Science of the Total Environment 829 (2022) 154610

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Carbon dioxide and methane fluxes from mariculture ponds: The potential of
sediment improvers to reduce carbon emissions
⁎
Dongxu Zhang a, Jie He a, Wenjun Xu a, , Shuang Li b, Huiling Liu a,c, Xinru Chai a,c
a
Zhejiang Province Key Laboratory of Mariculture and Enhancement, Zhejiang Marine Fisheries Research Institute, Zhoushan 316021, PR China
b
Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, PR China
c
Marine and Fisheries Institute, Zhejiang Ocean University, Zhoushan 316021, PR China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Mariculture ponds acted as carbon sinks

on the whole at the water-air interface.
• The oxidation-based sediment improver
reduced CH4 emissions but not CO2 influx.
• Photosynthesis may play vital roles in off-
setting the CO2 from sediment oxidation.
• The sediment improver may reduce CH4
emissions by improving the sediment
environment.

A R T I C L E I N F O A B S T R A C T

Article history: The CO2 and CH4 fluxes across the water-air interface were determined in two groups of swimming crab (Portunus
Received 8 December 2021 trituberculatus)-ridgetail white prawn (Exopalaemon carinicauda) polyculture ponds. One group of ponds with sediment
Received in revised form 12 March 2022 improver application were referred to as SAPs, and the other group receiving no sediment improver were as NSPs. Dur-
Accepted 12 March 2022
ing the farming season, both the SAPs and NSPs acted as CO2 sinks and CH4 sources. The cumulative CO2-C fluxes from
Available online 18 March 2022
the SAPs and NSPs were −26.78 and −23.49 g m−2, respectively, and the cumulative CH4-C emissions from the SAPs
Editor: Jay Gan and NSPs were 0.24 and 0.28 g m−2, respectively. CO2 fluxes were significantly related to net primary production and
water pH, and CH4 fluxes were mainly regulated by water temperature during the farming season. The application of
Keywords: the oxidation-based sediment improver had a positive effect on reducing the CH4 emissions across the water-air inter-
Mariculture ponds face but had no effect on CO2 fluxes. The sediment improver reduced the organic matter contents and improved the
CO2 flux sediment pH and redox potential, which may have facilitated a decrease in CH4 production in the sediment. The
CH4 flux CO2 produced through the oxidation of organic material in the sediment may have been absorbed by strong photosyn-
Sediment improver thesis, resulting in a nonsignificant difference in CO2 fluxes between the SAPs and NSPs. The results indicated that the
Oxidation
application of sediment improvers in coastal polyculture ponds can reduce carbon emissions, especially CH4 emissions,
during the farming period and could help mitigate global warming with regard to the sustained-flux global warming
potential (SGWP) and sustained-flux global cooling potential (SGCP) models over a 20-year time horizon. Future stud-
ies on the CO2 and CH4 production rates of the sediment and the related microbial community could improve our un-
derstanding of the effect mechanism of the application of sediment improvers on CO2 and CH4 emissions from
mariculture ponds.

⁎ Corresponding author.
E-mail address: wjxu1971@hotmail.com (W. Xu).

