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Renewable and Sustainable Energy Reviews 171 2023 113018 Available online 11 November 2022 1364-0321/© 2022 Elsevier Ltd. All rights reserved. Carbon sequestration via shellfish farming A potential negative emissions technology Jing-Chun Feng a,b,e,1,** , Liwei Sun a,b,e,1 , Jinyue Yan c,d,* a Research Centre of Ecology Received in revised form 1 October 2022; Accepted 23 October 2022 Renewable and Sustainable Energy Reviews 171 2023 113018 2 innovative cropland management, biochar application, and enhanced root phenotypes [9], all have good TRLs. However, the world’s soil degradation has had negative consequences on carbon storage in terms of the biological productivity, inducing the release of carbon back into the atmosphere [10]. BECCS seeks the win-win results of clean energy, negative emissions, and ecosystem services. Bioenergy crop production with extensive application of BECCS is conducted at the expense of pastures and grasslands, and can cause food security problems associ- ated with the reduction of the food crop production area [11]. Fertilizer utilization with BECCS inevitably causes environmental impacts [12]. It has been proven that other NETs, such as DAC, which directly pulls CO 2 from the atmosphere through chemical reactions, may only be feasible in specific and limited applications. Thus, it is difficult to conduct long-term CO 2 removal, which is restricted by high costs and low effi- ciency, on the scale with Gt a 1 [5]. NETs related to ocean activity have fewer challenges regarding food and land source competition, and such technologies are insensitive to the water intensity level [13]. The ocean is the largest active carbon pool on Earth, and thus, causing ocean related NETs are promising techniques for carbon emissions mitigation. Ocean liming and fertilization were once regarded as potential NETs. However, ocean fertilization has the drawback that the majority of the absorbed CO 2 is released back into the atmosphere when the phytoplankton decompose. Such methods may even reduce the yield of fisheries elsewhere by depleting other nutrients or increasing the risk of water deoxygenation [6]. Energy consumption for calcination, and sufficient vessels and port facilities are the main challenges in the large-scale application of ocean liming. In summary, it is difficult, if not impossible, to reliably mitigate the global warming trend before the 2050s. To tackle such difficulties related to the traditional NETs, NETs linked with anthropological economic activity, lower energy consump- tion, and lower capital and technology demands should be considered. Actually, mariculture in coastal areas can have an important impact on the marine carbon budget [13]. Like the carbon sequestration concept of BECCS, bivalve shellfish hereinafter referred as shellfish farming could be an effective method for capturing and removing carbon from the oceans [14,15]. More importantly, shellfish farming is characterized by low energy input, low costs, and technological feasibility. In shellfish farming, carbon storage is achieved naturally in shells, which enables the long-term, stable storage of carbon or cost-viable re-utilization as building materials. In addition, the interactions with phytoplankton populations via bio-deposition can significantly promote carbon sequestration in sediments, which is a long-term storage method [16]. However, whether or not shellfish farming can be considered a car- bon sink is controversial. In this study, the different perspectives were briefly reviewed. The positive point was mainly proposed by Tang et al. [14] and Humphreys et al. [17], who suggested that during shellfish farming, the unidirectional flow of carbon from the atmosphere to the sea as dissolved inorganic carbon, DIC and then into shells is seques- trated for a long time in solid form as CaCO 3 . Thus, the CO 2 is locked away from the atmospheric carbon cycle on the geological time scale. By harvesting shellfishes, DIC and organic carbon can be removed from the seawater. This view suggests that the carbon in the shells is a net CO 2 sink. According to the carbon budget, Ray et al. [18] suggested that the carbon sequestered in shells should be corrected to account for the CO 2 released during shell formation. In this case shellfish can either be a CO 2 sink or a source to the atmosphere. During calcification, 2 mol of HCO 3 are consumed and the released CO 2 basically has the same effect as the CO 2 captured from the atmosphere. In general, it is widely accepted that about 0.6 mol of CO 2 can be released into the atmosphere after buffering by the water column when producing 1 mol of CaCO 3 . However, this ratio highly depends on the temperature and salinity conditions of the seawater [19]. On the contrary, Munari et al. [20] suggested that shells are a net CO 2 source because the