However, the decrease in overall effect size on biodiversity with increasing publication year may not be a reflection of research bias, and rather a reflection of real changes in functional diversity of non-domesticated taxa observed on the ground. On the one hand, the reduction in the positive effect of diversified farming systems on species richness across time may be directly related to the unprecedented biodiversity loss terrestrial systems experienced in recent decades . On the other hand, over the years, diversified farming systems may provide shelter and the necessary resources to support more abundance, especially given the increasing reduction and degradation of natural habitats in agricultural landscapes.Aquaculture production has increased rapidly in the last decade, with the highest production mass in 2018.Shellfish mollusks constitute a significant portion of aquaculture production, accounting for 56.3% of marine and coastal aquaculture production in 2018 . China is the most productive country , and the production of fed aquaculture in China has quintupled since 2000 . The razor clam, constricted tagelus , is usually cultured along the coast of Fujian and Zhejiang provinces in China, accounting for 4.9% of the world’s total mollusk production in 2018 . The tagelus is an in faunal bivalve that inhabits fine sand, silt, or sandy-mud sediments . It filters suspended particles by stretching the “water tube” within the sediments to the water column, which filters suspended organic matter through its “water tube” and regulates the cycles of nutrients via filtration, ingestion, and excretion . Although mollusk aquaculture has wide-ranging benefits, such as providing protein and solving food security issues, there are potential environmental concerns that should be tackled to follow with this rapidly growing sector to maintain its sustainability . One of the most important environmental concerns is emissions of greenhouse gases ; the magnitude, ebb and flow tray pathway, and controlling factors in shellfish mariculture are poorly constrained.
Generally, there are two pathways in which the bivalve may introduce GHG to the water column and subsequently to the atmosphere: the bivalve produces GHGs in the gut and shell biofilm mediated by syntrophic microbes , and the sedimentary releases GHGs due to the benthic mollusks’ regulation of nutrients and GHG cycling . The most debated gas is carbon dioxide ; the inclusion of CO2 produced during bivalve shell production should be considered in the carbon trading system . Studies have shown that the growth of shelled mollusks releases CO2 via respiration . However, other studies have suggested that shellfish cultivation results in a CO2 removal process because calcification can fix carbon in a solid form . Methane and nitrous oxide are two non-CO2 GHGs that have a global warming potential that is 28 and 273 times that of CO2 over a hundred-year lifespan . They were recently found to be released significantly in coastal “blue carbon” systems and in aquaculture , which complicate GHG emission assessments . Thus, evaluating the potential of net GHG emissions from not only CO2 but also non-CO2 GHGs is reasonable. CH4 is mainly generated in a strictly anoxic environment mediated by microbes, known as methanogenesis , which is the last step in the degradation of organic matter. N2O is commonly produced in fresh and marine systems via microbial nitrification and denitrification . Bivalves were shown to induce a significant increase in CH4 and N2O efflux in marine sediments or in the anoxic gut, ascribed to microbial processes . In addition, dimethylsulfide is the most volatile sulfide in the oceans and is produced by the degradation of dimethylsulfoniopropionate . After being released into the air, DMS is oxidized to sulfate aerosols , an important driver that contributes partly to global warming . The global significance of GHG emissions from aquaculture ponds has been estimated , with large uncertainties due to poor-constrained consequences in emissions and insufficient data. In addition, different farming systems may introduce large discrepancies in GHG emissions; therefore, appropriate strategies are necessary to minimize the GHG footprint.
For example, the fed crab pond was found to be a significant GHG source, with emission rates of 18.8 mmol CH4/m2 /d and 0.002 mmol N2O/m2 /d . Another feeding aquaculture system, the shrimp pond, was a GHG hot spot, with 0.02 mmol CO2/m2 /d, 0.01 mmol CH4/m2 /d, and 0.47 μmol N2O/m2 /d . Ebullition is likely the major pathway contributing to CH4 emissions in specific ponds, accounting for over 80% of the total CH4 flux . Nutrient loading into ponds due to regular feeding can increase the availability of organic matter, which may stimulate primary production and eventually lead to high GHG emissions . Moreover, the literature suggested that water drainage can transform ponds from a sink to a source of atmospheric CO2 and strengthen CH4 and N2O emissions , indicating the role of sediment in GHG emissions. Notably, GHG fluxes and the net global warming potential of multiple GHGs from shellfish mariculture remain largely uncertain, with a few studies reporting the measured rates . In this study, we conducted two field surveys in a constricted tagelus farming system comprising two ponds: a man-made microalgae-bloom pond for fodder and a tagelus culture pond for harvest. We tracked the CO2, CH4, N2O, and DMS concentrations; estimated the sea-airfluxes of GHGs at the interface of seawater; and quantified the total potential effect of GHG emissions in a routine cycle of water exchange in these two ponds to evaluate the role of the tagelus farming system in GHG cycles. Moreover, we measured the environmental parameters and identified the drivers of GHG emissions to understand the factors controlling GHG emissions and propose suggestions for the management of shellfish mariculture.In this study, we examined the site-specific fluxes of three GHGs from two mariculture ponds. We found that the strongly positive CH4 and N2O fluxes in the ponds offset the uptake of CO2 in the microalgae-culture ponds despite the sea-air interface fluxes of CO2 being higher than those of non-CO2 GHGs . Consequently, the constricted tagelus farming system was a net GHG source during the two sampling periods by converting the CH4 and N2O fluxes into CO2-equivalent units. In general, the net emissions in the shellfish tanks were two to three times higher than that in the microalgae tanks,4×8 flood tray corresponding to the high emission rates of CH4 and N2O in pond B. In pond A, N2O was the main contributor of the total radiative forcing, contributing 47–55% of the total radiative forcing.