http://dx.doi.org/10.1016/j.scitotenv.2022.154610
0048-9697/© 2022 Elsevier B.V. All rights reserved.
D. Zhang et al.
1. Introduction
Methane (CH4) and carbon dioxide (CO2) are the two most vital long-
lived greenhouse gases (GHGs) that contribute to global warming (IPCC,
2014). According to the annual GHG Bulletin of the World Meteorological
Organization (WMO), the atmospheric CO2 and CH4 concentrations
reached new highs in 2020, with CO2 at 413.2 ppm and CH4 at 1.889
ppm, which constituted 149% and 262%, respectively, of preindustrial
levels (WMO Greenhouse Gas Bulletin, 2021). The ever-increasing concen-
trations of GHGs have incentivized a number of studies concerning CO2 and
CH4 cycles in aquatic ecosystems (e.g., Striegl et al., 2012; Kirschke et al.,
2013).
Aquatic ecosystems can absorb or release GHGs across the water-air in-
terface and therefore play vital roles in regulating regional and even global
climate change (Duarte and Prairie, 2005). The carbon sink or source func-
tion across the water-air interface in aquatic ecosystems is dependent on
the direction of the CO2 and CH4 concentration gradient between the sur-
face water and the air (Cole and Caraco, 1998). The CO2 concentration in
water is essentially the result of carbon metabolism in aquatic ecosystems,
including pelagic and benthic metabolism (Hopkinson, 1985). Pelagic me-
tabolism in aquatic ecosystems has been studied extensively and is consid-
ered an important factor regulating CO2 emissions across the water-air
interface (e.g., Halbedel and Koschorreck, 2013; Gong et al., 2021). Never-
theless, benthic metabolism could also make a great contribution to the CO2
concentration in the water column especially in shallow aquatic ecosystems
(Algesten et al., 2005; Kortelainen et al., 2006; Kristensen et al., 2008). CH4
is mainly produced in the sediment in aquatic ecosystems, and is then par-
tially oxidized in the water column while transferring to the water-air inter-
face (Cao et al., 1996). Production and oxidation processes are the two
main factors determining CH4 emissions across the water-air interface.
Based on the above understanding, CO2 and CH4 emissions are closely
related to the biogeochemical processes in aquatic ecosystems, and sedi-
ments may play an important part in the CO2 and CH4 dynamics in aquatic
ecosystems.
Aquaculture ponds are a vital part of the global aquatic ecosystem, and
cover an estimated area of 1.56 × 106 ha on the Chinese coast (Duan et al.,
2020). Some studies on the characterization of GHG fluxes from aquacul-
ture ponds in coastal areas have been conducted (e.g., Yang et al., 2018;
Zhang et al., 2020; Tong et al., 2021). Due to the differences in aquaculture
farming and management practices, such as the cultured species and feed
types, different aquaculture systems usually experience different biogeo-
chemical processes and gaseous carbon emission patterns (Zhang et al.,
2022). Therefore, the current number of field observations of GHG emis-
sions in aquaculture ponds is still insufficient to better understand the
role they play in the global carbon cycle. The effects of different farming
and management practices on GHG emissions should also receive more
attention.
In aquaculture ponds, sediments are important environments, espe-
cially for cultured animals that mostly inhabit the bottom, such as crabs,
clams, and sea cucumbers (Boyd, 1995). During the farming season, organic
matter from feeds, residues, dead plankton, and feces of farming species set-
tles to the bottom of the ponds and gradually mixes with the soil (Boyd
et al., 2010), which could cause the deterioration of the sediment environ-
ment. The good health of aquaculture sediments is one of the most impor-
tant components to the success of aquaculture. In recent years,
aquaculture sediment improvers have been increasingly applied in aquacul-
ture ponds (Robinson et al., 2018; Raul et al., 2020). Sediment improvers
are chemical or biological products that aim to improve the physical, chem-
ical and biological conditions of sediments by removing the harmful or-
ganic and inorganic substances in the sediment through absorption,
oxidation or probiotic domination. According to their ingredients and the
ways in which they work, sediment improvers can be generally divided
into three main types, i.e., absorption-based, oxidation-based, and
probiotics. Oxidation-based sediment improvers usually take effect quickly
and are also environmentally friendly and hence popular among farmers.
Oxidation-based sediment improvers, which are mainly made from
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Science of the Total Environment 829 (2022) 154610
peroxides and other additives, may primarily aid in improving sediment
conditions by accelerating organic matter degradation and the biogeo-
chemical processes involved, such as the carbon, nitrogen and phosphorus
cycles. Considering the oxidation process and the potential improvement of
sediment conditions by sediment improvers, it was hypothesized that the
application of oxidation-based sediment improvers might decrease the in-
ternal CH4 production and emission across the water-air interface, and
CO2 production and emission might increase.
Polyculture ponds with swimming crabs (Portunus trituberculatus) and
ridgetail white prawns (Exopalaemon carinicauda) are common in coastal
China, especially in Zhejiang and Jiangsu Provinces. In this study, the ef-
fects of oxidation-based sediment improvers on CO2 and CH4 fluxes from
typical polyculture ponds were investigated. Six ponds were investigated
in this study: three that received sediment improvers and three that did