amount of CO 2 released through metabolic processes and shell formation is more than the amount of carbon sequestered in the shell in the farming environment. Ahmed et al. [21] and Mistri et al. [22] also argued that shellfish farming is a CO 2 source since the amount of carbon released through the calcification and catabolic mechanisms combined is larger than that assimilated into the shell. In addition, Filgueira et al. [23] further added the bio-deposition and mineralization of bio-deposits to the organism level based on the results of Munari et al. [20]. Filgueira et al. [23,24] also argued that bivalves are primarily farmed with the aim of producing food, and thus, shell production can be considered to be a by-product of the main ecosystem value of bivalve aquaculture. They provided a justification for parti- tioning the respired CO 2 between the soft tissue and shell when considering the bivalve shells in the carbon trading system. Based on these investigations, shellfish farming has the potential to be a net CO 2 sink in the specific ocean and atmosphere carbon cycles. In conclusion, the majority of the models that consider shellfish farming as a carbon source ignored the ecosystem function of shellfish farming. For example, the coupling of the interactions with phyto- plankton populations, suspended particle organic carbon, and DIC can significantly alter the CO 2 cycle. In the following section, a new po- tential NET concept, namely, carbon sequestration via bivalve shellfish Farming CSSF from the ecosystem perspective, is introduced. To accomplish this, the following questions are addressed. 1 Whether shellfish farming can effectively improve the absorption and long-term sequestration of CO 2 . If so, what is the mechanism 2 When taking the life cycle of greenhouse gas GHG emissions into account, can CSSF be a net carbon sink 3 How does the efficiency of CSSF compare to those of other eco- systems, such as mangroves and seagrass beds In this context, the carbon sequestrated in shells and soft tissues and the bio-deposition are estimated. The possible negative effects and corresponding solutions are also discussed in section 4.5. In addition, a suggestion that appeals to more positive actions regarding the future of CSSF is provided in section 4.6. 2. Materials and methods 2.1. Estimation of carbon sequestration Shellfish mainly absorb and utilize carbon in two ways, that is, via by carbon input from DIC uptake and organic carbon through ingestion. First, dissolved HCO 3 is absorbed from seawater to generate calcium carbonate shells Ca 2 2HCO 3 CaCO 3 CO 2 H 2 O 1 Additionally, organic carbon is utilized for the growth of shellfish. As List of abbreviations GHGs Greenhouse gases NET Negative emissions technologies BECCS Bioenergy with carbon capture and storage DAC Direct air capture CSSF Carbon Sequestration via bivalve Shellfish farming CCS Carbon capture and storage DIC Dissolved inorganic carbon CO 2 -eq Carbon dioxide equivalence TRL Technology readiness level J.-C. Feng et al. Renewable and Sustainable Energy Reviews 171 2023 113018 3 was discussed in Section 3.2, the amount of carbon captured in the shells, soft tissue, and sediments is defined as the input into the carbon sink. To estimate how much carbon was removed from the ocean by shellfish farming, it was necessary to make several assumptions or lim- itations to simplify the study. The first simplification was to limit the categories of farmed shellfishes to the five major categories of oysters, clams, scallops, mussels, and cockles as these are the five most common and major farmed species worldwide and in China. Second, due to the limited available information, only 11 varieties of farmed shellfish were selected for measurement of the dry weight ratio and carbon and protein contents detailed information is provided in S5. The third limitation was to assume that the ratio of the dry weight DW of the soft tissue to the shell was constant in each variety, and it was assumed that the carbon content in the shell and soft tissue in each category was constant. Four main factors, the shell carbon content, soft tissue carbon con- tent, dry weight of harvested shellfishes, and dry weight ratio of soft tissue and shell, were considered to calculate the amount of carbon sequestration. The total carbon sequestration in each type of shellfish was calculated as follows C T X 5 i 1 C Ti 2 C Ti C STi C Si C bi 3 C STi M i D i D STi w STi 4 C Si M i D i D Si w Si 5 C bi C depi R bi 6 where C T is the total carbon sequestrated in the different categories t. C Ti is the carbon sequestration for each specie, and i denotes the specific species of shellfish. C STi , C Si , and C bi are the amounts of fixed carbon in the soft tissue, in the shell, and via bio-deposition, respectively. M i is the amount of shellfish production in wet weight t, which was obtained from the China Fishery Statistical Yearbook for 1985–2019. D i is the ratio of the dry weight to the wet weight for the shellfish. D STi is the ratio of the dry weight for soft tissue to the dry weight of the shellfish, and D Si is the ratio of the dry weight of the shell to the dry weight of the total shellfish. w STi and w Si are the carbon contents of the soft tissue and the shell, respectively. C depi is the amount of carbon in the bio-sediments; and R bi is the ratio of the carbon sequestrated via deposition to the total carbon in the bio-sediments details are presented in S1. 