Role of biochar in raising blue carbon stock capacity of salt marshes

Salt marshes are an important blue carbon ecosystem,with surprisingly fast carbon accumulation rates that are 40 times higher than those of terrestrial forests.In recent decades,salt marshes have suffered great degradation and loss all over the world.The idea to enhance carbon stock in salt marshes(so-called blue carbon)using biochar(so-called black carbon)has recently been proposed.Although experiments and observations remain limited,significant enhancements in soil organic carbon and plant growth have been documented in most case studies.However,due to the limited number of observations and their relatively short time window ranging from months to less than one year,there still exists a knowledge gap regarding the process,mechanism,and effect of biochar in enhancing carbon stock in salt marshes.Future research is urgently needed in the following perspectives:1)exploring the relationship between carbon stock enhancement efficiency and biochar properties,2)optimizing the physical and chemical properties of biochar to boost its efficiency,and 3)studying thein-situresponses of complex carbon pools to biochar addition,especially under tidal conditions and over a longer period of time.

Salt marshes are a typical blue carbon ecosystem widely distributed in intertidal zones,which can mitigate global climate change with surprisingly high efficiency.Globally,carbon accumulation rates of salt marshes are 218±24 g C m-2year-1,approximately 40 times higher than those of terrestrial forests(5.1±1.0 g C m-2year-1)(Mcleodet al.,2011).However,in recent decades,salt marshes have suffered great loss due to coastal urbanization,pollution,and reclamation caused by anthropogenic activities(Adam,2002).In China,more than 7 000 km2of salt marshes have disappeared at an average loss rate of 3.2% per year (Wuet al.,2020).

Biochar,also known as black carbon derived from natural materials,has high carbon content,environmental stability,and large specific surface area.The manufacturing process of biochar offers an efficient way of long-term carbon storage by preventing rapid degradation of organic matterin situ(Liuet al.,2015).Moreover,biochar naturally acts an effective sorbent,capturing CO2and pollutants such as heavy metals,polycyclic aromatic hydrocarbons,and pesticides in sediments,thereby promoting plant growth(Kavithaet al.,2018;Dissanayakeet al.,2020).Furthermore,the coast of China has been largely invaded bySpartina alterniflora,which comprises 48%of salt marshes in China(Huet al.,2021).The allelopathy ofS.alterniflorahas been considered a“chemical weapon”inhibiting the growth of native salt marshes,which facilitates its rapid invasion(Xuet al.,2019,2020),where biochar application may also mitigate allelopathy stress.

Biochar application to promote carbon storage in terrestrial ecosystems has been documented in numerous literature.However,the environmental conditions of salt marshes largely differ from those of terrestrial ecosystems(including saline-alkali land),thus posing further challenges in the specific intertidal environment.For instance,salt marshes are characterized by high salinity,low oxygen,and tidal flooding,with stronger hydrodynamic conditions when compared to terrestrial ecosystems.The presence of salt marshes can alter local hydrodynamic conditions and extend the path of organic particles,leading to an increase in allochthonous carbon deposition in sediments(Gaciaet al.,1999;Huanget al.,2021).Coastal vegetation has been observed to trap particles such as microplastics(enrichment of 1.3-17.6 times)and black carbon (Huanget al.,2020,2021;Liet al.,2021).Black carbon,including biochar,was reported to account for about 9%-25%of the organic carbon content in sediments of coastal vegetation fields(Liet al.,2021).This trapping capacity may make biochar application feasible under tidal currents in salt marsh ecosystems (Fig.1).However,at a high sedimentation rate,the effectiveness of biochar may be weakened by other fine particles adsorbed on its surface.

Fig.1 Effect of biochar on salt marshes under short(a)and long(b)time scales.Red arrows indicate that processes are strengthened.CEC=cation exchange capacity;SOC=soil organic carbon;EC=electrical conductivity;BD=bulk density;GHG=greenhouse gas;GWP=global warming potential.

Due to limited experiments and observations conducted on salt marshes,the effect of biochar on carbon stock of salt marshes remains largely ambiguous.Soil organic carbon contents increased by 22%-58%four months after biochar addition in a pot experiment onSesbania cannabina(Cuiet al.,2021).Likewise,a one-year field experiment onSuaeda salsashowed that carbon storage only increased by 0.4%-2.8%with 3%biochar addition in sediments(Chenet al.,2022).Soil organic carbon content ofS.salsaincreased by approximately 200%with no flooding,but only 50%with episodic flooding,suggesting weakened enhancement of carbon stock capacity under flooding condition(Caiet al.,2021).During a 90-d waterlogging experiment with salt marsh species biochar(Phragmites communisandS.alterniflora) added in the sediments,the emissions of CO2and N2O decreased by 36%-82%and 97%-123%,respectively,and those of CH4increased by 102%-132% (Yanet al.,2020).The corresponding global warming potential(GWP)decreased by 36%-87% after biochar addition under waterlogged condition,better than that under non-waterlogged situation(28%-69%)(Yanet al.,2020).Compared to reed biochar,S.alterniflorabiochar was reported to have a lower carbon content;withS.alterniflorabiochar,the reduction in CO2emissions in sediments was 43%-83%,whereas the reduction was 36%-83%with reed biochar(Yanet al.,2020;Wanget al.,2021).Significantly higher yields and specific growth rates of plants were also reported after biochar addition.For instance,the fine root biomass ofPhragmites australisincreased by 80%due to decreased soil electrical conductivity,which further contributed to 70%higher total biomass of plants after biochar rhizosphere addition(Lianget al.,2021).The growth ofS.cannabinaandKosteletzkya virginicawas promoted by 111%-152%and 118%-156%,respectively,with ≤5%biochar amendment in a 52-d pot experiment(Zhenget al.,2018a).Similar effect onS.salsawas also observed during a 60-d pot experiment(Caiet al.,2021).These emerging evidences suggest that soil and plant carbon pools in salt marshes may gain increments after biochar addition.