not. The objectives of the present study were 1) to characterize the possible
differences in the physical, chemical and biological parameters of water
and sediment between ponds with and without sediment improvers and
2) to determine the differences in the CH4 and CO2 fluxes between the
two treatments and the roles of sediment improvers in the CH4 and CO2
fluxes.
2. Materials and methods
2.1. Sampling ponds
The study was carried out on Daishan Island, Zhoushan city, China,
which has a typical subtropical monsoon climate. The mean annual temper-
ature is 17.2 °C and the mean annual precipitation is 1428.2 mm in the last
decade (2011−2020) according to the data from Zhoushan Municipal
Statistics Bureau (2022). The city of Zhoushan is an archipelago city, and
Daishan Island is the second largest island. Six ponds located in northwest-
ern Daishan Island were sampled in this study, and each pond covered an
area of approximately 2.3 × 104 m2 (~580 m in length and ~40 m in
width) (Fig. 1). All the ponds were stocked with swimming crab
(P. trituberculatus) and ridgetail white prawn (E. carinicauda), which is a
very popular farming pattern in the coastal areas of China, especially in
Zhejiang and Jiangsu Provinces. A total of 7.5 kg ha−1 stage II crabs were
stocked in early June, and 22.5 kg ha−1 berried prawns were stocked in
the middle of June in each pond. Trash fish were fed to the animals daily
during the farming season. The ponds were divided into two groups.
Three of them with sediment improver application were referred to as
SAPs. The sediment improver was used twice a month (4.5 kg ha−1 each
time) throughout the farming season (June 2020 to December 2020),
with an interval of ~15 days. The sediment improver applied in this
study was Dikang No. 1 and was produced by a biotechnology company
named Yumeikang (Hunan, China). According to the product information,
the main ingredients were peroxomonosulfate and chelators. The other
three ponds receiving no sediment improver during the farming season
were referred to as NSPs.
2.2. Gas sample collection and analysis
The initial sampling was conducted in late May after the ponds were
filled with water, and subsequent samples were taken approximately 1
week after the sediment improver was applied for the first time in each
month. The floating static chamber technique was applied to determine
the CO2 and CH4 fluxes. The floating chambers (inner diameter 30 cm,
height 50 cm) are composed of a transparent cylindrical acrylic resin cham-
ber without a bottom and a floating base (Chen et al., 2016). Three cham-
bers were deployed in each pond to measure the gas fluxes. The gas
samples were collected from each chamber with 100 mL syringes at 0, 10,
20, and 30 min and were then transferred into sample bags. Gas samples
were collected between 9:00 am and 12:00 am and were stored in a cooler
before being taken to the laboratory.
A gas chromatograph (GC-2010 Plus, Shimadzu, Japan) was used to de-
termine the CH4 and CO2 concentrations of the gas samples. CO2 and CH4
D. Zhang et al.
Fig. 1. Location of the mariculture ponds in Zhejiang, eastern China. NSPs, ponds without sediment improver; SAPs, ponds with sediment improver.
were separated at 40 °C by a Porapak Q column (60–80 mesh, SS-2 m × 2
mm) after gas sample injection. A flame ionization detector (FID) was
equipped to determine the CH4 concentrations at 100 °C, and CO2 was
first reduced to CH4 in an MTN-1 methanizer at 375 °C. CO2 and CH4 fluxes
were calculated from the slopes of gas concentrations over time. The equa-
tion is as follows:
M P T 0 dc
F¼ H
V 0 P0 T dt
where F is the flux (mg m−2 h−1 for CO2 and μg m−2 h−1 for CH4). T0, V0
and P0 refer to the air absolute temperature (K), gas molar volume (m3
mol−1) and atmospheric pressure (kPa) under standard conditions, respec-
tively. M is the molar mass (mg mol−1) of CO2 and CH4, P is the atmo-
spheric pressure (kPa), T is the air absolute temperature (K) during
sampling, and H is the height (m) of the chamber. dc/dt refers to the
slope of the gas concentration (c, ppm) curve variation over time (t, hour).
The sustained-flux global warming potential (SGWP, for gas emissions)
and sustained-flux global cooling potential (SGCP, for gas uptake) were cal-
culated to evaluate the warming or cooling effect of the aquaculture ponds
on climate, and the SGWP/SGCP values for CO2 were both 1, and the
SGWP/SGCP values for CH4 were 96 and 153, respectively, over a 20-
year period (Neubauer and Megonigal, 2015).
2.3. Water and sediment sample collection and analysis
In each pond (1.8 m in depth), the bottom, middle and surface layers
water samples of 3 different sites were collected using a horizontal sampler.
The dissolved oxygen (DO) and water temperature of the water samples
were determined using a YSI DO Meter (550A, USA). The accuracies for
3
Science of the Total Environment 829 (2022) 154610
DO and water temperature were 0.1% and 0.1 °C, respectively. Water salin-
ity was measured with a refractometer, and water pH was measured using a
pH meter (PHS-3C, REX Instruments, China). The accuracies for salinity
and water pH were 0.1 and 0.01, respectively. The samples were first stored
in plastic bottles and analyzed in the laboratory as soon as possible. Total
phosphorus (TP) and total nitrogen (TN) concentrations were determined
according to the method of Valderrama (1981). The detection limits of TP
and TN were 0.003 and 0.05 mg L−1, respectively, and the relative stan-
dard deviations were ≤3% and ≤2%, respectively. Total alkalinity (TA)
was analyzed with a titrator (848 Titrino plus, Metrohm, Switzerland).
The detection limit of TA was 0.002 mmol L−1, and the relative standard
