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Renewable and Sustainable Energy Reviews 171 (2023) 113018

Available online 11 November 2022

Carbon sequestration via shellsh farming: A potential negative

emissions technology

Jing-Chun Feng

, Liwei Sun

, Jinyue Yan

Research Centre of Ecology &Environment for Coastal Area and Deep Sea, Guangdong University of Technology, Guangzhou, 510006, PR China

Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, PR China

Future Energy Center, School of Business, Society and Engineering, M¨

alardalen University, SE-721 23, V¨

asterås, Sweden

Department of Building Environment and Energy Engineering, 999077, The Hong Kong Polytechnic University, Hongkong, China

Key Laboratory for City Cluster Environmental Safety and Green Development of the Ministry of Education, School of Ecology, Environment and Resources, Guangdong

University of Technology, Guangzhou, 510006, China

ARTICLE INFO

Keywords:

Shellsh farming

Carbon sink

Negative emissions technology

Carbon storage

Carbon budget

ABSTRACT

Negative emission technologies driven by nature with less energy input, lower costs, and long carbon storage

capacities are essential for meeting ambitious global carbon mitigation goals. This paper evaluates the carbon

sequestration potential of bivalve shellsh farming because its sequestration process is driven by nature, and it is

cost-effective and energy efcient. The carbon in shells and the carbon that enters sediments via bio-deposition

are long-lived forms of carbon. Using China as a case study, a preliminary estimation suggests that the carbon

sequestration efciency and intensity of cultivated shellshes are much higher than those of articial forests. In

China, approximately 6.23 Mt CO

-eq a

−1

was xed via net carbon sequestration during shellsh growth from

2015 to 2019. In addition, the farmed shellshes provided 0.37 Mt of harvested protein, and approximately

37.39 Mt CO2-eq a-1 were reduced compared to the same amount of protein provided by beef, and thus, shellsh

farming has the win-win benets of carbon sequestration and high-quality food provision. More importantly, a

total of 5.64 Gt CO

-eq, accounting for 17.63% of the total emissions in 2020, can be potentially sequestrated at

the global scale under the world’s largest farming area scenario.

1. Introduction

To best avoid a dangerous amount of global warming, a deep

reduction target of 2.0 ◦C and preferably 1.5 ◦C was proposed in the

2015 United Nations Framework Convention on Climate Change

(UNFCCC) Conference [1]. To achieve this goal, apart from a reduction

of industrial and agricultural emissions, approximately 600 Gt of CO

needs to be removed from the atmosphere and safely stored during this

century. Various negative emission technologies (NETs), including

reforestation and afforestation, ocean fertilization [2], bioenergy with

carbon capture and storage (BECCS) [3], and direct air capture (DAC)

have been proposed [4]. However, there are still a great deal of un-

certainties regarding the application of current NETs. Technology

readiness level (TRL), cost-effectiveness (in terms of both price and re-

sources), long-term storage capacity, and eco-friendliness or

environmental sustainability are the main constraining factors that

determine whether NETs can be effective enough to meet the ambitious

climate change mitigation goal in the Paris agreements (see Table 1).

Land-based technologies, such as reforestation, afforestation, habitat

restoration, and soil management, have gained signicant attention for

their negative emissions potential [5]. However, there are signicant

uncertainties regarding the actual achievable net negative emissions

rates, and the potential conicts related to the large amount of land use.

Afforestation directly competes with crops for arable land, and accord-

ingly causes food security problems. Increased res, droughts, pests, and

disease could jeopardize the stability of carbon storage in newly planted

forests [6]. In addition, the Amazon rainforest has been shown to be a

carbon source due to climate change and deforestation [7]. Large-scale

afforestation in mid-latitude and northern regions may have a net

warming effect [8].

Methods that can increase carbon storage in soils, including

* Corresponding author.

** Corresponding author. Research Centre of Ecology &Environment for Coastal Area and Deep Sea, Guangdong University of Technology, Guangzhou, 510006, PR

China.

E-mail addresses: fengjc@gdut.edu.cn (J.-C. Feng), jinyue@kth.se (J. Yan).

These authors contributed equally to this work.

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews

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

https://doi.org/10.1016/j.rser.2022.113018

Received 28 April 2022; Received in revised form 1 October 2022; Accepted 23 October 2022

Renewable and Sustainable Energy Reviews 171 (2023) 113018

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

from the atmosphere through chemical reactions, may only be feasible

in specic and limited applications. Thus, it is difcult to conduct

long-term CO

removal, which is restricted by high costs and low ef-

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

is released back into the

atmosphere when the phytoplankton decompose. Such methods may

even reduce the yield of sheries elsewhere by depleting other nutrients

or increasing the risk of water deoxygenation [6]. Energy consumption

for calcination, and sufcient vessels and port facilities are the main

challenges in the large-scale application of ocean liming. In summary, it

is difcult, if not impossible, to reliably mitigate the global warming

trend before the 2050s.

To tackle such difculties 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 shellsh (hereinafter referred as shellsh) farming could

be an effective method for capturing and removing carbon from the

oceans [14,15]. More importantly, shellsh farming is characterized by

low energy input, low costs, and technological feasibility. In shellsh

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 signicantly promote carbon

sequestration in sediments, which is a long-term storage method [16].

However, whether or not shellsh farming can be considered a car-

bon sink is controversial. In this study, the different perspectives were

briey reviewed. The positive point was mainly proposed by Tang et al.

[14] and Humphreys et al. [17], who suggested that during shellsh

farming, the unidirectional ow 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

. Thus, the CO

is locked

away from the atmospheric carbon cycle on the geological time scale. By

harvesting shellshes, DIC and organic carbon can be removed from the

seawater. This view suggests that the carbon in the shells is a net CO

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

released during shell formation. In this case shellsh can either be a CO

sink or a source to the atmosphere. During calcication, 2 mol of HCO

−

are consumed and the released CO

basically has the same effect as the

captured from the atmosphere. In general, it is widely accepted that

about 0.6 mol of CO

can be released into the atmosphere after buffering

by the water column when producing 1 mol of CaCO

. 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

source because the amount of CO

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 shellsh farming is a CO

source

since the amount of carbon released through the calcication 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 justication for parti-

tioning the respired CO

between the soft tissue and shell when

considering the bivalve shells in the carbon trading system. Based on

these investigations, shellsh farming has the potential to be a net CO

sink in the specic ocean and atmosphere carbon cycles.

In conclusion, the majority of the models that consider shellsh

farming as a carbon source ignored the ecosystem function of shellsh

farming. For example, the coupling of the interactions with phyto-

plankton populations, suspended particle organic carbon, and DIC can

signicantly alter the CO

cycle. In the following section, a new po-

tential NET concept, namely, carbon sequestration via bivalve shellsh

Farming (CSSF) from the ecosystem perspective, is introduced. To

accomplish this, the following questions are addressed.

(1) Whether shellsh farming can effectively improve the absorption

and long-term sequestration of CO

. 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 efciency 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

Shellsh 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

−

is absorbed from seawater to generate calcium

carbonate shells:

Ca2++2HCO−

3=CaCO3+CO2+H2O(1)

Additionally, organic carbon is utilized for the growth of shellsh. 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 Shellsh farming

CCS: Carbon capture and storage

DIC Dissolved inorganic carbon

-eq Carbon dioxide equivalence

TRL: Technology readiness level

J.-C. Feng et al.

