The high OM concentration at the two topographic locations (Table 2), at the
two seasons studied, and the respective negative correlation with CO2
flux (Table 5), confirm the importance of microbial activity in mangrove
soils (Gao et al., 2020). Also,
CH4 produced in flooded soils can be converted mainly to CO2 by
the anaerobic oxidation of CH4
(Boetius
et al., 2000; Milucka et al., 2015; Xu et al., 2015) which may contribute to
the higher CO2 efflux in the Mojuim River estuary compared to other
tropical mangroves
(Rosentreter et al.,
2018b). The belowground C stock is considered the largest C reservoir in a
mangrove ecosystem, and it results from the low OM decomposition rate due to
flooding (Marchand, 2017).
The higher water salinity influenced by the tidal movement in the dry season
(Table 1) seems to result in a lower CH4 flux at the low topography
(Dutta
et al., 2013; Lekphet et al., 2005; Shiau and Chiu, 2020). High
SO42- concentration in the marine sediments inhibits methane
formation due to competition between SO42- reduction and
methanogenic fermentation, as sulfate-reducing bacteria are more efficient
at using hydrogen than methanotrophic bacteria
(Abram and Nedwell, 1978;
Kristjansson et al., 1982), a key factor fostering reduced CH4
emissions. At high SO42- concentrations, methanotrophic bacteria
use CH4 as an energy source and oxidize it to CO2
(Coyne, 1999; Segarra et al.,
2015), increasing the efflux of CO2 and reduced CH4
(Megonigal and Schlesinger, 2002; Roslev
and King, 1996). This may explain the high CO2 and low CH4 efflux
found throughout the year at the high and especially at the low
topographies (Fig. 3).
Studies in coastal ecosystems in Taiwan have reported that methanotrophic
bacteria can be sensitive to soil pH, and reported an optimal growth at pH
ranging from 6.5 to 7.5 (Shiau et al., 2018).
The higher soil acidity in the Mojuim River wetland (Table 1) may be
inhibiting the activity of methanogenic bacteria by increasing the
population of methanotrophic bacteria, which are efficient in CH4
consumption
(Chen
et al., 2010; Hegde et al., 2003; Shiau and Chiu, 2020). In addition, the
pneumatophores present in R. mangle increase soil aeration and reduce CH4
emissions
(Allen
et al., 2011; He et al., 2019). Spatial differences (topography) in CH4
emissions in the soil can be attributed to substrate heterogeneity,
salinity, and the abundance of methanogenic and methanotrophic bacteria
(Gao et al., 2020). Increases in
CH4 efflux with reduced salinity were found as a consequence of intense
oxidation or reduced competition from the more energetically efficient
SO42- and NO3--reducing bacteria when compared to the
methanogenic bacteria
(Biswas et al.,
2007). This fact can be observed in the CH4 efflux in the mangrove of
the Mojuim River, because there was an increased CH4 production
especially in the low topography in the rainy season (Fig. 3), when water
salinity is reduced (Table 1) due to the increased precipitation. However,
we did not find a correlation between CH4 efflux and salinity, as
previously reported
(Purvaja and Ramesh,
2001).
Conclusions
Seasonality was important for CH4 efflux but did not influence
CO2 efflux. The differences in fluxes may be an effect of global
climate changes on the terrestrial biogeochemistry at the
plant–soil–atmosphere interface, as indicated by the deviation in
precipitation values from the climatology normal, making it necessary to
extend this study for more years. Using the factor of 23 to convert the
global warming potential of CH4 to CO2 (IPCC, 2001), the
CO2 equivalent emission was 35.4 Mg CO2eq. ha-1 yr-1.
Over a 100-year time period, a radiative forcing due to the continuous
emission of 0.05 kg CH4 m-2 yr-1 found in this study would be
offset if CO2 sequestration rates were 2.16 kg CO2 m-2 yr-1 (Neubauer and Megonigal, 2015).
Microtopography should be considered when determining the efflux of CO2
and CH4 in mangrove forests in an Amazon estuary. The low topography in
the mangrove forest of Mojuim River had a higher concentration of organic
carbon in the soil. However, it did not produce a higher CO2 efflux
because it was negatively influenced by soil moisture, which was indifferent
to CH4 efflux. OM, C/N ratio, and Eh were critical in soil microbial
activity, which resulted in a variation in CO2 flux during the year and
seasonal periods. Thus, the physicochemical properties of the soil are
important for CO2 flux, especially in the rainy season. Still, they did
not influence CH4 fluxes.
Data availability
The data used in this article belong to the doctoral thesis of Saul
Castellón, within the Postgraduate Program in Environmental Sciences, at
the Federal University of Pará. Access to these data can be requested from
Saúl Edgardo Martínez Castellón (saulmarz22@gmail.com), who holds the set of all data
used in this paper.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-19-5483-2022-supplement.
Author contributions
SEMC and JHC designed the study and wrote the article with the help of JFB,
MR, MdLR, and CN. JFB assisted in the field experiment. MR provided
logistical support in field activities.
Competing interests
The contact author has declared that none of the authors has any competing interests.
Disclaimer
Publisher's note: Copernicus Publications remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Special issue statement
This article is part of the special issue “Global change effects on terrestrial biogeochemistry at the plant–soil interface”. It is not associated with a conference.
Acknowledgements
The authors are grateful to the Program of Alliances for Education and
Training of the Organization of the American States and to Coimbra Group of
Brazilian Universities, for the financial support, as well as to Paulo
Sarmento for the assistance at laboratory analysis, and to Maridalva Ribeiro
and Lucivaldo da Silva for the fieldwork assistance. Furthermore, the
authors would like to thank the Laboratory of Biogeochemical Cycles
(Geosciences Institute, Federal University of Pará) for the equipment
provided for this research.
Financial support
This work has been financially supported by a doctoral thesis elaboration scholarship.
Review statement
This paper was edited by Lucia Fuchslueger and reviewed by two anonymous referees.
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