deviation was ≤0.1%. Chlorophyll a (Chl a) was determined by the method
described by the National Standardization Management Council (2007).
The detection limit of Chl a was 2 mg m−3, and the relative standard devi-
ation was ≤6%.
The light and dark bottle method was applied to measure the net pri-
mary production (NPP) (Eaton et al., 1995). Near-bottom, middle and
surface layer water samples were collected from 3 different sites in
each pond. The initial DO of water samples from each depth was deter-
mined by the Winkler method. After 24 h, the DO concentrations of
water samples from the suspended 3 dark and 3 light bottles at each
depth were determined. NPP was calculated from the cumulative DO
differences between the initial values and the light bottles at each
water depth.
Sediment cores were collected using a core sampler (diameter 8 cm).
The redox potential and sediment pH at 5 cm depth of the samples were de-
termined using a pH/mV meter (IQ150, Spectrum, USA). The core samples
were oven-dried to a constant weight at 60 °C, ground and sieved using an
80-mesh sieve. According to Piron et al. (1990), the organic matter contents
of the core samples were determined by the combustion method.
D. Zhang et al.
2.4. Statistical analysis
Data were analyzed by SPSS Version 18.0. Differences in the yields of
crabs and prawn production between the two groups of ponds were tested
using Student's t-test. Using two-way repeated-measures ANOVA, the ef-
fects of the sediment improver application, the time of experiment, and
their interactions on the environmental variables and the CO2 and CH4
fluxes were analyzed. Pearson correlation coefficients were reported to de-
termine the correlations between CH4 and CO2 fluxes and environmental
parameters. A stepwise regression analysis was performed to assess the con-
tributions of environmental variables in regulating the CH4 and CO2 fluxes
from the mariculture ponds.
3. Results
3.1. Variations in the environmental parameters of water and sediment between
the NSPs and SAPs
The variations in the environmental parameters of water are demon-
strated in Fig. 2. The maximum and minimum water temperatures were
31.9 °C in August and 8.0 °C in December, respectively (Fig. 2a). The
mean DO concentrations in the NSPs and SAPs during the farming season
were 8.89 and 8.80 mg L−1, respectively, with no significant difference be-
tween them (P > 0.05, Fig. 2b). Water salinity in the NSPs and SAPs aver-
aged 24.9 and 25.0, respectively, with no significant difference between
them (P > 0.05, Fig. 2c). The TA averaged 2.28 mmol L−1 in the NSPs
and 2.45 mmol L−1 in the SAPs, and the water pH averaged 8.36 in the
NSPs and 8.38 in the SAPs, and there was no significant difference between
the two groups for either of these variables (P > 0.05, Fig. 2d, e). The aver-
age Chl a concentration in the NSPs was 20.05 mg m−3, which was signif-
icantly lower than that in the SAPs (22.11 mg m−3, P < 0.05, Fig. 2f). The
TN and TP concentrations averaged 2.35 and 0.22 mg L−1 in the NSPs and
2.45 and 0.23 mg L−1 in the SAPs, respectively (Fig. 2g, h). A significant
Fig. 2. Variations in the environmental parameters of the water in the NSPs and SAPs during the farming season. The data are shown as the means ± S.D. (n = 3). NSPs,
ponds without sediment improver; SAPs, ponds with sediment improver.
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Science of the Total Environment 829 (2022) 154610
difference was observed in the TN (P < 0.05) concentration, while no signif-
icant differences were found in the TP concentration between the two
groups (P > 0.05). The NPP in the NSPs averaged 0.34 g C m−2 d−1,
which was significantly lower than that in the SAPs (0.38 g C m−2 d−1,
P < 0.05, Fig. 2i). In terms of the variations over time, all the water environ-
mental variables varied significantly over time (P < 0.05) except dissolved
oxygen (P > 0.05), and no interaction effect of treatment and the time of
experiment conduction was found in any of the water environmental
variables (P > 0.05).
Fig. 3 shows the variations in the environmental parameters of the sed-
iment during the farming season. The sediment temperature varied simi-
larly to the water temperature, with the maximum (30.0 °C in the NSPs
and 30.1 °C in the SAPs) occurring in August and the minimum (8.9 °C in
the NSPs and 8.8 °C in the SAPs) occurring in December (Fig. 3a). The
redox potential of the sediment in the NSPs ranged from −169.3 to
−91.3 mV (mean: −143.6 mV), which was significantly lower than that
in the SAPs (ranging from −153.3 to −94.3 mV; mean: −132.4 mV, P <
0.05, Fig. 3b). The average sediment pH was 7.60 in the NSP group and
7.70 in the SAP group, and there was a significant difference between the
two groups (P < 0.05, Fig. 3c). The organic matter content increased grad-
ually during the farming season, averaging 3.88% of the dry weight in the
NSPs and 3.08% in the SAPs (Fig. 3d), with a significant difference between
the two groups (P < 0.05). In terms of the variations over time, all the sed-
iment environmental variables varied significantly over time (P < 0.05),
and no interaction effect of treatment and the time of experiment conduc-
tion was found in all the environmental variables (P > 0.05).
3.2. CO2 and CH4 fluxes in the NSPs and SAPs
The CO2 fluxes in all the mariculture ponds were negative throughout
the farming period (Fig. 4a). The CO2 fluxes varied from −25.84
to −8.59 mg m−2 h−1 (mean: −14.95 mg m−2 h−1) in the NSPs and
− 26.60 to −9.69 mg m−2 h−1 (mean: −17.05 mg m−2 h−1) in the SAPs
D. Zhang et al. Science of the Total Environment 829 (2022) 154610