2.2. Carbon budgets and carbon sequestration efficiency The carbon sequestration via bio-deposition, mainly including the feces and pseudo-feces of the shellfishes, was estimated based on the carbon budgets of the shellfish. The carbon budgets were determined through field observations and laboratory experiments, and the specific calculation is described in S1. The carbon sequestration efficiency of each technology was considered to be the carbon capture ability per unit area per year, which is shown in S3 The detailed value is shown in Table 1. 2.3. Emissions reducing potential in food production sector Shellfish is a type of food with the dual benefits of high nutrition and protein, and it has a lower carbon footprint than livestock products S6. When estimating the carbon emissions potential in food production, the carbon emission differences between the high-carbon and low-carbon foods were compared via the function unit of the same amount of protein. 3. Results 3.1. Carbon sequestration function of shellfish farming In the above section, the role of bivalves as a potential CO 2 sink was introduced from the perspective of an ecosystem context was intro- duced. Although phytoplankton can efficiently capture CO 2 due to their high intensity photosynthesis [25], most of the carbon absorbed from near-surface photosynthesis will be respired back into the epipelagic zone. Usually, less than 1 will be buried in the marine sediments [26, 27], resulting in the limited effects of ocean fertilization experiments. Farmed shellfish can use phytoplankton as food, and then, they grow shells to further sequester carbon in the form of CaCO 3 . In addition, shellfish farming could accelerate organic carbon deposition in seawater by generating pseudo-feces and feces, which also enhances long-term carbon sequestration [23,24]. However, farmed shellfish metabolize organic carbon fixed by phytoplankton and respire the CO 2 back into the air. The formation of shells also releases CO 2 Equation 1. Thus, whether shellfish farming is a carbon sink is determined by the key point of whether shellfish farming can lead to more effective carbon seques- tration in an ecosystem. The permanent carbon storage capacity mainly depends on the difference between the stored carbon and emitted car- bon. The life cycle carbon budgets Fig. 1 shows that the effective net sequestration ratios i.e., N R in Equation S3 of oysters, scallops, mus- sels, cockles, and clams are 13.64, 27.55, 12.55, 29.46, and 33.68, respectively. These net sequestration ratios are all much higher than those in a natural ecosystem less than 1, indicating that shellfish farming could significantly promote carbon capture and storage in the oceans. Thus, shellfish farming can be considered to be a potential NET. 3.2. Carbon sequestration potential According to the above analysis, the harvested carbon in shells and the carbon bio-deposited in sediments can be considered permanently separated from the marine water and biosphere. Although the carbon trapped in the soft tissue is eaten by people and enters the terrestrial carbon cycle, it contributes to reducing GHG emissions from the food production system, especially that of the meat production Section 3.5. The net sequestrated carbon can be defined as the percentage of carbon stored in the shells and in the sediments through bio-deposition because these two storage processes are permanent. Thus, the carbon captured in the shells, soft tissue, and sediments is defined as the amount input into the carbon sink. Recently, globally farmed shellfish were dominated by bivalves, with 17.30 Mt of fresh live weight in 2018, and the majority were from mariculture and coastal aquaculture [29]. Fig. 2 illustrates that global shellfish farming rapidly increased before 1995, followed by a steady Table 1 Carbon sequestration efficiency t CO 2 -eq ha 1 y 1 of farmed shellfish in China during 2011–2019. Species 2011 2012 2013 2014 2015 2016 2017 2018 2019 Oysters 11.07 10.89 11.56 11.72 11.61 12.66 12.65 12.78 12.93 Scallops 1.09 1.13 1.53 1.70 2.02 2.39 2.45 2.65 3.13 Clams 1.70 1.76 1.80 1.86 1.79 2.03 1.90 2.02 1.84 Cockles 11.70 11.16 11.19 13.06 14.18 14.11 13.77 20.61 19.06 Mussels 2.41 2.45 2.35 2.42 2.56 3.82 4.05 4.03 3.51 J.-C. Feng et al.
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