Renewable and Sustainable Energy Reviews 171 (2023) 113018

was discussed in Section 3.2, the amount of carbon captured in the

shells, soft tissue, and sediments is dened as the input into the carbon

sink. To estimate how much carbon was removed from the ocean by

shellsh farming, it was necessary to make several assumptions or lim-

itations to simplify the study. The rst simplication was to limit the

categories of farmed shellshes to the ve major categories of oysters,

clams, scallops, mussels, and cockles as these are the ve most common

and major farmed species worldwide and in China. Second, due to the

limited available information, only 11 varieties of farmed shellsh 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 shellshes, 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 shellsh

was calculated as follows:

CT=∑

i=1

CTi(2)

CTi=CSTi+CSi+Cbi(3)

CSTi=Mi×Di×DSTi×wSTi(4)

CSi=Mi×Di×DSi×wSi(5)

Cbi=Cdepi×Rbi(6)

where C

is the total carbon sequestrated in the different categories (t).

is the carbon sequestration for each specie, and i denotes the specic

species of shellsh. C

STi

, C

, and C

are the amounts of xed carbon in

the soft tissue, in the shell, and via bio-deposition, respectively. M

is the

amount of shellsh production in wet weight (t), which was obtained

from the China Fishery Statistical Yearbook for 1985–2019. D

is the

ratio of the dry weight to the wet weight for the shellsh. D

STi

is the ratio

of the dry weight for soft tissue to the dry weight of the shellsh, and D

is the ratio of the dry weight of the shell to the dry weight of the total

shellsh. w

STi

and w

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

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 efciency

The carbon sequestration via bio-deposition, mainly including the

feces and pseudo-feces of the shellshes, was estimated based on the

carbon budgets of the shellsh. The carbon budgets were determined

through eld observations and laboratory experiments, and the specic

calculation is described in S1. The carbon sequestration efciency 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

Shellsh is a type of food with the dual benets 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 shellsh farming

In the above section, the role of bivalves as a potential CO

sink was

introduced from the perspective of an ecosystem context was intro-

duced. Although phytoplankton can efciently capture CO

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 shellsh can use phytoplankton as food, and then, they grow

shells to further sequester carbon in the form of CaCO

. In addition,

shellsh 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 shellsh metabolize

organic carbon (xed by phytoplankton) and respire the CO

back into

the air. The formation of shells also releases CO

(Equation (1)). Thus,

whether shellsh farming is a carbon sink is determined by the key point

of whether shellsh 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., NR 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 shellsh

farming could signicantly promote carbon capture and storage in the

oceans. Thus, shellsh 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 dened 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 dened as the amount input into

the carbon sink.

Recently, globally farmed shellsh 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