Fig. 3. Variations in the environmental parameters of the sediments in the NSPs and SAPs during the farming season. The data are shown as the means ± S.D. (n = 3). NSPs,
ponds without sediment improver; SAPs, ponds with sediment improver.

Fig. 4. Variations in the CO2 (a) and CH4 (b) fluxes in the NSPs and SAPs during the farming period. The boxes mark the 25th and 75th percentiles, whiskers mark the 5th and
95th percentiles; dashed and solid horizontal lines indicate the mean and median values, respectively. NSPs, ponds without sediment improver; SAPs, ponds with sediment
improver.

(Fig. 4a), and there was no significant difference between the pond types (P > 3.3. Correlation between gas fluxes and environmental parameters
0.05). The CH4 fluxes in all the ponds had positive values during the farming
season (Fig. 4b). The CH4 fluxes in the NSPs and SAPs increased from the be- As shown in Table 2, water pH and Chl a explained 47.1% and 10.7% of
ginning of the experimental period, and after reaching a maximum in August, the CO2 flux variation in the NSPs, respectively, and the best-fit regression
the CH4 fluxes decreased gradually to the end of the experiment. The CH4 flux equation for the NSPs was F = 360–43.6 pH–0.545 Chl a, with R2 = 0.578
varied from 15.37 to 120.17 μg m−2 h−1 (mean: 65.43 μg m−2 h−1) in the and P = 0.000. In the SAPs, water pH was found to be the only variable
NSPs, which was significantly higher than that in the SAPs (14.50 to 96.37 with a significant contribution to CO2 flux, explaining 61.6% of the
μg m−2 h−1, mean: 56.60 μg m−2 h−1, P < 0.05, Fig. 4b).
As shown in Table 1, the average CO2-C flux was −23.49 ± 2.40 g m−2
in the NSPs and − 26.78 ± 3.43 g m−2 in the SAPs, and there was no signif- Table 1
icant difference between the pond types (P > 0.05). The average CH4-C fluxes Cumulated CH4 and CO2 fluxes (g m−2) in the NSPs and SAPs during the farming
period.
in the NSPs and SAPs were 0.28 ± 0.016 and 0.24 ± 0.017 g m−2, respec-
tively, and a significant difference was found between the two pond types Pond type CH4-C CO2-C Total gaseous C
(P < 0.05, Table 1). The cumulative carbon fluxes in the NSPs and SAPs NSPs 0.28 ± 0.016b −23.49 ± 2.40 −23.21 ± 2.41
were − 23.21 ± 2.41 and − 26.54 ± 3.44 g m−2, respectively, during SAPs 0.24 ± 0.017a −26.78 ± 3.43 −26.54 ± 3.44
the experimental period (Table 1). According to the SGWP/SGCP models, NSPs, ponds without sediment improver; SAPs, ponds with sediment improver. The
the cumulative CO2-eq uptake by the NSPs and SAPs was 50.29 and values are represented as the means ± S.D. Means in the same column with differ-
67.47 g CO2-eq m−2, respectively, during the farming season. ent superscripts are significantly different (P < 0.05).