Carbon stock enhancement after biochar application may be attributed to factors such as nutrient supply,sediment amendment,negative priming effect,and trapping effect of salt marshes (Fig.1).Plant roots directly benefit from nutrient supply (N,P,K,etc.) and sediment amendment(pH,cation exchange capacity,electrical conductivity,bulk density,pollutants,etc.),which in turn facilitates plant growth and enables more CO2to be captured from the atmosphere.Furthermore,shoot height and density and leaf area are considered important in trapping allochthonous matter(Cozzolinoet al.,2020;Huanget al.,2020),which may contribute significant carbon stock in salt marshes.Under short-term scenarios,positive priming effect may occur due to labile carbon leaching from biochar and being consumed by opportunistic microorganisms producing more greenhouse gases (Rasulet al.,2022).At the same time,greenhouse gases may be partially dissolved in water column in salt marshes,as approximately 30%reduction in emissions was reported in waterlogged environment compared to nonwaterlogged environment(Yanet al.,2020).Under long-term scenarios,buried organic matter may be protected by the negative priming effect of biochar.This effect may resulted from stable sediment aggregates with an intimate association between biochar and soil minerals and high abundances of microorganisms with low carbon turnover taxa(Zhenget al.,2018b;Rasulet al.,2022).

However,the mechanisms behind carbon stock enhancement in salt marsh ecosystems have not been well explored.We still lack sufficient observations to establish the relationship between carbon stock enhancement and biochar properties.The responses of complex carbon pools(including biochar itself,plant litter,drifting external matter,dissolved organic carbon,and microbial carbon)of salt marshes may also be quite different,especially under the real or simulated tidal environment(Fig.2a,b).For instance,only a single case study simulated the flooding situation of salt marshes(Caiet al.,2021),but did not consider hydrodynamic conditions.In addition,there is a lack of field studies to determine the optimal amount of biochar additionin situ.Given that the current studies related to salt marshes were operated in a relatively short period of time ranging from months to less than one year,carbon stock variations over years after biochar amendment also require urgent investigation.

Fig.2 Biochar amendment in tidal salt marshes for their restoration and promoting blue carbon stock:degradation of native tidal salt marshes threatened by the invasive plant Spartina alterniflora in China(a),ordinary biochar(glycophyte-derived biochar normally applied in terrestrial ecosystems)added in degraded salt marshes enhancing carbon stock via mitigation of pollution stress,ameliorated microbes,and increased allochthonous and autochthonous matter in sediments(b),and addition of S.alterniflora biochar in invaded salt marshes helping remove the invasive plants and their allelopathy stress to native plants(c).Blue arrows indicate increasing carbon pools,purple arrows indicate increasing organic matter and optimized microbial community,and red arrows indicate pollutant and allelopathy mitigation.

In the future,biochar addition research needs to focus on its resistance to water flow and hybridize it with current restoration approaches to reduce its loss in tidal environment(Fig.1).Optimizing biochar properties(e.g.,physical and chemical modification)for enhancing carbon stock capacity is also desirable.Considering the widespread of the invasive plantS.alterniflorain China(Xiaet al.,2020),preparing biochar from this species may be a win-win strategy through 1)removing the invasive plants,2)mitigating allelopathic inhibitionin situ,3)restoring the native salt marshes,and 4)manipulating blue carbon pools through biochar approach(Fig.2c).Likewise,utilization of aged native salt marsh species(Suaeda altissima,S.salsa,Kalidium foliatum,P.australis,andTamarixchinensis)as feedstocks of biochar may also be a win-win strategy for reducing CO2emission(Xiaoet al.,2022).Biochar made from salt marsh plants is also encouraged to be applied in terrestrial ecosystems due to its higher ash content and pH compared to those of glycophytes,which are important for increasing plant productivity,particularly in acidic soils (Daiet al.,2020;Xiaoet al.,2022).Furthermore,biochar itself requires low energy and contributes to negative carbon emissions(e.g.,-0.9 kg CO2-equivalent kg-1in Alhashimi and Aktas(2017)),which may even have high carbon sequestration potential with the development of clean energy such as solar and tidal energy in coastal zones.We believe that biochar could serve as a promising approach for restoration and artificial stock enhancement of salt marshes and deserves further investigation in the future.

ACKNOWLEDGEMENTS

We acknowledge the financial support from the Provincial Natural Science Foundation for Distinguished Young Scientists of Zhejiang,China(No.LR22D06003),the Key Laboratory of Marine Ecological Monitoring and Restoration Technologies of the Ministry of Natural Resources of China (No.MEMRT202102),the Science Foundation of Donghai Laboratory,China(No.DH-2022KF01021),the Fundamental Research Fund for the Central Universities of China(No.226-2022-00119),and the Funding for ZJU Tang Scholars of China to Xi Xiao.