shellsh farming rapidly increased before 1995, followed by a steady

Table 1

Carbon sequestration efciency (t CO

-eq ha

−1

) of farmed shellsh 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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RenewableandSustainableEnergyReviews171(2023)113018Availableonline11November20221364-0321/©2022ElsevierLtd.Allrightsreserved.Carbonsequestrationviashellfishfarming:ApotentialnegativeemissionstechnologyJing-ChunFenga,b,e,1,,LiweiSuna,b,e,1,JinyueYanc,d,aResearchCentreofEcology&EnvironmentforCoastalAreaandDeepSea,GuangdongUniversityofTechnology,Guangzhou,510006,PRChinabSouthernMarineScienceandEngineeringGuangdongLaboratory(Guangzhou),Guangzhou,511458,PRChinacFutureEnergyCenter,SchoolofBusiness,SocietyandEngineering,M¨alardalenUniversity,SE-72123,V¨asterås,SwedendDepartmentofBuildingEnvironmentandEnergyEngineering,999077,TheHongKongPolytechnicUniversity,Hongkong,ChinaeKeyLaboratoryforCityClusterEnvironmentalSafetyandGreenDevelopmentoftheMinistryofEducation,SchoolofEcology,EnvironmentandResources,GuangdongUniversityofTechnology,Guangzhou,510006,ChinaARTICLEINFOKeywords:ShellfishfarmingCarbonsinkNegativeemissionstechnologyCarbonstorageCarbonbudgetABSTRACTNegativeemissiontechnologiesdrivenbynaturewithlessenergyinput,lowercosts,andlongcarbonstoragecapacitiesareessentialformeetingambitiousglobalcarbonmitigationgoals.Thispaperevaluatesthecarbonsequestrationpotentialofbivalveshellfishfarmingbecauseitssequestrationprocessisdrivenbynature,anditiscost-effectiveandenergyefficient.Thecarboninshellsandthecarbonthatenterssedimentsviabio-depositionarelong-livedformsofcarbon.UsingChinaasacasestudy,apreliminaryestimationsuggeststhatthecarbonsequestrationefficiencyandintensityofcultivatedshellfishesaremuchhigherthanthoseofartificialforests.InChina,approximately6.23MtCO2-eqa−1wasfixedvianetcarbonsequestrationduringshellfishgrowthfrom2015to2019.Inaddition,thefarmedshellfishesprovided0.37Mtofharvestedprotein,andapproximately37.39MtCO2-eqa-1werereducedcomparedtothesameamountofproteinprovidedbybeef,andthus,shellfishfarminghasthewin-winbenefitsofcarbonsequestrationandhigh-qualityfoodprovision.Moreimportantly,atotalof5.64GtCO2-eq,accountingfor17.63%ofthetotalemissionsin2020,canbepotentiallysequestratedattheglobalscaleundertheworld’slargestfarmingareascenario.1.IntroductionTobestavoidadangerousamountofglobalwarming,adeepreductiontargetof2.0◦Candpreferably1.5◦Cwasproposedinthe2015UnitedNationsFrameworkConventiononClimateChange(UNFCCC)Conference[1].Toachievethisgoal,apartfromareductionofindustrialandagriculturalemissions,approximately600GtofCO2needstoberemovedfromtheatmosphereandsafelystoredduringthiscentury.Variousnegativeemissiontechnologies(NETs),includingreforestationandafforestation,oceanfertilization[2],bioenergywithcarboncaptureandstorage(BECCS)[3],anddirectaircapture(DAC)havebeenproposed[4].However,therearestillagreatdealofuncertaintiesregardingtheapplicationofcurrentNETs.Technologyreadinesslevel(TRL),cost-effectiveness(intermsofbothpriceandresources),long-termstoragecapacity,andeco-friendlinessorenvironmentalsustainabilityarethemainconstrainingfactorsthatdeterminewhetherNETscanbeeffectiveenoughtomeettheambitiousclimatechangemitigationgoalintheParisagreements(seeTable1).Land-basedtechnologies,suchasreforestation,afforestation,habitatrestoration,andsoilmanagement,havegainedsignificantattentionfortheirnegativeemissionspotential[5].However,therearesignificantuncertaintiesregardingtheactualachievablenetnegativeemissionsrates,andthepotentialconflictsrelatedtothelargeamountoflanduse.Afforestationdirectlycompeteswithcropsforarableland,andaccordinglycausesfoodsecurityproblems.Increasedfires,droughts,pests,anddiseasecouldjeopardizethestabilityofcarbonstorageinnewlyplantedforests[6].Inaddition,theAmazonrainforesthasbeenshowntobeacarbonsourceduetoclimatechangeanddeforestation[7].Large-scaleafforestationinmid-latitudeandnorthernregionsmayhaveanetwarmingeffect[8].Methodsthatcanincreasecarbonstorageinsoils,includingCorrespondingauthor.Correspondingauthor.ResearchCentreofEcology&EnvironmentforCoastalAreaandDeepSea,GuangdongUniversityofTechnology,Guangzhou,510006,PRChina.E-mailaddresses:fengjc@gdut.edu.cn(J.-C.Feng),jinyue@kth.se(J.Yan).1Theseauthorscontributedequallytothiswork.ContentslistsavailableatScienceDirectRenewableandSustainableEnergyReviewsjournalhomepage:www.elsevier.com/locate/rserhttps://doi.org/10.1016/j.rser.2022.113018Received28April2022;Receivedinrevisedform1October2022;Accepted23October2022RenewableandSustainableEnergyReviews171(2023)1130182innovativecroplandmanagement,biocharapplication,andenhancedrootphenotypes[9],allhavegoodTRLs.However,theworld’ssoildegradationhashadnegativeconsequencesoncarbonstorageintermsofthebiologicalproductivity,inducingthereleaseofcarbonbackintotheatmosphere[10].BECCSseeksthewin-winresultsofcleanenergy,negativeemissions,andecosystemservices.BioenergycropproductionwithextensiveapplicationofBECCSisconductedattheexpenseofpasturesandgrasslands,andcancausefoodsecurityproblemsassociatedwiththereductionofthefoodcropproductionarea[11].FertilizerutilizationwithBECCSinevitablycausesenvironmentalimpacts[12].IthasbeenproventhatotherNETs,suchasDAC,whichdirectlypullsCO2fromtheatmospherethroughchemicalreactions,mayonlybefeasibleinspecificandlimitedapplications.Thus,itisdifficulttoconductlong-termCO2removal,whichisrestrictedbyhighcostsandlowefficiency,onthescalewithGta−1[5].NETsrelatedtooceanactivityhavefewerchallengesregardingfoodandlandsourcecompetition,andsuchtechnologiesareinsensitivetothewaterintensitylevel[13].TheoceanisthelargestactivecarbonpoolonEarth,andthus,causingoceanrelatedNETsarepromisingtechniquesforcarbonemissionsmitigation.OceanlimingandfertilizationwereonceregardedaspotentialNETs.However,oceanfertilizationhasthedrawbackthatthemajorityoftheabsorbedCO2isreleasedbackintotheatmospherewhenthephytoplanktondecompose.Suchmethodsmayevenreducetheyieldoffisherieselsewherebydepletingothernutrientsorincreasingtheriskofwaterdeoxygenation[6].Energyconsumptionforcalcination,andsufficientvesselsandportfacilitiesarethemainchallengesinthelarge-scaleapplicationofoceanliming.Insummary,itisdifficult,ifnotimpossible,toreliablymitigatetheglobalwarmingtrendbeforethe2050s.TotacklesuchdifficultiesrelatedtothetraditionalNETs,NETslinkedwithanthropologicaleconomicactivity,lowerenergyconsumption,andlowercapitalandtechnologydemandsshouldbeconsidered.Actually,maricultureincoastalareascanhaveanimportantimpactonthemarinecarbonbudget[13].LikethecarbonsequestrationconceptofBECCS,bivalveshellfish(hereinafterreferredasshellfish)farmingcouldbeaneffectivemethodforcapturingandremovingcarbonfromtheoceans[14,15].Moreimportantly,shellfishfarmingischaracterizedbylowenergyinput,lowcosts,andtechnologicalfeasibility.Inshellfishfarming,carbonstorageisachievednaturallyinshells,whichenablesthelong-term,stablestorageofcarbonorcost-viablere-utilizationasbuildingmaterials.Inaddition,theinteractionswithphytoplanktonpopulationsviabio-depositioncansignificantlypromotecarbonsequestrationinsediments,whichisalong-termstoragemethod[16].However,whetherornotshellfishfarmingcanbeconsideredacarbonsinkiscontroversial.Inthisstudy,thedifferentperspectiveswerebrieflyreviewed.ThepositivepointwasmainlyproposedbyTangetal.[14]andHumphreysetal.[17],whosuggestedthatduringshellfishfarming,theunidirectionalflowofcarbonfromtheatmospheretothesea(asdissolvedinorganiccarbon,DIC)andthenintoshellsissequestratedforalongtimeinsolidformasCaCO3.Thus,theCO2islockedawayfromtheatmosphericcarboncycleonthegeologicaltimescale.Byharvestingshellfishes,DICandorganiccarboncanberemovedfromtheseawater.ThisviewsuggeststhatthecarbonintheshellsisanetCO2sink.Accordingtothecarbonbudget,Rayetal.