5
D. Zhang et al. Science of the Total Environment 829 (2022) 154610

Table 2 According to previous studies, net primary production explains a large degree
Statistical results of the CH4 and CO2 multiple regression analysis of the NSPs, SAPs of CO2 flux variations in aquatic ecosystems and is an important factor affect-
and all ponds with explanatory environmental variables. ing CO2 dynamics (Yang et al., 2015; Bogard and del Giorgio, 2016), which
Pond type R2 value P value Contribution of each was in agreement with the results of this study. Considering that significant
variable correlations between Chl a concentration and CO2 flux were observed
pHwater Chl a (Tables 2 and Appendix Table A2), photosynthesis by phytoplankton might
CO2 0.578 0.000
NSPs
47.1% 10.7% play an essential role in regulating CO2 emissions in this study. In many
ST ORPsediment aquatic ecosystems, carbon metabolism in the water column usually domi-
CH4 0.885 0.000
69.6% 18.9%
pHwater
nates ecosystem metabolism (Duarte and Prairie, 2005). However, in addi-
CO2 0.616 0.000 tion to the carbon metabolism of water bodies, sediment metabolism can
61.6%
SAPs
ST ORPsediment also make a notable contribution to CO2 concentrations in the water column
CH4 0.825 0.000
69.4% 13.1% (Algesten et al., 2005; Kortelainen et al., 2006). Therefore, more detailed
pHwater Chl a
CO2 0.620 0.000 studies considering metabolic processes, including those in water and sedi-
55.2% 6.8%
All ponds
ST ORPsediment ment, are needed to clearly address the main drivers of CO2 flux within
CH4 0.849 0.000 aquatic systems.
66.9% 18.0%
In previous studies, CO2 flux from many aquatic ecosystems showed a
NSPs, ponds without sediment improver; SAPs, ponds with sediment improver.
pHwater, water pH; Chl a, chlorophyll a; ST, sediment temperature; ORPsediment, sed-
seasonal variation similar to temperature (e.g., Xiao et al., 2013; Yang
iment redox potential. et al., 2018), indicating the importance of temperature in driving CO2
flux variations. In this study, temperature was significantly positively corre-
lated with CO2 flux in all ponds (Appendix Table A2). In general, tempera-
variation in CO2 flux, and the best-fit regression equation was F = ture can affect CO2 flux in direct and indirect ways. First, water temperature
547–67.4 pH, with R2 = 0.616 and P = 0.000. According to the results can change the solubility of CO2 in the water, and in this regard, higher
of the combined analysis, water pH and Chl a contributed significantly to water temperature could promote CO2 emission from the water to the at-
variations in CO2 flux, explaining 55.2% and 6.8% of the CO2 flux variation, mosphere (Bates, 2006). Second, temperature might alter the CO2 concen-
respectively. The best-fit regression equation was F = 406–49.3 pH – 0.485 tration in the water by affecting the processes of carbon metabolism, such
Chl a, with R2 = 0.620 and P = 0.000. as photosynthesis (Chattopadhyay and Banerjee, 2008). In the present
Sediment temperature and sediment redox potential were found to con- study, Chl a and net primary production were significantly correlated
tribute significantly to the CH4 flux in the NSPs, SAPs and combined analysis with water temperature (r = 0.642 and 0.678, respectively, P < 0.01), dem-
according to the multiple stepwise regression results (Table 2). The sediment onstrating that water temperature could have a temporal effect on photo-
temperature and redox potential explained 69.6% and 18.9% of the CH4 flux synthesis and that CO2 flux can thus be affected in the process.
variation, respectively, in the NSPs, 69.4% and 13.1% in the SAPs, and 66.9% The main ingredient of the sediment improver used in the present study is
and 18.0% in the combined analysis. The best-fit regression equations were F potassium peroxomonosulfate, which has a strong oxidization capacity. With
= −117 + 4.60 ST – 0.548 ORPsediment (R2 = 0.885, P = 0.000) for the the application of the sediment improver, organic matter accumulation in the
NSPs, F = −79.4 + 3.61 ST – 0.410 ORPsediment (R2 = 0.825, P = 0.000) sediment of the SAPs could have been effectively alleviated; this may have
for the SAPs, and F = −101 + 4.10 ST – 0.505 ORPsediment (R2 = 0.849, been supported by the results of the significantly lower organic matter con-
P = 0.000) for the combined analysis. tent in the SAPs compared to the NSPs (P < 0.05, Fig. 3d). In general, the pro-
duction of CO2 from the oxidization of organic matter in sediment could have
4. Discussion contributed to the CO2 concentration increase in the water and possible sub-
sequent increase in CO2 emissions. However, in this study, the CO2 flux dur-
4.1. Influencing factors of CO2 flux and the effects of the sediment improver ing the farming season averaged −14.95 and − 17.05 mg m−2 h−1 in the
NSPs and SAPs, respectively (Fig. 4a), and there was no significant difference
In this study, water pH was significantly and negatively related to CO2 between the pond types (P > 0.05, Fig. 4a). This finding may be related to the
flux in the NSPs and SAPs and in the combined analysis (Tables 2 and release of nutrients from the sediment caused by the oxidization of the sedi-
Appendix Table A2), suggesting that water pH was an important variable ment improvers. During the oxidization process caused by the sediment im-
that was strongly linked to the CO2 flux variation. Given that HCO− 2−
3 , CO3 prover, the sediment could have released not only CO2 but also nutrients,
and CO2 contribute the majority of acid-base ions, water pH mainly depends especially nitrogen, into the water. The total nitrogen concentration in the
on the seawater carbonate system (Millero, 2000). According to the equilib- SAPs was significantly higher than that in the NSPs according to the results
rium of the carbonate system, when the proportion of CO2 in water bodies in- of the present study (P < 0.05, Fig. 2 g). Nutrients from sediment can promote
creases, the water pH usually decreases accordingly, and vice versa. As a the biomass of phytoplankton and subsequent primary production, and CO2
buffer system, the presence of the weak acid (H2CO3) and its conjugate produced from sediment oxidization could have been counterbalanced due
base (HCO− 3 ) could generally prevent a significant increase or decrease in to the stronger photosynthesis. The net primary production and Chl a concen-
seawater pH from dramatic ambient alterations. Since water pH can reflect tration in the SAPs in this study were significantly higher than those in the
the CO2 proportion in the inorganic carbon pool, a significant relationship be- NSPs, supporting this hypothesis.
tween CO2 flux and water pH has usually been observed in previous studies
(Soumis et al., 2004; Trolle et al., 2012; Zhang et al., 2020). Although 4.2. Factors influencing CH4 flux and the effects of the sediment improver
water pH could be affected by other biogeochemical processes, such as
phytoplankton photosynthesis, the connection between CO2 flux and water In this study, CH4 fluxes demonstrated an obvious seasonal variation in
pH was relatively stable and close. Therefore, the water pH in mariculture both the NSPs and SAPs, decreasing in the later parts of the experimental pe-
ponds can be considered a good indicator of CO2 flux. riod after peaking in August. The results of the correlation analysis and mul-
In this study, net primary production and Chl a were also found to be the tiple stepwise regression indicated that there was a significant positive
main factors significantly and negatively related to CO2 flux (Tables 2 and correlation between CH4 fluxes and temperature (Tables 2 and Appendix
Appendix Table A2). The CO2 concentration in water bodies is in fact the re- Table A2), suggesting that temperature was a vital variable affecting CH4
sult of the carbon metabolism process in aquatic ecosystems, which includes fluxes. In aquatic systems, the processes of CH4 formation in sediments and
processes of CO2 production, such as respiration, and processes of CO2 ab- CH4 oxidation during transmission of the water column eventually determine
sorption, such as photosynthesis. Net primary production could be a good in- the CH4 fluxes at the water-air interface. CH4 formation occurs exclusively in
terpreting variable that considers most of the abovementioned processes. anaerobic environments and is performed by methanogens; this process is