Combining the two ponds, our field measurement showed that the total CO2-equivalent fluxes in the tagelus farming system were 135.25 mmol/m2 /day in March and 30.37 mmol/m2 /day in April and that the draining water accounted for 56–71% of the fluxes. By considering the fluxes in the ditch to represent the natural processes, we can estimate that the potential of total radiative forcing was 47–83% higher in the tagelus farming system during one routine period of water exchange compared with that in the natural environment. However, by excluding the process of draining wastewater, which may disturb the sediment surface and result in high GHG emissions , the total radiative forcing was, in turn, 4–21% lower in the tagelus farming system than in the natural environment. Another notable finding is that non-CO2 GHGs accounted for 57% and 94% of the total CO2-equivalent fluxes in March and April, respectively, which indicates that non-CO2 GHG emissions could exacerbate the warming potential in the constricted tagelus culture. Reasonable control of water drainage and farming modes may reduce GHG emissions and nutrient excess. Our estimation of GHG emissions may be underestimated because of the unconsidered effect of ebullition, which may vary in different farming ponds. For example, ebullition was recorded as the major pathway of CH4 emissions in shrimp ponds and crab ponds but may be a minor source of atmospheric CH4 in reservoirs deeper than 5 m . Considering the shallow water depth of our ponds and the manner in which the constricted tagelus lives , more fieldwork is necessary to evaluate the contribution of ebullition. Comparing our results with those of other studies may reflect the complexity of GHG emissions from shellfish aquaculture. For example, the most recent study showed that only limited GHGs were released in a commercial oyster farm in Rhode Island based on laboratory incubations and field sediment cores , which is different from our results . The differences in farming modes , quantification methods , and living habits or species may explain this discrepancy. Specifically, our results were obtained in constricted tagelus farming ponds that require fertilizer to stimulate their production and growth. GHG emissions were calculated from empirical models, which provide a net value after all physical and biochemical processes. In addition, any activity of tagelus disturbs the sediments and increases the possibility of the sedimentary release of GHG . By contrast, oysters have naturally evolved to live in dense populations and did not require the supplementation of cultivated food for growth . They were lying in the farming facility or held in plastic mesh bags above the sediment surface, which may have had less effect on the sedimentary release of GHG. Importantly, the GHG emission rate of the specific species was directly evaluated by laboratory incubations, and the sediment GHG flux was measured using chambers in the field . Other studies on shellfish farming have also found low sea-air CH4 flux beneath oyster aquaculture, with a maximum value of 0.1 mmol/ m2 /d , which was different from our case, in which non-CO2 GHGs contributed to the main radiative forcing.
Hence, farm management, where rich nutrient water inflows into the shellfish pond, wastewater drains to the ditch, and there is man-made algae bloom for feeding , was the predominant driver in our study, leading to significant GHG emissions . Another study showed that mussels can cause the concomitant enrichment of organic matter in sediments . Although it may influence GHG biogeochemical processes in the system and increase the rate of GHG release below the farming sediments, the farming-caused GHG emission was not significantly different from reference conditions . Therefore, GHG emissions in shellfish mariculture may complicate not only different aquaculture modes but also the spatial and temporal variations in farming species. A finding from our results that may benefit the climate is the emission of DMS from the microalgae ponds, particularly during strong radiative forcing periods. DMS is believed to be one of the most important precursors of sulfate aerosols, contributing to cloud condensation nuclei . Thus, the release of DMS may reduce the potential effects of GHG emissions from the tagelus farming system. However, directly comparing the GHG emission potential between DMS and GHGs is difficult because no standard protocols are available. Because the DMS flux was less than 1% of the total CO2-equivalent flux, we did not discuss the contribution of the cooling effect driven by the DMS to the estimation of the potential of total radiative forcing. However, our results raised our attention to the local importance of the role of DMS in man-made algae-bloom aquaculture. From the results of the correlations and PCA , we deduced that the concentration of DIC in the pond is the main factor that determines the CO2 flux. Thus, the balance between CO2 from photosynthesis and respiration may lead to changes in CO2 emissions. When the solar radiation was weak in March, the DIC and pCO2 were relatively higher in pond A in March than in April during the daytime , which indicates low photosynthesis and high respiration in March. In addition, during the night, in the absence of photosynthesis, a significant increase in DIC and pCO2 was observed in March and April . High productivity may be linked to a subsequent high respiration rate during the night, resulting in more CO2 release, causing an S-shaped curve, which is consistent with our results. Moreover, microalgae tanks contain lesser DIC and release lesser CO2 than that in shellfish tanks; therefore, microalgae tanks can absorb more CO2 from the atmosphere, which can act as a short-time sequestered carbon pool. By contrast, shellfish tanks were found to be responsible for over 95% of the total CO2 emissions, with a higher DIC concentration than that in microalgae ponds.