[18]suggestedthatthecarbonsequesteredinshellsshouldbecorrectedtoaccountfortheCO2releasedduringshellformation.InthiscaseshellfishcaneitherbeaCO2sinkorasourcetotheatmosphere.Duringcalcification,2molofHCO3−areconsumedandthereleasedCO2basicallyhasthesameeffectastheCO2capturedfromtheatmosphere.Ingeneral,itiswidelyacceptedthatabout0.6molofCO2canbereleasedintotheatmosphereafterbufferingbythewatercolumnwhenproducing1molofCaCO3.However,thisratiohighlydependsonthetemperatureandsalinityconditionsoftheseawater[19].Onthecontrary,Munarietal.[20]suggestedthatshellsareanetCO2sourcebecausetheamountofCO2releasedthroughmetabolicprocessesandshellformationismorethantheamountofcarbonsequesteredintheshellinthefarmingenvironment.Ahmedetal.[21]andMistrietal.[22]alsoarguedthatshellfishfarmingisaCO2sourcesincetheamountofcarbonreleasedthroughthecalcificationandcatabolicmechanismscombinedislargerthanthatassimilatedintotheshell.Inaddition,Filgueiraetal.[23]furtheraddedthebio-depositionandmineralizationofbio-depositstotheorganismlevelbasedontheresultsofMunarietal.[20].Filgueiraetal.[23,24]alsoarguedthatbivalvesareprimarilyfarmedwiththeaimofproducingfood,andthus,shellproductioncanbeconsideredtobeaby-productofthemainecosystemvalueofbivalveaquaculture.TheyprovidedajustificationforpartitioningtherespiredCO2betweenthesofttissueandshellwhenconsideringthebivalveshellsinthecarbontradingsystem.Basedontheseinvestigations,shellfishfarminghasthepotentialtobeanetCO2sinkinthespecificoceanandatmospherecarboncycles.Inconclusion,themajorityofthemodelsthatconsidershellfishfarmingasacarbonsourceignoredtheecosystemfunctionofshellfishfarming.Forexample,thecouplingoftheinteractionswithphytoplanktonpopulations,suspendedparticleorganiccarbon,andDICcansignificantlyaltertheCO2cycle.Inthefollowingsection,anewpotentialNETconcept,namely,carbonsequestrationviabivalveshellfishFarming(CSSF)fromtheecosystemperspective,isintroduced.Toaccomplishthis,thefollowingquestionsareaddressed.(1)Whethershellfishfarmingcaneffectivelyimprovetheabsorptionandlong-termsequestrationofCO2.Ifso,whatisthemechanism?(2)Whentakingthelifecycleofgreenhousegas(GHG)emissionsintoaccount,canCSSFbeanetcarbonsink?(3)HowdoestheefficiencyofCSSFcomparetothoseofotherecosystems,suchasmangrovesandseagrassbeds?Inthiscontext,thecarbonsequestratedinshellsandsofttissuesandthebio-depositionareestimated.Thepossiblenegativeeffectsandcorrespondingsolutionsarealsodiscussedinsection4.5.Inaddition,asuggestionthatappealstomorepositiveactionsregardingthefutureofCSSFisprovidedinsection4.6.2.Materialsandmethods2.1.EstimationofcarbonsequestrationShellfishmainlyabsorbandutilizecarbonintwoways,thatis,viabycarboninputfromDICuptakeandorganiccarbonthroughingestion.First,dissolvedHCO3−isabsorbedfromseawatertogeneratecalciumcarbonateshells:Ca2++2HCO−3=CaCO3+CO2+H2O(1)Additionally,organiccarbonisutilizedforthegrowthofshellfish.AsListofabbreviations:GHGsGreenhousegasesNETNegativeemissionstechnologiesBECCSBioenergywithcarboncaptureandstorageDACDirectaircaptureCSSFCarbonSequestrationviabivalveShellfishfarmingCCS:CarboncaptureandstorageDICDissolvedinorganiccarbonCO2-eqCarbondioxideequivalenceTRL:TechnologyreadinesslevelJ.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)1130183wasdiscussedinSection3.2,theamountofcarboncapturedintheshells,softtissue,andsedimentsisdefinedastheinputintothecarbonsink.Toestimatehowmuchcarbonwasremovedfromtheoceanbyshellfishfarming,itwasnecessarytomakeseveralassumptionsorlimitationstosimplifythestudy.Thefirstsimplificationwastolimitthecategoriesoffarmedshellfishestothefivemajorcategoriesofoysters,clams,scallops,mussels,andcocklesasthesearethefivemostcommonandmajorfarmedspeciesworldwideandinChina.Second,duetothelimitedavailableinformation,only11varietiesoffarmedshellfishwereselectedformeasurementofthedryweightratioandcarbonandproteincontents(detailedinformationisprovidedinS5).Thethirdlimitationwastoassumethattheratioofthedryweight(DW)ofthesofttissuetotheshellwasconstantineachvariety,anditwasassumedthatthecarboncontentintheshellandsofttissueineachcategorywasconstant.Fourmainfactors,theshellcarboncontent,softtissuecarboncontent,dryweightofharvestedshellfishes,anddryweightratioofsofttissueandshell,wereconsideredtocalculatetheamountofcarbonsequestration.Thetotalcarbonsequestrationineachtypeofshellfishwascalculatedasfollows:CT=∑5i=1CTi(2)CTi=CSTi+CSi+Cbi(3)CSTi=Mi×Di×DSTi×wSTi(4)CSi=Mi×Di×DSi×wSi(5)Cbi=Cdepi×Rbi(6)whereCTisthetotalcarbonsequestratedinthedifferentcategories(t).CTiisthecarbonsequestrationforeachspecie,andidenotesthespecificspeciesofshellfish.CSTi,CSi,andCbiaretheamountsoffixedcarboninthesofttissue,intheshell,andviabio-deposition,respectively.Miistheamountofshellfishproductioninwetweight(t),whichwasobtainedfromtheChinaFisheryStatisticalYearbookfor1985–2019.Diistheratioofthedryweighttothewetweightfortheshellfish.DSTiistheratioofthedryweightforsofttissuetothedryweightoftheshellfish,andDSiistheratioofthedryweightoftheshelltothedryweightofthetotalshellfish.wSTiandwSiarethecarboncontentsofthesofttissueandtheshell,respectively.Cdepiistheamountofcarboninthebio-sediments;andRbiistheratioofthecarbonsequestratedviadepositiontothetotalcarboninthebio-sediments(detailsarepresentedinS1).2.2.CarbonbudgetsandcarbonsequestrationefficiencyThecarbonsequestrationviabio-deposition,mainlyincludingthefecesandpseudo-fecesoftheshellfishes,wasestimatedbasedonthecarbonbudgetsoftheshellfish.Thecarbonbudgetsweredeterminedthroughfieldobservationsandlaboratoryexperiments,andthespecificcalculationisdescribedinS1.Thecarbonsequestrationefficiencyofeachtechnologywasconsideredtobethecarboncaptureabilityperunitareaperyear,whichisshowninS3(ThedetailedvalueisshowninTable1).2.3.EmissionsreducingpotentialinfoodproductionsectorShellfishisatypeoffoodwiththedualbenefitsofhighnutritionandprotein,andithasalowercarbonfootprintthanlivestockproducts(S6).Whenestimatingthecarbonemissionspotentialinfoodproduction,thecarbonemissiondifferencesbetweenthehigh-carbonandlow-carbonfoodswerecomparedviathefunctionunitofthesameamountofprotein.3.Results3.1.CarbonsequestrationfunctionofshellfishfarmingIntheabovesection,theroleofbivalvesasapotentialCO2sinkwasintroducedfromtheperspectiveofanecosystemcontextwasintroduced.AlthoughphytoplanktoncanefficientlycaptureCO2duetotheirhighintensityphotosynthesis[25],mostofthecarbonabsorbedfromnear-surfacephotosynthesiswillberespiredbackintotheepipelagiczone.Usually,lessthan1%willbeburiedinthemarinesediments[26,27],resultinginthelimitedeffectsofoceanfertilizationexperiments.Farmedshellfishcanusephytoplanktonasfood,andthen,theygrowshellstofurthersequestercarbonintheformofCaCO3.Inaddition,shellfishfarmingcouldaccelerateorganiccarbondepositioninseawaterbygeneratingpseudo-fecesandfeces,whichalsoenhanceslong-termcarbonsequestration[23,24].However,farmedshellfishmetabolizeorganiccarbon(fixedbyphytoplankton)andrespiretheCO2backintotheair.TheformationofshellsalsoreleasesCO2(Equation(1)).Thus,whethershellfishfarmingisacarbonsinkisdeterminedbythekeypointofwhethershellfishfarmingcanleadtomoreeffectivecarbonsequestrationinanecosystem.Thepermanentcarbonstoragecapacitymainlydependsonthedifferencebetweenthestoredcarbonandemittedcarbon.Thelifecyclecarbonbudgets(Fig.1)showsthattheeffectivenetsequestrationratios(i.e.,NRinEquationS3)ofoysters,scallops,mussels,cockles,andclamsare13.64%,27.55%,12.55%,29.46%,and33.68%,respectively.Thesenetsequestrationratiosareallmuchhigherthanthoseinanaturalecosystem(lessthan1%),indicatingthatshellfishfarmingcouldsignificantlypromotecarboncaptureandstorageintheoceans.Thus,shellfishfarmingcanbeconsideredtobeapotentialNET.3.2.CarbonsequestrationpotentialAccordingtotheaboveanalysis,theharvestedcarboninshellsandthecarbonbio-depositedinsedimentscanbeconsideredpermanentlyseparatedfromthemarinewaterandbiosphere.Althoughthecarbontrappedinthesofttissueiseatenbypeopleandenterstheterrestrialcarboncycle,itcontributestoreducingGHGemissionsfromthefoodproductionsystem,especiallythatofthemeatproduction(Section3.5).Thenetsequestratedcarboncanbedefinedasthepercentageofcarbonstoredintheshellsandinthesedimentsthroughbio-depositionbecausethesetwostorageprocessesarepermanent.Thus,thecarboncapturedintheshells,softtissue,andsedimentsisdefinedastheamountinputintothecarbonsink.Recently,globallyfarmedshellfishweredominatedbybivalves,with17.30Mtoffreshliveweightin2018,andthemajoritywerefrommaricultureandcoastalaquaculture[29].Fig.2illustratesthatglobalshellfishfarmingrapidlyincreasedbefore1995,followedbyasteadyTable1Carbonsequestrationefficiency(tCO2-eqha−1y−1)offarmedshellfishinChinaduring2011–2019.Species201120122013201420152016201720182019Oysters11.0710.8911.5611.7211.6112.6612.6512.7812.93Scallops1.091.131.531.702.022.392.452.653.13Clams1.701.761.801.861.792.031.902.021.84Cockles11.7011.1611.1913.0614.1814.1113.7720.6119.06Mussels2.412.452.352.422.563.824.054.033.51J.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)1130184andslightincrease.Theglobalannualyieldoffarmedshellfishhasexceeded10Mtsince2002,amongwhichmorethan80%isfromChina.InChina,theaverageamountofcarbonsequestratedthroughshellfishfarmingwasapproximately6.23MtCO2-eqa−1during2015–2019.Oysterfarminghasthegreatestcarbonsequestrationabilitybecauseithasthehighestyieldamongalloftheshellfishspeciesandboaststhebiggestshellvolume.Thecarbonsequestratedinshellsduringoysterfarmingisabout1.31MtCO2-eqa−1,accountingforapproximately83.96%ofthecarbonremoved.Thecontributionofcocklefarmingtocarbonremovalisthesmallest.Intotal,thecarbonsequestrationcapacityofChina’scoastalzoneswasapproximately6.23MtCO2-eqperyearduring2015–2019.Sequestratingthisamountofcarbonisequivalenttoacarbonsinkvalueof12.22MhaofartificialforestsbecausethecarbonsequestrationefficiencyofartificialforestsinChinaiscurrently0.51tCO2-eqha−1a−1[30].Fig.3showsthatontheglobalscale,ChinaisthemaincontributortothemarinecarbonsinkviaCSSF.Chilemadethesecondlargecontributiontothiscarbonsink(0.30MtCO2-eq)in2019,followedbyKorea(0.23MtCO2-eq),Spain(0.18MtCO2-eq),andJapan(0.18MtCO2-eq).TheUnitedStatesalsohasarelativelyhighsequestrationamount(0.11MtCO2-eq)comparedtotheremainingcountries.Thecarbonsequestrationpotentialofthemaximumshellfishfarmingareawasalsoestimated,whichispresentedinSupplementaryInformation(SI)SectionS2indetail.Indonesiahasthemaximumexpansionandyieldproductionpotential(about0.93Gt).Brazilhasthesecondlargepotential(0.16Gt),followedbyArgentina(0.59Gt)andAustralia(0.50Gt).Underthemaximumfarmingareascenario,atotalof9.27Gtoffarmedshellfishcanbeharvestglobally,andshellfishfarminginChinacanreaches26.65Mta−1.Atotalof5.64GtofCO2,about17.63%ofthetotalemissionsin2020,canbesequestratedattheglobalscale,whichislargerthanthetotalemissionsinIndia,theworld’sthirdlargestcarbonemitterin2019.Consideringthatthemaximumecologicalcapacityfallsshortofthemaximumexpandedfarmingareascapacity,approximately1.19GtofCO2canbesequestratedviaCSSFonthepremiseofensuringtheecologicalsafetywithIndonesia(11.32%),Brazil(7.48%),Argentina(7.21%),Australia(6.08%),andNamibia(5.31%)beingthetopfivecontributors.Thus,shellfishfarmingcouldbeveryconducivetoachievingcarbonneutrality.3.3.CarbonsequestrationefficiencyAsisshowninFig.4,thecarbonsequestrationefficiencyofshellfishfarminginChinaismuchhigherthanthatofartificialforests(AF),exceptforthatofcocklesandclams.Musselfarminghasthehighestefficiency(14.31tCO2ha−1a−1),followedbyoysters(11.99tCO2ha−1a−1).Bothmusselandoysterfarminghavehighersequestrationefficienciesthanthoseofsaltmarshes(SM),mangroves(MG),andseagrass(SG),whichare7.99,8.29and5.06tCO2ha−1a−1,respectively[31].Althoughclam(1.86tCO2ha−1a−1)andcockle(2.00tCO2ha−1a−1)farmingislessefficientthanSM,MG,andSG,theyperformbetterthantheaveragevalueforEastAsia’sartificialforests(AAF)andthatofChina’sartificialforests(CAF),whichare0.84tCO2and0.51tCO2ha−1a−1,respectively[32].CSSFcouldachievestablestorageformorethan100yearsbecauseitresultsinCaCO3formationorlong-termsedimentdeposition,whichisanotherimportantfactorfordeterminingtheefficiencyofanNET.3.4.LifecycleGHGemissionsofshellfishfarminginChinaThemainserviceprovidedbyshellfishaquacultureismeatproduction,andcarbonsequestrationfunctioncanbeconsideredtobeaby-productofthisanthropogenicactivity.Therefore,itisimportanttoindependentlyquantifythelifecycleGHGemissionstoseewhetherthisprocesswilloffsetthebenefitsofCO2sequestration.Fivetypesoffarmedshellfish(C.gigas,M.nobilis,M.edulis,T.granosa,andR.philippinarum)inChinawereselected,andtheir“fromcradletogate”carbonfootprintswereanalyzed(detailsarepresentedinSectionS4).Theenergyconsumedduringshellfishfarmingmainlyincludesdieselandelectricity.Thedieselisappliedfortransportationandvesselconsumption.Theelectricityismainlyconsumedforpumpingseawaterandaerationduringthehatcheryculturestage.Thelifecyclecarbonemissionsofthefarmedoyster(C.gigas),scallop(M.nobilis),mussel(M.edulis),clam(R.philippinarum),andcockle(T.granosa)are0.07,0.13,0.20,0.08,and0.17kgCO2-eqperkg,respectively.TheemissionsintheseedcultureFig.1.Carbonbudgetforshellfishlifecycles.Thecarbonuptakemainlyconsistsoforganiccarboningestionandtheassimilationofdissolveinorganiccarbon.Thecarbonismainlyreleasedthroughrespiration,calcification,andreproduction.Carbonsequestrationmainlyoccursthroughbio-depositionandshellandsofttissueharvesting.(A)ThecarbonbudgetoffarmedC.gigas,whichrepresentsthecarbonbudgetofoysters.(B)ThecarbonbudgetoffarmedC.farreri,whichrepresentsthatofscallops.(C)ThecarbonbudgetofM.edulis,whichrepresentsthatofmussels.(D)ThecarbonbudgetofS.subcrenata,whichrepresentsthatofcockles.(E)ThecarbonbudgetoffarmedM.meretrix,whichrepresentsthatofclams.J.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)1130185stage,accountforthemostimportantpart,mainlycomefromenergyinputs.AccordingtoEquation(2),foreachkilogramoffarmedshellfishharvested,0.15,0.17,0.21,0.15,and0.10kgofcarbonwillbecapturedforoyster,scallop,mussel,cockle,andclamfarming,respectively.Whenconvertedtothecarbondioxideequivalent,thesevaluesare0.54,0.62,0.77,0.54,and0.38kg,respectively.Giventhattheisolatedcarboncantotallyoffsetthelifecycleemissions,shellfishfarmingcanbeconsideredtobeanetcarbonsink.Comparedwithtraditionalfoods(beef,milk,pork,chicken,andeggs),farmedshellfishisamoresustainableproteinsourceandhassignificantadvantagesintermsofGHGemissions.AsestimatedinS6,thefarmedshellfishcanprovideabout0.37Mthigh-qualityproteinperyearforhumanconsumptioninChinafrom2015to2019(Fig.4B).Toproducethesameamountofprotein,beefproductionemits37.39MtmoreCO2-eq.Eveneggproductionemits6.09MtmoreCO2-eq.Otherbenefitsregardingmitigatingclimatechange,e.g.,mitigationofeutrophicationandenhancementofprimaryproductioninthesea,arediscussedinS7.4.Discussion4.1.SimilaritiesbetweenBECCSandCSSFBECCS(Fig.5A)isawidelyacceptedcarbonsink,whichhasthebenefitsofcleanenergy,negativeemissions,andecosystemservices[13].Fromanecosystemperspective,CSSF(Fig.5B)hasmanysimilaritiestoBECCSintermsofsequestratingcarboninanaturalway.(1)InBECCS,atmosphericcarbonisfirstabsorbedbyplantsandconvertedintobiomass.Similarly,inCSSF,atmosphericcarbonisdissolvedintheoceanandconvertedtoDIC.Then,itisabsorbedbyphytoplanktonandconvertedintobiomass.