6
D. Zhang et al.
temperature dependent, and it was reported that higher temperatures could
promote CH4 emission by favoring the domination of methanogens that are
more effective in utilizing substrates and producing CH4 (Sekiguchi et al.,
1998; Ding and Cai, 2003). Moreover, the oxidation capacities of
methanotrophs, the main driver of CH4 oxidation, are also significantly posi-
tively correlated with temperature (Prieme and Christensen, 1997). Addition-
ally, higher temperatures may reduce the solubility of CH4 in the water
column and thus enhance CH4 emissions from water. Based on this under-
standing, temperature is generally considered a strong regulator of CH4
fluxes, and a significant correlation between CH4 fluxes and temperature is
usually observed in aquatic ecosystems when observed over a long period
of time (Xiao et al., 2013; Zhang et al., 2018).
According to the results of the correlation analysis in this study, net pri-
mary production and Chl a were significantly positively correlated with
CH4 fluxes, indicating that high algal production might contribute to CH4
emissions; this finding is consistent with the results of previous reports in
aquatic systems (e.g., Huttunen et al., 2002; Xing et al., 2005). It has been
demonstrated that newly produced organic carbon within aquatic systems
provides good substrates for methanogenesis and is very important for CH4
production, especially in shallow and highly productive waters (Damm
et al., 2008). Compared with old deposits, fresh carbon from primary produc-
tion may be more easily converted to CH4 given that methanogens can con-
sume photosynthate carbon more quickly (King and Reeburgh, 2002).
In the present study, the mean CH4 flux of all the ponds was
61.02 μg m−2 h−1, acting as a weaker CH4 source than inland waters
(Barros et al., 2011; Kirschke et al., 2013; Raymond et al., 2013). This could
be because the sediment condition of aquaculture ponds may not be the opti-
mum for methanogenesis. It was reported that the critical sediment redox po-
tential for the initiation of CH4 production was approximately from −150 mV
to −160 mV, and the optimum pH of CH4 production was near neutral (Wang
et al., 1993). However, in this study, the redox potentials in the ponds ranged
from −89 mV to −173 mV and the sediment pH ranged from 7.31 to 7.94.
The relatively higher values than the optimum were probably the limiting fac-
tors for CH4 production in the mariculture ponds. Furthermore, the mean or-
ganic matter content in the sediment was 3.48% in the ponds, one order of
magnitude smaller than those reported in lakes (e.g., Hahn-Schöfl et al.,
2011; Schrier-Uijl et al., 2011). This could be another reason for the lower
CH4 emissions from the ponds. Ecosystems such as reservoirs and lakes have
usually been flooded for decades; hence, a great amount of organic matter
has settled in the sediments in these environments. Mariculture ponds are
dried annually and then dredged. This management practice could result in
the oxidization of large quantities of organic matter due to exposure to air
and sunlight and thus favor the recovery of sediment pH and redox potential.
In this study, the CH4 fluxes in the SAPs were significantly lower than
those in the NSPs. The ANOVA results indicated that the sediment pH and
redox potential in the NSPs were significantly lower than those in the SAPs,
and the organic matter content in the NSPs was significantly higher than
that in the SAPs. These results suggested that sediment improvers might
have reduced CH4 emissions by altering the sediment condition to some-
where even less suitable for methanogenesis. CH4 is produced mainly in the
sediment, and in addition to temperature, the characteristics of the sediment,
such as organic substrate supply, sediment pH and redox potential, can also
have an impact on CH4 production (e.g., Dunfield et al., 1993; Megonigal
et al., 2005; Singh et al., 2000). The significant correlations between CH4
flux, sediment pH and redox potential in the present study (Appendix
Table A2) supported the findings in these previous reports. CH4 emissions
from aquatic ecosystems are ultimately regulated by microbial activities
(Reeburgh et al., 2007), and substrates for methanogenesis are a prerequisite.
In the anaerobic decomposition of organic matter, hydrolysis and fermenta-
tion produce initial substrates such as acetic acid for the final step of
methanogenesis (Duc et al., 2010). With the generation of acetic acid and uti-
lization of electrons in these preceding degradation processes, alterations in
sediment pH and redox potential could occur. Therefore, the application of
sediment improvers in the SAPs in the present study might have not only re-
duced the organic matter content in the sediment but also significantly in-
creased the sediment redox potential and pH.
7
Science of the Total Environment 829 (2022) 154610
Feed supply is one of the most important differences between aquacul-
ture systems and other aquatic ecosystems. Organic matter enrichment in
the sediment from residuals and feces could not only contribute to CH4 pro-
duction but also promote benthic aerobic respiration. Therefore, the reduc-
tion in organic matter accumulation in the sediment is of great significance
to making aquaculture ponds environmentally friendly with respect to the
mitigation of global warming. From the perspective of improving feed uti-
lization, establishing an efficient feeding strategy and integrated aquacul-
ture may be effective. A proper feeding frequency and feeding method
have been reported to improve feed utilization (Biswas et al., 2006; Silva
et al., 2007), and polyculture systems with proper combinations of cultured
animals could also enhance the utilization efficiencies of organic matter
(Zhang et al., 2016) and thus reduce organic matter accumulation in the
sediment. Additionally, based on the findings of this study, the application
of sediment improvers in aquaculture ponds during the farming season is
also helpful to mitigate organic matter enrichment in the sediment and
emissions of gaseous carbon, mainly CH4, across the water-air interface.
4.3. Limitations and future study
The results of the present study suggested the positive effect of
oxidation-based sediment improver on the reduction of GHG emissions, es-
pecially CH4, from mariculture ponds across the water-air interface. How-
ever, the study was conducted only during the farming season, rather
than based on year-round observations, including the farming and
nonfarming seasons. It was reported that pond sediment could also be a
hotspot of GHG emissions during the nonfarming season (Tong et al.,
2021). Given that the organic matter accumulation in pond sediment dur-
ing the farming season could be mitigated by sediment improvers, the
role of pond sediment in carbon sequestration and the total carbon budgets
of mariculture ponds still need to be clarified. In addition, future studies on
the GHG production rates of the sediment and the related microbial com-
munity could improve our understanding of the effect mechanism of the ap-
plication of sediment improvers on GHG emissions from mariculture ponds.
5. Conclusion
The results of the present study show that polyculture ponds with swim-
ming crabs and ridgetail white prawns are CO2 sinks but sources of CH4
emissions at the water-air interface during the farming period and could
help mitigate global warming with regard to the comprehensive GWP.
CO2 fluxes are significantly correlated with net primary production and
water pH, and CH4 fluxes are mainly regulated by water temperature dur-
ing the farming season. The application of oxidation-based sediment im-
provers had a positive impact on reducing CH4 emissions across the
water-air interface but had no effect on CO2 fluxes. Sediment improvers
can significantly reduce the organic matter content and improve the phys-
ical and chemical characteristics of the sediment, such as redox potential,
pH and organic matter content, thus reducing CH4 emissions. The results
also suggest that the CO2 produced by the oxidation of sediment improvers
can be absorbed by strong photosynthesis, which would not result in an in-
crease in the CO2 concentration in the water body.
CRediT authorship contribution statement
Dongxu Zhang: Conceptualization, Investigation, Formal analysis,
Writing - original draft. Jie He: Data curation, Formal analysis. Wenjun
Xu: Supervision, Writing - reviewing and editing. Shuang Li: Visualization,
Writing - reviewing and editing. Huiling Liu: Investigation. Xinru Chai:
Investigation.
Declaration of competing interest
The authors declare that they have no known competing financial inter-
ests or personal relationships that could have appeared to influence the
work reported in this paper.
D. Zhang et al. Science of the Total Environment 829 (2022) 154610

Acknowledgments Research Fund of Zhejiang Marine Fisheries Research Institute (Grant

No. 2020B04); the Major Agricultural Technology Cooperation Plan of
This work was supported by the National Science Foundation of Zhejiang Province (Grant No. 2020XTTGSC03). We sincerely
China (Grant No. 32002395); the National Key Research and Develop- thank the reviewers and editor for their constructive comments and
ment Program of China (Grant No. 2019YFD0900402); the Doctoral suggestions.

Appendix A

Table A1
Yields (kg ha−1) of the swimming crabs and ridgetail white prawns in the NSPs and SAPs.
Pond type Crabs Prawns

NSPs 660.0 ± 54.1a 785.0 ± 34.6

SAPs 780.0 ± 39.6b 835.0 ± 45.8

NSPs, ponds without sediment improver; SAPs, ponds with sediment improver. The values are represented as the means ± S.D. Means in the same column with different
superscripts are significantly different (P < 0.05).
The yield of crabs in the SAPs was 780.0 ± 39.6 kg ha−1, which was significantly higher than that in the NSPs (660.0 ± 54.1 kg ha−1, P < 0.05). No sig-
nificant difference was observed between the yields of prawns in the SAPs and NSPs, which were 835.0 ± 45.8 and 785.0 ± 34.6 kg ha−1, respectively (P >
0.05).

Table A2
Coefficients of Pearson correlation analysis between CH4/CO2 fluxes and environmental factors in mariculture ponds.
Environmental factors NSPs SAPs All ponds

CO2 flux CH4 flux CO2 flux CH4 flux CO2 flux CH4 flux

WT −0.511⁎ 0.741⁎⁎ −0.490⁎ 0.747⁎⁎ −0.493⁎⁎ 0.730⁎⁎

Chl a −0.592⁎⁎ 0.775⁎⁎ −0.617⁎⁎ 0.739⁎⁎ −0.616⁎⁎ 0.691⁎⁎
NPP −0.585⁎⁎ 0.814⁎⁎ −0.644⁎⁎ 0.847⁎⁎ −0.629⁎⁎ 0.748⁎⁎
pHwater −0.687⁎⁎ 0.677⁎⁎ −0.785⁎⁎ 0.671⁎⁎ −0.743⁎⁎ 0.643⁎⁎
TN −0.513⁎ 0.456⁎ −0.551⁎⁎ 0.524⁎⁎ −0.485⁎⁎ 0.452⁎⁎
ST −0.568⁎⁎ 0.834⁎⁎ −0.552⁎⁎ 0.833⁎⁎ −0.553⁎⁎ 0.818⁎⁎
ORPsediment 0.446⁎ −0.471⁎ NS NS 0.319⁎ −0.453⁎⁎
pHsediment NS −0.466⁎ NS NS NS −0.395⁎⁎

NSPs, ponds with no sediment improver; SAPs, ponds with sediment improver. WT, water temperature; Chl a, chlorophyll a; NPP, net primary production; pHwater, water pH;
TN, total nitrogen in water; ST, sediment temperature; ORPsediment, sediment redox potential; pHsediment, sediment pH. *, correlation is significant at the 0.05 level; **, cor-
relation is significant at the 0.01 level. n = 24 for both the NSPs and SAPs and n = 48 for all ponds.

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