(2)InBECCS,thebiomassenergyisfurtherconvertedintoheatorelectricity.InCSSF,theDIC,thebiomassofthephytoplankton,andtheenergyareconvertedintosofttissueandshells.(3)InBECCS,thereleasedcarboniscapturedandstoredingeologicalformationsorembeddedinlong-lastingproducts.InCSSF,thecarbonisnaturallyabsorbedfromtheoceanandisusedtocreatetheshellsofshellfish.Inaddition,shellfishfarmingcanaccelerateorganiccarbondepositionfromseawaterbygeneratingpseudo-fecesandfeces,whichisconducivetothemarinecarbonsink[27].(4)InBECCS,theuncapturedCO2isreleasedintotheatmosphereagain.InCSSF,theCO2fromrespirationandcalcification(Equation(1))isreleasedintotheseawater.(5)InBECCS,theenergyisharvestedasausefulproduct.InCSSF,meat(softtissue)isharvestedasahigh-qualityfood.CSSFischaracterizedbyalowerenergyinputbecausethisprocessisdrivenbynatureandresultsincarboncaptureinastableandsolidstate.Inaddition,CSSFhassignificanteconomicbenefitsbecausetheshellfisharemainlyfarmedforfoodandthecarbonsequestrationfunctionisaby-product.Moreover,theindirecteffectsofshellfishfarmingontheecosystem,suchasthemitigationofeutrophicationandenhancementofprimaryproductionthroughincreasedwaterclarityandnutrientFig.2.Annualvariationsinglobalfarmedshellfishandsequestratedcarbon.(A)TheyieldproductionoffarmedshellfishinChina(yellowbars)andglobally(greenbars).(B)ThecarbonsequestratedviashellfishfarminginChina.Thepinkbarsrepresentthecarbonsequestratedviaoysterfarming;andthegreen,orange,blue,andlightpurplebarsrepresentthecarbonsequestratedviaclam,cockle,mussel,andscallopfarming,respectively.Itshouldbenotedthatasmallfractionofnon-bivalvespecies,e.g.,seasnailsandabalone,areincludedintheyieldproductionandgrowthratebecausetheircontributionissmallenoughtoignoreandishardtopreciselydeducttheircontributionbasedontheavailabledata.J.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)1130186turnover,alsohavepositiveimpactsontheCO2absorption[27].Basedontheaboveperspectives,CSSFcanbeanNETfortheoceanandatmosphere.4.2.HighefficiencyofCSSFThetimescaleoftheisolationfromtheatmosphericcarboncycleisanotherimportantfactorfordeterminingtheefficiencyofanNET.AlthoughatmosphericCO2concentrationscanbereducedbyvegetationsequestration,thecarbonstorageistemporaryandcanonlyreducetheatmosphericCO2concentrationsintheshort-term.AfewstudieshaveevenreportedthatthistypeoftemporarysequestrationcannotpreventclimatechangeandmayevenincreaseCO2concentrationsinthelong-term[33,34].Althoughthisideaisdebatableandtherearesomeopposingopinions(e.g.,DornburgandMarland[35]),itiswidelyacceptedthattheeffectivenessofshort-termcarbonsequestrationinmitigatingglobalwarmingshouldbediscounted[36,37].Takingforestsystemsasanexample,theenormousamountofcarbonstoredintreeisaffectedbybothdeforestationandwildfires[38].Regardingcarbonsequestration,researchershavestatedthatsoonerandlongersequestrationispreferred[35].Currently,manyproductsareusedinshortcycles,suchasfood,grass,wood,fuel,andpaper.Fromthispointofview,theydonotcontributetolong-termcarbonsequestration,nordotheysubstituteforothermaterialsthathavehighcarbonfootprints.ThemostimportantadvantageofCSSFisthatitcouldsequesterCO2inthelong-termviaeithershellgrowthorbio-deposition.CSSFcouldovercometheshortagesofoceancarbonsequestrationtosomeextentandfacilitateeffectiveisolation.TherearetwoprimitiveFig.3.Distributionofglobalcarbonsequestrationviashellfishfarmingin(A)1985and(B)2019,andthatunderfuturescenarioswiththe(C)maximumfarmingareaand(D)maximumecologicalcapacity.Thecoloredbarsineachsub-figurerepresenttheproductionofthecorrespondingcountryorregion.Fig.4.TheCarbonsequestrationefficiencyofshellfishfarming:(A)Comparisonofdifferentcarbonsequestrationsystems.SMrepresentssaltmarshsystems;MGrepresentsmangroveforestsystems;SGrepresentsseagrasssystems;AAFrepresentsEastAsia’sartificialforests(averagevalue);andCAFrepresentsChina’sartificialforests.(B)EstimatedproteinproducedbyshellfishfarminginChinafrom2015to2019.Thered,green,purple,yellow,andbluebarsrepresenttheproteinproducedviascallop,mussel,clam,cockle,andoysterfarming,respectively.J.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)1130187pathwaysforCO2absorptionintheocean.ThefirstisthenaturalabsorptionofCO2,includingabsorptionpromotedbyrockweatheringanddirectdissolution.ThesecondisDICabsorptionviaphotosynthesisandconversiontoorganiccarbon.ThedirectabsorptionofCO2fromtheatmosphereandconversionintoDICcouldcauseoceanacidification(OA),whichwouldreducetheprimaryproductivitywhenitreachedacertainlevel.Furthermore,DICisareactiveformandcanbereleasedbackintotheatmosphereoverashortperiod.Regardingrockweatheringprocesses,theformofthecarbonischanged,butitisnotsequestered,aswasstatedbyCurletal.[2].SuchwatersmayalsoincreasethepartialpressureofCO2inthesurfacelayeroftheoceans,therebyeitherslowingdownorreversingthetransferofatmosphericCO2intotheocean.FortheDICcapturedbyphotosynthesis,theabsorbedCO2trendstoberecycledbackthroughdecompositioninthesurfaceorsubsurfacewaters.Lessthan1%settlesoutofthewaterandispermanentlysequesteredinthesediments.Eventheoceanfertilizationschemecannoteffectivelyimprovethis.CSSFcouldfacilitatebio-deposition,resultinginlong-termcarbonsequestration.Fig.5.Schematicdiagramillustratingthemechanismsof(A)BECCS(bioenergywithcarboncaptureandstorage)and(B)CSSF(CarbonSequestrationviaShellfishFarming).POCisparticulateorganiccarbon,andDICisdissolvedinorganiccarbon.Thecarbonemissionbarsin(A)and(B)representthecarbonbudgetsofBECCSandCSSF,respectively.Thebluesquareinsideindicatesthatthecarbonemissionis0fromthebeginningtothecurrentstage,andafter/belowthisstagetheemissionisnegative.InBECCSthe0emissionrepresentthattheCO2isfirstcapturedbytheplantsandthenreleasedviapowerplantburning.AfterthereleasedCO2isrecapturedandstorageviageologicalmethod,thetotalemissionsinBECCSisnegative.InCSSF(B),the0emissionrepresentthattheCO2isfirstcapturedbyphytoplankton,andthenreleasedviashellfishmetabolization.AftertheDICisisolatedintheshell,andthePOCsequestratedinsofttissueandseabed,thetotalcarboninCSSFemissionsisnegative.J.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)11301884.3.AdvantageofGHGsemissionsreductioninfoodproductionsystemInadditiontoNETs,climatesmartsolutionsarenecessarytotransformthecurrentfoodproductionsystemsintomorecircularandclimate-neutralsystemstobettermeettheParisagreement.Currently,theglobalfoodproductionsystemcontributesabout30%ofglobalGHGemissions[39,40],ofwhichthebio-basedproductionsystemsareoftencoupledwithhighGHGemissions[41].Nevertheless,reducingemissionsfromthisindustryhasreceivedlessattentionandisverychallenging.Bio-basedproductionisaveryvaluablesourceofessentialnutrients(e.g.,essentialaminoacids,minerals,andvitamins),andemissionsmayseemtobeanunavoidableenvironmentalcostoffeedingthegrowingpopulation[42].Itisnoteworthythattheglobalfoodproductionsystemswillhavealargerenvironmentalfootprintby2050[43].CSSFisapromisingmethodofachievingfoodsecurity[44–46]whilestillachievingthegoalsofreducingemissions.Toremove600GtofCO2duringthiscentury,430–580millionhectaresoflandareneeded(aboutone-thirdofthecurrenttotalarablelandonEarth)forplantingcropsforBECCS[6].CSSFdoesnotrequirearableland.Onthecontrary,CSSFincreasesthesupplyofaffordablenutritionforhumanconsumption[44].Itwasestimatedinthisstudythatfarmedoysters,scallops,mussels,cockles,andclamscouldprovideabout0.37Mtofhigh-qualityproteinperyearforhumanconsumptioninChina.Moreimportantly,theanalysisconductedinthisstudyindicatesthatfarmedshellfishhavelowlifecycleemissions.Similarresultshavebeenwidelyreported[47–50].Shellfishmeathasbeenacceptedasapopularfoodthatprovideshigh-qualityproteinforalonghistory,soithasthepotentialtoreplaceaproportionofmeatproduction[44].TakingChinaasanexample,comparedtobeefproduction,shellfishcouldrelieveCO2emissionsbyabout37.39MtCO2-eqperyear(showninS6).Evencomparedwitheggproduction,shellfishfarmingcouldproduceasignificantadvantageinGHGemissionsreduction.Becauseshellfishfarmingdoesnotrequireaddedchemicals,commodityfeed,orantibioticsduringthefarmingstageinthesea,shellfishmeatisamuchmoreenvironmentallyfriendlyproduct[51].Shellfishfarminghasagreatexpansionpotentialsincetherequirementsfornon-renewableresourcesoffreshwaterandterrestriallandareminimal[47,50],anditistechnologicallyfeasible.Afterconstrainingthesuitablefarmingarea,thatwiththewaterdepthsoflessthan200m,asuitabletemperaturerange,andahighchlorophyllcontent,andexcludingareasdesignatedformarineanimalprotectionandfishing-boatactivityareas,atleast1,500,000km2areavailableforshellfishfarming[52].Inthisscenario,morethan5.6GtofCO2a−1wouldbesequestratedattheglobalscale.4.4.SynergisticbenefitswithotherstrategiesAswaspreviouslydiscussed,shellfishfarmingcanhelpreduceemissionsinfoodproductionsystems.Therefore,CSSFcancertainlyplayasynergisticroleinemissionsreductionwithdietarymanagementstrategies.Aswasprojectedinapreviousstudy[53],thecumulativeGHGemissionscausedbyfoodconsumptionfrom2020to2060willbe374GtCO2equivalent.However,byreplacingthetraditionalmeatby10%,30%,and50%withmusselmeat,thecumulativeGHGemissionscanbereducedby4.5%,13.6%,and22.4%,respectively.Althoughaplant-richdietcanalsoresultinasignificantreduction,amusselorshellfishrichdietcouldbeahealthierandmorenutritiousoption,asshellfishmeatisrichinprotein,docosahexaenoicacid,andmicronutrients[44,54,55].ShellfishfarmingcouldbecoupledwithotheroceanicNETssuchasoceanfertilization.Forexample,oceanfertilizationcouldbeperformedinchlorophyllbarrenareasandeveninareaswithwaterdepthsofgreaterthan200m,whichcouldstimulateanalgaebloom,thuseffectivelyexpandingtheseaareasuitableforshellfishframing.Furthermore,shellfishfarmingcanrapidlyfilterouttheorganiccarbonanddeposititontheseedbed.Thus,thecarbonsequestrationintraditionalfertilizationexperimentscouldbesignificantlypromoted.Althoughthefeasibilityofthiscombinationlacksexperimentalevidence,itisworthattemptingbecauseithaslongbeenproventhatunderprecisecontrolofthefarmingvolumes,thecombinationofshellfishfarmingandphytoplanktonphotosynthesiscanabsorbmoreCO2fromtheatmospherethanasinglesystem[56].Thepositiveenvironmentalandecologicaleffectsofshellfishfarmingareimportantforclimatechangemitigation.Theindirecteffectsofshellfishfarmingontheecosystem,suchasthemitigationofeutrophicationandenhancementofprimaryproductionthroughincreasedwaterclarityandnutrientturnover,willaffecttheCO2cycle[24].Previousstudies[56],havereportedthatarelativelylowabundanceofclamscoulddoubleprimaryproductionandalterthephytoplanktoncommunitystructure.Ingeneral,intensivegrazingbyculturedbivalvesisexpectedtoreducewaterturbidity,andimprovelightpenetrationtothebottom,andthusextendsthewaterdepthsuitableforthegrowthofbenthicmacrophytesandmicrophytobenthos[57].Inanutrient-limitedsystem,shellfishperformbottom-upcontrolofphytoplanktonbyincreasingtherateofnutrientcyclingandconsequentlyimprovesthenutrientavailability[58].Insummary,itisimportantforshellfishfarmingtoworkinsynergywithotherecologicalmanagementandrestorationprojects.4.5.PotentialnegativeimpactsofshellfishfarmingLikeotherhumanactivities,large-scaleshellfishfarmingexpansionwillinevitablyexertnegativeimpacts.Oneofthemostfrequentlyreportedimpactisover-farming,inwhichthefarmingcapacityexceedsoverthemaximumecologicalcarryingcapacity[59].Thiswillcauseareductionintheprimaryproductivity[60].OnepromisingwaytoavoidtheseeffectsisthroughtheadoptionofIntegratedMulti-TrophicAquaculture(IMTA).Sar`aetal.[61]demonstratedthatmussels(M.galloprovincialis)andtheEuropeanflatoyster(O.edulis)hadhighergrowthratesnearfishfarmscomparedtothatintheopensea.Moreover,shellfishover-farmingmayalsohavenegativeeffectsonthebenthicenvironmentandspeciesassemblagesviaadditionalbio-deposition.Sedimentorganicenrichmentthroughfecaldepositionfromfarmedshellfishcouldcreateanaerobicandacidicconditions,resultinginadverseeffectscausedbyelevatedlevelsofsulfidesandammonium[62].OnepossiblewaytoavoidtheseimpactsisthroughtheadoptionofBestManagementPractices(BMPs),suchasselectionoffarmingsiteswithappropriatewaterdepthsandwaterflowcharacteristics,andtheadoptionoffarmlayoutsthatavoidexcessivedensity[63].Actually,thelocalwaterchemistrymaychangeinanegativewayintermsofthetotalalkalinity(TA)andoceanacidification(OA)ifshellfisharefarmedinanextremelyinappropriateway.However,theimpactontheTAisnegligiblecomparedtothestrongbufferingcapabilityoftheoceans,whichabsorblargeamountsofbicarbonateviarockweatheringandriverdischargeintothesea.TheimpactsonOAaremainlycausedbytheCO2releaseduringrespirationandcalcification,whichcouldbecompletelycounteractedbyphotosynthesiswhenthefarmingvolumeisproperlycontrolled.Forexample,aM.coruscusandG.lemaneiformispolyculture[64]witharatioof1:0.45couldeffectivelyincreasethepHandCO2absorptioncapacityofseawater.Phytoplankton,whichcouldabsorbmorethan18.3GtofCO2peryearintheocean,ismoreefficientintermofphotosynthesis[65]andismoreabletooffsettheimpactsofOA.4.6.PositiveactionsareimperativeAlthoughshellfishfarmingseldomdependsonnonrenewableresources,large-scaleexpansionofshellfishfarmingmaystillhavemanychallengesintermsofglobalwarming.Forshellfishfarmingexpansion,theearlierthebetter.Currently,mostareasinalmostallcoastalcountriesaresuitableforaquaculture[52].However,iftheglobalwarmingJ.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)1130189trendpersistsinthefuture,itwillmostlikelyresultinseriousshrinkageoftheareasuitableforaquacultureandshellfishfarming.AsproposedbyFroehlichetal.[60],theproductionpotentialofaquaculturewilldeclineinmostofthesuitableareasovertime,withthepotentialofsomeareasevendisappearingcompletelyduetotemperaturechangesandtheresultantdecreaseinthechlorophyllcontent.OAcausedbytheCO2emissionswillpersistentlyexistandwillfurtherlowerthepHofthesurfacelayeroftheoceans.Inaddition,OAwillpotentiallythreatenthebio-calcificationofshellfishfarming.Gazeauetal.[19]demonstratedthatthecalcificationratesofM.edulisandC.gigassignificantlydecreaseasthepCO2increases.Milleretal.[66]alsoreportedthatOAcouldhaveanegativeimpactontheoystergrowth.Tofacethispotentialchallenge,newgeneticbreedingtechniquescanbeusedtobreednewvarietiesofshellfishesthatcantolerateoradapttohightemperaturesandOA.Newfarmingmodels,suchastheshellfish-algaepolycultures,mightmoresustainableunderthecontextofOA.TheculturingofmacroalgaefacilitatesabsorbingmoreCO2fromtheseawaterandincreasesthepHofthelocalseawater.Thus,moreresearchisessentialinthesefields.5.ConclusionsExploringthecarbonsinkpotentialoftheoceanisessentialtoachievingtheambitiousgoalofcarbonneutrality.Thisstudyproposedanewconcept,carbonsequestrationviashellfishfarming(CSSF),whichisapotentialnegativeemissiontechnologydrivenbynaturalprocesses.ThecarbonsequestrationmechanismofCSSFwasanalyzedfromacomprehensiveandobjectiveperspective,andthecarbonsequestrationpotentialandefficiencyofCSSFwereinvestigatedandcomparedwithothernegativeemissionsystems.Theresultssuggestthatthecarbonsequestrationefficiencyandintensityofcultivatedshellfishesaremuchhigherthanthoseofartificialforests.Underthelargestfarmingareascenario,atotalof5.64GtCO2canbepotentiallysequestratedthroughcarbonsequestrationviashellfishfarming.Thisresearchhighlightsthefundamentalimplicationsofmarinecarbonsequestrationtechnologyandlow-carbonfoodsupply.Resultsshowthattheoysterandmusselfarmingshowsignificantadvantageincarbonsequestrationefficiency.Thescallopandcockleperformbetterinproteinproductionandcarbonfootprint,andthus,aremoreconducivetocarbonemissionreductioninfoodproduction.AnalysisfromtheperspectiveofecosystemshowsthatCSSFcanbeaNETswithwelltechnologyreadinesslevels.6.UncertaintiesandlimitationsofthisstudyThesuggestionoftheCO2sinkfunctionofshellfishfarmingwasbasedontheestimationthatshellfishfarminghasamuchhighernetcarbonsequestrationratiothannaturalmarinesystems(usuallylessthan1%).Accordingly,thecarbonstoredviatheshell,thecarboninthesofttissue,andthecarboninbio-depositionwereassumedtoperformacarboncapturefunction.However,theestimationofthenetsequestrationratiowasbasedonthelifecyclecarbonbudgetofashellfishdeterminedthroughobservationexperiments.Althoughallwerecontainedinthelifecyclecarbonbudget,thekineticprocesses,suchasfeedingonphytoplankton,shellfishgrowthrate,andmetabolicrate,havestronginteractionswiththelocalenvironmentandaretoocomplextoparameterizeandquantify.Therefore,thenetcarbonsequestrationratiomayvarysignificantly.Inthefuture,detailedresearchisneededtosystematicallyobservethedynamicprocessofthecarbonbudgetandprovidemoreaccurateestimations.Inthisstudy,onlyoysters,mussels,cockles,clams,andscallopswereselectedfortheestimationinthisstudybecauseoftheirwidedistributionsandlargeproductionglobally.TheyieldinformationfortheshellfishfarminginChinawasobtainedfromtheChinaFisheryStatisticalYearbook,whichdoesnotcontaindetailedinformationaboutthespeciesofeachtypeofshellfish(e.g.,C.gigasandC.hongkongensisproportionsforoysters).Thus,inthisstudy,thecarbonsequestrationofeachtypewasestimatedusingthemeanvalueforselectedrepresentativevarieties.Differentspecieshavedifferentdryweightratiosofsofttissuetoshells.Therecouldevenbelocalvariationsinthisratioforthesamespecieswhenfarmedindifferentregions.Thisvariationmayaffecttheestimatedamountofcarbonsequesteredintheshellsandsofttissue.Theassumptionthat40%ofthebio-depositionissequesteredintheseabedisarawestimation,becauseinformationabouttheactualvalueisverylimitedandstronglydependentonthelocalenvironmentalconditions.Theestimationsofthecarbonfootprintswerebasedontheinformationforachosenspeciesforeachtypeofshellfish(presentedinS3).Therewereconsiderabledifferencesbetweentheinformationobtainedthroughtheinterviewswithfarmersandexpertsandtheprimarydataforthecontributionstothecarbonfootprint.Thismaybeanaturalvarianceduetodifferentseaareaconditions,farmingmethods,andnutrientlevels.Thiscouldbefurtherinvestigatedbybroadeningthescopeoftheinvestigation.Theglobalmaximumareaproductionandthemaximumecologicalproductionwerealsorawestimations.Moreexactresultscouldbeobtainedbyrefiningthedetailofthelocalinformationaboutthehydrologyandecologyofpotentialfarmingareas,forinstance,thewaterresidencetimeinabayandtherateofphytoplanktonproduction.CreditauthorstatementJ.C.FengandJ.Y.Yandesignedresearch.J.C.FengandL.W.Sunperformedtheresearch,analyzeddata,andwrotethepaper.DeclarationofcompetinginterestTheauthorsdeclarethattheyhavenoknowncompetingfinancialinterestsorpersonalrelationshipsthatcouldhaveappearedtoinfluencetheworkreportedinthispaper.DataavailabilityDatawillbemadeavailableonrequest.AcknowledgmentsTheauthorsaregratefultotheeditorsandreviewersfortheirkindhelp.Dr.JinyueYanwouldliketothankProf.XunLiforhisinspirationandideasduringdiscussionsofCO2captureandstoragemorethan15yearsago,whichresultedinthelaterconceptofcapturingCO2usingshellfish.HewouldalsoliketothanktheSwedishEnergyAgencyforfinancialsupportfromtheNegativeEmissionTechnologies:ReadinessAssessment,PolicyInstrumentDesign,OptionsforGovernanceandDialogue(NET-RAPIDO)project(46193–1).Dr.Jing-ChunFengwouldliketoacknowledgethefinancialsupportforthisresearchreceivedfromtheNationalNaturalScienceFoundationofChina(42022046),theNationalKeyResearchandDevelopmentProgram(2021YFF0502300),andGuangdongNaturalResourcesFoundation,(GDNRC[2022]45).Dr.Jing-ChunFengwouldalsoliketothankProfs.SiZhang,SaiLiang,andZhifengYangfortheirkindguidance.Prof.LinlinXiaisespeciallyappreciatedforherhelpincreatingthefigures.Theauthorsalsothankmaster’scandidatesYanyanHuangandMingruiZhangfortheirhelpwiththedatacollection.AppendixA.SupplementarydataSupplementarydatatothisarticlecanbefoundonlineathttps://doi.org/10.1016/j.rser.2022.113018.References[1]McKinleyGA,PilcherDJ,FayAR,LindsayK,LongMC,LovenduskiNS.Timescalesfordetectionoftrendsintheoceancarbonsink.Nature2016;530(7591):469–72.J.-C.Fengetal.RenewableandSustainableEnergyReviews171(2023)11301810[2]CurlRL.Carbonshiftedbutnotsequestered.Science2012;335(6069).655-655.[3]M¨ollerstenK,YanJ,JoseRM.PotentialmarketnichesforbiomassenergywithCO2captureandstorage-OpportunitiesforenergysupplywithnegativeCO2emissions.BiomassBioenergy2003;25(3):273–85.[4]Krause-JensenD,DuarteCM.Substantialroleofmacroalgaeinmarinecarbonsequestration.NatGeosci2016;9(10):737–42.[5]McLarenD.Quantifyingthepotentialscaleofmitigationdeterrencefromgreenhousegasremovaltechniques.ClimChange2020;162(4):2411–28.[6]WilliamsonP.ScrutinizeCO2removalmethods.Nature2016;530(7589):153–5.[7]GattiLV,BassoLS,MillerJB,etal.Amazoniaasacarbonsourcelinkedtodeforestationandclimatechange.Nature2021;595(7867):388–93.[8]KellerDP,FengEY,OschliesA.Potentialclimateengineeringeffectivenessandsideeffectsduringahighcarbondioxide-emissionscenario.NatCom2014;5(1).[9]PaustianK,LehmannJ,OgleS,ReayD,RobertsonGP,SmithP.Climate-smartsoils.Nature2016;532(7597):49–57.[10]RumpelC,AmiraslaniF,Lydie-StellaKoutika,SmithP,WhiteheadD,WollenbergE.PutmorecarboninsoilstomeetParisclimatepledges.Nature2018;564(7734):32–4.[11]SmithP,DavisS,CreutzingF,etal.BiophysicalandeconomiclimitstonegativeCO2emissions.NatClimChange2016;6(1):42–50.[12]McLarenD.Acomparativeglobalassessmentofpotentialnegativeemissionstechnologies.ProcessSafEnvironProtect2012;90(6):489–500.[13]BauerJE,CaiWJ,RaymondPA,BianchiCS,etal.Thechangingcarboncycleofthecoastalocean.Nature2013;504(7478):61–70.[14]TangQ,ZhangJ,FangJ.ShellfishandseaweedmaricultureincreaseatmosphericCO2absorptionbycoastalecosystems.MarEcolProgSer2011;424:97–104.[15]RenW.StudyontheremovablecarbonsinkestimationanddecompositionofinfluencingfactorsofmaricultureshellfishandalgaeinChina—atwo-dimensionalperspectivebasedonscaleandstructure.EnvironSciPollutRes2021;28(17):21528–39.[16]JansenHM.Bivalvenutrientcycling.WageningenUniversity;2012.M1-PhD.[17]HumphreysMP,DanielsCJ,Wolf-GladrowDA,TyrrellT,AchterbergEP.OntheinfluenceofmarinebiogeochemicalprocessesoverCO2exchangebetweentheatmosphereandocean.MarChem2018;199:1–11.[18]RayNE,O’MearaT,WiliamsonT,IzursaJL,KangasPC.ConsiderationofcarbondioxidereleaseduringshellproductioninLCAofbivalves.IntJLifeCycleAssess2018;23(5):1042–8.[19]GazeauF,QuiblierG,JansenJM,etal.ImpactofelevatedCO2onshellfishcalcification.GeophysResLett2007;34(7).[20]MunariC,RossettiE,MistriM.Shellformationincultivatedbivalvescannotbepartofcarbontradingsystems:astudycasewithMytilusgalloprovincialis.MarEnvironRes2013;92:264–7.[21]AhmedN,BuntingSW,GlaserM,FlahertyMS,DianaJS.Cangreeningofaquaculturesequesterbluecarbon?Ambio2017;46(4):468–77.[22]MistriM,MunariC.ClamfarminggeneratesCO2:astudycaseintheMarinettalagoon(Italy).MarPollutBull2012;64(10):2261–4.[23]FilgueiraR,ByronCJ,ComeauLA,etal.Anintegratedecosystemapproachforassessingthepotentialroleofcultivatedbivalveshellsaspartofthecarbontradingsystem.MarEcolProgSer2015;518:281–7.[24]FilgueiraR,StrohmeierT,StrandO.Regulatingservicesofbivalvemolluscsinthecontextofthecarboncycleandimplicationsforecosystemvaluation.In:Goodsandservicesofmarinebivalves.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